Skip to main content
SpringerLink
Log in

Inflammation, oxidative stress, and higher expression levels of Nrf2 and NQO1 proteins in the airways of women chronically exposed to biomass fuel smoke

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

The study was carried out to examine whether chronic exposure to smoke during daily household cooking with biomass fuel (BMF) elicits changes in airway cytology and expressions of Nrf2 (nuclear factor erythroid 2 [NF-E2]-related factor 2 [Nrf2]), Keap1 (Kelch-like erythroid-cell-derived protein with CNC homology [ECH]-associated protein 1), and NQO1 (NAD(P)H:quinone oxidoreductase 1) proteins in the airways. For this, 282 BMF-using women (median age 34 year) and 236 age-matched women who cooked with liquefied petroleum gas (LPG) were enrolled. Particulate matter with diameters of < 10 µm (PM10) and < 2.5 µm (PM2.5) were measured in indoor air with real-time laser photometer. Routine hematology, sputum cytology, Nrf2, Keap1, NQO1, and generation of reactive oxygen species (ROS) along with the levels of superoxide dismutase (SOD) and catalase were measured in both groups. PM10 and PM2.5 levels were significantly higher in BMF-using households compared to LPG. Compared with LPG users, BMF users had 32% more leukocytes in circulation and their sputa were 1.4-times more cellular with significant increase in absolute number of neutrophils, lymphocytes, eosinophils, and alveolar macrophages, suggesting airway inflammation. ROS generation was 1.5-times higher in blood neutrophils and 34% higher in sputum cells of BMF users while erythrocyte SOD was 31% lower and plasma catalase was relatively unchanged, suggesting oxidative stress. In BMF users, Keap1 expression was reduced, the percentage of AEC with nuclear expression of Nrf2 was two- to three-times more, and NQO1 level in sputum cell lysate was two-times higher than that of LPG users. In conclusion, cooking with BMF was associated with Nrf2 activation and elevated NQO1 protein level in the airways. The changes may be adaptive cellular response to counteract biomass smoke-elicited oxidative stress and inflammation-related tissue injury in the airways.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Apte K, Salvi S (2016) Household air pollution and its effects on health. Version 1. F1000Res 5: F1000 Faculty Rev-2593. https://doi.org/10.12688/f1000research.7552.1

  2. Oluwole O, Arinola GO, Ana GR, Wiskel T, Huo D, Olopade OI, Olopade CO (2013) Relationship between household air pollution from biomass smoke exposure, and pulmonary dysfunction, oxidant-antioxidant imbalance and systemic inflammation in rural women and children in Nigeria. Glob J Health Sci 5:28–38

    Article  PubMed  PubMed Central  Google Scholar 

  3. Dutta A, Mukherjee B, Das D, Banerjee A, Ray MR (2011) Hypertension with elevated levels of oxidized low-density lipoprotein and anti-cardiolipin antibody in circulation of premenopausal Indian women chronically exposed to biomass smoke during cooking. Indoor Air 21:165–176

    Article  PubMed  CAS  Google Scholar 

  4. Dutta A, Bhattacharya P, Lahiri T, Ray MR (2012) Immune cells and cardiovascular health in premenopausal women of rural India chronically exposed to biomass smoke during daily household cooking. Sci Total Environ 438:293–298

    Article  PubMed  CAS  Google Scholar 

  5. Mondal NK, Mukherjee B, Das D, Ray MR (2010) Micronucleus formation, DNA damage and repair in premenopausal women chronically exposed to high level of indoor air pollution from biomass fuel use in rural India. Mutat Res 697:47–54

    Article  PubMed  CAS  Google Scholar 

  6. Mondal NK, Bhattacharya P, Ray MR (2011) Assessment of DNA damage by comet assay and fast halo assay in buccal epithelial cells of Indian women chronically exposed to biomass smoke. Int J Hyg Environ Health 214:311–318

