Curcumin protects human keratinocytes against inorganic arsenite-induced acute cytotoxicity through an NRF2-dependent mechanism

Oxidative Medicine and Cellular Longevity

Volumn , Issue , 2013, Pages

  Zhao, Rui ^a,b   Yang, Bei ^a,b   Wang, Linlin ^a   Xue, Peng ^b   Deng, Baocheng ^a   Zhang, Guohua ^a   Jiang, Shukun ^a   Zhang, Miao ^a   Liu, Min ^a   Pi, Jingbo ^b   Guan, Dawei ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b HAMNER INSTITUTES FOR HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-OXIDANT ACTIVITIES; ANTIOXIDANT RESPONSE ELEMENTS; HUMAN KERATINOCYTES; LOW CONCENTRATIONS; NUCLEAR ACCUMULATION; NUCLEAR FACTOR ERYTHROID 2-RELATED FACTOR 2; PROTECTIVE EFFECTS; PROTEIN EXPRESSIONS;

ARSENIC; CHEMICAL ACTIVATION; CHEMICAL COMPOUNDS; FLOW CYTOMETRY; GENE EXPRESSION; PROTEINS; TISSUE;

CYTOTOXICITY;

ARSENIC ACID; CASPASE 3; CURCUMIN; ISOPROTEIN; KELCH LIKE ECH ASSOCIATED PROTEIN 1; LENTIVIRUS VECTOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR NRF2; ANTIOXIDANT; ARSENIC TRIOXIDE; ARSENOUS ACID DERIVATIVE; LUCIFERASE; MESSENGER RNA; PROTECTIVE AGENT;

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CELL NUCLEUS; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY TEST; FLOW CYTOMETRY; GENE CONTROL; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; KERATINOCYTE; MOLECULAR MECHANICS; NITROBLUE TETRAZOLIUM TEST; PROTEIN EXPRESSION; APOPTOSIS; DNA RESPONSIVE ELEMENT; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY;

ANTIOXIDANTS; APOPTOSIS; ARSENITES; CURCUMIN; CYTOPROTECTION; GENE EXPRESSION REGULATION; HUMANS; KERATINOCYTES; LUCIFERASES; NF-E2-RELATED FACTOR 2; PROTECTIVE AGENTS; RESPONSE ELEMENTS; RNA, MESSENGER;

EID: 84878343958     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2013/412576     Document Type: Article

References (55)

