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Embryo—Maternal Interactions after Diapause in a Marsupial

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Part of the book series: Proceedings in the Serono Symposia USA Series ((SERONOSYMP))

Abstract

In all mammals, development of the embryo depends on complex interactions with the uterus. In the most commonly used experimental animals, mice and rats, the development of the egg cylinder and the formation of the invasive placenta at implantation early in gestation complicate analysis, so that the signals passing between the uterus and mother in early pregnancy are not clearly defined. Marsupials, in contrast, remain free and unattached to the uterus for two thirds of gestation, surrounded by an acellular mucoid coat and keratinous shell that prevents direct cell—cell contact between the endometrium and trophoblast cells. Embryo development must therefore be controlled by soluble factors in the uterine secretions. This is seen very clearly in the control of embryonic diapause, which is characteristic of about 35 marsupial species (1). Almost all of these species belong to the family Macropodidae; the kangaroos and wallabies, but it is important to note that diapause does occur in at least two small possum families, the Burramyidae and Tarsipedidae (2).

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References

  1. Renfree MB, Calaby JH. Background to delayed implantation and embryonic diapause. J Reprod Fertil 1981;29 (Suppl):1–9.

    CAS  Google Scholar 

  2. Renfree MB. Embryonic diapause in marsupials. J Reprod Fertil 1981;29(Suppl): 67–8.

    CAS  Google Scholar 

  3. Rudd CD. Sexual behaviour of male and female tammar wallabies (Macropus eugenii) at post-partum oestrus. J Zool (Lond)1994;232:151–62.

    Article  Google Scholar 

  4. Renfree MB, Tyndale-Biscoe CH. Intrauterine development after diapause in the marsupial Macropus eugenii. Devel Biol 1973;22:29–40.

    Google Scholar 

  5. Tyndale-Biscoe CH. Hormonal control of embryonic diapause and reactivation in the tammar wallaby. In: Maternal recognition of pregnancy, Ciba Found Symp 64 (new series). Amsterdam: Excerpta Medica, 1979;173–90.

    Google Scholar 

  6. Tyndale-Biscoe CH, Renfree MB. Reproductive physiology of marsupials. Cambridge: Cambridge University Press, 1987:476.

    Book  Google Scholar 

  7. Renfree MB. Endocrinology of pregnancy, parturition and lactation of marsupials. In: Lamming GE, ed. Marshall’s physiology of reproduction. London: Chapman and Hall, 1994;677–766.

    Google Scholar 

  8. Hearn JP. Pituitary inhibition of pregnancy. Nature 1973;241:207–8.

    Article  PubMed  CAS  Google Scholar 

  9. Hinds LA. Pregnancy deferred: an unusual role for prolactin in a marsupial. In: Yoshinaga K, ed. Blastocyst implantation. Boston: Serono Symposia USA, Adams Publishing Group, 1989:201–7.

    Google Scholar 

  10. Hinds LA. Morning pulse of prolactin maintains seasonal quiescence in the tammar, Macropus eugenii. J Reprod Fertil 1989;87:735–44.

    Article  PubMed  CAS  Google Scholar 

  11. Tyndale-Biscoe CH, Hawkins J. The corpora lutea of marsupials, aspects of function and control, In: Calaby JH, Tyndale-Biscoe CH, eds. Reproduction and evolution, Australian Academy of Sciences, 1977:245–52.

    Google Scholar 

  12. Tyndale-Biscoe CH, Hearn JP. Pituitary and ovarian factors associated with seasonal quiescence in the tammar wallaby Macropus eugenii. J Reprod Fertil 1981;63:225–30.

    Article  PubMed  CAS  Google Scholar 

  13. Hinds LA, Tyndale-Biscoe H. Plasma progesterone levels in the pregnant and nonpregnant tammar, Macropus eugenii. J Endocrinol 1982;93:99–107.

    Article  PubMed  CAS  Google Scholar 

  14. Renfree MB, Green SW, Young IR. Growth of the corpus luteum and its progesterone content during pregnancy in the tammar wallaby, Macropus eugenii. J Reprod Fertil 1979;57:131–6.

