Characterisation of an in vitro system to study maternal communication with spermatozoa
Ahmed Aldarmahi A , Sarah Elliott A , Jean Russell B , Thomas Klonisch C D E , Sabine Hombach-Klonisch C F and Alireza Fazeli A G
+ Author Affiliations
- Author Affiliations
A Academic Unit of Reproductive and Developmental Medicine, University of Sheffield, Level 4, The Jessop Wing, Tree Root Walk, Sheffield S10 2SF, UK.
B Corporate and Computing Services, University of Sheffield, Sheffield S3 7RF, UK.
C Human Anatomy and Cell Science, Gynaecology and Reproductive Medicine, Faculty of Medicine, University of Manitoba, 130-745 Bannatyne Avenue, Winnipeg, MB R3E 0J9, Canada.
D Medical Microbiology and Infectious Diseases, Gynaecology and Reproductive Medicine, Faculty of Medicine, University of Manitoba, 130-745 Bannatyne Avenue, Winnipeg, MB R3E 0J9, Canada.
E Surgery, Gynaecology and Reproductive Medicine, Faculty of Medicine, University of Manitoba, 130-745 Bannatyne Avenue, Winnipeg, MB R3E 0J9, Canada.
F Obstetrics, Gynaecology and Reproductive Medicine, Faculty of Medicine, University of Manitoba, 130-745 Bannatyne Avenue, Winnipeg, MB R3E 0J9, Canada.
G Corresponding author. Email: a.fazeli@sheffield.ac.uk
Reproduction, Fertility and Development 24(7) 988-998 https://doi.org/10.1071/RD11268
Submitted: 19 October 2011 Accepted: 9 February 2012 Published: 20 March 2012
Abstract
In vivo, gamete maturation, fertilisation and early embryonic development take place inside the oviduct. Several studies have indicated that local responses towards gametes and embryos are generated by the maternal reproductive tract. However, no defined in vitro model currently exists to allow detailed and systematic investigation of maternal communications with gametes and embryos. Therefore, we characterised an in vitro model based on the interaction of boar spermatozoa with an immortalised porcine oviduct epithelial cell line to evaluate different factors that may affect this model. The factors tested were sperm viability, source of spermatozoa, cell passage effect and the effect of reproductive and non-reproductive epithelial cells in the interaction with spermatozoa. After 24 h of co-incubation, RNA was extracted and used to synthesise cDNA for quantitative real-time PCR. Alteration in the expression of genes such as adrenomedullin, heat-shock 70-kDa protein 8 and prostaglandin E synthase was considered as the end point of this assay. The results showed that sperm viability and cell passage number had an effect on oviductal gene expression in response to spermatozoa. Oviductal cells showed significant alterations in gene expression when compared with non-reproductive epithelial cells. The simple in vitro system described here has potential application for further studies in our understanding of mechanisms involved in maternal interactions with spermatozoa.
Additional keywords: epithelial cells, in vitro model, oviduct, real-time PCR.
References
Ball, M. A., and Parker, G. A. (2003). Sperm competition games: sperm selection by females. J. Theor. Biol. 224, 27–42.| Sperm competition games: sperm selection by females.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3szms1CksQ%3D%3D&md5=d462fad865368b3b21ccd6d61ca03de7CAS | 12900202PubMed |
Bauersachs, S., Blum, H., Mallok, S., Wenigerkind, H., Rief, S., Prelle, K., and Wolf, E. (2003). Regulation of ipsilateral and contralateral bovine oviduct epithelial cell function in the postovulation period: a transcriptomics approach. Biol. Reprod. 68, 1170–1177.
| Regulation of ipsilateral and contralateral bovine oviduct epithelial cell function in the postovulation period: a transcriptomics approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisVert7g%3D&md5=853cbc3130b519a736467df169d82ee1CAS | 12606461PubMed |
Bland, J. M., and Altman, D. G. (1996). The use of transformation when comparing two means. BMJ 312, 1153.
