A Comparative Analysis of Oocyte Development in Mammals
Abstract
:1. Introduction
2. Gene Expression: Old Players and Newcomers Shape the Oocyte Transcriptome
2.1. Transcriptional Activity in the Oocyte Throughout Folliculogenesis
2.2. Posttranscriptional Control of Maternal RNA
2.3. The Oocyte Transcriptome
2.3.1. Genes Highly Conserved in Fly or Distant Vertebrates and the Mouse
2.3.2. Genes That Appeared Specifically in Mammals
2.3.3. Genes Lost in Several Vertebrate Species
Genes Involved in Controlling Histone Translation
Genes Involved in Fertilization
3. The Oocyte is a Driver of Folliculogenesis and Can Control the Ovulation Rate
3.1. The Oocyte Drives Follicular Cell Proliferation and Differentiation
3.2. The Underlying Mechanisms
3.3. The Oocyte-Secreted Factors GDF9 and BMP15 Regulate Granulosa and Cumulus Cell Function
3.3.1. Structural Features of GDF9 and BMP15 and Common Roles
3.3.2. Specific Roles of GDF9 and BMP15
3.4. Can Oocyte-Secreted Factors GDF9 and BMP15 Control the Ovulation Rate?
4. The Oocyte: A High Energy Demanding Cell that Can Sense Changes in Its Lipid Environment
4.1. Primary Nutrients Needed for Oocyte Development
4.1.1. Carbohydrates
4.1.2. Amino Acids and Proteins
4.1.3. Lipids
4.2. Lipid Metabolism
4.2.1. Oocyte Lipid Composition
4.2.2. Lipid Requirement for Oocyte and Follicular Cells Functions
4.3. Comparative Dependence to Lipid Metabolism between Mammal Species
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Bachvarova, R.; De Leon, V.; Johnson, A.; Kaplan, G.; Paynton, B.V. Changes in total RNA, polyadenylated RNA, and actin mRNA during meiotic maturation of mouse oocytes. Dev. Biol. 1985, 108, 325–331. [Google Scholar] [CrossRef]
- Gilbert, I.; Scantland, S.; Sylvestre, E.-L.; Gravel, C.; Laflamme, I.; Sirard, M.-A.; Robert, C. The dynamics of gene products fluctuation during bovine pre-hatching development. Mol. Reprod. Dev. 2009, 76, 762–772. [Google Scholar] [CrossRef] [PubMed]
- Kocabas, A.M.; Crosby, J.; Ross, P.J.; Otu, H.H.; Beyhan, Z.; Can, H.; Tam, W.-L.; Rosa, G.J.M.; Halgren, R.G.; Lim, B.; et al. The transcriptome of human oocytes. Proc. Natl. Acad. Sci. USA 2006, 103, 14027–14032. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lequarre, A.S.; Traverso, J.M.; Marchandise, J.; Donnay, I. Poly(A) RNA Is Reduced by Half During Bovine Oocyte Maturation but Increases when Meiotic Arrest Is Maintained with CDK Inhibitors1. Biol. Reprod. 2004, 71, 425–431. [Google Scholar] [CrossRef] [PubMed]
- Olszańska, B.; Borgul, A. Maternal RNA content in oocytes of several mammalian and avian species. J. Exp. Zool. 1993, 265, 317–320. [Google Scholar] [CrossRef]
- Olds, P.J.; Stern, S.; Biggers, J.D. Chemical estimates of the RNA and DNA contents of the early mouse embryo. J. Exp. Zool. 1973, 186, 39–45. [Google Scholar] [CrossRef] [PubMed]
- Moore, J.W.; Ramon, F. On numerical integration of the Hodgkin and Huxley equations for a membrane action potential. J. Theor. Biol. 1974, 45, 249–273. [Google Scholar] [CrossRef]
- Stahl, A.; Mirre, C.; Hartung, M.; Knibiehler, B. [Localization, structure and activity of ribosomal genes in the oocyte nucleolus during meiotic prophase]. Reprod. Nutr. Dev. 1980, 20, 469–483. [Google Scholar] [CrossRef]
- Fair, T.; Hyttel, P.; Greve, T.; Boland, M. Nucleus structure and transcriptional activity in relation to oocyte diameter in cattle. Mol. Reprod. Dev. 1996, 43, 503–512. [Google Scholar] [CrossRef]
- Fair, T.; Hulshof, S.C.; Hyttel, P.; Greve, T.; Boland, M. Nucleus ultrastructure and transcriptional activity of bovine oocytes in preantral and early antral follicles. Mol. Reprod. Dev. 1997, 46, 208–215. [Google Scholar] [CrossRef]
- Bjerregaard, B.; Maddox-Hyttel, P. Regulation of ribosomal RNA gene expression in porcine oocytes. Anim. Reprod. Sci. 2004, 82–83, 605–616. [Google Scholar] [CrossRef] [PubMed]
- Luciano, A.M.; Franciosi, F.; Dieci, C.; Lodde, V. Changes in large-scale chromatin structure and function during oogenesis: A journey in company with follicular cells. Anim. Reprod. Sci. 2014, 149, 3–10. [Google Scholar] [CrossRef] [PubMed]
- Bouniol-Baly, C.; Hamraoui, L.; Guibert, J.; Beaujean, N.; Szöllösi, M.S.; Debey, P. Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes. Biol. Reprod. 1999, 60, 580–587. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pan, L.-Z.; Zhu, S.; Zhang, M.; Sun, M.-J.; Lin, J.; Chen, F.; Tan, J.-H. A new classification of the germinal vesicle chromatin configurations in pig oocytes†. Biol. Reprod. 2018, 99, 1149–1158. [Google Scholar] [CrossRef] [PubMed]
- Lodde, V.; Modina, S.; Galbusera, C.; Franciosi, F.; Luciano, A.M. Large-scale chromatin remodeling in germinal vesicle bovine oocytes: Interplay with gap junction functionality and developmental competence. Mol. Reprod. Dev. 2007, 74, 740–749. [Google Scholar] [CrossRef]
- Wang, H.-L.; Sui, H.-S.; Liu, Y.; Miao, D.-Q.; Lu, J.-H.; Liang, B.; Tan, J.-H. Dynamic changes of germinal vesicle chromatin configuration and transcriptional activity during maturation of rabbit follicles. Fertility and Sterility 2009, 91, 1589–1594. [Google Scholar] [CrossRef]
- Reynaud, K.; de Lesegno, C.V.; Chebrout, M.; Thoumire, S.; Chastant-Maillard, S. Follicle population, cumulus mucification, and oocyte chromatin configuration during the periovulatory period in the female dog. Theriogenology 2009, 72, 1120–1131. [Google Scholar] [CrossRef]
- Lee, H.S.; Yin, X.J.; Jin, Y.X.; Kim, N.H.; Cho, S.G.; Bae, I.H.; Kong, I.K. Germinal vesicle chromatin configuration and meiotic competence is related to the oocyte source in canine. Anim. Reprod. Sci. 2008, 103, 336–347. [Google Scholar] [CrossRef]
- Anderson, J.E.; Matteri, R.L.; Abeydeera, L.R.; Day, B.N.; Prather, R.S. Degradation of maternal cdc25c during the maternal to zygotic transition is dependent upon embryonic transcription. Mol. Reprod. Dev. 2001, 60, 181–188. [Google Scholar] [CrossRef]
- Braude, P.; Bolton, V.; Moore, S. Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 1988, 332, 459–461. [Google Scholar] [CrossRef]
- Svoboda, P. Mammalian zygotic genome activation. Semin. Cell Dev. Biol. 2018, 84, 118–126. [Google Scholar] [CrossRef]
- Crosby, I.M.; Gandolfi, F.; Moor, R.M. Control of protein synthesis during early cleavage of sheep embryos. J. Reprod. Fertil. 1988, 82, 769–775. [Google Scholar] [CrossRef] [Green Version]
- Manes, C. The participation of the embryonic genome during early cleavage in the rabbit. Dev. Biol. 1973, 32, 453–459. [Google Scholar] [CrossRef]
- Dai, X.-X.; Jiang, J.-C.; Sha, Q.-Q.; Jiang, Y.; Ou, X.-H.; Fan, H.-Y. A combinatorial code for mRNA 3′-UTR-mediated translational control in the mouse oocyte. Nucl. Ac. Res. 2019, 47, 328–340. [Google Scholar] [CrossRef] [Green Version]
- Esencan, E.; Kallen, A.; Zhang, M.; Seli, E. Translational activation of maternally derived mRNAs in oocytes and early embryos and the role of embryonic poly(A) binding protein (EPAB). Biol. Reprod. 2019, 100, 1147–1157. [Google Scholar] [CrossRef]
- Winata, C.L.; Korzh, V. The translational regulation of maternal mRNAs in time and space. FEBS Lett. 2018, 592, 3007–3023. [Google Scholar] [CrossRef]
- Kang, M.-K.; Han, S.-J. Post-transcriptional and post-translational regulation during mouse oocyte maturation. BMB Reports 2011, 44, 147–157. [Google Scholar] [CrossRef] [Green Version]
- Gohin, M.; Fournier, E.; Dufort, I.; Sirard, M.-A. Discovery, identification and sequence analysis of RNAs selected for very short or long poly A tail in immature bovine oocytes. Mol. Hum. Reprod. 2014, 20, 127–138. [Google Scholar] [CrossRef] [Green Version]
- Reyes, J.M.; Chitwood, J.L.; Ross, P.J. RNA-Seq profiling of single bovine oocyte transcript abundance and its modulation by cytoplasmic polyadenylation. Mol. Reprod. Dev. 2015, 82, 103–114. [Google Scholar] [CrossRef] [Green Version]
