Fertilisation in the horse and paracrine signalling in the oviduct

Reproduction, Fertility and Development

Volumn 23, Issue 8, 2011, Pages 941-951

  Goudet, Ghyl̀ne ^a,b,c,d  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE TOURS   (France)

^d IFCE   (France)

Author keywords

equine; gamete; oocyte; spermatozoa

Indexed keywords

FERTILIZATION; GAMETE; HORSE; NONHUMAN; OOCYTE MATURATION; OVIDUCT; PARACRINE SIGNALING; REVIEW; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY;

ANIMALS; EPITHELIAL CELLS; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; HORSES; MALE; MODELS, ANIMAL; OOCYTES; OVIDUCTS; PARACRINE COMMUNICATION; PREGNANCY; SPERM-OVUM INTERACTIONS; SPERMATOZOA;

EQUIDAE; MAMMALIA;

EID: 80054108653     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD10285     Document Type: Review

References (113)

1. Aguilar, J. J., Losinno, L., Koncurat, M., and Miragaya, M. H. (2002). Nuclear, cytoplasmic and mitochondrial patterns of ovulated oocytes in young and aged mares. Theriogenology 58(2-4), 689-692 (Pubitemid 34875870)
2. Alm, H., and Torner, H. (1994). In vitro maturation of horse oocytes. Theriogenology 42(2), 345-349 doi:101016/0093-691X(94)90279-8
3. Alm, H., Torner, H., Blottner, S., Nurnberg, G., and Kanitz, W. (2001). Effect of sperm cryopreservation and treatment with calcium ionophore or heparin on in vitro fertilization of horse oocytes. Theriogenology 56(5), 817-829 doi:101016/S0093-691X(01)00610-0
4. Anderson, R. A., Feathergill, K. A., Drisdel, R. C., Rawlins, R. G., Mack, S. R., and Zaneveld, L. J. (1994). Atrial natriuretic peptide (ANP) as a stimulus of the human acrosome reaction and a component of ovarian follicular fluid: correlation of follicular ANP content with in vitro fertilization outcome. J. Androl. 15(1), 61-70 (Pubitemid 24061787)
5. Aviles, M., Gutierrez-Adan, A., and Coy, P. (2010). Oviductal secretions: will they be key factors for the future ARTs? Mol. Hum. Reprod. 16(12), 896-906 doi:101093/MOLEHR/GAQ056
6. Bader, H. (1982). An investigation of sperm migration into the oviducts of the mare. J. Reprod. Fertil. Suppl. 32, 59-64
7. Ball, B. A. (1996). Scanning electron microscopy of the equine oviduct and observations on ciliary currents in vitro at day 2 after ovulation. Theriogenology 46(7), 1305-1311 doi:101016/S0093-691X(96)00302-0 (Pubitemid 28163438)
8. Ball, B. A., Dobrinski, I., Fagnan, M. S., and Thomas, P. G. (1997). Distribution of glycoconjugates in the uterine tube (oviduct) of horses. Am. J. Vet. Res. 58(8), 816-822 (Pubitemid 127470791)
9. Battut, I., Palmer, E., and Driancourt, M. A. (1995). Proteins synthesized and released by equine oviducts: characterization, variations, and interactions with spermatozoa. Biology ofReproduction Monograph Series 1, 131-140
10. Bauersachs S.,Blum H.,Mallok S.,Wenigerkind H.,Rief S.,Prelle K.,Wolf E., 2003, Regulation of ipsilateral and contralateral bovine oviduct epithelial cell function in the postovulation period: A transcriptomics approach, Biol. Reprod., 68, 4, 1170-1177 doi:101095/BIOL REPROD.102010660 (Pubitemid 36359104)
11. Bauersachs, S., Rehfeld, S., Ulbrich, S. E., Mallok, S., Prelle, K., Wenigerkind, H., Einspanier, R., Blum, H., and Wolf, E. (2004). Monitoring gene expression changes in bovine o iduct epithelial cells during the oestrous cycle. J. Mol. Endocrinol. 32(2), 449-466 doi:101677/JME.00320449
12. Betteridge, K. J., and Mitchell, D. (1974). Direct evidence of retention of unfertilized ova in the oviduct of the mare. J. Reprod. Fertil. 39(1), 145-148 doi:101530/JRF.00390145