    Article  PubMed  CAS  Google Scholar 

  7. Roychoudhury S, Mondal NK, Mukherjee S, Dutta A, Siddique S, Ray MR (2012) Activation of protein kinase B (PKB/Akt) and risk of lung cancer among rural women in India who cook with biomass fuel. Toxicol Appl Pharmacol 259:45–53

    Article  PubMed  CAS  Google Scholar 

  8. Mondal NK, Roy A, Mukherjee B, Das D, Ray MR (2010) Indoor air pollution from biomass burning activates Akt in airway cells and peripheral blood lymphocytes: a study among premenopausal women in rural India. Toxicol Pathol 38:1085–1098

    Article  PubMed  CAS  Google Scholar 

  9. Mondal NK, Roychoudhury S, Ray MR (2015) Higher AgNOR expression in metaplastic and dysplastic airway epithelial cells predicts the risk of developing lung cancer in women chronically exposed to biomass smoke. J Environ Pathol Toxicol Oncol 34:35–51

    Article  PubMed  Google Scholar 

  10. Mondal NK, Dutta A, Banerjee A, Chakraborty S, Lahiri T, Ray MR (2009) Effect of indoor air pollution from biomass fuel use on argyrophilic nuclear organizer regions in buccal epithelial cells. J Environ Pathol Toxicol Oncol 28:253–259

    Article  PubMed  CAS  Google Scholar 

  11. Mondal NK, Das D, Mukherjee B, Ray MR (2011) Upregulation of AgNOR expression in epithelial cells and neutrophils in the airways and leukocytes in peripheral blood of women chronically exposed to biomass smoke. Anal Quant Cytol Histol 33:50–59

    PubMed  Google Scholar 

  12. Banerjee M, Siddique S, Dutta A, Mukherjee B, Ray MR (2012) Cooking with biomass increases the risk of depression in premenopausal women in India. Soc Sci Med 75:565–572

    Article  PubMed  Google Scholar 

  13. Zhang J, Smith KR (1996) Hydrocarbon emissions and health risks from cookstoves in developing countries. J Expo Anal Environ Epidemiol 6:147–161

    PubMed  Google Scholar 

  14. Morawska L, Zhang JJ (2002) Combustion sources of particles. I. Health relevance and source signatures. Chemosphere 49:1045–1058

    Article  PubMed  CAS  Google Scholar 

  15. Jezierska-Drutel A, Rosenzweig SA, Neumann CA (2013) Role of oxidative stress and the microenvironment in breast cancer development and progression. Adv Cancer Res 119:107–125

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Dutta A, Ray MR (2013) Changes in sputum cytology, airway inflammation and oxidative stress due to chronic inhalation of biomass smoke during cooking in premenopausal rural Indian women. Int J Hyg Environ Health 216:301–308

    Article  PubMed  CAS  Google Scholar 

  17. Seril DN, Liao J, Yang GY, Yang CS (2003) Oxidative stress and ulcerative colitis-associ-ated carcinogenesis: studies in humans and animal models. Carcinogenesis 24:353–362

    Article  PubMed  CAS  Google Scholar 

  18. Chang WC, Coudry RA, Clapper ML, Zhang X, Williams KL, Spittle CS, Li T, Cooper HS (2007) Loss of p53 enhances the induction of colitis-associated neoplasia by dextran sulfate sodium. Carcinogenesis 28:2375–2381

    Article  PubMed  CAS  Google Scholar 

  19. Ma Q (2013) Role of nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol 53:401–426

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Osburn WO, Kensler TW (2008) Nrf2 signaling: an adaptive response pathway for protection against environmental toxic insults. Mutat Res 659:31–39

    Article  PubMed  CAS  Google Scholar 

  21. Favreau LV, Pickett CB (1991) Transcriptional regulation of the rat NAD(P)H:quinonereductase gene. Identification of regulatory elements controlling basal level expression and inducible expression by planar aromatic compounds and phenolic antioxidants. J Biol Chem 266:4556–4561

    PubMed  CAS  Google Scholar 

  22. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I (1997) An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236:313–322

