Selenium-Binding Protein 1 (SELENBP1) Supports Hydrogen Sulfide Biosynthesis and Adipogenesis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Reagents
2.2. Cell Culture, Cell Differentiation, and Pharmacological Treatments
2.3. Generation of Stable Knock-Down Cell Lines
2.4. Western Blotting
2.5. Cell Proliferation Assay
2.6. Mitochondrial Activity Assay
2.7. Extracellular Flux Analysis
2.8. Live Cell H2S Detection Using a Fluorescent Probe
2.9. Detection of Cellular Lipid Accumulation with Oil Red O Staining
2.10. Statistical Analysis
3. Results
3.1. Effect of SELENBP1 Knock-Down on Suppression of Adiponectin Expression
3.2. SELENBP1 Knock-Down Suppresses Lipid Accumulation during Adipocyte Differentiation
3.3. Cellular H2S Levels Increase during Adipocyte Differentiation: Inhibitory Effect of SELENBP1 Knock-Down
3.4. SELENBP1 Knock-Down Affects Cell Proliferation during Adipocyte Differentiation
3.5. Effect of SELENBP1 Knock-Down on Metabolic Activity
3.6. SELENBP1 Knock-Down Decreases Mitochondrial Bioenergetics
3.7. GYY4137 Modulates H2S-Producing Enzyme Expression in ShSELENBP1 Cells
3.8. H2S Donation Restores Lipid Accumulation in SELENBP1 Knock-Down Adipocytes
3.9. Effect of GYY4137 on Cellular H2S Levels in SELENBP1 Knock-Down Adipocytes
3.10. GYY4137 Improves Bioenergetics in SELENBP1 Knock-Down Adipocytes
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Szabo, C. A timeline of hydrogen sulfide (H2S) research: From environmental toxin to biological mediator. Biochem. Pharmacol. 2018, 149, 5–19. [Google Scholar] [CrossRef] [PubMed]
- Aroca, A.; Gotor, C.; Bassham, D.C.; Romero, L.C. Hydrogen sulfide: From a toxic molecule to a key molecule of cell life. Antioxidants 2020, 9, 621. [Google Scholar] [CrossRef]
- Kimura, H. Hydrogen sulfide as a neuromodulator. Mol. Neurobiol. 2002, 26, 13–19. [Google Scholar] [CrossRef]
- Szabo, C. Hydrogen sulphide and its therapeutic potential. Nat. Rev. Drug Discov. 2007, 6, 917–935. [Google Scholar] [CrossRef]
- Kimura, H. Hydrogen sulfide: Its production, release and functions. Amino Acids 2011, 41, 113–121. [Google Scholar] [CrossRef] [PubMed]
- Li, L.; Rose, P.; Moore, P.K. Hydrogen sulfide and cell signaling. Annu. Rev. Pharmacol. Toxicol. 2011, 51, 169–187. [Google Scholar] [CrossRef] [Green Version]
- Whiteman, M.; Winyard, P.G. Hydrogen sulfide and inflammation: The good, the bad, the ugly and the promising. Expert Rev. Clin. Pharmacol. 2011, 4, 13–32. [Google Scholar] [CrossRef]
- Predmore, B.L.; Lefer, D.J.; Gojon, G. Hydrogen sulfide in biochemistry and medicine. Antioxid. Redox. Signal. 2012, 17, 119–140. [Google Scholar] [CrossRef] [Green Version]
- Wang, R. Physiological implications of hydrogen sulfide: A whiff exploration that blossomed. Physiol. Rev. 2012, 92, 791–896. [Google Scholar] [CrossRef] [Green Version]
- Li, Q.; Lancaster, J.R., Jr. Chemical foundations of hydrogen sulfide biology. Nitric Oxide 2013, 35, 21–34. [Google Scholar] [CrossRef] [Green Version]
- Kimura, H. The physiological role of hydrogen sulfide and beyond. Nitric Oxide 2014, 41, 4–10. [Google Scholar] [CrossRef]
