Theriogenology
Volume 73, Issue 6 , Pages 802-816 , 1 April 2010

In vitro systems for intercepting early embryo-maternal cross-talk in the bovine oviduct

  • S.E. Ulbrich

      Affiliations

    • Physiology Weihenstephan, and Z I E L Research Center for Nutrition and Food Sciences, Technical University of Munich, Freising, Germany
    • Corresponding Author InformationCorresponding author. Tel.: +49 8161 71 4429; fax: +49 8161 71 4204.
  • ,
  • K. Zitta

      Affiliations

    • Chair for Molecular Animal Breeding and Biotechnology, and Laboratory for Functional Genome Analysis (LAFUGA), Gene Center, LMU Munich, Munich, Germany
    • Present address: Department of Anaesthesiology and Intensive Care Medicine, University Hospital Schleswig-Holstein, Campus Kiel, Germany.
  • ,
  • S. Hiendleder

      Affiliations

    • JS Davies Epigenetics and Genetics Group, School of Agriculture, Food & Wine and Research Centre for Reproductive Health, The University of Adelaide, Roseworthy Campus, Adelaide, Australia
  • ,
  • E. Wolf

      Affiliations

    • Chair for Molecular Animal Breeding and Biotechnology, and Laboratory for Functional Genome Analysis (LAFUGA), Gene Center, LMU Munich, Munich, Germany

Received 30 September 2009 ,Accepted 30 September 2009.

