Cobalt protoporphyrin induces HO-1 expression mediated partially by FOXO1 and reduces mitochondria-derived reactive oxygen species production

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Liu, Xiaojun ^a   Cui, Ying ^a   Li, Meixia ^b   Xu, Haifeng ^c   Zuo, Jin ^a   Fang, Fude ^a   Chang, Yongsheng ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b INSTITUTE OF BIOPHYSICS   (China)

^c PEKING UNIVERSITY CANCER HOSPITAL AND INSTITUTE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; CYCLOHEXIMIDE; CYCLOOXYGENASE 2; CYTOCHROME C; HEME OXYGENASE 1; MANGANESE SUPEROXIDE DISMUTASE; PROTOPORPHYRIN COBALT; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR FKHR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME INDUCTION; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN STABILITY; UPREGULATION;

ANIMALS; CELL LINE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HEME OXYGENASE-1; HEPATOCYTES; HUMANS; MICE; MITOCHONDRIA; MODELS, BIOLOGICAL; OXIDATIVE STRESS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STABILITY; PROTOPORPHYRINS; REACTIVE OXYGEN SPECIES;

EID: 84892611045     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080521     Document Type: Article

References (40)

1. Manolagas SC, Almeida M (2007) Gone with the Wnts: beta-catenin, T-cell factor, forkhead box O, and oxidative stress in age-dependent diseases of bone, lipid, and glucose metabolism. Mol Endocrinol 21: 2605-2614. doi:10.1210/me.2007-0259. PubMed: 17622581.
2. McCoubrey WK Jr., Huang TJ, Maines MD (1997) Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem 247: 725-732. doi:10.1111/j.1432-1033.1997.00725.x. PubMed: 9266719.
3. Poss KD, Tonegawa S (1997) Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci U S A 94: 10919-10924. doi:10.1073/pnas.94.20.10919. PubMed: 9380735.
4. Poss KD, Tonegawa S (1997) Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci U S A 94: 10925-10930. doi:10.1073/pnas.94.20.10925. PubMed: 9380736.
5. Yachie A, Niida Y, Wada T, Igarashi N, Kaneda H et al. (1999) Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest 103: 129-135. doi:10.1172/JCI4165. PubMed: 9884342.
6. Gabunia K, Ellison SP, Singh H, Datta P, Kelemen SE et al. (2012) Interleukin-19 (IL-19) induces heme oxygenase-1 (HO-1) expression and decreases reactive oxygen species in human vascular smooth muscle cells. J Biol Chem 287: 2477-2484. doi:10.1074/jbc.M111.312470. PubMed: 22158875.
7. Min KJ, Lee JT, Joe EH, Kwon TK (2011) An IkappaBalpha phosphorylation inhibitor induces heme oxygenase-1(HO-1) expression through the activation of reactive oxygen species (ROS)-Nrf2-ARE signaling and ROS-PI3K/Akt signaling in an NF-kappaB-independent mechanism. Cell Signal 23: 1505-1513. doi:10.1016/j.cellsig.2011.05.013. PubMed: 21620964.
8. Shan Y, Pepe J, Lambrecht RW, Bonkovsky HL (2002) Mapping of the chick heme oxygenase-1 proximal promoter for responsiveness to metalloporphyrins. Arch Biochem Biophys 399: 159-166. doi:10.1006/abbi.2001.2742. PubMed: 11888201.
9. Srivastava KK, Cable EE, Donohue SE, Bonkovsky HL (1993) Molecular basis for heme-dependent induction of heme oxygenase in primary cultures of chick embryo hepatocytes. Demonstration of acquired refractoriness to heme. Eur J Biochem 213: 909-917. doi:10.1111/j.1432-1033.1993.tb17835.x. PubMed: 8504830.
10. Abraham NG, Botros FT, Rezzani R, Rodella L, Bianchi R et al. (2002) Differential effect of cobalt protoporphyrin on distributions of heme oxygenase in renal structure and on blood pressure in SHR. Cell Mol Biol Noisy Le Grand 48: 895-902. PubMed: 12699248.