13. Betteridge, K. J., and Mitchell, D. (1975). A surgical technique applied to the study of tubal eggs in the mare. J. Reprod. Fertil. Suppl. 23, 519-524
14. Bézard, J., Magistrini, M., Duchamp, G., and Palmer, E. (1989). Chronology of equine fertilisation and embryonic development in vivo and in vitro. Equine Vet. J. Suppl. 8, 105-110
15. Bézard, J., Mekarska, A., Goudet, G., Duchamp, G., and Palmer, E. (1997). Timing of in vivo maturation of equine preovulatory oocytes and competence for in vitro maturation of immature oocytes collected simultaneously. Equine Vet. J. Suppl. 25, 33-37
16. Brinsko, S. P., Ignotz, G. G., Ball, B. A., Thomas, P. G., Currie, W. B., and Ellington, J. E. (1996). Characterization of polypeptides synthesized and secreted by oviductal epithelial cell explants obtained from young, fertile and aged, subfertile mares. Am. J. Vet. Res. 57(9), 1346-1353 (Pubitemid 126449740)
17. Brüssow, K.-P., Ratky, J., and Rodriguez-Martinez, H. (2008). Fertilization and early embryonic development in the porcine fallopian tube. Reprod.Domest. Anim. 43(suppl. 2), 245-251 doi:101111/J.1439-05312008 01169X
18. Carnevale, E. M. (2004). Oocyte transfer and gamete intrafallopian transfer in the mare. Anim. Reprod. Sci. 82]83, 617-624 doi:101016/J.ANIR EPROSCI.200404002 (Pubitemid 39027089)
19. Carnevale, E. M., Maclellan, L. J., Coutinho da Silva, M. A., Scott, T. J., and Squires, E. L. (2000). Comparison of culture and insemination techniques for equine oocyte transfer. Theriogenology 54(6), 981-987 doi:101016/S0093- 691X(00)00406-4
20. Chapman, J. A., Chuah, M. I., and Breed, W. G. (2010). Glycoconjugates within the oviduct and their functional significance with special reference to marsupials. Histol. Histopathol. 25(1), 121-132
21. Chiu, P. C.,Wong, B. S., Lee, C. L., Lam, K. K., Chung,M. K., Lee, K. F., Koistinen, R., Koistinen, H., Gupta, S. K., Seppala, M., and Yeung, W. S. (2010). Zona pellucida-induced acrosome reaction in human spermatozoa is potentiated by glycodelin-A via down-regulation of extracellular signalregulated kinases and up-regulation of zona pellucida-induced calcium influx. Hum. Reprod. 25(11), 2721-2733 doi:101093/HUMREP/DEQ243
22. Coy, P., and Aviles, M. (2010). What controls polyspermy in mammals, the oviduct or the oocyte? Biol. Rev. Camb. Philos. Soc. 85(3), 593-605
23. Coy, P., Canovas, S., Mondejar, I., Saavedra, M. D., Romar, R., Grullon, L., Matas, C., and Aviles, M. (2008). Oviduct-specific glycoprotein and heparin modulate sperm-zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc. Natl. Acad. Sci. USA 105(41), 15 809-15 814 doi:101073/PNAS.0804422105
24. David, J. S. (1975). A survey of eggs in the oviducts of mares. J. Reprod. Fertil. Suppl. 23, 513-517
25. Davies Morel, M. C., and Newcombe, J. R. (2008). The efficacy of different hCG dose rates and the effect of hCG treatment on ovarian activity: ovulation, multiple ovulation, pregnancy, multiple pregnancy, synchrony of multiple ovulation; in the mare. Anim. Reprod. Sci. 109(1-4), 189-199 doi:101016/J.ANIREPROSCI.200710005
26. Day, F. T. (1942). Survival of spermatozoa in the genital tract of the mare. J. Agric. Sci. 32, 108-111 doi:101017/S0021859600047572
27. Deleuze, S., Dubois, C. S., Caillaud, M., Bruneau, B., Goudet, G., and Duchamp, G. (2010). Influence of cysteamine on in vitro maturation, in vitro and in vivo fertilization of equine oocytes. Reprod. Domest. Anim. 45(1), 1-7 doi:101111/J.1439-0531200801122X
