ShcA regulates thymocyte proliferation through specific transcription factors and a c-Abl-dependent signaling axis

Molecular and Cellular Biology

Volumn 35, Issue 8, 2015, Pages 1462-1476

  Trampont, Paul C ^a,c   Zhang, Li ^a   Giles, Amber J ^a   Walk, Scott F ^a   Gu, Jing J ^b   Pendergast, Ann Marie ^b   Ravichandran, Kodi S ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c Department of Technical Affairs   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; EARLY GROWTH RESPONSE FACTOR 1; EARLY GROWTH RESPONSE FACTOR 2; INHIBITOR OF DIFFERENTIATION 3; ISOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PRE T LYMPHOCYTE RECEPTOR; PROTEIN KINASE LCK; SHCA ADAPTER PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2A; UNCLASSIFIED DRUG; EARLY GROWTH RESPONSE FACTOR 3; EGR1 PROTEIN, MOUSE; EGR3 PROTEIN, MOUSE; IDB3 PROTEIN, MOUSE; INHIBITOR OF DIFFERENTIATION PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; MYC PROTEIN; PROTEIN SHC; SHC1 PROTEIN, MOUSE;

ALLELIC EXCLUSION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; GENE CONTROL; GENE INDUCTION; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; THYMOCYTE; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; SIGNAL TRANSDUCTION;

SACCHAROMYCES CEREVISIAE;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EARLY GROWTH RESPONSE PROTEIN 1; EARLY GROWTH RESPONSE PROTEIN 3; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INHIBITOR OF DIFFERENTIATION PROTEINS; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MAP KINASE SIGNALING SYSTEM; MICE, INBRED C57BL; MUTATION; PROTO-ONCOGENE PROTEINS C-ABL; PROTO-ONCOGENE PROTEINS C-MYC; RECEPTORS, ANTIGEN, T-CELL; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION; THYMOCYTES; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84925438549     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01084-14     Document Type: Article

References (46)

