Peroxynitrite-mediated nitrosative stress decreases motility and mitochondrial membrane potential in human spermatozoa

Molecular Human Reproduction

Volumn 21, Issue 3, 2014, Pages 237-243

  Uribe, P ^a   Boguen, R ^a   Treulen, F ^a   Sanchez R ^a   Villegas, J V ^a,b  

^a UNIVERSIDAD DE LA FRONTERA   (Chile)

^b UNIVERSIDAD DE LA FRONTERA   (Chile)

Author keywords

Infertility; Mitochondrial membrane potential; Peroxynitrite; Reactive nitrogen species; Sperm motility

Indexed keywords

DIHYDRORHODAMINE 123; LINSIDOMINE; PEROXYNITRITE; 5,5',6,6'-TETRACHLORO-1,1',3,3'-TETRAETHYLBENZIMIDAZOLOCARBOCYANINE; BENZIMIDAZOLE DERIVATIVE; CARBOCYANINE; FLUORESCENT DYE; MOLSIDOMINE; PEROXYNITROUS ACID; RHODAMINE;

AMPLITUDE OF LATERAL HEAD DISPLACEMENT; ARTICLE; AVERAGE PATH VELOCITY; BEAT CROSS FREQUENCY; CELL VIABILITY; COMPUTER ANALYSIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CURVILINEAR VELOCITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; INCUBATION TEMPERATURE; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; NITROSATIVE STRESS; NORMAL HUMAN; OXIDATION; PRIORITY JOURNAL; PROPIDIUM IODIDE ASSAY; SEMEN ANALYSIS; SPECTROPHOTOMETRY; SPERMATOZOON LINEARITY; SPERMATOZOON MOTILITY; SPERMATOZOON STRAIGHTNESS; SPERMATOZOON VIABILITY; SPERMATOZOON WOBBLE; STRAIGHT LINE VELOCITY; UROGENITAL SYSTEM PARAMETERS; ADULT; ANALOGS AND DERIVATIVES; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; OXIDATIVE STRESS; PHYSIOLOGY; SPECTROFLUOROMETRY; SPERMATOZOON;

ADULT; BENZIMIDAZOLES; CARBOCYANINES; CELL SURVIVAL; FLUORESCENT DYES; HUMANS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MOLSIDOMINE; OXIDATIVE STRESS; PEROXYNITROUS ACID; RHODAMINES; SEMEN ANALYSIS; SPECTROMETRY, FLUORESCENCE; SPERM MOTILITY; SPERMATOZOA;

EID: 84924500421     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gau107     Document Type: Article

References (51)

