Analysis of the role of Hsp25 phosphorylation reveals the importance of the oligomerization state of this small heat shock protein in its protective function against TNFα- and hydrogen peroxide-induced cell death

Journal of Cellular Biochemistry

Volumn 69, Issue 4, 1998, Pages 436-452

  Préville, Xavier ^a   Schultz, Heidi ^b   Knauf, Ursula ^b   Gaestel, Matthias ^b   Arrigo, André Patrick ^a  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Phosphorylation mutant; SB203580; Small heat shock proteins; TNF

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ALANINE; GLUTATHIONE; HEAT SHOCK PROTEIN; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE INHIBITOR; REACTIVE OXYGEN METABOLITE; SERINE; TUMOR NECROSIS FACTOR ALPHA;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL DEATH; CELL PROTECTION; CELL STRAIN L 929; CONTROLLED STUDY; CYTOTOXICITY; MOUSE; NONHUMAN; OLIGOMERIZATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL DEATH; DACTINOMYCIN; ENZYME INHIBITORS; GLUTATHIONE; HEAT-SHOCK PROTEINS; HYDROGEN PEROXIDE; IMIDAZOLES; L CELLS (CELL LINE); MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR WEIGHT; NEOPLASM PROTEINS; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN-SERINE-THREONINE KINASES; PYRIDINES; REACTIVE OXYGEN SPECIES; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA; MURINAE;

EID: 0039171658     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4644(19980615)69:4<436::AID-JCB5>3.0.CO;2-O     Document Type: Article

References (70)

