Involvement of Putative Heat Shock Element in Transcriptional Regulation of $p21^{WAF1/ClP1/SDl1}$ by Heat Shock

  • Woo, Sang-Hyeok (Department of Molecular Biology, Pusan National University) ;
  • Oh, Su-Young (Department of Molecular Biology, Pusan National University) ;
  • Han, Song-Iy (Department of Molecular Biology, Pusan National University) ;
  • Choi, Yung-Hyun (Department of Oriental Medicine, Dong-eui University) ;
  • Kang, Kwang-Il (Department of Oriental Medicine, Dong-eui University) ;
  • Yoo, Mi-Ae (Department of Molecular Biology, Pusan National University) ;
  • Kim, Han-Do (Department of Molecular Biology, Pusan National University) ;
  • Kang, Ho-Sung (Department of Molecular Biology, Pusan National University)
  • Published : 2000.06.01

Abstract

The expression of $p21^{WAF1/ClP1/SDl1}$, one of the cyclin-dependent kinase inhibitors, is regulated by a variety of transcription factors including p53 and STAT. Heat shock induces the expression of p21 in a temperature- and time-dependent manner. Although the p21 induction by heat shock has been reported to be controlled by p53, a p53-independent mechanism Is also involved. To understand the p53-independent regulation of heat shock-induced p21 expression, we searched the promoter region of p21 gene and found one or two heat shock element (HSE)-like sequences in human, rat, and mouse. Electromobility shift assay (EMSA) showed that heat shock factor (HSF) could bind to these HSE-like sequences In response to heat shock, even though to a lesser extent than to HSE. In addition, p21 promoter deletion analysis revealed that heat shock activated a p21 deletion promoter construct containing the HSE-like sequences but lacking p53-binding sites, but not a promoter construct containing neither HSE-like sequences nor the p53-responsive element. Furthermore, the p21 induction by heat shook was significantly inhibited in confluent cells in which heat shock-induced HSF activation was reduced. These results suggest that the transcriptional regulation of p21 by heat shock may be mediated through activation and binding to HSE-like sequences of HSF.

