Clustering T-cell GM1 lipid rafts increases cellular resistance to shear on fibronectin through changes in integrin affinity and cytoskeletal dynamics

Immunology and Cell Biology

Volumn 87, Issue 4, 2009, Pages 324-336

  Mitchell, Jason S ^a   Brown, Wells S ^a   Woodside, Darren G ^b   Vanderslice, Peter ^b   McIntyre, Bradley W ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b TEXAS HEART INSTITUTE   (United States)

Author keywords

Adhesion molecules; Cell trafficking; Human; Inflammation; T cells

Indexed keywords

CD59 ANTIGEN; F ACTIN; FIBRONECTIN; GANGLIOSIDE GM1; VERY LATE ACTIVATION ANTIGEN 4; VERY LATE ACTIVATION ANTIGEN 5; INTEGRIN; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; CYTOSKELETON; HUMAN; HUMAN CELL; INFLAMMATION; LEUKEMIA CELL LINE; LIPID RAFT; PROTEIN AGGREGATION; PROTEIN LIPID INTERACTION; T LYMPHOCYTE; CELL MEMBRANE; CHEMOTAXIS; IMMUNOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CELL ADHESION; CELL LINE, TUMOR; CHEMOTAXIS; CYTOSKELETON; FIBRONECTINS; G(M1) GANGLIOSIDE; HUMANS; INTEGRINS; JURKAT CELLS; MEMBRANE MICRODOMAINS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; VASCULAR CELL ADHESION MOLECULE-1;

EID: 67449099930     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2008.103     Document Type: Article

References (58)

