FOXD1 Is a Transcription Factor Important for Uveal Melanocyte Development and Associated with High-Risk Uveal Melanoma
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. (sc)RNA-Seq Datasets and Identification of Melanocyte-Specific Markers Utilizing Public Datasets
2.2. Bulk RNA-Sequencing Dataset Analysis of the TCGA and ROMS Uveal Melanoma Cohort
2.3. Immunohistochemistry (IHC) of FOXD1
2.4. Statistical Analysis
3. Results
3.1. Identification of Ocular Melanocytic Clusters in Whole Zebrafish Single-Cell RNA Sequencing
3.2. Orthologue Prediction, Function Annotation and Expression Validation in Human Melanocytes and UM
3.3. RNA Expression Analysis of Transcription Regulator Genes of Interest in UM
3.4. FOXD1, ELL2, RBFOX2, KDM5B and REXO4 as and RNA-Based Biomarkers in Uveal Melanoma
3.5. Immunohistochemistry (IHC) of FOXD1 in Uveal Melanoma
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
Arp2-3 | Actin Related Protein 2/3 |
BAP1 | BRCA1 associated protein 1 |
Brg1 | Brahma-related gene 1 |
Cdc42 | Cell Division Cycle 42 |
CDH1 | Cadherin 1 |
CPM | Counts per mean |
dct | Dopachrome tautomerase |
DIOPT | DRSC integrative ortholog prediction tool |
ECM1 | Extracellular Matrix Protein 1 |
EIF1AX | Eukaryotic Translation Initiation Factor 1A X-Linked |
ELL2 | Elongation Factor For RNA Polymerase II 2 |
EMT | Epithelial-mesenchymal transition |
FOXD1 | Forkhead box D1 |
GEO | Gene expression omnibus |
GEP | Gene expression profiling |
hpf | Hours post fertilization |
HTR2B | 5-Hydroxytryptamine receptor 2B |
IHC | Immunohistochemistry |
IPA | Ingenuity pathway analysis |
IPSC | Induced pluripotent stem cells |
ISH | In situ hybridisation |
KDM5B | Lysine Demethylase 5B |
KO | Knock-out |
mitfa | Microphthalmia-associated transcription factor A |
mitfb | Microphthalmia-associated transcription factor B |
Myo10 | Myosin X |
OTX | Orthodenticle Homeobox |
PMEL | Premelanosome protein |
pmela | Premelanosome protein A |
pmelb | Premelanosome protein B |
RAB31 | Ras-related protein Rab-31 |
Rac1 | Rac Family Small GTPase 1 |
RAC1B | Rac Family Small GTPase 1B |
RBFOX2 | RNA Binding Fox-1 Homolog 2 |
REXO4 | REX4 Homolog, 3′-5′ Exonuclease |
ROMS | Rotterdam Ocular Melanoma Study |
roy | Roy Orbison |
scRNA-seq | Single-cell RNA sequencing |
SF3B1 | Splicing factor 3b Subunit 1 |
SNAI2 | Snail Family Transcriptional Repressor 2 |
TCGA | The Cancer Genome Atlas |
tyrp1b | Tyrosinase related protein 1B |
UM | Uveal melanoma |
UMAP | Uniform manifold approximation and projection |
WT | Wild-type |
References
- Pleasance, E.D.; Cheetham, R.K.; Stephens, P.J.; McBride, D.J.; Humphray, S.J.; Greenman, C.D.; Varela, I.; Lin, M.L.; Ordonez, G.R.; Bignell, G.R.; et al. A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 2010, 463, 191–196. [Google Scholar] [CrossRef] [PubMed]