28. Dell'Aquila, M. E., Fusco, S., Lacalandra, G. M., and Maritato, F. (1996). In vitro maturation and fertilization of equine oocytes recovered during the breeding season. Theriogenology 45(3), 547-560 doi:101016/0093-691X(95) 00402-T (Pubitemid 126649690)
29. Dell'Aquila, M. E., Albrizio, M., Guaricci, A. C., De Santis, T., Maritato, F., Tremoleda, J. L., Colenbrander, B., Guerra, L., Casavola, V., and Minoia, P. (2008). Expression and localization of the mu-opioid receptor (MOR) in the equine cumulus-oocyte complex and its involvement in the seasonal regulation of oocyte meiotic competence. Mol. Reprod. Dev. 75(8), 1229-1246 doi:101002/MRD.20869 (Pubitemid 351898586)
30. Desantis, S., Acone, F., Corriero, A., Deflorio, M., Zubani, D., Ventriglia, G., Palmieri, G., and De Metrio, G. (2004). Distribution of sialoglycoconjugates in the oviductal isthmus of the horse during anoestrus, oestrus and pregnancy: a lectin histochemistry study. Eur. J. Histochem. 48(4), 403-412
31. Desantis, S., Ventriglia, G., Zizza, S., Guaricci, A. C., Losurdo, M., Zarrilli, A., and Albrizio, M. (2010). Changes in the expression of the mu-opioid receptor in the mare oviduct during oestrus and anoestrus. nim. Reprod. Sci. 119(1-2), 40-49 doi:101016/J.ANIREPROSCI.200912004
32. Dobrinski, I., Thomas, P. G., and Ball, B. A. (1995). Cryopreservation reduces the ability of equine spermatozoa to attach to oviductal epithelial cells and zonae pellucidae in vitro. J. Androl. 16(6), 536-542 (Pubitemid 26017824)
33. Dobrinski, I., Ignotz, G. G., Thomas, P. G., and Ball, B. A. (1996a). Role of carbohydrates in the attachment of equine spermatozoa to uterine tubal (oviductal) epithelial cells in vitro. Am. J. Vet. Res. 57(11), 1635-1639 (Pubitemid 126449469)
34. Dobrinski, I., Suarez, S. S., and Ball, B. A. (1996b). Intracellular calcium concentration in equine spermatozoa attached to oviductal epithelial cells in vitro. Biol. Reprod. 54(4), 783-788 doi:101095/BIOLRE PROD544783 (Pubitemid 26086833)
35. Dobrinski, I., Ignotz, G. G., Fagnan, M. S., Yudin, S. I., and Ball, B. A. (1997a). Isolation and characterization of a protein with homology to angiotensin converting enzyme fromthe periacrosomal plasmamembrane of equine spermatozoa. Mol. Reprod. Dev. 48(2), 251-260 doi:101002/(SICI)1098-2795(199710) 48:2,251::AID-MRD1330CO;2-0
36. Dobrinski, I., Smith, T. T., Suarez, S. S., and Ball, B. A. (1997b). Membrane contact with oviductal epithelium modulates the intracellular calcium concentration of equine spermatozoa in vitro. Biol. Reprod. 56(4), 861-869 doi:101095/BIOLREPROD564861
37. Ekhlasi-Hundrieser, M., Schäfer, B., Kirchhoff, C., Hess, O., Bellair, S., Müller, P., and Töpfer-Petersen, E. (2005). Structural and molecular characterization of equine sperm-binding fibronectin-II module proteins. Mol. Reprod. Dev. 70(1), 45-57 doi:101002/MRD.20187
38. Ellington, J. E., Ball, B. A., Blue, B. J., and Wilker, C. E. (1993a). Capacitation-like membrane changes and prolonged viability in vitro of equine spermatozoa cultured with uterine tube epithelial cells. Am. J. Vet. Res. 54(9), 1505-1510
39. Ellington, J. E., Ball, B. A., and Yang, X. (1993b). Binding of stallion spermatozoa to the equine zona pellucida after coculture with oviductal epithelial cells. J. Reprod. Fertil. 98(1), 203-208 doi:101530/JRF.0 0980203 (Pubitemid 23204765)
40. Ellington, J. E., Ignotz, G. G., Miller, P. G., Currie, W. B., and Meyers- Wallen, V. N. (1993c). Oviduct epithelial cell co-culture modifies stallion and bull sperm cell surface proteins. Biol. Reprod. Suppl. 1 (48), 107
