Induction of heme oxygenase 1 by arsenite inhibits cytokine-induced monocyte adhesion to human endothelial cells

Toxicology and Applied Pharmacology

Volumn 236, Issue 2, 2009, Pages 202-209

  Sun, Xi ^a   Pi, Jingbo ^b   Liu, Wenlan ^a   Hudson, Laurie G ^a   Liu, Ke Jian ^a   Feng, Changjian ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

^b HAMNER INSTITUTES FOR HEALTH SCIENCES   (United States)

Author keywords

Arsenic; Cytokine; Endothelial cells; Heme oxygenase 1; Monocyte adhesion

Indexed keywords

ARSENIC TRIOXIDE; HEME OXYGENASE 1; INTERCELLULAR ADHESION MOLECULE 1; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL ADHESION; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MONOCYTE; PROTEIN EXPRESSION; UMBILICAL VEIN; UPREGULATION;

ARSENITES; CELL ADHESION; CELLS, CULTURED; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; ENZYME INDUCTION; HEME OXYGENASE-1; HUMANS; MONOCYTES;

RODENTIA;

EID: 62549154830     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2009.01.023     Document Type: Article

References (66)

1. Andrew A.S., Warren A.J., Barchowsky A., Temple K.A., Klei L., Soucy N.V., O'Hara K.A., and Hamilton J.W. Genomic and proteomic profiling of responses to toxic metals in human lung cells. Environ. Health Perspect. 111 (2003) 825-838
2. Balakumar P., Kaur T., and Singh M. Potential target sites to modulate vascular endothelial dysfunction: current perspectives and future directions. Toxicology 245 (2008) 49-64
3. Basu P., Ghosh R.N., Grove L.E., Klei L., and Barchowsky A. Angiogenic potential of 3-nitro-4-hydroxy benzene arsonic acid (Roxarsone). Environ. Health Perspect. 116 (2008) 520-523
4. Bau D.T., Wang T.S., Chung C.H., Wang A.S.S., and Jan K.Y. Oxidative DNA adducts and DNA-protein cross-links are the major DNA lesions induced by arsenite. Environ. Health Perspect. 110 (2002) 753-756
5. Benbrahim-Tallaa L., Waterland R.A., Styblo M., Achanzar W.E., Webber M.M., and Waalkes M.P. Molecular events associated with arsenic-induced malignant transformation of human prostatic epithelial cells: aberrant genomic DNA methylation and K-ras oncogene activation. Toxicol. Appl. Pharmacol. 206 (2005) 288-298
6. Berger S.P., Hunger M., Yard B.A., Schnuelle P., and Van Der Woude F.J. Dopamine induces the expression of heme oxygenase-1 by human endothelial cells in vitro. Kidney Int. 58 (2000) 2314-2319
7. Bunderson M., Coffin J.D., and Beall H.D. Arsenic induces peroxynitrite generation and cyclooxygenase-2 protein expression in aortic endothelial cells: possible role in atherosclerosis. Toxicol. Appl. Pharmacol. 184 (2002) 11-18
8. Bunderson M., Brooks D.M., Walker D.L., Rosenfeld M.E., Coffin J.D., and Beall H.D. Arsenic exposure exacerbates atherosclerotic plaque formation and increases nitrotyrosine and leukotriene biosynthesis. Toxicol. Appl. Pharmacol. 201 (2004) 32-39
9. Chen S.C., and Chen W.C. Vascular leakage induced by exposure to arsenic via increased production of NO, hydroxyl radical and peroxynitrite. Microvasc. Res. 75 (2008) 373-380
10. Chen S.C., Tsai M.H., Wang H.J., Yu H.S., and Chang L.W. Vascular permeability alterations induced by arsenic. Hum. Exp. Toxicol. 23 (2004) 1-7
11. Chen X.L., Dodd G., Thomas S., Zhang X.L., Wasserman M.A., Rovin B.H., and Kunsch C. Activation of Nrf2/ARE pathway protects endothelial cells from oxidant injury and inhibits inflammatory gene expression. Am. J. Physiol, Heart Circ. Physiol. 290 (2006) H1862-H1870