- Royer-Bertrand, B.; Torsello, M.; Rimoldi, D.; El Zaoui, I.; Cisarova, K.; Pescini-Gobert, R.; Raynaud, F.; Zografos, L.; Schalenbourg, A.; Speiser, D.; et al. Comprehensive Genetic Landscape of Uveal Melanoma by Whole-Genome Sequencing. Am. J. Hum. Genet. 2016, 99, 1190–1198. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jager, M.J.; Shields, C.L.; Cebulla, C.M.; Abdel-Rahman, M.H.; Grossniklaus, H.E.; Stern, M.H.; Carvajal, R.D.; Belfort, R.N.; Jia, R.; Shields, J.A.; et al. Uveal melanoma. Nat. Rev. Dis. Primers 2020, 6, 24. [Google Scholar] [CrossRef] [PubMed]
- Singh, A.D.; Turell, M.E.; Topham, A.K. Uveal melanoma: Trends in incidence, treatment, and survival. Ophthalmology 2011, 118, 1881–1885. [Google Scholar] [CrossRef] [PubMed]
- Kujala, E.; Makitie, T.; Kivela, T. Very long-term prognosis of patients with malignant uveal melanoma. Investig. Ophthalmol. Vis. Sci. 2003, 44, 4651–4659. [Google Scholar] [CrossRef] [Green Version]
- Van Raamsdonk, C.D.; Griewank, K.G.; Crosby, M.B.; Garrido, M.C.; Vemula, S.; Wiesner, T.; Obenauf, A.C.; Wackernagel, W.; Green, G.; Bouvier, N.; et al. Mutations in GNA11 in uveal melanoma. N. Engl. J. Med. 2010, 363, 2191–2199. [Google Scholar] [CrossRef] [Green Version]
- Koopmans, A.E.; Verdijk, R.M.; Brouwer, R.W.; van den Bosch, T.P.; van den Berg, M.M.; Vaarwater, J.; Kockx, C.E.; Paridaens, D.; Naus, N.C.; Nellist, M.; et al. Clinical significance of immunohistochemistry for detection of BAP1 mutations in uveal melanoma. Mod. Pathol. 2014, 27, 1321–1330. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martin, M.; Masshofer, L.; Temming, P.; Rahmann, S.; Metz, C.; Bornfeld, N.; van de Nes, J.; Klein-Hitpass, L.; Hinnebusch, A.G.; Horsthemke, B.; et al. Exome sequencing identifies recurrent somatic mutations in EIF1AX and SF3B1 in uveal melanoma with disomy 3. Nat. Genet. 2013, 45, 933–936. [Google Scholar] [CrossRef] [Green Version]
- Yavuzyigitoglu, S.; Koopmans, A.E.; Verdijk, R.M.; Vaarwater, J.; Eussen, B.; van Bodegom, A.; Paridaens, D.; Kilic, E.; de Klein, A.; Rotterdam Ocular Melanoma Study Group. Uveal Melanomas with SF3B1 Mutations: A Distinct Subclass Associated with Late-Onset Metastases. Ophthalmology 2016, 123, 1118–1128. [Google Scholar] [CrossRef]
- Johansson, P.; Aoude, L.G.; Wadt, K.; Glasson, W.J.; Warrier, S.K.; Hewitt, A.W.; Kiilgaard, J.F.; Heegaard, S.; Isaacs, T.; Franchina, M.; et al. Deep sequencing of uveal melanoma identifies a recurrent mutation in PLCB4. Oncotarget 2016, 7, 4624–4631. [Google Scholar] [CrossRef] [Green Version]
- Moore, A.R.; Ceraudo, E.; Sher, J.J.; Guan, Y.; Shoushtari, A.N.; Chang, M.T.; Zhang, J.Q.; Walczak, E.G.; Kazmi, M.A.; Taylor, B.S.; et al. Recurrent activating mutations of G-protein-coupled receptor CYSLTR2 in uveal melanoma. Nat. Genet. 2016, 48, 675–680. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nathan, P.; Hassel, J.C.; Rutkowski, P.; Baurain, J.F.; Butler, M.O.; Schlaak, M.; Sullivan, R.J.; Ochsenreither, S.; Dummer, R.; Kirkwood, J.M.; et al. Overall Survival Benefit with Tebentafusp in Metastatic Uveal Melanoma. N. Engl. J. Med. 2021, 385, 1196–1206. [Google Scholar] [CrossRef] [PubMed]
