The science of implantation emerges blinking into the light

Reproductive BioMedicine Online

Volumn 27, Issue 5, 2013, Pages 453-460

  Sharkey, Andrew M ^a   Macklon, Nick S ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

embryo; endometrium; implantation; infertility; receptivity

Indexed keywords

ACETYLSALICYLIC ACID; CHORIONIC GONADOTROPIN; CORTICOSTEROID; ESTROGEN; GROWTH FACTOR; LOW MOLECULAR WEIGHT HEPARIN; MICRORNA; PROGESTERONE;

BASEMENT MEMBRANE; BLASTOCYST; DECIDUA; ENDOMETRIUM; ENDOMETRIUM BIOPSY; EPITHELIUM; FERTILIZATION; GENE EXPRESSION; HUMAN; INFERTILITY THERAPY; NIDATION; NONHUMAN; REVIEW; STROMA CELL; TROPHOBLAST; UTERUS FLUID;

EMBRYO; ENDOMETRIUM; IMPLANTATION; INFERTILITY; RECEPTIVITY;

CELL COMMUNICATION; CELLULAR MICROENVIRONMENT; EMBRYO IMPLANTATION; EMBRYO, MAMMALIAN; ENDOMETRIUM; FEMALE; HUMANS; INFERTILITY, FEMALE; PLACENTATION; PREGNANCY;

EID: 84887320489     PISSN: 14726483     EISSN: 14726491     Source Type: Journal    
DOI: 10.1016/j.rbmo.2013.08.005     Document Type: Review

References (59)

