Pinopodes, leukemia inhibitory factor, integrin-β3, and mucin-1 expression in the peri-implantation endometrium of women with unexplained recurrent pregnancy loss

Fertility and Sterility

Volumn 98, Issue 2, 2012, Pages 389-395

  Xu, Bufang ^a   Sun, Xiaoxi ^b   Li, Lu ^b   Wu, Ling ^a   Zhang, Aijun ^a   Feng, Yun ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

Author keywords

Endometrial receptivity; implantation; pinopodes; recurrent pregnancy loss

Indexed keywords

BETA3 INTEGRIN; ESTROGEN; FOLLITROPIN; LEUKEMIA INHIBITORY FACTOR; LUTEINIZING HORMONE; MUCIN 1;

ADULT; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; ENDOMETRIUM; ENDOMETRIUM BIOPSY; ESTROGEN BLOOD LEVEL; FEMALE; FOLLITROPIN BLOOD LEVEL; HORMONE BLOOD LEVEL; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INFERTILITY THERAPY; LUTEINIZING HORMONE BLOOD LEVEL; MAJOR CLINICAL STUDY; MORPHOLOGY; PINOPODE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECURRENT PREGNANCY LOSS; SCANNING ELECTRON MICROSCOPY; SPONTANEOUS ABORTION; UTERUS;

ABORTION, HABITUAL; ADULT; EMBRYO IMPLANTATION; ENDOMETRIUM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INFERTILITY, FEMALE; INTEGRIN BETA3; LEUKEMIA INHIBITORY FACTOR; MUCIN-1; PREGNANCY;

EID: 84864460637     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2012.04.032     Document Type: Article

References (36)

