Biochemical and phosphoproteomic analysis of the helix-loop-helix protein E47

Molecular and Cellular Biology

Volumn 32, Issue 9, 2012, Pages 1671-1682

  Teachenor, Robert ^a   Beck, Kristina ^a,b   Wright, Lilyan Y T ^a   Shen, Zhouxin ^a   Briggs, Steven P ^a   Murre, Cornelis ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HELIX LOOP HELIX PROTEIN; HELIX LOOP HELIX PROTEIN E47; INHIBITOR OF DIFFERENTIATION 1; INHIBITOR OF DIFFERENTIATION 2; INHIBITOR OF DIFFERENTIATION 3; INHIBITOR OF DIFFERENTIATION 4; INHIBITOR OF DIFFERENTIATION PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELL MATURATION; CHEMICAL ANALYSIS; MASS SPECTROMETRY; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEOMICS;

14-3-3 PROTEINS; AMINO ACID SEQUENCE; ANIMALS; B-LYMPHOCYTES; BASE SEQUENCE; CELL DIFFERENTIATION; CELL LINE; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; PROTEIN BINDING; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-AKT; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTOR 3;

EID: 84861424634     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.06452-11     Document Type: Article

References (52)

1. Adams MD, et al. 1991. Complementary DNA sequencing: expressed sequence tags and human genome project. Science 252:1651-1656.
2. Bain G, et al. 1994. E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 79:885-892.
3. Beck K, Peak MM, Ota T, Nemazee D, Murre C. 2009. Distinct roles for E12 and E47 in B cell specification and the sequential rearrangement of immunoglobulin light chain loci. J. Exp. Med. 206:2271-2284.
4. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. 1990. The protein Id: a negative regulator of helix-loop-helixDNAbinding proteins. Cell 61:49-59.
5. Borghesi L, et al. 2005. E47 is required for V(D)J recombinase activity in common lymphoid progenitors. J. Exp. Med. 202:1669-1677.
6. Bradney C, et al. 2003. Regulation of E2A activities by histone acetyltransferases in B lymphocyte development. J. Biol. Chem. 278:2370-2376.
7. Chen M, Manley JL. 2009. Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat. Rev. Mol. Cell Biol. 10:741-754.
8. de Pooter RF, Kee BL. 2010. E proteins and the regulation of early lymphocyte development. Immunol. Rev. 238:93-109.
9. Dias S, Mansson R, Gurbuxani S, Sigvardsson M, Kee BL. 2008. E2A proteins promote development of lymphoid-primed multipotent progenitors. Immunity 29:217-227.
10. Greenbaum S, Zhuang Y. 2002. Identification of E2A target genes in B lymphocyte development by using a gene tagging-based chromatin immunoprecipitation system. Proc. Natl. Acad. Sci. U. S. A. 99:15030-15035.
11. Inlay MA, et al. 2009. Ly6d marks the earliest stage of B-cell specification and identifies the branchpoint between B-cell and T-cell development. Genes Dev. 23:2376-2381.
12. κ rearrangement. J. Exp. Med. 200:1205-1211.
13. Johnson SE, Wang X, Hardy S, Taparowsky EJ, Konieczny SF. 1996. Casein kinase II increases the transcriptional activities of MRF4 and MyoD independently of their direct phosphorylation. Mol. Cell. Biol. 16:1604-1613.
14. King AM, Van der Put E, Blomberg BB, Riley RL. 2007. Accelerated Notch-dependent degradation of E47 proteins in aged B cell precursors is associated with increased ERK MAPK activation. J. Immunol. 178:3521-3529.
15. Kwon K, et al. 2008. Instructive role of the transcription factor E2A in early B lymphopoiesis and germinal center B cell development. Immunity 28:751-762.
16. Lakso M, et al. 1996. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. U. S. A. 93:5860-5865.
17. Langlands K, Yin X, Anand G, Prochownik EV. 1997. Differential interactions of Id proteins with basic-helix-loop-helix transcription factors. J. Biol. Chem. 272:19785-19793.
18. Lazorchak A, Jones ME, Zhuang Y. 2005. New insights into E-protein function in lymphocyte development. Trends Immunol. 26:334-338.
19. Lin YC, et al. 2010. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat. Immunol. 11:635-643.
20. Loveys DA, Streiff MB, Kato GJ. 1996. E2A basic-helix-loop-helix transcription factors are negatively regulated by serum growth factors and by the Id3 protein. Nucleic Acids Res. 24:2813-2820.
21. Mandel EM, Grosschedl R. 2010. Transcription control of early B cell differentiation. Curr. Opin. Immunol. 22:161-167.
22. Massari ME, Murre C. 2000. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell. Biol. 20:429-440.
23. Mercer EM, Lin YC, Murre C. 2011. Factors and networks that underpin early hematopoiesis. Semin. Immunol. 23:317-325.
24. Miyazaki M, et al. 2011. The opposing roles of the transcription factor E2A and its antagonist Id3 that orchestrate and enforce the naive fate of T cells. Nat. Immunol. 12:992-1001.
