Coordinated transcriptional regulation of hspa1a gene by multiple transcription factors: Crucial roles for HSF-1, NF-Y, NF-κB, and CREB

Journal of Molecular Biology

Volumn 426, Issue 1, 2014, Pages 116-135

  Sasi, Binu K ^a   Sonawane, Parshuram J ^a   Gupta, Vinayak ^a   Sahu, Bhavani S ^a   Mahapatra, Nitish R ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY MADRAS   (India)

Author keywords

gene expression; heat shock protein; regulatory motifs; transcription factors

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FORSKOLIN; HEAT SHOCK TRANSCRIPTION FACTOR 1; I KAPPA B; NUCLEAR FACTOR Y;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ELECTROPHORETIC MOBILITY; GENE; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEART MUSCLE ISCHEMIA; HSPA1A GENE; HUMAN; HUMAN CELL; MYOBLAST; PRIORITY JOURNAL; PROTEIN MOTIF; TRANSACTIVATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

EID: 84890860946     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.09.008     Document Type: Article

References (68)

1. C.M. Milner, and R.D. Campbell Structure and expression of the three MHC-linked HSP70 genes Immunogenetics 32 1990 242 251
2. C.A. Sargent, I. Dunham, J. Trowsdale, and R.D. Campbell Human major histocompatibility complex contains genes for the major heat shock protein HSP70 Proc Natl Acad Sci U S A 86 1989 1968 1972
3. A. Goate, D. Cooper, C. Hall, T.C. Leung, E. Solomon, and L. Lim Localization of a human heat-shock HSP 70 gene sequence to chromosome 6 and detection of two other loci by somatic-cell hybrid and restriction fragment length polymorphism analysis Hum Genet 75 1987 123 128
4. G. Harrison, H. Drabkin, F.-T. Kao, J. Hartz, I. Hart, and E.Y. Chu et al. Chromosomal location of human genes encoding major heat-shock protein HSP70 Somat Cell Mol Genet 13 1987 119 130
5. C.R. Hunt, D.L. Gasser, D.D. Chaplin, J.C. Pierce, and C.A. Kozak Chromosomal localization of five murine HSP70 gene family members: Hsp, 70.1, Hsp70-2, Hsp70-3, Hsc70t, and Grp78 Genomics 16 1993 193 198
6. M. Snoek, M. Jansen, M.G. Olavesen, R.D. Campbell, C. Teuscher, and H. van Vugt Three Hsp70 genes are located in the C4-H-2D region: possible candidates for the Orch-1 locus Genomics 15 1993 350 356
7. L. Huang, N.F. Mivechi, and D. Moskophidis Insights into regulation and function of the major stress-induced hsp70 molecular chaperone in vivo: analysis of mice with targeted gene disruption of the hsp70.1 orhsp70.3 gene Mol Cell Biol 21 2001 8575 8591
8. C. Hunt, and S. Calderwood Characterization and sequence of a mouse hsp70 gene and its expression in mouse cell lines Gene 87 1990 199 204
9. S.K. Calderwood Heat shock proteins in breast cancer progression - a suitable case for treatment? Int J Hyperthermia 26 2010 681 685
10. J.G. Kiang, and G.C. Tsokos Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology Pharmacol Ther 80 1998 183 201
11. J. Kocsis, B. Madaras, E.K. Toth, G. Fust, and Z. Prohaszka Serum level of soluble 70-kD heat shock protein is associated with high mortality in patients with colorectal cancer without distant metastasis Cell Stress Chaperones 15 2010 143 151
12. S.M. Chafekar, and M.L. Duennwald Impaired heat shock response in cells expressing full-length polyglutamine-expanded huntingtin PLoS One 7 2012 e37929
13. X. Zhang, Z. Xu, L. Zhou, Y. Chen, M. He, and L. Cheng et al. Plasma levels of Hsp70 and anti-Hsp70 antibody predict risk of acute coronary syndrome Cell Stress Chaperones 15 2010 675 686