| The use of transformation when comparing two means.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK283hsFGrtQ%3D%3D&md5=71823e7499d516f4bca909723053c8f6CAS | 8620137PubMed |
Boatman, D. E. (1997). Responses of gametes to the oviductal environment. Hum. Reprod. 12, 133–149.
| 1:STN:280:DyaK1c%2FpsVSmuw%3D%3D&md5=2cb58cc0b5cf4668d3e3b307c4e6a4e8CAS | 9433970PubMed |
Boilard, M., Bailey, J., Collin, S., Dufour, M., and Sirard, M. A. (2002). Effect of bovine oviduct epithelial cell apical plasma membranes on sperm function assessed by a novel flow cytometric approach. Biol. Reprod. 67, 1125–1132.
| Effect of bovine oviduct epithelial cell apical plasma membranes on sperm function assessed by a novel flow cytometric approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsV2rtr0%3D&md5=0b91622bc5a322d9e2487237a40283b6CAS | 12297527PubMed |
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., Vandesompele, J., and Wittwer, C. T. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611–622.
| The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVWqs7g%3D&md5=0508fe77e67eed035779984ba50fa02cCAS | 19246619PubMed |
Caron, K. M., and Smithies, O. (2001). Extreme hydrops fetalis and cardiovascular abnormalities in mice lacking a functional adrenomedullin gene. Proc. Natl. Acad. Sci. USA 98, 615–619.
| Extreme hydrops fetalis and cardiovascular abnormalities in mice lacking a functional adrenomedullin gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslKntg%3D%3D&md5=d5e904043ed34fb388628530b929778cCAS | 11149956PubMed |
Chang-Liu, C. M., and Woloschak, G. E. (1997). Effect of passage number on cellular response to DNA-damaging agents: cell survival and gene expression. Cancer Lett. 113, 77–86.
| Effect of passage number on cellular response to DNA-damaging agents: cell survival and gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXht1Khsb8%3D&md5=c3780ba1762a5aff46a1b30f050d8fceCAS | 9065805PubMed |
Chiu, P. C., Liao, S., Lam, K. K., Tang, F., Ho, J. C., Ho, P. C., O, W. S., Yao, Y. Q., and Yeung, W. S. (2010). Adrenomedullin regulates sperm motility and oviductal ciliary beat via cyclic adenosine 5′-monophosphate/protein kinase A and nitric oxide. Endocrinology 151, 3336–3347.
| Adrenomedullin regulates sperm motility and oviductal ciliary beat via cyclic adenosine 5′-monophosphate/protein kinase A and nitric oxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpt1Cms7Y%3D&md5=f71050d74a1752b04eb0bacdf5bf80b0CAS | 20444935PubMed |
Di Iorio, R., Marinoni, E., and Cosmi, E. V. (1998). New peptides, hormones and parturition. Gynecol. Endocrinol. 12, 429–434.
| New peptides, hormones and parturition.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7msVGlsQ%3D%3D&md5=1c188b1658f5361016b2910ad89e8df4CAS | 10065169PubMed |
Dunnett, C. W., and Crisafio, R. (1955). The operating characteristics of some official weight variation tests for tablets. J. Pharm. Pharmacol. 7, 314–327.
| The operating characteristics of some official weight variation tests for tablets.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG2M%2FntVaisw%3D%3D&md5=7e53b02fa87d1cd5a3bcd684026b155fCAS | 14368526PubMed |
Ebers, K. L., Zhang, C. Y., Zhang, M. Z., Bailey, R. H., and Zhang, S. (2009). Transcriptional profiling avian beta-defensins in chicken oviduct epithelial cells before and after infection with Salmonella enterica serovar Enteritidis. BMC Microbiol. 9, 153.
| Transcriptional profiling avian beta-defensins in chicken oviduct epithelial cells before and after infection with Salmonella enterica serovar Enteritidis.Crossref | GoogleScholarGoogle Scholar | 19642979PubMed |
Ellington, J. E., Ignotz, G. G., Varner, D. D., Marcucio, R. S., Mathison, P., and Ball, B. A. (1993). In vitro interaction between oviduct epithelial and equine sperm. Arch. Androl. 31, 79–86.