1. Agbani E,CoatsP,Wadsworth RM. Threshold of peroxynitrite cytotoxicity in bovine pulmonary artery endothelial and smooth muscle cells. Toxicol In Vitro 2011;25:1680-1686.
2. Aitken RJ, Whiting S, De Iuliis GN, McClymont S, Mitchell LA, Baker MA. Electrophilic aldehydes generated by sperm metabolism activate mitochondrial reactive oxygen species generation and apoptosis by targeting succinate dehydrogenase. J Biol Chem 2012;287:33048-33060.
3. Aksoy Y, Ozbey I, Aksoy H, Polat O, Akcay F. Seminal plasma nitric oxide concentration in oligo- and/or asthenozoospermic subjects with/ without varicocele. Arch Androl 2002;48:181-185.
4. Amiri I, Sheikh N, NajafiR. Nitric oxide level in seminal plasma and its relation with sperm DNA damages. Iran Biomed J 2007;11:259-264.
5. Aziz N, Novotny J, Oborna I, Fingerova H, Brezinova J, Svobodova M. Comparison of chemiluminescence and flow cytometry in the estimation of reactive oxygen and nitrogen species in human semen. Fertil Steril 2010;94:2604-2608.
6. Balercia G, Moretti S, Vignini A, Magagnini M, Mantero F, Boscaro M, Ricciardo-Lamonica G, Mazzanti L. Role of nitric oxide concentrations on human sperm motility. J Androl 2004;25:245-249.
7. Belen HerreroM, Chatterjee S, Lefievre L, de Lamirande E, Gagnon C. Nitric oxide interacts with thecAMPpathway to modulate capacitation of human spermatozoa. Free Radic Biol Med 2000;29:522-536.
8. Blanco Garcia J, Aldinucci C, Maiorca SM, Palmi M, Valoti M, Buonocore G, Pessina GP. Physiopathological effects of the NO donor 3-morpholinosydnonimine on rat cortical synaptosomes. Neurochem Res 2009;34:931-941.
9. Buchczyk DP, Grune T, Sies H, Klotz LO. Modifications of glyceraldehyde-3-phosphate dehydrogenase induced by increasing concentrations of peroxynitrite: early recognition by 20S proteasome. Biol Chem 2003;384:237-241.
10. Crow JP. Dichlorodihydrofluorescein and dihydrorhodamine 123 are sensitive indicators of peroxynitrite in vitro: implications for intracellular measurement of reactive nitrogen and oxygen species. Nitric Oxide 1997;1:145-157.
11. Ehren I, Adolfsson J,Wiklund NP. Nitric oxide synthase activity in the human urogenital tract. Urol Res 1994;22:287-290.
12. Espinoza JA, Schulz MA, Sanchez R, Villegas JV. Integrity of mitochondrial membranepotential reflectshumanspermquality. Andrologia 2009;41:51-54.
13. Gharagozloo P, Aitken RJ. The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. Hum Reprod 2011; 26:1628-1640.
14. Herrero MB, Cebral E, Boquet M, Viggiano JM, Vitullo A, Gimeno MA. Effect of nitric oxide on mouse sperm hyperactivation. Acta Physiol Pharmacol Ther Latinoam 1994;44:65-69.
15. Herrero MB, Perez Martinez S, Viggiano JM, Polak JM, de Gimeno MF. Localization by indirect immunofluorescence of nitric oxide synthase in mouse and human spermatozoa. Reprod Fertil Dev 1996;8:931-934.
16. Kasai T, Ogawa K, Mizuno K, Nagai S, Uchida Y, Ohta S, Fujie M, Suzuki K, Hirata S, Hoshi K. Relationship between sperm mitochondrial membrane potential, sperm motility, and fertility potential. Asian J Androl 2002;4:97-103.
17. Khosravi F, Valojerdi MR, Amanlou M, Karimian L, Abolhassani F. Relationship of seminal reactive nitrogen and oxygen species and total antioxidant capacity with sperm DNA fragmentation in infertile couples with normal and abnormal sperm parameters. Andrologia 2012;46:17-23.
18. Koeck T, Levison B, Hazen SL, Crabb JW, Stuehr DJ, Aulak KS. Tyrosine nitration impairs mammalian aldolase A activity. Mol Cell Proteomics 2004;3:548-557.
19. Lewis SE, Donnelly ET, Sterling ES, Kennedy MS, Thompson W, Chakravarthy U. Nitric oxide synthase and nitrite production in human spermatozoa: evidence that endogenous nitric oxide is beneficial to sperm motility. Mol Hum Reprod 1996;2:873-878.
20. Makker K, Agarwal A, Sharma R. Oxidative stress and male infertility. Indian J Med Res 2009;129:357-367.
21. Marchetti C, Obert G, Deffosez A, Formstecher P, Marchetti P. Study of mitochondrial membrane potential, reactive oxygen species, DNA fragmentation and cell viability by flow cytometry in human sperm. Hum Reprod 2002;17:1257-1265.
22. Medeiros CM, Forell F, Oliveira AT, Rodrigues JL. Current status of sperm cryopreservation: why isn't it better? Theriogenology 2002;57:327-344.
23. Miraglia E, De Angelis F, Gazzano E, Hassanpour H, Bertagna A, Aldieri E, Revelli A, Ghigo D. Nitric oxide stimulates human sperm motility via activation of the cyclic GMP/protein kinase G signaling pathway. Reproduction 2011;141:47-54.
24. Mitropoulos D, Deliconstantinos G, Zervas A, Villiotou V, Dimopoulos C, Stavrides J. Nitric oxide synthase and xanthine oxidase activities in the spermatic vein of patients with varicocele: a potential role for nitric oxide and peroxynitrite in sperm dysfunction. J Urology 1996;156:1952-1958.
25. Mukai C, Okuno M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol Reprod 2004; 71:540-547.
