Theriogenology
Volume 73, Issue 6 , Pages 777-785 , 1 April 2010

Culture of bovine embryos in intermediate host oviducts with emphasis on the isolated mouse oviduct

  • D. Rizos

      Affiliations

    • Departamento de Reproducción Animal y Conservación de Recursos Zoogenéticos, INIA, Madrid, Spain
    • Corresponding Author InformationCorresponding author. Tel.: +34 913474045; fax: +34 913474014.
  • ,
  • M.A. Ramirez

      Affiliations

    • Departamento de Reproducción Animal y Conservación de Recursos Zoogenéticos, INIA, Madrid, Spain
  • ,
  • B. Pintado

      Affiliations

    • Departamento de Reproducción Animal y Conservación de Recursos Zoogenéticos, INIA, Madrid, Spain
  • ,
  • P. Lonergan

      Affiliations

    • School of Agriculture, Food Science and Veterinary Medicine, College of Life Sciences, University College Dublin, Dublin, Ireland
  • ,
  • A. Gutierrez-Adan

      Affiliations

    • Departamento de Reproducción Animal y Conservación de Recursos Zoogenéticos, INIA, Madrid, Spain

Received 1 April 2009 ,Accepted 27 August 2009.

References 

  1. Hunter RHF. The Fallopian Tubes: Their Role in Fertility and Infertility. Berlin: Springer-Verlag; 1988;
  2. Hackett AJ, Durnford R, Mapletoft RJ, Marcus GJ. Location and status of embryos in the genital tract of superovulated cows 4 to 6 days after insemination. Theriogenology. 1993;40:1147–1153
  3. Boni R, Tosti E, Roviello S, Dale B. Intercellular communication in in vivo and in vitro produced bovine embryos. Biol Reprod. 1999;61:1050–1055
  4. van Soom A, Ysebaert MT, de Kruif A. Relationship between timing of development, morula morphology, and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos. Mol Reprod Dev. 1997;47:47–56
  5. Iritani A, Niwa K. Capacitation of bull spermatozoa and fertilization in vitro of cattle follicular oocytes matured in culture. J Reprod Fertil. 1977;50:119–121
  6. Brackett BG, Bousquet D, Boice ML, Donawick WJ, Evans JF, Dressel MA. Normal development following in vitro fertilization in the cow. Biol Reprod. 1982;27:147–158
  7. Lambert RD, Sirard MA, Bernard C, Beland R, Rioux JE, Leclert P, et al. In vitro fertilization of bovine oocytes matured in vivo and collected at laparoscopy. Theriogenology. 1986;25:117–133
  8. Hanada A, Enya Y, Suzuki T. Birth of calves by non-surgical transfer of in vitro fertilised embryos obtained from oocytes matured in vitro. Jpn J Anim Reprod. 1986;32:208
  9. Lu KH, Gordon I, Gallagher M, McGovern H. Pregnancy established in cattle by transfer of embryos derived from in vitro fertilisation of oocytes matured in vitro. Vet Rec. 1987;121:259–260
  10. Thibier M. The worldwide activity in farm animals embryo transfer. International Embryo Transfer Society Newsletter 2008;December:4–9.
  11. Galli C, Lazzari G. Practical aspects of IVM/IVF in cattle. Anim Reprod Sci. 1996;42:371–379
  12. Enright BP, Lonergan P, Dinnyes A, Fair T, Ward FA, Yang X, et al. Culture of in vitro produced bovine zygotes in vitro vs in vivo: implications for early embryo development and quality. Theriogenology. 2000;54:659–673
  13. Rizos D, Ward F, Duffy P, Boland MP, Lonergan P. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev. 2002;61:234–248
  14. Rizos D, Lonergan P, Boland MP, Arroyo-Garcia R, Pintado B, de la Fuente J, et al. Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality. Biol Reprod. 2002;66:589–595
  15. Rizos D, Gutierrez-Adan A, Perez-Garnelo S, De La Fuente J, Boland MP, Lonergan P. Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression. Biol Reprod. 2003;68:236–243