1. Grabovsky V, Feigelson S, Chen C, Bleijs DA, Peled A, Cinamon G et al. Subsecond induction of alpha4 integrin clustering by immobilized chemokines stimulates leukocyte tethering and rolling on endothelial vascular cell adhesion molecule 1 under flow conditions. J Exp Med 2000; 192: 495-506.
2. Feigelson SW, Grabovsky V, Winter E, Chen LL, Pepinsky RB, Yednock T et al. The Src kinase p56(lck) up-regulates VLA-4 integrin affinity. Implications for rapid spontaneous and chemokine-triggered T cell adhesion to VCAM-1 and fibronectin. J Biol Chem 2001; 276: 13891-13901.
3. Laudanna C, Alon R. Right on the spot. Chemokine triggering of integrin-mediated arrest of rolling leukocytes. Thromb Haemost 2006; 95: 5-11.
4. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997; 387: 569-572.
5. Foger N, Marhaba R, Zoller M. Involvement of CD44 in cytoskeleton rearrangement and raft reorganization in T cells. J Cell Sci 2001; 114: 1169-1178.
6. Stulnig TM, Berger M, Sigmund T, Raederstorff D, Stockinger H, Waldhausl W. Polyunsaturated fatty acids inhibit T cell signal transduction by modification of detergent-insoluble membrane domains. JCell Biol 1998; 143: 637-644.
7. Brown DA, London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J BiolChem 2000; 275: 17221-17224.
8. Gomez-Mouton C, Abad JL, Mira E, Lacalle RA, Gallardo E, Jimenez-Baranda S et al. Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc Natl Acad Sci USA 2001; 98: 9642-9647.
9. van Heyningen S. The subunits of cholera toxin: structure, stoichiometry, and function. J InfectDis 1976; 133 (Suppl): 5-13.
10. Janes PW, Ley SC, Magee AI. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J Cell Biol 1999; 147: 447-461.
11. Viola A, Schroeder S, Sakakibara Y, Lanzavecchia A. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 1999; 283: 680-682.
12. Mitchell JS, Kanca O, Mclntyre BW. Lipid microdomain clustering induces a redistribution of antigen recognition and adhesion molecules on human T lymphocytes. J Immunol 2002; 168: 2737-2744.
13. Krauss K, Altevogt P. Integrin leukocyte function-associated antigen-1-mediated cell binding can be activated by clustering of membrane rafts. J BiolChem 1999; 274: 36921-36927.
14. Bazzoni G, Hemler ME. Are changes in integrin affinity and conformation overemphasized? Trends Biochem Sci 1998; 23:30-34.
15. Carman CV, Springer TA. Integrin avidity regulation: are changes in affinity and conformation underemphasized? Curr Opin Cell Bio! 2003; 15: 547-556.
16. Liu L, Schwartz BR, Tupper J, Lin N, Winn RK, Harlan JM. TheGTPase Rapl regulates phorbol 12-myristate 13-acetate-stimulated but not ligand-induced beta 1 integrin- dependent leukocyte adhesion. JBio! Chem 2002; 277: 40893-40900.
17. Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA 1999; 282: 2035-2042.
18. Bunnell SC, Kapoor V, Trible RP, Zhang W, Samelson LE. Dynamic actin polymerization drives Tcell receptor-induced spreading: a role for the signal transduction adaptor LAT. Immunity 2001; 14: 315-329.
19. Dustin ML. Stop and go traffic to tune Tcell responses. Immunity 2004; 21: 305-314.
20. Hyduk SJ, Cybulsky MI. Alpha 4 integrin signaling activates phosphatidylinositol 3-kinase and stimulates T cell adhesion to intercellular adhesion molecule-1 to a similar extent as CD3, but induces a distinct rearrangement of the actin cytoskeleton. J Immunol 2002; 168:696-704.
21. Frank RS. Time-dependent alterations in the deformability of human neutrophils in response to chemotactic activation. Blood 1990; 76: 2606-2612.
22. Smith A, Carrasco YR, Stanley P, Kieffer N, Batista FD, Hogg N. Atalin-dependent LFA- 1 focal zone is formed by rapidly migrating T lymphocytes. JCel! Bio! 2005; 170: 141-151.
23. Verschueren H. Interference reflection microscopy in cell biology: methodology and applications. J Cell Sci 1985; 75: 279-301.
24. Serrador JM, Nieto M, Sanchez-Madrid F. Cytoskeletal rearrangement during migration and activation of T lymphocytes. Trends Cell Biol 1999; 9: 228-233.
25. Peacock JW, Jirik FR. TCR activation inhibits chemotaxis toward stromal cell-derived factor-1: evidence for reciprocal regulation between CXCR4 and the TCR. JImmunol 1999; 162: 215-223.
26. Straus DB, Weiss A. Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell 1992; 70: 585-593.
27. Salas A, Shimaoka M, Phan U, Kim M, Springer TA. Transition from rolling to Arm adhesion can be mimicked by extension of integrin {alpha}Lbeta2 in an intermediate affinity state. J Biol Chem 2006; 281: 10876-10882.
28. Takagi J, Petre BM, Walz T, Springer TA. Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell2002; 110: 599-611.
29. Faull RJ, Kovach NL, Harlan JM, Ginsberg MH. Stimulation of integrin-mediated adhesion of T lymphocytes and monocytes: two mechanisms with divergent biological consequences. J Exp Med 1994; 179: 1307-1316.
30. Woods ML, Cabanas C, Shimizu Y. Activation-dependent changes in solublefibronectin binding and expression of beta1 integrin activation epitopes in T cells: relationship to Tcell adhesion and migration. Eur J Immunol 2000; 30:38-49.
31. Chan JR, Hyduk SJ, Cybulsky MI. 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 ExpMed 2001; 193: 1149-1158.