41. Ellington, J. E., Ignotz, G. G., Varner, D. D., Marcucio, R. S., Mathison, P., and Ball, B. A. (1993d). In vitro interaction between oviduct epithelial and equine sperm. Arch. Androl. 31(2), 79-86 doi:103109/ 01485019308988384 (Pubitemid 23282985)
42. Ellington, J. E., Varner, D. D., Burghardt, R. C., Meyers-Wallen, V. N., Barhoumi, R., Brinsko, S. P., and Ball, B. A. (1993e). Cell-to-cell communication of equine uterine tube (oviduct) cells as determined by anchored cell analysis in culture. Anim. Reprod. Sci. 30(4), 313-324 doi:101016/0378- 4320(93)90081-2
43. Ellington, J. E., Samper, J., Jones, A., Oliver, S. A., Burnett, K., and Wright, R. W. (1999a). Effects of bovine serum albumin on function of cryopreserved stallion spermatozoa during medium culture and uterine tube epithelial cell coculture. Am. J. Vet. Res. 60(3), 363-367
44. Ellington, J. E., Samper, J. C., Jones, A. E., Oliver, S. A., Burnett, K. M., and Wright, R. W. (1999b). In vitro interactions of cryopreserved stallion spermatozoa and oviduct (uterine tube) epithelial cells or their secretory products. Anim. Reprod. Sci. 56(1), 51-65 doi:101016/S0378-4320(99) 00030-5
45. Enders, A. C., Liu, I. K., Bowers, J., Lantz, K. C., Schlafke, S., and Suarez, S. (1987). The ovulated ovum of the horse: cytology of nonfertilized ova to pronuclear stage ova. Biol. Reprod. 37(2), 453-466 doi:101095/BIOL REPROD372453
46. Fazeli, A., Affara, N. A., Hubank, M., and Holt, W. V. (2004). Sperminduced modification of the oviductal gene expression profile after natural insemination in mice. Biol. Reprod. 71(1), 60-65 doi:101095/ BIOLREPROD.103026815 (Pubitemid 38915309)
47. Galli, C., Colleoni, S., Duchi, R., Lagutina, I., and Lazzari, G. (2007). Developmental competence of equine oocytes and embryos obtained by in vitro procedures ranging from in vitro maturation and ICSI to embryo culture, cryopreservation and somatic cell nuclear transfer. Anim. Reprod. Sci. 98(1-2), 39-55 doi:101016/J.ANIREPROSCI.200610011
48. Georgiou, A. S., Sostaric, E., Wong, C. H., Snijders, A. P., Wright, P. C., Moore, H. D., and Fazeli, A. (2005). Gametes alter the oviductal secretory proteome. Mol. Cell. Proteomics 4(11), 1785-1796 doi:101074/MCP.M500119-MCP200
49. Georgiou, A. S., Snijders, A. P., Sostaric, E., Aflatoonian, R., Vazquez, J. L., Vazquez, J. M., Roca, J., Martinez, E. A., Wright, P. C., and Fazeli A. (2007). Modulation of the oviductal environment by gametes. J. Proteome Res. 6(12), 4656-4666 doi:101021/PR070349M
50. Gonçalves, R. F., Chapman, D. A., Bertolla, R. P., Eder, I., and Killian, G. J. (2008a). Pre-treatment of cattle semen or oocytes with purified milk osteopontin affects in vitro fertilization and embryo development. Anim. Reprod. Sci. 108(3-4), 375-383 doi:101016/J.ANIREPROSCI.2007 09006
51. Gonçalves, R. F., Staros, A. L., and Killian, G. J. (2008b). Oviductal fluid proteins associated with the bovine zona pellucida and the effect on in vitro sperm-egg binding, fertilization and embryo development. Reprod. Domest. Anim. 43(6), 720-729 doi:101111/J.1439-0531200700978X
52. Goudet, G., Bézard, J., Duchamp, G., Gérard, N., and Palmer, E. (1997). Equine oocyte competence for nuclear and cytoplasmic in vitro maturation: effect of follicle size and hormonal environment. Biol. Reprod. 57(2), 232-245 doi:101095/BIOLREPROD572232 (Pubitemid 27343681)
53. Goudet, G., Belin, F., Bézard, J., and Gérard, N. (1998a). Maturationpromoting factor (MPF) and mitogen activated protein kinase (MAPK) expression in relation to oocyte competence for in-vitro maturation in the mare. Mol. Hum. Reprod. 4(6), 563-570 doi:101093/MOLEHR/ 46563 (Pubitemid 28282835)
