Blastocysts don't go it alone. Extrinsic signals fine-tune the intrinsic developmental program of trophoblast cells

Developmental Biology

Volumn 280, Issue 2, 2005, Pages 260-280

  Armant, D Randall ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Blastocyst implantation; Cell adhesion; Cell invasion; Epigenetic regulation; Extracellular matrix; Integrins; Intracellular calcium; Paracrine signaling; Protein trafficking; Trophoblast

Indexed keywords

FIBRONECTIN; FIBRONECTIN RECEPTOR; GROWTH FACTOR; INTEGRIN;

AUTOCRINE EFFECT; BLASTOCYST; CELL ADHESION; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINEAGE; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE EXPRESSION REGULATION; MICROENVIRONMENT; MOTHER FETUS RELATIONSHIP; NIDATION; NONHUMAN; PRIORITY JOURNAL; REGULATOR GENE; REVIEW; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; TROPHOBLAST; UTERUS;

EID: 18844381390     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2005.02.009     Document Type: Review

References (184)

1. A.L. Abbott, and T. Ducibella Calcium and the control of mammalian cortical granule exocytosis Front Biosci. 6 2001 D792 D806
2. S.L. Adamson, Y. Lu, K.J. Whiteley, D. Holmyard, M. Hemberger, C. Pfarrer, and J.C. Cross Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta Dev. Biol. 250 2002 358 373
3. A.E. Aplin, A. Howe, S.K. Alahari, and R.L. Juliano Signal transduction and signal modulation by cell adhesion receptors: the role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins Pharm. Rev. 50 1998 197 263
4. J.D. Aplin, T. Haigh, C.J. Jones, H.J. Church, and L. Vicovac Development of cytotrophoblast columns from explanted first-trimester human placental villi: role of fibronectin and integrin alpha 5 beta 1 Biol. Reprod. 60 1999 828 838
5. D.R. Armant Cell interactions with laminin and its proteolytic fragments during outgrowth of mouse primary trophoblast cells Biol. Reprod. 45 1991 664 672
6. D.R. Armant, and S. Kameda Mouse trophoblast cell invasion of extracellular matrix purified from endometrial tissue: a model for peri-implantation development J. Exp. Zool. 269 1994 146 156
7. D.R. Armant, H.A. Kaplan, and W.J. Lennarz Fibronectin and laminin promote in vitro attachment and outgrowth of mouse blastocysts Dev. Biol. 116 1986 519 523
8. D.R. Armant, H.A. Kaplan, and W.J. Lennarz N-linked glycoprotein biosynthesis in the developing mouse embryo Dev. Biol. 113 1986 228 237
9. D.R. Armant, H.A. Kaplan, H. Mover, and W.J. Lennarz 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. U. S. A. 83 1986 6751 6755
10. D.R. Armant, J. Wang, and Z. Liu Intracellular signaling in the developing blastocyst as a consequence of the maternal-embryonic dialogue Semin. Reprod. Med. 18 2000 273 287
11. B. Babiarz, L. Romagnano, S. Afonso, and G. Kurila Localization and expression of fibronectin during mouse decidualization in vitro: mechanisms of cell:matrix interactions Dev. Dyn. 206 1996 330 342
12. F. Beck, T. Erler, A. Russell, and R. James Expression of Cdx-2 in the mouse embryo and placenta: possible role in patterning of the extra-embryonic membranes Dev. Dyn. 204 1995 219 227
13. S.L. Bellis Variant glycosylation: an underappreciated regulatory mechanism for beta1 integrins Biochim. Biophys. Acta 1663 2004 52 60
14. E.J. Blake, J. Schindler, and M.I. Sherman Protein synthetic requirements for the outgrowth of trophoblast cells from mouse blastocysts J. Exp. Zool. 224 1982 401 408
15. T.N. Blankenship, and R.L. Given Penetration of the uterine epithelial basement membrane during blastocyst implantation in the mouse Anat. Rec. 233 1992 196 204
16. K. Burridge, and M. Chrzanowska-Wodnicka Focal adhesions, contractility, and signaling Annu. Rev. Cell Dev. Biol. 12 1996 463 518
17. T.D. Burrows, A. King, and Y.W. Loke Expression of integrins by human trophoblast and differential adhesion to laminin or fibronectin Hum. Reprod. 8 1993 475 484
18. P.R. Cammarata, L. Oakford, D. Cantu-Crouch, and R. Wordinger Attachment of blastocysts to lens capsule: a model system for trophoblast-epithelial cell interaction on a natural basement membrane Cell Tissue Res. 250 1987 633 640
19. S. Campbell, M. Otis, M. Cote, N. Gallo-Payet, and M.D. Payet Connection between integrins and cell activation in rat adrenal glomerulosa cells: a role for Arg-Gly-Asp peptide in the activation of the p42/p44(mapk) pathway and intracellular calcium Endocrinology 144 2003 1486 1495
