Effect of cryopreservation on nitric oxide production by stallion spermatozoa

Biology of Reproduction

Volumn 81, Issue 6, 2009, Pages 1106-1111

  Ortega Ferrusola, C ^a   Gonzalez Fernandez L ^a   Macias Garcia B ^a   Salazar Sandoval, C ^a   Morillo Rodriguez A ^a   Rodriguez Martinez H ^b   Tapia, J A ^a   Pena F J ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Assisted reproductive technology; Cryopreservation; Flow cytometry; Gamete biology; Nitric oxide; Nitric oxide synthase; Sperm; Stallion

Indexed keywords

4,5 DIAMINOFLUORESCEIN DIACETATE; ISOPROTEIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; CRYOPROTECTIVE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL LYSATE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CRYOPRESERVATION; EGG YOLK; FLOW CYTOMETRY; FREEZING; IMMUNODETECTION; MALE; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; SPERMATOZOON; SPERMATOZOON MOTILITY; STALLION; THAWING; WESTERN BLOTTING; ANIMAL; CONFOCAL MICROSCOPY; DRUG EFFECT; HORSE; METABOLISM; NONPARAMETRIC TEST; SPERM; SPERM PRESERVATION;

ANIMALS; BLOTTING, WESTERN; CRYOPRESERVATION; CRYOPROTECTIVE AGENTS; EGG YOLK; FLOW CYTOMETRY; HORSES; MALE; MICROSCOPY, CONFOCAL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SEMEN; SEMEN PRESERVATION; SPERM MOTILITY; SPERMATOZOA; STATISTICS, NONPARAMETRIC;

EID: 73949091562     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.078220     Document Type: Article

References (41)

