SAPK2/p38-dependent F-actin reorganization regulates early membrane blebbing during stress-induced apoptosis

Journal of Cell Biology

Volumn 143, Issue 5, 1998, Pages 1361-1373

  Huot, Jacques ^a   Houle, François ^a   Rousseau, Simon ^a   Deschesnes, Réna G ^a   Shah, Girish M ^a   Landry, Jacques ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

Apoptosis; Blebbing; F actin; HSP27; SAPK2 p38

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CASPASE; CISPLATIN; CYTOCHALASIN D; DNA FRAGMENT; F ACTIN; HEAT SHOCK PROTEIN 27; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE;

ACTIN POLYMERIZATION; APOPTOSIS; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVITY; FIBROBLAST; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STRESS;

ACTINS; ANIMALS; APOPTOSIS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL ADHESION; CELL MEMBRANE; CELLS, CULTURED; CISPLATIN; CRICETINAE; ENZYME ACTIVATION; HEAT-SHOCK PROTEINS; HUMANS; HYDROGEN PEROXIDE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES;

EID: 0032583203     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.143.5.1361     Document Type: Article

References (70)

1. Alexander, M.A., J.E., Meredith, and W.K. Kiosses. 1998. An activated Rac mutant functions as a dominant negative for membrane ruffling. Oncogene. 17:625-629.
2. Bauer, P.I., G. Farkas, L. Buday, G. Mikala, G. Meszaros, E. Kun, and A. Farago. 1992. Inhibition of DNA binding by the phosphorylation of poly ADP-ribose polymerase protein catalyzed by protein kinase C. Biochem. Biuphys. Res. Commun. 187:730-736.
3. Becker, L.C., and G. Ambrosio. 1987. Myocardial consequences of reperfusion. Progr. Cardiovasc. Dis. 30:23-44.
4. Benndorf, R., K. Haye, S. Ryazantsev, M. Wieske, J. Behlke, and G. Lutsch. 1994. Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerizion-inhibiting activity. J. Biol. Chem. 269:255-261.
5. Bradley, J.R., S. Thiru, and J.S. Pober. 1995. Hydrogen peroxide-induced endothelial retraction is accompanied by a loss of the normal spatial organization of endothelial cell adhesion molecules. Am. J. Pathol. 147:627-641.
6. Brenner, B., U. Koppenhoefer, C. Weinstock, O. Linderkamp, F. Lang, and E. Gulbins. 1997. Fas-or ceramide-induced apoptosis is mediated by a Rac1-regulated activation of Jun N-terminal kinase/p38 kinases and GADD153. J. Biol. Chem. 272:22173-22181.
7. Burridge, K., M. Chrzanowska-Wodnicka, and C. Zhong. 1997. Focal adhesion assembly. Trends Cell Biol. 7:342-347.
8. Cahill, M.A., M.E. Peter, F.C. Kischkel, A.R. Chinnaiyan, V.D. Dixit, P.H. Krammer, and A. Nordheim. 1996. CD95 (APO-1/Fas) induces activation of SAP kinases downstream of ICE-like proteases. Oncogene. 13:2087-2096.
9. Cardone, M.H., G.S. Salvesen, C. Widmann, G. Johnson, and S.M. Frish. 1997. The regulation of anoikis: MEKK-1 activation requires cleavage by caspases. Cell. 90:315-323.
10. Cohen, P. 1997. The search for physiological substrates of MAP and SAP kinases in mammalian cells. Trends Cell Biol. 7:353-361.
11. Cuenda, A., J. Rouse, Y.N. Doza, R. Meier, P. Cohen, T.F. Gallagher, P.R. Young, and J.C. Lee. 1995. SB203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 364:229-233.
12. Cunningham, C.C. 1995. Actin polymerization and intracellular solvent flow in cell surface blebbing. J. Cell Biol. 129:1589-1599.
13. Darmon, A.J, D.W. Nicholson, and R.C. Beackley. 1995. Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme B. Nature. 377: 446-448.
14. de Murcia, G., and J. Ménissier-de Murcia. 1994. Poly (ADP-ribose) polymerase: a molecular nick sensor. Trends Biochem. Sci. 19:172-176.
15. Dudley, D.T., L. Pang, S.J. Decker, A.J. Bridges, and A.L Saltiel. 1995. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA. 92:7686-7689.
