Embryo implantation: A time for recalling and forwarding

Chinese Science Bulletin

Volumn 54, Issue 22, 2009, Pages 4083-4093

  Chen, Qi ^a,b   Peng, HongYing ^a   Zhang, Ying ^a,b   Lei, Li ^a,b   Cao, YuJing ^a   Duan, EnKui ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Blastocyst activation; Embryo implantation; Research history; Uterine receptivity

Indexed keywords

EID: 74549165443     PISSN: 10016538     EISSN: 18619541     Source Type: Journal    
DOI: 10.1007/s11434-009-0631-3     Document Type: Review

References (80)

1. Norwitz E R, Schust D J, Fisher S J. Implantation and the survival of early pregnancy. N Engl J Med, 2001, 345: 1400-1408.
2. Wilcox A J, Baird D D, Weinberg C R. Time of implantation of the conceptus and loss of pregnancy. N Engl J Med, 1999, 340: 1796-1799.
3. Dey S K. Reproductive biology: fatty link to fertility. Nature, 2005, 435: 34-35.
4. Song H, Lim H, Paria B C, et al. Cytosolic phospholipase A2alpha is crucial [correction of A2alpha deficiency is crucial] for 'on-time' embryo implantation that directs subsequent development. Development, 2002, 129(12): 2879-2889.
5. Ye X, Hama K, Contos J J, et al. LPA3-mediated lysophosphatidic acid signalling in embryo implantation and spacing. Nature, 2005, 435: 104-108.
6. Doyle L L, Gates A H, Noyes R W. Asynchronous transfer of mouse ova. Fertil Steril, 1963, 14: 215-225.
7. Dickmann Z N R. The fate of ova transferred into the uterus of the rat. J Reprod Fertil, 1960: 197-212.
8. Goto Y, Noda Y, Shiotani M, et al. The fate of embryos transferred into the uterus. J Assist Reprod Genet, 1993, 10: 197-201.
9. Paria B C, Huet-hudson Y M, Dey S K. Blastocyst's state of activity determines the "window" of implantation in the receptive mouse uterus. Proc Natl Acad Sci USA, 1993, 90: 10159-10162.
10. Finn C A, Martin L. The control of implantation. J Reprod Fertil, 1974, 39: 195-206.
11. Wang H, Dey S K. Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet, 2006, 7: 185-199.
12. Finn C A, Martin L. Endocrine control of the timing of endometrial sensitivity to a decidual stimulus. Biol Reprod, 1972, 7: 82-86.
13. Curtis H S, Goulding E H, Eddy E M, et al. Studies using the estrogen receptor alpha knockout uterus demonstrate that implantation but not decidualization-associated signaling is estrogen dependent. Biol Reprod, 2002, 67: 1268-1277.
14. Corner W M A A G W. PHYSIOLOGY OF THE CORPUS LUTEUM: III. Normal growth and implantation of embryos after very early ablation of the ovaries, under the influence of extracts of the corpus luteum. Am J Physiol, 1929, 88: 340-346.
15. Tranguch S, Smith D F, Dey S K. Progesterone receptor requires a co-chaperone for signalling in uterine biology and implantation. Reprod Biomed Online, 2006, 13: 651-660.
16. Lydon J P, Demayo F J, Conneely O M, et al. Reproductive phenotpes of the progesterone receptor null mutant mouse. J Steroid Biochem Mol Biol, 1996, 56(1-6 Spec No): 67-77.
17. Lydon J P, Demayo F J, Funk C R, et al. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev, 1995, 9: 2266-2278.
18. Dey S K, Lim H, Das S K, et al. Molecular cues to implantation. Endocr Rev, 2004, 25: 341-373.
19. Wang X, Matsumoto H, Zhao X, et al. Embryonic signals direct the formation of tight junctional permeability barrier in the decidualizing stroma during embryo implantation. J Cell Sci, 2004, 117: 53-62.
20. Collins M K, Tay C S, Erlebacher A. Dendritic cell entrapment within the pregnant uterus inhibits immune surveillance of the maternal/fetal interface in mice. J Clin Invest, 2009, 119: 2062-2073.