References 

  1. Humblot P. Use of pregnancy specific proteins and progesterone assays to monitor pregnancy and determine the timing, frequencies and sources of embryonic mortality in ruminants. Theriogenology. 2001;56:1417–1433
  2. Leese HJ, Hugentobler SA, Gray SM, Morris DG, Sturmey RG, Whitear SL, et al. Female reproductive tract fluids: composition, mechanism of formation and potential role in the developmental origins of health and disease. Reprod Fertil Dev. 2008;20:1–8
  3. Rodriguez-Martinez H. Role of the oviduct in sperm capacitation. Theriogenology. 2007;68(Suppl 1):S138–S146
  4. Lloyd RE, Romar R, Matas C, Gutierrez-Adan A, Holt WV, Coy P. Effects of oviductal fluid on the development, quality and gene expression of porcine blastocyst produced in vitro. Reproduction. 2009;137:679–687
  5. Wrenzycki C, Herrmann D, Lucas-Hahn A, Gebert C, Korsawe K, Lemme E, et al. Epigenetic reprogramming throughout preimplantation development and consequences for assisted reproductive technologies. Birth Defects Res C Embryo Today. 2005;75:1–9
  6. Fazeli A. Maternal communication with gametes and embryos. Theriogenology. 2008;70:1182–1187
  7. Menezo YJ, Herubel F. Mouse and bovine models for human IVF. Reprod Biomed Online. 2002;4:170–175
  8. Elsik CG, Tellam RL, Worley KC, Gibbs RA, Muzny DM, Weinstock GM, et al. The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science. 2009;324:522–528
  9. Thibodeaux JK, Godke RA. Potential use of embryo coculture with human in vitro fertilization procedures. J Assist Reprod Genet. 1995;12:665–677
  10. Lee KF, Yao YQ, Kwok KL, Xu JS, Yeung WS. Early developing embryos affect the gene expression patterns in the mouse oviduct. Biochem Biophys Res Commun. 2002;292:564–570
  11. Evans AC, Forde N, O’Gorman GM, Zielak AE, Lonergan P, Fair T. Use of microarray technology to profile gene expression patterns important for reproduction in cattle. Reprod Domest Anim. 2008;43(Suppl 2):359–367
  12. Brussow KP, Ratky J, Rodriguez-Martinez H. Fertilization and early embryonic development in the porcine fallopian tube. Reprod Domest Anim. 2008;43(Suppl 2):245–251
  13. Ellington JE. The bovine oviduct and its role in reproduction: a review of the literature. Cornell Vet. 1991;81:313–328
  14. Hugentobler SA, Humpherson PG, Leese HJ, Sreenan JM, Morris DG. Energy substrates in bovine oviduct and uterine fluid and blood plasma during the oestrous cycle. Mol Reprod Dev. 2008;75:496–503
  15. Hugentobler SA, Diskin MG, Leese HJ, Humpherson PG, Watson T, Sreenan JM, et al. Amino acids in oviduct and uterine fluid and blood plasma during the estrous cycle in the bovine. Mol Reprod Dev. 2007;74:445–454
  16. Buhi WC, Alvarez IM, Kouba AJ. Oviductal regulation of fertilization and early embryonic development. J Reprod Fertil Suppl. 1997;52:285–300
  17. Watson AJ, Westhusin ME, Winger QA. IGF paracrine and autocrine interactions between conceptus and oviduct. J Reprod Fertil Suppl. 1999;54:303–315
  18. Winger QA, de los RP, Han VK, Armstrong DT, Hill DJ, Watson AJ. Bovine oviductal and embryonic insulin-like growth factor binding proteins: possible regulators of “embryotrophic” insulin-like growth factor circuits. Biol Reprod. 1997;56:1415–1423
  19. Xia P, Han VK, Viuff D, Armstrong DT, Watson AJ. Expression of insulin-like growth factors in two bovine oviductal cultures employed for embryo co-culture. J Endocrinol. 1996;149:41–53
  20. Lei ZM, Rao CV. Expression of epidermal growth factor (EGF) receptor and its ligands. EGF and transforming growth factor-alpha, in human fallopian tubes. Endocrinology. 1992;131:947–957
  21. Thibodeaux JK, Del Vecchio RP, Hansel W. Role of platelet-derived growth factor in development of in vitro matured and in vitro fertilized bovine embryos. J Reprod Fertil. 1993;98:61–66
  22. Gabler C, Plath-Gabler A, Einspanier A, Einspanier R. Insulin-like and fibroblast growth factors and their receptors are differentially expressed in the oviducts of the common marmoset monkey (Callithrix jacchus) during the ovulatory cycle. Biol Reprod. 1998;58:1451–1457
  23. Einspanier R, Gabler C, Bieser B, Einspanier A, Berisha B, Kosmann M, et al. Growth factors and extracellular matrix proteins in interactions of cumulus-oocyte complex, spermatozoa and oviduct. J Reprod Fertil Suppl. 1999;54:359–365
