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PMID: 11585912 Published · ppublish English Journal Article

Transformation of chicken embryo fibroblasts by v-src uncouples beta1 integrin-mediated outside-in but not inside-out signaling.

Molecular and cellular biology ·Vol. 21 ·No. 21 ·2001-11-00 ·Pages 7295-306

Datta A, Shi Q, Boettiger DE

Abstract

Adhesion of cells to extracellular matrix is mediated by integrin family receptors. The process of receptor-ligand binding is dependent on metabolic energy and is regulated by intracellular signals, termed inside-out signals. The strength of the initial alpha5beta1-mediated adhesion of v-src-transformed chicken embryo fibroblasts (v-srcCEF) was similar to that of normal CEF. A chemically cross-linked fibronectin substrate was able to restore cell spreading and the ability of v-srcCEF to assemble a fibronectin matrix. Over time, v-srcCEF showed decreased adhesion due to the reduction of alpha5beta1-fibronectin bonds consequent on the reduction of substrate-bound fibronectin due to the secretion of proteases by v-srcCEF. Excess synthesis of hyaluronic acid by v-srcCEF also reduced the alpha5beta1-fibronectin bonds and contributed to cell detachment at later times in culture. Thus, the adhesion defects were not due to a failure of alpha5beta1 function and adhesion of the v-srcCEF was alpha5beta1 dependent. Integrin-mediated adhesion also produces signals that affect cell proliferation and cell differentiation. An early consequence of these "outside-in" signals was the phosphorylation of FAK Y397 in direct proportion to the number of alpha5beta1-fibronectin bonds formed. In contrast, v-srcCEF had an increased level of phosphorylation on five different tyrosines in FAK, and none of these phosphorylation levels were sensitive to the number of alpha5beta1-fibronectin bonds. In the absence of serum, CEF proliferation was sensitive to changes in alpha5beta1-mediated adhesion levels. Transformation by v-src increased the serum-free proliferation rate and made it insensitive to alpha5beta1-mediated adhesion. Thus, the v-srcCEF were insensitive to the normal outside-in signals from alpha5beta1 integrin.

MeSH Terms
Animals Cell Adhesion Cell Differentiation Cell Division Cell Movement Cell Transformation, Neoplastic Cells, Cultured Chick Embryo Cross-Linking Reagents/pharmacology Culture Media, Serum-Free/pharmacology Enzyme-Linked Immunosorbent Assay Fibroblasts/cytology,metabolism Fibronectins/metabolism Focal Adhesion Kinase 1 Focal Adhesion Protein-Tyrosine Kinases Humans Hyaluronic Acid/pharmacology Integrin beta1/metabolism Microscopy, Fluorescence Oncogene Protein pp60(v-src)/metabolism Phosphorylation Protein Structure, Tertiary Protein-Tyrosine Kinases/metabolism Receptors, Fibronectin/metabolism Signal Transduction Time Factors
Chemicals
Cross-Linking Reagents Culture Media, Serum-Free Fibronectins Integrin beta1 Receptors, Fibronectin Hyaluronic Acid Protein-Tyrosine Kinases Focal Adhesion Kinase 1 Focal Adhesion Protein-Tyrosine Kinases Oncogene Protein pp60(v-src) PTK2 protein, human
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Datta A
Department of Microbiology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.
Shi Q
Boettiger D E
References (69)
69 references, click to expand
  1. Structure of integrin, a glycoprotein involved in the transmembrane linkage between fibronectin and actin.
    Cell. 1986 Jul 18;46(2):271-82 PMID: 3487386
  2. Phosphorylation of the fibronectin receptor complex in cells transformed by oncogenes that encode tyrosine kinases.
    Proc Natl Acad Sci U S A. 1986 Sep;83(17):6470-4 PMID: 3018734
  3. A laminin substrate promotes myogenesis in rat skeletal muscle cultures: analysis of replication and development using antidesmin and anti-BrdUrd monoclonal antibodies.
    Dev Biol. 1987 Jul;122(1):11-20 PMID: 3297850
  4. Occupation of the extracellular matrix receptor, integrin, is a control point for myogenic differentiation.
    Cell. 1987 Oct 9;51(1):51-7 PMID: 3115595
  5. Activation of the oncogenic potential of the avian cellular src protein by specific structural alteration of the carboxy terminus.