    Article  PubMed  CAS  Google Scholar 

  23. Moinova HR, Mulcahy RT (1998) An electrophile responsive element (EpRE) regulates beta-naphthoflavone induction of the human gamma-glutamylcysteinesynthetase regulatory subunit gene. Constitutive expression is mediated by an adjacent AP-1 site. J Biol Chem 273:14683–14689

    Article  PubMed  CAS  Google Scholar 

  24. Stachel I, Geismann C, Aden K, Deisinger F, Rosenstiel P, Schreiber S, Sebens S, Arlt A, Schaefer H (2014) Modulation of Nuclear factor E2 related factor-2 (Nrf2) activation by the stress response gene Immediate Early Response-3 (IER3) in colonic epithelial cells - a novel mechanism of cellular adaption to inflammatory stress. J Biol Chem 289:1917–1929

    Article  PubMed  CAS  Google Scholar 

  25. Trachootham D, Lu W, Ogasawara MA, Nilsa RD, Huang P (2008) Redox regulation of cell survival. Antioxid Redox Signal 10:1343–1374

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Kensler TW, Wakabayashi N, Biswal S (2007) Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47:89–116

    Article  PubMed  CAS  Google Scholar 

  27. Stępkowski TM, Kruszewski MK (2011) Molecular cross-talk between the NRF2/KEAP1 signaling pathway, autophagy, and apoptosis. Free Radica Biol Med 1186–1195

  28. Itoh K, Ishii T, Wakabayashi N, Yamamoto M (1999) Regulatory mechanisms of cellular response to oxidative stress. Free Radic Res 31:319–324

    Article  PubMed  CAS  Google Scholar 

  29. Bloom DA, Jaiswal AK (2003) Phosphorylation of Nrf2 at Ser40 by protein kinase C in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant response element-mediated NAD(P)H:quinone oxidoreductase-1 gene expression. J Biol Chem 278:44675–44682

    Article  PubMed  CAS  Google Scholar 

  30. Itoh K, Tong KI, Yamamoto M (2004) Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic Biol Med 36:1208–1213

    Article  PubMed  CAS  Google Scholar 

  31. Giudice A, Arra C, Turco MC (2010) Review of molecular mechanisms involved in the activation of the Nrf2-ARE signaling pathway by chemopreventive agents. Methods Mol Biol 647:37–74

    Article  PubMed  CAS  Google Scholar 

  32. Kansanen E, Jyrkkänen HK, Levonen AL (2012) Activation of stress signaling pathways by electrophilic oxidized and nitratedlipids. Free Radical Biol Med 52:973–982

    Article  CAS  Google Scholar 

  33. Longhin E, Gualtieri M, Capasso L, Bengalli R, Mollerup S, Holme JA, Øvrevik J, Casadei S, Di Benedetto C, Parenti P, Camatini M (2016) Physico-chemical properties and biological effects of diesel and biomass particles. Environ Pollut 215:366–375

    Article  PubMed  CAS  Google Scholar 

  34. Stone V, Johnston H, Clift MJ (2007) Air pollution, ultrafine and nanoparticle toxicology: cellular and molecular interactions. IEEE Trans Nanobiosci 6:331–340

    Article  Google Scholar 

  35. Kensler TW, Wakabayashi N (2010) Nrf2: friend or foe for chemoprevention? Carcinogenesis 31:90–99

    Article  PubMed  CAS  Google Scholar 

  36. Hayes JD, McMahon M, Chowdhry S, Dinkova-Kostova AT (2010) Cancer chemoprevention mechanisms mediated through the Keap1-Nrf2 pathway. Antioxid Redox Signal 13:1713–1748

    Article  PubMed  CAS  Google Scholar 

  37. Lau A, Villeneuve NF, Sun Z, Wong PK, Zhang DD (2008) Dual roles of Nrf2 in cancer. Pharmacol Res 58:262–270

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB (2010) Oxidative stress, inflammation, and cancer: how are they linked? Free Rad Biol Med 49:1603–1616

