This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Charette, S. J.
Right arrow Articles by Landry, J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Charette, S. J.
Right arrow Articles by Landry, J.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, October 2000, p. 7602-7612, Vol. 20, No. 20
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Inhibition of Daxx-Mediated Apoptosis by Heat Shock Protein 27

Steve J. Charette, Josée N. Lavoie, Herman Lambert, and Jacques Landry*

Centre de Recherche en Cancérologie de l'Université Laval, L'Hôtel-Dieu de Québec, Québec, Canada G1R 2J6

Received 18 February 2000/Returned for modification 13 April 2000/Accepted 25 July 2000

Heat shock protein 27 (HSP27) confers cellular protection against a variety of cytotoxic stresses and also against physiological stresses associated with growth arrest or receptor-mediated apoptosis. Phosphorylation modulates the activity of HSP27 by causing a major change in the supramolecular organization of the protein, which shifts from oligomers to dimers. Here we show that phosphorylated dimers of HSP27 interact with Daxx, a mediator of Fas-induced apoptosis, preventing the interaction of Daxx with both Ask1 and Fas and blocking Daxx-mediated apoptosis. No such inhibition was observed with an HSP27 phosphorylation mutant that is only expressed as oligomers or when apoptosis was induced by transfection of a Daxx mutant lacking its HSP27 binding domain. HSP27 expression had no effect on Fas-induced FADD- and caspase-dependent apoptosis. However, HSP27 blocked Fas-induced translocation of Daxx from the nucleus to the cytoplasm and Fas-induced Daxx- and Ask1-dependent apoptosis. The observations revealed a new level of regulation of the Fas pathway and suggest a mechanism for the phosphorylation-dependent protective function of HSP27 during stress and differentiation.


* Corresponding author. Mailing address: Centre de recherche en cancérologie de l'Université Laval, L'Hôtel-Dieu de Québec, Centre hospitalier universitaire de Québec, 9, rue McMahon, Quebec, Canada G1R 2J6. Phone: (418) 525-4444, ext. 5555. Fax: (418) 691-5439. E-mail: jacques.landry{at}med.ulaval.ca.


Molecular and Cellular Biology, October 2000, p. 7602-7612, Vol. 20, No. 20
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Kitamura, T., Fukuyo, Y., Inoue, M., Horikoshi, N. T., Shindoh, M., Rogers, B. E., Usheva, A., Horikoshi, N. (2009). Mutant p53 Disrupts the Stress MAPK Activation Circuit Induced by ASK1-Dependent Stabilization of Daxx. Cancer Res. 69: 7681-7688 [Abstract] [Full Text]  
  • Mathew, S. S., Della Selva, M. P., Burch, A. D. (2009). Modification and Reorganization of the Cytoprotective Cellular Chaperone Hsp27 during Herpes Simplex Virus Type 1 Infection. J. Virol. 83: 9304-9312 [Abstract] [Full Text]  
  • Dai, T., Patel-Chamberlin, M., Natarajan, R., Todorov, I., Ma, J., LaPage, J., Phillips, L., Nast, C. C., Becerra, D., Chuang, P., Tong, L., de Belleroche, J., Wells, D. J., Wang, Y., Adler, S. G. (2009). Heat Shock Protein 27 Overexpression Mitigates Cytokine-Induced Islet Apoptosis and Streptozotocin-Induced Diabetes. Endocrinology 150: 3031-3039 [Abstract] [Full Text]  
  • Rojanathammanee, L., Harmon, E. B., Grisanti, L. A., Govitrapong, P., Ebadi, M., Grove, B. D., Miyagi, M., Porter, J. E. (2009). The 27-kDa Heat Shock Protein Confers Cytoprotective Effects through a {beta}2-Adrenergic Receptor Agonist-Initiated Complex with {beta}-Arrestin. Mol. Pharmacol. 75: 855-865 [Abstract] [Full Text]  