- Jochems, A.; van der Kooij, M.K.; Fiocco, M.; Schouwenburg, M.G.; Aarts, M.J.; van Akkooi, A.C.; van den Berkmortel, F.; Blank, C.U.; van den Eertwegh, A.J.M.; Franken, M.G.; et al. Metastatic Uveal Melanoma: Treatment Strategies and Survival-Results from the Dutch Melanoma Treatment Registry. Cancers 2019, 11, 1007. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reddy, J.; Fonseca, M.A.S.; Corona, R.I.; Nameki, R.; Segato Dezem, F.; Klein, I.A.; Chang, H.; Chaves-Moreira, D.; Afeyan, L.K.; Malta, T.M.; et al. Predicting master transcription factors from pan-cancer expression data. Sci. Adv. 2021, 7, eabf6123. [Google Scholar] [CrossRef] [PubMed]
- Stemmler, M.P.; Eccles, R.L.; Brabletz, S.; Brabletz, T. Non-redundant functions of EMT transcription factors. Nat. Cell Biol. 2019, 21, 102–112. [Google Scholar] [CrossRef]
- Smit, K.N.; Boers, R.; Vaarwater, J.; Boers, J.; Brands, T.; Mensink, H.; Verdijk, R.M.; van IJcken, W.F.J.; Gribnau, J.; de Klein, A.; et al. Genome-wide aberrant methylation in primary metastatic UM and their matched metastases. Sci. Rep. 2022, 12, 42. [Google Scholar] [CrossRef] [PubMed]
- Smit, K.N.; Chang, J.; Derks, K.; Vaarwater, J.; Brands, T.; Verdijk, R.M.; Wiemer, E.A.C.; Mensink, H.W.; Pothof, J.; de Klein, A.; et al. Aberrant MicroRNA Expression and Its Implications for Uveal Melanoma Metastasis. Cancers 2019, 11, 815. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Robertson, A.G.; Shih, J.; Yau, C.; Gibb, E.A.; Oba, J.; Mungall, K.L.; Hess, J.M.; Uzunangelov, V.; Walter, V.; Danilova, L.; et al. Integrative Analysis Identifies Four Molecular and Clinical Subsets in Uveal Melanoma. Cancer Cell 2017, 32, 204–220.e15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mort, R.L.; Jackson, I.J.; Patton, E.E. The melanocyte lineage in development and disease. Development 2015, 142, 620–632. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Woodham, E.F.; Paul, N.R.; Tyrrell, B.; Spence, H.J.; Swaminathan, K.; Scribner, M.R.; Giampazolias, E.; Hedley, A.; Clark, W.; Kage, F.; et al. Coordination by Cdc42 of Actin, Contractility, and Adhesion for Melanoblast Movement in Mouse Skin. Curr. Biol. 2017, 27, 624–637. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Papalazarou, V.; Swaminathan, K.; Jaber-Hijazi, F.; Spence, H.; Lahmann, I.; Nixon, C.; Salmeron-Sanchez, M.; Arnold, H.H.; Rottner, K.; Machesky, L.M. The Arp2/3 complex is crucial for colonisation of the mouse skin by melanoblasts. Development 2020, 147, dev194555. [Google Scholar] [CrossRef] [PubMed]
- Marathe, H.G.; Watkins-Chow, D.E.; Weider, M.; Hoffmann, A.; Mehta, G.; Trivedi, A.; Aras, S.; Basuroy, T.; Mehrotra, A.; Bennett, D.C.; et al. BRG1 interacts with SOX10 to establish the melanocyte lineage and to promote differentiation. Nucleic Acids Res. 2017, 45, 6442–6458. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tokuo, H.; Bhawan, J.; Coluccio, L.M. Myosin X is required for efficient melanoblast migration and melanoma initiation and metastasis. Sci. Rep. 2018, 8, 10449. [Google Scholar] [CrossRef] [PubMed]