- Reyes, J.M.; Ross, P.J. Cytoplasmic polyadenylation in mammalian oocyte maturation: Oocyte cytoplasmic polyadenylation. WIREs RNA 2016, 7, 71–89. [Google Scholar] [CrossRef]
- Tremblay, K.; Vigneault, C.; McGraw, S.; Sirard, M.-A. Expression of Cyclin B1 Messenger RNA Isoforms and Initiation of Cytoplasmic Polyadenylation in the Bovine Oocyte1. Biol. Reprod. 2005, 72, 1037–1044. [Google Scholar] [CrossRef]
- Nishimura, Y.; Kano, K.; Naito, K. Porcine CPEB1 is involved in Cyclin B translation and meiotic resumption in porcine oocytes: PIG CPEB WORKS ON MEIOTIC RESUMPTION. Anim. Sci. J. 2010, 81, 444–452. [Google Scholar] [CrossRef] [PubMed]
- Prochazkova, B.; Komrskova, P.; Kubelka, M. CPEB2 Is Necessary for Proper Porcine Meiotic Maturation and Embryonic Development. Int. J. Mol.Sci. 2018, 19, 3138. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, X.-P.; Cooper, N.G.F. Comparative in Silico Analyses of Cpeb1–4 with Functional Predictions. Bioinform. Biol. Insights 2010, 4, BBI-S5087. [Google Scholar] [CrossRef]
- Uzbekova, S.; Arlot-Bonnemains, Y.; Dupont, J.; Dalbiès-Tran, R.; Papillier, P.; Pennetier, S.; Thélie, A.; Perreau, C.; Mermillod, P.; Prigent, C.; et al. Spatio-temporal expression patterns of aurora kinases a, B, and C and cytoplasmic polyadenylation-element-binding protein in bovine oocytes during meiotic maturation. Biol. Reprod. 2008, 78, 218–233. [Google Scholar] [CrossRef]
- Racki, W.J.; Richter, J.D. CPEB controls oocyte growth and follicle development in the mouse. Development 2006, 133, 4527–4537. [Google Scholar] [CrossRef] [Green Version]
- Tay, J.; Richter, J.D. Germ Cell Differentiation and Synaptonemal Complex Formation Are Disrupted in CPEB Knockout Mice. Dev. Cell 2001, 1, 201–213. [Google Scholar] [CrossRef] [Green Version]
- Elis, S.; Desmarchais, A.; Cardona, E.; Fouchecourt, S.; Dalbies-Tran, R.; Nguyen, T.; Thermes, V.; Maillard, V.; Papillier, P.; Uzbekova, S.; et al. Genes Involved in Drosophila melanogaster Ovarian Function Are Highly Conserved Throughout Evolution. Genome Biol. Evol. 2018, 10, 2629–2642. [Google Scholar] [CrossRef]
- Drouilhet, L.; Paillisson, A.; Bontoux, M.; Jeanpierre, E.; Mazerbourg, S.; Monget, P. Use of combined in silico expression data and phylogenetic analysis to identify new oocyte genes encoding RNA binding proteins in the mouse. Mol. Reprod. Dev. 2008, 75, 1691–1700. [Google Scholar] [CrossRef]
- Mihalas, B.P.; Western, P.S.; Loveland, K.L.; McLaughlin, E.A.; Holt, J.E. Changing expression and subcellular distribution of karyopherins during murine oogenesis. Reproduction 2015, 150, 485–496. [Google Scholar] [CrossRef] [Green Version]
- Tejomurtula, J.; Lee, K.-B.; Tripurani, S.K.; Smith, G.W.; Yao, J. Role of Importin Alpha8, a New Member of the Importin Alpha Family of Nuclear Transport Proteins, in Early Embryonic Development in Cattle1. Biol. Reprod. 2009, 81, 333–342. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.; Ma, H.; Fu, L.; Yao, J. Kpna7 interacts with egg-specific nuclear factors in the rainbow trout (Oncorhynchus mykiss): K PNA7 I NTERACTS W ITH E GG -S PECIFIC F ACTORS. Mol. Reprod. Dev. 2014, 81, 1136–1145. [Google Scholar] [CrossRef]
- Hu, J.; Wang, F.; Yuan, Y.; Zhu, X.; Wang, Y.; Zhang, Y.; Kou, Z.; Wang, S.; Gao, S. Novel Importin-α Family Member Kpna7 Is Required for Normal Fertility and Fecundity in the Mouse. J. Biol. Chem. 2010, 285, 33113–33122. [Google Scholar] [CrossRef] [Green Version]
- Wang, X.; Park, K.-E.; Koser, S.; Liu, S.; Magnani, L.; Cabot, R.A. KPNA7, an oocyte- and embryo-specific karyopherin?subtype, is required for porcine embryo development. Reprod. Fertil. Dev. 2012, 24, 382. [Google Scholar] [CrossRef]
- Vallee, M.; Aiba, K.; Piao, Y.; Palin, M.-F.; Ko, M.S.H.; Sirard, M.-A. Comparative analysis of oocyte transcript profiles reveals a high degree of conservation among species. Reproduction 2008, 135, 439–448. [Google Scholar] [CrossRef] [Green Version]
- Sylvestre, E.-L.; Robert, C.; Pennetier, S.; Labrecque, R.; Gilbert, I.; Dufort, I.; Léveillé, M.-C.; Sirard, M.-A. Evolutionary conservation of the oocyte transcriptome among vertebrates and its implications for understanding human reproductive function. Mol. Hum. Reprod. 2013, 19, 369–379. [Google Scholar] [CrossRef] [Green Version]
- Rajkovic, A.; Yan, C.; Klysik, M.; Matzuk, M. Discovery of germ cell–specific transcripts by expressed sequence tag database analysis. Fertil. Steril. 2001, 76, 550–554. [Google Scholar] [CrossRef]
- Dadé, S.; Callebaut, I.; Mermillod, P.; Monget, P. Identification of a new expanding family of genes characterized by atypical LRR domains. Localization of a cluster preferentially expressed in oocyte. FEBS Lett. 2003, 555, 533–538. [Google Scholar] [CrossRef] [Green Version]
- Dadé, S.; Callebaut, I.; Paillisson, A.; Bontoux, M.; Dalbiès-Tran, R.; Monget, P. In silico identification and structural features of six new genes similar to MATER specifically expressed in the oocyte. Biochem. Biophys. Res. Commun. 2004, 324, 547–553. [Google Scholar] [CrossRef]
- Paillisson, A.; Levasseur, A.; Gouret, P.; Callebaut, I.; Bontoux, M.; Pontarotti, P.; Monget, P. Bromodomain testis-specific protein is expressed in mouse oocyte and evolves faster than its ubiquitously expressed paralogs BRD2, -3, and -4. Genomics 2007, 89, 215–223. [Google Scholar] [CrossRef]
- Pierre, A.; Gautier, M.; Callebaut, I.; Bontoux, M.; Jeanpierre, E.; Pontarotti, P.; Monget, P. Atypical structure and phylogenomic evolution of the new eutherian oocyte- and embryo-expressed KHDC1/DPPA5/ECAT1/OOEP gene family. Genomics 2007, 90, 583–594. [Google Scholar] [CrossRef] [Green Version]
- Dalbiès-Tran, R.; Papillier, P.; Pennetier, S.; Uzbekova, S.; Monget, P. Bovine mater-like NALP9 is an oocyte marker gene. Mol. Reprod. Dev. 2005, 71, 414–421. [Google Scholar] [CrossRef]
- Tong, Z.B.; Gold, L.; Pfeifer, K.E.; Dorward, H.; Lee, E.; Bondy, C.A.; Dean, J.; Nelson, L.M. Mater, a maternal effect gene required for early embryonic development in mice. Nat. Genet. 2000, 26, 267–268. [Google Scholar] [CrossRef]
- Hamatani, T.; Falco, G.; Carter, M.G.; Akutsu, H.; Stagg, C.A.; Sharov, A.A.; Dudekula, D.B.; VanBuren, V.; Ko, M.S.H. Age-associated alteration of gene expression patterns in mouse oocytes. Hum. Mol. Genet. 2004, 13, 2263–2278. [Google Scholar] [CrossRef] [Green Version]
- Paillisson, A.; Dadé, S.; Callebaut, I.; Bontoux, M.; Dalbiès-Tran, R.; Vaiman, D.; Monget, P. Identification, characterization and metagenome analysis of oocyte-specific genes organized in clusters in the mouse genome. BMC Genomics 2005, 6, 76. [Google Scholar] [CrossRef]
- Thélie, A.; Papillier, P.; Pennetier, S.; Perreau, C.; Traverso, J.M.; Uzbekova, S.; Mermillod, P.; Joly, C.; Humblot, P.; Dalbiès-Tran, R. Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo. BMC Dev. Biol. 2007, 7, 125. [Google Scholar] [CrossRef] [Green Version]
- Angulo, L.; Perreau, C.; Lakhdari, N.; Uzbekov, R.; Papillier, P.; Freret, S.; Cadoret, V.; Guyader-Joly, C.; Royere, D.; Ponsart, C.; et al. Breast-cancer anti-estrogen resistance 4 (BCAR4) encodes a novel maternal-effect protein in bovine and is expressed in the oocyte of humans and other non-rodent mammals. Hum. Reprod. 2013, 28, 430–441. [Google Scholar] [CrossRef] [Green Version]
- Meijer, D.; van Agthoven, T.; Bosma, P.T.; Nooter, K.; Dorssers, L.C.J. Functional Screen for Genes Responsible for Tamoxifen Resistance in Human Breast Cancer Cells. Mol. Cancer Res. 2006, 4, 379–386. [Google Scholar] [CrossRef] [Green Version]
