Cadmium-mediated toxicity of lung epithelia is enhanced through NF-κB-mediated transcriptional activation of the human zinc transporter ZIP8

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 302, Issue 9, 2012, Pages

  Napolitano, Jessica R ^a,b   Liu, Ming Jie ^b   Bao, Shengying ^b   Crawford, Melissa ^b   Nana Sinkam, Patrick ^b,c   Cormet Boyaka, Estelle ^b,c   Knoell, Daren L ^b,c  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Chronic obstructive pulmonary disease; Cigarette smoke; Inflammation

Indexed keywords

CADMIUM; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ZINC; ZINC TRANSPORTER; ZIP8 PROTEIN;

APOPTOSIS; ARTICLE; CELL CULTURE; CELL DEATH; CELL STRAIN; CONTROLLED STUDY; CYTOTOXICITY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG ALVEOLUS EPITHELIUM; LUNG TOXICITY; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOKING; TRANSCRIPTION INITIATION;

APOPTOSIS; CADMIUM; CATION TRANSPORT PROTEINS; CELL LINE; CELL POLARITY; CYTOPROTECTION; EPITHELIAL CELLS; HUMANS; LUNG; NECROSIS; NF-KAPPA B; NITRILES; PRIMARY CELL CULTURE; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; SMOKING; SULFONES; TRANSCRIPTIONAL ACTIVATION; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION; ZINC;

EID: 84860540850     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00351.2011     Document Type: Article

References (56)