    Article  PubMed  CAS  Google Scholar 

  15. Hinds LA, Tyndale-Biscoe H. Prolactin in the marsupial, Macropus eugenii during the estrous cycle, pregnancy and lactation. Biol Reprod 1982;26:391–8.

    Article  PubMed  CAS  Google Scholar 

  16. Sharman GB. Delayed implantation in marsupials. In: Enders AC, ed. Delayed implantation. Chicago: University of Chicago Press, 1963:3–14.

    Google Scholar 

  17. Tyndale-Biscoe CH, Hinds LA. Seasonal patterns of circulating progesterone and prolactin and response to bromocriptine in the female tammar, Macropus eugenii. Gen Endocrinol 1984;53:58–68.

    Article  CAS  Google Scholar 

  18. Renfree MB, Lincoln DW, Almeida OFX, Short RV. Abolition of seasonal embryonic diapause in the tammar wallaby by sympathetic denervation of the pineal gland. Nature (Lond) 1981;293:138–9.

    Article  CAS  Google Scholar 

  19. Renfree MB, Short RV. Seasonal reproduction in marsupials. In: Labrie F, Proulx L, eds. Proceedings of the 7’h International Congress of Endocrinology; Excerpta Medica International Congress Series. Amsterdam: Elsevier, 1984:789–92.

    Google Scholar 

  20. McConnell SJ, Hinds LA. Effect of pinealectomy on plasma melatonin, prolactin and progesterone concentrations during seasonal reproductive quiescence in the tammar. Macropus eugenii. J Reprod Fertil 1985;7:433–40.

    Google Scholar 

  21. McConnell SJ, Tyndale-Biseoe CH. Response to photoperiod in peripheral plasma melatonin and the effects of exogenous melatonin on seasonal quiescence in the tammar Macropus eugenii. J Reprod Fertil 1985;73:529–38.

    Article  Google Scholar 

  22. Fletcher TP, Renfree MB. Effects of corpus luteum removal on progesterone, oestradiol-1713 and LH in early pregnancy of the tammar wallaby Macropus eugenii. J Reprod Fertil 1988;83:185–91.

    Article  PubMed  CAS  Google Scholar 

  23. Fletcher TP, Jetton AE, Renfree MB. Influence of progesterone and oestradiol-170 on blastocysts of the tammar during seasonal diapause. J Reprod Fertil 1988;83: 193–200.

    Article  PubMed  CAS  Google Scholar 

  24. Tyndale-Biscoe CH. Resumption of development by quiescent blastocysts transferred to primed, ovariectomised recipients, in the marsupial Macropus eugenii. J Reprod Fertil 1970;23:25–32.

    Article  PubMed  CAS  Google Scholar 

  25. Renfree MB, Heap RB. Steroid metabolism in the placenta, corpus luteum, and endometrium of the marsupial Macropus eugenii. Theriogenology 1977;8:164.

    Article  CAS  Google Scholar 

  26. Heap RB, Renfree MB, Burton RD. Steroid metabolism in the yolk sac placenta and endometrium of the tammar wallaby, Macropus eugenii. J Endocrinol 1980;87: 339–49.

    Article  PubMed  CAS  Google Scholar 

  27. Shaw G, Renfree MB, Fletcher TP. A role for glucocorticoids in parturition in a marsupial, Macropus eugenii. Biol Reprod 1995;54:728–33.

    Article  Google Scholar 

  28. Renfree MB. Shaw G, Harry JL, Whitworth DJ. Sexual determination and differentiation in the marsupial Macropus eugenii. In: Saunders NA, Hinds LA, eds. Recent advances in marsupial biology. University of New South Wales Press, 1997:132–41.

    Google Scholar 

  29. Parry LJ, Rust W, Ivell R. Marsupial relaxin: complementary deoxyribonucleic acid sequence and gene expression in the female and male tammar wallaby, Macropus eugenii. Biol Reprod 1997;57:119–27.

    Article  PubMed  CAS  Google Scholar 

  30. Renfree MB, Lewis A. McD. Cleavage in vivo and in vitro in the marsupial Macropus eugenii. Reprod Fertil 1996;8:725–42.