  24. Gandolfi F. Functions of proteins secreted by oviduct epithelial cells. Microsc Res Tech. 1995;32:1–12
  25. Rosselli M, Imthurn B, Macas E, Keller PJ. Endothelin production by bovine oviduct epithelial cells. J Reprod Fertil. 1994;101:27–30
  26. Reinhart KC, Dubey RK, Cometti B, Keller PJ, Rosselli M. Differential effects of natural and environmental estrogens on endothelin synthesis in bovine oviduct cells. Biol Reprod. 2003;68:1430–1436
  27. Rosselli M, Dubey RK, Rosselli MA, Macas E, Fink D, Lauper U, et al. Identification of nitric oxide synthase in human and bovine oviduct. Mol Hum Reprod. 1996;2:607–612
  28. Ulbrich SE, Kettler A, Einspanier R. Expression and localization of estrogen receptor alpha, estrogen receptor beta and progesterone receptor in the bovine oviduct in vivo and in vitro. J Steroid Biochem Mol Biol. 2003;84:279–289
  29. Wijayagunawardane MP, Kodithuwakku SP, Yamamoto D, Miyamoto A. Vascular endothelial growth factor system in the cow oviduct: a possible involvement in the regulation of oviductal motility and embryo transport. Mol Reprod Dev. 2005;72:511–520
  30. Wijayagunawardane MP, Miyamoto A, Cerbito WA, Acosta TJ, Takagi M, Sato K. Local distributions of oviductal estradiol, progesterone, prostaglandins, oxytocin and endothelin-1 in the cyclic cow. Theriogenology. 1998;49:607–618
  31. Odau S, Gabler C, Holder C, Einspanier R. Differential expression of cyclooxygenase 1 and cyclooxygenase 2 in the bovine oviduct. J Endocrinol. 2006;191:263–274
  32. Harvey MB, Rcellana-Panlilio MY, Zhang X, Schultz GA, Watson AJ. Expression of genes encoding antioxidant enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo coculture. Biol Reprod. 1995;53:532–540
  33. Cheong AW, Lee YL, Liu WM, Yeung WS, Lee KF. Oviductal microsomal epoxide hydrolase (EPHX1) reduces reactive oxygen species (ROS) level and enhances preimplantation mouse embryo development. Biol Reprod. 2009;81:126–132
  34. Bauersachs S, Rehfeld S, Ulbrich SE, Mallok S, Prelle K, Wenigerkind H, et al. Monitoring gene expression changes in bovine oviduct epithelial cells during the oestrous cycle. J Mol Endocrinol. 2004;32:449–466
  35. Seytanoglu A, Georgiou AS, Sostaric E, Watson PF, Holt WV, Fazeli A. Oviductal cell proteome alterations during the reproductive cycle in pigs. J Proteome Res. 2008;7:2825–2833
  36. Sostaric E, Georgiou AS, Wong CH, Watson PF, Holt WV, Fazeli A. Global profiling of surface plasma membrane proteome of oviductal epithelial cells. J Proteome Res. 2006;5:3029–3037
  37. Georgiou AS, Sostaric E, Wong CH, Snijders AP, Wright PC, Moore HD, et al. Gametes alter the oviductal secretory proteome. Mol Cell Proteomics. 2005;4:1785–1796
  38. Ellington JE, Evenson DP, Wright RW, Jones AE, Schneider CS, Hiss GA, et al. Higher-quality human sperm in a sample selectively attach to oviduct (fallopian tube) epithelial cells in vitro. Fertil Steril. 1999;71:924–929
  39. De Pauw I, Van Soom A, Laevens H, Verberckmoes S, de Kruif A. Sperm binding to epithelial oviduct explants in bulls with different nonreturn rates investigated with a new in vitro model. Biol Reprod. 2002;67:1073–1079
  40. Boilard M, Bailey J, Collin S, Dufour M, Sirard MA. Effect of bovine oviduct epithelial cell apical plasma membranes on sperm function assessed by a novel flow cytometric approach. Biol Reprod. 2002;67:1125–1132
  41. Hunter RH. Reflections upon sperm-endosalpingeal and sperm-zona pellucida interactions in vivo and in vitro. Reprod Domest Anim. 2003;38:147–154
  42. Talevi R, Gualtieri R. In vivo versus in vitro fertilization. Eur J Obstet Gynecol Reprod Biol. 2004;115(Suppl 1):S68–S71
  43. Sostaric E, Dieleman SJ, van de Lest CH, Colenbrander B, Vos PL, Garcia-Gil N, et al. Sperm binding properties and secretory activity of the bovine oviduct immediately before and after ovulation. Mol Reprod Dev. 2008;75:60–74
  44. Lee KF, Yeung WS. Gamete/embryo-oviduct interactions: implications on in vitro culture. Hum Fertil (Camb). 2006;9:137–143
  45. Weber JA, Freeman DA, Vanderwall DK, Woods GL. Prostaglandin E2 hastens oviductal transport of equine embryos. Biol Reprod. 1991;45:544–546
  46. Freeman DA, Woods GL, Vanderwall DK, Weber JA. Embryo-initiated oviductal transport in mares. J Reprod Fertil. 1992;95:535–538
