Identification of RANBP16 and RANBP17 as novel interaction partners for the bHLH transcription factor E12

Journal of Cellular Biochemistry

Volumn 111, Issue 1, 2010, Pages 195-206

  Lee, Jun Ho ^a   Zhou, Shengli ^a   Smas, Cynthia M ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

BHLH transcription factor; CRM1; E box; E2A proteins (E12 and E47); Nucleocytoplasmic transport; RANBP16; RANBP17; Yeast two hybrid

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR E 12; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR E 47; CYCLIN DEPENDENT KINASE INHIBITOR 1; EXPORTIN 1; KARYOPHERIN BETA; PROTEIN RANBP 16; PROTEIN RANBP 17; TRANSCRIPTION FACTOR E2A; UNCLASSIFIED DRUG;

ARTICLE; GENE TARGETING; HUMAN; IMMUNOPRECIPITATION; MAMMAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; YEAST;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; GENES, REPORTER; HELA CELLS; HUMANS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RAN GTP-BINDING PROTEIN; TRANSCRIPTION FACTOR 3; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TWO-HYBRID SYSTEM TECHNIQUES;

MAMMALIA;

EID: 77957139564     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22689     Document Type: Article

References (62)

1. Bayly R, Chuen L, Currie RA, Hyndman BD, Casselman R, Blobel GA, LeBrun DP. 2004. E2A-PBX1 interacts directly with the KIX domain of CBP/p300 in the induction of proliferation in primary hematopoietic cells. J Biol Chem 279:55362-55371.
2. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. 1990. The protein Id: A negative regulator of helix-loop-helix DNA binding proteins. Cell 61:49-59. (Pubitemid 20134378)
3. Berger R, Dastugue N, Busson M, Van Den Akker J, Perot C, Ballerini P, Hagemeijer A, Michaux L, Charrin C, Pages MP, Mugneret F, Andrieux J, Talmant P, Helias C, Mauvieux L, Lafage-Pochitaloff M, Mozziconacci MJ, Cornillet-Lefebvre P, Radford I, Asnafi V, Bilhou-Nabera C, Nguyen Khac F, Leonard C, Speleman F, Poppe B, Bastard C, Taviaux S, Quilichini B, Herens C, Gregoire MJ, Cave H, Bernard OA. 2003. t(5;14)/HOX11L2-positive T-cell acute lymphoblastic leukemia. A collaborative study of the Groupe Francais de Cytogenetique Hematologique (GFCH). Leukemia 17:1851-1857.
4. Berkes CA, Tapscott SJ. 2005. MyoD and the transcriptional control of myogenesis. Semin Cell Dev Biol 16:585-595.
5. Bernard OA, Busson-LeConiat M, Ballerini P, Mauchauffe M, Della Valle, Monni V, Nguyen R, Khac F, Mercher T, Penard-Lacronique V, Pasturaud P, Gressin L, Heilig R, Daniel MT, Lessard M, Berger R. 2001. A new recurrent and specific cryptic translocation, t(5;14)(q35;q32), is associated with expression of the Hox11L2 gene in T acute lymphoblastic leukemia. Leukemia 15:1495-1504. (Pubitemid 32994666)
6. Chu C, Kohtz DS. 2001. Identification of the E2A gene products as regulatory targets of the G1 cyclin-dependent kinases. J Biol Chem 276:8524-8534.
7. Cook A, Bono F, Jinek M, Conti E. 2007. Structural biology of nucleocytoplasmic transport. Annu Rev Biochem 76:647-671.
8. Desprez PY, Sumida T, Coppe JP. 2003. Helix-loop-helix proteins in mammary gland development and breast cancer. J Mammary Gland Biol Neoplasia 8:225-239. (Pubitemid 38129944)
9. Dorfman J, Macara IG. 2008. STRADalpha regulates LKB1 localization by blocking access to importin-alpha, and by association with Crm1 and exportin-7. Mol Biol Cell 19:1614-1626.
