The secretions of oviduct epithelial cells increase the equine in vitro fertilization rate: are osteopontin, atrial natriuretic peptide A and oviductin involved?
Mugnier, S.; Kervella, M.; Douet, Cécileet al.
2009 • In Reproductive Biology and Endocrinology, 7 (1), p. 129
[en] ABSTRACT: BACKGROUND: Oviduct epithelial cells (OEC) co-culture promotes in vitro fertilization (IVF) in human, bovine and porcine species, but no data are available from equine species. Yet, despite numerous attempts, equine IVF rates remain low. Our first aim was to verify a beneficial effect of the OEC on equine IVF. In mammals, oviductal proteins have been shown to interact with gametes and play a role in fertilization. Thus, our second aim was to identify the proteins involved in fertilization in the horse. Methods & results In the first experiment, we co-incubated fresh equine spermatozoa treated with calcium ionophore and in vitro matured equine oocytes with or without porcine OEC. We showed that the presence of OEC increases the IVF rates. In the subsequent experiments, we co-incubated equine gametes with OEC and we showed that the IVF rates were not significantly different between 1) gametes co-incubated with equine vs porcine OEC, 2) intact cumulus-oocyte complexes vs denuded oocytes, 3) OEC previously stimulated with human Chorionic Gonadotropin, Luteinizing Hormone and/or oestradiol vs non stimulated OEC, 4) in vivo vs in vitro matured oocytes. In order to identify the proteins responsible for the positive effect of OEC, we first searched for the presence of the genes encoding oviductin, osteopontin and atrial natriuretic peptide A (ANP A) in the equine genome. We showed that the genes coding for osteopontin and ANP A are present. But the one for oviductin either has become a pseudogene during evolution of horse genome or has been not well annotated in horse genome sequence. We then showed that osteopontin and ANP A proteins are present in the equine oviduct using a surface plasmon resonance biosensor, and we analyzed their expression during oestrus cycle by Western blot. Finally, we co-incubated equine gametes with or without purified osteopontin or synthesized ANP A. No significant effect of osteopontin or ANP A was observed, though osteopontin slightly increased the IVF rates. CONCLUSION: Our study shows a beneficial effect of homologous and heterologous oviduct cells on equine IVF rates, though the rates remain low. Furthers studies are necessary to identify the proteins involved. We showed that the surface plasmon resonance technique is efficient and powerful to analyze molecular interactions during fertilization.
Disciplines :
Biochemistry, biophysics & molecular biology Veterinary medicine & animal health
Author, co-author :
Mugnier, S.; Institut Scientifique de Recherche Agronomique - INRA > INRA, UMR85, Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France
Kervella, M.; Institut Scientifique de Recherche Agronomique - INRA > INRA, UMR85, Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France
Douet, Cécile; Institut Scientifique de Recherche Agronomique - INRA > INRA, UMR85, Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France
Canepa, S.; Institut Scientifique de Recherche Agronomique - INRA > UMR85, Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France
Pascal, G.; Institut Scientifique de Recherche Agronomique - INRA > UMR85, Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France
Deleuze, Stefan ; Université de Liège - ULiège > Département clinique des animaux de compagnie et des équidés > Anesthésiologie gén. et pathologie chirurg. des grds animaux
Duchamp, G.; Institut Scientifique de Recherche Agronomique - INRA > UE1297 Unité Expérimentale de Physiologie Animale de l’Orfrasière, F- 37380 Nouzilly, France
Monget, P.; Institut Scientifique de Recherche Agronomique - INRA > INRA, UMR85, Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France
Goudet, Ghylene; Institut Scientifique de Recherche Agronomique - INRA > INRA, UMR85, Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France
Language :
English
Title :
The secretions of oviduct epithelial cells increase the equine in vitro fertilization rate: are osteopontin, atrial natriuretic peptide A and oviductin involved?
Yanagimachi R. Mammalian fertilization. The Physiology of Reproduction 1994, 1:189-317. New York: Raven Press, Knobil E, Neill JD.
Leese HJ. The formation and function of oviduct fluid. J Reprod Fertil 1988, 82:843-856.