    Article  PubMed  CAS  Google Scholar 

  39. Dacie JV, Lewis SM (1975) Practical haematology, 5th edn. Churchill Livingstone, London, p. 628

    Google Scholar 

  40. Erkiliç S, Ozsaraç C, Küllü S (2003) Sputum cytology for the diagnosis of lung cancer: comparison of smear and modified cell block methods. Acta Cytol 47:1023–1027

    Article  PubMed  Google Scholar 

  41. Hughes HE, Dodds TC (1968) Handbook of diagnostic cytology. E&S Livingstone, Edinburgh, pp. 215–217

    Google Scholar 

  42. Adelroth E, Hedlund U, Blomberg A, Helleday R, Ledin MC, Levin JO, Pourazar J, Sandström T, Järvholm B (2006) Airway inflammation in iron ore miners exposed to dust and diesel exhaust. Eur Respir J 27:714–719

    Article  PubMed  CAS  Google Scholar 

  43. Grubb C (1988) Diagnostic cytopathology—a textbook and colour atlas. Churchill Livingstone, Edinburgh, pp 65–112

    Google Scholar 

  44. Pearse AGE (1962) histochemistry theoretical and applied. Little Brown, Boston

    Google Scholar 

  45. Rothe G, Valet G (1990) Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2,7-dichlorofluorescein. J Leukoc Biol 47:440–448

    Article  PubMed  CAS  Google Scholar 

  46. Cho HY, Kleeberger SR (2014) Noblesse oblige: NRF2 functions in the airways. Am J Respir Cell Mol Biol 50:844–847

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Li L, Dong H, Song E, Xu X, Liu L, Song Y (2014) Nrf2/ARE pathway activation, HO-1 and NQO1 induction by polychlorinated biphenyl quinone is associated with reactive oxygen species and PI3K/AKT signaling. Chem Biol Interact 209:56–67

    Article  PubMed  CAS  Google Scholar 

  48. Venugopal R, Jaiswal AK (1996) Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc Natl Acad Sci USA 93:14960–14965

    Article  PubMed  CAS  Google Scholar 

  49. Thimmulappa RK, Scollick C, Traore K, Yates M, Trush MA, Liby KT, Sporn MB, Yamamoto M, Kensler TW, Biswal S (2006) Nrf2-dependent protection from LPS induced inflammatory response and mortality by CDDO-Imidazolide. Biochem Biophys Res Commun 351:883–889

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Chen XL, Dodd G, Thomas S, Zhang X, Wasserman MA, Rovin BH, Kunsch C (2006) Activation of Nrf2/ARE pathway protects endothelial cells from oxidant injury and inhibits inflammatory gene expression. Am J Physiol Heart Circ Physiol 290:H1862-1870

    Google Scholar 

  51. Iizuka T, Ishii Y, Itoh K, Kiwamoto T, Kimura T, Matsuno Y, Morishima Y, Hegab AE, Homma S, Nomura A, Sakamoto T, Shimura M, Yoshida A, Yamamoto M, Sekizawa K (2005) Nrf2-deficient mice are highly susceptible to cigarette smoke-induced emphysema. Genes Cells 10:1113–1125

    Article  PubMed  CAS  Google Scholar 

  52. Asher G, Lotem J, Cohen B, Sachs L, Shaul Y (2001) Regulation of p53 stability and p53-dependent apoptosis by NADH quinone oxidoreductase 1. Proc Natl Acad Sci USA 98:1188–1193

    Article  PubMed  CAS  Google Scholar 

  53. Blake DJ, Singh A, Kombairaju P, Malhotra D, Mariani TJ, Tuder RM, Gabrielson E, Biswal S (2010) Deletion of Keap1 in the lung attenuates acute cigarette smoke-induced oxidative stress and inflammation. Am J Respir Cell Mol Biol 42:524–536

    Article  PubMed  CAS  Google Scholar 

  54. Deng X, Rui W, Zhang F, Ding W (2013) PM2.5 induces Nrf2-mediated defense mechanisms against oxidative stress by activating PIK3/AKT signaling pathway in human lung type II alveolar epithelial A549 cells. Cell Biol Toxicol 29:143–157

