Integrins and Extracellular Matrix Proteins at the Maternal-Fetal Interface in Domestic AnimalsBurghardt R.C.a,b · Johnson G.A.d · Jaeger L.A.a,b · Ka H.a,c · Garlow J.E.a,c · Spencer T.E.a,c · Bazer F.W.a,c
aCenter for Animal Biotechnology and Genomics, Department of Veterinary Anatomy and Public Health, bCollege of Veterinary Medicine, cDepartment of Animal Science, Texas A&M University, College Station, Tex., dDepartment of Animal and Veterinary Science and Center for Reproductive Biology, University of Idaho, Moscow, Idaho, USA
Do you have an account?
- Rent for 48h to view
- Buy Cloud Access for unlimited viewing via different devices
- Synchronizing in the ReadCube Cloud
- Printing and saving restrictions apply
Rental: USD 8.50
Cloud: USD 20.00
Establishment of pregnancy in mammals requires coordinated conceptus-maternal interactions involving numerous hormones, growth factors and cytokines acting via specific receptors in the uterus. Uterine secretions play an important role in establishing synchrony between development of the conceptus and uterine receptivity, as well as in conceptus remodeling, adhesion, implantation and placentation in domestic species. Studies of non-invasive implantation in domestic livestock provide valuable opportunities to investigate fundamental processes of the initial events of apposition, attachment and adhesive interactions that are shared among species. In pigs and sheep, it appears that integrins play a dominant role in these fundamental processes via interactions with extracellular matrix molecules and other ligands to transduce cellular signals in uterine epithelial cells and conceptus trophectoderm. This review considers several of the potential integrin-binding ligands involved in the complex implantation adhesion cascade in pigs and sheep along with in vitro evidence for the transduction of cytoplasmic signals that may be required to sustain fetal and maternal contributions to the formation of the epitheliochorial placenta.
© 2002 S. Karger AG, Basel
- Aoki, R., M.N. Fukuda (2000) Recent molecular approaches to elucidate the mechanism of embryo implantation: trophinin, bystin, and tastin as molecules involved in the initial attachment of blastocysts to the uterus in humans. Semin Reprod Med 18: 265–271.
- Aplin, J.D., C. Spanswick, F. Behzad, S.J. Kimber, L.J. Vicova (1996) Integrins β5,β3 and αv are apically distributed in human and mouse endometrial epithelium. Mol Human Reprod 2:527–534.
- Aplin, J.D. (1997) Adhesion molecules in implantation. Rev Reprod 2: 84–93.
- Aplin, J.D. (1999) Muc-1 glycosylation in endometrium: possible roles of the apical glycocalyx at implantation. Human Reprod 14(suppl 2): 17–25.
- Aplin, J.D, T. Haigh, C. J.P. Jones, H. J. Church, L. Vicovac (1999) Development of cytotrophoblast columns from explanted first-trimester human placental villi: role of fibronectin and integrin α5β1. Biol Reprod 60: 828–838.
- Aplin, J.D., H. Lacey, T. Haigh, C.J. Jones, C.P. Chen, M. Westwood (2000) Growth factor-extracellular matrix synergy in the control of trophoblast invasion. Biochem Soc Trans 28:199–202.
Apparao, K.B.C., A.F. Chambers, B.A. Lessey (2001) Progesterone receptor isoform-B modulates the expression of osteopontin in human endometrial epithelium during the window of implantation. SGI Year 2001 Annual Meeting abstract 43.
- Armant, D.R., H.A. Kaplan, W.I. Lennarz (1986a) Fibronectin and laminin promote in vitro-attachment and outgrowth of mouse blastocyst. Dev Biol 116: 519–529.
- Armant, D.R., H.A. Kaplan, H. Mover, W.I. Lennarz (1986b) The effects 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 83:6751–6755.
- Bartlett, S.E., A.R. Menino Jr. (1993) Partial characterization of the plasminogen activator produced by ovine embryos in vitro. Biol Reprod 49: 381–386.
- Bayless, K.J., G.E. Davis (2001) Identification of dual alpha 4beta 1 integrin binding sites within a 38 amino acid domain in the N-terminal thrombin fragment of human osteopontin. J Biol Chem. 276: 13483–13489.
- Bayless, K.J., G.A. Meininger, J.M. Scholtz , G.E. Davis (1998) Osteopontin is a ligand for the α4β1 integrin. J Cell Sci 111: 1165–1174.
- Bazer, F.W. (1975) Uterine protein secretions: relationship to development of the conceptus. J Anim Sci 41: 1376–1382.