Verhage HG, Mavrogianis PA, Boice ML, Li W, Fazleabas AT. Oviductal epithelium of the baboon: hormonal control and the immuno-gold localization of oviduct-specific glycoproteins. Am J Anat 1990, 187:81-90. 10.1002/aja.1001870109, 2296912.
Abe H. The mammalian oviduct epithelium: regional variations in cytological and functional aspects of the oviductal secretory cells. Histol Histopathol 1996, 11:743-768.
Bongso A, Ng SC, Fong CY, Ratnam S. Improved fertilization rates of human oocytes in coculture. J In Vitro Fert Embryo Transf 1991, 8:216-221. 10.1007/BF01130808, 1753168.
Kervancioglu ME, Saridogan E, Atasü T, Camlibel T, Demircan A, Sarikamis B, Djahanbakhch O. Human Fallopian tube epithelial cell co-culture increases fertilization rates in male factor infertility but not in tubal or unexplained infertility. Hum Reprod 1997, 12:1253-1258. 10.1093/humrep/12.6.1253, 9222012.
Chian RC, Sirard MA. Fertilizing ability of bovine spermatozoa cocultured with oviduct epithelial cells. Biol Reprod 1995, 52:156-162. 10.1095/biolreprod52.1.156, 7711174.
Way AL, Schuler AM, Killian GJ. Influence of bovine ampullary and isthmic oviductal fluid on sperm-egg binding and fertilization in vitro. J Reprod Fertil 1997, 109:95-101.
Martus NS, Verhage HG, Mavrogianis PA, Thibodeaux JK. Enhancement of bovine oocyte fertilization in vitro with a bovine oviductal specific glycoprotein. J Reprod Fertil 1998, 113:323-329.
McCauley TC, Buhi WC, Wu GM, Mao J, Caamano JN, Didion BA, Day BN. Oviduct-Specific Glycoprotein modulates sperm-zona binding and improves efficiency of porcine fertilization in vitro. Biol Reprod 2003, 69:828-834. 10.1095/biolreprod.103.016444, 12748122.
Romar R, Coy P, Campos I, Gadea J, Matas C, Ruiz S. Effect of co-culture of porcine sperm and oocytes with porcine oviductal epithelial cells on in vitro fertilization. Anim Reprod Sci 2001, 68:85-98. 10.1016/S0378-4320(01)00133-6, 11600277.
Berg DK, Thompson JG, Pugh PA, Tervit HR, Asher GW. Successful in vitro culture of early cleavage stage embryos recovered from superovulatory red deer (Cervus elaphus). Theriogenology 1995, 44:247-254. 10.1016/0093-691X(95)00174-7, 16727724.
Locatelli Y, Cognié Y, Vallet JC, Baril G, Verdier M, Poulin N, Legendre X, Mermillod P. Successful use of oviduct epithelial cell coculture for in vitro production of viable red deer (Cervus elaphus) embryos. Theriogenology 2005, 64:1729-1739. 10.1016/j.theriogenology.2005.04.002, 15890398.
Khatir H, Anouassi A, Tibary A. Production of dromedary (Camelus dromedarius) embryos by IVM and IVF and co-culture with oviductal or granulosa cells. Theriogenology 2004, 62:1175-1185. 10.1016/j.theriogenology.2004.01.016, 15325545.
Coy P, Cánovas S, Mondéjar I, Saavedra MD, Romar R, Grullón L, Matás C, Avilés M. Oviduct-specific glycoprotein and heparin modulate sperm-zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc Natl Acad Sci USA 2008, 105:15809-15814. 10.1073/pnas.0804422105, 2572915, 18838686.
O'Day-Bowman MB, Mavrogianis PA, Reuter LM, Johnson DE, Fazleabas AT, Verhage HG. Association of oviduct-specific glycoproteins with human and baboon (Papio anubis) ovarian oocytes and enhancement of human sperm binding to human hemizonae following in vitro incubation. Biol Reprod 1996, 54:60-69. 10.1095/biolreprod54.1.60, 8838001.
Hao Y, Mathialagan N, Walters E, Mao J, Lai L, Becker D, Li W, Critser J, Prather RS. Osteopontin reduces polyspermy during in vitro fertilization of porcine oocytes. Biol Reprod 2006, 75:726-733. 10.1095/biolreprod.106.052589, 16870945.
