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PMID: 7962101 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Modulation of cell surface fibronectin assembly sites by lysophosphatidic acid.

The Journal of cell biology ·Vol. 127 ·No. 5 ·1994-12-00 ·Pages 1447-59

Zhang Q, Checovich WJ, Peters DM, Albrecht RM, Mosher DF

Abstract

Lysophosphatidic acid is a product of activated platelets and has diverse actions on cells. We have characterized the effect of lysophosphatidic acid on cell-mediated binding and assembly of fibronectin, an extracellular matrix protein. Serum made from whole blood, but neither platelet-poor plasma nor serum made from platelet-poor plasma, caused enhanced binding of fibronectin to cultured fibroblastic cells. The ability of whole blood serum to enhance binding of fibronectin was abolished by phospholipase B. These results indicate that lysophosphatidic acid derived from platelets is the principal component in whole blood serum that is active in the fibronectin binding assay. 1-oleoyl lysophosphatidic acid, 20-200 nM, was as active as 0.1-0.2% whole blood serum. The stimulatory effect of lysophosphatidic acid on the binding of fibronectin or the amino-terminal 70-kD fragment of fibronectin was rapid, sustained, and lost upon removal of lysophosphatidic acid. The stimulatory effect on binding could not be duplicated by bradykinin, platelet-activating factor, bombesin, or a peptide agonist of the thrombin receptor. Enhanced binding of the 70-kD fragment was due to increases in both the number and affinity of binding sites. Enhanced binding and assembly of fibronectin correlated with changes in cell shape and actin-containing cytoskeleton. The binding sites for fibronectin on lysophosphatidic acid-stimulated cells, as assessed by fluorescence, video, and scanning electron microscopy, were on areas of cell membrane containing numerous filopodia that extended between cells or between cells and substratum. These observations suggest that lysophosphatidic acid functions as a powerful and specific modulator of cell shape and early matrix assembly during wound healing.

MeSH Terms
Actin Cytoskeleton/drug effects,metabolism,ultrastructure Binding Sites Blood Bradykinin/pharmacology Cell Membrane/drug effects,metabolism Cell Size/drug effects Dose-Response Relationship, Drug Fibronectins/metabolism Humans Kinetics Lysophospholipids/pharmacology Microscopy, Electron, Scanning Peptide Fragments/pharmacology Platelet Activating Factor/pharmacology Receptors, Thrombin Tumor Cells, Cultured
Chemicals
Fibronectins Lysophospholipids Peptide Fragments Platelet Activating Factor Receptors, Thrombin lysophosphatidic acid Bradykinin
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Zhang Q
Department of Medicine, University of Wisconsin-Madison 53706.
Checovich W J
Peters D M
Albrecht R M
Mosher D F
References (69)
69 references, click to expand
  1. Critical micellar concentrations of palmitoyl dehydroxyacetone phosphate and 1-palmitoyl-rac-glycerol 3-phosphate.
    J Biol Chem. 1992 May 15;267(14):9731 PMID: 1577809
  2. Identification of a putative membrane receptor for the bioactive phospholipid, lysophosphatidic acid.
    EMBO J. 1992 Jul;11(7):2495-501 PMID: 1321033
  3. Thrombin receptor activation causes rapid neural cell rounding and neurite retraction independent of classic second messengers.
    J Cell Biol. 1992 Jul;118(2):411-9 PMID: 1321160
  4. 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
  5. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors.
    Cell. 1992 Aug 7;70(3):389-99 PMID: 1643657
  6. Cultured human fibroblasts synthesize and secrete thrombospondin and incorporate it into extracellular matrix.
    Proc Natl Acad Sci U S A. 1983 Feb;80(4):998-1002 PMID: 6341993
  7. Binding of plasma fibronectin to cell layers of human skin fibroblasts.
    J Cell Biol. 1983 Aug;97(2):466-72 PMID: 6309861
  8. Mechanism of formation of disulfide-bonded multimers of plasma fibronectin in cell layers of cultured human fibroblasts.
