Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-06-02T11:55:18.233Z Has data issue: false hasContentIssue false
  • English
  • Français

Integrins in the endometrium

Published online by Cambridge University Press:  03 June 2009

Bruce A Lessey  and
Arthur J Castelbaum
Bruce A Lessey*
Affiliation:
University of North Carolina at Chapel Hill, Chapel Hill, North Carolina
Arthur J Castelbaum
Affiliation:
Northern Fertility and Reproduction, Abington, Pennsylvania, USA
*
CB#7570 MacNider Building, University of North Carolina, Chapel Hill, NC 27599, USA.
Get access Rights & Permissions [Opens in a new window]

Extract

The endometrium expresses many of the same integrins displayed by other tissues. Endometrial epithelial cells maintain the ‘classic’ epithelial integrins, including α2, α3, α6, and β4, while the stroma expresses the fibronectin receptor, α5β1. During the menstrual cycle, the endometrium undergoes dynamic changes in morphology in preparation for implantation. With these histological changes are concomitant alterations in integrin expression that appear to ‘frame’ the window of implantation, by the co-expression of glandular αvβ3 and α4β1 during days 20 to 24 of the menstrual cycle. The changes in integrin expression shift from epithelial to stroma predominance late in the menstrual cycle, extending into early pregnancy. Decidual integrins that appear upregulated in pregnancy include α1β1, α3β1, α6β1 and αvβ3. Markers of uterine receptivity hold promise for a better understanding of the implantation process and may help to explain many different types of infertility. These markers will be essential for monitoring and improving infertility therapies. The importance of integrins in the human endometrium now seems well established and promises to be an area of great clinical and basic science activity in the future.

Type
Articles
Information
Reproductive Medicine Review , Volume 4 , Issue 1 , March 1995 , pp. 43 - 58
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1Ruoslahti, E, Noble, NA, Kagami, S, Border, WA. Integrins. Kidney Int 1994; 45 (suppl 44): S17–S22.Google Scholar
2Hynes, RO. Integrins: a family of cell surface receptors. Cell 1987; 48: 549–54.CrossRefGoogle ScholarPubMed
3Albelda, SM, Buck, CA. Integrins and other cell adhesion molecules. FASEB J 1990; 4: 2868–80.CrossRefGoogle ScholarPubMed
4Lessey, BA, Damjanovich, L, Coutifaris, C, Castelbaum, A, Albelda, SM, Buck, CA. Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle. J Clin Invest 1992; 90: 188–95.CrossRefGoogle ScholarPubMed
5Tabibzadeh, S. Patterns of expression of integrin molecules in human endometrium throughout the menstrual cycle. Hum Reprod 1992; 7: 876–82.CrossRefGoogle ScholarPubMed
6Lessey, BA, Castelbaum, AJ, Buck, CA, Lei, Y, Yowell, CW, Sun, J. Further characterization of endometrial integrins during the menstrual cycle and in pregnancy. Fertil Steril 1994; 62: 497–506.CrossRefGoogle ScholarPubMed
7Bischof, P, Redard, M, Gindre, P, Vassilakos, P, Campana, A. Localization of alpha 2, alpha 5 and alpha 6 integrin subunits in human endometrium, decidua and trophoblast. Eur J Obstet Gynecol Reprod Biol 1993; 51: 217–26.CrossRefGoogle ScholarPubMed
8Ruck, P, Marzusch, K, Kaiserling, E et al. Distribution of cell adhesion molecules in decidua of early human pregnancy: an immunohistochemical study. Lab Invest 1994; 71: 94–101.Google ScholarPubMed
9Horwitz, A, Duggan, K, Greggs, R, Decker, C, Buck, C. The cell substrate attachment (CSAT) antigen has properties of a receptor for laminin and fibronectin. J Cell Biol 1985; 101: 2134–44.CrossRefGoogle ScholarPubMed
10Buck, CA, Shea, E, Duggan, K, Horwitz, AF. Integrin (the CSAT antigen) functionality requires oligomeric integrity. J Cell Biol 1986; 103: 2421–28.CrossRefGoogle ScholarPubMed
11Buck, CA, Horwitz, AF. Integrin, a transmembrane glycoprotein complex mediating cell-substratum adhesion. J Cell Sci Suppl 1987; 8: 231–50.CrossRefGoogle ScholarPubMed
12Ruoslahti, E, Pierschbacher, MD. New perspectives in cell adhesion: RGD and integrins. Science 1987; 238: 491–97.CrossRefGoogle ScholarPubMed
13Hemler, ME, Huang, C, Takada, Y, Schwarz, L, Strominger, JL, Clabby, ML. Characterization of the cell surface heterodimer VLA-4 and related peptides. J Biol Chem 1987; 262: 11478–85.CrossRefGoogle ScholarPubMed
