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PMID: 10725328 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The small GTPase, Rap1, mediates CD31-induced integrin adhesion.

The Journal of cell biology ·Vol. 148 ·No. 6 ·2000-03-20 ·Pages 1151-8

Reedquist KA, Ross E, Koop EA, Wolthuis RM, Zwartkruis FJ, van Kooyk Y, Salmon M, Buckley CD, Bos JL

Abstract

Integrin-mediated leukocyte adhesion is a critical aspect of leukocyte function that is tightly regulated by diverse stimuli, including chemokines, antigen receptors, and adhesion receptors. How cellular signals from CD31 and other adhesion amplifiers are integrated with those from classical mitogenic stimuli to regulate leukocyte function remains poorly understood. Here, we show that the cytoplasmic tail of CD31, an important integrin adhesion amplifier, propagates signals that induce T cell adhesion via beta1 (VLA-4) and beta2 (LFA-1) integrins. We identify the small GTPase, Rap1, as a critical mediator of this effect. Importantly, CD31 selectively activated the small Ras-related GTPase, Rap1, but not Ras, R-Ras, or Rap2. An activated Rap1 mutant stimulated T lymphocyte adhesion to intercellular adhesion molecule (ICAM) and vascular cell adhesion molecule (VCAM), as did the Rap1 guanine nucleotide exchange factor C3G and a catalytically inactive mutant of RapGAP. Conversely, negative regulators of Rap1 signaling blocked CD31-dependent adhesion. These findings identify a novel important role for Rap1 in regulating ligand-induced cell adhesion and suggest that Rap1 may play a more general role in coordinating adhesion-dependent signals during leukocyte migration and extravasation. Our findings also suggest an alternative mechanism, distinct from interference with Ras-proximal signaling, by which Rap1 might mediate transformation reversion.

