Kinase activity, heat shock protein 27 phosphorylation, and lung epithelial cell glutathione

Experimental Lung Research

Volumn 34, Issue 5, 2008, Pages 245-262

  Jackson, Robert M ^a,b   Garcia Rojas, Rolando ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Glutathione; Heat shock protein; Hypoxia; Kinases; Reactive oxygen species

Indexed keywords

2,3 DIMETHOXY 1,4 NAPHTHOQUINONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; GLUTATHIONE; GLUTATHIONE DISULFIDE; HEAT SHOCK PROTEIN 27; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38;

ANTIOXIDANT ACTIVITY; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INCUBATION TIME; LUNG ALVEOLUS CELL; LUNG ALVEOLUS EPITHELIUM; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; STATISTICAL SIGNIFICANCE; WILD TYPE;

ADENOCARCINOMA, PAPILLARY; CELL LINE, TUMOR; ENZYME INHIBITORS; EPITHELIAL CELLS; GLUTATHIONE; GLUTATHIONE DISULFIDE; HUMANS; IMIDAZOLES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUNG NEOPLASMS; NAPHTHOQUINONES; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PYRIDINES; RESPIRATORY MUCOSA; TRANSFECTION;

EID: 45849137517     PISSN: 01902148     EISSN: 15210499     Source Type: Journal    
DOI: 10.1080/01902140802022500     Document Type: Article

References (40)

