Physiology and Pathology of Implantation in the Human and Nonhuman Primate

Asgerally T. Fazleabas

doi:10.1055/s-2007-991037

Seminars in Reproductive Medicine, Table of Contents

Semin Reprod Med 2007; 25(6): 405-409
DOI: 10.1055/s-2007-991037

PREFACE

Physiology and Pathology of Implantation in the Human and Nonhuman Primate

Asgerally T. Fazleabas¹ Guest Editor

¹Department of Obstetrics & Gynecology, University of Illinois College of Medicine, Chicago, Illinois

Abstract

ABSTRACT

Infertility affects 10 to 15% of the general population, and although advances in assisted reproductive therapies have had a major input, pregnancy rates continue to be relatively low. This has lead to an increasing interest in understanding the interaction between the embryo and the endometrium during the window of implantation. Multiple experimental approaches have been used to evaluate the morphological, cellular, and molecular changes in the endometrium during the normal menstrual cycle and as a consequence of numerous benign gynecological diseases that contribute to infertility. Successful implantation requires interplay between the embryo and the endometrium during a very narrow window of time within the menstrual cycle. Given that there are limitations to evaluating this intricate dialog in the human, nonhuman primates serve as a valuable model by which to obtain insights into this critical period of uterine receptivity. Articles in this issue provide a comprehensive summary of approaches to understand the complex biology that is required for successful implantation, and the potential adverse consequences of ovarian hyperstimulation and benign gynecological diseases on uterine receptivity and embryo implantation.

KEYWORDS

Uterine receptivity - embryo - implantation - endometrial pathologies - infertility