1. Pi J., Kumagai Y., Sun G., Yamauchi H., Yoshida T., Iso H., Endo A., Yu L., Yuki K., Miyauchi T., Shimojo N., Decreased serum concentrations of nitric oxide metabolites among Chinese in an endemic area of chronic arsenic poisoning in inner Mongolia. Free Radical Biology and Medicine 2000 28 7 1137 1142 2-s2.0-0034068291 10.1016/S0891-5849(00)00209-4 (Pubitemid 30314713)
2. Yoshida T., Yamauchi H., Fan Sun G., Chronic health effects in people exposed to arsenic via the drinking water: dose-response relationships in review. Toxicology and Applied Pharmacology 2004 198 3 243 252 2-s2.0-3242761550 10.1016/j.taap.2003.10.022 (Pubitemid 38969953)
3. Wong S. S., Tan K. C., Goh C. L., Cutaneous manifestations of chronic arsenicism: review of seventeen cases. Journal of the American Academy of Dermatology 1998 38 2 179 185 2-s2.0-0031913210 10.1016/S0190-9622(98)70596-1 (Pubitemid 28100830)
4. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans, Some drinking-water disinfectants and contaminants, including arsenic. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans 2004 84 1 477
5. Pi J., Yamauchi H., Kumagai Y., Sun G., Yoshida T., Aikawa H., Hopenhayn-Rich C., Shimojo N., Evidence for induction of oxidative stress caused by chronic exposure of Chinese residents to arsenic contained in drinking water. Environmental Health Perspectives 2002 110 4 331 336 2-s2.0-0036226578 (Pubitemid 34308595)
6. Pi J., Qu W., Reece J. M., Kumagai Y., Waalkes M. P., Transcription factor Nrf2 activation by inorganic arsenic in cultured keratinocytes: involvement of hydrogen peroxide. Experimental Cell Research 2003 290 2 234 245 2-s2.0-0142058235 10.1016/S0014-4827(03)00341-0 (Pubitemid 37272168)
7. Zhao R., Hou Y., Xue P., Woods C. G., Fu J., Feng B., Guan D., Sun G., Chan J. Y., Waalkes M. P., Andersen M. E., Pi J., Long isoforms of NRF1 contribute to arsenic-induced antioxidant response in human keratinocytes. Environmental Health Perspectives 2011 119 1 56 62 2-s2.0-78751560531 10.1289/ehp.1002304
8. Zhao R., Hou Y., Zhang Q., Cross-regulations among NRFs and KEAP1 and effects of their silencing on arsenic-induced antioxidant response and cytotoxicity in human keratinocytes. Environmental Health Perspectives 2012 120 583 589
9. Biswas M., Chan J. Y., Role of Nrf1 in antioxidant response element-mediated gene expression and beyond. Toxicology and Applied Pharmacology 2010 244 1 16 20 2-s2.0-77649275112 10.1016/j.taap.2009.07.034
10. Hayes J. D., McMahon M., NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer. Trends in Biochemical Sciences 2009 34 4 176 188 2-s2.0-63549121490 10.1016/j.tibs.2008.12.008
11. Aono J., Yanagawa T., Itoh K., Li B., Yoshida H., Kumagai Y., Yamamoto M., Ishii T., Activation of Nrf2 and accumulation of ubiquitinated A170 by arsenic in osteoblasts. Biochemical and Biophysical Research Communications 2003 305 2 271 277 2-s2.0-0038367669 10.1016/S0006-291X(03)00728-9 (Pubitemid 36555463)
12. Zhou H., Beevers C. S., Huang S., The targets of curcumin. Current Drug Targets 2011 12 3 332 347 2-s2.0-79551618617
13. Mano Y., Usui T., Kamimura H., In vitro inhibitory effects of non-steroidal anti-inflammatory drugs on 4-methylumbelliferone glucuronidation in recombinant human UDP-glucuronosyltransferase 1A9-potent inhibition by niflumic acid. Biopharmaceutics and Drug Disposition 2006 27 1 1 6 2-s2.0-31744443743 10.1002/bdd.475 (Pubitemid 43173968)
14. Divya C. S., Pillai M. R., Antitumor action of curcumin in human papillomavirus associated cells involves downregulation of viral oncogenes, prevention of NFkB and AP-1 translocation, and modulation of apoptosis. Molecular Carcinogenesis 2006 45 5 320 332 2-s2.0-33646730760 10.1002/mc.20170
