Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

β1 and β3 integrins disassemble from basal focal adhesions and β3 integrin is later localised to the apical plasma membrane of rat uterine luminal epithelial cells at the time of implantation

Yui Kaneko A C , Laura Lecce A , Margot L. Day B and Christopher R. Murphy A
+ Author Affiliations
- Author Affiliations

A School of Medical Sciences (Discipline of Anatomy and Histology) and The Bosch Institute, Anderson Stuart Building, The University of Sydney, Sydney, NSW 2006, Australia.

B School of Medical Sciences (Discipline of Physiology) and The Bosch Institute, The Medical Foundation Building, The University of Sydney, Sydney, NSW 2050, Australia.

C Corresponding author. Email: ykan0009@anatomy.usyd.edu.au

Reproduction, Fertility and Development 23(3) 481-495 https://doi.org/10.1071/RD10211
Submitted: 1 September 2010  Accepted: 27 October 2010   Published: 16 March 2011

Abstract

The present study investigated the expression of integrin subunits that are known to be associated with focal adhesions, namely β1 and β3 integrins in rat uterine luminal epithelial cells during early pregnancy. The β1 and β3 integrins were concentrated along the basal cell surface and were colocalised and structurally interacted with talin, a principal focal adhesion protein, on Day 1 of pregnancy. At the time of implantation, β1 and β3 integrins disassembled from the site of focal adhesions, facilitating the removal of uterine luminal epithelial cells for embryo invasion. Also at this time, β3 integrin markedly increased along the apical membrane, suggesting a role in embryo attachment. This distributional change in β1 and β3 integrins seen at the time of implantation was predominantly under the influence of progesterone. Taken together, β1 and β3 integrin disassembly from focal adhesions and the increase in β3 integrin apically are key components of hormonally regulated endometrial receptivity.

Additional keyword: ovarian hormones.


References

Ahmad, I., Hoessli, D. C., Walker-Nasir, E., Choudhary, M. I., Rafik, S. M., Shakoori, A. R., and Nasir-ud-Din, (2006). Phosphorylation and glycosylation interplay: protein modifications at hydroxy amino acids and prediction of signaling functions of the human beta 3 integrin family. J. Cell. Biochem. 99, 706–718.
Phosphorylation and glycosylation interplay: protein modifications at hydroxy amino acids and prediction of signaling functions of the human beta 3 integrin family.CrossRef | 1:CAS:528:DC%2BD28XhtVClu77J&md5=253ba6690edbc49d9e9038eeb5ec4fd8CAS | 16676352PubMed |

Aplin, J. D. (1997). Adhesion molecules in implantation. Rev. Reprod. 2, 84–93.
Adhesion molecules in implantation.CrossRef | 1:CAS:528:DyaK2sXktV2nurw%3D&md5=cc9979eea2b71202b8f88e8e98a81b08CAS | 9414470PubMed |

Aplin, J. D., Spanswick, C., Behzad, F., Kimber, S. D., and Vićovac, L. (1996). Integrins beta 5, beta 3 and alpha v are apically distributed in endometrial epithelium. Mol. Hum. Reprod. 2, 527–534.
Integrins beta 5, beta 3 and alpha v are apically distributed in endometrial epithelium.CrossRef | 1:CAS:528:DyaK28Xls1Cmsb4%3D&md5=b400537cedfc921a9433b22e81b7a1b5CAS | 9239663PubMed |

Bellis, S. L. (2004). Variant glycosylation: an underappreciated regulatory mechanism for beta 1 integrins. Biochim. Biophys. Acta 1663, 52–60.
Variant glycosylation: an underappreciated regulatory mechanism for beta 1 integrins.CrossRef | 1:CAS:528:DC%2BD2cXkt1Smtrk%3D&md5=0f94b2dc2cdb38603a58dfe83e34a693CAS | 15157607PubMed |

Bhatt, A., Irina, K., Otey, O., and Huttenlocher, A. (2002). Regulation of focal complex composition and disassembly by the calcium-dependent protease calpain. J. Cell Sci. 115, 3415–3425.
| 1:CAS:528:DC%2BD38XntFamt7Y%3D&md5=098d0e4fc9b8e66564475cbcb6fd7b5eCAS | 12154072PubMed |