14DeSimone, DW, Stepp, MA, Patel, RS, Hynes, RO. The integrin family of cell surface receptors. Biochem Soc Trans 1987; 15: 789–91.CrossRefGoogle ScholarPubMed
15Elices, MJ, Hemler, ME. The human integrin VLA-2 is a collagen receptor on some cells and a collagen/laminin receptor on others. Proc Natl Acad Sci USA 1989; 86: 9906–10.CrossRefGoogle Scholar
16Elices, MJ, Urry, LA, Hemler, ME. Receptor functions for the integrin VLA-3: fibronectin, collagen, and laminin binding are differentially influenced by Arg-Gly-Asp peptide and by divalent cations. J Cell Biol 1991; 112: 169–81.CrossRefGoogle ScholarPubMed
17Languino, LR, Gehlsen, KR, Wayner, E, Carter, WG, Engvall, E, Ruoslahti, E. Endothelial cells use alpha 2 beta 1 integrin as a laminin receptor. J Cell Biol 1989; 109: 2455–62.CrossRefGoogle ScholarPubMed
18Conforti, G, Zanetti, A, Pasquali-Ronchetti, I, Quaglino, D Jr, Neyroz, P, Dejana, E. Modulation of vitronectin receptor binding by membrane lipid composition. J Biol Chem 1990; 265: 4011–19.CrossRefGoogle ScholarPubMed
19Filardo, EJ, Cheresh, DA. A β turn in the cytoplasmic tail of the integrin av subunit influences conformation and ligand binding of αvβ3. J Biol Chem 1994; 269: 4641–47.CrossRefGoogle Scholar
20Chan, BM, Kassner, PD, Schiro, JA, Byers, HR, Kupper, TS, Hemler, ME. Distinct cellular functions mediated by different VLA integrin alpha subunit cytoplasmic domains. Cell 1992; 68: 1051–60.CrossRefGoogle ScholarPubMed
21Hemler, ME. VLA proteins in the integrin family: structures, functions, and their role on leukocytes. Annu Rev Immunol 1990; 8: 365–400.CrossRefGoogle ScholarPubMed
22Akiyama, SK, Yamada, SS, Yamada, KM, LaFlamme, SE. Transmembrane signal transduction by integrin cytoplasmic domains expressed in single-subunit chimeras. J Biol Chem 1994; 269: 15961–64.CrossRefGoogle ScholarPubMed
23Pasqualini, R, Hemler, ME. Contrasting roles for integrili β1 and β5 cytoplasmic domains in subcellular localization, cell proliferation, and cell migration. J Cell Biol 1994; 125: 447–60.CrossRefGoogle ScholarPubMed
24Streuli, CH, Bailey, N, Bissell, MJ. Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological polarity. J Cell Biol 1991; 115: 1383–95.CrossRefGoogle ScholarPubMed
25Hynes, RO. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992; 69: 11–25.CrossRefGoogle ScholarPubMed
26Smith, JW, Cheresh, DA. Integrin (alpha v beta 3)- ligand interaction. Identification of a heterodimeric RGD binding site on the vitronectin receptor. J Biol Chem 1990; 265: 2168–72.CrossRefGoogle ScholarPubMed
27Hall, DE, Reichardt, LF, Crowley, E et al. The alpha 1/beta 1 and alpha 6/beta 1 integrin heterodimers mediate cell attachment to distinct sites on laminin. J Cell Biol 1990; 110: 2175–84.CrossRefGoogle ScholarPubMed
28Kramer, RH, Marks, N. Identification of integrin collagen receptors on human melanoma cells. J Biol Chem 1989; 264: 4684–88.CrossRefGoogle ScholarPubMed
29Hemler, ME, Elices, MJ, Parker, C, Takada, Y. Structure of the integrin VLA-4 and its cell-cell and cell-matrix adhesion functions. Immunol Rev 1990; 114: 45–65.CrossRefGoogle ScholarPubMed
30Sonnenberg, A, Modderman, PW, Hogervorst, F. Laminin receptor on platelets is the integrin VLA-6. Nature 1988; 336: 487–89.CrossRefGoogle ScholarPubMed
31Sonnenberg, A, Gehlsen, KR, Aumailley, M, Timpl, R. Isolation of alpha 6 beta 1 integrins from platelets and adherent cells by affinity chromatography on mouse laminin fragment E8 and human laminin pepsin fragment. Exp Cell Res 1991; 197: 234–44.CrossRefGoogle ScholarPubMed
32Song, WK, Wang, W, Foster, RF, Bielser, DA, Kaufman, SJ. H36-alpha 7 is a novel integrin alpha subunit that is developmentally regulated during skeletal muscle myogenesis. J Cell Biol 1992; 117: 643–57.CrossRefGoogle Scholar
33Bossy, B, Bossy-Wetzel, E, Reichardt, LF. Characterization of the integrin alpha 8 subunit: a new integrin beta 1-associated subunit, which is prominently expressed on axons and on cells in contact with basal laminae in chick embryos. EMBO J 1991; 10: 2375–85.CrossRefGoogle ScholarPubMed
34Palmer, EL, Rüegg, C, Ferrando, R, Pytela, R, Sheppard, D. Sequence and tissue distribution of the integrin α9 subunit, a novel partner of β1 that is widely distributed in epithelia and muscle. J Cell Biol 1993; 123: 1289–97.CrossRefGoogle Scholar