Gonçalves RF, Chapman DA, Bertolla RP, Eder I, Killian GJ. Pre-treatment of cattle semen or oocytes with purified milk osteopontin affects in vitro development. Anim Reprod Sci 2008, 108:375-383. 10.1016/j.anireprosci.2007.09.006, 18024016.
Monaco E, Gasparrini B, Boccia L, De Rosa A, Attanasio L, Zicarelli L, Killian G. Effect of osteopontin (OPN) on in vitro embryo development in cattle. Theriogenology 2009, 71:450-457. 10.1016/j.theriogenology.2008.08.012, 18835636.
Anderson RA, Feathergill KA, Drisdel RC, Rawlins RG, Mack SR, Zaneveld LJ. Atrial Natriuretic peptide (ANP) as a stimulus of the human accrosome reaction and a component of ovarian follicular fluid: correlation of follicular ANP content with in vitro fertilization outcome. J Androl 1994, 15:61-70.
Zamir N, Barkan D, Keynan N, Naor Z, Breitbart H. Atrial Natriuretic peptide induces acrosomal exocytosis in bovine spermatozoa. Am J Physiol 1995, 269:E216-E221.
Zhang M, Hong H, Zhou B, Jin S, Wang C, Fu M, Wang S, Xia G. The expression of atrial natriuretic peptide in the oviduct and its functions in pig spermatozoa. J Endocrinol 2006, 189:493-507. 10.1677/joe.1.06483, 16731781.
Buhi WC. Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein. Reproduction 2002, 123:355-362. 10.1530/rep.0.1230355, 11882012.
Palmer E, Bézard J, Magistrini M, Duchamp G. In vitro fertilization in the horse. A retrospective study. J Reprod Fertil 1991, 44(Suppl):375-384.
Dell'Aquila ME, Fusco S, Lacalandra GM, Maritato F. In vitro maturation and fertilization of equine oocytes recovered during the breeding season. Theriogenology 1996, 45:547-560. 10.1016/0093-691X(95)00402-T, 16727818.
Alm H, Torner H, Blottner S, Nürnberg G, Kanitz W. Effect of sperm cryopreservation and treatment with calcium ionophore or heparin on in vitro fertilization of horse oocytes. Theriogenology 2001, 56:817-829. 10.1016/S0093-691X(01)00610-0, 11665884.
McPartlin LA, Suarez SS, Czaya CA, Hinrichs K, Bedford-Guaus SJ. Hyperactivation of stallion sperm is required for successful in vitro fertilization of equine oocytes. Biol Reprod 2009, 81:199-206. 10.1095/biolreprod.108.074880, 19208544.
Abeydeera LR, Day BN. Fertilization and subsequent development in vitro of pig oocytes inseminated in a modified tris-buffered medium with frozen-thawed ejaculated spermatozoa. Biol Reprod 1997, 57:729-734. 10.1095/biolreprod57.4.729, 9314573.
Funahashi H, Day BN. Advances in in-vitro production of porcine embryos. J Reprod Fertil 1997, 52(Suppl):271-283.
Day BN. Reproductive biotechnologies: current status in porcine reproduction. Anim Reprod Sci 2000, 60-61:161-172. 10.1016/S0378-4320(00)00079-8, 10844192.
Nagai T, Funahashi H, Yoshioka K, Kikuchi K. Up date of in vitro production of porcine embryos. Front Biosci 2006, 11:2565-2573. 10.2741/1991, 16720334.
Hashimoto S. Application of in vitro maturation to assisted reproductive technology. J Reprod Dev 2009, 55:1-10. 10.1262/jrd.20127, 19276618.
Crozet N, Ahmed-Ali M, Dubos MP. Developmental competence of goat oocytes from follicles of different size categories following maturation, fertilization and culture in vitro. J Reprod Fertil 1995, 103:293-298.
Keskintepe L, Darwish GM, Kenimer AT, Brackett BG. Term development of caprine embryos derived from immature oocytes in vitro. Theriogenology 1994, 42:527-35. 10.1016/0093-691X(94)90690-K, 16727559.