10. Eckner R, Yao TP, Oldread E, Livingston DM. 1996. Interaction and functional collaboration of p300/CBP and bHLH proteins in muscle and B-cell differentiation. Genes Dev 10:2478-2490. (Pubitemid 26341882)
11. Fabbro M, Henderson BR. 2003. Regulation of tumor suppressors by nuclearcytoplasmic shuttling. Exp Cell Res 282:59-69.
12. French BA, Chow KL, Olson EN, Schwartz RJ. 1991. Heterodimers of myogenic helix-loop- helix regulatory factors and E12 bind a complex element governing myogenic induction of the avian cardiac alpha-actin promoter. Mol Cell Biol 11:2439-2450.
13. Funato N, Ohtani K, Ohyama K, Kuroda T, Nakamura M. 2001. Common regulation of growth arrest and differentiation of osteoblasts by helix-loophelix factors. Mol Cell Biol 21:7416-7428.
14. Funato N, Ohyama K, Kuroda T, Nakamura M. 2003. Basic helix-loop-helix transcription factor epicardin/capsulin/Pod-1 suppresses differentiation by negative regulation of transcription. J Biol Chem 278:7486-7493. (Pubitemid 36800755)
15. Funk WD, Ouellette M, Wright WE. 1991. Molecular biology of myogenic regulatory factors. Mol Biol Med 8:185-195.
16. Glick E, Leshkowitz D, Walker MD. 2000. Transcription factor BETA2 acts cooperatively with E2A and PDX1 to activate the insulin gene promoter. J Biol Chem 275:2199-2204.
17. Gorlich D, Pante N, Kutay U, Aebi U, Bischoff FR. 1996. Identification of different roles for RanGDP and RanGTP in nuclear protein import. EMBO J 15:5584-5594. (Pubitemid 26385618)
18. Gould KA, Bresnick EH. 1998. Sequence determinants of DNA binding by the hematopoietic helix-loop-helix transcription factor TAL1: Importance of sequences flanking the E-box core. Gene Expr 7:87-101.
19. Greenbaum S, Zhuang Y. 2002. Regulation of early lymphocyte development by E2A family proteins. Semin Immunol 14:405-414.
20. Hansen-Hagge TE, Schafer M, Kiyoi H, Morris SW, Whitlock JA, Koch P, Bohlmann I, Mahotka C, Bartram CR, Janssen JW. 2002. Disruption of the RanBP17/Hox11L2 region by recombination with the TCRdelta locus in acute lymphoblastic leukemias with t(5;14)(q34;q11). Leukemia 16:2205-2212.
21. Hikima J, Middleton DL, Wilson MR, Miller NW, Clem LW, Warr GW. 2005. Regulation of immunoglobulin gene transcription in a teleost fish: Identification, expression and functional properties of E2A in the channel catfish. Immunogenetics 57:273-282.
22. Hsu HL, Huang L, Tsan JT, Funk W, Wright WE, Hu JS, Kingston RE, Baer R. 1994. Preferred sequences for DNA recognition by the TAL1 helix-loop-helix proteins. Mol Cell Biol 14:1256-1265. (Pubitemid 24984256)
23. Huggins GS, Chin MT, Sibinga NE, Lee SL, Haber E, Lee ME. 1999. Characterization of the mUBC9-binding sites required for E2A protein degradation. J Biol Chem 274:28690-28696.
24. Kau TR, Way JC, Silver PA. 2004. Nuclear transport and cancer: From mechanism to intervention. Nat Rev Cancer 4:106-117.
25. Kim W, Kook S, Kim DJ, Teodorof C, Song WK. 2004. The 31-kDa caspase-generated cleavage product of p130cas functions as a transcriptional repressor of E2A in apoptotic cells. J Biol Chem 279:8333-8342. (Pubitemid 38294725)
26. Koch P, Bohlmann I, Schafer M, Hansen-Hagge TE, Kiyoi H, Wilda M, Hameister H, Bartram CR, Janssen JW. 2000. Identification of a novel putative Ran-binding protein and its close homologue. Biochem Biophys Res Commun 278:241-249.