- Yang, G.; Wang, R. H2S and blood vessels: An overview. In Handbook of Experimental Pharmacolology; Springer: Cham, Switzerland, 2015; Volume 230, pp. 85–110. [Google Scholar]
- Wang, R.; Szabo, C.; Ichinose, F.; Ahmed, A.; Whiteman, M.; Papapetropoulos, A. The role of H2S bioavailability in endothelial dysfunction. Trends Pharmacol. Sci. 2015, 36, 568–578. [Google Scholar] [CrossRef] [Green Version]
- Papapetropoulos, A.; Whiteman, M.; Cirino, G. Pharmacological tools for hydrogen sulphide research: A brief, introductory guide for beginners. Br. J. Pharmacol. 2015, 172, 1633–1637. [Google Scholar] [CrossRef] [Green Version]
- Szabo, C. Hydrogen sulfide, an enhancer of vascular nitric oxide signaling: Mechanisms and implications. Am. J. Physiol. Cell. Physiol. 2017, 312, C3–C15. [Google Scholar] [CrossRef]
- Szabo, C.; Papapetropoulos, A. International Union of Basic and Clinical Pharmacology. CII: Pharmacological Modulation of H2S Levels: H2S Donors and H2S Biosynthesis Inhibitors. Pharmacol. Rev. 2017, 69, 497–564. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Blachier, F.; Andriamihaja, M.; Larraufie, P.; Ahn, E.; Lan, A.; Kim, E. Production of hydrogen sulfide by the intestinal microbiota and epithelial cells and consequences for the colonic and rectal mucosa. Am. J. Physiol. Gastrointest. Liver Physiol. 2020, 320, G125–G135. [Google Scholar] [CrossRef] [PubMed]
- Szabo, C. The re-emerging pathophysiological role of the cystathionine-beta-synthase—Hydrogen sulfide system in Down syndrome. FEBS J. 2020, 287, 3150–3160. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dilek, N.; Papapetropoulos, A.; Toliver-Kinsky, T.; Szabo, C. Hydrogen sulfide: An endogenous regulator of the immune system. Pharmacol. Res. 2020, 161, 105119. [Google Scholar] [CrossRef]
- Zuhra, K.; Augsburger, F.; Majtan, T.; Szabo, C. Cystathionine-β-synthase: Molecular regulation and pharmacological inhibition. Biomolecules 2020, 10, 697. [Google Scholar] [CrossRef]
- Cortese-Krott, M.M.; Koning, A.; Kuhnle, G.G.C.; Nagy, P.; Bianco, C.L.; Pasch, A.; Wink, D.A.; Fukuto, J.M.; Jackson, A.A.; van Goor, H.; et al. The reactive species interactome: Evolutionary emergence, biological significance, and opportunities for redox metabolomics and personalized medicine. Antioxid. Redox. Signal. 2017, 27, 684–712. [Google Scholar] [CrossRef] [Green Version]
- Kimura, H. Signaling by hydrogen sulfide (H2S) and polysulfides (H2Sn) in the central nervous system. Neurochem. Int. 2019, 126, 118–125. [Google Scholar] [CrossRef] [PubMed]
- Sies, H.; Jones, D.P. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat. Rev. Mol. Cell. Biol. 2020, 21, 363–383. [Google Scholar] [CrossRef] [PubMed]
- Shibuya, N.; Koike, S.; Tanaka, M.; Ishigami-Yuasa, M.; Kimura, Y.; Ogasawara, Y.; Fukui, K.; Nagahara, N.; Kimura, H. A novel pathway for the production of hydrogen sulfide from D-cysteine in mammalian cells. Nat. Commun. 2013, 4, 1366. [Google Scholar] [CrossRef] [Green Version]