- Peyny, M.; Jarrier-Gaillard, P.; Boulanger, L.; Daniel, N.; Lavillatte, S.; Cadoret, V.; Papillier, P.; Monniaux, D.; Peynot, N.; Duranthon, V.; et al. Investigating the role of BCAR4 in ovarian physiology and female fertility by genome editing in rabbit. Sci. Rep. 2020, 10, 4992. [Google Scholar] [CrossRef] [Green Version]
- Wang, Z.F.; Ingledue, T.C.; Dominski, Z.; Sanchez, R.; Marzluff, W.F. Two Xenopus proteins that bind the 3’ end of histone mRNA: Implications for translational control of histone synthesis during oogenesis. Mol. Cell. Biol. 1999, 19, 835–845. [Google Scholar] [CrossRef] [Green Version]
- Pennetier, S.; Uzbekova, S.; Guyader-Joly, C.; Humblot, P.; Mermillod, P.; Dalbiès-Tran, R. Genes Preferentially Expressed in Bovine Oocytes Revealed by Subtractive and Suppressive Hybridization1. Biol. Reprod. 2005, 73, 713–720. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thelie, A.; Pascal, G.; Angulo, L.; Perreau, C.; Papillier, P.; Dalbies-Tran, R. An oocyte-preferential histone mRNA stem-loop-binding protein like is expressed in several mammalian species. Mol. Reprod. Dev. 2012, 79, 380–391. [Google Scholar] [CrossRef]
- Goudet, G.; Mugnier, S.; Callebaut, I.; Monget, P. Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates. Biol. Reprod. 2008, 78, 796–806. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Meslin, C.; Mugnier, S.; Callebaut, I.; Laurin, M.; Pascal, G.; Poupon, A.; Goudet, G.; Monget, P. Evolution of genes involved in gamete interaction: Evidence for positive selection, duplications and losses in vertebrates. PLoS ONE 2012, 7, e44548. [Google Scholar] [CrossRef] [PubMed]
- Eppig, J.J. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001, 122, 829–838. [Google Scholar] [CrossRef]
- Guigon, C.J.; Magre, S. Contribution of Germ Cells to the Differentiation and Maturation of the Ovary: Insights from Models of Germ Cell Depletion. Biol. Reprod. 2006, 74, 450–458. [Google Scholar] [CrossRef] [Green Version]
- Gilchrist, R.B.; Lane, M.; Thompson, J.G. Oocyte-secreted factors: Regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update 2008, 14, 159–177. [Google Scholar] [CrossRef] [Green Version]
- Kidder, G.M.; Vanderhyden, B.C. Bidirectional communication between oocytes and follicle cells: Ensuring oocyte developmental competence. Can. J. Physiol. Pharmacol. 2010, 88, 399–413. [Google Scholar] [CrossRef] [Green Version]
- Monniaux, D. Driving folliculogenesis by the oocyte-somatic cell dialog: Lessons from genetic models. Theriogenology 2016, 86, 41–53. [Google Scholar] [CrossRef]
- el-Fouly, M.A.; Cook, B.; Nekola, M.; Nalbandov, A.V. Role of the ovum in follicular luteinization. Endocrinology 1970, 87, 286–293. [Google Scholar] [CrossRef]
- Guigon, C.J.; Coudouel, N.; Mazaud-Guittot, S.; Forest, M.G.; Magre, S. Follicular Cells Acquire Sertoli Cell Characteristics after Oocyte Loss. Endocrinology 2005, 146, 2992–3004. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vandormael-Pournin, S.; Guigon, C.J.; Ishaq, M.; Coudouel, N.; Avé, P.; Huerre, M.; Magre, S.; Cohen-Tannoudji, J.; Cohen-Tannoudji, M. Oocyte-specific inactivation of Omcg1 leads to DNA damage and c-Abl/TAp63-dependent oocyte death associated with dramatic remodeling of ovarian somatic cells. Cell Death Differ. 2015, 22, 108–117. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vanderhyden, B.C.; Telfer, E.E.; Eppig, J.J. Mouse Oocytes Promote Proliferation of Granulosa Cells from Preantral and Antral Follicles in Vitro1. Biol. Reprod. 1992, 46, 1196–1204. [Google Scholar] [CrossRef] [Green Version]
- Lanuza, G.M.; Fischman, M.L.; Barañao, J.L. Growth Promoting Activity of Oocytes on Granulosa Cells Is Decreased upon Meiotic Maturation. Dev. Biol. 1998, 197, 129–139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, R.; Norman, R.J.; Armstrong, D.T.; Gilchrist, R.B. Oocyte-Secreted Factor(s) Determine Functional Differences Between Bovine Mural Granulosa Cells and Cumulus Cells1. Biol. Reprod. 2000, 63, 839–845. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eppig, J.J.; Wigglesworth, K.; Pendola, F.L. The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc. Natl. Acad. Sci. USA 2002, 99, 2890–2894. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stubbs, S.A.; Stark, J.; Dilworth, S.M.; Franks, S.; Hardy, K. Abnormal Preantral Folliculogenesis in Polycystic Ovaries Is Associated with Increased Granulosa Cell Division. J. Clin. Endocr. Metab. 2007, 92, 4418–4426. [Google Scholar] [CrossRef] [Green Version]
- Eppig, J.J.; Wigglesworth, K.; Pendola, F.; Hirao, Y. Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells. Biol. Reprod. 1997, 56, 976–984. [Google Scholar] [CrossRef] [Green Version]
- Vanderhyden, B.C.; Cohen, J.N.; Morley, P. Mouse oocytes regulate granulosa cell steroidogenesis. Endocrinology 1993, 133, 423–426. [Google Scholar] [CrossRef]
- Coskun, S.; Uzumcu, M.; Lin, Y.C.; Friedman, C.I.; Alak, B.M. Regulation of Cumulus Cell Steroidogenesis by the Porcine Oocyte and Preliminary Characterization of Oocyte-Produced Factor(s). Biol. Reprod. 1995, 53, 670–675. [Google Scholar] [CrossRef]
- Vanderhyden, B.C.; Tonary, A.M. Differential Regulation of Progesterone and Estradiol Production by Mouse Cumulus and Mural Granulosa Cells by a Factor(s) Secreted by the Oocyte. Biol. Reprod. 1995, 53, 1243–1250. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vanderhyden, B.C.; Macdonald, E.A. Mouse Oocytes Regulate Granulosa Cell Steroidogenesis Throughout Follicular Development. Biol. Reprod. 1998, 59, 1296–1301. [Google Scholar] [CrossRef] [Green Version]
- Buccione, R.; Vanderhyden, B.C.; Caron, P.J.; Eppig, J.J. FSH-induced expansion of the mouse cumulus oophorus in vitro is dependent upon a specific factor(s) secreted by the oocyte. Dev. Biol. 1990, 138, 16–25. [Google Scholar] [CrossRef]
- Salustri, A. Paracrine actions of oocytes in the mouse pre-ovulatory follicle. Int. J. Dev. Biol. 2000, 44, 591–597. [Google Scholar] [PubMed]
- Zhang, M.; Su, Y.-Q.; Sugiura, K.; Xia, G.; Eppig, J.J. Granulosa Cell Ligand NPPC and Its Receptor NPR2 Maintain Meiotic Arrest in Mouse Oocytes. Science 2010, 330, 366–369. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Makabe, S.; Naguro, T.; Stallone, T. Oocyte–follicle cell interactions during ovarian follicle development, as seen by high resolution scanning and transmission electron microscopy in humans. Microsc. Res. Tech. 2006, 69, 436–449. [Google Scholar] [CrossRef]
- El-Hayek, S.; Yang, Q.; Abbassi, L.; FitzHarris, G.; Clarke, H.J. Mammalian Oocytes Locally Remodel Follicular Architecture to Provide the Foundation for Germline-Soma Communication. Curr. Biol. 2018, 28, 1124–1131. [Google Scholar] [CrossRef] [Green Version]
- Norris, R.P.; Ratzan, W.J.; Freudzon, M.; Mehlmann, L.M.; Krall, J.; Movsesian, M.A.; Wang, H.; Ke, H.; Nikolaev, V.O.; Jaffe, L.A. Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 2009, 136, 1869–1878. [Google Scholar] [CrossRef] [Green Version]
- Vaccari, S.; Weeks, J.L.; Hsieh, M.; Menniti, F.S.; Conti, M. Cyclic GMP Signaling Is Involved in the Luteinizing Hormone-Dependent Meiotic Maturation of Mouse Oocytes1. Biol. Reprod. 2009, 81, 595–604. [Google Scholar] [CrossRef]
- Chastant-Maillard, S.; Viaris de Lesegno, C.; Chebrout, M.; Thoumire, S.; Meylheuc, T.; Fontbonne, A.; Chodkiewicz, M.; Saint-Dizier, M.; Reynaud, K. The canine oocyte: Uncommon features of in vivo and in vitro maturation. Reprod. Fertil. Dev. 2011, 23, 391. [Google Scholar] [CrossRef]
- de Lesegno, C.V.; Reynaud, K.; Pechoux, C.; Thoumire, S.; Chastant-Maillard, S. Ultrastructure of canine oocytes during in vivo maturation. Mol. Reprod. Dev. 2008, 75, 115–125. [Google Scholar] [CrossRef] [PubMed]
- Songsasen, N.; Yu, I.; Gomez, M.; Leibo, S.P. Effects of meiosis-inhibiting agents and equine chorionic gonadotropin on nuclear maturation of canine oocytes. Mol. Reprod. Dev. 2003, 65, 435–445. [Google Scholar] [CrossRef] [PubMed]