20. D.D. Carson The glycobiology of implantation Front Biosci. 7 2002 d1535 d1544
21. D.D. Carson, J.P. Tang, and S. Gay Collagens support embryo attachment and outgrowth in vitro: effects of the Arg-Gly-Asp sequence Dev. Biol. 127 1988 368 375
22. D.D. Carson, I. Bagchi, S.K. Dey, A.C. Enders, A.T. Fazleabas, B.A. Lessey, and K. Yoshinaga Embryo implantation Dev. Biol. 223 2000 217 237
23. M. Cavagna, and J.C. Mantese Biomarkers of endometrial receptivity-A review Placenta 24 2003 S39 S47 (Suppl B)
24. N. Chai, Y. Patel, K. Jacobson, J. McMahon, A. McMahon, and D.A. Rappolee FGF is an essential regulator of the fifth cell division in preimplantation mouse embryos Dev. Biol. 198 1998 105 115
25. L.H. Chamberlain, D. Roth, A. Morgan, and R.D. Burgoyne Distinct effects of alpha-SNAP, 14-3-3 proteins, and calmodulin on priming and triggering of regulated exocytosis J. Cell Biol. 130 1995 1063 1070
26. N. Chatterjee, and A. Chatterjee Role of alphavbeta3 integrin receptor in the invasive potential of human cervical cancer (SiHa) cells J. Environ. Pathol., Toxicol. Oncol. 20 2001 211 221
27. K. Chawengsaksophak, R. James, V.E. Hammond, F. Kontgen, and F. Beck Homeosis and intestinal tumours in Cdx2 mutant mice Nature 386 1997 84 87
28. K. Chawengsaksophak, W. de Graaff, J. Rossant, J. Deschamps, and F. Beck Cdx2 is essential for axial elongation in mouse development Proc. Natl. Acad. Sci. U. S. A. 101 2004 7641 7645
29. Y.Q. Chen, M. Trikha, X. Gao, R. Bazaz, A.T. Porter, J. Timar, and K.V. Honn Ectopic expression of platelet integrin alphaIIb beta3 in tumor cells from various species and histological origin Int. J. Cancer 72 1997 642 648
30. Y.A. Chen, V. Duvvuri, H. Schulman, and R.H. Scheller Calmodulin and protein kinase C increase Ca(2+)-stimulated secretion by modulating membrane-attached exocytic machinery J. Biol. Chem. 274 1999 26469 26476
31. K. Chobotova, I. Spyropoulou, J. Carver, S. Manek, J.K. Heath, W.J. Gullick, D.H. Barlow, I.L. Sargent, and H.J. Mardon Heparin-binding epidermal growth factor and its receptor ErbB4 mediate implantation of the human blastocyst Mech. Dev. 119 2002 137 144
32. J.E. Collins, and T.P. Fleming Epithelial differentiation in the mouse preimplantation embryo: making adhesive cell contacts for the first time Trends Biochem. Sci. 20 1995 307 312
33. J.J. Contos, I. Ishii, and J. Chun Lysophosphatidic acid receptors Mol. Pharmacol. 58 2000 1188 1196
34. J.C. Cross Genetic insights into trophoblast differentiation and placental morphogenesis Semin. Cell Dev. Biol. 11 2000 105 113
35. J.C. Cross, Z. Werb, and S.J. Fisher Implantation and the placenta: key pieces of the development puzzle Science 266 1994 1508 1518
36. C.H. Damsky, C. Librach, K.H. Lim, M.L. Fitzgerald, M.T. McMaster, M. Janatpour, Y. Zhou, S.K. Logan, and S.J. Fisher Integrin switching regulates normal trophoblast invasion Development 120 1994 3657 3666
37. S.K. Das, X.N. Wang, B.C. Paria, D. Damm, J.A. Abraham, M. Klagsbrun, G.K. Andrews, and S.K. Dey Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation Development 120 1994 1071 1083
38. H.W. Denker Implantation: a cell biological paradox J. Exp. Zool. 266 1993 541 558
39. S.M. Dethlefsen, G. Raab, M.A. Moses, R.M. Adam, M. Klagsbrun, and M.R. Freeman Extracellular calcium influx stimulates metalloproteinase cleavage and secretion of heparin-binding EGF-like growth factor independently of protein kinase C J. Cell Biochem. 69 1998 143 153
40. S.K. Dey, H. Lim, S.K. Das, J. Reese, B.C. Paria, T. Daikoku, and H. Wang Molecular cues to implantation Endocr. Rev. 25 2004 341 373
41. A.D. Dickson Trophoblastic giant cell transformation of mouse blastocysts J. Reprod. Fertil. 6 1963 465 466
42. J. Dong, and H.S. Wiley Trafficking and proteolytic release of epidermal growth factor receptor ligands are modulated by their membrane-anchoring domains J. Biol. Chem. 275 2000 557 564
43. K.M. Downs Early placental ontogeny in the mouse Placenta 23 2002 116 131
44. U. Earl, C. Estlin, and J.N. Bulmer Fibronectin and laminin in the early human placenta Placenta 11 1990 223 231
45. J.J. Eckert, A. McCallum, A. Mears, M.G. Rumsby, I.T. Cameron, and T.P. Fleming Specific PKC isoforms regulate blastocoel formation during mouse preimplantation development Dev. Biol. 274 2004 384 401
