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. 1988 Apr 1;106(4):1331–1348. doi: 10.1083/jcb.106.4.1331

Expression and function of cell surface extracellular matrix receptors in mouse blastocyst attachment and outgrowth

PMCID: PMC2115031  PMID: 2834405

Abstract

Mouse-hatched blastocysts cultured in vitro will attach and form outgrowths of trophoblast cells on appropriate substrates, providing a model for implantation. Immediately after hatching, the surfaces of blastocysts are quiescent and are not adhesive. Over the period 24-36 h post-hatching, blastocysts cultured in serum-free medium become adhesive and attach and spread on the extracellular matrix components fibronectin, laminin, and collagen type IV in a ligand specific manner. Attachment and trophoblast outgrowth on these substrates can be inhibited by addition to the culture medium of an antibody, anti-ECMr (anti-extracellular matrix receptor), that recognizes a group of 140-kD glycoproteins similar to those of the 140-kD extracellular matrix receptor complex (integrin) recognized in avian cells by CSAT and JG22 monoclonal antibodies. Addition to the culture medium of a synthetic peptide containing the Arg-Gly-Asp tripeptide cell recognition sequence of fibronectin inhibits trophoblast outgrowth on both laminin and fibronectin. However, the presence of the peptide does not affect attachment of the blastocysts to either ligand. Immunoprecipitation of 125I surface-labeled embryos using anti-ECMr reveals that antigens recognized by this antibody are exposed on the surfaces of embryos at a time when they are spreading on the substrate, but are not detectable immediately after hatching. Immunofluorescence experiments show that both the ECMr antigens and the cytoskeletal proteins vinculin and talin are enriched on the cell processes and ventral surfaces of trophectoderm cells in embryo outgrowths, in patterns similar to those seen in fibroblasts, and consistent with their role in adhesion of the trophoblast cells to the substratum.

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Selected References

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  1. Akiyama S. K., Yamada S. S., Yamada K. M. Characterization of a 140-kD avian cell surface antigen as a fibronectin-binding molecule. J Cell Biol. 1986 Feb;102(2):442–448. doi: 10.1083/jcb.102.2.442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Argraves W. S., Pytela R., Suzuki S., Millán J. L., Pierschbacher M. D., Ruoslahti E. cDNA sequences from the alpha subunit of the fibronectin receptor predict a transmembrane domain and a short cytoplasmic peptide. J Biol Chem. 1986 Oct 5;261(28):12922–12924. [PubMed] [Google Scholar]
  3. Armant D. R., Kaplan H. A., Lennarz W. J. Fibronectin and laminin promote in vitro attachment and outgrowth of mouse blastocysts. Dev Biol. 1986 Aug;116(2):519–523. doi: 10.1016/0012-1606(86)90152-1. [DOI] [PubMed] [Google Scholar]
  4. Armant D. R., Kaplan H. A., Mover H., Lennarz W. J. 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. 1986 Sep;83(18):6751–6755. doi: 10.1073/pnas.83.18.6751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Banerjee S. D., Cohn R. H., Bernfield M. R. Basal lamina of embryonic salivary epithelia. Production by the epithelium and role in maintaining lobular morphology. J Cell Biol. 1977 May;73(2):445–463. doi: 10.1083/jcb.73.2.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bard J. B., Hay E. D., Meller S. M. Formation of the endothelium of the avian cornea: a study of cell movement in vivo. Dev Biol. 1975 Feb;42(2):334–361. doi: 10.1016/0012-1606(75)90339-5. [DOI] [PubMed] [Google Scholar]