- Dong, J.; Albertini, D.F.; Nishimori, K.; Kumar, T.R.; Lu, N.; Matzuk, M.M. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 1996, 383, 531–535. [Google Scholar] [CrossRef] [PubMed]
- Galloway, S.M.; McNatty, K.P.; Cambridge, L.M.; Laitinen, M.P.; Juengel, J.L.; Jokiranta, T.S.; McLaren, R.J.; Luiro, K.; Dodds, K.G.; Montgomery, G.W.; et al. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 2000, 25, 279–283. [Google Scholar] [CrossRef] [PubMed]
- Shimasaki, S.; Moore, R.K.; Otsuka, F.; Erickson, G.F. The bone morphogenetic protein system in mammalian reproduction. Endocr. Rev. 2004, 25, 72–101. [Google Scholar] [CrossRef] [PubMed]
- Juengel, J.L.; McNatty, K.P. The role of proteins of the transforming growth factor-beta superfamily in the intraovarian regulation of follicular development. Hum. Reprod. Update 2005, 11, 143–160. [Google Scholar] [CrossRef] [PubMed]
- McPherron, A.C.; Lee, S.J. GDF-3 and GDF-9: Two new members of the transforming growth factor-beta superfamily containing a novel pattern of cysteines. J. Biol. Chem. 1993, 268, 3444–3449. [Google Scholar]
- Dube, J.L.; Wang, P.; Elvin, J.; Lyons, K.M.; Celeste, A.J.; Matzuk, M.M. The Bone Morphogenetic Protein 15 Gene Is X-Linked and Expressed in Oocytes. Mol. Endocrinol. 1998, 12, 1809–1817. [Google Scholar] [CrossRef]
- Laitinen, M.; Vuojolainen, K.; Jaatinen, R.; Ketola, I.; Aaltonen, J.; Lehtonen, E.; Heikinheimo, M.; Ritvos, O. A novel growth differentiation factor-9 (GDF-9) related factor is co-expressed with GDF-9 in mouse oocytes during folliculogenesis. Mech. Dev. 1998, 78, 135–140. [Google Scholar] [CrossRef]
- Liao, W.X.; Moore, R.K.; Otsuka, F.; Shimasaki, S. Effect of Intracellular Interactions on the Processing and Secretion of Bone Morphogenetic Protein-15 (BMP-15) and Growth and Differentiation Factor-9: IMPLICATION OF THE ABERRANT OVARIAN PHENOTYPE OF BMP-15 MUTANT SHEEP. J. Biol. Chem. 2003, 278, 3713–3719. [Google Scholar] [CrossRef] [Green Version]
- McGrath, S.A.; Esquela, A.F.; Lee, S.J. Oocyte-specific expression of growth/differentiation factor-9. Mol. Endocrinol. 1995, 9, 131–136. [Google Scholar] [PubMed] [Green Version]
- Aaltonen, J.; Laitinen, M.P.; Vuojolainen, K.; Jaatinen, R.; Horelli-Kuitunen, N.; Seppä, L.; Louhio, H.; Tuuri, T.; Sjöberg, J.; Bützow, R.; et al. Human Growth Differentiation Factor 9 (GDF-9) and Its Novel Homolog GDF-9B Are Expressed in Oocytes during Early Folliculogenesis 1. J. Clin. Endocr. Metab. 1999, 84, 2744–2750. [Google Scholar] [CrossRef] [PubMed]
- Bodensteiner, K.J.; Clay, C.M.; Moeller, C.L.; Sawyer, H.R. Molecular Cloning of the Ovine Growth/Differentiation Factor-9 Gene and Expression of Growth/Differentiation Factor-9 in Ovine and Bovine Ovaries1. Biol. Reprod. 1999, 60, 381–386. [Google Scholar] [CrossRef] [PubMed]
- Jaatinen, R.; Laitinen, M.P.; Vuojolainen, K.; Aaltonen, J.; Louhio, H.; Heikinheimo, K.; Lehtonen, E.; Ritvos, O. Localization of growth differentiation factor-9 (GDF-9) mRNA and protein in rat ovaries and cDNA cloning of rat GDF-9 and its novel homolog GDF-9B. Mol. Cell. Endocrinol. 1999, 156, 189–193. [Google Scholar] [CrossRef]
- Elvin, J.A.; Yan, C.; Matzuk, M.M. Oocyte-expressed TGF-beta superfamily members in female fertility. Mol. Cell. Endocrinol. 2000, 159, 1–5. [Google Scholar] [CrossRef]
- Otsuka, F.; Yao, Z.; Lee, T.; Yamamoto, S.; Erickson, G.F.; Shimasaki, S. Bone Morphogenetic Protein-15: Identification of target cells and biological functions. J. Biol. Chem. 2000, 275, 39523–39528. [Google Scholar] [CrossRef] [Green Version]
- Paradis, F.; Novak, S.; Murdoch, G.K.; Dyck, M.K.; Dixon, W.T.; Foxcroft, G.R. Temporal regulation of BMP2, BMP6, BMP15, GDF9, BMPR1A, BMPR1B, BMPR2 and TGFBR1 mRNA expression in the oocyte, granulosa and theca cells of developing preovulatory follicles in the pig. Reproduction 2009, 138, 115–129. [Google Scholar] [CrossRef]
- Guéripel, X.; Brun, V.; Gougeon, A. Oocyte Bone Morphogenetic Protein 15, but not Growth Differentiation Factor 9, Is Increased During Gonadotropin-Induced Follicular Development in the Immature Mouse and Is Associated with Cumulus Oophorus Expansion1. Biol. Reprod. 2006, 75, 836–843. [Google Scholar] [CrossRef]
- Prochazka, R.; Nemcova, L.; Nagyova, E.; Kanka, J. Expression of Growth Differentiation Factor 9 Messenger RNA in Porcine Growing and Preovulatory Ovarian Follicles1. Biol. Reprod. 2004, 71, 1290–1295. [Google Scholar] [CrossRef] [Green Version]
- Silva, J.R.V.; van den Hurk, R.; van Tol, H.T.A.; Roelen, B.A.J.; Figueiredo, J.R. Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15), and BMP receptors in the ovaries of goats. Mol. Reprod. Dev. 2005, 70, 11–19. [Google Scholar] [CrossRef]
- Assou, S.; Anahory, T.; Pantesco, V.; Le Carrour, T.; Pellestor, F.; Klein, B.; Reyftmann, L.; Dechaud, H.; De Vos, J.; Hamamah, S. The human cumulus–oocyte complex gene-expression profile. Hum. Reprod. 2006, 21, 1705–1719. [Google Scholar] [CrossRef] [PubMed]
- Hosoe, M.; Kaneyama, K.; Ushizawa, K.; Hayashi, K.; Takahashi, T. Quantitative analysis of bone morphogenetic protein 15 (BMP15) and growth differentiation factor 9 (GDF9) gene expression in calf and adult bovine ovaries. Reprod. Biol. Endocrinol. 2011, 9, 33. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fernandez, T.; Palomino, J.; Parraguez, V.H.; Peralta, O.A.; De los Reyes, M. Differential expression of GDF-9 and BMP- 15 during follicular development in canine ovaries evaluated by flow cytometry. Anim. Reprod. Sci. 2016, 167, 59–67. [Google Scholar] [CrossRef]
- Palomino, J.; De los Reyes, M. Temporal expression of GDF-9 and BMP-15 mRNAs in canine ovarian follicles. Theriogenology 2016, 86, 1541–1549. [Google Scholar] [CrossRef]
- Peng, J.; Li, Q.; Wigglesworth, K.; Rangarajan, A.; Kattamuri, C.; Peterson, R.T.; Eppig, J.J.; Thompson, T.B.; Matzuk, M.M. Growth differentiation factor 9:bone morphogenetic protein 15 heterodimers are potent regulators of ovarian functions. Proc. Natl. Acad. Sci. USA 2013, 110, E776–E785. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mottershead, D.G.; Sugimura, S.; Al-Musawi, S.L.; Li, J.-J.; Richani, D.; White, M.A.; Martin, G.A.; Trotta, A.P.; Ritter, L.J.; Shi, J.; et al. Cumulin, an Oocyte-secreted Heterodimer of the Transforming Growth Factor-β Family, Is a Potent Activator of Granulosa Cells and Improves Oocyte Quality. J. Biol. Chem. 2015, 290, 24007–24020. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vitt, U.A.; Hayashi, M.; Klein, C.; Hsueh, A.J. Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol. Reprod. 2000, 62, 370–377. [Google Scholar] [CrossRef] [Green Version]
- Hickey, T.E.; Marrocco, D.L.; Amato, F.; Ritter, L.J.; Norman, R.J.; Gilchrist, R.B.; Armstrong, D.T. Androgens Augment the Mitogenic Effects of Oocyte-Secreted Factors and Growth Differentiation Factor 9 on Porcine Granulosa Cells1. Biol. Reprod. 2005, 73, 825–832. [Google Scholar] [CrossRef] [Green Version]
- Spicer, L.J.; Aad, P.Y.; Allen, D.; Mazerbourg, S.; Hsueh, A.J. Growth differentiation factor-9 has divergent effects on proliferation and steroidogenesis of bovine granulosa cells. J. Endocrinol. 2006, 189, 329–339. [Google Scholar] [CrossRef] [Green Version]
- Fabre, S.; Pierre, A.; Mulsant, P.; Bodin, L.; Di Pasquale, E.; Persani, L.; Monget, P.; Monniaux, D. Regulation of ovulation rate in mammals: Contribution of sheep genetic models. Reprod. Biol. Endocrinol. 2006, 4, 20. [Google Scholar] [CrossRef] [Green Version]