  • Stetler, R. A., Cao, G., Gao, Y., Zhang, F., Wang, S., Weng, Z., Vosler, P., Zhang, L., Signore, A., Graham, S. H., Chen, J. (2008). Hsp27 Protects against Ischemic Brain Injury via Attenuation of a Novel Stress-Response Cascade Upstream of Mitochondrial Cell Death Signaling. J. Neurosci. 28: 13038-13055 [Abstract] [Full Text]  
  • Vidyasagar, A., Reese, S., Acun, Z., Hullett, D., Djamali, A. (2008). HSP27 is involved in the pathogenesis of kidney tubulointerstitial fibrosis. Am. J. Physiol. Renal Physiol. 295: F707-F716 [Abstract] [Full Text]  
  • Li, G., Ali, I. S., Currie, R. W. (2008). Insulin-induced myocardial protection in isolated ischemic rat hearts requires p38 MAPK phosphorylation of Hsp27. Am. J. Physiol. Heart Circ. Physiol. 294: H74-H87 [Abstract] [Full Text]  
  • Ryo, A., Hirai, A., Nishi, M., Liou, Y.-C., Perrem, K., Lin, S.-C., Hirano, H., Lee, S. W., Aoki, I. (2007). A Suppressive Role of the Prolyl Isomerase Pin1 in Cellular Apoptosis Mediated by the Death-associated Protein Daxx. J. Biol. Chem. 282: 36671-36681 [Abstract] [Full Text]  
  • Huang, W., Fileta, J. B., Filippopoulos, T., Ray, A., Dobberfuhl, A., Grosskreutz, C. L. (2007). Hsp27 Phosphorylation in Experimental Glaucoma. IOVS 48: 4129-4135 [Abstract] [Full Text]  
  • Voss, O. H., Batra, S., Kolattukudy, S. J., Gonzalez-Mejia, M. E., Smith, J. B., Doseff, A. I. (2007). Binding of Caspase-3 Prodomain to Heat Shock Protein 27 Regulates Monocyte Apoptosis by Inhibiting Caspase-3 Proteolytic Activation. J. Biol. Chem. 282: 25088-25099 [Abstract] [Full Text]  
  • Wu, R., Kausar, H., Johnson, P., Montoya-Durango, D. E., Merchant, M., Rane, M. J. (2007). Hsp27 Regulates Akt Activation and Polymorphonuclear Leukocyte Apoptosis by Scaffolding MK2 to Akt Signal Complex. J. Biol. Chem. 282: 21598-21608 [Abstract] [Full Text]  
  • Zhang, Y., Shen, X. (2007). Heat Shock Protein 27 Protects L929 Cells from Cisplatin-Induced Apoptosis by Enhancing Akt Activation and Abating Suppression of Thioredoxin Reductase Activity. Clin. Cancer Res. 13: 2855-2864 [Abstract] [Full Text]  
  • Schmitt, E., Gehrmann, M., Brunet, M., Multhoff, G., Garrido, C. (2007). Intracellular and extracellular functions of heat shock proteins: repercussions in cancer therapy. J. Leukoc. Biol. 81: 15-27 [Abstract] [Full Text]  
  • Vertii, A., Hakim, C., Kotlyarov, A., Gaestel, M. (2006). Analysis of Properties of Small Heat Shock Protein Hsp25 in MAPK-activated Protein Kinase 2 (MK2)-deficient Cells: MK2-DEPENDENT INSOLUBILIZATION OF Hsp25 OLIGOMERS CORRELATES WITH SUSCEPTIBILITY TO STRESS. J. Biol. Chem. 281: 26966-26975 [Abstract] [Full Text]  
  • Wick, G. (2006). The Heat Is on: Heat-Shock Proteins and Atherosclerosis. Circulation 114: 870-872 [Full Text]  
  • Martin-Ventura, J. L., Nicolas, V., Houard, X., Blanco-Colio, L. M., Leclercq, A., Egido, J., Vranckx, R., Michel, J.-B., Meilhac, O. (2006). Biological Significance of Decreased HSP27 in Human Atherosclerosis. Arterioscler. Thromb. Vasc. Bio. 26: 1337-1343 [Abstract] [Full Text]  
  • Lelj-Garolla, B., Mauk, A. G. (2006). Self-association and Chaperone Activity of Hsp27 Are Thermally Activated. J. Biol. Chem. 281: 8169-8174 [Abstract] [Full Text]  
  • Healy, D. A., Daly, P. J., Docherty, N. G., Murphy, M., Fitzpatrick, J. M., Watson, R. W. G. (2006). Heat Shock-Induced Protection of Renal Proximal Tubular Epithelial Cells from Cold Storage and Rewarming Injury. J. Am. Soc. Nephrol. 17: 805-812 [Abstract] [Full Text]  
  • Ackerley, S., James, P. A., Kalli, A., French, S., Davies, K. E., Talbot, K. (2006). A mutation in the small heat-shock protein HSPB1 leading to distal hereditary motor neuronopathy disrupts neurofilament assembly and the axonal transport of specific cellular cargoes. Hum Mol Genet 15: 347-354 [Abstract] [Full Text]  