1. Arrigo A-P (1980): Investigation of the function of the heat shock proteins in Drosophila melanogaster tissue culture cells. Mol Gen Genet 178:517-524.
2. Arrigo A-P (1987): Cellular localization of HSP23 during Drosophila development and following subsequent heat shock. Dev Biol 122:39-48.
3. Arrigo A-P (1990): Tumor necrosis factor induces the rapid phosphorylation of the mammalian heat shock protein hsp28. Mol Cell Biol 10:1276-1280.
4. Arrigo AP (1998): Small stress proteins: chaperones that act as regulators of intracellular redox state and programmed cell death. Biol Chem 379:19-26.
5. Arrigo A-P, Ahmad-Zadeh C (1981): Immunofluorescence localization of a small heat shock protein (hsp 23) in salivary gland cells of Drosophila melanogaster. Mol Gen Genet 184:73-79.
6. Arrigo A, Welch W (1987): Characterization and purification of the small 28,000-dalton mammalian heat shock protein. J Biol Chem 262:15359-5369.
7. Arrigo A-P, Suhan JP, Welch WJ (1988): Dynamic changes in the structure and intracellular locale of the mammalian low-molecular-weight heat shock protein. Mol Cell Biol 8:5059-5071.
8. Bass D, Parce J, Dechatelet L, Szejda P, Seeds M, Thomas M (1983): Flow cytometric studies of oxidative product formation by neutrophils: A graded response to membrane stimulation. J Immunol 130:1910-1917.
9. Benndorf R, Hayess K, Ryazantsev S, Wieske M, Behlke J, Lutsch G (1994): Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J Biol Chem 269:20780-20784.
10. Beyaert R, Cuenda A, Vanden Berghe W, Plaisance S, Lee J, Haegeman G, Cohen P, Fiers W (1996): The p38/RK mitogen-activated protein kinase pathway regulates interleukin-6 synthesis response to tumor necrosis factor. EMBO J 15:1914-1923.
11. Burow S, Valet G (1987): Flow-cytometric characterization of stimulation, free radical formation, peroxidase activity and phagocytosis of human granulocytes with 2,7-dichlorofluorescein (DCF). Eur J Cell Biol 43:128-133.
12. Buttke TM, Sandstrom PA (1994): Oxidative stress as a mediator of apoptosis. Immunol Today 15:7-10.
13. Crête P, Landry J (1990): Induction of HSP27 phosphorylation and thermoresistance in Chinese hamster cells by arsenite, cycloheximide, A23187 and EGTA. Radiat Res 121:320-327.
14. Cuenda A, Rouse J, Doza Y, Meier R, Cohen P, Gallagher T, Young P, Lee J (1995): SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett 364:229-233.
15. Denizot F, Lang R (1986): Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods 89:271-277.
16. Ehrnsperger M, Graber S, Gaestel M, 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.
17. Freshney NW, Rawlinson L, Guesdon F, Jones E, Cowley S, Hsuan J, Saklatvala J (1994): Interleukin-1 activates a novel protein kinase cascade that results in the phosphorylation of Hsp27. Cell 78:1039-1049.
18. Gaestel M, Gross B, Benndorf R, Strauss M, Schunk W-H, Kraft R, Otto A, Bohm H, Stahl J, Drabsch H, Bielka H (1989): Molecular cloning, sequencing and expression in Escherichia coli of the 25-kDa growth-related protein of Ehrlich ascites tumor and its homology to mammalian stress proteins. Eur J Biochem 179:209-213.
19. Gaestel M, Schroder W, Benndorf R, Lippman C, Buchner K, Hucho F, Erdmann VA, Bielka H (1991): Identification of the phosphorylation sites of the murine small heat shock protein hsp 25. J Biol Chem 266:14721-14724.
20. Gaestel M, Benndorf R, Hayess K, Priemer E, Engel K (1992): Dephosphorylation of the small heat shock protein hsp25 by calcium/calmodulin-dependent (type 2B) protein phosphatase. J Biol Chem 267:21607-21611.
21. Goossens V, Grooten J, De Vos K, Fiers W (1995): Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvment in cytotoxicity. Proc Natl Acad Sci USA 92:8115-8119.
22. Guy G, Cairns J, Ng S, Tan Y (1993): Inactivation of a redox-sensitive protein phosphatase during the early events of tumor necrosis factor/interleukin-1 signal transduction. J Biol Chem 268:2141-2148.
23. Horwitz J, Huang Q-L, Ding L-L (1992): Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89:10449-10453.
24. Huot J, Roy G, Lambert H, Chretien P, 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 51:5245-5252.
25. Huot J, Lambert H, Lavoie JN, Guimond A, Houle F, Landry J (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.