  16. Lonergan P, Rizos D, Gutierrez-Adan A, Fair T, Boland MP. Effect of culture environment on embryo quality and gene expression—experience from animal studies. Reprod Biomed Online. 2003;7:657–663
  17. Lonergan P, Fair T, Corcoran D, Evans AC. Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos. Theriogenology. 2006;65:137–152
  18. Wrenzycki C, Herrmann D, Lucas-Hahn A, Korsawe K, Lemme E, Niemann H, et al. expression patterns in bovine embryos derived from in vitro procedures and their implications for development. Reprod Fertil Dev. 2005;17:23–35
  19. Sreenan JM, Scanlon P, Gordon I. Culture of fertilised cattle eggs. J Agric Sci. 1968;70:183–185
  20. Lawson RA, Adams CE, Rowson LE. The development of sheep eggs in the rabbit oviduct and their viability after re-transfer to ewes. J Reprod Fertil. 1972;29:105–116
  21. Polge C, Adams CE, Baker RD. Development and survival of pig embryos in the rabbit oviduct. In: Proceedings of 7th ICAR Congress, 6–9 June 1972, Munich, Germany, pp. 513–517.
  22. Boland MP. Use of the rabbit oviduct as a screening tool for the viability of mammalian eggs. Theriogenology. 1984;21:126–137
  23. Prather RS, Sims MM, First NL. Culture of porcine embryos from the one- and two-cell stage to the blastocyst stage in sheep oviducts. Theriogenology. 1991;35:1147–1151
  24. Eyestone WH, Leibfried-Rutledge ML, Northey DL, Gilligan BG, First NL. Culture of one- and two-cell bovine embryos to the blastocyst stage in the ovine oviduct. Theriogenology. 1987;28:1–7
  25. 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
  26. Biggers JD, Gwatkin RB, Brinster RL. Development of mouse embryos in organ cultures of fallopian tubes on a chemically defined medium. Nature. 1962;194:747–749
  27. Papaioanou VE, Ebert KM. Development of fertilized embryos transferred to oviducts of immature mice. J Reprod Fertil. 1986;76:603–608
  28. Whittingham DG. Development of zygotes in cultured mouse oviducts. I. The effect of varying oviductal conditions. J Exp Zool. 1968;169:391–397
  29. Whittingham DG. Intra- and inter-specific transfer of ova between explanted rat and mouse oviducts. J Reprod Fertil. 1968;17:575–578
  30. Minami N, Bavister BD, Iritani A. Development of hamster two-cell embryos in the isolated mouse oviduct in organ culture system. Gamete Res. 1988;19:235–240
  31. Krisher RL, Petters RM, Johnson BH, Bavister BD, Archibong AE. Development of porcine embryos from the one-cell stage to blastocyst in mouse oviducts maintained in organ culture. J Exp Zool. 1989;249:235–239
  32. Chung BH, Chung HM, Uhm SJ, Chang WK, Seung KR, Lee HT, et al. Organ culture of in vitro produced porcine embryos from follicular oocytes using mouse oviduct. Theriogenology. 1994;41:178
  33. Sharif H, Lonergan P, Monaghan P, Gallagher M, Gordon I., Comparison of bovine embryonic development in an isolated mouse oviduct culture system with bovine oviductal epithelial cell co-culture. In: 12th International Congress on Animal Reproduction (ICAR), The Hague, 1992, p. 389.
  34. Sharif H, Lonergan P, Monaghan P, Wahid H, Gallagher M, Gordon I. Development of early bovine embryos in isolated mouse oviducts maintained in organ culture under two gas atmospheres. Theriogenology. 1992;37:279
  35. Sharif H, Lonergan P, Monaghan P, Wahid H, Gallagher M, Gordon I. Early bovine embryonic development in cultured mouse oviduct obtained at various stage of the oestrous cycle. In: Proceedings of the 7th Meeting of the European Embryo Transfer Association, Cambridge, 1991, p. 206.
  36. Sharif H, Lonergan P, Monaghan P, Wahid HA, Gallagher M, Gordon I. Effect of oviductal condition on the development of early bovine embryos in cultured mouse oviducts. J Reprod Fertil. 1991;57:103