15. Rukkumani R., Aruna K., Varma P. S., Menon V. P., Curcumin influences hepatic expression patterns of matrix metalloproteinases in liver toxicity. The Italian Journal of Biochemistry 2004 53 2 61 66 2-s2.0-15844384868
16. Wang H., Geng Q. R., Wang L., Lu Y., Curcumin potentiates antitumor activity of L-asparaginase via inhibition of the AKT signaling pathway in acute lymphoblastic leukemia. Leukemia & Lymphoma 53 1376 1382
17. Jeong G. S., Oh G. S., Pae H. O., Jeong S. O., Kim Y. C., Shin M. K., Byeong Y. S., Sang Y. H., Ho S. L., Jeong J. G., Koh J. S., Chung H. T., Comparative effects of curcuminoids on endothelial heme oxygenase-1 expression: ortho-methoxy groups are essential to enhance heme oxygenase activity and protection. Experimental and Molecular Medicine 2006 38 4 393 400 2-s2.0-33748467392 (Pubitemid 44351434)
18. Balogun E., Foresti R., Green C. J., Motterlini R., Changes in temperature modulate heme oxygenase-1 induction by curcumin in renal epithelial cells. Biochemical and Biophysical Research Communications 2003 308 4 950 955 2-s2.0-0043161924 10.1016/S0006-291X(03)01517-1 (Pubitemid 36976551)
19. Scapagnini G., Foresti R., Calabrese V., Giuffrida Stella A. M., Green C. J., Motterlini R., Caffeic acid phenethyl ester and curcumin: a novel class of heme oxygenase-1 inducers. Molecular Pharmacology 2002 61 5 554 561 (Pubitemid 34171921)
20. Khan S., Vala J. A., Nabi S. U., Protective effect of curcumin against arsenic-induced apoptosis in murine splenocytes in vitro. Journal of Immunotoxicology 9 148 159
21. Farombi E. O., Shrotriya S., Na H. K., Kim S. H., Surh Y. J., Curcumin attenuates dimethylnitrosamine-induced liver injury in rats through Nrf2-mediated induction of heme oxygenase-1. Food and Chemical Toxicology 2008 46 4 1279 1287 2-s2.0-39149106003 10.1016/j.fct.2007.09.095 (Pubitemid 351258204)
22. Lele R. D., Beyond reverse pharmacology: mechanism-based screening of Ayurvedic drugs. Journal of Ayurveda and Integrative Medicine 2010 1 4 257 265 2-s2.0-79952952177 10.4103/0975-9476.74435
23. Yadav A., Lomash V., Samim M., Flora S. J., Curcumin encapsulated in chitosan nanoparticles: a novel strategy for the treatment of arsenic toxicity. Chemico-Biological Interactions 2012 199 49 61
24. Biswas J., Roy S., Mukherjee S., Sinha D., Roy M., Indian spice curcumin may be an effective strategy to combat the genotoxicity of arsenic in Swiss albino mice. Asian Pacific Journal of Cancer Prevention 2010 11 1 239 247 2-s2.0-77955828074
25. Yadav R. S., Shukla R. K., Sankhwar M. L., Patel D. K., Ansari R. W., Pant A. B., Islam F., Khanna V. K., Neuroprotective effect of curcumin in arsenic-induced neurotoxicity in rats. NeuroToxicology 2010 31 5 533 539 2-s2.0-77956227830 10.1016/j.neuro.2010.05.001
26. Suwannateep N., Wanichwecharungruang S., Haag S. F., Encapsulated curcumin results in prolonged curcumin activity in vitro and radical scavenging activity ex vivo on skin after UVB-irradiation. European Journal of Pharmaceutics and Biopharmaceutics 2012 82 485 490
27. Yadav R. S., Sankhwar M. L., Shukla R. K., Chandra R., Pant A. B., Islam F., Khanna V. K., Attenuation of arsenic neurotoxicity by curcumin in rats. Toxicology and Applied Pharmacology 2009 240 3 367 376 2-s2.0-70350028185 10.1016/j.taap.2009.07.017
28. McMahon M., Itoh K., Yamamoto M., Chanas S. A., Henderson C. J., McLellan L. I., Wolf C. R., Cavin C., Hayes J. D., The cap "n" collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Research 2001 61 8 3299 3307 2-s2.0-0035870298 (Pubitemid 32695017)