46. A.C. Enders, D.J. Chavez, and S. Schlafke Comparison of implantation in utero and in vitro S.R. Glasser D.W. Bullock Cellular and molecular aspects of implantation 1981 Plenum Press New York, NY 365 382
47. J.P. Evans, R.M. Schultz, and G.S. Kopf Identification and localization of integrin subunits in oocytes and eggs of the mouse Mol. Reprod. Dev. 40 1995 211 220
48. T.N. Faria, S. Deb, S.C. Kwok, F. Talamantes, and M.J. Soares Ontogeny of placental lactogen-I and placental lactogen-II expression in the developing rat placenta Dev. Biol. 141 1990 279 291
49. J.D. Farrar, and D.D. Carson Differential temporal and spatial expression of mRNA encoding extracellular matrix components in decidua during the peri-implantation period Biol. Reprod. 46 1992 1095 1108
50. R.F. Feinberg, H.J. Kliman, and C.J. Lockwood Is oncofetal fibronectin a trophoblast glue for human implantation? Am. J. Pathol. 138 1991 537 543
51. F.M. Fusi, M. Vignali, J. Gailit, and R.A. Bronson Mammalian oocytes exhibit specific recognition of the RGD (Arg-Gly-Asp) tripeptide and express oolemmal integrins Mol. Reprod. Dev. 36 1993 212 219
52. R.L. Gardner Flow of cells from polar to mural trophectoderm is polarized in the mouse blastocyst Hum. Reprod. 15 2000 694 701
53. R.L. Gardner, V.E. Papaioannou, and S.C. Barton Origin of the ectoplacental cone and secondary giant cells in mouse blastocysts reconstituted from isolated trophoblast and inner cell mass J. Embryol. Exp. Morphol. 30 1973 561 572
54. B. Gerami-Naini, O.V. Dovzhenko, M. Durning, F.H. Wegner, J.A. Thomson, and T.G. Golos Trophoblast differentiation in embryoid bodies derived from human embryonic stem cells Endocrinology 145 2004 1517 1524
55. F.G. Giancotti, and E. Ruoslahti Integrin signaling Science 285 1999 1028 1032
56. M.H. Ginsberg, D. Xiaoping, T.E. O'Toole, J.C. Loftus, and E.F. Plow Platelet integrins Thromb. Haemostasis 70 1993 87 93
57. R.H. Glass, A.I. Spindle, and R.A. Pedersen Differential inhibition of trophoblast outgrowth and inner cell mass growth by actinomycin D in cultured mouse embryos J. Reprod. Fertil. 48 1976 443 445
58. S.R. Glasser, S. Lampelo, M.I. Munir, and J. Julian Expression of desmin, laminin and fibronectin during in situ differentiation (decidualization) of rat uterine stromal cells Differentiation 35 1987 132 142
59. S.R. Goldring, A.H. Gorn, M. Yamin, S.M. Krane, and J.T. Wang Characterization of the structural and functional properties of cloned calcitonin receptor cDNAs Horm. Metab. Res. 25 1993 477 480
60. X. Guo, D.A. Przywara, T.D. Wakade, and A.R. Wakade Exocytosis coupled to mobilization of intracellular calcium by muscarine and caffeine in rat chromaffin cells J. Neurochem. 67 1996 155 162
61. R.B. Gwatkin Defined media and development of mammalian eggs in vitro Ann. N.Y. Acad. Sci. 139 1966 79 90
62. R.B. Gwatkin, and P.E. Meckley Chromosomes of the mouse blastocyst following its attachment and outgrowth in vitro Ann. Med. Exp. Biol. Fenn. 44 1966 125 127
63. T. Hamatani, M.G. Carter, A.A. Sharov, and M.S. Ko Dynamics of global gene expression changes during mouse preimplantation development Dev. Cell 6 2004 117 131
64. T. Hamatani, T. Daikoku, H. Wang, H. Matsumoto, M.G. Carter, M.S. Ko, and S.K. Dey Global gene expression analysis identifies molecular pathways distinguishing blastocyst dormancy and activation Proc. Natl. Acad. Sci. U. S. A. 101 2004 10326 10331
65. S.N. Hancock, S.I. Agulnik, L.M. Silver, and V.E. Papaioannou Mapping and expression analysis of the mouse ortholog of Xenopus Eomesodermin Mech. Dev. 81 1999 205 208
66. B.P. Hierck, S. Thorsteinsdottir, C.M. Niessen, E. Freund, L.V. Iperen, A. Feyen, F. Hogervorst, R.E. Poelmann, C.L. Mummery, and A. Sonnenberg Variants of the alpha-6 beta-1 laminin receptor in early murine development: distribution, molecular cloning and chromosomal localization of the mouse integrin alpha-6 subunit Cell Adhes. Commun. 1 1993 33 53
67. S.J. Hill, C.R. Ganellin, H. Timmerman, J.C. Schwartz, N.P. Shankley, J.M. Young, W. Schunack, R. Levi, and H.L. Haas International union of pharmacology: XIII. Classification of histamine receptors Pharmacol. Rev. 49 1997 253 278
68. S. Huang, D. Stupack, A. Liu, D. Cheresh, and G.R. Nemerow Cell growth and matrix invasion of EBV-immortalized human B lymphocytes is regulated by expression of alpha(v) integrins Oncogene 19 2000 1915 1923
69. R.O. Hynes Integrins: versatility, modulation, and signaling in cell adhesion Cell 69 1992 11 25