| In vitro interaction between oviduct epithelial and equine sperm.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c%2FivFartg%3D%3D&md5=5c823685495e97f9f5b6cb32f7126e24CAS | 8215695PubMed |
Elliott, R. M., Lloyd, R. E., Fazeli, A., Sostaric, E., Georgiou, A. S., Satake, N., Watson, P. F., and Holt, W. V. (2009). Effects of HSPA8, an evolutionarily conserved oviductal protein, on boar and bull spermatozoa. Reproduction 137, 191–203.
| Effects of HSPA8, an evolutionarily conserved oviductal protein, on boar and bull spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovV2ks7g%3D&md5=a875f2aad84d584215c3ba03d04c5432CAS | 18996976PubMed |
Fazeli, A., and Pewsey, E. (2008). Maternal communication with gametes and embryos: a complex interactome. Brief. Funct. Genomics Proteomics 7, 111–118.
| Maternal communication with gametes and embryos: a complex interactome.Crossref | GoogleScholarGoogle Scholar |
Fazeli, A., Duncan, A. E., Watson, P. F., and Holt, W. V. (1999). Sperm–oviduct interaction: induction of capacitation and preferential binding of uncapacitated spermatozoa to oviductal epithelial cells in porcine species. Biol. Reprod. 60, 879–886.
| Sperm–oviduct interaction: induction of capacitation and preferential binding of uncapacitated spermatozoa to oviductal epithelial cells in porcine species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitVGru7k%3D&md5=6f2d978a4dd967afe9b70b319d631834CAS | 10084961PubMed |
Fazeli, A., Elliott, R. M., Duncan, A. E., Moore, A., Watson, P. F., and Holt, W. V. (2003). In vitro maintenance of boar sperm viability by a soluble fraction obtained from oviductal apical plasma membrane preparations. Reproduction 125, 509–517.
| In vitro maintenance of boar sperm viability by a soluble fraction obtained from oviductal apical plasma membrane preparations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFOqt7c%3D&md5=9222babbc72e9eb4a9d0c25acc8e2dc8CAS | 12683921PubMed |
Fazeli, A., Affara, N. A., Hubank, M., and Holt, W. V. (2004). Sperm-induced modification of the oviductal gene expression profile after natural insemination in mice. Biol. Reprod. 71, 60–65.
| Sperm-induced modification of the oviductal gene expression profile after natural insemination in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFKktLY%3D&md5=4a0b2d5c0b943970574b381d8934b002CAS | 14973272PubMed |
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, 1785–1796.
| Gametes alter the oviductal secretory proteome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Cgtb%2FK&md5=b884abe229212e9130df8976ff79ae47CAS | 16105986PubMed |
Green, C. E., Bredl, J., Holt, W. V., Watson, P. F., and Fazeli, A. (2001). Carbohydrate mediation of boar sperm binding to oviductal epithelial cells in vitro. Reproduction 122, 305–315.
| Carbohydrate mediation of boar sperm binding to oviductal epithelial cells in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFWjtb0%3D&md5=86e4a7753ed469e081b838c49960bee5CAS | 11467982PubMed |
Holt, W. V., and Fazeli, A. (2010). The oviduct as a complex mediator of mammalian sperm function and selection. Mol. Reprod. Dev. 77, 934–943.
| The oviduct as a complex mediator of mammalian sperm function and selection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVCktrnL&md5=4531393e86f8dc60f6bfb9833d01dffeCAS | 20886635PubMed |
Hombach-Klonisch, S., Pocar, P., Kauffold, J., and Klonisch, T. (2006). Dioxin exerts anti-oestrogenic actions in a novel dioxin-responsive telomerase-immortalized epithelial cell line of the porcine oviduct (TERT-OPEC). Toxicol. Sci. 90, 519–528.
