Capacitation-like changes in equine spermatozoa following cryopreservation

Theriogenology

Volumn 65, Issue 8, 2006, Pages 1531-1550

  Thomas, A D ^a   Meyers, S A ^a   Ball, B A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Capacitation; Cryocapacitation; Cryopreservation; Equine; Sperm

Indexed keywords

CRYOPROTECTIVE AGENT; ENZYME INHIBITOR; PHOSPHOLIPID TRANSFER PROTEIN; STAUROSPORINE;

ANIMAL; ANIMAL DISEASE; ARTICLE; CELL MEMBRANE; CRYOPRESERVATION; DRUG EFFECT; HORSE; IN VITRO STUDY; MALE; METABOLISM; METHODOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPERM PRESERVATION; SPERMATOZOON; SPERMATOZOON CAPACITATION;

ANIMALS; CELL MEMBRANE; CRYOPRESERVATION; CRYOPROTECTIVE AGENTS; ENZYME INHIBITORS; HORSES; MALE; PHOSPHOLIPID TRANSFER PROTEINS; SEMEN PRESERVATION; SIGNAL TRANSDUCTION; SPERM CAPACITATION; SPERMATOZOA; STAUROSPORINE;

EQUIDAE;

EID: 33645929059     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2005.08.022     Document Type: Article

References (65)