11. Glanemann M, Schirmeier A, Lippert S, Langrehr JM, Neuhaus P et al. (2005) Cobalt-protoporphyrin induced heme oxygenase overexpression and its impact on liver regeneration. Transplant Proc 37: 3223-3225. doi:10.1016/j.transproceed.2005.07.002. PubMed: 16213353.
12. Hsu BR, Chen ST, Fu SH (2005) A single-dose of cobalt-protoporphyrin protects islet beta cells from glucocorticoid suppression. Transplant Proc 37: 1826-1827. doi:10.1016/j.transproceed.2005.02.085. PubMed: 15919478.
13. Shan Y, Lambrecht RW, Donohue SE, Bonkovsky HL (2006) Role of Bach1 and Nrf2 in up-regulation of the heme oxygenase-1 gene by cobalt protoporphyrin. FASEB J 20: 2651-2653. doi:10.1096/fj.06-6346fje. PubMed: 17065227.
14. Eijkelenboom A, Burgering BM (2013) FOXOs: signalling integrators for homeostasis maintenance. Nat Rev Mol Cell Biol 14: 83-97. doi:10.1038/nrm3507. PubMed: 23325358.
15. Birkenkamp KU, Coffer PJ (2003) Regulation of cell survival and proliferation by the FOXO (Forkhead box, class O) subfamily of Forkhead transcription factors. Biochem Soc Trans 31: 292-297. PubMed: 12546704.
16. Lam EW, Francis RE, Petkovic M (2006) FOXO transcription factors: key regulators of cell fate. Biochem Soc Trans 34: 722-726. doi:10.1042/BST0340722. PubMed: 17052182.
17. Glauser DA, Schlegel W (2007) The emerging role of FOXO transcription factors in pancreatic beta cells. J Endocrinol 193: 195-207. doi:10.1677/JOE-06-0191. PubMed: 17470511.
18. Brown J, Wang H, Suttles J, Graves DT, Martin M (2011) Mammalian target of rapamycin complex 2 (mTORC2) negatively regulates Toll-like receptor 4-mediated inflammatory response via FoxO1. J Biol Chem 286: 44295-44305. doi:10.1074/jbc.M111.258053. PubMed: 22045807.
19. Subauste AR, Burant CF (2007) Role of FoxO1 in FFA-induced oxidative stress in adipocytes. Am J Physiol Endocrinol Metab 293: E159-E164. doi:10.1152/ajpendo.00629.2006. PubMed: 17374693.
20. Cheng Z, Guo S, Copps K, Dong X, Kollipara R et al. (2009) Foxo1 integrates insulin signaling with mitochondrial function in the liver. Nat Med 15: 1307-1311. doi:10.1038/nm.2049. PubMed: 19838201.
21. Matsumoto M, Ogawa W, Teshigawara K, Inoue H, Miyake K et al. (2002) Role of the insulin receptor substrate 1 and phosphatidylinositol 3-kinase signaling pathway in insulin-induced expression of sterol regulatory element binding protein 1c and glucokinase genes in rat hepatocytes. Diabetes 51: 1672-1680. doi:10.2337/diabetes.51.6.1672. PubMed: 12031952.
22. Luo J, Deng ZL, Luo X, Tang N, Song WX et al. (2007) A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc 2: 1236-1247. doi:10.1038/nprot.2007.135. PubMed: 17546019.
23. Dong XC, Copps KD, Guo S, Li Y, Kollipara R et al. (2008) Inactivation of hepatic Foxo1 by insulin signaling is required for adaptive nutrient homeostasis and endocrine growth regulation. Cell Metab 8: 65-76. doi:10.1016/j.cmet.2008.06.006. PubMed: 18590693.
24. Kong X, Wang R, Xue Y, Liu X, Zhang H et al. (2010) Sirtuin 3, a new target of PGC-1alpha, plays an important role in the suppression of ROS and mitochondrial biogenesis. PLOS ONE 5: e11707. doi:10.1371/journal.pone.0011707. PubMed: 20661474.
25. Mukhopadhyay P, Rajesh M, Haskó G, Hawkins BJ, Madesh M et al. (2007) Simultaneous detection of apoptosis and mitochondrial superoxide production in live cells by flow cytometry and confocal microscopy. Nat Protoc 2: 2295-2301. doi:10.1038/nprot.2007.327. PubMed: 17853886.
26. Altomonte J, Richter A, Harbaran S, Suriawinata J, Nakae J et al. (2003) Inhibition of Foxo1 function is associated with improved fasting glycemia in diabetic mice. Am J Physiol Endocrinol Metab 285: E718-E728. PubMed: 12783775.