| Dioxin exerts anti-oestrogenic actions in a novel dioxin-responsive telomerase-immortalized epithelial cell line of the porcine oviduct (TERT-OPEC).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xit1Ons7k%3D&md5=65e9419d7579c99d6be9791e9c1d1c67CAS | 16431846PubMed |
Hunter, R. H. (2008). Sperm release from oviduct epithelial binding is controlled hormonally by peri-ovulatory graafian follicles. Mol. Reprod. Dev. 75, 167–174.
| Sperm release from oviduct epithelial binding is controlled hormonally by peri-ovulatory graafian follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2snkslOlsg%3D%3D&md5=2ef073340e4ac0e21d265a71e33e0884CAS | 17722022PubMed |
Kodithuwakku, S. P., Miyamoto, A., and Wijayagunawardane, M. P. (2007). Spermatozoa stimulate prostaglandin synthesis and secretion in bovine oviductal epithelial cells. Reproduction 133, 1087–1094.
| Spermatozoa stimulate prostaglandin synthesis and secretion in bovine oviductal epithelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGnu7Y%3D&md5=122d892a9cb427c4ba19688175e66ca1CAS | 17636163PubMed |
Lee, K. F., Chow, J. F., Xu, J. S., Chan, S. T., Ip, S. M., and Yeung, W. S. (2001). A comparative study of gene expression in murine embryos developed in vivo, cultured in vitro and co-cultured with human oviductal cells using messenger ribonucleic acid differential display. Biol. Reprod. 64, 910–917.
| A comparative study of gene expression in murine embryos developed in vivo, cultured in vitro and co-cultured with human oviductal cells using messenger ribonucleic acid differential display.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsVKjtrY%3D&md5=52491f708ba51d357b95aae4079c50c4CAS | 11207208PubMed |
Lee, K. F., Yao, Y. Q., Kwok, K. L., Xu, J. S., and Yeung, W. S. (2002). Early developing embryos affect the gene expression patterns in the mouse oviduct. Biochem. Biophys. Res. Commun. 292, 564–570.
| Early developing embryos affect the gene expression patterns in the mouse oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitFeitL8%3D&md5=76e8b0fcd8f1e2e328031dd9d70e1b66CAS | 11906198PubMed |
Li, H. W., Liao, S. B., Chiu, P. C., Tam, W. W., Ho, J. C., Ng, E. H., Ho, P. C., Yeung, W. S., Tang, F., and O, W. S. (2010). Expression of adrenomedullin in human oviduct, its regulation by the hormonal cycle and contact with spermatozoa, and its effect on ciliary beat frequency of the oviductal epithelium. J. Clin. Endocrinol. Metab. 95, E18–E25.
| Expression of adrenomedullin in human oviduct, its regulation by the hormonal cycle and contact with spermatozoa, and its effect on ciliary beat frequency of the oviductal epithelium.Crossref | GoogleScholarGoogle Scholar | 20534761PubMed |
Liao, S. B., Ho, J. C., Tang, F., and O, W. S. (2011). Adrenomedullin increases ciliary beat frequency and decreases muscular contraction in the rat oviduct. Reproduction 141, 367–372.
| Adrenomedullin increases ciliary beat frequency and decreases muscular contraction in the rat oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkt1Crt74%3D&md5=dfcf5f052ac5aca31cb056b043033396CAS | 21173072PubMed |
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(–Delta Delta C(T)) Method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2(–Delta Delta C(T)) Method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=c02316d2aa02af4c464251269a77c9c9CAS | 11846609PubMed |
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, 408–418.
| Effects of oviductal proteins, including heat-shock 70-kDa protein 8, on survival of ram spermatozoa over 48 h in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFemsLw%3D&md5=cc0ad63160a449de73cc5428402848ffCAS | 19261218PubMed |
Long, E. L., Sonstegard, T. S., Long, J. A., Van Tassell, C. P., and Zuelke, K. A. (2003). Serial analysis of gene expression in turkey sperm storage tubules in the presence and absence of resident sperm. Biol. Reprod. 69, 469–474.