  47. Ortiz ME, Bedregal P, Carvajal MI, Croxatto HB. Fertilized and unfertilized ova are transported at different rates by the hamster oviduct. Biol Reprod. 1986;34:777–781
  48. Wetscher F, Havlicek V, Huber T, Muller M, Brem G, Besenfelder U. Effect of morphological properties of transferred embryonic stages on tubal migration Implications for in vivo culture in the bovine oviduct. Theriogenology. 2005;64:41–48
  49. Kolle S, Dubielzig S, Reese S, Wehrend A, Konig P, Kummer W. Ciliary transport, gamete interaction, and effects of the early embryo on the oviduct: ex vivo analyses using a new digital videomicroscopic system in the cow. Biol Reprod. 2009;81:267–274
  50. Fazeli A, Affara NA, Hubank M, Holt WV. Sperm-induced modification of the oviductal gene expression profile after natural insemination in mice. Biol Reprod. 2004;71:60–65
  51. Spencer TE, Bazer FW. Conceptus signals for establishment and maintenance of pregnancy. Reprod Biol Endocrinol. 2004;2:49–64
  52. Robinson RS, Fray MD, Wathes DC, Lamming GE, Mann GE. In vivo expression of interferon tau mRNA by the embryonic trophoblast and uterine concentrations of interferon tau protein during early pregnancy in the cow. Mol Reprod Dev. 2006;73:470–474
  53. Bauersachs S, Ulbrich SE, Gross K, Schmidt SE, Meyer HH, Einspanier R, et al. Gene expression profiling of bovine endometrium during the oestrous cycle: detection of molecular pathways involved in functional changes. J Mol Endocrinol. 2005;34:889–908
  54. Mitko K, Ulbrich SE, Wenigerkind H, Sinowatz F, Blum H, Wolf E, et al. Dynamic changes in messenger RNA profiles of bovine endometrium during the oestrous cycle. Reproduction. 2008;135:225–240
  55. Bauersachs S, Ulbrich SE, Gross K, Schmidt SE, Meyer HH, Wenigerkind H, et al. Embryo-induced transcriptome changes in bovine endometrium reveal species-specific and common molecular markers of uterine receptivity. Reproduction. 2006;132:319–331
  56. Klein C, Bauersachs S, Ulbrich SE, Einspanier R, Meyer HH, Schmidt SE, et al. Monozygotic twin model reveals novel embryo-induced transcriptome changes of bovine endometrium in the preattachment period. Biol Reprod. 2006;74:253–264
  57. Berendt FJ, Frohlich T, Schmidt SE, Reichenbach HD, Wolf E, Arnold GJ. Holistic differential analysis of embryo-induced alterations in the proteome of bovine endometrium in the preattachment period. Proteomics. 2005;5:2551–2560
  58. Bauersachs S, Ulbrich SE, Zakhartchenko V, Minten M, Reichenbach M, Reichenbach HD, et al. The endometrium responds differently to cloned versus fertilized embryos. Proc Natl Acad Sci U S A. 2009;106(14):5681–5686
  59. Thatcher WW, Guzeloglu A, Mattos R, Binelli M, Hansen TR, Pru JK. Uterine-conceptus interactions and reproductive failure in cattle. Theriogenology. 2001;56:1435–1450
  60. Bauersachs S, Blum H, Mallok S, Wenigerkind H, Rief S, Prelle K, et al. Regulation of ipsilateral and contralateral bovine oviduct epithelial cell function in the postovulation period: a transcriptomics approach. Biol Reprod. 2003;68:1170–1177
  61. Kodithuwakku SP, Miyamoto A, Wijayagunawardane MP. Spermatozoa stimulate prostaglandin synthesis and secretion in bovine oviductal epithelial cells. Reproduction. 2007;133:1087–1094
  62. Gabler C, Odau S, Muller K, Schon J, Bondzio A, Einspanier R. Exploring cumulus-oocyte-complex-oviductal cell interactions: gene profiling in the bovine oviduct. J Physiol Pharmacol. 2008;59(Suppl 9):29–42
  63. Wolf E, Arnold GJ, Bauersachs S, Beier HM, Blum H, Einspanier R, et al. Embryo-maternal communication in bovine—strategies for deciphering a complex cross-talk. Reprod Domest Anim. 2003;38:276–289
  64. McGee ZA, Johnson AP, Taylor-Robinson D. Human fallopian tubes in organ culture: preparation, maintenance, and quantitation of damage by pathogenic microorganisms. Infect Immun. 1976;13:608–618
  65. Stalheim OH, Proctor SJ, Gallagher JE. Growth and effects of ureaplasmas (T mycoplasmas) in bovine oviductal organ cultures. Infect Immun. 1976;13:915–925
  66. Biggers JD, Moore BD, Whittingham DG. Development of mouse embryos in vivo after cultivation from two-cell ova to blastocysts in vitro. Nature. 1965;206:734–735
