Early stages of implantation as revealed by an in vitro model

Reproduction

Volumn 139, Issue 5, 2010, Pages 905-914

  Singh, H ^a   Nardo, L ^a   Kimber, S J ^a   Aplin, J D ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; MEDROXYPROGESTERONE ACETATE; MUCIN 1; SIALOMUCIN; STEROID HORMONE; STEROID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL ADHESION; CELL SURFACE; CONTROLLED STUDY; EMBRYO; EPITHELIUM; FEMALE; HATCHING; HUMAN; HUMAN CELL; IMPLANTATION; IN VITRO STUDY; MONOLAYER CULTURE; MOUSE; NONHUMAN; OVULATION; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; ZONA PELLUCIDA;

ANIMALS; ANTIGENS, CD164; BLASTOCYST; CELL LINE; DOWN-REGULATION; EMBRYO IMPLANTATION; EMBRYO, MAMMALIAN; ENDOMETRIUM; ESTRADIOL; ESTROGENS; FEMALE; MEDROXYPROGESTERONE ACETATE; MICE; MODELS, BIOLOGICAL; MUCIN-1; PREGNANCY; PROGESTINS; SUPEROVULATION; UP-REGULATION; ZONA PELLUCIDA;

MUS;

EID: 77951605880     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-09-0271     Document Type: Article

References (72)

