HSP27 expression regulates CCK-induced changes of the actin cytoskeleton in CHO-CCK-A cells

American Journal of Physiology

Volumn 277, Issue 6 PART 1, 1999, Pages

  Schäfer, Claus ^a,c   Clapp, Peter ^a   Welsh, Michael J ^a   Benndorf, Rainer ^a   Williams, John A ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Cholecystokinin; Heat shock protein; Microfilaments; p38 mitogen activated protein kinase

Indexed keywords

CHOLECYSTOKININ; HEAT SHOCK PROTEIN 27; MITOGEN ACTIVATED PROTEIN KINASE;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL PROTECTION; CHO CELL; CONTROLLED STUDY; CYTOSKELETON; HORMONAL REGULATION; HORMONE ACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ACTINS; ACUTE DISEASE; ANIMALS; CAERULEIN; CELL FRACTIONATION; CHO CELLS; CRICETINAE; CULTURE MEDIA, SERUM-FREE; DETERGENTS; ENZYME ACTIVATION; ENZYME INHIBITORS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; HEAT-SHOCK PROTEINS; HUMANS; IMIDAZOLES; MAP KINASE SIGNALING SYSTEM; MICROFILAMENTS; MITOGEN-ACTIVATED PROTEIN KINASES; MUTAGENESIS; OCTOXYNOL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PANCREATITIS; PHOSPHORYLATION; PYRIDINES; RATS; RECEPTOR, CHOLECYSTOKININ A; RECEPTORS, CHOLECYSTOKININ; SINCALIDE; TRANSFECTION;

ANIMALIA; CRICETINAE; CRICETULUS GRISEUS; RODENTIA; STAPHYLOCOCCUS PHAGE 3A;

EID: 0033373475     PISSN: 00029513     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.1999.277.6.c1032     Document Type: Article

References (37)