- Li, A.; Ma, Y.; Yu, X.; Mort, R.L.; Lindsay, C.R.; Stevenson, D.; Strathdee, D.; Insall, R.H.; Chernoff, J.; Snapper, S.B.; et al. Rac1 drives melanoblast organization during mouse development by orchestrating pseudopod- driven motility and cell-cycle progression. Dev. Cell 2011, 21, 722–734. [Google Scholar] [CrossRef] [Green Version]
- White, R.M.; Sessa, A.; Burke, C.; Bowman, T.; LeBlanc, J.; Ceol, C.; Bourque, C.; Dovey, M.; Goessling, W.; Burns, C.E.; et al. Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell 2008, 2, 183–189. [Google Scholar] [CrossRef] [Green Version]
- Lane, B.M.; Lister, J.A. Otx but not Mitf transcription factors are required for zebrafish retinal pigment epithelium development. PLoS ONE 2012, 7, e49357. [Google Scholar] [CrossRef] [Green Version]
- Watt, B.; van Niel, G.; Raposo, G.; Marks, M.S. PMEL: A pigment cell-specific model for functional amyloid formation. Pigment Cell Melanoma Res. 2013, 26, 300–315. [Google Scholar] [CrossRef] [Green Version]
- Cechmanek, P.B.; McFarlane, S. Retinal pigment epithelium expansion around the neural retina occurs in two separate phases with distinct mechanisms. Dev. Dyn. 2017, 246, 598–609. [Google Scholar] [CrossRef] [Green Version]
- Farnsworth, D.R.; Saunders, L.M.; Miller, A.C. A single-cell transcriptome atlas for zebrafish development. Dev. Biol. 2020, 459, 100–108. [Google Scholar] [CrossRef]
- Voigt, A.P.; Mulfaul, K.; Mullin, N.K.; Flamme-Wiese, M.J.; Giacalone, J.C.; Stone, E.M.; Tucker, B.A.; Scheetz, T.E.; Mullins, R.F. Single-cell transcriptomics of the human retinal pigment epithelium and choroid in health and macular degeneration. Proc. Natl. Acad. Sci. USA 2019, 116, 24100–24107. [Google Scholar] [CrossRef] [Green Version]
- Hao, Y.; Hao, S.; Andersen-Nissen, E.; Mauck, W.M., 3rd; Zheng, S.; Butler, A.; Lee, M.J.; Wilk, A.J.; Darby, C.; Zager, M.; et al. Integrated analysis of multimodal single-cell data. Cell 2021, 184, 3573–3587.e29. [Google Scholar] [CrossRef]
- Hu, Y.; Flockhart, I.; Vinayagam, A.; Bergwitz, C.; Berger, B.; Perrimon, N.; Mohr, S.E. An integrative approach to ortholog prediction for disease-focused and other functional studies. BMC Bioinform. 2011, 12, 357. [Google Scholar] [CrossRef] [Green Version]
- Kramer, A.; Green, J.; Pollard, J., Jr.; Tugendreich, S. Causal analysis approaches in Ingenuity Pathway Analysis. Bioinformatics 2014, 30, 523–530. [Google Scholar] [CrossRef]
- Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011, 17, 10–12. [Google Scholar] [CrossRef]
- Kim, D.; Langmead, B.; Salzberg, S.L. HISAT: A fast spliced aligner with low memory requirements. Nat. Methods 2015, 12, 357–360. [Google Scholar] [CrossRef] [Green Version]
- Anders, S.; Pyl, P.T.; Huber, W. HTSeq—A Python framework to work with high-throughput sequencing data. Bioinformatics 2015, 31, 166–169. [Google Scholar] [CrossRef] [PubMed]
