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PMID: 3181137 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Attachment, spreading and locomotion of avian neural crest cells are mediated by multiple adhesion sites on fibronectin molecules.

The EMBO journal ·Vol. 7 ·No. 9 ·1988-09-00 ·Pages 2661-71

Dufour S, Duband JL, Humphries MJ, Obara M, Yamada KM, Thiery JP

Abstract

Cellular adhesion to fibronectin (FN) can be mediated by several sequences located in different portions of the molecule. In human FN, these are: (i) the bipartite RGDS domain containing the RGDS cell-binding sequence functioning in synergy for full cellular adhesion with a second site (termed here the synergistic adhesion site) and (ii) the recently characterized CS1 and REDV adhesion sites within the alternatively-spliced type III homology-connecting segment. Using specific adhesive ligands and inhibitory probes, we have examined the role of each of these domains in the adhesion, spreading, and motility of avian neural crest cells in vitro. Both the RGDS domain and the CS1 adhesion site were found to promote attachment of neural crest cells, but only the RGDS domain supported their spreading. However, the RGDS sequence could mediate both attachment and spreading efficiently only when it was associated with the synergistic adhesion site. In migratory assays, it was found that both the RGDS domain and the CS1 site are required in association, each with functional specificity, to permit effective locomotion of neural crest cells. The REDV adhesion site was apparently not recognized by avian neural crest cells, presumably because this sequence is absent from chicken FN. Finally, it was found that recognition of both the RGDS domain and CS1 binding site by neural crest cells involved receptors belonging to the integrin family. From these results, we conclude that neural crest cells can interact with several binding sites of FN molecules, and use them for distinct functions. Our results also suggest the possibility of an instructive role for FN in the control of adhesive and migratory events during embryonic development.

