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Biochemistry Research International
Volume 2011 (2011), Article ID 238601, 8 pages
http://dx.doi.org/10.1155/2011/238601
Review Article

Transcriptional Modulation of Heat-Shock Protein Gene Expression

Medical Molecular Biology Unit, Institute of Child Health, University College London, 30 Guilford Street, London WC1N 1EH, UK

Received 1 June 2010; Accepted 2 August 2010

Academic Editor: Daniel N. Hebert

Copyright © 2011 Anastasis Stephanou and David S. Latchman. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. J. Ellis and S. M. van der Vies, “Molecular chaperones,” Annual Review of Biochemistry, vol. 60, pp. 321–347, 1991. View at Google Scholar · View at Scopus
  2. A. Mathew and R. I. Morimoto, “Role of the heat-shock response in the life and death of proteins,” Annals of the New York Academy of Sciences, vol. 851, pp. 99–111, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. F. Ritossa, “A new puffing pattern induced by temperature shock and DNP in drosophila,” Experientia, vol. 18, no. 12, pp. 571–573, 1962. View at Publisher · View at Google Scholar · View at Scopus
  4. R. I. Morimoto, M. P. Kline, D. N. Bimston, and J. J. Cotto, “The heat-shock response: regulation and function of heat-shock proteins and molecular chaperones,” Essays in Biochemistry, vol. 32, pp. 17–29, 1997. View at Google Scholar · View at Scopus
  5. C. Jolly and R. I. Morimoto, “Role of the heat shock response and molecular chaperones in oncogenesis and cell death,” Journal of the National Cancer Institute, vol. 92, no. 19, pp. 1564–1572, 2000. View at Google Scholar · View at Scopus
  6. F. C. Neidhardt, R. A. VanBogelen, and V. Vaughn, “The genetics and regulation of heat-shock proteins,” Annual Review of Genetics, vol. 18, pp. 295–329, 1984. View at Google Scholar · View at Scopus
  7. D. Walsh, Z. Li, Y. Wu, and K. Nagata, “Heat shock and the role of the HSPs during neural plate induction in early mammalian CNS and brain development,” Cellular and Molecular Life Sciences, vol. 53, no. 2, pp. 198–211, 1997. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Åkerfelt, R. I. Morimoto, and L. Sistonen, “Heat shock factors: integrators of cell stress, development and lifespan,” Nature Reviews Molecular Cell Biology, vol. 11, no. 8, pp. 545–555, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. Y. Shi, D. D. Mosser, and R. I. Morimoto, “Molecular chaperones as HSF1-specific transcriptional repressors,” Genes and Development, vol. 12, no. 5, pp. 654–666, 1998. View at Google Scholar · View at Scopus
  10. A. Ali, S. Bharadwaj, R. O'Carroll, and N. Ovsenek, “Hsp90 interacts with and regulates the activity of heat shock factor 1 in Xenopus oocytes,” Molecular and Cellular Biology, vol. 18, no. 9, pp. 4949–4960, 1998. View at Google Scholar · View at Scopus
  11. I. J. Xavier, P. A. Mercier, C. M. McLoughlin, A. Ali, J. R. Woodgett, and N. Ovsenek, “Glycogen synthase kinase 3β negatively regulates both DNA-binding and transcriptional activities of heat shock factor 1,” Journal of Biological Chemistry, vol. 275, no. 37, pp. 29147–29152, 2000. View at Google Scholar
  12. J. Park and A. Y. C. Liu, “JNK phosphorylates the HSF1 transcriptional activation domain: role of JNK in the regulation of the heat shock response,” Journal of Cellular Biochemistry, vol. 82, no. 2, pp. 326–338, 2001. View at Publisher · View at Google Scholar · View at PubMed