| Serial analysis of gene expression in turkey sperm storage tubules in the presence and absence of resident sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVertbw%3D&md5=0f9708f5314fffa4a061e9caa166bd0cCAS | 12672662PubMed |
Marinoni, E., Di Iorio, R., Villaccio, B., Vellucci, O., Di Netta, T., Sessa, M., Letizia, C., and Cosmi, E. V. (2005). Adrenomedullin in human male reproductive system. Eur. J. Obstet. Gynecol. Reprod. Biol. 122, 195–198.
| Adrenomedullin in human male reproductive system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFWms73E&md5=af4f519388751acad0d923d093a4ba07CAS | 15908101PubMed |
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, 828–834.
| Oviduct-specific glycoprotein modulates sperm–zona binding and improves efficiency of porcine fertilization in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvVeitL0%3D&md5=a4786ab19e9c4dcf9877fdabfd469ba0CAS | 12748122PubMed |
Murray, M. K. (1997). Morphological features of epithelial cells in the sheep isthmus oviduct during early pregnancy. Anat. Rec. 247, 368–378.
| Morphological features of epithelial cells in the sheep isthmus oviduct during early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3hvFKhsQ%3D%3D&md5=6edc2b1fee2369fb4f1ab801189f383dCAS | 9066914PubMed |
Neumann, E., Riepl, B., Knedla, A., Lefevre, S., Tarner, I. H., Grifka, J., Steinmeyer, J., Scholmerich, J., Gay, S., and Muller-Ladner, U. (2010). Cell culture and passaging alters gene expression pattern and proliferation rate in rheumatoid arthritis synovial fibroblasts. Arthritis Res. Ther. 12, R83.
| Cell culture and passaging alters gene expression pattern and proliferation rate in rheumatoid arthritis synovial fibroblasts.Crossref | GoogleScholarGoogle Scholar | 20462438PubMed |
Overstreet, J. W., and Adams, C. E. (1971). Mechanisms of selective fertilization in the rabbit: sperm transport and viability. J. Reprod. Fertil. 26, 219–231.
| Mechanisms of selective fertilization in the rabbit: sperm transport and viability.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3M3lt1Ggsw%3D%3D&md5=65154e1c9b2ca2ff1becd01ce69a9163CAS | 5558409PubMed |
Parrish, J. J., Susko-Parrish, J., Winer, M. A., and First, N. L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–1180.
| Capacitation of bovine sperm by heparin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXkslWit7g%3D&md5=f45cbc9d70f88613dedbf00729038d72CAS | 3408784PubMed |
Pursel, V. G., and Johnson, L. A. (1975). Freezing of boar spermatozoa: fertilizing capacity with concentrated semen and a new thawing procedure. J. Anim. Sci. 40, 99–102.
| 1:STN:280:DyaE2M%2FnslCjtw%3D%3D&md5=4f504cde4bb8c000eaf1bf861438ac4dCAS | 1110222PubMed |
Satake, N., Elliott, R. M., Watson, P. F., and Holt, W. V. (2006). Sperm selection and competition in pigs may be mediated by the differential motility activation and suppression of sperm subpopulations within the oviduct. J. Exp. Biol. 209, 1560–1572.
| Sperm selection and competition in pigs may be mediated by the differential motility activation and suppression of sperm subpopulations within the oviduct.Crossref | GoogleScholarGoogle Scholar | 16574812PubMed |
Shin, S., Dimitri, C. A., Yoon, S. O., Dowdle, W., and Blenis, J. (2010). ERK2 but not ERK1 induces epithelial-to-mesenchymal transformation via DEF motif-dependent signalling events. Mol. Cell 38, 114–127.
| ERK2 but not ERK1 induces epithelial-to-mesenchymal transformation via DEF motif-dependent signalling events.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvFynsbY%3D&md5=a7d2c10267acf504bb40ccabfa6b4d0fCAS | 20385094PubMed |
Smith, T. T., and Nothnick, W. B. (1997). Role of direct contact between spermatozoa and oviductal epithelial cells in maintaining rabbit sperm viability. Biol. Reprod. 56, 83–89.