MeSH Terms
Animals Cell Adhesion Cell Movement Cells, Cultured Coturnix Fibronectins/metabolism Humans Neural Crest/cytology,metabolism
Chemicals
Fibronectins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Dufour S
Laboratoire de Physiopathologie du Développement, Centre National de la Recherche Scientifique et Ecole Normale Supérieure, Paris, France.
Duband J L
Humphries M J
Obara M
Yamada K M
Thiery J P
References (38)
38 references, click to expand
  1. The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite.
    J Embryol Exp Morphol. 1985 Dec;90:437-55 PMID: 3834038
  2. Pathways of avian neural crest cell migration in the developing gut.
    Dev Biol. 1986 Aug;116(2):439-50 PMID: 3732616
  3. An antibody to a receptor for fibronectin and laminin perturbs cranial neural crest development in vivo.
    Dev Biol. 1986 Oct;117(2):528-36 PMID: 2944780
  4. Identification of an alternatively spliced site in human plasma fibronectin that mediates cell type-specific adhesion.
    J Cell Biol. 1986 Dec;103(6 Pt 2):2637-47 PMID: 3025221
  5. Peptide inhibitors of fibronectin, laminin, and other adhesion molecules: unique and shared features.
    J Cell Physiol. 1987 Jan;130(1):21-8 PMID: 3805128
  6. Integrins: a family of cell surface receptors.
    Cell. 1987 Feb 27;48(4):549-54 PMID: 3028640
  7. Cell migration in the vertebrate embryo: role of cell adhesion and tissue environment in pattern formation.
    Annu Rev Cell Biol. 1985;1:91-113 PMID: 3916324
  8. Expression of the cell-binding domain of human fibronectin in E. coli. Identification of sequences promoting full to minimal adhesive function.
    FEBS Lett. 1987 Mar 23;213(2):261-4 PMID: 3104088
  9. Formation of the dorsal root ganglia in the avian embryo: segmental origin and migratory behavior of neural crest progenitor cells.
    Dev Biol. 1987 Apr;120(2):329-47 PMID: 3549390
  10. Identification of two distinct regions of the type III connecting segment of human plasma fibronectin that promote cell type-specific adhesion.
    J Biol Chem. 1987 May 15;262(14):6886-92 PMID: 3571291
  11. Selective interaction of peripheral and central nervous system cells with two distinct cell-binding domains of fibronectin.
    J Cell Biol. 1987 Sep;105(3):1435-42 PMID: 2958484
  12. New perspectives in cell adhesion: RGD and integrins.
    Science. 1987 Oct 23;238(4826):491-7 PMID: 2821619
  13. 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):1873-84 PMID: 2822727
  14. Thrombospondin-induced tumor cell migration: haptotaxis and chemotaxis are mediated by different molecular domains.
    J Cell Biol. 1987 Nov;105(5):2409-15 PMID: 3680388
  15. Cell surface receptors for extracellular matrix molecules.
    Annu Rev Cell Biol. 1987;3:179-205 PMID: 2825736
  16. Alternative splicing of chicken fibronectin in embryos and in normal and transformed cells.
    Mol Cell Biol. 1987 Dec;7(12):4297-307 PMID: 2830487
  17. Modulation of matrix adhesive responses of human neuroblastoma cells by neighboring sequences in the fibronectins.
    J Cell Biol. 1988 Mar;106(3):931-43 PMID: 3346330
  18. Neurite extension of chicken peripheral nervous system neurons on fibronectin: relative importance of specific adhesion sites in the central cell-binding domain and the alternatively spliced type III connecting segment.
    J Cell Biol. 1988 Apr;106(4):1289-97 PMID: 3360854
  19. Site-directed mutagenesis of the cell-binding domain of human fibronectin: separable, synergistic sites mediate adhesive function.
    Cell. 1988 May 20;53(4):649-57 PMID: 3286012
  20. Adhesive protein receptors on hematopoietic cells.
    Immunol Today. 1988 Apr;9(4):109-13 PMID: 2855703
  21. Morphology and behaviour of neural crest cells of chick embryo in vitro.
    Cell Tissue Res. 1979 Nov;203(1):115-40 PMID: 509508
  22. Ultrastructural and tissue-culture studies on the role of fibronectin, collagen and glycosaminoglycans in the migration of neural crest cells in the fowl embryo.
    Cell Tissue Res. 1982;221(3):521-49 PMID: 7034954
  23. Pathways and mechanisms of avian trunk neural crest cell migration and localization.
    Dev Biol. 1982 Oct;93(2):324-43 PMID: 7141101
  24. Neural crest cell migration: requirements for exogenous fibronectin and high cell density.
    J Cell Biol. 1983 Feb;96(2):462-73 PMID: 6833366
  25. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule.
    Nature. 1984 May 3-9;309(5963):30-3 PMID: 6325925
  26. 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 PMID: 6736130
  27. Morphology and behavior of quail neural crest cells in artificial three-dimensional extracellular matrices.
    Dev Biol. 1984 Aug;104(2):390-405 PMID: 6745490
  28. A single rat fibronectin gene generates three different mRNAs by alternative splicing of a complex exon.
    Proc Natl Acad Sci U S A. 1984 Aug;81(16):5140-4 PMID: 6089177
  29. Variants of the cell recognition site of fibronectin that retain attachment-promoting activity.
    Proc Natl Acad Sci U S A. 1984 Oct;81(19):5985-8 PMID: 6237366
  30. 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):1822-30 PMID: 6490722
  31. A monoclonal antibody identifies a glycoprotein complex involved in cell-substratum adhesion.
    Exp Cell Res. 1985 Mar;157(1):218-26 PMID: 2578969
  32. Development of cell surface linkage complexes in cultured fibroblasts.
    J Cell Biol. 1985 Apr;100(4):1103-14 PMID: 3884631
  33. Primary structure of human fibronectin: differential splicing may generate at least 10 polypeptides from a single gene.
    EMBO J. 1985 Jul;4(7):1755-9 PMID: 2992939
  34. The interaction of fibronectin fragments with fibroblastic cells.
    J Biol Chem. 1985 Oct 25;260(24):13256-60 PMID: 2932436
  35. Characterization of a membrane-associated glycoprotein complex implicated in cell adhesion to fibronectin.
    J Cell Biochem. 1985;28(4):307-18 PMID: 4055919
  36. 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):160-78 PMID: 2934401
  37. Human fibronectin contains distinct adhesion- and motility-promoting domains for metastatic melanoma cells.
    J Cell Biol. 1986 Jan;102(1):179-88 PMID: 3941152
  38. Amino acid sequence specificities of an adhesive recognition signal.
    J Cell Biochem. 1985;28(2):99-104 PMID: 4077927
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1988-09-00
Pages
2661-71
Language
English
Region
England
NLM ID
8208664
PMCID
PMC457054
Subset
IM
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