26. Huot J, Houle F, Spitz DR, Landry J (1996): HSP27 phosphorylation-mediated resistance against actin fragmentation and cell death induced by oxidative stress. Cancer Res 56:273-279.
27. Ingolia TD, Craig EA (1982): Four small heat shock proteins are related to each other and to mammalian α-crystallin. Proc Natl Acad Sci USA 79:2360-2364.
28. Jaattela M (1993): Overexpression of major heat shock protein hsp70 inhibits tumor necrosis factor-induced activation of phospholipase A2. J Immunol 151:4286-4294.
29. Jaattela M, Wissing D (1993): Heat-shock proteins protect cells from monocyte cytotoxicity: Possible mechanism of self-protection. J Exp Med 177:231-236.
30. Jaattela M, Wissing D, Bauer P, Li G (1992): Major heat shock protein hsp70 protects tumor cells from tumor necrosis factor cytotoxicity. EMBO J 11:3507-3512.
31. Jakob U, Gaestel M, Engels K, Buchner J (1993): Small heat shock proteins are molecular chaperones. J Biol Chem 268:1517-1520.
32. Kane D, Sarafian T, Anton R, Hahn H, Gralla E, Valentine J, Ord T, Bredesen D.(1993): Bcl-2 inhibition of neural death: Decreased generation of reactive oxygen species. Science 262:1274-1277.
33. Kato K, Hasegawa K, Goto S, Inaguma Y (1994): Dissociation as a result of phosphorylation of an aggregated form of the small stress protein, hsp27. J Biol Chem 269:11274-11278.
34. Katz D, Reginato M, Lazar M (1995): Functional regulation of thyroid hormone receptor variant TR alpha 2 by phosphorylation. Mol Cell Biol 15:2341-2348.
35. Kaur P, Saklatvala J (1988): Interleukin 1 and tumour necrosis factor increase phosphorylation of fibroblast proteins. FEBS Lett 241:6-10.
36. Kim Y-J, Shuman J, Sette M, Przybyla A (1984): Nuclear localization and phosphorylation of three 25-kilodalton rat stress proteins. Mol Cell Biol 4:468-474.
37. Knauf U, Bielka H, Gaestel M (1992): Over-expression of the small heat-shock protein, hsp25, inhibits growth of Ehrlich ascites tumor cells. FEBS Lett 3:297-302.
38. Knauf U, Jakob U, Engel K, Buchner J, 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.
39. Landry J, Lambert H, Zhou M, Lavoie JN, Hickey E, Weber LA, Anderson CW (1992): Human HSP 27 is phosphorylated at serines 78 and 82 by heat shock and mitogen-activated kinases that recognize the same amino acid moif as S6 kinase II. J Biol Chem 267:794-803.
40. Lavoie JN, Gingras-Breton G, Tanguay RM, Landry J (1993a): Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock. J Biol Chem 268:3420-3429.
41. Lavoie JN, Hickey E, Weber LA, Landry J (1993b): Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of Heat Shock Protein 27. J Biol Chem 268:24210-24214.
42. Lavoie JN, Lambert H, Hickey E, Weber LA, 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.
43. Lee GJ, Roseman AM, Saibil HR, Vierling E (1997): A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J 16:659-671.
44. Lee J, Laydon J, McDonnell P, Gallagher T, Kumar S, Green D, McNulty D, Blumenthal M, Keys J, Landvatter S (1994): A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372:739-746.
45. Lim K, Chae C (1989): A simple assay for DNA transfection by incubation of the cells in culture dishes with substrates for beta-galactosidase. Biotechniques 7:576-579.
46. Ludwig S, Engel K, Hoffmeyer A, Sithanandam G, Neufeld B, Palm D, Gaestel M, Rapp UR (1996): 3pK, a novel MAP kinase activated protein kinase is targeted by three MAP kinase pathways. Mol Cell Biol 16:6687-6697.
47. Matsuda M, Masutani H, Nakamura H, Miyajima S, Yamauchi A, Yonehara S, Uchida A, Irimajiri K, Horiuchi A, Yodoi J (1991): Protective activity of adult T cell leukemia-derived factor (ADF) against tumor necrosis factor-dependant cytotoxicity on U937 cells. J Immunol 147: 3837-3841.
48. Mayer M, Noble M (1994): N-Acetyl-L-cysteine is a pluripotent protector against cell death and enhancer of trophic factor-mediated cell survival in vitro. Proc Natl Acad Sci USA 91:7496-7500.
49. Mehlen P, Arrigo A (1994): The serum-induced phosphorylation of mammalian hsp27 correlates with changes in its intracellular localization and levels of oligomerization. Eur J Biochem 221:327-34.
