NAD(P)H Quinone Oxidoreductase 1 is Essential for Ozone-induced Oxidative Stress in Mice and Humans

Overview

Journal Am J Respir Cell Mol Biol

Specialties Cell Biology
Molecular Biology

Date 2008 Dec 9

PMID 19059883

Citations 20

Authors

Judith A Voynow

Bernard M Fischer

Shuo Zheng

Erin N Potts

Amy R Grover

Anil K Jaiswal

Andrew J Ghio

W Michael Foster

Affiliations

Soon will be listed here.

Abstract

One host susceptibility factor for ozone identified in epidemiologic studies is NAD(P)H quinone oxidoreductase 1 (NQO1). We hypothesized that after ozone exposure, NQO1 is required to increase 8-isoprostane (also known as F(2)-isoprostane) production, a recognized marker of ozone-induced oxidative stress, and to enhance airway inflammation and hyperresponsiveness. In this report, we demonstrate that in contrast to wild-type mice, NQO1-null mice are resistant to ozone and have blunted responses, including decreased production of F(2)-isoprostane and keratinocyte chemokine, decreased airway inflammation, and diminished airway hyperresponsiveness. Importantly, these results in mice correlate with in vitro findings in humans. In primary human airway epithelial cells, inhibition of NQO1 by dicumarol blocks ozone-induced F(2)-isoprostane production and IL-8 gene expression. Together, these results demonstrate that NQO1 modulates cellular redox status and influences the biologic and physiologic effects of ozone.

Citing Articles

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Thanh Tung N, Ho S, Lu Y, Chen T, Lee K, Chen K Front Med (Lausanne). 2021; 8:705792.

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Erratum: NAD(P)H Quinone Oxidoreductase 1 Is Essential for Ozone-Induced Oxidative Stress in Mice and Humans.

Am J Respir Cell Mol Biol. 2016; 55(6):909.

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References

Janssen L, Catalli A, Helli P . The pulmonary biology of isoprostanes. Antioxid Redox Signal. 2005; 7(1-2):244-55. DOI: 10.1089/ars.2005.7.244. View

Romieu I, Ramirez-Aguilar M, Sienra-Monge J, Moreno-Macias H, Del Rio-Navarro B, David G . GSTM1 and GSTP1 and respiratory health in asthmatic children exposed to ozone. Eur Respir J. 2006; 28(5):953-9. DOI: 10.1183/09031936.06.00114905. View

Bey E, Bentle M, Reinicke K, Dong Y, Yang C, Girard L . An NQO1- and PARP-1-mediated cell death pathway induced in non-small-cell lung cancer cells by beta-lapachone. Proc Natl Acad Sci U S A. 2007; 104(28):11832-7. PMC: 1913860. DOI: 10.1073/pnas.0702176104. View

Samet J, Hatch G, Horstman D, Steck-Scott S, Arab L, Bromberg P . Effect of antioxidant supplementation on ozone-induced lung injury in human subjects. Am J Respir Crit Care Med. 2001; 164(5):819-25. DOI: 10.1164/ajrccm.164.5.2008003. View

Janssen L . Isoprostanes: an overview and putative roles in pulmonary pathophysiology. Am J Physiol Lung Cell Mol Physiol. 2001; 280(6):L1067-82. DOI: 10.1152/ajplung.2001.280.6.L1067. View

Hazbun M, Hamilton R, Holian A, Eschenbacher W . Ozone-induced increases in substance P and 8-epi-prostaglandin F2 alpha in the airways of human subjects. Am J Respir Cell Mol Biol. 1993; 9(5):568-72. DOI: 10.1165/ajrcmb/9.5.568. View

Navarro F, Navas P, Burgess J, Bello R, de Cabo R, Arroyo A . Vitamin E and selenium deficiency induces expression of the ubiquinone-dependent antioxidant system at the plasma membrane. FASEB J. 1998; 12(15):1665-73. DOI: 10.1096/fasebj.12.15.1665. View

Li Y, Gauderman W, Avol E, Dubeau L, Gilliland F . Associations of tumor necrosis factor G-308A with childhood asthma and wheezing. Am J Respir Crit Care Med. 2006; 173(9):970-6. PMC: 2662916. DOI: 10.1164/rccm.200508-1256OC. View

Voynow J, Fischer B, Malarkey D, Burch L, Wong T, Longphre M . Neutrophil elastase induces mucus cell metaplasia in mouse lung. Am J Physiol Lung Cell Mol Physiol. 2004; 287(6):L1293-302. DOI: 10.1152/ajplung.00140.2004. View

10.

