Role of the Nrf2-heme oxygenase-1 pathway in silver nanoparticle-mediated cytotoxicity

Toxicology and Applied Pharmacology

Volumn 258, Issue 1, 2012, Pages 89-98

  Kang, Su Jin ^a,b   Ryoo, In geun ^a   Lee, Young Joon ^b   Kwak, Mi Kyoung ^a,c  

^a Yeungnam University   (South Korea)

^b Daegu Haany University   (South Korea)

^c The Catholic University of Korea   (South Korea)

Author keywords

DNA damage; HO 1; Nrf2; P38MAPK; PI3K; Silver nanoparticles

Indexed keywords

HEME OXYGENASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTOPORPHYRIN; SHORT HAIRPIN RNA; SILVER NANOPARTICLE; TRANSCRIPTION FACTOR NRF2;

APOPTOSIS; ARTICLE; CELL VIABILITY; CYTOTOXICITY; DNA DAMAGE; HUMAN; HUMAN CELL;

APOPTOSIS; CELL LINE, TUMOR; DNA DAMAGE; HEME OXYGENASE-1; HUMANS; METAL NANOPARTICLES; NF-E2-RELATED FACTOR 2; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SILVER;

EID: 84855424509     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.10.011     Document Type: Article

References (51)

1. Ahamed M., Karns M., Goodson M., Rowe J., Hussain S.M., Schlager J.J., Hong Y. DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells. Toxicol. Appl. Pharmacol. 2008, 233:404-410.
2. Ahamed M., Alsalhi M.S., Siddiqui M.K. Silver nanoparticle applications and human health. Clin. Chim. Acta 2010, 411:1841-1848.
3. Alam J. Multiple elements within the 5' distal enhancer of the mouse heme oxygenase-1 gene mediate induction by heavy metals. J. Biol. Chem. 1994, 269:25049-25056.
4. Alam J., Den Z. Distal AP-1 binding sites mediate basal level enhancement and TPA induction of the mouse heme oxygenase-1 gene. J. Biol. Chem. 1992, 267:21894-21900.
5. Alam J., Shibahara S., Smith A. Transcriptional activation of the heme oxygenase gene by heme and cadmium in mouse hepatoma cells. J. Biol. Chem. 1989, 264:6371-6375.
6. Alam J., Camhi S., Choi A.M. Identification of a second region upstream of the mouse heme oxygenase-1 gene that functions as a basal level and inducer-dependent transcription enhancer. J. Biol. Chem. 1995, 270:11977-11984.
7. Alam J., Stewart D., Touchard C., Boinapally S., Choi A.M., Cook J.L. Nrf2, a Cap 'n' Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem. 1999, 274:26071-26078.
8. Arisawa T., Tahara T., Shibata T., Nagasaka M., Nakamura M., Kamiya Y., Fujita H., Yoshioka D., Okubo M., Hirata I., Nakano H. Nrf2 gene promoter polymorphism and gastric carcinogenesis. Hepatogastroenterology 2008, 55:750-754.
9. Arora S., Jain J., Rajwade J.M., Paknikar K.M. Interactions of silver nanoparticles with primary mouse fibroblasts and liver cells. Toxicol. Appl. Pharmacol. 2009, 236:310-318.
10. AshaRani P.V., Low Kah Mun G., Hande M.P., Valiyaveettil S. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 2009, 3:279-290.
11. Brunet A., Bonni A., Zigmond M.J., Lin M.Z., Juo P., Hu L.S., Anderson M.J., Arden K.C., Blenis J., Greenberg M.E. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999, 96:857-868.
12. Carlson C., Hussain S.M., Schrand A.M., Braydich-Stolle L.K., Hess K.L., Jones R.L., Schlager J.J. Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J. Phys. Chem. B 2008, 112:13608-13619.
13. Chaloupka K., Malam Y., Seifalian A.M. Nanosilver as a new generation of nanoproduct in biomedical applications. Trends Biotechnol. 2010, 28:580-588.
