Embryo-endometrial interactions during early development after embryonic diapause in the marsupial tammar wallaby

International Journal of Developmental Biology

Volumn 58, Issue 2-4, 2014, Pages 175-181

  Renfree, Marilyn B ^a   Shaw, Geoff ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Embryonic diapause; LIF; Marsupial; MSX; PAF

Indexed keywords

EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR; LEUKEMIA INHIBITORY FACTOR; PLATELET DERIVED GROWTH FACTOR; SOMATOMEDIN; THROMBOCYTE ACTIVATING FACTOR; THROMBOCYTE ACTIVATING FACTOR RECEPTOR; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR MSX2; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN;

ANIMAL EMBRYO; ARTICLE; BLASTOCYST; CORPUS LUTEUM; DOWN REGULATION; EMBRYO DEVELOPMENT; ENDOMETRIUM; ESTRUS CYCLE; GENE; GENE EXPRESSION; MACROPUS EUGENII; MSX1 GENE; MSX2 GENE; NONHUMAN; OVARY; PRIORITY JOURNAL; SECRETION (PROCESS); UPREGULATION; UTERUS; ANIMAL; DELAYED IMPLANTATION; EMBRYOLOGY; FEMALE; HUMAN; KANGAROO; METABOLISM; MOUSE; PHYSIOLOGY;

ANIMALS; EMBRYO IMPLANTATION, DELAYED; EMBRYO, MAMMALIAN; ENDOMETRIUM; FEMALE; HUMANS; MACROPODIDAE; MICE;

EID: 84904178731     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.140059mr     Document Type: Article

References (90)