    Article  CAS  Google Scholar 

  31. Hughes RL. Morphological studies on implantation in marsupials. J Reprod Fertil 1974;39:173–86.

    Article  PubMed  CAS  Google Scholar 

  32. Tyndale-Biscoe CH, Hinds LA. The hormonal milieu during early development in marsupials, In: Yoshinaga K, ed. Development of preimplantation embryos and their environment. New York: Liss, 1989:237–46.

    Google Scholar 

  33. Roberts CT, Breed WG, Mayrhofer G. Origin of the oocyte shell membrane of a dasyurid marsupial: an immunohistochemical study. J Exp Zool 1994;270:321–31.

    Article  PubMed  CAS  Google Scholar 

  34. Roberts CT, Breed WG. The Marsupial shell membrane: an ultrastructural and immunogold localization study. Cell Tissue Res 1996;284:99–110.

    Article  PubMed  CAS  Google Scholar 

  35. Shaw G. Pregnancy after diapause in the tammar wallaby, Macropus eugenii. PhD thesis, Murdoch University, Western Australia, 1983.

    Google Scholar 

  36. Renfree MB. Proteins in the uterine secretion of the marsupial Macropus eugenii. Devel Biol 1973;32:41–9.

    Article  CAS  Google Scholar 

  37. Renfree MB. Influence of the embryo on the marsupial uterus. Nature 1972;240: 475–7.

    Article  PubMed  CAS  Google Scholar 

  38. Shaw G, Renfree MB. Uterine and embryonic metabolism after embryonic diapause in the tammar wallaby (Macropus eugenii). J Reprod Fertil 1986; 76:339–47.

    Article  PubMed  CAS  Google Scholar 

  39. Shaw G. The uterine environment in early pregnancy in the tammar wallaby. Reprod Fertil Devel 1996;8:811–8.

    Article  CAS  Google Scholar 

  40. Young CE, McDonald IR. Oestrogen receptors in the genital tract of the Australian marsupial Trichosurus vulpecula. Gen Comp Endocrinol 1982;46:417–27.

    Article  PubMed  CAS  Google Scholar 

  41. Curlewis J, Stone GM. Effects of oestradiol, the oestrous cycle and pregnancy on weight, metabolism and cytosol receptors in the uterus of the brush-tail possum (Trichosurus vulpecula). J Endocrinol 1986;108:201–10.

    Article  PubMed  CAS  Google Scholar 

  42. O’Neill C. A consideration of the factors which influence the viability and developmental potential of the preimplantation embryo. Bailliere’s Clin Obstet Gynecol 1991;5: 159–78.

    Google Scholar 

  43. Roberts CC, Wright L. Platelet activating factor (PAF) enhances mitosis in preimplantation mouse embryos. Reprod Fertil Devel 1993;5:271–9.

    Article  CAS  Google Scholar 

  44. Kojima T, Hinds LA, Muller WJ, O’Neill C, Tyndale-Biscoe CH. Production and secretion of progesterone in vitro and presence of platelet activating factor (PAF) in early pregnancy of the marsupial, Macropus eugenii. Reprod Fertil Devel 1993;5: 15–25.

    Article  CAS  Google Scholar 

  45. Weitlauf HM. (1994) Biology of implantation. In: Knobil E, O’Neill JD, eds. The physiology of reproduction, 2nd ed. New York: Raven, 1994:391–440.

    Google Scholar 

  46. Surani MAH, Fishel SB. Embryonic and uterine factors in delayed implantation in rodents. J Reprod Fertil 1981;29(Suppl):159–72.

    CAS  Google Scholar 

  47. O’Neill C, Quinn P. Inhibitory influence of uterine flushings on mouse blastocysts decreases at the time of blastocyst activation. J Reprod Fertil 1983;68:269–74.

    Article  PubMed  Google Scholar 

  48. Thomber EJ, Renfree MB, Wallace GI. Biochemical studies of intrauterine components of tammar wallaby Macropus eugenii during pregnancy. J Embryol Exp Morphol 1981;62:325–38.