- Souza, L.K.; Araújo, T.S.; Sousa, N.A.; Sousa, F.B.; Nogueira, K.M.; Nicolau, L.A.; Medeiros, J.V. Evidence that d-cysteine protects mice from gastric damage via hydrogen sulfide produced by d-amino acid oxidase. Nitric Oxide 2017, 64, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Akaike, T.; Ida, T.; Wei, F.Y.; Nishida, M.; Kumagai, Y.; Alam, M.M.; Ihara, H.; Sawa, T.; Matsunaga, T.; Kasamatsu, S.; et al. Cysteinyl-tRNA synthetase governs cysteine polysulfidation and mitochondrial bioenergetics. Nat. Commun. 2017, 8, 1177. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pol, A.; Renkema, G.H.; Tangerman, A.; Winkel, E.G.; Engelke, U.F.; de Brouwer, A.P.M.; Lloyd, K.C.; Araiza, R.S.; van den Heuvel, L.; Omran, H.; et al. Mutations in SELENBP1, encoding a novel human methanethiol oxidase, cause extraoral halitosis. Nat. Genet. 2018, 50, 120–129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Elhodaky, M.; Hong, L.K.; Kadkol, S.; Diamond, A.M. Selenium-binding protein 1 alters energy metabolism in prostate cancer cells. Prostate 2020, 80, 962–976. [Google Scholar] [CrossRef]
- Tangerman, A. Measurement and biological significance of the volatile sulfur compounds hydrogen sulfide, methanethiol and dimethyl sulfide in various biological matrices. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2009, 877, 3366–3377. [Google Scholar] [CrossRef]
- Zebisch, K.; Voigt, V.; Wabitsch, M.; Brandsch, M. Protocol for effective differentiation of 3T3-L1 cells to adipocytes. Anal. Biochem. 2012, 425, 88–90. [Google Scholar] [CrossRef]
- Randi, E.B.; Vervaet, B.; Tsachaki, M.; Porto, E.; Vermeylen, S.; Lindenmeyer, M.T.; Thuy, L.T.T.; Cohen, C.D.; Devuyst, O.; Kistler, A.D.; et al. The antioxidative role of cytoglobin in podocytes: Implications for a role in chronic kidney disease. Antioxid. Redox. Signal. 2020, 32, 1155–1171. [Google Scholar] [CrossRef]
- Augsburger, F.; Randi, E.B.; Jendly, M.; Ascencao, K.; Dilek, N.; Szabo, C. Role of 3-mercaptopyruvate sulfurtransferase in the regulation of proliferation, migration, and bioenergetics in murine colon cancer cells. Biomolecules 2020, 10, 447. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ascenção, K.; Dilek, N.; Augsburger, F.; Panagaki, T.; Zuhra, K.; Szabo, C. Pharmacological induction of mesenchymal-epithelial transition via inhibition of H2S biosynthesis and consequent suppression of ACLY activity in colon cancer cells. Pharmacol. Res. 2021, 165, 105393. [Google Scholar] [CrossRef]
- Szczesny, B.; Módis, K.; Yanagi, K.; Coletta, C.; Le Trionnaire, S.; Perry, A.; Wood, M.E.; Whiteman, M.; Szabo, C. AP39, a novel mitochondria-targeted hydrogen sulfide donor, stimulates cellular bioenergetics, exerts cytoprotective effects and protects against the loss of mitochondrial DNA integrity in oxidatively stressed endothelial cells in vitro. Nitric Oxide 2014, 41, 120–130. [Google Scholar] [CrossRef] [Green Version]
- Panagaki, T.; Randi, E.B.; Augsburger, F.; Szabo, C. Overproduction of H2S, generated by CBS, inhibits mitochondrial Complex IV and suppresses oxidative phosphorylation in Down syndrome. Proc. Natl. Acad. Sci. USA 2019, 116, 18769–18771. [Google Scholar] [CrossRef] [Green Version]