    Article  PubMed  CAS  Google Scholar 

  55. Shibata T, Ohta T, Tong KI, Kokubu A, Odogawa R, Tsuta K, Asamura H, Yamamoto M, Hirohashi S (2008) Cancer related mutations in NRF2 impair its recognition by Keap1-Cul3 E3 ligase and promotemalignancy. Proc Natl Acad Sci USA 105:13568–13573

    Article  PubMed  Google Scholar 

  56. Kim YR, Oh JE, Kim MS, Kang MR, Park SW, Han JY, Eom HS, Yoo NJ, Lee SH (2010) Oncogenic NRF2 mutations in squamous cell carcinomas of oesophagus and skin. J Pathol 220:446–451

    Article  PubMed  CAS  Google Scholar 

  57. Padmanabhan B, Tong KI, Ohta T, Nakamura Y, Scharlock M, Ohtsuji M, Kang MI, Kobayashi A, Yokoyama S, Yamamoto M (2006) Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer. Mol Cell 21:689–700

    Article  PubMed  CAS  Google Scholar 

  58. Singh A, Misra V, Thimmulappa RK, Lee H, Ames S, Hoque MO, Herman JG, Baylin SB, Sidransky D, Gabrielson E, Brock MV, Biswal S (2006) Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Med 3(10):e420

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Ohta T, Iijima K, Miyamoto M, Nakahara I, Tanaka H, Ohtsuji M, Suzuki T, Kobayashi A, Yokota J, Sakiyama T, Shibata T, Yamamoto M, Hirohashi S (2008) Loss of Keap1 function activates Nrf2 and provides advantages for lung cancer cell growth. Cancer Res 68:1303–1309

    Article  PubMed  CAS  Google Scholar 

  60. Choi EJ, Jung BJ, Lee SH, Yoo HS, Shin EA, Ko HJ, Chang S, Kim SY, Jeon SM (2017) A clinical drug library screen identifies clobetasol propionate as an NRF2 inhibitor with potential therapeutic efficacy in KEAP1 mutant lung cancer. Oncogene. https://doi.org/10.1038/onc.2017.153 (Epub ahead of print)

    Article  PubMed Central  PubMed  Google Scholar 

  61. Wang L, Chen Y, Sternberg P, Cai J (2008) Essential roles of the PI3 kinase/Akt pathway in regulating Nrf2-dependent antioxidant functions in the RPE. Invest Ophthalmol Vis Sci 49:1671–1678

    Article  PubMed  PubMed Central  Google Scholar 

  62. Zhang H, Liu H, Davies KJ, Sioutas C, Finch CE, Morgan TE, Forman HJ (2012) Nrf2-regulated phase II enzymes are induced by chronic ambient nanoparticle exposure in young mice with age-related impairments. Free Radical Biol Med 52:2038–2046

    Article  CAS  Google Scholar 

  63. Abbas I, Saint-Georges F, Billet S, Verdin A, Mulliez P, Shirali P, Garçon G (2009) Air pollution particulate matter (PM2.5)-induced gene expression of volatile organic compound and/or polycyclic aromatic hydrocarbon-metabolizing enzymes in an in vitro coculture lung model. Toxicol In Vitro 23:37–46

    Article  PubMed  CAS  Google Scholar 

  64. Elovaara E, Mikkola J, Stockmann-Juvala H, Luukkanen L, Keski-Hynnilä H, Kostiainen R, Pasanen M, Pelkonen O, Vainio H (2007) Polycyclic aromatic hydrocarbon (PAH) metabolizing enzyme activities in human lung, and their inducibility by exposure to naphthalene, phenanthrene, pyrene, chrysene, and benzo(a)pyrene as shown in the rat lung and liver. Arch Toxicol 81:169–182