  7. Bayna E. M., Runyan R. B., Scully N. F., Reichner J., Lopez L. C., Shur B. D. Cell surface galactosyltransferase as a recognition molecule during development. Mol Cell Biochem. 1986 Nov-Dec;72(1-2):141–151. doi: 10.1007/BF00230641. [DOI] [PubMed] [Google Scholar]
  8. Bernfield M., Banerjee S. D. The turnover of basal lamina glycosaminoglycan correlates with epithelial morphogenesis. Dev Biol. 1982 Apr;90(2):291–305. doi: 10.1016/0012-1606(82)90378-5. [DOI] [PubMed] [Google Scholar]
  9. Bluemink J. G., Van Maurik P., Lawson K. A. Intimate cell contacts at the epithelial/mesenchymal interface in embryonic mouse lung. J Ultrastruct Res. 1976 May;55(2):257–270. doi: 10.1016/s0022-5320(76)80071-8. [DOI] [PubMed] [Google Scholar]
  10. Boucaut J. C., Darribère T., Poole T. J., Aoyama H., Yamada K. M., Thiery J. P. Biologically active synthetic peptides as probes of embryonic development: a competitive peptide inhibitor of fibronectin function inhibits gastrulation in amphibian embryos and neural crest cell migration in avian embryos. J Cell Biol. 1984 Nov;99(5):1822–1830. doi: 10.1083/jcb.99.5.1822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Bronner-Fraser M. Alterations in neural crest migration by a monoclonal antibody that affects cell adhesion. J Cell Biol. 1985 Aug;101(2):610–617. doi: 10.1083/jcb.101.2.610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Bronner-Fraser M. An antibody to a receptor for fibronectin and laminin perturbs cranial neural crest development in vivo. Dev Biol. 1986 Oct;117(2):528–536. doi: 10.1016/0012-1606(86)90320-9. [DOI] [PubMed] [Google Scholar]
  13. Brown P. J., Juliano R. L. Expression and function of a putative cell surface receptor for fibronectin in hamster and human cell lines. J Cell Biol. 1986 Oct;103(4):1595–1603. doi: 10.1083/jcb.103.4.1595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Brown P. J., Juliano R. L. Selective inhibition of fibronectin-mediated cell adhesion by monoclonal antibodies to a cell-surface glycoprotein. Science. 1985 Jun 21;228(4706):1448–1451. doi: 10.1126/science.4012302. [DOI] [PubMed] [Google Scholar]
  15. Buck C. A., Shea E., Duggan K., Horwitz A. F. Integrin (the CSAT antigen): functionality requires oligomeric integrity. J Cell Biol. 1986 Dec;103(6 Pt 1):2421–2428. doi: 10.1083/jcb.103.6.2421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Burridge K., Connell L. A new protein of adhesion plaques and ruffling membranes. J Cell Biol. 1983 Aug;97(2):359–367. doi: 10.1083/jcb.97.2.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Burridge K., Feramisco J. R. Microinjection and localization of a 130K protein in living fibroblasts: a relationship to actin and fibronectin. Cell. 1980 Mar;19(3):587–595. doi: 10.1016/s0092-8674(80)80035-3. [DOI] [PubMed] [Google Scholar]
  18. Chen W. T., Chen J. M., Mueller S. C. Coupled expression and colocalization of 140K cell adhesion molecules, fibronectin, and laminin during morphogenesis and cytodifferentiation of chick lung cells. J Cell Biol. 1986 Sep;103(3):1073–1090. doi: 10.1083/jcb.103.3.1073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Chen W. T., Hasegawa E., Hasegawa T., Weinstock C., Yamada K. M. Development of cell surface linkage complexes in cultured fibroblasts. J Cell Biol. 1985 Apr;100(4):1103–1114. doi: 10.1083/jcb.100.4.1103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Damsky C. H., Knudsen K. A., Bradley D., Buck C. A., Horwitz A. F. Distribution of the cell substratum attachment (CSAT) antigen on myogenic and fibroblastic cells in culture. J Cell Biol. 1985 May;100(5):1528–1539. doi: 10.1083/jcb.100.5.1528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Damsky C. H., Knudsen K. A., Buck C. A. Integral membrane glycoproteins related to cell-substratum adhesion in mammalian cells. J Cell Biochem. 1982;18(1):1–13. doi: 10.1002/jcb.1982.240180102. [DOI] [PubMed] [Google Scholar]
