Skip to main content

Advertisement

Log in

Reduction of DNA mismatch repair protein expression in airway epithelial cells of premenopausal women chronically exposed to biomass smoke

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Biomass burning is a major source of indoor air pollution in rural India. This study examined whether chronic inhalation of biomass smoke causes change in the DNA mismatch repair (MMR) pathway in the airway cells. For this, airway cells exfoliated in sputum were collected from 72 premenopausal nonsmoking rural women (median age 34 years) who cooked with biomass (wood, dung, crop residues) and 68 control women who cooked with cleaner fuel liquefied petroleum gas (LPG) for the past 5 years or more. The levels of particulate matters with diameters less than 10 and 2.5 μm (PM10 and PM2.5) in indoor air were measured by real-time aerosol monitor. Benzene exposure was monitored by measuring trans,trans-muconic acid (t,t-MA) in urine by high-performance liquid chromatography with ultraviolet detector. Generation of reactive oxygen species (ROS) and level of superoxide dismutase (SOD) in airway cells were measured by flow cytometry and spectrophotometry, respectively. Immunocytochemical assay revealed lower percentage of airway epithelial cells expressing MMR proteins mutL homolog 1 (MLH1) and mutS homolog 2 (MSH2) in biomass-using women compared to LPG-using controls. Women who cooked with biomass had 6.7 times higher level of urinary t,t-MA, twofold increase in ROS generation, and 31 % depletion of SOD. Indoor air of biomass-using households had three times more particulate matters than that of controls. ROS, urinary t,t-MA, and particulate pollution in biomass-using kitchen had negative correlation, while SOD showed positive correlation with MSH2 and MLH1 expression. It appears that chronic exposure to biomass smoke reduces MMR response in airway epithelial cells, and oxidative stress plays an important role in the process.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Akoum R, Ghaoui A, Brihi E, Ghabash M, Hajjar N (2009) Early-onset breast cancer in a Lebanese family with Lynch syndrome due to MSH2 gene mutation. Hered Cancer Clin Pract 7:10. doi:10.1186/1897-4287-7-10

    Article  Google Scholar 

  • Albalak R, Bruce N, McCracken JP, Smith KR, De Gallardo T (2001) Indoor respirable particulate matter concentrations from an open fire, improved cookstove, and LPG/open fire combination in a rural Guatemalan community. Environ Sci Technol 35:2650–2655

    Article  CAS  Google Scholar 

  • Bonner MR, Han D, Nie J, Rogerson P, Vena JE, Muti P, Trevisan M, Edge SB, Freudenheim JL (2005) Breast cancer risk and exposure in early life to polycyclic aromatic hydrocarbons using total suspended particulates as a proxy measure. Cancer Epidemiol Biomarkers Prev 14:53–60

    CAS  Google Scholar 

  • Boogaard PJ, van Sittert NJ (1996) Suitability of S-phenyl mercapturic acid and trans-trans-muconic acid as biomarkers for exposure to low concentrations of benzene. Environ Health Perspect 104:1151–1157

    CAS  Google Scholar 

  • Carrieri M, Tranfo G, Pigini D, Paci E, Salamon F, Scapellato ML, Fracasso ME, Manno M, Bartolucci GB (2010) Correlation between environmental and biological monitoring of exposure to benzene in petrochemical industry operators. Toxicol Lett 192:17–21. doi:10.1016/j.toxlet.2009.07.015

    Article  CAS  Google Scholar 

  • Chaksangchaichot P, Punyarit P, Petmitr S (2007) Novel hMSH2, hMSH6 and hMLH1 gene mutations and microsatellite instability in sporadic colorectal cancer. J Cancer Res Clin Oncol 133:65–70. doi:10.1007/s00432-006-0147-z

    Article  CAS  Google Scholar 

  • Chang CL, Marra G, Chauhan DP, Ha HT, Chang DK, Ricciardiello L, Randolph A, Carethers JM, Boland CR (2002) Oxidative stress inactivates the human DNA mismatch repair system. Am J Physiol Cell Physiol 283:C148-C154. doi: 10.1152/ajpcell.00422.2001

