Controlled cooling during semen cryopreservation does not induce capacitation of spermatozoa from two portions of the boar ejaculate

International Journal of Andrology

Volumn 30, Issue 6, 2007, Pages 485-499

  Saravia, F ^a   Hernandez M ^b   Wallgren, M ^a,c   Johannisson, A ^a   Rodriguez Martinez H ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UNIVERSITY OF MURCIA   (Spain)

^c Quality Genetics   (Sweden)

Author keywords

Boar; Capacitation; Computer assisted sperm analysis; Cryopreservation; Plasma membrane integrity; Plasma membrane stability; Spermatozoa

Indexed keywords

BICARBONATE; GLYCEROL; LACTOSE; LIPOCORTIN 5; MEROCYANINE; PHOSPHATIDYLSERINE; PROPIDIUM IODIDE;

ANIMAL CELL; ARTICLE; BOAR (MALE PIG); CELL DAMAGE; CELL MEMBRANE; COMPUTER ANALYSIS; CONTROLLED STUDY; COOLING; CRYOPRESERVATION; CULTURE MEDIUM; FLOW CYTOMETRY; INCUBATION TIME; LIPID MEMBRANE; MALE; MEMBRANE DAMAGE; NONHUMAN; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL; SEMEN ANALYSIS; SEMINAL PLASMA; SPERM PRESERVATION; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON MIGRATION; SPERMATOZOON MOTILITY; THAWING;

ANIMALS; CELL MEMBRANE; CELL SURVIVAL; CENTRIFUGATION; CRYOPRESERVATION; CRYOPROTECTIVE AGENTS; FLOW CYTOMETRY; KINETICS; MALE; PHOSPHATIDYLSERINES; SEMEN PRESERVATION; SPERM CAPACITATION; SPERM MOTILITY; SPERMATOZOA; SUS SCROFA;

EID: 36248932171     PISSN: 01056263     EISSN: 13652605     Source Type: Journal    
DOI: 10.1111/j.1365-2605.2006.00741.x     Document Type: Article

References (70)