21. Whitten W K. Endocrine studies on delayed implantation in lactating mice; role of the pituitary in implantation. J Endocrinol, 1958, 16: 435-440.
22. Ma W G, Song H, Das S K, et al. Estrogen is a critical determinant that specifies the duration of the window of uterine receptivity for implantation. Proc Natl Acad Sci USA, 2003, 100: 2963-2968.
23. Finn C A, Pope M D, Milligan S R. Timing of the window of uterine sensitivity to decidual stimuli in mice. Reprod Fertil Dev, 1992, 4: 565-571.
24. Das A, Mantena S R, Kannan A, et al. De novo synthesis of estrogen in pregnant uterus is critical for stromal decidualization and angiogenesis. Proc Natl Acad Sci USA, 2009, 106: 12542-12547.
25. Finn C A, Martin L. The role of the oestrogen secreted before oestrus in the preparation of the uterus for implantation in the mouse. J Endocrinol, 1970, 47: 431-438.
26. Wang X, Wang H, Matsumoto H, et al. Dual source and target of heparin-binding EGF-like growth factor during the onset of implantation in the hamster. Development, 2002, 129: 4125-4134.
27. Reese J, Wang H, Ding T, et al. The hamster as a model for embryo implantation: Insights into a multifaceted process. Semin Cell Dev Biol, 2008, 19: 194-203.
28. Stromstedt M, Keeney D S, Waterman M R, et al. Preimplantation mouse blastocysts fail to express CYP genes required for estrogen biosynthesis. Mol Reprod Dev, 1996, 43: 428-436.
29. Hetherington C M. Induction of deciduomata in the mouse by carbon dioxide. Nature, 1968, 219: 863-864.
30. Mclaren A. Stimulus and response during early pregnancy in the mouse. Nature, 1969, 221: 739-741.
31. Bany B M, Cross J C. Post-implantation mouse conceptuses produce paracrine signals that regulate the uterine endometrium undergoing decidualization. Dev Biol, 2006, 294: 445-456.
32. Kashiwagi A, Digirolamo C M, Kanda Y, et al. The postimplantation embryo differentially regulates endometrial gene expression and decidualization. Endocrinology, 2007, 148: 4173-4184.
33. Lefevre P, Campos D B, Murphy B D. Talk to me: the embryo dictates gene expression by the endometrium. Endocrinology, 2007, 148: 4170-4172.
34. Herington J L, Underwood T, Mcconaha M, et al. Paracrine signals from the mouse conceptus are not required for the normal progression of decidualization. Endocrinology, 2009, doi: 10. 1210/en. 2009-0036.
35. Stewart C L, Kaspar P, Brunet L J, et al. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature, 1992, 359: 76-79.
36. Robb L, Li R, Hartley L, et al. Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nat Med, 1998, 4: 303-308.
37. Song H, Lim H, Das S K, et al. Dysregulation of EGF family of growth factors and COX-2 in the uterus during the preattachment and attachment reactions of the blastocyst with the luminal epithelium correlates with implantation failure in LIF-deficient mice. Mol Endocrinol, 2000, 14: 1147-1161.
38. Lim H, Paria B C, Das S K, et al. Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell, 1997, 91: 197-208.
39. Lim H, Gupta R A, Ma W G, et al. Cyclo-oxygenase-2-derived prostacyclin mediates embryo implantation in the mouse via PPARdelta. Genes Dev, 1999, 13: 1561-1574.
40. Wang H, Xie H, Sun X, et al. Stage-specific integration of maternal and embryonic peroxisome proliferator-activated receptor delta signaling is critical to pregnancy success. J Biol Chem, 2007, 282: 37770-37782.
41. Xie H, Wang H, Tranguch S, et al. Maternal heparin-binding-EGF deficiency limits pregnancy success in mice. Proc Natl Acad Sci USA, 2007, 104: 18315-18320.
42. Laws M J, Taylor R N, Sidell N, et al. Gap junction communication between uterine stromal cells plays a critical role in pregnancy-associated neovascularization and embryo survival. Development, 2008, 135: 2659-2668.
43. Plaks V, Birnberg T, Berkutzki T, et al. Uterine DCs are crucial for decidua formation during embryo implantation in mice. J Clin Invest, 2008, 118: 3954-3965.
44. Lee K, Jeong J, Kwak I, et al. Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nat Genet, 2006, 38: 1204-1209.
45. Lee K Y, Jeong J W, Wang J, et al. Bmp2 is critical for the murine uterine decidual response. Mol Cell Biol, 2007, 27: 5468-5478.
46. Li Q, Kannan A, Wang W, et al. Bone morphogenetic protein 2 functions via a conserved signaling pathway involving Wnt4 to regulate uterine decidualization in the mouse and the human. J Biol Chem, 2007, 282: 31725-31732.
47. Carson D D, Bagchi I, Dey S K, et al. Embryo implantation. Dev Biol, 2000, 223: 217-237.
48. Paria B C, Reese J, Das S K, et al. Deciphering the cross-talk of implantation: advances and challenges. Science, 2002, 296: 2185-2188.
49. Lee K Y, Jeong J W, Tsai S Y, et al. Mouse models of implantation. Trends Endocrinol Metab, 2007, 18: 234-239.
50. Hou Q, Paria B C, Mui C, et al. Immunolocalization of estrogen receptor protein in the mouse blastocyst during normal and delayed implantation. Proc Natl Acad Sci USA, 1996, 93: 2376-2381.
51. Paria B C, Lim H, Wang X N, et al. Coordination of differential effects of primary estrogen and catecholestrogen on two distinct targets mediates embryo implantation in the mouse. Endocrinology, 1998, 139: 5235-5246.
52. Hamatani T, Daikoku T, Wang H, et al. Global gene expression analysis identifies molecular pathways distinguishing blastocyst dormancy and activation. Proc Natl Acad Sci USA, 2004, 101: 10326-10331.
53. Wang H, Matsumoto H, Guo Y, et al. Differential G protein-coupled cannabinoid receptor signaling by anandamide directs blastocyst activation for implantation. Proc Natl Acad Sci USA, 2003, 100: 14914-14919.
54. Das S K, Wang X N, Paria B C, et al. Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation. Development, 1994, 120: 1071-1083.
55. Paria B C, Ma W, Tan J, et al. Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc Natl Acad Sci USA, 2001, 98: 1047-1052.
56. Paria B C, Das S K, Andrews G K, et al. Expression of the epidermal growth factor receptor gene is regulated in mouse blastocysts during delayed implantation. Proc Natl Acad Sci USA, 1993, 90: 55-59.
57. Wang J, Mayernik L, Schultz J F, et al. Acceleration of trophoblast differentiation by heparin-binding EGF-like growth factor is dependent on the stage-specific activation of calcium influx by ErbB receptors in developing mouse blastocysts. Development, 2000, 127: 33-44.
58. Paria B C, Elenius K, Klagsbrun M, et al. Heparin-binding EGF-like growth factor interacts with mouse blastocysts independently of ErbB1: A possible role for heparan sulfate proteoglycans and ErbB4 in blastocyst implantation. Development, 1999, 126: 1997-2005.
59. Das S K, Chakraborty I, Paria B C, et al. Amphiregulin is an implantation-specific and progesterone-regulated gene in the mouse uterus. Mol Endocrinol, 1995, 9: 691-705.
60. Guo Y, Wang H, Okamoto Y, et al. N-acylphosphatidylethanolamine-hydrolyzing phospholipase D is an important determinant of uterine anandamide levels during implantation. J Biol Chem, 2005, 280: 23429-23432.