1. Bedford S.J., Meyers S.A., and Varner D.D. Acrosomal status of fresh, cooled and cryopreserved stallion spermatozoa. J Reprod Fertil 56 Suppl. (2000) 133-140
2. Green C.E., and Watson P.F. Comparison of the capacitation-like state of cooled boar spermatozoa with true capacitation. Reproduction 122 (2001) 889-898
3. Schembri M.A., Major D.A., Suttie J.J., Maxwell W.M.C., and Evans G. Capacitation-like changes in equine spermatozoa throughout the cryopreservation process. Reprod Fertil Dev 14 (2002) 225-233
4. Cormier N., and Bailey J.L. A differential mechanism is involved during heparin-and cryopreservation-induced capacitation of bovine spermatozoa. Biol Reprod 69 (2003) 177-185
5. Neild D.M., Gadella B.M., Chaves M.G., Miragaya M.H., Colenbrander B., and Agüero A. Membrane changes during different stages of a freeze-thaw protocol for equine semen cryopreservation. Theriogenology 59 (2003) 1693-1705
6. Ellington J.E., Samper J.C., Jones A.E., Oliver S.A., Burnett K.M., and Wright R.W. In vitro interactions of cryopreserved stallion spermatozoa and oviduct (uterine tube) epithelial cells or their secretory products. Anim Reprod Sci 56 (1999) 51-65
7. Sion B., Janny L., Boucher D., and Grizard G. Annexin V binding to plasma membrane predicts the quality of human cryopreserved spermatozoa. Int J Androl 27 (2004) 108-114
8. Bevers E.M., Comfurius P., Dekkers D.W.C., and Zwaal R.F.A. Lipid translocation across the plasma membrane of mammalian cells. Biochim Biophys Acta 1439 (1999) 317-330
9. Gadella B.M., and Harrison RA.P. Capacitation induces cyclic adenosine 3′,5′-mono-phosphate-dependent, but apoptosis-unrelated, exposure of amino-phospholipids at the apical head plasma membrane of boar sperm cells. Biol Reprod 67 (2002) 340-350
10. Glander H.J., and Schaller J. Binding of annexin V to plasma membranes of human spermatozoa: a rapid assay for detection of membrane changes after cryostorage. Mol Hum Reprod 5 (1999) 109-115
11. Duru N.K., Morshedi M., Schuffner A., and Oehninger S. Cryopreservation-thawing of fractionated human spermatozoa and plasma membrane translocation of phosphatidylserine. Fertil Steril 75 (2001) 263-268
12. Duru N.K., Morshedi M.S., Schuffner A., and Oehninger S. Cryopreservation- thawing of fractionated human spermatozoa is associated with membrane phosphatidyl-serine externalization and not DNA fragmentation. J Androl 22 (2001) 646-651
13. Schuffner A., Morshedi M., and Oehninger S. Cryopreservation of fractionated, highly motile human spermatozoa: effect on membrane phosphatidylserine externalization and lipid peroxidation. Hum Reprod 16 (2001) 2148-2153
14. Anzar M., He L., Buhr M.M., Kroetsch T.G., and Pauls K.P. Sperm apoptosis in fresh and cryopreserved bull semen detected by flow cytometry and its relationship with fertility. Biol Reprod 66 (2002) 354-360
15. Flesch F.M., Brouwers J.F.H.M., Nievelstein P.F.E.M., Verkleij A.J., van Golde L.M.G., Colenbrander B., et al. Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. J Cell Sci 114 (2001) 3543-3555
16. de Vries K.J., Wiedmer T., Sims P.J., and Gadella B.M. Caspase-independent exposure of aminophospholipids and tyrosine phosphorylation in bicarbonate responsive human sperm cells. Biol Reprod 68 (2003) 2122-2134
17. Cross N.L. Decrease in order of human sperm lipids during capacitation. Biol Reprod 69 (2003) 529-534
18. Sieber F. Meyocyanine 540. Photochem Photobiol 46 (1987) 1035-1042
19. Rathi R., Colenbrander B., Bevers M.M., and Gadella B.M. Evaluation of in vitro capacitation of stallion spermatozoa. Biol Reprod 65 (2001) 462-470
20. Go K.J., and Wolf D.P. The role of sterols in sperm capacitation. Adv Lipid Res 20 (1983) 317-330
21. Bavister B.D., Kinsey D.L., Lane M., and Gardner D.K. Recombinant human albumin supports hamster in-vitro fertilization. Hum Reprod 18 (2003) 113-116
22. Visconti P.E., Westbrook V.A., Chertihin O., Demarco I., Sleight S., and Diekman A.B. Novel signaling pathways involved in sperm acquisition of fertilizing capacity. J Reprod Immunol 53 (2002) 133-150
23. Huang Y.-H., Chu S.-T., and Chen Y.-H. A seminal vesicle autoantigen of mouse is able to suppress sperm capacitation-related events stimulated by serum albumin. Biol Reprod 63 (2000) 1562-1566
24. Stewart-Savage J. Effect of bovine serum albumin concentration and source on sperm capacitation in the golden hamster. Biol Reprod 49 (1993) 74-81
25. Choi Y.H., Landim-Alvarenga F.C., Seidel Jr. G.E., and Squires E.L. Effect of capacitation of stallion sperm with polyvinylalcohol or bovine serum albumin on penetration of bovine zona-free or partially zona-removed equine oocytes. J Anim Sci 81 (2003) 2080-2087
26. Bhattacharyya A. Albumin is required for the guinea pig sperm capacitation but is not essential for acrosome reaction and fusion with eggs. Arch Androl 28 (1992) 235-239
27. Heitland A.V., Jasko D.J., Squires E.L., Graham J.K., Pickett B.W., and Hamilton C. Factors affecting motion characteristics of frozen-thawed stallion spermatozoa. Equine Vet J 28 (1996) 47-53
28. van Heerde W.L., de Groot P.G., and Reutelingsperger C.P. The complexity of the phospholipid binding protein Annexin V. Thromb Haemost 73 (1995) 172-179
29. van Engeland M., Nieland L.J.W., Ramaekers F.C.S., Schutte B., and Reutelingsperger C.P.M. Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31 (1998) 1-9
30. Baumber J., Ball B.A., and Linfor J. Assessment of the cryopreservation of equine spermatozoa in the presence of enzyme scavengers and antioxidants. Am J Vet Res 66 (2005) 772-779
31. Pommer A.C., Rutllant J., and Meyers S.A. Phosphorylation of protein tyrosine residues in fresh and cryopreserved stallion spermatozoa under capacitating conditions. Biol Reprod 68 (2003) 1208-1214
32. Baumber J., Sabeur K., Vo A., and Ball B.A. Reactive oxygen species promote tyrosine phosphorylation and capacitation in equine spermatozoa. Theriogenology 60 (2003) 1239-1247