- Bazer, F.W. (1992) Mediators of maternal recognition of pregnancy in mammals. Proc Soc Exp Biol Med 199: 373–384.
- Bazer, F.W., R.M. Roberts (1983) Biochemical aspects of conceptus-endometrial interactions. J Exp Zool 228: 373–384.
- Bischof, P., E. Freidli, M. Martelli, A. Campana (1991) Expression of extracellular matrix degrading metalloproteinases by cultured human cytotrophoblast cells: effects of cell adhesion and immunopurification. Am J Obstet Gynecol 165: 1791–1801.
- Bischof, P., M. Martelli (1992) Proteolysis in the penetration phase of the implantation process. Placenta 13: 17–24.
- Bowen, J.A., F.W. Bazer, R.C. Burghardt (1996) Spatial and temporal analysis of integrin and Muc-1 expression in porcine uterine epithelium and trophectoderm in vivo. Biol Reprod 55: 1098–1106.
- Bowen, J.A., F.W. Bazer, R.C. Burghardt (1997) Spatial and temporal analyses of integrin and Muc-1 expression in porcine uterine luminal epithelium and trophectoderm in vitro. Biol Reprod 56: 409–415.
- Brown, L.F., B. Berse, L.Van de Water, A. Papadopoulos-Sergiose, C.A. Peruzzi, E.J. Manseau, H.F. Dvorak, D.R. Senger (1992) Expression and distribution of osteopntin in human tissues: widespread association with luminal epithelial surfaces. Mol Biol Cell 3: 1169–1180.
Burghardt, R.C., J.A. Bowen, G.R. Newton, F.W. Bazer (1997) Extracellular matrix and the implantation cascade in pigs. J Reprod Fert Suppl 52: 151–164.
Burton, G.J. (1992) Human and animal models: limitations and comparisons; in Barnea, E.R., J.Hustin, E. Janiaux (eds): The first twelve weeks of gestation. Berlin, Springer, pp 469–485.
Butler, W.T., A.L. Ridall, M.D. McKee (1996) Osteopontin; in Principals of bone biology. New York, Academic Press, pp 167–181.
- Campbell S., H.R. Swann, M.W. Seif, S.J. Kimber, J.D. Aplin (1995) Cell adhesion molecules on the oocyte and preimplantation human embryo. Hum Reprod 10: 1571–1578.
- Cancel, A.M., D.A. Chapman, G.J. Killian (1999) Osteopontin localization in the Holstein bull reproductive tract. Biol Reprod 60: 454–460.
- Carson, D.D., M.M. DeSouza, R. Kardon, X. Zhou, E. Lagow, J. Julian (1998) Mucin expression and function in the female reproductive tract. Hum Reprod Update 4: 459–464.
- Carson, D.D., I. Bagchi, S.K.Dey, A.C. Enders, A.T. Fazleabas, B.A. Lessey, K. Yoshinaga (2000) Embryo implantation. Dev Biol 223:217–237.
- Casslen, B., B. Astedt (1983) Occurrence of both urokinase and tissue plasminogen activator in the human endometrium. Contraception 28:553–564.
- Corthorn, J., Valdes G. (1994) Variations in uterine kallikrein during cycle and early pregnancy in the rat. Biol Reprod 50: 1261–1264.
- Corthorn, J., C. Figueroa, G. Valdes (1997) Estrogen and luminal stimulation of rat uterine kallikrein. Biol Reprod 56: 1432–1438.
Coutifaris, C., P. Ziolkiewicz, A. Omigbodun, J. Harper (1997) Osteopontin in human endometrium: a role for this secretory protein in uterine receptivity and embryo implantation; in Serono Symposia USA. International Symposium on Embryo Implantation: Molecular, Cellular and Clinical Aspects; 14 (abstract).
- Coutifaris, C., A. Omigbodun, G. Coukos (1998) Integrins, endometrial maturation, & human embryo implantation. Sem Reprod Endocrinol 16: 219–229.
- Craig, A.M., D.T. Denhardt (1991) The murine gene encoding secreted phosphoprotein 1 (osteopontin), promoter structure, activity and induction in vivo by estrogen and progesterone. Gene 100: 163–171.
- Critchley, D.R. (2000) Focal adhesions – the cytoskeletal connection. Curr Opin Cell Biol 12:133–139.
- Daiter, E., A. Omigbodum, S. Wang, D. Walinsky, J.F. Strass III, J.R. Hoyer, C. Coutifaris (1996) Cell differentiation and endogenous cyclic adenosine 3′,5′-monophosphate regulate osteopontin expression in human trophoblasts. Endocrinology 137: 1785–1790.