1. AGER, E.I., PASK, A.J., SHAW, G. and RENFREE, M.B. (2008). Expression and protein localisation of IGF2 in the marsupial placenta. BMC Dev Biol 8: 17.
2. ARNOLD, R. and SHOREY, C.D. (1985). Structure of the uterine luminal epithelium of the brush-tailed possum (Trichosurus vulpecula). J Reprod Fertil 74: 565-573.
3. BHATT, H., BRUNET, L.J. and STEWART, C.L. (1991). Uterine expression of leukemia inhibitory factor coincides with the onset of blastocyst implantation. Proc Natl Acad Sci USA 88: 11408-11412.
4. CHA, J., SUN, X., BARTOS, A., FENELON, J., LEFEVRE, P., DAIKOKU, T., SHAW, G., MAXSON, R., MURPHY, B.D., RENFREE, M.B. et al., (2013). A new role for muscle segment homeobox genes in mammalian embryonic diapause. Open Biol 3: 130035.
5. CLARK, M. and POOLE, W. (1967). The reproductive system and embryonic diapause in the female kangaroo, Marcopodus giganteus. Aust J Zool 15: 441-459.
6. CRUZ, Y.P. and SELWOOD, L. (1993). Uterine histology of the dasyurid marsupial, Antechinus stuartii: relationship with differentiation of the embryo. J Reprod Fertil 99: 237-242.
7. CRUZ, Y.P. and SELWOOD, L. (1997). Histological differences between gravid and non-gravid uteri in the dasyurid marsupial, Sminthopsis macroura (Spencer). J Reprod Fertil 111: 319-325.
8. CUI, S. and SELWOOD, L. (2000). cDNA cloning, characterization, expression and recombinant protein production of leukemia inhibitory factor (LIF) from the marsupial, the brushtail possum (Trichosurus vulpecula). Gene 243: 167-178.
9. DAIKOKU, T., CHA, J., SUN, X., TRANGUCH, S., XIE, H., FUJITA, T., HIROTA, Y., LYDON, J., DEMAYO, F., MAXSON, R. et al., (2011). Conditional deletion of Msx homeobox genes in the uterus inhibits blastocyst implantation by altering uterine receptivity. Dev Cell 21: 1014-1025.
10. DAIKOKU, T., SONG, H., GUO, Y., RIESEWIJK, A., MOSSELMAN, S., DAS, S.K. and DEY, S.K. (2004). Uterine Msx-1 and Wnt4 signaling becomes aberrant in mice with the loss of leukemia inhibitory factor or Hoxa-10: evidence for a novel cytokine-homeobox-Wnt signaling in implantation. Mol Endocrinol 18: 1238-1250.
11. DENKER, H.W. and Tyndale-Biscoe, C.H. (1986). Embryo implantation and proteinase activities in a marsupial (Macropus eugenii). Cell and Tissue Research 246: 279-291.
12. DEY, S.K., LIM, H., DAS, S.K., REESE, J., PARIA, B.C., DAIKOKU, T. and WANG, H. (2004). Molecular cues to implantation. Endocr Rev 25: 341-373.
13. FENELON, J.C., BANERJEE, A. and MURPHY, B.D. Embryonic diapause: development on hold. Int J Dev Biol (this issue).
14. FENELON, J.C., SHAW, G., O'neill, C., Frankenberg, S. and Renfree, M.B. (2014). Paf receptor expression in the marsupial embryo and endometrium during embryonic diapause. Reproduction 147: 21-31.
15. FLEMING, M.W. and HARDER, J.D. (1981). Uterine histology and reproductive cycles in pregnant and non-pregnant opossums, Didelphis virginiana. J Reprod Fertil 63: 21-24.
16. FLETCHER, T.P., JETTON, A.E. and RENFREE, M.B. (1988). Infuence of progesterone and oestradiol-17b on blastocysts of the tammar wallaby (Macropus eugenii) during seasonal diapause. J Reprod Fertil 83: 193-200.
17. FLINT, A.P. and RENFREE, M.B. (1982). Oestradiol-17b in the blood during seasonal reactivation of the diapausing blastocyst in a wild population of tammar wallabies. J Endocrinol 95: 293-300.
18. FLINT, A.P.F., RENFREE, M.B. and WEIR, B.J. (1981). Embryonic diapause in mammals. In Journal of Reproduction and Fertility Supplement, (ed., pp. v, 260 p, 22 p of plates. Cambridge, Colchester: Journal of Reproduction & Fertility; Biochemical Society Book Depot.
19. FOTEDAR, R., BENDJENNAT, M. and FOTEDAR, A. (2004). Functional analysis of CDK inhibitor p21WAF1. Methods Mol Biol 281: 55-71.
20. FREYER, C., ZELLER, U. and RENFREE, M.B. (2002). Ultrastructure of the placenta of the tammar wallaby, Macropus eugenii: comparison with the grey short-tailed opossum, Monodelphis domestica. J Anat 201: 101-119.
