Activation of extracellular signal-regulated kinase but not of p38 mitogen-activated protein kinase pathways in lymphocytes requires allosteric activation of SOS

Molecular and Cellular Biology

Volumn 33, Issue 12, 2013, Pages 2470-2484

  Jun, Jesse E ^a   Yang, Ming ^b   Chen, Hang ^c   Chakraborty, Arup K ^b,c   Roose, Jeroen P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOLIPASE C DELTA; PROTEIN SOS1; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ALLOSTERISM; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; THYMOCYTE;

ANIMALS; CELL LINE; CHICKENS; DNA-BINDING PROTEINS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; MICE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SOS1 PROTEIN; T-LYMPHOCYTES;

EID: 84878968522     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01593-12     Document Type: Article

References (78)

1. Chang L, Karin M. 2001. Mammalian MAP kinase signalling cascades. Nature 410:37-40.
2. Marshall CJ. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185.
3. Santos SD, Verveer PJ, Bastiaens PI. 2007. Growth factor-induced MAPK network topology shapes Erk response determining PC-12 cell fate. Nat. Cell Biol. 9:324-330.
4. Ferrell JE, Jr, Machleder EM. 1998. The biochemical basis of an all-ornone cell fate switch in Xenopus oocytes. Science 280:895-898.
5. Markevich NI, Hoek JB, Kholodenko BN. 2004. Signaling switches and bistability arising from multisite phosphorylation in protein kinase cascades. J. Cell Biol. 164:353-359.
6. O'Shaughnessy EC, Palani S, Collins JJ, Sarkar CA. 2011. Tunable signal processing in synthetic MAP kinase cascades. Cell 144:119-131.
7. Tian T, Harding A, Inder K, Plowman S, Parton RG, Hancock JF. 2007. Plasma membrane nanoswitches generate high-fidelity Ras signal transduction. Nat. Cell Biol. 9:905-914.
8. Altan-Bonnet G, Germain RN. 2005. Modeling T cell antigen discrimination based on feedback control of digital ERK responses. PLoS Biol. 3:e356. doi:10.1371/journal.pbio.0030356.
9. Harding A, Tian T, Westbury E, Frische E, Hancock JF. 2005. Subcellular localization determines MAP kinase signal output. Curr. Biol. 15: 869-873.
10. Das J, Ho M, Zikherman J, Govern C, Yang M, Weiss A, Chakraborty AK, Roose JP. 2009. Digital signaling and hysteresis characterize ras activation in lymphoid cells. Cell 136:337-351.
11. Lin J, Harding A, Giurisato E, Shaw AS. 2009. KSR1 modulates the sensitivity of mitogen-activated protein kinase pathway activation in T cells without altering fundamental system outputs. Mol. Cell. Biol. 29:2082-2091.
12. Prasad A, Zikherman J, Das J, Roose JP, Weiss A, Chakraborty AK. 2009. Origin of the sharp boundary that discriminates positive and negative selection of thymocytes. Proc. Natl. Acad. Sci. U. S. A. 106:528-533.
13. Starr TK, Jameson SC, Hogquist KA. 2003. Positive and negative selection of T cells. Annu. Rev. Immunol. 21:139-176.
14. Genot E, Cantrell DA. 2000. Ras regulation and function in lymphocytes. Curr. Opin. Immunol. 12:289-294.
15. D'Ambrosio D, Cantrell DA, Frati L, Santoni A, Testi R. 1994. Involvement of p21ras activation in T cell CD69 expression. Eur. J. Immunol. 24:616-620.
16. Swan KA, Alberola-Ila J, Gross JA, Appleby MW, Forbush KA, Thomas JF, Perlmutter RM. 1995. Involvement of p21ras distinguishes positive and negative selection in thymocytes. EMBO J. 14:276-285.
17. Stone JC. 2011. Regulation and function of the RasGRP family of Ras activators in blood cells. Genes Cancer 2:320-334.
18. Dower NA, Stang SL, Bottorff DA, Ebinu JO, Dickie P, Ostergaard HL, Stone JC. 2000. RasGRP is essential for mouse thymocyte differentiation and TCR signaling. Nat. Immunol. 1:317-321.
19. Oh-hora M, Johmura S, Hashimoto A, Hikida M, Kurosaki T. 2003. Requirement for Ras guanine nucleotide releasing protein 3 in coupling phospholipase C-gamma2 to Ras in B cell receptor signaling. J. Exp. Med. 198:1841-1851.
