Hydrogen Sulfide Impairs Meiosis Resumption in Xenopuslaevis Oocytes
Language English Country Switzerland Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
31963573
PubMed Central
PMC7017156
DOI
10.3390/cells9010237
PII: cells9010237
Knihovny.cz E-resources
- Keywords
- Xenopus laevis, cell cycle, hydrogen sulfide, meiosis, oocyte,
- MeSH
- Apoptosis drug effects MeSH
- Cyclin B metabolism MeSH
- Cystathionine beta-Synthase antagonists & inhibitors metabolism MeSH
- Cystathionine gamma-Lyase antagonists & inhibitors metabolism MeSH
- Cytoplasm metabolism MeSH
- Maturation-Promoting Factor metabolism MeSH
- cdc25 Phosphatases metabolism MeSH
- Catalase metabolism MeSH
- Meiosis drug effects MeSH
- Metaphase drug effects MeSH
- Oocytes chemistry enzymology metabolism MeSH
- Meiotic Prophase I drug effects MeSH
- Protein Kinases metabolism MeSH
- Cell Cycle Proteins metabolism MeSH
- Xenopus Proteins metabolism MeSH
- Reactive Oxygen Species metabolism MeSH
- Signal Transduction drug effects MeSH
- Hydrogen Sulfide metabolism MeSH
- Sulfides metabolism pharmacology MeSH
- Sulfurtransferases antagonists & inhibitors metabolism MeSH
- Superoxide Dismutase metabolism MeSH
- Cell Survival drug effects MeSH
- Xenopus laevis MeSH
- Animals MeSH
- Check Tag
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- 3-mercaptopyruvate sulphurtransferase MeSH Browser
- CDC25C protein, human MeSH Browser
- CDK1 protein, Xenopus MeSH Browser
- Cyclin B MeSH
- Cystathionine beta-Synthase MeSH
- Cystathionine gamma-Lyase MeSH
- Maturation-Promoting Factor MeSH
- cdc25 Phosphatases MeSH
- Catalase MeSH
- Protein Kinases MeSH
- Cell Cycle Proteins MeSH
- Xenopus Proteins MeSH
- Reactive Oxygen Species MeSH
- sodium bisulfide MeSH Browser
- Hydrogen Sulfide MeSH
- Sulfides MeSH
- Sulfurtransferases MeSH
- Superoxide Dismutase MeSH
The role of hydrogen sulfide (H2S) is addressed in Xenopuslaevis oocytes. Three enzymes involved in H2S metabolism, cystathionine β-synthase, cystathionine γ-lyase, and 3-mercaptopyruvate sulfurtransferase, were detected in prophase I and metaphase II-arrested oocytes and drove an acceleration of oocyte meiosis resumption when inhibited. Moreover, meiosis resumption is associated with a significant decrease in endogenous H2S. On another hand, a dose-dependent inhibition was obtained using the H2S donor, NaHS (1 and 5 mM). NaHS impaired translation. NaHS did not induce the dissociation of the components of the M-phase promoting factor (MPF), cyclin B and Cdk1, nor directly impacted the MPF activity. However, the M-phase entry induced by microinjection of metaphase II MPF-containing cytoplasm was diminished, suggesting upstream components of the MPF auto-amplification loop were sensitive to H2S. Superoxide dismutase and catalase hindered the effects of NaHS, and this sensitivity was partially dependent on the production of reactive oxygen species (ROS). In contrast to other species, no apoptosis was promoted. These results suggest a contribution of H2S signaling in the timing of amphibian oocytes meiosis resumption.