Vacchiano C, Tempel G . Role of nonenzymatically generated prostanoid, 8-iso-PGF2 alpha, in pulmonary oxygen toxicity. J Appl Physiol (1985). 1994; 77(6):2912-7. DOI: 10.1152/jappl.1994.77.6.2912. View

11.

Brar S, Kennedy T, Whorton A, Sturrock A, Huecksteadt T, Ghio A . Reactive oxygen species from NAD(P)H:quinone oxidoreductase constitutively activate NF-kappaB in malignant melanoma cells. Am J Physiol Cell Physiol. 2001; 280(3):C659-76. DOI: 10.1152/ajpcell.2001.280.3.C659. View

12.

Holtzman M, Fabbri L, OByrne P, Gold B, Aizawa H, Walters E . Importance of airway inflammation for hyperresponsiveness induced by ozone. Am Rev Respir Dis. 1983; 127(6):686-90. DOI: 10.1164/arrd.1983.127.6.686. View

13.

Hiltermann J, Lapperre T, van Bree L, Steerenberg P, Brahim J, Sont J . Ozone-induced inflammation assessed in sputum and bronchial lavage fluid from asthmatics: a new noninvasive tool in epidemiologic studies on air pollution and asthma. Free Radic Biol Med. 2000; 27(11-12):1448-54. DOI: 10.1016/s0891-5849(99)00191-4. View

14.

Pryor W, Squadrito G, Friedman M . The cascade mechanism to explain ozone toxicity: the role of lipid ozonation products. Free Radic Biol Med. 1995; 19(6):935-41. DOI: 10.1016/0891-5849(95)02033-7. View

15.

Winski S, Swann E, Hargreaves R, Dehn D, Butler J, Moody C . Relationship between NAD(P)H:quinone oxidoreductase 1 (NQO1) levels in a series of stably transfected cell lines and susceptibility to antitumor quinones. Biochem Pharmacol. 2001; 61(12):1509-16. DOI: 10.1016/s0006-2952(01)00631-1. View

16.

Peden D . The epidemiology and genetics of asthma risk associated with air pollution. J Allergy Clin Immunol. 2005; 115(2):213-9. DOI: 10.1016/j.jaci.2004.12.003. View

17.

David G, Romieu I, Sienra-Monge J, Collins W, Ramirez-Aguilar M, Del Rio-Navarro B . Nicotinamide adenine dinucleotide (phosphate) reduced:quinone oxidoreductase and glutathione S-transferase M1 polymorphisms and childhood asthma. Am J Respir Crit Care Med. 2003; 168(10):1199-204. DOI: 10.1164/rccm.200305-684OC. View

18.

. Health effects of outdoor air pollution. Part 2. Committee of the Environmental and Occupational Health Assembly of the American Thoracic Society. Am J Respir Crit Care Med. 1996; 153(2):477-98. DOI: 10.1164/ajrccm.153.2.8564086. View

19.

Siegel D, Franklin W, Ross D . Immunohistochemical detection of NAD(P)H:quinone oxidoreductase in human lung and lung tumors. Clin Cancer Res. 1998; 4(9):2065-70. View

20.

Romieu I, Sienra-Monge J, Ramirez-Aguilar M, Moreno-Macias H, Reyes-Ruiz N, Estela del Rio-Navarro B . Genetic polymorphism of GSTM1 and antioxidant supplementation influence lung function in relation to ozone exposure in asthmatic children in Mexico City. Thorax. 2003; 59(1):8-10. PMC: 1758856. View