20. Roose JP, Mollenauer M, Ho M, Kurosaki T, Weiss A. 2007. Unusual interplay of two types of Ras activators, RasGRP and SOS, establishes sensitive and robust Ras activation in lymphocytes. Mol. Cell. Biol. 27:2732-2745.
21. Buday L, Downward J. 1993. Epidermal growth factor regulates p21ras through the formation of a complex of receptor, Grb2 adapter protein, and Sos nucleotide exchange factor. Cell 73:611-620.
22. Lowenstein EJ, Daly RJ, Batzer AG, Li W, Margolis B, Lammers R, Ullrich A, Skolnik EY, Bar-Sagi D, Schlessinger J. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70:431-442.
23. Margarit SM, Sondermann H, Hall BE, Nagar B, Hoelz A, Pirruccello M, Bar-Sagi D, Kuriyan J. 2003. Structural evidence for feedback activation by Ras·GTP of the Ras-specific nucleotide exchange factor SOS. Cell 112:685-695.
24. Freedman TS, Sondermann H, Friedland GD, Kortemme T, Bar-Sagi D, Marqusee S, Kuriyan J. 2006. A Ras-induced conformational switch in the Ras activator Son of sevenless. Proc. Natl. Acad. Sci. U. S. A. 103: 16692-16697.
25. Chakraborty AK, Das J, Zikherman J, Yang M, Govern CC, Ho M, Weiss A, Roose J. 2009. Molecular origin and functional consequences of digital signaling and hysteresis during Ras activation in lymphocytes. Sci. Signal. 2:pt2. doi:10.1126/scisignal.266pt2.
26. Palmer E. 2003. Negative selection-clearing out the bad apples from the T-cell repertoire. Nat. Rev. Immunol. 3:383-391.
27. Fischer AM, Katayama CD, Pages G, Pouyssegur J, Hedrick SM. 2005. The role of erk1 and erk2 in multiple stages of T cell development. Immunity 23:431-443.
28. Gong Q, Cheng AM, Akk AM, Alberola-Ila J, Gong G, Pawson T, Chan AC. 2001. Disruption of T cell signaling networks and development by Grb2 haploid insufficiency. Nat. Immunol. 2:29-36.
29. Kortum RL, Sommers CL, Alexander CP, Pinski JM, Li W, Grinberg A, Lee J, Love PE, Samelson LE. 2011. Targeted Sos1 deletion reveals its critical role in early T-cell development. Proc. Natl. Acad. Sci. U. S. A. 108:12407-12412.
30. McGargill MA, Ch'en IL, Katayama CD, Pages G, Pouyssegur J, Hedrick SM. 2009. Cutting edge: extracellular signal-related kinase is not required for negative selection of developing T cells. J. Immunol. 183: 4838-4842.
31. Kortum RL, Sommers CL, Pinski JM, Alexander CP, Merrill RK, Li W, Love PE, Samelson LE. 2012. Deconstructing Ras signaling in the thymus. Mol. Cell. Biol. 32:2748-2759.
32. Sugawara T, Moriguchi T, Nishida E, Takahama Y. 1998. Differential roles of ERK and p38 MAP kinase pathways in positive and negative selection of T lymphocytes. Immunity 9:565-574.
33. Rincon M, Pedraza-Alva G. 2003. JNK and p38 MAP kinases in CD4 and CD8 T cells. Immunol. Rev. 192:131-142.
34. Werlen G, Hausmann B, Naeher D, Palmer E. 2003. Signaling life and death in the thymus: timing is everything. Science 299:1859-1863.
35. Riese MJ, Grewal J, Das J, Zou T, Patil V, Chakraborty AK, Koretzky GA. 2011. Decreased diacylglycerol metabolism enhances ERK activation and augments CD8 T cell functional responses. J. Biol. Chem. 286: 5254-5265.
36. Locasale JW, Shaw AS, Chakraborty AK. 2007. Scaffold proteins confer diverse regulatory properties to protein kinase cascades. Proc. Natl. Acad. Sci. U. S. A. 104:13307-13312.
37. Gillespie DT. 1977. Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 81:2340-2361.
38. Qian X, Vass WC, Papageorge AG, Anborgh PH, Lowy DR. 1998. N terminus of Sos1 Ras exchange factor: critical roles for the Dbl and pleckstrin homology domains. Mol. Cell. Biol. 18:771-778.
39. Boykevisch S, Zhao C, Sondermann H, Philippidou P, Halegoua S, Kuriyan J, Bar-Sagi D. 2006. Regulation of ras signaling dynamics by Sos-mediated positive feedback. Curr. Biol. 16:2173-2179.
40. Dong C, Davis RJ, Flavell RA. 2002. MAP kinases in the immune response. Annu. Rev. Immunol. 20:55-72.
