Essential function for the GTPase TC21 in homeostatic antigen receptor signaling

Nature Immunology

Volumn 10, Issue 8, 2009, Pages 880-888

  Delgado, Pilar ^a   Cubelos, Beatriz ^a   Calleja, Enrique ^a   Martínez Martín, Nuria ^a   Ciprés, Angel ^a   Mérida, Isabel ^a   Bellas, Carmen ^b   Bustelo, Xosé R ^c   Alarcón, Balbino ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

^c UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD3 ANTIGEN; CD3 ANTIGEN GAMMA; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE TC21; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P110; PROTEIN P110 DELTA; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; GERMINAL CENTER; HOMEOSTASIS; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; LYMPHOCYTOPENIA; LYMPHOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; B-LYMPHOCYTES; CELL SURVIVAL; HOMEOSTASIS; HUMANS; LYMPH NODES; LYMPHOMA, B-CELL; LYMPHOMA, T-CELL; MEMBRANE PROTEINS; MICE; MONOMERIC GTP-BINDING PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTORS, ANTIGEN, B-CELL; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 67651151038     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.1749     Document Type: Article

References (56)

1. Freitas, A.A. & Rocha, B. Population biology of lymphocytes: The flight for survival. Annu. Rev. Immunol. 18, 83-111 (2000).
2. Khaled, A.R. & Durum, S.K. Lymphocide: Cytokines and the control of lymphoid homeostasis. Nat. Rev. Immunol. 2, 817-830 (2002).
3. Seddon, B. & Zamoyska, R. Regulation of peripheral T-cell homeostasis by receptor signalling. Curr. Opin. Immunol. 15, 321-324 (2003).
4. Woodland, R.T., Schmidt, M.R. & Thompson, C.B. BLyS and B cell homeostasis. Semin. Immunol. 18, 318-326 (2006).
5. Schiemann, B. et al. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293, 2111-2114 (2001).
6. Tan, J.T. et al. IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc. Natl. Acad. Sci. USA 98 8732-8737 (2001).
7. Lin, J. & Weiss, A. T cell receptor signalling. J. Cell Sci. 114, 243-244 (2001).
8. Rudolph, M.G., Luz, J.G. & Wilson, I.A. Structural and thermodynamic correlates of T cell signaling. Annu. Rev. Biophys. Biomol. Struct. 31, 121-149 (2002).
9. Werlen, G. & Palmer, E. The T-cell receptor signalosome: A dynamic structure with expanding complexity. Curr. Opin. Immunol. 14 299-305 (2002).
10. Reth, M. Antigen receptor tail clue. Nature 338, 383-384 (1989).
11. Labrecque, N. et al. How much TCR does a T cell need? Immunity 15, 71-82 (2001).
12. Polic, B., Kunkel, D., Scheffold, A. & Rajewsky, K. How αb T cells deal with induced TCRa ablation. Proc. Natl. Acad. Sci. USA 98, 8744-8749 (2001).
13. + T cells: Half-life and survival signals in the absence of major histocompatibility complex class II molecules. J. Exp. Med. 191 355-364 (2000).
14. Lam, K.P., Kuhn, R. & Rajewsky, K. In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell 90, 1073-1083 (1997).
15. Kraus, M., Alimzhanov, M.B., Rajewsky, N. & Rajewsky, K. Survival of resting mature B lymphocytes depends on BCR signaling via the Iga/b heterodimer. Cell 117, 787-800 (2004).
16. Seddon, B., Legname, G., Tomlinson, P. & Zamoyska, R. Long-term survival but impaired homeostatic proliferation of naive T cells in the absence of p56lck. Science 290, 127-131 (2000).
17. Seddon, B. & Zamoyska, R. TCR signals mediated by Src family kinases are essential for the survival of naive T cells. J. Immunol. 169 2997-3005 (2002).
18. Vanhaesebroeck, B. et al. Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 70, 535-602 (2001).
19. Fabre, S., Lang, V. & Bismuth, G. PI3-kinase and the control of T cell growth and proliferation by FoxOs. Bull. Cancer 93, E36-E38 (2006).
20. Okkenhaug, K., Ali, K. & Vanhaesebroeck, B. Antigen receptor signalling: a distinctive role for the p110delta isoform of PI3K. Trends Immunol. 28, 80-87 (2007).
21. Okkenhaug, K. & Vanhaesebroeck, B. PI3K in lymphocyte development, differentiation and activation. Nat. Rev. Immunol. 3, 317-330 (2003).
22. Clayton, E. et al. A crucial role for the p110delta subunit of phosphatidylinositol 3-kinase in B cell development and activation. J. Exp. Med. 196, 753-763 (2002).
23. Jou, S.T. et al. Essential, nonredundant role for the phosphoinositide 3-kinase p110delta in signaling by the B-cell receptor complex. Mol. Cell. Biol. 22, 8580-8591 (2002).
24. Okkenhaug, K. et al. Impaired B and T cell antigen receptor signaling in p110delta PI 3-kinase mutant mice. Science. 297 1031-1034 (2002).
25. Ehrhardt, A., Ehrhardt, G.R., Guo, X. & Schrader, J.W. Ras and relatives-job sharing and networking keep an old family together. Exp. Hematol. 30, 1089-1106 (2002).
26. Rodriguez-Viciana, P., Sabatier, C. & McCormick, F. Signaling specificity by Ras family GTPases is determined by the full spectrum of effectors they regulate. Mol. Cell. Biol. 24, 4943-4954 (2004).