1. Petrie HT, Zuniga-Pflucker JC. 2007. Zoned out: functional mapping of stromal signaling microenvironments in the thymus. Annu Rev Immunol 25:649-679. http://dx.doi.org/10.1146/annurev.immunol.23.021704.115715.
2. Kruisbeek AM, Haks MC, Carleton M, Michie AM, Zuniga-Pflucker JC, Wiest DL. 2000. Branching out to gain control: how the pre-TCR is linked to multiple functions. Immunol Today 21:637-644. http://dx.doi.org/10.1016/S0167-5699(00)01744-8.
3. Aifantis I, Mandal M, Sawai K, Ferrando A, Vilimas T. 2006. Regulation of T-cell progenitor survival and cell-cycle entry by the pre-T-cell receptor. Immunol Rev 209:159-169. http://dx.doi.org/10.1111/j.0105-2896.2006.00343.x.
4. Ciofani M, Zuniga-Pflucker JC. 2007. The thymus as an inductive site for T lymphopoiesis. Annu Rev Cell Dev Biol 23:463-493. http://dx.doi.org/10.1146/annurev.cellbio.23.090506.123547.
5. Lucas JA, Felices M, Evans JW, Berg LJ. 2007. Subtle defects in pre-TCR signaling in the absence of the Tec kinase Itk. J Immunol 179:7561-7567. http://dx.doi.org/10.4049/jimmunol.179.11.7561.
6. Palacios EH, Weiss A. 2004. Function of the Src-family kinases, Lck and Fyn, in T-cell development and activation. Oncogene 23:7990-8000. http://dx.doi.org/10.1038/sj.onc.1208074.
7. Zhang W, Sommers CL, Burshtyn DN, Stebbins CC, DeJarnette JB, Trible RP, Grinberg A, Tsay HC, Jacobs HM, Kessler CM, Long EO, Love PE, Samelson LE. 1999. Essential role of LAT in T cell development. Immunity 10:323-332. http://dx.doi.org/10.1016/S1074-7613(00)80032-1.
8. Clements JL, Yang B, Ross-Barta SE, Eliason SL, Hrstka RF, Williamson RA, Koretzky GA. 1998. Requirement for the leukocyte-specific adapter protein SLP-76 for normal T cell development. Science 281:416-419. http://dx.doi.org/10.1126/science.281.5375.416.
9. Ravichandran KS, Lee KK, Songyang Z, Cantley LC, Burn P, Burakoff SJ. 1993. Interaction of Shc with the zeta chain of the T cell receptor upon T cell activation. Science 262:902-905. http://dx.doi.org/10.1126/science.8235613.
10. Trampont P, Zhang L, Ravichandran KS. 2006. ShcA mediates the dominant pathway to extracellular signal-regulated kinase activation during early thymic development. Mol Cell Biol 26:9035-9044. http://dx.doi.org/10.1128/MCB.00988-06.
11. Xi H, Kersh GJ. 2004. Early growth response gene 3 regulates thymocyte proliferation during the transition from CD4-CD8- to CD4+CD88+. J Immunol 172:964-971. http://dx.doi.org/10.4049/jimmunol.172.2.964.
12. Xi H, Schwartz R, Engel I, Murre C, Kersh GJ. 2006. Interplay between RORgammat, Egr3, and E proteins controls proliferation in response to pre-TCR signals. Immunity 24:813-826. http://dx.doi.org/10.1016/j.immuni.2006.03.023.
13. Ravichandran KS, Lorenz U, Shoelson SE, Burakoff SJ. 1995. Interaction of Shc with Grb2 regulates association of Grb2 with mSOS. Mol Cell Biol 15:593-600.
14. Lai KM, Pawson T. 2000. The ShcA phosphotyrosine docking protein sensitizes cardiovascular signaling in the mouse embryo. Genes Dev 14:1132-1145.
15. Zhang L, Camerini V, Bender TP, Ravichandran KS. 2002. A nonredundant role for the adapter protein Shc in thymic T cell development. Nat Immunol 3:749-755. http://dx.doi.org/10.1038/ni820.
16. Trampont PC, Tosello-Trampont AC, Shen Y, Duley AK, Sutherland AE, Bender TP, Littman DR, Ravichandran KS. 13 December 2009, posting date. CXCR4 acts as a costimulator during thymic beta-selection. Nat Immunol http://dx.doi.org/10.1038/ni.1830.
17. Massari ME, Murre C. 2000. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20:429-440. http://dx.doi.org/10.1128/MCB.20.2.429-440.2000.
18. Bain G, Cravatt CB, Loomans C, Alberola-Ila J, Hedrick SM, Murre C. 2001. Regulation of the helix-loop-helix proteins, E2A and Id3, by the Ras-ERK MAPK cascade. Nat Immunol 2:165-171. http://dx.doi.org/10.1038/84273.
19. Rothenberg EV, Taghon T. 2005. Molecular genetics of T cell development. Annu Rev Immunol 23:601-649. http://dx.doi.org/10.1146/annurev.immunol.23.021704.115737.
20. Gu JJ, Zhang N, He YW, Koleske AJ, Pendergast AM. 2007. Defective T cell development and function in the absence of Abelson kinases. J Immunol 179:7334-7343. http://dx.doi.org/10.4049/jimmunol.179.11.7334.
21. Schmitt TM, Zuniga-Pflucker JC. 2002. Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17:749-756. http://dx.doi.org/10.1016/S1074-7613(02)00474-0.
22. Ciofani M, Schmitt TM, Ciofani A, Michie AM, Cuburu N, Aublin A, Maryanski JL, Zuniga-Pflucker JC. 2004. Obligatory role for cooperative signaling by pre-TCR and Notch during thymocyte differentiation. J Immunol 172:5230-5239. http://dx.doi.org/10.4049/jimmunol.172.9.5230.
23. Murphy KM, Heimberger AB, Loh DY. 1990. Induction by antigen of intrathymic apoptosis of CD4+CD88+TCRlo thymocytes in vivo. Science 250:1720-1723. http://dx.doi.org/10.1126/science.2125367.
24. Molina TJ, Kishihara K, Siderovski DP, van Ewijk W, Narendran A, Timms E, Wakeham A, Paige CJ, Hartmann KU, Veillette A, Davidson D, Mak TW. 1992. Profound block in thymocyte development in mice lacking p56lck. Nature 357:161-164. http://dx.doi.org/10.1038/357161a0.