  22. Damsky C. H., Knudsen K. A., Dorio R. J., Buck C. A. Manipulation of cell-cell and cell-substratum interactions in mouse mammary tumor epithelial cells using broad spectrum antisera. J Cell Biol. 1981 May;89(2):173–184. doi: 10.1083/jcb.89.2.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Damsky C. H., Richa J., Solter D., Knudsen K., Buck C. A. Identification and purification of a cell surface glycoprotein mediating intercellular adhesion in embryonic and adult tissue. Cell. 1983 Sep;34(2):455–466. doi: 10.1016/0092-8674(83)90379-3. [DOI] [PubMed] [Google Scholar]
  24. Duband J. L., Rocher S., Chen W. T., Yamada K. M., Thiery J. P. Cell adhesion and migration in the early vertebrate embryo: location and possible role of the putative fibronectin receptor complex. J Cell Biol. 1986 Jan;102(1):160–178. doi: 10.1083/jcb.102.1.160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ducibella T., Anderson E. Cell shape and membrane changes in the eight-cell mouse embryo: prerequisites for morphogenesis of the blastocyst. Dev Biol. 1975 Nov;47(1):45–58. doi: 10.1016/0012-1606(75)90262-6. [DOI] [PubMed] [Google Scholar]
  26. Engvall E., Davis G. E., Dickerson K., Ruoslahti E., Varon S., Manthorpe M. Mapping of domains in human laminin using monoclonal antibodies: localization of the neurite-promoting site. J Cell Biol. 1986 Dec;103(6 Pt 1):2457–2465. doi: 10.1083/jcb.103.6.2457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Farach M. C., Tang J. P., Decker G. L., Carson D. D. Heparin/heparan sulfate is involved in attachment and spreading of mouse embryos in vitro. Dev Biol. 1987 Oct;123(2):401–410. doi: 10.1016/0012-1606(87)90398-8. [DOI] [PubMed] [Google Scholar]
  28. Fink R. D., McClay D. R. Three cell recognition changes accompany the ingression of sea urchin primary mesenchyme cells. Dev Biol. 1985 Jan;107(1):66–74. doi: 10.1016/0012-1606(85)90376-8. [DOI] [PubMed] [Google Scholar]
  29. Geiger B. A 130K protein from chicken gizzard: its localization at the termini of microfilament bundles in cultured chicken cells. Cell. 1979 Sep;18(1):193–205. doi: 10.1016/0092-8674(79)90368-4. [DOI] [PubMed] [Google Scholar]
  30. Geiger B., Tokuyasu K. T., Dutton A. H., Singer S. J. Vinculin, an intracellular protein localized at specialized sites where microfilament bundles terminate at cell membranes. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4127–4131. doi: 10.1073/pnas.77.7.4127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Giancotti F. G., Tarone G., Knudsen K., Damsky C., Comoglio P. M. Cleavage of a 135 kD cell surface glycoprotein correlates with loss of fibroblast adhesion to fibronectin. Exp Cell Res. 1985 Jan;156(1):182–190. doi: 10.1016/0014-4827(85)90272-1. [DOI] [PubMed] [Google Scholar]
  32. Glass R. H., Spindle A. I., Pedersen R. A. Mouse embryo attachment to substratum and interaction of trophoblast with cultured cells. J Exp Zool. 1979 Jun;208(3):327–336. doi: 10.1002/jez.1402080309. [DOI] [PubMed] [Google Scholar]
  33. Gonda M. A., Hsu Y. C. Correlative scanning electron, transmission electron, and light microscopic studies of the in vitro development of mouse embryos on a plastic substrate at the implantation stage. J Embryol Exp Morphol. 1980 Apr;56:23–39. [PubMed] [Google Scholar]