- Damsky, C., A. Sutherland, S. Fisher (1993) Extracellular matrix 5: adhesive interactions in early mammalian embryogenesis, implantation, and placentation. FASEB J 7: 1320–1329.
- Damsky, C.H., C. Librach, K.H. Lim, M.L. Fitzgerald, M.T. McMaster, M. Janatpour, Y. Zhou, S.K. Logan, S.J. Fisher (1994) Integrin switching regulates normal trophoblast invasion. Development 120: 3657–3666.
- Das, S.K., S. Yano, J. Wang, D.R. Edwards, H. Nagese, S.K. Dey (1997) Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in the mouse uterus during the peri-implantation period. Dev Genet 21: 44–54.
- Dedhar, S. (1999) Integrins and signal transduction. Curr Opin Hematol. 6: 37–43.
- Denda, S., L.F. Reichardt, U. Muller (1998) Identification of osteopontin as a novel ligand for the integrin alpha8 beta1 and potential roles for this integrin-ligand interaction in kidney morphogenesis. Mol Biol Cell 9: 1425–1435.
- Denhardt, D.T., X. Guo (1993) Osteopontin: a protein with diverse functions. FASEB J 7: 1475–1483.
- DeSouza, M.M., S.K. Mani, J. Julian, D.D. Carson (1998) Reduction of mucin-1 expression during the receptive phase in the rat uterus. Biol Reprod 58: 1503–1507.
- Fazleabas, A.T., R.D. Geisert, F.W. Bazer, R.M. Roberts (1983) Relationship between release of plasminogen activator and estrogens by blastocysts and secretion of plasmin inhibitor by uterine endometrium in the pregnant pig. Biol Reprod 29: 225–238.
- Fazleabas, A.T., S.C. Bell, S. Fleming, J. Sun, B.A. Lessey (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.
- Feinberg, R.F., H.J. Kliman, C.J. Lockwood (1991) Is oncofetal fibronectin a trophoblast glue for human implantation. Am J Pathol 138: 537–543.
- Feinberg, R.F., H.J. Kliman, C.L. Wang (1994) Transforming growth factor-beta stimulates trophoblast oncofetal fibronectin synthesis in vitro: implications for trophoblast implantation in vivo. J Clin Endocrinol Metab 78: 1241–1248.
- Feng, J., J.F. Woessner, Jr, C. Zhu (1998) Matrilysin activity in the rat uterus during the oestrous cycle and implantation. J Reprod Fertil 114:347–350.
- Fisher, L.W., D.A. Torchia, B. Fohr, M.F. Young, N.S. Fedarko (2001) Flexible structures of SIBLING proteins, bone sialoprotein, and osteopontin. Biochem Biophys Res Comm 280: 460–465.
- Franzen, A., D. Heinegard (1985) Isolation and characterization of two sialoproteins present only in bovine calcified matrix. Biochem J 232:715–724.
Gabler, C., D.A.Chapman, R.L. Gerena, E.S. Sorenso, G.J. Killian (1999) Osteopontin is present in the bovine oviduct epithelium and luminal fluid. Biol Reprod 60(suppl 1): 186.
- Garlow, J.E., H. Ka, G.A. Johnson, R.C. Burghardt, L.A. Jaeger, F.W. Bazer (2002) Analysis of osteopontin at the maternal-placental interface in pigs. Biol Reprod 66:718–725.
- Geisert, R.D., R.M. Blair, T. Pratt, M.T. Zavy (1997) Characterization and proteolytic activity of a cathepsin L-like polypeptide in endometrium and uterine flushings of cycling, pregnant and steroid-treated ovariectomized gilts. Reprod Fertil Dev 9: 395–402.
- Geisert, R.D., J.V. Yelich (1997) Regulation of conceptus development and attachment in pigs. J Reprod Fertil Suppl 52: 133–149.
- Geisert, R.D., J.V. Yelich, T. Pratt, D. Pomp (1998) Expression of an inter-α-trypsin inhibitor heavy chain-like protein in the pig endometrium during the oestrous cycle and early pregnancy. J Reprod Fert 114: 35–43.
- George, E.L., E.N. George-Labouesse, R.S. Patel-King, H. Rayburn, R.O. Hynes (1993) Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119: 1079–1091.
- Giancotti, F.G., E. Ruoslahti (1999) Integrin Signaling. Science 285: 1028–1032.
- Gray, C.A., K.M. Taylor, F.W. Bazer, T.E. Spencer (2000) Mechanisms regulating norgestomet inhibition of endometrial gland morphogenesis in the neonatal ovine uterus. Mol Reprod Dev 57: 67–78.