  • Christmann M, Tomicic MT, Roos WP, Kaina B (2003) Mechanisms of human DNA repair: an update. Toxicology 193:3–34. doi:10.1016/S0300-483×(03)00287-7

    Article  CAS  Google Scholar 

  • Chung A, Chang DPY, Kleeman MJ, Perry K, Cahill TA, Dutcher D, McDougall EM, Stroud K (2001) Comparison of real-time instruments used to monitor airborne particulate matter. J Air Waste Manag Assoc 51:109–120

    Article  CAS  Google Scholar 

  • Colnaghi R, Carpenter G, Volker M, O'Driscoll M (2011) The consequences of structural genomic alterations in humans: genomic disorders, genomic instability and cancer. Semin Cell Dev Biol 22:875–885. doi:10.1016/j.semcdb.2011.07.010

    Article  CAS  Google Scholar 

  • Colombino M, Cossu A, Arba A, Manca A, Curci A, Avallone A, Comella G, Botti G, Scintu F, Amoruso M, D'Abbicco D, d'Agnessa MR, Spanu A, Tanda F, Palmieri G (2003) Microsatellite instability and mutation analysis among southern Italian patients with colorectal carcinoma: detection of different alterations accounting for MLH1 and MSH2 inactivation in familial cases. Ann Oncol 14:1530–1536. doi: 10.1093/annonc/mdg402

    Google Scholar 

  • Cynthia A, Edwards RD, Johnson M, Zuk M, Rojas L, Jiménez RD, Riojas-Rodriguez H, Masera O (2008) Reduction in personal exposures to particulate matter and carbon monoxide as a result of the installation of a Patsari improved cook stove in Michoacan Mexico. Indoor Air 18: 93–105. doi: 10.1111/j.1600-0668.2007.00509.x

    Google Scholar 

  • Danielsen PH, Loft S, Kocbach A, Schwarze PE, Møller P (2009) Oxidative damage to DNA and repair induced by Norwegian wood smoke particles in human A549 and THP-1 cell lines. Mutat Res 674:116–122. doi:10.1016/j.mrgentox.2008.10.014

    Article  CAS  Google Scholar 

  • Ducos P, Gaudin R, Robert A, Francin JM, Marie C (1990) Improvement in HPLC analysis of urinary trans, trans-muconic acid, a promising substitute for phenol in the assessment of benzene exposure. Int Arch Occup Environ Health 62:529–534. doi:10.1007/BF00381185

    Article  CAS  Google Scholar 

  • Dutta A, Mukherjee B, Das D, Banerjee A, Ray MR (2011) Hypertension with elevated levels of oxidized low-density lipoprotein and anticardiolipin antibody in the circulation of premenopausal Indian women chronically exposed to biomass smoke during cooking. Indoor Air 21:165–176. doi:10.1111/j.1600-0668.2010.00694.x

    Article  CAS  Google Scholar 

  • Fishel R, Kolodner RD (1995) Identification of mismatch repair genes and their role in the development of cancer. Curr Opin Genet Dev 5:382–395. doi:10.1016/0959-437×(95)80055-7

    Article  CAS  Google Scholar 

  • Franco R, Schoneveld O, Georgakilas AG, Panayiotidis MI (2008) Oxidative stress, DNA methylation and carcinogenesis. Cancer Lett 266:6–11. doi:10.1016/j.canlet.2008.02.026

    Article  CAS  Google Scholar 

  • Fubini B, Fenoglio I, Ceschino R, Ghiazza M, Martra G, Tomatis M, Borm P, Schins R, Bruch J (2004) Relationship between the state of the surface of four commercial quartz flours and their biological activity in vitro and in vivo. Int J Hyg Environ Health 207:89–104

    Article  CAS  Google Scholar 

  • Fustinoni S, Buratti M, Campo L, Colombi A, Consonni D, Pesatori AC, Bonzini M, Farmer P, Garte S, Valerio F, Merlo DF, Bertazzi PA (2005) Urinary t, t-muconic acid, S-phenylmercapturic acid and benzene as biomarkers of low benzene exposure. Chem Biol Interact 153–154:253–256. doi:10.1016/j.cbi.2005.03.031