27. Kutay U, Bischoff FR, Kostka S, Kraft R, Gorlich D. 1997. Export of importin alpha from the nucleus is mediated by a specific nuclear transport factor. Cell 90:1061-1071.
28. Kutay U, Hartmann E, Treichel N, Calado A, Carmo-Fonseca M, Prehn S, Kraft R, Gorlich D, Bischoff FR. 2000. Identification of two novel RanGTP-binding proteins belonging to the importin beta superfamily. J Biol Chem 275:40163-40168.
29. 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. (Pubitemid 27340071)
30. Lassar AB, Davis RL, Wright WE, Kadesch T, Murre C, Voronova A, Baltimore D, Weintraub H. 1991. Functional activity of myogenic HLH proteins requires hetero-oligomerization with E12/E47-like proteins in vivo. Cell 66:305-315.
31. Lee JE. 1997. NeuroD and neurogenesis. Dev Neurosci 19:27-32.
32. Lingbeck JM, Trausch-Azar JS, Ciechanover A, Schwartz AL. 2008. In vivo interactions of MyoD, Id1, and E2A proteins determined by acceptor photo-bleaching fluorescence resonance energy transfer. FASEB J 22:1694-1701.
33. Liu Y, Encinas M, Comella JX, Aldea M, Gallego C. 2004. Basic helix-loophelix proteins bind to TrkB and p21(Cip1) promoters linking differentiation and cell cycle arrest in neuroblastoma cells. Mol Cell Biol 24:2662-2672.
34. MacLeod RA, Nagel S, Kaufmann M, Janssen JW, Drexler HG. 2003. Activation of HOX11L2 by juxtaposition with 3′-BCL11B in an acute lymphoblastic leukemia cell line (HPB- ALL) with t(5;14)(q35;q32.2). Genes Chromosomes Cancer 37:84-91. (Pubitemid 36417925)
35. Massari ME, Murre C. 2000. Helix-loop-helix proteins: Regulators of transcription in eucaryotic organisms. Mol Cell Biol 20:429-440.
36. Massari ME, Grant PA, Pray-Grant MG, Berger SL, Workman JL, Murre C. 1999. A conserved motif present in a class of helix-loop-helix proteins activates transcription by direct recruitment of the SAGA complex. Mol Cell 4:63-73.
37. Mingot JM, Bohnsack MT, Jakle U, Gorlich D. 2004. Exportin 7 defines a novel general nuclear export pathway. EMBO J 23:3227-3236. (Pubitemid 39209147)
38. Mitsui K, Shirakata M, Paterson BM. 1993. Phosphorylation inhibits the DNA-binding activity of MyoD homodimers but not MyoD-E12 heterodimers. J Biol Chem 268:24415-24420.
39. Murre C, McCaw PS, Vaessin H, Caudy M, Jan LY, Jan YN, Cabrera CV, Buskin JN, Hauschka SD, Lassar AB., et al. 1989. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58:537-544.
40. Murre C, Bain G, van Dijk MA, Engel I, Furnari BA, Massari ME, Matthews JR, Quong MW, Rivera RR, Stuiver MH. 1994. Structure and function of helixloop- helix proteins. Biochim Biophys Acta 1218:129-135.
41. Mutoh H, Fung BP, Naya FJ, Tsai MJ, Nishitani J, Leiter AB. 1997. The basic helix-loop-helix transcription factor BETA2/NeuroD is expressed in mammalian enteroendocrine cells and activates secretin gene expression. Proc Natl Acad Sci USA 94:3560-3564. (Pubitemid 27180411)
42. Neufeld B, Grosse-Wilde A, Hoffmeyer A, Jordan BW, Chen P, Dinev D, Ludwig S, Rapp UR. 2000. Serine/Threonine kinases 3pK and MAPK-activated protein kinase 2 interact with the basic helix-loop-helix transcription factor E47 and repress its transcriptional activity. J Biol Chem 275:20239-20242.
43. Norton JD. 2000. ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J Cell Sci 113(Pt 22): 3897-3905.