29. Reisman S. A., Csanaky I. I., Aleksunes L. M., Klaassen C. D., Altered disposition of acetaminophen in Nrf2-null and keap1-knockdown mice. Toxicological Sciences 2009 109 1 31 40 2-s2.0-65549114152 10.1093/toxsci/kfp047
30. Brzóska K., Stepkowski T. M., Kruszewski M., Putative proto-oncogene pir expression is significantly up-regulated in the spleen and kidney of cytosolic superoxide dismutase-deficient mice. Redox Report 2011 16 3 129 133 2-s2.0-79960774467 10.1179/1351000211Y.0000000002
31. Guo X. F., Zhu X. F., Zhong G. S., Deng B. G., Retracted: lapatinib, a dual inhibitor of epidermal growth factor receptor and human epidermal growth factor receptor 2, potentiates the antitumor effects of cisplatin on esophageal carcinoma. Diseases of the Esophagus 2012 10.1111/j.1442-2050.2012.01332.x
32. Jeong S. O., Oh G. S., Ha H. Y., Koo B. S., Kim H. S., Kim Y. C., Kim E. C., Lee K. M., Chung H. T., Pae H. O., Dimethoxycurcumin, a synthetic curcumin analogue, induces heme oxygenase-1 expression through Nrf2 activation in RAW264.7 macrophages. Journal of Clinical Biochemistry and Nutrition 2009 44 1 79 84 2-s2.0-60849126108 10.3164/jcbn.08-194
33. Nishinaka T., Ichijo Y., Ito M., Kimura M., Katsuyama M., Iwata K., Miura T., Terada T., Yabe-Nishimura C., Curcumin activates human glutathione S-transferase P1 expression through antioxidant response element. Toxicology Letters 2007 170 3 238 247 2-s2.0-34248186574 10.1016/j.toxlet.2007.03.011 (Pubitemid 46710275)
34. Du Y., Villeneuve N. F., Wang X. J., Sun Z., Chen W., Li J., Lou H., Wong P. K., Zhang D. D., Oridonin confers protection against arsenic-induced toxicity through activation of the Nrf2-mediated defensive response. Environmental Health Perspectives 2008 116 9 1154 1161 2-s2.0-54149084936 10.1289/ehp.11464
35. Thangapazham R. L., Sharma A., Maheshwari R. K., Beneficial role of curcumin in skin diseases. Advances in Experimental Medicine and Biology 2007 595 343 357 2-s2.0-34347250483 10.1007/978-0-387-46401-5-15
36. Kulac M., Aktas C., Tulubas F., The effects of topical treatment with curcumin on burn wound healing in rats. Journal of Molecular Histology 2013 44 1 83 90
37. Heng M. C. Y., Curcumin targeted signaling pathways: basis for anti-photoaging and anti-carcinogenic therapy. International Journal of Dermatology 2010 49 6 608 622 2-s2.0-77954188904 10.1111/j.1365-4632.2010.04468. x
38. Yang C., Zhang X., Fan H., Liu Y., Curcumin upregulates transcription factor Nrf2, HO-1 expression and protects rat brains against focal ischemia. Brain Research 2009 1282 133 141 2-s2.0-67649670106 10.1016/j.brainres.2009.05. 009
39. Hatcher H., Planalp R., Cho J., Torti F. M., Torti S. V., Curcumin: from ancient medicine to current clinical trials. Cellular and Molecular Life Sciences 2008 65 11 1631 1652 2-s2.0-44749093175 10.1007/s00018-008-7452-4
40. Rushworth S. A., Ogborne R. M., Charalambos C. A., O'Connell M. A., Role of protein kinase C δ in curcumin-induced antioxidant response element-mediated gene expression in human monocytes. Biochemical and Biophysical Research Communications 2006 341 4 1007 1016 2-s2.0-32344432720 10.1016/j.bbrc.2006.01.065 (Pubitemid 43221766)
41. Natarajan V. T., Singh A., Kumar A. A., Sharma P., Kar H. K., Marrot L., Meunier J. R., Natarajan K., Rani R., Gokhale R. S., Transcriptional upregulation of Nrf2-dependent phase II detoxification genes in the involved epidermis of vitiligo vulgaris. The Journal of Investigative Dermatology 2010 130 12 2781 2789 2-s2.0-78149466029 10.1038/jid.2010.201
42. Banning A., Deubel S., Kluth D., Zhou Z., Brigelius-Flohé R., The GI-GPx gene is a target for Nrf2. Molecular and Cellular Biology 2005 25 12 4914 4923 2-s2.0-20344405468 10.1128/MCB.25.12.4914-4923.2005 (Pubitemid 40781093)