14. Chen X., Thakkar H., Tyan F., Gim S., Robinson H., Lee C., Pandey S.K., Nwokorie C., Onwudiwe N., Srivastava R.K. Constitutively active Akt is an important regulator of TRAIL sensitivity in prostate cancer. Oncogene 2001, 20:6073-6083.
15. Choi O., Deng K.K., Kim N.J., Ross L., Surampalli R.Y., Hu Z. The inhibitory effects of silver nanoparticles, silver ions, and silver chloride colloids on microbial growth. Water Res. 2008, 42:3066-3074.
16. Cohen M.S., Stern J.M., Vanni A.J., Kelley R.S., Baumgart E., Field D., Libertino J.A., Summerhayes I.C. In vitro analysis of a nanocrystalline silver-coated surgical mesh. Surg. Infect. (Larchmt.) 2007, 8:397-403.
17. Dudek H., Datta S.R., Franke T.F., Birnbaum M.J., Yao R., Cooper G.M., Segal R.A., Kaplan D.R., Greenberg M.E. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 1997, 275:661-665.
18. Foldbjerg R., Olesen P., Hougaard M., Dang D.A., Hoffmann H.J., Autrup H. PVP-coated silver nanoparticles and silver ions induce reactive oxygen species, apoptosis and necrosis in THP-1 monocytes. Toxicol. Lett. 2009, 190:156-162.
19. Gong P., Hu B., Stewart D., Ellerbe M., Figueroa Y.G., Blank V., Beckman B.S., Alam J. Cobalt induces heme oxygenase-1 expression by a hypoxia-inducible factor-independent mechanism in Chinese hamster ovary cells: regulation by Nrf2 and MafG transcription factors. J. Biol. Chem. 2001, 276:27018-27025.
20. Harrington L.S., Findlay G.M., Lamb R.F. Restraining PI3K: mTOR signalling goes back to the membrane. Trends Biochem. Sci. 2005, 30:35-42.
21. Hay N. Interplay between FOXO, TOR, and Akt. Biochim. Biophys. Acta 2011, 1813:1965-1970.
22. Hwang E.T., Lee J.H., Chae Y.J., Kim Y.S., Kim B.C., Sang B.I., Gu M.B. Analysis of the toxic mode of action of silver nanoparticles using stress-specific bioluminescent bacteria. Small 2008, 4:746-750.
23. Jomova K., Valko M. Advances in metal-induced oxidative stress and human disease. Toxicology 2011, 283:65-87.
24. Kennedy S.G., Wagner A.J., Conzen S.D., Jordan J., Bellacosa A., Tsichlis P.N., Hay N. The PI 3-kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes Dev. 1997, 11:701-713.
25. Kensler T.W., Wakabayashi N., Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 2007, 47:89-116.
26. Keyse S.M., Tyrrell R.M. 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. 1989, 86:99-103.
27. Kim D.H., Kim J.H., Kim E.H., Na H.K., Cha Y.N., Chung J.H., Surh Y.J. 15-Deoxy-delta12,14-prostaglandin J2 upregulates the expression of heme oxygenase-1 and subsequently matrix metalloproteinase-1 in human breast cancer cells: possible roles of iron and ROS. Carcinogenesis 2009, 30:645-654.
28. Kim S., Choi J.E., Choi J., Chung K.H., Park K., Yi J., Ryu D.Y. Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol. In Vitro 2009, 23:1076-1084.
29. Kobayashi M., Yamamoto M. Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Redox Signal. 2005, 7:385-394.
30. Kobayashi A., Kang M.I., Okawa H., Ohtsuji M., Zenke Y., Chiba T., Igarashi K., Yamamoto M. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 2004, 24:7130-7139.
31. Kocanova S., Buytaert E., Matroule J.Y., Piette J., Golab J., de Witte P., Agostinis P. Induction of heme-oxygenase 1 requires the p38MAPK and PI3K pathways and suppresses apoptotic cell death following hypericin-mediated photodynamic therapy. Apoptosis 2007, 12:731-741.