  67. Rizos D, Clemente M, Bermejo-Alvarez P, de la FJ, Lonergan P, Gutierrez-Adan A. Consequences of in vitro culture conditions on embryo development and quality. Reprod Domest Anim. 2008;43(Suppl 4):44–50
  68. Havlicek V, Kuzmany A, Cseh S, Brem G, Besenfelder U. The effect of long-term in vivo culture in bovine oviduct and uterus on the development and cryo-tolerance of in vitro produced bovine embryos. Reprod Domest Anim. 2009;in press
  69. Gandolfi F, Moor RM. Stimulation of early embryonic development in the sheep by co-culture with oviduct epithelial cells. J Reprod Fertil. 1987;81:23–28
  70. Galli C, Moor RM. Co-culture: the future for embryo development in vitro. Acta Eur Fertil. 1989;20:231–235
  71. Gandolfi F, Brevini TA, Richardson L, Brown CR, Moor RM. Characterization of proteins secreted by sheep oviduct epithelial cells and their function in embryonic development. Development. 1989;106:303–312
  72. Verhage HG, Fazleabas AT, Donnelly K. The in vitro synthesis and release of proteins by the human oviduct. Endocrinology. 1988;122:1639–1645
  73. Boice ML, Geisert RD, Blair RM, Verhage HG. Identification and characterization of bovine oviductal glycoproteins synthesized at estrus. Biol Reprod. 1990;43:457–465
  74. Buhi WC. Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein. Reproduction. 2002;123:355–362
  75. Killian GJ. Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development. Anim Reprod Sci. 2004;82–83:141–153
  76. Coy P, Canovas S, Mondejar I, Saavedra MD, Romar R, Grullon L, et al. Oviduct-specific glycoprotein and heparin modulate sperm-zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc Natl Acad Sci U S A. 2008;105:15809–15814
  77. Joshi MS. Isolation, cell culture, and characterization of oviduct epithelial cells of the cow. Microsc Res Tech. 1995;31:507–518
  78. Joshi MS. Isolation, cell culture and immunocytochemical characterization of oviduct epithelial cells of the cow. J Reprod Fertil. 1988;83:249–261
  79. Joshi MS. Growth and differentiation of the cultured secretory cells of the cow oviduct on reconstituted basement membrane. J Exp Zool. 1991;260:229–238
  80. Ouhibi N, Menezo Y, Benet G, Nicollet B. Culture of epithelial cells derived from the oviduct of different species. Hum Reprod. 1989;4:229–235
  81. Gardner DK, Lane M. Ex vivo early embryo development and effects on gene expression and imprinting. Reprod Fertil Dev. 2005;17:361–370
  82. Fleming TP, Kwong WY, Porter R, Ursell E, Fesenko I, Wilkins A, et al. The embryo and its future. Biol Reprod. 2004;71:1046–1054
  83. Orsi NM, Reischl JB. Mammalian embryo co-culture: trials and tribulations of a misunderstood method. Theriogenology. 2007;67:441–458
  84. Haeusler G, Tempfer C, Lehner R, Sam C, Kainz C. Fallopian tissue sampling with a cytobrush during hysteroscopy: a new approach for detecting tubal infection. Fertil Steril. 1997;67:580–582
  85. McCracken JA, Schramm W, Einer-Jensen N. The structure of steroids and their diffusion through blood vessel walls in a counter-current system. Steroids. 1984;43:293–303
  86. Stefanczyk-Krzymowska S, Krzymowski T. Local adjustment of blood and lymph circulation in the hormonal regulation of reproduction in female pigs—facts, conclusions and suggestions for future research. Reprod Biol. 2002;2:115–132
  87. Einer-Jensen N, Hunter R. Counter-current transfer in reproductive biology. Reproduction. 2005;129:9–18
  88. Rottmayer R, Ulbrich SE, Kolle S, Prelle K, Neumueller C, Sinowatz F, et al. A bovine oviduct epithelial cell suspension culture system suitable for studying embryo-maternal interactions: morphological and functional characterization. Reproduction. 2006;132:637–648
  89. Abe H. The mammalian oviductal epithelium: regional variations in cytological and functional aspects of the oviductal secretory cells. Histol Histopathol. 1996;11:743–768
  90. Yaniz JL, Lopez-Gatius F, Santolaria P, Mullins KJ. Study of the functional anatomy of bovine oviductal mucosa. Anat Rec. 2000;260:268–278
  91. Walter I, Miller I. S-100 protein subunits in bovine oviduct epithelium: in situ distribution and changes during primary cell culture. Histochem J. 1996;28:671–680
  92. Abe H, Onodera M, Sugawara S, Satoh T, Hoshi H. Ultrastructural features of goat oviductal secretory cells at follicular and luteal phases of the oestrous cycle. J Anat. 1999;195(Pt 4):515–521
