The Ras GTPase-activating protein neurofibromin 1 promotes the positive selection of thymocytes

Molecular Immunology

Volumn 55, Issue 3-4, 2013, Pages 292-302

  Oliver, Jennifer A ^a   Lapinski, Philip E ^a   Lubeck, Beth A ^a   Turner, Jackson S ^a   Parada, Luis F ^b   Zhu, Yuan ^a   King, Philip D ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Neurofibromin; Ras GTPase activating proteins; Signal transduction; T cells

Indexed keywords

NEUROFIBROMIN;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL PROLIFERATION; CELL SELECTION; CYTOKINE PRODUCTION; FEMALE; HOMEOSTASIS; MAJOR HISTOCOMPATIBILITY COMPLEX; MAJOR HISTOCOMPATIBILITY COMPLEX CLASS I; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; THYMOCYTE;

ANIMALS; CELL DIFFERENTIATION; CLONAL SELECTION, ANTIGEN-MEDIATED; FEMALE; LYMPHOCYTE ACTIVATION; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEUROFIBROMIN 1; RAS PROTEINS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTE SUBSETS;

MUS;

EID: 84877588598     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2013.03.005     Document Type: Article

References (50)

1. Abernathy C.R., Rasmussen S.A., Stalker H.J., Zori R., Driscoll D.J., Williams C.A., Kousseff B.G., Wallace M.R. NF1 mutation analysis using a combined heteroduplex/SSCP approach. Human Mutation 1997, 9:548-554.
2. Alberola-Ila J., Forbush K.A., Seger R., Krebs E.G., Perlmutter R.M. Selective requirement for MAP kinase activation in thymocyte differentiation. Nature 1995, 373:620-623.
3. Alberola-Ila J., Hernandez-Hoyos G. The Ras/MAPK cascade and the control of positive selection. Immunological Reviews 2003, 191:79-96.
4. Bauler T.J., Hendriks W.J., King P.D. The FERM and PDZ domain-containing protein tyrosine phosphatases, PTPN4 and PTPN3, are both dispensable for T cell receptor signal transduction. PLoS One 2008, 3:e4014.
5. Bernards A. GAPs galore! A survey of putative Ras superfamily GTPase activating proteins in man and Drosophila. Biochimica et Biophysica Acta 2003, 1603:47-82.
6. Bollag G., Clapp D.W., Shih S., Adler F., Zhang Y.Y., Thompson P., Lange B.J., Freedman M.H., McCormick F., Jacks T., Shannon K. Loss of NF1 results in activation of the Ras signaling pathway and leads to aberrant growth in haematopoietic cells. Nature Genetics 1996, 12:144-148.
7. Brannan C.I., Perkins A.S., Vogel K.S., Ratner N., Nordlund M.L., Reid S.W., Buchberg A.M., Jenkins N.A., Parada L.F., Copeland N.G. Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crest-derived tissues. Genes and Development 1994, 8:1019-1029.
8. Cawthon R.M., Weiss R., Xu G.F., Viskochil D., Culver M., Stevens J., Robertson M., Dunn D., Gesteland R., O'Connell P., et al. A major segment of the neurofibromatosis type 1 gene: cDNA sequence, genomic structure, and point mutations. Cell 1990, 62:193-201.
9. Chang L., Karin M. Mammalian MAP kinase signalling cascades. Nature 2001, 410:37-40.
10. Crompton T., Gilmour K.C., Owen M.J. The MAP kinase pathway controls differentiation from double-negative to double-positive thymocyte. Cell 1996, 86:243-251.
11. Das J., Ho M., Zikherman J., Govern C., Yang M., Weiss A., Chakraborty A.K., Roose J.P. Digital signaling and hysteresis characterize ras activation in lymphoid cells. Cell 2009, 136:337-351.
12. Dong C., Davis R.J., Flavell R.A. MAP kinases in the immune response. Annual Review of Immunology 2002, 20:55-72.
13. Donovan S., Shannon K.M., Bollag G. GTPase activating proteins: critical regulators of intracellular signaling. Biochimica et Biophysica Acta 2002, 1602:23-45.
14. Ebinu J.O., Stang S.L., Teixeira C., Bottorff D.A., Hooton J., Blumberg P.M., Barry M., Bleakley R.C., Ostergaard H.L., Stone J.C. RasGRP links T-cell receptor signaling to Ras. Blood 2000, 95:3199-3203.