    J Biol Chem. 1984 Oct 10;259(19):12210-5 PMID: 6480605
  9. Interaction of the 70,000-mol-wt amino-terminal fragment of fibronectin with the matrix-assembly receptor of fibroblasts.
    J Cell Biol. 1985 Feb;100(2):364-74 PMID: 3155749
  10. Decanoyl lysophosphatidic acid induces platelet aggregation through an extracellular action. Evidence against a second messenger role for lysophosphatidic acid.
    Biochem J. 1985 Nov 15;232(1):61-6 PMID: 3853461
  11. Growth factor-like action of phosphatidic acid.
    Nature. 1986 Sep 11-17;323(6084):171-3 PMID: 3748188
  12. Localization of cell surface sites involved in fibronectin fibrillogenesis.
    J Cell Biol. 1987 Jan;104(1):121-30 PMID: 2947903
  13. Assembly and alignment of fibronectin-coated gold beads into fibrils by human skin fibroblasts.
    Scanning Microsc. 1987 Jun;1(2):757-63 PMID: 3616572
  14. Matrix assembly sites for exogenous fibronectin are decreased on human fibroblasts after treatment with agents which increase intracellular cAMP.
    J Biol Chem. 1987 Oct 15;262(29):14361-5 PMID: 2821002
  15. Factor XIII cross-linking of fibronectin at cellular matrix assembly sites.
    J Biol Chem. 1988 Jul 25;263(21):10464-9 PMID: 2899077
  16. Extracellular matrix assembly of cell-derived and plasma-derived fibronectins by substrate-attached fibroblasts.
    J Cell Physiol. 1988 Jun;135(3):459-66 PMID: 3294235
  17. Transforming growth factor beta increases cell surface binding and assembly of exogenous (plasma) fibronectin by normal human fibroblasts.
    Mol Cell Biol. 1988 Oct;8(10):4234-42 PMID: 3054513
  18. Assembly of phospholipids into cellular membranes: biosynthesis, transmembrane movement and intracellular translocation.
    Annu Rev Cell Biol. 1988;4:579-610 PMID: 3058167
  19. Identification of the molecular species of lysophosphatidic acid produced when platelets are stimulated by thrombin.
    Biochim Biophys Acta. 1989 Feb 20;1001(3):282-5 PMID: 2917152
  20. Factor XIIIa-mediated cross-linking of fibronectin in fibroblast cell layers. Cross-linking of cellular and plasma fibronectin and of amino-terminal fibronectin fragments.
    J Biol Chem. 1989 Mar 5;264(7):4179-85 PMID: 2917995
  21. Analysis of fibronectin receptor function with monoclonal antibodies: roles in cell adhesion, migration, matrix assembly, and cytoskeletal organization.
    J Cell Biol. 1989 Aug;109(2):863-75 PMID: 2527241
  22. Distribution and movement of membrane-associated platelet glycoproteins: use of colloidal gold with correlative video-enhanced light microscopy, low-voltage high-resolution scanning electron microscopy, and high-voltage transmission electron microscopy.
    Am J Anat. 1989 Jun-Jul;185(2-3):149-64 PMID: 2773810
  23. Lysophosphatidate-induced cell proliferation: identification and dissection of signaling pathways mediated by G proteins.
    Cell. 1989 Oct 6;59(1):45-54 PMID: 2551506
  24. Signaling through phosphatidylcholine breakdown.
    J Biol Chem. 1990 Jan 5;265(1):1-4 PMID: 2104616
  25. Temporal relationships of F-actin bundle formation, collagen and fibronectin matrix assembly, and fibronectin receptor expression to wound contraction.
    J Cell Biol. 1990 Jan;110(1):133-45 PMID: 2136860
  26. Elevated levels of the alpha 5 beta 1 fibronectin receptor suppress the transformed phenotype of Chinese hamster ovary cells.
    Cell. 1990 Mar 9;60(5):849-59 PMID: 2155708
  27. Fibronectin levels are enhanced in human fibroblasts overexpressing the c-sis protooncogene.
    J Biol Chem. 1990 Mar 25;265(9):5219-25 PMID: 2180962
  28. Co-assembly of plasma and cellular fibronectins into fibrils in human fibroblast cultures.
    J Cell Biol. 1990 Jul;111(1):249-56 PMID: 2114411
  29. Lysophosphatidic acid, but not phosphatidic acid, is a potent Ca2(+)-mobilizing stimulus for fibroblasts. Evidence for an extracellular site of action.