- Chang, H.-M.; Cheng, J.-C.; Klausen, C.; Leung, P.C.K. BMP15 Suppresses Progesterone Production by Down-Regulating StAR via ALK3 in Human Granulosa Cells. Mol. Endocrinol. 2013, 27, 2093–2104. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fenwick, M.A.; Mora, J.M.; Mansour, Y.T.; Baithun, C.; Franks, S.; Hardy, K. Investigations of TGF-β Signaling in Preantral Follicles of Female Mice Reveal Differential Roles for Bone Morphogenetic Protein 15. Endocrinology 2013, 154, 3423–3436. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McIntosh, C.J.; Lun, S.; Lawrence, S.; Western, A.H.; McNatty, K.P.; Juengel, J.L. The proregion of mouse BMP15 regulates the cooperative interactions of BMP15 and GDF9. Biol. Reprod. 2008, 79, 889–896. [Google Scholar] [CrossRef] [PubMed]
- Su, Y.-Q.; Sugiura, K.; Li, Q.; Wigglesworth, K.; Matzuk, M.M.; Eppig, J.J. Mouse Oocytes Enable LH-Induced Maturation of the Cumulus-Oocyte Complex via Promoting EGF Receptor-Dependent Signaling. Mol. Endocrinol. 2010, 24, 1230–1239. [Google Scholar] [CrossRef] [PubMed]
- Sugiura, K.; Su, Y.-Q.; Li, Q.; Wigglesworth, K.; Matzuk, M.M.; Eppig, J.J. Estrogen Promotes the Development of Mouse Cumulus Cells in Coordination with Oocyte-Derived GDF9 and BMP15. Mol. Endocrinol. 2010, 24, 2303–2314. [Google Scholar] [CrossRef]
- Wigglesworth, K.; Lee, K.-B.; O’Brien, M.J.; Peng, J.; Matzuk, M.M.; Eppig, J.J. Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammalian oocytes. Proc. Natl. Acad. Sci. USA 2013, 110, E3723–E3729. [Google Scholar] [CrossRef] [Green Version]
- De los Reyes, M.; Rojas, C.; Parraguez, V.H.; Palomino, J. Expression of growth differentiation factor 9 (GDF-9) during in vitro maturation in canine oocytes. Theriogenology 2013, 80, 587–596. [Google Scholar] [CrossRef]
- Garcia, P.; Aspee, K.; Ramirez, G.; Dettleff, P.; Palomino, J.; Peralta, O.A.; Parraguez, V.H.; De los Reyes, M. Influence of growth differentiation factor 9 and bone morphogenetic protein 15 on in vitro maturation of canine oocytes. Reprod. Dom. Anim. 2019, 54, 373–380. [Google Scholar] [CrossRef]
- Di Pasquale, E.; Beck-Peccoz, P.; Persani, L. Hypergonadotropic Ovarian Failure Associated with an Inherited Mutation of Human Bone Morphogenetic Protein-15 (BMP15) Gene. Am. J. Hum. Genet. 2004, 75, 106–111. [Google Scholar] [CrossRef] [Green Version]
- Di Pasquale, E.; Rossetti, R.; Marozzi, A.; Bodega, B.; Borgato, S.; Cavallo, L.; Einaudi, S.; Radetti, G.; Russo, G.; Sacco, M.; et al. Identification of New Variants of Human BMP15 Gene in a Large Cohort of Women with Premature Ovarian Failure. J. Clin. Endocr. Metab. 2006, 91, 1976–1979. [Google Scholar] [CrossRef] [Green Version]
- Dixit, H.; Rao, L.K.; Padmalatha, V.; Kanakavalli, M.; Deenadayal, M.; Gupta, N.; Chakravarty, B.; Singh, L. Mutational screening of the coding region of growth differentiation factor 9 gene in Indian women with ovarian failure. Menopause 2005, 12, 749–754. [Google Scholar] [CrossRef] [PubMed]
- Dixit, H.; Rao, L.K.; Padmalatha, V.V.; Kanakavalli, M.; Deenadayal, M.; Gupta, N.; Chakrabarty, B.; Singh, L. Missense mutations in the BMP15 gene are associated with ovarian failure. Hum. Genet. 2006, 119, 408–415. [Google Scholar] [CrossRef] [PubMed]
- Laissue, P.; Christin-Maitre, S.; Touraine, P.; Kuttenn, F.; Ritvos, O.; Aittomaki, K.; Bourcigaux, N.; Jacquesson, L.; Bouchard, P.; Frydman, R.; et al. Mutations and sequence variants in GDF9 and BMP15 in patients with premature ovarian failure. Eur. J. Endocrinol. 2006, 154, 739–744. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kovanci, E.; Rohozinski, J.; Simpson, J.; Heard, M.; Bishop, C.; Carson, S. Growth differentiating factor-9 mutations may be associated with premature ovarian failure. Fertil. Steril. 2007, 87, 143–146. [Google Scholar] [CrossRef] [PubMed]
- Zhao, H.; Qin, Y.; Kovanci, E.; Simpson, J.L.; Chen, Z.-J.; Rajkovic, A. Analyses of GDF9 mutation in 100 Chinese women with premature ovarian failure. Fertil. Steril. 2007, 88, 1474–1476. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, B.; Wen, Q.; Ni, F.; Zhou, S.; Wang, J.; Cao, Y.; Ma, X. Analyses of growth differentiation factor 9 (GDF9) and bone morphogenetic protein 15 (BMP15) mutation in Chinese women with premature ovarian failure: Letters to the Editor. Clin. Endocrinol. 2010, 72, 135–136. [Google Scholar] [CrossRef] [PubMed]
- Wang, T.-T.; Ke, Z.-H.; Song, Y.; Chen, L.-T.; Chen, X.-J.; Feng, C.; Zhang, D.; Zhang, R.-J.; Wu, Y.-T.; Zhang, Y.; et al. Identification of a mutation in GDF9 as a novel cause of diminished ovarian reserve in young women. Hum. Reprod. 2013, 28, 2473–2481. [Google Scholar] [CrossRef] [Green Version]
- Persani, L.; Rossetti, R.; Di Pasquale, E.; Cacciatore, C.; Fabre, S. The fundamental role of bone morphogenetic protein 15 in ovarian function and its involvement in female fertility disorders. Hum. Reprod. Update 2014, 20, 869–883. [Google Scholar] [CrossRef] [Green Version]
- Simpson, C.M.; Robertson, D.M.; Al-Musawi, S.L.; Heath, D.A.; McNatty, K.P.; Ritter, L.J.; Mottershead, D.G.; Gilchrist, R.B.; Harrison, C.A.; Stanton, P.G. Aberrant GDF9 Expression and Activation Are Associated with Common Human Ovarian Disorders. J. Clin. Endocr. Metab. 2014, 99, E615–E624. [Google Scholar] [CrossRef] [Green Version]
- Gilchrist, R.B. Molecular basis of oocyte-paracrine signalling that promotes granulosa cell proliferation. J. Cell Sci. 2006, 119, 3811–3821. [Google Scholar] [CrossRef] [Green Version]
- Otsuka, F.; Shimasaki, S. A negative feedback system between oocyte bone morphogenetic protein 15 and granulosa cell kit ligand: Its role in regulating granulosa cell mitosis. Proc. Natl. Acad. Sci. USA 2002, 99, 8060–8065. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carabatsos, M.J.; Elvin, J.; Matzuk, M.M.; Albertini, D.F. Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev. Biol. 1998, 204, 373–384. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, C.; Peng, J.; Matzuk, M.M.; Yao, H.H.-C. Lineage specification of ovarian theca cells requires multicellular interactions via oocyte and granulosa cells. Nat. Commun. 2015, 6, 6934. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Elvin, J.A.; Yan, C.; Wang, P.; Nishimori, K.; Matzuk, M.M. Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol. Endocrinol. 1999, 13, 1018–1034. [Google Scholar] [CrossRef] [PubMed]
- Gui, L.-M.; Joyce, I.M. RNA Interference Evidence That Growth Differentiation Factor-9 Mediates Oocyte Regulation of Cumulus Expansion in Mice1. Biol. Reprod. 2005, 72, 195–199. [Google Scholar] [CrossRef] [PubMed]
- Yan, C.; Wang, P.; DeMayo, J.; DeMayo, F.J.; Elvin, J.A.; Carino, C.; Prasad, S.V.; Skinner, S.S.; Dunbar, B.S.; Dube, J.L.; et al. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol. Endocrinol. 2001, 15, 854–866. [Google Scholar] [CrossRef]
- Varani, S.; Elvin, J.A.; Yan, C.; DeMayo, J.; DeMayo, F.J.; Horton, H.F.; Byrne, M.C.; Matzuk, M.M. Knockout of Pentraxin 3, a Downstream Target of Growth Differentiation Factor-9, Causes Female Subfertility. Mol. Endocrinol. 2002, 16, 1154–1167. [Google Scholar] [CrossRef]
- Hreinsson, J.G.; Scott, J.E.; Rasmussen, C.; Swahn, M.L.; Hsueh, A.J.W.; Hovatta, O. Growth Differentiation Factor-9 Promotes the Growth, Development, and Survival of Human Ovarian Follicles in Organ Culture. J. Clin. Endocr. Metab. 2002, 87, 316–321. [Google Scholar] [CrossRef]
- Teixeira Filho, F.L.; Baracat, E.C.; Lee, T.H.; Suh, C.S.; Matsui, M.; Chang, R.J.; Shimasaki, S.; Erickson, G.F. Aberrant Expression of Growth Differentiation Factor-9 in Oocytes of Women with Polycystic Ovary Syndrome. J. Clin. Endocr. Metab. 2002, 87, 1337–1344. [Google Scholar] [CrossRef]
- Otsuka, F.; Moore, R.K.; Shimasaki, S. Biological Function and Cellular Mechanism of Bone Morphogenetic Protein-6 in the Ovary. J. Biol. Chem. 2001, 276, 32889–32895. [Google Scholar] [CrossRef] [Green Version]