35Ruoslahti, E. Integrins. J Clin Invest 1991; 87: 1–5.CrossRefGoogle ScholarPubMed
36Weinacker, A, Chen, A, Agrez, M et al. Role of the integrin αvβ6 in cell attachment to fibronectin. Heterologous expression of intact and secreted forms of the receptor. J Biol Chem 1994; 269: 6940–48.CrossRefGoogle ScholarPubMed
37Du, XP, Plow, EF, Frelinger, AL III, O'Toole, TE, Loftus, JC, Ginsberg, MH. Ligands ‘activate’ integrin alpha IIb beta 3 (platelet GPIIb-IIIa). Cell 1991; 65: 409–16.CrossRefGoogle ScholarPubMed
38Vogel, BE, Tarone, G, Giancotti, FG, Gailit, J, Ruoslahti, E. A novel fibronectin receptor with an unexpected subunit composition (alpha v beta 1). J Biol Chem 1990; 265: 5934–37.CrossRefGoogle ScholarPubMed
39Krissansen, GW, Elliott, MJ, Lucus, CM et al. Identification of a novel integrin beta subunit expressed on cultured monocytes (macrophages). Evidence that one alpha subunit can associate with multiple beta subunits. J Biol Chem 1990; 265: 823–30.CrossRefGoogle ScholarPubMed
40Hautanen, A, Gailit, J, Mann, DM, Ruoslahti, E. Effects of modifications of the RGD sequence and its context on recognition by the fibronectin receptor. J Biol Chem 1989; 264: 1437–42.CrossRefGoogle ScholarPubMed
41Frojmovic, MM, O'Toole, TE, Plow, EF, Loftus, JC, Ginsberg, MJ. Platelet glycoprotein IIb–IIIa (alpha IIb beta 3 integrin) confers fibrinogen- and activation-dependent aggregation on heterologous cells. Blood 1991; 78: 369–76.CrossRefGoogle ScholarPubMed
42Nesbitt, S, Nesbit, A, Helfrich, M, Horton, M. Biochemical characterization of human osteoclast integrins. Osteoclasts express alpha v beta 3, alpha 2 beta 1, and alpha v beta 1 integrins. J Biol Chem 1993; 268: 16737–45.CrossRefGoogle ScholarPubMed
43Lakkakorpi, PT, Horton, MA, Helfrich, MH, Karhukorpi, EK, Vaananen, HK. Vitronectin receptor has a role in bone resorption but does not mediate tight sealing zone attachment of osteoclasts to the bone surface. J Cell Biol 1991; 115: 1179–86.CrossRefGoogle Scholar
44Brooks, PC, Clark, RAF, Cheresh, DA. Requirement of vascular integrin alpha v/β3 for angiogenesis. Science 1994; 264: 569–71.CrossRefGoogle Scholar
45Albelda, SM. Role of integrins and other cell adhesion molecules in tumor progression and metastasis. Lab Invest 1993; 68: 4–17.Google ScholarPubMed
46Heino, J, Ignotz, RA, Hemler, ME, Crouse, C, Massague, J. Regulation of cell adhesion receptors by transforming growth factor-beta. Concomitant regulation of integrins that share a common beta 1 subunit. J Biol Chem 1989; 264: 380–88.CrossRefGoogle Scholar
47Sheppard, D, Cohen, DS, Wang, A, Busk, M. Transforming growth factor β differentially regulates expression of integrin subunits in guinea pigs airway epithelial cells. J Biol Chem 1992; 267: 17409–14.CrossRefGoogle ScholarPubMed
48Ruoslahti, E. Control of cell motility and tumour invasion by extracellular matrix interactions. Br J Cancer 1992; 66: 239–42.CrossRefGoogle ScholarPubMed
49Cheresh, DA. Integrins in thrombosis, wound healing and cancer. Biochem Soc Trans 1991; 19: 835–38.CrossRefGoogle ScholarPubMed
50Albelda, SM, Smith, CW, Ward, PA. Adhesion molecules and inflammatory injury. FASEB J 1994; 8: 504–12.CrossRefGoogle ScholarPubMed
51Klein, S, Giancotti, FG, Presta, M, Albelda, SM, Buck, CA, Rifkin, DB. Basic fibroblast growth factor modulates integrili expression in microvascular endothelial cells. Mol Biol Cell 1993; 4: 973–82.CrossRefGoogle ScholarPubMed
52Defilippi, P, Silengo, L, Tarone, G. α6β1 integrin (laminin receptor) is down-regulated by tumor necrosis factor α and interleukin-1 β in human endothelial cells. J Biol Chem 1992; 267: 18303–307.CrossRefGoogle Scholar
53Leslie, KK, Watanabe, S, Lei, KJ et al. Linkage of two human pregnancy-specific β1-glycoprotein genes: one is associated with hydatidiform mole. Proc Natl Acad Sci USA 1990; 87: 5822–26.CrossRefGoogle ScholarPubMed
54Santala, P, Heino, J. Regulation of integrin-type cell adhesion receptors by cytokines. J Biol Chem 1991; 266: 23505–509.CrossRefGoogle ScholarPubMed
55Massagué, J. The TGF-β family of growth and differentiation factors. Cell 1987; 49: 437–38.CrossRefGoogle ScholarPubMed