21. GORDON, K., FLETCHER, T.P. and RENFREE, M.B. (1988). 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 83: 401-406.
22. HAMATANI, T., DAIKOKU, T., WANG, H., MATSUMOTO, H., CARTER, M.G., KO, M.S. and DEY, S.K. (2004). Global gene expression analysis identifes molecular pathways distinguishing blastocyst dormancy and activation. Proc Natl Acad Sci USA 101: 10326-10331.
23. HEARN, C.M., SHAW, G., SHORT, R.V. and RENFREE, M.B. (1998). Effects of cabergoline on reproduction in three families of Australian marsupials. J Reprod Fertil 113: 151-157.
24. HEARN, J.P. (1973). Pituitary inhibition of pregnancy. Nature 241: 207-208.
25. HEARN, J.P. (1974). The pituitary gland and implantation in the tammar wallaby, Macropus eugenii. J Reprod Fertil 39: 235-241.
26. HEARN, J.P. (1975). Hypophysectomy of the tammar wallaby, Macropus eugenii: surgical approach and general effects. J Endocrinol 64: 403-416.
27. HINDS, L.A. (1989). Morning pulse of prolactin maintains seasonal quiescence in the tammar, Macropus eugenii. J Reprod Fertil 87: 735-474.
28. HINDS, L.A., DIGGLE, P.J. and Tyndale-Biscoe, C.H. (1992). Effects of the ovary, sucking stimulus and season on the pattern of LH and FSH release in the female tammar, Macropus eugenii. Reprod Fertil Dev 4: 25-34.
29. HINDS, L.A. and Tyndale-Biscoe, C.H. (1982). Plasma progesterone levels in the pregnant and non-pregnant tammar, Macropus eugenii. J Endocrinol 93: 99-107.
30. HIRZEL, D.J., WANG, J., DAS, S.K., DEY, S.K. and MEAD, R.A. (1999). Changes in uterine expression of leukemia inhibitory factor during pregnancy in the Western spotted skunk. Biol Reprod 60: 484-492.
31. INGRAM, J.N., SHAW, G. and RENFREE, M.B. (1999). Cortisol in fetal fuids and the fetal adrenal at parturition in the tammar wallaby (Macropus eugenii). Biol Reprod 60: 651-655.
32. JIN, X.L., CHANDRAKANTHAN, V., MORGAN, H.D. and O'neill, C. (2009). Pre-implantation embryo development in the mouse requires the latency of TRP53 expression, which is induced by a ligand-activated PI3 kinase/AKT/MDM2-mediated signaling pathway. Biol Reprod 81: 234-242.
33. JIN, X.L. and O'neill, C. (2011). Regulation of the expression of proto-oncogenes by autocrine embryotropins in the early mouse embryo. Biol Reprod 84: 1216-1224.
34. KOJIMA, T., HINDS, L.A., MULLER, W.J., O'neill, C. and Tyndale-Biscoe, C.H. (1993). Production and secretion of progesterone in vitro and presence of platelet activating factor (PAF) in early pregnancy of the marsupial, Macropus eugenii. Reprod Fertil Dev 5: 15-25.
35. LEFEVRE, P.L., PALIN, M.F., CHEN, G., TURECKI, G. and MURPHY, B.D. (2011a). Polyamines are implicated in the emergence of the embryo from obligate diapause. Endocrinology 152: 1627-1639.
36. LEFEVRE, P.L., PALIN, M.F. and MURPHY, B.D. (2011b). Polyamines on the reproductive landscape. Endocr Rev 32: 694-712.
37. LOPES, F.L., DESMARAIS, J., GEVRY, N.Y., LEDOUX, S. and MURPHY, B.D. (2003). Expression of vascular endothelial growth factor isoforms and receptors Flt-1 and KDR during the peri-implantation period in the mink, Mustela vison. Biol Reprod 68: 1926-1933.
38. LOPES, F.L., DESMARAIS, J., LEDOUX, S., GEVRY, N.Y., LEFEVRE, P. and MURPHY, B.D. (2006). Transcriptional regulation of uterine vascular endothelial growth factor during early gestation in a carnivore model, Mustela vison. J Biol Chem 281: 24602-24611.
39. LOPES, F.L., DESMARAIS, J.A. and MURPHY, B.D. (2004). Embryonic diapause and its regulation. Reproduction 128: 669-678.
40. LUO, Z.X., YUAN, C.X., MENG, Q.J. and JI, Q. (2011). A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 476: 442-445.
41. MCLAREN, A. (1982). The embryo. In Reproduction in Mammals. Book 2 Embryonic and Fetal Development, (ed. AUSTIN, C. R. and SHORT, R. V.). Cambridge University Press, Cambridge, pp.1-25.
42. MENZIES, B.R., PASK, A.J. and RENFREE, M.B. (2011). Placental expression of pituitary hormones is an ancestral feature of therian mammals. Evodevo 2: 16.