MeSH Terms
Antigens, CD/physiology Cell Adhesion/physiology Cell Adhesion Molecules/metabolism Humans Integrin alpha4beta1 Integrins/physiology Jurkat Cells Lymphocyte Function-Associated Antigen-1/physiology Platelet Endothelial Cell Adhesion Molecule-1/chemistry,physiology Receptors, Lymphocyte Homing/physiology Recombinant Fusion Proteins/metabolism Signal Transduction T-Lymphocytes/physiology Transfection Vascular Cell Adhesion Molecule-1/metabolism rap1 GTP-Binding Proteins/metabolism
Chemicals
Antigens, CD Cell Adhesion Molecules Integrin alpha4beta1 Integrins Lymphocyte Function-Associated Antigen-1 Platelet Endothelial Cell Adhesion Molecule-1 Receptors, Lymphocyte Homing Recombinant Fusion Proteins Vascular Cell Adhesion Molecule-1 rap1 GTP-Binding Proteins
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Reedquist K A
Laboratory for Physiological Chemistry, Centre for Biomedical Genetics, Utrecht University Medical Center, Universiteitsweg 100, 3584 CG, Utrecht, The Netherlands.
Ross E
Koop E A
Wolthuis R M
Zwartkruis F J
van Kooyk Y
Salmon M
Buckley C D
Bos J L
References (39)
39 references, click to expand
  1. A ras-related gene with transformation suppressor activity.
    Cell. 1989 Jan 13;56(1):77-84 PMID: 2642744
  2. A novel role for H-Ras in the regulation of very late antigen-4 integrin and VCAM-1 via c-Myc-dependent and -independent mechanisms.
    J Immunol. 1999 Nov 1;163(9):4901-8 PMID: 10528192
  3. Molecular cloning of a GTPase activating protein specific for the Krev-1 protein p21rap1.
    Cell. 1991 Jun 14;65(6):1033-42 PMID: 1904317
  4. Two dominant inhibitory mutants of p21ras interfere with insulin-induced gene expression.
    Mol Cell Biol. 1991 Dec;11(12):5963-7 PMID: 1658621
  5. Adhesion of T and B lymphocytes to extracellular matrix and endothelial cells can be regulated through the beta subunit of VLA.
    J Cell Biol. 1992 Apr;117(2):461-70 PMID: 1560035
  6. CD31 expressed on distinctive T cell subsets is a preferential amplifier of beta 1 integrin-mediated adhesion.
    J Exp Med. 1992 Jul 1;176(1):245-53 PMID: 1377224
  7. GTPase-activating protein SH2-SH3 domains induce gene expression in a Ras-dependent fashion.
    Mol Cell Biol. 1992 Aug;12(8):3425-30 PMID: 1321335
  8. Ligand intercellular adhesion molecule 1 has a necessary role in activation of integrin lymphocyte function-associated molecule 1.
    Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5838-42 PMID: 7685913
  9. H-Ras signals to cytoskeletal machinery in induction of integrin-mediated adhesion of T cells.
    J Immunol. 1999 Dec 1;163(11):6209-16 PMID: 10570313
  10. Interaction of the low-molecular-weight GTP-binding protein rap2 with the platelet cytoskeleton is mediated by direct binding to the actin filaments.
    J Cell Biochem. 1999 Dec 15;75(4):675-85 PMID: 10572250
  11. KIM185, a monoclonal antibody to CD18 which induces a change in the conformation of CD18 and promotes both LFA-1- and CR3-dependent adhesion.
    Eur J Immunol. 1993 Sep;23(9):2217-22 PMID: 7690325
  12. C3G, a guanine nucleotide-releasing protein expressed ubiquitously, binds to the Src homology 3 domains of CRK and GRB2/ASH proteins.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3443-7 PMID: 7512734
  13. Ligation of platelet/endothelial cell adhesion molecule 1 (PECAM-1/CD31) on monocytes and neutrophils increases binding capacity of leukocyte CR3 (CD11b/CD18).
    J Immunol. 1995 Jan 1;154(1):299-307 PMID: 7995949
  14. Localization of multiple functional domains on human PECAM-1 (CD31) by monoclonal antibody epitope mapping.
    Cell Adhes Commun. 1995 Feb;3(1):45-66 PMID: 7538415
  15. Roles of platelet/endothelial cell adhesion molecule-1 (PECAM-1, CD31) in natural killer cell transendothelial migration and beta 2 integrin activation.
    J Immunol. 1996 Feb 15;156(4):1515-24 PMID: 8568255
  16. Integrin activation by R-ras.
    Cell. 1996 Apr 5;85(1):61-9 PMID: 8620538
  17. Regulation of leukocyte integrin function: affinity vs. avidity.
    J Cell Biochem. 1996 Jun 15;61(4):554-61 PMID: 8806078
  18. Minimal Ras-binding domain of Raf1 can be used as an activation-specific probe for Ras.
    Oncogene. 1997 Feb 6;14(5):623-5 PMID: 9053862
  19. Rapid Ca2+-mediated activation of Rap1 in human platelets.
    EMBO J. 1997 Jan 15;16(2):252-9 PMID: 9029146
  20. Cross-talk between cell adhesion molecules regulates the migration velocity of neutrophils.
    Curr Biol. 1997 May 1;7(5):316-25 PMID: 9115397
  21. Residues on both faces of the first immunoglobulin fold contribute to homophilic binding sites of PECAM-1/CD31.
    J Biol Chem. 1997 Aug 15;272(33):20555-63 PMID: 9252369
  22. Biochemical characterization of C3G: an exchange factor that discriminates between Rap1 and Rap2 and is not inhibited by Rap1A(S17N).
    Oncogene. 1997 Aug 14;15(7):845-50 PMID: 9266971
  23. Association of Krev-1/rap1a with Krit1, a novel ankyrin repeat-containing protein encoded by a gene mapping to 7q21-22.
    Oncogene. 1997 Aug 28;15(9):1043-9 PMID: 9285558
  24. Characterization of phosphotyrosine binding motifs in the cytoplasmic domain of platelet/endothelial cell adhesion molecule-1 (PECAM-1) that are required for the cellular association and activation of the protein-tyrosine phosphatase, SHP-2.
    J Biol Chem. 1997 Oct 3;272(40):24868-75 PMID: 9312087
  25. Human SPA-1 gene product selectively expressed in lymphoid tissues is a specific GTPase-activating protein for Rap1 and Rap2. Segregate expression profiles from a rap1GAP gene product.
    J Biol Chem. 1997 Oct 31;272(44):28081-8 PMID: 9346962
  26. Ras-like GTPases.
    Biochim Biophys Acta. 1997 Oct 24;1333(2):M19-31 PMID: 9395281
  27. The biology of PECAM-1.
    J Clin Invest. 1997 Dec 1;100(11 Suppl):S25-9 PMID: 9413397
  28. Costimulation through CD28 suppresses T cell receptor-dependent activation of the Ras-like small GTPase Rap1 in human T lymphocytes.
    J Biol Chem. 1998 Feb 27;273(9):4944-9 PMID: 9478939
  29. Extracellular signal-regulated activation of Rap1 fails to interfere in Ras effector signalling.
    EMBO J. 1998 Oct 15;17(20):5905-12 PMID: 9774335
  30. Integrin associated proteins.
    Curr Opin Cell Biol. 1998 Oct;10(5):578-85 PMID: 9818167
  31. A role for p21ras/MAP kinase in TCR-mediated activation of LFA-1.
    J Immunol. 1998 Dec 1;161(11):5800-3 PMID: 9834054
  32. All in the family? New insights and questions regarding interconnectivity of Ras, Rap1 and Ral.
    EMBO J. 1998 Dec 1;17(23):6776-82 PMID: 9843482
  33. H-Ras is involved in the inside-out signaling pathway of interleukin-3-induced integrin activation.
    Blood. 1999 Mar 1;93(5):1540-8 PMID: 10029582
  34. Genetic evidence for functional redundancy of Platelet/Endothelial cell adhesion molecule-1 (PECAM-1): CD31-deficient mice reveal PECAM-1-dependent and PECAM-1-independent functions.
    J Immunol. 1999 Mar 1;162(5):3022-30 PMID: 10072554
  35. Thermodynamic and kinetic characterization of the interaction between the Ras binding domain of AF6 and members of the Ras subfamily.
    J Biol Chem. 1999 May 7;274(19):13556-62 PMID: 10224125
  36. CrkL activates integrin-mediated hematopoietic cell adhesion through the guanine nucleotide exchange factor C3G.
    Blood. 1999 Jun 1;93(11):3713-22 PMID: 10339478
  37. Differential association of cytoplasmic signalling molecules SHP-1, SHP-2, SHIP and phospholipase C-gamma1 with PECAM-1/CD31.
    FEBS Lett. 1999 Apr 30;450(1-2):77-83 PMID: 10350061
  38. Rap1 GTPase-activating protein SPA-1 negatively regulates cell adhesion.
    J Biol Chem. 1999 Jun 25;274(26):18463-9 PMID: 10373454
  39. Regulated expression of Mg2+ binding epitope on leukocyte integrin alpha subunits.
    EMBO J. 1989 Dec 1;8(12):3759-65 PMID: 2479549
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
2000-03-20
Pages
1151-8
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2174316
Subset
IM
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