The Interaction of NO and H2S in Boar Spermatozoa under Oxidative Stress

. 2022 Feb 28 ; 12 (5) : . [epub] 20220228

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35268171

Various recent studies dedicated to the role of nitric oxide (NO) and hydrogen sulfide (H2S) in somatic cells provide evidence for an interaction of the two gasotransmitters. In the case of male gametes, only the action of a single donor of each gasotransmitter has been investigated up until today. It has been demonstrated that, at low concentrations, both gasotransmitters alone exert a positive effect on sperm quality parameters. Moreover, the activity of gaseous cellular messengers may be affected by the presence of oxidative stress, an underlying condition of several male reproductive disorders. In this study, we explored the effect of the combination of two donors SNP and NaHS (NO and H2S donors, respectively) on boar spermatozoa under oxidative stress. We applied NaHS, SNP, and their combination (DD) at 100 nM concentration in boar spermatozoa samples treated with Fe2+/ascorbate system. After 90 min of incubation at 38 °C, we have observed that progressive motility (PMot) and plasma membrane integrity (PMI) were improved (p < 0.05) in DD treatment compared to the Ctr sample under oxidative stress (CtrOX). Moreover, the PMot of DD treatment was higher (p < 0.05) than that of NaHS. Similar to NaHS, SNP treatment did not overcome the PMot and PMI of CtrOX. In conclusion, for the first time, we provide evidence that the combination of SNP and NaHS surmounts the effect of single-donor application in terms of PMot and PMI in porcine spermatozoa under oxidative stress.

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Buzadzic B., Vucetic M., Jankovic A., Stancic A., Korac A., Korac B., Otasevic V. New insights into male (in)fertility: The importance of NO. Br. J. Pharmacol. 2015;172:1455–1467. doi: 10.1111/bph.12675. PubMed DOI PMC

Toor J.S., Sikka S.C. Human Spermatozoa and Interactions with Oxidative Stress. Volume 2. Elsevier Inc.; Amsterdam, The Netherlands: 2019.

Di Villa Bianca R.D.E., 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

Pintus E., Jovičić M., Kadlec M., Ros-Santaella J.L. Divergent effect of fast- and slow-releasing H2S donors on boar spermatozoa under oxidative stress. Sci. Rep. 2020;10:6508. doi: 10.1038/s41598-020-63489-4. PubMed DOI PMC

Kadlec M., Ros-Santaella J.L., Pintus E. The roles of no and h2s in sperm biology: Recent advances and new perspectives. Int. J. Mol. Sci. 2020;21:2174. doi: 10.3390/ijms21062174. PubMed DOI PMC

Otasevic V., Stancic A., Korac A., Jankovic A., Korac B. Reactive oxygen, nitrogen, and sulfur species in human male fertility. A crossroad of cellular signaling and pathology. BioFactors. 2020;46:206–219. doi: 10.1002/biof.1535. PubMed DOI

Lee N.P.Y., Cheng C.Y. Nitric oxide and cyclic nucleotides: Their roles in junction dynamics and spermatogenesis. Oxid. Med. Cell. Longev. 2008;1:25–32. doi: 10.4161/oxim.1.1.6856. PubMed DOI PMC

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

Wang R. Gasotransmitters: Growing pains and joys. Trends Biochem. Sci. 2014;39:227–232. doi: 10.1016/j.tibs.2014.03.003. PubMed DOI

Bahmanzadeh M., Abolhassani F., Amidi F., Ejtemaiemehr S.H., Salehi M., Abbasi M. The effects of nitric oxide synthase inhibitor (L-NAME) on epididymal sperm count, motility, and morphology in varicocelized rat. Mol. Cell. Neurosci. 2008;16:23–38.

Türkyilmaz Z., Gülen Ş., Sönmez K., Karabulut R., Dinçer S., Başaklar A.C., Kale N. Increased nitric oxide is accompanied by lipid oxidation in adolescent varicocele. Int. J. Androl. 2004;27:183–187. doi: 10.1111/j.1365-2605.2004.00474.x. PubMed DOI

Hellstrom W.J.G., Bell M., Wang R., Sikka S.C. Effect of sodium nitroprusside on sperm motility, viability, and lipid peroxidation. Fertil. Steril. 1994;61:1117–1122. doi: 10.1016/S0015-0282(16)56766-1. PubMed DOI

Wang J., Wang W., Li S., Han Y., Zhang P., Meng G., Xiao Y., Xie L., Wang X., Sha J., et al. Hydrogen Sulfide As a Potential Target in Preventing Spermatogenic Failure and Testicular Dysfunction. Antioxid. Redox Signal. 2018;28:1447–1462. doi: 10.1089/ars.2016.6968. PubMed DOI