Blystone, S. D., Williams, M. P., Slater, S. E., and Brown, E. J. (1997). Requirement of integrin β3 tyrosine 747 for β3 tyrosine phosphorylation and regulation of αvβ3 avidity. J. Biol. Chem. 272, 28 757–28 761.
Requirement of integrin β3 tyrosine 747 for β3 tyrosine phosphorylation and regulation of αvβ3 avidity.CrossRef | 1:CAS:528:DyaK2sXntlCqu70%3D&md5=47afca4ed9180acd132afc14ca2af05cCAS |

Boettiger, D., Lynch, L., Blystone, S. D., and Huber, F. (2001). Distict ligand-binding modes for integrin αvβ3 mediated adhesion to fibronectin versus vitronectin. J. Biol. Chem. 276, 31 684–31 690.
Distict ligand-binding modes for integrin αvβ3 mediated adhesion to fibronectin versus vitronectin.CrossRef | 1:CAS:528:DC%2BD3MXms1Smsrs%3D&md5=d269470f12f0f1b3d72ca70d158a3d02CAS |

Bowen, J. A., and Hunt, J. S. (2000). The role of integrins in reproduction. Proc. Soc. Exp. Biol. Med. 223, 331–343.
The role of integrins in reproduction.CrossRef | 1:CAS:528:DC%2BD3cXitlCqtrc%3D&md5=84248272b5400d0ba20277cfc83b0d4cCAS | 10721002PubMed |

Bowen, J. A., Bazer, F. W., and Burghardt, R. C. (1996). Spatial and temporal analyses of integrin and Muc-1 expression in porcine uterine epithelium and trophectoderm in vivo. Biol. Reprod. 55, 1098–1106.
Spatial and temporal analyses of integrin and Muc-1 expression in porcine uterine epithelium and trophectoderm in vivo.CrossRef | 1:CAS:528:DyaK28Xmtlart78%3D&md5=c48ea6ac2bc6a3b36e33bec0b39d2e0bCAS | 8902223PubMed |

Bronson, R. A., and Fusi, F. M. (1996). Integrins and human reproduction. Mol. Hum. Reprod. 2, 153–168.
Integrins and human reproduction.CrossRef | 1:CAS:528:DyaK28XkslGrtrY%3D&md5=e93aceb9ef06705e773ad7304b80f727CAS | 9238675PubMed |

Brown, M. C., and Turner, C. E. (2004). Paxillin: adapting to change. Physiol. Rev. 84, 1315–1339.
Paxillin: adapting to change.CrossRef | 1:CAS:528:DC%2BD2cXovVyltbw%3D&md5=8a106b9e2eb18b7ec083f8bd4ee31da6CAS | 15383653PubMed |

Calderwood, D. A. (2004a). Integrin activation. J. Cell Sci. 117, 657–666.
Integrin activation.CrossRef | 1:CAS:528:DC%2BD2cXhvVOntrc%3D&md5=5e638a5a8dacf781622f37a606dd0211CAS | 14754902PubMed |

Calderwood, D. A. (2004b). Talin controls integrin activation. Biochem. Soc. Trans. 32, 434–437.
Talin controls integrin activation.CrossRef | 1:CAS:528:DC%2BD2cXksFyhsLo%3D&md5=c112617f2671aa28e23e8a1240b068f5CAS | 15157154PubMed |

Calderwood, D. A., and Ginsberg, M. H. (2003). Talin forges the links between integrins and actin. Nat. Cell Biol. 5, 694–697.
Talin forges the links between integrins and actin.CrossRef | 1:CAS:528:DC%2BD3sXlvV2gtrw%3D&md5=c8c0c3258c8c36b18959319e0fdcc07cCAS | 12894175PubMed |