  34. Grabel L. B., Watts T. D. The role of extracellular matrix in the migration and differentiation of parietal endoderm from teratocarcinoma embryoid bodies. J Cell Biol. 1987 Jul;105(1):441–448. doi: 10.1083/jcb.105.1.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Graf J., Iwamoto Y., Sasaki M., Martin G. R., Kleinman H. K., Robey F. A., Yamada Y. Identification of an amino acid sequence in laminin mediating cell attachment, chemotaxis, and receptor binding. Cell. 1987 Mar 27;48(6):989–996. doi: 10.1016/0092-8674(87)90707-0. [DOI] [PubMed] [Google Scholar]
  36. Grant M. M., Cutts N. R., Brody J. S. Alterations in lung basement membrane during fetal growth and type 2 cell development. Dev Biol. 1983 May;97(1):173–183. doi: 10.1016/0012-1606(83)90074-x. [DOI] [PubMed] [Google Scholar]
  37. Greve J. M., Gottlieb D. I. Monoclonal antibodies which alter the morphology of cultured chick myogenic cells. J Cell Biochem. 1982;18(2):221–229. doi: 10.1002/jcb.1982.240180209. [DOI] [PubMed] [Google Scholar]
  38. Grinnell F., Head J. R., Hoffpauir J. Fibronectin and cell shape in vivo: studies on the endometrium during pregnancy. J Cell Biol. 1982 Sep;94(3):597–606. doi: 10.1083/jcb.94.3.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Grover A., Andrews G., Adamson E. D. Role of laminin in epithelium formation by F9 aggregates. J Cell Biol. 1983 Jul;97(1):137–144. doi: 10.1083/jcb.97.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Gwatkin R. B. Defined media and development of mammalian eggs in vitro. Ann N Y Acad Sci. 1966 Oct 7;139(1):79–90. doi: 10.1111/j.1749-6632.1966.tb41186.x. [DOI] [PubMed] [Google Scholar]
  41. Hall D. E., Neugebauer K. M., Reichardt L. F. Embryonic neural retinal cell response to extracellular matrix proteins: developmental changes and effects of the cell substratum attachment antibody (CSAT). J Cell Biol. 1987 Mar;104(3):623–634. doi: 10.1083/jcb.104.3.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Hasegawa T., Hasegawa E., Chen W. T., Yamada K. M. Characterization of a membrane-associated glycoprotein complex implicated in cell adhesion to fibronectin. J Cell Biochem. 1985;28(4):307–318. doi: 10.1002/jcb.240280409. [DOI] [PubMed] [Google Scholar]
  43. Horwitz A., Duggan K., Buck C., Beckerle M. C., Burridge K. Interaction of plasma membrane fibronectin receptor with talin--a transmembrane linkage. Nature. 1986 Apr 10;320(6062):531–533. doi: 10.1038/320531a0. [DOI] [PubMed] [Google Scholar]
  44. Horwitz A., Duggan K., Greggs R., Decker C., Buck C. The cell substrate attachment (CSAT) antigen has properties of a receptor for laminin and fibronectin. J Cell Biol. 1985 Dec;101(6):2134–2144. doi: 10.1083/jcb.101.6.2134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Hsu Y. C. Differentiation in vitro of mouse embryos to the stage of early somite. Dev Biol. 1973 Aug;33(2):403–411. doi: 10.1016/0012-1606(73)90145-0. [DOI] [PubMed] [Google Scholar]
  46. Hsu Y. C. Post-blastocyst differentiation in vitro. Nature. 1971 May 14;231(5298):100–102. doi: 10.1038/231100a0. [DOI] [PubMed] [Google Scholar]
  47. Hynes R. O. Integrins: a family of cell surface receptors. Cell. 1987 Feb 27;48(4):549–554. doi: 10.1016/0092-8674(87)90233-9. [DOI] [PubMed] [Google Scholar]
  48. Knudsen K. A., Horwitz A. F., Buck C. A. A monoclonal antibody identifies a glycoprotein complex involved in cell-substratum adhesion. Exp Cell Res. 1985 Mar;157(1):218–226. doi: 10.1016/0014-4827(85)90164-8. [DOI] [PubMed] [Google Scholar]