70. R.O. Hynes Targeted mutations in cell adhesion genes: what have we learned from them? Dev. Biol. 180 1996 402 412
71. R.O. Hynes Integrins: bidirectional, allosteric signaling machines Cell 110 2002 673 687
72. J.A. Irving, J.J. Lysiak, C.H. Graham, S. Hearn, V.K. Han, and P.K. Lala Characteristics of trophoblast cells migrating from first trimester chorionic villus explants and propagated in culture Placenta 16 1995 413 433
73. R. Iwamoto, and E. Mekada Heparin-binding EGF-like growth factor: a juxtacrine growth factor Cytokine Growth Factor Rev. 11 2000 335 344
74. P.K. Jackson, A.G. Eldridge, E. Freed, L. Furstenthal, J.Y. Hsu, B.K. Kaiser, and J.D. Reimann The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases Trends Cell Biol. 10 2000 429 439
75. E.J. Jenkinson, and I.B. Wilson In vitro studies on the control of trophoblast outgrowth in the mouse J. Embryol. Exp. Morphol. 30 1973 21 30
76. M.A. Khidir, J.J. Stachecki, S.A. Krawetz, and D.R. Armant Rapid inhibition of mRNA synthesis during preimplantation embryo development: vital permeabilization by lysolecithin potentiates the action of α-amanitin Exp. Cell 219 1995 619 623
77. G.M. Kidder, and J.R. McLachlin Timing of transcription and protein synthesis underlying morphogenesis in preimplantation mouse embryos Dev. Biol. 112 1985 265 275
78. S.J. Kimber Molecular interactions at the maternal-embryonic interface during the early phase of implantation Semin. Reprod. Med. 18 2000 237 253
79. S.J. Kimber, and C. Spanswick Blastocyst implantation: the adhesion cascade Semin. Cell Dev. Biol. 11 2000 77 92
80. C.E. Kiraly-Borri, A. Morgan, R.D. Burgoyne, U. Weller, C.B. Wollheim, and J. Lang Soluble N-ethylmaleimide-sensitive-factor attachment protein and N-ethylmaleimide-insensitive factors are required for Ca2+-stimulated exocytosis of insulin Biochem. J. 314 1996 199 203
81. D.R. Kirby, D.M. Potts, and I.B. Wilson On the orientation of the implanting blastocyst J. Embryol. Exp. Morphol. 17 1967 527 532
82. L.L. Kisalus, J.C. Herr, and C.D. Little Immunolocalization of extracellular matrix proteins and collagen synthesis in first-trimester human decidua Anat. Rec. 218 1987 402 415
83. E. Klaffky, R. Williams, C.C. Yao, B. Ziober, R. Kramer, and A. Sutherland Trophoblast-specific expression and function of the integrin alpha 7 subunit in the peri-implantation mouse embryo Dev. Biol. 239 2001 161 175
84. R.D. Klausner, J.G. Donaldson, and J. Lippincott-Schwartz Brefeldin A: insights into the control of membrane traffic and organelle structure J. Cell Biol. 116 1992 1071 1080
85. L.J. Kornberg, H.S. Earp, C.E. Turner, C. Prockop, and R.L. Juliano Signal transduction by integrins: increased protein tyrosine phosphorylation caused by clustering of beta 1 integrins Proc. Natl. Acad. Sci. U. S. A. 88 1991 8392 8396
86. S. Kumar, L.J. Zhu, M. Polihronis, S.T. Cameron, D.T. Baird, F. Schatz, A. Dua, Y.K. Ying, M.K. Bagchi, and I.C. Bagchi Progesterone induces calcitonin gene expression in human endometrium within the putative window of implantation J. Clin. Endocrinol. Metab. 83 1998 4443 4450
87. T. Kunath, D. Strumpf, and J. Rossant Early trophoblast determination and stem cell maintenance in the mouse-A review Placenta 25 2004 S32 S38 (Suppl A)
88. J.Y. Lan, V.A. Skeberdis, T. Jover, S.Y. Grooms, Y. Lin, R.C. Araneda, X. Zheng, M.V. Bennett, and R.S. Zukin Protein kinase C modulates NMDA receptor trafficking and gating Nat. Neurosci. 4 2001 382 390
89. R.E. Leach, R. Khalifa, N.D. Ramirez, S.K. Das, J. Wang, S.K. Dey, R. Romero, and D.R. Armant Multiple roles for heparin-binding epidermal growth factor-like growth factor are suggested by its cell specific expression during the human endometrial cycle and early placentation J. Clin. Endocrinol. Metab. 84 1999 3355 3363
90. R.E. Leach, U.K. Rout, J.F. Schultz, D.E. Saunders, and D.R. Armant Ethanol elevates c-Myc levels in cultured mouse preimplantation embryos Alcohol. Clin. Exp. Res. 23 1999 778 784
91. R.E. Leach, R. Romero, Y.M. Kim, T. Chaiworapongsa, B.A. Kilburn, S.K. Das, S.K. Dey, A. Johnson, F. Qureshi, S. Jacques, and D.R. Armant Pre-eclampsia and expression of heparin-binding EGF-like growth factor Lancet 360 2002 1215 1219
92. R.E. Leach, B.A. Kilburn, J. Wang, Z. Liu, R. Romero, and D.R. Armant Heparin-binding EGF-like growth factor regulates human extravillous cytotrophoblast development during conversion to the invasive phenotype Dev. Biol. 266 2004 223 237
