Role of reactive nitrogen species in male infertility

Reproductive Biology and Endocrinology

Volumn 10, Issue , 2012, Pages

  Doshi, Sejal B ^a   Khullar, Karishma ^a   Sharma, Rakesh K ^a   Agarwal, Ashok ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Infertility; Nitric oxide; Oxidative stress; Reactive nitrogen species

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; REACTIVE NITROGEN SPECIES;

APOPTOSIS; BLOOD TESTIS BARRIER; CAPILLARY ELECTROPHORESIS; CHEMILUMINESCENCE IMMUNOASSAY; CHEMOLUMINESCENCE; DIABETES MELLITUS; ELECTROCHEMICAL ANALYSIS; ERECTILE DYSFUNCTION; FLOW CYTOMETRY; HUMAN; LIPID PEROXIDATION; MALE GENITAL SYSTEM; MALE INFERTILITY; MEASUREMENT; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; VARICOCELE; ZONA PELLUCIDA;

FEMALE; HUMANS; INFERTILITY, MALE; MALE; MODELS, BIOLOGICAL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDATIVE STRESS; REACTIVE NITROGEN SPECIES; REPRODUCTION; TESTIS;

EID: 84870942445     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-10-109     Document Type: Review

References (69)

1. Agarwal A, Prabakaran SA. Mechanism, measurement, and prevention of oxidative stress in male reproductive physiology. Indian J Exp Biol 2005, 43:963-974.
2. Kreeger KY, Rubbo H, Radi R, Trujillo M, Telleri R, Kalyanaraman B, Barnes S, Kirk M, Freeman BA. Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. J Biol Chem 1994, 269:26066-26075.
3. Sampson JB, Rosen H, Beckman JS. Peroxynitrite dependent tyrosine nitration catalyzed by superoxide dismutase, myeloperoxidase and horseradish peroxidase. Methods Enzvmol 1996, 269:210-218.
4. Agarwal A, Makker K, Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol 2008, 59:2-11.
5. Pryor WA, Squadrito GL. The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am J Physiol 1995, 12:L699-L722.
6. Tarpey MM, Beckman JS, Ischiropoulos H, Gore JS, Brock TA. Peroxynitrite stimulates vascular smooth muscle cell cyclic GMP synthesis. FEBS Lett 1995, 364:314-318. 10.1016/0014-5793(95)00413-4, 7758588.
7. Kothari S, Thompson A, Agarwal A, du Plessis SS. Free radicals: their beneficial and detrimental effects on sperm function. Indian J Exp Biol 2010, 48:425-435.
8. Beckman JS, Carson M, Smith CD, Koppenol WH. ALS, SOD and peroxynitrite. Nature Lond 1993, 364:584. 10.1038/364584a0, 8350919.
9. de Lamirande E, Gagnon C. Capacitation-associated production of superoxide anion by human spermatozoa. Free Radic Biol Med 1995, 18:487-495. 10.1016/0891-5849(94)00169-K, 9101239.
10. Sikka SC. Relative impact of oxidative stress on male reproductive function. Curr Med Chem 2001, 8:851-862. 10.2174/0929867013373039, 11375755.
11. Choudhary R, Chawala VK, Soni ND, Kumar J, Vyas RK. Oxidative stress and role of antioxidants in male infertility. Pak J Physiol 2010, 6:54-59.
12. Beckman JS, Conger K. Direct measurement of nitric oxide in solutions with an ozone based chemiluminescent detector. Methods 1995, 7:35-39.
13. Agarwal A, Nandipati KC, Sharma RK, Zippe CD, Raina R. Role of oxidative stress in the pathophysiological mechanism of erectile dysfunction. J Androl 2006, 27:335-347. 10.2164/jandrol.05136, 16339449.
14. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. Apparent hydroxyl radical production from peroxynitrite: implications for endothelial injury by nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA 1990, 87:1620-1624. 10.1073/pnas.87.4.1620, 53527, 2154753.
15. Makker K, Agarwal A, Sharma R. Oxidative stress & male infertility. Indian J Med Res 2009, 129:357-367.