1. Aplin JD 1991 Glycans as biochemical markers of human endometrial secretory differentiation. Journal of Reproduction and Fertility 92 525-541.
2. Aplin JD 1996 The cell biology of human implantation. Placenta 17 269-275.
3. Aplin JD 1997 Adhesion molecules in implantation. Reviews of Reproduction 2 84-93.
4. Aplin JD 2000 The cell biological basis of human implantation. Baillieres Best Practice & Research. Clinical Obstetrics & Gynaecology 14 757-764.
5. Aplin JD 2006 Embryo implantation: the molecular mechanism remains elusive. Reproductive Biomedicine Online 13 833-839.
6. Aplin JD & Kimber SJ 2004 Trophoblast-uterine interactions at implantation. Reproductive Biology and Endocrinology 2 48.
7. Aplin JD & Singh H 2008 Bioinformatics and transcriptomics studies of early implantation. Annals of the New York Academy of Sciences 1127 116-120. (Pubitemid 351563098)
8. Aplin JD, Hey NA & Li TC 1996 MUC1 as a cell surface and secretory component of endometrial epithelium: reduced levels in recurrent miscarriage. American Journal of Reproductive Immunology 35 261-266.
9. Aplin JD, Jones CJ, McGinlay PB, Croxatto HB & Fazleabas AT 1997 Progesterone regulates glycosylation in endometrium. Biochemical Society Transactions 25 1184-1187.
10. Aplin JD, Hey NA & Graham RA 1998 Human endometrial MUC1 carries keratan sulfate: characteristic glycoforms in the luminal epithelium at receptivity. Glycobiology 8 269-276.
11. Bentin-Ley U, Sjogren A, Nilsson L, Hamberger L, Larsen JF & Horn T 1999 Presence of uterine pinopodes at the embryo-endometrial interface during human implantation in vitro. Human Reproduction 14 515-520. (Pubitemid 29097411)
12. Bergh PA & Navot D 1992 The impact of embryonic development and endometrial maturity on the timing of implantation. Fertility and Sterility 58 537-542.
13. Cameo P, Srisuparp S, Strakova Z & Fazleabas AT 2004 Chorionic gonadotropin and uterine dialogue in the primate. Reproductive Biology and Endocrinology 2 50. (Pubitemid 39130529)
14. Campbell S, Seif MW, Aplin JD, Richmond SJ, Haynes P & Allen TD 1988 Expression of a secretory product by microvillous and ciliated cells of the human endometrial epithelium in vivo and in vitro. Human Reproduction 3 927-934. (Pubitemid 18267944)
15. Campbell S, Larsen J, Seif MW, Allen TD, Knox F, Jones CJ & Aplin JD 2000 Mosaic characteristics of human endometrial epithelium in vitro: analysis of secretory markers and cell surface ultrastructure. Molecular Human Reproduction 6 41-49. (Pubitemid 30043587)
16. Castelbaum AJ, Ying L, Somkuti SG, Sun J, Ilesanmi AO & Lessey BA 1997 Characterization of integrin expression in a well differentiated endometrial adenocarcinoma cell line (Ishikawa). Journal of Clinical Endocrinology and Metabolism 82 136-142. (Pubitemid 27021284)
17. Cervero A, Horcajadas JA, Dominguez F, Pellicer A & Simon C 2005 Leptin system in embryo development and implantation: a protein in search of a function. Reproductive Biomedicine Online 10 217-223. (Pubitemid 40246637)
18. Devine PL & McKenzie IF 1992 Mucins: structure, function, and associations with malignancy. BioEssays 14 619-625.
19. Dominguez F, Pellicer A & Simon C 2002 Paracrine dialogue in implantation. Molecular and Cellular Endocrinology 186 175-181.
20. Enders AC 2000 Trophoblast-uterine interactions in the first days of implantation: models for the study of implantation events in the human. Seminars in Reproductive Medicine 18 255-263.
21. Enders AC & Schlafke S 1969 Cytological aspects of trophoblast-uterine interaction in early implantation. American Journal of Anatomy 125 1-29.
22. Fouladi-Nashta AA, Jones CJ, Nijjar N, Mohamet L, Smith A, Chambers I & Kimber SJ 2005 Characterization of the uterine phenotype during the peri-implantation period for LIF-null, MF1 strain mice. Developmental Biology 281 1-21. (Pubitemid 40558719)
23. Galan A, O'Connor JE, Valbuena D, Herrer R, Remohi J, Pampfer S, Pellicer A & Simon C 2000 The human blastocyst regulates endometrial epithelial apoptosis in embryonic adhesion. Biology of Reproduction 63 430-439. (Pubitemid 30639929)
24. Genbacev OD, Prakobphol A, Foulk RA, Krtolica AR, Ilic D, Singer MS, Yang ZQ, Kiessling LL, Rosen SD & Fisher SJ 2003 Trophoblast L-selectin-mediated adhesion at the maternal-fetal interface. Science 299 405-408. (Pubitemid 36120046)
25. Glass RH, Spindle AI, Maglio M & Pedersen RA 1980 The free surface of mouse trophoblast in culture is non-adhesive for other cells. Journal of Reproduction and Fertility 59 403-407. (Pubitemid 10012874)
26. Grewal S, Carver JG, Ridley AJ & Mardon HJ 2008 Implantation of the human embryo requires Rac1-dependent endometrial stromal cell migration. PNAS 105 16189-16194.