    Article  Google Scholar 

  • Ghosh A, Ghosh S, Maiti GP, Sabbir MG, Alam N, Sikdar N, Roy B, Roychoudhury S, Panda CK (2009) SH3GL2 and CDKN2A/2B loci are independently altered in early dysplastic lesions of head and neck: correlation with HPV infection and tobacco habit. J Pathol 217:408–419. doi:10.1002/path.2464

    Article  CAS  Google Scholar 

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

  • Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70. doi:10.1016/S0092-8674(00)81683-9

    Article  CAS  Google Scholar 

  • Hansen LT, Thykjaer T, Ørntoft TF, Rasmussen LJ, Keller P, Spang-Thomsen M, Edmonston TB, Schmutte C, Fishel R, Petersen LN (2003) The role of mismatch repair in small-cell lung cancer cells. Eur J Cancer 39:1456–1467. doi:10.1016/S0959-8049(03)00306-X

    Article  CAS  Google Scholar 

  • Hoeijmakers JH (2001) Genome maintenance mechanisms for preventing cancer. Nature 411:366–374. doi:10.1038/35077232

    Article  CAS  Google Scholar 

  • Hughes HE, Dodds TC (1968) Handbook of diagnostic cytology. Churchill Livingstone, Edinburgh, pp 607–618

    Google Scholar 

  • Kámory E, Kolacsek O, Ottó S, Csuka O (2003) hMLH1 and hMSH2 somatic inactivation mechanisms in sporadic colorectal cancer patients. Pathol Oncol Res 9:236–241

    Article  Google Scholar 

  • Karihtala P, Winqvist R, Syväoja JE, Kinnula VL, Soini Y (2006) Increasing oxidative damage and loss of mismatch repair enzymes during breast carcinogenesis. Eur J Cancer 42:2653–2659. doi:10.1016/j.ejca.2006.05.037

    Article  CAS  Google Scholar 

  • Kinsella TJ (2009) Coordination of DNA mismatch repair and base excision repair processing of chemotherapy and radiation damage for targeting resistant cancers. Clin Cancer Res 15:1853–1859. doi:10.1158/1078-0432.CCR-08-1307

    Article  CAS  Google Scholar 

  • Kleeman MJ, Riddle SG, Robert MA, Jakober CA, Fine PM, Hays MD, Schauer JJ, Hannigan MP (2009) Source apportionment of fine (PM1.8) and ultrafine (PM0.1) airborne particulate matter during a severe winter pollution episode. Environ Sci Technol 43:272–279

    Article  CAS  Google Scholar 

  • Knaapen AM, Borm PJ, Albrecht C, Schins RP (2004) Inhaled particles and lung cancer. Part A: mechanisms. Int J Cancer 109:799–809. doi:10.1002/ijc.11708

    Article  CAS  Google Scholar 

  • Kolodner RD, Putnam CD, Myung K (2002) Maintenance of genome stability in Saccharomyces cerevisiae. Science 297:552–557. doi:10.1126/science.1075277

    Article  CAS  Google Scholar 

  • Lehocky AH, Williams PL (1996) Comparison of respirable samplers to direct-reading real time aerosol monitors for measuring coal dust. Am Ind Hyg Assoc J 57:1013–1018

    Article  CAS  Google Scholar 

  • Lengauer C, Kinzler KW, Vogelstein B (1998) Genetic instabilities in human cancers. Nature 396:643–649. doi:10.1038/25292

    Article  CAS  Google Scholar 

  • Li N, Sioutas C, Cho A, Schmitz D, Misra C, Sempf J, Wang M, Oberley T, Froines J, Nel A (2003) Ultrafine particulate pollutants induce oxidative stress and mitochondrial damage. Environ Health Perspect 111:455–460. doi:10.1289/ehp.6000

    Article  CAS  Google Scholar 

  • Lo YL, Hsiao CF, Jou YS, Chang GC, Tsai YH, Su WC, Chen KY, Chen YM, Huang MS, Hsieh WS, Chen CJ, Hsiung CA (2011) Polymorphisms of MLH1 and MSH2 genes and the risk of lung cancer among never smokers. Lung Cancer 72:280–286. doi:10.1016/j.lungcan.2010.10.009