16. Koppenol WH, Moreno JJ, Pryor WA, Ischiropoulos H, Beckman JS. Peroxynitrite: a cloaked oxidant from superoxide and nitric oxide. Chem Res Toxicol 1992, 5:834-842. 10.1021/tx00030a017, 1336991.
17. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007, 87:315-424. 10.1152/physrev.00029.2006, 2248324, 17237348.
18. Jourd'heuil D, Jourd'heuil FL, Kutchukian PS, Musah RA, Wink DA, Grisham MB. Reaction of superoxide and nitric oxide with peroxynitrite: implications for peroxynitrite-mediated oxidation reactions in vivo. J Biol Chem 2001, 276:28799-28805. 10.1074/jbc.M102341200, 11373284.
19. Ramya T, Misro MM, Sinha D, Nandan D, Mithal S. Altered levels of seminal nitric oxide, nitric oxide synthase, and enzymatic antioxidants and their association with sperm function in infertile subjects. Fertil Steril 2011, 95:135-140. 10.1016/j.fertnstert.2010.06.044, 20684956.
20. Lee NP, Cheng CY. Nitric oxide/nitric oxide synthase, spermatogenesis, and tight junction dynamics. Biol Reprod 2004, 70:267-276. 10.1095/biolreprod.103.021329, 14522829.
21. Baker MA, Aitken RJ. Reactive oxygen species in spermatozoa: methods for monitoring and significance for the origins of genetic disease and infertility. Reprod Biol Endocrinol 2005, 3:1-9. 10.1186/1477-7827-3-1, 548295, 15642115.
22. Cornwell TL, Arnold E, Boerth NJ, Lincoln TM. Inhibition of smooth muscle cell growth by nitric oxide and activation of CAMP-dependent protein kinase by cGMP. Am J Physiol 1994, 267:C1405-C1413.
23. Zhang H, Zheng RL. Possible role of nitric oxide on fertile and asthenozoospermic infertile human sperm functions. Free Radic Res 1996, 25:347-354. 10.3109/10715769609149057, 8889498.
24. Rosselli M, Keller PJ, Dubey RK. Role of nitric oxide in the biology, physiology, and pathophysiology of reproduction. Hum Reprod Update 1998, 4:3-24. 10.1093/humupd/4.1.3, 9622410.
25. Archer S. Measurement of nitric oxide in biological models. FASB J 1993, 7:349-360.
26. O'Bryan MK, Zini A, Cheng CY, Schlegel PN. Human sperm endothelial nitric oxide synthase expression: correlation with sperm motility. Fertil Steril 1998, 70:1143-1147. 10.1016/S0015-0282(98)00382-3, 9848308.
27. Ehren I, Adolfsson J, Wiklund NP. Nitric oxide synthase activity in the human urogenital tract. Urol Res 1994, 22:287-290. 10.1007/BF00297196, 7533444.
28. Kitamura Y, Ogawa H, Oka K. Real-time measurement of nitric oxide using a bio-imaging and an electrochemical technique. Talanta 2003, 61:717-724. 10.1016/S0039-9140(03)00333-3, 18969236.
29. 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. 10.1007/s00240-003-0322-5, 12802542.
30. 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. 10.1095/biolreprod55.5.935, 8902202.
31. Lee NP, Cheng CY. Nitric oxide and cyclic nucleotides: their roles in junction dynamics and spermatogenesis. Adv Exp Med Biol 2008, 636:172-285.
32. Yan HH, Cheng CY. Blood-testis barrier dynamics are regulated by an engagement/disengagement mechanism between tight and adherens junctions via peripheral adaptors. Proc Natl Acad Sci USA 2005, 102:11722-11727. 10.1073/pnas.0503855102, 1183102, 16085710.
33. Santoro G, Romeo C, Impellizzeri P, Lentile R, Cutroneo G, Trimarchi F, Pedale S, Turiaco N, Gentile C. Nitric oxide synthase patterns in normal and varicocele testis in adolescents. BJU Int 2001, 88:967-973.