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Qu K., Lee S.W., Bian J.S., Low C.-M., Wong P.T.-H. Hydrogen sulfide: Neurochemistry and neurobiology. Neurochem. Int. 2008;52:155–165. doi: 10.1016/j.neuint.2007.05.016. PubMed DOI
Wang X.-B., Du J.-B., Cui H. Signal pathways involved in the biological effects of sulfur dioxide. Eur. J. Pharmacol. 2015;764:94–99. doi: 10.1016/j.ejphar.2015.06.044. PubMed DOI
Wang R. Two’s company, three’s a crowd: Can H2S be the third endogenous gaseous transmitter? FASEB J. 2002;16:1792–1798. doi: 10.1096/fj.02-0211hyp. PubMed DOI
Shibuya N., Tanaka M., Yoshida M., Ogasawara Y., Togawa T., Ishii K., Kimura H. 3-Mercaptopyruvate Sulfurtransferase Produces Hydrogen Sulfide and Bound Sulfane Sulfur in the Brain. Antioxid. Redox Signal. 2009;11:703–714. doi: 10.1089/ars.2008.2253. PubMed DOI
Zhao H., Chan S.-J., Ng Y.-K., Wong P.T.-H. Brain 3-Mercaptopyruvate Sulfurtransferase (3MST): Cellular Localization and Downregulation after Acute Stroke. PLoS ONE. 2013;8:e67322. doi: 10.1371/journal.pone.0067322. PubMed DOI PMC
Liang R., Yu W., Du J., Yang L., Shang M., Guo J. Localization of cystathionine beta synthase in mice ovaries and its expression profile during follicular development. Chin. Med. J. (Engl.) 2006;119:1877–1883. doi: 10.1097/00029330-200611020-00006. PubMed DOI
Sugiura Y., Kashiba M., Maruyama K., Hoshikawa K., Sasaki R., Saito K., Kimura H., Goda N., Suematsu M. Cadmium exposure alters metabolomics of sulfur-containing amino acids in rat testes. Antioxid. Redox Signal. 2005;7:781–787. doi: 10.1089/ars.2005.7.781. PubMed DOI
Patel P., Vatish M., Heptinstall J., Wang R., Carson R.J. The endogenous production of hydrogen sulphide in intrauterine tissues. Reprod. Biol. Endocrinol. 2009;7:10. doi: 10.1186/1477-7827-7-10. PubMed DOI PMC
Srilatha B., Hu L., Adaikan G.P., Moore P.K. Initial characterization of hydrogen sulfide effects in female sexual function. J. Sex. Med. 2009;6:1875–1884. doi: 10.1111/j.1743-6109.2009.01291.x. PubMed DOI
Guzmán M.A., Navarro M.A., Carnicer R., Sarría A.J., Acín S., Arnal C., Muniesa P., Surra J.C., Arbonés-Mainar J.M., Maeda N., et al. Cystathionine beta-synthase is essential for female reproductive function. Hum. Mol. Genet. 2006;15:3168–3176. doi: 10.1093/hmg/ddl393. PubMed DOI
Oi Y., Imafuku M., Shishido C., Kominato Y., Nishimura S., Iwai K. Garlic supplementation increases testicular testosterone and decreases plasma corticosterone in rats fed a high protein diet. J. Nutr. 2001;131:2150–2156. doi: 10.1093/jn/131.8.2150. PubMed DOI
Srilatha B., Adaikan P.G., Moore P.K. Possible role for the novel gasotransmitter hydrogen sulphide in erectile dysfunction—A pilot study. Eur. J. Pharmacol. 2006;535:280–282. doi: 10.1016/j.ejphar.2006.02.001. PubMed DOI
Ghasemi M., Dehpour A.R., Moore K.P., Mani A.R. Role of endogenous hydrogen sulfide in neurogenic relaxation of rat corpus cavernosum. Biochem. Pharmacol. 2012;83:1261–1268. doi: 10.1016/j.bcp.2012.01.026. PubMed DOI