Rho GJ, Hahnel AC, Betteridge KJ. Comparisons of oocyte maturation times and of three methods of sperm preparation for their effects on the production of goat embryos in vitro. Theriogenology 2001, 56:503-516. 10.1016/S0093-691X(01)00581-7, 11516129.
Katska-Ksiazkiewicz L, Ryñska B, Gajda B, Smorag Z. Effect of donor stimulation, frozen semen and heparin treatment on the efficiency of in vitro embryo production in goats. Theriogenology 2004, 62:576-586. 10.1016/j.theriogenology.2003.11.007, 15226013.
Crozet N, Huneau D, Desmedt V, Théron MC, Szöllösi D, Torrès S, Sévellec C. In vitro fertilization with normal development in the sheep. Gamete Res 1987, 16:159-170. 10.1002/mrd.1120160207, 3506906.
Wan PC, Hao ZD, Zhou P, Wu Y, Yang L, Cui MS, Liu SR, Zeng SM. Effects of SOF and CR1 media on developmental competence and cell apoptosis of ovine in vitro fertilization embryos. Anim Reprod Sci 2009, 114:279-288. 10.1016/j.anireprosci.2008.09.020, 19008058.
Ellington JE, Ball BA, Yang X. Binding of stallion spermatozoa to the equine zona pellucida after coculture with oviductal epithelial cells. J Reprod Fertil 1993, 98:203-208.
Ellington JE, Samper JC, Jones AE, Oliver SA, Burnett KM, Wright RW. In vitro interactions of cryopreserved stallion spermatozoa and oviduct (uterine tube) epithelial cells or their secretory products. Anim Reprod Sci 1999, 56:51-65. 10.1016/S0378-4320(99)00030-5, 10401702.
Dobrinski I, Suarez SS, Ball BA. Intracellular calcium concentration in equine spermatozoa attached to oviductal epithelial cells in vitro. Biol Reprod 1996, 54:783-788. 10.1095/biolreprod54.4.783, 8924497.
Dobrinski I, Smith TT, Suarez SS, Ball BA. Membrane contact with oviductal epithelium modulates the intracellular calcium concentration of equine spermatozoa in vitro. Biol Reprod 1997, 56:861-869. 10.1095/biolreprod56.4.861, 9096866.
Thomas PG, Ball BA, Brinsko SP. Interaction of equine spermatozoa with oviduct epithelial cell explants is affected by estrous cycle and anatomic origin of explants. Biol Reprod 1994, 51:222-228. 10.1095/biolreprod51.2.222, 7948476.
Thomas PG, Ball BA, Miller PG, Brinsko SP, Southwood L. A subpopulation of morphologically normal, motile spermatozoa attach to equine oviduct epithelial cell monolayers. Biol Reprod 1994, 51:303-309. 10.1095/biolreprod51.2.303, 7948486.
Hinrichs K, Love CC, Brinsko SP, Choi YH, Varner DD. 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 transfert. Biol Reprod 2002, 67:256-262. 10.1095/biolreprod67.1.256, 12080025.
Deleuze S, Goudet G, Caillaud M, Lahuec C, Duchamp G. Efficiency of embryonic development after intrafollicular and intraoviductal transfer of in vitro and in vivo matured horse oocytes. Theriogenology 2009, 72:203-209. 10.1016/j.theriogenology.2009.02.001, 19339039.
Deleuze S, Dubois CS, Caillaud M, Bruneau B, Goudet G, Duchamp G. Influence of cysteamine on in vitro maturation, in vitro and in vivo fertilization of equine oocytes. Reprod Domest Anim 2008,
Duchamp G, Bour B, Combarnous Y, Palmer E. Alternative solutions to hCG induction of ovulation in the mare. J Reprod Fertil 1987, 35(Suppl):221-228.
Mugnier S, Boittin S, Douet C, Monget P, Magistrini M, Goudet G. The involvement of beta-1,4-Galactosyltransferase and N-Acetylglucosamine residues in fertilization has been lost in the horse. Reprod Biol Endocrinol 2008, 6:51. 10.1186/1477-7827-6-51, 2607279, 19014565.
Goudet G, Belin F, Mlodawska W, Bezard J. Influence of Epidermal Growth Factor on in vitro maturation of equine oocytes. J Reprod Fertil 2000, 15(Suppl):49-52.