- Gray, C.A., F.W. Bazer, T.E. Spencer (2001) Effects of neonatal progestin exposure on female reproductive tract structure and function in the adult ewe. Biol Reprod 64: 797–804.
- Gupta, A., F.W. Bazer and L.A. Jaeger (1996) Differential expression of TGFβs (TGFβ1, TGFβ2, TGFβ3) and their receptors (Type I and Type II) in peri-implantation porcine conceptuses. Biol Reprod 55: 796–802.
- Gupta, A., F.W. Bazer and L.A. Jaeger (1997) Immunolocalization of acidic and basic fibroblast growth factors in porcine uterine and conceptus tissues. Biol Reprod 56: 1527–1536.
- Gupta, A., C.M. Dekaney, F.W. Bazer, M.M. Madrigal, L.A. Jaeger (1998a) Beta transforming growth factors (TGFβs) at the porcine conceptus-maternal interface. Part II: Uterine TGFβ bioactivity and expression of immunoreactive TGFβs (TGFβ1, TGFβ2, and TGFβ 3) and their receptors (Type I and Type II). Biol Reprod 59: 911–917.
- Gupta, A., N.H. Ing, F.W. Bazer, L.S. Bustamante, L.A. Jaeger (1998b) Beta transforming growth factors (TGFβs) at the porcine conceptus-maternal interface. Part I: Expression of TGFβ1, TGFβ2, and TGFβ3 messenger ribonucleic acids. Biol Reprod 59: 905–910.
- Henrikson, K.P., E.S. Hall, Y. Lin (1994) Cellular localization of tissue factor and prothrombin in the estrogen-treated immature rat uterus. Biol Reprod 50: 1145–1150.
- Hettinger, A.M., M.R. Allen, B.R. Zhang, D.W. Goad, J.R. Malayer, R.D. Geisert (2001) Presence of the acute phase protein, bikunin, in the endometrium of gilts during estrous cycle and early pregnancy. Biol Reprod 65: 507–513.
Hocking, D.C., J.Sottile, K.J. Langenbach (2000) Stimulation of integrin-mediated cell contractility by fibronectin polymerization J Biol Chem 275: 10673–10682.
- Hoffman, L.H., G.E. Olson, D.D. Carson, B.S. Chilton (1998) Progesterone and implanting blastocysts regulate Muc1 expression in rabbit uterine epithelium. Endocrinology 139: 266–271.
- Hu, D.D., E.C.K. Lin, N.L. Kovach, J.R. Hoyer, J.W. Smith (1995) A biochemical characterization of the binding of osteopontin to integrins αvβ1 and αvβ5. J Biol Chem 270: 26232–26238.
- Illera, M.J., E. Cullinan, Y. Gui, S.A. Beyler, B.A. Lessey (2000) Blockade of the αvβ3 integrin adversely affects implantation in the mouse. Biol Reprod 62: 1285–1290.
Irwin, J.C., L.C. Giudice (1998) IGFBP-1 binds to the placental cytotrophoblast α5β1 integrin and inhibits cytotrophoblast invasion into decidualized endometrial stromal cell cultures. Growth Horm IGF Res 8: 21–31.
Jaeger, L.A., L.S. Bustamante, G.A. Johnson, F.W. Bazer, R.C. Burghardt (2000a) Functional activation of conceptus and maternal integrins. FASEB J 14: A783.
Jaeger, L.A., R.C. Burghardt, G.A. Johnson, F.W. Bazer (2000b) Activation of conceptus and maternal integrins by transforming growth factor beta latency associated peptide. Biol Reprod 62(suppl 1): 281.
- Johansson, S., G. Svineng, K. Wennerberg, A. Armulik, L. Lohikangas (1997) Fibronectin-integrin interactions. Front Biosci 2:d126–146.
- Johnson, G.A., T.E. Spencer, R.C. Burghardt, F.W. Bazer (1999a) Ovine osteopontin: I. Cloning and expression of mRNA in the uterus during the peri-implantation period. Biol Reprod 61:884–891.
- Johnson, G.A., R.C. Burghardt, T.E. Spencer, G.R. Newton, T.L. Ott, F.W. Bazer (1999b) Ovine osteopontin: II. Osteopontin and αvβ3 integrin expression in the uterus and conceptus during the peri-implantation period. Biol Reprod 61:892–899.
