Adenosine diphosphate (ADP)-ribosylation of the guanosine triphosphatase (GTPase) Rho in resting peripheral blood human T lymphocytes results in pseudopodial extension and the inhibition of T cell activation

Journal of Experimental Medicine

Volumn 188, Issue 7, 1998, Pages 1211-1221

  Woodside, Darren G ^a,c   Wooten, David K ^a   McIntyre, Bradley W ^a,b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Cell adhesion; Cytoskeleton; Extracellular matrix; Integrins; Interleukin 2

Indexed keywords

ADENOSINE DIPHOSPHATE; CD28 ANTIGEN; CD3 ANTIGEN; FIBRONECTIN; GUANOSINE TRIPHOSPHATASE; INTERLEUKIN 2; IONOMYCIN; PHORBOL 13 ACETATE 12 MYRISTATE; RHO FACTOR;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IMMUNOREGULATION; LEUKOCYTE ADHERENCE; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ACTINS; ADENOSINE DIPHOSPHATE; ADP RIBOSE TRANSFERASES; ANTIGENS, CD18; ANTIGENS, CD28; ANTIGENS, CD29; ANTIGENS, CD3; BOTULINUM TOXINS; CELL ADHESION; CELL DIVISION; CELL LINE; CELLS, CULTURED; DOWN-REGULATION; GTP PHOSPHOHYDROLASES; GTP-BINDING PROTEINS; HUMANS; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RHOA GTP-BINDING PROTEIN; RIBOSE; T-LYMPHOCYTES;

EID: 0032487579     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.188.7.1211     Document Type: Article

References (78)

1. Pardi, R., L. Inverardi, C. Rugarli, and J.R. Bender. 1992. Antigen-receptor complex stimulation triggers protein kinase C-dependent CD11a/CD18-cytoskeleton association in T lymphocytes. J. Cell Biol. 116:1211-1220.
2. Bourguignon, L.Y., S.J. Suchard, M.L. Nagpal, and J.R. Glenney. 1985. A T-lymphoma transmembrane glycoprotein (gp180) is linked to the cytoskeletal protein, fodrin. J. Cell Biol. 101:477-487.
3. Taffs, R.E., and S.J. Ewald. 1989. Concanavalin A induces a cytoskeletal association of T200 molecules in T lymphocytes. Mol. Immunol. 26:925-937.
4. Geppert, T.D., and P.E. Lipsky. 1991. Association of various T cell-surface molecules with the cytoskeleton. Effect of cross-linking and activation. J. Immunol. 146:3298-3305.
5. Caplan, S., S. Zeliger, L. Wang, and M. Baniyash. 1995. Cell surface-expressed T-cell antigen-receptor ζ chain is associated with the cytoskeleton. Proc. Natl. Acad. Sci. USA. 92:4768-4772.
6. Rozdzial, M.M., B. Malissen, and T.H. Finkel. 1995. Tyrosine-phosphorylated T cell receptor C chain associates with the actin cytoskeleton upon activation of mature T lymphocytes. Immunity. 3:623-633.
7. Caplan, S., and M. Baniyash. 1996. Normal T cells express two T cell antigen receptor populations, one of which is linked to the cytoskeleton via ζ chain and displays a unique activation-dependent phosphorylation pattern. J. Biol. Chem. 271:20705-20712.
8. Valitutti, S., M. Dessing, K. Aktories, H. Gallati, and A. Lanzavecchia. 1995. Sustained signaling leading to T cell activation results from prolonged T cell receptor occupancy. Role of T cell actm cytoskeleton. J. Exp. Med. 181:577-584.
9. Shaw, A.S., and M.L. Dustin. 1997. Making the T cell receptor go the distance: a topological view of T cell activation. Immunity. 6:361-369.
10. Ridley, A.J. 1995. Rho-related proteins: actin cytoskeleton and cell cycle. Curr. Opin. Gen. Dev. 5:24-30.
11. van Aelst, L., and C. D'Souza-Schorey. 1997. Rho GTPases and signaling networks. Genes Dev. 11:2295-2322.