Xia Y., Ning J., Cheng F., Yu W., Rao T., Ruan Y., Yuan R., Du Y. GYY4137 a H2S donor, attenuates ipsilateral epididymis injury in experimentally varicocele-induced rats via activation of the PI3K/Akt pathway. Iran. J. Basic Med. Sci. 2019;22:729–735. doi: 10.22038/ijbms.2019.30588.7372. PubMed DOI PMC

Li G., Xie Z.Z., Chua J.M.W., Wong P.C., Bian J. Hydrogen sulfide protects testicular germ cells against heat-induced injury. Nitric Oxide-Biol. Chem. 2015;46:165–171. doi: 10.1016/j.niox.2014.10.005. PubMed DOI

Hancock J.T., Whiteman M. Hydrogen sulfide signaling: Interactions with nitric oxide and reactive oxygen species. Ann. N. Y. Acad. Sci. 2016;1365:5–14. doi: 10.1111/nyas.12733. PubMed DOI

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

O’Flaherty C., Matsushita-Fournier D. Reactive oxygen species and protein modifications in spermatozoa. Biol. Reprod. 2017;97:577–585. doi: 10.1093/biolre/iox104. PubMed DOI

Aitken R.J., Jones K.T., Robertson S.A. Reactive oxygen species and sperm function-in sickness and in health. J. Androl. 2012;33:1096–1106. doi: 10.2164/jandrol.112.016535. PubMed DOI

Aitken R.J., Gibb Z., Baker M.A., Drevet J., Gharagozloo P. Causes and consequences of oxidative stress in Spermatozoa. Reprod. Fertil. Dev. 2016;28:1–10. doi: 10.1071/RD15325. PubMed DOI

Zhang W., Zhao Y., Zhang P., Hao Y., Yu S., Min L., Li L., Ma D., Chen L., Yi B., et al. Decrease in male mouse fertility by hydrogen sulfide and/or ammonia can Be inheritable. Chemosphere. 2018;194:147–157. doi: 10.1016/j.chemosphere.2017.11.164. PubMed DOI

Radi R. Oxygen radicals, nitric oxide, and peroxynitrite: Redox pathways in molecular medicine. Proc. Natl. Acad. Sci. USA. 2018;115:5839–5848. doi: 10.1073/pnas.1804932115. PubMed DOI PMC

Uribe P., Boguen R., Treulen F., Sänchez R., Villegas J.V. Peroxynitrite-mediated nitrosative stress decreases motility and mitochondrial membrane potential in human spermatozoa. Mol. Hum. Reprod. 2014;21:237–243. doi: 10.1093/molehr/gau107. PubMed DOI

Serrano R., Garrido N., Céspedes J.A., González-Fernández L., García-Marín L.J., Bragado M.J. Molecular Mechanisms Involved in the Impairment of Boar Sperm Motility by Peroxynitrite-Induced Nitrosative Stress. Int. J. Mol. Sci. 2020;21:1208. doi: 10.3390/ijms21041208. PubMed DOI PMC

Cirino G., Vellecco V., Bucci M. Nitric oxide and hydrogen sulfide: The gasotransmitter paradigm of the vascular system. Br. J. Pharmacol. 2017;174:4021–4031. doi: 10.1111/bph.13815. PubMed DOI PMC

Panthi S., Manandhar S., Gautam K. Hydrogen sulfide, nitric oxide, and neurodegenerative disorders. Transl. Neurodegener. 2018;7:3. doi: 10.1186/s40035-018-0108-x. PubMed DOI PMC

Wallace J.L., Ianaro A., de Nucci G. Gaseous Mediators in Gastrointestinal Mucosal Defense and Injury. Dig. Dis. Sci. 2017;62:2223–2230. doi: 10.1007/s10620-017-4681-0. PubMed DOI

King A.L., Polhemus D.J., Bhushan S., Otsuka H., Kondo K., Nicholson C.K., Bradley J.M., Islam K.N., Calvert J.W., Tao Y.X., et al. Hydrogen sulfide cytoprotective signaling is endothelial nitric oxide synthase-nitric oxide dependent. Proc. Natl. Acad. Sci. USA. 2014;111:3182–3187. doi: 10.1073/pnas.1321871111. PubMed DOI PMC

Staicu F.D., Lopez-Úbeda R., Romero-Aguirregomezcorta J., Martínez-Soto J.C., Matás Parra C. Regulation of boar sperm functionality by the nitric oxide synthase/nitric oxide system. J. Assist. Reprod. Genet. 2019;36:1721–1736. doi: 10.1007/s10815-019-01526-6. PubMed DOI PMC

Lee N.P.Y., Cheng C.Y. Nitric Oxide/Nitric Oxide Synthase, Spermatogenesis, and Tight Junction Dynamics. Biol. Reprod. 2004;70:267–276. doi: 10.1095/biolreprod.103.021329. PubMed DOI