34. Turker KI, Erdoǧru T, Gülkesen H, Sezer C, Usta M, Ciftçioǧlu A, Baykara M. The potential role of inducible nitric oxide synthase (iNOS) activity in the testicular dysfunction associated with varicocele: an experimental study. Int Urol Nephrol 2004, 36:67-72.
35. Bolaños JP, Delgado-Esteban M, Herrero-Mendez A, Fernandez-Fernandez S, Almeida A. Regulation of glycolysis and pentose-phosphate pathway by nitric oxide: impact on neuronal survival. Biochim Biophys Acta 2008, 1777:789-793. 10.1016/j.bbabio.2008.04.011, 18455501.
36. 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.
37. Vanasco V, Evelson P, Boveris A, Alvarez S. In situ and real time muscle chemiluminescence determines singlet oxygen involvement in oxidative damage during endotoxemia. Chem Biol Interact 2010, 184:313-318. 10.1016/j.cbi.2010.01.011, 20079347.
38. 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.
39. Miraglia E, Rullo ML, Bosia A, Massobrio M, Revelli A, Ghigo D. Stimulation of the nitric oxide/cyclic guanosine monophosphate signaling pathway elicits human sperm chemotaxis in vitro. Fertil Steril 2007, 87:1059-1063. 10.1016/j.fertnstert.2006.07.1540, 17280661.
40. 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. 10.1093/molehr/2.11.873, 9237228.
41. Nobunaga T, Tokugawa Y, Hashimoto K, Kubota Y, Sawai K, Kimura T, Shimoya K, Takemura M, Matsuzaki N, Azuma C. Elevated nitric oxide concentration in the seminal plasma of infertile males: nitric oxide inhibits sperm motility. Am J Reprod Immunol 1996, 36:193-197. 10.1111/j.1600-0897.1996.tb00162.x, 8911625.
42. Donnelly ET, Lewis SE, Thompson W, Chakravarthy U. Sperm nitric oxide and motility: the effects of nitric oxide synthase stimulation and inhibition. Mol Hum Reprod 1997, 3:755-762. 10.1093/molehr/3.9.755, 9358000.
43. Hellstrom WJ, Bell M, Wang R, Sikka SC. Effect of sodium nitroprusside on sperm motility, viability, and lipid peroxidation. Fertil Steril 1994, 61:1117-1122.
44. Miraglia EE, De Angelis FF, Gazzano E, Hassanpour HH, Bertagna AA, Aldieri EE, Revelli AA, Ghigo DD, Alberto R. Dar: nitric oxide stimulates human sperm motility via activation of the cyclicGMP/protein kinase G signaling pathway. J Reprod Fertil Suppl 2011, 141:47-54.
45. Tomlinson MJ, East SJ, Barratt CL, Bolton AE, Cooke ID. Preliminary communication: possible role of reactive nitrogen intermediates in leucocyte-mediated sperm dysfunction. Am J Reprod Immunol 1992, 27:89-92.
46. Wu TP, Huang BM, Tsai HC, Lui MC, Liu MY. Effects of nitric oxide on human spermatozoa activity, fertilization and mouse embryonic development. Arch Androl 2004, 50:173-179. 10.1080/01485010490455494, 15204684.
47. Burnett AL, Tillman TL, Chang TS, Epstein JI, Lowenstein CJ, Bredt DS, Snyder SH, Walsh PC. Immunohistochemical localization of nitric oxide synthase in the autonomic innervation of the penis. J Urol 1993, 150:73-76.
48. 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. 10.1095/biolreprod64.6.1708, 11369599.
49. Amiri I, Sheikh N, Najafi R. Nitric oxide level in seminal plasma and its relation with sperm DNA damages. Iran Biomed J 2007, 11:259-264.
50. Aitken RJ, Baker MA, O'Bryan M. Shedding light on chemiluminescence: the application of chemiluminescence in diagnostic andrology. J Androl 2004, 25:455-465.
51. Bain J. Testosterone and the aging male: to treat or not to treat?. Maturitas 2010, 66:16-22. 10.1016/j.maturitas.2010.01.009, 20153946.
52. Dhindsa S, Prabhakar S, Sethi M, Bandyopadhyay A, Chaudhuri A, Dandona P. Frequent occurrence of hypogonadotropic hypogonadism in type 2 diabetes. J Clinical Endocrinol Metab 2004, 89:5462-5468.