16. Enari, M., R.V. Talanian, W.W. Wong, and S. Nagata. 1996. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature. 380:723-726.
17. Fishkind, D.J., L. Cao, and Y. Wang. 1991. Microinjection of the catalytic fragment of myosin light chain kinase into dividing cells: effects on mitosis and cytokinesis. J. Cell Biol. 114:967-975.
18. Frisch, S.M., and H. Francis. 1994. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124:619-626.
19. Gores, G.J., B. Herman, and J.J. Lemasters. 1990. Plasma membrane bleb formation and rupture: a common feature of hepatocellular injury. Hepatology. 4:609-698.
20. Guay, J., H. Lambert, G. Gingras-Breton, J.N. Lavoie, J. Huot, and J. Landry. 1997. Regulation of actin filament dynamics by p38 map kinase mediated phosphorylation of heat shock protein. J. Cell Sci. 110:357-368.
21. 2. J. Biol. Chem. 271:4138-4142.
22. Hardy, M.M., A.G. Flickinger, D.P. Riley, R.H. Weiss, and U.S. Ryan. 1994. Superoxide dismutase mimetics inhibit neutrophil-mediated human aortic endothelial cell injury in vitro. J. Biol. Chem. 269:18535-18540.
23. Hastie, L.E., W.F. Patton, H.B. Hechtman, and D. Shepro. 1997. Filamin redistribution in an endothelial cell reoxygenation injury model. Free Radic. Biol. Med. 22:955-966.
24. Huot, J., H. Lambert, J.N. Lavoie, A. Guimond, F. Houle, and J. Landry. 1995. Characterization of 45-kDa/54-kDa HSP27 kinase, a stress-sensitive kinase which may activate the phosphorylation-dependent protective function of mammalian 27-kDa heat shock protein HSP27. Eur. J. Biochem. 227:416-427.
25. Huot, J., F. Houle, D.R. Spitz, and J. Landry. 1996. HSP27 phosphorylation-mediated resistance against actin fragmentation and cell death induced by oxidative stress. Cancer Res. 56:273-279.
26. Huot, J., F. Houle, F. Marceau, and J. Landry. 1997. Oxidative stress-induced actin reorganization mediated by the p38 mitogen-activated protein kinase/ heat shock protein 27 pathway in vascular endothelial cells. Circ. Res. 80: 383-392.
27. Juo, P., C.J. Kuo, S.E. Reynolds, R.F. Konz, J. Raingeaud, R.J. Davis, H.P. Biemann, and J. Blenis. 1997. Fas activation of the p38 mitogen-activated protein kinase signalling pathway requires ICE/CED-family proteases. Mol. Cell Biol. 17:24-35.
28. Katoh, O., H. Tauchi, K. Kawaishi, A. Kimura, and Y. Satow. 1995. Expression of the vascular endothelial growth factor (VEGF) receptor gene, KDR, in hematopoietic cells and inhibitory effect of VEGF on apoptotic cell death caused by ionizing radiation. Cancer Res. 55:5687-5692.
29. Kawasaki, H., T. Morooka, S. Shimohama, J. Kimura, T. Hirano, Y. Gotoh, and E. Nishida. 1997. Activation and involvement of p38 mitogen-activated protein kinase in glutamate-induced apoptosis in rat cerebellar granule cells. J. Biol. Chem. 272:18518-18521.
30. Kumar, S., M.J., Orsini, J.C. Lee, P.C. McDonnell, C. Debouck, and P.R. Young. 1996. Activation of the HIV-1 long terminal repeat by cytokines and environmental stress requires an active CSBP/p38 MAP kinase. J. Biol. Chem. 271:30864-30869.
31. Kummer, J.L., P.R. Rao, and K.R. Heidenreich. 1997. Apoptosis induced by withdrawal of trophic factors is mediated by p38 mitogen-activated protein kinase. J. Biol. Chem. 272:20490-20494.
32. Landry, J., P. Chrétien, H. Lambert, E. Hickey, and L.A. Weber. 1989. Heat shock resistance conferred by expression of the human HSP27 gene in rodent cells. J. Cell Biol. 109:93-101.
33. Lavoie, J.N., E. Hickey, L.A. Weber, and J. Landry. 1993. Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27. J. Biol. Chem. 268:24210-24214.