Full Text

References

REFERENCES

1 Spandorfer S D, Davis O K, Barmat L I, Chung P H, Rosenwaks Z. Relationship between maternal age and aneuploidy in in vitro fertilization pregnancy loss. Fertil Steril. 2004; 81 1265-1269
2 Norwitz E R, Schust D J, Fisher S J. Implantation and the survival of early pregnancy. N Engl J Med. 2001; 345 1400-1408
3 Everett C. Incidence and outcome of bleeding before the 20th week of pregnancy: prospective study from general practice. BMJ. 1997; 315 32-34
4 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
5 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
6 Nybo Andersen A M, Wohlfahrt J, Christens P, Olsen J, Melbye M. Maternal age and fetal loss: population based register linkage study. BMJ. 2000; 320 1708-1712
7 Tabibzadeh S. Molecular control of the implantation window. Hum Reprod Update. 1998; 4 465-471
8 Muyan M, Boime I. Secretion of chorionic gonadotropin from human trophoblasts. Placenta. 1997; 18 237-241
9 Niswender G D, Juengel J L, Silva P J, Rollyson M K, McIntush E W. Mechanisms controlling the function and life span of the corpus luteum. Physiol Rev. 2000; 80 1-29
10 Cameo P, Szmidt M, Strakova Z, Mavrogianis P, Sharpe-Timms K L, Fazleabas A T. Decidualization regulates the expression of the endometrial chorionic gonadotropin receptor in the primate. Biol Reprod. 2006; 75 681-689
11 Fazleabas A T, Donnelly K M, Srinivasan S, Fortman J D, Miller J B. Modulation of the baboon (Papio anubis) uterine endometrium by chorionic gonadotrophin during the period of uterine receptivity. Proc Natl Acad Sci USA. 1999; 96 2543-2548
12 Sherwin J R, Sharkey A M, Cameo P et al.. Identification of novel genes regulated by chorionic gonadotropin in baboon endometrium during the window of implantation. Endocrinology. 2007; 148 618-626
13 Lessey B A. Two pathways of progesterone action in the human endometrium: implications for implantation and contraception. Steroids. 2003; 68 809-815
14 Ma W G, Song H, Das S K, Paria B C, Dey S K. 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
15 Garcia E, Bouchard P, De Brux J et al.. Use of immunocytochemistry of progesterone and estrogen receptors for endometrial dating. J Clin Endocrinol Metab. 1988; 67 80-87
16 Carson D D, Lagow E, Thathiah A et al.. Changes in gene expression during the early to mid-luteal (receptive phase) transition in human endometrium detected by high-density microarray screening. Mol Hum Reprod. 2002; 8 871-879
17 Kao L C, Tulac S, Lobo S et al.. Global gene profiling in human endometrium during the window of implantation. Endocrinology. 2002; 143 2119-2138
18 Adams E C, Hertig A T, Rock J. A description of 34 human ova within the first 17 days of development. Am J Anat. 1956; 98 435-493
19 Enders A C, Schlafke S, Hendrickx A G. Differentiation of the embryonic disc, amnion, and yolk sac in the rhesus monkey. Am J Anat. 1986; 177 161-185
20 Lee K Y, DeMayo F J. Animal models of implantation. Reproduction. 2004; 128 679-695
21 Dey S K, Lim H, Das S K et al.. Molecular cues to implantation. Endocr Rev. 2004; 25 341-373
22 Fazleabas A T, Kim J J, Srinivasan S. Implantation in the baboon: endometrial responses. Semin Reprod Endocrinol. 1999; 17 257-265
23 Lobo S C, Srisuparp S, Peng X, Fazleabas A T. Uterine receptivity in the baboon: modulation by chorionic gonadotropin. Semin Reprod Med. 2001; 19 69-74
24 Srisuparp S, Strakova Z, Brudney A et al.. Signal transduction pathways activated by chorionic gonadotropin in the primate endometrial epithelial cells. Biol Reprod. 2003; 68 457-464
25 Banaszak S, Brudney A, Donnelly K, Chai D, Chwalisz K, Fazleabas A T. Modulation of the action of chorionic gonadotropin in the baboon (Papio anubis) uterus by a progesterone receptor antagonist (ZK 137. 316). Biol Reprod. 2000; 63 820-825
26 Christensen S, Verhage H G, Nowak G et al.. Smooth muscle myosin II and alpha smooth muscle actin expression in the baboon (Papio anubis) uterus is associated with glandular secretory activity and stromal cell transformation. Biol Reprod. 1995; 53 598-608
27 Rao C V. An overview of the past, present, and future of nongonadal LH/hCG actions in reproductive biology and medicine. Semin Reprod Med. 2001; 19 7-17
28 Reshef E, Lei Z M, Rao C V, Pridham D D, Chegini N, Luborsky J L. The presence of gonadotropin receptors in nonpregnant human uterus, human placenta, fetal membranes, and decidua. J Clin Endocrinol Metab. 1990; 70 421-430
29 Jasinska A, Strakova Z, Szmidt M, Fazleabas A T. Human chorionic gonadotropin and decidualization in vitro inhibits cytochalasin-D-induced apoptosis in cultured endometrial stromal fibroblasts. Endocrinology. 2006; 147 4112-4121
30 Lovely L P, Fazleabas A T, Fritz M A, McAdams D G, Lessey B A. Prevention of endometrial apoptosis: randomized prospective comparison of human chorionic gonadotropin versus progesterone treatment in the luteal phase. J Clin Endocrinol Metab. 2005; 90 2351-2356
31 Kim J J, Jaffe R C, Fazleabas A T. Blastocyst invasion and the stromal response in primates. Hum Reprod. 1999; 14(Suppl 2) 45-55
32 Kim J J, Jaffe R C, Fazleabas A T. Insulin-like growth factor binding protein-1 expression in baboon endometrial stromal cells: regulation by filamentous actin and requirement for de novo protein synthesis. Endocrinology. 1999; 140 997-1004
33 Strakova Z, Mavrogianis P, Meng X et al.. In vivo infusion of interleukin-1beta and chorionic gonadotropin induces endometrial changes that mimic early pregnancy events in the baboon. Endocrinology. 2005; 146 4097-4104
34 Bentin-Ley U, Pedersen B, Lindenberg S, Larsen J F, Hamberger L, Horn T. Isolation and culture of human endometrial cells in a three-dimensional culture system. J Reprod Fertil. 1994; 101 327-332
35 Mercader A, Garcia-Velasco J A, Escudero E, Remohi J, Pellicer A, Simon C. Clinical experience and perinatal outcome of blastocyst transfer after coculture of human embryos with human endometrial epithelial cells: a 5-year follow-up study. Fertil Steril. 2003; 80 1162-1168
36 Ponnampalam A P, Weston G C, Trajstman A C, Susil B, Rogers P A. Molecular classification of human endometrial cycle stages by transcriptional profiling. Mol Hum Reprod. 2004; 10 879-893
37 Punyadeera C, Dassen H, Klomp J et al.. Oestrogen-modulated gene expression in the human endometrium. Cell Mol Life Sci. 2005; 62 239-250
38 Talbi S, Hamilton A E, Vo K C et al.. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology. 2006; 147 1097-1121
39 Borthwick J M, Charnock-Jones D S, Tom B D et al.. Determination of the transcript profile of human endometrium. Mol Hum Reprod. 2003; 9 19-33
40 Mirkin S, Arslan M, Churikov D et al.. In search of candidate genes critically expressed in the human endometrium during the window of implantation. Hum Reprod. 2005; 20 2104-2117
41 Riesewijk A, Martin J, van Os R et al.. Gene expression profiling of human endometrial receptivity on days LH + 2 versus LH + 7 by microarray technology. Mol Hum Reprod. 2003; 9 253-264
42 Burney R O, Talbi S, Hamilton A E et al.. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology. 2007; 148 3814-3828
43 Horcajadas J A, Riesewijk A, Polman J et al.. Effect of controlled ovarian hyperstimulation in IVF on endometrial gene expression profiles. Mol Hum Reprod. 2005; 11 195-205
44 Fazleabas A T, Brudney A, Chai D, Langoi D, Bulun S E. Steroid receptor and aromatase expression in baboon endometriotic lesions. Fertil Steril. 2003; 80(suppl 2) 820-827
45 Fazleabas A T, Brudney A, Chai D, Mwenda J. Endometriosis in the baboon. Gynecol Obstet Invest. 2004; 57 46-47
46 Fazleabas A T, Brudney A, Gurates B, Chai D, Bulun S. A modified baboon model for endometriosis. Ann N Y Acad Sci. 2002; 955 308-317 discussion 340-302 396-406
47 Hastings J M, Fazleabas A T. A baboon model for endometriosis: implications for fertility. Reprod Biol Endocrinol. 2006; 4(suppl 1) S7
48 Hastings J M, Jackson K S, Mavrogianis P A, Fazleabas A T. The estrogen early response gene FOS is altered in a baboon model of endometriosis. Biol Reprod. 2006; 75 176-182
49 Gashaw I, Hastings J M, Jackson K S, Winterhager E, Fazleabas A T. Induced endometriosis in the baboon (Papio anubis) increases the expression of the proangiogenic factor CYR61 (CCN1) in eutopic and ectopic endometria. Biol Reprod. 2006; 74 1060-1066
50 Kim J J, Taylor H S, Lu Z et al.. Altered expression of HOXA10 in endometriosis: potential role in decidualization. Mol Hum Reprod. 2007; 13 323-332