  49. Knudsen K. A., Rao P. E., Damsky C. H., Buck C. A. Membrane glycoproteins involved in cell--substratum adhesion. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6071–6075. doi: 10.1073/pnas.78.10.6071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Krotoski D. M., Domingo C., Bronner-Fraser M. Distribution of a putative cell surface receptor for fibronectin and laminin in the avian embryo. J Cell Biol. 1986 Sep;103(3):1061–1071. doi: 10.1083/jcb.103.3.1061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  52. MINTZ B. FORMATION OF GENETICALLY MOSAIC MOUSE EMBRYOS, AND EARLY DEVELOPMENT OF "LETHAL (T12/T12)-NORMAL" MOSAICS. J Exp Zool. 1964 Nov;157:273–292. doi: 10.1002/jez.1401570210. [DOI] [PubMed] [Google Scholar]
  53. Manasek F. J. Embryonic development of the heart. I. A light and electron microscopic study of myocardial development in the early chick embryo. J Morphol. 1968 Jul;125(3):329–365. doi: 10.1002/jmor.1051250306. [DOI] [PubMed] [Google Scholar]
  54. Markwald R. R., Fitzharris T. P., Manasek F. J. Structural development of endocardial cushions. Am J Anat. 1977 Jan;148(1):85–119. doi: 10.1002/aja.1001480108. [DOI] [PubMed] [Google Scholar]
  55. Markwald R. R., Fitzharris T. P., Smith W. N. Sturctural analysis of endocardial cytodifferentiation. Dev Biol. 1975 Jan;42(1):160–180. doi: 10.1016/0012-1606(75)90321-8. [DOI] [PubMed] [Google Scholar]
  56. Neff N. T., Lowrey C., Decker C., Tovar A., Damsky C., Buck C., Horwitz A. F. A monoclonal antibody detaches embryonic skeletal muscle from extracellular matrices. J Cell Biol. 1982 Nov;95(2 Pt 1):654–666. doi: 10.1083/jcb.95.2.654. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Patel V. P., Lodish H. F. The fibronectin receptor on mammalian erythroid precursor cells: characterization and developmental regulation. J Cell Biol. 1986 Feb;102(2):449–456. doi: 10.1083/jcb.102.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Peyriéras N., Hyafil F., Louvard D., Ploegh H. L., Jacob F. Uvomorulin: a nonintegral membrane protein of early mouse embryo. Proc Natl Acad Sci U S A. 1983 Oct;80(20):6274–6277. doi: 10.1073/pnas.80.20.6274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Pierschbacher M. D., Ruoslahti E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature. 1984 May 3;309(5963):30–33. doi: 10.1038/309030a0. [DOI] [PubMed] [Google Scholar]
  60. Pierschbacher M. D., Ruoslahti E. Variants of the cell recognition site of fibronectin that retain attachment-promoting activity. Proc Natl Acad Sci U S A. 1984 Oct;81(19):5985–5988. doi: 10.1073/pnas.81.19.5985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Pytela R., Pierschbacher M. D., Ginsberg M. H., Plow E. F., Ruoslahti E. Platelet membrane glycoprotein IIb/IIIa: member of a family of Arg-Gly-Asp--specific adhesion receptors. Science. 1986 Mar 28;231(4745):1559–1562. doi: 10.1126/science.2420006. [DOI] [PubMed] [Google Scholar]
  62. Pytela R., Pierschbacher M. D., Ruoslahti E. A 125/115-kDa cell surface receptor specific for vitronectin interacts with the arginine-glycine-aspartic acid adhesion sequence derived from fibronectin. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5766–5770. doi: 10.1073/pnas.82.17.5766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Pytela R., Pierschbacher M. D., Ruoslahti E. Identification and isolation of a 140 kd cell surface glycoprotein with properties expected of a fibronectin receptor. Cell. 1985 Jan;40(1):191–198. doi: 10.1016/0092-8674(85)90322-8. [DOI] [PubMed] [Google Scholar]