- Su, Y.-Q.; Sugiura, K.; Wigglesworth, K.; O’Brien, M.J.; Affourtit, J.P.; Pangas, S.A.; Matzuk, M.M.; Eppig, J.J. Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 2008, 135, 111–121. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Caixeta, E.S.; Sutton-McDowall, M.L.; Gilchrist, R.B.; Thompson, J.G.; Price, C.A.; Machado, M.F.; Lima, P.F.; Buratini, J. Bone morphogenetic protein 15 and fibroblast growth factor 10 enhance cumulus expansion, glucose uptake, and expression of genes in the ovulatory cascade during in vitro maturation of bovine cumulus–oocyte complexes. Reproduction 2013, 146, 27–35. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, Q.; Rajanahally, S.; Edson, M.A.; Matzuk, M.M. Stable expression and characterization of N-terminal tagged recombinant human bone morphogenetic protein 15. Mol. Hum. Reprod. 2009, 15, 779–788. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hussein, T.S.; Thompson, J.G.; Gilchrist, R.B. Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 2006, 296, 514–521. [Google Scholar] [CrossRef]
- Sugiura, K.; Su, Y.-Q.; Diaz, F.J.; Pangas, S.A.; Sharma, S.; Wigglesworth, K.; O’Brien, M.J.; Matzuk, M.M.; Shimasaki, S.; Eppig, J.J. Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 2007, 134, 2593–2603. [Google Scholar] [CrossRef] [Green Version]
- Hayashi, M.; McGee, E.A.; Min, G.; Klein, C.; Rose, U.M.; van Duin, M.; Hsueh, A.J.W. Recombinant Growth Differentiation Factor-9 (GDF-9) Enhances Growth and Differentiation of Cultured Early Ovarian Follicles*. Endocrinology 1999, 140, 1236–1244. [Google Scholar] [CrossRef]
- Gittens, J.E.I.; Barr, K.J.; Vanderhyden, B.C.; Kidder, G.M. Interplay between paracrine signaling and gap junctional communication in ovarian follicles. J. Cell Sci. 2005, 118, 113–122. [Google Scholar] [CrossRef] [Green Version]
- Yoshino, O.; McMahon, H.E.; Sharma, S.; Shimasaki, S. A unique preovulatory expression pattern plays a key role in the physiological functions of BMP-15 in the mouse. Proc. Natl. Acad. Sci. USA 2006, 103, 10678–10683. [Google Scholar] [CrossRef] [Green Version]
- Davis, G.H.; McEwan, J.C.; Fennessy, P.F.; Dodds, K.G.; McNatty, K.P.; O, W.-S. Infertility Due to Bilateral Ovarian Hypoplasia in Sheep Homozygous (FecX1 FecX1) for the Inverdale Prolificacy Gene Located on the X Chromosome. Biol. Reprod. 1992, 46, 636–640. [Google Scholar] [CrossRef] [Green Version]
- Braw-Tal, R.; McNatty, K.P.; Smith, P.; Heath, D.A.; Hudson, N.L.; Phillips, D.J.; McLeod, B.J.; Davis, G.H. Ovaries of ewes homozygous for the X-linked Inverdale gene (FecXI) are devoid of secondary and tertiary follicles but contain many abnormal structures. Biol. Reprod. 1993, 49, 895–907. [Google Scholar] [CrossRef] [Green Version]
- Bodin, L.; Di Pasquale, E.; Fabre, S.; Bontoux, M.; Monget, P.; Persani, L.; Mulsant, P. A novel mutation in the bone morphogenetic protein 15 gene causing defective protein secretion is associated with both increased ovulation rate and sterility in Lacaune sheep. Endocrinology 2007, 148, 393–400. [Google Scholar] [CrossRef] [PubMed]
- Santos, M.; Cordts, E.B.; Peluso, C.; Dornas, M.; Neto, F.H.V.; Bianco, B.; Barbosa, C.P.; Christofolini, D.M. Association of BMP15 and GDF9 variants to premature ovarian insufficiency. J. Assist. Reprod. Genet. 2019, 36, 2163–2169. [Google Scholar] [CrossRef] [PubMed]
- Hanrahan, J.P.; Gregan, S.M.; Mulsant, P.; Mullen, M.; Davis, G.H.; Powell, R.; Galloway, S.M. Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol. Reprod. 2004, 70, 900–909. [Google Scholar] [CrossRef] [PubMed]
- Nicol, L.; Bishop, S.C.; Pong-Wong, R.; Bendixen, C.; Holm, L.-E.; Rhind, S.M.; McNeilly, A.S. Homozygosity for a single base-pair mutation in the oocyte-specific GDF9 gene results in sterility in Thoka sheep. Reproduction 2009, 138, 921–933. [Google Scholar] [CrossRef] [Green Version]
- Silva, B.D.M.; Castro, E.A.; Souza, C.J.H.; Paiva, S.R.; Sartori, R.; Franco, M.M.; Azevedo, H.C.; Silva, T.A.S.N.; Vieira, A.M.C.; Neves, J.P.; et al. A new polymorphism in the Growth and Differentiation Factor 9 (GDF9) gene is associated with increased ovulation rate and prolificacy in homozygous sheep: New polymorphism in GDF9 and prolificacy. Anim. Genet. 2011, 42, 89–92. [Google Scholar] [CrossRef] [Green Version]
- Martinez-Royo, A.; Jurado, J.J.; Smulders, J.P.; Martí, J.I.; Alabart, J.L.; Roche, A.; Fantova, E.; Bodin, L.; Mulsant, P.; Serrano, M.; et al. A deletion in the bone morphogenetic protein 15 gene causes sterility and increased prolificacy in Rasa Aragonesa sheep: A deletion in the BMP15 gene. Anim. Genet. 2008, 39, 294–297. [Google Scholar] [CrossRef]
- Monteagudo, L.V.; Ponz, R.; Tejedor, M.T.; Laviña, A.; Sierra, I. A 17bp deletion in the Bone Morphogenetic Protein 15 (BMP15) gene is associated to increased prolificacy in the Rasa Aragonesa sheep breed. Anim. Reprod. Sci. 2009, 110, 139–146. [Google Scholar] [CrossRef]
- Moore, R.K.; Shimasaki, S. Molecular biology and physiological role of the oocyte factor, BMP-15. Mol. Cell. Endocrinol. 2005, 234, 67–73. [Google Scholar] [CrossRef]
- Mulsant, P.; Lecerf, F.; Fabre, S.; Schibler, L.; Monget, P.; Lanneluc, I.; Pisselet, C.; Riquet, J.; Monniaux, D.; Callebaut, I.; et al. Mutation in bone morphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Mérino ewes. Proc. Natl. Acad. Sci. USA 2001, 98, 5104–5109. [Google Scholar] [CrossRef] [Green Version]
- Souza, C.J.; MacDougall, C.; MacDougall, C.; Campbell, B.K.; McNeilly, A.S.; Baird, D.T. The Booroola (FecB) phenotype is associated with a mutation in the bone morphogenetic receptor type 1 B (BMPR1B) gene. J. Endocrinol. 2001, 169, R1–R6. [Google Scholar] [CrossRef] [Green Version]
- Wilson, T.; Wu, X.Y.; Juengel, J.L.; Ross, I.K.; Lumsden, J.M.; Lord, E.A.; Dodds, K.G.; Walling, G.A.; McEwan, J.C.; O’Connell, A.R.; et al. Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK-6) that is expressed in both oocytes and granulosa cells. Biol. Reprod. 2001, 64, 1225–1235. [Google Scholar] [CrossRef] [PubMed]
- Demars, J.; Fabre, S.; Sarry, J.; Rossetti, R.; Gilbert, H.; Persani, L.; Tosser-Klopp, G.; Mulsant, P.; Nowak, Z.; Drobik, W.; et al. Genome-Wide Association Studies Identify Two Novel BMP15 Mutations Responsible for an Atypical Hyperprolificacy Phenotype in Sheep. PLoS Genet 2013, 9, e1003482. [Google Scholar] [CrossRef] [PubMed]
- Juengel, J.L.; Hudson, N.L.; Heath, D.A.; Smith, P.; Reader, K.L.; Lawrence, S.B.; O’Connell, A.R.; Laitinen, M.P.E.; Cranfield, M.; Groome, N.P.; et al. Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol. Reprod. 2002, 67, 1777–1789. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Juengel, J.L.; Bodensteiner, K.J.; Heath, D.A.; Hudson, N.L.; Moeller, C.L.; Smith, P.; Galloway, S.M.; Davis, G.H.; Sawyer, H.R.; McNatty, K.P. Physiology of GDF9 and BMP15 signalling molecules. Anim. Reprod. Sci. 2004, 82–83, 447–460. [Google Scholar] [CrossRef]
- Juengel, J.L.; Hudson, N.L.; Berg, M.; Hamel, K.; Smith, P.; Lawrence, S.B.; Whiting, L.; McNatty, K.P. Effects of active immunization against growth differentiation factor 9 and/or bone morphogenetic protein 15 on ovarian function in cattle. Reproduction 2009, 138, 107–114. [Google Scholar] [CrossRef] [Green Version]
- McNatty, K.P.; Hudson, N.L.; Whiting, L.; Reader, K.L.; Lun, S.; Western, A.; Heath, D.A.; Smith, P.; Moore, L.G.; Juengel, J.L. The Effects of Immunizing Sheep with Different BMP15 or GDF9 Peptide Sequences on Ovarian Follicular Activity and Ovulation Rate1. Biol. Reprod. 2007, 76, 552–560. [Google Scholar] [CrossRef] [Green Version]
- Silva, P.V.; Guimarães, S.E.F.; Guimarães, J.D.; Nascimento, C.S.; Lopes, P.S.; Siqueira, J.B.; Amorim, L.S.; Fonseca e Silva, F.; Foxcroft, G.R. Follicular dynamics and gene expression in granulosa cells, corpora lutea and oocytes from gilts of breeds with low and high ovulation rates. Reprod. Fertil. Dev. 2014, 26, 316. [Google Scholar] [CrossRef] [Green Version]