1. Age-Related Eye Disease Study Research Group. A randomized, placebo-controlled, clinical trial of high-dose supplementation with vitamins C and E, beta-carotene, and zinc for age-related macular degeneration and vision loss. Arch Ophthalmol 119: 1417-1436, 2001.
2. Bao S, Knoell DL. Zinc modulates airway epithelium susceptibility to death receptor-mediated apoptosis. Am J Physiol Lung Cell Mol Physiol 290: L433-L441, 2006.
3. Bao S, Liu MJ, Lee B, Besecker B, Lai JP, Guttridge DC, Knoell DL. Zinc modulates the innate immune response in vivo to polymicrobial sepsis through regulation of NF-κB. Am J Physiol Lung Cell Mol Physiol 298: L744-L754, 2010.
4. Barber S, Henricks PA, Nijkamp FP, Kraneveld AD, Folkerts G. Inflammatory changes in the airways of mice caused by cigarette smoke exposure are only partially reversed after smoking cessation. Respir Res 11: 99, 2010.
5. Begum NA, Kobayashi M, Moriwaki Y, Matsumoto M, Toyoshima K, Seya T. Mycobacterium bovis BCG cell wall and lipopolysaccharide induce a novel gene, BIGM103, encoding a 7-TM protein: identification of a new protein family having Zn-transporter and Zn-metalloprotease signatures. Genomics 80: 630-645, 2002.
6. Besecker B, Bao S, Bohacova B, Papp A, Sadee W, Knoell DL. The human zinc transporter SLC39A8 (Zip8) is critical in zinc-mediated cytoprotection in lung epithelia. Am J Physiol Lung Cell Mol Physiol 294: L1127-L1136, 2008.
7. Besecker BY, Exline MC, Hollyfield J, Phillips G, Disilvestro RA, Wewers MD, Knoell DL. A comparison of zinc metabolism, inflammation, and disease severity in critically ill infected and noninfected adults early after intensive care unit admission. Am J Clin Nutr 93: 1356-1364, 2011.
8. Centers for Disease Control, and Prevention. National Center for Health Statistics: National Health Interview Survey Raw Data, 2008.
9. Chung KF. Cytokines in chronic obstructive pulmonary disease. Eur Respir J Suppl 34: 50s-59s, 2001.
10. Churg A, Dai J, Tai H, Xie C, Wright JL. Tumor Necrosis Factor-alpha Is Central to Acute Cigarette Smoke-induced Inflammation and Connective Tissue Breakdown. Am J Respir Crit Care Med 166: 849-54, 2002.
11. Cosio MG, Saetta M, Augusti A. Immunologic aspects of chronic obstructive pulmonary disease. N Engl J Med 360: 2445-54, 2009.
12. Dalton TP, He L, Wang B, Miller ML, Jin L, Stringer KF, Chang X, Baxter CS, Nebert DW. Identification of mouse SLC39A8 as the transporter responsible for cadmium-induced toxicity in the testis. Proc Natl Acad Sci USA 102: 3401-3406, 2005.
13. Eide DJ. The SLC39 family of metal ion transporters. Pflügers Arch 447: 796-800, 2004.
14. Ferhani N, Letuve S, Kozhich A, Thibaudeau O, Grandsaigne M, Maret M, Dombret MC, Sims GP, Kolbeck R, Coyle AJ, Aubier M, Pretolani M. Expression of high-mobility group box 1 and of receptor for advanced glycation end products in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 181: 917-927, 2010.
15. Fouad AA, Jresat I. Protective effect of telmisartan against cadmiuminduced nephrotoxicity in mice. Life Sci 89: 29-35, 2011.
16. Freitas M, Fernandes E. Zinc, cadmium and nickel increase the activation of NF-κB and the release of cytokines from THP-1 monocytic cells. Metallomics 3: 1238-1243, 2011.
17. Gan WQ, Man SF, Senthilselvan A, Sin DD. Association between chronic obstructive pulmonary disease and systemic inflammation: a systematic review and a meta-analysis. Thorax 59: 574-580, 2004.
18. Gavrilin MA, Bouakl IJ, Knatz NL, Duncan MD, Hall MW, Gunn JS, Wewers MD. Internalization and phagosome escape required for Francisella to induce human monocyte IL-1beta processing and release. Proc Natl Acad Sci USA 103: 141-146, 2006.
19. Haase H, Ober-Blöbaum JL, Engelhardt G, Hebel S, Rink L. Cadmium ions induce monocytic production of tumor necrosis factor-alpha by inhibiting mitogen activated protein kinase dephosphorylation. Toxicol Lett 198: 152-158, 2010.
20. He L, Girijashanker K, Dalton TP, Reed J, Li H, Soleimani M, Nebert DW. ZIP8, member of the solute-carrier-39 (SLC39) metal-transporter family: characterization of transporter properties. Mol Pharmacol 70: 171-180, 2006.
21. He L, Wang B, Hay EB, Nebert DW. Discovery of ZIP transporters that participate in cadmium damage to testis and kidney. Toxicol Appl Pharmacol 238: 250-257, 2009.
22. Herzog R, Cunningham-Rundles S. Immunologic impact of nutrient depletion in chronic obstructive pulmonary disease. Curr Drug Targets 12: 489-500, 2011.
23. Husten C, Jackson K, Office on Smoking and Health, National Center for Chronic Disease Prevention and Health Promotion, Lee C. Cigarette Smoking Among Adults. Atlanta, GA: CDC, 2002.
24. Järup L. Cadmium overload and toxicity. Nephrol Dial Transplant 17: 35-39, 2002.
25. Jin T, Wu X, Tang Y, Nordberg M, Bernard A, Ye T, Kong Q, Lundström NG, Nordberg GF. Environmental epidemiological study and estimation of benchmark dose for renal dysfunction in a cadmiumpolluted area in China. Biometals 17: 525-530, 2004.
26. Joshi PC, Mehta A, Jabber WS, Fan X, Guidot DM. Zinc deficiency mediates alcohol-induced alveolar epithelial and macrophage dysfunction in rats. Am J Respir Cell Mol Biol 41: 207-216, 2009.
27. Karadag F, Cildag O, Altinisik M, Kozaci LD, Kiter G, Altun C. Trace elements as a component of oxidative stress in COPD. Respirology 9: 33-37, 2004.