| Role of direct contact between spermatozoa and oviductal epithelial cells in maintaining rabbit sperm viability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXis1Gqsg%3D%3D&md5=013dcfe1430aa8adf7bb55bde5dba8d8CAS | 9002636PubMed |
Suarez, S. S. (2007). Interactions of spermatozoa with the female reproductive tract: inspiration for assisted reproduction. Reprod. Fertil. Dev. 19, 103–110.
| Interactions of spermatozoa with the female reproductive tract: inspiration for assisted reproduction.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s7ovFKmsA%3D%3D&md5=1e0d4dab74b65a026300a382dad2129bCAS | 17389139PubMed |
Ulbrich, S. E., Zitta, K., Hiendleder, S., and Wolf, E. (2010). In vitro systems for intercepting early embryo–maternal cross-talk in the bovine oviduct. Theriogenology 73, 802–816.
| In vitro systems for intercepting early embryo–maternal cross-talk in the bovine oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXivFGltr0%3D&md5=0c9097ba61542d9d898825d7838c6624CAS | 19963260PubMed |
Wenger, S. L., Senft, J. R., Sargent, L. M., Bamezai, R., Bairwa, N., and Grant, S. G. (2004). Comparison of established cell lines at different passages by karyotype and comparative genomic hybridization. Biosci. Rep. 24, 631–639.
| Comparison of established cell lines at different passages by karyotype and comparative genomic hybridization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvFOksLk%3D&md5=f0d26f854b17f7c7571956e6b6980998CAS | 16158200PubMed |
Winer, J., Jung, C. K., Shackel, I., and Williams, P. M. (1999). Development and validation of real-time quantitative reverse transcriptase–polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal. Biochem. 270, 41–49.
| Development and validation of real-time quantitative reverse transcriptase–polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjtVersr0%3D&md5=01fb33a7f6ffa115c9632fb10d93088eCAS | 10328763PubMed |
Yao, Y. Q., Ho, P. C., and Yeung, W. S. (1999). Effects of human oviductal cell co-culture on various functional parameters of human spermatozoa. Fertil. Steril. 71, 232–239.
| Effects of human oviductal cell co-culture on various functional parameters of human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7ktV2iuw%3D%3D&md5=c05d4bd73e5a41879eb834d40e81e35aCAS | 9988390PubMed |
Yeste, M., Lloyd, R. E., Badia, E., Briz, M., Bonet, S., and Holt, W. V. (2009). Direct contact between boar spermatozoa and porcine oviductal epithelial cell (OEC) cultures is needed for optimal sperm survival in vitro. Anim. Reprod. Sci. 113, 263–278.
| Direct contact between boar spermatozoa and porcine oviductal epithelial cell (OEC) cultures is needed for optimal sperm survival in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3pvFSmtA%3D%3D&md5=62eff38b60d6ee6cf28fd9933d552763CAS | 18824315PubMed |
Yeung, W. S., Lau, E. Y., Chan, S. T., and Ho, P. C. (1996). Co-culture with homologous oviductal cells improved the implantation of human embryos – a prospective randomised control trial. J. Assist. Reprod. Genet. 13, 762–767.
| Co-culture with homologous oviductal cells improved the implantation of human embryos – a prospective randomised control trial.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s7ktVSitg%3D%3D&md5=53c7f683860a0eea684ad3795fe71466CAS | 8986585PubMed |
Zumoffen, C. M., Caille, A. M., Munuce, M. J., Cabada, M. O., and Ghersevich, S. A. (2010). Proteins from human oviductal tissue-conditioned medium modulate sperm capacitation. Hum. Reprod. 25, 1504–1512.
| Proteins from human oviductal tissue-conditioned medium modulate sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsVOnur0%3D&md5=9bbf268cdd423db5ae88b6e52d18ec6bCAS | 20338958PubMed |
