RhoH regulates subcellular localization of ZAP-70 and Lck in T cell receptor signaling

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Chae, Hee Don ^a,c   Siefring, Jamie E ^a   Hildeman, David A ^b   Gu, Yi ^a,d   Williams, David A ^a,e  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d ASTRAZENECA   (United Kingdom)

^e BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; PROTEIN KINASE LCK; PROTEIN KINASE ZAP 70; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOH; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; CD3 ANTIGEN, ZETA CHAIN; LYMPHOCYTE ANTIGEN RECEPTOR; RHOH PROTEIN, MOUSE; TRANSCRIPTION FACTOR; ZAP70 PROTEIN, MOUSE;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; BONE MARROW CELL; CELL ISOLATION; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; IMMUNOPRECIPITATION; MOUSE; MYRISTYLATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMOCYTE; 129 MOUSE; ANIMAL; C57BL MOUSE; CELL STRAIN HEK293; FEMALE; GENETICS; HUMAN; IMMUNOBLOTTING; INTRACELLULAR SPACE; LEUKEMIA CELL LINE; MALE; METABOLISM; MOUSE MUTANT; PHOSPHORYLATION; PROTEIN BINDING; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD3; FEMALE; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; INTRACELLULAR SPACE; JURKAT CELLS; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PHOSPHORYLATION; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSCRIPTION FACTORS; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 78649735549     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013970     Document Type: Article

References (45)

1. Dallery E, Galiegue-Zouitina S, Collyn-d'Hooghe M, Quief S, Denis C, et al. (1995) TTF, a gene encoding a novel small G protein, fuses to the lymphoma-associated LAZ3 gene by t(3;4) chromosomal translocation. Oncogene 10: 2171-2178.
2. Aspenstrom P, Ruusala A, Pacholsky D (2007) Taking Rho GTPases to the next level: the cellular functions of atypical Rho GTPases. Exp Cell Res 313: 3673-3679.
3. Gu Y, Chae H, Siefring J, Jast IJ, Hildeman D, et al. (2006) RhoH, a GTPase recruits and activates Zap70 required for T cell receptor signaling and thymocyte development. Nat Immunol 7: 1182-1190.
4. Li X, Bu X, Lu B, Avraham H, Flavell RA, et al. (2002) The hematopoiesis-specific GTP-binding protein RhoH is GTPase deficient and modulates activities of other Rho GTPases by an inhibitory function. Mol Cell Biol 22: 1158-1171.
5. Chae HD, Lee KE, Williams DA, Gu Y (2008) Cross-talk between RhoH and Rac1 in regulation of actin cytoskeleton and chemotaxis of hematopoietic progenitor cells. Blood 111: 2597-2605.
6. Gu Y, Jasti AC, Jansen M, Siefring JE (2005) RhoH, a hematopoietic-specific Rho GTPase, regulates proliferation, survival, migration, and engraftment of hematopoietic progenitor cells. Blood 105: 1467-1475.
7. Dorn T, Kuhn U, Bungartz G, Stiller S, Bauer M, et al. (2007) RhoH is important for positive thymocyte selection and T-cell receptor signaling. Blood 109: 2346-2355.
8. Ashe JM, Wiest DL, Abe R, Singer A (1999) ZAP-70 protein promotes tyrosine phosphorylation of T cell receptor signaling motifs (ITAMs) in immature CD4(+)8(+) thymocytes with limiting p56(lck). J Exp Med 189: 1163-1168.
9. Steinberg M, Adjali O, Swainson L, Merida P, Di Bartolo V, et al. (2004) T-cell receptor-induced phosphorylation of the zeta chain is efficiently promoted by ZAP-70 but not Syk. Blood 104: 760-767.
10. Thome M, Duplay P, Guttinger M, Acuto O (1995) Syk and ZAP-70 mediate recruitment of p56lck/CD4 to the activated T cell receptor/CD3/zeta complex. J Exp Med 181: 1997-2006.