    Article  PubMed  CAS  Google Scholar 

  65. Aoshiba K, Yasuda K, Yahui S, Tamaoki J, Nagai A (2001) Serine proteases increase oxidative stress in lung cells. Am J Physiol Lung Cell Mol Physiol 281:L556-L564

    Google Scholar 

  66. Shao MX, Nadel JA (2005) Dual oxidase1 dependent MUC5AC mucin expression in cultured human airway epithelial cells. Proc Natl Acad Sci USA 102:767–772

    Article  PubMed  CAS  Google Scholar 

  67. Fischer BM, Domowicz DA, Zheng S, Carter JL, McElvaney NG, Taggart C, Lehmann JR, Voynow JA, Ghio AJ (2009) Neutrophil elastase increases airway epithelial nonheme iron levels. Clin Transl Sci 2:333–339

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Zheng S, Byrd AS, Fischer BM, Grover AR, Ghio AJ, Voynow JA (2007) Regulation of MUC5AC expression by NAD(P)H:quinone oxidoreductase 1. Free Radical Biol Med 42:1398–1408

    Article  CAS  Google Scholar 

  69. Mukherjee S, Roychoudhury S, Siddique S, Banerjee M, Bhattacharya P, Lahiri T, Ray MR (2014) Respiratory symptoms, lung function decrement and chronic obstructive pulmonary disease in pre-menopausal Indian women exposed to biomass smoke. Inhalation Toxicol 26:866–872

    Article  CAS  Google Scholar 

  70. Malhotra D, Portales-Casamar E, Singh A, Srivastava S, Arenillas D, Happel C, Shyr C, Wakabayashi N, Kensler TW, Wasserman WW, Biswal S (2010) Global mapping of binding sites for Nrf2 identifies novel targets in cell survival response through ChIP-Seq profiling and network analysis. Nucleic Acids Res 38:5718–5734

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Arlt A, Bauer I, Schafmayer C, Tepel J, Muerkoster SS, Brosch M, Röder C, Kalthoff H, Hampe J, Moyer MP, Fölsch UR, Schäfe H (2009) Increased proteasome subunit protein expression and proteasome activity in colon cancer relate to an en-hanced activation of nuclear factor E2-related factor 2 (Nrf2). Oncogene 28:3983–3996

    Article  PubMed  CAS  Google Scholar 

  72. Liu Y, Yang H, Wen Y, Li B, Zhao Y, Xing J, Zhang M, Chen Y (2017) Nrf2 inhibits periodontal ligament stem cell apoptosis under excessive oxidative stress. Int J Mol Sci. https://doi.org/10.3390/ijms18051076

    Article  PubMed  PubMed Central  Google Scholar 

  73. Kiyohara C, Yoshimasu K, Takayama K, Nakanishi Y (2005) NQO1, MPO, and the risk of lung cancer: a HuGE review. Genet Med 7:463–478

    Article  PubMed  CAS  Google Scholar 

  74. Cadenas E (1995) Antioxidant and prooxidant functions of DT-diaphorase in quinone metabolism. Biochem Pharmacol 49:127–140

    Article  PubMed  CAS  Google Scholar 

  75. Butsri S, Kukongviriyapan V, Senggunprai L, Kongpetch S, Zeekpudsa P, Prawan A (2017) Downregulation of NAD(P)H:quinone oxidoreductase 1 inhibits proliferation, cell cycle and migration of cholangiocarcinoma cells. Oncol Lett 13:4540–4548

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Bergamaschi E, De Palma G, Mozzoni P, Vanni S, Vettori MV, Broeckaert F, Bernard A, Mutti A (2001) Polymorphism of quinone-metabolizing enzymes and susceptibility to ozone-induced acute effects. Am J Respir Crit Care Med 163:1426–1431

    Article  PubMed  CAS  Google Scholar 

  77. David G, Romieu I, Sienra-Monge JJ, Collins WJ, Ramirez-Auilar M, del Rio-Navarro BE, Reyes-Ruiz NI, Morris RW, Marzec JM, London SJ (2003) Nicotinamide adenine dinucleotide (phosphate) reduced: quinone oxidoreductase and glutathione s-transferase M1 polymorphisms and childhood asthma. Am J Respir Crit Care Med 168:1199–1204