  93. Suuroia T, Aunapuu M, Arend A, Sepp E. Light” epithelial cells of swine and bovine oviducts. Tsitologiia. 2002;44:656–660
  94. Einspanier R, Gabler C, Kettler A, Kloas W. Characterization and localization of beta2-adrenergic receptors in the bovine oviduct: indication for progesterone-mediated expression. Endocrinology. 1999;140:2679–2684
  95. Ulbrich SE, Schoenfelder M, Thoene S, Einspanier R. Hyaluronan in the bovine oviduct--modulation of synthases and receptors during the estrous cycle. Mol Cell Endocrinol. 2004;214:9–18
  96. Hiendleder S, Bauersachs S, Boulesteix A, Blum H, Arnold GJ, Frohlich T, et al. Functional genomics: tools for improving farm animal health and welfare. Rev Sci Tech. 2005;24:355–377
  97. Ireland JJ, Murphee RL, Coulson PB. Accuracy of predicting stages of bovine estrous cycle by gross appearance of the corpus luteum. J Dairy Sci. 1980;63:155–160
  98. Rief S, Sinowatz F, Stojkovic M, Einspanier R, Wolf E, Prelle K. Effects of a novel co-culture system on development, metabolism and gene expression of bovine embryos produced in vitro. Reproduction. 2002;124:543–556
  99. Wijayagunawardane MP, Cerbito WA, Miyamoto A, Acosta TJ, Takagi M, Miyazawa K, et al. Oviductal progesterone concentration and its spatial distribution in cyclic and early pregnant cows. Theriogenology. 1996;46:1149–1158
  100. Thibodeaux JK, Goodeaux LL, Roussel JD, Menezo Y, Amborski GF, Moreau JD, et al. Effects of stage of the bovine oestrous cycle on in-vitro characteristics of uterine and oviductal epithelial cells. Hum Reprod. 1991;6:751–760
  101. Stojkovic M, Wolf E, Van LA, Vansteenbrugge A, Charpigny G, Reinaud P, et al. Correlations between chemical parameters, mitogenic activity and embryotrophic activity of bovine oviduct-conditioned medium. Theriogenology. 1997;48:659–673
  102. Thibodeaux JK, Menezo Y, Roussel JD, Hansel W, Goodeaux LL. Thompson DL Jr. Godke RA. ;1; Coculture of in vitro fertilized bovine embryos with oviductal epithelial cells originating from different stages of the estrous cycle. J Dairy Sci. 1992;75:1448–1455
  103. Bosch P, de Avila JM, Ellington JE, Wright RW. Heparin and Ca2+-free medium can enhance release of bull sperm attached to oviductal epithelial cell monolayers. Theriogenology. 2001;56:247–260
  104. Ellington JE, Jones AE, Davitt CM, Schneider CS, Brisbois RS, Hiss GA. Wright RW Jr. Human sperm function in co-culture with human, macaque or bovine oviduct epithelial cell monolayers. Hum Reprod. 1998;13:2797–2804
  105. Boquest AC, Summers PM. Effects of 17beta-oestradiol or oestrous stage-specific cow serum on the ability of bovine oviductal epithelial cell monolayers to prolong the viability of bull spermatozoa. Anim Reprod Sci. 1999;57:1–14
  106. Mishra S, Lei ZM, Rao C. A novel role of luteinizing hormone in the embryo development in cocultures. Biol Reprod. 2003;68:1455–1462
  107. 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
  108. Pegoraro LM, Thuard JM, Delalleau N, Guerin B, Deschamps JC, Marquant Le GB, et al. Comparison of sex ratio and cell number of IVM-IVF bovine blastocysts co-cultured with bovine oviduct epithelial cells or with Vero cells. Theriogenology. 1998;49:1579–1590
  109. Abe H, Hoshi H. Bovine oviductal epithelial cells: their cell culture and applications in studies for reproductive biology. Cytotechnology. 1997;23:171–183
  110. Lim JM, Reggio BC, Godke RA, Hansel W. Perifusion culture system for bovine embryos: improvement of embryo development by use of bovine oviduct epithelial cells, an antioxidant and polyvinyl alcohol. Reprod Fertil Dev. 1997;9:411–418
  111. Yadav PS, Saini A, Kumar A, Jain GC. Effect of oviductal cell co-culture on cleavage and development of goat IVF embryos. Anim Reprod Sci. 1998;51:301–306
  112. Kamishita H, Takagi M, Choi YH, Wijayagunawardane MP, Miyazawa K, Sato K. Development of in vitro matured and fertilized bovine embryos cocultured with bovine oviductal epithelial cells obtained from oviducts ipsilateral to cystic follicles. Anim Reprod Sci. 1999;56:201–209
  113. Gualtieri R, Talevi R. In vitro-cultured bovine oviductal cells bind acrosome-intact sperm and retain this ability upon sperm release. Biol Reprod. 2000;62:1754–1762