11. Gauen LK, Zhu Y, Letourneur F, Hu Q, Bolen JB, et al. (1994) Interactions of p59fyn and ZAP-70 with T-cell receptor activation motifs: defining the nature of a signalling motif. Mol Cell Biol 14: 3729-3741.
12. Kobune M, Xu Y, Baum C, Kelley MR, Williams DA (2001) Retrovirus-mediated expression of the base excision repair proteins, fapy DNA glycosylase or human oxoguanine DNA glycosylase, protects hematopoietic cells from ThioTEPA-induced toxicity in vitro and in vivo. Cancer Research 61: 5116-5125.
13. Wahlers A, Schwieger M, Li Z, Meier-Tackmann D, Lindemann C, et al. (2001) Influence of multiplicity of infection and protein stability on retroviral vector-mediated gene expression in hematopoietic cells. Gene Ther 8: 477-486.
14. Gallardo HF, Tan C, Ory D, Sadelain M (1997) Recombinant retroviruses pseudotyped with the vesicular stomatitis virus G glycoprotein mediate both stable gene transfer and pseudotransduction in human peripheral blood lymphocytes. Blood 90: 952-957.
15. Moritz T, Patel VP, Williams DA (1994) Bone marrow extracellular matrix molecules improve gene transfer into human hematopoietic cells via retroviral vectors. J Clin Invest 93: 1451-1457.
16. Kumaraguru U, Rouse RJ, Nair SK, Bruce BD, Rouse BT (2000) Involvement of an ATP-dependent peptide chaperone in cross-presentation after DNA immunization. J Immunol 165: 750-759.
17. Brdicka T, Kadlecek TA, Roose JP, Pastuszak AW, Weiss A (2005) Intramolecular regulatory switch in ZAP-70: analogy with receptor tyrosine kinases. Mol Cell Biol 25: 4924-4933.
18. Giannini A, Bijlmakers MJ (2004) Regulation of the Src family kinase Lck by Hsp90 and ubiquitination. Mol Cell Biol 24: 5667-5676.
19. Nel AE, Slaughter N (2002) T-cell activation through the antigen receptor. Part 2: role of signaling cascades in T-cell differentiation, anergy, immune senescence, and development of immunotherapy. J Allergy Clin Immunol 109: 901-915.
20. van Oers NS, Killeen N, Weiss A (1996) Lck regulates the tyrosine phosphorylation of the T cell receptor subunits and ZAP-70 in murine thymocytes. J Exp Med 183: 1053-1062.
21. Underhill DM, Goodridge HS (2007) The many faces of ITAMs. Trends Immunol 28: 66-73.
22. Hermiston ML, Xu Z, Majeti R, Weiss A (2002) Reciprocal regulation of lymphocyte activation by tyrosine kinases and phosphatases. J Clin Invest 109: 9-14.
23. Clayton LK, D'Adamio L, Howard FD, Sieh M, Hussey RE, et al. (1991) CD3 eta and CD3 zeta are alternatively spliced products of a common genetic locus and are transcriptionally and/or post-transcriptionally regulated during T-cell development. Proc Natl Acad Sci U S A 88: 5202-5206.
24. Friedl P, den Boer AT, Gunzer M (2005) Tuning immune responses: diversity and adaptation of the immunological synapse. Nat Rev Immunol 5: 532-545.
25. Monks CR, Freiberg BA, Kupfer H, Sciaky N, Kupfer A (1998) Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395: 82-86.
26. Saito T, Yokosuka T (2006) Immunological synapse and microclusters: the site for recognition and activation of T cells. Curr Opin Immunol 18: 305-313.
27. Cannon JL, Burkhardt JK (2002) The regulation of actin remodeling during T-cell-APC conjugate formation. Immunol Rev 186: 90-99.