33. Kaul G., Kumar M., Gandhi K.K., and Anand S.R. Surface protein changes in goat spermatozoa during capacitation. Indian J Exp Biol 38 (2000) 18-25
34. Sasaki Y., Shukla R., and Smith B.D. Facilitated phosphatidylserine flip-flop across vesicle and cell membranes using urea-derived synthetic translocases. Org Biomol Chem 2 (2004) 214-219
35. 2+-dependent transbilayer movement of phosphopholipid. J Biol Chem 271 (1996) 17205-17210
36. Littell R.C., Freund R.J., and Spector P.C. SAS system for linear models. 3rd ed. (1991), SAS Institute Inc., Cary, NC 329p
37. Dinkins M.B., and Brackett B.G. Chlortetracycline staining patterns of frozen-thawed bull spermatozoa treated with β-cyclodextrins, dibutyryl cAMP and progesterone. Zygote 8 (2000) 245-256
38. Toyoda Y., and Chang M.C. Capacitation of epididymal spermatozoa with high K/Na ratio and cyclic AMP for the fertilization of rat eggs in vitro. J Reprod Fertil 36 (1974) 125-134
39. Rosado A., Hicks J.J., Reyes A., and Blanco I. Capacitation in vitro of rabbit spermatozoa with cyclic adenosine monophosphate and human follicular fluid. Fertil Steril 25 (1974) 821-824
40. Fraser L.R. Dibutyryl cyclic AMP decreases capacitation time in vitro in mouse spermatozoa. J Reprod Fertil 62 (1981) 63-72
41. Thundathil J., de Lamirande E., and Gagnon C. Different signal transduction pathways are involved during human sperm capacitation induced by biological and pharmacological agents. Mol Hum Reprod 8 (2002) 811-816
42. Gadella B.M., and Harrison R.A.P. The capacitating agent bicarbonate induces protein kinase A-dependent changes in phospholipid transbilayer behavior in the sperm plasma membrane. Development 127 (2000) 2407-2420
43. Furuya S., Endo Y., Oba M., Nozawa S., and Suzuki S. Effects of modulators of protein kinases and phosphatases on mouse sperm capacitation. J Assist Reprod Genet 9 (1992) 391-399
44. Boatman D.E., and Bavister B.D. Stimulation of rhesus monkey sperm capacitation by cyclic nucleotide mediators. J Reprod Fertil 71 (1984) 357-366
45. Harrison R.A.P., and Miller N.G.A. cAMP-dependent protein kinase control of plasma membrane lipid architecture in boar sperm. Mol Reprod Dev 55 (2000) 220-228
46. 2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol Reprod Dev 45 (1996) 378-391
47. Flesch F.M., Colenbrander B., van Golde L.M.G., and Gadella B.M. Capacitation induces tyrosine phosphorylation of proteins in the boar sperm plasma membrane. Biochem Biophys Res Commun 262 (1999) 787-792
48. Harrison RA.P. Rapid PKA-catalysed phosphorylation of boar sperm proteins induced by the capacitating agent bicarbonate. Mol Reprod Dev 67 (2004) 337-352
49. Sun J., Zhao J., Schwartz M.A., Wang J.Y., Wiedmer T., and Sims P.J. cAbl tyrosine kinase binds and phosphorylates phospholipid scramblase I. J Biol Chem 276 (2001) 28984-28990
50. Parks J.E., and Graham J.K. Effects of cryopreservation procedures on sperm membranes. Theriogenology 38 (1992) 209-222
51. Wiebe J.P., Kowalik A., Gallardi R.L., Egeler O., and Clubb B.H. Glycerol disrupts tight junction-associated actin microfilaments, occludin, and microtubules in Sertoli cells. J Androl 21 (2000) 625-635
52. Slaninova I., Sestak S., Svoboda A., and Farkas V. Cell wall and cytoskeleton reorganization as the response to hyperosmotic shock in Saccharomyces cerevisiae. Arch Microbiol 173 (2000) 245-252
53. de Lamirande E., and Gagnon C. The extracellular signal-regulated kinase (ERK) pathway is involved in human sperm function and modulated by the superoxide anion. Mol Hum Reprod 8 (2002) 124-135
54. Houle F., Rousseau S., Morrice N., Luc M., Mongrain S., Turner C.E., et al. Extracellular signal-regulated kinase mediates phosphorylation of tropomyosin-1 to promote cytoskeleton remodeling in response to oxidative stress: impact on membrane blebbing. Mol Biol Cell 14 (2003) 1418-1432
55. Huot J., Houle F., Marceau F., and Landry J. Oxidative stress-induced actin reorganization mediated by the p38 mitogen-activated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ Res 80 (1997) 383-392
56. 14) via activation of p38 mitogen-activated protein kinase and c-Src kinase. Evidence for caveolae, the actin cytoskeleton, and focal adhesions as mechanical sensors of osmotic stress. J Biol Chem 276 (2001) 8094-8103
57. Bode J.G., Gatsios P., Ludwig S., Rapp U.R., Häussinger D., Heinrich P.C., et al. The mitogen-activated protein (MAP) kinase p38 and its upstream activator MAP kinase kinase 6 are involved in the activation of signal transducer and activator of transcription by hyperosmolarity. J Biol Chem 274 (1999) 30222-30227
58. Anderson N.G., Maller J.L., Tonks N.K., and Sturgill T.W. Requirement for integration of signals from two distinct phosphorylation pathways for activation of MAP kinase. Nature 343 (1990) 651-653
59. Payne D.M., Rossomando A.J., Martino P., Erickson A.K., Her J.H., Shabanowitz J., et al. Identification of the regulatory phosphorylation sites in pp42/mitogen-activated protein kinase (MAP kinase). EMBO J 10 (1991) 885-892
60. Schindler C., Shuai K., Prezioso V.R., and Darnell Jr. J.E. Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257 (1992) 809-813
61. Shuai K., Schindler C., Prezioso V.R., and Darnell Jr. J.E. Activation of transcription by IFN-gamma: tyrosine phosphorylation of a 91-kD DNA binding protein. Science 258 (1992) 1808-1812
62. Shuai K., Ziemiecki A., Wilks A.F., Harpur A.G., Sadowski H.B., Gilman M.Z., et al. Polypeptide signaling to the nucleus through tyrosine phosphorylation of Jak and Stat proteins. Nature 366 (1993) 580-583
63. Tomes C.N., Rogerro C.M., De Blas G., Saling P.M., and Mayorga L.S. Requirement of protein tyrosine kinase and phosphatase activities for human sperm exocytosis. Dev Biol 265 (2004) 399-415
64. 2+] signalling in human spermatozoa. Mol Hum Reprod 8 (2002) 326-332
65. Rathi R., Colenbrander B., Stout T.A.E., Bevers M.M., and Gadella B.M. Progesterone induces acrosome reaction in stallion spermatozoa via a protein tyrosine kinase dependent pathway. Mol Reprod Dev 64 (2003) 120-128