The molecular basis of recurrent pregnancy loss: Impaired natural embryo selection

Molecular Human Reproduction

Volumn 16, Issue 12, 2010, Pages 886-895

  Teklenburg, G ^a   Salker, Madhuri ^b   Heijnen, Cobi ^a   Macklon, Nick S ^a,c   Brosens, Jan J ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b HAMMERSMITH HOSPITAL   (United Kingdom)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Decidualization; Embryo; Endometrium; Fertility; Miscarriage

Indexed keywords

CHROMOSOME ABERRATION; CORRELATION COEFFICIENT; DECIDUALIZATION; DISEASE PREDISPOSITION; EMBRYO DEVELOPMENT; HUMAN; MENSTRUAL CYCLE; PLACENTA INSUFFICIENCY; PRIORITY JOURNAL; RECURRENT ABORTION; REVIEW; SPONTANEOUS ABORTION;

ABORTION, HABITUAL; CELL DIFFERENTIATION; DECIDUA; EMBRYO IMPLANTATION; EMBRYO, MAMMALIAN; ENDOMETRIUM; FEMALE; HUMANS; PREGNANCY; TIME FACTORS;

EID: 78649493373     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gaq079     Document Type: Review

References (103)

1. Aghajanova L, Horcajadas JA, Weeks JL, Esteban FJ, Nezhat CN, Conti M, Giudice LC. The protein kinase A pathway-regulated transcriptome of endometrial stromal fibroblasts reveals compromised differentiation and persistent proliferative potential in endometriosis. Endocrinology 2010;151:1341-1355.
2. Aplin JD, Hey NA, Li TC. MUC1 as a cell surface and secretory component of endometrial epithelium: reduced levels in recurrent miscarriage. Am J Reprod Immunol 1996;35:261-266.
3. Apter D, Vihko R. Serum pregnenolone, progesterone, 17-hydroxyprogesterone, testosterone and 5 alpha-dihydrotestosterone during female puberty. J Clin Endocrinol Metab 1977;45:1039-1048.
4. Backdahl L, Bushell A, Beck S. Inflammatory signalling as mediator of epigenetic modulation in tissue-specific chronic inflammation. Int J Biochem Cell Biol 2009;41:176-184.
5. Barash A, Dekel N, Fieldust S, Segal I, Schechtman E, Granot I. Local injury to the endometrium doubles the incidence of successful pregnancies in patients undergoing in vitro fertilization. Fertil Steril 2003;79:1317-1322.
6. Bartsch O, Bartlick B, Ivell R. Phosphodiesterase 4 inhibition synergizes with relaxin signaling to promote decidualization of human endometrial stromal cells. J Clin Endocrinol Metab 2004;89:324-334.
7. Bielanska M, Tan SL, Ao A. Chromosomal mosaicism throughout human preimplantation development in vitro: incidence, type, and relevance to embryo outcome. Hum Reprod 2002;17:413-419.
8. Billinski P, Roopenian D, Gossler A. Maternal IL-11Ralpha function is required for normal decidua and fetoplacental development in mice. Genes Dev 1998;12:2234-2243.
9. Boomsma CM, Kavelaars A, Eijkemans MJ, Lentjes EG, Fauser BC, Heijnen CJ, Macklon NS. Endometrial secretion analysis identifies a cytokine profile predictive of pregnancy in IVF. Hum Reprod 2009;24:1427-1435.
10. Brosens I, Robertson WB, Dixon HG. The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol 1967;93:569-579.
11. Brosens JJ, de Souza NM, Barker FG. Uterine junctional zone: function and disease. Lancet 1995;346:558-560.
12. Brosens JJ, Hayashi N, White JO. Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cells. Endocrinology 1999;140:4809-4820.
13. Brosens JJ, Pijnenborg R, Brosens IA. The myometrial junctional zone spiral arteries in normal and abnormal pregnancies: a review of the literature. Am J Obstet Gynecol 2002;187:1416-1423.