Srilatha B., Adaikan P.G., Li L., Moore P.K. Hydrogen sulphide: A novel endogenous gasotransmitter facilitates erectile function. J. Sex. Med. 2007;4:1304–1311. doi: 10.1111/j.1743-6109.2007.00561.x. PubMed DOI
D’Emmanuele di Villa Bianca R., Sorrentino R., Maffia P., Mirone V., Imbimbo C., Fusco F., De Palma R., Ignarro L.J., Cirino G. Hydrogen sulfide as a mediator of human corpus cavernosum smooth-muscle relaxation. Proc. Natl. Acad. Sci. USA. 2009;106:4513–4518. doi: 10.1073/pnas.0807974105. PubMed DOI PMC
Hemminki K., Niemi M.L. Community study of spontaneous abortions : Relation to occupation and air pollution by sulfur dioxid, hydrogen sulfide, and carbon disulfide. Int. Arch. Occup. Environ. Health. 1982;51:55–63. doi: 10.1007/BF00378410. PubMed DOI
Zhu X.Y., Gu H., Ni X. Hydrogen sulfide in the endocrine and reproductive systems. Expert Rev. Clin. Pharmacol. 2011;4:75–82. doi: 10.1586/ecp.10.125. PubMed DOI
Yang G., Wu L., Jiang B., Yang W., Qi J., Cao K., Meng Q., Mustafa A.K., Mu W., Zhang S., et al. H2S as a physiologic vasorelaxant: Hypertension in mice with deletion of cystathionine gamma-lyase. Science. 2008;322:587–590. doi: 10.1126/science.1162667. PubMed DOI PMC
Liang R., Yu W.-D., Du J.-B., Yang L.-J., Yang J.-J., Xu J., Shang M., Guo J.-Z. Cystathionine beta synthase participates in murine oocyte maturation mediated by homocysteine. Reprod. Toxicol. 2007;24:89–96. doi: 10.1016/j.reprotox.2007.04.002. PubMed DOI
Krejcova T., Smelcova M., Petr J., Bodart J.-F., Sedmikova M., Nevoral J., Dvorakova M., Vyskocilova A., Weingartova I., Kucerova-Chrpova V., et al. Hydrogen sulfide donor protects porcine oocytes against aging and improves the developmental potential of aged porcine oocytes. PLoS ONE. 2015;10:e0116964. doi: 10.1371/journal.pone.0116964. PubMed DOI PMC
Nevoral J., Žalmanová T., Zámostná K., Kott T., Kučerová-Chrpová V., Bodart J.-F., Gelaude A., Procházka R., Orsák M., Šulc M., et al. Endogenously produced hydrogen sulfide is involved in porcine oocyte maturation in vitro. Nitric Oxide. 2015;51:24–35. doi: 10.1016/j.niox.2015.09.007. PubMed DOI
Nevoral J., Petr J., Gelaude A., Bodart J.F., Kucerova-Chrpova V., Sedmikova M., Krejcova T., Kolbabova T., Dvorakova M., Vyskocilova A., et al. Dual effects of hydrogen sulfide donor on meiosis and cumulus expansion of porcine cumulus-oocyte complexes. PLoS ONE. 2014;1:9. doi: 10.1371/journal.pone.0099613. PubMed DOI PMC
Masui Y., Markert C.L. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J. Exp. Zool. 1971;177:129–145. doi: 10.1002/jez.1401770202. PubMed DOI
Rime H., Huchon D., De Smedt V., Thibier C., Galaktionov K., Jessus C., Ozon R. Microinjection of Cdc25 protein phosphatase into Xenopus prophase oocyte activates MPF and arrests meiosis at metaphase I. Biol. Cell. 1994;82:11–22. doi: 10.1016/0248-4900(94)90061-2. PubMed DOI
Ferrell J.E., Wu M., Gerhart J.C., Martin G.S. Cell cycle tyrosine phosphorylation of p34cdc2 and a microtubule-associated protein kinase homolog in Xenopus oocytes and eggs. Mol. Cell. Biol. 1991;11:1965–1971. doi: 10.1128/MCB.11.4.1965. PubMed DOI PMC