    EMBO J. 1987 Aug;6(8):2359-64 PMID: 2822389
  6. Force required to break alpha5beta1 integrin-fibronectin bonds in intact adherent cells is sensitive to integrin activation state.
    J Biol Chem. 1998 May 1;273(18):10988-93 PMID: 9556578
  7. Requirement for MAPK activation for normal mitotic progression in Xenopus egg extracts.
    Science. 1998 Nov 13;282(5392):1312-5 PMID: 9812894
  8. Two-stage activation for alpha5beta1 integrin binding to surface-adsorbed fibronectin.
    J Biol Chem. 1998 Dec 25;273(52):34710-5 PMID: 9856993
  9. How regulated protein translocation can produce switch-like responses.
    Trends Biochem Sci. 1998 Dec;23(12):461-5 PMID: 9868363
  10. pp60(v-src) induction of cyclin D1 requires collaborative interactions between the extracellular signal-regulated kinase, p38, and Jun kinase pathways. A role for cAMP response element-binding protein and activating transcription factor-2 in pp60(v-src) signaling in breast cancer cells.
    J Biol Chem. 1999 Mar 12;274(11):7341-50 PMID: 10066798
  11. Modulation of cell proliferation and differentiation through substrate-dependent changes in fibronectin conformation.
    Mol Biol Cell. 1999 Mar;10(3):785-98 PMID: 10069818
  12. Src family kinases are required for integrin but not PDGFR signal transduction.
    EMBO J. 1999 May 4;18(9):2459-71 PMID: 10228160
  13. Characteristics of an assay for Rous sarcoma virus and Rous sarcoma cells in tissue culture.
    Virology. 1958 Dec;6(3):669-88 PMID: 13616179
  14. AGAR SUSPENSION CULTURE FOR THE SELECTIVE ASSAY OF CELLS TRANSFORMED BY POLYOMA VIRUS.
    Virology. 1964 Jun;23:291-4 PMID: 14187925
  15. Changes in integrin receptors on oncogenically transformed cells.
    Cell. 1989 Jan 27;56(2):281-90 PMID: 2521461
  16. Integrins isolated from Rous sarcoma virus-transformed chicken embryo fibroblasts.
    Oncogene. 1989 Mar;4(3):325-33 PMID: 2468126
  17. Plasminogen activator gene expression is induced by the src oncogene product and tumor promoters.
    J Biol Chem. 1990 Jan 25;265(3):1333-8 PMID: 2153128
  18. Monoclonal antibodies to individual tyrosine-phosphorylated protein substrates of oncogene-encoded tyrosine kinases.
    Proc Natl Acad Sci U S A. 1990 May;87(9):3328-32 PMID: 2110361
  19. Association between the PDGF receptor and members of the src family of tyrosine kinases.
    Cell. 1990 Aug 10;62(3):481-92 PMID: 1696179
  20. Integrin-fibronectin interactions at the cell-material interface: initial integrin binding and signaling.
    Biomaterials. 1999 Dec;20(23-24):2427-33 PMID: 10614947
  21. Integrin dynamics and matrix assembly: tensin-dependent translocation of alpha(5)beta(1) integrins promotes early fibronectin fibrillogenesis.
    J Cell Biol. 2000 Mar 6;148(5):1075-90 PMID: 10704455
  22. v-Src induces tyrosine phosphorylation of focal adhesion kinase independently of tyrosine 397 and formation of a complex with Src.
    J Biol Chem. 2000 Jul 28;275(30):23333-9 PMID: 10816598
  23. Role of the cytoplasmic tyrosines of beta 1A integrins in transformation by v-src.
    Proc Natl Acad Sci U S A. 2001 Mar 27;98(7):3808-13 PMID: 11259684
  24. The v-Src SH3 domain facilitates a cell adhesion-independent association with focal adhesion kinase.
    J Biol Chem. 2001 May 25;276(21):17653-62 PMID: 11278488
  25. Phosphorylation and activation of epidermal growth factor receptors in cells transformed by the src oncogene.
    Mol Cell Biol. 1991 Jan;11(1):309-21 PMID: 1702513
  26. Effect of platelet activation on the conformation of the plasma membrane glycoprotein IIb-IIIa complex.
    J Biol Chem. 1991 Apr 25;266(12):7345-52 PMID: 1902217
  27. Cellular partitioning of beta-1 integrins and their phosphorylated forms is altered after transformation by Rous sarcoma virus or treatment with cytochalasin D.
