Heme oxygenase-1 protects human melanocytes from H2O 2-Induced oxidative stress via the Nrf2-ARE pathway

Journal of Investigative Dermatology

Volumn 131, Issue 7, 2011, Pages 1420-1427

  Jian, Zhe ^a   Li, Kai ^a   Liu, Ling ^a   Zhang, Ying ^a   Zhou, Zhou ^a   Li, Chunying ^a   Gao, Tianwen ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME; GLUTAMATE CYSTEINE LIGASE CATALYTIC SUBUNIT; GLUTAMATE CYSTEINE LIGASE MODULATORY SUBUNIT; HEME OXYGENASE 1; HEMIN; HYDROGEN PEROXIDE; MESSENGER RNA; PROTOPORPHYRIN ZINC; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ARTICLE; CELL ASSAY; CELL DEATH; CELL IMMORTALIZATION; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME SUBUNIT; FLOW CYTOMETRY; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MELANOCYTE; OXIDATIVE STRESS; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSCRIPTION INITIATION; UPREGULATION;

EID: 79958856350     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2011.56     Document Type: Article

References (43)

1. Alam J, Wicks C, Stewart D et al. (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 275:27694-702
2. Apopa PL, He X, Ma Q (2008) Phosphorylation of Nrf2 in the transcription activation domain by casein kinase 2 (CK2) is critical for the nuclear translocation and transcription activation function of Nrf2 in IMR-32 neuroblastoma cells. J Biochem Mol Toxicol 22:63-76 (Pubitemid 351360163)
3. Barbouti A, Doulias PT, Nousis L et al. (2002) DNA damage and apoptosis in hydrogen peroxide-exposed Jurkat cells: bolus addition versus continuous generation of H(2)O(2). Free Radic Biol Med 33:691-702 (Pubitemid 35245842)
4. Beyer TA, Auf DKU, Braun S et al. (2007) Roles and mechanisms of action of the Nrf2 transcription factor in skin morphogenesis, wound repair and skin cancer. Cell Death Differ 14:1250-4 (Pubitemid 46965255)
5. Bickers DR, Athar M (2006) Oxidative stress in the pathogenesis of skin disease. J Invest Dermatol 126:2565-75 (Pubitemid 44764040)
6. Braun S, Hanselmann C, Gassmann MG et al. (2002) Nrf2 transcription factor, a novel target of keratinocyte growth factor action which regulates gene expression and inflammation in the healing skin wound. Mol Cell Biol 22:5492-505 (Pubitemid 34755759)
7. Chan K, Han XD, Kan YW (2001) An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc Natl Acad Sci USA 98:4611-6 (Pubitemid 32295024)
8. Chen XL, Varner SE, Rao AS et al. (2003) Laminar flow induction of antioxidant response element-mediated genes in endothelial cells. A novel anti-inflammatory mechanism. J Biol Chem 278:703-11 (Pubitemid 36790739)
9. Enomoto A, Itoh K, Nagayoshi E et al. (2001) High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol Sci 59:169-77 (Pubitemid 32117993)
10. Fahey JW, Haristoy X, Dolan PM et al. (2002) Sulforaphane inhibits extracellular, intracellular, and antibiotic-resistant strains of Helicobac-ter pylori and prevents benzo[a]pyrene-induced stomach tumors. Proc Natl Acad Sci USA 99:7610-5 (Pubitemid 34568739)
11. Fahey JW, Talalay P (1999) Antioxidant functions of sulforaphane: a potent inducer of phase II detoxication enzymes. Food Chem Toxicol 37:973-9 (Pubitemid 29481800)
12. Giovannelli L, Bellandi S, Pitozzi V et al. (2004) Increased oxidative DNA damage in mononuclear leukocytes in vitiligo. Mutat Res 556:101-6 (Pubitemid 39371182)
13. Gopinathan V, Miller NJ, Milner AD et al. (1994) Bilirubin and ascorbate antioxidant activity in neonatal plasma. Febs Lett 349:197-200 (Pubitemid 24263261)
14. Guan CP, Zhou MN, Xu AE et al. (2008) The susceptibility to vitiligo is associated with NF-E2-related factor2 (Nrf2) gene polymorphisms: a study on Chinese Han population. Exp Dermatol 17:1059-62
15. Ishii T, Itoh K, Takahashi S et al. (2000) Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem 275:16023-9 (Pubitemid 30366908)
16. Itoh K, Chiba T, Takahashi S et al. (1997) An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236:313-22 (Pubitemid 27373291)
17. Itoh K, Ishii T, Wakabayashi N et al. (1999a) Regulatory mechanisms of cellular response to oxidative stress. Free Radic Res 31:319-24 (Pubitemid 29452857)
18. Itoh K, Wakabayashi N, Katoh Y et al. (1999b) Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 13:76-86 (Pubitemid 29045117)