41. Ebinu JO, Stang SL, Teixeira C, Bottorff DA, Hooton J, Blumberg PM, Barry M, Bleakley RC, Ostergaard HL, Stone JC. 2000. RasGRP links T-cell receptor signaling to Ras. Blood 95:3199-3203.
42. Waters SB, Holt KH, Ross SE, Syu LJ, Guan KL, Saltiel AR, Koretzky GA, Pessin JE. 1995. Desensitization of Ras activation by a feedback disassociation of the SOS-Grb2 complex. J. Biol. Chem. 270:20883-20886.
43. Porfiri E, McCormick F. 1996. Regulation of epidermal growth factor receptor signaling by phosphorylation of the ras exchange factor hSOS1. J. Biol. Chem. 271:5871-5877.
44. Corbalan-Garcia S, Yang SS, Degenhardt KR, Bar-Sagi D. 1996. Identification of the mitogen-activated protein kinase phosphorylation sites on human Sos1 that regulate interaction with Grb2. Mol. Cell. Biol. 16: 5674-5682.
45. Zhao H, Li YY, Fucini RV, Ross SE, Pessin JE, Koretzky GA. 1997. T cell receptor-induced phosphorylation of Sos requires activity of CD45, Lck, and protein kinase C, but not ERK. J. Biol. Chem. 272:21625-21634.
46. Kamioka Y, Yasuda S, Fujita Y, Aoki K, Matsuda M. 2010. Multiple decisive phosphorylation sites for the negative feedback regulation of SOS1 via ERK. J. Biol. Chem. 285:33540-33548.
47. Bhalla US, Ram PT, Iyengar R. 2002. MAP kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network. Science 297:1018-1023.
48. Sondermann H, Soisson SM, Boykevisch S, Yang SS, Bar-Sagi D, Kuriyan J. 2004. Structural analysis of autoinhibition in the Ras activator Son of sevenless. Cell 119:393-405.
49. Ashwell JD. 2006. The many paths to p38 mitogen-activated protein kinase activation in the immune system. Nat. Rev. Immunol. 6:532-540.
50. Salvador JM, Mittelstadt PR, Guszczynski T, Copeland TD, Yamaguchi H, Appella E, Fornace AJ, Jr, Ashwell JD. 2005. Alternative p38 activation pathway mediated by T cell receptor-proximal tyrosine kinases. Nat. Immunol. 6:390-395.
51. Mittelstadt PR, Yamaguchi H, Appella E, Ashwell JD. 2009. T cell receptor-mediated activation of p38{alpha} by mono-phosphorylation of the activation loop results in altered substrate specificity. J. Biol. Chem. 284:15469-15474.
52. Roose JP, Diehn M, Tomlinson MG, Lin J, Alizadeh AA, Botstein D, Brown PO, Weiss A. 2003. T cell receptor-independent basal signaling via Erk and Abl kinases suppresses RAG gene expression. PLoS Biol. 1:e53. doi:10.1371/journal.pbio.0000053.
53. Nimnual A, Bar-Sagi D. 2002. The two hats of SOS. Sci. STKE 2002:pe36. doi:10.1126/stke.2002.145.pe36.
54. Nimnual AS, Yatsula BA, Bar-Sagi D. 1998. Coupling of Ras and Rac guanosine triphosphatases through the Ras exchanger Sos. Science 279: 560-563.
55. Scita G, Nordstrom J, Carbone R, Tenca P, Giardina G, Gutkind S, Bjarnegard M, Betsholtz C, Di Fiore PP. 1999. EPS8 and E3B1 transduce signals from Ras to Rac. Nature 401:290-293.
56. Mettouchi A, Klein S, Guo W, Lopez-Lago M, Lemichez E, Westwick JK, Giancotti FG. 2001. Integrin-specific activation of Rac controls progression through the G(1) phase of the cell cycle. Mol. Cell 8:115-127.
57. Houtman JC, Yamaguchi H, Barda-Saad M, Braiman A, Bowden B, Appella E, Schuck P, Samelson LE. 2006. Oligomerization of signaling complexes by the multipoint binding of GRB2 to both LAT and SOS1. Nat. Struct. Mol. Biol. 13:798-805.
58. Soisson SM, Nimnual AS, Uy M, Bar-Sagi D, Kuriyan J. 1998. Crystal structure of the Dbl and pleckstrin homology domains from the human Son of sevenless protein. Cell 95:259-268.
59. Hart MJ, Eva A, Zangrilli D, Aaronson SA, Evans T, Cerione RA, Zheng Y. 1994. Cellular transformation and guanine nucleotide exchange activity are catalyzed by a common domain on the dbl oncogene product. J. Biol. Chem. 269:62-65.
60. Kuhne MR, Ku G, Weiss A. 2000. A guanine nucleotide exchange factorindependent function of Vav1 in transcriptional activation. J. Biol. Chem. 275:2185-2190.