54. Goudet, G., Bézard, J., Belin, F., Duchamp, G., Palmer, E., and Gérard, N. (1998b). Oocyte competence for in vitro maturation is associated with histone H1 kinase activity and is influenced by estrous cycle stage in the mare. Biol. Reprod. 59(2), 456-462 doi:101095/BIOLREPROD59 2456 (Pubitemid 28354891)
55. Grøndahl, C., Grøndahl Nielsen, C., Eriksen, T., Greve, T., and Hyttel P. (1993). In-vivo fertilisation and initial embryogenesis in the mare. Equine Vet. J. Suppl. 15, 79-83
56. Grøndahl, C., Hyttel, P., Grøndahl, M. L., Eriksen, T., Gotfredsen, P., and Greve, T. (1995). Structural and endocrine aspects of equine oocyte maturation in vivo. Mol. Reprod. Dev. 42(1), 94-105 doi:101002/ MRD.1080420113
57. Hao, Y., Mathialagan, N., Walters, E., Mao, J., Lai, L., Becker, D., Li W., Critser, J., and Prather, R. S. (2006). Osteopontin reduces polyspermy during in vitro fertilization of porcine oocytes. Biol. Reprod. 75(5), 726-733 doi:101095/BIOLREPROD.106052589 (Pubitemid 44720392)
58. Hawley, L.R., Enders, A.C., and Hinrichs, K. (1995). Comparison of equine and bovine oocyte-cumulus morphology within the ovarian follicle. Biology of Reproduction Monograph Series 1, 243-252
59. Hinrichs, K. (2010). The equine oocyte: factors affecting meiotic and developmental competence. Mol. Reprod. Dev. 77(8), 651-661 doi:101002/MRD.21186
60. Hinrichs, K., Love, C. C., Brinsko, S. P., Choi, Y. H., and Varner, D. D. (2002). In vitro fertilization of in vitro-matured equine oocytes: effect of maturation medium, duration of maturation, and sperm calcium ionophore treatment, and comparison with rates of fertilization in vivo after oviductal transfer. Biol. Reprod. 67(1), 256-262 doi:101095/BIOLRE PROD671256 (Pubitemid 34680661)
61. Hunter, R. H. (2008). Sperm release from oviduct epithelial binding is controlled hormonally by peri-ovulatory graafian follicles. Mol. Reprod. Dev. 75(1), 167-174 doi:101002/MRD.20776 (Pubitemid 350224002)
62. Jennings, M. W., Boime, I., Daphna-Iken, D., Jablonka-Shariff, A., Conley, A. J., Colgin, M., Bidstrup, L. A., Meyers-Brown, G. A., Famula, T. R., and Roser, J. F. (2009). The efficacy of recombinant equine follicle stimulating hormone (reFSH) to promote follicular growth in mares using a follicular suppression model. Anim. Reprod. Sci. 116(3-4), 291-307 doi:101016/J. ANIREPROSCI.200901013
63. Katila, T. (2001). Sperm-uterine interactions: a review. Anim. Reprod. Sci. 68(3-4), 267-272 doi:101016/S0378-4320(01)00162-2 (Pubitemid 34029596)
64. Kim, S. H., Cho, K. W., Oh, S. H., Hwang, Y. H., Lim, S. H., Ryu, H., Seul, K. H., Jeong, G. B., and Yoon, S. (1993). Immunoreactive atrial natriuretic peptides in the oocyte. Comp. Biochem. Physiol. Comp. Physiol. 104(2), 219-223 (Pubitemid 23045615)
65. King, W. A., Bézard, J., Bousquet, D., Palmer, E., and Betteridge, K. J. (1987). The meiotic stage of preovulatory oocytes in mares. Genome 29(4), 679-682 doi:101139/G87-114
66. Laurincik, J., Hyttel, P., Rath, D., and Pivko, J. (1994). Ovulation, fertilization and pronucleus development in superovulated gilts. Theriogenology 41(2), 447-452 doi:101016/0093-691X(94)90080-3
67. Lazzari, G., Colleoni, S., Lagutina, I., Crotti, G., Turini, P., Tessaro, I., Brunetti, D., Duchi, R., and Galli, C. (2010). Short-term and long-term effects of embryo culture in the surrogate sheep oviduct versus in vitro culture for different domestic species. Theriogenology 73(6), 748-757 doi:101016/J.THERIOGENOLOGY.200908001