28. Villalba M, Bi K, Rodriguez F, Tanaka Y, Schoenberger S, et al. (2001) Vav1/ Rac-dependent actin cytoskeleton reorganization is required for lipid raft clustering in T cells. J Cell Biol 155: 331-338.
29. Garofalo T, Lenti L, Longo A, Misasi R, Mattei V, et al. (2002) Association of GM3 with Zap-70 induced by T cell activation in plasma membrane microdomains: GM3 as a marker of microdomains in human lymphocytes. J Biol Chem 277: 11233-11238.
30. Montixi C, Langlet C, Bernard AM, Thimonier J, Dubois C, et al. (1998) Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. Embo J 17: 5334-5348.
31. Xavier R, Brennan T, Li Q, McCormack C, Seed B (1998) Membrane compartmentation is required for efficient T cell activation. Immunity 8: 723-732.
32. Chan AC, Iwashima M, Turck CW, Weiss A (1992) ZAP-70: a 70 kd protein-tyrosine kinase that associates with the TCR zeta chain. Cell 71: 649-662.
33. Wange RL, Kong AN, Samelson LE (1992) A tyrosine-phosphorylated 70-kDa protein binds a photoaffinity analogue of ATP and associates with both the zeta chain and CD3 components of the activated T cell antigen receptor. J Biol Chem 267: 11685-11688.
34. Deindl S, Kadlecek TA, Brdicka T, Cao X, Weiss A, et al. (2007) Structural basis for the inhibition of tyrosine kinase activity of ZAP-70. Cell 129: 735-746.
35. Graef IA, Holsinger LJ, Diver S, Schreiber SL, Crabtree GR (1997) Proximity and orientation underlie signaling by the non-receptor tyrosine kinase ZAP70. Embo J 16: 5618-5628.
36. Yamasaki S, Takamatsu M, Iwashima M (1996) The kinase, SH3, and SH2 domains of Lck play critical roles in T-cell activation after ZAP-70 membrane localization. Mol Cell Biol 16: 7151-7160.
37. Roumier A, Olivo-Marin JC, Arpin M, Michel F, Martin M, et al. (2001) The membrane-microfilament linker ezrin is involved in the formation of the immunological synapse and in T cell activation. Immunity 15: 715-728.
38. Xavier R, Rabizadeh S, Ishiguro K, Andre N, Ortiz JB, et al. (2004) Discs large (Dlg1) complexes in lymphocyte activation. J Cell Biol 166: 173-178.
39. Preudhomme C, Roumier C, Hildebrand MP, Dallery-Prudhomme E, Lantoine D, et al. (2000) Nonrandom 4p13 rearrangements of the RhoH/ TTF gene, encoding a GTP- binding protein, in non-Hodgkin's lymphoma and multiple myeloma. Oncogene 19: 2023-2032.
40. Pasqualucci L, Neumeister P, Goossens T, Nanjangud G, Chaganti RS, et al. (2001) Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature 412: 341-346.
41. Gaidano G, Pasqualucci L, Capello D, Berra E, Deambrogi C, et al. (2003) Aberrant somatic hypermutation in multiple subtypes of AIDS-associated non-Hodgkin lymphoma. Blood 102: 1833-1841.
42. Cherry LK, Li X, Schwab P, Lim B, Klickstein LB (2004) RhoH is required to maintain the integrin LFA-1 in a nonadhesive state on lymphocytes. Nat Immunol 5: 961-967.
43. Dumont C, Blanchard N, Di Bartolo V, Lezot N, Dufour E, et al. (2002) TCR/ CD3 down-modulation and zeta degradation are regulated by ZAP-70. J Immunol 169: 1705-1712.
44. Dorn T (2007) Analysis of RhoH function in vivo [Dissertation]. Munich: ludwig-maximilians-universität. 148 p.
45. Wang L, Zheng Y (2007) Cell type-specific functions of Rho GTPases revealed by gene targeting in mice. Trends Cell Biol 17: 58-64.