Slow cooling prevents cold-induced damage to sperm motility and acrosomal integrity in the black-footed ferret (Mustela nigripes)

Reproduction, Fertility and Development

Volumn 19, Issue 5, 2007, Pages 652-663

  Santymire, R M ^a,c,d   Marinari, P E ^b   Kreeger, J S ^b   Wildt, D E ^a   Howard, J G ^a  

^a SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^b US Fish and Wildlife Service   (United States)

^c GEORGE MASON UNIVERSITY   (United States)

^d LINCOLN PARK ZOO   (United States)

Author keywords

Assisted reproduction; Conservation; Genome resource banking; Mustelid

Indexed keywords

GLYCEROL;

ACROSOME REACTION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; COOLING; CRYOPRESERVATION; EGG YOLK; EJACULATION; FERRET; FREEZING; GAMETE; INCUBATION TEMPERATURE; MALE; MUSTELA NIGRIPES; NONHUMAN; SEMEN ANALYSIS; SEMINAL PLASMA; SPERM PRESERVATION; SPERMATOZOON DENSITY; SPERMATOZOON MOTILITY; STATISTICAL SIGNIFICANCE; SURVIVAL; TEMPERATURE SENSITIVITY; THAWING;

ACROSOME; ANIMALS; COLD; CONSERVATION OF NATURAL RESOURCES; CRYOPRESERVATION; CRYOPROTECTIVE AGENTS; FERRETS; GLUCOSE; INSEMINATION, ARTIFICIAL; MALE; SEMEN; SEMEN PRESERVATION; SPERM MOTILITY; TROMETHAMINE;

MUSTELA; MUSTELA NIGRIPES; MUSTELIDAE;

EID: 34347396576     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD06096     Document Type: Article

References (64)