93. D.I. Leavesley, G.D. Ferguson, E.A. Wayner, and D.A. Cheresh Requirement of the integrin beta 3 subunit for carcinoma cell spreading or migration on vitronectin and fibrinogen J. Cell Biol. 117 1992 1101 1107
94. I. Leivo, A. Vaheri, R. Timpl, and J. Wartiovaara Appearance and distribution of collagens and laminin in the early mouse embryo Dev. Biol. 76 1980 100 114
95. Z. Liu, and D.R. Armant Lysophosphatidic acid regulates murine blastocyst development by transactivation of receptors for heparin-binding EGF-like growth factor Exp. Cell Res. 296 2004 317 326
96. J. Liu, C. Chakraborty, C.H. Graham, Y.P. Barbin, S.J. Dixon, and P.K. Lala Noncatalytic domain of uPA stimulates human extravillous trophoblast migration by using phospholipase C, phosphatidylinositol 3-kinase and mitogen-activated protein kinase Exp. Cell Res. 286 2003 138 151
97. D. Lohnes The Cdx1 homeodomain protein: an integrator of posterior signaling in the mouse BioEssays 25 2003 971 980
98. A. Long, D. Kelleher, S. Lynch, and Y. Volkov Cutting edge: protein kinase C beta expression is critical for export of Il-2 from T cells J. Immunol. 167 2001 636 640
99. K.P. Lu, and A.R. Means Regulation of the cell cycle by calcium and calmodulin Endocr. Rev. 14 1993 40 58
100. K.W. Marek, I.K. Vijay, and J.D. Marth A recessive deletion in the GlcNAc-1-phosphotransferase gene results in peri-implantation embryonic lethality Glycobiology 9 1999 1263 1271
101. U.M. Marinari, M. Nitti, M.A. Pronzato, and C. Domenicotti Role of PKC-dependent pathways in HNE-induced cell protein transport and secretion Mol. Aspects Med. 24 2003 205 211
102. J.F. Marshall, and I.R. Hart The role of alpha v-integrins in tumour progression and metastasis Semin. Cancer Biol. 7 1996 129 138
103. K.L. Martin, D.H. Barlow, and I.L. Sargent Heparin-binding epidermal growth factor significantly improves human blastocyst development and hatching in serum-free medium Hum. Reprod. 13 1998 1645 1652
104. H.P. McNamee, D.E. Ingber, and M.A. Schwartz Adhesion to fibronectin stimulates inositol lipid synthesis and enhances PDGF-induced inositol lipid breakdown J. Cell Biol. 121 1993 673 678
105. J.H. Miner, C. Li, J.L. Mudd, G. Go, and A.E. Sutherland Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation Development 131 2004 2247 2256
106. S. Miyamoto, H. Teramoto, O.A. Coso, J.S. Gutkind, P.D. Burbelo, S.K. Akiyama, and K.M. Yamada Integrin function: molecular hierarchies of cytoskeletal and signaling molecules J. Cell Biol. 131 1995 791 805
107. H. Nechushtan, M. Leitges, C. Cohen, G. Kay, and E. Razin Inhibition of degranulation and interleukin-6 production in mast cells derived from mice deficient in protein kinase Cbeta Blood 95 2000 1752 1757
108. J. Ng-Sikorski, R. Andersson, M. Patarroyo, and T. Andersson Calcium signaling capacity of the CD11b/CD18 integrin on human neutrophils Exp. Cell Res. 195 1991 504 508
109. R. Pardi, J.R. Bender, C. Dettori, E. Giannazza, and E.G. Engleman Heterogeneous distribution and transmembrane signaling properties of lymphocyte function-associated antigen (LFA-1) in human lymphocyte subsets J. Immunol. 143 1989 3157 3166
110. B.C. Paria, S.K. Dey, and G.K. Andrews Antisense c-myc effects on preimplantation mouse embryo development Proc. Natl. Acad. Sci. U. S. A. 89 1992 10051 10055
111. B.C. Paria, Y.M. Huet-Hudson, and S.K. Dey Blastocyst's state of activity determines the "window" of implantation in the receptive mouse uterus Proc. Natl. Acad. Sci. U. S. A. 90 1993 10159 10162
112. B.C. Paria, N. Das, S.K. Das, X. Zhao, K.N. Dileepan, and S.K. Dey Histidine decarboxylase gene in the mouse uterus is regulated by progesterone and correlates with uterine differentiation for blastocyst implantation Endocrinology 139 1998 3958 3966
113. B.C. Paria, K. Elenius, M. Klagsburn, and S.K. Dey Heparin-binding EGF-like growth factor interacts with mouse blastocysts independently of ErbB1: a possible role for herparan sulfate proteoglycans and ErbB4 in blastocyst implantation Development 126 1999 1997 2005
114. B.C. Paria, W. Ma, J. Tan, S. Raja, S.K. Das, S.K. Dey, and B.L. Hogan Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors Proc. Natl. Acad. Sci. U. S. A. 98 2001 1047 1052
115. E.L. Parr, H.N. Tung, and M.B. Parr Apoptosis as the mode of uterine epithelial cell death during embryo implantation in mice and rats Biol. Reprod. 36 1987 211 225