  114. Mann GE, Scholey DV, Robinson RS. Identification of elevated concentrations of estradiol in bovine uterine endometrium. Domest Anim Endocrinol. 2007;33:437–441
  115. Purpera MN, Giraldo AM, Ballard CB, Hylan D, Godke RA, Bondioli KR. Effects of culture medium and protein supplementation on mRNA expression of in vitro produced bovine embryos. Mol Reprod Dev. 2009;76(8):783–793
  116. Mermillod P, Vansteenbrugge A, Wils C, Mourmeaux JL, Massip A, Dessy F. Characterization of the embryotrophic activity of exogenous protein-free oviduct-conditioned medium used in culture of cattle embryos. Biol Reprod. 1993;49:582–587
  117. Van Langendonckt A, Vansteenbrugge A, Dessy-Doizé C, Flechon JE, Charpigny G, Mermillod P, et al. Characterization of bovine oviduct epithelial cell monolayers cultured under serum-free conditions. In Vitro Cell Dev Biol Anim. 1995;31:664–670
  118. Cox CI, Leese HJ. Retention of functional characteristics by bovine oviduct and uterine epithelia in vitro. Anim Reprod Sci. 1997;46:169–178
  119. Nutt-Scott TL, Harris C. Modulation of intracellular glutathione and cysteine metabolism in bovine oviduct epithelial cells cultured In vitro. Biol Reprod. 1998;59:314–320
  120. Reischl J, Prelle K, Schol H, Neumuller C, Einspanier R, Sinowatz F, et al. Factors affecting proliferation and dedifferentiation of primary bovine oviduct epithelial cells in vitro. Cell Tissue Res. 1999;296:371–383
  121. Berendt FJ, Frohlich T, Bolbrinker P, Boelhauve M, Gungor T, Habermann FA, et al. Highly sensitive saturation labeling reveals changes in abundance of cell cycle-associated proteins and redox enzyme variants during oocyte maturation in vitro. Proteomics. 2009;9:550–564
  122. Schoen J, Bondzio A, Topp K, Einspanier R. Establishment and characterization of an adherent pure epithelial cell line derived from the bovine oviduct. Theriogenology. 2008;69:536–545
  123. Walter I. Culture of bovine oviduct epithelial cells (BOEC). Anat Rec. 1995;243:347–356
  124. Comer MT, Leese HJ, Southgate J. Induction of a differentiated ciliated cell phenotype in primary cultures of Fallopian tube epithelium. Hum Reprod. 1998;13:3114–3120
  125. Lefebvre R, Chenoweth PJ, Drost M, LeClear CT, MacCubbin M, Dutton JT, et al. Characterization of the oviductal sperm reservoir in cattle. Biol Reprod. 1995;53:1066–1074
  126. Thibodeaux JK, Myers MW, Goodeaux LL, Menezo Y, Roussel JD, Broussard JR, et al. Evaluating an in vitro culture system of bovine uterine and oviduct epithelial cells for subsequent embryo co-culture. Reprod Fertil Dev. 1992;4:573–583
  127. Baillie HS, Pacey AA, Warren MA, Scudamore IW, Barratt CL. Greater numbers of human spermatozoa associate with endosalpingeal cells derived from the isthmus compared with those from the ampulla. Hum Reprod. 1997;12:1985–1992
  128. Briton-Jones C, Lok IH, Yuen PM, Chiu TT, Cheung LP, Haines C. Human oviductin mRNA expression is not maintained in oviduct mucosal cell culture. Fertil Steril. 2002;77:576–580
  129. Briton-Jones C, Lok IH, Cheung CK, Chiu TT, Cheung LP, Haines C. Estradiol regulation of oviductin/oviduct-specific glycoprotein messenger ribonucleic acid expression in human oviduct mucosal cells in vitro. Fertil Steril. 2004;81(Suppl 1):749–756
  130. Leese HJ, Tay JI, Reischl J, Downing SJ. Formation of fallopian tubal fluid: role of a neglected epithelium. Reproduction. 2001;121:339–346
  131. Lapointe J, Kimmins S, MacLaren LA, Bilodeau JF. Estrogen selectively up-regulates the phospholipid hydroperoxide glutathione peroxidase in the oviducts. Endocrinology. 2005;146:2583–2592
  132. Kohler PO, O’Malley BW. Estrogen-induced morphologic changes in monolayer cultures of immature chick oviduct. Endocrinology. 1967;81:1422–1427
  133. O’Malley BW, Kohler PO. Studies on steroid regulation of synthesis of a specific oviduct protein in a new monolayer culture system. Proc Natl Acad Sci U S A. 1967;58:2359–2366
  134. 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
  135. Wijayagunawardane MP, Choi YH, Miyamoto A, Kamishita H, Fujimoto S, Takagi M, et al. Effect of ovarian steroids and oxytocin on the production of prostaglandin E2, prostaglandin F2alpha and endothelin-1 from cow oviductal epithelial cell monolayers in vitro. Anim Reprod Sci. 1999;56:11–17