1. Aboagla, E. M.-E., and Terada,T. (2004). Effects of egg yolk during the freezing step of cryopreservation on the viability of goat spermatozoa. Theriogenology 62, 1160-1172. doi:10.1016/J.THERIOGENOLOGY.2004. 01.013
2. Ashworth, P. J. C., Harrison, R. A. P., Miller, N. G. A., Plummer, J. M., and Watson, P. F. (1994). Survival of ram spermatozoa at high dilution: protective effect of simple constituents of culture media as compared with seminal plasma. Reprod. Fertil. Dev. 6, 173-180. doi:10.1071/RD9940173
3. Atherton, R. W., Straley, M., Curry, P., Slaughter, R., Burgess, W., and Kitchin, R. M. (1989). Electroejaculation and cryopreservation of domestic ferret sperm. In 'Conservation Biology of the Black-Footed Ferret'. (Eds U. S. Seal, E. T. Thorne, S. H. Anderson and M. A. Bodan.) pp. 177-189. (Yale University Press: New Haven.)
4. Aurich, J. E., Kuhne, A., Hoppe, H., and Aurich, C. (1996). Seminal plasma affects membrane integrity and motility of equine spermatozoa after cryopreservation. Theriogenology 46, 791-797. doi:10.1016/S0093- 691X(96)00237-3
5. Azeredo, G. A., Esper, C. R., and Resende, K. T. (2001). Evaluation of plasma membrane integrity of frozen-thawed goat spermatozoa with or without seminal plasma. Small Rumin. Res. 41, 257-263. doi:10.1016/S0921-4488(01)00189-4
6. Baas, J.W., Molan, P. C., and Shannon, P. (1983). Factors in seminal plasma of bulls that affect the viability and motility of spermatozoa. J. Reprod. Fertil. 68, 275-280.
7. Barthelemy, C., Royere, D., Hammahah, S., Lebos, C., Tharanne, M. J., and Lansac, J. (1990). Ultrastructural changes in membranes and acrosome of human sperm during cryopreservation. Arch. Androl. 25, 29-40.
8. Berger, T., and Clegg, E. (1985). Effect of male accessory gland secretions on sensitivity of porcine sperm acrosomes to cold shock. Initiation of motility and loss of cytoplasmic droplets. J. Anim. Sci. 60, 1295-1302.
9. Byrd, W., and Wolf, D. P. (1986). Acrosomal status in fresh and capacitated human ejaculated sperm. Biol. Reprod. 34, 859-869. doi:10.1095/BIOLREPROD34.5.859
10. Chang, M. (1957). A detrimental effect of seminal plasma on the fertilizing capacity of sperm. Nature 179, 258-259. doi:10.1038/179258A0
11. Critser, J. K., Huse-Benda, A. R., Aaker, D. V., Arneson, B. W., and Ball, G. D. (1988). Cryopreservation of human spermatozoa. III. The effect of cryoprotectants on motility. Fertil. Steril. 50, 314-320.
12. Cross, N. L. (1993). Multiple effects of seminal plasma on the acrosome reaction of human sperm. Mol. Reprod. Dev. 35, 316-323. doi:10.1002/MRD.1080350314
13. Davis, B., and Niwa, K. (1974). Inhibition of mammalian fertilization in vitro by membrane vesicles from seminal plasma. Proc. Soc. Exp. Biol. Med. 146, 11-16.
14. De Lamirande, E., and Gagnon, C. (1984). Origin of a motility inhibitor within the male reproductive tract. J. Androl. 5, 269-276.
15. Dot, H. M., Harrison, R. A. P., and Foster, G. C.A. (1979). The maintenance of motility and the surface properties of epididymal spermatozoa from bull, rabbit and ram in homologous seminal and epididymal plasma. J. Reprod. Fertil. 62, 113-124.
16. Gamzu, R., Yavetz, H., Lichtenberg, D., Paz, G., Homonnai, Z.T., and Yogev, L. (1994). The effect of egg yolk on the binding capacity of human spermatozoa to zona pellucida. Fertil. Steril. 62, 1221-1225.
17. Gamzu, R., Yogev, L., Botchan, A., Amit, A., Lessing, J. B., Lichtenberg, D., Paz, G., and Yavetz, H. (1997). Effect of sperm preparation with TEST yolk buffer on sperm-binding capacity under hemizona assay conditions. Andrologia 29, 17-21.
18. Gao, D., and Critser, J. K. (2000). Mechanisms of cryoinjury in living cells. Inst. Lab. Anim. Res. J. 41, 187-196.