116. C.M. Pauken, and D.G. Capco The expression and stage-specific localization of protein kinase C isotypes during mouse preimplantation development Dev. Biol. 223 2000 411 421
117. C. Peters, and A. Mayer Ca2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion Nature 396 1998 575 580
118. D.R. Phillips, I.F. Charo, L.V. Parise, and L.A. Fitzgerald The platelet membrane glycoprotein IIb-IIIa complex Blood 71 1988 831 843
119. R. Pijnenborg, W.B. Robertson, I. Brosens, and G. Dixon Review article: trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals Placenta 2 1981 71 91
120. E.F. Plow, T.A. Haas, L. Zhang, J. Loftus, and J.W. Smith Ligand binding to integrins J. Biol. Chem. 275 2000 21785 21788
121. P. Pomies, P. Frachet, and M.R. Block Control of the alpha 5 beta 1 integrin/fibronectin interaction in vitro by the serine/threonine protein phosphatase calcineurin Biochemistry 34 1995 5104 5112
122. A. Psychoyos Endocrine control of egg implantation R.O. Greep E.G. Astood S.R. Geiger Handbook of physiology 1973 American Physiology Society Washington, DC 187 215
123. S. Quetglas, C. Leveque, R. Miquelis, K. Sato, and M. Seagar Ca2+-dependent regulation of synaptic SNARE complex assembly via a calmodulin-and phospholipid-binding domain of synaptobrevin Proc. Natl. Acad. Sci. U. S. A. 97 2000 9695 9700
124. G. Raab, K. Kover, B.C. Paria, S.K. Dey, R.M. Ezzell, and M. Klagsbrun Mouse preimplantation blastocysts adhere to cells expressing the transmembrane form of heparin-binding EGF-like growth factor Development 122 1996 637 645
125. K. Red-Horse, Y. Zhou, O. Genbacev, A. Prakobphol, R. Foulk, M. McMaster, and S.J. Fisher Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface J. Clin. Invest. 114 2004 744 754
126. R.W. Redline, and C.Y. Lu Localization of fetal major histocompatibility complex antigens and maternal leukocytes in murine placenta, Implications for maternal-fetal immunological relationship Lab. Invest. 61 1989 27 36
127. J. Richa, C.H. Damsky, C.A. Buck, B.B. Knowles, and D. Solter Cell surface glycoproteins mediate compaction, trophoblast attachment, and endoderm formation during early mouse development Dev. Biol. 108 1985 513 521
128. V. Rider, D.L. Carlone, D. Witrock, C. Cai, and N. Oliver Uterine fibronectin mRNA content and localization are modulated during implantation Dev. Dyn. 195 1992 1 14
129. J. Rossant, and J.C. Cross Placental development: lessons from mouse mutants Nat. Rev., Genet. 2 2001 538 548
130. U.K. Rout, S.A. Krawetz, and D.R. Armant Ethanol-induced intracellular calcium mobilization rapidly alters gene expression in the mouse blastocyst Cell Calcium 22 1997 463 474
131. U.K. Rout, J. Wang, B.C. Paria, and D.R. Armant alpha5beta1, alphaVbeta3 and the platelet-associated integrin alphaIIbbeta3 coordinately regulate adhesion and migration of differentiating mouse trophoblast cells Dev. Biol. 268 2004 135 151
132. E. Ruoslahti RGD and other recognition sequences for integrins Annu. Rev. Cell Dev. Biol. 12 1996 697 715
133. A.P. Russ, S. Wattler, W.H. Colledge, S.A. Aparicio, M.B. Carlton, J.J. Pearce, S.C. Barton, M.A. Surani, K. Ryan, M.C. Nehls, V. Wilson, and M.J. Evans Eomesodermin is required for mouse trophoblast development and mesoderm formation Nature 404 2000 95 99
134. S.K. Sastry, and K. Burridge Focal adhesions: a nexus for intracellular signaling and cytoskeletal dynamics Exp. Cell Res. 261 2000 25 36
135. B. Savage, E. Saldivar, and Z.M. Ruggeri Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor Cell 84 1996 289 297
136. J. Schindler, and M.I. Sherman Effect of α-amanatin on programming of mouse blastocyst development Dev. Biol. 84 1981 332 340
137. S. Schlafke, and A.C. Enders Cellular basis of interaction between trophoblast and uterus at implantation Biol. Reprod. 12 1975 41 65
138. S. Schlafke, A.O. Welsh, and A.C. Enders Penetration of the basal lamina of the uterine luminal epithelium during implantation in the rat Anat. Rec. 212 1985 47 56
139. P.C. Schmid, B.C. Paria, R.J. Krebsbach, H.H. Schmid, and S.K. Dey Changes in anandamide levels in mouse uterus are associated with uterine receptivity for embryo implantation Proc. Natl. Acad. Sci. U. S. A. 94 1997 4188 4192
140. J.F. Schultz, and D.R. Armant Beta1-and beta3-class integrins mediate fibronectin binding activity at the surface of developing mouse peri-implantation blastocysts. Regulation by ligand-induced mobilization of stored receptor J. Biol. Chem. 270 1995 11522 11531