  • Junn, E., Taniguchi, H., Jeong, B. S., Zhao, X., Ichijo, H., Mouradian, M. M. (2005). Interaction of DJ-1 with Daxx inhibits apoptosis signal-regulating kinase 1 activity and cell death. Proc. Natl. Acad. Sci. USA 102: 9691-9696 [Abstract] [Full Text]  
  • Carra, S., Sivilotti, M., Chavez Zobel, A. T., Lambert, H., Landry, J. (2005). HspB8, a small heat shock protein mutated in human neuromuscular disorders, has in vivo chaperone activity in cultured cells. Hum Mol Genet 14: 1659-1669 [Abstract] [Full Text]  
  • Shin, J., Park, B., Cho, S., Lee, S., Kim, Y., Lee, S.-O., Cho, K., Lee, S., Jin, B.-S., Ahn, J.-H., Choi, E.-J., Ahn, K. (2004). Promyelocytic Leukemia Is a Direct Inhibitor of SAPK2/p38 Mitogen-activated Protein Kinase. J. Biol. Chem. 279: 40994-41003 [Abstract] [Full Text]  
  • Beere, H. M. (2004). `The stress of dying': the role of heat shock proteins in the regulation of apoptosis. J. Cell Sci. 117: 2641-2651 [Abstract] [Full Text]  
  • Theriault, J. R., Lambert, H., Chavez-Zobel, A. T., Charest, G., Lavigne, P., Landry, J. (2004). Essential Role of the NH2-terminal WD/EPF Motif in the Phosphorylation-activated Protective Function of Mammalian Hsp27. J. Biol. Chem. 279: 23463-23471 [Abstract] [Full Text]  
  • Mo, Y.-Y., Yu, Y., Ee, P. L. R., Beck, W. T. (2004). Overexpression of a Dominant-Negative Mutant Ubc9 Is Associated with Increased Sensitivity to Anticancer Drugs. Cancer Res. 64: 2793-2798 [Abstract] [Full Text]  
  • Boellmann, F., Guettouche, T., Guo, Y., Fenna, M., Mnayer, L., Voellmy, R. (2004). DAXX interacts with heat shock factor 1 during stress activation and enhances its transcriptional activity. Proc. Natl. Acad. Sci. USA 101: 4100-4105 [Abstract] [Full Text]  
  • Duverger, O., Paslaru, L., Morange, M. (2004). HSP25 Is Involved in Two Steps of the Differentiation of PAM212 Keratinocytes. J. Biol. Chem. 279: 10252-10260 [Abstract] [Full Text]  
  • Hofmann, T. G., Stollberg, N., Schmitz, M. L., Will, H. (2003). HIPK2 Regulates Transforming Growth Factor-{beta}-Induced c-Jun NH2-Terminal Kinase Activation and Apoptosis in Human Hepatoma Cells. Cancer Res. 63: 8271-8277 [Abstract] [Full Text]  
  • Song, J. J., Lee, Y. J. (2003). Role of the ASK1-SEK1-JNK1-HIPK1 Signal in Daxx Trafficking and ASK1 Oligomerization. J. Biol. Chem. 278: 47245-47252 [Abstract] [Full Text]  
  • Chen, L.-Y., Chen, J. D. (2003). Daxx Silencing Sensitizes Cells to Multiple Apoptotic Pathways. Mol. Cell. Biol. 23: 7108-7121 [Abstract] [Full Text]  
  • Gober, M. D., Smith, C. C., Ueda, K., Toretsky, J. A., Aurelian, L. (2003). Forced Expression of the H11 Heat Shock Protein Can Be Regulated by DNA Methylation and Trigger Apoptosis in Human Cells. J. Biol. Chem. 278: 37600-37609 [Abstract] [Full Text]  
  • Kim, E.-J., Park, J.-S., Um, S.-J. (2003). Identification of Daxx interacting with p73, one of the p53 family, and its regulation of p53 activity by competitive interaction with PML. Nucleic Acids Res 31: 5356-5367 [Abstract] [Full Text]  
  • Park, K.-J., Gaynor, R. B., Kwak, Y. T. (2003). Heat Shock Protein 27 Association with the I{kappa}B Kinase Complex Regulates Tumor Necrosis Factor {alpha}-induced NF-{kappa}B Activation. J. Biol. Chem. 278: 35272-35278 [Abstract] [Full Text]  
  • Chavez Zobel, A. T., Loranger, A., Marceau, N., Theriault, J. R., Lambert, H., Landry, J. (2003). Distinct chaperone mechanisms can delay the formation of aggresomes by the myopathy-causing R120G {alpha}B-crystallin mutant. Hum Mol Genet 12: 1609-1620 [Abstract] [Full Text]  