12. Chen Y., Santella R.M., Kibriya M.G., Wang Q., Kappil M., Verret W.J., Graziano J.H., and Ahsan H. Association between arsenic exposure from drinking water and plasma levels of soluble cell adhesion molecules. Environ. Health Perspect. 115 (2007) 1415-1420
13. Chung H.T., Pae H.O., and Cha Y.N. Role of heme oxygenase-1 in vascular disease. Curr. Pharm. Des. 14 (2008) 422-428
14. Cooper K.L., Liu K.J., and Hudson L.G. Contributions of reactive oxygen species and mitogen-activated protein kinase signaling in arsenite-stimulated hemeoxygenase-1 production. Toxicol. Appl. Pharmacol. 218 (2007) 119-127
15. Cybulsky M.I., and Gimbrone Jr. M.A. Endothelial expression of a mononuclear leukocyte adhesion molecule during atherogenesis. Science 251 (1991) 788-791
16. Dulak J., Deshane J., Jozkowicz A., and Agarwal A. Heme oxygenase-1 and carbon monoxide in vascular pathobiology. Circulation 117 (2008) 231-241
17. Edelman P. Environmental and workplace contamination in the semiconductor industry - implications for future health of the workforce and community. Environ. Health Perspect. 86 (1990) 291-295
18. Engel R.R., and Smith A.H. Arsenic in drinking water and mortality from vascular disease - an ecologic analysis in 30 counties in the United States. Arch. Environ. Health 49 (1994) 418-427
19. Engel R.R., Hopenhaynrich C., Receveur O., and Smith A.H. Vascular effects of chronic arsenic exposure - a review. Epidemiol. Rev. 16 (1994) 184-209
20. Glass C.K., and Witztum J.L. Atherosclerosis: the road ahead. Cell 104 (2001) 503-516
21. Gutiérrez G., Mendoza C., Zapata E., Montiel A., Reyes E., Montaño L.F., and López-Marure R. Dehydroepiandrosterone inhibits the TNF-alpha-induced inflammatory response in human umbilical vein endothelial cells. Atherosclerosis 190 (2007) 90-99
22. He X.-Q., Chen R., Yang P., Li A.-P., Zhou J.W., and Liu Q.-Z. Biphasic effect of arsenite on cell proliferation and apoptosis is associated with the activation of JNK and ERK1/2 in human embryo lung fibroblast cells. Toxicol. Appl. Pharmacol. 220 (2007) 18-24
23. Hewitt D.J., Millner G.C., Nye A.C., and Simmons H.F. Investigation of arsenic exposure from soil at a superfund site. Environ. Res. 68 (1995) 73-81
24. Immenschuh S., and Schroder H. Heme oxygenase-1 and cardiovascular disease. Histol. Histopathol. 21 (2006) 679-685
25. Ishikawa K., Navab M., Leitinger N., Fogelman A.M., and Lusis A.J. Induction of heme oxygenase-1 inhibits the monocyte transmigration induced by mildly oxidized LDL. J. Clin. Invest. 100 (1997) 1209-1216
26. Kao Y.H., Yu C.L., Chang L.W., and Yu H.S. Low concentrations of arsenic induce vascular endothelial growth factor and nitric oxide release and stimulate angiogenesis in vitro. Chem. Res. Toxicol. 16 (2003) 460-468
27. Klei L.R., and Barchowsky A. Positive signaling interactions between arsenic and ethanol for angiogenic gene induction in human microvascular endothelial cells. Toxicol. Sci. 102 (2008) 319-327
28. Kwon H.-M., Choi Y.-J., Choi J.-S., Kang S.-W., Bae J.-Y., Kang I.-J., Jun J.-G., Lee S.-S., Lim S.S., and Kang Y.-H. Blockade of cytokine-induced endothelial cell adhesion molecule expression by licorice isoliquiritigenin through NF-{kappa}B signal disruption. Exp. Biol. Med. 232 (2007) 235-245
29. Lee C., Lee Y.M., and Rice R.H. Human epidermal cell protein responses to arsenite treatment in culture. Chem.-Biol. Interact. 155 (2005) 43-54