Baert F., Bodart J.-F., Bocquet-Muchembled B., Lescuyer-Rousseau A., Vilain J.-P. Xp42(Mpk1) activation is not required for germinal vesicle breakdown but for Raf complete phosphorylation in insulin-stimulated Xenopus oocytes. J. Biol. Chem. 2003;278:49714–49720. doi: 10.1074/jbc.M308067200. PubMed DOI
Dupré A., Jessus C., Ozon R., Haccard O. Mos is not required for the initiation of meiotic maturation in Xenopus oocytes. EMBO J. 2002;21:4026–4036. doi: 10.1093/emboj/cdf400. PubMed DOI PMC
Furuno N., Kawasaki A., Sagata N. Expression of cell-cycle regulators during Xenopus oogenesis. Gene Expr. Patterns. 2003;3:165–168. doi: 10.1016/S1567-133X(03)00037-1. PubMed DOI
Ferrell J.E., Jr., Machleder E.M. The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes. Science. 1998;280:895–898. doi: 10.1126/science.280.5365.895. PubMed DOI
Bagowski C.P., Besser J., Frey C.R., Ferrell J.E., Jr. The JNK cascade as a biochemical switch in mammalian cells: Ultrasensitive and all-or-none responses. Curr. Biol. 2003;13:315–320. doi: 10.1016/S0960-9822(03)00083-6. PubMed DOI
Bhatt R.R., Ferrell J.E., Jr. The protein kinase p90 rsk as an essential mediator of cytostatic factor activity. Science. 1999;286:1362–1365. doi: 10.1126/science.286.5443.1362. PubMed DOI
Bhatt R.R., Ferrell J.E., Jr. Cloning and characterization of Xenopus Rsk2, the predominant p90 Rsk isozyme in oocytes and eggs. J. Biol. Chem. 2000;275:32983–32990. doi: 10.1074/jbc.M006386200. PubMed DOI
Szabó C. Hydrogen sulphide and its therapeutic potential. Nat. Rev. Drug Discov. 2007;6:917–935. doi: 10.1038/nrd2425. PubMed DOI
Gaffré M., Martoriati A., Belhachemi N., Chambon J.P., Houliston E., Jessus C., Karaiskou A. A critical balance between Cyclin B synthesis and Myt1 activity controls meiosis entry in Xenopus oocytes. Development. 2011;138:3735–3744. doi: 10.1242/dev.063974. PubMed DOI
Morel M., Vanderstraete M., Cailliau K., Hahnel S., Grevelding C.G., Dissous C. SmShb, the SH2-Containing Adaptor Protein B of Schistosoma mansoni Regulates Venus Kinase Receptor Signaling Pathways. PLoS ONE. 2016;11:e0163283. doi: 10.1371/journal.pone.0163283. PubMed DOI PMC
Tokmakov A.A., Iguchi S., Iwasaki T., Fukami Y. Unfertilized frog eggs die by apoptosis following meiotic exit. BMC Cell Biol. 2011;12:56. doi: 10.1186/1471-2121-12-56. PubMed DOI PMC
Sigel E. Use of Xenopus oocytes for the functional expression of plasma membrane proteins. J. Membr. Biol. 1990;117:201–221. doi: 10.1007/BF01868451. PubMed DOI
Cailliau K., Browaeys-Poly E. A microinjectable biological system, the Xenopus oocyte, as an approach to understanding signal transduction protein function. Methods Mol. Biol. 2009;518:43–55. PubMed
Truong D.H., Eghbal M.A., Hindmarsh W., Roth S.H., O’Brien P.J. Molecular mechanisms of hydrogen sulfide toxicity. Drug Metab. Rev. 2006;38:733–744. doi: 10.1080/03602530600959607. PubMed DOI
Eghbal M.A., Pennefather P.S., O’Brien P.J. H2S cytotoxicity mechanism involves reactive oxygen species formation and mitochondrial depolarisation. Toxicology. 2004;203:69–76. doi: 10.1016/j.tox.2004.05.020. PubMed DOI
