A novel approach to identifying physical markers of cryo-damage in bull spermatozoa

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Yoon, Sung Jae ^a   Kwon, Woo Sung ^a   Rahman, Md Saidur ^a   Lee, June Sub ^a   Pang, Myung Geol ^a  

^a Chung Ang University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CRYOPROTECTIVE AGENT; BIOLOGICAL MARKER;

ACROSOME REACTION; ANIMAL CELL; ARTICLE; BULL (BOVINE); CELL ACTIVITY; CELL DAMAGE; CELL VIABILITY; COLD INJURY; CONTROLLED STUDY; COOLING; CRYOPRESERVATION; DILUTION; FLOW CYTOMETRY; FLUORESCENCE ANALYSIS; FREEZING; HYPOOSMOTIC SWELLING TEST; KINEMATICS; MALE; MITOCHONDRIAL ACTIVITY; MOTION KINEMATICS; NONHUMAN; PROCEDURES CONCERNING CELLS; SEMEN ANALYSIS; SOUTH KOREA; SPERM PRESERVATION; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY; SPERMATOZOON VIABILITY; STAINING; ANIMAL; BOVINE; CYTOLOGY; METABOLISM; MITOCHONDRION; PHYSIOLOGY; PROCEDURES; SPERMATOZOON;

BOVINAE;

ACROSOME REACTION; ANIMALS; BIOMARKERS; CATTLE; CRYOPRESERVATION; FLOW CYTOMETRY; MALE; MITOCHONDRIA; SEMEN ANALYSIS; SEMEN PRESERVATION; SPERM MOTILITY; SPERMATOZOA;

EID: 84929120398     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126232     Document Type: Article

References (55)