12. Ridley, A.J., and A. Hall. 1992. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 70:389-399.
13. Tominaga, T., K. Sugie, M. Hirata, N. Morii, J. Fukata, A. Uchida, H. Imura, and S. Narumiya. 1993. Inhibition of PMA-induced, LFA-1-dependent lymphocyte aggregation by ADP ribosylation of the small molecular weight GTP binding protein, rho. J. Cell Biol. 120:1529-1537.
14. Laudanna, C., J.J. Campbell, and E.C. Butcher. 1996. Role of rho in chemoattractant-activated leukocyte adhesion through integrins. Science. 271:981-983.
15. Koch, G., J. Norgauer, and K. Aktories. 1994. ADP-ribosylation of the GTP-binding protein rho by clostridium limosum exoenzyme affects basal, but not N-formyl-peptide-stimulated, actin polymerization in human myeloid leukaemic (HL-60) cells. Biochem. J. 299:775-779.
16. Ehrengruber, M.U., P. Boquet, T.D. Coates, and D.A. Deranleau. 1995. ADP-ribosylation of rho enhances actin polymerization-coupled shape oscillations in human neutrophils. FEBS Lett. 373:161-164.
17. Lang, P., L. Guizani, I. Vitte-Mony, R. Stancou, O. Dorseuil, G. Gacon, and J. Bertoglio. 1992. ADP-ribosylation of the ras-related, GTP-binding protein RhoA inhibits lymphocyte-mediated cytotoxicity. J. Biol. Chem. 267: 11677-11680.
18. Lang, P., F. Gesbert, M. Delespine-Carmagnat, R. Stancou, M. Pouchelet, and J. Bertoglio. 1996. Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO (Eur. Mol. Biol. Organ.) J. 15:510-519.
19. Aepfelbacher, M., M. Essler, E. Huber, A. Czech, and P.C. Weber. 1996. Rho is a negative regulator of human monocyte spreading. J. Immunol. 157:5070-5075.
20. Allen, W.E., G.E. Jones, J.W. Pollard, and A.J. Ridley. 1997. Rho, rac and cdc42 regulate actin organization and cell adhesion in macrophages. J. Cell Sci. 110:707-720.
21. Henning, S.W., R. Galandrini, A. Hall, and D.A. Cantrell. 1997. The GTPase Rho has a critical regulatory role in thymus development. EMBO (Eur. Mol. Biol. Organ.) J. 18: 2397-2407.
22. Hynes, R.O. 1993. Fibronectins. A. Rich, editor. Springer-Verlag, NY. p. 12.
23. Bednarczyk, J.L., M.C. Szabo, J.N. Wygant, A.I. Lazarovits, and B.W. McIntyre. 1994. Identification of a combinatorial epitope expressed by the integrin α4β1 heterodimer involved in the regulation of cell adhesion. J. Biol. Chem. 269:8348-8354.
24. Bednarczyk, J.L., J.N. Wygant, M.C. Szabo, L. Molinari-Storey, M. Renz, S. Fong, and B.W. McIntyre. 1993. Homotypic leukocyte aggregation triggered by a monoclonal antibody specific for a novel epitope expressed by the integrin β1 subunit: conversion ot nonresponsive cells by transfecting human integrin α4 subunit cDNA. J. Cell. Biochem. 51:465-478.
25. Woodside, D.G., T.K. Teague, and B.W. McIntyre. 1996. Specific inhibition of T lymphocyte coactivation by triggering integrin β1 reveals convergence of β1, β2, and β7 integrin signaling pathways. J. Immunol. 157:700-706.
26. Faull, R.J., N.L. Kovach, J.M. Harlan, and M.H. Ginsberg. 1994. Stimulation of integrin-mediated adhesion of T lymphocytes and monocytes: two mechanisms with divergent biological consequences. J. Exp. Med. 179:1307-1316.
27. Szabo, M.C., T.K. Teague, and B.W. McIntyre. 1995. Regulation of lymphocyte pseudopodia formation by triggering the integrin α4β1. J. Immunol. 154:2112-2124.