    Article  PubMed  Google Scholar 

  78. Siegel D, Franklin WA, Ross D (1998) Immunohistochemical detection of NAD(P)H:quinone oxidoreductase in human lung and lung tumors. Clin Cancer Res 4:2065–2070

    PubMed  CAS  Google Scholar 

  79. Risse EK, Van’t Hof MA, Laurini RN, Vooijs PG (1985) Sputum cytology by the Saccomanno method in diagnosing lung malignancy. Diagn Cytopathol 1:286–291

    Article  PubMed  CAS  Google Scholar 

  80. Hubers AJ, Prinsen CF, Sozzi G, Witte BI, Thunnissen E (2013) Molecular sputum analysis for the diagnosis of lung cancer. Br J Cancer 109:530–537

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Ammanagi AS, Dombale VD, Miskin AT, Dandagi GL, Sangolli SS (2012) Sputum cytology in suspected cases of carcinoma of lung (Sputum cytology a poor man’s bronchoscopy!). Lung India 29:19–23

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Naeher LP, Smith KR, Brauer M, Chowdhury Z, Simpson C, Koenig JQ, Lipsett M, Zelikoff JD (2005) Critical review on the health effects of wood smoke. Funding for preparation of this report provided by the air health effects division. Health Canada, Ottawa

    Google Scholar 

  83. Nandakumar A, Gupta PC, Gangadharan P, Visweswara RN (2004) Development of an atlas of cancer in India. In: First all India report—2001–2002. National Cancer Registry Programme (ICMR), Bangalore, pp 15–17

    Google Scholar 

  84. Meyer ML, Potts-Kant EN, Ghio AJ, Fischer BM, Foster WM, Voynow JA (2012) NAD(P)H quinone oxidoreductase 1 regulates neutrophil elastase-induced mucous cell metaplasia. Am J Physiol Lung Cell Mol Physiol 303:L181-188

    Article  CAS  Google Scholar 

  85. Speer CP (2003) Inflammation and bronchopulmonary dysplasia. Semin Neonatol 8:29–38

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge the financial support received from the Central Pollution Control Board under Ministry of Environment and Forests, Government of India and World Health Organization, India.

Author information

Authors and Affiliations

  1. Department of Experimental Hematology, Chittaranjan National Cancer Institute, Kolkata, India

    Nandan Kumar Mondal, Hirak Saha, Bidisha Mukherjee & Manas Ranjan Ray

  2. Department of Cardiovascular and Thoracic Surgery, University of Louisville School of Medicine, Louisville, KY, USA

    Nandan Kumar Mondal

  3. Department of Physiology, University of Louisville School of Medicine, Health Sciences Center, A-1201, University of Louisville, Louisville, KY, 40202, USA

    Nandan Kumar Mondal & Neetu Tyagi

  4. Kabi Nazrul College, University of Burdwan, Bardhaman, West Bengal, India

    Nandan Kumar Mondal

Authors
  1. Nandan Kumar Mondal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hirak Saha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bidisha Mukherjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Neetu Tyagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Manas Ranjan Ray
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nandan Kumar Mondal.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest. All the authors actively participated in this study and were agreed with their authorship.

Ethical approval

All procedures performed in studies involving human participants (premenopausal women) were in accordance with the approval of the Institutional Ethics Committee (IEC) of Chittaranjan National Cancer Institute, Kolkata, West Bengal, India. The research was conducted according to the principles of the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mondal, N.K., Saha, H., Mukherjee, B. et al. Inflammation, oxidative stress, and higher expression levels of Nrf2 and NQO1 proteins in the airways of women chronically exposed to biomass fuel smoke. Mol Cell Biochem 447, 63–76 (2018). https://doi.org/10.1007/s11010-018-3293-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-018-3293-0

Keywords

Search

Navigation