- Johnson, G.A., T.E. Spencer, R.C. Burghardt, K.M. Taylor, C.A. Gray, F.W. Bazer (2000) Progesterone modulation of osteopontin gene expression in the ovine uterus. Biol Reprod 62: 1315–1321.
- Johnson, G.A., F.W. Bazer, L.A. Jaeger, H. Ka, J.E. Garlow, C. Pfarrer, T.E. Spencer, R.C. Burghardt (2001) Muc-1, integrin and osteopontin expression during the implantation cascade in sheep. Biol Reprod 65: 820–828.
- Jones, J.I., A. Gockerman, W.H. Busby, D.R. Clemmons (1993) IGFBP-1 stimulates cell migration and binds to the α5β1 integrin by means of its Arg-Gly Asp sequence. Proc Natl Acad Sci USA 90: 10553–10557.
- Kimber, S.J., C. Spanswick (2000) Blastocyst implantation: the adhesion cascade. Semin Cell Develop Biol 11: 77–92.
- Komatsu, M., C.A.C. Carraway, N.L. Fregien, K.L. Carraway (1997) Reversible disruption of cell-matrix and cell-cell interactions by overexpression of sialomucin complex. J Biol Chem 272:33245–33254.
- Lasky, L.A., M. Singer, D. Dowbenko, Y. Imai, W. Henzel, C. Grimley, C. Finnie, N. Gillett, S. Watson, S. Rosen (1992) An endothelial ligand for L-selectin is a novel mucin-like molecule. Cell 69: 927–938
- Lecrone, V., W. Li, R.E. Devoll, C. Logothetis, M.C. Farach-Carson (2000) Calcium signals in prostate cancer cells: specific activation by bone matrix proteins. Cell Calcium 27: 35–42.
- Lefevre, F., F. Martinat-Botte, M. Guillomot, K. Zouari, B. Charley, C. La Bonnardiere (1990) Interferon-gamma gene and protein are spontaneously expressed by the porcine trophectoderm early in gestation. Eur J Immunol 20:2485–2490.
- Lefevre, F., F. Martinat-Botte, A. Locatelli, P. De Niu, M. Terqui C. La Bonnardiere (1998) Intrauterine infusion of high doses of pig trophoblast interferons has no antiluteolytic effect in cyclic gilts. Biol Reprod 58: 1026–1031.
- Lessey, B.A., L. Damjanovich, C. Coutifaris, A. Castelbaum, S.M. Albelda, C.A. Buck (1992) Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle. J Clin Invest 90: 188–195.
- Lessey, B.A., A.J. Castelbaum, C.A. Buck, Y. Lei, C.W. Yowell, J. Sun (1994a) Further characterization of endometrial integrins during the menstrual cycle and in pregnany. Fertil Steril 62: 497–506.
- Lessey, B.A., A.J. Castelbaum, S.W. Sawin, C.A. Buck, R. Schinnar, W. Bilker, B.L. Strom (1994b) Aberrant integrin expression in the endometrium of women with endometriosis. J Clin Endocrinol Metab 79: 643–649.
Lessey, B.A. (1995) Endometrial integrins. Endocrinologist 5: 214–221.
- Lessey, B.A., A.J. Castelbaum, S.W. Sawin, J. Sun (1995) Integrins as markers of uterine receptivity in women with primary unexplained infertility. Fertil Steril 63: 535–542.
Lessey, B.A., A.O. Ilesanmi, M.A. Lessey, M. Riben, J.F. Harris, K. Chwalisy (1996) Luminal and glandular endometrial epithelium express integrins differentially throughout the menstrual cycle: implications for implantation, contraception and infertility. Am J Reprod Immunol 35: 195–204.
Lessey, B.A. (2000) The role of the endometrium during embryo implantation. Hum Reprod (Suppl) 6: 39–50.
Liaw, L., D.E. Birk, C.B. Ballas, J.S. Whitsitt, J.M. Davidson, B.L.M. Hogan (1998) Altered wound healing in mice lacking a functional osteopontin gene (spp1). J Clin Invest 101:1468–1478.
Massague, J. (1998) TGF-β signal transduction Ann Rev Biochem 67: 753–791.
- McKee, M.D., A. Nanci, S.R. Khan (1995) Ultrastructural immunodetection of osteopontin and osteocalcin as major matrix components of renal calculi. J Bone Mineral Res 10: 1913–1929.
- Menino, A.R., A. Hogan, G.A. Schultz, S. Novak, W. Dixon, G.H. Foxcroft (1997) Expression of proteinases and proteinase inhibitors during embryo-uterine contact in the pig. Dev Genet 21: 68–74.