28. Woodside, D.G., and B.W. McIntyre. 1998. Inhibition of CD28/CD3 mediated costimulation of naive and memory human T lymphocytes by intracellular incorporation of polyclonal antibodies specific for the AP-1 transcriptional complex. J. Immunol. 161:649-658.
29. Udagawa, T., and B.W. McIntyre. 1996. ADP-ribosylation of the G protein rho inhibits integrin regulation of tumor cell growth. J. Biol. Chem. 271:12542-12548.
30. Rubin, E.J., D.M. Gill, P. Boquet, and M.R. Popoff. 1988. Functional modification of a 21-kilodalton G protein when ADP-ribosylated by exoenzyme C3 of clostridium botulinum. Mol. Cell. Biol. 8:418-416.
31. Shimizu, Y., G.A. Van Seventer, K.J. Horgan, and S. Shaw. 1990. Regulated expression and binding of three VLA (β1) integrin receptors on T cells. Nature. 345:250-253.
32. Gailit, J., and E. Ruoslahti. 1988. Regulation of the fibronectin receptor affinity by divalent cations. J. Biol. Chem. 263: 12927-12932.
33. Chan, B.M., M.J. Elices, E. Murphy, and M.E. Hemler. 1992. Adhesion to vascular cell adhesion molecule 1 and fibronectin. Comparison of α4β1 (VLA-4) and α4β7 on the human B cell line JY. J. Biol. Chem. 267:8366-8370.
34. Paterson, H.F., A.J. Self, M.D. Garrett, I. Just, K. Aktories, and A. Hall. 1990. Microinjection of recombinant p21 rho induces rapid changes in cell morphology. J. Cell Biol. 111: 1001-1007.
35. Aepfelbacher, M. 1995. ADP-ribosylation of Rho enhances adhesion of U937 cell to fibronectin via the α5β1 integrin receptor. FEBS Lett. 363:78-80.
36. Lauffenburger, D.A., and A.F. Horwitz. 1996. Cell migration: a physically integrated molecular process. Cell. 84:359-369.
37. Mitchison, T.J., and L.P. Cramer. 1996. Actin-based cell motility and cell locomotion. Cell. 84:371-379.
38. Kozma, R., S. Sarner, S. Ahmed, and L. Lim. 1997. Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell. Biol. 17:1201-1211.
39. Wayner, E.A., A. Garcia-Pardo, M.J. Humphries, J.A. McDonald, and W.G. Carter. 1989. Identification and characterization of the lymphocyte adhesion receptor for an alternative cell attachment domain in plasma fibronectin. J. Cell Biol. 109:1321-1330.
40. Pytela, R., M.D. Pierschbacher, and E. Ruoslahti. 1985. Identification and isolation of a 140 kd cell surface glycoprotein with properties expected of a fibronectin receptor. Cell. 40:191-198.
41. van Kooyk, Y., E. van de Wiel-van Kemenade, P. Weder, R.J.F. Huijbens, and C.G. Figdor. 1993. Lymphocyte function-associated antigen 1 dominates very late antigen 4 in binding of activated T cells to endothelium. J. Exp. Med. 177:185-190.
42. Blystone, S.D., I.L. Graham, F.P. Lindberg, and E.J. Brown. 1994. Integrin αvβ3 differentially regulated adhesive and phagocytic functions of the fibronectin receptor α5β1. J. Cell Biol. 127:1129-1137.
43. Blystone, S.D., F.P. Lindberg, S.E. LaFlamme, and E.J. Brown. 1995. Integrin β3 cytoplasmic tail is necessary and sufficient for regulation of α5β1 phagocytosis by αvβ3 and integrin-associated protein. J. Cell Biol. 130:745-754.
44. Huhtala, P., M.J. Humphries, J.B. McCarthy, P.M. Tremble, Z. Werb, and C.H. Damsky. 1995. Cooperative signaling by α5β1 and α4β1 integrins regulates metalloproteinase gene expression in fibroblasts adhering to fibronectin. J. Cell Biol. 129:867-879.
45. Diaz-Gonzalez, F., J. Forsyth, B. Steiner, and M.H. Ginsberg. 1996. Trans-dominant inhibition of integrin function. Mol. Biol. Cell. 7:1939-1951.