44. Norton JD, Deed RW, Craggs G, Sablitzky F. 1998. Id helix-loop-helix proteins in cell growth and differentiation. Trends Cell Biol 8:58-65.
45. Ossareh-Nazari B, Dargemont C. 1999. Domains of Crm1 involved in the formation of the Crm1, RanGTP, and leucine-rich nuclear export sequences trimeric complex. Exp Cell Res 252:236-241. (Pubitemid 29485142)
46. Perry C, Soreq H. 2002. Transcriptional regulation of erythropoiesis. Fine tuning of combinatorial multi-domain elements. Eur J Biochem 269:3607-3618.
47. Petosa C, Schoehn G, Askjaer P, Bauer U, Moulin M, Steuerwald U, Soler- Lopez M, Baudin F, Mattaj IW, Muller CW. 2004. Architecture of CRM1/ Exportin1 suggests how cooperativity is achieved during formation of a nuclear export complex. Mol Cell 16:761-775.
48. Prabhu S, Ignatova A, Park ST, Sun XH. 1997. Regulation of the expression of cyclin-dependent kinase inhibitor p21 by E2A and Id proteins. Mol Cell Biol 17:5888-5896. (Pubitemid 27411095)
49. Quong MW, Romanow WJ, Murre C. 2002. E protein function in lymphocyte development. Annu Rev Immunol 20:301-322.
50. Saarikettu J, Sveshnikova N, Grundstrom T. 2004. Calcium/calmodulin inhibition of transcriptional activity of E-proteins by prevention of their binding to DNA. J Biol Chem 279:41004-41011.
51. 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 USA 106:1930-1935.
52. Shirakata M, Paterson BM. 1995. The E12 inhibitory domain prevents homodimer formation and facilitates selective heterodimerization with the MyoD family of gene regulatory factors. EMBO J 14:1766-1772.
53. 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.
54. Su XY, Della-Valle V, Andre-Schmutz I, Lemercier C, Radford-Weiss I, Ballerini P, Lessard M, Lafage-Pochitaloff M, Mugneret F, Berger R, Romana SP, Bernard OA, Penard-Lacronique V. 2006. HOX11L2/TLX3 is transcriptionally activated through T-cell regulatory elements downstream of BCL11B as a result of the t(5;14)(q35;q32). Blood 108:4198-4201.
55. Sun XH, Baltimore D. 1991. An inhibitory domain of E12 transcription factor prevents DNA binding in E12 homodimers but not in E12 heterodimers. Cell 64:459-470. (Pubitemid 121001269)
56. Sun R, Su Y, Zhao X, Qi J, Luo X, Yang Z, Yao Y, Xia Z. 2009. Human calcium/calmodulin- dependent serine protein kinase regulates the expression of p21 via the E2A transcription factor. Biochem J 419:457-466.
57. Turner EC, Cureton CH, Weston CJ, Smart OS, Allemann RK. 2004. Controlling the DNA binding specificity of bHLH proteins through intramolecular interactions. Chem Biol 11:69-77.
58. Venuti JM, Cserjesi P. 1996. Molecular embryology of skeletal myogenesis. Curr Top Dev Biol 34:169-206.
59. Yagita K, Tamanini F, Yasuda M, Hoeijmakers JH, van der Horst GT, Okamura H. 2002. Nucleocytoplasmic shuttling and mCRY-dependent inhibition of ubiquitylation of the mPER2 clock protein. EMBO J 21: 1301-1314.
60. Yokota Y, Mori S. 2002. Role of Id family proteins in growth control. J Cell Physiol 190:21-28.
61. Yoneda Y. 2000. Nucleocytoplasmic protein traffic and its significance to cell function. Genes Cells 5:777-787.
62. Yutzey KE, Konieczny SF. 1992. Different E-box regulatory sequences are functionally distinct when placed within the context of the troponin I enhancer. Nucleic Acids Res 20:5105-5113.