  13. S. J. Wigmore, K. Sangster, S. J. McNally et al., “De-repression of heat shock transcription factor-1 in interleukin-6- treated hepatocytes is mediated by downregulation of glycogen synthase kinase 3beta and MAPK/ERK-1,” International Journal of Molecular Medicine, vol. 19, no. 3, pp. 413–420, 2007. View at Google Scholar
  14. F. Soncin, X. Zhang, B. Chu et al., “Transcriptional activity and DNA binding of heat shock factor-1 involve phosphorylation on threonine 142 by CK2,” Biochemical and Biophysical Research Communications, vol. 303, no. 2, pp. 700–706, 2003. View at Publisher · View at Google Scholar
  15. X. Xiao, X. Zuo, A. A. Davis et al., “HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice,” The EMBO Journal, vol. 18, no. 21, pp. 5943–5952, 1999. View at Publisher · View at Google Scholar · View at PubMed
  16. Y. Xie, C. Chen, M. A. Stevenson, P. E. Auron, and S. K. Calderwood, “Heat shock factor 1 represses transcription of the IL-1β gene through physical interaction with the nuclear factor of interleukin 6,” Journal of Biological Chemistry, vol. 277, no. 14, pp. 11802–11810, 2002. View at Publisher · View at Google Scholar · View at PubMed
  17. C. Chen, Y. Xie, M. A. Stevenson, P. E. Auron, and S. K. Calderwood, “Heat shock factor 1 represses Ras-induced transcriptional activation of the c-fos gene,” Journal of Biological Chemistry, vol. 272, no. 43, pp. 26803–26806, 1997. View at Publisher · View at Google Scholar
  18. H. Reinke, C. Saini, F. Fleury-Olela, C. Dibner, I. J. Benjamin, and U. Schibler, “Differential display of DNA-binding proteins reveals heat-shock factor 1 as a circadian transcription factor,” Genes and Development, vol. 22, no. 3, pp. 331–345, 2008. View at Publisher · View at Google Scholar · View at PubMed
  19. L. Sistonen, K. D. Sarge, B. Phillips, K. Abravaya, and R. I. Morimoto, “Activation of heat shock factor 2 during hemin-induced differentiation of human erythroleukemia cells,” Molecular and Cellular Biology, vol. 12, no. 9, pp. 4104–4111, 1992. View at Google Scholar
  20. M. L. Goodson, O.-K. Park-Sarge, and K. D. Sarge, “Tissue-dependent expression of heat shock factor 2 isoforms with distinct transcriptional activities,” Molecular and Cellular Biology, vol. 15, no. 10, pp. 5288–5293, 1995. View at Google Scholar
  21. Y. Chang, P. Östling, M. Åkerfelt et al., “Role of heat-shock factor 2 in cerebral cortex formation and as a regulator of p35 expression,” Genes and Development, vol. 20, no. 7, pp. 836–847, 2006. View at Publisher · View at Google Scholar · View at PubMed
  22. H. Xing, D. C. Wilkerson, C. N. Mayhew et al., “Mechanism of hsp70i gene bookmarking,” Science, vol. 307, no. 5708, pp. 421–423, 2005. View at Publisher · View at Google Scholar · View at PubMed
  23. D. C. Wilkerson, H. S. Skaggs, and K. D. Sarge, “HSF2 binds to the Hsp90, Hsp27, and c-Fos promoters constitutively and modulates their expression,” Cell Stress and Chaperones, vol. 12, no. 3, pp. 283–290, 2007. View at Publisher · View at Google Scholar
  24. A. Nakai and R. I. Morimoto, “Characterization of a novel chicken heat shock transcription factor, heat shock factor 3, suggests a new regulatory pathway,” Molecular and Cellular Biology, vol. 13, no. 4, pp. 1983–1997, 1993. View at Google Scholar
  25. C. Kanei-Ishii, J. Tanikawa, A. Nakai, R. I. Morimoto, and S. Ishii, “Activation of heat shock transcription factor 3 by c-Myb in the absence of cellular stress,” Science, vol. 277, no. 5323, pp. 246–248, 1997. View at Publisher · View at Google Scholar