19. Garcia, M. A., and Graham, E. F. (1987a). Dialysis of bovine semen and its effects on fresh and freeze-thawed spermatozoa. Cryobiology 24, 446-454. doi:10.1016/0011-2240(87)90048-4
20. Garcia, M. A., and Graham, E. F. (1987b). Effects of low-molecular weight fractions (LMWF) from milk, egg yolk and seminal plasma on freezability of bovine spermatozoa. Cryobiology 24, 429-436. doi:10.1016/0011-2240(87)90046-0
21. Garcia, M. A., and Graham, E. F. (1987c). Factors affecting the removal of low-molecular weight fractions (LMWF) from egg yolk and seminal plasma in extended semen by dialysis: Effect of post-thaw sperm survival. Cryobiology 24, 437-445. doi:10.1016/0011-2240(87)90047-2
22. Garcia-Lopez, N., Ollero, M., Cebrian-Perez, J. A., and Muino-Blanco, T. (1996). Reversion of thermic-shock effect on ram spermatozoa by adsorption of seminal plasma proteins revealed by partition in aqueous two-phase systems. J. Chromatogr. B 680, 137-143. doi:10.1016/0378-4347(95)00394-0
23. Gilmore, J. A., Liu, J., Peter, A. T., and Critser, J. K. (1998). Determination of plasma membrane characteristics of boar spermatozoa and their relevance to cryopreservation. Biol. Reprod. 58, 28-36. doi:10.1095/BIOLREPROD58.1.28
24. Goodrowe, K. L., Hay, M. A., Platz, C. C., Behrns, S. K., Jones, M. H., and Waddell, W. T. (1998). Characteristics of fresh and frozen-thawed red wolf (Canis rufus) spermatozoa. Anim. Reprod. Sci. 53, 299-308. doi:10.1016/S0378-4320(98)00119-5
25. Graham, J. K. (1994). Effect of seminal plasma on the motility of the epididymal and ejaculated spermatozoa of the ram and bull during the cryopreservation process. Theriogenology 41, 1151-1162. doi:10.1016/S0093-691X(05)80037-8
26. Graham, J. K., and Foote, R. H. (1987). Effect of several lipids, fatty acyl chain length and degree of unsaturation on the motility of bull spermatozoa after cold shock and freezing. Cryobiology 24, 42-52. doi:10.1016/0011-2240(87)90005-8
27. Hay, M. A., King, W. A., Gartley, C. J., Leibo, S. P., and Goodrowe, K. L. (1997). Canine spermatozoa: cryopreservation and evaluation of gamete interaction. Theriogenology 48, 1329-1342. doi:10.1016/S0093- 691X(97)00374-9
28. Holt, W. V. (2000). Fundamental aspects of sperm cryobiology: the importance of species and individual differences. Theriogenology 53, 47-58. doi:10.1016/S0093-691X(99)00239-3
29. Holt, W. V., Abaigar, T., Watson, P. F., and Wildt, D. E. (2003). Genetic resource banks for species conservation. In 'Reproductive Science and Integrated Conservation'. (Eds W. V. Holt, A. R. Pickard, J. C. Rodger and D. E. Wildt.) pp. 267-280. (Cambridge University Press: Cambridge.)
30. Howard, J. G. (1992). Feline semen analysis and artificial insemination. In 'Current Veterinary Therapy XI'. (Ed. R. W. Kirk.) pp. 929-938. (WB Saunders: Philadelphia.)
31. Howard, J. G. (1993). Semen collection and analysis in nondomestic carnivores. In 'Zoo and Wild Animal Medicine: Current Therapy III'. (Ed. M. E. Fowler.) pp. 390-399. (WB Saunders: Philadelphia.)
32. Howard, J. G., Bush, M., and Wildt, D. E. (1986). Semen collection, analysis and cryopreservation in nondomestic mammals. In 'Current Therapy in Theriogenology'. (Ed. D. Morrow.) pp. 1047-1053. (WB Saunders: Philadelphia.)
33. Howard, J. G., Bush, M., Morton, C., Morton, F., and Wildt, D. E. (1991). Comparative semen cryopreservation in ferrets (Mustela putorius furo) and pregnancies after laparoscopic intrauterine insemination with frozen-thawed spermatozoa. J. Reprod. Fertil. 92, 109-118.
