Development, Vol 119, Issue 4 1175-1186, Copyright © 1993 by Company of Biologists

JOURNAL ARTICLES

Developmental regulation of integrin expression at the time of implantation in the mouse embryo

AE Sutherland, PG Calarco and CH Damsky
Department of Stomatology, University of California San Francisco 94143.

The trophectoderm layer of the mouse blastocyst differentiates at the late blastocyst stage to form the invasive trophoblast that mediates implantation of the embryo into the uterine wall. The first sign that trophoblast cells have developed an invasion-specific cell behavior appears about 10-15 hours after the embryo hatches from the zona pellucida, when the quiescent, non-adherent trophectoderm cells initiate protrusive activity and become adhesive to extracellular matrix. Our previous findings that trophoblast outgrowth on extracellular-matrix-coated substrata involves the integrin family of adhesion receptors (Sutherland, A. E., Calarco, P. G. and Damsky, C. H., 1988, J. Cell Biol. 106, 1331-1348), suggested that the onset of trophoblast adhesive and migratory behavior at the time of implantation may be due to changes in expression or distribution of integrin receptors. We have thus examined the mRNA and protein expression of individual integrin subunits during pre- and periimplantation development (E0-E7.5). A basic repertoire of integrins, including receptors for fibronectin (alpha 5 beta 1), laminin (alpha 6B beta 1) and vitronectin (alpha v beta 3), was expressed continuously throughout this period, whereas the expression of five other integrin subunits was developmentally regulated. The mRNA for three of these (alpha 2, alpha 6A and alpha 7) was first detected in the late blastocyst, coincident with endoderm differentiation and development of attachment competence. The mRNA for another (alpha 1) was not detected until after trophoblast outgrowth had begun, suggesting that its expression may be induced by contact with matrix. At E7.5, three of the temporally regulated integrins (alpha 1, apha 6A, alpha 7), all of which can form receptors for laminin, were detected only in the ectoplacental cone (differentiating trophoblast), and may thus play specific roles in trophoblast adhesion and/or differentiation. Because laminin expression is upregulated in decidualized uterine stroma in response to the implanting embryo, we examined trophoblast-laminin interactions, using laminin fragments and integrin antibodies to determine which integrin receptors were involved. Trophoblast cells attached and spread on both the E8 and P1' fragments of laminin; however, the P1' binding site was cryptic in intact laminin. Interaction with P1' was RGD- and alpha v beta 3-dependent, whereas outgrowth on E8 was RGD-independent and not inhibited by antibodies to the laminin receptor alpha 6 beta 1, suggesting that alpha 7 beta 1 is the major trophoblast integrin E8 receptor.(ABSTRACT TRUNCATED AT 400 WORDS)
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				C. A. Souders, S. L.K. Bowers, and T. A. Baudino Cardiac Fibroblast: The Renaissance Cell Circ. Res., December 4, 2009; 105(12): 1164 - 1176. [Abstract] [Full Text] [PDF]

				P. Snider, K. N. Standley, J. Wang, M. Azhar, T. Doetschman, and S. J. Conway Origin of Cardiac Fibroblasts and the Role of Periostin Circ. Res., November 6, 2009; 105(10): 934 - 947. [Abstract] [Full Text] [PDF]

				U. Vjugina, X. Zhu, E. Oh, N. J. Bracero, and J. P. Evans Reduction of Mouse Egg Surface Integrin Alpha9 Subunit (ITGA9) Reduces the Egg's Ability to Support Sperm-Egg Binding and Fusion Biol Reprod, April 1, 2009; 80(4): 833 - 841. [Abstract] [Full Text] [PDF]

				J. E. Roberts, S. N. Nikolopoulos, O. Oktem, F. Giancotti, and K. Oktay Integrin {beta}-4 Signaling Plays a Key Role in Mouse Embryogenesis Reproductive Sciences, March 1, 2009; 16(3): 286 - 293. [Abstract] [PDF]

				F. J White, R. C Burghardt, J. Hu, M. M Joyce, T. E Spencer, and G. A Johnson Secreted phosphoprotein 1 (osteopontin) is expressed by stromal macrophages in cyclic and pregnant endometrium of mice, but is induced by estrogen in luminal epithelium during conceptus attachment for implantation. Reproduction, December 1, 2006; 132(6): 919 - 929. [Abstract] [Full Text] [PDF]