68. Lefebvre, R., and Samper, J. C. (1993). Interaction between stallion spermatozoa and oviductal epithelial cells in vitro. Equine Vet. J. Suppl. 15, 39-41
69. Lefebvre, R., DeMott, R.P., Suarez, S.S., and Samper, J.C. (1995). Specific inhibition of equine sperm binding to oviductal epithelium. Biology of Reproduction Monograph Series 1, 689-696
70. + flux of equine spermatozoa. J. Reprod. Fertil. Suppl. 23, 431-445
71. Li, X., Morris, L. H., and Allen, W. R. (2001). Influence of co-culture during maturation on the developmental potential of equine oocytes fertilized by intracytoplasmic sperm injection (ICSI). Reproduction 121(6), 925-932 doi:101530/REP.01210925 (Pubitemid 32547321)
72. Liu, Y. X. (2007). Involvement of plasminogen activator and plasminogen activator inhibitor type 1 in spermatogenesis, sperm capacitation, and fertilization. Semin. Thromb. Hemost. 33(1), 29-40 doi:101055/S- 2006-958459
73. Lloyd, R. E., Elliott, R. M., Fazeli, A., Watson, P. F., and Holt, W. V. (2009). Effects of oviductal proteins, including heat shock 70 kDa protein 8, on survival of ram spermatozoa over 48 h in vitro. Reprod. Fertil. Dev. 21(3), 408-418 doi:101071/RD08204
74. Logan, N. L., McCue, P. M., Alonso, M. A., and Squires, E. L. (2007). Evaluation of three equine FSH superovulation protocols in mares. Anim. Reprod. Sci. 102(1-2), 48-55 doi:101016/J.ANIREPROSCI. 200609027 (Pubitemid 47332937)
75. Mann, T., Polge, C., and Rowson, L. E. (1956). Participation of seminal plasma during the passage of spermatozoa in the female reproductive tract of the pig and horse. J. End crinol. 13(2), 133-140 doi:101677/ JOE.00130133
76. Marín-Briggiler, C. I., González-Echeverría, M. F., Munuce, M. J., Ghersevich, S., Caille, A. M., Hellman, U., Corrigall, V. M., and Vazquez-Levin, M. H. (2010). Glucose-regulated protein 78 (Grp78/BiP) is secreted by human oviduct epithelial cells and the recombinant protein modulates sperm-zona pellucida binding. Fertil. Steril. 93(5), 1574-1584 doi:101016/J.FERTNSTERT.200812132
77. Martus, N. S., Verhage, H. G., Mavrogianis, P. A., and Thibodeaux J. K. (1998). Enhancement of bovine oocyte fertilization in vitro with a bovine oviductal specific glycoprotein. J. Reprod. Fertil. 113(2), 323-329 doi:101530/JRF.01130323
78. McCauley, T. C., Buhi, W. C., Wu, G. M., Mao, J., Caamano, J. N., Didion, B. A., and Day, B. N. (2003). Oviduct-specific glycoprotein modulates sperm-zona binding and improves efficiency of porcine fertilization in vitro. Biol. Reprod. 69(3), 828-834 doi:101095/BIOLREPROD.103 016444 (Pubitemid 37064610)
79. McDowell, K. J., Adams, M. H., and Williams, N. M. (1993). Characterization of equine oviductal proteins synthesized and released at estrus and atday 4 after ovulation in bred and nonbred mares. J. Exp. Zool. 267(2), 217-224 doi:101002/JEZ.1402670215
80. McKinnon, A. O.,Carnevale E. M., Squires E. L., Voss, J. L., Seidel G. E. Jr(1988). Heterogenous and xenogenous fertilization of in vivo matured equine oocytes. J. Equine Vet. Sci. 8 143-147 doi:101016/ S0737-0806(88)80037-6
81. McPartlin, L. A., Suarez, S. S., Czaya, C. A., Hinrichs, K., and Bedford- Guaus, S. J. (2009). Hyperactivation of stallion sperm is required for successful in vitro fertilization of equine oocytes. Biol. Reprod. 81(1), 199-206 doi:101095/BIOLREPROD.108074880
82. Monaco, E., Gasparrini, B., Boccia, L., De Rosa, A., Attanasio, L., Zicarelli, L., and Killian, G. (2009). Effect of osteopontin (OPN) on in vitro embryo development in cattle. Theriogenology 71(3), 450-457 doi:101016/J. THERIOGENOLOGY.200808012 (Pubitemid 50290332)