    Cell Regul. 1991 Apr;2(4):271-83 PMID: 1647822
  28. Monoclonal antibodies to ligand-occupied conformers of integrin alpha IIb beta 3 (glycoprotein IIb-IIIa) alter receptor affinity, specificity, and function.
    J Biol Chem. 1991 Sep 15;266(26):17106-11 PMID: 1894607
  29. Signal transduction by integrins: increased protein tyrosine phosphorylation caused by clustering of beta 1 integrins.
    Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8392-6 PMID: 1717976
  30. Integrins: versatility, modulation, and signaling in cell adhesion.
    Cell. 1992 Apr 3;69(1):11-25 PMID: 1555235
  31. Fibronectin/integrin interaction induces tyrosine phosphorylation of a 120-kDa protein.
    Cell Regul. 1991 Nov;2(11):951-64 PMID: 1725602
  32. Identification of amino acid sequences in the integrin beta 1 cytoplasmic domain implicated in cytoskeletal association.
    J Cell Biol. 1992 Jun;117(6):1321-30 PMID: 1376731
  33. A fibronectin self-assembly site involved in fibronectin matrix assembly: reconstruction in a synthetic peptide.
    J Cell Biol. 1992 Jul;118(2):421-9 PMID: 1629240
  34. Inside-out integrin signalling.
    Curr Opin Cell Biol. 1992 Oct;4(5):766-71 PMID: 1419055
  35. Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion-associated tyrosine kinase.
    J Biol Chem. 1992 Nov 25;267(33):23439-42 PMID: 1429685
  36. Tyrosine phosphorylation of paxillin and pp125FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly.
    J Cell Biol. 1992 Nov;119(4):893-903 PMID: 1385444
  37. Integrin-dependent phosphorylation and activation of the protein tyrosine kinase pp125FAK in platelets.
    J Cell Biol. 1992 Nov;119(4):905-12 PMID: 1385445
  38. Affinity modulation of integrin alpha 5 beta 1: regulation of the functional response by soluble fibronectin.
    J Cell Biol. 1993 Apr;121(1):155-62 PMID: 8458867
  39. Beta 1 integrins mediate chondrocyte interaction with type I collagen, type II collagen, and fibronectin.
    Exp Cell Res. 1993 Apr;205(2):276-85 PMID: 8387015
  40. Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength.
    J Cell Biol. 1993 Aug;122(3):729-37 PMID: 8335696
  41. Stable association of pp60src and pp59fyn with the focal adhesion-associated protein tyrosine kinase, pp125FAK.
    Mol Cell Biol. 1994 Jan;14(1):147-55 PMID: 7505391
  42. Evaluation of integrin molecules involved in substrate adhesion.
    Cell Adhes Commun. 1993 Dec;1(3):191-202 PMID: 7521753
  43. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase.
    Nature. 1994 Dec 22-29;372(6508):786-91 PMID: 7997267
  44. Integrins and signal transduction pathways: the road taken.
    Science. 1995 Apr 14;268(5208):233-9 PMID: 7716514
  45. c-Src enhances the spreading of src-/- fibroblasts on fibronectin by a kinase-independent mechanism.
    Genes Dev. 1995 Jun 15;9(12):1505-17 PMID: 7541382
  46. Integrin-dependent activation of MAP kinase: a link to shape-dependent cell proliferation.
    Mol Biol Cell. 1995 Mar;6(3):273-82 PMID: 7612963
  47. Integrin activation and cytoskeletal interaction are essential for the assembly of a fibronectin matrix.
    Cell. 1995 Dec 1;83(5):715-24 PMID: 8521488
  48. Beta 1 integrin-dependent and -independent polymerization of fibronectin.
    J Cell Biol. 1996 Jan;132(1-2):227-38 PMID: 8567726
  49. Adhesion-dependent cell cycle progression linked to the expression of cyclin D1, activation of cyclin E-cdk2, and phosphorylation of the retinoblastoma protein.