  26. J. Tanikawa, E. Ichikawa-Iwata, C. Kanei-Ishii et al., “p53 suppresses the c-Myb-induced activation of heat shock transcription factor 3,” Journal of Biological Chemistry, vol. 275, no. 20, pp. 15578–15585, 2000. View at Publisher · View at Google Scholar · View at PubMed
  27. A. Nakai, M. Tanabe, Y. Kawazoe, J. Inazawa, R. I. Morimoto, and K. Nagata, “HSF4, a new member of the human heat shock factor family which lacks properties of a transcriptional activator,” Molecular and Cellular Biology, vol. 17, no. 1, pp. 469–481, 1997. View at Google Scholar
  28. M. Tanabe, N. Sasai, K. Nagata et al., “The mammalian HSF4 gene generates both an activator and a repressor of heat shock genes by alternative splicing,” Journal of Biological Chemistry, vol. 274, no. 39, pp. 27845–27856, 1999. View at Publisher · View at Google Scholar
  29. A. Nakai, “Heat shock transcription factors and sensory placode development,” BMB Reports, vol. 42, no. 10, pp. 631–635, 2009. View at Google Scholar
  30. M. Fujimoto, H. Izu, K. Seki et al., “HSF4 is required for normal cell growth and differentiation during mouse lens development,” The EMBO Journal, vol. 23, no. 21, pp. 4297–4306, 2004. View at Publisher · View at Google Scholar · View at PubMed
  31. J. N. Ihle, “The Stat family in cytokine signaling,” Current Opinion in Cell Biology, vol. 13, pp. 211–217, 2001. View at Google Scholar
  32. T. E. Battle and D. A. Frank, “The role of STATs in apoptosis,” Current Molecular Medicine, vol. 2, no. 4, pp. 381–392, 2002. View at Publisher · View at Google Scholar
  33. A. Stephanou, T. Brar, and A. K. Scarabelli, “Ischaemia-induced STAT1 expression and activation plays a critical role in cardiac myocyte apoptosis,” Journal of Biological Chemistry, vol. 275, pp. 10002–10008, 2000. View at Google Scholar
  34. A. Stephanou, T. M. Scarabelli, B. K. Brar et al., “Induction of apoptosis and Fas receptor/Fas ligand expression by ischemia/reperfusion in cardiac myocytes requires serine 727 of the STAT-1 transcription factor but not tyrosine 701,” Journal of Biological Chemistry, vol. 276, no. 30, pp. 28340–28347, 2001. View at Publisher · View at Google Scholar · View at PubMed
  35. A. Stephanou, T. M. Scarabelli, P. A. Townsend et al., “The carboxyl-terminal activation domain of the STAT-1 transcription factor enhances ischemia/reperfusion-induced apoptosis in cardiac myocytes,” The FASEB Journal, vol. 16, no. 13, pp. 1841–1843, 2002. View at Google Scholar
  36. P. A. Townsend, T. M. Scarabelli, S. M. Davidson, R. A. Knight, D. S. Latchman, and A. Stephanou, “STAT-1 interacts with p53 to enhance DNA damage-induced apoptosis,” Journal of Biological Chemistry, vol. 279, no. 7, pp. 5811–5820, 2004. View at Publisher · View at Google Scholar · View at PubMed
  37. S. M. Soond, C. Carroll, P. A. Townsend et al., “STAT1 regulates p73-mediated Bax gene expression,” FEBS Letters, vol. 581, no. 6, pp. 1217–1226, 2007. View at Publisher · View at Google Scholar · View at PubMed
  38. D. Xu, L. P. Zalmas, and N. B. La Thangue, “A transcription cofactor required for the heat-shock response,” EMBO Reports, vol. 9, no. 7, pp. 662–669, 2008. View at Publisher · View at Google Scholar · View at PubMed
  39. T. Kishimoto, S. Akira, M. Narazaki, and T. Taga, “Interleukin-6 family of cytokines and gp130,” Blood, vol. 86, no. 4, pp. 1243–1254, 1995. View at Google Scholar
  40. T. Nakajima, S. Kinoshita, T. Sasagawa et al., “Phosphorylation at threonine-235 by a ras-dependent mitogen-activated protein kinase cascade is essential for transcription factor NF-IL6,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 6, pp. 2207–2211, 1993. View at Google Scholar
  41. S. Kinoshita, S. Akira, and T. Kishimoto, “A member of the C/EBP family, NF-IL6β, forms a heterodimer and transcriptionally synergizes with NF-IL6,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 4, pp. 1473–1476, 1992. View at Google Scholar
  42. U. Ganter, R. Arcone, C. Toniatti, G. Morrone, and G. Ciliberto, “Dual control of C-reactive protein gene expression by interleukin-1 and interleukin-6,” The EMBO Journal, vol. 8, no. 12, pp. 3773–3779, 1989. View at Google Scholar
  43. A. Stephanou, V. Amin, D. A. Isenberg, S. Akira, T. Kishimoto, and D. S. Latchman, “Interleukin 6 activates heat-shock protein 90β gene expression,” Biochemical Journal, vol. 321, no. 1, pp. 103–106, 1997. View at Google Scholar
  44. A. Stephanou, D. A. Isenberg, S. Akira, T. Kishimoto, and D. S. Latchman, “NF-IL6 and STAT3 signalling pathways co-operate to mediate the activation of the Hsp90β gene by interleukin-6 but have opposite effects on its inducibility by heat shock,” Biochemical Journal, vol. 330, no. 1, pp. 189–195, 1998. View at Google Scholar
  45. A. Stephanou, D. A. Isenberg, K. Nakajima, and D. S. Latchman, “Signal transducer and activator of transcription-1 and heat shock factor-1 interact and activate the transcription of the Hsp-70 and Hsp-90β gene promoters,” Journal of Biological Chemistry, vol. 274, no. 3, pp. 1723–1728, 1999. View at Publisher · View at Google Scholar
  46. B. M. Twomey, V. B. Dhillon, S. McCallum, D. A. Isenberg, and D. S. Latchman, “Elevated levels of the 90 kD heat shock protein in patients with systemic lupus erythematosus are dependent upon enhanced transcription of the Hsp90β gene,” Journal of Autoimmunity, vol. 6, no. 4, pp. 495–506, 1993. View at Publisher · View at Google Scholar · View at PubMed
  47. F. De Benedetti, M. Massa, P. Robbioni, A. Ravelli, G. R. Burgio, and A. Martini, “Correlation of serum interleukin-6 levels with joint involvement and thrombocytosis in systemic juvenile rheumatoid arthritis,” Arthritis and Rheumatism, vol. 34, no. 9, pp. 1158–1163, 1991. View at Publisher · View at Google Scholar
  48. M. Linker-Israeli, R. J. Deans, D. J. Wallace, J. Prehn, T. Ozeri-Chen, and J. R. Klinenberg, “Elevated levels of endogenous IL-6 in systemic lupus erythematosus: a putative role in pathogenesis,” Journal of Immunology, vol. 147, no. 1, pp. 117–123, 1991. View at Google Scholar
  49. B. K. Finck, B. Chan, and D. Wofsy, “Interleukin 6 promotes murine lupus in NZB/NZW F1 mice,” Journal of Clinical Investigation, vol. 94, no. 2, pp. 585–591, 1994. View at Google Scholar
  50. B. J. M. Ripley, D. A. Isenberg, and D. S. Latchman, “Elevated levels of the 90 kDa heat shock protein (Hsp90) in SLE correlate with levels of IL-6 and autoantibodies to Hsp90,” Journal of Autoimmunity, vol. 17, no. 4, pp. 341–346, 2001. View at Publisher · View at Google Scholar · View at PubMed
  51. S. Suematsu, T. Matsuda, K. Aozasa et al., “IgG1 plasmacytosis in interleukin 6 transgenic mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 19, pp. 7547–7551, 1989. View at Google Scholar
  52. I. Screpanti, L. Romani, P. Musiani et al., “Lymphoproliferative disorder and imbalanced T-helper response in C/EBPβ-deficient mice,” The EMBO Journal, vol. 14, no. 9, pp. 1932–1941, 1995. View at Google Scholar