83. Mugnier, S., Kervella, M., Douet, C., Canepa, S., Pascal, G., Deleuze S., Duchamp, G., Monget, P., and Goudet, G. (2009). The secretions of oviduct epithelial cells increase the equine in vitro fertilization rate: are osteopontin, atrial natriuretic peptide A and oviductin involved? Reprod. Biol. Endocrinol. 7, 129 doi:101186/1477-7827-7-129
84. Onuma, H., and Ohnami, Y. (1975). Retention of tubal eggs in mares. J. Reprod. Fertil. Suppl. 23, 507-511
85. Palmer, E., Bezard, J., Magistrini, M., and Duchamp, G. (1991). In vitro fertilization in the horse. A retrospective study. J. Reprod. Fertil. Suppl. 44, 375-384
86. Parker, W. G., Sullivan, J. J., and First, N. L. (1975). Sperm transport and distribution in the mare. J. Reprod. Fertil. Suppl. 23, 63-66
87. Raz, T., Gray, A., Hunter, B., and Card, C. (2009). Early effects of equine FSH (eFSH) treatment on hormonal and reproductive parameters in mares intended to carry their own pregnancy. Anim. Reprod. Sci. 115(1-4), 76-87 doi:101016/J.ANIREPROSCI.200811001
88. Russinova, A., Mourdjeva, M., Kyurkchiev, S., and Kehayov, I. (2001). Immunohistochemical detection of atrial natriuretic factor (ANF) in different ovarian cell types. Endocr. Regul. 35(2), 81-89 (Pubitemid 33712498)
89. Sabeur, K., and Ball, B. A. (2007). Characterization of galactose-binding proteins in equine testis and spermatozoa. Anim. Reprod. Sci. 101(1-2), 74-84 doi:101016/J.ANIREPROSCI.200608028 (Pubitemid 46962247)
90. Scott, T. J., Carnevale, E. M., Maclellan, L. J., Scoggin, C. F., and Squires, E. L. (2001). Embryo development rates after transfer of oocytesmatured in vivo, in vitro, or within oviducts of mares. Theriogenology 55(3), 705-715 doi:101016/S0093-691X(01)00438-1 (Pubitemid 32180210)
91. Seytanoglu, A., Georgiou, A. S., Sostaric, E., Watson, P. F., Holt, W. V., and Fazeli, A. (2008). Oviductal cell proteome alterations during the reproductive cycle in pigs. J. Proteome Res. 7(7), 2825-2833 doi:101021/PR8000095
92. Shaw, J. L., Smith, C. R., and Diamandis, E. P. (2007). Proteomic analysis of human cervico-vaginal fluid. J. Proteome Res. 6(7), 2859-2865 doi:101021/PR0701658 (Pubitemid 47122380)
93. Siddiqui, M. A., Gastal, E. L., Ju, J. C., Gastal, M. O., Beg, M. A., and Ginther, O. J. (2009). Nuclear configuration, spindle morphology and cytoskeletal organization of in vivo maturing horse oocytes. Reprod. Domest. Anim. 44(3), 435-440 doi:101111/J.1439-0531 200801105X
94. Song, X. X., Xu, Z., Piao, Y. J., Park, C. K., and Niwa, K. (2008). Effect of chondroitin sulfate C on sperm capacitation and fertilization parameters in vitro in pigs. Anim. Reprod. Sci. 108(1-2), 144-156 doi:101016/ J.ANIREPROSCI.200707010
95. Sostaric, E., Georgiou, A. S., Wong, C. H., Watson, P. F., Holt, W. V., and Fazeli, A. (2006). Global profiling of surface plasma membrane proteome of oviductal epithelial cells. J. Proteome Res. 5(11), 029-3037 doi:101021/PR060366W
96. Stalheim, O. H., Gallagher, J. E., and Deyoe, B. L. (1975). Scanning electron microscopy of the bovine, equine, porcine, and caprine uterine tube (oviduct). Am. J. Vet. Res. 36(08), 1069-1075
97. Suarez, S. S. (2008). Regulation of sperm storage and movement in the mammalian oviduct. Int. J. Dev. Biol. 52(5-6), 455-462 doi:101387/ IJDB.072527SS
98. Talevi, R., and Gualtieri, R. (2010). Molecules involved in sperm-oviduct adhesion and release. Theriogenology 73(6), 796-801 doi:101016/ J.THERIOGENOLOGY.200907005
