Home LiteratureArticle Details
PMID: 17591693 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

WAVE2 regulates high-affinity integrin binding by recruiting vinculin and talin to the immunological synapse.

Molecular and cellular biology ·Vol. 27 ·No. 17 ·2007-09-00 ·Pages 5986-6000

Nolz JC, Medeiros RB, Mitchell JS, Zhu P, Freedman BD, Shimizu Y, Billadeau DD

Abstract

T-cell-receptor (TCR)-mediated integrin activation is required for T-cell-antigen-presenting cell conjugation and adhesion to extracellular matrix components. While it has been demonstrated that the actin cytoskeleton and its regulators play an essential role in this process, no mechanism has been established which directly links TCR-induced actin polymerization to the activation of integrins. Here, we demonstrate that TCR stimulation results in WAVE2-ARP2/3-dependent F-actin nucleation and the formation of a complex containing WAVE2, ARP2/3, vinculin, and talin. The verprolin-connecting-acidic (VCA) domain of WAVE2 mediates the formation of the ARP2/3-vinculin-talin signaling complex and talin recruitment to the immunological synapse (IS). Interestingly, although vinculin is not required for F-actin or integrin accumulation at the IS, it is required for the recruitment of talin. In addition, RNA interference of either WAVE2 or vinculin inhibits activation-dependent induction of high-affinity integrin binding to VCAM-1. Overall, these findings demonstrate a mechanism in which signals from the TCR produce WAVE2-ARP2/3-mediated de novo actin polymerization, leading to integrin clustering and high-affinity binding through the recruitment of vinculin and talin.