25. Murre C. 2005. Helix-loop-helix proteins and lymphocyte development. Nat. Immunol. 6:1079-1086.
26. Murre C, McCaw PS, Baltimore D. 1989. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 56:777-783.
27. Muslin AJ, Tanner JW, Allen PM, Shaw AS. 1996. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84:889-897.
28. Nie L, Xu M, Vladimirova A, Sun XH. 2003. Notch-induced E2A ubiquitination and degradation are controlled by MAP kinase activities. EMBO J. 22:5780-5792.
29. Novak R, Jacob E, Haimovich J, Avni O, Melamed D. 2010. The MAPK/ERK and PI3K pathways additively coordinate the transcription of recombination-activating genes in B lineage cells. J. Immunol. 185:3239-3247.
30. Nutt SL, Kee BL. 2007. The transcriptional regulation of B cell lineage commitment. Immunity 26:715-725.
31. Omori SA, et al. 2006. Regulation of class-switch recombination and plasma cell differentiation by phosphatidylinositol 3-kinase signaling. Immunity 25:545-557.
32. Page JL, Wang X, Sordillo LM, Johnson SE. 2004. MEKK1 signaling through p38 leads to transcriptional inactivation of E47 and repression of skeletal myogenesis. J. Biol. Chem. 279:30966-30972.
33. Qiu Y, Sharma A, Stein R. 1998. p300 mediates transcriptional stimulation by the basic helix-loop-helix activators of the insulin gene. Mol. Cell. Biol. 18:2957-2964.
34. Quong MW, Harris DP, Swain SL, Murre C. 1999. E2A activity is induced during B-cell activation to promote immunoglobulin class switch recombination. EMBO J. 18:6307-6318.
35. Quong MW, et al. 2004. Receptor editing and marginal zone B cell development are regulated by the helix-loop-helix protein, E2A. J. Exp. Med. 199:1101-1112.
36. Riechmann V, van Cruchten I, Sablitzky F. 1994. The expression pattern of Id4, a novel dominant negative helix-loop-helix protein, is distinct from Id1, Id2 and Id3. Nucleic Acids Res. 22:749-755.
37. Rivera R, Murre C. 2001. The regulation and function of the Id proteins in lymphocyte development. Oncogene 20:8308-8316.
38. Rivera RR, Johns CP, Quan J, Johnson RS, Murre C. 2000. Thymocyte selection is regulated by the helix-loop-helix inhibitor protein, Id3. Immunity 12:17-26.
39. Ruzinova MB, Benezra R. 2003. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 13:410-418.
40. Sayegh CE, Quong MW, Agata Y, Murre C. 2003. E-proteins directly regulate expression of activation-induced deaminase in mature B cells. Nat. Immunol. 4:586-593.
41. Schwartz R, Engel I, Fallahi-Sichani M, Petrie HT, Murre C. 2006. Gene expression patterns define novel roles for E47 in cell cycle progression, cytokine-mediated signaling, and T lineage development. Proc. Natl. Acad. Sci. U. S. A. 103:9976-9981.
42. Semerad CL, Mercer EM, Inlay MA, Weissman IL, Murre C. 2009. E2A proteins maintain the hematopoietic stem cell pool and promote the maturation of myelolymphoid and myeloerythroid progenitors. Proc. Natl. Acad. Sci. U. S. A. 106:1930-1935.
43. Sloan SR, Shen CP, McCarrick-Walmsley R, Kadesch T. 1996. Phosphorylation of E47 as a potential determinant of B-cell-specific activity. Mol. Cell. Biol. 16:6900-6908.
44. Sun XH, Copeland NG, Jenkins NA, Baltimore D. 1991. Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol. Cell. Biol. 11:5603-5611.
45. Tzivion G, Avruch J. 2002. 14-3-3 Proteins: active cofactors in cellular regulation by serine/threonine phosphorylation. J. Biol. Chem. 277:3061-3064.
46. Welinder E, et al. 2011. The transcription factors E2A and HEB act in concert to induce the expression of FOXO1 in the common lymphoid progenitor. Proc. Natl. Acad. Sci. U. S. A. 108:17402-17407.
47. Yan W, et al. 1997. High incidence of T-cell tumors in E2A-null mice and E2A/Id1 double-knockout mice. Mol. Cell. Biol. 17:7317-7327.
48. Yang Q, et al. 2008. E47 controls the developmental integrity and cell cycle quiescence of multipotential hematopoietic progenitors. J. Immunol. 181:5885-5894.
49. Zhang J, Kalkum M, Yamamura S, Chait BT, Roeder RG. 2004. E protein silencing by the leukemogenic AML1-ETO fusion protein. Science 305:1286-1289.
50. Zhang SH, Kobayashi R, Graves PR, Piwnica-Worms H, Tonks NK. 1997. Serine phosphorylation-dependent association of the band 4.1-related protein-tyrosine phosphatase PTPH1 with 14-3-3β protein. J. Biol. Chem. 272:27281-27287.
51. Zhuang Y, Jackson A, Pan L, Shen K, Dai M. 2004. Regulation of E2A gene expression in B-lymphocyte development. Mol. Immunol. 40:1165-1177.
52. Zhuang Y, Soriano P, Weintraub H. 1994. The helix-loop-helix gene E2A is required for B cell formation. Cell 79:875-884.