Gangwar D.K., Atreja S.K. Signalling Events and Associated Pathways Related to the Mammalian Sperm Capacitation. Reprod. Domest. Anim. 2015;50:705–711. doi: 10.1111/rda.12541. PubMed DOI

Kolluru G.K., Shen X., Yuan S., Kevil C.G. Gasotransmitter heterocellular signaling. Antioxid. Redox Signal. 2017;26:936–960. doi: 10.1089/ars.2016.6909. PubMed DOI PMC

Ivanovic-Burmazovic I., Filipovic M.R. Saying NO to H2S: A Story of HNO, HSNO, and SSNO. Inorg. Chem. 2019;58:4039–4051. doi: 10.1021/acs.inorgchem.8b02592. PubMed DOI

Eberhardt M., Dux M., Namer B., Miljkovic J., Cordasic N., Will C., Kichko T.I., De La Roche J., Fischer M., Suárez S.A., et al. H2S and NO cooperatively regulate vascular tone by activating a neuroendocrine HNO-TRPA1-CGRP signalling pathway. Nat. Commun. 2014;5:4381. doi: 10.1038/ncomms5381. PubMed DOI PMC

Andrews K.L., Lumsden N.G., Farry J., Jefferis A.M., Kemp-Harper B.K., Chin-Dusting J.P.F. Nitroxyl: A vasodilator of human vessels that is not susceptible to tolerance. Clin. Sci. 2015;129:179–187. doi: 10.1042/CS20140759. PubMed DOI

Lopez B.E., Shinyashiki M., Han T.H., Fukuto J.M. Antioxidant actions of nitroxyl (HNO) Free Radic. Biol. Med. 2007;42:482–491. doi: 10.1016/j.freeradbiomed.2006.11.015. PubMed DOI

Nagpure B.V., Bian J.S. Interaction of Hydrogen Sulfide with Nitric Oxide in the Cardiovascular System. Oxid. Med. Cell. Longev. 2016;2016:6904327. doi: 10.1155/2016/6904327. PubMed DOI PMC

Kajimura M., Fukuda R., Bateman R.M., Yamamoto T., Suematsu M. Interactions of multiple gas-transducing systems: Hallmarks and uncertainties of CO, NO, and H2S Gas Biology. Antioxid. Redox Signal. 2010;13:157–192. doi: 10.1089/ars.2009.2657. PubMed DOI PMC

Harrison R.A.P., Vickers S.E. Use of fluorescent probes to assess membrane integrity in mammalian spermatozoa. J. Reprod. Fertil. 1990;88:343–352. doi: 10.1530/jrf.0.0880343. PubMed DOI

García-Vázquez F.A., Hernández-Caravaca I., Yánez-Quintana W., Matás C., Soriano-Úbeda C., Izquierdo-Rico M.J. Morphometry of boar sperm head and flagellum in semen backflow after insemination. Theriogenology. 2015;84:566–574. doi: 10.1016/j.theriogenology.2015.04.011. PubMed DOI

Brzezinska-Slebodzinska E., Slebodzinska A.B., B P., Wieczorek G. Antioxidant effect of vitamin E and glutathione on lipid peroxidation in boar semen plasma. Biol. Trace Elem. Res. 1995;47:69–74. doi: 10.1007/BF02790102. PubMed DOI

Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin. Biochem. 2004;37:277–285. doi: 10.1016/j.clinbiochem.2003.11.015. PubMed DOI

Yong Q.C., Hu L.F., Wang S., Huang D., Bian J.S. Hydrogen sulfide interacts with nitric oxide in the heart: Possible involvement of nitroxyl. Cardiovasc. Res. 2010;88:482–491. doi: 10.1093/cvr/cvq248. PubMed DOI

Yong Q.C., Cheong J.L., Hua F., Deng L.W., Khoo Y.M., Lee H.S., Perry A., Wood M., Whiteman M., Bian J.S. Regulation of heart function by endogenous gaseous mediators-crosstalk between nitric oxide and hydrogen sulfide. Antioxid. Redox Signal. 2011;14:2081–2091. doi: 10.1089/ars.2010.3572. PubMed DOI

Powell C.R., Dillon K.M., Matson J.B. A review of hydrogen sulfide (H2S) donors: Chemistry and potential therapeutic applications. Biochem. Pharmacol. 2018;149:110–123. doi: 10.1016/j.bcp.2017.11.014. PubMed DOI PMC

Jovičić M., Pintus E., Fenclová T., Imoník O.S., Chmelíková E., Ros-Santaella J.L., Sedmíková M. Effect of nitric oxide on boar sperm motility, membrane integrity, and acrosomal status during semen storage. Pol. J. Vet. Sci. 2018;21:73–82. doi: 10.24425/119024. PubMed DOI