MeSH Terms
Actin-Related Protein 2-3 Complex/genetics,metabolism Actins/metabolism CD18 Antigens/genetics,metabolism Calcium/metabolism Cell Line Cytoskeleton/metabolism Humans Immune System/physiology Integrin beta1/genetics,metabolism Jurkat Cells Lymphocyte Function-Associated Antigen-1/metabolism Multiprotein Complexes Protein Structure, Tertiary Proto-Oncogene Proteins c-vav/metabolism Receptors, Antigen, T-Cell/genetics,metabolism Signal Transduction/physiology Talin/metabolism Vinculin/metabolism Wiskott-Aldrich Syndrome Protein Family/genetics,metabolism cdc42 GTP-Binding Protein/metabolism rac1 GTP-Binding Protein/metabolism
Chemicals
Actin-Related Protein 2-3 Complex Actins CD18 Antigens Integrin beta1 Lymphocyte Function-Associated Antigen-1 Multiprotein Complexes Proto-Oncogene Proteins c-vav Receptors, Antigen, T-Cell Talin VAV1 protein, human WASF2 protein, human Wiskott-Aldrich Syndrome Protein Family Vinculin cdc42 GTP-Binding Protein rac1 GTP-Binding Protein Calcium
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Nolz Jeffrey C
Department of Immunology and Division of Oncology Research, Mayo Clinic College of Medicine, 200 First Street SW, Rochester, MN 55905, USA.
Medeiros Ricardo B
Mitchell Jason S
Zhu Peimin
Freedman Bruce D
Shimizu Yoji
Billadeau Daniel D
References (48)
48 references, click to expand
  1. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1.
    Nature. 1989 Oct 19;341(6243):619-24 PMID: 2477710
  2. Formins regulate the actin-related protein 2/3 complex-independent polarization of the centrosome to the immunological synapse.
    Immunity. 2007 Feb;26(2):177-90 PMID: 17306570
  3. Differential activation-dependent regulation of integrin function in cultured human T-leukemic cell lines.
    Blood. 1994 Feb 15;83(4):1039-50 PMID: 7906564
  4. The duration of antigenic stimulation determines the fate of naive and effector T cells.
    Immunity. 1998 Jan;8(1):89-95 PMID: 9462514
  5. Defects in actin-cap formation in Vav-deficient mice implicate an actin requirement for lymphocyte signal transduction.
    Curr Biol. 1998 May 7;8(10):563-72 PMID: 9601640
  6. Phosphorylation of WAVE downstream of mitogen-activated protein kinase signaling.
    J Biol Chem. 1999 Sep 24;274(39):27605-9 PMID: 10488099
  7. The Talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation.
    J Biol Chem. 1999 Oct 1;274(40):28071-4 PMID: 10497155
  8. Dynamin 2 regulates T cell activation by controlling actin polymerization at the immunological synapse.
    Nat Immunol. 2005 Mar;6(3):261-70 PMID: 15696170
  9. Vav-family proteins in T-cell signalling.
    Curr Opin Immunol. 2005 Jun;17(3):267-74 PMID: 15886116
  10. Regulation of beta 1 integrin-mediated adhesion by T cell receptor signaling involves ZAP-70 but differs from signaling events that regulate transcriptional activity.
    J Immunol. 2000 Nov 1;165(9):4941-9 PMID: 11046020
  11. IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling.
    Nature. 2000 Dec 7;408(6813):732-5 PMID: 11130076
  12. A novel function for the Tec family tyrosine kinase Itk in activation of beta 1 integrins by the T-cell receptor.
    EMBO J. 2001 Mar 15;20(6):1232-44 PMID: 11250890
  13. Chemoattractants induce a rapid and transient upregulation of monocyte alpha4 integrin affinity for vascular cell adhesion molecule 1 which mediates arrest: an early step in the process of emigration.
    J Exp Med. 2001 May 21;193(10):1149-58 PMID: 11369786
  14. Wasp recruitment to the T cell:APC contact site occurs independently of Cdc42 activation.
    Immunity. 2001 Aug;15(2):249-59 PMID: 11520460
  15. Positive regulation of T cell activation and integrin adhesion by the adapter Fyb/Slap.
    Science. 2001 Sep 21;293(5538):2260-3 PMID: 11567140
  16. Coupling of the TCR to integrin activation by Slap-130/Fyb.
    Science. 2001 Sep 21;293(5538):2263-5 PMID: 11567141
  17. Superantigen-induced T cell:B cell conjugation is mediated by LFA-1 and requires signaling through Lck, but not ZAP-70.
    J Immunol. 2001 Nov 15;167(10):5708-18 PMID: 11698443
  18. The intersectin 2 adaptor links Wiskott Aldrich Syndrome protein (WASp)-mediated actin polymerization to T cell antigen receptor endocytosis.
    J Exp Med. 2001 Dec 17;194(12):1777-87 PMID: 11748279
  19. Rap1A positively regulates T cells via integrin activation rather than inhibiting lymphocyte signaling.
    Nat Immunol. 2002 Mar;3(3):251-8 PMID: 11836528
  20. Vav1 controls integrin clustering and MHC/peptide-specific cell adhesion to antigen-presenting cells.
    Immunity. 2002 Mar;16(3):331-43 PMID: 11911819
  21. Pleiotropic defects in TCR signaling in a Vav-1-null Jurkat T-cell line.
    EMBO J. 2002 Sep 16;21(18):4809-19 PMID: 12234921