  • Hammel, J. M., Caldarone, C. A., Van Natta, T. L., Wang, L. X., Welke, K. F., Li, W., Niles, S., Barner, E., Scholz, T. D., Behrendt, D. M., Segar, J. L. (2003). Myocardial apoptosis after cardioplegic arrest in the neonatal lamb. J. Thorac. Cardiovasc. Surg. 125: 1268-1275 [Abstract] [Full Text]  
  • Akbar, M. T., Lundberg, A. M. C., Liu, K., Vidyadaran, S., Wells, K. E., Dolatshad, H., Wynn, S., Wells, D. J., Latchman, D. S., de Belleroche, J. (2003). The Neuroprotective Effects of Heat Shock Protein 27 Overexpression in Transgenic Animals against Kainate-induced Seizures and Hippocampal Cell Death. J. Biol. Chem. 278: 19956-19965 [Abstract] [Full Text]  
  • Michaelson, J. S., Leder, P. (2003). RNAi reveals anti-apoptotic and transcriptionally repressive activities of DAXX. J. Cell Sci. 116: 345-352 [Abstract] [Full Text]  
  • Ohiro, Y., Usheva, A., Kobayashi, S., Duffy, S. L., Nantz, R., Gius, D., Horikoshi, N. (2003). Inhibition of Stress-Inducible Kinase Pathways by Tumorigenic Mutant p53. Mol. Cell. Biol. 23: 322-334 [Abstract] [Full Text]  
  • Sakamoto, H., Mashima, T., Yamamoto, K., Tsuruo, T. (2002). Modulation of Heat-shock Protein 27 (Hsp27) Anti-apoptotic Activity by Methylglyoxal Modification. J. Biol. Chem. 277: 45770-45775 [Abstract] [Full Text]  
  • Robert, A., Miron, M.-J., Champagne, C., Gingras, M.-C., Branton, P. E., Lavoie, J. N. (2002). Distinct cell death pathways triggered by the adenovirus early region 4 ORF 4 protein. JCB 158: 519-528 [Abstract] [Full Text]  
  • Rafiee, P., Shi, Y., Kong, X., Pritchard, K. A. Jr, Tweddell, J. S., Litwin, S. B., Mussatto, K., Jaquiss, R. D., Su, J., Baker, J. E. (2002). Activation of Protein Kinases in Chronically Hypoxic Infant Human and Rabbit Hearts: Role in Cardioprotection. Circulation 106: 239-245 [Abstract] [Full Text]  
  • Lin, D.-Y., Shih, H.-M. (2002). Essential Role of the 58-kDa Microspherule Protein in the Modulation of Daxx-dependent Transcriptional Repression as Revealed by Nucleolar Sequestration. J. Biol. Chem. 277: 25446-25456 [Abstract] [Full Text]  
  • Wyttenbach, A., Sauvageot, O., Carmichael, J., Diaz-Latoud, C., Arrigo, A.-P., Rubinsztein, D. C. (2002). Heat shock protein 27 prevents cellular polyglutamine toxicity and suppresses the increase of reactive oxygen species caused by huntingtin. Hum Mol Genet 11: 1137-1151 [Abstract] [Full Text]  
  • Narberhaus, F. (2002). {alpha}-Crystallin-Type Heat Shock Proteins: Socializing Minichaperones in the Context of a Multichaperone Network. Microbiol. Mol. Biol. Rev. 66: 64-93 [Abstract] [Full Text]  
  • Gingras, M.-C., Champagne, C., Roy, M., Lavoie, J. N. (2002). Cytoplasmic Death Signal Triggered by Src-Mediated Phosphorylation of the Adenovirus E4orf4 Protein. Mol. Cell. Biol. 22: 41-56 [Abstract] [Full Text]  
  • Ko, Y.-G., Kang, Y.-S., Park, H., Seol, W., Kim, J., Kim, T., Park, H.-S., Choi, E.-J., Kim, S. (2001). Apoptosis Signal-regulating Kinase 1 Controls the Proapoptotic Function of Death-associated Protein (Daxx) in the Cytoplasm. J. Biol. Chem. 276: 39103-39106 [Abstract] [Full Text]  
  • Jiang, T., Altman, S. (2001). Protein-protein interactions with subunits of human nuclear RNase P. Proc. Natl. Acad. Sci. USA 10.1073/pnas.021561498v1 [Abstract] [Full Text]  
  • Charette, S. J., Lambert, H., Landry, J. (2001). A Kinase-independent Function of Ask1 in Caspase-independent Cell Death. J. Biol. Chem. 276: 36071-36074 [Abstract] [Full Text]  
  • Jiang, T., Altman, S. (2001). Protein-protein interactions with subunits of human nuclear RNase P. Proc. Natl. Acad. Sci. USA 98: 920-925 [Abstract] [Full Text]