27. Tang ED, Nuñez G, Barr FG, Guan KL (1999) Negative regulation of the forkhead transcription factor FKHR by Akt. J Biol Chem 274: 16741-16746. doi:10.1074/jbc.274.24.16741. PubMed: 10358014.
28. Dowell P, Otto TC, Adi S, Lane MD (2003) Convergence of peroxisome proliferator-activated receptor gamma and Foxo1 signaling pathways. J Biol Chem 278: 45485-45491. doi:10.1074/jbc.M309069200. PubMed: 12966085.
29. Turkseven S, Kruger A, Mingone CJ, Kaminski P, Inaba M et al. (2005) Antioxidant mechanism of heme oxygenase-1 involves an increase in superoxide dismutase and catalase in experimental diabetes. Am J Physiol Heart Circ Physiol 289: H701-H707. doi:10.1152/ajpheart.00024.2005. PubMed: 15821039.
30. Cai C, Teng L, Vu D, He JQ, Guo Y et al. (2012) The heme oxygenase 1 inducer (CoPP) protects human cardiac stem cells against apoptosis through activation of the extracellular signal-regulated kinase (ERK)/NRF2 signaling pathway and cytokine release. J Biol Chem 287: 33720-33732. doi:10.1074/jbc. M112.385542. PubMed: 22879597.
31. Abraham NG, Lavrovsky Y, Schwartzman ML, Stoltz RA, Levere RD et al. (1995) Transfection of the human heme oxygenase gene into rabbit coronary microvessel endothelial cells: protective effect against heme and hemoglobin toxicity. Proc Natl Acad Sci U S A 92: 6798-6802. doi:10.1073/pnas.92.15.6798. PubMed: 7624322.
32. Lee PJ, Alam J, Wiegand GW, Choi AM (1996) Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc Natl Acad Sci U S A 93: 10393-10398. doi:10.1073/pnas.93.19.10393. PubMed: 8816811.
33. Shan Y, Pepe J, Lu TH, Elbirt KK, Lambrecht RW et al. (2000) Induction of the heme oxygenase-1 gene by metalloporphyrins. Arch Biochem Biophys 380: 219-227. doi:10.1006/abbi.2000.1921. PubMed: 10933875.
34. Ye G, Metreveli NS, Donthi RV, Xia S, Xu M et al. (2004) Catalase protects cardiomyocyte function in models of type 1 and type 2 diabetes. Diabetes 53: 1336-1343. doi:10.2337/diabetes.53.5.1336. PubMed: 15111504.
35. Salvi M, Battaglia V, Brunati AM, La Rocca N, Tibaldi E et al. (2007) Catalase takes part in rat liver mitochondria oxidative stress defense. J Biol Chem 282: 24407-24415. doi:10.1074/jbc.M701589200. PubMed: 17576767.
36. Atlante A, Calissano P, Bobba A, Azzariti A, Marra E et al. (2000) Cytochrome c is released from mitochondria in a reactive oxygen species (ROS)-dependent fashion and can operate as a ROS scavenger and as a respiratory substrate in cerebellar neurons undergoing excitotoxic death. J Biol Chem 275: 37159-37166. doi:10.1074/jbc.M002361200. PubMed: 10980192.
37. Vane JR, Bakhle YS, Botting RM (1998) Cyclooxygenases 1 and 2. Annu Rev Pharmacol Toxicol 38: 97-120. doi:10.1146/annurev.pharmtox.38.1.97. PubMed: 9597150.
38. Kim EH, Na HK, Kim DH, Park SA, Kim HN et al. (2008) 15-Deoxy-Delta12,14- prostaglandin J2 induces COX-2 expression through Akt-driven AP-1 activation in human breast cancer cells: a potential role of ROS. Carcinogenesis 29: 688-695. doi:10.1093/carcin/bgm299. PubMed: 18192694.
39. Di Noia MA, Van Driesche S, Palmieri F, Yang LM, Quan S et al. (2006) Heme oxygenase-1 enhances renal mitochondrial transport carriers and cytochrome C oxidase activity in experimental diabetes. J Biol Chem 281: 15687-15693. doi:10.1074/jbc.M510595200. PubMed: 16595661.
40. Bindu S, Pal C, Dey S, Goyal M, Alam A et al. (2011) Translocation of heme oxygenase-1 to mitochondria is a novel cytoprotective mechanism against non-steroidal anti-inflammatory drug-induced mitochondrial oxidative stress, apoptosis, and gastric mucosal injury. J Biol Chem 286: 39387-39402. doi:10.1074/jbc.M111.279893. PubMed: 21908612.