14. Brosens I, Hernalsteen P, Devos A, Cloke B, Brosens JJ. Self-assessment of the cervical pupil sign as a new fertility-awareness method. Fertil Steril 2009a;91:937-939.
15. Brosens JJ, Parker MG, McIndoe A, Pijnenborg R, Brosens IA. A role for menstruation in preconditioning the uterus for successful pregnancy. Am J Obstet Gynecol 2009b;200:615-616.
16. Brosens JJ, Hodgetts A, Feroze-Zaidi F, Sherwin JR, Fusi L, Salker MS, Higham J, Rose GL, Kajihara T, Young SL et al. Proteomic analysis of endometrium from fertile and infertile patients suggests a role for apolipoprotein A-I in embryo implantation failure and endometriosis. Mol Hum Reprod 2010;16:273-285.
17. Catalano RD, Johnson MH, Campbell EA, Charnock-Jones DS, Smith SK, Sharkey AM. Inhibition of Stat3 activation in the endometrium prevents implantation: a nonsteroidal approach to contraception. Proc Natl Acad Sci USA 2005;102:8585-8590.
18. Catalano RD, Critchley HO, Heikinheimo O, Baird DT, Hapangama D, Sherwin JR, Charnock-Jones DS, Smith SK, Sharkey AM. Mifepristone induced progesterone withdrawal reveals novel regulatory pathways in human endometrium. Mol Hum Reprod 2007;13:641-654.
19. Chard T. Frequency of implantation and early pregnancy loss in natural cycles. Baillieres Clin Obstet Gynaecol 1991;5:179-189.
20. Christiansen OB, Steffensen R, Nielsen HS, Varming K. Multifactorial etiology of recurrent miscarriage and its scientific and clinical implications. Gynecol Obstet Invest 2008;66:257-267.
21. Cloke B, Huhtinen K, Fusi L, Kajihara T, Yliheikkila M, Ho KK, Teklenburg G, Lavery S, Jones MC, Trew G et al. The androgen and progesterone receptors regulate distinct gene networks and cellular functions in decidualizing endometrium. Endocrinology 2008;149:4462-4474.
22. Cornet PB, Picquet C, Lemoine P, Osteen KG, Bruner-Tran KL, Tabibzadeh S, Courtoy PJ, Eeckhout Y, Marbaix E, Henriet P. Regulation and function of LEFTY-A/EBAF in the human endometrium. mRNA expression during the menstrual cycle, control by progesterone, and effect on matrix metalloproteinases. J Biol Chem 2002;277:42496-42504.
23. Croy BA, van den Heuvel MJ, Borzychowski AM, Tayade C. Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol Rev 2006;214:161-185.
24. Devroey P, Fauser BC, Diedrich K. Approaches to improve the diagnosis and management of infertility. Hum Reprod Update 2009;15:391-408.
25. Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T, Wang H. Molecular cues to implantation. Endocr Rev 2004;25:341-373.
26. DiMattia GE, Gellersen B, Duckworth ML, Friesen HG. Human prolactin gene expression. The use of an alternative noncoding exon in decidua and the IM-9-P3 lymphoblast cell line. J Biol Chem 1990;265:16412-16421.
27. Dimitriadis E, Salamonsen LA, Robb L. Expression of interleukin-11 during the human menstrual cycle: coincidence with stromal cell decidualization and relationship to leukaemia inhibitory factor and prolactin. Mol Hum Reprod 2000;6:907-914.
28. Dosiou C, Giudice LC. Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives. Endocr Rev 2005;26:44-62.
29. Dunson DB, Baird DD, Wilcox AJ, Weinberg CR. Day-specific probabilities of clinical pregnancy based on two studies with imperfect measures of ovulation. Hum Reprod 1999;14:1835-1839.
30. Evans J, Catalano RD, Brown P, Sherwin R, Critchley HO, Fazleabas AT, Jabbour HN. Prokineticin 1 mediates fetal-maternal dialogue regulating endometrial leukemia inhibitory factor. FASEB J 2009;23:2165-2175.
