Expression of HSP27 results in increased sensitivity to tumor necrosis factor, etoposide, and H2O2 in an oxidative stress-resistant cell line

Journal of Cellular Physiology

Volumn 177, Issue 4, 1998, Pages 606-617

  Mairesse, N ^a   Bernaert, D ^a   Del Bino, G ^a   Horman, S ^a   Mosselmans, R ^a   Robaye, B ^a   Galand, P ^a  

^a FREE UNIVERSITY OF BRUSSELS   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ETOPOSIDE; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ARTICLE; CELL GROWTH; CELL PROTECTION; CELL SPREADING; CYTOSKELETON; CYTOTOXICITY; GENETIC TRANSFECTION; MOUSE; NONHUMAN; OSTEOBLAST; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TARGET CELL;

ACTINS; ANIMALS; CELL DIVISION; CYTOSKELETON; DRUG RESISTANCE; ETOPOSIDE; FIBROSARCOMA; HEAT; HEAT-SHOCK PROTEINS; HUMANS; HYDROGEN PEROXIDE; MICE; NEOPLASM PROTEINS; NUCLEIC ACID SYNTHESIS INHIBITORS; OSTEOBLASTS; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT FUSION PROTEINS; TRANSFECTION; TUMOR CELLS, CULTURED; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0031795906     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199812)177:4<606::AID-JCP11>3.0.CO;2-Z     Document Type: Article

References (77)

1. Arata, S., Hamaguchi, S., and Nose, K. (1995) Effects of the overexpression of the small heat shock protein HSP27 on the sensitivity of human fibroblast cells exposed to oxidative stress. J. Cell. Physiol., 163:458-465.
2. Arrigo, A. P. (1990) Tumor necrosis factor induces the rapid phosphorylation of the mammalian heat shock protein HSP28. Mol. Cell. Biol., 10:1276-1280.
3. Arrigo, A. P., and Landry, J. (1994) Expression and function of the low-molecular weight heat shock proteins. In: The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Springs Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 335-383.
4. Arrigo, A. P., Mehlen, P., Preville, X., Chaufour, S., Kretz-Remy, C., Gonin, S., and Diaz-Lataud, C. (1997) Les petites protéines de stress: des nouveaux modulateurs de la mort cellulaire. Med. Sci., 13:740-741.
5. Benndorf, K., Hayeb, K., Ryazantser, S., Wicsk, M., Behlke, J., and Lutsch, G. (1994) Phosphorylation and supramolecular organisation in murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J. Biol. Chem., 269:20780-20784.
6. Beyaert, R., and Fiers, W. (1994) Molecular mechanisms of tumor necrosis factor-induced cytotoxicity. FEBS Lett., 340:9-16.
7. Blackburn, P., Galoforo, S., Berns, C. M., Ireland, M., Cho, J. M., Corry, P. N., and Lee, Y. (1996) Thermal response in murine L929 cells lacking αβ-crystallin expression and αβ-crystallin expressing L929 transfectants. Mol. Cell. Biochem., 155:51-60.
8. Bonelli, G., Sacchi, M. C., Barbiero, G., Duranti, F., Goblio, G., Verdun di Cantogno, L., Amenta, J. S., Piacentini, M., Tacehetti, C., and Baccino, F. M. (1996) Apoptosis of L929 cells by eposide: A quantitative and kinetic approach. Exp. Cell Res., 228:292-305.
9. Buttke, M., and Sandstrom, P. A. (1994) Oxidative stress as a mediator of apoptosis. Immunol. Today, 15:7-10.
10. Carper, S. W., Rocheleau, T. A., and Storm, F. K. (1990) cDNA sequence of a human heat shock protein HSP27. Nucleic Acid Res., 18:6457.
11. Chen, Q., Kinch, M. S., Lin, Th., Burridge, K., and Juliano, R. L. (1994) Integrin-mediated cell adhesion activates mitogen-activated protein kinases. J. Biol. Chem., 26:602-626.