15. Ernst B., Lee D.S., Chang J.M., Sprent J., Surh C.D. The peptide ligands mediating positive selection in the thymus control T cell survival and homeostatic proliferation in the periphery. Immunity 1999, 11:173-181.
16. Fahsold R., Hoffmeyer S., Mischung C., Gille C., Ehlers C., Kucukceylan N., Abdel-Nour M., Gewies A., Peters H., Kaufmann D., Buske A., Tinschert S., Nurnberg P. Minor lesion mutational spectrum of the entire NF1 gene does not explain its high mutability but points to a functional domain upstream of the GAP-related domain. American Journal of Human Genetics 2000, 66:790-818.
17. Fischer A.M., Katayama C.D., Pages G., Pouyssegur J., Hedrick S.M. The role of erk1 and erk2 in multiple stages of T cell development. Immunity 2005, 23:431-443.
18. Genot E., Cantrell D.A. Ras regulation and function in lymphocytes. Current Opinion in Immunology 2000, 12:289-294.
19. Hennet T., Hagen F.K., Tabak L.A., Marth J.D. T-cell-specific deletion of a polypeptide N-acetylgalactosaminyl-transferase gene by site-directed recombination. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:12070-12074.
20. Hernandez-Hoyos G., Anderson M.K., Wang C., Rothenberg E.V., Alberola-Ila J. GATA-3 expression is controlled by TCR signals and regulates CD4/CD8 differentiation. Immunity 2003, 19:83-94.
21. Hope D.G., Mulvihill J.J. Malignancy in neurofibromatosis. Advances in Neurology 1981, 29:33-56.
22. Ingram D.A., Zhang L., McCarthy J., Wenning M.J., Fisher L., Yang F.C., Clapp D.W., Kapur R. Lymphoproliferative defects in mice lacking the expression of neurofibromin: functional and biochemical consequences of Nf1 deficiency in T-cell development and function. Blood 2002, 100:3656-3662.
23. Ismat F.A., Xu J., Lu M.M., Epstein J.A. The neurofibromin GAP-related domain rescues endothelial but not neural crest development in Nf1 mice. Journal of Clinical Investigation 2006, 116:2378-2384.
24. Jacks T., Shih T.S., Schmitt E.M., Bronson R.T., Bernards A., Weinberg R.A. Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nature Genetics 1994, 7:353-361.
25. Kaye J., Hsu M.L., Sauron M.E., Jameson S.C., Gascoigne N.R., Hedrick S.M. Selective development of CD4+ T cells in transgenic mice expressing a class II MHC-restricted antigen receptor. Nature 1989, 341:746-749.
26. King, P.D., Lubeck, B.A., Lapinski, P.E., 2013. Non-redundant functions for Ras GTPase-activating proteins in tissue homeostasis. Science Signaling 6, re1.
27. Kisielow P., Bluthmann H., Staerz U.D., Steinmetz M., von Boehmer H. Tolerance in T-cell-receptor transgenic mice involves deletion of nonmature CD4+8+ thymocytes. Nature 1988, 333:742-746.
28. Kortum R.L., Sommers C.L., Pinski J.M., Alexander C.P., Merrill R.K., Li W., Love P.E., Samelson L.E. Deconstructing Ras signaling in the thymus. Molecular and Cellular Biology 2012.
29. Lapinski P.E., King P.D. Regulation of Ras signal transduction during T cell development and activation. American Journal of Clinical and Experimental Immunology 2012, 1:147-153.
30. Lapinski P.E., Oliver J.A., Kamen L.A., Hughes E.D., Saunders T.L., King P.D. Genetic analysis of SH2D4A, a novel adapter protein related to T cell-specific adapter and adapter protein in lymphocytes of unknown function, reveals a redundant function in T cells. Journal of Immunology 2008, 181:2019-2027.
31. Lapinski P.E., Qiao Y., Chang C.H., King P.D. A role for p120 RasGAP in thymocyte positive selection and survival of naive T cells. Journal of Immunology 2011, 187:151-163.
32. Largaespada D.A., Brannan C.I., Jenkins N.A., Copeland N.G. Nf1 deficiency causes Ras-mediated granulocyte/macrophage colony stimulating factor hypersensitivity and chronic myeloid leukaemia. Nature Genetics 1996, 12:137-143.