50. Mehlen P, Briolay J, Smith L, Diaz-Latoud C, Pauli D, Arrigo A-P (1993): Analysis of the resistance to heat and hydrogen peroxide stresses in COS cells transiently expressing wid type or deletion mutants of the Drosophila 27-kDa heat-shock protein. Eur J Biochem 215:277-284.
51. Mehlen P, Kretz-Remy C, Briolay J, Fostan P, Mirault ME, Arrigo AP (1995a): Intracellular reactive oxygen species as apparent modulators of heat-shock protein 27 (hsp27) structural organization and phosphorylation in basal and tumour necrosis factor alpha-treated T47D human carcinoma cells. Biochem J 312:367-375.
52. Mehlen P, Mehlen A, Guillet D, Préville X, Arrigo A-P (1995b): 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.
53. Mehlen P, Préville X, Chareyron P, Briolay J, Klemenz R, Arrigo A-P (1995c): Constitutive expression of human hsp27, Drosophila hsp27, or human alpha B-crystallin confers resistance to TNF-and oxidative stress-induced cytotoxicity in stably transfected murine L929 fibroblasts. J Immunol 154:363-374.
54. Mehlen P, Préville X, Kretz-Remy C, Arrigo A-P (1996): Human hsp27, Drosophila hsp27 and human αB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these protein against TNFα-induced cell death. EMBO J 15:2695-2706.
55. Mehlen P, Hickey E, Weber LA, Arrigo A-P (1997): Large unphosphorylated aggregates as the active germ 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.
56. Mendelsohn ME, Zhu Y, O'Neill S (1991): The 29 kDa proteins phosphorylated in thrombin activated human platelets are forms of the estrogen receptor-related 27-kDa heat shock protein. Proc Natl Acad Sci USA 88:11212-11216.
57. Miron T, Vancompernolle K, Vandekerckhove J, Wilchek M, Geiger B (1991): A 25-kD inhibitor of actin polymerization is a low molecular mass heat shock protein. J Cell Biol 114:255-261.
58. Oesterreich S, Weng C-N, Qiu M, Hilsenbeck SG, Osborne CK, Fuqua SAW (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.
59. Rollet E, Best-Belpomme M (1986): HSP 26 and 27 are phosphorylated in response to heat shock and ecdysterone in Drosophila melanogaster cells. Biochem Biophys Res Commun 141:426-433.
60. Rouse J, Cohen P, Trigon S, Morange M, Alonsollamazares A, Zamanillo D, Hunt T, Nebreda AR (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.
61. Schulze-Osthoff K, Bakker AC, Vandevoorde V, Baeyaert R, Haegeman G, Fiers W (1992): Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation. J Biol Chem 267:5317-5323.
62. Schulze-Osthoff K, Baeyaert R, Vandevoorde V, Haegerman G, Fiers W (1993): Depletion of the mitochondrial electron transport abrogates the cytotoxic and gene-inducible effects of TNF. EMBO J 12:3095-3104.
63. Spector A, Li LK, Augusteyn RC, Schneider A, Freund T.(1971): α-cristallin: The isolation and characterization of distinct macromolecular fractions. Biochem J 124:337-343.
64. Spector NL, Mehlen P, Ryan C, Hardy L, Samson W, Levine H, Nadler LM, Fabre N, 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.
65. Stokoe D, Engel K, Campbell D, Cohen P, Gaestel M (1992): Identification of MAPKAP kinase 2 as a major enzyme responsible for the phosphorylation of the small mammalian heat shock proteins. FEBS Lett 313:307-313.
66. Welch WJ (1985): Phorbol ester, calcium ionophore, or serum added to quiescent rat embryo fibroblasts cells all result in the elevated phosphorylation of two 28,000-Dalton mammalian stress proteins. J Biol Chem 260: 3058-3062.
67. Wigler M, Pellicer A, Silverstein S, Axel R, Urlaub G, Chasin L (1979): DNA-mediated transfer of the adenine phosphoribosyl transferase locus into mammalian cells. Proc Natl Acad Sci USA 76:1373-1376.
68. Wong GHW, Elwell JE, Oberby LW, Goeddel D (1989): Manganous superoxide dismutase is essential for cellular resistance to tumor necrosis factor. Cell 58:923-931.
69. Yamauchi N, Kuriyama YH, Watanabe N, Neda H, Maeda M, Himeno T, Tsuji Y (1990): Suppressive effects of intracellular glutathione on hydroxyl radical production induced by tumor necrosis factor. Int J Cancer 46:884-888.
70. Zhou M, Lambert H, Landry J (1993): Transient activation of a distinct serine protein kinase is responsible for 27-kDa heat shock protein phosphorylation in mitogen-stimulated and heat-shocked cells. J Biol Chem 268:35-43.