34. Howard, J. G., Kwiatkowski, D. R., Williams, E. S., Atherton, R. W., Kitchin, R. M., Thorne, E. T., Bush, M., and Wildt, D. E. (1996). Pregnancies in black-footed ferrets and Siberian polecats after laparoscopic artificial insemination with fresh and frozen-thawed semen. In 'Proceedings of the American Society of Andrology'. J. Androl. (Suppl.) 16 (Abstract 115.) p. 51.
35. Howard, J. G., Wolf, K. N., Vargas, A., Marinari, P., Kreeger, J., Williamson, L., and Wildt, D. E. (1997). Enhanced reproductive efficiency and pregnancies after artificial insemination in black-footed ferrets. In 'Proceedings of the American Association of Zoo Veterinarians'. (Ed. American Association of Zoo Veterinarians.) pp. 351-352. (American Association of Zoo Veterinarians: Houston, TX.)
36. Howard, J. G., Marinari, P. E., and Wildt, D. E. (2003). Black-footed ferret: model for assisted reproductive technologies contributing to in situ conservation. In 'Reproductive Science and Integrated Conservation'. (Eds W. V. Holt, A. R. Pickard, J. C. Rodger and D. E. Wildt.) pp. 249-266. (Cambridge University Press: Cambridge.)
37. Howard, J. G., Santymire, R. M., Marinari, P. E., Kreeger, J. S., Williamson, L., and Wildt, D. E. (2006). Use of reproductive technology for black-footed ferret recovery. In 'U.S. Geological Survey Scientific Investigations Report 2005-5293'. (Eds J. E. Roelle, B. J. Miller, J. L. Godbey and D. E. Biggin.) pp. 28-36. (US Geological Survey: Reston, VA.)
38. Iwamoto, T., and Gagnon, C. (1988). Purification and characterization of a spermmotility inhibitor in human seminal plasma. J.Androl. 9, 377-383.
39. Iwamoto, T., Tanaka, H., Osada, T., Shinagawa, T., Osamura, Y., and Gagnon, C. (1993). Origin of a spermmotility inhibitor from boar seminal plasma. Mol. Reprod. Dev. 36, 475-481. doi:10.1002/MRD.1080360411
40. Jacobs, B. R., Caulfield, J., and Boldt, J. (1995). Analysis of TEST (TES and Tris) yolk buffer effects on human sperm. Fertil. Steril. 63, 1064-1070.
41. Kampschmidt, R. F., Mayer, D. T., and Herman, H. A. (1953). Lipid and lipoprotein constituents of egg yolk in the resistance and storage of bull spermatozoa. J. Dairy Sci. 36, 733-742.
42. Kawano, N., Shimada, M., and Terada, T. (2004). Motility and penetration competence of frozen-thawed miniature pig spermatozoa are substantially altered by exposure to seminal plasma before freezing. Theriogenology 61, 351-364. doi:10.1016/S0093-691X(03)00218-8
43. Koshimoto, C., Gamliel, E., and Mazur, P. (2000). Effect of osmolality and oxygen tension on the survival of mouse sperm frozen to various temperatures in various concentrations of glycerol and raffinose. Cryobiology 41, 204-231. doi:10.1006/CRYO.2000.2281
44. Maxwell, W. M. C., and Johnson, L. A. (1999). Physiology of spermatozoa at high dilution rates: The influence of seminal plasma. Theriogenology 52, 1353-1362. doi:10.1016/S0093-691X(99)00222-8
45. Maxwell, W. M. C., Welch, G. R., and Johnson, L. A. (1996). Viability and membrane integrity of spermatozoa after dilution and flow cytometric sorting in the presence or absence of seminal plasma. Reprod. Fertil. Dev. 8, 1165-1178. doi:10.1071/RD9961165
46. Medeiros, C. M. O., Forell, F., Oliveira, A. T. D., and Rodrigues, J. L. (2002). Current status of sperm cryopreservation: Why isn't it better? Theriogenology 57, 327-344. doi:10.1016/S0093-691X(01)00674-4
47. Moore, H. D. M., and Hibbit, K. G. (1977). Fertility of boar spermatozoa after freezing in the absence of seminal vesicular proteins. J. Reprod. Fertil. 50, 349-352.
48. Ollero, M., Garcia-Lopez, N., Cebrian-Perez, J. A., and Muino-Blanco, T. (1997). Surface changes of ram spermatozoa by adsorption of homologous and heterologous seminal plasma proteins revealed by partition in an aqueous two-phase system. Reprod. Fertil. Dev. 9, 381-390. doi:10.1071/R96037