    J Cell Biol. 1996 Apr;133(2):391-403 PMID: 8609171
  50. Integrins: emerging paradigms of signal transduction.
    Annu Rev Cell Dev Biol. 1995;11:549-99 PMID: 8689569
  51. p130Cas, a substrate associated with v-Src and v-Crk, localizes to focal adhesions and binds to focal adhesion kinase.
    J Biol Chem. 1996 Jun 7;271(23):13649-55 PMID: 8662921
  52. Quantification of cell adhesion using a spinning disc device and application to surface-reactive materials.
    Biomaterials. 1997 Aug;18(16):1091-8 PMID: 9247346
  53. Rho-stimulated contractility contributes to the fibroblastic phenotype of Ras-transformed epithelial cells.
    Mol Biol Cell. 1997 Nov;8(11):2329-44 PMID: 9362072
  54. Modulation of beta1A integrin functions by tyrosine residues in the beta1 cytoplasmic domain.
    J Cell Biol. 1998 Apr 20;141(2):527-38 PMID: 9548729
  55. Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly.
    J Cell Biol. 1998 Apr 20;141(2):539-51 PMID: 9548730
  56. Studies of carcinogenesis by avian sarcoma viruses. II. Virus-induced increase in hyaluronic acid synthetase in chicken fibroblasts.
    J Biol Chem. 1966 May 10;241(9):2052-7 PMID: 4287759
  57. Temperature-sensitive expression of differentiation in transformed myoblasts.
    Nature. 1975 Apr 3;254(5499):429-31 PMID: 163986
  58. Inhibition of protease activity in cultures of rous sarcoma virus-transformed cells: effect on the transformed phenotype.
    Cell. 1975 Jul;5(3):253-61 PMID: 167981
  59. Cell surface protein partially restores morphology, adhesiveness, and contact inhibition of movement to transformed fibroblasts.
    Proc Natl Acad Sci U S A. 1976 Apr;73(4):1217-21 PMID: 177979
  60. Restoration of normal morphology, adhesion and cytoskeleton in transformed cells by addition of a transformation-sensitive surface protein.
    Cell. 1977 May;11(1):115-26 PMID: 326414
  61. Adhesion plaques of Rous sarcoma virus-transformed cells contain the src gene product.
    Proc Natl Acad Sci U S A. 1980 Jun;77(6):3514-8 PMID: 6251464
  62. Early changes in the distribution and organization of microfilament proteins during cell transformation.
    Cell. 1981 Apr;24(1):175-84 PMID: 6263486
  63. Transformation by Rous sarcoma virus induces similar patterns of glycosaminoglycan synthesis in chick embryo skin fibroblasts and vertebral chondroblasts.
    J Biol Chem. 1983 Jan 25;258(2):810-6 PMID: 6296083
  64. Immunological characterization of the major chick cartilage proteoglycan and its intracellular localization in cultured chondroblasts: a comparison with Type II procollagen.
    J Cell Biol. 1983 Dec;97(6):1724-36 PMID: 6358233
  65. Expression of transformation-associated protease(s) that degrade fibronectin at cell contact sites.
    J Cell Biol. 1984 Apr;98(4):1546-55 PMID: 6325472
  66. Monoclonal antibody against human fibronectin which inhibits cell attachment.
    Hybridoma. 1982;1(2):99-108 PMID: 6208125
  67. Local degradation of fibronectin at sites of expression of the transforming gene product pp60src.
    Nature. 1985 Jul 11-17;316(6024):156-8 PMID: 2989711
  68. Rous sarcoma virus-transformed fibroblasts adhere primarily at discrete protrusions of the ventral membrane called podosomes.
    Exp Cell Res. 1985 Jul;159(1):141-57 PMID: 2411576
  69. An anticatalytic monoclonal antibody to avian plasminogen activator: its effect on behavior of RSV-transformed chick fibroblasts.
    Cell. 1986 Jun 20;45(6):905-15 PMID: 3011282
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2001-11-00
Pages
7295-306
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC99904
Subset
IM
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