1. S. Altmäe, J.A. Martinez-Conejero, F.J. Esteban, M. Ruiz-Alonso, A. Stavreus-Evers, J.A. Horcajadas, and A. Salumets MicroRNAs miR-30b, miR-30d, and miR-494 regulate human endometrial receptivity Reprod. Sci. 20 2013 308 317 10.1177/1933719112453507
2. U. Bentin-Ley, and A. Lopata In vitro models of human blastocyst implantation Baillieres Best Pract. Res. Clin. Obstet. Gynaecol. 14 2000 765 774
3. C.M. Boomsma, A. Kavelaars, M.J. Eijkemans, E.G. Lentjes, B.C. Fauser, C.J. Heijnen, and N.S. Macklon Endometrial secretion analysis identifies a cytokine profile predictive of pregnancy in IVF Hum. Reprod. 24 2009 1427 1435
4. R.O. Burney, S. Talbi, A.E. Hamilton, K.C. Vo, M. Nyegaard, C.R. Nezhat, B.A. Lessey, and L.C. Giudice Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis Endocrinology 148 2007 3814 3826
5. H. Cakmak, and H.S. Taylor Implantation failure: molecular mechanisms and clinical treatment Hum. Reprod. Update 17 2011 242 253 10.1093/humupd/dmq037
6. A. Chakrabarty, S. Tranguch, T. Daikoku, K. Jensen, H. Furneaux, and S.K. Dey MicroRNA regulation of cyclooxygenase-2 during embryo implantation Proc. Natl. Acad. Sci. U. S. A. 104 2007 15144 15149
7. Y. Cheong, C. Boomsma, C. Heijnen, and N. Macklon Uterine secretomics: a window on the maternal-embryo interface Fertil. Steril. 99 2013 093 99
8. W.N. Cooper, B. Khulan, S. Owens, C.E. Elks, V. Seidel, A.M. Prentice, G. Belteki, K.K. Ong, N.A. Affara, M. Constancia, and D.B. Dunger DNA methylation profiling at imprinted loci after periconceptional micronutrient supplementation in humans: results of a pilot randomized controlled trial FASEB J. 26 2012 1782 1790
9. P. Díaz-Gimeno, J.A. Horcajadas, J.A. Martínez-Conejero, F.J. Esteban, P. Alamá, A. Pellicer, and C.A. Simón Genomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature Fertil. Steril. 95 2011 50 60
10. W.C. Duncan, J.L. Shaw, S. Burgess, S.E. McDonald, H.O. Critchley, and A.W. Horne Ectopic pregnancy as a model to identify endometrial genes and signaling pathways important in decidualization and regulated by local trophoblast PLoS One 6 2011 e23595 10.1371/journal.pone.0023595
11. T.A. Edgell, L.J.F. Rombauts, and L.A. Salamonsen Assessing receptivity in the endometrium: the need for a rapid, non-invasive test Reprod. Biomed. Online 27 2013 486 496
12. J. Evans, N.J. Hannan, C. Hincks, L.J. Rombauts, and L.A. Salamonsen Defective soil for a fertile seed? Altered endometrial development is detrimental to pregnancy success PLoS One 7 2012 e53098
13. G.E. Evans, J.A. Martínez-Conejero, G.T. Phillipson, C. Simón, L.A. McNoe, P.H. Sykes, J.A. Horcajadas, E.Y. Lam, C.G. Print, I.L. Sin, and J.J. Evans Gene and protein expression signature of endometrial glandular and stromal compartments during the window of implantation Fertil. Steril. 97 2012 1365 1373
14. H.M. Fatemi, and B. Popovic-Todorovic Implantation in ART: a look at endometrial receptivity Reprod. Biomed. Online 27 2013 530 538
15. W. Filipowicz, S.N. Bhattacharyya, and N. Sonenberg Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 9 2008 102 114 10.1038/nrg2290
16. T.P. Fleming, M.A. Velazquez, J.J. Eckert, E.S. Lucas, and A.J. Watkins Nutrition of females during the peri-conceptional period and effects on foetal programming and health of offspring Anim. Reprod. Sci. 130 2012 193 197
17. B. Gellersen, I.A. Brosens, and J.J. Brosens Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives Sem. Reprod. Med. 25 2007 445 453
18. D. Haouzi, H. Dechaud, S. Assou, J. De Vos, and S. Hamamah Insights into human endometrial receptivity from transcriptomic and proteomic data Reprod. Biomed. Online 24 2012 23 34
19. A.T. Hertig, J. Rock, and E.C. Adams A description of 34 human ova within the first 17 days of development Am. J. Anat. 98 1956 435 493
20. J.A. Horcajadas, P. Mínguez, J. Dopazo, F.J. Esteban, F. Domínguez, L.C. Giudice, A. Pellicer, and C. Simón Controlled ovarian stimulation induces a functional genomic delay of the endometrium with potential clinical implications J. Clin. Endocrinol. Metab. 93 2008 4500 4510