31. Evers JL. Female subfertility. Lancet 2002;360:151-159.
32. Fluhr H, Spratte J, Ehrhardt J, Steinmuller F, Licht P, Zygmunt M. Heparin and low-molecular-weight heparins modulate the decidualization of human endometrial stromal cells. Fertil Steril 2010;93:2581-2587.
33. Galloway SM, McNatty KP, Cambridge LM, Laitinen MP, Juengel JL, Jokiranta TS, McLaren RJ, Luiro K, Dodds KG, Montgomery GW et al. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet 2000;25:279-283.
34. Gellersen B, Brosens J. Cyclic AMP and progesterone receptor cross-talk in human endometrium: a decidualizing affair. J Endocrinol 2003;178:357-372.
35. Gellersen B, Kempf R, Telgmann R, DiMattia GE. Nonpituitary human prolactin gene transcription is independent of Pit-1 and differentially controlled in lymphocytes and in endometrial stroma. Mol Endocrinol 1994;8:356-373.
36. Gellersen B, Brosens IA, Brosens JJ. Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives. Semin Reprod Med 2007;25:445-453.
37. Gleicher N, Ryan E, Weghofer A, Blanco-Mejia S, Barad DH. Miscarriage rates after dehydroepiandrosterone (DHEA) supplementation in women with diminished ovarian reserve: a case control study. Reprod Biol Endocrinol 2009;7:108.
38. Haig D. Genetic conflicts in human pregnancy. Q Rev Biol 1993;68:495-532.
39. Haig D. Placental hormones, genomic imprinting, and maternal-fetal communication. J Evol Biol 1996;9:357-380.
40. Hey NA, Li TC, Devine PL, Graham RA, Saravelos H, Aplin JD. MUC1 in secretory phase endometrium: expression in precisely dated biopsies and flushings from normal and recurrent miscarriage patients. Hum Reprod 1995;10:2655-2662.
41. Hiby SE, Regan L, Lo W, Farrell L, Carrington M, Moffett A. Association of maternal killer-cell immunoglobulin-like receptors and parental HLA-C genotypes with recurrent miscarriage. Hum Reprod 2008;23:972-976.
42. Hochner-Celnikier D, Ron M, Eldor A, Segal S, Palti Z, Fuks Z, Vlodavsky I. Growth characteristics of human first trimester decidual cells cultured in serum-free medium: production of prolactin, prostaglandins and fibronectin. Biol Reprod 1984;31:827-836.
43. Hohn HP, Donner AJ, Denker HW. Endometrial receptivity: selective adhesion competence of rabbit uterine epithelium for trophoblast but not for various tumor cells. Cells Tissues Organs 2003;173:204-216.
44. Horcajadas JA, Pellicer A, Simon C. Wide genomic analysis of human endometrial receptivity: new times, new opportunities. Hum Reprod Update 2007;13:77-86.
45. Hu W, Feng Z, Teresky AK, Levine AJ. p53 regulates maternal reproduction through LIF. Nature 2007;450:721-724.
46. Jabbour HN, Kelly RW, Fraser HM, Critchley HO. Endocrine regulation of menstruation. Endocr Rev 2006;27:17-46.
47. Jauniaux E, Farquharson RG, Christiansen OB, Exalto N. Evidence-based guidelines for the investigation and medical treatment of recurrent miscarriage. Hum Reprod 2006;21:2216-2222.
48. Jennings RB, Murry CE, Steenbergen C Jr, Reimer KA. Development of cell injury in sustained acute ischemia. Circulation 1990;82:II2-II12.
49. Jones MC, Fusi L, Higham JH, Abdel-Hafiz H, Horwitz KB, Lam EW, Brosens JJ. Regulation of the SUMO pathway sensitizes differentiating human endometrial stromal cells to progesterone. Proc Natl Acad Sci USA 2006;103:16272-16277.