				A. D. Gultice, K. L. Selesniemi, and T. L. Brown Hypoxia Inhibits Differentiation of Lineage-Specific Rcho-1 Trophoblast Giant Cells Biol Reprod, June 1, 2006; 74(6): 1041 - 1050. [Abstract] [Full Text] [PDF]

				L. J. Van Winkle, J. K. Tesch, A. Shah, and A. L. Campione System B0,+ amino acid transport regulates the penetration stage of blastocyst implantation with possible long-term developmental consequences through adulthood Hum. Reprod. Update, March 1, 2006; 12(2): 145 - 157. [Abstract] [Full Text] [PDF]

				K. D. Cowden Dahl, S. E. Robertson, V. M. Weaver, and M. C. Simon Hypoxia-inducible Factor Regulates {alpha}v{beta}3 Integrin Cell Surface Expression Mol. Biol. Cell, April 1, 2005; 16(4): 1901 - 1912. [Abstract] [Full Text] [PDF]

				K. Y Lee and F. J DeMayo Animal models of implantation Reproduction, December 1, 2004; 128(6): 679 - 695. [Abstract] [Full Text] [PDF]

				O. A. Mohamed, D. Dufort, and H. J. Clarke Expression and Estradiol Regulation of Wnt Genes in the Mouse Blastocyst Identify a Candidate Pathway for Embryo-Maternal Signaling at Implantation Biol Reprod, August 1, 2004; 71(2): 417 - 424. [Abstract] [Full Text] [PDF]

				A H K El-Hashash and S J Kimber Trophoblast differentiation in vitro: establishment and characterisation of a serum-free culture model for murine secondary trophoblast giant cells Reproduction, July 1, 2004; 128(1): 53 - 71. [Abstract] [Full Text] [PDF]

				S. K. Dey, H. Lim, S. K. Das, J. Reese, B. C. Paria, T. Daikoku, and H. Wang Molecular Cues to Implantation Endocr. Rev., June 1, 2004; 25(3): 341 - 373. [Abstract] [Full Text] [PDF]

				Y.-L. Lee, K.-F. Lee, J.-S. Xu, Q.-Y. He, J.-F. Chiu, W. M. Lee, J. M. Luk, and W. S. B. Yeung The Embryotrophic Activity of Oviductal Cell-derived Complement C3b and iC3b, a Novel Function of Complement Protein in Reproduction J. Biol. Chem., March 26, 2004; 279(13): 12763 - 12768. [Abstract] [Full Text] [PDF]

				K. Nagaoka, H. Nojima, F. Watanabe, K.-T. Chang, R. K. Christenson, S. Sakai, and K. Imakawa Regulation of Blastocyst Migration, Apposition, and Initial Adhesion by a Chemokine, Interferon {gamma}-inducible Protein 10 kDa (IP-10), during Early Gestation J. Biol. Chem., August 1, 2003; 278(31): 29048 - 29056. [Abstract] [Full Text] [PDF]

				K.B.C. Apparao, M. J. Illera, S. A. Beyler, G. E. Olson, K. G. Osteen, M. H. Corjay, K. Boggess, and B. A. Lessey Regulated Expression of Osteopontin in the Peri-Implantation Rabbit Uterus Biol Reprod, May 1, 2003; 68(5): 1484 - 1490. [Abstract] [Full Text] [PDF]

				M. J. Illera, P.L. Lorenzo, Y.-t. Gui, S. A. Beyler, K.B.C. Apparao, and B. A. Lessey A Role for {alpha}v{beta}3 Integrin During Implantation in the Rabbit Model Biol Reprod, March 1, 2003; 68(3): 766 - 771. [Abstract] [Full Text] [PDF]

				S. Basak, R. Dhar, and C. Das Steroids Modulate the Expression of {alpha}4 Integrin in Mouse Blastocysts and Uterus During Implantation Biol Reprod, June 1, 2002; 66(6): 1784 - 1789. [Abstract] [Full Text] [PDF]

				D. M. MacIntyre, H. C. Lim, K. Ryan, S. Kimmins, J. A. Small, and L. A. MacLaren Implantation-Associated Changes in Bovine Uterine Expression of Integrins and Extracellular Matrix Biol Reprod, May 1, 2002; 66(5): 1430 - 1436. [Abstract] [Full Text] [PDF]

				X. Zhu and J. P. Evans Analysis of the Roles of RGD-Binding Integrins, {alpha}4/{alpha}9 Integrins, {alpha}6 Integrins, and CD9 in the Interaction of the Fertilin {beta} (ADAM2) Disintegrin Domain with the Mouse Egg Membrane Biol Reprod, April 1, 2002; 66(4): 1193 - 1202. [Abstract] [Full Text] [PDF]