14. C.R. Hunt, D.J. Dix, G.G. Sharma, R.K. Pandita, A. Gupta, and M. Funk et al. Genomic instability and enhanced radiosensitivity in Hsp70.1- and Hsp70.3-deficient mice Mol Cell Biol 24 2004 899 911
15. Y.-K. Kim, J. Suarez, Y. Hu, P.M. McDonough, C. Boer, and D.J. Dix et al. Deletion of the inducible 70-kDa heat shock protein genes in mice impairs cardiac contractile function and calcium handling associated with hypertrophy Circulation 113 2006 2589 2597
16. M. He, H. Guo, X. Yang, X. Zhang, L. Zhou, and L. Cheng et al. Functional SNPs in HSPA1A gene predict risk of coronary heart disease PLoS One 4 2009 e4851
17. H. Guo, Q. Deng, C. Wu, L. Hu, S. Wei, and P. Xu et al. Variations in HSPA1B at 6p21.3 are associated with lung cancer risk and prognosis in Chinese populations Cancer Res 71 2011 7576 7586
18. R.S. Friese, P. Mahboubi, N.R. Mahapatra, S.K. Mahata, N.J. Schork, and G.W. Schmid-Schonbein et al. Common genetic mechanisms of blood pressure elevation in two independent rodent models of human essential hypertension Am J Hypertens 18 2005 633 652
19. R. Mantovani A survey of 178 NF-Y binding CCAAT boxes Nucleic Acids Res 26 1998 1135 1143
20. L.S. Lum, L.A. Sultzman, R.J. Kaufman, D.I. Linzer, and B.J. Wu A cloned human CCAAT-box-binding factor stimulates transcription from the human hsp70 promoter Mol Cell Biol 10 1990 6709 6717
21. W.D. Morgan Transcription factor Sp1 binds to and activates a human hsp70 gene promoter Mol Cell Biol 9 1989 4099 4104
22. M. Tranter, X. Ren, T. Forde, M.E. Wilhide, J. Chen, and M.A. Sartor et al. NF-kB driven cardioprotective gene programs; Hsp70.3 and cardioprotection after late ischemic preconditioning J Mol Cell Cardiol 49 2010 664 672
23. C. Imbriano, F. Bolognese, A. Gurtner, G. Piaggio, and R. Mantovani HSP-CBF Is an NF-Y-dependent coactivator of the heat shock promoters CCAAT boxes J Biol Chem 276 2001 26332 26339
24. M. Bienz A CCAAT box confers cell-type-specific regulation on the Xenopus hsp70 gene in oocytes Cell 46 1986 1037 1042
25. J.A. DiDonato, M. Hayakawa, D.M. Rothwarf, E. Zandi, and M. Karin A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB Nature 388 1997 548 554
26. F. Mercurio, H. Zhu, B.W. Murray, A. Shevchenko, B.L. Bennett, and J.W. Li et al. IKK-1 and IKK-2: cytokine-activated IκB kinases essential for NF-κB activation Science 278 1997 860 866
27. L. Osborn, S. Kunkel, and G.J. Nabel Tumor necrosis factor alpha and interleukin 1 stimulate the human immunodeficiency virus enhancer by activation of the nuclear factor kappa B Proc Natl Acad Sci U S A 86 1989 2336 2340
28. T. Pfeuffer, B. Gaugler, and H. Metzger Isolation of homologous and heterologous complexes between catalytic and regulatory components of adenylate cyclase by forskolin-Sepharose FEBS Lett 164 1983 154 160
29. R.D. Huang, M.F. Smith, and W.L. Zahler Inhibition of forskolin-activated adenylate cyclase by ethanol and other solvents J Cyclic Nucleotide Res 8 1982 385 394
30. K. Abravaya, B. Phillips, and R.I. Morimoto Heat shock-induced interactions of heat shock transcription factor and the human hsp70 promoter examined by in vivo footprinting Mol Cell Biol 11 1991 586 592
31. K. Abravaya, M.P. Myers, S.P. Murphy, and R.I. Morimoto The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression Genes Dev 6 1992 1153 1164
32. F. Le Masson, and E. Christians HSFs and regulation of Hsp70.1 (Hspa1b) in oocytes and preimplantation embryos: new insights brought by transgenic and knockout mouse models Cell Stress Chaperones 16 2011 275 285