1. Abeydeera, L. R., Funahashi, H., Kim, N. H. Day, B. N. (1997) Chlortetracycline fluorescence patterns and in vitro fertilisation of frozen-thawed boar spermatozoa incubated under various bicarbonate concentrations. Zygote 5, 117 125.
2. Almid, T. Hofmo, P. O. (1996) A brief review of frozen semen application under Norwegian AI service conditions. Reproduction in Domestic Animals 31, 169 173.
3. Ashworth, P. J., Harrison, R. A. P., Miller, N. G., Plummer, J. M. Watson, P. F. (1995) Flow cytometric detection of bicarbonate-induced changes in lectin binding in boar and ram sperm populations. Molecular Reproduction and Development 40, 164 176.
4. Austin, C. R. (1951) Observations on the penetration of the sperm into the Fallopian tube and in the uterus. Journal of Experimental Zoology 151, 159 166.
5. Bergqvist, A.-S., Ballester, J., Johannisson, A., Hernández, M., Lundeheim, N. Rodríguez-Martínez, H. (2006) In vitro capacitation of bull spermatozoa by oviductal fluid and its components. Zygote 14, 259 273.
6. Brackett, B. G. Oliphant, G. (1975) Capacitation of rabbit spermatozoa in vitro. Biology of Reproduction 12, 260 274.
7. Bravo, M. M., Aparicio, I. M., Garcia-Herreros, M., Gil, M. C., Peña, F. J. Garcia-Marin, L. J. (2005) Changes in tyrosine phosphorylation associated with true capacitation and capacitation-like state in boar spermatozoa. Molecular Reproduction and Development 71, 88 96.
8. Buhr, M. M., Curtis, E. F. Kakuda, N. S. (1994) Composition and behavior of head membrane lipids of fresh and cryopreserved boar sperm. Cryobiology 31, 224 238.
9. Chang, M. C. (1951) Fertilising capacity of spermatozoa deposited into the Fallopian tubes. Nature (London) 168, 697 698.
10. Cormier, N., Sirard, M. A. Bailey, J. L. (1997) Premature capacitation of bovine spermatozoa is initiated by cryopreservation. Journal of Andrology 18, 461 468.
11. Cremades, T., Roca, J., Rodríguez-Martínez, H., Abaigar, T., Vázquez, J. M. Martínez, E. (2005) Kinematic changes during the cryopreservation of boar spermatozoa. Journal of Andrology 26, 610 618.
12. Eddy, E. M. (1994) The spermatozoon. In : The Physiology of Reproduction, 2nd edn (eds E. Knobil J. D. Neill pp. 29 78. Raven Press, New York, NY.
13. Ekwall, H., Hernández, M., Saravia, F. Rodríguez- Martínez, H. (2007) Cryo-scanning electron microscopy (Cryo-SEM) of boar semen frozen in medium-straws and MiniFlatPacks. Theriogenology, in press.
14. Eriksson, B. M. Rodríguez-Martínez, H. (2000a) Deep-freezing of boar semen in plastic film ''cochettes''. Journal of Veterinary Medicine. A, Physiology, Pathology, Clinical Medicine 47, 89 97.
15. Eriksson, B. M. Rodríguez-Martínez, H. (2000b) Effect of freezing and thawing rates on the post-thaw viability of boar spermatozoa frozen in FlatPacks and Maxi-straws. Animal Reproduction Science 63, 205 220.
16. Eriksson, B. M., Vázquez, J. M., Martínez, E., Roca, J., Lucas, X. Rodríguez-Martínez, H. (2001) Effects of holding time during cooling and of type of package on plasma membrane integrity, motility and in vitro oocyte penetration ability of frozen-thawed boar spermatozoa. Theriogenology 55, 1593 1605.
17. Flesch, F. M. Gadella, B. M. (2000) Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochimica et Biophysica Acta, Rev 1469, 197 235.
18. Fraser, L. R., Abeydeera, L. R. Niwa, K. (1995) Ca(2+)-regulating mechanisms that modulate bull sperm capacitation and acrosomal exocytosis as determined by chlortetracycline analysis. Molecular Reproduction and Development 40, 233 241.
19. Fuller, S. J. Whittingham, D. G. (1996) Effect of cooling mouse spermatozoa to 4 degrees C on fertilization and embryonic development. Journal of Reproduction and Fertility 108, 139 145.
20. Gadella, B. M. Harrison, R. A. P. (2000) The capacitating agent bicarbonate induces protein kinase A-dependent changes in phospholipid transbilayer behavior in the sperm plasma membrane. Development 127, 2407 2420.
21. Gadella, B. M. Harrison, R. A. P. (2002) Capacitation induces cyclic adenosine 3′,5′-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells. Biology of Reproduction 67, 340 350.
22. Graham, E. F., Rajamannan, A. H. J., Schmehl, M. K. L., Maki-Laurila, M. Bower, R. E. (1971) Preliminary report on procedure and rationale for freezing boar semen. Artificial Insemination Digest 19, 12 14.
23. Green, C. E. Watson, P. F. (2001) Comparison of the capacitation-like state of cooled boar spermatozoa with true capacitation. Reproduction 122, 889 898.