				D.J. Bloor, A.D. Metcalfe, A. Rutherford, D.R. Brison, and S.J. Kimber Expression of cell adhesion molecules during human preimplantation embryo development Mol. Hum. Reprod., March 1, 2002; 8(3): 237 - 245. [Abstract] [Full Text] [PDF]

				S. Lacin, S. Vatansever, N.K. Kuscu, F. Koyuncu, K. Ozbilgin, and E. Ceylan Clomiphene citrate does not affect the secretion of {alpha}3, {alpha}V and {beta}1 integrin molecules during the implantation window in patients with unexplained infertility Hum. Reprod., November 1, 2001; 16(11): 2305 - 2309. [Abstract] [Full Text] [PDF]

				G. A. Johnson, F. W. Bazer, L. A. Jaeger, H. Ka, J. E. Garlow, C. Pfarrer, T. E. Spencer, and R. C. Burghardt Muc-1, Integrin, and Osteopontin Expression During the Implantation Cascade in Sheep Biol Reprod, September 1, 2001; 65(3): 820 - 828. [Abstract] [Full Text] [PDF]

				S. Shiokawa, K. Sakai, Y. Akimoto, N. Suzuki, H. Hanashi, S. Nagamatsu, M. Iwashita, Y. Nakamura, H. Hirano, and Y. Yoshimura Function of the Small Guanosine Triphosphate-Binding Protein RhoA in the Process of Implantation J. Clin. Endocrinol. Metab., December 1, 2000; 85(12): 4742 - 4749. [Abstract] [Full Text]

				J. Hescheler and B. K. Fleischmann Integrins and cell structure: powerful determinants of heart development and heart function Cardiovasc Res, September 1, 2000; 47(4): 645 - 647. [Full Text] [PDF]

				M. J. Illera, E. Cullinan, Y. Gui, L. Yuan, S. A. Beyler, and B. A. Lessey Blockade of the {alpha}v{beta}3 Integrin Adversely Affects Implantation in the Mouse Biol Reprod, May 1, 2000; 62(5): 1285 - 1290. [Abstract] [Full Text]

				J. A. Bowen and J. S. Hunt The Role of Integrins in Reproduction Experimental Biology and Medicine, April 1, 2000; 223(4): 331 - 343. [Abstract] [Full Text] [PDF]

				K. Blaschuk, E. Frost, and C ffrench-Constant The regulation of proliferation and differentiation in oligodendrocyte progenitor cells by alphaV integrins Development, January 5, 2000; 127(9): 1961 - 1969. [Abstract] [PDF]

				M. Janatpour, M. McMaster, O Genbacev, Y Zhou, J Dong, J. Cross, M. Israel, and S. Fisher Id-2 regulates critical aspects of human cytotrophoblast differentiation, invasion and migration Development, January 2, 2000; 127(3): 549 - 558. [Abstract] [PDF]

				J Wang, L Mayernik, J. Schultz, and D. Armant Acceleration of trophoblast differentiation by heparin-binding EGF-like growth factor is dependent on the stage-specific activation of calcium influx by ErbB receptors in developing mouse blastocysts Development, January 1, 2000; 127(1): 33 - 44. [Abstract] [PDF]

				T. Maruyama, Y. Yoshimura, and H. Sabe Tyrosine Phosphorylation and Subcellular Localization of Focal Adhesion Proteins during in Vitro Decidualization of Human Endometrial Stromal Cells Endocrinology, December 1, 1999; 140(12): 5982 - 5990. [Abstract] [Full Text]

				S. Kimmins and L. A. MacLaren Cyclic Modulation of Integrin Expression in Bovine Endometrium Biol Reprod, November 1, 1999; 61(5): 1267 - 1274. [Abstract] [Full Text]

				S. Shiokawa, Y. Yoshimura, H. Sawa, S. Nagamatsu, H. Hanashi, K. Sakai, M. Ando, and Y. Nakamura Functional Role of Arg-Gly-Asp (RGD)-Binding Sites on ß1 Integrin in Embryo Implantation Using Mouse Blastocysts and Human Decidua Biol Reprod, June 1, 1999; 60(6): 1468 - 1474. [Abstract] [Full Text]