- Kamalludin, M.H.; Garcia-Guerra, A.; Wiltbank, M.C.; Kirkpatrick, B.W. Trio, a novel high fecundity allele: I. Transcriptome analysis of granulosa cells from carriers and noncarriers of a major gene for bovine ovulation rate†. Biology of Reproduction 2018, 98, 323–334. [Google Scholar] [CrossRef]
- Montgomery, G.W.; Zhao, Z.Z.; Marsh, A.J.; Mayne, R.; Treloar, S.A.; James, M.; Martin, N.G.; Boomsma, D.I.; Duffy, D.L. A Deletion Mutation in GDF9 in Sisters with Spontaneous DZ Twins. Twin Res 2004, 7, 548–555. [Google Scholar] [CrossRef]
- Palmer, J.S.; Zhao, Z.Z.; Hoekstra, C.; Hayward, N.K.; Webb, P.M.; Whiteman, D.C.; Martin, N.G.; Boomsma, D.I.; Duffy, D.L.; Montgomery, G.W. Novel Variants in Growth Differentiation Factor 9 in Mothers of Dizygotic Twins. J. Clin. Endocr. Metab. 2006, 91, 4713–4716. [Google Scholar] [CrossRef] [Green Version]
- Morón, F.J.; de Castro, F.; Royo, J.L.; Montoro, L.; Mira, E.; Sáez, M.E.; Real, L.M.; González, A.; Mañes, S.; Ruiz, A. Bone morphogenetic protein 15 (BMP15) alleles predict over-response to recombinant follicle stimulation hormone and iatrogenic ovarian hyperstimulation syndrome (OHSS). Pharmacogenet. Genom. 2006, 16, 485–495. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Crawford, J.L.; McNatty, K.P. The ratio of growth differentiation factor 9: Bone morphogenetic protein 15 mRNA expression is tightly co-regulated and differs between species over a wide range of ovulation rates. Mol. Cell. Endocrinol. 2012, 348, 339–343. [Google Scholar] [CrossRef] [PubMed]
- Christoforou, E.R.; Pitman, J.L. Intrafollicular growth differentiation factor 9: Bone morphogenetic 15 ratio determines litter size in mammals†. Biol. Reprod. 2019, 100, 1333–1343. [Google Scholar] [CrossRef] [PubMed]
- Fontana, R.; Torre, S. The Deep Correlation between Energy Metabolism and Reproduction: A View on the Effects of Nutrition for Women Fertility. Nutrients 2016, 8, 87. [Google Scholar] [CrossRef] [PubMed]
- Broughton, D.E.; Moley, K.H. Obesity and female infertility: Potential mediators of obesity’s impact. Fertil. Steril. 2017, 107, 840–847. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- El-Toukhy, T.; Osman, A. Macronutrient Intake, Fertility, and Pregnancy Outcome. In Nutrition, Fertility, and Human Reproductive Function; Tremellen, K., Pearce, K., Eds.; CRC Press, Taylor & Francis Group: Boca Raton, FL, USA, 2015; pp. 51–68. ISBN 978-1-4822-1530-4. [Google Scholar]
- Brannian, J.D.; Hansen, K.A. Leptin and Ovarian Folliculogenesis: Implications for Ovulation Induction and ART Outcomes. Seminars in Reproductive Medicine 2002, 20, 103–112. [Google Scholar] [CrossRef]
- Nteeba, J.; Ganesan, S.; Keating, A.F. Progressive Obesity Alters Ovarian Folliculogenesis with Impacts on Pro-Inflammatory and Steroidogenic Signaling in Female Mice1. Biol. Reprod. 2014, 91, 1–11. [Google Scholar] [CrossRef]
- Lin, X.; Wang, H.; Wu, D.; Ullah, K.; Yu, T.; Ur Rahman, T.; Huang, H. High Leptin Level Attenuates Embryo Development in Overweight/Obese Infertile Women by Inhibiting Proliferation and Promotes Apoptosis in Granule Cell. Hormone and Metabolic Research 2017, 49, 534–541. [Google Scholar] [CrossRef]
- Dupont, J.; Reverchon, M.; Cloix, L.; Froment, P.; Ramé, C. Involvement of adipokines, AMPK, PI3K and the PPAR signaling pathways in ovarian follicle development and cancer. Int. J. Dev. Biol. 2012, 56, 959–967. [Google Scholar] [CrossRef] [Green Version]
- Reverchon, M.; Ramé, C.; Bertoldo, M.; Dupont, J. Adipokines and the Female Reproductive Tract. Int. J. Endocrinol. 2014, 2014, 1–10. [Google Scholar] [CrossRef]
- Vitti, M.; Di Emidio, G.; Di Carlo, M.; Carta, G.; Antonosante, A.; Artini, P.G.; Cimini, A.; Tatone, C.; Benedetti, E. Peroxisome Proliferator-Activated Receptors in Female Reproduction and Fertility. PPAR Res. 2016, 2016, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Collado-Fernandez, E.; Picton, H.M.; Dumollard, R. Metabolism throughout follicle and oocyte development in mammals. Int. J. Dev. Biol. 2012, 56, 799–808. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bradley, J.; Swann, K. Mitochondria and lipid metabolism in mammalian oocytes and early embryos. Int. J. Dev. Biol. 2019, 63, 93–103. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chavarro, J.E.; Gaskins, A.J.; Afeiche, A.C. Nutrition and Ovulatory Function. In Nutrition, Fertility, and Human Reproductive Function; Tremellen, K., Pearce, K., Eds.; CRC Press: Boca Raton, FL, USA, 2015; ISBN 978-0-429-15721-9. [Google Scholar]
- Sutton-McDowall, M.L.; Gilchrist, R.B.; Thompson, J.G. The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 2010, 139, 685–695. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sinclair, K.D.; Lunn, L.A.; Kwong, W.Y.; Wonnacott, K.; Linforth, R.S.T.; Craigon, J. Amino acid and fatty acid composition of follicular fluid as predictors of in-vitro embryo development. Reprod. Biomed. Online 2008, 16, 859–868. [Google Scholar] [CrossRef]
- Dupont, J.; Reverchon, M.; Bertoldo, M.J.; Froment, P. Nutritional signals and reproduction. Mol. Cell. Endocrinol. 2014, 382, 527–537. [Google Scholar] [CrossRef]
- Auclair, S.; Uzbekov, R.; Elis, S.; Sanchez, L.; Kireev, I.; Lardic, L.; Dalbies-Tran, R.; Uzbekova, S. Absence of cumulus cells during in vitro maturation affects lipid metabolism in bovine oocytes. Am. J. Physiol. Endocrinol. Metab. 2013, 304, E599–E613. [Google Scholar] [CrossRef] [Green Version]
- Bonnet, A.; Servin, B.; Mulsant, P.; Mandon-Pepin, B. Spatio-Temporal Gene Expression Profiling during In Vivo Early Ovarian Folliculogenesis: Integrated Transcriptomic Study and Molecular Signature of Early Follicular Growth. PLoS ONE 2015, 10, e0141482. [Google Scholar] [CrossRef]
- Paczkowski, M.; Silva, E.; Schoolcraft, W.B.; Krisher, R.L. Comparative Importance of Fatty Acid Beta-Oxidation to Nuclear Maturation, Gene Expression, and Glucose Metabolism in Mouse, Bovine, and Porcine Cumulus Oocyte Complexes1. Biol. Reprod. 2013, 88, 1–11. [Google Scholar] [CrossRef]
- Dunning, K.R.; Anastasi, M.R.; Zhang, V.J.; Russell, D.L.; Robker, R.L. Regulation of Fatty Acid Oxidation in Mouse Cumulus-Oocyte Complexes during Maturation and Modulation by PPAR Agonists. PLoS ONE 2014, 9, e87327. [Google Scholar] [CrossRef] [Green Version]
- Sanchez-Lazo, L.; Brisard, D.; Elis, S.; Maillard, V.; Uzbekov, R.; Labas, V.; Desmarchais, A.; Papillier, P.; Monget, P.; Uzbekova, S. Fatty Acid Synthesis and Oxidation in Cumulus Cells Support Oocyte Maturation in Bovine. Mol. Endocr. 2014, 28, 1502–1521. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leroy, J.L.M.R.; Vanholder, T.; Mateusen, B.; Christophe, A.; Opsomer, G.; de Kruif, A.; Genicot, G.; Van Soom, A. Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 2005, 130, 485–495. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Desmet, K.L.J.; Van Hoeck, V.; Gagné, D.; Fournier, E.; Thakur, A.; O’Doherty, A.M.; Walsh, C.P.; Sirard, M.A.; Bols, P.E.J.; Leroy, J.L.M.R. Exposure of bovine oocytes and embryos to elevated non-esterified fatty acid concentrations: Integration of epigenetic and transcriptomic signatures in resultant blastocysts. BMC Genomics 2016, 17, 1004. [Google Scholar] [CrossRef] [PubMed]
- Van Hoeck, V.; Leroy, J.L.M.R.; Arias Alvarez, M.; Rizos, D.; Gutierrez-Adan, A.; Schnorbusch, K.; Bols, P.E.J.; Leese, H.J.; Sturmey, R.G. Oocyte developmental failure in response to elevated nonesterified fatty acid concentrations: Mechanistic insights. Reproduction 2013, 145, 33–44. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leroy, J.; Sturmey, R.; Van Hoeck, V.; De Bie, J.; McKeegan, P.; Bols, P. Dietary Fat Supplementation and the Consequences for Oocyte and Embryo Quality: Hype or Significant Benefit for Dairy Cow Reproduction? Reprod. Dom. Anim. 2014, 49, 353–361. [Google Scholar] [CrossRef]