1. Olaciregui M, Gil L, Monton A, Luno V, Jerez RA, Marti JI. Cryopreservation of epididymal stallion sperm. Cryobiology. 2014; 68(1):91-5. doi: 10.1016/j.cryobiol.2013.12.009 PMID: 24412395.
2. Mota Filho AC, Silva HV, Nunes TG, de Souza MB, de Freitas LA, de Araujo AA, et al. Cryopreservation of canine epididymal sperm using ACP-106c and TRIS. Cryobiology. 2014; 69(1):17-21. doi: 10.1016/j.cryobiol.2014.04.013 PMID: 24824725.
3. Watson PF. The causes of reduced fertility with cryopreserved semen. Animal reproduction science. 2000; 60-61:481-92. PMID: 10844218.
4. Ardon F, Suarez SS. Cryopreservation increases coating of bull sperm by seminal plasma binder of sperm proteins BSP1, BSP3, and BSP5. Reproduction. 2013; 146(2):111-7. doi: 10.1530/REP-12-0468 PMID: 23740081.
5. Brugnon F, Ouchchane L, Pons-Rejraji H, Artonne C, Farigoule M, Janny L. Density gradient centrifugation prior to cryopreservation and hypotaurine supplementation improve post-thaw quality of sperm from infertile men with oligoasthenoteratozoospermia. Human reproduction. 2013; 28(8):2045-57. doi: 10.1093/humrep/det253 PMID: 23760160.
6. Ramon M, Perez-Guzman MD, Jimenez-Rabadan P, Esteso MC, Garcia-Alvarez O, Maroto-Morales A, et al. Sperm cell population dynamics in ram semen during the cryopreservation process. PloS one. 2013; 8(3):e59189. doi: 10.1371/journal.pone.0059189 PMID: 23544054; PubMed Central PMCID: PMC3609831.
7. Martins M, Justino RC, Sant'anna MC, Trautwein LG, Souza FF. Comparison of two different extenders for cryopreservation of epididymal dog sperm. Reproduction in domestic animals = Zuchthygiene. 2012; 47 Suppl 6:293-4. doi: 10.1111/rda.12042 PMID: 23279522.
8. Peris SI, Bilodeau JF, Dufour M, Bailey JL. Impact of cryopreservation and reactive oxygen species on DNA integrity, lipid peroxidation, and functional parameters in ram sperm. Molecular reproduction and development. 2007; 74(7):878-92. doi: 10.1002/mrd.20686 PMID: 17186553.
9. Hammerstedt RH, Graham JK, Nolan JP. Cryopreservation of mammalian sperm: what we ask them to survive. Journal of andrology. 1990; 11(1):73-88. PMID: 2179184.
10. Liu Q, Wang X, Wang W, Zhang X, Xu S, Ma D, et al. Effect of the addition of six antioxidants on sperm motility, membrane integrity and mitochondrial function in red seabream (Pagrus major) sperm cryopreservation. Fish physiology and biochemistry. 2014. doi: 10.1007/s10695-014-9993-9 PMID: 25255938.
11. Viveiros AT, Isau ZA, Caneppele D, Leal MC. Sperm cryopreservation affects postthaw motility, but not embryogenesis or larval growth in the Brazilian fish Brycon insignis (Characiformes). Theriogenology. 2012; 78(4):803-10. doi: 10.1016/j.theriogenology.2012.03.028 PMID: 22541324.
12. Celeghini EC, de Arruda RP, de Andrade AF, Nascimento J, Raphael CF, Rodrigues PH. Effects that bovine sperm cryopreservation using two different extenders has on sperm membranes and chromatin. Animal reproduction science. 2008; 104(2-4):119-31. doi: 10.1016/j.anireprosci.2007.02.001 PMID: 17368970.
13. Wang AW, Zhang H, Ikemoto I, Anderson DJ, Loughlin KR. Reactive oxygen species generation by seminal cells during cryopreservation. Urology. 1997; 49(6):921-5. PMID: 9187701.
14. Sorrenti G, Bagnoli A, Miraglia V, Crocetta F, Vitiello V, Ristoratore F, et al. Investigating sperm cryopreservation in a model tunicate, Ciona intestinalis sp. A. Cryobiology. 2014; 68(1):43-9. doi: 10.1016/j.cryobiol.2013.11.005 PMID: 24269530.
15. D'Amours O, Frenette G, Fortier M, Leclerc P, Sullivan R. Proteomic comparison of detergent-extracted sperm proteins from bulls with different fertility indexes. Reproduction. 2010; 139(3):545-56. doi: 10.1530/REP-09-0375 PMID: 19952166.
16. Ahmad M, Nasrullah R, Riaz H, Sattar A, Ahmad N. Changes in motility, morphology, plasma membrane and acrosome integrity during stages of cryopreservation of buck sperm. Journal of the South African Veterinary Association. 2014; 85(1):972. doi: 10.4102/jsava.v85i1.972 PMID: 24832216.
17. Wang S, Wang W, Xu Y, Tang M, Fang J, Sun H, et al. Proteomic characteristics of human sperm cryopreservation. Proteomics. 2014; 14(2-3):298-310. doi: 10.1002/pmic.201300225 PMID: 24259508.
18. Drobnis EZ, Crowe LM, Berger T, Anchordoguy TJ, Overstreet JW, Crowe JH. Cold shock damage is due to lipid phase transitions in cell membranes: a demonstration using sperm as a model. The Journal of experimental zoology. 1993; 265(4):432-7. doi: 10.1002/jez.1402650413 PMID: 8463792.