33. H. Pelham Activation of heat-shock genes in eukaryotes Trends Genet 1 1985 31 35
34. G. Wiederrecht, D.J. Shuey, W.A. Kibbe, and C.S. Parker The Saccharomyces and Drosophila heat shock transcription factors are identical in size and DNA binding properties Cell 48 1987 507 515
35. C. Wu, S. Wilson, B. Walker, I. Dawid, T. Paisley, and V. Zimarino et al. Purification and properties of Drosophila heat shock activator protein Science 238 1987 1247 1253
36. Y. Kabe, J. Yamada, H. Uga, Y. Yamaguchi, T. Wada, and H. Handa NF-Y is essential for the recruitment of RNA polymerase II and inducible transcription of several CCAAT box-containing genes Mol Cell Biol 25 2005 512 522
37. R. Mantovani The molecular biology of the CCAAT-binding factor NF-Y Gene 239 1999 15 27
38. A. Ronchi, M. Bellorini, N. Mongelli, and R. Mantovani CCAAT-box binding protein NF-Y (CBF, CP1)recognizes the minor groove and distorts DNA Nucleic Acids Res 23 1995 4565 4572
39. R.H. Kim, and J. Sodek Transcription of the bone sialoprotein gene is stimulated by v-Src acting through an inverted CCAAT box Cancer Res 59 1999 565 571
40. M. Su, A.K. Bansal, R. Mantovani, and J. Sodek Recruitment of nuclear factor Y to the inverted CCAAT element (ICE) by c-Jun and E1A stimulates basal transcription of the bone sialoprotein gene in osteosarcoma cells J Biol Chem 280 2005 38365 38375
41. M.C. Motta, G. Caretti, G.F. Badaracco, and R. Mantovani Interactions of the CCAAT-binding trimer NF-Y with nucleosomes J Biol Chem 274 1999 1326 1333
42. T. Tomita, and S. Kimura Regulation of mouse Scgb3a1 gene expression by NF-Y and association of CpG methylation with its tissue-specific expression BMC Mol Biol 9 2008 5
43. B.J. Wu, R.E. Kingston, and R.I. Morimoto Human HSP70 promoter contains at least two distinct regulatory domains Proc Natl Acad Sci U S A 83 1986 629 633
44. W.D. Morgan, G.T. Williams, R.I. Morimoto, J. Greene, R.E. Kingston, and R. Tjian Two transcriptional activators, CCAAT-box-binding transcription factor and heat shock transcription factor, interact with a human hsp70 gene promoter Mol Cell Biol 7 1987 1129 1138
45. G. Ghosh, V.Y.-F. Wang, D.-B. Huang, and A. Fusco NF-κB regulation: lessons from structures Immunol Rev 246 2012 36 58
46. U. Siebenlist, G. Franzoso, and K. Brown Structure, regulation and function of NF-kappaB Annu Rev Cell Biol 10 1994 405 455
47. F.E. Chen, and G. Ghosh Regulation of DNA binding by Rel/NF-kappaB transcription factors: structural views Oncogene 18 1999 6845 6852
48. Vivien Y.-F. Wang, W. Huang, M. Asagiri, N. Spann, A. Hoffmann, and C. Glass et al. The transcriptional specificity of NF-kB dimers is coded within the kB DNA response elements Cell Rep 2 2012 824 839
49. F.E. Chen, D.B. Huang, Y.Q. Chen, and G. Ghosh Crystal structure of p50/p65 heterodimer of transcription factor NF-kappaB bound to DNA Nature 391 1998 410 413
50. M. Ammirante, A. Rosati, A. Gentilella, M. Festa, A. Petrella, and L. Marzullo et al. The activity of hsp90 alpha promoter is regulated by NF-kappa B transcription factors Oncogene 27 2008 1175 1178
51. S. Ikuyama, H. Shimura, J.P. Hoeffler, and L.D. Kohn Role of the cyclic adenosine 3′,5′-monophosphate response element in efficient expression of the rat thyrotropin receptor promoter Mol Endocrinol 6 1992 1701 1715