34. Lavoie, J.N., H. Lambert, E. Hickey, L.A. Weber, and J. Landry. 1995. Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27. Mol. Cell. Biol. 15:505-516.
35. Lee, J.U., R. Hosotani, M. Wada, R. Doi, T. Kosiba, K. Fujimoto, C. Mori, N. Nakamura, K. Shiota, and M. Imamura. 1997. Mechanism of apoptosis induced by cisplatin and VP16 in PANC-1 cells. Anticancer Res. 17:3445-3450.
36. Martin, S.J., G.A. O'Brien, W.K. Nishioka, A.J. McGahon, A. Mahboubi, T.C. Saido, and D.R. Green. 1995. Proteolysis of fodrin (non erythroid spectrin) during apoptosis. J. Biol. Chem. 270:6425-6428.
37. Martin, S.M., D.R. Green, and T.G. Cotter. 1994. Dicing with death: dissecting the components of the apoptosis machinery. Trends Biol. Sci. 19:26-30.
38. McCarthy, N.J., M.K.B. Whyte, C.S. Gilbert, and G.I. Evan. 1997. Inhibition of Ced-3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or the Bcl-2 homologue Bak. J. Cell Biol. 136:215-227.
39. McLaughlin, M.M., S. Kumar, P.C. McDonnell, S. Van Horn, J.C. Lee, G.P. Livi, and P.R. Young. 1996. Identification of mitogen-activated protein (MAP) kinase-activated protein kinase-3, a novel substrate of CSBP p38 MAP kinase. J. Biol. Chem. 271:8488-8492.
40. Michiels, C., T. Arnoud, A. Houbion, and J. Remacle. 1992. Human umbilical vein endothelial cells submitted to hypoxia-reoxygenation in vitro: implication of free radicals, xanthine oxidase, energy deficiency. J. Cell. Physiol. 153:53-61.
41. Mills, J.C., N.L. Stone, J. Erhardt, and R.N. Pittman. 1998. Apoptotic membrane blebbing is regulated by myosin light chain phosphorylation. J. Cell Biol. 140:627-636.
42. Mirabelli, F., A. Salis, V. Marinoni, G. Finardi, G. Bellomo, H. Thor, and S. Orrenius. 1988. Menadione-induced bleb formation in hepatocytes is associated with the oxidation of thiol groups in actin. Arch. Biochem. Biophys. 264: 261-269.
43. Mitchison, T.J., and L.P. Cramer. 1996. Actin-based cell motility and cell locomotion. Cell. 84:371-379.
44. Miyoshi, H., K. Umeshita, M. Sakon, S. Imajoh-Ohmi, K. Fujitani, M. Gotoh, E. Oiki, J. Kambayashi, and M. Monden. 1996. Calpain activation in plasma membrane bleb formation during tert-butyl hydroperoxide-induced rat hepatocyte injury. Gastroenterology. 110:1897-1904.
45. Mosser, D.D., A.W. Caron, L. Bourget, C. Denis-Larose, and B. Massie. 1997. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol. Cell. Biol. 17:5317-5327.
46. Na, S., T.H. Chuang, A. Cunningham, T.G. Turi, J.H. Hanke, G.M. Bokoch, and D.E. Danley. 1996. D4-GDI, a substrate of CPP32, is proteolyzed during Fas-induced apoptosis. J. Biol. Chem. 271:11209-11213.
47. Nobes, C.D., and A. Hall. 1995. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 81:53-62.
48. Phelps, P.C., M.W. Smith, and B.F. Trump. 1989. Cytosolic ionized calcium and bleb formation after acute cell injury of cultured rabbit renal tubule cells. Lab. Invest. 60:630-642.
49. Pietrowicz, R.S., and E.G. Levin. 1997. Basolateral membrane-associated 27-kDa heat shock protein and microfilament polymerization. J. Biol. Chem. 272:25920-25927.
50. Re, F., A. Zanetti, M. Sironi, N. Polentarutti, L. Lanfrancone, E. Dejana, and F. Colotta. 1994. Inhibition of anchorage-dependent cell spreading triggers apoptosis in cultured human endothelial cells. J. Cell Biol. 127:537-546.
51. Rouse, J., P. Cohen, S. Trigon, M. Morange, A. Alonso-Llamazares, D. Zamanillo, T. Hunt, and A.R. Nebrada. 1994. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell. 78:1027-1037.
52. Rousseau, S., F. Houle, J. Landry, and J. Huot. 1997. p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene. 15:2169-2177.
53. Ruscetti, T., B.E. Lehnert, J. Halbrook, H. Le Trong, M.F. Hoekstra, D.J. Chen, and S.R. Peterson. 1998. Stimulation of the DNA-dependent protein kinase by poly (ADP-ribose) polymerase. J. Biol. Chem. 273:14461-14467.