99. Thomas, P. G., and Ball, B. A. (1996). Cytofluorescent assay to quantify adhesion of equine spermatozoa to oviduct epithelial cells in vitro. Mol. Reprod. Dev. 43(1), 55-61 doi:101002/(SICI)1098-2795(199601) 43:1,55::AID-MRD730CO;2-T (Pubitemid 26021947)
100. Thomas, P. G., Ball, B. A., and Brinsko, S. P. (1994a). Interaction of equine spermatozoa with oviduct epithelial cell explants is affected by estrous cycle and anatomic origin of explant. Biol. Reprod. 51(2), 222-228 doi:101095/BIOLREPROD512222 (Pubitemid 24220929)
101. Thomas, P. G., Ball, B. A., Miller, P. G., Brinsko, S. P., and Southwood L. (1994b). A subpopulation of morphologically normal, motile spermatozoa attach to equine oviductal epithelial cell monolayers. Biol. Reprod. 51(2), 303-309 doi:101095/BIOLREPROD512303 (Pubitemid 24220940)
102. Thomas, P. G., Ball, B. A., and Brinsko, S. P. (1995a). Changes associated with induced capacitation influence the interaction between equine spermatozoa and oviduct epithelial cell monolayers. Biology of Reproduction Monograph Series 1, 697-705
103. Thomas, P. G., Ignotz, G. G., Ball, B. A., Brinsko, S. P., and Currie, W. B. (1995b). Effect of coculture with stallion spermatozoa on de novo protein synthesis and secretion by equine oviduct epithelial cells. Am. J. Vet. Res. 56(12), 1657-1662
104. Thomas, P. G., Ball, B. A., Ignotz, G. G., Dobrinski, I., Parks, J. E., and Currie, W. B. (1997). Antibody directed against plasma membrane components of equine spermatozoa inhibits adhesion of spermatozoa to oviduct epithelial cells in vitro. Biol. Reprod. 56(3), 720-730 doi:101095/BIOLREPROD563720 (Pubitemid 27084109)
105. Töpfer-Petersen, E., Ekhlasi-Hundrieser, M., Kirchhoff, C., Leeb, T., and Sieme, H. (2005). The role of stallion seminal proteins in fertilisation.Anim. Reprod. Sci. 89(1-4), 159-170 doi:101016/J.ANIREPROSCI. 200506018 (Pubitemid 41330953)
106. Töpfer-Petersen, E., Ekhlasi-Hundrieser, M., and Tsolova, M. (2008). Glycobiology of fertilization in the pig. Int. J. Dev. Biol. 52(5-6), 717-736 doi:101387/IJDB.072536ET
107. Troedsson, M. H., Liu, I. K., and Crabo, B. G. (1998). Sperm transport and survival in the mare: a review. Theriogenology 50(5), 807-818
108. Way, A. L., and Killian, G. J. (2006). Sperm binding, in vitro fertilization, and in vitro embryonic development of bovine oocytes fertilized with spermatozoa incubated with norepinephrine. Anim. Reprod. Sci. 96(1-2), 1-9 doi:101016/J.ANIREPROSCI.200510006 (Pubitemid 44353973)
109. Willis, P., Sekhar, K. N., Brooks, P., and Fayrer-Hosken, R. A. (1994). Electrophoretic characterization of equine oviductal fluid. J. Exp. Zool. 268(6), 477-485 doi:101002/JEZ.1402680608 (Pubitemid 2065266)
110. Yeung, W. S., Lee, K. F., Koistinen, R., Koistinen, H., Seppala, M., and Chiu, P. C. (2009). Effects of glycodelins on functional competence of spermatozoa. J. Reprod. Immunol. 83(1-2), 26-30 doi:101016/J.JRI. 200904012
111. Zamir, N., Barkan, D., Keynan, N., Naor, Z., and Breitbart, H. (1995). Atrial natriuretic peptide induces acrosomal exocytosis in bovine spermatozoa. Am. J. Physiol. 269(2 Pt 1), E216-E221
112. Zervos, I. A., Lavrentiadou, S. N., Tsantarliotou, M. P., Georgiadis, M. P., Kokolis, N. A., and Taitzoglou, I. A. (2010). Seasonal variation of plasminogen activator activity in spermatozoa and seminal plasma of boar, buck, bull and stallion. Reprod. Domest. Anim. 45(6), e440-e446 doi:101111/J.1439- 0531201001597X
113. Zhang, M., Hong, H., Zhou, B., Jin, S., Wang, C., Fu, M., Wang, S., and Xia, G. (2006). The expression of atrial natriuretic peptide in the oviduct and its functions in pig spermatozoa. J. Endocrinol. 189(3), 493-507 doi:101677/JOE.106483