- Harbour, J.W.; Chen, R. The DecisionDx-UM Gene Expression Profile Test Provides Risk Stratification and Individualized Patient Care in Uveal Melanoma. PLoS Curr. 2013, 5. [Google Scholar] [CrossRef] [PubMed]
- Wu, H.; Larribere, L.; Sun, Q.; Novak, D.; Sachindra, S.; Granados, K.; Umansky, V.; Utikal, J. Loss of neural crest-associated gene FOXD1 impairs melanoma invasion and migration via RAC1B downregulation. Int. J. Cancer 2018, 143, 2962–2972. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Z.; Pascal, L.E.; Chandran, U.R.; Chaparala, S.; Lv, S.; Ding, H.; Qi, L.; Wang, Z. ELL2 Is Required for the Growth and Survival of AR-Negative Prostate Cancer Cells. Cancer Manag. Res. 2020, 12, 4411–4427. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Zhong, M.; Song, Q.; Pascal, L.E.; Yang, Z.; Wu, Z.; Wang, K.; Wang, Z. Anti-apoptotic factor Birc3 is up-regulated by ELL2 knockdown and stimulates proliferation in LNCaP cells. Am. J. Clin. Exp. Urol. 2019, 7, 223–231. [Google Scholar] [PubMed]
- Ali, M.; Ajore, R.; Wihlborg, A.K.; Niroula, A.; Swaminathan, B.; Johnsson, E.; Stephens, O.W.; Morgan, G.; Meissner, T.; Turesson, I.; et al. The multiple myeloma risk allele at 5q15 lowers ELL2 expression and increases ribosomal gene expression. Nat. Commun. 2018, 9, 1649. [Google Scholar] [CrossRef] [PubMed]
- Qiu, X.; Pascal, L.E.; Song, Q.; Zang, Y.; Ai, J.; O’Malley, K.J.; Nelson, J.B.; Wang, Z. Physical and Functional Interactions between ELL2 and RB in the Suppression of Prostate Cancer Cell Proliferation, Migration, and Invasion. Neoplasia 2017, 19, 207–215. [Google Scholar] [CrossRef]
- Dai, B.; Hu, Z.; Huang, H.; Zhu, G.; Xiao, Z.; Wan, W.; Zhang, P.; Jia, W.; Zhang, L. Overexpressed KDM5B is associated with the progression of glioma and promotes glioma cell growth via downregulating p21. Biochem. Biophys. Res. Commun. 2014, 454, 221–227. [Google Scholar] [CrossRef] [PubMed]
- Chen, B.; Chen, H.; Lu, S.; Zhu, X.; Que, Y.; Zhang, Y.; Huang, J.; Zhang, L.; Zhang, Y.; Sun, F.; et al. KDM5B promotes tumorigenesis of Ewing sarcoma via FBXW7/CCNE1 axis. Cell Death Dis. 2022, 13, 354. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.; Li, W.; Wei, B.; Wu, K.; Liu, D.; Zhu, D.; Zhang, C.; Wen, F.; Fan, Y.; Zhao, S. MicroRNA let-7i Inhibits Histone Lysine Demethylase KDM5B to Halt Esophageal Cancer Progression. Mol. Ther. Nucleic Acids 2020, 22, 846–861. [Google Scholar] [CrossRef]
- Bamodu, O.A.; Huang, W.C.; Lee, W.H.; Wu, A.; Wang, L.S.; Hsiao, M.; Yeh, C.T.; Chao, T.Y. Aberrant KDM5B expression promotes aggressive breast cancer through MALAT1 overexpression and downregulation of hsa-miR-448. BMC Cancer 2016, 16, 160. [Google Scholar] [CrossRef] [Green Version]
- Ruan, Y.; Chen, W.; Gao, C.; Xu, Y.; Shi, M.; Zhou, Z.; Zhou, G. REXO4 acts as a biomarker and promotes hepatocellular carcinoma progression. J. Gastrointest. Oncol. 2021, 12, 3093–3106. [Google Scholar] [CrossRef] [PubMed]
- Chen, W.; Gao, C.; Shen, J.; Yao, L.; Liang, X.; Chen, Z. The expression and prognostic value of REXO4 in hepatocellular carcinoma. J. Gastrointest. Oncol. 2021, 12, 1704–1717. [Google Scholar] [CrossRef]