Calderwood, D. A., Zent, R., Grant, R., Rees, D. J., Hynes, R. O., and Ginsberg, M. H. (1999). The talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation. J. Biol. Chem. 274, 28 071–28 074.
The talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation.CrossRef | 1:CAS:528:DyaK1MXmsFWgsLc%3D&md5=bce2e717754e63392ffb3b7ef224620bCAS |

Chammas, R., Veiga, S. S., Travassos, L. R., and Brentani, R. R. (1993). Functionally distinct roles for glycosylation of α and β integrin chains in cell–matrix interactions. Proc. Natl Acad. Sci. USA 90, 1795–1799.
Functionally distinct roles for glycosylation of α and β integrin chains in cell–matrix interactions.CrossRef | 1:CAS:528:DyaK3sXhs1KjsL8%3D&md5=acf3d675996227d73b91ffe893df5dbeCAS |

Critchley, D. R. (2000). Focal adhesions: the cytoskeletal connection. Curr. Opin. Cell Biol. 12, 133–139.
Focal adhesions: the cytoskeletal connection.CrossRef | 1:CAS:528:DC%2BD3cXhsVOjt74%3D&md5=75488c57695d1bbadf139912df243d23CAS | 10679361PubMed |

Fässler, R., Georges-Labouesse, E., and Hirsch, E. (1996). Genetic analyses of integrin function in mice. Curr. Opin. Cell Biol. 8, 641–646.
Genetic analyses of integrin function in mice.CrossRef | 8939651PubMed |

Fazleabas, A. T., Bell, S. C., Fleming, S., Sun, J., and Lessey, B. A. (1997). Distribution of integrins and the extracellular matrix proteins in the baboon endometrium during the menstrual cycle and early pregnancy. Biol. Reprod. 56, 348–356.
Distribution of integrins and the extracellular matrix proteins in the baboon endometrium during the menstrual cycle and early pregnancy.CrossRef | 1:CAS:528:DyaK2sXosFOntA%3D%3D&md5=9fe7f1a065a47d7d6229dc24dca2b12fCAS | 9116133PubMed |

Finn, C. A., and Porter, D. G. (1975). ‘The Uterus.’ (Elek Science:London.)

Franco, S. J., and Huttenlocher, A. (2005). Regulating cell migration: calpains make the cut. J. Cell Sci. 118, 3829–3838.
Regulating cell migration: calpains make the cut.CrossRef | 1:CAS:528:DC%2BD2MXhtVOqtr7O&md5=7173890bb6eaaebed5c7c54b6abb176eCAS | 16129881PubMed |

Franco, S., Perrin, B., and Huttenlocher, A. (2004a). Isoform specific function of calpain 2 in regulating membrane protrusion. Exp. Cell Res. 299, 179–187.
Isoform specific function of calpain 2 in regulating membrane protrusion.CrossRef | 1:CAS:528:DC%2BD2cXmsVKgu70%3D&md5=f438e4772e079fc056a9bd3d5a7a4aa0CAS | 15302585PubMed |

Franco, S. J., Rodgers, M. A., Perrin, B. J., Han, J., Bennin, D. A., Critchley, D. R., and Huttenlocher, A. (2004b). Calpain-mediated proteolysis of talin regulates adhesion dynamics. Nat. Cell Biol. 6, 977–983.
Calpain-mediated proteolysis of talin regulates adhesion dynamics.CrossRef | 1:CAS:528:DC%2BD2cXnvFGqs7Y%3D&md5=791be467dd066eeac06dfbc74af328fbCAS | 15448700PubMed |

Frisch, S. M., and Screaton, R. A. (2001). Anoikis mechanisms. Curr. Opin. Cell Biol. 13, 555–562.
Anoikis mechanisms.CrossRef | 1:CAS:528:DC%2BD3MXmsFersLs%3D&md5=c4db8160dc66f4a35fd82b8265d289eaCAS | 11544023PubMed |

Galán, A., O’Connor, J. E., Valbuena, D., Herrer, R., Remohí, J., Pampfer, S., Pellicer, A., and Simón, C. (2000). The human blastocyst regulates endometrial epithelial apoptosis in embryonic adhesion. Biol. Reprod. 63, 430–439.
| 10906047PubMed |