21. A.W. Horne, W.C. Duncan, A.E. King, S. Burgess, P.C. Lourenco, P. Cornes, P. Ghazal, A.R. Williams, L. Udby, and H.O. Critchley Endometrial cysteine-rich secretory protein 3 is inhibited by human chorionic gonadotrophin, and is increased in the decidua of tubal ectopic pregnancy Mol. Hum. Reprod. 15 2009 287 294 10.1093/molehr/gap019
22. M.L. Hull, and V. Nisenblat Tissue and circulating microRNAs influence reproductive function in endometrial disease Biomed. Online 27 2013 515 529
23. S. Kuokkanen, B. Chen, L. Ojalvo, L. Benard, N. Santoro, and J.W. Pollard Genomic profiling of microRNAs and messenger RNAs reveals hormonal regulation in microRNA expression in human endometrium Biol. Reprod. 82 2010 791 801 10.1095/biolreprod.109.081059
24. D.H. Ledbetter Chaos in the embryo Nat. Med. 15 2009 490 491 10.1038/nm0509-490
25. B.A. Lessey Implantation defects in infertile women with endometriosis Ann. N. Y. Acad. Sci. 955 2002 265 280
26. B.A. Lessey Assessment of endometrial receptivity Fertil. Steril. 96 2011 522 529 10.1016/j.fertnstert.2011.07.1095
27. 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
28. P. Licht, H. Fluhr, J. Neuwinger, D. Wallwiener, and L. Wildt Is human chorionic gonadotropin directly involved in the regulation of human implantation? Mol. Cell. Endocrinol. 269 2007 85 92
29. S. Lindenberg Ultrastructure in human implantation: transmission and scanning electron microscopy Baillieres Clin. Obstet. Gynaecol. 5 1991 1 14
30. E. Lucas Epigenetic effects on the embryo as a result of periconceptional environment and ART Reprod. Biomed. Online 27 2013 477 485
31. E. Lucas, M.S. Salker, and J.J. Brosens Uterine plasticity and reproductive fitness Biomed. Online 27 2013 506 514
32. N.S. Macklon, J.P. Geraedts, and B.C. Fauser Conception to ongoing pregnancy: the 'black box' of early pregnancy loss Hum. Reprod. Update 8 2002 333 343
33. B.A. Malizia, L.E. Dodge, A.S. Penzias, and M.R. Hacker The cumulative probability of liveborn multiples after in vitro fertilization: a cohort study of more than 10,000 women Fertil. Steril. 99 2013 393 399 10.1016/j.fertnstert. 2012.10.018
34. M.R.W. Mann, and M.M. Denomme Maternal control of genomic imprint maintenance Reprod. Biomed. Online (in press). 2013 10.1016/j.rbmo.2013.06.004
35. M. Montag, B. Toth, and T. Strowitzki New approaches to embryo selection Reprod. Biomed. Online 27 2013 539 546
36. D. Navot, P.A. Bergh, M. Williams, G.J. Garrisi, I. Guzman, B. Sandler, J. Fox, P. Schreiner-Engel, G.E. Hofmann, and L. Grunfeld An insight into early reproductive processes through the in vivo model of ovum donation J. Clin. Endocrinol. Metab. 72 1991 408 414
37. E.C. Nelissen, A.P. Van Montfoort, L.J. Smits, P.P. Menheere, J.L. Evers, E. Coonen, J.G. Derhaag, L.L. Peeters, A.B. Coumans, and J.C. Dumoulin IVF culture medium affects human intrauterine growth as early as the second trimester of pregnancy Hum. Reprod. 28 2013 2067 2074
38. Q. Pan, X. Luo, T. Toloubeydokhti, and N. Chegini The expression profile of micro-RNA in endometrium and endometriosis and the influence of ovarian steroids on their expression Mol. Hum. Reprod. 13 2007 797 806
39. A. Psychoyos Uterine receptivity for nidation Ann. N. Y. Acad. Sci. 476 1986 36 42
40. A. Revel, H. Achache, J. Stevens, Y. Smith, and R. Reich MicroRNAs are associated with human embryo implantation defects Hum. Reprod. 26 2011 2830 2840 10.1093/humrep/der255
41. M. Ruiz-Alonso, D. Blesa, and C. Simón The genomics of the human endometrium Biochim. Biophys. Acta 1822 2012 1931 1942
42. M. Ruiz-Alonso, D. Blesa, P. Díaz-Gimeno, E. Gómez, M. Fernández-Sánchez, F. Carranza, J. Carrera, F. Vilella, A. Pellicer, and C. Simón The endometrial receptivity array for diagnosis and personalized embryo transfer as a treatment for patients with repeated implantation failure Fertil. Steril. 2013 10.1016/j.fertnstert.2013.05.004 pii:S0015-0282(13)00567-0