19. Jeong GS, Oh GS, Pae HO et al. (2006) Comparative effects of curcuminoids on endothelial heme oxygenase-1 expression: ortho-methoxy groups are essential to enhance heme oxygenase activity and protection. Exp Mol Med 38:393-400
20. Kaspar JW, Niture SK, Jaiswal AK (2009) Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 47:1304-9
21. Kensler TW, Wakabayashi N, Biswal S (2007) Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47:89-116
22. Kim JW, Li MH, Jang JH et al. (2008) 15-Deoxy-Delta(12,14)-prostaglandin J(2) rescues PC12 cells from H2O2-induced apoptosis through Nrf2-mediated upregulation of heme oxygenase-1: potential roles of Akt and ERK1/2. Biochem Pharmacol 76:1577-89
23. 0 collar family transcription factor Nrf3. J Biol Chem 274:6443-52 (Pubitemid 29111059)
24. Lau A, Villeneuve NF, Sun Z et al. (2008) Dual roles of Nrf2 in cancer. Pharmacol Res 58:262-70
25. Le PI, van den Berg FM, van den Wijngaard RM et al. (1997) Generation of a human melanocyte cell line by introduction of HPV16 E6 and E7 genes. In Vitro Cell Dev Biol Anim 33:42-9
26. Lee YJ, Shacter E (2000) Hydrogen peroxide inhibits activation, not activity, of cellular caspase-3 in vivo. Free Radic Biol Med 29:684-92
27. Lin Q, Weis S, Yang G et al. (2007) Heme oxygenase-1 protein localizes to the nucleus and activates transcription factors important in oxidative stress. J Biol Chem 282:20621-33 (Pubitemid 47100046)
28. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-8 (Pubitemid 34164012)
29. Marrot L, Jones C, Perez P et al. (2008) The significance of Nrf2 pathway in (photo)-oxidative stress response in melanocytes and keratinocytes of the human epidermis. Pigment Cell Melanoma Res 21:79-88 (Pubitemid 351421462)
30. Mastore M, Kohler L, Nappi AJ (2005) Production and utilization of hydrogen peroxide associated with melanogenesis and tyrosinase-mediated oxidations of DOPA and dopamine. FEBS J 272:2407-15 (Pubitemid 40705062)
31. Motohashi H, Yamamoto M (2004) Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 10: 549-57 (Pubitemid 39433824)
32. Natarajan VT, Singh A, Kumar AA et al. (2010) Transcriptional upregulation of Nrf2-dependent phase II detoxification genes in the involved epidermis of vitiligo vulgaris. J Invest Dermatol 130:2781-9
33. Nguyen T, Sherratt PJ, Huang HC et al. (2003) Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome. J Biol Chem 278:4536-41 (Pubitemid 36800950)
34. Otterbein LE, Bach FH, Alam J et al. (2000) Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6:422-8 (Pubitemid 30208159)
35. Pi J, Qu W, Reece JM et al. (2003) Transcription factor Nrf2 activation by inorganic arsenic in cultured keratinocytes: involvement of hydrogen peroxide. Exp Cell Res 290:234-45 (Pubitemid 37272168)
36. Radhakrishnan N, Bhaskaran M, Singhal PC (2005) Hepatocyte growth factor modulates H2O2-induced mesangial cell apoptosis through induction of heme oxygenase-1. Nephron Physiol 101:p92-8
37. Ramos-Gomez M, Kwak MK, Dolan PM et al. (2001) Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci USA 98:3410-5 (Pubitemid 32220859)
38. Ryter SW, Alam J, Choi AM (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86: 583-650
39. Schallreuter KU, Gibbons NC, Zothner C et al. (2007) Hydrogen peroxide-mediated oxidative stress disrupts calcium binding on calmodulin: more evidence for oxidative stress in vitiligo. Biochem Biophys Res Commun 360:70-5 (Pubitemid 46992795)
40. Tanaka A, Hamada N, Fujita Y et al. (2010) A novel kavalactone derivative protects against H2O2-induced PC12 cell death via Nrf2/ARE activation. Bioorg Med Chem 18:3133-9
41. Trouba KJ, Hamadeh HK, Amin RP et al. (2002) Oxidative stress and its role in skin disease. Antioxid Redox Signal 4:665-73 (Pubitemid 35001451)
42. Tusi SK, Ansari N, Amini M et al. (2010) Attenuation of NF-kappaB and activation of Nrf2 signaling by 1,2,4-triazine derivatives, protects neuron-like PC12 cells against apoptosis. Apoptosis 15:738-51
43. Zhou Z, Li CY, Li K et al. (2009) Decreased methionine sulphoxide reductase A expression renders melanocytes more sensitive to oxidative stress: a possible cause for melanocyte loss in vitiligo. Br J Dermatol 161:504-9