García, P., Nieto, A., Sánchez, M. A., Pizarro, M., and Flores, J. M. (2004). Expression of αv, α4, α5 and β3 integrin subunits, fibronectin and vitronectin in goat peri-implantation. Anim. Reprod. Sci. 80, 91–100.
Expression of αv, α4, α5 and β3 integrin subunits, fibronectin and vitronectin in goat peri-implantation.CrossRef | 15036518PubMed |

Giancotti, F. G., and Ruoslahti, E. (1999). Integrin signaling. Science 285, 1028–1032.
Integrin signaling.CrossRef | 1:CAS:528:DyaK1MXlt1Gns7o%3D&md5=d6031ddac1cc3a6e68f11887ec188c85CAS | 10446041PubMed |

Gu, J., and Taniguchi, N. (2004). Regulation of integrin functions by N-glycans. Glycoconj. J. 21, 9–15.
Regulation of integrin functions by N-glycans.CrossRef | 1:CAS:528:DC%2BD2cXotFWntb0%3D&md5=7c88cb6577f004509a4e1ade797d965aCAS | 15467392PubMed |

Hodivala-Dilke, K. M., McHugh, K. P., Tsakiris, D. A., Rayburn, H., Crowley, D., Ullman-Culleré, M., Ross, F. P., Coller, B. S., Teitelbaum, S., and Hynes, R. O. (1999). Beta3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J. Clin. Invest. 103, 229–238.
Beta3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival.CrossRef | 1:CAS:528:DyaK1MXltFeqtQ%3D%3D&md5=fd2eb04d874713a6ce5a626f6e2db684CAS | 9916135PubMed |

Hynes, R. O. (1992). Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11–25.
Integrins: versatility, modulation, and signaling in cell adhesion.CrossRef | 1:CAS:528:DyaK38XitFWmtrg%3D&md5=ef862d6c39f1185701b754aa0c33a732CAS | 1555235PubMed |

Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673–687.
Integrins: bidirectional, allosteric signaling machines.CrossRef | 1:CAS:528:DC%2BD38XnsFKis70%3D&md5=2f54b90a313b79f198459c45d65284c6CAS | 12297042PubMed |

Illera, M. J., Cullinan, E., Gui, Y., Yuan, L., Beyler, S. A., and Lessey, B. A. (2000). Blockade of the alpha(v)beta(3) integrin adversely affects implantation in the mouse. Biol. Reprod. 62, 1285–1290.
Blockade of the alpha(v)beta(3) integrin adversely affects implantation in the mouse.CrossRef | 1:CAS:528:DC%2BD3cXisl2htLo%3D&md5=89ac722fcc744ca5091b6b082e299d30CAS | 10775178PubMed |

Illera, M. J., Lorenzo, P. L., Gui, Y., Beyler, S. A., Apparao, K. B. C., and Lessey, B. A. (2003). A role for alphavbeta3 integrin during implantation in the rabbit model. Biol. Reprod. 68, 766–771.
| 1:CAS:528:DC%2BD3sXhsFGlurY%3D&md5=552bf377db94c8423e8a2699b825b9bfCAS | 12604624PubMed |

Johnson, G. A., Bazer, F. W., Jaeger, L. A., Ka, H., Garlow, J. E., Pfarrer, C., Spencer, T. E., and Burghardt, R. C. (2001). Muc-1, integrin, and osteopontin expression during the implantation cascade in sheep. Biol. Reprod. 65, 820–828.
Muc-1, integrin, and osteopontin expression during the implantation cascade in sheep.CrossRef | 1:CAS:528:DC%2BD3MXmtFems7k%3D&md5=9efcb2b8a0eff7e3e0c5ba62e481474dCAS | 11514347PubMed |

Kaneko, Y., Lindsay, L., and Murphy, C. R. (2008). Focal adhesions disassemble during early pregnancy in rat uterine epithelial cells. Reprod. Fertil. Dev. 20, 892–899.
Focal adhesions disassemble during early pregnancy in rat uterine epithelial cells.CrossRef | 1:CAS:528:DC%2BD1cXht1Oks77E&md5=ab273052c2e41ffc2c0c963e94b232f3CAS | 19007553PubMed |