    J Biol Chem. 1990 Jul 25;265(21):12232-9 PMID: 2373690
  30. Inhibition of binding of fibronectin to matrix assembly sites by anti-integrin (alpha 5 beta 1) antibodies.
    J Cell Biol. 1990 Aug;111(2):699-708 PMID: 2380248
  31. Platelet-activating factor.
    J Biol Chem. 1990 Oct 15;265(29):17381-4 PMID: 2170377
  32. Role of the I-9 and III-1 modules of fibronectin in formation of an extracellular fibronectin matrix.
    J Biol Chem. 1991 Jun 15;266(17):10851-8 PMID: 1710215
  33. Mechanisms for organization of fibronectin matrix.
    Cell Differ Dev. 1990 Dec 2;32(3):439-50 PMID: 2151569
  34. Lysophosphatidic acid induces inward currents in Xenopus laevis oocytes; evidence for an extracellular site of action.
    Eur J Pharmacol. 1992 Mar 24;213(2):313-5 PMID: 1521564
  35. Lipoproteins enhance fibronectin binding to adherent cells.
    Arterioscler Thromb. 1992 Oct;12(10):1122-30 PMID: 1390584
  36. Regulation of morphology by rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI) in Swiss 3T3 cells.
    J Biol Chem. 1993 Jan 5;268(1):510-5 PMID: 8416955
  37. Pertussis toxin-sensitive activation of p21ras by G protein-coupled receptor agonists in fibroblasts.
    Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1257-61 PMID: 7679495
  38. The bioactive phospholipid lysophosphatidic acid is released from activated platelets.
    Biochem J. 1993 May 1;291 ( Pt 3):677-80 PMID: 8489494
  39. Surface distribution of LETS protein in relation to the cytoskeleton of normal and transformed cells.
    J Cell Biol. 1977 Dec;75(3):743-68 PMID: 925079
  40. Thrombin stimulates the production and release of a major surface-associated glycoprotein (fibronectin) in cultures of human fibroblasts.
    Exp Cell Res. 1978 Mar 15;112(2):323-34 PMID: 75807
  41. Stimulatory effect of lysophosphatidic acids on uterine smooth muscles of non-pregant rats.
    Arch Int Pharmacodyn Ther. 1980 May;245(1):74-83 PMID: 6902643
  42. Effect of collagen and cell shape on binding of fibronectin to cells.
    Arch Biochem Biophys. 1981 Jan;206(1):205-12 PMID: 7194018
  43. Phospholipase A2 activity specific for phosphatidic acid. A possible mechanism for the production of arachidonic acid in platelets.
    J Biol Chem. 1981 Jun 10;256(11):5399-403 PMID: 7240145
  44. Lysophosphatidic acid induces neuronal shape changes via a novel, receptor-mediated signaling pathway: similarity to thrombin action.
    Cell Growth Differ. 1993 Apr;4(4):247-55 PMID: 7684247
  45. Lysophosphatidic acid stimulates mitogen-activated protein kinase activation via a G-protein-coupled pathway requiring p21ras and p74raf-1.
    J Biol Chem. 1993 Oct 5;268(28):20717-20 PMID: 8407893
  46. The alpha 5 beta 1 integrin fibronectin receptor, but not the alpha 5 cytoplasmic domain, functions in an early and essential step in fibronectin matrix assembly.
    J Biol Chem. 1993 Oct 15;268(29):21883-8 PMID: 7691819
  47. Lysophosphatidic acid enhances fibronectin binding to adherent cells.
    Arterioscler Thromb. 1993 Nov;13(11):1662-7 PMID: 8218108
  48. Protein kinase C modulation of fibronectin matrix assembly.
    J Biol Chem. 1993 Oct 25;268(30):22277-80 PMID: 8226736
  49. ADP-ribosylation of rho p21 inhibits lysophosphatidic acid-induced protein tyrosine phosphorylation and phosphatidylinositol 3-kinase activation in cultured Swiss 3T3 cells.