54. Saitoh, M., H. Nishitoh, M. Fujii, K. Takeda, K. Tobiume, Y. Sawada, M. Kawabata, K. Miyazono, and H. Ichijo. 1998. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO (Eur. Mol. Bio. Organ.) J. 17:2596-2606.
55. Sanchez-Perez, I., J.R. Murguia, and R. Perona. 1998. Cisplatin induces a persistent activation of JNK that is related to cell death. Oncogene. 16:533-540.
56. Schwenger, P., P. Bellosta, I. Victor, C. Basilico, E.Y. Skolnik, and J. Vilcek. 1997. Sodium salicylate induces apoptosis via p38 mitogen-activated protein kinase but inhibits tumor necrosis factor-induced c-Jun N-terminal stress-activated protein kinase activation. Proc. Natl. Acad. Sci. USA. 94:2869-2873.
57. 2-terminal kinase-mediated activation of interleukin-1β converting enzyme/CED-3-like protease during anticancer drug-induced apoptosis. J. Biol. Chem. 272:4631-4636.
58. Shah, G.M., S.H. Kaufman, and G.G. Poirier. 1995. Detection of poly-(ADP-ribose) polymerase and its apoptosis-specific fragment by a nonisotopic activity-Western blot technique. Anal. Biochem. 232:251-254.
59. Shah, G.M., R.G. Shah, and G.G. Poirier. 1996. Different cleavage pattern for poly(ADP-ribose) polymerase during apoptosis and necrosis in HL-60 cells. Biochem. Biophys. Res. Commun. 229:838-844.
60. Toyoshima, F., T. Moriguchi, and E. Nishida. 1997. Fas induces cytoplasmic responses and activation of the MKK7-JNK/SAPK and MKK6-p38 pathways independent of CPP32-like proteases. J. Cell Biol. 139:1005-1015.
61. Van de Voorde, J., H. Vanderstichele, and I. Levsen. 1987. Release of endothelium-derived relaxing factor from human umbilical vessels. Circ. Res. 60: 517-522.
62. van der Zee, R., T. Murohara, Z. Luo, F. Zollmann, J. Passeri, C. Lekutat, and J.M. Isner. 1997. Vascular endothelial growth factor/vascular permeability factor augments nitric oxide release from quiescent rabbit and human vascular endothelium. Circulation. 18:1030-1037.
63. Verheij, M., R. Bose, X.H. Lin, B. Yao, W.D. Jarvis, S. Grant, M.J. Birrer, E. Szabo, L.J. Zon, J.M. Kyriakis, et al. 1996. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature. 380:75-79.
64. Waskiewicz, A.J., and J.A. Cooper. 1995. Mitogen and stress response pathways: Map kinase cascades and phosphatase regulation in mammals and yeast. Curr. Opin. Cell Biol. 7:798-805.
65. Watanabe, N., P. Madaule, T. Reid, T. Ishizaki, G. Watanabe, A. Kakizuka, Y. Saito, K. Nakao, B.M. Jockusch, and S. Narumiya. 1997. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO (Eur. Mol. Biol. Organ.) J. 16: 3044-3056.
66. Wei, Y.Q., X. Zhao, Y. Karya, K. Teshigawara, and A. Uchida. 1995. Inhibition of proliferation and induction of apoptosis by abrogation of heat shock protein (HSP)70 expression in tumor cells. Cancer Immunol. Immunother. 40: 73-78.
67. Xia, Z., M. Dickens, J. Raingeaud, R.J. Davis, and M.E. Greenberg. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science. 270: 1326-1331.
68. Zanke, B.W., K. Boudreau, E. Rubie, E. Winnett, L.A. Tibbles, L. Zon, J. Kyriakis, F.F. Liu, and J.R. Woodgett. 1996. The stress activated protein kinase pathway mediates cell death following injury induced by cis-platinum, UV irradiation or heat. Curr. Biol. 6:606-613.
69. Zhao, Y., and H.W. Davis. 1998. Hydrogen peroxide-induced cytoskeletal rearrangement in cultured pulmonary endothelial cells. J. Cell. Physiol. 174:370-379.
70. Zulueta, J.J., R. Sawhney, F.S. Yu, C.C. Cote, and P.M. Hassoum. 1997. Intracellular generation of reactive oxygen species in endothelial cells exposed to anoxia-reoxygenation. Am. J. Physiol. 272:L897-L902.