Kaneko, Y., Lecce, L., and Murphy, C. R. (2009). Ovarian hormones regulate expression of the focal adhesion proteins, talin and paxillin, in rat uterine luminal but not glandular epithelial cells. Histochem. Cell Biol. 132, 613–622.
Ovarian hormones regulate expression of the focal adhesion proteins, talin and paxillin, in rat uterine luminal but not glandular epithelial cells.CrossRef | 1:CAS:528:DC%2BD1MXhsVWms7%2FK&md5=2838df3fd48ea90624a144d090d51c43CAS | 19779731PubMed |

Lessey, B. A. (1997). Integrins and the endometrium: new markers of uterine receptivity. Ann. N. Y. Acad. Sci. 828, 111–122.
Integrins and the endometrium: new markers of uterine receptivity.CrossRef | 1:CAS:528:DyaK2sXmvFyksL0%3D&md5=af3716f8f12eaf02ba5afe9863ff14b7CAS | 9329829PubMed |

Lessey, B. A., and Arnold, J. T. (1998). Paracrine signaling in the endometrium: integrins and the establishment of uterine receptivity. J. Reprod. Immunol. 39, 105–116.
Paracrine signaling in the endometrium: integrins and the establishment of uterine receptivity.CrossRef | 1:CAS:528:DyaK1cXls1yms7o%3D&md5=583d922fdaa147b944330c711f4a43bcCAS | 9786456PubMed |

Lessey, B. A., Damjanovich, L., Coutifaris, C., Castelbaum, A., Albelda, S. M., and Buck, C. A. (1992). Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle. J. Clin. Invest. 90, 188–195.
Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle.CrossRef | 1:CAS:528:DyaK38XltVyruro%3D&md5=d8d8d18723788b9c1c49146d819d34faCAS | 1378853PubMed |

Lessey, B. A., Castelbaum, A. J., Buck, C. A., Lei, Y., Yowell, C. W., and Sun, J. (1994a). Further characterization of endometrial integrins during the menstral cycle and in pregnancy. Fertil. Steril. 62, 497–506.
| 1:STN:280:DyaK2czktFeqtg%3D%3D&md5=fa570b9493031830020c7eab33442354CAS | 8062944PubMed |

Lessey, B. A., Castelbaum, A. J., Sawin, S. W., Buck, C. A., Schinnar, R., Bilker, W., and Strom, B. L. (1994b). Aberrant integrin expression in the endometrium of women with endometriosis. J. Clin. Endocrinol. Metab. 79, 643–649.
Aberrant integrin expression in the endometrium of women with endometriosis.CrossRef | 1:STN:280:DyaK2czitFCqtg%3D%3D&md5=4a354cfb80f0de51d2922dd970c4429eCAS | 7519194PubMed |

Lessey, B. A., Castelbaum, A. J., Sawin, S. W., and Sun, J. (1995). Integrins as markers of uterine receptivity in women with primary unexplained infertility. Fertil. Steril. 63, 535–542.
| 1:STN:280:DyaK2M7lsVGjsw%3D%3D&md5=c4505c272b5abad62589581f2a719415CAS | 7851583PubMed |

Lessey, B. A., Castelbaum, A. J., Wolf, L., Greene, W., Paulson, M., Meyer, W. R., and Fritz, M. A. (2000). Use of integrins to date the endometrium. Fertil. Steril. 73, 779–787.
Use of integrins to date the endometrium.CrossRef | 1:STN:280:DC%2BD3c7pvVWjug%3D%3D&md5=5d3cf7382c8d26e58b4efa84b1eaed1cCAS | 10731541PubMed |

Lin, H., Wang, X., Liu, G., Fu, J., and Wang, A. (2007). Expression of alphaV and beta3 integrin subunits during implantation in pig. Mol. Reprod. Dev. 74, 1379–1385.
Expression of alphaV and beta3 integrin subunits during implantation in pig.CrossRef | 1:CAS:528:DC%2BD2sXhtFektr7N&md5=2441f63153a858e557253ebf44e56f6fCAS | 17440962PubMed |