- Verma, S.K.; Deshmukh, V.; Thatcher, K.; Belanger, K.K.; Rhyner, A.M.; Meng, S.; Holcomb, R.J.; Bressan, M.; Martin, J.F.; Cooke, J.P.; et al. RBFOX2 is required for establishing RNA regulatory networks essential for heart development. Nucleic Acids Res. 2022, 50, 2270–2286. [Google Scholar] [CrossRef]
- Gehman, L.T.; Meera, P.; Stoilov, P.; Shiue, L.; O’Brien, J.E.; Meisler, M.H.; Ares, M., Jr.; Otis, T.S.; Black, D.L. The splicing regulator Rbfox2 is required for both cerebellar development and mature motor function. Genes Dev. 2012, 26, 445–460. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Newman, E.A.; Kim, D.W.; Wan, J.; Wang, J.; Qian, J.; Blackshaw, S. Foxd1 is required for terminal differentiation of anterior hypothalamic neuronal subtypes. Dev. Biol. 2018, 439, 102–111. [Google Scholar] [CrossRef] [PubMed]
- Hernandez-Bejarano, M.; Gestri, G.; Spawls, L.; Nieto-Lopez, F.; Picker, A.; Tada, M.; Brand, M.; Bovolenta, P.; Wilson, S.W.; Cavodeassi, F. Opposing Shh and Fgf signals initiate nasotemporal patterning of the zebrafish retina. Development 2015, 142, 3933–3942. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Braeutigam, C.; Rago, L.; Rolke, A.; Waldmeier, L.; Christofori, G.; Winter, J. The RNA-binding protein Rbfox2: An essential regulator of EMT-driven alternative splicing and a mediator of cellular invasion. Oncogene 2014, 33, 1082–1092. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, J.H.; Jeong, K.; Li, J.; Murphy, J.M.; Vukadin, L.; Stone, J.K.; Richard, A.; Tran, J.; Gillespie, G.Y.; Flemington, E.K.; et al. SON drives oncogenic RNA splicing in glioblastoma by regulating PTBP1/PTBP2 switching and RBFOX2 activity. Nat. Commun. 2021, 12, 5551. [Google Scholar] [CrossRef] [PubMed]
- Naro, C.; De Musso, M.; Delle Monache, F.; Panzeri, V.; de la Grange, P.; Sette, C. The oncogenic kinase NEK2 regulates an RBFOX2-dependent pro-mesenchymal splicing program in triple-negative breast cancer cells. J. Exp. Clin. Cancer Res. 2021, 40, 397. [Google Scholar] [CrossRef]
- Cooper, A.M.; Nutter, C.A.; Kuyumcu-Martinez, M.N.; Wright, C.W. Alternative Splicing of the Aryl Hydrocarbon Receptor Nuclear Translocator (ARNT) Is Regulated by RBFOX2 in Lymphoid Malignancies. Mol. Cell Biol. 2022, 42, e0050321. [Google Scholar] [CrossRef]
- Cao, J.; O’Day, D.R.; Pliner, H.A.; Kingsley, P.D.; Deng, M.; Daza, R.M.; Zager, M.A.; Aldinger, K.A.; Blecher-Gonen, R.; Zhang, F.; et al. A human cell atlas of fetal gene expression. Science 2020, 370, eaba7721. [Google Scholar] [CrossRef] [PubMed]
- Gautam, P.; Hamashima, K.; Chen, Y.; Zeng, Y.; Makovoz, B.; Parikh, B.H.; Lee, H.Y.; Lau, K.A.; Su, X.; Wong, R.C.B.; et al. Multi-species single-cell transcriptomic analysis of ocular compartment regulons. Nat. Commun. 2021, 12, 5675. [Google Scholar] [CrossRef]