12. Ciocca, D. R., Fuqua, S. A. W., Lock-Lin, S., Toft, D. O., and Welch, W. J. (1992) Response of human breast cancer cells to heat shock and chemotherapeutic drugs. Cancer Res., 52:3648-3654.
13. Ciocca, D. R., Oesterreich, S., Chamnes, G. C., McGuire, W. L., and Fuqua, S. A. W. (1993) Biological and clinical implications of heat shock protein 27,000 (hsp27): A review. J. Natl. Cancer Inst., 85: 1558-1570.
14. Dartsch, P. C., Rotter, M., Häussinger, D., and Lang, F. (1994) Cytoskeletal reorganization in NIH3T3 fibroblasts expressing the ras oncogene. Eur. J. Cell. Biol., 63:316-325.
15. Darzynkiewicz, Z., Bruno, S., Del Bino, G., Gorczyca, W., Hotz, M. A., Lassota, P., and Tragonos, F. (1992) Features of apoptotic cells measured by flow cytometry. Cytometry, 13:795-808.
16. Earle, W. R., Schilling, E. L., Stark, T. H., Straus, N. P., Brown, M. F., and Shelton, E. (1943) Production of malignancy in vitro. The mouse fibroblast cultures and changes seen in the living cells. J. Natl. Cancer Inst., 4:165-212.
17. Ehrnsperger, M., Gräber, S., Gaestel, M., and Buchner, J. (1997) Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J., 16: 221-229.
18. Engel, K., Ahlers, A., Brach, A., Herrmann, F., and Gaestel, M. (1995) MAPKAP kinase 2 is activated by heat shock and TNF-α: In vivo phosphorylation of small heat shock protein results from stimulation of the MAP kinase cascade. J. Cell. Biochem., 57:321-330.
19. Gernhold, M., Knauf, U., Gaestel, M., Stahl, J., and Loetzel, P. M. (1993) Development and tissue-specific distribution of mouse small heat shock protein hsp25. Dev. Genet., 14:103-111.
20. Goossens, V., Grooten, J., De Vos, K., and Fiers, W. (1995) Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc. Natl. Acad. Sci. USA, 92:8115-8119.
21. Guay, J., Lambert, M., Gingras-Breton, G., Lavoie, J., Huot, J., and Landry, J. (1997) Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J. Cell Sci., 110:357-368.
22. Hepburn, A., Demolle, D., Boeynaems, J. M., Fiers, W., and Dumont, J. E. (1988) Rapid phosphorylation of a 27 kDa protein induced by tumor necrosis factor. FEBS Lett., 227:175-178.
23. Huot, J., Roy, G., Lambert, H., Chretien, P., and Landry, J. (1991) Increased survival after treatments with anticancer agents of Chinese hamster cells expressing the human Mr 27,000 heat shock protein. Cancer Res., 51:245-252.
24. Huot, J., Houle, F., Spitz, D. R., and Landry, J. (1996) HSP27 phosphorylation-mediated resistance against actin fragmentation and cell death induced by Oxidative stress. Cancer Res., 56:273-279.
25. Kindas-Mügge, I., and Trautinger, F. (1994) Increased expression of the M(r) 27000 heat shock protein (HSP27) in in vitro differentiated human keratinocytes. Cell Growth Differ., 5:777-781.
26. Kindas-Mügge, I., Herbace, I., Jantschitsch, C., Micksche, M., and Trautinger, F. (1996) Modification of growth and tumorigenicity of epidermal cell lines by DNA-mediated gene transfer of Mr 27,000 heat shock protein (hsp27). Cell Growth Differ., 7:1167-1174.
27. Knauf, U., Bielka, H., and Gaestel, M. (1992) Over-expression of the small heat-shock protein, hsp25, inhibits growth of Ehrlich ascites tumor cells. FEBS Lett., 309:297-302.
28. Knauf, U., Jakob, U., Engel, K., Buchner, J., and Gaestel, M. (1994) 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.
29. Knight, J. B., Yamouchi, R. Y., and Pessin, J. E. (1995) Divergent factor regulation of focal adhesion kinase (pp 125 FAK) tyrosine phosphorylation and rearrangement of actin stress fibers. J. Biol. Chem., 270:10199-10203.
