Haem oxygenase 1 gene induction by glucose deprivation is mediated by reactive oxygen species via the mitochondrial electron-transport chain

Biochemical Journal

Volumn 371, Issue 3, 2003, Pages 877-885

  Chang, Se Ho ^a,d   Garcia, Jairo ^a   Melendez, J Andres ^b   Kilberg, Michael S ^c   Agarwal, Anupam ^a,c  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b ALBANY MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d Gyeongsang National University School of Medicine   (South Korea)

Author keywords

Antioxidant; Hydrogen peroxide; Mitochondrial respiration; Oxidant stress

Indexed keywords

ANTIOXIDANTS; CARBON MONOXIDE; ELECTRONS; GLUCOSE; OXYGEN; RNA;

REACTIVE OXYGEN SPECIES (ROS);

GENES;

ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; ANTIMYCIN A1; ANTIOXIDANT; BILIVERDIN; CARBON MONOXIDE; CATALASE; CYCLIC AMP DEPENDENT PROTEIN KINASE; DEFEROXAMINE; DEOXYGLUCOSE; ENZYME INHIBITOR; GLUCOSAMINE; GLUCOSE; HEME OXYGENASE 1; HYDROGEN PEROXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IRON; IRON CHELATING AGENT; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MYXOTHIAZOL; OLIGOMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE A2; PROSTAGLANDIN SYNTHASE; PROTEIN KINASE C; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; UBIQUINOL CYTOCHROME C REDUCTASE;

ARTICLE; CELL STRAIN HEPG2; ENZYME ACTIVATION; ENZYME INHIBITION; GENE INDUCTION; GENE OVEREXPRESSION; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; MITOCHONDRIAL RESPIRATION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN INDUCTION; RESPIRATORY CHAIN;

CATALASE; ELECTRON TRANSPORT; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE; HEME OXYGENASE (DECYCLIZING); HUMANS; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; PHOSPHOLIPASES A; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; REACTIVE OXYGEN SPECIES; RNA, MESSENGER;

EID: 0037907756     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021731     Document Type: Article

References (56)