46. Weber, C., R. Alon, B. Moser, and T.A. Springer. 1996. Sequential regulation of α4β1 and α5β1 integrin avidity by CC chemokines in monocytes: implications for transendothelial chemotaxis. J. Cell Biol. 134:1063-1073.
47. Chong, L.D., A. Traynor-Kaplan, G.M. Bokoch, and M.A. Schwartz. 1994. The small GTP-binding protein rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells. Cell. 79:507-513.
48. Jockusch, B.M., P. Bubeck, K. Giehl, M. Kroemker, J. Moschner, M. Rothkegel, M. Rudiger, K. Schluter, G. Stanke, and J. Winkler. 1995. The molecular architecture of focal adhesions. Annu. Rev. Cell Dev. Biol. 11:379-416.
49. Negulescu, P.A., T.B. Krasieva, A. Khan, H.H. Kerschbaum, and M.D. Cahalan. 1996. Polarity of T cell shape, motility, and sensitivity to antigen. Immunity. 4:421-430.
50. Sun, H.Q., K. Lin, and H.L. Yin. 1997. Gelsolin modulates phosphohpase C activity in vivo through phospholipid binding. J. Cell Biol. 138:811-820.
51. Hill, C.S., J. Wynne, and R. Treisman. 1995. The Rho Family of GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell. 81:1159-1170.
52. Olson, M.F., A. Ashworth, and A. Hall. 1995. An essential role for rho, rac, and cdc42 GTPases in cell cycle progression through G1. Science. 269:1270-1272.
53. Damle, N.K., and A. Aruffo. 1991. Vascular cell adhesion molecule-1 induces T-cell antigen receptor-dependent activation of CD4+ T lymphocytes. Proc. Natl. Acad. Sci. USA. 88:6403-6407.
54. Davis, L.S., N. Oppenheimer-Marks, J.L. Bednarczyk, B.W. McIntyre, and P.E. Lipsky. 1990. Fibronectin promotes proliferation of naive and memory T cells by signaling through both the VLA-4 and VLA-5 integrin molecules. J. Immunol. 145:785-793.
55. Matsuyama, T., A. Yamada, J. Kay, K.M. Yamada, S.K. Akiyama, S.F. Schlossman, and C. Morimoto. 1989. Activation of CD4 cells by fibronectin and anti-CD3 antibody: a synergistic effect mediated by the VLA-5 fibronectin receptor complex. J. Exp. Med. 170:1133-1148.
56. Shimizu, Y., G.A. van Seventer, K.J. Horgan, and S. Shaw. 1990. Costimulation of proliferative responses of resting CD4+ T cells by the interaction of VLA-4 and VLA-5 with fibronectin or VLA-6 with laminin. J. Immunol. 145:59-67.
57. Udagawa, T., and B.W. McIntyre. 1992. A VLA-4 α-chain specific monoclonal antibody enhances CD3-induced IL-2/ IL-2 receptor-dependent T-cell proliferation. Lymphokine Cytokine Res. 11:193-199.
58. van Seventer, G.A., Y. Shimizu, K.J. Horgan, and S. Shaw. 1990. The LFA-1 ligand ICAM-1 provides an important co-stimulatory signal for T cell receptor-mediated activation of resting T cells. J. Immunol. 144:4579-4586.
59. Bednarczyk, J.L., T.K. Teague, J.N. Wygant, L.S. Davis, P.E. Lipsky, and B.W. McIntyre. 1992. Regulation of T cell proliferation by anti-CD49d and anti-CD29 monoclonal antibodies. J. Leuk. Biol. 52:456-462.
60. Firpo, E.J., A. Koff, M.J. Solomon, and J.M. Roberts. 1994. Inactivation of a Cdk-2 inhibitor during interleukin-2 induced proliferation of human T lymphocytes. Mol. Cell. Biol. 14:4889-4901.
61. Polyak, K., M.H. Lee, H. Erdjument-Bromage, A. Koff, J.M. Roberts, P. Tempst, and J. Massague. 1994. Cloning of p27kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular mitogenic signals. Cell. 78:59-66.