56Sporn, MB, Roberts, AB, Wakefield, LM, de Crombrugghe, B. Some recent advances in the chemistry and biology of transforming growth factor-beta. J Cell Biol 1987; 105: 1039–45.CrossRefGoogle ScholarPubMed
57Mustoe, TA, Pierce, GF, Thomason, A, Gramates, P, Sporn, MB, Deuel, T. Accelerated healing of incisional wounds in rats induced by transforming growth factor-β. Science 1987; 237: 1333–36.CrossRefGoogle ScholarPubMed
58Ignotz, RA, Massagué, J. Transforming growth factor-β stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J Cell Biol 1986; 261: 4337–45.Google ScholarPubMed
59Bassols, A, Massagué, J. Transforming growth factor β regulates the expression and structure of extracellular matrix chondroitin/Dermatan sulfate proteoglycans. J Biol Chem 1988; 263: 3039–45.CrossRefGoogle ScholarPubMed
60Noda, M, Yoon, K, Prince, CW, Butler, WT, Rodan, GA. Transcriptional regulation of osteopontin production in rat osteosarcoma cells by type B transforming growth factor. J Biol Chem 1988; 263: 13916–21.CrossRefGoogle Scholar
61Pearson, CA, Pearson, D, Shibahara, S, Hofsteenge, J, Chiquet-Ehrismann, R. Tenascin: cDNA cloning and induction by TGF-beta. EMBO J 1988; 7: 2977–82.CrossRefGoogle ScholarPubMed
62Laiho, M, Saksela, O, Andreasen, PA, Keski-Oja, J. Enhanced production and extracellular matrix depostion of the endothelial-type plasminogen activator inhibitor in cultured human lung fibroblasts by transforming growth factor-β. J Cell Biol 1986; 103: 2403–10.CrossRefGoogle Scholar
63Edwards, DR, Murphy, G, Reynolds, JJ et al. Transforming growth factor beta modulates the expression of collagenase and metalloproteinase inhibitor. EMBO J 1987; 6: 1899–904.CrossRefGoogle ScholarPubMed
64Ignotz, RA, Massagué, J. Cell adhesion protein receptors as targets for transforming growth factorbeta action. Cell 1987; 51: 189–97.CrossRefGoogle ScholarPubMed
65Ignotz, RA, Heino, J, Massagué, J. Regulation of cell adhesion receptors by transforming growth factorbeta. Regulation of vitronectin receptor and LFA-1. J Biol Chem 1989; 264: 389–92.CrossRefGoogle ScholarPubMed
66Heino, J, Massagué, J. Transforming growth factorbeta switches the pattern of integrins expressed in MG-63 human osteosarcoma cells and causes a selective loss of cell adhesion to laminin. J Biol Chem 1989; 264: 21806–11.CrossRefGoogle ScholarPubMed
67Chegini, N, Zhao, Y, Williams, RS, Flanders, KC. Human uterine tissue throughout the menstrual cycle expresses transforming growth factor-β1 (TGFβ1), TGFβ2, TGFβ3, and TGFβ type II receptor messenger ribonucleic acid and protein and contains [125I]TGFβ1-binding sites. Endocrinology 1994; 135: 439–49.CrossRefGoogle Scholar
68Tabibzadeh, SS, Satyaswaroop, PG. Progestin-mediated induction of VLA-1 in glandular epithelium of human endometrium in vitro [Abstract]. 72nd Annual Meeting of The Endocrine Society, Atlanta, GA, 1990, Abstract 700:199.Google Scholar
69Lessey, BA, Castelbaum, AJ, Sawin, SJ et al. Aberrant integrin expression in the endometrium of women with endometriosis. J Clin Endocrinol Metab 1994; 79: 643–49.Google ScholarPubMed
70Castelbaum, AJ, Sun, J, Shell, K, Fritz, M, Freedman, MF, Lessey, BA. Decreased αvβ3 integrin expression identifies abnormal endometricalphenotype in luteal phase deficiency (LPD). Annual Meeting of the Society of Gynecological Investigation, Chicago, IL, USA, 1995. P285: 359.Google Scholar
71Klentzeris, LD, Bulmer, JN, Trejdosiewicz, LK, Morrison, L, Cooke, ID. Beta-1 integrin cell adhesion molecules in the endometrium of fertile and infertile women. Hum Reprod 1993; 8: 1223–30.CrossRefGoogle ScholarPubMed
72van der Linden, PJ, de Goeij, AF, Dunselman, GA, van der Linden, EP, Ramaekers, FC, Evers, JL. Expression of integrins and E-cadherin in cells from menstrual effluent, endometrium, peritoneal fluid, peritoneum, and endometriosis. Fértil Steril 1994; 61: 85–90.CrossRefGoogle ScholarPubMed
73Taskin, O, Brown, RW, Young, DC, Poindexter, AN, Wiehle, RD. High doses of oral contraceptives do not alter endomentrial al and avb3 integrins in the late implantation window. Fertil Steril 1994; 61: 850–55.CrossRefGoogle ScholarPubMed
74Bridges, JE, Prentice, A, Rouche, W, Englefield, P, Thomas, EJ. Expression of integrin adhesion molecules in endometrium and endometriosis. Br J Obstet Gynaecol 1994; 101: 696–700.CrossRefGoogle ScholarPubMed