1. Arrigo, A.-P., and J. Landry. Expression and function of the low-molecular-weight heat shock proteins. In: The Biology of Heat Shock Proteins and Molecular Chaperones, edited by R. I. Morimoto, A. Tissieres, and C. Georgopoulos. New York: Cold Spring Harbor Laboratory, 1994, p. 335-374.
2. Benndorf, R., K. Hayess, S. Ryazantsev, M. Wieske, J. Behlke, and G. Lusch. Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J. Biol. Chem. 269: 20780-20784, 1994.
3. Burridge, K., K. Fath, T. Kelly, G. Nuckolls, and C. Turner. Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 4: 487-525, 1988.
4. Del Vecchio, P. J., K. S. MacElroy, M. P. Rosser, and R. L. Church. Association of α-crystallin with actin in cultured lens cells. Curr. Eye Res. 3: 1213-1219, 1984.
5. Gething, M. J., and J. Sambrook. Protein folding in the cell. Nature 355: 33-45, 1992.
6. Goh, E. L. K., T. J. Pircher, T. J. J. Wood, G. Norstedt, R. Graichen, and P. E. Lobie. Growth hormone-induced reorganization of the actin cytoskeleton is not required for STAT5 (signal transducer and activator of transcription-5)-mediated transcription. Endocrinology 138: 3207-3215, 1997.
7. Groblewski, G. E., T. Grady, N. Mehta, H. Lambert, C. D. Logsdon, J. Landry, and J. A. Williams. Cholecystokinin stimulates heat shock protein 27 phosphorylation in rat pancreas both in vivo and in vitro. Gastroenterology 112: 1354-1361, 1997.
8. Guay, J., H. Lambert, G. Gingras-Breton, J. N. 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. 110: 357-368, 1997.
9. Hickey, E., S. E. Brandon, R. Potter, G. Stein, J. Stein, and L. A. Weber. Sequence and organization of genes encoding the human 27 kDa heat shock protein. Nucleic Acids Res. 14: 4127-4145, 1986.
10. Huot, J., F. Houle, F. Marceau, and J. Landry. Oxidative stress-induced reorganization mediated by the p38 mitogen-activated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ. Res. 80: 383-392, 1997.
11. Huot, J., F. Houle, D. R. Spitz, and J. Landry. HSP27 phosphorylation-mediated resistance against actin fragmentation and cell death induced by oxidative stress. Cancer Res. 56: 273-279, 1996.
12. r 27,000 heat-shock protein. Cancer Res. 51: 5245-5252, 1991.
13. Jakob, U., M. Gaestel, K. Engel, and J. Buchner. Small heat shock proteins are molecular chaperones. J. Biol. Chem. 268: 1517-1520, 1993.
14. Knauf, U., U. Jakob, K. Engel, J. Buchner, and M. Gaestel. Stress- and mitogen-induced phosphorylation of the small heat shock protein Hsp25 by MAPKAP kinase 2 is not essential for chaperone properties and cellular thermoresistance. EMBO J. 13: 54-60, 1994.
15. Landry, J., P. Chretien, H. Lambert, E. Hickey, and L. A. Weber. Heat shock resistance conferred by expression of the human HSP27 gene in rodent cells. J. Cell Biol. 109: 7-15, 1989.
16. Landry, J., and J. Huot. Modulation of actin dynamics during stress and physiological stimulation by a signaling pathway involving p38 MAP kinase and heat-shock protein 27. Biochem. Cell Biol. 73: 703-707, 1995.
17. Lavoie, J. N., G. Gingras-Breton, R. M. Tanguay, and J. Landry. Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock. HSP27 stabilization of the microfilament organization. J. Biol. Chem. 268: 3420-3429, 1993.
18. Lavoie, J. N., H. Lambert, E. Hickey, L. A. Weber, and J. Landry. Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27. J. Biol. Chem. 268: 24210-24214, 1993.
19. Lavoie, J. N., H. Lambert, E. Hickey, L. A. Weber, and J. Landry. 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, 1995.
20. Lee, S.-W., and J. J. Otto. Vinculin and talin: kinetics of entry and exit from the cytoskeletal pool. Cell Motil. Cytoskeleton 36: 101-111, 1997.
21. Loktionova, S. A., and A. E. Kabakov. Protein phosphatase inhibitors and heat preconditioning prevent Hsp27 dephosphorylation, F-actin disruption and deterioration of morphology in ATP-depleted endothelial cells. FEBS Lett. 433: 294-300, 1998.
22. Lutsch, G., R. Vetter, U. Offhaus, 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 αB-crystallin in rat and human heart. Circulation 96: 3466-3476, 1997.
23. Mehlen, P., E. Hickey, L. A. Weber, and A. P. Arrigo. Large unphosphorylated aggregates as the active forms of hsp27 which controls intracellular reactive oxygen species and glutathione levels and generates a protection against TNFα in NIH-3T3-ras cells. Biochem. Biophys. Res. Commun. 241: 187-192, 1997.
24. Mehlen, P., X. Preville, P. Chareyron, J. Briolay, R. Klemenz, and A. P. Arrigo. Constitutive expression of human hsp27, Drosophila hsp27, or human B-crystallin confers resistance to TNF- and oxidative stress-induced cytotoxicity in stably transfected murine L929 fibroblasts. J. Immunol. 154: 363-374, 1995.
25. Mehlen, P., K. Schulze-Osthoff, and A. P. Arrigo. Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/APO-1 and staurosporine-induced cell death. J. Biol. Chem. 271: 16510-16514, 1996.
26. Miron, T., K. Vancompernolle, J. Vandekerckhove, M. Wilchek, and B. Geiger. A 25-kD inhibitor of actin polymerization is a low molecular mass heat shock protein. J. Cell Biol. 114: 255-261, 1991.
27. Miron, T., M. Wilchek, and B. Geiger. Characterization of an inhibitor of actin polymerization in vinculin-rich fraction of turkey gizzard smooth muscle. Eur. J. Biochem. 178: 543-553, 1988.
28. Muallem, S., K. Kwiatkowska, X. Xu, and H. L. Yin. Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J. Cell Biol. 128: 589-598, 1995.
29. Musch, M. W., K. Sugi, D. Strauss, and E. B. Chang. Heat-shock protein 72 protects against oxidant-induced injury of barrier function of human colonic epithelial Caco2/bbe cells. Gastroenterology 117: 115-122, 1999.
30. O'Konski, M. S., and S. J. Pandol. Cholecystokinin JMV-180 and caerulein effects on the pancreatic acinar cell cytoskeleton. Pancreas 8: 638-646, 1993.
31. Piotrowicz, R. S., E. Hickey, and E. G. Levin. Heat shock protein 27 kDa expression and phosphorylation regulates endothelial cell migration. FASEB J. 12: 1481-1490, 1998.
32. Piotrowicz, R. S., and E. G. Levin. Basolateral membrane-associated 27-kDa heat shock protein and microfilament polymerization. J. Biol. Chem. 272: 25920-25927, 1998.
33. Sakamoto, K., T. Urushidani, and T. Nagao. Translocation of Hsp27 to cytoskeleton by repetitive hypoxia-reoxygenation in the rat myoblast cell line, H9c2. Biochem. Biophys. Res. Commun 251: 576-579, 1998.
34. Schäfer, C., S. E. Ross, M. J. Bragado, G. E. Groblewski, S. A. Ernst, and J. A. Williams. A role for the p38 mitogen-activated protein kinase/Hsp27 pathway in cholecystokinin-induced changes in the actin cytoskeleton in rat pancreatic acini. J. Biol. Chem. 273: 24173-24180, 1998.
35. Stokoe, D., K. Engel, D. G. Campbell, P. Cohen, and M. Gaestel. Identification of MAPKAP kinase 2 as a major enzyme responsible for the phosphorylation of the small heat shock proteins. FEBS Lett. 313: 307-313, 1992.
36. Taniguchi, T., K. Takaishi, T. Murayam, M. Ito, N. Iwata, K. Chihara, T. Sasaki, Y. Takai, and T. Matsui. Cholecystokinin-B/gastrin receptors mediate rapid formation of actin stress fibers. Oncogens 12: 1357-1360, 1996.
37. Yule, D. I., M.-J. Tseng, J. A. Williams, and C. D. Logsdon. A cloned CCK-A receptor transduces multiple signals in response to full and partial agonists. Am. J. Physiol. 265 (Gastrointest. Liver Physiol. 28): G999-G1004, 1993.