61. Hashimoto A, Okada H, Jiang A, Kurosaki M, Greenberg S, Clark EA, Kurosaki T. 1998. Involvement of guanosine triphosphatases and phospholipase C-gamma2 in extracellular signal-regulated kinase, c-Jun NH2- terminal kinase, and p38 mitogen-activated protein kinase activation by the B cell antigen receptor. J. Exp. Med. 188:1287-1295.
62. Markegard E, Trager E, Yang CW, Zhang W, Weiss A, Roose JP. 2011. Basal LAT-diacylglycerol-RasGRP1 signals in T cells maintain TCRα gene expression. PLoS One 6:e25540. doi:10.1371/journal.pone.0025540.
63. Jirmanova L, Sarma DN, Jankovic D, Mittelstadt PR, Ashwell JD. 2009. Genetic disruption of p38α Tyr323 phosphorylation prevents T-cell receptor- mediated p38α activation and impairs interferon-gamma production. Blood 113:2229-2237.
64. Tybulewicz VL, Henderson RB. 2009. Rho family GTPases and their regulators in lymphocytes. Nat. Rev. Immunol. 9:630-644.
65. Welch HC, Coadwell WJ, Stephens LR, Hawkins PT. 2003. Phosphoinositide 3-kinase-dependent activation of Rac. FEBS Lett. 546:93-97.
66. Gerard A, van der Kammen RA, Janssen H, Ellenbroek SI, Collard JG. 2009. The Rac activator Tiam1 controls efficient T-cell trafficking and route of transendothelial migration. Blood 113:6138-6147.
67. Lambert JM, Lambert QT, Reuther GW, Malliri A, Siderovski DP, Sondek J, Collard JG, Der CJ. 2002. Tiam1 mediates Ras activation of Rac by a PI(3)K-independent mechanism. Nat. Cell Biol. 4:621-625.
68. Turner M, Billadeau DD. 2002. VAV proteins as signal integrators for multi-subunit immune-recognition receptors. Nat. Rev. Immunol. 2:476-486.
69. Han J, Luby-Phelps K, Das B, Shu X, Xia Y, Mosteller RD, Krishna UM, Falck JR, White MA, Broek D. 1998. Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine trisphosphates by Vav. Science 279:558-560.
70. Caloca MJ, Zugaza JL, Matallanas D, Crespo P, Bustelo XR. 2003. Vav mediates Ras stimulation by direct activation of the GDP/GTP exchange factor Ras GRP1. EMBO J. 22:3326-3336.
71. Reynolds LF, de Bettignies C, Norton T, Beeser A, Chernoff J, Tybulewicz VL. 2004. Vav1 transduces T cell receptor signals to the activation of the Ras/ERK pathway via LAT, Sos, and RasGRP1. J. Biol. Chem. 279: 18239-18246.
72. Zugaza JL, Caloca MJ, Bustelo XR. 2004. Inverted signaling hierarchy between RAS and RAC in T-lymphocytes. Oncogene 23:5823-5833.
73. Sherman E, Barr V, Manley S, Patterson G, Balagopalan L, Akpan I, Regan CK, Merrill RK, Sommers CL, Lippincott-Schwartz J, Samelson LE. 2011. Functional nanoscale organization of signaling molecules downstream of the T cell antigen receptor. Immunity 35:705-720.
74. Sylvain NR, Nguyen K, Bunnell SC. 2011. Vav1-mediated scaffolding interactions stabilize SLP-76 microclusters and contribute to antigen-dependentT cell responses. Sci. Signal. 4:ra14. doi:10.1126/scisignal.2001178.
75. Fu G, Vallee S, Rybakin V, McGuire MV, Ampudia J, Brockmeyer C, Salek M, Fallen PR, Hoerter JA, Munshi A, Huang YH, Hu J, Fox HS, Sauer K, Acuto O, Gascoigne NR. 2009. Themis controls thymocyte selection through regulation of T cell antigen receptor-mediated signaling. Nat. Immunol. 10:848-856.
76. Johnson AL, Aravind L, Shulzhenko N, Morgun A, Choi SY, Crockford TL, Lambe T, Domaschenz H, Kucharska EM, Zheng L, Vinuesa CG, Lenardo MJ, Goodnow CC, Cornall RJ, Schwartz RH. 2009. Themis is a member of a new metazoan gene family and is required for the completion of thymocyte positive selection. Nat. Immunol. 10:831-839.
77. Lesourne R, Uehara S, Lee J, Song KD, Li L, Pinkhasov J, Zhang Y, Weng NP, Wildt KF, Wang L, Bosselut R, Love PE. 2009. Themis, a T cell-specific protein important for late thymocyte development. Nat. Immunol. 10:840-847.
78. Warnecke N, Poltorak M, Kowtharapu BS, Arndt B, Stone JC, Schraven B, Simeoni L. 2012. TCR-mediated Erk activation does not depend on Sos and Grb2 in peripheral human T cells. EMBO Rep. 13:386-391.