Cooper C.E., Brown G.C. The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: Chemical mechanism and physiological significance. J. Bioenerg. Biomembr. 2008;40:533–539. doi: 10.1007/s10863-008-9166-6. PubMed DOI

Awda B.J., Mackenzie-bell M., Buhr M.M. Reactive Oxygen Species and Boar Sperm Function. Biol. Reprod. 2009;81:553–561. doi: 10.1095/biolreprod.109.076471. PubMed DOI

Cortese-Krott M.M., Fernandez B.O., Kelm M., Butler A.R., Feelisch M. On the chemical biology of the nitrite/sulfide interaction. Nitric Oxide-Biol. Chem. 2015;46:14–24. doi: 10.1016/j.niox.2014.12.009. PubMed DOI

Schulze M., Ruediger K., Mueller K., Jung M., Well C., Reissmann M. Development of an in vitro index to characterize fertilizing capacity of boar ejaculates. Anim. Reprod. Sci. 2013;140:70–76. doi: 10.1016/j.anireprosci.2013.05.012. PubMed DOI

Sutkeviciene N., Riskeviciene V., Januskauskas A., Zilinskas H., Andersson M. Assessment of sperm quality traits in relation to fertility in boar semen. Acta Vet. Scand. 2009;51:53. doi: 10.1186/1751-0147-51-53. PubMed DOI PMC

Gil M.A., Almiñana C., Roca J., Vázquez J.M., Martínez E.A. Boar semen variability and its effects on IVF efficiency. Theriogenology. 2008;70:1260–1268. doi: 10.1016/j.theriogenology.2008.06.004. PubMed DOI

Berger T., Anderson D.L., Penedo M.C.T. Porcine sperm fertilizing potential in relationship to sperm functional capacities. Anim. Reprod. Sci. 1996;44:231–239. doi: 10.1016/0378-4320(96)01565-5. DOI

Brito L.F.C., Barth A.D., Bilodeau-Goeseels S., Panich P.L., Kastelic J.P. Comparison of methods to evaluate the plasmalemma of bovine sperm and their relationship with in vitro fertilization rate. Theriogenology. 2003;60:1539–1551. doi: 10.1016/S0093-691X(03)00174-2. PubMed DOI

Ramu S., Jeyendran R.S. The hypo-osmotic swelling test for evaluation of sperm membrane integrity. Methods Mol. Biol. 2013;927:21–25. doi: 10.1007/978-1-62703-38-0_3. PubMed DOI

Beltrán C., Treviño C.L., Mata-Martínez E., Chávez J.C., Sánchez-Cárdenas C., Baker M., Darszon A. In: Sperm Acrosome Biogenesis and Function during Fertilization. Buffone M.G., editor. Volume 220. Springer International Publishing; Cham, Switzerland: 2016. Advances in Anatomy, Embryology and Cell Biology.

Aquila S., Giordano F., Guido C., Rago V., Carpino A. Nitric oxide involvement in the acrosome reaction triggered by leptin in pig sperm. Reprod. Biol. Endocrinol. 2011;9:133. doi: 10.1186/1477-7827-9-133. PubMed DOI PMC

Staicu F.-D., Parra C.M. Nitric Oxide Synthase-Simple Enzyme-Complex Roles. Volume i. InTech; London, UK: 2017. Nitric Oxide: Key Features in Spermatozoa; p. 13.

Revelli A., Costamagna C., Moffa F., Aldieri E., Ochetti S., Bosia A., Massobrio M., Lindblom B., Ghigo D. Signaling pathway of nitric oxide-induced acrosome reaction in human spermatozoa. Biol. Reprod. 2001;64:1708–1712. doi: 10.1095/biolreprod64.6.1708. PubMed DOI

Sengoku K., Tamate K., Yoshida T., Takaoka Y., Miyamoto T., Ishikawa M. Effects of low concentrations of nitric oxide on the zona pellucida binding ability of human spermatozoa. Fertil. Steril. 1998;69:522–527. doi: 10.1016/S0015-0282(97)00537-2. PubMed DOI

Hou M.L., Huang S.Y., Lai Y.K., Lee W.C. Geldanamycin augments nitric oxide production and promotes capacitation in boar spermatozoa. Anim. Reprod. Sci. 2008;104:56–68. doi: 10.1016/j.anireprosci.2007.01.006. PubMed DOI

Funahashi H. Induction of capacitation and the acrosome reaction of boar spermatozoa by L-arginine and nitric oxide synthesis associated with the anion transport system. Reproduction. 2002;124:857–864. doi: 10.1530/rep.0.1240857. PubMed DOI

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