  64. Richa J., Damsky C. H., Buck C. A., Knowles B. B., Solter D. Cell surface glycoproteins mediate compaction, trophoblast attachment, and endoderm formation during early mouse development. Dev Biol. 1985 Apr;108(2):513–521. doi: 10.1016/0012-1606(85)90054-5. [DOI] [PubMed] [Google Scholar]
  65. Ruoslahti E., Pierschbacher M. D. Arg-Gly-Asp: a versatile cell recognition signal. Cell. 1986 Feb 28;44(4):517–518. doi: 10.1016/0092-8674(86)90259-x. [DOI] [PubMed] [Google Scholar]
  66. Shirayoshi Y., Okada T. S., Takeichi M. The calcium-dependent cell-cell adhesion system regulates inner cell mass formation and cell surface polarization in early mouse development. Cell. 1983 Dec;35(3 Pt 2):631–638. doi: 10.1016/0092-8674(83)90095-8. [DOI] [PubMed] [Google Scholar]
  67. Shur B. D., Oettgen P., Bennett D. UDPgalactose inhibits blastocyst formation in the mouse. Implications for the mode of action of T/t-complex mutations. Dev Biol. 1979 Nov;73(1):178–181. doi: 10.1016/0012-1606(79)90146-5. [DOI] [PubMed] [Google Scholar]
  68. Spindle A. I., Pedersen R. A. Hatching, attachment, and outgrowth of mouse blastocysts in vitro: fixed nitrogen requirements. J Exp Zool. 1973 Dec;186(3):305–318. doi: 10.1002/jez.1401860308. [DOI] [PubMed] [Google Scholar]
  69. Spindle A. An improved culture medium for mouse blastocysts. In Vitro. 1980 Aug;16(8):669–674. doi: 10.1007/BF02619196. [DOI] [PubMed] [Google Scholar]
  70. Tamkun J. W., DeSimone D. W., Fonda D., Patel R. S., Buck C., Horwitz A. F., Hynes R. O. Structure of integrin, a glycoprotein involved in the transmembrane linkage between fibronectin and actin. Cell. 1986 Jul 18;46(2):271–282. doi: 10.1016/0092-8674(86)90744-0. [DOI] [PubMed] [Google Scholar]
  71. Tomaselli K. J., Damsky C. H., Reichardt L. F. Interactions of a neuronal cell line (PC12) with laminin, collagen IV, and fibronectin: identification of integrin-related glycoproteins involved in attachment and process outgrowth. J Cell Biol. 1987 Nov;105(5):2347–2358. doi: 10.1083/jcb.105.5.2347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Toole B. P., Trelstad R. L. Hyaluronate production and removal during corneal development in the chick. Dev Biol. 1971 Sep;26(1):28–35. doi: 10.1016/0012-1606(71)90104-7. [DOI] [PubMed] [Google Scholar]
  73. Tuszynski G. P., Rothman V., Murphy A., Siegler K., Smith L., Smith S., Karczewski J., Knudsen K. A. Thrombospondin promotes cell-substratum adhesion. Science. 1987 Jun 19;236(4808):1570–1573. doi: 10.1126/science.2438772. [DOI] [PubMed] [Google Scholar]
  74. Wayner E. A., Carter W. G. Identification of multiple cell adhesion receptors for collagen and fibronectin in human fibrosarcoma cells possessing unique alpha and common beta subunits. J Cell Biol. 1987 Oct;105(4):1873–1884. doi: 10.1083/jcb.105.4.1873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Wewer U. M., Faber M., Liotta L. A., Albrechtsen R. Immunochemical and ultrastructural assessment of the nature of the pericellular basement membrane of human decidual cells. Lab Invest. 1985 Dec;53(6):624–633. [PubMed] [Google Scholar]
  76. Wilson I. B., Jenkinson E. J. Blastocyst differentiation in vitro. J Reprod Fertil. 1974 Jul;39(1):243–249. doi: 10.1530/jrf.0.0390243. [DOI] [PubMed] [Google Scholar]
  77. Yamada K. M., Kennedy D. W. Dualistic nature of adhesive protein function: fibronectin and its biologically active peptide fragments can autoinhibit fibronectin function. J Cell Biol. 1984 Jul;99(1 Pt 1):29–36. doi: 10.1083/jcb.99.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]

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