30. Lee P.-C., Ho I.C., and Lee T.-C. Oxidative stress mediates sodium arsenite-induced expression of heme oxygenase-1, monocyte chemoattractant protein-1, and interleukin-6 in vascular smooth muscle cells. Toxicol. Sci. 85 (2005) 541-550
31. Lewis D.R., Southwick J.W., Ouellet-Hellstrom R., Rench J., and Calderon R.L. Drinking water arsenic in Utah: a cohort mortality study. Environ. Health Perspect. 107 (1999) 359-365
32. Libby P. Inflammation in atherosclerosis. Nature 420 (2002) 868-874
33. Liu F., and Jan K.Y. DNA damage in arsenite- and cadmium-treated bovine aortic endothelial cells. Free Radic. Biol. Med. 28 (2000) 55-63
34. Liu J., Kadiiska M.B., Liu Y., Lu T., Qu W., and Waalkes M.P. Stress-related gene expression in mice treated with inorganic arsenicals. Toxicol. Sci. 61 (2001) 314-320
35. Maines M.D., and Gibbs P.E.M. 30 some years of heme oxygenase: from a "molecular wrecking ball" to a "mesmerizing" trigger of cellular events. Biochem. Biophys. Res. Commun. 338 (2005) 568-577
36. McKone T.E., and Daniels J.I. Estimating human exposure through multiple pathways from air, water, and soil. Regul. Toxicol. Pharmacol. 13 (1991) 36-61
37. Morita T. Heme oxygenase and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 1786-1795
38. Morse D., and Choi A.M.K. Heme oxygenase-1. The "emerging molecule" has arrived. Am. J. Respir. Cell Mol. Biol. 27 (2002) 8-16
39. Mukherjee T.K., Mishra A.K., Mukhopadhyay S., and Hoidal J.R. High concentration of antioxidants N-acetylcysteine and mitoquinone-Q induces intercellular adhesion molecule 1 and oxidative stress by increasing intracellular glutathione. J. Immunol. 178 (2007) 1835-1844
40. Navas-Acien A., Sharrett A.R., Silbergeld E.K., Schwartz B.S., Nachman K.E., Burke T.A., and Guallar E. Arsenic exposure and cardiovascular disease: a systematic review of the epidemiologic evidence. Am. J. Epidemiol. 162 (2005) 1037-1049
41. Otterbein L.E., Soares M.P., Yamashita K., and Bach F.H. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 24 (2003) 449-455
42. Pae H.-O., Oh G.-S., Lee B.-S., Rim J.-S., Kim Y.-M., and Chung H.-T. 3-Hydroxyanthranilic acid, one of l-tryptophan metabolites, inhibits monocyte chemoattractant protein-1 secretion and vascular cell adhesion molecule-1 expression via heme oxygenase-1 induction in human umbilical vein endothelial cells. Atherosclerosis 187 (2006) 274-284
43. Prawan A., Kundu J.K., and Surh Y.J. Molecular basis of heme oxygenase-1 induction: implications for chemoprevention and chemoprotection. Antioxid. Redox Signal. 7 (2005) 1688-1703
44. Prozialeck W.C., Edwards J.R., Nebert D.W., Woods J.M., Barchowsky A., and Atchison W.D. The vascular system as a target of metal toxicity. Toxicol. Sci. 102 (2008) 207-218
45. Pysher M.D., Chen Q.M., and Vaillancourt R.R. Arsenic alters vascular smooth muscle cell focal adhesion complexes leading to activation of FAK-src mediated pathways. Toxicol. Appl. Pharmacol. 231 (2008) 135-141
46. Rea M.A., Gregg J.P., Qin Q., Phillips M.A., and Rice R.H. Global alteration of gene expression in human keratinocytes by inorganic arsenic. Carcinogenesis 24 (2003) 747-756
47. Ross R. Atherosclerosis - an inflammatory disease. N. Engl. J. Med. 340 (1999) 115-126
48. Ryter S.W., and Choi A.M.K. Heme oxygenase-1: redox regulation of a stress protein in lung and cell culture models. Antioxid. Redox Signal. 7 (2005) 80-91
49. Ryter S.W., Alam J., and Choi A.M.K. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 86 (2006) 583-650