    J Biol Chem. 1993 Nov 25;268(33):24535-8 PMID: 8227009
  50. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin.
    Development. 1993 Dec;119(4):1079-91 PMID: 8306876
  51. Embryonic mesodermal defects in alpha 5 integrin-deficient mice.
    Development. 1993 Dec;119(4):1093-105 PMID: 7508365
  52. Fibroblasts, myofibroblasts, and wound contraction.
    J Cell Biol. 1994 Feb;124(4):401-4 PMID: 8106541
  53. Superfibronectin is a functionally distinct form of fibronectin.
    Nature. 1994 Jan 13;367(6459):193-6 PMID: 8114919
  54. A candidate molecule for the matrix assembly receptor to the N-terminal 29-kDa fragment of fibronectin in chick myoblasts.
    J Biol Chem. 1994 Mar 11;269(10):7651-7 PMID: 8125991
  55. Lysophosphatidic acid stimulates tyrosine phosphorylation of focal adhesion kinase, paxillin, and p130. Signaling pathways and cross-talk with platelet-derived growth factor.
    J Biol Chem. 1994 Mar 25;269(12):9345-51 PMID: 7510708
  56. Integrin cytoplasmic domains mediate inside-out signal transduction.
    J Cell Biol. 1994 Mar;124(6):1047-59 PMID: 7510712
  57. Assembly of amino-terminal fibronectin dimers into the extracellular matrix.
    J Biol Chem. 1994 Jun 24;269(25):17192-8 PMID: 8006027
  58. Fibronectin's III-1 module contains a conformation-dependent binding site for the amino-terminal region of fibronectin.
    J Biol Chem. 1994 Jul 22;269(29):19183-7 PMID: 8034677
  59. Substrate-specific binding of the amino terminus of fibronectin to an integrin complex in focal adhesions.
    J Biol Chem. 1994 Jul 29;269(30):19646-52 PMID: 7518462
  60. Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho.
    J Cell Biol. 1994 Aug;126(3):801-10 PMID: 8045941
  61. Protein measurement with the Folin phenol reagent.
    J Biol Chem. 1951 Nov;193(1):265-75 PMID: 14907713
  62. The phosphatidylinositol cycle and the regulation of arachidonic acid production.
    Nature. 1981 Jul 23;292(5821):367-9 PMID: 6265791
  63. Association of fibronectin and vinculin with focal contacts and stress fibers in stationary hamster fibroblasts.
    J Cell Biol. 1982 Feb;92(2):398-408 PMID: 6801062
  64. Are lysophosphatidic acids or phosphatidic acids involved in stimulus activation coupling in platelets?
    Blood. 1982 Sep;60(3):642-9 PMID: 6921047
  65. Five type I modules of fibronectin form a functional unit that binds to fibroblasts and Staphylococcus aureus.
    J Biol Chem. 1991 Jul 15;266(20):12840-3 PMID: 1677003
  66. Characterization of a human cDNA that encodes a functional receptor for platelet activating factor.
    Biochem Biophys Res Commun. 1991 Oct 15;180(1):105-11 PMID: 1656963
  67. Molecular cloning and expression of platelet-activating factor receptor from human leukocytes.
    J Biol Chem. 1991 Oct 25;266(30):20400-5 PMID: 1657923
  68. Isolation of an amino-terminal fibronectin-binding protein on human U937 cells and rat peritoneal macrophages.
    J Biol Chem. 1992 Feb 25;267(6):3968-75 PMID: 1531479
  69. Arrangement of cellular fibronectin in noncollagenous fibrils in human fibroblast cultures.
    J Cell Sci. 1991 Nov;100 ( Pt 3):605-12 PMID: 1808208
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1994-12-00
Pages
1447-59
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120255
Subset
IM
Grants
NIGMS NIH HHS · GM-47221 · United States
NHLBI NIH HHS · HL-21644 · United States
Analysis Services
Analysis Services

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