32. Chan JR, Hyduk SJ, Cybulsky MI. Detecting rapid and transient upregulation of leukocyte integrin affinity induced by chemokines and chemoattractants. JImmunol Methods 2003; 273:43-52.
33. Rose DM, Cardarelli PM, Cobb RR, Ginsberg MH. Soluble VCAM-1 binding to alpha4 integrins is cell-type specific and activation dependent and is disrupted during apoptosis in T cells. Blood 2000; 95:602-609.
34. Alon R, FeigelsonSW, Manevich E, Rose DM, SchmitzJ, Overby DR etal. Alpha4beta1- dependent adhesion strengthening under mechanical strain is regulated by paxillin association with the alpha4-cytoplasmic domain. JCellBiol 2005; 171 : 1073-1084.
35. Chan AS, Reynolds PJ, Shimizu Y. Tyrosine kinase activity associated with the CD7 antigen: correlation with regulation of T cell integrin function. Eur J Immunol 1994; 24: 2602-2608.
36. Chan JR, HydukSJ, Cybulsky MI. Alpha 4 beta 1 integrin/VCAM-1 interaction activates alpha L beta 2 integrin-mediated adhesion to ICAM-1 in human T cells. JImmunol 2000; 164: 746-753.
37. Kivens WJ, Hunt III SW, Mobley JL, Zell T, Dell CL, Bierer BE etal. Identification of a proline-rich sequence in the CD2 cytoplasmic domain critical for regulation of integrin- mediated adhesion and activation of phosphoinositide 3-kinase. Mol Cell Biol 1998; 18: 5291-5307.
38. Shimizu Y, Van Seventer GA, Horgan KJ, Shaw S. Regulated expression and binding of three VLA (beta 1) integrin receptors on T cells. Nature 1990; 345:250-253.
39. Zell T, Hunt III SW, Mobley JL, Finkelstein LD, Shimizu Y. CD28-mediated up-regulation of beta 1-integrin adhesion involves phosphatidylinositol 3-kinase. JImmunol 1996; 156: 883-886.
40. Chen C, Mobley JL, Dwir O, Shimron F, Grabovsky V, Lobb RR etal. High affinity very late antigen-4 subsets expressed on T cells are mandatory for spontaneous adhesion strengthening but not for rolling on VCAM-1 in shear flow. JImmunol 1999; 162: 1084-1095.
41. Boer J, Gottschling D, Schuster A, Semmrich M, Holzmann B, Kessler H. Design and synthesis of potent and selective alpha(4)beta(7) integrin antagonists. J Med Chem 2001; 44: 2586-2592.
42. Han J, Rose DM, Woodside DG, Goldfinger LE, Ginsberg MH. Integrin alpha 4 beta 1-dependent T cell migration requires both phosphorylation and dephosphorylation of the alpha 4 cytoplasmic domain to regulate the reversible binding of paxillin. J Biol Chem 2003; 278: 34845-34853.
43. Liu S, Thomas SM, Woodside DG, Rose DM, Kiosses WB, Pfaff M et al. Binding of paxillin to alpha4 integrins modifies integrin-dependent biological responses. Nature 1999; 402: 676-681.
44. Harder T, Simons K. Clusters of glycolipid and glycosylphosphatidylinositol-anchored proteins in lymphoid cells: accumulation of actin regulated bylocal tyrosine phosphor-ylation. Eur J Immunol 1999; 29: 556-562.
45. Shamri R, Grabovsky V, Feigelson SW, Dwir O, Van Kooyk Y, Alon R. Chemokine stimulation of lymphocyte alpha 4 integrin avidity but not of leukocyte function- associated antigen-1 avidity to endothelial ligands under shear flow requires cholesterol membrane rafts. J Biol Chem 2002; 277: 40027-40035.
46. Janes PW, Ley SC, Magee AI, Kabouridis PS. The role of lipid rafts in T cell antigen receptor (TCR) signalling. Semin Immunol 2000; 12:23-34.
47. Kniep B, Cinek T, Angelisova P, Horejsi V. Association of the GPI-anchored leucocyte surface glycoproteins with ganglioside GM3. Biochem Biophys Res Commun 1994; 203: 1069-1075.
48. Leitinger B, Hogg N. The involvement of lipid rafts in the regulation of integrin function. JCell Sci 2002; 115: 963-972.
49. Buensuceso C, deVirgilio M, Shattil SJ. Detection of integrin alpha IIbbeta 3 clustering in living cells. J BiolChem 2003; 278: 15217-15224.
50. Kim M, Carman CV, Yang W, Salas A, Springer TA. The primacy of affinity over clustering in regulation of adhesiveness of the integrin {alpha}L{beta}2. J CellBiol 2004; 167: 1241-1253.
51. Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B et al. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 2005; 437: 426-431.
52. Khan AA, Bose C, Yam LS, Soloski MJ, Rupp F. Physiological regulation of the immunological synapse by agrin. Science 2001; 292: 1681-1686.
53. Vicente-Manzanares M, Rey M, Perez-Martinez M, Yanez-Mo M, Sancho D, Cabrero JR et al. The RhoA effector mDia is induced during T cell activation and regulates actin polymerization and cell migration in T lymphocytes. JImmunol 2003; 171: 1023-1034.
54. Wooten DK, Teague TK, McIntyre BW. Separation of integrin-dependent adhesion from morphological changes based on differential PLC specificities. JLeukoc Biol 1999; 65:127-136.
55. McIntyre BW, Woodside DG, Caruso DA, Wooten DK, Simon SI, Neelamegham S et al. Regulation of human T lymphocyte coactivation with an alpha4 integrin antagonist peptide. JImmunol 1997; 158: 4180-4186.
56. Woodside DG, Kram RM, Mitchell JS, Belsom T, Billard MJ, McIntyre BW et al. Contrasting roles for domain 4 of VCAM-1 in the regulation of cell adhesion and soluble VCAM-1 binding to integrin alpha4beta1. JImmunol 2006; 176: 5041-5049.
57. Rose DM, Grabovsky V, Alon R, Ginsberg MH. The affinity of integrin alpha(4)beta(1) governs lymphocyte migration. JImmunol 2001; 167: 2824-2830.
58. McIntyre BW, Evans EL, Bednarczyk JL. Lymphocyte surface antigen L25 is a member of the integrin receptor superfamily. J Biol Chem 1989; 264: 13745-13750.