24. Guthrie, H. D. Welch, G. R. (2005a) Impact of storage prior to cryopreservation on plasma membrane function and fertility of boar sperm. Theriogenology 63, 396 410.
25. Guthrie, H. D. Welch, G. R. (2005b) Effects of hypothermic liquid storage and cryopreservation on basal and induced plasma membrane phospholipid disorder and acrosome exocytosis in boar spermatozoa. Reproduction, Fertility, and Development 17, 467 477.
26. Harrison, R. A. P. (1996) Capacitation mechanisms, and the role of capacitation as seen in eutherian mammals. Reproduction, Fertility, and Development 8, 581 594.
27. Harrison, R. A. P. (2004) Rapid PKA-catalysed phosphorylation of boar sperm proteins induced by the capacitating agent bicarbonate. Molecular Reproduction and Development 67, 337 352.
28. Harrison, R. A. P. Gadella, B. M. (2005) Bicarbonate-induced membrane processing in sperm capacitation. Theriogenology 63, 342 351.
29. Harrison, R. A. P. Miller, N. G. (2000) cAMP-dependent protein kinase control of plasma membrane lipid architecture in boar sperm. Molecular Reproduction and Development 55, 220 228.
30. 2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Molecular Reproduction and Development 45, 378 391.
31. Hernández M., Ekwall H., Roca J., Vázquez J. M., Martínez E. Rodríguez-Martínez H. (2007) Cryo-scanning electron microscopy (Cryo-SEM) of semen frozen in medium-straws from good and sub-standard freezer AI-boars. Cryobiology 54, 63 70.
32. Ho, H.-C. Suarez, S. S. (2001) Hyperactivation of mammalian spermatozoa: function and regulation. Reproduction 122, 519 526.
33. Hunter, R. H. Rodríguez-Martínez, H. (2004) Capacitation of mammalian in vivo, with a specific focus on events in the Fallopian tubes. Molecular Reproduction and Development 67, 243 250.
34. Januskauskas, A., Lukoseviciute, K., Nagy, S., Johannisson, A. Rodríguez-Martínez, H. (2005) Assessment of the efficacy of Sephadex G-15 filtration of bovine spermatozoa for cryopreservation. Theriogenology 63, 160 178.
35. Kaneto, M., Harayama, H., Miyake, M. Kato, S. (2002) Capacitation-like alterations in cooled boar spermatozoa: assessment by the chlortetracycline staining assay and immunodetection of tyrosine-phosphorylated sperm proteins. Animal Reproduction Science 73, 197 209.
36. Koopman, G., Reutelingsperger, C. P., Kuijten, G. A., Keehnen, R. M., Pals, S. T. Van Oers, M. H. (1994) Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84, 1415 1420.
37. Langner, M. Hui, S. W. (1993) Merocyanine interaction in phosphatidylcholine bilayers. Biochimica et Biophysica Acta 1149, 175 179.
38. Lee, M. A. Storey, B. T. (1986) Bicarbonate is essential for fertilization of mouse eggs: mouse sperm require it to undergo the acrosome reaction. Biology of Reproduction 34, 349 356.
39. Maxwell, W. M. C. Johnson, L. A. (1997a) Chlortetracycline analysis of boar spermatozoa after incubation, flow cytometric sorting, cooling or cryopreservation. Molecular Reproduction and Development 46, 408 418.
40. Maxwell, W. M. C. Johnson, L. A. (1997b) Membrane status of boar spermatozoa after cooling or cryopreservation. Theriogenology 48, 209 219.
41. Mazur P. (1985) Basic concepts in freezing cells. In : Deep Freezing of Boar Semen (eds L. A. Johnson K. Larsson pp. 91 111. Proc. 1st Int. Conf. Deep Freezing of Boar Semen, SLU, Uppsala, Sweden.
42. Neild D. M., Flores M. C. Agüero A. (1999) Espermatozoides equinos: inducción de la capacitación por efecto de la criopreservación. (Equine spermatozoa: induction of capacitation for the purpose of cryopreservation.) Revista Brasileira Reprodução Animal 23, 293 295 [in Spanish].
43. Okamura, N., Tajima, Y., Soejima, A., Masuda, H. Sugita, Y. (1985) Sodium bicarbonate in seminal plasma stimulates the motility of mammalian spermatozoa through direct activation of adenylate cyclase. The Journal of Biological Chemistry 260, 9699 9705.
44. Parks, J. E. Graham, J. K. (1992) Effects of cryopreservation procedures on sperm membranes. Theriogenology 38, 209 222.
45. Peña, F. J., Johannisson, A., Wallgren, M. Rodríguez- Martínez, H. (2003) Assessment of fresh and frozen-thawed boar semen using an Annexin-V assay: a new method of evaluating sperm membrane integrity. Theriogenology 60, 677 689.
46. Peña, F. J., Johannisson, A., Wallgren, M. Rodríguez- Martínez, H. (2004) Antioxidant supplementation of boar spermatozoa from different fractions of the ejaculate improves cryopreservation: changes in sperm membrane lipid architecture. Zygote 12, 117 124.