43. MURPHY, B.D. (2012). Embryonic diapause: advances in understanding the enigma of seasonal delayed implantation. Reprod Domest Anim 47 Suppl 6: 121-124.
44. NALLASAMY, S., LI, Q., BAGCHI, M.K. and BAGCHI, I.C. (2012). Msx homeobox genes critically regulate embryo implantation by controlling paracrine signaling between uterine stroma and epithelium. PLoS Genet 8: e1002500.
45. NICHOLS, J., CHAMBERS, I., TAGA, T. and SMITH, A. (2001). Physiological rationale for responsiveness of mouse embryonic stem cells to gp130 cytokines. Development 128: 2333-2339.
46. NICHOLS, J., DAVIDSON, D., TAGA, T., YOSHIDA, K., CHAMBERS, I. and SMITH, A. (1996). Complementary tissue-specific expression of LIF and LIF-receptor mRNAs in early mouse embryogenesis. Mech Dev 57: 123-131.
47. O'neill, C. (1991). A physiological role for PAF in the stimulation of mammalian embryonic development. Trends Pharmacol Sci 12: 82-84.
48. PADYKULA, H.A. and TAYLOR, J.M. (1976). Cellular mechanisms involved in cyclic stromal renewal of the uterus. I. The opossum, Didelphis virginiana. Anat Rec 184: 5-25.
49. PARRY, L.J., GUYMER, F.J., FLETCHER, T.P. and RENFREE, M.B. (1996). Release of an oxytocic peptide at parturition in the marsupial, Macropus eugenii. J Reprod Fertil 107: 191-198.
50. RENFREE, M.B. (1972). Influence of the embryo on the marsupial uterus. Nature 240: 475-477.
51. RENFREE, M.B. (1973a). The composition of fetal fuids of the marsupial Macropus eugenii. Dev Biol 33: 62-79.
52. RENFREE, M.B. (1973b). Proteins in the uterine secretions of the marsupial Macropus eugenii. Dev Biol 32: 41-49.
53. RENFREE, M.B. (1981). Embryonic diapause in marsupials. J Reprod Fertil Suppl 29: 67-78.
54. RENFREE, M.B. (1994). Endocrinology of pregnancy, parturition and lactation in marsupials. In Marshall's Physiology of Reproduction, vol. 3: Pregnancy and Lactation (ed. LAMMING, G. E.). Chapman & Hall, London, UK, pp. 677-766.
55. RENFREE, M.B. (2000). Maternal recognition of pregnancy in marsupials. Rev Reprod 5: 6-11.
56. RENFREE, M.B. and CALABY, J.H. (1981). Background to delayed implantation and embryonic diapause. J Reprod Fertil Suppl 29.
57. RENFREE, M.B. and LEWIS, A.M. (1996). Cleavage in vivo and in vitro in the Marsupial Macropus eugenii. Reprod Fertil Dev 8: 725-742.
58. RENFREE, M.B. and SHAW, G. (2000). Diapause. Ann. Rev. Physiol. 62: 353-375.
59. RENFREE, M.B., SHAW, G. and FLETCHER, T.P. (1994). Evidence for the essential role of prostaglandins for parturition in a marsupial, Macropus eugenii. J Reprod Fertil 102: 433-446.
60. RENFREE, M.B. and Tyndale-Biscoe, C.H. (1973). Intrauterine development after diapause in the marsupial Macropus eugenii. Dev Biol 32: 28-40.
61. ROBERTS, C., O'neill, C. and Wright, L. (1993). Platelet activating factor (PAF) enhances mitosis in preimplantation mouse embryos. Reprod Fertil Dev 5: 271-279.
62. RUDD, C.D. (1994). Sexual behaviour of male and female tammar wallabies (Macropus eugenii) at post-partum oestrus. J. Zoology 232: 151-162.
63. SELWOOD, L. and WOOLLEY, P.A. (1991). A timetable of embryonic development, and ovarian and uterine changes during pregnancy, in the stripe-faced dunnart, Sminthopsis macroura (Marsupialia: Dasyuridae). J Reprod Fertil 91: 213-227.
64. SERNIA, C. and Tyndale-Biscoe, C.H. (1979). Prolactin receptors in the mammary gland, corpus luteum and other tissues of the tammar wallaby, Macropus eugenii. J Endocrinol 83: 79-89.
65. SHARKEY, A. (1998). Cytokines and implantation. Rev Reprod 3: 52-61.
66. SHAW, G. (1996). The uterine environment in early pregnancy in the tammar wallaby. Reprod Fertil Dev 8: 811-818.
67. SHAW, G. and RENFREE, M.B. (1984). Concentrations of oestradiol-17 beta in plasma and corpora lutea throughout pregnancy in the tammar, Macropus eugenii. J Reprod Fertil 72: 29-37.
68. SHAW, G. and RENFREE, M.B. (1986). Uterine and embryonic metabolism after diapause in the tammar wallaby, Macropus eugenii. J Reprod Fertil 76: 339-347.
69. SHAW, G. and RENFREE, M.B. (2001). Fetal control of parturition in marsupials. Reprod Fertil Dev 13: 653-659.