- Meseuger, M., J.D. Aplin, P. Caballero-Campo, J.E. O’Connor, J.C. Martín, J. Remohí, A. Pellicer, C. Simón (2001) Human endometrial MUC1 is up-regulated by progesterone and down-regulated in vitro by the human blastocyst. Biol Reprod 64: 590–601.
- Miyamoto, S., H. Teramoto, O.A. Coso, J.S Gutkind, P.D. Burbelo, S.K. Akiyama, K.M. Yamada (1995) Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J Cell Biol 131: 791–805.
- Miyamoto, S., H. Teramoto, J.S. Gutkind, K.M.Yamada (1996) Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation: roles of integrin aggregation and occupancy of receptors. J Cell Biol 135: 1633–1642.
- Monkley, S.J., X.H. Zhou, S.J. Kinston, S.M. Giblett, L. Hemmings, J.E. Brown, C.A. Pritchard, D.R. Critchley, R. Fassler (2000) Disruption of the talin gene arrests mouse development at the gastrulation stage. Dev Dyn 219: 560–574.
- Moro, L., M. Venturino, C. Bozzo, L. Silengo, F. Altruda, L. Beguinot, G. Tarone, P. Defilippi (1998) Integrins induce activation of EGF receptor: role in MAP kinase induction and adhesion-dependent cell survival. EMBO J 17: 6622–6632.
- Mukherjee, B.B., M. Nemir, S. Beninati, E. Cordella-Miele, K. Singh, I. Chackalaparampil, V. Shanmugam, M.W. DeVouge, A.B. Mukherjee (1995) Interaction of osteopontin with fibronectin and other extracellular matrix molecules. Ann NY Acad Sci 760: 201–202.
- Munger, J.S., J.G. Harpel, P.E. Gleizes, R. Mazzieri, I. Nunes, D.B. Rifkin (1997) Latent transforming growth factor beta – structural features and mechanisms of activation. Kidney Int 51: 1376–1382.
- Munger, J.S., J.G. Harpel, F.G. Giancotti, D.B. Rifkin (1998) Interactions between growth factors and integrins: latent forms of transforming growth factor-β are ligands for integrin αβ1. Mol Biol Cell 9: 2627–2638.
- Nomura, S., A.J. Wills, J.K. Edwards, J.K. Heath, B.L.M. Hogan (1988) Developmental expression of 2ar (osteopontin) and SPARC (osteonectin) RNA as revealed by in situ hybridization. J Cell Biol 106: 441–450.
- Omigbodun, A., P. Ziolkiewicz, C. Tessler, J.R. Hoyer, C. Coutifaris (1997) Progesterone regulates osteopontin expression in human trophoblasts: a model of paracrine control in the placenta. Endocrinology 138: 4308–4315.
- Ossowski, L., J.A. Aguirre-Ghiso (2000) Urokinase receptor and integrin partnership: coordination of signaling for cell adhesion, migration and growth. Curr Opin Cell Biol 12: 613–620.
- Preissner, K.T., S.M. Kanse, A.E. May (2000) Urokinase receptor: a molecular organizer in cellular communication. Curr Opin Cell Biol 12:621–628.
- Prince, C.W., D. Dickie, C.L. Krumdieck (1991) Osteopontin, a substrate for transglutaminase and factor XIII activity. Biochem Biophys Res Commun 177: 1205–1210.
- Psychoyos, A. (1976) Hormonal control of uterine receptivity for nidation. J Reprod Fertil Suppl 25: 17–28.
Rider, V., M. Piva (1998) Role of growth factors of uterine and fetal-placental origin during pregnancy; in Bazer, F.W. (ed): Endocrinology of pregnancy. New Jersey, Humana Press, pp 83–124.
- Rifkin, D.B., R. Mazzieri, J.S. Munger, I. Moguera, J. Sung (1999) Proteolytic control of growth factor availability. APMIS 107: 80–85.
- Riley, S.C., R. Leask, T. Chard, N.C. Wathen, A.A. Calder, D.C. Howe (1999) Secretion of matrix metalloproteinase-2, matrix metalloproteinase-9 and tissue inhibitor of metalloproteinases into the intrauterine compartments during early pregnancy. Mol Hum Reprod 5: 376–381.
- Rittling S.R., K.E. Novick (1997) Osteopontin expression in mammary gland development and tumorigenesis. Cell Growth Differ 8: 1061–1069.
- Rosen, S.D. (1993) L-Selectin and its biological ligands. Histochemistry 100: 185–191.
- Safran, J.P., W.T. Butler, M.C. Farach-Carson (1998) Modulation of osteopontin post-translational state by 1,25-(OH)2-vitamine D3. J Biol Chem 273: 29935–29941.