Mugnier S, Dell'Aquila ME, Pelaez J, Douet C, Ambruosi B, De Santis T, Lacalandra GM, Lebos C, Sizaret PY, Delaleu B, Monget P, Mermillod P, Magistrini M, Meyers SA, Goudet G. New insights into the mechanisms of fertilization: Comparison of the fertilization steps, composition, and structure of the zona pellucida between horses and pigs. Biol Reprod 2009, 81:856-870. 10.1095/biolreprod.109.077651, 19587333.
Magistrini M, Palmer E. Motility, triple stain and electron microscopic analysis of spermatozoa treated with ionophore A23187 for in vitro fertilization. J Reprod Fertil 1991, 44(Suppl):661-663.
Goudet G, Bézard J, Duchamp G, Gérard N, Palmer E. Equine oocyte competence for nuclear and cytoplasmic in vitro maturation: effect of follicle size and hormonal environment. Biol Reprod 1997, 57:232-245. 10.1095/biolreprod57.2.232, 9241036.
Hubbard TJ, Aken BL, Ayling S, Ballester B, Beal K, Bragin E, Brent S, Chen Y, Clapham P, Clarke L, Coates G, Fairley S, Fitzgerald S, Fernandez-Banet J, Gordon L, Graf S, Haider S, Hammond M, Holland R, Howe K, Jenkinson A, Johnson N, Kahari A, Keefe D, Keenan S, Kinsella R, Kokocinski F, Kulesha E, Lawson D, Longden I, Megy K, Meidl P, Overduin B, Parker A, Pritchard B, Rios D, Schuster M, Slater G, Smedley D, Spooner W, Spudich G, Trevanion S, Vilella A, Vogel J, White S, Wilder S, Zadissa A, Birney E, Cunningham F, Curwen V, Durbin R, Fernandez-Suarez XM, Herrero J, Kasprzyk A, Proctor G, Smith J, Searle S, Flicek P. Ensembl 2009. Nucleic Acids Res 2009, (37 Database):D690-7. 10.1093/nar/gkn828, 2686571, 19033362.
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-402. 10.1093/nar/25.17.3389, 146917, 9254694.
Birney E, Clamp M, Durbin R. GeneWise and Genomewise. Genome Res 2004, 14(5):988-995. 10.1101/gr.1865504, 479130, 15123596.
Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 1992, 8:275-282.
Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599. 10.1093/molbev/msm092, 17488738.
Martus NS, Verhage HG, Mavrogianis PA, Thibodeaux JK. Enhancement of bovine oocyte fertilization in vitro with a bovine oviductal specific glycoprotein. J Reprod Fertil 1998, 113:323-329.
Rizos D, Pintado B, de la Fuente J, Lonergan P, Gutiérrez-Adan A. Development and pattern of mRNA relative abundance of bovine embryos cultured in the isolated mouse oviduct in organ culture. Mol Reprod Dev 2007, 74:716-723. 10.1002/mrd.20652, 17154298.
Ellington JE, Jones AE, Davitt CM, Schneider CS, Brisbois RS, Hiss GA, Wright RW. Human sperm function in co-culture with human, macaque or bovine oviduct epithelial cell monolayers. Hum Reprod 1998, 13:2797-2804.
Petrunkina AM, Simon K, Günzel-Apel AR, Töpfer-Petersen E. Kinetics of protein tyrosine phosporylation in sperm selected by binding to homologous and heterologous oviductal explants: how specific is the regulation by the oviduct?. Theriogenology 2004, 61:1617-1634. 10.1016/j.theriogenology.2003.09.011, 15019459.
Bézard J, Magistrini M, Duchamp G, Palmer E. Chronology of equine fertilization and embryonic development in vivo and in vitro. Equine Vet J 1989, 8(Suppl):105-110.
Laurincik J, Hyttel P, Rath D, Pivko J. Ovulation, fertilization and pronucleus development in superovulated gilts. Theriogenology 1994, 41:447-452. 10.1016/0093-691X(94)90080-3, 16727402.