43. McNally S. J., Harrison E. M., Ross J. A., Garden O. J., Wigmore S. J., Curcumin induces heme oxygenase 1 through generation of reactive oxygen species, p38 activation and phosphatase inhibition. International Journal of Molecular Medicine 2007 19 1 165 172 2-s2.0-34147165621
44. Kossler S., Nofziger C., Jakab M., Dossena S., Paulmichl M., Curcumin affects cell survival and cell volume regulation in human renal and intestinal cells. Toxicology 2012 292 123 135
45. Dujic J., Kippenberger S., Hoffmann S., Ramirez-Bosca A., Miquel J., Diaz-Alperi J., Bereiter-Hahn J., Kaufmann R., Bernd A., Low concentrations of curcumin induce growth arrest and apoptosis in skin keratinocytes only in combination with UVA or visible light. The Journal of Investigative Dermatology 2007 127 8 1992 2000 2-s2.0-34447572751 10.1038/sj.jid.5700801 (Pubitemid 47075359)
46. Chendil D., Ranga R. S., Meigooni D., Sathishkumar S., Ahmed M. M., Curcumin confers radiosensitizing effect in prostate cancer cell line PC-3. Oncogene 2004 23 8 1599 1607 2-s2.0-1542426626 10.1038/sj.onc.1207284 (Pubitemid 38406523)
47. Pi J., He Y., Bortner C., Huang J., Liu J., Zhou T., Qu W., North S. L., Kasprzak K. S., Diwan B. A., Chignell C. F., Waalkes M. P., Low level, long-term inorganic arsenite exposure causes generalized resistance to apoptosis in cultured human keratinocytes: potential role in skin co-carcinogenesis. International Journal of Cancer 2005 116 1 20 26 2-s2.0-20444450161 10.1002/ijc.20990 (Pubitemid 40827751)
48. Perera R. M., Bardeesy N., Cancer: When antioxidants are bad. Nature 2011 475 7354 43 44 2-s2.0-79960034499 10.1038/475043a
49. Costa R., Abdulhaq H., Haq B., Shadduck R. K., Latsko J., Zenati M., Atem F. D., Rossetti J. M., Sahovic E. A., Lister J., Activity of azacitidine in chronic myelomonocytic leukemia. Cancer 2011 117 12 2690 2696 2-s2.0-79958794151 10.1002/cncr.25759
50. Hayes J. D., McMahon M., The double-edged sword of Nrf2: subversion of redox homeostasis during the evolution of cancer. Molecular Cell 2006 21 6 732 734 2-s2.0-33644856080 10.1016/j.molcel.2006.03.004 (Pubitemid 43376123)
51. Wang X. J., Sun Z., Chen W., Eblin K. E., Gandolfi J. A., Zhang D. D., Nrf2 protects human bladder urothelial cells from arsenite and monomethylarsonous acid toxicity. Toxicology and Applied Pharmacology 2007 225 2 206 213 2-s2.0-36049010730 10.1016/j.taap.2007.07.016 (Pubitemid 350088062)
52. Marrot L., Jones C., Perez P., Meunier J. R., The significance of Nrf2 pathway in (photo)-oxidative stress response in melanocytes and keratinocytes of the human epidermis. Pigment Cell and Melanoma Research 2008 21 1 79 88 2-s2.0-41049099735 10.1111/j.1755-148X.2007.00424.x (Pubitemid 351421462)
53. Shinkai Y., Sumi D., Fukami I., Ishii T., Kumagai Y., Sulforaphane, an activator of Nrf2, suppresses cellular accumulation of arsenic and its cytotoxicity in primary mouse hepatocytes. FEBS Letters 2006 580 7 1771 1774 2-s2.0-33644882749 10.1016/j.febslet.2006.02.031
54. Chan J. Y., Kwong M., Lu R., Chang J., Wang B., Yen T. S. B., Kan Y. W., Targeted disruption of the ubiquitous CNC-bZIP transcription factor, Nrf-1, results in anemia and embryonic lethality in mice. The EMBO Journal 1998 17 6 1779 1787 2-s2.0-0032536783 10.1093/emboj/17.6.1779 (Pubitemid 28119131)
55. Zhang Y., Hayes J. D., Identification of topological determinants in the N-terminal domain of transcription factor Nrf1 that control its orientation in the endoplasmic reticulum membrane. Biochemical Journal 2010 430 3 497 510 2-s2.0-77956661152 10.1042/BJ20100471