				M.S. Chen, E.A.C. Almeida, A.-P.J. Huovila, Y. Takahashi, L.M. Shaw, A.M. Mercurio, and J.M. White Evidence that Distinct States of the Integrin {alpha}6{beta}1 Interact with Laminin and an ADAM J. Cell Biol., February 8, 1999; 144(3): 549 - 561. [Abstract] [Full Text] [PDF]

				J. A. Bowen and J. S. Hunt Expression of Cell Adhesion Molecules in Murine Placentas and a Placental Cell Line Biol Reprod, February 1, 1999; 60(2): 428 - 434. [Abstract] [Full Text] [PDF]

				S Testaz, M Delannet, and J Duband Adhesion and migration of avian neural crest cells on fibronectin require the cooperating activities of multiple integrins of the (beta)1 and (beta)3 families J. Cell Sci., January 12, 1999; 112(24): 4715 - 4728. [Abstract] [PDF]

				A De Arcangelis, M Mark, J Kreidberg, L Sorokin, and E Georges-Labouesse Synergistic activities of alpha3 and alpha6 integrins are required during apical ectodermal ridge formation and organogenesis in the mouse Development, January 9, 1999; 126(17): 3957 - 3968. [Abstract] [PDF]

				R Anderson, R Fassler, E Georges-Labouesse, R. Hynes, B. Bader, J. Kreidberg, K Schaible, J Heasman, and C Wylie Mouse primordial germ cells lacking beta1 integrins enter the germline but fail to migrate normally to the gonads Development, January 4, 1999; 126(8): 1655 - 1664. [Abstract] [PDF]

				P. Clément-Lacroix, C. Ormandy, L. Lepescheux, P. Ammann, D. Damotte, V. Goffin, B. Bouchard, M. Amling, M. Gaillard-Kelly, N. Binart, et al. Osteoblasts Are a New Target for Prolactin: Analysis of Bone Formation in Prolactin Receptor Knockout Mice Endocrinology, January 1, 1999; 140(1): 96 - 105. [Abstract] [Full Text]

				A.I. Rojas and A.R. Ahmed Adhesion Receptors in Health and Disease Critical Reviews in Oral Biology & Medicine, January 1, 1999; 10(3): 337 - 358. [Abstract] [Full Text] [PDF]

				S. S. Sidhu and S. J. Kimber Hormonal Control of H-Type {alpha}(1-2)Fucosyltransferase Messenger Ribonucleic Acid in the Mouse Uterus Biol Reprod, January 1, 1999; 60(1): 147 - 157. [Abstract] [Full Text]

				D.-K. Kim, E. Morii, H. Ogihara, K. Hashimoto, K. Oritani, Y.-M. Lee, T. Jippo, S. Adachi, Y. Kanakura, and Y. Kitamura Impaired Expression of Integrin alpha -4 Subunit in Cultured Mast Cells Derived From Mutant Mice of mi/mi Genotype Blood, September 15, 1998; 92(6): 1973 - 1980. [Abstract] [Full Text] [PDF]

				A. Pozzi, K. K. Wary, F. G. Giancotti, and H. A. Gardner Integrin {alpha}1{beta}1 Mediates a Unique Collagen-dependent Proliferation Pathway In Vivo J. Cell Biol., July 27, 1998; 142(2): 587 - 594. [Abstract] [Full Text] [PDF]

				C. Baudoin, M.-J. Goumans, C. Mummery, and A. Sonnenberg Knockout and knockin of the beta 1 exon D define distinct roles for integrin splice variants in heart function and embryonic development Genes & Dev., April 15, 1998; 12(8): 1202 - 1216. [Abstract] [Full Text]

				A. MacAuley, J. C. Cross, and Z. Werb Reprogramming the Cell Cycle for Endoreduplication in Rodent Trophoblast Cells Mol. Biol. Cell, April 1, 1998; 9(4): 795 - 807. [Abstract] [Full Text]

				M. L. Kireeva, S. C.-T. Lam, and L. F. Lau Adhesion of Human Umbilical Vein Endothelial Cells to the Immediate-Early Gene Product Cyr61 Is Mediated through Integrin alpha vbeta 3 J. Biol. Chem., January 30, 1998; 273(5): 3090 - 3096. [Abstract] [Full Text] [PDF]

				J Wang, U. Rout, I. Bagchi, and D. Armant Expression of calcitonin receptors in mouse preimplantation embryos and their function in the regulation of blastocyst differentiation by calcitonin Development, January 11, 1998; 125(21): 4293 - 4302. [Abstract] [PDF]