141. J.F. Schultz, L. Mayernik, U.K. Rout, and D.R. Armant Integrin trafficking regulates adhesion to fibronectin during differentiation of mouse peri-implantation blastocysts Dev. Genet. 21 1997 31 43
142. M.A. Schwartz Spreading of human endothelial cells on fibronectin or vitronectin triggers elevation of intracellular free calcium J. Cell Biol. 120 1993 1003 1010
143. M.I. Sherman, and S.B. Atienza-Samols In vitro studies on the surface adhesiveness of mouse blastocysts H. Ludwig P.F. Tauber Human fertilization 1978 Georg Thieme Publishers Stuttgart, Germany 179 183
144. 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 beta1 integrin in embryo implantation using mouse blastocysts and human decidua Biol. Reprod. 60 1999 1468 1474
145. C. Showell, O. Binder, and F.L. Conlon T-box genes in early embryogenesis Dev. Dyn. 229 2004 201 218
146. M.D. Sjaastad, R.S. Lewis, and W.J. Nelson Mechanisms of integrin-mediated calcium signaling in MDCK cells: regulation of adhesion by IP3- and store-independent calcium influx Mol. Biol. Cell 7 1996 1025 1041
147. M. Slater, and C.R. Murphy Temporal changes in the expression of platelet-derived growth factor and fibronectin in the uterine epithelium during early pregnancy Anat. Rec. 255 1999 1 6
148. J.B. Smith, C. Dangelmaier, M.A. Selak, and J.L. Daniel Facile platelet adhesion to collagen requires metabolic energy and actin polymerization and evokes intracellular free calcium mobilization J. Cell. Biochem. 47 1991 54 61
149. 2+ in pancreatic acinar cells via activation of phospholipase C Biochem. J. 299 1994 603 611
150. A.I. Spindle, and R.A. Pedersen Hatching, attachment, and outgrowth of mouse blastocysts in vitro: fixed nitrogen requirements J. Exp. Zool. 186 1973 305 318
151. J.J. Stachecki, F.D. Yelian, R.E. Leach, and D.R. Armant Mouse blastocyst outgrowth and implantation rates following exposure to ethanol or A23187 during culture in vitro J. Reprod. Fertil. 101 1994 611 617
152. 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. 9 1995 1883 1895
153. M.A. Surani Glycoprotein synthesis and inhibition of glycosylation by tunicamycin in preimplantation mouse embryos: compaction and trophoblast adhesion Cell 18 1979 217 227
154. A. Sutherland Mechanisms of implantation in the mouse: differentiation and functional importance of trophoblast giant cell behavior Dev. Biol. 258 2003 241 251
155. A.E. Sutherland, P.G. Calarco, and C.H. Damsky Developmental regulation of integrin expression at the time of implantation in the mouse embryo Development 119 1993 1175 1186
156. P. Sutovsky, J. Motlik, E. Neuber, A. Pavlok, G. Schatten, J. Palecek, P. Hyttel, O.T. Adebayo, K. Adwan, R. Alberio, H. Bagis, Z. Bataineh, B. Bjerregaard, S. Bodo, V. Bryja, M. Carrington, M. Couf, F.R. de la, J. Diblik, M. Esner, J. Forejt, J. Fulka Jr., G. Geussova, J.O. Gjorret, M. Libik, A. Hampl, M.S. Hassane, M. Houshmand, P. Hozak, M. Jezova, G. Kania, J. Kanka, O.M. Kandil, T. Kishimoto, J. Klima, J. Kohoutek, T. Kopska, M. Kubelka, G. Lapathitis, J. Laurincik, B. Lefevre, J. Mihalik, M. Novakova, R. Oko, R. Omelka, D. Owiny, J. Pachernik, J. Pacholikova, J. Peknicova, A. Pesty, Z. Ponya, H. Preclikova, A. Sloskova, P. Svoboda, F. Strejcek, S. Toth, O. Tepla, M. Valdivia, P. Vodicka, and D. Zudova Accumulation of the proteolytic marker peptide ubiquitin in the trophoblast of mammalian blastocysts Cloning Stem Cells 3 2001 157 161
157. P. Svoboda, P. Stein, and R.M. Schultz RNAi in mouse oocytes and preimplantation embryos: effectiveness of hairpin dsRNA Biochem. Biophys. Res. Commun. 287 2001 1099 1104
158. A. Tabuchi, A. Yoshioka, T. Higashi, R. Shirakawa, H. Nishioka, T. Kita, and H. Horiuchi Direct demonstration of involvement of protein kinase Calpha in the Ca2+-induced platelet aggregation J. Biol. Chem. 278 2003 26374 26379
159. S. Tanaka, T. Kunath, A.K. Hadjantonakis, A. Nagy, and J. Rossant Promotion of trophoblast stem cell proliferation by FGF4 Science 282 1998 2072 2075
160. G. Tarone, M.A. Russo, E. Hirsch, T. Odorisio, F. Altruda, L. Silengo, and G. Siracusa Expression of beta 1 integrin complexes on the surface of unfertilized mouse oocyte Development 117 1993 1369 1375
161. M. Trikha, J. Timar, A. Zacharek, J.A. Nemeth, Y. Cai, B. Dome, B. Somlai, E. Raso, A. Ladanyi, and K.V. Honn Role for beta3 integrins in human melanoma growth and survival Int. J. Cancer 101 2002 156 167