- Bucci, M.; Papapetropoulos, A.; Vellecco, V.; Zhou, Z.; Pyriochou, A.; Roussos, C.; Roviezzo, F.; Brancaleone, V.; Cirino, G. Hydrogen sulfide is an endogenous inhibitor of phosphodiesterase activity. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 1998–2004. [Google Scholar] [CrossRef] [Green Version]
- Bucci, M.; Papapetropoulos, A.; Vellecco, V.; Zhou, Z.; Zaid, A.; Giannogonas, P.; Cantalupo, A.; Dhayade, S.; Karalis, K.P.; Wang, R.; et al. cGMP-dependent protein kinase contributes to hydrogen sulfide-stimulated vasorelaxation. PLoS ONE 2012, 7, e53319. [Google Scholar] [CrossRef] [Green Version]
- Sheng, X.; Tucci, J.; Malvar, J.; Mittelman, S.D. Adipocyte differentiation is affected by media height above the cell layer. Int J. Obes. 2014, 38, 315–320. [Google Scholar] [CrossRef] [Green Version]
- Steinbrenner, H.; Micoogullari, M.; Hoang, N.A.; Bergheim, I.; Klotz, L.O.; Sies, H. Selenium-binding protein 1 (SELENBP1) is a marker of mature adipocytes. Redox. Biol. 2019, 20, 489–495. [Google Scholar] [CrossRef]
- Green, H.; Meuth, M. An established pre-adipose cell line and its differentiation in culture. Cell 1974, 3, 127–133. [Google Scholar] [CrossRef]
- Tsai, C.Y.; Peh, M.T.; Feng, W.; Dymock, B.W.; Moore, P.K. Hydrogen sulfide promotes adipogenesis in 3T3L1 cells. PLoS ONE 2015, 10, e0119511. [Google Scholar] [CrossRef] [PubMed]
- Cai, J.; Shi, X.; Wang, H.; Fan, J.; Feng, Y.; Lin, X.; Yang, J.; Cui, Q.; Tang, C.; Xu, G.; et al. Cystathionine γ lyase-hydrogen sulfide increases peroxisome proliferator-activated receptor γ activity by sulfhydration at C139 site thereby promoting glucose uptake and lipid storage in adipocytes. Biochim. Biophys. Acta Mol. Cell Biol. 2016, 1861, 419–429. [Google Scholar] [CrossRef]
- Yang, G.; Ju, Y.; Fu, M.; Zhang, Y.; Pei, Y.; Racine, M.; Baath, S.; Merritt, T.J.S.; Wang, R.; Wu, L. Cystathionine gamma-lyase/hydrogen sulfide system is essential for adipogenesis and fat mass accumulation in mice. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2018, 1863, 165–176. [Google Scholar] [CrossRef]
- Alkhouri, N.; Eng, K.; Cikach, F.; Patel, N.; Yan, C.; Brindle, A.; Rome, E.; Hanouneh, I.; Grove, D.; Lopez, R.; et al. Breathprints of childhood obesity: Changes in volatile organic compounds in obese children compared with lean controls. Pediatr. Obes. 2015, 10, 23–29. [Google Scholar] [CrossRef] [Green Version]
- Comas, F.; Latorre, J.; Ortega, F.; Arnoriaga Rodríguez, M.; Lluch, A.; Sabater, M.; Rius, F.; Ribas, X.; Costas, M.; Ricart, W.; et al. Morbidly obese subjects show increased serum sulfide in proportion to fat mass. Int. J. Obes. 2020, 45, 415–426. [Google Scholar] [CrossRef]
- Ding, Y.; Wang, H.; Geng, B.; Xu, G. Sulfhydration of perilipin 1 is involved in the inhibitory effects of cystathionine gamma lyase/hydrogen sulfide on adipocyte lipolysis. Biochem. Biophys. Res. Commun. 2020, 521, 786–790. [Google Scholar] [CrossRef]