52. P.G. Quinn, T.W. Wong, M.A. Magnuson, J.B. Shabb, and D.K. Granner Identification of basal and cyclic AMP regulatory elements in the promoter of the phosphoenolpyruvate carboxykinase gene Mol Cell Biol 8 1988 3467 3475
53. D. Spengler, R. Rupprecht, L.P. Van, and F. Holsboer Identification and characterization of a 3′,5′-cyclic adenosine monophosphate- responsive element in the human corticotropin-releasing hormone gene promoter Mol Endocrinol 6 1992 1931 1941
54. H. Cha-Molstad, D.M. Keller, G.S. Yochum, S. Impey, and R.H. Goodman Cell-type-specific binding of the transcription factor CREB to the cAMP-response element Proc Natl Acad Sci U S A 101 2004 13572 13577
55. K.K. Yamamoto, G.A. Gonzalez, W.H. Biggs III, and M.R. Montminy Phosphorylation-induced binding and transcriptional efficacy of nuclear factor CREB Nature 334 1988 494 498
56. P.J. Sonawane, B.S. Sahu, B.K. Sasi, P. Geedi, G. Lenka, and N.R. Mahapatra Functional promoter polymorphisms govern differential expression of HMG-CoA reductase gene in mouse models of essential hypertension PLoS One 6 2011 e16661
57. M. Jordan, and F. Wurm Transfection of adherent and suspended cells by calcium phosphate Methods 33 2004 136 143
58. N.R. Mahapatra, M. Mahata, S. Ghosh, J.R. Gayen, D.T. O'Connor, and S.K. Mahata Molecular basis of neuroendocrine cell type-specific expression of the chromogranin B gene: crucial role of the transcription factors CREB, AP-2, Egr-1 and Sp1 J Neurochem 99 2006 119 133
59. N.R. Mahapatra, M. Mahata, D.T. O'Connor, and S.K. Mahata Secretin activation of chromogranin A gene transcription J Biol Chem 278 2003 19986 19994
60. J. Zuo, D. Rungger, and R. Voellmy Multiple layers of regulation of human heat shock transcription factor 1 Mol Cell Biol 15 1995 4319 4330
61. D.W. Ballard, E.P. Dixon, N.J. Peffer, H. Bogerd, S. Doerre, and B. Stein et al. The 65-kDa subunit of human NF-kappa B functions as a potent transcriptional activator and a target for v-Rel-mediated repression Proc Natl Acad Sci U S A 89 1992 1875 1879
62. A. Riccio, S. Ahn, C.M. Davenport, J.A. Blendy, and D.D. Ginty Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons Science 286 1999 2358 2361
63. K.M. Walton, R.P. Rehfuss, J.C. Chrivia, J.E. Lochner, and R.H. Goodman A dominant repressor of cyclic adenosine 3′,5′-monophosphate (cAMP)-regulated enhancer-binding protein activity inhibits the cAMP-mediated induction of the somatostatin promoter in vivo Mol Endocrinol 6 1992 647 655
64. S. Andersson, D.L. Davis, H. Dahlbäck, H. Jörnvall, and D.W. Russell Cloning, structure, and expression of the mitochondrial cytochrome P-450 sterol 26-hydroxylase, a bile acid biosynthetic enzyme J Biol Chem 264 1989 8222 8229
65. K. Ruscher, N. Isaev, G. Trendelenburg, M. Weih, L. Iurato, and A. Meisel et al. Induction of hypoxia inducible factor 1 by oxygen glucose deprivation is attenuated by hypoxic preconditioning in rat cultured neurons Neurosci Lett 254 1998 117 120
66. J. Schefe, K. Lehmann, I. Buschmann, T. Unger, and H. Funke-Kaiser Quantitative real-time RT-PCR data analysis: current concepts and the novel "gene expression's CT difference" formula J Mol Med 84 2006 901 910
67. M.J. Solomon, P.L. Larsen, and A. Varshavsky Mapping protein-DNA interactions in vivo with formaldehyde: evidence that histone H4 is retained on a highly transcribed gene Cell 53 1988 937 947
68. Z. He, J. Cai, J.-W. Lim, K. Kroll, and L. Ma A novel KRAB domain-containing zinc finger transcription factor ZNF431 directly represses Patched1 transcription J Biol Chem 286 2010 7279 7289