1. E. Tuckerman, S.M. Laird, R. Stewart, M. Wells, and T.C. Li Markers of endometrial function in women with unexplained recurrent pregnancy loss: a comparison between morphologically normal and retarded endometrium Hum Reprod 19 2004 196 205
2. R. Rai, and L. Regan Recurrent miscarriage Lancet 368 2006 601 611
3. C. Bulletti, C. Flamigni, and E. Giacomucci Reproductive failure due to spontaneous abortion and recurrent pregnancy loss Hum Reprod Update 2 1996 118 136
4. A.J. Wilcox, D.D. Baird, and C.R. Weinberg Time of implantation of the conceptus and loss of pregnancy N Engl J Med 340 1999 1796 1799
5. G. Teklenburg, M. Salker, C. Heijnen, N.S. Macklon, and J.J. Brosens The molecular basis of recurrent pregnancy loss: impaired natural embryo selection Mol Hum Reprod 16 2010 886 895
6. D.D. Carson, I. Bagchi, S.K. Dey, A.C. Enders, A.T. Fazleabas, and B.A. Lessey Embryo implantation Dev Biol 223 2000 217 237
7. G. Nikas, and A. Markrigiannakis Endometrial pinopodes and uterine receptivity Ann NY Acad Sci 997 2003 120 123
8. I. Oborná, R. Novotný, J. Brezinová, P. Petrová, V. Lichnovský, and H. Fingerová Changes in the development of uterine pinopodes in steroid hormone supplemented cycles Physiol Res 53 2004 423 429
9. A.W. Horne, J.O. White, el-N. Lalani, M.A. Mobberley, R.A. Margara, and G.H. Trew Analysis of epitopes on endometrial epithelium by scanning immunoelectron microscopy Biochem Biophys Res Commun 22 2002 102 108
10. C.E. Quinn, and R.F. Casper Pinopodes: a questionable role in endometrial receptivity Hum Reprod Update 15 2009 229 236
11. I.K. Gipson, T. Blalock, A. Tisdale, S. Spurr-Michaud, S. Allcorn, and A. Stavreus-Evers MUC16 is lost from the uterodome (pinopode) surface of the receptive human endometrium: in vitro evidence that MUC16 is a barrier to trophoblast adherence Biol Reprod 78 2008 134 142
12. L. Aghajanova, A. Stavreus-Evers, Y. Nikas, O. Hovatta, and B.M. Landgren Coexpression of pinopodes and leukemia inhibitory factor, as well as its receptor, in human endometrium Fertil Steril 79 Suppl 1 2003 808 814
13. E.B. Cullinan, S.J. Abbondanzo, P.S. Anderson, J.W. Pollard, B.A. Lessey, and C.L. Stewart Leukemia inhibitory factor (LIF) and LIF receptor expression in human endometrium suggests a potential autocrine/paracrine function in regulating embryo implantation Proc Natl Acad Sci USA 93 1996 3115 3120
14. M. Creus, J. Ordi, F. Fábregues, R. Casamitjana, B. Ferrer, and E. Coll Alphavbeta3 integrin expression and pinopod formation in normal and out-of-phase endometria of fertile and infertile women Hum Reprod 17 2002 2279 2286
15. B.A. Lessey, A.J. Castelbaum, C.A. Buck, Y. Lei, C.W. Yowell, and J. Sun Further characterization of endometrial integrins during the menstrual cycle and in pregnancy Fertil Steril 62 1994 497 506
16. B.A. Lessey, A.J. Castelbaum, S.W. Sawin, and J. Sun Integrins as markers of uterine receptivity in women with primary unexplained infertility Fertil Steril 63 1995 535 542
17. E. Serle, J.D. Aplin, T.C. Li, M.A. Warren, R.A. Graham, and M.W. Seif Endometrial differentiation in the peri-implantation phase of women with recurrent pregnancy loss: a morphological and immunohistochemical study Fertil Steril 62 1994 989 996
18. T.C. Li, E.M. Tuckerman, and S.M. Laird Endometrium factors in recurrent pregnancy loss Hum Reprod Update 8 2002 43 52
19. S. Quenby, G. Vince, R. Farquharson, and J. Aplin Recurrent pregnancy loss: a defect in nature's quality control? Hum Reprod 17 2002 1959 1963
20. J.D. Aplin, N.A. Hey, and T.C. Li MUC1 as a cell surface and secretory component of endometrial epithelium: reduced levels in recurrent pregnancy loss Am J Reprod Immunol 35 1996 261 266
21. A.W. Horne, E.N. Lalani, R.A. Margara, T.A. Ryder, M.A. Mobberley, and J.O. White The expression pattern of MUC1 glycoforms and other biomarkers of endometrial receptivity in fertile and infertile women Mol Reprod 72 2005 216 229
22. C. Quinn, E. Ryan, E.A. Claessens, E. Greenblatt, P. Hawrylyshyn, and B. Cruickshank The presence of pinopodes in the human endometrium does not delineate the implantation window Fertil Steril 87 2007 1015 1021
23. L.J. Song, R.J. Liu, Z. Zeng, S.L. Alper, H.J. Cui, and Y. Lu Gastrin inhibits a novel, pathological colon cancer signaling pathway involving EGR1, AE2, and P-ERK J Mol Med (Berl) 90 2012 707 718
24. H. Wang, E. Isaksson, B. von Schoultz, J.M. Cline, and L. Sahlin Effect of long-term treatment with steroid hormones or tamoxifen on the progesterone receptor and androgen receptor in the endometrium of ovariectomized cynomolgus macaques Reprod Biol Endocrinol 1 2003 7
25. L. Li, B.F. Xu, Q.J. Chen, and X.X. Sun Effects of hydrosalpinx on pinopodes, leukaemia inhibitory factor, integrin beta3 and MUC1 expression in the peri-implantation endometrium Eur J Obstet Gynecol Reprod Biol 151 2010 171 175
26. M. Salker, G. Teklenburg, M. Molokhia, S. Lavery, G. Trew, and T. Aojanepong Natural selection of human embryos: impaired decidualization of endometrium disables embryo-maternal interactions and causes recurrent pregnancy loss PLoS One 5 2010 e10287
27. S.M. Adams, N. Gayer, M.J. Hosie, and C.R. Murphy Human uterodomes (pinopods) do not display pinocytotic function Hum Reprod 17 2002 1980 1986
28. C.E. Quinn, J. Detmar, and R.F. Casper Pinopodes are present in Lif null and Hoxa10 null mice Fertil Steril 88 Suppl 4 2007 1021 1028
29. A. Zhioua, H. Elloumi, S. Fourati, G. Merdassi, A. Ben Ammar, and B.S. Sajia Morphometric analysis of the human endometrium during the implantation window. Light and transmission electron microscopy study J Gynecol Obstet Biol Reprod (Paris) 41 2012 235 242
30. M. Mikoajczyk, J. Skrzypczak, and P. Wirstlein No correlation between pinopode formation and LIF and MMP2 expression in endometrium during implantation window Folia Histochem Cytobiol 49 2011 615 621
31. S. Quenby, M. Anim-Somuah, C. Kalumbi, R. Farquharson, and J.D. Aplin Different types of recurrent miscarriage are associated with varying patterns of adhesion molecule expression in endometrium Reprod Biomed Online 14 2007 224 234
32. M. Meseguer, A. Pellicer, and C. Simon MUC1 and endometrial receptivity Mol Hum Reprod 4 1998 1089 1098
33. M.M. DeSouza, G.A. Surveyor, R.E. Price, J. Julian, R. Kardon, and X. Zhou MUC1/episialin: a critical barrier in the female reproductive tract Reprod Immunol 45 1999 127 158
34. N.A. Hey, T.C. Li, P.L. Devine, R.A. Graham, H. Saravelos, and J.D. Aplin MUC1 in secretory phase endometrium: expression in precisely dated biopsies and flushings from normal and recurrent pregnancy loss patients Hum Reprod 10 1995 2655 2662
35. J.D. Aplin, N.A. Hey, and R.A. Graham Human endometrial MUC1 carries keratan sulphate: characteristic glycoforms in the luminal epithelium at receptivity Glycobiology 8 1998 269 276
36. N.A. Hey, R.A. Graham, M.W. Seif, and J.D. Aplin The polymorphic epithelial mucin MUC1 is regulated with maximal expression in the implantation phase J Clin Endocrinol Metab 78 1994 337 342