50. Simeonova P.P., and Luster M.I. Arsenic and atherosclerosis. Toxicol. Appl. Pharmacol. 198 (2004) 444-449
51. Simeonova P.P., Hulderman T., Harki D., and Luster M.I. Arsenic exposure accelerates atherogenesis in apolipoprotein E-/- mice. Environ. Health Perspect. 111 (2003) 1744-1748
52. Snow E.T., Sykora P., Durham T.R., and Klein C.B. Arsenic, mode of action at biologically plausible low doses: what are the implications for low dose cancer risk?. Toxicol. Appl. Pharmacol. 207 (2005) 557-564
53. Soares M.P., Seldon M.P., Gregoire I.P., Vassilevskaia T., Berberat P.O., Yu J., Tsui T.-Y., and Bach F.H. Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J. Immunol. 172 (2004) 3553-3563
54. Stocker R., and Perrella M.A. Heme oxygenase-1 - a novel drug target for atherosclerotic diseases?. Circulation 114 (2006) 2178-2189
55. Straub A.C., Stolz D.B., Ross M.A., Hernandez-Zavala A., Soucy N.V., Klei L.R., and Barchowsky A. Arsenic stimulates sinusoidal endothelial cell capillarization and vessel remodeling in mouse liver. Hepatology 45 (2007) 205-212
56. Takahashi M., Ikeda U., Masuyama J.-I., Kitagawa S.-I., Kasahara T., Shimpo M., Kano S., and Shimada K. Monocyte-endothelial cell interaction induces expression of adhesion molecules on human umbilical cord endothelial cells. Cardiovasc. Res. 32 (1996) 422-429
57. Takahashi T., Morita K., Akagi R., and Sassa S. Heme oxygenase-1: a novel therapeutic target in oxidative tissue injuries. Curr. Med. Chem. 11 (2004) 1545-1561
58. Tsai S.H., Liang Y.C., Chen L., Ho F.M., Hsieh M.S., and Lin J.K. Arsenite stimulates cyclooxygenase-2 expression through activating I kappa B kinase and nuclear factor kappa B in primary and ECV304 endothelial cells. J. Cell. Biochem. 84 (2002) 750-758
59. Tseng C.H. Cardiovascular disease in arsenic-exposed subjects living in the arseniasis-hyperendemic areas in Taiwan. Atherosclerosis 199 (2008) 12-18
60. Tsou T.C., Yeh S.C., Tsai E.M., Tsai F.Y., Chao H.R., and Chang L.W. Arsenite enhances tumor necrosis factor-alpha-induced expression of vascular cell adhesion molecule-1. Toxicol. Appl. Pharmacol. 209 (2005) 10-18
61. Tsou T.-C., Yeh S.C., Tsai F.-Y., Chen J.-W., and Chiang H.-C. Glutathione regulation of redox-sensitive signals in tumor necrosis factor-[alpha]-induced vascular endothelial dysfunction. Toxicol. Appl. Pharmacol. 221 (2007) 168-178
62. Wang C.-H., Hsiao C.K., Chen C.-L., Hsu L.-I., Chiou H.-Y., Chen S.-Y., Hsueh Y.-M., Wu M.-M., and Chen C.-J. A review of the epidemiologic literature on the role of environmental arsenic exposure and cardiovascular diseases. Toxicol. Appl. Pharmacol. 222 (2007) 315-326
63. Wei M., Arnold L., Cano M., and Cohen S.M. Effects of co-administration of antioxidants and arsenicals on the rat urinary bladder epithelium. Toxicol. Sci. 83 (2005) 237-245
64. Xie Y.X., Trouba K.J., Liu J., Waalkes M.P., and Germolec D.R. Biokinetics and subchronic toxic effects of oral arsenite, arsenate, monomethylarsonic acid, and dimethylarsinic acid in v-Ha-ras transgenic (Tg.AC) mice. Environ. Health Perspect. 112 (2004) 1255-1263
65. Zheng X.H., Watts G.S., Vaught S., and Gandolfi A.J. Low-level arsenite induced gene expression in HEK293 cells. Toxicology 187 (2003) 39-48
66. Zhou Z., Connell M.C., and MacEwan D.J. TNFR1-induced NF-[kappa]B, but not ERK, p38MAPK or JNK activation, mediates TNF-induced ICAM-1 and VCAM-1 expression on endothelial cells. Cell. Signal. 19 (2007) 1238-1248