47. Pérez, L. J., Valcárcel, A., De las Heras, M. A., Moses, D. Baldassarre, H. (1996) Evidence that frozen/thawed ram spermatozoa show accelerated capacitation in vitro as assessed by chlortetracycline assay. Theriogenology 46, 131 140.
48. Rathi, R., Colenbrander, B., Bevers, M. M. Gadella, B. M. (2001) Evaluation of in vitro capacitation of stallion spermatozoa. Biology of Reproduction 65, 462 470.
49. Roca, J., Rodríguez-Martínez, H., Vázquez, J. M., Bolarín, A., Hernández, M., Saravia, F., Wallgren, M. Martínez, E. A. (2005) Strategies to improve the fertility of frozen-thawed boar semen for artificial insemination. In : Control of Pig Reproduction VII, 1st edn (eds C. J. Ashworth R. R. Kraeling pp. 261 275. Nottingham University Press, Nottingham, UK.
50. Rodríguez-Martínez, H., Saravia, F., Wallgren, M., Tienthai, P., Johannisson, A., Vázquez, J. M., Martínez, E., Roca, J., Sanz, L. Calvete, J. J. (2005) Boar spermatozoa in the oviduct. Theriogenology 63, 514 535.
51. Saravia, F., Wallgren, M., Nagy, S., Johannisson, A. Rodríguez- Martínez, H. (2005) Deep freezing of concentrated boar semen for intrauterine insemination: effect on sperm viability. Theriogenology 63, 1320 1333.
52. Schmidt, H. Kamp, G. (2004) Induced hyperactivity in boar spermatozoa and its evaluation by computer-assisted analysis. Reproduction 128, 171 179.
53. Sieber, F. (1987) Merocyanine 540. Photochemistry and Photobiology 46, 1035 1042.
54. Silva, P. F. Gadella, B. M. (2006) Detection of damage in mammalian sperm cells. Theriogenology 65, 958 978.
55. Simonsson A. (1994) Näringsrekommendationer och fodermedel till svin. (Nutritional Recommendations and Feedstuff for Swine.), Vol. 75, p. 71. Research Information Centre, Swedish University of Agricultural Sciences Uppsala, Sweden [in Swedish].
56. Steponkus, P. L. Lynch, D. V. (1989) Freeze/thaw-induced destabilization of the plasma membrane and the effects of cold acclimation. Journal of Bioenergetics and Biomembranes 21, 21 41.
57. Tardif, S., Dube, C. Bailey, J. L. (2003) Porcine sperm capacitation and tyrosine kinase activity are dependent on bicarbonate and calcium but protein tyrosine phosphorylation is only associated with calcium. Biology of Reproduction 68, 207 213.
58. Thomas, A. D., Meyers, S. A. Ball, B. A. (2006) Capacitation-like changes in equine spermatozoa following cryopreservation. Theriogenology 65, 1531 1550.
59. Tienthai, P., Johannisson, A. Rodríguez-Martínez, H. (2004) Sperm capacitation in the porcine oviduct. Animal Reproduction Science 80, 131 146.
60. Tsien, R. Y. (1989) Fluorescent indicators of ion concentrations. In : Fluorescence Microscopy of Living Cells in Culture. Part 6B (ed Yu-Li Wang D. Lansing Taylor Academic Press, San Diego, USA. pp. 127 156.
61. Vadnais, M. L., Kirkwood, R. N., Tempelman, R. J., Sprecher, D. J. Chou, K. (2005) Effect of cooling and seminal plasma on the capacitation status of fresh boar sperm as determined using chlortetracycline assay. Animal Reproduction Science 87, 121 132.
62. Verhoven, B., Schlegel, R. A. Williamson, P. (1995) Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal, on apoptotic T lymphocytes. The Journal of Experimental Medicine 182, 1597 1601.
63. Vermes, I., Haanen, C., Steffens-Nakken, H. Reutelingsperger, C. (1995) A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. Journal of Immunological Methods 184, 39 51.
64. Visconti, P. E., Westbrook, V. A., Chertihin, O., Demarco, S., Sleight, S. Diekman, A. B. (2002) Novel signalling pathways involved in sperm acquisition of fertility capacity. Journal of Reproductive Immunology 53, 133 150.
65. Waberski, D., Weitze, K. F., Gleumes, T., Schwarz, M., Willmen, T. Petzoldt, R. (1994) Effect of time of insemination relative to ovulation on fertility with liquid and frozen boar semen. Theriogenology 42, 831 840.
66. Watson, P. F. (1995) Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function. Reproduction, Fertility, and Development 7, 871 891.
67. Williamson, P. Schlegel, R. A. (1994) Back and forth: the regulation and function of transbilayer phospholipids movement in eukaryotic cells. Molecular Membrane Biology 11, 199 216.
68. Williamson, P., Mattocks, K. Schlegel, R. A. (1983) Merocyanine 540, a fluorescent probe sensitive to lipid packing. Biochimica et Biophysica Acta 732, 387 393.
69. Yanagimachi, R. (1994) Mammalian fertilization. In : The Physiology of Reproduction, 2nd edn (eds E. Knobil J. D. Neill pp. 189 317. Raven Press, New York, NY.
70. Zachowski, A. (1993) Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. The Biochemical Journal 294, 1 14.