62. Hirai, A., S. Nakamura, Y. Noguchi, T. Yasuda, M. Kitagawa, I. Tatsuno, T. Oeda, K. Tahara, T. Terano, S. Narumiya, et al. 1997. Geranylgeranylated rho small GTPase(s) are essential for the degradation of p27kip1 and facilitate the progression from G1 to S phase in growth-stimulated Rat FRTL-5 cells. J. Biol. Chem. 272:13-16.
63. Wang, J., X. Chenivesse, B. Henglein, and C. Brechot. 1990. Hepatitis B virus integration in a cyclin A gene in a hepatocellular carcinoma. Nature. 343:555-557.
64. Sander, B., J. Andersson, and U. Andersson. 1991. Assessment of cytokines by immunofluorescence and the paraformaldehyde-saponin procedure. Immunol. Rev. 119:65-93.
65. Zanders E.D., J.R. Lamb, M. Feldmann, N. Green, and P.C. Beverley. 1983. Tolerance of T-cell clones is associated with membrane antigen changes. Nature. 303:625-627.
66. Krangel, M.S. 1987. Endocytosis and recycling of the T3-T cell receptor complex. The role of T3 phosphorylation. J. Exp. Med. 165:1141-1159.
67. Schwartz, M.A., M.D. Schaller, and M.H. Ginsberg. 1995. Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell Dev. Biol. 11:549-599.
68. Divecha, N., and R.F. Irvine. 1995. Phospholipid Signaling. Cell. 80:269-278.
69. Weiss, A., and D.R. Littman. 1994. Signal transduction by lymphocyte antigen receptors. Cell. 76:263-274.
70. Castagna, M., Y. Takai, K. Kaibuchi, K. Sano, U. Kikkawa, and Y. Nishizuka. 1982. Direct activation of calcium-activated phospholipid-dependent protein kinase by tumor-promoting phorbol esters. J. Biol. Chem. 247:7847-7851.
71. Hackam, D.J., O.D. Rotstein, A. Schreiber, W. Zhang, and S. Grinstein. 1997. Rho is required for the initiation of calcium signaling and phagocytosis by Fcγ receptors in macrophages. J. Exp. Med. 186:955-966.
72. Han, J., B. Das, W. Wei, L. Van Aelst, R.D. Mosteller, R. Khosravi-Far, J.K. Westwick, C.J. Der, and D. Broek. 1997. Lck regulates vav activation of members of the rho family of GTPases. Mol. Cell. Biol. 17:1346-1353.
73. Hart, M.J., A. Eva, T. Evans, S.A. Aaronson, and R.A. Cerione. 1991. Catalysis of guanine nucleotide exchange on the cdc42Hs protein by the dbl oncogene product. Nature. 354: 311-314.
74. Hart, M.J., A. Eva, D. Zangrilli, S.A. Aaronson, T. Evans, R.A. Cerione, and Y. Zheng. 1994. Cellular transformation and guanine nucleotide exchange activity are catalyzed by a common domain on the dbl oncogene. J. Biol. Chem. 269: 62-65.
75. Chan, A.C., D.M. Desai, and A. Weiss. 1994. The role of protein tyrosine kinases and protein tyrosine phosphatases in T cell antigen receptor signal transduction. Annu. Rev. Immunol. 12:555-592.
76. Ellis, C., M. Moran, F. McCormick, and T. Pawson. 1990. Phosphorylation of GAP and GAP-associated proteins by transforming and mitogenic tyrosine kinases. Nature. 343: 377-381.
77. Moran, M.F., P. Polakis, F. McCormick, T. Pawson, and C. Ellis. 1991. Protein-tyrosine kinases regulate the phosphorylation, protein interactions, subcellular distribution, and activity of p21ras GTPase-activating protein. Mol. Cell. Biol. 11:1804-1812.
78. Bryant, S.S., S. Briggs, T.E. Smithgall, G.A. Martin, F. McCormick, J.H. Chang, S.J. Parsons, and R. Jove. 1995. Two SH2 domains of p120 Ras GTPase-activating protein bind synergistically to tyrosine phosphorylated p190 Rho GTPase-activating protein. J. Biol. Chem. 270:17947-17952.