- Salamonsen, L.A., H. Nagase, D.E. Woolley (1991) Production of matrix metalloproteinase 3 (stromelysin) by cutlured ovine endometrial cells. J Cell Sci 100: 381–385.
- Salamonsen, L.A., H. Nagase, R. Suzuki, D.E. Woolley (1993) Production of matrix metalloproteinase 1 (interstitial collagenase) and matrix metalloproteinase 2 (gelatinase A: 72 kDa gelatinase) by ovine endometrial cells in vitro: different regulation and preferential expression by stromal fibroblasts. J Reprod Fertil 98: 583–589.
Salamonsen, L.A., R. Suzuki, H. Nagase, D.E. Woolley (1994) Matrix metalloproteinases: a role in implantation?; in Glasser, S.R., J. Mulholland, A. Psychoyos (eds): Endocrinology of embryo-endometrium interactions. New York, Plenum Press, pp 365–377.
- Salamonsen, L.A. (1999) Role of proteases in implantation. Rev Reprod 4: 11–22.
- Samuel, C.A., J.S. Perry (1972) The ultrastructure of pig trophoblast transplanted to an ectopic site in the uterine wall. J Anat 113: 139–149.
- Sappino, A.P., J. Huarte, D. Belin, J.D. Vassalli (1989) Plasminogen activators in tissue remodeling and invasion: mRNA localization in mouse ovaries and implanting embryos. J Cell Biol 109: 2471–2479.
- Schneller, M., K. Vuori, E. Ruoslahti (1997) αvβ3 integrin associates with activated insulin and PDGF receptors and potentiates the biological activity of PDGF. EMBO J 16: 5600–5607.
- Schultz, J.F., L. Mayernik, U.K. Rout, D.R. Armant (1997) Integrin trafficking regulates adhesion to fibronectin during differentiation of mouse peri-implantation blastocysts. Dev Genet 21: 31–43.
- Schwartz, M.A., K. Denninghoff (1994) Alpha v integrins mediate the rise in intracellular calcium in endothelial cells on fibronectin even though they play a minor role in adhesion. J Biol Chem 269: 11133–11137.
Senger, D.R., S.R. Ledbetter, K.P. Claffey, A. Papadopoulos-Sergiou, C.A. Peruzzi, M. Detmer (1996) Stimulation of endothelial cell migration by vascular permeability factor/vascular endothelial growth factor through cooperative mechanisms involving the alpha v beta 3 integrin, osteopontin, and thrombin. Am J Pathol 149: 203–305.
Sharpe-Timms, K.L., K.E. Cox, B. Ray, B.A. Lessey (2000) Localization of matrix metalloproteinase (MMP) enzymes, MMP-2 and MMP-3, to luminal endometrial epithelia by interaction with αvβ3 and αvβ5 integrins during the window of implantation. Biol Reprod 62(suppl. 1): 282.
- Smith, L.L., H.K. Cheung, L.E. Ling, J. Chen, D. Sheppard, R. Pytela, C.M.Giachelli (1996) Osteopontin N-terminal domain contains a cryptic adhesive sequence recognized by α9β1 integrin. J Biol Chem 271: 28485–28491.
- Soldi, R., S. Mitola, M. Strasly, P. Defilippi, G. Tarone, F. Bussolino (1999) Role of alphavbeta3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J 18:882–892.
- Spencer, T.E., Bazer F.W. (1995) Temporal and spatial alterations in uterine estrogen receptor and progesterone receptor gene expression during the estrous cycle and early pregnancy in the ewe. Bio Reprod 53: 1527–1543.
- Spencer, T.E., F.F. Bartol, F.W. Bazer, G.A. Johnson, M.M. Joyce (1999a) Identification and characterization of glycosylation-dependent cell adhesion molecule 1-like protein expression in the ovine uterus. Biol Reprod 60: 241–250.
- Spencer, T.E., A. Gray, G.A. Johnson, K.M. Taylor, A. Gertler, E. Gootwine, T.L. Ott, F.W Bazer (1999b) Effects of recombinant ovine interferon tau, placental lactogen, and growth hormone on the ovine uterus. Biol Reprod 61:1409–1418.
- Stewart, C.L., P. Kaspar, L.J. Brunet, H. Bhatt, I. Gadi, F. Kontgen, S.J. Abbondanzo (1992) Blastocyst implantation depends on maternal expression of leukemia inhibiting factor. Nature 359: 76–79.