Keywords

References

  1. Arellano M and Moreno S (1997) Regulation of CDK/cyclin complexes during the cell cycle. Int J Biochem Cell Biol 29: 559-573 https://doi.org/10.1016/S1357-2725(96)00178-1
  2. Baler R, Welch WJ, and Voellmy R (1992) Hat shock gene regulation by nascent polypeptides and denatured proteins:hap 70 as a potential autoregulatory factor. J Cell Biol 117: 1151-1159 https://doi.org/10.1083/jcb.117.6.1151
  3. Brown JP, Wei W, and Sedivy JM (1997) Bypass of sene scence sfter disruption of p21CIP1/WAF1 gene in normal diploid human fibroblasts. Science 277: 831-834 https://doi.org/10.1126/science.277.5327.831
  4. Datto MB, Li Y, Panus JF, Howe DJ, Xiong Y, and Wang XF (1995) Transforming growth factor beta induces the cyclindependent kinase inhibitor p21 through a p53-independent mechanism. Proc Natl Acad Sci USA 92: 5545-5549 https://doi.org/10.1073/pnas.92.12.5545
  5. Dewey WC (1989) The search for critical cellular targets damaged by heat. Radiat Res 120: 191-204 https://doi.org/10.2307/3577707
  6. Di Nocera PP and Dawid IB (1983) Transient expression of genes introduced into cultured cells of Drosophila. Proc Natl Acad Sci USA 80: 7095-7098 https://doi.org/10.1073/pnas.80.23.7095
  7. Edlund T, Walker MD, Barr PJ, and Rutter WJ (1985) Cellspecific expression of the rat insulin gene: evidence for role of two distinct 5 flanking elements. Science 230: 912-916 https://doi.org/10.1126/science.3904002
  8. El-Deiry WS, Harper JW, O'Connor PM, Velculescu VE, Canman CE, Jackman J, Pietenpol JA, Burrell M, Hill DE, and Wang Y (1994) WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res 54: 1169-1174
  9. El-Deiry WS, Tokino T, Waldman T, Oliner JD, Velculescu VE, Burrell M, Hill DE, Healy E, Rees JL, and Hamilton SR (1995) Topological control of p21WAF1/CIP1 expression in normal and neoplastic tissues. Cancer Res 55: 2910-2919
  10. Fuse T, Yamada K, Asai K, Kato T, and Nakanishi M (1996) Heat shock-mediated cell cycle arrest is accompanied by induction of p21 CKI. Biochem Biophys Res Commun 225: 759-763 https://doi.org/10.1006/bbrc.1996.1247
  11. Gartel AL and Tyner AL (1999) Transcriptional regulation of the p21(WAF1/CIP1) gene. Exp Cell Res 246: 280-289 https://doi.org/10.1006/excr.1998.4319
  12. Kim HR, Kang HS, and Kim HD (1999) Geldanamycin induces heat shock protein expression through activation of HSF1 in K562 erytholeukemic cells. IUBMB Life 48: 429-433 https://doi.org/10.1080/713803536
  13. Kim HT, Kim YH, Nam JW, Lee HJ, Rho HM, and Jung G (1994) Study of 5-flanking region of human Cu/Zn superoxide dismutase. Biochem Biophys Res Commun 201: 1526-1533 https://doi.org/10.1006/bbrc.1994.1877
  14. LaBaer J, Garrett MD, Stevenson LF, Sliberland JM, Sandhu C, Chou HS, Fattaey A, and Harlow E ((1997) New functional activities for the p21 family of CDK inhibitors. Genes & Dev 11: 847-862 https://doi.org/10.1101/gad.11.7.847
  15. Lee SJ, Ha MJ, Lee J, Nguyen P, Choi YH, Pirnia F, Kang WK, Wang XF, Kim SJ, and Trepel JB (1998) Inhibition of the 3-hydroxy-3-methylglutaryl-coenzyme A reductase pathway induces p53-independent transcriptional regulation of p21(WAF1/CIP1) in human prostate carcinoma cells. J Biol Chem 273: 10618-10623 https://doi.org/10.1074/jbc.273.17.10618
  16. Liu M, Lee MH, Cohen M, Bommakanti M, and Freedman LP (1996) Transcriptional activation of the Cdk inhibitor p21 by vitamin D3 leads to the induced & differentiation of the myelomonocytic cell line U937. Genes & Dev 10: 142-153 https://doi.org/10.1101/gad.10.2.142
  17. Macleod KF, Sherry N, Hannon G, Beach D, Tokino T, Kinzler K, and Vogelstein B, and Jacks T (1995) p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes & Dev 9: 935-944 https://doi.org/10.1101/gad.9.8.935
  18. Morimoto Rl (1993) Cells in stress: transcriptional activation of heat shock genes. Science 259: 1409-1410 https://doi.org/10.1126/science.8451637
  19. Nitta M, Okamura H, Aizawa S, and Yamaizumi M (1997) Heat shock induces transient p53-dependent cell cycle arrest at G1/S. Oncogene 15: 561-568 https://doi.org/10.1038/sj.onc.1201210
  20. Ohnishi K, Wang X, Takahashi A, and Ohnishi T (1998) Contribution of protein kinase C to p53-dependent WAF1 induction pathway after treatment in human glioblastoma cell lines. Exp Cell Res 238: 399-406 https://doi.org/10.1006/excr.1997.3842
  21. Ohnishi T, Wang X, Ohnishi K, Matsumoto H, and Takahashi A (1996) p53-dependent induction of WAF1 by heat treatment in human gliblastoma cells. J Biol Chem 271: 14510-14513 https://doi.org/10.1074/jbc.271.24.14510
  22. Okinaga S, Takahashi K, Takeda K, Yoshizawa M, Fujita H, Sasaki H, and Shibahara S (1996) Regulation of human heme oxygenase-1 gene expression under thermal stress. Blood 87: 5074-5084
  23. Prowse DM, Bolgan L, Molnar A and Dotto GP (1997) Involvement of the Sp3 transcription factor in induction of p21Cip1/WAF1 in keratincyte differentiation. J Biol Chem 272: 1308-1314 https://doi.org/10.1074/jbc.272.2.1308
  24. Sarge KD, Murphy SP, and Morimoto RI (1993) Activation of heat shock gene transcription of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol Cell Biol 13: 1392-1407
  25. Welch WJ, Kang HS, Beckmann RP, and Mizzen LA (1991) Response of mammalian cells to metabolic stress proteins. Curr Top Microbiol Immunol 167: 31-55
  26. Yan GZ and Ziff EB (1997) Nerve growth factor induces transcription of the p21 WAF1/CIp1 and cyclin D1 genes in PC12 cells by activating the Sp1 transcription factor. J Neurosci 17: 6122-6132
  27. Yanagisawa K, Kosaka A, Iwahana H, Nakanishi M, and Tominaga S (1999) Opposite regulation of the expression of cyclin-dependent kinase inhibitors during contact inhibition. J Biochem 25: 36-40