- Herreros-Villanueva, M.; Zhang, J.S.; Koenig, A.; Abel, E.V.; Smyrk, T.C.; Bamlet, W.R.; de Narvajas, A.A.; Gomez, T.S.; Simeone, D.M.; Bujanda, L.; et al. SOX2 promotes dedifferentiation and imparts stem cell-like features to pancreatic cancer cells. Oncogenesis 2013, 2, e61. [Google Scholar] [CrossRef] [PubMed]
- Ray, D.; Yun, Y.C.; Idris, M.; Cheng, S.; Boot, A.; Iain, T.B.H.; Rozen, S.G.; Tan, P.; Epstein, D.M. A tumor-associated splice-isoform of MAP2K7 drives dedifferentiation in MBNL1-low cancers via JNK activation. Proc. Natl. Acad. Sci. USA 2020, 117, 16391–16400. [Google Scholar] [CrossRef]
- Malta, T.M.; Sokolov, A.; Gentles, A.J.; Burzykowski, T.; Poisson, L.; Weinstein, J.N.; Kaminska, B.; Huelsken, J.; Omberg, L.; Gevaert, O.; et al. Machine Learning Identifies Stemness Features Associated with Oncogenic Dedifferentiation. Cell 2018, 173, 338–354.e15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Field, M.G.; Kuznetsov, J.N.; Bussies, P.L.; Cai, L.Z.; Alawa, K.A.; Decatur, C.L.; Kurtenbach, S.; Harbour, J.W. BAP1 Loss Is Associated with DNA Methylomic Repatterning in Highly Aggressive Class 2 Uveal Melanomas. Clin. Cancer Res. 2019, 25, 5663–5673. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, D.; Fan, S.; Yu, F.; Zhu, X.; Song, Y.; Ye, M.; Fan, L.; Lv, Z. FOXD1 Promotes Cell Growth and Metastasis by Activation of Vimentin in NSCLC. Cell. Physiol. Biochem. 2018, 51, 2716–2731. [Google Scholar] [CrossRef] [PubMed]
- Sun, Q.; Novak, D.; Huser, L.; Poelchen, J.; Wu, H.; Granados, K.; Federico, A.; Liu, K.; Steinfass, T.; Vierthaler, M.; et al. FOXD1 promotes dedifferentiation and targeted therapy resistance in melanoma by regulating the expression of connective tissue growth factor. Int. J. Cancer 2021, 149, 657–674. [Google Scholar] [CrossRef]
- Chen, C.; Xu, Z.Q.; Zong, Y.P.; Ou, B.C.; Shen, X.H.; Feng, H.; Zheng, M.H.; Zhao, J.K.; Lu, A.G. CXCL5 induces tumor angiogenesis via enhancing the expression of FOXD1 mediated by the AKT/NF-kappaB pathway in colorectal cancer. Cell Death Dis. 2019, 10, 178. [Google Scholar] [CrossRef] [Green Version]
- Chang, S.; Sun, L.; Feng, G. SP1-mediated long noncoding RNA POU3F3 accelerates the cervical cancer through miR-127-5p/FOXD1. Biomed. Pharm. 2019, 117, 109133. [Google Scholar] [CrossRef]
- Nagel, S.; Meyer, C.; Kaufmann, M.; Drexler, H.G.; MacLeod, R.A. Deregulated FOX genes in Hodgkin lymphoma. Genes Chromosomes Cancer 2014, 53, 917–933. [Google Scholar] [CrossRef]
- Sun, D.S.; Guan, C.H.; Wang, W.N.; Hu, Z.T.; Zhao, Y.Q.; Jiang, X.M. LncRNA NORAD promotes proliferation, migration and angiogenesis of hepatocellular carcinoma cells through targeting miR-211-5p/FOXD1/VEGF-A axis. Microvasc. Res. 2021, 134, 104120. [Google Scholar] [CrossRef]
- Ma, X.L.; Shang, F.; Ni, W.; Zhu, J.; Luo, B.; Zhang, Y.Q. MicroRNA-338-5p plays a tumor suppressor role in glioma through inhibition of the MAPK-signaling pathway by binding to FOXD1. J. Cancer Res. Clin. Oncol. 2018, 144, 2351–2366. [Google Scholar] [CrossRef]