49. Parks, J. E. (1997). Hypothermia and mammalian gametes. In 'Reproductive Tissue Banking'. (Eds A. M. Karow and J. K. Critser.) pp. 229-261. (Academic Press: San Diego.)
50. Pukazhenthi, B. S., Pelican, K., Wildt, D., and Howard, J. (1999). Sensitivity of domestic cat (Felis catus) sperm from normospermic versus teratospermic donors to cold-induced acrosomal damage. Biol. Reprod. 61, 135-141. doi:10.1095/BIOLREPROD61.1.135
51. Pursel, V. G., Johnson, L. A., and Schulman, L. L. (1973). Effect of dilution, seminal plasma and incubation period on cold shock susceptibility of boar spermatozoa. J. Anim. Sci. 37, 528-531.
52. Ritar, A. J., and Salamon, S. (1982). Effect of seminal plasma and its removal and of egg yolk in the diluent on the survival of fresh and frozen thawed spermatozoa of Angor goat. Aust. J. Biol. Sci. 35, 305-312.
53. Santymire, R. M., Marinari, P. E., Kreeger, J. S., Wildt, D. E., and Howard, J. G. (2006). Spermviability in the black-footed ferret (Mustela nigripes) is influenced by seminal and medium osmolality. Cryobiology 53, 37-50.
54. Schmehl, M. K., Anderson, S. P., Vazquez, I. A., and Graham, E. F. (1986). The effect of dialysis of extended ram semen prior to freezing on post-thaw survival and fertility. Cryobiology 23, 406-414. doi:10.1016/0011-2240(86)90025-8
55. Thomas, C. A., Garner, D. L., DeJarnette, J. M., and Marshall, C. E. (1998). Effect of cryopreservation on bovine sperm organelle function and viability as determined by flow cytometry. Biol. Reprod. 58, 786-793. doi:10.1095/BIOLREPROD58.3.786
56. Watson, P. F. (1979). The preservation of semen in mammals. In 'Oxford Reviews of Reproductive Biology'. (Ed. C. A. Finn.) pp. 283-350. (Oxford University Press: London.)
57. Watson, P. F. (1995). Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function. Reprod. Fertil. Dev. 7, 871-891. doi:10.1071/RD9950871
58. Wildt,D. E. (1997). Genome resource banking: impact on biotic conservation and society. In 'Reproductive Tissue Banking'. (Eds A. M. Karow and J. K. Critser.) pp. 399-439. (Academic Press: San Diego.)
59. Wildt, D. E., and Goodrowe, K. (1989). The potential for embryo technology in the black-footed ferret. In 'Conservation Biology and the Black-Footed Ferret'. (Eds U. S. Seal, E. T. Thorne, M. A. Bogan and S. H. Anderson.) pp. 160-176. (Yale University Press: New Haven.)
60. Wildt, D. E., Bush, M., Morton, C., Morton, F., and Howard, J. G. (1989). Semen characteristics and testosterone profiles in ferrets kept in long-day photoperiod, and the influence of hCG timing and sperm dilution on pregnancy rate after laparoscopic insemination. J. Reprod. Fertil. 86, 349-358.
61. Wildt, D. E., Rall, W. F., Critser, J. K., Monfort, S. L., and Seal, U. S. (1997). Genome resource banks: living collections for biodiversity conservation. Bioscience 47, 689-698. doi:10.2307/1313209
62. Wolf, K. N., Wildt, D. E., Vargas, A., Marinari, P. E., Kreeger, J. S., Ottinger, M. A., and Howard, J. G. (2000a). Age dependent changes in sperm production, semen quality and testicular volume in black-footed ferrets (Mustela nigripes). Biol. Reprod. 63, 179-187. doi:10.1095/BIOLREPROD63.1.179
63. Wolf, K. N., Wildt, D. E., Vargas, A., Marinari, P. E., Ottinger, M. A., and Howard, J. G. (2000b). Reproductive inefficiency in male black-footed ferrets (Mustela nigripes). Zoo Biol. 19, 517-528. doi:10.1002/1098-2361(2000)19:6〈517::AID-ZOO4〉3.0.CO;2-V
64. Yogev, L., Homonnai, Z. T., Gamzu, R., Amit, A., Lessing, J. B., Paz, G., and Yavetz, H. (1995). The use of hemizona assay in the evaluation of the optimal sperm preparation technique. Hum. Reprod. 10, 851-854.