30. Koopman, G., Reutelingsperger, C. A. M., Kuijten, G. A. M., Keenen, R. J. M., Pals, S. T., and Van Oers, M. H. J. (1994) Annexin V for flow cytometric detection of phosphatidylserine expression of B cells undergoing apoptosis. Blood, 84:1415-1420.
31. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227:680-685.
32. Landry, J., and Huot, J. (1995) 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., 79:703-707.
33. Landry, J., Chretien, P., Lambert, H., Hicky, E., and Weber, L. A. (1989) Heat shock resistance conferred by expression of the human HSP27 gene in rodent cells. J. Cell Biol., 109:7-15.
34. Lavoie, J. N., Hickey, E., Weber, L. A., and Landry, J. (1993a) Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27. J. Biol. Chem 268: 24210-24214.
35. Lavoie, J. N., Gringas-Breton, G., Tanguay, R. M., and Landry J. (1993b) Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock. J. Biol. Chem., 268: 3420-3429.
36. Lavoie, J. N., Lambert, N., Hickey, E., Weber, L. A., and Landry, J. (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.
37. Lee, Y. J., Zheng Hou, Z., Curetty, L., and Borrelli, M. J. (1992) Development of acute thermotolerance in L929 cells: Lack of hsp28 synthesis and phosphorylation. J. Cell. Physiol., 152:118-125.
38. Mairesse, N., Horman, S., Mosselmans, R., and Galand, P. (1996) Antisense inhibition of the 27 kDa heat shock protein production affects growth rate and cytoskeletal organization in MCF-7 cells. Cell Biol. Int., 20:205-212.
39. Matsumara, F., Lin, J. J.-C., Yamashiro-Matsumara, S., Thomas, G. P., and Topp, W. C. (1983) Differential expression of tropomyosin forms in the microfilaments isolated from normal and transformed rat culture cells. J. Cell. Chem., 104:1085-1089.
40. Mehlen, P., and Arrigo, A. P. (1994) The serum-induced phosphorylation of mammalian HSP27 correlates with changes in its intracellular localization and levels of oligomerization. Eur. J. Biochem., 221:334-337.
41. Mehlen, P., Mehlen, A., Guillet, D., Preville, X., and Arrigo, A. P. (1995a) Tumor necrosis factor-α induces changes in the phosphorylation, cellular localization, and oligomerization of human hsp27, a stress protein that confers cellular resistance to this cytokine. J. Cell. Biochem., 58:248-259.
42. Mehlen, P., Preville, X., Chareyon, P., Briolay, J., Klemenz, R., and Arrigo, A. P. (1995b) Constitutive expression of human hsp27, Drosophila hsp27, or human αβ-crystallin confers resistance to TNF-and oxidative stress-induced cytotoxicity in stably transfected murine L929 fibroblasts. J. Immunol., 154:363-374.
43. Mehlen, P., Kretz-Remy Preville, X., and Arrigo, A. P. (1996a) Human hsp27, Drosophila hsp27 and human αβ-crystallin expression-medialed increase in glutathione is essential for the protective activity of these proteins against TNFα-induced cell death. EMBO J., 11: 2695-2706.
44. Mehlen, P., Schulze-Osthoff, K., and Arrigo, A. P. (1996b) Small stress proteins as novel regulators of apoptosis. J. Biol. Chem., 271:16510-16514.
45. Mehlen, P., Hickey, E., Weber, L. A., and Arrigo, A. P. (1997) Large unphosphorylated aggregates as the active form of hsp27 which controls intracellular reactive oxygen species and glutathione levels and generates a protection against TNF-α in NIH-3T3-ras cells. Biochem. Biophys. Res. Commun., 241:187-192.
46. Miron, T., Vancampernolle, K., Vanderkerckhove, J., Wilchek, M., and Geiger, B. (1991) A 25 kD inhibitor of actin polymerization is a low molecular weight heat shock protein. J. Cell. Biol., 114:255-261.