- Wu, Q.; Ma, J.; Wei, J.; Meng, W.; Wang, Y.; Shi, M. FOXD1-AS1 regulates FOXD1 translation and promotes gastric cancer progression and chemoresistance by activating the PI3K/AKT/mTOR pathway. Mol. Oncol. 2021, 15, 299–316. [Google Scholar] [CrossRef]
- Zhou, H.; Lv, Q.; Guo, Z. Transcriptomic signature predicts the distant relapse in patients with ER+ breast cancer treated with tamoxifen for five years. Mol. Med. Rep. 2018, 17, 3152–3157. [Google Scholar] [CrossRef] [Green Version]
- Chen, Y.; Liang, W.; Liu, K.; Shang, Z. FOXD1 promotes EMT and cell stemness of oral squamous cell carcinoma by transcriptional activation of SNAI2. Cell Biosci. 2021, 11, 154. [Google Scholar] [CrossRef] [PubMed]
- Serrano-Gomez, S.J.; Maziveyi, M.; Alahari, S.K. Regulation of epithelial-mesenchymal transition through epigenetic and post-translational modifications. Mol. Cancer 2016, 15, 18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Decatur, C.L.; Ong, E.; Garg, N.; Anbunathan, H.; Bowcock, A.M.; Field, M.G.; Harbour, J.W. Driver Mutations in Uveal Melanoma: Associations With Gene Expression Profile and Patient Outcomes. JAMA Ophthalmol. 2016, 134, 728–733. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Uner, O.E.; See, T.R.O.; Szalai, E.; Grossniklaus, H.E.; Stalhammar, G. Estimation of the timing of BAP1 mutation in uveal melanoma progression. Sci. Rep. 2021, 11, 8923. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
van den Bosch, Q.C.C.; Nguyen, J.Q.N.; Brands, T.; van den Bosch, T.P.P.; Verdijk, R.M.; Paridaens, D.; Naus, N.C.; de Klein, A.; Kiliç, E.; Brosens, E., on behalf of the Rotterdam Ocular Melanoma Study Group . FOXD1 Is a Transcription Factor Important for Uveal Melanocyte Development and Associated with High-Risk Uveal Melanoma. Cancers 2022, 14, 3668. https://doi.org/10.3390/cancers14153668
van den Bosch QCC, Nguyen JQN, Brands T, van den Bosch TPP, Verdijk RM, Paridaens D, Naus NC, de Klein A, Kiliç E, Brosens E on behalf of the Rotterdam Ocular Melanoma Study Group . FOXD1 Is a Transcription Factor Important for Uveal Melanocyte Development and Associated with High-Risk Uveal Melanoma. Cancers. 2022; 14(15):3668. https://doi.org/10.3390/cancers14153668
Chicago/Turabian Stylevan den Bosch, Quincy C. C., Josephine Q. N. Nguyen, Tom Brands, Thierry P. P. van den Bosch, Robert M. Verdijk, Dion Paridaens, Nicole C. Naus, Annelies de Klein, Emine Kiliç, and Erwin Brosens on behalf of the Rotterdam Ocular Melanoma Study Group . 2022. "FOXD1 Is a Transcription Factor Important for Uveal Melanocyte Development and Associated with High-Risk Uveal Melanoma" Cancers 14, no. 15: 3668. https://doi.org/10.3390/cancers14153668
APA Stylevan den Bosch, Q. C. C., Nguyen, J. Q. N., Brands, T., van den Bosch, T. P. P., Verdijk, R. M., Paridaens, D., Naus, N. C., de Klein, A., Kiliç, E., & Brosens, E., on behalf of the Rotterdam Ocular Melanoma Study Group . (2022). FOXD1 Is a Transcription Factor Important for Uveal Melanocyte Development and Associated with High-Risk Uveal Melanoma. Cancers, 14(15), 3668. https://doi.org/10.3390/cancers14153668