53. Semenova AV, Tomilova IK, Panikratov KD, Kadykova EL, Basharin AV. The role of nitric oxide in fertility disorders in men. Urologiia 2005, 6:31-36.
54. Kruger TF, Menkveld R, Stander FS, Lombard CJ, Van der Merwe JP, van Zyl JA, Smith K. Sperm morphologic features as a prognostic factor in in vitro fertilization. Fertil Steril 1986, 46:1118-1123.
55. Burnett AL, Ricker DD, Chamness SL, Maguire MP, Crone JK, Bredt DS, Snyder SH, Chang TS. Localization of nitric oxide synthase in the reproductive organs of the male rat. Biol Reprod 1995, 52:1-7. 10.1095/biolreprod52.1.1, 7536043.
56. Huang I, Jones J, Khorram O. Human seminal plasma nitric oxide: correlation with sperm morphology and testosterone. Med Sci Monit 2006, 12:CR103-CR106.
57. WHO World health organization laboratory manual for the examination of human semen and semen-cervical mucus interaction 1999, Cambridge: Cambridge University Press, 4, WHO.
58. Shiraishi K, Naito K. Nitric oxide produced in the testis is involved in dilatation of the internal spermatic vein that compromises spermatogenesis in infertile men with varicocele. BJU Int 2007, 99:1086-1090. 10.1111/j.1464-410X.2007.06800.x, 17346270.
59. 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 Urol 1996, 156:1952-1958. 10.1016/S0022-5347(01)65403-X, 8911364.
60. Ozbek E, Turkoz Y, Gokdeniz R, Davarci M, Ozugurlu F. Increased nitric oxide production in the spermatic vein of patients with varicocele. Eur Urol 2000, 37:172-175. 10.1159/000020135, 10705195.
61. Romeo C, Lentile R, Impellizzeri P, Turiaco N, Teletta M, Antonuccio P, Basile M, Gentile C. Preliminary report on nitric oxide mediated oxidative damage in adolescent varicocele. Hum Reprod 2003, 18:26-29. 10.1093/humrep/deg004, 12525436.
62. Du Plessis SS, Cabler S, McAlister DA, Sabanegh E, Agarwal A. The effect of obesity on sperm disorders and male infertility. Nat Rev Urol 2010, 7:153-161. 10.1038/nrurol.2010.6, 20157305.
63. Agbaje IM, Rogers DA, McVicar CM, McClure N, Atkinson AB, Mallidis C, Lewis SEM. Insulin dependent diabetes mellitus: implications for male reproductive function. Hum Reprod 2007, 22:1871-1877. 10.1093/humrep/dem077, 17478459.
64. World Precision Instruments Lab equipment for the life sciences http://www.wpiinc.cn/pdf/iso-nop-maintenance.pdf, World Precision Instruments.
65. Navarro-Antolin J, Lamas S. Nitrosative stress by cyclosporin A in the endothelium: studies with the NO-sensitive probe diaminoflurescein-2/diacetateusing flow cytometry. Nephrol Dial Transplant 2001, 16:6-9. 10.1093/ndt/16.suppl_1.6, 11369812.
66. Liebhafsky HA, Winslow EH. Spectrophotometric determination of nitrite: and of nitric oxide in furnace atmosphere. Ind Eng Chem Anal Ed 1939, 11:189-190.
67. Giustarini D, Rossi R, Milzani A, Dalle-Donne I. Nitrite and nitrate measurement by griess reagent in human plasma: evaluation of interferences and standardization. Methods Enzymol 2008, 440:361-380.
68. Leone AM, Francis PL, Rhodes P, Moncada S. A rapid and simple method for the measurement of nitrite and nitrate in plasma by high performance capillary electrophoresis. Biochem Biophys Res Commun 1994, 200:951-957. 10.1006/bbrc.1994.1542, 8179632.
69. Gally JA, Montague PR, Reeke GM, Edelman GM. The NO hypothesis: possible effects of a short-lived, rapidly diffusible signal in the development and function of the nervous system. Proc Natl Acad Sci U S A 1990, 87:3547-3551. 10.1073/pnas.87.9.3547, 53939, 2333301.