Dehennaut V., Lefebvre T., Sellier C., Leroy Y., Gross B., Walker S., Cacan R., Michalski J.-C., Vilain J.-P., Bodar J.-F. O-linked N-acetylglucosaminyltransferase inhibition prevents G2/M transition in Xenopus laevis oocytes. J. Biol. Chem. 2007;282:12527–12536. doi: 10.1074/jbc.M700444200. PubMed DOI
Coll O., Morales A., Fernández-Checa J.C., Garcia-Ruiz C. Neutral sphingomyelinase-induced ceramide triggers germinal vesicle breakdown and oxidant-dependent apoptosis in Xenopus laevis oocytes. J. Lipid Res. 2007;48:1924–1935. doi: 10.1194/jlr.M700069-JLR200. PubMed DOI
Zhou Y., Ma C., Karmouch J., Katbi H.A., Liu X.J. Antiapoptotic role for ornithine decarboxylase during oocyte maturation. Mol. Cell. Biol. 2009;29:1786–1795. doi: 10.1128/MCB.01815-08. PubMed DOI PMC
Du Pasquier D., Dupré A., Jessus C. Unfertilized Xenopus eggs die by Bad-dependent apoptosis under the control of Cdk1 and JNK. PLoS ONE. 2011;6:e23672. doi: 10.1371/journal.pone.0023672. PubMed DOI PMC
Bhatia M., Wong F.L., Fu D., Lau H.Y., Moochhala S.M., Moore P.K. Role of hydrogen sulfide in acute pancreatitis and associated lung injury. FASEB J. 2005;19:623–625. doi: 10.1096/fj.04-3023fje. PubMed DOI
Soleymanlou N., Jurisica I., Nevo O., Ietta F., Zhang X., Zamudio S., Post M., Caniggia I. Molecular evidence of placental hypoxia in preeclampsia. J. Clin. Endocrinol. Metab. 2005;90:4299–4308. doi: 10.1210/jc.2005-0078. PubMed DOI PMC
Reynhout J.K., Smith L.D. Studies on the appearance and nature of a maturation-inducing factor in the cytoplasm of amphibian oocytes exposed to progesterone. Dev. Biol. 1974;38:394–400. doi: 10.1016/0012-1606(74)90016-5. PubMed DOI
Drury K.C., Schorderet-Slatkine S. Effects of cycloheximide on the “autocatalytic” nature of the maturation promoting factor (MPF) in oocytes of Xenopus laevis. Cell. 1975;4:269–274. doi: 10.1016/0092-8674(75)90175-0. PubMed DOI
Wasserman W.J., Masui Y. Effects of cyclohexamide on a cytoplasmic factor initiating meiotic naturation in Xenopus oocytes. Exp. Cell Res. 1975;91:381–388. doi: 10.1016/0014-4827(75)90118-4. PubMed DOI
Karaïskou A., Jessus C., Brassac T., Ozon R. Phosphatase 2A and polo kinase, two antagonistic regulators of cdc25 activation and MPF auto-amplification. J. Cell Sci. 1999;112:3747–3756. PubMed
Karaiskou A., Leprêtre A.-C., Pahlavan G., Du Pasquier D., Ozon R., Jessus C. Polo-like kinase confers MPF autoamplification competence to growing Xenopus oocytes. Development. 2004;131:1543–1552. doi: 10.1242/dev.01050. PubMed DOI
Abrieu A., Brassac T., Galas S., Fisher D., Labbé J.C., Dorée M. The Polo-like kinase Plx1 is a component of the MPF amplification loop at the G2/M-phase transition of the cell cycle in Xenopus eggs. J. Cell Sci. 1998;111:1751–1757. PubMed
Hochegger H., Klotzbücher A., Kirk J., Howell M., le Guellec K., Fletcher K., Duncan T., Sohail M., Hunt T. New B-type cyclin synthesis is required between meiosis I and II during Xenopus oocyte maturation. Development. 2001;128:3795–3807. PubMed