47. Mooney, D. J., Langer, R., and Ingber, D. E. (1995) Cytoskeletal filament assembly and the control of cell spreading and function by extracellular matrix. J. Cell Sci., 108:2311-2320.
48. Nadler, L., Fabre, N., and Arrigo, A. P. (1994) Regulation of the 28 kDa heat shock protein by retinoic acid during differentiation of human leukemic HL-60 cells. FEBS Lett., 337:184-188.
49. Oesterreich, S., Benndorf, R., and Bielka, H. (1990) The expression of the growth-related 25 kDA protein (p25) of Ehrlich ascites tumor cells is increased by hyperthermic treatment (heat shock). Biomed. Biochim. Acta, 49:219-226.
50. Oesterreich, S., Schunk, H., Benndorf, R., and Bielka, H. (1991) Cisplatin induces the small heat shock protein hsp25 and thermotolerance in Ehrlich ascites tumor cells. Biochem. Biophys. Res. Commun., 180:243-248.
51. Osterreich, S., Weng, C. N., Qiu, M., Hilsenbeck, S. G., Osborne, C. K., and Fuqua, S. A. N. (1993) The small heat shock protein hsp27 is correlated with growth and drug resistance in human breast cancer cell lines. Cancer Res., 53:4443-4448.
52. O'Farrell P.Z. (1975) pH high resolution two-dimensional electrophoresis of proteins. J. Biol. Chem., 250:4007-4021.
53. Pauli, D., Tonka, C., Tissieres, A., and Arrigo, A. P. (1990) Tissue-specific expression of the heat shock protein HSP27 during Drosophila melanogaster development. J. Cell Biol., 111:817-828.
54. Regazzi, R., Eppenberger, U., and Fabbro, D. (1988) The 27,000 daltons stress proteins are phosphorylated by protein kinase C during the tumor promoter-mediated growth inhibition of human mammary carcinoma cells. Biochem. Biophys. Res. Commun., 152:62-68.
55. Richards, E. H., Mickey, E., Weber, L., and Masters, J. R. W. (1996) Effect of overexpression of the small heat shock protein HSP27 on the heat and drug sensitivities of human testis tumor cells. Cancer Res., 56:2446-2451.
56. Robaye, B., Hepburn, A., Lecocq, R., Fiers, W., Boeynaems, J. M., and Dumont, J. E. (1989) Tumor necrosis factor-α induces the phosphorylation of 28 kDa stress proteins in endothelial cells: Possible role in protection against cytotoxicity? Biochem. Biophys. Res. Commun., 163:301-308.
57. Robaye, B., Mosselmans, R., Fiers, W., Dumont, J. E., and Galand, P. (1991) Tumor necrosis factor induces apoptosis (programmed cell death) in normal endothelial cells in vitro. Am. J. Pathol., 138:447-453.
58. Roger, P. P., Rickaert, F., Lamy, F., Authelet, M., and Dumont, J. E. (1989) Actin stress fibers disruption and tropomyosia isoform switching in normal thyroid cells stimulated by thyrotropin and phorbol esters. Exp. Cell Res., 182:1-13.
59. Rollet, E., Lavoie, J. N., Landry, J., and Tanguay, R. M. (1992) Expression of Drosophila's 27 kDa heat shock protein into rodent cells confers thermal resistance. Biochem. Biophys. Res. Commun., 185:116-120.
60. Rondeaux, P., Horman, S., Galand, P., and Mairesse, N. (1997) Effect of the transfection of the hsp27 gene in antisense orientation on cell growth and morphology in human osteosarcoma MG-63 cells. In Vitro Cell. Dev. Biol., 33:655-658.
61. Roskelley, C. D., Desprez, P. Y., and Bissel, M. J. (1994) Extracellular matrix-dependent tissue specific gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proc. Natl. Acad. Sci. USA, 91:12378-12382.
62. Rouse, J., Cohen, P., Trigon, S., Morange, M., Alonso-Llamazares, A., Zamarillo, D., Hunt, T., and Nebrada, A. R. (1994) A novel kinase triggered by stress and heat shock that stimulates MAPKAP kinase 2 and phosphorylation of the small heat shock proteins. Cell, 78: 1027-1037.