50. Kajihara T, Jones M, Fusi L, Takano M, Feroze-Zaidi F, Pirianov G, Mehmet H, Ishihara O, Higham JM, Lam EW et al. Differential expression of FOXO1 and FOXO3a confers resistance to oxidative cell death upon endometrial decidualization. Mol Endocrinol 2006;20:2444-2455.
51. Karimzadeh MA, Ayazi RM, Tabibnejad N. Endometrial local injury improves the pregnancy rate among recurrent implantation failure patients undergoing in vitro fertilisation/intra cytoplasmic sperm injection: a randomised clinical trial. Aust N Z J Obstet Gynaecol 2009;49:677-680.
52. Karow WG, Gentry WC, Skeels RF, Payne SA. Endometrial biopsy in the luteal phase of the cycle of conception. Fertil Steril 1971;22:482-495.
53. Keulers MJ, Hamilton CJ, Franx A, Evers JL, Bots RS. The length of the fertile window is associated with the chance of spontaneously conceiving an ongoing pregnancy in subfertile couples. Hum Reprod 2007;22:1652-1656.
54. Kim JJ, Fazleabas AT. Uterine receptivity and implantation: the regulation and action of insulin-like growth factor binding protein-1 (IGFBP-1), HOXA10 and forkhead transcription factor-1 (FOXO-1) in the baboon endometrium. Reprod Biol Endocrinol 2004;16:2-34.
55. Kim JJ, Taylor HS, Lu Z, Ladhani O, Hastings JM, Jackson KS, Wu Y, Guo SW, Fazleabas AT. Altered expression of HOXA10 in endometriosis: potential role in decidualization. Mol Hum Reprod 2007;13:323-332.
56. King AE, Critchley HO. Oestrogen and progesterone regulation of inflammatory processes in the human endometrium. J Steroid Biochem Mol Biol 2010;120:116-126.
57. Kitaya K, Yasuda J, Yagi I, Tada Y, Fushiki S, Honjo H. IL-15 expression at human endometrium and decidua. Biol Reprod 2000;63:683-687.
58. Klemmt PA, Carver JG, Kennedy SH, Koninckx PR, Mardon HJ. Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity. Fertil Steril 2006;85:564-572.
59. Koot YEM, Boomsma CB, Eijkemans MCJ, Lentjes EG, Macklon NS. Is pre-clinical pregnancy loss a ëcauseí of unexplained infertility? Hum Reprod 2010;25:i28-i30.
60. Ledbetter DH. Chaos in the embryo. Nat Med 2009;15:490-491.
61. Leese HJ, Sturmey RG, Baumann CG, McEvoy TG. Embryo viability and metabolism: obeying the quiet rules. Hum Reprod 2007;22:3047-3050.
62. Leitao B, Jones MC, Fusi L, Higham J, Lee Y, Takano M, Goto T, Christian M, Lam EW, Brosens JJ. Silencing of the JNK pathway maintains progesterone receptor activity in decidualizing human endometrial stromal cells exposed to oxidative stress signals. FASEB J 2010;24:1541-1551.
63. Lim HJ, Dey SK. HB-EGF: a unique mediator of embryo-uterine interactions during implantation. Exp Cell Res 2009;315:619-626.
64. Lopes FL, Desmarais JA, Murphy BD. Embryonic diapause and its regulation. Reproduction 2004;128:669-678.
65. Lynch VJ, Tanzer A, Wang Y, Leung FC, Gellersen B, Emera D, Wagner GP. Adaptive changes in the transcription factor HoxA-11 are essential for the evolution of pregnancy in mammals. Proc Natl Acad Sci USA 2008;105:14928-14933.
66. Macklon NS, Geraedts JP, Fauser BC. Conception to ongoing pregnancy: the 'black box' of early pregnancy loss. Hum Reprod Update 2002;8:333-343.
67. Mansouri-Attia N, Sandra O, Aubert J, Degrelle S, Everts RE, Giraud-Delville C, Heyman Y, Galio L, Hue I, Yang X et al. Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc Natl Acad Sci USA 2009;106:5687-5692.