Liu, S., Calderwood, D. A., and Ginsberg, M. H. (2000). Integrin cytoplasmic domain-binding proteins. J. Cell Sci. 113, 3563–3571.
| 1:CAS:528:DC%2BD3cXosVKgtLY%3D&md5=e27834837d691685917b79e4622e3b93CAS | 11017872PubMed |

Lo, S. H. (2006). Focal adhesions: what’s new inside. Dev. Biol. 294, 280–291.
Focal adhesions: what’s new inside.CrossRef | 1:CAS:528:DC%2BD28XmtVOhtbw%3D&md5=2caa2d5330c6d8331f5da7e3965b448cCAS | 16650401PubMed |

Meredith, J., Mu, Z., Saido, T., and Du, X. (1998). Cleavage of the cytoplasmic domain of the integrin beta 3 subunit during endothelial cell apoptosis. J. Biol. Chem. 273, 19 525–19 531.
Cleavage of the cytoplasmic domain of the integrin beta 3 subunit during endothelial cell apoptosis.CrossRef | 1:CAS:528:DyaK1cXlt1Citr8%3D&md5=df2e437997e58c77f0560ebb65c11ae8CAS |

Murphy, C. R. (2001). The plasma membrane transformation: a key concept in uterine receptivity. Reprod. Med. Rev. 9, 197–208.
The plasma membrane transformation: a key concept in uterine receptivity.CrossRef | 1:CAS:528:DC%2BD38XlsFOlur0%3D&md5=7e9d5b125cd6057d2fd42658b92f7fa4CAS |

Murphy, C. R. (2004). Uterine receptivity and the plasma membrane transformation. Cell Res. 14, 259–267.
Uterine receptivity and the plasma membrane transformation.CrossRef | 15353123PubMed |

Murphy, C. R., Swift, J. G., Mukherjee, T. M., and Rogers, A. W. (1981). Effects of ovarian hormones on cell membranes in the rat uterus II. Freeze-fracture studies on tight junctions of the lateral plasma membrane of the luminal epithelium. Cell Biophys. 3, 57–69.
Effects of ovarian hormones on cell membranes in the rat uterus II. Freeze-fracture studies on tight junctions of the lateral plasma membrane of the luminal epithelium.CrossRef | 1:CAS:528:DyaL3MXktlKju7k%3D&md5=d062798dcc09b2c47d4f70d19575f0eaCAS | 6167362PubMed |

Parr, E. L., Tung, H. N., and Parr, M. B. (1987). Apoptosis as the mode of uterine epithelial cell death during embryo implantation in mice and rats. Biol. Reprod. 36, 211–225.
Apoptosis as the mode of uterine epithelial cell death during embryo implantation in mice and rats.CrossRef | 1:STN:280:DyaL2s7osFKkuw%3D%3D&md5=03070f47cde8e865ded089208b6e2e12CAS | 3567276PubMed |

Pfaff, M., Liu, S., Erle, D. J., and Ginsberg, M. H. (1998). Integrin b cytoplasmic domains differentially bind to cytoskeletal proteins. J. Biol. Chem. 273, 6104–6109.
Integrin b cytoplasmic domains differentially bind to cytoskeletal proteins.CrossRef | 1:CAS:528:DyaK1cXitFalsrg%3D&md5=bb2e1c90cd42cef7d5a019be8ad0a55aCAS | 9497328PubMed |

Reddy, K. V. R., and Mangale, S. S. (2003). Integrin receptors: the dynamic modulators of endometrial function. Tissue Cell 35, 260–273.
Integrin receptors: the dynamic modulators of endometrial function.CrossRef | 1:CAS:528:DC%2BD3sXmt1egtL8%3D&md5=f12af42496f8d376aced71a07051d0c6CAS | 12921709PubMed |