75Albelda, SM. Endothelial and epithelial cell adhesion molecules. Am J Respir Cell Mol Biol 1991; 4: 195–203.CrossRefGoogle ScholarPubMed
76Quaranta, V. Epithelial integrins. Cell Differ Dev 1990; 32: 361–65.CrossRefGoogle ScholarPubMed
77Jones, JC, Kurpakus, MA, Cooper, HM, Quaranta, V. A function for the integrin alpha 6 beta 4 in the hemidesmosome. Cell Regul 1991; 2: 427–38.CrossRefGoogle ScholarPubMed
78Aplin, JD, Charlton, AK, Ayad, S. An immunohistochemical study of human endometrial extracellular matrix during the menstrual cycle and first trimester of pregnancy. Cell Tissue Res 1988; 253: 231–40.CrossRefGoogle ScholarPubMed
79Giudice, LC. Growth factors and growth modulators in human uterine endometrium: their potential relevance to reproductive medicine. Fertil Steril 1994; 61: 1–17.CrossRefGoogle ScholarPubMed
80Seppälä, M, Koistinen, R, Rutanen, E-M. Uterine endocrinology and paracrinology: insulin-like growth factor binding protein-1 and placental protein 14 revisited. Hum Reprod 1994; 9: 917–25.CrossRefGoogle ScholarPubMed
81Jones, JI, Gockerman, A, Busby, WH, Wright, G, Clemmons, DR. Insulin-like growth factor binding protein 1 stimulates cell migration and binds to the alpha 5/b1 integrin by means of its ARG-GLY-ASP sequence. Proc Natl Acad Sci USA 1993; 90: 10553–57.CrossRefGoogle Scholar
82Frost, RA, Mazella, J, Tseng, L. Insulin-like growth factor binding protein-1 inhibits the mitogenic effect of insulin-like growth factors and progestins in human endometrial stromal cells. Biol Reprod 1993; 49: 104–111.CrossRefGoogle ScholarPubMed
83Gospodarowicz, D, Greenburg, G, Birdwell, CR. Determination of cellular shape by the extracellular matrix and its correlation with the control of cellular growth. Cancer Res 1978; 38: 4155–71.Google ScholarPubMed
84Getzenberg, RH, Pienta, KJ, Coffey, DS. The tissue matrix: cell dynamics and hormone action. Endocr Rev 1990; 11: 399–417.CrossRefGoogle ScholarPubMed
85Bissell, MJ, Aggeler, J. Dynamic receprocity: how do extracellular matrix and hormones direct gene expression? In: Smoe, J ed. Mechanisms of signal transduction by hormones and growth factors. New York: Alan R Liss, 1987; 251–62.Google Scholar
86Finn, CA. The implantation reaction: In: Wynn, RM ed. Biology of the uterus. New York: Plenum Press, 1977:245–303.CrossRefGoogle Scholar
87Apiin, JD. Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro. J Cell Sci 1991; 99: 681–92.Google Scholar
88Castelbaum, AJ, Sawin, SW, Lessey, BA. Endometrial integrin expression of diethylstilbestrol exposed compared to normal women. Annual Meeting of the Society of Gynecological Investigations, Chicago, IL, 1994, 0–17: 95.Google Scholar
89Tabibzadeh, S. Immunoreactivity of human endometrium: correlation with endometrial dating. Fertil Steril 1990; 54: 624–31.CrossRefGoogle ScholarPubMed
90Lessey, BA, Metzger, DA, Haney, AF, McCarty, KS Jr. Immunohistochemical analysis of estrogen and progesterone receptors in endometriosis: comparison with normal endometrium during the menstrual cycle and the effect of medical therapy. Fertil Steril 1989; 51: 409–15.CrossRefGoogle ScholarPubMed
91Garcia, 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.CrossRefGoogle ScholarPubMed
92Lessey, BA, Castelbaum, A, Ilesanmi, A, Yeh, I. Immunohistochemical diagnosis of luteal phase deficiency: comparison between endometrial progesterone receptor distribution and TAG-72 [Abstract]. Washington, DC: The Endocrine Society, 1991: Abstract: 1670: 448.Google Scholar
93Albelda, SM, Mette, SA, Elder, DE et al. Integrin distribution in malignant melanoma: association of the beta 3 subunit with tumor progression. Cancer Res 1990; 50: 6757–64.Google ScholarPubMed
94Mardon, HJ, Sebastio, G. Regulation of alternative splicing in the IIICS region of human fibronectin pre-mRNA encoding cell binding sites CS1 and CS5. J Cell Sci 1992; 103: 423–33.CrossRefGoogle ScholarPubMed
95Feinberg, RF, Kliman, HJ, Lockwood, CJ. Is oncofetal fibronectin a trophoblast glue for human implantation. Am J Pothol 1991; 138: 537–43.Google ScholarPubMed
96Lessey, BA. The use of integrins for the assessment of uterine receptivity. Fertil Steril 1994; 61: 812–84.CrossRefGoogle ScholarPubMed