27. Murphy, G.A. et al. Involvement of phosphatidylinositol 3-kinase, but not RalGDS, in TC21/R-Ras2-mediated transformation. J. Biol. Chem. 277, 9966-9975 (2002).
28. Rosario, M., Paterson, H.F. & Marshall, C.J. Activation of the Ral and phosphatidylinositol 3′ kinase signaling pathways by the ras-related protein TC21. Mol. Cell. Biol. 21, 3750-3762 (2001).
29. Graham, S.M. et al. Aberrant function of the Ras-related protein TC21/R-Ras2 triggers malignant transformation. Mol. Cell. Biol. 14, 4108-4115 (1994).
30. Chan, A.M., Miki, T., Meyers, K.A. & Aaronson, S.A. A human oncogene of the RAS superfamily unmasked by expression cDNA cloning. Proc. Natl. Acad. Sci. USA 91, 7558-7562 (1994).
31. Huang, Y. et al. A novel insertional mutation in the TC21 gene activates its transforming activity in a human leiomyosarcoma cell line. Oncogene 11, 1255-1260 (1995).
32. Clark, G.J., Kinch, M.S., Gilmer, T.M., Burridge, K. & Der, C.J. Overexpression of the Ras-related TC21/R-Ras2 protein may contribute to the development of human breast cancers. Oncogene 12, 169-176 (1996).
33. Arora, S., Matta, A., Shukla, N.K., Deo, S.V. & Ralhan, R. Identification of differentially expressed genes in oral squamous cell carcinoma. Mol. Carcinog. 42, 97-108 (2005).
34. Sharma, R., Sud, N., Chattopadhyay, T.K. & Ralhan, R. TC21/R-Ras2 upregulation in esophageal tumorigenesis: Potential diagnostic implications. Oncology 69, 10-18 (2005).
35. Kim, R. et al. Genome-based identification of cancer genes by proviral tagging in mouse retrovirus-induced T-cell lymphomas. J. Virol. 77, 2056-2062 (2003).
36. Aronheim, A. Membrane recruitment systems for analysis of protein-protein interactions. Methods Mol. Biol. 177, 319-328 (2001).
37. Graham, S.M. et al. TC21 causes transformation by Raf-independent signaling pathways. Mol. Cell. Biol. 16, 6132-6140 (1996).
38. Lopez-Barahona, M., Bustelo, X.R. & Barbacid, M. The TC21 oncoprotein interacts with the Ral guanosine nucleotide dissociation factor. Oncogene 12, 463-470 (1996).
39. Ashwell, J.D., Cunningham, R.E., Noguchi, P.D. & Hernandez, D. Cell growth cycle block of T cell hybridomas upon activation with antigen. J. Exp. Med. 165, 173-194 (1987).
40. Cemerski, S. & Shaw, A. Immune synapses in T-cell activation. Curr. Opin. Immunol. 18, 298-304 (2006).
41. Dustin, M.L. T-cell activation through immunological synapses and kinapses. Immunol. Rev. 221, 77-89 (2008).
42. Hogquist, K.A. et al. T cell receptor antagonist peptides induce positive selection. Cell 76, 17-27 (1994).
43. Pillai, S., Cariappa, A. & Moran, S.T. Marginal zone B cells. Annu. Rev. Immunol. 23, 161-196 (2005).
44. Klein, U. & Dalla-Favera, R. Germinal centres: Role in B-cell physiology and malignancy. Nat. Rev. Immunol. 8, 22-33 (2008).
45. Rosario, M., Paterson, H.F. & Marshall, C.J. Activation of the Raf/MAP kinase cascade by the Ras-related protein TC21 is required for the TC21-mediated transformation of NIH 3T3 cells. EMBO J. 18, 1270-1279 (1999).
46. Tanchot, C., Lemonnier, F.A., Perarnau, B., Freitas, A.A. & Rocha, B. Differential requirements for survival and proliferation of CD8 naive or memory T cells. Science 276, 2057-2062 (1997).
47. Movilla, N., Crespo, P. & Bustelo, X.R. Signal transduction elements of TC21, an oncogenic member of the R-Ras subfamily of GTP-binding proteins. Oncogene 18, 5860-5869 (1999).
48. Jarrett, R.F. Viruses and lymphoma/leukaemia. J. Pathol. 208 176-186 (2006).
49. Merchant, M., Caldwell, R.G. & Longnecker, R. The LMP2A ITAM is essential for providing B cells with development and survival signals in vivo. J. Virol. 74, 9115-9124 (2000).
50. Caldwell, R.G., Wilson, J.B., Anderson, S.J. & Longnecker, R. Epstein-Barr virus LMP2A drives B cell development and survival in the absence of normal B cell receptor signals. Immunity 9, 405-411 (1998).
51. Grande, S.M., Ross, S.R. & Monroe, J.G. Viral immunoreceptor-associated tyrosine-based activation motifs: Potential players in oncogenesis. Future Oncol. 2, 301-310 (2006).
52. Peter, M.E., Wileman, T. & Terhorst, C. Covalent binding of guanine nucleotides to the CD3-gamma chain of the T cell receptor/CD3 complex. Eur. J. Immunol. 23, 461-466 (1993).
53. Surh, C.D. & Sprent, J. Regulation of mature T cell homeostasis. Semin. Immunol. 17, 183-191 (2005).
54. Delgado, P. & Alarcon, B. An orderly inactivation of intracellular retention signals controls surface expression of the Tcell antigen receptor. J. Exp. Med. 201, 555-566 (2005).
55. Gil, D., Schamel, W.W, Montoya, M., Sanchez-Madrid, F. & Alarcon, B. Recruitment of Nck by CD3F reveals a ligand-induced conformational change essential for T cell receptor signaling and synapse formation. Cell 109, 901-912 (2002).
56. Cubelos, B. et al. Cux-2 controls the proliferation of neuronal intermediate precursors of the cortical subventricular zone. Cereb. Cortex 18, 1758-1770 (2008).