19. Xu X, Liu Y, Cui Z, Wei Y, Zhang L. Effects of osmotic and cold shock on adherent human mesenchymal stem cells during cryopreservation. Journal of biotechnology. 2012; 162(2-3):224-31. doi: 10.1016/j.jbiotec.2012.09.004 PMID: 22989486.
20. Ebertz SL, McGann LE. Osmotic parameters of cells from a bioengineered human corneal equivalent and consequences for cryopreservation. Cryobiology. 2002; 45(2):109-17. PMID: 12482376.
21. Gilmore JA, Du J, Tao J, Peter AT, Critser JK. Osmotic properties of boar spermatozoa and their relevance to cryopreservation. Journal of reproduction and fertility. 1996; 107(1):87-95. PMID: 8699439.
22. D'Amours O, Frenette G, Bordeleau LJ, Allard N, Leclerc P, Blondin P, et al. Epididymosomes transfer epididymal sperm binding protein 1 (ELSPBP1) to dead spermatozoa during epididymal transit in bovine. Biology of reproduction. 2012; 87(4):94. doi: 10.1095/biolreprod.112.100990 PMID: 22875906.
23. Hinton BT, Dott HM, Setchell BP. Measurement of the motility of rat spermatozoa collected by micropuncture from the testis and from different regions along the epididymis. Journal of reproduction and fertility. 1979; 55(1):167-72. PMID: 423154.
24. Pholpramool C, Zupp JL, Setchell BP. Motility of undiluted bull epididymal spermatozoa collected by micropuncture. Journal of reproduction and fertility. 1985; 75(2):413-20. PMID: 4067922.
25. Shabanowitz RB, Killian GJ. Two-dimensional electrophoresis of proteins in principal cells, spermatozoa, and fluid associated with the rat epididymis. Biology of reproduction. 1987; 36(3):753-68. PMID: 3593846.
26. Awad MM, Graham JK. A new pellet technique for cryopreserving ram and bull spermatozoa using the cold surface of cattle fat. Animal reproduction science. 2004; 84(1-2):83-92. doi: 10.1016/j.anireprosci.2003.12.001. WOS:000223569500007.
27. Kwon WS, Rahman MS, Lee JS, Kim J, Yoon SJ, Park YJ, et al. A comprehensive proteomic approach to identifying capacitation related proteins in boar spermatozoa. BMC genomics. 2014; 15(1):897. doi: 10.1186/1471-2164-15-897 PMID: 25315394.
28. Rahman MS, Kwon WS, Lee JS, Kim J, Yoon SJ, Park YJ, et al. Sodium nitroprusside suppresses male fertility in vitro. Andrology. 2014; 2(6):899-909. doi: 10.1111/j.2047-2927.2014.00273.x PMID: 25180787.
29. Kwon WS, Park YJ, Mohamed el SA, Pang MG. Voltage-dependent anion channels are a key factor of male fertility. Fertility and sterility. 2013; 99(2):354-61. doi: 10.1016/j.fertnstert.2012.09.021 PMID: 23062735.
30. Ludovico P, Sansonetty F, Corte-Real M. Assessment of mitochondrial membrane potential in yeast cell populations by flow cytometry. Microbiology. 2001; 147(Pt 12):3335-43. PMID: 11739765.
31. Li JJ, Tang Q, Li Y, Hu BR, Ming ZY, Fu Q, et al. Role of oxidative stress in the apoptosis of hepatocellular carcinoma induced by combination of arsenic trioxide and ascorbic acid. Acta pharmacologica Sinica. 2006; 27(8):1078-84. doi: 10.1111/j.1745-7254.2006.00345.x PMID: 16867262.
32. Barbas JP, Mascarenhas RD. Cryopreservation of domestic animal sperm cells. Cell and tissue banking. 2009; 10(1):49-62. doi: 10.1007/s10561-008-9081-4 PMID: 18548333.
33. Sariozkan S, Bucak MN, Tuncer PB, Ulutas PA, Bilgen A. The influence of cysteine and taurine on microscopic-oxidative stress parameters and fertilizing ability of bull semen following cryopreservation. Cryobiology. 2009; 58(2):134-8. doi: 10.1016/j.cryobiol.2008.11.006 PMID: 19070613.
34. Kwon WS, Rahman MS, Pang MG. Diagnosis and prognosis of male infertility in mammal: the focusing of tyrosine phosphorylation and phosphotyrosine proteins. Journal of proteome research. 2014; 13(11):4505-17. doi: 10.1021/pr500524p PMID: 25223855.
35. Rahman MS, Lee JS, Kwon WS, Pang MG. Sperm proteomics: road to male fertility and contraception. International journal of endocrinology. 2013; 2013:360986. doi: 10.1155/2013/360986 PMID: 24363670; PubMed Central PMCID: PMC3864079.
36. Jin J, Jin N, Zheng H, Ro S, Tafolla D, Sanders KM, et al. Catsper3 and Catsper4 are essential for sperm hyperactivated motility and male fertility in the mouse. Biology of reproduction. 2007; 77(1):37-44. doi: 10.1095/biolreprod.107.060186 PMID: 17344468.
37. Mostafapor S, Farrokhi Ardebili F. Effects of diluting medium and holding time on sperm motility analysis by CASA in ram. Veterinary research forum: an international quarterly journal. 2014; 5(2):101-5. PMID: 25568702; PubMed Central PMCID: PMC4279634.