Qian Y, Shi WQ, Ding JT, Liu JY, Sha JH, Fan BQ. Effects of type and state of co-culture cells on in-vitro development of porcine oocytes matured and fertilized in vitro. J Assist Reprod Genet 2005, 22:233-238. 10.1007/s10815-005-5145-6, 16021851.
Wegner CC, Killian GJ. In vitro and in vivo association of an oviduct estrus-associated protein with bovine zona pellucida. Mol Reprod Dev 1991, 29:77-84. 10.1002/mrd.1080290112, 2054184.
Buhi WC, O'Brien B, Alvarez IM, Erdos G, Dubois D. Immunogold localization of porcine oviductal secretory proteins within the zona pellucida, perivitelline space, and plasma membrane of oviductal and uterine oocytes and early embryos. Biol Reprod 1993, 48:1274-1283. 10.1095/biolreprod48.6.1274, 8318581.
Gonçalves RF, Staros AL, Killian GJ. 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 2008, 43:720-729. 10.1111/j.1439-0531.2007.00978.x, 18484958.
Familiari G, Heyn R, Relucenti M, Sathananthan H. Structural changes of the zona pellucida during fertilization and embryo development. Front Biosci 2008, 13:6730-6751. 10.2741/3185, 18508691.
Kidson A, Schoevers E, Langendijk P, Verheijden J, Colenbrander B, Bevers M. The effect of oviductal epithelial cell co-culture during in vitro maturation on sow oocyte morphology, fertilization and embryo development. Theriogenology 2003, 59:1889-1903. 10.1016/S0093-691X(02)01291-8, 12600727.
Romar R, Coy P, Gadea J, Rath D. Effect of oviductal and cumulus cells on zona pellucida and cortical granules of porcine oocytes fertilized in vitro with epididymal spermatozoa. Anim Reprod Sci 2005, 85:287-300. 10.1016/j.anireprosci.2004.04.040, 15581512.
Wang WH, Abeydeera LR, Okuda K, Niwa K. Penetration of porcine oocytes during maturation in vitro by cryopreserved, ejaculated spermatozoa. Biol Reprod 1994, 50:510-515. 10.1095/biolreprod50.3.510, 8167222.
Wongsrikeao P, Kaneshige Y, Ooki R, Taniguchi M, Agung B, Nii M, Otoi T. Effect of the removal of cumulus cells on the nuclear maturation, fertilization and development of porcine oocytes. Reprod Domest Anim 2005, 40:166-170. 10.1111/j.1439-0531.2005.00576.x, 15819969.
Romar R, Coy P, Ruiz S, Gadea J, Rath D. Effects of oviductal and cumulus cells on in vitro fertilization and embryo development of porcine oocytes fertilized with epididymal spermatozoa. Theriogenology 2003, 59:975-986. 10.1016/S0093-691X(02)01138-X, 12517398.
Fatehi AN, Zeinstra EC, Kooij RV, Colenbrander B, Bevers MM. Effect of cumulus cell removal of in vitro matured bovine oocytes prior to in vitro fertilization on subsequent cleavage rate. Theriogenology 2002, 57:1347-1355. 10.1016/S0093-691X(01)00717-8, 12013454.
Thomas WK, Seidel GE. Effects of cumulus cells on culture of bovine embryos derived from oocytes matured and fertilized in vitro. J Anim Sci 1993, 71:2506-2510.
Abe H, Hoshi H. Regional and cyclic variations in the ultrastructual features of secretory cells in the oviductal epithelium of the Chinese Meishan pig. Reprod Domest Anim 2007, 42:292-298. 10.1111/j.1439-0531.2006.00781.x, 17506808.
Xia P, Rutledge J, Watson AJ, Armstrong DT. Effect of estrogen-treated porcine ampulla oviductal epithelial cells on early embryonic development in vitro and characterization of their protein synthetic activity. Anim Reprod Sci 1996, 45:217-229. 10.1016/S0378-4320(96)01579-5, 9227924.
Sun T, Lei ZM, Rao CV. A novel regulation of the oviductal glycoprotein gene expression by luteinizing hormone in bovine tubal epithelial cells. Mol Cell Endocrinol 1997, 131:97-108. 10.1016/S0303-7207(97)00104-4, 9256368.