  136. Monkkonen KS, Aflatoonian R, Lee KF, Yeung WS, Tsao SW, Laitinen JT, et al. Hormonal regulation of Galphai2 and mPRalpha in immortalized human oviductal cell line OE-E6/E7. Mol Hum Reprod. 2007;13:845–851
  137. Petersen DD, Koch SR, Granner DK. 3’ Noncoding region of phosphoenolpyruvate carboxykinase mRNA contains a glucocorticoid-responsive mRNA-stabilizing element. Proc Natl Acad Sci U S A. 1989;86:7800–7804
  138. Ellington JE, Farrell PB, Simkin ME, Foote RH, Goldman EE, McGrath AB. Development and survival after transfer of cow embryos cultured from 1-2-cells to morulae or blastocysts in rabbit oviducts or in a simple medium with bovine oviduct epithelial cells. J Reprod Fertil. 1990;89:293–299
  139. Gandolfi F, Brevini TA, Moor RM. Effect of oviduct environment on embryonic development. J Reprod Fertil Suppl. 1989;38:107–115
  140. Nancarrow CD, Hill JL. Co-culture, oviduct secretion and the function of oviduct-specific glycoproteins. Cell Biol Int. 1994;18:1105–1114
  141. Thompson JG. In vitro culture and embryo metabolism of cattle and sheep embryos—a decade of achievement. Anim Reprod Sci. 2000;60–61:263–275
  142. Vanroose G, Van Soom A, de Kruif A. From co-culture to defined medium: state of the art and practical considerations. Reprod Domest Anim. 2001;36:25–28
  143. Ellington JE, Carney EW, Farrell PB, Simkin ME, Foote RH. Bovine 1-2-cell embryo development using a simple medium in three oviduct epithelial cell coculture systems. Biol Reprod. 1990;43:97–104
  144. Ouhibi N, Hamidi J, Guillaud J, Menezo Y. Co-culture of 1-cell mouse embryos on different cell supports. Hum Reprod. 1990;5:737–743
  145. Takeuchi K, Nagata Y, Sandow BA, Hodgen GD. Primary culture of human fallopian tube epithelial cells and co-culture of early mouse pre-embryos. Mol Reprod Dev. 1992;32:236–242
  146. Liu LP, Chan ST, Ho PC, Yeung WS. Human oviductal cells produce high molecular weight factor(s) that improves the development of mouse embryo. Hum Reprod. 1995;10:2781–2786
  147. Wiemer KE, Hoffman DI, Maxson WS, Eager S, Muhlberger B, Fiore I, et al. Embryonic morphology and rate of implantation of human embryos following co-culture on bovine oviductal epithelial cells. Hum Reprod. 1993;8:97–101
  148. Feng HL, Wen XH, Presser SC. Effect of different co-culture systems in early human embryo development. Hum Reprod. 1996;11:1525–1528
  149. Goto K, Kajihara Y, Kosaka S, Koba M, Nakanishi Y, Ogawa K. Pregnancies after co-culture of cumulus cells with bovine embryos derived from in-vitro fertilization of in-vitro matured follicular oocytes. J Reprod Fertil. 1988;83:753–758
  150. Rehman N, Collins AR, Suh TK, Wright RW. Development of IVM-IVF produced 8-cell bovine embryos in simple, serum-free media after conditioning or co-culture with buffalo rat liver cells. Mol Reprod Dev. 1994;38:251–255
  151. Eyestone WH, First NL. Co-culture of early cattle embryos to the blastocyst stage with oviducal tissue or in conditioned medium. J Reprod Fertil. 1989;85:715–720
  152. McCaffrey C, McEvoy TG, Diskin MG, Gwazdauskas FC, Kane MT, Sreenan JM. Successful co-culture of 1-4-cell cattle ova to the morula or blastocyst stage. J Reprod Fertil. 1991;92:119–124
  153. Hunter RH, Einer-Jensen N, Greve T. Somatic cell amplification of early pregnancy factors in the fallopian tube. Ital J Anat Embryol. 2005;110:195–203
  154. Hofmann A, Zakhartchenko V, Weppert M, Sebald H, Wenigerkind H, Brem G, et al. Generation of transgenic cattle by lentiviral gene transfer into oocytes. Biol Reprod. 2004;71:405–409
  155. Wuensch A, Habermann FA, Kurosaka S, Klose R, Zakhartchenko V, Reichenbach HD, et al. Quantitative monitoring of pluripotency gene activation after somatic cloning in cattle. Biol Reprod. 2007;76:983–991
  156. Habermann FA, Wuensch A, Sinowatz F, Wolf E. Reporter genes for embryogenesis research in livestock species. Theriogenology. 2007;68(Suppl 1):S116–S124
  157. Mansouri-Attia N, Sandra O, Aubert J, Degrelle S, Everts RE, Giraud-Delville C, et al. Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc Natl Acad Sci U S A. 2009;106:5687–5692

PII: S0093-691X(09)00470-1

doi: 10.1016/j.theriogenology.2009.09.036

Theriogenology
Volume 73, Issue 6 , Pages 802-816 , 1 April 2010