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HSP27 Phosphorylation-mediated Resistance against Actin Fragmentation and Cell Death Induced by Oxidative Stress¹

Centre de Recherche en Cancérologie de l'Université Laval, L'Hôtel-Dieu de Québec, 11 Côte du Palais, Québec, G1R 2J6 Canada [J. H., F. H., J. L.], and Washington University School of Medicine, Section of Cancer Biology, St. Louis, Missouri [D. R. S.]

Phosphorylation of heat shock protein 27 (HSP27) has been suggested to play an important role in the regulation of F-actin dynamics in response to growth factors and stress. Because the microfilament network is one of the earliest targets of oxidative stress and because phosphorylation of HSP27 is strongly induced by reactive oxygen metabolites, we have investigated the role of HSP27 phosphorylation in regulating actin dynamics in response to oxidative stress. Experiments were done in Chinese hamster CCL39 cells overexpressing various levels of the wild-type or a nonphosphorylatable form of human HSP27 (pm3 HSP27). In control cells, both H₂O₂ and menadione induced fragmentation of F-actin, which forms aggregates and patches concentrated around the nucleus. Stable overexpression of wild-type HSP27, but not of pm3 HSP27, conferred resistance against actin fragmentation, suggesting that HSP27 has a phosphorylation-activated protective function against actin disruption by oxidative stress. Cell lines that overexpressed the highest levels of the wild-type form of human HSP27 also showed an increased cell survival following exposure to H₂O₂. In contrast, cells expressing pm3 HSP27 were as sensitive as the controls to the lethal effect of H₂O₂. These results suggest that phosphorylation of HSP27 is causally related to the regulation of microfilatment dynamics following oxidative stress and may be involved in mediating an adaptive response to oxyradical-generating agents such as carcinogens, anticancer drugs, and other xenobiotics.

¹ This work was supported by La Société de Recherche sur le Cancer Inc (to J. L. and J. H.), Grant MT-7088 from the Medical Research Council of Canada (to J. L.), and NIH Grants HL 51469 and PO1-CA51116 (to D. R. S.).

² To whom requests for reprints should be addressed.

Received 5/ 4/95. Accepted 11/ 6/95.

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				R. Z. Lin, Z.-W. Hu, J. H. Chin, and B. B. Hoffman Heat Shock Activates c-Src Tyrosine Kinases and Phosphatidylinositol 3-Kinase in NIH3T3 Fibroblasts J. Biol. Chem., December 5, 1997; 272(49): 31196 - 31202. [Abstract] [Full Text] [PDF]

				G. Lutsch, R. Vetter, U. Offhauss, M. Wieske, H.-J. Grone, R. Klemenz, I. Schimke, J. Stahl, and R. Benndorf Abundance and Location of the Small Heat Shock Proteins HSP25 and {alpha}B-Crystallin in Rat and Human Heart Circulation, November 18, 1997; 96(10): 3466 - 3476. [Abstract] [Full Text]

				M. R. Leroux, R. Melki, B. Gordon, G. Batelier, and E. P. M. Candido Structure-Function Studies on Small Heat Shock Protein Oligomeric Assembly and Interaction with Unfolded Polypeptides J. Biol. Chem., September 26, 1997; 272(39): 24646 - 24656. [Abstract] [Full Text] [PDF]

				J. Huot, F. Houle, F. Marceau, and J. Landry Oxidative Stress–Induced Actin Reorganization Mediated by the p38 Mitogen-Activated Protein Kinase/Heat Shock Protein 27 Pathway in Vascular Endothelial Cells Circ. Res., March 1, 1997; 80(3): 383 - 392. [Abstract] [Full Text]

				P Liang and T. MacRae Molecular chaperones and the cytoskeleton J. Cell Sci., January 7, 1997; 110(13): 1431 - 1440. [Abstract] [PDF]

				J Guay, H Lambert, G Gingras-Breton, J. Lavoie, J Huot, and J Landry Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27 J. Cell Sci., January 2, 1997; 110(3): 357 - 368. [Abstract] [PDF]

				C. Liu, R. R. Gilmont, R. Benndorf, and M. J. Welsh Identification and Characterization of a Novel Protein from Sertoli Cells, PASS1, That Associates with Mammalian Small Stress Protein hsp27 J. Biol. Chem., June 16, 2000; 275(25): 18724 - 18731. [Abstract] [Full Text] [PDF]

				K. M. Park, A. Chen, and J. V. Bonventre Prevention of Kidney Ischemia/Reperfusion-induced Functional Injury and JNK, p38, and MAPK Kinase Activation by Remote Ischemic Pretreatment J. Biol. Chem., April 6, 2001; 276(15): 11870 - 11876. [Abstract] [Full Text] [PDF]

				M. Razandi, A. Pedram, and E. R. Levin Estrogen Signals to the Preservation of Endothelial Cell Form and Function J. Biol. Chem., December 1, 2000; 275(49): 38540 - 38546. [Abstract] [Full Text] [PDF]

				D. Volonte, F. Galbiati, R. G. Pestell, and M. P. Lisanti Cellular Stress Induces the Tyrosine Phosphorylation of Caveolin-1 (Tyr14) via Activation of p38 Mitogen-activated Protein Kinase and c-Src kinase. EVIDENCE FOR CAVEOLAE, THE ACTIN CYTOSKELETON, AND FOCAL ADHESIONS AS MECHANICAL SENSORS OF OSMOTIC STRESS J. Biol. Chem., March 9, 2001; 276(11): 8094 - 8103. [Abstract] [Full Text] [PDF]

				K. M. Park, C. Kramers, M. Vayssier-Taussat, A. Chen, and J. V. Bonventre Prevention of Kidney Ischemia/Reperfusion-induced Functional Injury, MAPK and MAPK Kinase Activation, and Inflammation by Remote Transient Ureteral Obstruction J. Biol. Chem., January 11, 2002; 277(3): 2040 - 2049. [Abstract] [Full Text] [PDF]