Regidor, P. A., Vogel, C., Regidor, M., Schindler, A. E., and Winterhager, E. (1998). Expression pattern of integrin adhesion molecules in endometriosis and human endometrium. Hum. Reprod. Update 4, 710–718.
Expression pattern of integrin adhesion molecules in endometriosis and human endometrium.CrossRef | 1:CAS:528:DyaK1MXhvVShtrg%3D&md5=3ae830c549c5b91d2ff42ba16cb30912CAS | 10027624PubMed |

Schwartz, M. A., Schaller, M. D., and Ginsberg, M. H. (1995). Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell Dev. Biol. 11, 549–599.
Integrins: emerging paradigms of signal transduction.CrossRef | 1:CAS:528:DyaK2MXps1aqt7w%3D&md5=5cc7193273f6a0950940b4f75653d458CAS | 8689569PubMed |

Srinivasan, K. R., Blesson, C. S., Fatima, I., Kitchlu, S., Jain, S. K., Mehrotra, P. K., and Dwivedi, A. (2009). Expression of alphaVbeta3 integrin in rat endometrial epithelial cells and its functional role during implantation. Gen. Comp. Endocrinol. 160, 124–133.
Expression of alphaVbeta3 integrin in rat endometrial epithelial cells and its functional role during implantation.CrossRef | 1:CAS:528:DC%2BD1MXksVGgtg%3D%3D&md5=88ff9886f3d652d287aeab2fdf5852b6CAS | 19027743PubMed |

Tabibzadeh, S. (1992). Patterns of expression of integrin molecules in human endometrium throughout the menstrual cycle. Hum. Reprod. 7, 876–882.
| 1:CAS:528:DyaK38XlvVyqurg%3D&md5=d884259a21d47ebe3f125e907e7644b0CAS | 1500489PubMed |

Tassell, W., Slater, M., Barden, J. A., and Murphy, C. R. (2000). Endometrial cell death during early pregnancy in the rat. Histochem. J. 32, 373–379.
Endometrial cell death during early pregnancy in the rat.CrossRef | 1:STN:280:DC%2BD3M%2FltlWlsg%3D%3D&md5=c551b1cd2bca847120baa82de72d874fCAS | 10943852PubMed |

Turner, C. E. (2000). Paxillin and focal adhesion signalling. Nat. Cell Biol. 2, E231–E236.
Paxillin and focal adhesion signalling.CrossRef | 1:CAS:528:DC%2BD3cXptFShtbw%3D&md5=81061dbef415c0fd95c6f724405e327fCAS | 11146675PubMed |

Vuori, K. (1998). Integrin signaling: tyrosine phosphorylation events in focal adhesions. J. Membr. Biol. 165, 191–199.
Integrin signaling: tyrosine phosphorylation events in focal adhesions.CrossRef | 1:STN:280:DyaK1cvktVOntw%3D%3D&md5=38d68e0cb86c9066ee861d3ff43ae223CAS | 9767673PubMed |

Wang, J., and Armant, D. R. (2002). Integrin-mediated adhesion and signaling during blastocyst implantation. Cells Tissues Organs 172, 190–201.
Integrin-mediated adhesion and signaling during blastocyst implantation.CrossRef | 1:CAS:528:DC%2BD38XpsVSjur4%3D&md5=8a33bc8844611d0f83235391e97c7413CAS | 12476048PubMed |

Welsh, A. O. (1993). Uterine cell death during implantation and early placentation. Microsc. Res. Tech. 25, 223–245.
Uterine cell death during implantation and early placentation.CrossRef | 1:STN:280:DyaK2c%2FgtlCksw%3D%3D&md5=3e36310226c2a10efba2720a65bdb0b8CAS | 8400423PubMed |

Yamada, K. M., and Geiger, B. (1997). Molecular interactions in cell adhesion complexes. Curr. Opin. Cell Biol. 9, 76–85.
Molecular interactions in cell adhesion complexes.CrossRef | 1:CAS:528:DyaK2sXhtFams7k%3D&md5=7931d91b73dc4b6a04c933989ddb9256CAS | 9013677PubMed |



Rent Article (via Deepdyve) Export Citation Cited By (24)