97Bruess, JM, Gillett, N, Lu, L, Sheppard, D, Pytela, R. Restricted distribution of integrin b6 mRNA in primate epithelial tissues. J Histochem Cythochem 1993; 41: 1521–27.CrossRefGoogle Scholar
98Weitlauf, HM. Embryonic signalling at implantation in the mouse. In: Yoshinaga, K, Mori, T eds. Development of preimplantation embryos and their environment. New York: Alan R Liss, 1989: 359–76.Google Scholar
99Hayman, EG, Pierschbacher, MD, Öhgren, Y, Ruoslahti, E. Serum spreading factor (vitronectin) is present at the cell surface and in tissues. Proc Natl Acad Sci USA 1983; 80: 4003–07.CrossRefGoogle ScholarPubMed
100Armant, DR, Kaplan, HA, Mover, H, Lennarz, WJ. The effect of hexapeptides on attachment and outgrowth of mouse blastocysts cultured in vitro: evidence for the involvement of the cell recognition tripeptide Arg-Gly-Asp. Proc Natl Acad Sci USA 1986;83: 6751–55.CrossRefGoogle ScholarPubMed
101Armant, DR. Cell interactions with laminin and its proteolytic fragments during outgrowth of mouse primary trophoblast cells. Biol Reprod 1991; 45: 664–72.CrossRefGoogle ScholarPubMed
102Kao, L-C, Caltabiano, S, Wu, S, Strauss, JF III, Kliman, HJ. The human villous cytotrophoblast: interactions with extracellular matrix proteins, endocrine function, and cytoplasmic differentiation in the absence of syncytium formation. Dev Biol 1988; 130: 693–702.CrossRefGoogle ScholarPubMed
103Reddy, RL, Raj, GS, Pang, Y, Raj, HGM. Role of extracellular matrix components in the implantation process of the rat [Abstract]. Biol Reprod 1993; 48: 25.Google Scholar
104Plow, EF, Pierschbacher, MD, Ruoslahti, E, Marguerie, GA, Ginsberg, MH. The effect of Arg-Gly-Asp-containing peptides on fribrinogen and von Willebrand factor binding to platelets. Proc Natl Acad Sci USA 1985; 82: 8057–61.CrossRefGoogle Scholar
105Coukos, G, Lessey, BA, Coutifaris, C. Human trophoblast implantation: a role for the b3 integrin subunii in trophoblast attachment and migration? [Abstract]. Annual Meeting of the American Fertility Society, 1992; New Orleans, 0–106:50.Google Scholar
106Vanderpuye, OA, Labarrere, CA, McIntyre, JA. A vitronectin-receptor-related molecule in human placental brush border membranes. Biochem J 1991; 280: 9–17.CrossRefGoogle ScholarPubMed
107Sutherland, AE, Calarco, PG, Damsky, CH. Developmental regulation of integrin expression at the time of implantation in the mouse embryo. Development 1993; 119: 1175–86.CrossRefGoogle ScholarPubMed
108Coutifaris, C, Lessey, BA. Co-expression of endometrial osteopontin and its receptor, the αvβ integrin, define the window of human receptivity to embryo implantation. Annual Meeting of the Society of Gynecological Investigation 1993; Toronto: S-135:136.Google Scholar
109Damsky, C, Sutherland, A, Fisher, S. Extracellular matrix 5: adhesive interactions in early mammalian embryogenesis, implantation, and placentation. FASEB J 1993; 7: 1320–29.CrossRefGoogle ScholarPubMed
110Marchbanks, PA, Peterson, HB, Rubin, GL, Wingo, PA. Research on infertility: definition makes a difference. The cancer and steroid hormone study group. Am J Epidemiol 1989; 130: 259–67.CrossRefGoogle ScholarPubMed
111The American Fertility Society. Medical Research International Society for Assisted Reproductive Technology (SART). In vitro fertilization-embryo transfer (IVF-ET) in the United States: 1990 results from the IVF-ET Registry. Fertil Steril 1992; 57: 15–24.CrossRefGoogle Scholar
112Jones, GS. Some newer aspects of management of infertility. J Am Med Assoc 1949; 141: 1123–29.CrossRefGoogle ScholarPubMed
113Daly, DC, Walters, CA, Soto-Albors, CE, Riddick, DH. Endometrial biopsy during treatment of luteal phase defects is predictive of therapeutic outcome. Fertil Steril 1983; 40: 305–10.CrossRefGoogle ScholarPubMed
114Fleming, R, Carswell, W, Black, WP et al. The deficient corpus luteum as a cause of infertility. In: Coutts, JRT eds. Functional morphology of the human ovary. Lancaster: MTP Press, 1981: 205–20.Google Scholar
115Soules, MR, Wiebe, RH, Aksel, S, Hammond, CB. The diagnosis and therapy of luteal phase deficiency. Fertil Steril 1977; 28: 1033–37.CrossRefGoogle ScholarPubMed
116Bergh, PA, Navot, D. The impact of embryonic development and endometrial maturity on the timing of implantation. Fertil Steril 1992; 58: 537–42.CrossRefGoogle ScholarPubMed