1. Lee, A. S. (2001) The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem. Sci. 26, 504-510
2. Pahl, H. L. (1999) Signal transduction from the endoplasmic reticulum to the cell nucleus. Physiol. Rev. 79, 683-701
3. Chang, S. H., Barbosa-Tessmann, I., Chen, C., Kilberg, M. S. and Agarwal, A. (2002) Glucose deprivation induces heme oxygenase-1 gene expression by a pathway independent of the unfolded protein response. J. Biol. Chem. 277, 1933-1940
4. Maines, M. D. (1997) The heme oxygenase system. A regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37, 517-554
5. Platt, J. L. and Nath, K. A. (1998) Heme oxygenase: protective gene or Trojan horse. Nat. Med. 4, 1364-1365
6. Immenschuh, S. and Ramadori, G. (2000) Gene regulation of heme oxygenase-1 as a therapeutic target. Biochem. Pharmacol. 60, 1121-1128
7. Poss, K. D. and Tonegawa, S. (1997) Heme oxygenase 1 is required for mammalian iron reutilization. Proc. Natl. Acad. Sci. U.S.A. 94, 10919-10924
8. Yachie, A., Niida, Y., Wada, T., Igarashi, N., Kaneda, H., Toma, T., Ohta, K., Kasahara, Y. and Koizumi, S. (1999) Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J. Clin. Invest. 103, 129-135
9. Jeney, V., Balla, J., Yachie, A., Varga, Z., Vercellotti, G. M., Eaton, J. W. and Balla, G. (2002) Pro-oxidant and cytotoxic effects of circulating heme. Blood 100, 879-887
10. Stocker, R., Yamamoto, Y., McDonagh, A. F., Glazer, A. N. and Ames, B. N. (1987) Bilirubin is an antioxidant of possible physiological importance. Science 235, 1043-1046
11. Llesuy, S. F. and Tomaro, M. L. (1994) Heme oxygenase and oxidative stress. Evidence of involvement of bilirubin as physiological protector against oxidative damage. Biochim. Biophys. Acta 1223, 9-14
12. Otterbein, L. E., Bach, F. H., Alam, J., Soares, M., Tao Lu, H., Wysk, M., Davis, R. J., Flavell, R. A. and Choi, A. M. (2000) Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6, 422-428
13. Brouard, S., Otterbein, L. E., Anrather, J., Tobiasch, E., Bach, F. H., Choi, A. M. and Soares, M. P. (2000) Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J. Exp. Med. 192, 1015-1025
14. Balla, G., Jacob, H. S., Balla, J., Rosenberg, M., Nath, K., Apple, F., Eaton, J. W. and Vercellotti, G. M. (1992) Ferritin: a cytoprotective antioxidant strategem of endothelium. J. Biol. Chem. 267, 18148-18153
15. Ferris, C. D., Jaffrey, S. R., Sawa, A., Takahashi, M., Brady, S. D., Barrow, R. K., Tysoe, S. A., Wolosker, H., Baranano, D. E., Dore, S. et al. (1999) Haem oxygenase-1 prevents cell death by regulating cellular iron. Nat. Cell Biol. 1, 152-157
16. Stocker, R. (1990) Induction of haem oxygenase as a defence against oxidative stress. Free Radic. Res. Commun. 9, 101-112
17. Keyse, S. M. and Tyrrell, R. M. (1989) Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc. Natl. Acad. Sci. U.S.A. 86, 99-103
18. Lee, Y. J., Galoforo, S. S., Berns, C.M., Chen, J. C., Davis, B. H., Sim, J. E., Corry, P. M. and Spitz, D. R. (1998) Glucose deprivation-induced cytotoxicity and alterations in mitogen-activated protein kinase activation are mediated by oxidative stress in multidrug-resistant human breast carcinoma. J. Biol. Chem. 273, 5294-5299
19. Lee, Y. J., Galoforo, S. S., Sim, J. E., Ridnoour, L. A., Choi, J., Forman, H. J., Corry, P. M. and Spitz, D. R. (2000) Dominant negative Jun N-terminal protein kinase (JNK-1) inhibits metabolic oxidative stress during glucose deprivation in a human breast carcinoma cell line. Free Radic. Biol. Med. 28, 575-584
20. Blackburn, R. V., Spitz, D. R., Liu, X., Galoforo, S. S., Sim, J. E., Ridnour, L. A., Chen, J. C., Davis, B. H., Corry, P. M. and Lee, Y. J. (1999) Metabolic oxidative stress activates signal transduction and gene expression during glucose deprivation in human tumor cells. Free Radic. Biol. Med. 26, 419-430
21. Spitz, D. R., Sim, J. E., Ridnour, L. A., Galoforo, S. S., Corry, P. M. and Lee, Y. J. (2000) Glucose deprivation-induced oxidative stress in human tumor cells. A fundamental defect in metabolism? Ann. N.Y. Acad. Sci. 899, 349-362
22. Ravagnan, L., Roumier, T. and Kroemer, G. (2002) Mitochondria, the killer organelles and their weapons. J. Cell Physiol. 192, 131-137
23. 2 in vitro and in vivo and reduce menadione-induced DNA injury and cytotoxicity. Am. J. Physiol. 268, C227-C236
24. Goossens, V., Stange, G., Moens, K., Pipeleers, D. and Grooten, L. (1999) Regulation of tumor necrosis factor-induced, mitochondria- and reactive oxygen species-dependent cell death by the electron flux through the electron transport chain complex I. Antioxid. Redox Signal. 1, 285-295
25. Markley, M. A., Pierro, A. and Eaton, S. (2002) Hepatocyte mitochondrial metabolism is inhibited in neonatal rat endotoxaemia: effects of glutamine. Clin. Sci. (London) 102, 337-344
26. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159
27. 2. Free Radic. Biol. Med. 29, 801-813
28. Agarwal, A., Balla, J. Balla, G., Croatt, A. J., Vercellotti, G. M. and Nath, K. A. (1996) Renal tubular epithelial cells mimic endothelial cells upon exposure to oxidized LDL. Am. J. Physiol. 271, F814-F823
29. Fogg, S., Agarwal, A., Nick, H. S. and Visner, G. A. (1999) Iron regulates hyperoxia-dependent human heme oxygenase 1 gene expression in pulmonary endothelial cells. Am. J. Resp. Cell Mol. Biol. 20, 797-804