  37. Sharif H, Vergos E, Lonergan P, Gallagher M, Kinis A, Gordon I. Development of early bovine embryos in the isolated mouse oviduct maintained in organ culture. Theriogenology. 1991;35:270
  38. Hosoi Y, Minami N, Iritani A. Embryo culture in explanted oviducts in mice and cattle. Horm Res. 1995;44:9–14
  39. Rizos D, Pintado B, de la Fuente J, Lonergan P, Gutierrez-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
  40. Ellington JE. The bovine oviduct and its role in reproduction: a review of the literature. Cornell Vet. 1991;81:313–328
  41. Leese HJ. Human embryo culture: back to nature. J Assist Reprod Genet. 1998;15:466–468
  42. 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
  43. Leese HJ, Tay JI, Reischl J, Downing SJ. Formation of fallopian tubal fluid: role of a neglected epithelium. Reproduction. 2001;121:339–346
  44. Miller JGO, Schultz GA. Amino acid content of preimplantation rabbit embryos and fluids of the reproductive tract. Biol Reprod. 1987;36:125–129
  45. Nichol R, Hunter RH, Gardner DK, Leese HJ, Cooke GM. Concentrations of energy substrates in oviductal fluid and blood plasma of pigs during the peri-ovulatory period. J Reprod Fertil. 1992;96:699–707
  46. Dickens CJ, Maguiness SD, Comer MT, Palmer A, Rutherford AJ, Leese HJ. Human tubal fluid: formation and composition during vascular perfusion of the fallopian tube. Hum Reprod. 1995;10:505–508
  47. Boatman DE. Responses of gametes to the oviductal environment. Hum Reprod. 1997;12:133–149
  48. Tay JI, Rutherford AJ, Killick SR, Maguiness SD, Partridge RJ, Leese HJ. Human tubal fluid: production, nutrient composition and response to adrenergic agents. Hum Reprod. 1997;12:2451–2456
  49. Bergqvist AS, Yokoo M, Heldin P, Frendin J, Sato E, Rodriguez-Martinez H. Hyaluronan and its binding proteins in the epithelium and intraluminal fluid of the bovine oviduct. Zygote. 2005;13:207–218
  50. 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
  51. 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
  52. Hugentobler SA, Morris DG, Sreenan JM, Diskin MG. Ion concentrations in oviduct and uterine fluid and blood serum during the estrous cycle in the bovine. Theriogenology. 2007;68:538–548
  53. Roberts GP, Parker JM, Symonds HW. Proteins in the luminal fluid from the bovine oviduct. J Reprod Fertil. 1975;45:301–313
  54. Hunter RH. Modulation of gamete and embryonic microenvironments by oviduct glycoproteins. Mol Reprod Dev. 1994;39:176–181
  55. Mastroianni L, Jones R. Oxygen tension within the rabbit fallopian tube. J Reprod Fertil. 1965;9:99–102
  56. Bavister BD. Culture of preimplantation embryos: facts and artifacts. Hum Reprod Update. 1995;1:91–148
  57. Fischer B, Bavister BD. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil. 1993;99:673–679
  58. Averill RL, Adams CE, Rowson LE. Transfer of mammalian ova between species. Nature. 1955;176:167–168
  59. Ectors FJ, Thonon F, Delval A, Fontes RS, Touati K, Beckers JF, et al. Comparison between culture of bovine embryos in vitro versus development in rabbit oviducts and in vivo. Livestock Prod Sci. 1993;36:29–34
  60. Allen WR, Stewart F, Trounson AO, Tischner M, Bielanski W. Viability of horse embryos after storage and long-distance transport in the rabbit. J Reprod Fertil. 1976;47:387–390
  61. Gutierrez-Adan A, Behboodi E, Andersen GB, Medrano JF, Murray JD. Relationship between stage of development and sex of bovine IVM-IVF embryos cultured in vitro versus in the sheep oviduct. Theriogenology. 1996;46:515–525