  53. A. Stephanou, S. Conroy, D. A. Isenberg et al., “Elevation of IL-6 in transgenic mice results in increased levels of the 90 kDA heat shock protein and production of anti-Hsp90 antibodies,” Journal of Autoimmunity, vol. 11, no. 3, pp. 249–253, 1998. View at Publisher · View at Google Scholar · View at PubMed
  54. B. J. M. Ripley, A. Stephanou, D. A. Isenberg, and D. S. Latchman, “Interleukin-10 activates heat-shock protein 90β gene expression,” Immunology, vol. 97, no. 2, pp. 226–231, 1999. View at Publisher · View at Google Scholar
  55. T. Kishimoto, “Interleukin-6: from basic science to medicine—40years in immunology,” Annual Review of Immunology, vol. 23, pp. 1–21, 2005. View at Publisher · View at Google Scholar · View at PubMed
  56. E. D. Rosen, “The transcriptional basis of adipocyte development,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 73, no. 1, pp. 31–34, 2005. View at Publisher · View at Google Scholar · View at PubMed
  57. J. Lekstrom-Himes and K. G. Xanthopoulos, “Biological role of the CCAAT/enhancer-binding protein family of transcription factors,” Journal of Biological Chemistry, vol. 273, no. 44, pp. 28545–28548, 1998. View at Publisher · View at Google Scholar
  58. M. Lut, J. Seufert, and J. F. Habener, “Pancreatic β-cell-specific repression of insulin gene transcription by CCAAT/enhancer-binding protein β: inhibitory interactions with basic helix-loop-helix transcription factor E47,” Journal of Biological Chemistry, vol. 272, no. 45, pp. 28349–28359, 1997. View at Publisher · View at Google Scholar
  59. T. Matsuda, Y. Kido, S.-I. Asahara et al., “Ablation of C/EBPβ alleviates ER stress and pancreatic β cell failure through the GRP78 chaperone in mice,” Journal of Clinical Investigation, vol. 120, no. 1, pp. 115–126, 2010. View at Publisher · View at Google Scholar · View at PubMed
  60. D. Mahalingam, R. Swords, J. S. Carew, S. T. Nawrocki, K. Bhalla, and F. J. Giles, “Targeting Hsp90 for cancer therapy,” British Journal of Cancer, vol. 100, no. 10, pp. 1523–1529, 2009. View at Publisher · View at Google Scholar · View at PubMed
  61. H. Yu, D. Pardoll, and R. Jove, “STATs in cancer inflammation and immunity: a leading role for STAT3,” Nature Reviews Cancer, vol. 9, no. 11, pp. 798–809, 2009. View at Publisher · View at Google Scholar · View at PubMed
  62. J. F. Bromberg, M. H. Wrzeszczynska, G. Devgan et al., “Stat3 as an oncogene,” Cell, vol. 98, no. 3, pp. 295–303, 1999. View at Google Scholar
  63. L. Whitesell and S. L. Lindquist, “Hsp90 and the chaperoning of cancer,” Nature Reviews Cancer, vol. 5, no. 10, pp. 761–772, 2005. View at Publisher · View at Google Scholar · View at PubMed
  64. R. Bagatell and L. Whitesell, “Altered Hsp90 function in cancer: a unique therapeutic opportunity,” Molecular Cancer Therapeutics, vol. 3, no. 8, pp. 1021–1030, 2004. View at Google Scholar
  65. D. B. Solit and G. Chiosis, “Development and application of Hsp90 inhibitors,” Drug Discovery Today, vol. 13, no. 1-2, pp. 38–43, 2008. View at Publisher · View at Google Scholar · View at PubMed
  66. C. Dai, L. Whitesell, A. B. Rogers, and S. Lindquist, “Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis,” Cell, vol. 130, no. 6, pp. 1005–1018, 2007. View at Publisher · View at Google Scholar · View at PubMed
  67. J.-N. Min, L. Huang, D. B. Zimonjic, D. Moskophidis, and N. F. Mivechi, “Selective suppression of lymphomas by functional loss of Hsf1 in a p53-deficient mouse model for spontaneous tumors,” Oncogene, vol. 26, no. 35, pp. 5086–5097, 2007. View at Publisher · View at Google Scholar · View at PubMed