26. Nascimento JM, Shi LZ, Tam J, Chandsawangbhuwana C, Durrant B, Botvinick EL, Berns MW. Comparison of glycolysis and oxidative phosphorylation as energy sources for mammalian sperm motility, using the combination of fluorescence imaging, laser tweezers, and real-time automated tracking and trapping. J Cell Physiol 2008;217:745-751.
27. Nash KM, Rockenbauer A, Villamena FA. Reactive nitrogen species reactivities with nitrones: theoretical and experimental studies. Chem Res Toxicol 2012;25:1581-1597.
28. Nobunaga T, Tokugawa Y, Hashimoto K, Kubota Y, Sawai K, Kimura T, Shimoya K, Takemura M, Matsuzaki N, Azuma C et al. Elevated nitric oxide concentration in the seminal plasma of infertile males: nitric oxide inhibits sperm motility. Am J Reprod Immunol 1996;36:193-197.
29. O'BryanMK, Zini A, ChengCY, Schlegel PN.Humansperm endothelial nitric oxide synthase expression: correlation with sperm motility. Fertil Steril 1998;70:1143-1147.
30. Oztezcan S, Turkoglu UM, Kervancioglu E, Kocak T, Kocak-Toker N, Aykac-Toker G. In vitro effects of peroxynitrite on human spermatozoa. Andrologia 1999;31:195-198.
31. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007;87:315-424.
32. Radi R, Beckman JS, Bush KM, Freeman BA. Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys 1991;288:481-487.
33. Radi R, Cassina A, Hodara R. Nitric oxide and peroxynitrite interactions with mitochondria. Biol Chem 2002;383:401-409.
34. Revelli A, Soldati G, Costamagna C, Pellerey O, Aldieri E, Massobrio M, Bosia A, Ghigo D. Follicular fluid proteins stimulate nitric oxide (NO) synthesis in human sperm: a possible role for NO in acrosomal reaction. J Cell Physiol 1999;178:85-92.
35. Rodriguez PC, BeconiMT. Peroxynitrite participates in mechanisms involved in capacitation of cryopreserved cattle. Anim Reprod Sci 2009;110:96-107.
36. Rodriguez PC,O'FlahertyCM, BeconiMT, BeorleguiNB. Nitric oxide-induced capacitation of cryopreserved bull spermatozoa and assessment of participating regulatory pathways. Anim Reprod Sci 2005;85:231-242.
37. Rosselli M, Dubey RK, Imthurn B, Macas E, Keller PJ. Effects of nitric oxide on human spermatozoa: evidence that nitric oxide decreases sperm motility and induces sperm toxicity. Hum Reprod 1995;10:1786-1790.
38. Salvolini E, Buldreghini E, Lucarini G, Vignini A, Di Primio R, Balercia G. Nitric oxide synthase and tyrosine nitration in idiopathic asthenozoospermia: an immunohistochemical study. Fertil Steril 2012;97:554-560.
39. Santiso R, Tamayo M, Gosalvez J, Johnston S, Marino A, Fernandez C, Losada C, Fernandez JL. DNA fragmentation dynamics allows the assessment of cryptic sperm damage in human: evaluation of exposure to ionizing radiation, hyperthermia, acidic pH and nitric oxide. Mutat Res 2012;734:41-49.
40. 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.
41. Souza JM, Radi R. Glyceraldehyde-3-phosphate dehydrogenase inactivation by peroxynitrite. Arch Biochem Biophys 1998;360:187-194.
42. Szabo C, Ischiropoulos H, Radi R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov 2007;6:662-680.
43. Tomlinson MJ, East SJ, Barratt CL, Bolton AE, Cooke ID. Preliminary communication: possible role of reactive nitrogen intermediates in leucocyte-mediated sperm dysfunction. AmJ Reprod Immunol 1992;27:89-92.
44. Uckert S, Stanarius A, Stief CG, Wolf G, Jonas U, Machtens S. Immunocytochemical distribution of nitric oxide synthase in the human seminal vesicle: a light and electron microscopical study. Urol Res 2003; 31:262-266.
45. Vignini A, Nanetti L, Buldreghini E, Moroni C, Ricciardo-Lamonica G, Mantero F, Boscaro M, Mazzanti L, Balercia G. The production of peroxynitrite by human spermatozoa may affect sperm motility through the formation of protein nitrotyrosine. Fertil Steril 2006;85:947-953.
46. VigniniA,Buldreghini E,NanettiL,AmorosoS, BoscaroM,Ricciardo-LamonicaG, Mazzanti L, Balercia G. Free thiols in human spermatozoa: are Na+/ K+-ATPase, Ca2+-ATPase activities involved in sperm motility through peroxynitrite formation? Reprod Biomed Online 2009;18:132-140.
47. Weinberg JB, Doty E, Bonaventura J, Haney AF. Nitric oxide inhibition of human sperm motility. Fertil Steril 1995;64:408-413.
48. World Health Organization. WHOLaboratory Manual for the Examination and Processing of Human Semen, 5th edn. Geneva: WHO press, 2010.
49. WuTP, Huang BM, Tsai HC, Lui MC, LiuMY. Effects of nitric oxide on human spermatozoa activity, fertilization and mouse embryonic development. Arch Androl 2004;50:173-179.
50. Zini A,DeLamirande E, Gagnon C. Lowlevels of nitric oxide promote human sperm capacitation in vitro. J Androl 1995;16:424-431.
51. Zini A, O'Bryan MK, Magid MS, Schlegel PN. Immunohistochemical localization of endothelial nitric oxide synthase in human testis, epididymis, and vas deferens suggests a possible role for nitric oxide in spermatogenesis, sperm maturation, and programmed cell death. Biol Reprod 1996;55:935-941.