    Article  Google Scholar 

  • 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. doi:10.1016/j.mrgentox.2010.02.006

    Article  CAS  Google Scholar 

  • Mukherjee B, Dutta A, Roychoudhury S, Ray MR (2013) Chronic inhalation of biomass smoke is associated with DNA damage in airway cells: involvement of particulate pollutants and benzene. J Appl Toxicol 33:281–289. doi:10.1002/jat.1748

    Article  Google Scholar 

  • Naeher LP, Brauer M, Lipsett M, Zelikoff J, Simpson CD, Koenig JQ, Smith KR (2007) Woodsmoke health effects: a review. Inhal Toxicol 19:67–106. doi:10.1080/08958370600985875

    Article  CAS  Google Scholar 

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

  • O'Brien V, Brown R (2006) Signalling cell cycle arrest and cell death through the MMR system. Carcinogenesis 27:682–692. doi:10.1093/carcin/bgi298

    Article  Google Scholar 

  • Paoletti F, Aldinucci D, Mocali A, Caparrini A (1986) A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Anal Biochem 154:536–541. doi:10.1016/0003-2697(86)90026-6

    Article  CAS  Google Scholar 

  • Paz-y-Miño C, López-Cortés A, Arévalo M, Sánchez ME (2008) Monitoring of DNA damage in individuals exposed to petroleum hydrocarbons in Ecuador. Ann N Y Acad Sci 1140:121–128. doi:10.1196/annals.1454.013

    Article  Google Scholar 

  • Ramachandran G, Adgate JL, Pratt GC, Sexton K (2003) Characterizing indoor and outdoor 15 minute average PM2.5 concentrations in urban neighbourhoods. Aerosol Sci Technol 37:33–45

    Article  CAS  Google Scholar 

  • Reddy TS, Guleria R, Sinha S, Sharma SK, Pande JN (2004) Domestic cooking fuel and lung functions in healthy non-smoking women. Indian J Chest Dis Allied Sci 46:85–90

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Sági J, Chenna A, Hang B, Singer B (1998) A single cyclic p-benzoquinone adduct can destabilize a DNA oligonucleotide duplex. Chem Res Toxicol 11:329–334. doi:10.1021/tx9701992

    Article  Google Scholar 

  • Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73:39–85. doi:10.1146/annurev.biochem.73.011303.073723

    Article  CAS  Google Scholar 

  • Scartozzi M, Franciosi V, Campanini N, Benedetti G, Barbieri F, Rossi G, Berardi R, Camisa R, Silva RR, Santinelli A, Ardizzoni A, Crinò L, Rindi G, Cascinu S (2006) Mismatch repair system (MMR) status correlates with response and survival in non-small cell lung cancer (NSCLC) patients. Lung Cancer 53:103–109. doi:10.1016/j.lungcan.2006.03.008

    Article  Google Scholar 

  • Siddiqui AR, Lee K, Bennett D, Yang X, Brown KH, Bhutta ZA, Gold EB (2009) Indoor carbon monoxide and PM2.5 concentrations by cooking fuels in Pakistan. Indoor Air 19:75–82. doi:10.1111/j.1600-0668.2008.00563.x

    Article  CAS  Google Scholar 

  • Sinha SN, Kulkarni PK, Shah SH, Desai NM, Patel GM, Mansuri MM, Saiyed HN (2006) Environmental monitoring of benzene and toluene produced in indoor air due to combustion of solid biomass fuels. Sci Total Environ 357:280–287. doi:10.1016/j.scitotenv.2005.08.011

    Article  CAS  Google Scholar 

  • Stasikowska-Kanicka O, Stawerski P, Wagrowska-Danilewicz M, Danilewicz M (2009) Immunohistochemical analysis of hMLH1 and hMSH2 proteins in serous ovarian tumours. Pol J Pathol 60:174–178

    Google Scholar 

  • Vilkin A, Niv Y, Nagasaka T, Morgenstern S, