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생화학분자생물학회 (Korean Society for Biochemistry and Molecular Biology)
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Heat shock transcription factors and sensory placode development

  • Nakai, Akira (Department of Biochemistry and Molecular Biology, Yamaguchi University School of Medicine)
  • 발행 : 2009.10.31
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초록

The heat shock transcription factor (HSF) family consists of at least three members in mammals and regulates expression of heat shock proteins in response to heat shock and proteotoxic stresses. Especially, HSF1 is indispensable for this response. Members of this family are also involved in development of some tissues such as the brain and reproductive organs. However, we did not know the molecular mechanisms that regulate developmental processes. Involvement of HSFs in the sensory development was implicated by the finding that human hereditary cataract is associated with mutations of the HSF4 gene. Analysis of gene-disrupted mice showed that HSF4 and HSF1 are required for the lens and the olfactory epithelium, respectively. Furthermore, a common molecular mechanism that regulates developmental processes was revealed by analyzing roles of HSFs in the two developmentally-related organs.

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참고문헌

  1. Parsell, D. A. and Lindquist, S. (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genet. 27, 437-496 https://doi.org/10.1146/annurev.ge.27.120193.002253
  2. Balch, W. E., Morimoto, R. I., Dillin, A. and Kelly, J. W. (2008) Adapting proteostasis for disease intervention. Science 319, 916-919 https://doi.org/10.1126/science.1141448
  3. Wu, C. (1995). Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11, 441-469 https://doi.org/10.1146/annurev.cb.11.110195.002301
  4. Morimoto, R. I. (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12, 3788-3796 https://doi.org/10.1101/gad.12.24.3788
  5. Pirkkala, L., Nykanen, P. and Sistonen, L. (2001) Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J. 15, 1118-1131 https://doi.org/10.1096/fj00-0294rev
  6. Morimoto, R. I. (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev. 22, 1427-1438 https://doi.org/10.1101/gad.1657108
  7. Christians, E., Davis, A. A., Thomas, S. D. and Benjamin, I. J. (2000) Maternal effect of Hsf1 on reproductive success Nature 407, 693-694 https://doi.org/10.1038/35037669
  8. Nakai, A., Suzuki, M. and Tanabe, M. (2000) Arrest of spermatogenesis in mice expressing an active heat shock transcription factor 1. EMBO J. 19, 1545-1554 https://doi.org/10.1093/emboj/19.7.1545
  9. Kallio, M., Chang, Y., Manuel, M., Alastalo, T. P., Rallu, M., Gitton, Y., Pirkkala, L., Loones, M. T., Paslaru, L., Larney, S., Hiard, S., Morange, M., Sistonen, L. and Mezger, V. (2002) Brain abnormalities, defective meiotic chromosome synapsis and female subfertility in HSF2 null mice. EMBO J. 21, 2591-2601 https://doi.org/10.1093/emboj/21.11.2591
  10. Izu, H., Inouye, S., Fujimoto, M., Shiraishi, K., Naito, K. and Nakai, A. (2004) Heat-shock transcription factor 1 is involvedin quality control mechanisms in male germ cells. Biol. Reprod. 70, 18-24 https://doi.org/10.1095/biolreprod.103.020065
  11. Wang, G., Ying, Z., Jin, X., Tu, N., Zhang, Y., Phillips, M., Moskophidis, D. and Mivechi, N. F. (2004) Essential requirement for both hsf1 and hsf2 transcriptional activity in spermatogenesis and male fertility. Genesis 38, 66-80 https://doi.org/10.1002/gene.20005
  12. Metchat, A., Akerfelt, M., Bierkamp, C., Delsinne, V., Sistonen, L., Alexandre, H. and Christians, E. S. (2009) Mammalian heat shock factor 1 is essential for oocyte meiosis and directly regulates Hsp90alpha expression. J. Biol. Chem. 284, 9521-9528 https://doi.org/10.1074/jbc.M808819200
  13. Wang, G., Zhang, J., Moskophidis, D. and Mivechi, N. F. (2003) Targeted disruption of the heat shock transcription factor (hsf)-2 gene results in increased embryonic lethality, neuronal defects, and reduced spermatogenesis. Genesis 36, 48-61 https://doi.org/10.1002/gene.10200
  14. Santos, S. D. and Saraiva, M. J. (2004) Enlarged ventricles, astrogliosis and neurodegeneration in heat shock factor 1 null mouse brain. Neuroscience 126, 657-663 https://doi.org/10.1016/j.neuroscience.2004.03.023
  15. Chang, Y., Ostling, P., Akerfelt, M., Trouillet, D., Rallu, M., Gitton, Y., El Fatimy, R., Fardeau, V., Le Crom, S., Morange, M., Sistonen, L. and Mezger, V. (2006) Role of heat-shock factor 2 in cerebral cortex formation and as a regulator of p35 expression. Genes Dev. 20, 836-847 https://doi.org/10.1101/gad.366906
  16. Homma, S., Jin, X., Wang, G., Tu, N., Min, J., Yanasak, N. and Mivechi, N. F. (2007) Demyelination, astrogliosis, and accumulation of ubiquitinated proteins, hallmarks of CNS disease in hsf1-deficient mice. J. Neurosci. 27, 7974-7986 https://doi.org/10.1523/JNEUROSCI.0006-07.2007
  17. Inouye, S., Izu, H., Takaki, E., Suzuki, H., Shirai, M., Yokota, Y., Ichikawa, H., Fujimoto, M. and Nakai, A. (2004) Impaired IgG production in mice deficient for heat shock transcription factor 1. J. Biol. Chem. 279, 38701-38709 https://doi.org/10.1074/jbc.M405986200
  18. Inouye, S., Fujimoto, M., Nakamura, T., Takaki, E., Hayashida, N., Hai, T. and Nakai, A. (2007) Heat shock transcription factor 1 opens chromatin structure of interleukin- 6 promoter to facilitate binding of an activator or a repressor. J. Biol. Chem. 282, 33210-33217 https://doi.org/10.1074/jbc.M704471200
  19. Zheng, H. and Li, Z. (2004) Cutting edge: cross-presentation of cell-associated antigens to MHC class I molecule is regulated by a major transcription factor for heat shock proteins. J. Immunol. 173, 5929-5933 https://doi.org/10.4049/jimmunol.173.10.5929
  20. Takaki, E., Fujimoto, M., Nakahari, T., Yonemura, S., Miyata, Y., Hayashida, N., Yamamoto, K., Vallee, R. B., Mikuriya, T., Sugahara, K., Yamashita, H., Inouye, S. and Nakai, A. (2007) Heat shock transcription factor 1 is required for maintenance of ciliary beating in mice. J. Biol. Chem. 282, 37285-37292 https://doi.org/10.1074/jbc.M704562200
  21. Jedlicka, P., Mortin, M. A. and Wu, C. (1997) Multiple functions of Drosophila heat shock transcription factor in vivo. EMBO J. 16, 2452-2462 https://doi.org/10.1093/emboj/16.9.2452
  22. Xiao, X., Zuo, X., Davis, A. A., McMillan, D. R., Curry, B. B., Richardson, J. A. and Benjamin, I. J. (1999) HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J. 18, 5943-5952 https://doi.org/10.1093/emboj/18.21.5943
  23. Bhattacharyya, S. and Bronner-Fraser, M. (2004) Hierarchy of regulatory events in sensory placode development. Curr. Opin. Genet. Dev. 14, 520-526 https://doi.org/10.1016/j.gde.2004.08.002
  24. Schlosser, G. (2006) Induction and specification of cranial placodes. Dev. Biol. 294, 303-351 https://doi.org/10.1016/j.ydbio.2006.03.009
  25. Bhattacharyya, S., Bailey, A. P., Bronner-Fraser, M. and Streit, A. (2004) Segregation of lens and olfactory precursors from a common territory: cell sorting and reciprocity of Dlx5 and Pax6 expression. Dev. Biol. 271, 403-414 https://doi.org/10.1016/j.ydbio.2004.04.010
  26. Grindley, J. C., Davidson, D. R. and Hill, R. E. (1995) The role of Pax-6 in eye and nasal development. Development 121, 1433-1442
  27. Quinn, J. C., West, J. D. and Hill, R. E. (1996) Multiple functions for Pax6 in mouse eye and nasal development. Genes Dev 10, 435-446 https://doi.org/10.1101/gad.10.4.435
  28. Xu, P. X., Woo, I., Her, H., Beier, D. R. and Maas, R. L. (1997) Mouse Eya homologues of the Drosophila eyes absent gene require Pax6 for expression in lens and nasal placode. Development 124, 219-231
  29. Nakai, A. (1999) New aspects in the vertebrate heat shock factor system: Hsf3 and Hsf4. Cell Stress Chaperones 4, 86-93 https://doi.org/10.1379/1466-1268(1999)004<0086:NAITVH>2.3.CO;2
  30. Nakai, A., Tanabe, M., Kawazoe, Y., Inazawa, J., Morimoto, R. I. and Nagata, K. (1997) HSF4, a new member of the human heat shock factor family which lacks properties of a transcriptional activator. Mol. Cell. Biol. 17, 469-481 https://doi.org/10.1128/MCB.17.1.469
  31. Tanabe, M., Sasai, N., Nagata, K., Liu, X. D., Liu, P. C., Thiele, D. J. and Nakai, A. (1999) The mammalian HSF4 gene generates both an activator and a repressor of heat shock genes by alternative splicing. J. Biol. Chem. 274, 27845-27856 https://doi.org/10.1074/jbc.274.39.27845
  32. Bu, L., Jin, Y., Shi, Y., Chu, R., Ban, A., Eiberg, H., Andres, L., Jiang, H., Zheng, G., Qian, M., Cui, B., Xia, Y., Liu, J., Hu, L., Zhao, G., Hayden, M. R. and Kong, X. (2002) Mutant DNA-binding domain of HSF4 is associated with autosomal dominant lamellar and Marner cataract. Nat. Genet. 31, 276-278 https://doi.org/10.1038/ng921
  33. Smaoui, N., Beltaief, O., BenHamed, S., M'Rad, R., Maazoul, F., Ouertani, A., Chaabouni, H. and Hejtmancik, J. F. (2004) A homozygous splice mutation in the HSF4 gene is associated with an autosomal recessive congenital cataract. Invest. Ophthalmol. Vis. Sci. 45, 2716-2721 https://doi.org/10.1167/iovs.03-1370
  34. Forshew, T., Johnson, C. A., Khaliq, S., Pasha, S., Willis, C., Abbasi, R., Tee, L., Smith, U., Trembath, R. C., Mehdi, S. Q., Moore, A. T. and Maher, E. R. (2005) Locus heterogeneity in autosomal recessive congenital cataracts: linkage to 9q and germline HSF4 mutations. Hum. Genet. 117, 452-459 https://doi.org/10.1007/s00439-005-1309-9
  35. Ke, T., Wang, Q. K., Ji, B., Wang, X., Liu, P., Zhang, X., Tang, Z., Ren, X. and Liu, M. (2006) Novel HSF4 mutation causes congenital total white cataract in a Chinese family. Am. J. Ophthalmol. 142, 298-303 https://doi.org/10.1016/j.ajo.2006.03.056
  36. Shi, Y., Shi, X., Jin, Y., Miao, A., Bu, L., He, J., Jiang, H., Lu, Y., Kong, X. and Hu, L. (2008) Mutation screening of HSF4 in 150 age-related cataract patients. Mol. Vis. 14, 1850-1855
  37. McAvoy, J. W., Chamberlain, C. G., de Iongh, R. U., Hales, A. M. and Lovicu, F. J. (1999) Lens development. Eye 13, 425-437 https://doi.org/10.1038/eye.1999.117
  38. Fagerholm, P. P., Philipson, B. T. and Lindstrom, B. (1981) Normal human lens - the distribution of protein. Exp. Eye Res. 33, 615-620 https://doi.org/10.1016/S0014-4835(81)80101-7
  39. Zigler, J. S. Jr. (1994) Lens proteins; in Principles and Practice of Ophthalmology. Albert, D. M. and Jakobiec, F. A. (eds.), pp. 97-113. W. B. Saunders Company, Pennsylvania, USA
  40. Bhat, S. P. (2003) Crystallins, genes and cataract. Prog. Drug. Res. 60, 205-262
  41. Somasundaram, T. and Bhat, S. P. (2000) Canonical heat shock element in the $\alpha$B-crystallin gene shows tissue-specific and developmentally controlled interactions with heat shock factor. J. Biol. Chem. 275, 17154-17159 https://doi.org/10.1074/jbc.M000304200
  42. Fujimoto, M., Izu, H., Seki, K., Fukuda, K., Nishida, T., Yamada, S., Kato, K., Yonemura, S., Inouye, S. and Nakai, A. (2004) HSF4 is required for normal cell growth and differentiation during mouse lens development. EMBO J. 23, 4297-4306 https://doi.org/10.1038/sj.emboj.7600435
  43. Min. J. N., Zhang, Y., Moskophidis, D. and Mivechi, N. F. (2004) Unique contribution of heat shock transcription factor 4 in ocular lens development and fiber cell differentiation. Genesis 40, 205-217 https://doi.org/10.1002/gene.20087
  44. Shi, X., Cui, B., Wang, Z., Weng, L., Xu, Z., Ma, J., Xu, G., Kong, X. and Hu, L. (2009) Removal of Hsf4 leads to cataract development in mice through down-regulation of gamma S-crystallin and Bfsp expression. BMC Mol. Biol. 10, 10 https://doi.org/10.1186/1471-2199-10-10
  45. McAvoy, J. W. and Chamberlain, C. G. (1989) Fibroblast growth factor (FGF) induces different responses in lens epithelial cells depending on its concentration. Development 107, 221-228
  46. Robinson, M. L., Overbeek, P. A., Verran, D. J., Grizzle, W. E., Stockard, C. R., Friesel, R., Maciag, T. and Thompson, J. A. (1995) Extracellular FGF-1 acts as a lens differentiation factor in transgenic mice. Development 121, 505-514
  47. Lovicu, F. J. and Overbeek, P. A. (1998) Overlapping effects of different members of the FGF family on lens fiber differentiation in transgenic mice. Development 125, 3365- 3377
  48. Burgess, W. H. and Maciag, T. (1989) The heparin-binding (fibroblast) growth factor family of proteins. Annu. Rev. Biochem. 58, 575-606 https://doi.org/10.1146/annurev.bi.58.070189.003043
  49. Fujimoto, M., Oshima, I., Shinkawa, T., Wang, B. B., Inouye, S., Hayashida, N., Takii, R. and Nakai, A. (2008) Analysis of HSF4 binding regions reveals its necessity for gene regulation during development and heat shock response in mouse lenses. J. Biol. Chem. 283, 29961- 29970 https://doi.org/10.1074/jbc.M804629200
  50. Trinklein, N. D., Murray, J. I., Hartman, S. J., Botstein, D. and Myers, R. M. (2004) The role of heat shock transcription factor 1 in the genome-wide regulation of the mammalian heat shock response. Mol. Biol. Cell 15, 1254-1261 https://doi.org/10.1091/mbc.E03-10-0738
  51. Page, T. J., Sikder, D., Yang, L., Pluta, L., Wolfinger, R. D., Kodadek, T. and Thomas, R. S. (2006) Genome-wide analysis of human HSF1 signaling reveals a transcriptional program linked to cellular adaptation and survival. Mol. Biosyst. 2, 627-639 https://doi.org/10.1039/b606129j
  52. Westwood, J.T., Clos, J. and Wu, C. (1991) Stress-induced oligomerization and chromosomal relocalization of heatshock factor. Nature 353, 822-827 https://doi.org/10.1038/353822a0
  53. Yao, J., Munson, K. M., Webb, W. W. and Lis, J. T. (2006) Dynamics of heat shock factor association with native gene loci in living cells. Nature 442, 1050-1053 https://doi.org/10.1038/nature05025
  54. Hahn, J. S., Hu, Z., Thiele, D. J. and Iyer, V. R. (2004) Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol. Cell. Biol. 24, 5249-5256 https://doi.org/10.1128/MCB.24.12.5249-5256.2004
  55. Hu, Z., Killion, P. J. and Iyer, V. R. (2007) Genetic reconstruction of a functional transcriptional regulatory network. Nat. Genet. 39, 683-687 https://doi.org/10.1038/ng2012
  56. Takaki, E., Fujimoto, M., Sugahara, K., Nakahari, T., Yonemura, S., Tanaka, Y., Hayashida, N., Inouye, S., Takemoto, T., Yamashita, H. and Nakai, A. (2006) Maintenance of olfactory neurogenesis requires HSF1, a major heat shock transcription factor in mice. J. Biol. Chem. 281, 4931-4937 https://doi.org/10.1074/jbc.M506911200
  57. Guillemot, F., Lo, L. C., Johnson, J. E., Auerbach, A., Anderson, D. J. and Joyner, A. L. (1993) Mammalian achaetescute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75, 463-476 https://doi.org/10.1016/0092-8674(93)90381-Y
  58. Cau, E., Casarosa, S. and Guillemot, F. (2002) Mash1 and Ngn1 control distinct steps of determination and differentiation in the olfactory sensory neuron lineage. Development 129, 1871-1880
  59. Farbman, A. I. (1994) Developmental biology of olfactory sensory neurons. Semin. Cell Biol. 5, 3-10 https://doi.org/10.1038/ncb0103-3
  60. Mackay-Sima, A. and Chuahb, M. I. (2000) Neurotrophic factors in the primary olfactory pathway. Prog. Neurobiol. 62, 527-559 https://doi.org/10.1016/S0301-0082(00)00009-5
  61. Schwob, J. E. (2002) Neural regeneration and the peripheral olfactory system. Anat. Rec. 269, 33-49 https://doi.org/10.1002/ar.10047
  62. Metcalf, D. (2003) The unsolved enigmas of leukemia inhibitory factor. Stem Cells 21, 5-14 https://doi.org/10.1634/stemcells.21-1-5
  63. Sugahara, K., Inouye, S., Izu, H., Katoh, Y., Katsuki, K., Takemoto, T., Shimogori, H., Yamashita, H. and Nakai, A. (2003) Heat shock transcription factor HSF1 is required for survival of sensory hair cells against acoustic overexposure. Hear. Res. 182, 88-96 https://doi.org/10.1016/S0378-5955(03)00180-1
  64. Fairfield, D. A., Lomax, M. I., Dootz, G. A., Chen, S., Galecki, A. T., Benjamin, I. J., Dolan, D. F. and Altschuler, R. A. (2005) Heat shock factor 1-deficient mice exhibit decreased recovery of hearing following noise overstimulation. J. Neurosci. Res. 81, 589-596 https://doi.org/10.1002/jnr.20417
  65. Mikuriya, T., Sugahara, K., Sugimoto, K., Fujimoto, M., Takemoto, T., Hashimoto, M., Hirose, Y., Shimogori, H., Hayashida, N., Inouye, S., Nakai, A. and Yamashita, H. (2008) Attenuation of progressive hearing loss in a model of age-related hearing loss by a heat shock protein inducer, geranylgeranylacetone. Brain Res. 1212, 9-17 https://doi.org/10.1016/j.brainres.2008.03.031

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