- Li, M.; Xu, C.; Shi, J.; Ding, J.; Wan, X.; Chen, D.; Gao, J.; Li, C.; Zhang, J.; Lin, Y.; et al. Fatty acids promote fatty liver disease via the dysregulation of 3-mercaptopyruvate sulfurtransferase/hydrogen sulfide pathway. Gut 2018, 67, 2169–2180. [Google Scholar] [CrossRef]
- Peh, M.T.; Anwar, A.B.; Ng, D.S.; Atan, M.S.; Kumar, S.D.; Moore, P.K. Effect of feeding a high fat diet on hydrogen sulfide (H2S) metabolism in the mouse. Nitric Oxide 2014, 41, 138–145. [Google Scholar] [CrossRef]
- Katsouda, A.; Szabo, C.; Papapetropoulos, A. Reduced adipose tissue H2S in obesity. Pharmacol. Res. 2018, 128, 190–199. [Google Scholar] [CrossRef] [PubMed]
- Feng, X.; Chen, Y.; Zhao, J.; Tang, C.; Jiang, Z.; Geng, B. Hydrogen sulfide from adipose tissue is a novel insulin resistance regulator. Biochem. Biophys. Res. Commun. 2009, 380, 153–159. [Google Scholar] [CrossRef]
- Whiteman, M.; Gooding, K.M.; Whatmore, J.L.; Ball, C.I.; Mawson, D.; Skinner, K.; Tooke, J.E.; Shore, A.C. Adiposity is a major determinant of plasma levels of the novel vasodilator hydrogen sulphide. Diabetologia 2010, 53, 1722–1726. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Szabo, C.; Ransy, C.; Módis, K.; Andriamihaja, M.; Murghes, B.; Coletta, C.; Olah, G.; Yanagi, K.; Bouillaud, F. Regulation of mitochondrial bioenergetic function by hydrogen sulfide. Part I. Biochemical and physiological mechanisms. Br. J. Pharmacol. 2014, 171, 2099–2122. [Google Scholar] [CrossRef] [Green Version]
- Carter, R.N.; Morton, N.M. Cysteine and hydrogen sulphide in the regulation of metabolism: Insights from genetics and pharmacology. J. Pathol. 2016, 238, 321–332. [Google Scholar] [CrossRef] [Green Version]
- Bełtowski, J.; Jamroz-Wiśniewska, A. Hydrogen sulfide in the adipose tissue-physiology, pathology and a target for pharmacotherapy. Molecules 2016, 22, 63. [Google Scholar] [CrossRef] [Green Version]
- Katsouda, A.; Bibli, S.I.; Pyriochou, A.; Szabo, C.; Papapetropoulos, A. Regulation and role of endogenously produced hydrogen sulfide in angiogenesis. Pharmacol. Res. 2016, 113, 175–185. [Google Scholar] [CrossRef] [Green Version]
- Pichette, J.; Gagnon, J. Implications of hydrogen sulfide in glucose regulation: How H2S can alter glucose homeostasis through metabolic hormones. Oxid. Med. Cell. Longev. 2016, 2016, 3285074. [Google Scholar] [CrossRef] [Green Version]
- Candela, J.; Velmurugan, G.V.; White, C. Hydrogen sulfide depletion contributes to microvascular remodeling in obesity. Am. J. Physiol. Heart Circ. Physiol. 2016, 310, H1071–H1080. [Google Scholar] [CrossRef] [Green Version]
- Zhang, H.; Huang, Y.; Chen, S.; Tang, C.; Wang, G.; Du, J.; Jin, H. Hydrogen sulfide regulates insulin secretion and insulin resistance in diabetes mellitus, a new promising target for diabetes mellitus treatment? A review. J. Adv. Res. 2020, 27, 19–30. [Google Scholar] [CrossRef]
- Ali, A.; Wang, Y.; Wu, L.; Yang, G. Gasotransmitter signaling in energy homeostasis and metabolic disorders. Free Radic. Res. 2020, 23, 1–23. [Google Scholar] [CrossRef]
- Gheibi, S.; Samsonov, A.P.; Gheibi, S.; Vazquez, A.B.; Kashfi, K. Regulation of carbohydrate metabolism by nitric oxide and hydrogen sulfide: Implications in diabetes. Biochem. Pharmacol. 2020, 176, 113819. [Google Scholar] [CrossRef]