1. Li C, Jackson R: Cellular and molecular mechanisms of reoxygenation injury. Am J Physiol (Cell Physiol). 2002;282:C227-C241.
2. Dickinson D, Forman H: Glutathione in defense and signaling: lessons from a small thiol. Ann NY Acad Sci. 2002;973:488-504.
3. Forman H, Torres M, and Fukuto J: Redox signaling. Mol Cell Biochem. 2002;234/235:49-62.
4. Jackson R, Brannen A, Veal C, Fulmer J: Superoxide dismutase and cytochrome oxidase in collapsed lungs: possible role in re-expansion edema. J Appl Physiol. 1988;65:235-241.
5. Li C, Wright M, Jackson R: Reactive species mediated injury of human lung epithelial cells after hypoxia-reoxygenation. Exp Lung Res. 2002;38:373-389.
6. Gaitanaki C, Konstantina S, Chrysa S, Beis I: Oxidative stress stimulates multiple MAPK pathways and phosphorylation of the small Hsp27 in the perfused amphibian heart. J Exp Biol. 2003;206:2759-2769.
7. p38-dependent regulation of pro-inflammatory cytokine production. Biochem Pharmacol. 2002;63:305-320.
8. Whitmarsh A, Davis R: Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med. 1996;74:589-607.
9. Laderoute K, Webster K: Hypoxia/reoxygenation stimulated Jun kinase activity through redox signaling in cardiac myocytes. Circ Res. 1997;80:336-344.
10. Powell C, Wright M, Jackson R: Mitochondrial complex I and aconitase during hypoxiareoxygenation: Modulation of enzyme activities by mitochondrial MnSOD augmentation. Am J Physiol (Lung Cell Molec Physiol). 2003;285:L189-L198.
11. MAPK and MEK1/2 inhibition contribute to cellular oxidant injury after hypoxia. Am J Physiol (Lung Cell Mol Physiol). 2004;286:L826-L833.
12. Raha S, McEachern G, Myint A, Robinson B: Superoxides from mitochondrial complex III: the role of manganese superoxide dismutase. Free Radic Biol Med. 2000;29:170-180.
13. 2 in cells and thereby their biological state. Free Radic Biol Med. 2006;41:1338-1350.
14. Dickinson D, Forman H: Cellular glutathione and thiols metabolism. Biochem Pharmacol. 2002;64:1019-1026.
15. Haddad J: Hypoxia and the regulation of mitogen-activated protein kinases: gene transcription and the assessment of potential pharmacologic therapeutic interventions. Int Rev Immunopharmacol. 2004;4:1249-1285.
16. Eaton P, Fuller W, Shattock M: S-thiolation of Hsp27 regulates its multimeric aggregate size independently of phosphorylation. J Biol Chem. 2002;277:21189-21196.
17. Thrane E, Refnes M, Thoresen G, Lag M, Schwarze P: Fluoride-induced apoptosis in epithelial lung cells involves activation of MAP kinases p38 and possibly JNK. Toxicol Sci. 2001;61:83-91.
18. Zhang X, Bedard E, Potter R, Zhong R, Alam J, Choi A, Lee P: Mitogen-activated protein kinases regulate HO-1 gene transcription after ischemia-reperfusion lung injury. Am J Physiol (Lung Cell Mol Physiol). 2002;283:L815-L829.
19. Zhang X, Shan P, J. Alam R, Davis R, Flavell R, Lee P: Carbon monoxide modulates fas/fas ligand, caspases, and bcl-2 family proteins via the p38 α mitogen-activated protein kinase pathway during ischemia-reperfusion lung injury. J Biol Chem. 2003;278:22061-22070.
20. Zhang X, Shan P, Otterbein L, Alam J, Flavell R, Davis R, Choi A, Lee, P: Carbon monoxide inhibition of apoptosis during ischemia-reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase pathway and involves caspase 3. J Biol Chem. 2003;278:1248-1258.
21. Moellering D, McAndrew J, Jo H, Darley-Usmar V: Effects of pyrolidine dithiocarbamate on endothelial cells: protection against oxidative stress. Free Radic Biol Med. 1999;26:1138-1145.
22. Hickey E, Brandon S, Potter R, Stein G, Stein J, Weber L: Sequence and organization of genes encoding the human 27 kDa heat shock protein. Nucleic Acids Res. 1986;14:4127-4145.
23. Mehlen P, Arrigo A: The serum-induced phosphorylation of mammalian Hsp27 correlates with changes in its intracellular localization and levels of oligomerization. Eur J Biochem. 1994;221:327-334.
24. Rogalla T, Ehrnsperger M, Preville X, Kotlyarov A, Lutsch G, Ducasse C, Paul C, Wieske M, Arrigo A, Buchner J, Gaestel M: Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor-/alpha by phosphorylation. J Biol Chem. 1999;274:18947-18956.
25. Kayyali U, Pennella C, Trujillo C, Villa O, Gaestel M, Hassoun P: Cytoskeletal changes in hypoxic pulmonary endothelial cells are dependent on MAPK-activated protein kinase MK2. J Biol Chem. 2002;277:42596-42602.
26. Gazdar A, Linnoi R, Kurita Y, Oie H, Mulshine J, Clark J, Whitsett J: Peripheral airway cell differentiation in human lung cancer cell lines. Cancer Res. 1990;50:5481-5487.
27. Mehlen P, Hickey E, Weber L, Arrigo A: 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. 1997;241:187-192.
28. Vander Heide R: Increased expression of Hsp27 protects canine myocytes from simulated ischemia-reperfusion injury. Am J Physiol (Heart Circ Physiol). 2002;282:H935-H941.
29. MAPK and phosphorylation of small heat shock protein 27. Am J Physiol (Heart Circ Physiol). 2006;291:H2680-H2691.
30. Hansen J, Go Y, Jones D: Nuclear and mitochondrial compartmentation of oxidative stress and redox signaling. Annu Rev Pharmacol Toxicol. 2006;46:215-234.
31. Preville X, Salvemini F, Giraud S, Chaufour S, Paul C, Steplen G, Ursini M, Arrigo P: Mammalian small stress proteins protect against oxidative stress through their ability to increase glucose 6-phosphate dehydrogenase activity and bymaintaining optimal cellular detoxifying machinery. Exp Cell Res. 1999;247:61-78.
32. Arrigo A, Virot S, Chaufour S, Firdaus W, Kretz-Remy C, Diaz-Latoud C: Hsp27 consolidates intracellular redox homeostasis by upholding glutathione in its reduced form and by decreasing intracellular iron levels. Antioxidants Redox Signal. 2005;7:414-424.
33. Hollander J, Martin J, Belke D, Scott B, Swanson E, Krishnamoorthy V, Dillman W: Overexpression of wild-type heat shock protein 27 and a nonphosphorylatable heat shock protein 27 mutant protects against ischemia-reperfusion injury in a transgenic mouse model. Circulation. 2004;110:3544-3552.
34. Borelli M, Bernock L, Landry J, Spitz D, Weber L, Hickey E, Freeman M, Corry P: Stress protection by a fluorescent Hsp27 chimera that is independent of nuclear translocation or multimeric dissociation. Cell Stress Chaperones. 2002;7:281-296.
35. Mehlen P, Kretz-Remy C, Preville X, Arrigo A: Human Hsp27, Drosophila hsp27 and human alpha-B-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNF-α induced cell death. EMBO J. 1996;15:2695-2706.
36. Mehlen P, Kretz-Remy C, Briolay J, Fostan P, Mirault M, Arrigo A: Intracellular reactive oxygen species as apparent modulators of heat-shock protein 27 (Hsp27) structural organization and phosphorylation in basal and tumour necrosis factor α-treated T47D human carcinoma cells. Biochem J. 1995;312:367-375.
37. Paul C, Arrigo A: Comparison of protective activities generated by two survival proteins: Bcl-2 and Hsp27 in L929 murine fibroblasts exposed to menadione or staurosporine. Exp Gerontol. 2000;35:757-766.
38. Salinthone S, Ba M, Hanson L, Martin J, Halayko A, Gerthoffer W: Overexpression of human Hsp27 inhibits serum-induced proliferation in airway smooth muscle myocytes and confers resistance to hydrogen peroxide cytotoxicity. Am J Physiol Lung Mol Cell Physiol. 2007;293:L1194-L1207.
39. Ito H, Okamoto K, Kato K: Enhancement of expression of stress proteins by agents that lower the levels of glutathione in cells. Biochim Biophys Acta. 1998;1397:223-230.
40. Bruey J, Ducasse C, Bonniaud P, Ravagnan L, Susin S, Diaz-Latoud C, Gurbuxani S, Arrigo A, Kroemer G, Solary E, Garrido C: Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat Cell Biol. 2000;2:645-652.