33. Lauritsen J.P., Kurella S., Lee S.Y., Lefebvre J.M., Rhodes M., Alberola-Ila J., Wiest D.L. Egr2 is required for Bcl-2 induction during positive selection. Journal of Immunology 2008, 181:7778-7785.
34. McGargill M.A., Ch'en I.L., Katayama C.D., Pages G., Pouyssegur J., Hedrick S.M. Cutting edge: Extracellular signal-related kinase is not required for negative selection of developing T cells. Journal of Immunology 2009, 183:4838-4842.
35. Oliver J.A., Stolberg V.R., Chensue S.W., King P.D. IL-4 acts as a potent stimulator of IFN-gamma expression in CD8+ T cells through STAT6-dependent and independent induction of Eomesodermin and T-bet. Cytokine 2012, 57:191-199.
36. Priatel J.J., Teh S.J., Dower N.A., Stone J.C., Teh H.S. RasGRP1 transduces low-grade TCR signals which are critical for T cell development, homeostasis, and differentiation. Immunity 2002, 17:617-627.
37. Rincon M., Flavell R.A., Davis R.J. Signal transduction by MAP kinases in T lymphocytes. Oncogene 2001, 20:2490-2497.
38. Rocha B., von Boehmer H. Peripheral selection of the T cell repertoire. Science 1991, 251:1225-1228.
39. Roose J.P., Mollenauer M., Gupta V.A., Stone J., Weiss A. A diacylglycerol-protein kinase C-RasGRP1 pathway directs Ras activation upon antigen receptor stimulation of T cells. Molecular and Cellular Biology 2005, 25:4426-4441.
40. Roose J.P., Mollenauer M., Ho M., Kurosaki T., Weiss A. Unusual interplay of two types of Ras activators, RasGRP and SOS, establishes sensitive and robust Ras activation in lymphocytes. Molecular and Cellular Biology 2007, 27:2732-2745.
41. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nature Protocols 2008, 3:1101-1108.
42. Sharp L.L., Schwarz D.A., Bott C.M., Marshall C.J., Hedrick S.M. The influence of the MAPK pathway on T cell lineage commitment. Immunity 1997, 7:609-618.
43. Suzuki A., Yamaguchi M.T., Ohteki T., Sasaki T., Kaisho T., Kimura Y., Yoshida R., Wakeham A., Higuchi T., Fukumoto M., Tsubata T., Ohashi P.S., Koyasu S., Penninger J.M., Nakano T., Mak T.W. T cell-specific loss of Pten leads to defects in central and peripheral tolerance. Immunity 2001, 14:523-534.
44. Swan K.A., Alberola-Ila J., Gross J.A., Appleby M.W., Forbush K.A., Thomas J.F., Perlmutter R.M. Involvement of p21ras distinguishes positive and negative selection in thymocytes. EMBO Journal 1995, 14:276-285.
45. Viskochil D., Buchberg A.M., Xu G., Cawthon R.M., Stevens J., Wolff R.K., Culver M., Carey J.C., Copeland N.G., Jenkins N.A., et al. Deletions and a translocation interrupt a cloned gene at the neurofibromatosis type 1 locus. Cell 1990, 62:187-192.
46. Wallace M.R., Marchuk D.A., Andersen L.B., Letcher R., Odeh H.M., Saulino A.M., Fountain J.W., Brereton A., Nicholson J., Mitchell A.L., et al. Type 1 neurofibromatosis gene: identification of a large transcript disrupted in three NF1 patients. Science 1990, 249:181-186.
47. Wennerberg K., Rossman K.L., Der C.J. The Ras superfamily at a glance. Journal of Cell Science 2005, 118:843-846.
48. Yang F.C., Ingram D.A., Chen S., Zhu Y., Yuan J., Li X., Yang X., Knowles S., Horn W., Li Y., Zhang S., Yang Y., Vakili S.T., Yu M., Burns D., Robertson K., Hutchins G., Parada L.F., Clapp D.W. Nf1-dependent tumors require a microenvironment containing Nf1+/- and c-kit-dependent bone marrow. Cell 2008, 135:437-448.
49. Zhu Y., Ghosh P., Charnay P., Burns D.K., Parada L.F. Neurofibromas in NF1: Schwann cell origin and role of tumor environment. Science 2002, 296:920-922.
50. Zhu Y., Romero M.I., Ghosh P., Ye Z., Charnay P., Rushing E.J., Marth J.D., Parada L.F. Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes and Development 2001, 15:859-876.