  22. Modulation of Kv channel expression and function by TCR and costimulatory signals during peripheral CD4(+) lymphocyte differentiation.
    J Exp Med. 2002 Oct 7;196(7):897-909 PMID: 12370252
  23. Recruitment of the Arp2/3 complex to vinculin: coupling membrane protrusion to matrix adhesion.
    J Cell Biol. 2002 Dec 9;159(5):881-91 PMID: 12473693
  24. RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1.
    Nat Immunol. 2003 Aug;4(8):741-8 PMID: 12845325
  25. Talin binding to integrin beta tails: a final common step in integrin activation.
    Science. 2003 Oct 3;302(5642):103-6 PMID: 14526080
  26. Actin cytoskeleton regulates calcium dynamics and NFAT nuclear duration.
    Mol Cell Biol. 2004 Feb;24(4):1628-39 PMID: 14749378
  27. Rap1-mediated lymphocyte function-associated antigen-1 activation by the T cell antigen receptor is dependent on phospholipase C-gamma1.
    J Biol Chem. 2004 Mar 19;279(12):11875-81 PMID: 14702343
  28. Role of the cytoskeleton during leukocyte responses.
    Nat Rev Immunol. 2004 Feb;4(2):110-22 PMID: 15040584
  29. Purification and architecture of the ubiquitous Wave complex.
    Proc Natl Acad Sci U S A. 2004 Mar 30;101(13):4379-83 PMID: 15070726
  30. Control of TCR-mediated activation of beta 1 integrins by the ZAP-70 tyrosine kinase interdomain B region and the linker for activation of T cells adapter protein.
    J Immunol. 2004 May 1;172(9):5379-87 PMID: 15100278
  31. PtdIns(3,4,5)P3 binding is necessary for WAVE2-induced formation of lamellipodia.
    Nat Cell Biol. 2004 May;6(5):420-6 PMID: 15107862
  32. Differential roles for Wiskott-Aldrich syndrome protein in immune synapse formation and IL-2 production.
    J Immunol. 2004 Aug 1;173(3):1658-62 PMID: 15265894
  33. VLA-4 integrin concentrates at the peripheral supramolecular activation complex of the immune synapse and drives T helper 1 responses.
    Proc Natl Acad Sci U S A. 2004 Jul 27;101(30):11058-63 PMID: 15263094
  34. The talin-tail interaction places integrin activation on FERM ground.
    Trends Biochem Sci. 2004 Aug;29(8):429-35 PMID: 15362227
  35. Intracellular signalling controlling integrin activation in lymphocytes.
    Nat Rev Immunol. 2005 Jul;5(7):546-59 PMID: 15965491
  36. The c-SMAC: sorting it all out (or in).
    J Cell Biol. 2005 Jul 18;170(2):177-82 PMID: 16009722
  37. Protein kinase D1 and the beta 1 integrin cytoplasmic domain control beta 1 integrin function via regulation of Rap1 activation.
    Immunity. 2005 Aug;23(2):213-26 PMID: 16111639
  38. Tec kinases regulate TCR-mediated recruitment of signaling molecules and integrin-dependent cell adhesion.
    J Immunol. 2005 Nov 1;175(9):5923-30 PMID: 16237085
  39. Lymphocyte calcium signaling from membrane to nucleus.
    Nat Immunol. 2006 Jan;7(1):25-32 PMID: 16357855
  40. Rap1A-deficient T and B cells show impaired integrin-mediated cell adhesion.
    Mol Cell Biol. 2006 Jan;26(2):643-53 PMID: 16382154
  41. The WAVE2 complex regulates actin cytoskeletal reorganization and CRAC-mediated calcium entry during T cell activation.
    Curr Biol. 2006 Jan 10;16(1):24-34 PMID: 16401421
  42. Contrasting roles for domain 4 of VCAM-1 in the regulation of cell adhesion and soluble VCAM-1 binding to integrin alpha4beta1.
    J Immunol. 2006 Apr 15;176(8):5041-9 PMID: 16585601
  43. HS1 functions as an essential actin-regulatory adaptor protein at the immune synapse.
    Immunity. 2006 Jun;24(6):741-52 PMID: 16782030
  44. Spatiotemporal regulation of the kinase Mst1 by binding protein RAPL is critical for lymphocyte polarity and adhesion.
    Nat Immunol. 2006 Sep;7(9):919-28 PMID: 16892067
  45. The structure and regulation of vinculin.
    Trends Cell Biol. 2006 Sep;16(9):453-60 PMID: 16893648
  46. Talin1 regulates TCR-mediated LFA-1 function.
    J Immunol. 2006 Dec 1;177(11):7707-14 PMID: 17114441
  47. CD14 is a ligand for the integrin alpha4beta1.
    FEBS Lett. 2007 Feb 20;581(4):757-63 PMID: 17274987
  48. Regulated expression and binding of three VLA (beta 1) integrin receptors on T cells.
    Nature. 1990 May 17;345(6272):250-3 PMID: 2139716
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2007-09-00
Epub
2007-00-25
Pages
5986-6000
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC1952166
Subset
IM
Grants
NIAID NIH HHS · R01-AI065474 · United States
NIAID NIH HHS · R01-AI038474 · United States
NIAID NIH HHS · R01 AI065474 · United States
NIAID NIH HHS · T32-AI07425 · United States
NCI NIH HHS · T32-CA009138 · United States
NCI NIH HHS · T32 CA009138 · United States
NIAID NIH HHS · R01-AI031126 · United States
NIAID NIH HHS · R01-AI060921 · United States
NIAID NIH HHS · T32 AI007425 · United States
NIAID NIH HHS · R01 AI031126 · United States
NIAID NIH HHS · R01 AI060921 · United States
NIAID NIH HHS · R01 AI038474 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com