Mishra S, Lei ZM, Rao C. A novel role of luteinizing hormone in the embryo development in cocultures. Biol Reprod 2003, 68:1455-1462. 10.1095/biolreprod.102.011874, 12606322.
Gawronska B, Paukku T, Huhtaniemi I, Wasowicz G, Ziecik AJ. Oestrogen-dependent expression of LH/hCG receptors in pig Fallopian tube and their role in relaxation of the oviduct. J Reprod Fertil 1999, 115:293-301.
Gawronska B, Stepien A, Ziecik AJ. Effect of estradiol and progesterone on oviductal LH-receptors and LH-dependent relaxation of the porcine oviduct. Theriogenology 2000, 53:659-672. 10.1016/S0093-691X(99)00265-4, 10735034.
Grondahl C, Host T, Brück I, Viuff D, Bézard J, Fair T, Greve T, Hyttel P. In vitro production of equine embryos. Biol Reprod 1995, 1(Mono):299-307.
Brown LF, Berse B, Water L, Papadopoulos-Sergiou A, Perruzzi CA, Manseau EJ, Dvorak HF, Senger DR. Expression and distribution of osteopontin in human tissues: widespread association with luminal epithelial surfaces. Mol Biol Cell 1992, 3:1169-1180. 275680, 1421573.
Gabler C, Chapman DA, Killian GJ. Expression and presence of osteopontin and integrins in the bovine oviduct during the oestrous cycle. Reproduction 2003, 126:721-729. 10.1530/rep.0.1260721, 14748691.
Tian X, Pascal G, Fouchécourt S, Pontarotti P, Monget P. Gene birth, death, and divergence: the different scenarios of reproduction-related gene evolution. Biol Reprod 2009, 80:616-621. 10.1095/biolreprod.108.073684, 19129511.
Verhage HG, Mavrogianis PA, O'Day-Bowman MB, Schmidt A, Arias EB, Donnelly KM, Boomsma RA, Thibodeaux JK, Fazleabas AT, Jaffe RC. Characteristics of an oviductal glycoprotein and its potential role in the fertilization process. Biol Reprod 1998, 58:1098-1101. 10.1095/biolreprod58.5.1098, 9603239.
Kim SH, Cho KW, Kim SZ, Koh GY. Characterization of the atrial natriuretic peptide system in the oviduct. Endocrinology 1997, 138:2410-2416. 10.1210/en.138.6.2410, 9165030.
Rotem R, Zamir N, Keynan N, Barkan D, Breitbart H, Naor Z. Atrial natriuretic peptide induces acrosomal exacytosis of human spermatozoa. Am J Physiol 1998, 274:218-223.
Bauersachs S, Blum H, Mallok S, Wenigerkind H, Rief S, Prelle K, Wolf E. Regulation of ipsilateral and contralateral bovine oviduct epithelial cell function in the postovulation period: a transcriptomics approach. Biol Reprod 2003, 68:1170-1177. 10.1095/biolreprod.102.010660, 12606461.
Bauersachs S, Rehfeld S, Ulbrich SE, Mallok S, Prelle K, Wenigerkind H, Einspanier R, Blum H, Wolf E. Monitoring gene expression changes in bovine oviduct epithelial cells during the oestrous cycle. J Mol Endocrinol 2004, 32:449-466. 10.1677/jme.0.0320449, 15072551.
Georgiou AS, Snijders AP, Sostaric E, Aflatoonian R, Vazquez JL, Vazquez JM, Roca J, Martinez EA, Wright PC, Fazeli A. Modulation of the oviductal environment by gametes. J Proteome Res 2007, 6:4656-4666. 10.1021/pr070349m, 18004800.
Carrasco LC, Romar R, Avilés M, Gadea J, Coy P. Determination of glycosidase activity in porcine oviductal fluid at the different phases of the estrous cycle. Reproduction 2008, 136:833-842. 10.1530/REP-08-0221, 18753246.
Cooper MA. Optical biosensors in drug discovery. Nat Rev Drug Discov 2002, 1:515-28. 10.1038/nrd838, 12120258.
Rich RL, Myszka DG. A survey of the year 2002 commercial optical biosensor literature. J Mol Recognit 2003, 16:351-382. 10.1002/jmr.649, 14732928.