Dorée M., Hunt T. From Cdc2 to Cdk1: When did the cell cycle kinase join its cyclin partner? J. Cell Sci. 2002;115:2461–2464. PubMed
Kimura H. Hydrogen sulfide induces cyclic AMP and modulates the NMDA receptor. Biochem. Biophys. Res. Commun. 2000;267:129–133. doi: 10.1006/bbrc.1999.1915. PubMed DOI
Iciek M., Kowalczyk-Pachel D., Bilska-Wilkosz A., Kwiecień I., Górny M., Włodek L. S-sulfhydration as a cellular redox regulation. Biosci. Rep. 2015;36:e00304. doi: 10.1042/BSR20150147. PubMed DOI PMC
Kimura H. Physiological role of hydrogen sulfide and polysulfide in the central nervous system. Neurochem. Int. 2013;63:492–497. doi: 10.1016/j.neuint.2013.09.003. PubMed DOI
Krishnan N., Fu C., Pappin D.J., Tonks N.K. H2S-Induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci. Signal. 2011;4:ra86. doi: 10.1126/scisignal.2002329. PubMed DOI PMC
Viry E., Anwar A., Kirsch G., Jacob C., Diederich M., Bagrel D. Antiproliferative effect of natural tetrasulfides in human breast cancer cells is mediated through the inhibition of the cell division cycle 25 phosphatases. Int. J. Oncol. 2011;38:1103–1111. PubMed
Tomko R.J., Lazo J.S. Multimodal control of Cdc25A by nitrosative stress. Cancer Res. 2008;68:7457–7465. doi: 10.1158/0008-5472.CAN-08-0625. PubMed DOI PMC
Foster M.W., Forrester M.T., Stamler J.S. A protein microarray-based analysis of S-nitrosylation. Proc. Natl. Acad. Sci. USA. 2009;106:18948–18953. doi: 10.1073/pnas.0900729106. PubMed DOI PMC
Majumdar U., Biswas P., Subhra Sarkar T., Maiti D., Ghosh S. Regulation of cell cycle and stress responses under nitrosative stress in Schizosaccharomyces pombe. Free Radic. Biol. Med. 2012;52:2186–2200. doi: 10.1016/j.freeradbiomed.2012.03.026. PubMed DOI
Rudolph J. Redox regulation of the Cdc25 phosphatases. Antioxid. Redox Signal. 2005;7:761–767. doi: 10.1089/ars.2005.7.761. PubMed DOI
Chen J., Lin L., Su J., Li B., Zhang X., Chen T. Proteomic analysis of G2/M arrest triggered by natural borneol/curcumin in HepG2 cells, the importance of ROS-p53 pathway. J. Agric. Food Chem. 2015;63:6440–6449. doi: 10.1021/acs.jafc.5b01773. PubMed DOI
Peng A., Lewellyn A.L., Maller J.L. DNA damage signaling in early Xenopus embryos. Cell Cycle. 2008;7:3–6. doi: 10.4161/cc.7.1.5157. PubMed DOI
Berger L., Wilde A. Glycolytic metabolites are critical modulators of oocyte maturation and viability. PLoS ONE. 2013;8:e77612. doi: 10.1371/journal.pone.0077612. PubMed DOI PMC
Mishanina T.V., Libiad M., Banerjee R. Biogenesis of reactive sulfur species for signaling by hydrogen sulfide oxidation pathways. Nat. Chem. Biol. 2015;11:457–464. doi: 10.1038/nchembio.1834. PubMed DOI PMC
Olson K.R., Gao Y., DeLeon E.R., Arif M., Arif F., Arora N., Straub K.D. Catalase as a sulfide-sulfur oxido-reductase: An ancient (and modern?) regulator of reactive sulfur species (RSS) Redox Biol. 2017;12:325–339. doi: 10.1016/j.redox.2017.02.021. PubMed DOI PMC
Jeseta M.J., Bodart J.-F.L. In: Aneuploidy in Health and Disease. Storchova Z., editor. Volume 10. InTech Open; Rijeka, Croatia: 2012. pp. 193–216.
Hydrogen sulfide and its role in female reproduction