70. SHAW, G. and RENFREE, M.B. (2006). Parturition and perfect prematurity: birth in marsupials. Aust J Zool 54: 139-149.
71. SHAW, G., RENFREE, M.B. and FLETCHER, T.P. (1996). A role for glucocorticoids in parturition in a marsupial, Macropus eugenii. Biol Reprod 54: 728-733.
72. SHAW, G. and ROSE, R. (1979). Delayed gestation in the Potoroo Potorous tridactylus (Kerr). Aust J Zool 27: 901-912.
73. SHOREY, C.D. and HUGHES, R.L. (1973). Cyclical changes in the uterine endo-metrium and peripheral plasma concentrations of progesterone in the marsupial Trichosurus vulpecula. Aust J Zool 21: 1-19.
74. SMITH, M.J. (1981). Morphological observations on the diapausing blastocyst of some macropodid marsupials. J Reprod Fertil 61: 483-486.
75. SONG, J.H., HOUDE, A. and MURPHY, B.D. (1998). Cloning of leukemia inhibitory factor (LIF) and its expression in the uterus during embryonic diapause and implantation in the mink (Mustela vison). Mol Reprod Dev 51: 13-21.
76. SPINDLER, R.E. (1997). The metabolism and control of blastocysts during diapause and reactivation in the Tammar wallaby (Macropus eugenii). Thesis (Ph.D.) University of Melbourne, Dept. of Zoology, 1997.
77. SPINDLER, R.E., RENFREE, M.B. and GARDNER, D.K. (1995). Metabolic assessment of wallaby blastocysts during embryonic diapause and subsequent reactivation. Reprod Fertil Dev 7: 1157-1162.
78. SPINDLER, R.E., RENFREE, M.B., SHAW, G. and GARDNER, D.K. (1998). Reactivating tammar wallaby blastocysts oxidize glucose. Biol Reprod 58: 1425-1431.
79. STEWART, C.L., KASPAR, P., BRUNET, L.J., BHATT, H., GADI, I., KONTGEN, F. and ABBONDANZO, S.J. (1992). Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359: 76-79.
80. TOWERS, P.A., SHAW, G. and RENFREE, M.B. (1986). Urogenital vasculature and local steroid concentrations in the uterine branch of the ovarian vein of the female tammar wallaby (Macropus eugenii). J Reprod Fertil 78: 37-47.
81. Tyndale-Biscoe, C.H. (1970). Resumption of development by quiescent blasto-cysts transferred to primed, ovariectomized recipients in the marsupial, Macropus eugenii. J Reprod Fertil 23: 25-32.
82. Tyndale-Biscoe, C.H. (1979). Hormonal control of embryonic diapause and reactivation in the tammar wallaby. In Maternal Recognition of Pregnancy. Ciba Found. Symp. 64, (ed. CARSON, D. D.). Excerpta Medica, Amsterdam, pp.173-190.
83. Tyndale-Biscoe, C.H. and Hearn, J.P. (1981). Pituitary and ovarian factors associated with seasonal quiescence of the tammar wallaby, Macropus eugenii. J Reprod Fertil 63: 225-230.
84. Tyndale-Biscoe, C.H. and Hinds, L.A. (1984). Seasonal patterns of circulating progesterone and prolactin and response to bromocriptine in the female tammar Macropus eugenii. Gen Comp Endocrinol 53: 58-68.
85. Tyndale-Biscoe, C.H., HINDS, L.A., HORN, C.A. and JENKIN, G. (1983). Hormonal changes at oestrus, parturition and post-partum oestrus in the tammar wallaby (Macropus eugenii). J Endocrinol 96: 155-161.
86. Tyndale-Biscoe, H. and RENFREE, M.B. (1987). Reproductive Physiology of Marsupials. Cambridge University Press, Cambridge; Melbourne; New York.
87. WALKER, M.T. and HUGHES, R.L. (1981). Ultrastructural changes after diapause in the uterine glands, corpus luteum and blastocyst of the red-necked wallaby, Macropus rufogriseus banksianus. J Reprod Fertil Suppl 29: 151-158.
88. WALLACE, G.I. (1981). Uterine factors and delayed implantation in macropodid marsupials. In Journal of Reproduction and Fertility Supplement, (ed. FLINT, A. P. F., RENFREE, M. B. and WEIR, B. J.). Journal of Reproduction & Fertility; Biochemical Society Book Depot, Cambridge, Colchester, pp.173-181.
89. WARD, S.J. and RENFREE, M.B. (1988). Reproduction in females of the feathertail gliders, Acrobates pygmeaus (Marsupialia). J. Zool. (Lond). 216: 225-240.
90. YOUNG, I.R. and RENFREE, M.B. (1979). The effects of corpus luteum removal during gestation on parturition in the tammar wallaby (Macorpus eugenii). J Reprod Fertil 56: 249-254.