25. Walk SF, March ME, Ravichandran KS. 1998. Roles of Lck, Syk and ZAP-70 tyrosine kinases in TCR-mediated phosphorylation of the adapter protein Shc. Eur J Immunol 28:2265-2275. http://dx.doi.org/10.1002/(SICI)1521-4141(199808)28:08<2265::AID-IMMU2265>3.0.CO;2-P.
26. Mombaerts P, Anderson SJ, Perlmutter RM, Mak TW, Tonegawa S. 1994. An activated lck transgene promotes thymocyte development in RAG-1 mutant mice. Immunity 1:261-267. http://dx.doi.org/10.1016/1074-7613(94)90077-9.
27. Anderson SJ, Abraham KM, Nakayama T, Singer A, Perlmutter RM. 1992. Inhibition of T-cell receptor beta-chain gene rearrangement by overexpression of the non-receptor protein tyrosine kinase p56lck. EMBO J 11:4877-4886.
28. Aifantis I, Feinberg J, Fehling HJ, Di Santo JP, von Boehmer H. 1999. Early T cell receptor beta gene expression is regulated by the pre-T cell receptor-CD3 complex. J Exp Med 190:141-144. http://dx.doi.org/10.1084/jem.190.1.141.
29. Shinkai Y, Koyasu S, Nakayama K, Murphy KM, Loh DY, Reinherz EL, Alt FW. 1993. Restoration of T cell development in RAG-2-deficient mice by functional TCR transgenes. Science 259:822-825. http://dx.doi.org/10.1126/science.8430336.
30. Haks MC, Krimpenfort P, van den Brakel JH, Kruisbeek AM. 1999. Pre-TCR signaling and inactivation of p53 induces crucial cell survival pathways in pre-T cells. Immunity 11:91-101. http://dx.doi.org/10.1016/S1074-7613(00)80084-9.
31. Opferman JT. 2007. Life and death during hematopoietic differentiation. Curr Opin Immunol 19:497-502. http://dx.doi.org/10.1016/j.coi.2007.06.002.
32. Lord JD, McIntosh BC, Greenberg PD, Nelson BH. 1998. The IL-2 receptor promotes proliferation, bcl-2 and bcl-x induction, but not cell viability through the adapter molecule Shc. J Immunol 161:4627-4633.
33. Dose M, Khan I, Guo Z, Kovalovsky D, Krueger A, von Boehmer H, Khazaie K, Gounari F. 2006. c-Myc mediates pre-TCR-induced proliferation but not developmental progression. Blood 108:2669-2677. http://dx.doi.org/10.1182/blood-2006-02-005900.
34. Patrussi L, Savino MT, Pellegrini M, Paccani SR, Migliaccio E, Plyte S, Lanfrancone L, Pelicci PG, Baldari CT. 2005. Cooperation and selectivity of the two Grb2 binding sites of p52Shc in T-cell antigen receptor signaling to Ras family GTPases and Myc-dependent survival. Oncogene 24:2218-2228. http://dx.doi.org/10.1038/sj.onc.1208384.
35. Cairo S, De Falco F, Pizzo M, Salomoni P, Pandolfi PP, Meroni G. 2005. PML interacts with Myc, and Myc target gene expression is altered in PML-null fibroblasts. Oncogene 24:2195-2203. http://dx.doi.org/10.1038/sj.onc.1208338.
36. Sicinska E, Aifantis I, Le Cam L, Swat W, Borowski C, Yu Q, Ferrando AA, Levin SD, Geng Y, von Boehmer H, Sicinski P. 2003. Requirement for cyclin D3 in lymphocyte development and T cell leukemias. Cancer Cell 4:451-461. http://dx.doi.org/10.1016/S1535-6108(03)00301-5.
37. Haks MC, Lefebvre JM, Lauritsen JP, Carleton M, Rhodes M, Miyazaki T, Kappes DJ, Wiest DL. 2005. Attenuation of gammadeltaTCR signaling efficiently diverts thymocytes to the alphabeta lineage. Immunity 22:595-606. http://dx.doi.org/10.1016/j.immuni.2005.04.003.
38. Engel I, Johns C, Bain G, Rivera RR, Murre C. 2001. Early thymocyte development is regulated by modulation of E2A protein activity. J Exp Med 194:733-745. http://dx.doi.org/10.1084/jem.194.6.733.
39. Engel I, Murre C. 2001. The function of E- and Id proteins in lymphocyte development. Nat Rev Immunol 1:193-199. http://dx.doi.org/10.1038/35105060.
40. Pear WS, Miller JP, Xu L, Pui JC, Soffer B, Quackenbush RC, Pendergast AM, Bronson R, Aster JC, Scott ML, Baltimore D. 1998. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 92:3780-3792.
41. Tauchi T, Boswell HS, Leibowitz D, Broxmeyer HE. 1994. Coupling between p210bcr-abl and Shc and Grb2 adaptor proteins in hematopoietic cells permits growth factor receptor-independent link to ras activation pathway. J Exp Med 179:167-175. http://dx.doi.org/10.1084/jem.179.1.167.
42. Michie AM, Soh JW, Hawley RG, Weinstein IB, Zuniga-Pflucker JC. 2001. Allelic exclusion and differentiation by protein kinase C-mediated signals in immature thymocytes. Proc Natl Acad Sci U S A 98:609-614. http://dx.doi.org/10.1073/pnas.98.2.609.
43. Bettini M, Xi H, Milbrandt J, Kersh GJ. 2002. Thymocyte development in early growth response gene 1-deficient mice. J Immunol 169:1713-1720. http://dx.doi.org/10.4049/jimmunol.169.4.1713.
44. Engel I, Murre C. 2004. E2A proteins enforce a proliferation checkpoint in developing thymocytes. EMBO J 23:202-211. http://dx.doi.org/10.1038/sj.emboj.7600017.
45. Ikawa T, Kawamoto H, Goldrath AW, Murre C. 2006. E proteins and Notch signaling cooperate to promote T cell lineage specification and commitment. J Exp Med 203:1329-1342. http://dx.doi.org/10.1084/jem.20060268.
46. Gotoh N, Toyoda M, Shibuya M. 1997. Tyrosine phosphorylation sites at amino acids 239 and 240 of Shc are involved in epidermal growth factor-induced mitogenic signaling that is distinct from Ras/mitogen-activated protein kinase activation. Mol Cell Biol 17:1824-1831.