68. Medawar PB. Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. Soc Exp Biol 1953;7:320-328.
69. Minici F, Tiberi F, Tropea A, Orlando M, Gangale MF, Romani F, Campo S, Bompiani A, Lanzone A, Apa R. Endometriosis and human infertility: a new investigation into the role of eutopic endometrium. Hum Reprod 2008;23:530-537.
70. Munro SK, Farquhar CM, Mitchell MD, Ponnampalam AP. Epigenetic regulation of endometrium during the menstrual cycle. Mol Hum Reprod 2010;16:297-310.
71. Nakamura H, Kimura T, Koyama S, Ogita K, Tsutsui T, Shimoya K, Taniguchi T, Koyama M, Kaneda Y, Murata Y. Mouse model of human infertility: transient and local inhibition of endometrial STAT-3 activation results in implantation failure. FEBS Lett 2006;580:2717-2722.
72. Narvekar SA, Gupta N, Shetty N, Kottur A, Srinivas M, Rao KA. Does local endometrial injury in the nontransfer cycle improve the IVF-ET outcome in the subsequent cycle in patients with previous unsuccessful IVF? A randomized controlled pilot study. J Hum Reprod Sci 2010;3:15-19.
73. Norwitz ER. Defective implantation and placentation: laying the blueprint for pregnancy complications. Reprod Biomed Online 2006;13:591-599. Otani H. Ischemic preconditioning: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 2008;10:207-247.
74. Picton HM, Elder K, Houghton FD, Hawkhead JA, Rutherford AJ, Hogg JE, Leese HJ, Harris SE. Association between amino acid turnover and chromosome aneuploidy during human preimplantation embryo development in vitro. Mol Hum Reprod 2010;16:557-569.
75. Pijnenborg R, Bland JM, Robertson WB, Dixon G, Brosens I. The pattern of interstitial trophoblastic invasion of the myometrium in early human pregnancy. Placenta 1981;2:303-316.
76. Promislow JH, Baird DD, Wilcox AJ, Weinberg CR. Bleeding following pregnancy loss before 6 weeks' gestation. Hum Reprod 2007;22:853-857.
77. Quenby S, Vince G, Farquharson R, Aplin J. Recurrent miscarriage: a defect in nature's quality control? Hum Reprod 2002;17:1959-1963.
78. Quenby S, Nik H, Innes B, Lash G, Turner M, Drury J, Bulmer J. Uterine natural killer cells and angiogenesis in recurrent reproductive failure. Hum Reprod 2009;24:45-54.
79. Rai R, Regan L. Recurrent miscarriage. Lancet 2006;368:601-611.
80. Salamonsen LA, Woolley DE. Menstruation: induction by matrix metalloproteinases and inflammatory cells. J Reprod Immunol 1999;44:1-27.
81. Salker M, Teklenburg G, Molokhia M, Lavery S, Trew G, Aojanepong T, Mardon HJ, Lokugamage AU, Rai R, Landles C et al. Natural selection of human embryos: impaired decidualization of endometrium disables embryo-maternal interactions and causes recurrent pregnancy loss. PLoS ONE 2010;5:e10287.
82. Serle E, Aplin JD, Li TC, Warren MA, Graham RA, Seif MW, Cooke ID. Endometrial differentiation in the peri-implantation phase of women with recurrent miscarriage: a morphological and immunohistochemical study. Fertil Steril 1994;62:989-996.
83. Simon L, Spiewak KA, Ekman GC, Kim J, Lydon JP, Bagchi MK, Bagchi IC, DeMayo FJ, Cooke PS. Stromal progesterone receptors mediate induction of Indian Hedgehog (IHH) in uterine epithelium and its downstream targets in uterine stroma. Endocrinology 2009;150:3871-3876.
84. Stevens VC. Some reproductive studies in the baboon. Hum Reprod Update 1997;3:533-540.
85. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F, Abbondanzo SJ. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992;359:76-79.