				C Brakebusch, E Hirsch, A Potocnik, and R Fassler Genetic analysis of beta1 integrin function: confirmed, new and revised roles for a crucial family of cell adhesion molecules J. Cell Sci., January 12, 1997; 110(23): 2895 - 2904. [Abstract] [PDF]

				A. J. Castelbaum, L. Ying, S. G. Somkuti, J. Sun, A. O. Ilesanmi, and B. A. Lessey Characterization of Integrin Expression in a Well Differentiated Endometrial Adenocarcinoma Cell Line (Ishikawa) J. Clin. Endocrinol. Metab., January 1, 1997; 82(1): 136 - 142. [Abstract] [Full Text] [PDF]

				B. L. Ziober and R. H. Kramer Identification and Characterization of the Cell Type-specific and Developmentally Regulated alpha 7 Integrin Gene Promoter J. Biol. Chem., September 13, 1996; 271(37): 22915 - 22922. [Abstract] [Full Text] [PDF]

				R Fassler, J Rohwedel, V Maltsev, W Bloch, S Lentini, K Guan, D Gullberg, J Hescheler, K Addicks, and A. Wobus Differentiation and integrity of cardiac muscle cells are impaired in the absence of beta 1 integrin J. Cell Sci., January 12, 1996; 109(13): 2989 - 2999. [Abstract] [PDF]

				T. Lallier, C. Whittaker, and D. DeSimone Integrin alpha 6 expression is required for early nervous system development in Xenopus laevis Development, January 8, 1996; 122(8): 2539 - 2554. [Abstract] [PDF]

				G Raab, K Kover, B. Paria, S. Dey, R. Ezzell, and M Klagsbrun Mouse preimplantation blastocysts adhere to cells expressing the transmembrane form of heparin-binding EGF-like growth factor Development, January 2, 1996; 122(2): 637 - 645. [Abstract] [PDF]

				L E Stephens, A E Sutherland, I V Klimanskaya, A Andrieux, J Meneses, R A Pedersen, and C H Damsky Deletion of beta 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes & Dev., August 1, 1995; 9(15): 1883 - 1895. [Abstract] [PDF]

				R Fassler and M Meyer Consequences of lack of beta 1 integrin gene expression in mice. Genes & Dev., August 1, 1995; 9(15): 1896 - 1908. [Abstract] [PDF]

				W. Yin, E. Smiley, J. Germiller, C. Sanguineti, T. Lawton, L. Pereira, F. Ramirez, and J. Bonadio Primary Structure and Developmental Expression of Fbn-1, the Mouse Fibrillin Gene J. Biol. Chem., January 27, 1995; 270(4): 1798 - 1806. [Abstract] [Full Text] [PDF]

				O Behrendtsen, C. Alexander, and Z Werb Cooperative interactions between extracellular matrix, integrins and parathyroid hormone-related peptide regulate parietal endoderm differentiation in mouse embryos Development, January 12, 1995; 121(12): 4137 - 4148. [Abstract] [PDF]

				J. Evans, R. Schultz, and G. Kopf Mouse sperm-egg plasma membrane interactions: analysis of roles of egg integrins and the mouse sperm homologue of PH-30 (fertilin) beta J. Cell Sci., January 10, 1995; 108(10): 3267 - 3278. [Abstract] [PDF]

				E. Newman-Smith and Z Werb Stem cell defects in parthenogenetic peri-implantation embryos Development, January 7, 1995; 121(7): 2069 - 2077. [Abstract] [PDF]

				J. Cross, Z Werb, and S. Fisher Implantation and the placenta: key pieces of the development puzzle Science, December 2, 1994; 266(5190): 1508 - 1518. [Abstract] [PDF]

				C. Damsky, C Librach, K. Lim, M. Fitzgerald, M. McMaster, M Janatpour, Y Zhou, S. Logan, and S. Fisher Integrin switching regulates normal trophoblast invasion Development, January 12, 1994; 120(12): 3657 - 3666. [Abstract] [PDF]

				S. E. Domino, L. Zhang, and J. B. Lowe Molecular Cloning, Genomic Mapping, and Expression of Two Secretor Blood Group alpha (1,2)Fucosyltransferase Genes Differentially Regulated in Mouse Uterine Epithelium and Gastrointestinal Tract J. Biol. Chem., June 22, 2001; 276(26): 23748 - 23756. [Abstract] [Full Text] [PDF]