28. Karp PH, Moninger TO, Weber SP, Nesselhauf TS, Launspach Zabner J JL, Welsh MJ. An in vitro model of differentiated human airway epithelia. Methods for establishing primary cultures. Methods Mol Biol 188: 115-137, 2002.
29. Koizumi T, Shirakura H, Kumagai H, Tatsumoto H, Suzuki KT. Mechanism of cadmium-induced cytotoxicity in rat hepatocytes: cadmiuminduced active oxygen-related permeability changes of the plasma membrane. Toxicology 114: 125-134, 1996.
30. Låg M, Rodionov D, Ovrevik J, Bakke O, Schwarze PE, Refsnes M. Cadmium-induced inflammatory responses in cells relevant for lung toxicity: Expression and release of cytokines in fibroblasts, epithelial cells and macrophages. Toxicol Lett 193: 252-260, 2010.
31. Lin YS, Caffrey JL, Chang MH, Dowling N, Lin JW. Cigarette smoking, cadmium exposure, and zinc intake on obstructive lung disorder. Respir Res 11: 53, 2010.
32. 2+ uptake by the ZIP8 HCO3-dependent symporter: kinetics, electrogenicity and trafficking. Biochem Biophys Res Commun 365: 814-820, 2008.
33. Liuzzi JP, Cousins RJ. Mammalian zinc transporters. Annu Rev Nutr 24: 151-172, 2004.
34. Lommatzsch M, Cicko S, Muller T, Lucattelli M, Bratke K, Stoll P, Grimm M, Dürk T, Zissel G, Ferrari D, Di Virgilio F, Sorichter S, Lungarella G, Virchow JC, Idzko M. Extracellular adenosine triphosphate and chronic obstructive pulmonary disease. Am J Respir Crit Care Med 181: 928-934, 2010.
35. Lopez AD, Murray CC. The global burden of disease, 1990-2020. Nat Med 4: 1241-1243, 1998.
36. Maldonado F, Bartholmai BJ, Swensen SJ, Midthun DE, Decker PA, Jett JR. Are airflow obstruction and radiographic evidence of emphysema risk factors for lung cancer? A nested case-control study using quantitative emphysema analysis. Chest 138: 1295-1302, 2010.
37. Mannino DM, Holguin F, Greves HM, Savage-Brown A, Stock AL, Jones RL. Urinary cadmium levels predict lower lung function in current and former smokers: data from the Third National Health and Nutrition Examination Survey. Thorax 59: 194-198, 2004.
38. Maret W. Zinc coordination environments in proteins as redox sensors and signal transducers. Antioxid Redox Signal 8: 1419-1441, 2006.
39. Murray CJ, Lopez AD. Mortality by cause for eight regions of the world: Global Burden of Disease Study. Lancet 349: 1269-1276, 1997.
40. Opitz B, van Laak V, Eitel J, Suttorp N. Innate immune recognition in infectious and noninfectious diseases of the lung. Am J Respir Crit Care Med 181: 1294-1309, 2010.
41. Pourahmad J, O'Brien PJ, Jokar F, Daraei B. Carcinogenic metal induced sites of reactive oxygen species formation in hepatocytes. Toxicology 17: 803-810, 2003.
42. Prasad AS. Clinical spectrum of human zinc deficiency. In: Biochemistry of Zinc, edited by AS Prasad. New York: Plenum Press, 1993.
43. Prasad AS. Zinc deficiency. Br Med J 326: 409-410, 2003.
44. Prasad AS, Bao B, Beck FW, Kucuk O, Sarkar FH. Antioxidant effect of zinc in humans. Free Radic Biol Med 37: 1182-1190, 2004.
45. Raguso CA, Luthy C. Nutritional status in chronic obstructive pulmonary disease: role of hypoxia. Nutrition 27: 138-143, 2011.
46. Raymond AD, Gekonge B, Giri MS, Hancock A, Papasavvas E, Chehimi J, Kossenkov AV, Nicols C, Yousef M, Mounzer K, Shull J, Kostman J, Showe L, Montaner LJ. Increased metallothionein gene expression, zinc, and zinc-dependent resistance to apoptosis in circulating monocytes during HIV viremia. J Leukoc Biol 88: 589-596, 2010.
47. Satarug S, Baker JR, Urbenjapol S, Haswell-Elkins M, Reilly PE, Williams DJ, Moore MR. A global perspective on cadmium pollution and toxicity in non-occupationally exposed population. Toxicol Lett 137: 65-83, 2003.
48. Shankar AH, Prasad AS. Zinc and immune function: the biological basis of altered resistance to infection. Am J Clin Nutr 68: 447S-463S, 1998.
49. Szulakowski P, Crowther AJ, Jiménez LA, Donaldson K, Mayer R, Leonard TB, MacNee W, Drost EM. The effect of smoking on the transcriptional regulation of lung inflammation in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 174: 41-50, 2006.
50. Thevenod F. Cadmium and cellular signaling cascades: To be or not to be? Toxicol Appl Pharmacol 238: 221-239, 2009.
51. Truong-Tran AQ, Grosser D, Ruffin RE, Murgia C, Zalewski PD. Apoptosis in the normal and inflamed airway epithelium: role of zinc in epithelial protection and procaspase-3 regulation. Biochem Pharmacol 66: 1459-1468, 2003.
52. Waalkes MP. Cadmium carcinogenesis. Mutat Res 533: 107-120, 2003.
53. Wilson DO, Weissfeld JL, Balkan A, Schragin JG, Fuhrman CR, Fisher SN, Wilson J, Leader JK, Siegfried JM, Shapiro SD, Sciurba FC. Association of radiographic emphysema and airflow obstruction with lung cancer. Am J Respir Crit Care Med 178: 738-744, 2008.
54. Wu X, Lu Z, Chen J, Wang J, Huang F. Hepatic c-fos expression is independent of oxidative stress and inflammation induced by acute cadmium exposure in rats. Ann Nutr Metab 51: 258-263, 2007.
55. Yagi O, Aoshiba K, Nagai A. Activation of nuclear factor-κB in airway epithelial cells in patients with chronic obstructive pulmonary disease. Respiration 73: 610-616, 2006.
56. Yang CF, Shen HM, Shen Y, Zhuang ZX, Ong CN. Cadmium-induced oxidative cellular damage in human fetal lung fibroblasts (MRC-5 cells). Environ Health Perspect 105: 712-716, 1997.