61. Liu W M, Duan E K, Cao Y J. Effects of anandamide on embryo implantation in the mouse. Life Sci, 2002, 71: 1623-1632.
62. Xie H, Tranguch S, Jia X, et al. Inactivation of nuclear Wnt-beta-catenin signaling limits blastocyst competency for implantation. Development, 2008, 135: 717-727.
63. Ueda O, Yorozu K, Kamada N, et al. Possible expansion of "Window of Implantation" in pseudopregnant mice: time of implantation of embryos at different stages of development transferred into the same recipient. Biol Reprod, 2003, 69: 1085-1090.
64. Shiotani M, Noda Y, Mori T. Embryo-dependent induction of uterine receptivity assessed by an in vitro model of implantation in mice. Biol Reprod, 1993, 49: 794-801.
65. Wakuda K, Takakura K, Nakanishi K, et al. Embryo-dependent induction of embryo receptivity in the mouse endometrium. J Reprod Fertil, 1999, 115: 315-324.
66. Matorras R, Matorras F, Mendoza R, et al. The implantation of every embryo facilitates the chances of the remaining embryos to implant in an IVF programme: a mathematical model to predict pregnancy and multiple pregnancy rates. Hum Reprod, 2005, 20: 2923-2931.
67. van M A, Fiddelers A A, Janssen J M, et al. In unselected patients, elective single embryo transfer prevents all multiples, but results in significantly lower pregnancy rates compared with double embryo transfer: A randomized controlled trial. Hum Reprod, 2006, 21: 338-343.
68. Wimsatt W A. Some comparative aspects of implantation. Biol Reprod, 1975, 12: 1-40.
69. Mclaren A, Michie D. The spacing of implantations in the mouse uterus. Mem Soc Endocr, 1959, 6: 65-75.
70. Restall B J, Bindon B M. The timing and variation of pre-implantation events in the mouse. J Reprod Fertil, 1971, 24: 423-426.
71. Wellstead J R, Bruce N W, Rahima A. Effects of indomethacin on spacing of conceptuses within the uterine horn and on fetal and placental growth in the rat. Anat Rec, 1989, 225: 101-105.
72. Kinoshita K, Satoh K, Ishihara O, et al. Involvement of prostaglandins in implantation in the pregnant mouse. Adv Prostaglandin Thromboxane Leukot Res, 1985, 15: 605-607.
73. Hama K, Aoki J, Inoue A, et al. Embryo spacing and implantation timing are differentially regulated by LPA3-mediated lysophosphatidic acid signaling in mice. Biol Reprod, 2007, 77: 954-959.
74. Pusey J, Kelly W A, Bradshaw J M, et al. Myometrial activity and the distribution of blastocysts in the uterus of the rat: Interference by relaxin. Biol Reprod, 1980, 23: 394-397.
75. Yoshinaga K, Rice C, Krenn J, et al. Effects of nicotine on early pregnancy in the rat. Biol Reprod, 1979, 20: 294-303.
76. Legrand C, Banuelos-nevarez A, Rigolot C, et al. Comparative effects of 6-hydroxydopamine and alpha-adrenoceptor antagonists on intrauterine migration and spacing of blastocysts in the rat. J Reprod Fertil, 1987, 81: 51-58.
77. Alden R H. Implantation of the rat egg. I. Experimental alteration of uterine polarity. J Exp Zool, 1945, 100: 229-235.
78. Yang Z M, Das S K, Wang J, et al. Potential sites of prostaglandin actions in the periimplantation mouse uterus: differential expression and regulation of prostaglandin receptor genes. Biol Reprod, 1997, 56: 368-379.
79. Haffner-krausz R, Gorivodsky M, Chen Y, et al. Expression of Fgfr2 in the early mouse embryo indicates its involvement in preimplantation development. Mech Dev, 1999, 85: 167-172.
80. Pinborg A, Lidegaard O, Andersen A N. The vanishing twin: a major determinant of infant outcome in IVF singleton births. Br J Hosp Med (Lond), 2006, 67: 417-420.