32. Kumaravel T.S., Jha A.N. Reliable comet assay measurements for detecting DNA damage induced by ionising radiation and chemicals. Mutat. Res. 2006, 605:7-16.
33. Kwak M.K., Wakabayashi N., Kensler T.W. Chemoprevention through the Keap1-Nrf2 signaling pathway by phase 2 enzyme inducers. Mutat. Res. 2004, 555:133-148.
34. Laity J.H., Andrews G.K. Understanding the mechanisms of zinc-sensing by metal-response element binding transcription factor-1 (MTF-1). Arch. Biochem. Biophys. 2007, 463:201-210.
35. Li M.H., Cha Y.N., Surh Y.J. Peroxynitrite induces HO-1 expression via PI3K/Akt-dependent activation of NF-E2-related factor 2 in PC12 cells. Free Radic. Biol. Med. 2006, 41:1079-1091.
36. Maines M.D. The heme oxygenase system: update 2005. Antioxid. Redox Signal. 2005, 7:1761-1766.
37. Manandhar, S., Choi, B.H., Ryoo, I.G., Kang, S.J., Kim, J.A., Choi, H.G., Park, P.H., Kwak, M.K., submitted for publication. NRF2 inhibition represses ErbB2 signaling in ovarian carcinoma cells: Implications for tumor growth retardation and docetaxel sensitivity.
38. McMahon M., Itoh K., Yamamoto M., Hayes J.D. Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J. Biol. Chem. 2003, 278:21592-21600.
39. Paine A., Eiz-Vesper B., Blasczyk R., Immenschuh S. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem. Pharmacol. 2010, 80:1895-1903.
40. Ryter S.W., Alam J., Choi A.M. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 2006, 86:583-650.
41. Salh B., Marotta A., Wagey R., Sayed M., Pelech S. Dysregulation of phosphatidylinositol 3-kinase and downstream effectors in human breast cancer. Int. J. Cancer 2002, 98:148-154.
42. Sarbassov D.D., Guertin D.A., Ali S.M., Sabatini D.M. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005, 307:1098-1101.
43. Shibahara S., Muller R.M., Taguchi H. Transcriptional control of rat heme oxygenase by heat shock. J. Biol. Chem. 1987, 262:12889-12892.
44. Singh N.P., McCoy M.T., Tice R.R., Schneider E.L. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 1988, 175:184-191.
45. Sondi I., Salopek-Sondi B. Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J. Colloid Interface Sci. 2004, 275:177-182.
46. Taketani S., Kohno H., Yoshinaga T., Tokunaga R. The human 32-kDa stress protein induced by exposure to arsenite and cadmium ions is heme oxygenase. FEBS Lett. 1989, 245:173-176.
47. Tran H., Brunet A., Grenier J.M., Datta S.R., Fornace A.J., DiStefano P.S., Chiang L.W., Greenberg M.E. DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science 2002, 296:530-534.
48. Tzivion G., Dobson M., Ramakrishnan G. FoxO transcription factors; Regulation by AKT and 14-3-3 proteins. Biochim. Biophys. Acta 2011, 1813:1938-1945.
49. Wu M.M., Chiou H.Y., Chen C.L., Wang Y.H., Hsieh Y.C., Lien L.M., Lee T.C., Chen C.J. GT-repeat polymorphism in the heme oxygenase-1 gene promoter is associated with cardiovascular mortality risk in an arsenic-exposed population in northeastern Taiwan. Toxicol. Appl. Pharmacol. 2010, 248:226-233.
50. Zhang X., Tang N., Hadden T.J., Rishi A.K. Akt, FoxO and regulation of apoptosis. Biochim. Biophys. Acta 2011, 1813:1978-1986.
51. Zhou B.B., Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature 2000, 408:433-439.