117Baird, DD, Weinberg, CR, Wilcox, AJ, McConnaughey, DR, Musey, PI, Collins, DC. Hormonal profiles of natural conception cycles ending in early, unrecognized pregnancy loss. J Clin Endocrinol Metab 1991; 72: 793–800.CrossRefGoogle ScholarPubMed
118Stewart, DR, Overstreet, JW, Nakajima, ST, Lasley, BL. Enhanced ovarian steroid secretion before implantation in early human pregnancy. J Clin Endocrinol Metab 1993; 76: 1470–76.Google ScholarPubMed
119Noyes, RW, Hertig, AI, Rock, J. Dating the endometrial biopsy. Fertil Steril 1950; 1: 3–25.CrossRefGoogle Scholar
120Jordan, J, Craig, K, Clifton, DK, Soules, MR. Luteal phase defect: the sensitivity and specificity of diagnostic methods in common clinical use. Fertil Steril 1994; 62: 54–62.CrossRefGoogle ScholarPubMed
121Li, TC, Cooke, ID. Evaluation of the luteal phase. Hum Reprod 1991; 6: 484–99.CrossRefGoogle ScholarPubMed
122Gibson, M. Clinical evaluation of luteal function. Semin Reprod Endocrinol 1990; 8: 130–41.CrossRefGoogle Scholar
123Gibson, M, Badger, GJ, Byrn, F, Lee, KR, Korson, R, Trainer, TD. Error in histologie dating of secretory endometrium: variance component analysis. Fertil Steril 1991; 56: 242–47.CrossRefGoogle Scholar
124Graham, RA, Seif, MW, Aplin, JD et al. An endometrial factor in unexplained infertility. BMJ 1990; 300: 1428–31.CrossRefGoogle ScholarPubMed
125Klentzeris, LD, Bulmer, JN, Li, TC, Morrison, L, Warren, A, Cookie, ID. Lectin binding of endometrium in women with unexplained infertility. Fertil Steril 1991; 56: 660–67.CrossRefGoogle ScholarPubMed
126Weed, JC, Arguembourg, PC. Endometriosis: can it produce an autoimmune response resulting in infertility. Clin Obstet Cynecol 1980; 23: 885–93.CrossRefGoogle ScholarPubMed
127Lessey, BA, Castelbaum, A. Characterization of the αvβ3 integrin in endometrium of patients with unexplained infertility: a prospective controlled study. [Abstract]. Annual Meeting of the Society of Gynaecological Investigation, Toronto, Canada, 1993; S-168:152.Google Scholar
128Lessey, BA, Castelbaum, AJ, Sawin, SJ, Sun, J. Integrins as markers of uterine receptivity in women with primary unexplained infertility. Fertil Steril 1995 (in press).CrossRefGoogle Scholar
129Klentzeris, LD, Li, TC, Dockery, P, Cooke, ID. The endometrial biopsy as a predictive factor of pregnancy rate in women with unexplained infertility. Eur J Obstet Gynecol Reprod Biol 1992; 45: 119–24.CrossRefGoogle ScholarPubMed
130Rogers, PAW, Murphy, CR. Uterine receptivity for implantation: human studies. In: Yoshinaga, K ed. Blastocyst implantation. Norwell, MA: Serono Symposia, 1989: 231–38.Google Scholar
131Psychoyos, A. Uterine receptivity for nidation. Ann NY Acad Sci 1986; 476: 36–42.CrossRefGoogle ScholarPubMed
132Anderson, TL, Hodgen, GD. Uterine receptivity in the primate. Prog Clin Biol Res 1989; 294: 389–99.Google ScholarPubMed
133Hodgen, GD. Surrogate embryo transfer combined with estrogen-progesterone therapy in monkeys: implantation, gestation, and delivery without ovaries. J Am Med Assoc 1983; 250: 2167–71.CrossRefGoogle ScholarPubMed
134McLaren, A. The control of implantation. In: Thompson, W, Joyce, DN, Newton, JR eds. In vitro fertilization and donor insemination. London: Royal College of Obstetricians and Gynaecologists, 1985:13–22.Google Scholar
135Yoshinaga, K. Receptor concept in implantation research. In: Yoshinaga, K, Mori, T eds. Development of preimplantation embryos and their environment. New York: Alan R Liss, 1989: 379–87.Google Scholar
136Hertig, AT, Rock, J, Adams, EC. A description of 34 human ova within the first 17 days of development. Am J Anat 1956; 98: 435–93.CrossRefGoogle ScholarPubMed
137Navot, D, Bergh, P. Preparation of the human endometrium for implantation. Ann NY Acad Sci 1991; 622: 212–19.CrossRefGoogle ScholarPubMed
138Navot, D, Scott, RT, Droesch, K, Veeck, LL, Liu, HC, Rosenwaks, Z. The window of embryo transfer and the efficiency of human conception in vitro. Fertil Steril 1991; 55: 114–18.CrossRefGoogle ScholarPubMed
139Yaron, Y, Botchan, A, Amit, A, Peyser, MR, David, MP, Lessing, JB. Endometrial receptivity in the light of modern assisted reproductive technologies. Fertil Steril 1994; 62: 225–32.Google ScholarPubMed