27. Hannan NJ, Paiva P, Dimitriadis E & Salamonsen LA 2009 Models for study of human embryo implantation: choice of cell lines? Biology of Reproduction 82 235-245.
28. Hata H & Kuramoto H 1992 Immunocytochemical determination of estrogen and progesterone receptors in human endometrial adenocarcinoma cells (Ishikawa cells). Journal of Steroid Biochemistry and Molecular Biology 42 201-210.
29. Heneweer C, Schmidt M, Denker HW & Thie M 2005 Molecular mechanisms in uterine epithelium during trophoblast binding: the role of small GTPase RhoA in human uterine Ishikawa cells. Journal of Experimental & Clinical Assisted Reproduction 2 4. (Pubitemid 40605249)
30. Hertig AT, Rock J, Adams EC & Menkin MC 1959 Thirty-four fertilized human ova, good, bad and indifferent, recovered from 210 women of known fertility; a study of biologic wastage in early human pregnancy. Pediatrics 23 202-211.
31. Hey NA & Aplin JD 1996 Sialyl-Lewis x and Sialyl-Lewis a are associated with MUC1 in human endometrium. Glycoconjugate Journal 13 769-779. (Pubitemid 26354270)
32. Hey NA, Graham RA, Seif MW & Aplin JD 1994 The polymorphic epithelial mucin MUC1 in human endometrium is regulated with maximal expression in the implantation phase. Journal of Clinical Endocrinology and Metabolism 78 337-342.
33. Hey NA, Li TC, Devine PL, Graham RA, Saravelos H & Aplin JD 1995 MUC1 in secretory phase endometrium: expression in precisely dated biopsies and flushings from normal and recurrent miscarriage patients. Human Reproduction 10 2655-2662.
34. Hilkens J, Ligtenberg MJ, Vos HL & Litvinov SV 1992 Cell membrane-associated mucins and their adhesion-modulating property. Trends in Biochemical Sciences 17 359-363.
35. Hoadley ME, Seif MW & Aplin JD 1990 Menstrual-cycle-dependent expression of keratan sulphate in human endometrium. Biochemical Journal 266 757-763. (Pubitemid 20103709)
36. Hoffman LH, Olson GE, Carson DD & Chilton BS 1998 Progesterone and implanting blastocysts regulate Muc1 expression in rabbit uterine epithelium. Endocrinology 139 266-271.
37. Hohn HP, Linke M & Denker HW 2000 Adhesion of trophoblast to uterine epithelium as related to the state of trophoblast differentiation: in vitro studies using cell lines. Molecular Reproduction and Development 57 135-145.
38. Horne AW, Lalani EN, Margara RA, Ryder TA, Mobberley MA & White JO 2005 The expression pattern of MUC1 glycoforms and other biomarkers of endometrial receptivity in fertile and infertile women. Molecular Reproduction and Development 72 216-229.
39. Jones CJ, Fazleabas AT, McGinlay PB & Aplin JD 1998 Cyclic modulation of epithelial glycosylation in human and baboon (Papio anubis) endometrium demonstrated by the binding of the agglutinin from Dolichos biflorus. Biology of Reproduction 58 20-27.
40. Kimber SJ & Spanswick C 2000 Blastocyst implantation: the adhesion cascade. Seminars in Cell and Developmental Biology 11 77-92.
41. Kovalevsky G & Patrizio P 2005 High rates of embryo wastage with use of assisted reproductive technology: a look at the trends between 1995 and 2001 in the United States. Fertility and Sterility 84 325-330. (Pubitemid 41125252)
42. Kovarik A, Peat N, Wilson D, Gendler SJ & Taylor-Papadimitriou J 1993 Analysis of the tissue-specific promoter of the MUC1 gene. Journal of Biological Chemistry 268 9917-9926. (Pubitemid 23146057)
43. Lagow E, DeSouza MM & Carson DD 1999 Mammalian reproductive tract mucins. Human Reproduction Update 5 280-292.
44. Lalitkumar PG, Lalitkumar S, Meng CX, Stavreus-Evers A, Hambiliki F, Bentin-Ley U & Gemzell-Danielsson K 2007 Mifepristone, but not levonogestrel, inhibits human blastocyst attachment to an in vitro endometrial three-dimensional cell culture model. Human Reproduction 22 3031-3037. (Pubitemid 351696826)
45. Lavranos TC & Seamark RF 1989 Addition of steroids to embryo-uterine monolayer co-culture enhances embryo survival and implantation in vitro. Reproduction, Fertility, and Development 1 41-46.
46. Lessey BA 2002 Adhesion molecules and implantation. Journal of Reproductive Immunology 55 101-112.
47. Lessey BA, Killam AP, Metzger DA, Haney AF, Greene GL & McCarty KS Jr 1988 Immunohistochemical analysis of human uterine estrogen and progesterone receptors throughout the menstrual cycle. Journal of Clinical Endocrinology and Metabolism 67 334-340.
48. Lessey BA, Ilesanmi AO, Castelbaum AJ, Yuan L, Somkuti SG, Chwalisz K & Satyaswaroop PG 1996 Characterization of the functional progesterone receptor in an endometrial adenocarcinoma cell line (Ishikawa): progesterone-induced expression of the alpha1 integrin. Journal of Steroid Biochemistry and Molecular Biology 59 31-39. (Pubitemid 27014139)