38. de Lamirande E, Gagnon C. Reactive oxygen species and human spermatozoa. I. Effects on the motility of intact spermatozoa and on sperm axonemes. Journal of andrology. 1992; 13(5):368-78. PMID: 1331006.
39. Kwon WS, Rahman MS, Lee JS, Kim J, Yoon SJ, Park YJ, et al. A comprehensive proteomic approach to identifying capacitation related proteins in boar spermatozoa. BMC genomics. 2014; 15:897. doi: 10.1186/1471-2164-15-897 PMID: 25315394; PubMed Central PMCID: PMC4287242.
40. Dona G, Kozuh I, Brunati AM, Andrisani A, Ambrosini G, Bonanni G, et al. Effect of astaxanthin on human sperm capacitation. Marine drugs. 2013; 11(6):1909-19. doi: 10.3390/md11061909 PMID: 23736766; PubMed Central PMCID: PMC3721213.
41. Zaneveld LJ, De Jonge CJ, Anderson RA, Mack SR. Human sperm capacitation and the acrosome reaction. Human reproduction. 1991; 6(9):1265-74. PMID: 1752929.
42. Garcia-Herreros M, Leal CL. Sperm volumetric dynamics during in vitro capacitation process in bovine spermatozoa. Animal: an international journal of animal bioscience. 2015:1-9. doi: 10.1017/S1751731115000129 PMID: 25684453.
43. Pons-Rejraji H, Bailey JL, Leclerc P. Modulation of bovine sperm signalling pathways: correlation between intracellular parameters and sperm capacitation and acrosome exocytosis. Reproduction, fertility, and development. 2009; 21(4):511-24. doi: 10.1071/RD07169 PMID: 19383258.
44. White IG. Lipids and calcium uptake of sperm in relation to cold shock and preservation: a review. Reproduction, fertility, and development. 1993; 5(6):639-58. PMID: 9627725.
45. Liu Z, Foote RH. Osmotic effects on volume and motility of bull sperm exposed to membrane permeable and nonpermeable agents. Cryobiology. 1998; 37(3):207-18. doi: 10.1006/cryo.1998.2116 PMID: 9787066.
46. Melville DF, Johnston SD, Miller RR Jr. Flying-fox (Pteropus spp.) sperm membrane fatty acid composition, its relationship to cold shock injury and implications for cryopreservation success. Cryobiology. 2012; 65(3):224-9. doi: 10.1016/j.cryobiol.2012.06.007 PMID: 22771758.
47. Miller RR Jr, Sheffer CJ, Cornett CL, McClean R, MacCallum C, Johnston SD. Sperm membrane fatty acid composition in the Eastern grey kangaroo (Macropus giganteus), koala (Phascolarctos cinereus), and common wombat (Vombatus ursinus) and its relationship to cold shock injury and cryopreservation success. Cryobiology. 2004; 49(2):137-48. doi: 10.1016/j.cryobiol.2004.06.002 PMID: 15351685.
48. Kim YH, Park YJ, Yoon SJ, Kwon WS, Kim SH, Pang MG. Effect of BTS and Androhep during Storage Times on the Kinematics and Capacitation Status in Liquid Boar Semen. Reprod Dev Biol. 2010; 34(3):241-6.
49. Spungin B, Margalit I, Breitbart H. Sperm exocytosis reconstructed in a cell-free system: evidence for the involvement of phospholipase C and actin filaments in membrane fusion. Journal of cell science. 1995; 108 (Pt 6):2525-35. PMID: 7673366.
50. Kutluyer F, Kayim M, Ogretmen F, Buyukleblebici S, Tuncer PB. Cryopreservation of rainbow trout Oncorhynchus mykiss spermatozoa: effects of extender supplemented with different antioxidants on sperm motility, velocity and fertility. Cryobiology. 2014; 69(3):462-6. doi: 10.1016/j.cryobiol.2014.10.005 PMID: 25445462.
51. Alapati R, Stout M, Saenz J, Gentry GT Jr, Godke RA, Devireddy RV. Comparison of the permeability properties and post-thaw motility of ejaculated and epididymal bovine spermatozoa. Cryobiology. 2009; 59(2):164-70. doi: 10.1016/j.cryobiol.2009.06.009 PMID: 19545558.
52. Lessard C, Parent S, Leclerc P, Bailey JL, Sullivan R. Cryopreservation alters the levels of the bull sperm surface protein P25b. Journal of andrology. 2000; 21(5):700-7. PMID: 10975417.
53. Prathalingam NS, Holt WV, Revell SG, Mirczuk S, Fleck RA, Watson PF. Impact of antifreeze proteins and antifreeze glycoproteins on bovine sperm during freeze-thaw. Theriogenology. 2006; 66(8):1894-900. doi: 10.1016/j.theriogenology.2006.04.041 PMID: 16777208.
54. Ball BA, Vo A. Osmotic tolerance of equine spermatozoa and the effects of soluble cryoprotectants on equine sperm motility, viability, and mitochondrial membrane potential. Journal of andrology. 2001; 22(6):1061-9. PMID: 11700853.
55. De Leeuw FE, Chen HC, Colenbrander B, Verkleij AJ. Cold-induced ultrastructural changes in bull and boar sperm plasma membranes. Cryobiology. 1990; 27(2):171-83. PMID: 2331890.