63. Ryan, M. P., and Higgins, J. (1988) Cytoarchitecture of kirsten sarcoma virus-transformed rat kidney fibroblasts: Butyrate-induced reorganization within the actin microfilament network. J. Cell. Physiol., 137:25-34.
64. Ryan, M. P., and Higgins, P. J. (1994) Control of p52 (PAI-1) gene pression in normal and transformed rat kidney cells: Relationships between p52 (PA-I) induction and actin cytoarchitecture. In: Actin: Biophysics, Biochemistry and Cell Biology. J. E. Estes and P. J. Higgins, eds., Plenum Press, New York, 215-230.
65. Saklatvala, J., Kaur, P., and Guesdon, F. (1991) Phosphorylation of the small heat shock protein is regulted by interleukin-1, tumor necrosis factor, growth factors, bradykinin and ATP. Biochem. J., 277:635-642.
66. Scanlon, M., Laster, S. M., Wood, J. G., and Gooding, L. R. (1989) Cytolysis by tumor necrosis factor is preceded by a rapid and specific dissolution of microfilaments. Proc. Natl. Acad. Sci. USA, 86: 182-186.
67. Shakoori, A. R., Oberdorf, A. M., Owen, T. A., Weber, L. A., Hickey, E., Stein, J. L., Lian, J. B., and Stein, G. S. (1992) Expression of heat shock genes during differentiation of mammalian osteoblasts and promyeolocytic leukemia cells. J. Cell. Biochem., 48:277-287.
68. Souren, J. E. M., Van Aken, H., and Van Wijr, R. (1996) Enhancement of Superoxide production and protection against heat shock by HSP27 in fibroblasts. Biochem. Biophys. Res. Commun., 227:816-821.
69. Spector, N. L., Ryan, C., Samson, W., Levine, H., Nadler, L. M., and Arrigo, A. P. (1993) Heat shock protein is a unique marker of growth arrest during macrophage differentiation of HL-60 cells. J. Cell. Physiol., 156:619-625.
70. Spector, N. L., Mehlen, P., Ryan, C., Harsley, L., Samson, N., Levine, H., Marshall, M., Nadler, L., Fahre, N., and Arrigo, A. P. (1994) Regulation of the 28 kDa heat shock protein by retiuoic acid during differentiation of human leukemic HL-60 cells. FEBS Lett., 337: 184-188.
71. Stoian, I., Oros, A., and Holdovean, E. (1996) Apoptosis and free radicals. Biochem. Mol. Med., 59:93-97.
72. Towbin, H., Staehelin, T., and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. USA, 76:4350-4354.
73. Wahrman, M. Z., Gagnier, S. E., Kobrin, D. R., Higgins, P. J., and Avgenlicht, L. H. (1985) Cellular and molecular changes in 3T3 cells transformed spontaneously or by DNA transfection. Tumor Biol., 6:41-47.
74. Wang, G., Kolstergard, J., Khodadadian, M., Wu, J., Wu, T., Fung, K. P., Carper, S. W., and Tomasovic, S. P. (1996) Murine cells transfected with human HSP27 cDNA resist TNF-induced cytotoxicity. J. Immunother. Emphasis Tumor Immunol., 19:9-20.
75. Welch, W. J. (1985) Phorbol ester, calcium ionophore or serum added quiescent rat embryo fibroblast cells: All result in the elevated phosphorylation of two 28,000 dalton mammalian stress proteins. J. Biol. Chem., 260:3058-3062.
76. Yamashiro, S., Yoshida, K., Yamakita, Y., and Matsumura, F. (1994) Caldermon: Possible functions in microfilaments reorganization during mitosis and cell transformation. In: Actin: Biophysics, Biochemistry and Cell Biology. J. E. Estes and P. J. Higgins, eds., Plenum Press, New York, pp. 113-122.
77. Young, P. R. (1989) Enhancement of immunoblot staining using a mixed chromogenic substrate. Immunol. Methods, 121:295-296.