86. Tabibzadeh S, Mason JM, Shea W, Cai Y, Murray MJ, Lessey B. Dysregulated expression of ebaf, a novel molecular defect in the endometria of patients with infertility. J Clin Endocrinol Metab 2000;85:2526-2536.
87. Teklenburg G, Macklon NS. Review: in vitro models for the study of early human embryo-endometrium interactions. Reprod Sci 2009;16:811-818.
88. Teklenburg G, Salker M, Molokhia M, Lavery S, Trew G, Aojanepong T, Mardon HJ, Lokugamage AU, Rai R, Landles C et al. Natural selection of human embryos: decidualizing endometrial stromal cells serve as sensors of embryo quality upon implantation. PLoS ONE 2010;5:e10258.
89. Telgmann R, Maronde E, Tasken K, Gellersen B. Activated protein kinase A is required for differentiation-dependent transcription of the decidual prolactin gene in human endometrial stromal cells. Endocrinology 1997;138:929-937.
90. Tietze C, Guttmacher AF, Rubin S. Time required for conception in 1727 planned pregnancies. Fertil Steril 1950;1:338-346.
91. van den Heuvel MJ, Xie X, Tayade C, Peralta C, Fang Y, Leonard S, Paffaro VA Jr. Sheikhi AK, Murrant C, Croy BA. A review of trafficking and activation of uterine natural killer cells. Am J Reprod Immunol 2005;54:322-331.
92. van Oppenraaij RH, Jauniaux E, Christiansen OB, Horcajadas JA, Farquharson RG, Exalto N. Predicting adverse obstetric outcome after early pregnancy events and complications: a review. Hum Reprod Update 2009;15:409-421.
93. Vanneste E, Voet T, Le CC, Ampe M, Konings P, Melotte C, Debrock S, Amyere M, Vikkula M, Schuit F et al. Chromosome instability is common in human cleavage-stage embryos. Nat Med 2009;15:577-583.
94. Venturoli S, Porcu E, Fabbri R, Magrini O, Gammi L, Paradisi R, Flamigni C. Longitudinal evaluation of the different gonadotropin pulsatile patterns in anovulatory cycles of young girls. J Clin Endocrinol Metab 1992;74:836-841.
95. Vitiello D, Kodaman PH, Taylor HS. HOX genes in implantation. Semin Reprod Med 2007;25:431-436.
96. Viudes-de-Castro MP, Vicente JS. Effect of sperm count on the fertility and prolificity rates of meat rabbits. Anim Reprod Sci 1997;46:313-319.
97. Voullaire L, Slater H, Williamson R, Wilton L. Chromosome analysis of blastomeres from human embryos by using comparative genomic hybridization. Hum Genet 2000;106:210-217.
98. Wagner GP, Lynch VJ. Evolutionary novelties. Curr Biol 2010;20:R48-R52.
99. Wang X, Chen C, Wang L, Chen D, Guang W, French J. Conception, early pregnancy loss, and time to clinical pregnancy: a population-based prospective study. Fertil Steril 2003;79:577-584.
100. Wells D, Delhanty JD. Comprehensive chromosomal analysis of human preimplantation embryos using whole genome amplification and single cell comparative genomic hybridization. Mol Hum Reprod 2000;6:1055-1062.
101. Wilcox AJ, Weinberg CR, Baird DD. Timing of sexual intercourse in relation to ovulation. Effects on the probability of conception, survival of the pregnancy, and sex of the baby. N Engl J Med 1995;333:1517-1521.
102. Wilcox AJ, Baird DD, Weinberg CR. Time of implantation of the conceptus and loss of pregnancy. N Engl J Med 1999;340:1796-1799.
103. Zhou L, Li R, Wang R, Huang HX, Zhong K. Local injury to the endometrium in controlled ovarian hyperstimulation cycles improves implantation rates. Fertil Steril 2008;89:1166-1176.