43. L.A. Salamonsen, T. Edgell, L.J. Rombauts, A.N. Stephens, D.M. Robertson, A. Rainczuk, G. Nie, and N.J. Hannan Proteomics of the human endometrium and uterine fluid: a pathway to biomarker discovery Fertil. Steril. 99 2013 1086 1092 10.1016/j.fertnstert.2012.09.013
44. M.S. Salker, M. Christian, J.H. Steel, J. Nautiyal, S. Lavery, G. Trew, Z. Webster, M. Al-Sabbagh, G. Puchchakayala, M. Föller, C. Landles, A.M. Sharkey, S. Quenby, J.D. Aplin, L. Regan, F. Lang, and J.J. Brosens Deregulation of the serum- and glucocorticoid-inducible kinase SGK1 in the endometrium causes reproductive failure Nat. Med. 17 2011 1509 1513 10.1038/nm.2498
45. C. Schwarzer, T.C. Esteves, M.J. Arauzo-Bravo, S. Le Gac, V. Nordhoff, S. Schlatt, and M. Boiani ART culture conditions change the probability of mouse embryo gestation through defined cellular and molecular responses Hum. Reprod. 27 2012 2627 2640
46. C.E. Senner The role of DNA methylation in mammalian development Reprod. Biomed. Online 22 2011 529 535
47. J.R. Sherwin, A.M. Sharkey, P. Cameo, P.M. Mavrogianis, R.D. Catalano, S. Edassery, and A.T. Fazleabas Identification of novel genes regulated by chorionic gonadotropin in baboon endometrium during the window of implantation Endocrinology 148 2007 618 626
48. J.R. Sherwin, J.M. Hastings, K.S. Jackson, P.A. Mavrogianis, A.M. Sharkey, and A.T. Fazleabas The endometrial response to chorionic gonadotropin is blunted in a baboon model of endometriosis Endocrinology 151 2010 4982 4993
49. C. Simón, M.J. Gimeno, A. Mercader, J.E. O'Connor, J. Remohí, M.L. Polan, and A. Pellicer Embryonic regulation of integrins beta 3, alpha 4, and alpha 1 in human endometrial epithelial cells in vitro J. Clin. Endocrinol. Metab. 82 1997 2607 2616
50. S. Sunderam, D.M. Kissin, L. Flowers, J.E. Anderson, S.G. Folger, D.J. Jamieson, W.D. Barfield Centers for Disease Control and Prevention (CDC) Assisted reproductive technology surveillance - United States, 2009 MMWR Surveill. Summ. 61 2012 1 23
51. G. Teklenburg, M. Salker, M. Molokhia, S. Lavery, G. Trew, T. Aojanepong, H.J. Mardon, A.U. Lokugamage, R. Rai, C. Landles, B.A. Roelen, S. Quenby, E.W. Kuijk, A. Kavelaars, C.J. Heijnen, L. Regan, J.J. Brosens, and N.S. Macklon Natural selection of human embryos: decidualizing endometrial stromal cells serve as sensors of embryo quality upon implantation PLoS One 5 2010 e10258
52. M.E. Torres-Padilla Generating different epigenotypes Reprod. Biomed. Online 2013 10.1016/j.rbmo.2013.07.016 (in press)
53. I. Van Vaerenbergh, R. McIntire, L. Van Lommel, P. Devroey, L. Giudice, and C. Bourgain Gene expression during successful implantation in a natural cycle Fertil. Steril. 93 2010 268.e15 268.e18 10.1016/j.fertnstert.2009.08.057
54. E. Walters A new title to an old song: some observations on the conduct of meta-analyses Reprod. Biomed. Online 27 2013 562 567
55. H. Wang, and S.K. Dey Roadmap to embryo implantation: clues from mouse models Nat. Rev. Genet. 7 2006 185 199
56. A.J. Watkins, D. Platt, T. Papenbrock, A. Wilkins, J.J. Eckert, W.Y. Kwong, C. Osmond, M. Hanson, and T.P. Fleming Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure Proc. Natl. Acad. Sci. U. S. A. 104 2007 5449 5454
57. C.H.E. Weimar, E.D. Post Uiterweer, G. Teklenburg, C.J. Heijnen, and N.S. Macklon In-vitro model systems for the study of human embryo-endometrial interactions Reprod. Biomed. Online 27 2013 461 476
58. C.H. Weimar, A. Kavelaars, J.J. Brosens, B. Gellersen, J.M. de Vreeden-Elbertse, C.J. Heijnen, and N.S. Macklon Endometrial stromal cells of women with recurrent miscarriage fail to discriminate between high- and low-quality human embryos PLoS One 7 2012 e41424 10.1371/journal.pone.0041424
59. S. Young Oestrogen and progesterone action on endometrium: a translational approach to understanding embryo receptivity Reprod. Biomed. Online 27 2013 497 505