162. T. Umata, M. Hirata, T. Takahashi, F. Ryu, S. Shida, Y. Takahashi, M. Tsuneoka, Y. Miura, M. Masuda, Y. Horiguchi, and E. Mekada A dual signaling cascade that regulates the ectodomain shedding of heparin-binding epidermal growth factor-like growth factor J. Biol. Chem. 276 2001 30475 30482
163. J. Wang, and D.R. Armant Integrin-mediated adhesion and signaling during blastocyst implantation Cells Tissues Organs 172 2002 190 201
164. J. Wang, U.K. Rout, I.C. Bagchi, and D.R. Armant Expression of calcitonin receptors in mouse preimplantation embryos and their function in the regulation of blastocyst differentiation by calcitonin Development 125 1998 4293 4302
165. J. Wang, B.C. Paria, S.K. Dey, and D.R. Armant Stage-specific excitation of cannabinoid receptor exhibits differential effects on mouse embryonic development Biol. Reprod. 60 1999 839 844
166. J. Wang, L. Mayernik, J.F. Schultz, and D.R. 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 127 2000 33 44
167. J. Wang, L. Mayernik, and D.R. Armant Integrin signaling regulates blastocyst adhesion to fibronectin at implantation: intracellular calcium transients and vesicle trafficking in primary trophoblast cells Dev. Biol. 245 2002 270 279
168. H. Wang, H. Matsumoto, Y. Guo, B.C. Paria, R.L. Roberts, and S.K. Dey Differential G protein-coupled cannabinoid receptor signaling by anandamide directs blastocyst activation for implantation Proc. Natl. Acad. Sci. U. S. A. 100 2003 14914 14919
169. Q.T. Wang, K. Piotrowska, M.A. Ciemerych, L. Milenkovic, M.P. Scott, R.W.
170. J. Wartiovaara, I. Leivo, and A. Vaheri Expression of the cell surface-associated glycoprotein, fibronectin, in the early mouse embryo Dev. Biol. 69 1979 247 257
171. A.J. Watson, and L.C. Barcroft Regulation of blastocyst formation Front. Biosci. 6 2001 D708 D730
172. A.O. Welsh, and A.C. Enders Chorioallantoic placenta formation in the rat: I. Luminal epithelial cell death and extracellular matrix modifications in the mesometrial region of implantation chambers Am. J. Anat. 192 1991 215 231
173. U.M. Wewer, A. Damjanov, J. Weiss, L.A. Liotta, and I. Damjanov Mouse endometrial stromal cells produce basement-membrane components Differentiation 32 1986 49 58
174. R.J. Wordinger, and M. McGrath The collagen substratum influences in vitro hatching and attachment of the mouse blastocyst in a serumless medium Experientia 35 1979 1683 1684
175. R.J. Wordinger, A.M. Brun-Zinkernagel, and T. Jackson An ultrastructural study of in-vitro interaction of guinea-pig and mouse blastocysts with extracellular matrices J. Reprod. Fertil. 93 1991 585 597
176. T.C. Wu, Y.J. Wan, A.E. Chung, and I. Damjanov Immunohistochemical localization of entactin and laminin in mouse embryos and fetuses Dev. Biol. 100 1983 496 505
177. X. Wu, J.E. Mogford, S.H. Platts, G.E. Davis, G.A. Meininger, and M.J. Davis Modulation of calcium current in arteriolar smooth muscle by alphav beta3 and alpha5 beta1 integrin ligands J. Cell Biol. 143 1998 241 252
178. R.H. Xu, X. Chen, D.S. Li, R. Li, G.C. Addicks, C. Glennon, T.P. Zwaka, and J.A. Thomson BMP4 initiates human embryonic stem cell differentiation to trophoblast Nat. Biotechnol. 20 2002 1261 1264
179. J.T. Yang, H. Rayburn, and R.O. Hynes Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development Development 121 1995 549 560
180. F.D. Yelian, N.A. Edgeworth, L.J. Dong, A.E. Chung, and D.R. Armant Recombinant entactin promotes mouse primary trophoblast cell adhesion and migration through the Arg-Gly-Asp (RGD) recognition sequence J. Cell Biol. 121 1993 923 929
181. F.D. Yelian, Y. Yang, J.D. Hirata, J.F. Schultz, and D.R. Armant Molecular interactions between fibronectin and integrins during mouse blastocyst outgrowth Mol. Reprod. Dev. 41 1995 435 448
182. H.J. Yoo, D.H. Barlow, and H.J. Mardon Temporal and spatial regulation of expression of heparin-binding epidermal growth factor-like growth factor in the human endometrium: a possible role in blastocyst implantation Dev. Genet. 21 1997 102 108
183. X. Zhang, M.A. Shu, M.B. Harvey, and G.A. Schultz Regulation of urokinase plasminogen activator production in implanting mouse embryo: effect of embryo interaction with extracellular matrix Biol. Reprod. 54 1996 1052 1058
184. C.A. Ziomek, M.H. Johnson, and A.H. Handyside The developmental potential of mouse 16-cell blastomeres J. Exp. Zool. 221 1982 345 355