- Szabo, C. Hydrogen sulfide, an endogenous stimulator of mitochondrial function in cancer cells. Cells 2021, 10, 220. [Google Scholar] [CrossRef]
- Scislowski, P.W.; Pickard, K. The regulation of transaminative flux of methionine in rat liver mitochondria. Arch. Biochem. Biophys. 1994, 314, 412–416. [Google Scholar] [CrossRef]
- Yamada, H.; Akahoshi, N.; Kamata, S.; Hagiya, Y.; Hishiki, T.; Nagahata, Y.; Matsuura, T.; Takano, N.; Mori, M.; Ishizaki, Y.; et al. Methionine excess in diet induces acute lethal hepatitis in mice lacking cystathionine γ-lyase, an animal model of cystathioninuria. Free Radic. Biol. Med. 2012, 52, 1716–1726. [Google Scholar] [CrossRef]
- Zhao, C.; Zeng, H.; Wu, R.T.; Cheng, W.H. Loss of selenium-binding protein 1 decreases sensitivity to clastogens and intracellular selenium content in HeLa cells. PLoS ONE 2016, 11, e0158650. [Google Scholar] [CrossRef]
- Caswell, D.R.; Chuang, C.H.; Ma, R.K.; Winters, I.P.; Snyder, E.L.; Winslow, M.M. Tumor suppressor activity of Selenbp1, a direct Nkx2-1 target, in lung adenocarcinoma. Mol. Cancer Res. 2018, 16, 1737–1749. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Zhu, W.; Chen, X.; Wei, G.; Jiang, G.; Zhang, G. Selenium-binding protein 1 transcriptionally activates p21 expression via p53-independent mechanism and its frequent reduction associates with poor prognosis in bladder cancer. J. Transl. Med. 2020, 18, 17. [Google Scholar] [CrossRef]
- Shin, S.K.; Cho, H.W.; Song, S.E.; Im, S.S.; Bae, J.H.; Song, D.K. Oxidative stress resulting from the removal of endogenous catalase induces obesity by promoting hyperplasia and hypertrophy of white adipocytes. Redox. Biol. 2020, 37, 101749. [Google Scholar] [CrossRef]
- Nitta, Y.; Muraoka-Hirayama, S.; Sakurai, K. Catalase is required for peroxisome maintenance during adipogenesis. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2020, 1865, 158726. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 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 (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Randi, E.B.; Casili, G.; Jacquemai, S.; Szabo, C. Selenium-Binding Protein 1 (SELENBP1) Supports Hydrogen Sulfide Biosynthesis and Adipogenesis. Antioxidants 2021, 10, 361. https://doi.org/10.3390/antiox10030361
Randi EB, Casili G, Jacquemai S, Szabo C. Selenium-Binding Protein 1 (SELENBP1) Supports Hydrogen Sulfide Biosynthesis and Adipogenesis. Antioxidants. 2021; 10(3):361. https://doi.org/10.3390/antiox10030361
Chicago/Turabian StyleRandi, Elisa B., Giovanna Casili, Simona Jacquemai, and Csaba Szabo. 2021. "Selenium-Binding Protein 1 (SELENBP1) Supports Hydrogen Sulfide Biosynthesis and Adipogenesis" Antioxidants 10, no. 3: 361. https://doi.org/10.3390/antiox10030361
APA StyleRandi, E. B., Casili, G., Jacquemai, S., & Szabo, C. (2021). Selenium-Binding Protein 1 (SELENBP1) Supports Hydrogen Sulfide Biosynthesis and Adipogenesis. Antioxidants, 10(3), 361. https://doi.org/10.3390/antiox10030361