  62. Lonergan P, Rizos D, Gutierrez-Adan A, Moreira PM, Pintado B, de la Fuente J, et al. Temporal divergence in the pattern of messenger RNA expression in bovine embryos cultured from the zygote to blastocyst stage in vitro or in vivo. Biol Reprod. 2003;69:1424–1431
  63. Besenfelder U, Brem G. Tubal transfer of bovine embryos: a simple endoscopic method reducing long-term exposure of in vitro produced embryos. Theriogenology. 1998;50:739–745
  64. Besenfelder U, Havlicek V, Mosslacher G, Brem G. Collection of tubal stage bovine embryos by means of endoscopy. A technique report. Theriogenology. 2001;55:837–845
  65. Wetscher F, Havlicek V, Huber T, Gilles M, Tesfaye D, Griese J, et al. Intrafallopian transfer of gametes and early stage embryos for in vivo culture in cattle. Theriogenology. 2005;64:30–40
  66. Hafez ESE, Sugie T. Reciprocal transfer of cattle and rabbit embryos. J Anim Sci. 1963;22:30
  67. Adams CE, Moor RM, Rowson LEA. Survival of cow and sheep eggs in the rabbit oviduct. In: 6th International Congress on Animal Reproduction and Artificial Insemination, Paris, 1968; pp. 573–574.
  68. Rowson LE, Moor RM, Lawson RA. Fertility following egg transfer in the cow; effect of method, medium and synchronization of oestrus. J Reprod Fertil. 1969;18:517–523
  69. Polge C, Rowson LEA. Recent progress in techniques for increasing reproductive potential in farm animals. In: 3rd World Conference on Animal Production, Sydney University Press, 1975, pp. 633-634.
  70. Hanada A. In vitro fertilisation in cattle, with particular reference to sperm capacitation by ionophore A23187. Jpn J Anim Prod. 1985;31:56–61
  71. Sirard MA, Lambert RD. In vitro fertilization of bovine follicular oocytes obtained by laparoscopy. Biol Reprod. 1985;33:487–494
  72. Ueda S, Kuwayama M, Shuioya Y, Handa A. Culture of in vitro fertilized bovine embryos in a chemically defined medium (BO-medium). Jpn J Anim Reprod 1988; 34:56–60.
  73. Hawk HW, Wall RJ, Conley HH. In vivo culture of pronuclear cow embryos injected with foreign DNA. J Anim Sci. 1988;66:407
  74. Jimenez C, Rumph N, Moore H, Walmsely S, Buckrell B, Pollard JW. Sheep intermediate recipient culture of in vitro produced bovine embryos: culture in ligated oviducts versus combined oviductal-uterine culture. Theriogenology. 2001;55:336
  75. Pugh A, Cox S, Peterson J, Ledgard A, Forsyth J, Cockrem K, et al. Culture of bovine embryos in sheep oviducts improves frozen but not fresh embryo survival. Theriogenology. 2001;55:314
  76. Lazzari G, Wrenzycki C, Herrmann D, Duchi R, Kruip T, Niemann H, et al. Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome. Biol Reprod. 2002;67:767–775
  77. Galli C, Duchi R, Lazzari G., Pregnancy rate following conventional or direct transfer of IVM-IVF cattle embryos grown into the sheep oviduct. In: 11th Meeting of the European Embryo Transfer Association, Hannover, 1995, p. 174.
  78. Hasler JF, Henderson WB, Hurtgen PJ, Lin ZQ, McCauley AD, Mower SA, et al. Production, freezing and transfer of bovine IVF embryos and subsequent calving results. 1995; 43:141-152.
  79. Nagy A, Gertsenstein M, Vintersten K, Behringer R. Manipulating the Mouse Embryo: A Laboratory Manual. 3rd edition. Cold Spring Harbor Laboratory Press; 2003;
  80. Capitan SS, Marshall VS, Wathes DC, Scaramuzzi RJ, Jabbour HN. Development of preimplantation sheep embryos in the oviduct of live mice. J Reprod Fertil. 1994;14:22–23
  81. Kim CH, Seo BB, Yamanouchi K, Sawasaki T, Hamano S, Tachi C, et al. In vivo culture of IVF-bovine embryos in murine oviducts. J Reprod Dev. 2000;46:409–414

PII: S0093-691X(09)00429-4

doi: 10.1016/j.theriogenology.2009.10.001

Theriogenology
Volume 73, Issue 6 , Pages 777-785 , 1 April 2010