30. Ryter, S. W., Si, M., Lai, C. C. and Su, C. Y. (2000) Regulation of endothelial heme oxygenase activity during hypoxia is dependent on chelatable iron. Am. J. Physiol. Heart Circ. Physiol. 279, H2889-H2897
31. Hill-Kapturczak, N., Truong, L., Thamilselvan, V., Visner, G. A., Nick, H. S. and Agarwal, A. (2000) Smad7-dependent regulation of heme oxygenase-1 by transforming growth factor-β in human renal epithelial cells. J. Biol. Chem. 275, 40904-40909
32. Hill-Kapturczak, N., Thamilselvan, V., Liu, F., Nick, H. S. and Agarwal, A. (2001) Mechanism of heme oxygenase-1 gene induction by curcumin in human renal proximal tubule cells. Am. J. Physiol. Renal Physiol. 281, F851-F859
33. Kehrer, J. P. (2000) The Haber-Weiss reaction and mechanisms of toxicity. Toxicology 149, 43-50
34. Liang, M., Croatt, A. J. and Nath, K. A. (2000) Mechanisms underlying induction of heme oxygenase-1 by nitric oxide in renal tubular epithelial cells. Am. J. Physiol. Renal Physiol. 279, F728-F735
35. Ryter, S. W., Otterbein, L. E., Morse, D. and Choi, A. M. (2002) Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol. Cell. Biochem. 234/235, 249-263
36. Alam, J., Wicks, C., Stewart, D., Gong, P., Touchard, C., Otterbein, S., Choi, A. M., Burow, M. E. and Tou, J. (2000) Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells. Role of p38 kinase and Nrf2 transcription factor. J. Biol. Chem. 275, 27694-27702
37. 2 in endothelial cells. Am. J. Physiol. 276, H1493-H1501
38. Immenschuh, S., Kietzmann, T., Hinke, V., Wiederhold, M., Katz, N. and Muller-Eberhard, U. (1998) The rat heme oxygenase-1 gene is transcriptionally induced via the protein kinase A signaling pathway in rat hepatocyte cultures. Mol. Pharmacol. 53, 483-491
39. Masuya, Y., Hioki, K., Tokunaga, R. and Taketani, S. (1998) Involvement of the tyrosine phosphorylation pathway in induction of human heme oxygenase-1 by hemin, sodium arsenite, and cadmium chloride. J. Biochem. (Tokyo) 124, 628-633
40. Nadkarni, V., Gabbay, K. H., Bohren, K. M. and Sheikh-Hamad, D. (1998) Osmotic response element enhancer activity: regulation through p38 kinase and mitogen-activated extracellular signal-regulated kinase kinase. J. Biol. Chem. 274, 20185-20190
41. Tacchini, L., Dansi, P., Matteucci, E. and Desiderio, M. A. (2001) Hepatocyte growth factor signaling stimulates hypoxia inducible factor-1 (HIF-1) activity in HepG2 hepatoma cells. Carcinogenesis 22, 1363-1371
42. Wu, D. and Cederbaum, A. I. (2003) Role of p38 MAPK in CYP2E1-dependent arachidonic acid toxicity. J. Biol. Chem. 278, 1115-1124
43. MAPK cascade alone is sufficient to induce LDL receptor expression. J. Lipid Res. 40, 1911-1919
44. Song, M. S., Park, Y. K., Lee, J. H. and Park, K. (2001) Induction of glucose-regulated protein 78 by chronic hypoxia in human gastric tumor cells through a protein kinase C-ε/ERK/AP-1 signaling cascade. Cancer Res. 61, 8322-8330
45. Callejas, N. A., Casado, M., Bosca, L. and Martin-Sanz, P. (2002) Absence of nuclear factor κB inhibition by NSAIDs in hepatocytes. Hepatology 35, 341-348
46. Lee, J., Bruce-Keller, A. J., Kruman, Y., Chan, S. L. and Mattson, M. P. (1999) 2-Deoxy-D-glucose protects hippocampal neurons against excitotoxic and oxidative injury: evidence for the involvement of stress proteins. J. Neurosci. 57, 48-61
47. Sheridan, A. M., Schwartz, J. H., Kroshian, V. M., Tercyak, A. M., Laraia, J., Masino, S. and Lieberthal, W. (1993) Renal mouse proximal tubular cells are more susceptible than MDCK cells to chemical anoxia. Am. J. Physiol. 265, F342-F350
48. Wu, G., Haynes, T. E., Li, H., Yan, W. and Meininger, C. J. (2001) Glutamine metabolism to glucosamine is necessary for glutamine inhibition of endothelial nitric oxide synthesis. Biochem. J. 353, 245-252
49. Hresko, R. C., Heimberg, H., Chi, M. M. Y. and Mueckler, M. (1998) Glucosamine-induced insulin resistance in 3T3-L1 adipocytes is caused by depletion of intracellular ATP. J. Biol. Chem. 273, 20658-20668
50. Rogers, R. J., Monnier, J. M. and Nick, H. S. (2001) Tumor necrosis factor-α selectively induces MnSOD expression via mitochondria-to-nucleus signaling, whereas interleukin-1β utilizes an alternative pathway. J. Biol. Chem. 276, 20419-20427
51. Ebert, B. L., Firth, J. D. and Ratcliffe, P. J. (1995) Hypoxia and mitochondrial inhibitors regulate expression of glucose transporter-1 via distinct Cis-acting sequences. J. Biol. Chem. 270, 29083-29089
52. Finkel, T. (1998) Oxygen radicals and signaling. Curr. Opin. Cell Biol. 10, 248-253
53. 2 and TNF-α and its effects on ICAM-1 expression in endothelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 279, L302-L311
54. Arnold, R. S., Shi, J., Murad, E., Whalen, A. M., Sun, C. Q., Polavarapu, R., Parthasarathy, S., Petros, J. A. and Lambeth, J. D. (2001) Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proc. Natl. Acad. Sci. U.S.A. 98, 5550-5555
55. Kvam, E., Noel, A., Basu-Modak, S. and Tyrrell, R. M. (1999) Cyclooxygenase dependent release of heme from microsomal hemeproteins correlates with induction of heme oxygenase 1 transcription in human fibroblasts. Free Radic. Biol. Med. 26, 511-517
56. Bennett, B. L., Sasaki, D. T., Murray, B. W., O'Leary, E. C., Sakata, S. T., Xu, W., Leisten, J. C., Motiwala, A., Pierce, S., Satoh, Y. et al. (2001) SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. U.S.A. 98, 13681-13686