- Marei, W.F.A.; De Bie, J.; Mohey-Elsaeed, O.; Wydooghe, E.; Bols, P.E.J.; Leroy, J.L.M.R. Alpha-linolenic acid protects the developmental capacity of bovine cumulus–oocyte complexes matured under lipotoxic conditions in vitro†. Biol. Reprod. 2017, 96, 1181–1196. [Google Scholar] [CrossRef]
- Elis, S.; Freret, S.; Desmarchais, A.; Maillard, V.; Cognié, J.; Briant, E.; Touzé, J.-L.; Dupont, M.; Faverdin, P.; Chajès, V.; et al. Effect of a long chain n-3 PUFA-enriched diet on production and reproduction variables in Holstein dairy cows. Anim. Reprod. Sci. 2016, 164, 121–132. [Google Scholar] [CrossRef]
- Freret, S.; Oseikria, M.; Bourhis, D.L.; Desmarchais, A.; Briant, E.; Desnoes, O.; Dupont, M.; Le Berre, L.; Ghazouani, O.; Bertevello, P.S.; et al. Effects of a n-3 polyunsaturated fatty acid-enriched diet on embryo production in dairy cows. Reproduction 2019, 158, 71–83. [Google Scholar] [CrossRef] [Green Version]
- Moallem, U. Invited review: Roles of dietary n-3 fatty acids in performance, milk fat composition, and reproductive and immune systems in dairy cattle. J. Dairy Sci. 2018, 101, 8641–8661. [Google Scholar] [CrossRef] [Green Version]
- Zeron, Y.; Sklan, D.; Arav, A. Effect of polyunsaturated fatty acid supplementation on biophysical parameters and chilling sensitivity of ewe oocytes. Mol. Reprod. Dev. 2002, 61, 271–278. [Google Scholar] [CrossRef]
- Wakefield, S.L.; Lane, M.; Schulz, S.J.; Hebart, M.L.; Thompson, J.G.; Mitchell, M. Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse. Am. J. Physiol. Endocrinol. Metab. 2008, 294, E425–E434. [Google Scholar] [CrossRef] [PubMed]
- Oseikria, M.; Elis, S.; Maillard, V.; Corbin, E.; Uzbekova, S. N-3 polyunsaturated fatty acid DHA during IVM affected oocyte developmental competence in cattle. Theriogenology 2016, 85, 1625–1634. [Google Scholar] [CrossRef] [PubMed]
- Elis, S.; Oseikria, M.; Vitorino Carvalho, A.; Bertevello, P.S.; Corbin, E.; Teixeira-Gomes, A.-P.; Lecardonnel, J.; Archilla, C.; Duranthon, V.; Labas, V.; et al. Docosahexaenoic acid mechanisms of action on the bovine oocyte-cumulus complex. J. Ovarian Res. 2017, 10, 74. [Google Scholar] [CrossRef] [PubMed]
- Hoyos-Marulanda, V.; Alves, B.S.; Rosa, P.R.A.; Vieira, A.D.; Gasperin, B.G.; Mondadori, R.G.; Lucia, T. Effects of polyunsaturated fatty acids on the development of pig oocytes in vitro following parthenogenetic activation and on the lipid content of oocytes and embryos. Anim. Reprod. Sci. 2019, 205, 150–155. [Google Scholar] [CrossRef] [PubMed]
- Bertevello, P.; Teixeira-Gomes, A.-P.; Seyer, A.; Vitorino Carvalho, A.; Labas, V.; Blache, M.-C.; Banliat, C.; Cordeiro, L.; Duranthon, V.; Papillier, P.; et al. Lipid Identification and Transcriptional Analysis of Controlling Enzymes in Bovine Ovarian Follicle. Int. J. Mol.Sci. 2018, 19, 3261. [Google Scholar] [CrossRef] [Green Version]
- Uzbekova, S.; Elis, S.; Teixeira-Gomes, A.-P.; Desmarchais, A.; Maillard, V.; Labas, V. MALDI Mass Spectrometry Imaging of Lipids and Gene Expression Reveals Differences in Fatty Acid Metabolism between Follicular Compartments in Porcine Ovaries. Biology 2015, 4, 216–236. [Google Scholar] [CrossRef] [Green Version]
- González-Serrano, A.F.; Pirro, V.; Ferreira, C.R.; Oliveri, P.; Eberlin, L.S.; Heinzmann, J.; Lucas-Hahn, A.; Niemann, H.; Cooks, R.G. Desorption Electrospray Ionization Mass Spectrometry Reveals Lipid Metabolism of Individual Oocytes and Embryos. PLoS ONE 2013, 8, e74981. [Google Scholar] [CrossRef]
- Reader, K.; Stanton, J.-A.; Juengel, J. The Role of Oocyte Organelles in Determining Developmental Competence. Biology 2017, 6, 35. [Google Scholar] [CrossRef]
- Aardema, H.; van Tol, H.T.A.; Wubbolts, R.W.; Brouwers, J.F.H.M.; Gadella, B.M.; Roelen, B.A.J. Stearoyl-CoA desaturase activity in bovine cumulus cells protects the oocyte against saturated fatty acid stress. Biol. Reprod. 2017, 96, 982–992. [Google Scholar] [CrossRef] [Green Version]
- Downs, S.M.; Mosey, J.L.; Klinger, J. Fatty acid oxidation and meiotic resumption in mouse oocytes. Mol. Reprod. Dev. 2009, 76, 844–853. [Google Scholar] [CrossRef] [Green Version]
- Valsangkar, D.; Downs, S.M. A Requirement for Fatty Acid Oxidation in the Hormone-Induced Meiotic Maturation of Mouse Oocytes1. Biol. Reprod. 2013, 89, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Elis, S.; Desmarchais, A.; Maillard, V.; Uzbekova, S.; Monget, P.; Dupont, J. Cell proliferation and progesterone synthesis depend on lipid metabolism in bovine granulosa cells. Theriogenology 2015, 83, 840–853. [Google Scholar] [CrossRef] [PubMed]
- Dunning, K.R.; Robker, R.L. Promoting lipid utilization with l-carnitine to improve oocyte quality. Anim. Reprod. Sci. 2012, 134, 69–75. [Google Scholar] [CrossRef] [PubMed]
- Dunning, K.R.; Cashman, K.; Russell, D.L.; Thompson, J.G.; Norman, R.J.; Robker, R.L. Beta-Oxidation Is Essential for Mouse Oocyte Developmental Competence and Early Embryo Development1. Biol. Reprod. 2010, 83, 909–918. [Google Scholar] [CrossRef] [Green Version]
- Ferreira, C.R.; Saraiva, S.A.; Catharino, R.R.; Garcia, J.S.; Gozzo, F.C.; Sanvido, G.B.; Santos, L.F.A.; Lo Turco, E.G.; Pontes, J.H.F.; Basso, A.C.; et al. Single embryo and oocyte lipid fingerprinting by mass spectrometry. J. Lipid Res. 2010, 51, 1218–1227. [Google Scholar] [CrossRef] [Green Version]
- McEvoy, T.G.; Coull, G.D.; Broadbent, P.J.; Hutchinson, J.S.; Speake, B.K. Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J. Reprod. Fertil. 2000, 118, 163–170. [Google Scholar] [CrossRef]
- Genicot, G.; Leroy, J.L.M.R.; Soom, A.V.; Donnay, I. The use of a fluorescent dye, Nile red, to evaluate the lipid content of single mammalian oocytes. Theriogenology 2005, 63, 1181–1194. [Google Scholar] [CrossRef]
- Lapa, M.; Marques, C.; Alves, S.; Vasques, M.; Baptista, M.; Carvalhais, I.; Silva Pereira, M.; Horta, A.; Bessa, R.; Pereira, R. Effect of trans-10 cis-12 conjugated linoleic acid on Bovine Oocyte Competence and Fatty Acid Composition: Effects of t10,c12 CLA on Bovine Oocytes. Reprod. Dom. Anim. 2011, 46, 904–910. [Google Scholar] [CrossRef]
- González-Serrano, A.F.; Ferreira, C.R.; Pirro, V.; Lucas-Hahn, A.; Heinzmann, J.; Hadeler, K.-G.; Baulain, U.; Aldag, P.; Meyer, U.; Piechotta, M.; et al. Effects of long-term dietary supplementation with conjugated linoleic acid on bovine oocyte lipid profile. Reprod. Fertil. Dev. 2015, 28, 1326–1339. [Google Scholar] [CrossRef] [Green Version]
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Dalbies-Tran, R.; Cadoret, V.; Desmarchais, A.; Elis, S.; Maillard, V.; Monget, P.; Monniaux, D.; Reynaud, K.; Saint-Dizier, M.; Uzbekova, S. A Comparative Analysis of Oocyte Development in Mammals. Cells 2020, 9, 1002. https://doi.org/10.3390/cells9041002
Dalbies-Tran R, Cadoret V, Desmarchais A, Elis S, Maillard V, Monget P, Monniaux D, Reynaud K, Saint-Dizier M, Uzbekova S. A Comparative Analysis of Oocyte Development in Mammals. Cells. 2020; 9(4):1002. https://doi.org/10.3390/cells9041002
Chicago/Turabian StyleDalbies-Tran, Rozenn, Véronique Cadoret, Alice Desmarchais, Sébastien Elis, Virginie Maillard, Philippe Monget, Danielle Monniaux, Karine Reynaud, Marie Saint-Dizier, and Svetlana Uzbekova. 2020. "A Comparative Analysis of Oocyte Development in Mammals" Cells 9, no. 4: 1002. https://doi.org/10.3390/cells9041002
APA StyleDalbies-Tran, R., Cadoret, V., Desmarchais, A., Elis, S., Maillard, V., Monget, P., Monniaux, D., Reynaud, K., Saint-Dizier, M., & Uzbekova, S. (2020). A Comparative Analysis of Oocyte Development in Mammals. Cells, 9(4), 1002. https://doi.org/10.3390/cells9041002