1. Morris GJ, Faszer K, Green JE, Draper D, Grout BW, Fonseca F. Rapidly cooled horse spermatozoa: loss of viability is due to osmotic imbalance during thawing, not intracellular ice formation. Theriogenology 2007; 68: 804-812.
2. Watson PF. The causes of reduced fertility with cryopreserved semen. Anim Reprod Sci 2000; 60-61:481-492.
3. Ball BA. Oxidative stress, osmotic stress and apoptosis: impacts on sperm function and preservation in the horse. Anim Reprod Sci 2008; 107:257-267.
4. Bravo MM, Aparicio IM, Garcia-Herreros M, Gil MC, Peña FJ, García-Marín LJ. Changes in tyrosine phosphorylation associated with true capacitation and capacitation like state in boar spermatozoa. Mol Reprod Dev 2005; 71:88-96.
5. Martin G, Cagnon N, Sabido O, Sion B, Grizard G, Durand P, Levy R. Kinetics of occurrence of some features of apoptosis during the cryopreservation process of bovine spermatozoa. Hum Reprod 2007; 22: 380-388.
6. Martin G, Sabido O, Durand P, Levy R. Cryopreservation induces an apoptosis-like mechanism in bull sperm. Biol Reprod 2004; 71:28-37.
7. Ortega Ferrusola C, Sotillo Galán Y, Varela Fernández E, Gallardo Bolaños JM, Gonźalez Fernández L, Tapia JA, Peña FJ. Detection of "apoptosis-like" changes during the cryopreservation process in equine sperm. J Androl 2008; 29:213-221.
8. Peña FJ, Johannisson A, Wallgren M, Rodriguez Martinez H. Assessment of fresh and frozen-thawed boar semen using an annexin-v assay: a new method of evaluating sperm membrane integrity. Theriogenology 2003; 60:677-689.
9. Peña FJ, Rodríguez Martínez H, Tapia JA, Ortega Ferrusola C, González Fernández L, Macias García B. Mitochondria in mammalian sperm physiology and pathology: a review. Reprod Dom Anim 2009; 44:345-349.
10. Agarwall A, Said TM. Oxidative stress, DNA damage and apoptosis in male infertility a clinical approach. BJU Int 2005; 95:503-507.
11. Aitken RJ, Wingate JK, De Iulius GN, McLaughlin EA. Analysis of lipid peroxidation in human spermatozoa using BODIPY C11. Mol Hum Reprod 2007; 13:203-211.
12. Alvarez JG, Storey B. Evidence for increased lipid peroxidative damage and loss of superoxide dismutase activity as a mode of sublethal cryodamage to human sperm during cryopreservation. J Androl 1992; 13:232-241.
13. Baker MA, Aitken RJ. The importance of redox regulated pathways in sperm cell biology. Mol Cel Endocrinol 2004; 216:47-54.
14. Baker MA, Aitken RJ. Reactive oxygen species in spermatozoa: methods for monitoring and significance for the origin of genetic disease and infertihty. Reprod Biol Endocrinol 2005; 3:67-76.
15. Baumber J, Ball BA, Gravance CG, Medina V, Davies Morel MCG. The effect of reactive oxygen species on equine sperm motility, viability, acrosomal integrity, mitochondrial membrane potential and membrane lipid peroxidation. J Androl 2000; 21:895-902.
16. Herrero MB, Gagnon C. Nitric oxide: a novel mediator of sperm function. J Androl 2001; 22:349-356.
17. Roselli M, Keller PJ, Dubey RK. Role of nitric oxide in the biology physiology and pathophysiology of reproduction. Hum Reprod Update 1998; 4:3-24.
18. 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.
19. Balercia G, Moretti S, Vignini A, Magagnini M, Mantero F, Boscaro M, Riccardo Lamonica G, Mazzanti L. Role of nitric oxide concentrations on human sperm motility. J Androl 2004; 2:245-249.
20. Herrero MB, Chatterjee S, Lefievre L, De Lamirande E, Gagnon C. Nitric oxide interacts with the cAMP pathway to modulate capacitation of human spermatozoa. Free Radic Biol Med 2000; 29:522-536.
21. Herrero MB, de Lamirande E, Gagnon C. Nitric oxide regulates sperm capacitation and protein tyrosine phosphorylation in vitro. Biol Reprod 1999; 61:575-581.
22. Herrero MB, Goin JC, Boquet M, Cameras MG, Franchi AM, Perez Martinez S, Polak JM, Viggiano JM, Gimeno MAF. The nitric oxide synthase of mouse spermatozoa. FEBS Lett 1997; 411:39-42.
23. Lewis SEM, Donnelly ET, Sterling ESL, Kennedy MS, Thompson W, Chakravarthy U. Nitric oxide syndiase and nitrite production in human spermatozoa: evidence mat endogenous nitric oxide is beneficial for sperm motility. Mol Hum Reprod 1996; 11:873-878.
24. Kuo RC, Baxter GT, Thompson SH, Stricker SA, Patton C, Bonaventura J, Epel D. NO is necessary and sufficient for egg activation at fertilization. Nature 2000; 406:633-636.
25. Vignini A, Nanetti L, Buldreghini E, Moroni C, Ricciardo Lamonina G, Mantero F, Boscaro M, Mazzanti L, Balercia G. The production of peroxynitrite by human spermatozoa may affect sperm motUity through the formation of protein nitrotyrosine. Fertil Steril 2006; 85:947-953.
26. Goud PT, Goud AP, Diamond MP, Gonik MP, Abu Soud H. Nitric oxide extends the oocyte temporal window for optimal fertilization. Free Radic Biol Med 2008; 45:453-459.
27. Francavilla F, Santucci R, Macerola B, Ruvolo G, Romano R. Nitric oxide syndiase inhibition in human sperm affects sperm-oocyte fusion but not zona pellucida binding. Biol Reprod 2000; 63:425-429.
28. Kojima H, Nakatsubo N, Kikuchi K, Kawahara S, Kirino Y, Nagoshi H, Hirata Y, Nagano T. Detection and imaging of nitric oxide with novel fluorescent indicators diaminofluoresceins. Anal Chem 1998; 70:2446-2453.
29. Strijdom H, Muller C, Lochner A. Direct intracellular nitric oxide detection in isolated adult cardiomyocytes: flow cytometric analysis using the fluorescent probe diaminofluorescein. J Mol Cell Cardiol 2004; 37: 897-902.
30. Tiscoria A, Cairoli E, Marquez M, Denicola A, Pritsch O, Cayota A. Use of diaminofluoresceins to detect and measure nitric oxide in low level generating human immune cells. J Immunol Meth 2009; 342:49-57.
31. Moran JM, Madejón L, Ortega Ferrusola C, Peña FJ. Nitric oxide induces caspase activity in boar spermatozoa. Theriogenology 2008; 70:91-96.
32. Ormerod MG, Sun XM, Snowden RT, Davies R, Feamhead H, Cohen GM. Increased membrane permeability of apoptotic thymocites: a flow cytometric study. Cytometry 1993; 14:595-602.
33. Wronsky R, Golob N, Grygar E, Winsdish M. Two color, fluorescence-based microplate assay for apoptosis detection. Biotechniques 2002; 32: 666-668.
34. Idziorek T, Estaquier J, de Bels F, Ameisen JC. YOPRO-1 permits cytofluorometric analysis of programmed cell dead (apoptosis) without interfering with cell viability. J Immunol Meth 1995; 185:249-285.
35. Gonzalez-Fernandez L, Ortega-Ferrusola C, Macias-Garcia B, Salido GM, Peña FJ, Tapia JA. Identification of protein tyrosine phosphatases and dual-specificity phosphatases in mammalian spermatozoa and their role in sperm motility and protein tyrosine phosphorylation. Biol Reprod 2009; 80:1239-1252.
36. López Figueroa MO, Caamaño C, Morano MI, Ronn LC, Akil L, Watson SJ. Direct evidence of nitric oxide presence within mitochondria. Biochem Biophys Res Commun 2000; 272:129-133.
37. Alderton WK, Cooper CE, Knowles RG. Nitric oxide syndiases: structure function and inhibition. Biochem J 2001; 357(pt 3):593-615.
38. Coers W, Timens W, Kempinga C, Klok PA, Moshage H. Specificity of antibodies to nitric oxide syndiase isoforms in human, guinea pig, rat, and mouse tissues. J Histochem Cytochem 1998; 46:1385-1392.
39. Hurst WJ, Moroz LL, Gillette MU, Gillette R. Nitric oxide synthase imunolabeling in the molluscan CNS and peripheral tissues. Biochem Biophys Res Commun 1999; 262:545-548.
40. Srivastava S, Desai P, Couinho E, Govil G. Mechanism of action of Larginine on the vitality of spermatozoa is primarily through increased biosynthesis of nitric oxide. Biol Reprod 2006; 74:954-958.
41. Chatterjee S, Gagnon C. Production of reactive oxygen species by spermatozoa undergoing cooling freezing and thawing. Mol Reprod Dev 2001; 59:451-458.