140Lee, MC, Damjanov, I. Pregnancy-related changes in the human endometrium revealed by lectin histochemistry. Histochemistry 1985; 82: 275–80.CrossRefGoogle ScholarPubMed
141Tabibzadeh, SS. Human endometrium: an active site of cytokine production and action. Endocr Rev 1991; 12: 272–90.CrossRefGoogle ScholarPubMed
142McRae, MA, Newman, GR, Walker, SM, Jasani, B. Immunohistochemical identification of prolactin and 24K protein in secretory endometrium. Fertil Steril 1986; 45: 643–48.CrossRefGoogle ScholarPubMed
143Kauma, S, Shapiro, SS. Immunoperoxidase localization of prolactin in endometrium during normal menstrual, luteal phase defect, and corrected luteal phase defect cycles. Fertil Steril 1986; 46: 37–42.CrossRefGoogle ScholarPubMed
144Aplin, JD, Seif, MW, Foden, LJ, Bradley, MD, Hallam, LJ. Expression of a high molecular weight secretory glycoprotein in human endometrium switches from epithelium to interstitium after implantation. Placenta 1986; 7: 458.Google Scholar
145Kliman, HJ, Feinberg, RF, Schwartz, LB, Feinman, MA, Lavi, E, Meadough, EL. A mucin-like glycoprotein identified by MAG (mouse ascites golgi) antibodies: menstrual cycle-dependent localization in human endometrium. Am J Pathol 1995 (in press).Google Scholar
146Joshi, SG, Ebert, KM, Swartz, DP. Detection and synthesis of a progestagen-dependent protein in human endometrium. J Reprod Fertil 1980; 59: 273–85.CrossRefGoogle ScholarPubMed
147Joshi, SG, Ebert, KM, Smith, RA. Properties of the progestagen-dependent protein of the endometrium. J Reprod Fertil 1980; 59: 287–96.CrossRefGoogle Scholar
148Bohn, H, Kraus, W, Winkler, W. New soluble placental tissue proteins: their isolation, characterization, localization and quantification. Placenta 1982; 4: 67–81.Google ScholarPubMed
149Klentzeris, LD, Bulmer, JN, Seppälä, M, Li, TC, Warren, MA, Cooke, ID. Placental protein 14 in cycles with normal and retarded endometrial differentiation. Hum Reprod 1994; 9: 394–98.CrossRefGoogle ScholarPubMed
150Batista, MC, Bravo, N, Cartledge, TP, Loriaux, DL, Merriam, GR, Nieman, LK. Serum levels of placental protein 14 do not accurately reflect histologic maturation of the endometrium. Obstet Gynecol 1993; 81: 439–43.Google Scholar
151Li, TC, Dalton, C, Hunjan, KS, Warren, MA, Bolton, AE. The correlation of placental protein 14 concentrations in uterine flushing and endometrial morphology in the peri-implantation period. Hum Reprod 1993; 8: 1923–27.CrossRefGoogle ScholarPubMed
152McRae, MA, Galle, PC, Joshi, SG. The role of measurement of progestagen-associated endometrial protein in predicting adequate endometrial differentiation. Hum Reprod 1991; 6: 761–65.CrossRefGoogle ScholarPubMed
153Seif, MW, Apiin, JD, Foden, LJ, Tindall, VR. A novel approach for monitoring the endometrial cycle and detecting ovulation. Am J Obstet Gynecol 1989; 160: 357–62.CrossRefGoogle ScholarPubMed
154Seif, MW, Aplin, JD, Buckley, CH. Luteal phase defect: the possibility of an immunohistochemical diagnosis. Fertil Steril 1989; 51: 273–79.CrossRefGoogle ScholarPubMed
155Seif, MW, Pearson, JM, Ibrahim, ZH et al. Endometrium in in vitro fertilization cycles: morphological and functional differentiation in the implantation phase. Hum Reprod 1992; 7: 6–11.CrossRefGoogle ScholarPubMed
156Lessey, BA, Castelbaum, AJ, Guzick, D, Sun, J, Fritz, M. The use ofintegrins as markers of uterine receptivity to date the endometrial biopsy [Abstract]. Annual Meeting of the American Fertility Society, San Antonio, TX, 1994; 0–77: S38.Google Scholar
157Somkuti, SG, Yowell, CM, Lessey, BA. Effect of oral contraceptive pills on markers of uterine receptivity [Abstract], Annual Meeting of the American Fertility Society, San Antonio, TX, 1994; 0–139: S68.Google Scholar
158Lessey, BA, Castelbaum, AJ, Riben, M, Howarth, J, Tureck, R, Meyer, WR. Effect of hydrosalpinges on markers of uterine receptivity and success in IVF [Abstract]. Annual Meeting of the American Fertility Society, San Antonio, TX, 1994; 0–91: S45.Google Scholar
159Sharara, FI, Beatse, SN, Leonardi, MR, Navot, D, Scott, RT Jr. Cigarette smoking accelerates the development of diminished ovarian reserve as evidenced by the clomiphene citrate challenge test. Fertil Steril 1994; 62: 257–62.CrossRefGoogle ScholarPubMed