- Strickland, S., E. Reich, M.I. Sherman (1976) Plasminogen activator in early embryogenesis: enzyme production by trophoblast and parietal endoderm. Cell 9: 231–240.
- Surveyor, G.A., S.J. Gendler, L. Pemberton, S.K. Das, I. Chakraborty, J. Julian, R.A. Pimental, C.C. Wegner, S.K. Dey, D.D. Carson (1995) Expression and steroid hormonal control of muc-1 in the mouse uterus. Endocrinology 136:3639–3647.
- Sutherland, A.E., P.G. Calarco, C.H. Damsky (1993) Developmental regulation of integrin expression at the time of implantation in the mouse embryo. Development 119: 1175–1186.
- Thorsteinsdottir, S., B.A. Roelen, E. Freund, A.C. Gaspar, A. Sonnenberg, C.L. Mummery (1995) Expression patterns of laminin receptor splice variants alpha 6A beta 1 and alpha 6B beta 1 suggest different roles in mouse development. Dev Dyn 204: 240–258.
- Tuo, W.B., F.W. Bazer (1996a) Expression of oncofetal fibronectin in porcine conceptuses and uterus throughout gestation. Reprod Fertil Dev 8: 1207–1213.
- Tuo, W.B., J.P., Harney, F.W. Bazer (1996b) Developmentally regulated expression of interleukin-1 beta by peri-implantation conceptuses in swine. J Reprod Immunol 31: 185–198.
- Valdes, G., J. Corthorn, A.G. Scicli, V. Gaete, J. Soto, M.E. Oritz, A. Foradori, G.M. Saed (1993) Uterine kallikrein in the early pregnant rat. Biol Reprod 49: 802–808.
- Valdes, G., C.D. Figueroa, J. Corthorn (1996) Temporospatial changes of kallikrein-like enzymes during the estrous cycle and pregnancy in the rat uterus. Biol Reprod 55: 236–245.
- Vonnahme, K.A., J.R. Malayer, H.O. Spivey, S.P. Ford, A. Clutter, R.D. Geisert (1999) Detection of kallikrein gene expression and enzymatic activity in porcine endometrium during the estrous cycle and early pregnancy. Biol Reprod 61: 1235–1241.
- Weber, G.F., H. Cantor (1996) The immunology of Eta-1/osteopontin. Cytokine Growth Factor Rev 7: 241–248.
- Wennerberg, K., L. Lohikangas, D. Gullberg, M. Pfaff, S. Johansson, R. Fässler (1996) B1 integrin-dependent and -independent polymerization of fibronectin. J Cell Biol 132: 227–238.
- Werb, Z., P. Tremble, C.H. Damsky (1990) Regulation of extracellular matrix degradation by cell-extracellular matrix interactions. Cell Differ Dev 32: 299–306.
- Wesseling, J., S.W. Van der Valk, H.L Vos, A. Sonnenberg, J. Hilkens (1995) Episialin (MUC-1) overexpression inhibits integrin mediated cell adhesion to extracellular matrix components. J Cell Biol 129: 255–265.
- Yelian, F.D., Y. Yang, J.D. Hirata, J.F. Schultz, D.R. Armant (1995) Molecular interactions between fibronectin and integrins during mouse blastocyst outgrowth. Mol Reprod Dev 41:435–448.
- Yelich, J.V., D. Pomp, R.D. Geisert (1997) Detection of transcripts for retinoic acid receptors, retinol-binding protein, and transforming growth factors during rapid trophoblastic elongation in the porcine conceptus. Biol Reprod 57: 286–294.
- Young, M.F., J.M. Kerr, J.D. Termine, U.M. Wewer, M.G. Wang, O.W. McBride, L.W. Fisher (1990) cDNA cloning, mRNA distribution and heterogeneity, chromosomal location, and RFLP analysis of human osteopontin (OPN). Genomics 7: 491–502.
- Zheng, X., T.L. Saunders, S.A. Camper, L.D. Samuelson, D. Ginsberg (1995) Vitronectin is not essential for mouse development and fertility. Proc Natl Acad Sci USA 92: 12426–12430.
- Zhou, Y., C.H. Damsky, K. Chiu, J.M. Roberts, S.J. Fisher (1993) Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J Clin Invest 91: 950–960.
- Zhu, L.-J., K. Cullinan-Bove, M. Polihronis, M.K. Bagchi, I.C. Bagchi (1998) Calcitonin is a progesterone-regulated marker that forecasts the receptive state of endometrium during implantation. Endocrinology 139: 3923–3934.
Article / Publication Details
Copyright / Drug Dosage / DisclaimerCopyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.