49. Ligtenberg MJ, Buijs F, Vos HL & Hilkens J 1992 Suppression of cellular aggregation by high levels of episialin. Cancer Research 52 2318-2324.
50. Lindenberg S, Hyttel P, Sjogren A & Greve T 1989 A comparative study of attachment of human, bovine and mouse blastocysts to uterine epithelial monolayer. Human Reproduction 4 446-456. (Pubitemid 19144685)
51. Lopata A 1996 Blastocyst-endometrial interaction: an appraisal of some old and new ideas. Molecular Human Reproduction 2 519-525. (Pubitemid 126717491)
52. Lopata A, Bentin-Ley U & Enders A 2002 "Pinopodes" and implantation. Reviews in Endocrine and Metabolic Disorders 3 77-86.
53. Meseguer M, Aplin JD, Caballero-Campo P, O'Connor JE, Martin JC, Remohi J, Pellicer A & Simon C 2001 Human endometrial mucin MUC1 is up-regulated by progesterone and down-regulated in vitro by the human blastocyst. Biology of Reproduction 64 590-601. (Pubitemid 32109748)
54. Mo B, Vendrov AE, Palomino WA, DuPont BR, Apparao KB & Lessey BA 2006 ECC-1 cells: a well-differentiated steroid-responsive endometrial cell line with characteristics of luminal epithelium. Biology of Reproduction 75 387-394. (Pubitemid 44268073)
55. Morris JE, Potter SW, Rynd LS & Buckley PM 1983 Adhesion of mouse blastocysts to uterine epithelium in culture: a requirement for mutual surface interactions. Journal of Experimental Zoology 225 467-479.
56. Nishida M, Kasahara K, Kaneko M, Iwasaki H & Hayashi K 1985 Establishment of a new human endometrial adenocarcinoma cell line, Ishikawa cells, containing estrogen and progesterone receptors. Nippon Sanka Fujinka Gakkai Zasshi 37 1103-1111. (Pubitemid 15047811)
57. Pampfer S & Donnay I 1999 Apoptosis at the time of embryo implantation in mouse and rat. Cell Death and Differentiation 6 533-545. (Pubitemid 29292109)
58. Paria BC, Das SK & Dey SK 1998 Embryo implantation requires estrogen-directed uterine preparation and catecholestrogen-mediated embyronic activation. Advances in Pharmacology 42 840-843.
59. Parr EL, Tung HN & Parr MB 1987 Apoptosis as the mode of uterine epithelial cell death during embryo implantation in mice and rats. Biology of Reproduction 36 211-225.
60. Psychoyos A 1986 Uterine receptivity for nidation. Annals of the New York Academy of Sciences 476 36-42.
61. Salamonsen LA, Nie G, Hannan NJ & Dimitriadis E 2009 Society for Reproductive Biology Founders' Lecture 2009. Preparing fertile soil: the importance of endometrial receptivity. Reproduction, Fertility, and Development 21 923-934.
62. de los Santos MJ, Mercader A, Galan A, Albert C, Romero JL & Pellicer A 2003 Implantation rates after two, three, or five days of embryo culture. Placenta 24 (Supplement B) S13-S19.
63. Singh H & Aplin JD 2009 Adhesion molecules in endometrial epithelium: tissue integrity and embryo implantation. Journal of Anatomy 215 3-13.
64. Somkuti SG, Yuan L, Fritz MA & Lessey BA 1997 Epidermal growth factor and sex steroids dynamically regulate amarker of endometrial receptivity in Ishikawa cells. Journal of Clinical Endocrinology and Metabolism 82 2192-2197. (Pubitemid 27287583)
65. Surveyor GA, Gendler SJ, Pemberton L, Das SK, Chakraborty I, Julian J, Pimental RA, Wegner CC, Dey SK & Carson DD 1995 Expression and steroid hormonal control of Muc-1 in the mouse uterus. Endocrinology 136 3639-3647.
66. Sutherland AE, Calarco PG & Damsky CH 1993 Developmental regulation of integrin expression at the time of implantation in the mouse embryo. Development 119 1175-1186. (Pubitemid 23358585)
67. Thathiah A & Carson DD 2004 MT1-MMP mediates MUC1 shedding independent of TACE/ADAM17. Biochemical Journal 382 363-373. (Pubitemid 39141600)
68. Thathiah A, Blobel CP & Carson DD 2003 Tumor necrosis factor-alpha converting enzyme/ADAM 17 mediates MUC1 shedding. Journal of Biological Chemistry 278 3386-3394. (Pubitemid 36801254)
69. Uchida H, Maruyama T, Ohta K, Ono M, Arase T, Kagami M, Oda H, Kajitani T, Asada H & Yoshimura Y 2007 Histone deacetylase inhibitor-induced glycodelin enhances the initial step of implantation. Human Reproduction 22 2615-2622. (Pubitemid 47434203)
70. Wesseling J, van der Valk SW & Hilkens J 1996 A mechanism for inhibition of E-cadherin-mediated cell-cell adhesion by the membrane-associated mucin episialin/MUC1. Molecular Biology of the Cell 7 565-577. (Pubitemid 26112564)
71. Widra EA, Weeraratna A, Stepp MA, Stillman RJ & Patierno SR 1997 Modulation of implantation-associated integrin expression but not uteroglobin by steroid hormones in an endometrial cell line. Molecular Human Reproduction 3 563-568. (Pubitemid 127512052)
72. Yoshinaga K 1988 Uterine receptivity for blastocyst implantation. Annals of the New York Academy of Sciences 541 424-431.