    Google Scholar 

  49. Spindler RE, Renfree MB, Gardner DK. Mouse embryos used as a bioassay to determine the control of marsupial embryonic diapause. Biol Reprod 1997;56(Suppl):1:379.

    Google Scholar 

  50. Sharman GB, Berger PJ. Embryonic diapause in marsupials. Adv Reprod Physiol 1969;4:211–40.

    Google Scholar 

  51. Gordon K, Fletcher TP, Renfree MB. Reactivation of the quiescent corpus luteum and diapausing embryo after temporary removal of the sucking stimulus in the tammar wallaby (Macropus eugenii). J Reprod Fertil 1988;83:401–6.

    Article  PubMed  CAS  Google Scholar 

  52. Spindler RE, Renfree MB, Gardner DK. Metabolic assessment of wallaby blastocysts during embryonic diapause and subsequent reactivation. Reprod Fertil Dev 1995;7:1157–62.

    Article  PubMed  CAS  Google Scholar 

  53. Moore GPM. Embryonic diapause in the marsupial Macropus eugenii. Stimulation of nuclear RNA polymerase activity during resumption of development. J Cell Physiol 1978;94:31–6.

    Article  PubMed  CAS  Google Scholar 

  54. Pike IL. Comparative studies of embryo metabolism in early pregnancy. J Reprod Fertil 1981;29(Suppl.):203–13.

    CAS  Google Scholar 

  55. Gardner DK, Lane M, Batt P. Uptake and metabolism of pyruvate and glucose by individual sheep preattachment embryos developed in vivo. Mol Reprod Devel 1993;36:313–9.

    Article  PubMed  CAS  Google Scholar 

  56. Denker HW, Tyndale-Biscoe CH. Embryo implantation and proteinase activities in a marsupial (Macropus eugenii). Cell Tissus Res 1986;246:279–91.

    Article  Google Scholar 

  57. Brigstock DR, Heap RB, Brown KD. Polypeptide growth factors in uterine tissues and secretions. J Reprod Fertil 1989;85:747–58.

    Article  PubMed  CAS  Google Scholar 

  58. Schultz GA, Heyner S. Growth factors in preimplantation mammalian embryos. Oxf Rev Reprod Biol 1993;15:43–81.

    PubMed  CAS  Google Scholar 

  59. Harvey MB, Leco KJ, Arcellana-Panlilio MY, Zhang X, Edwards DR, Schultz GA. Roles of growth factors during peri-implantation development. Hum Reprod 1995;10:712–8.

    PubMed  CAS  Google Scholar 

  60. Stewart CL, Kaspar P, Burnet L. Blastocyst implantation depends on natural expression of leukemia inhibitory factor. Nature 1992;359:76.

    Article  PubMed  CAS  Google Scholar 

  61. Bhatt H, Burnet L, Stewart C. Uterine expression of leukemia inhibitory factor coincides with the onset of blastocyst implantation. Proc Natl Acad Sci USA 1991;164: 956–9.

    Google Scholar 

  62. Nelson KG, Takahasi T, Bossert NL. Epidermal growth factor replaces estrogen in the stimulation of female genital tract growth and differentiation. Proc Natl Acad Sci USA 1991;622:383.

    Google Scholar 

  63. Harvey MB, Leco KJ, Arcellana-Panlilio MY, Zhang X, Edwards DR, Schultz GA. Proteinase expression in early mouse embryos is regulated by leukaemia inhibitory factor and epidermal growth factor. Development 1995;121:1005–14.

    PubMed  CAS  Google Scholar 

  64. Cake MH, Owen FJ, Bradshaw SD. Differences in concentration of progesterone in the plasma between pregnant and non-pregnant quokkas (Setonix brachyurus). J Endocrino! 1980;84:153–8.

    Article  CAS  Google Scholar 

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Renfree, M.B., Shaw, G. (1999). Embryo—Maternal Interactions after Diapause in a Marsupial. In: Carson, D.D. (eds) Embryo Implantation. Proceedings in the Serono Symposia USA Series. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-1548-6_5

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  • DOI: https://doi.org/10.1007/978-1-4612-1548-6_5

  • Publisher Name: Springer, New York, NY

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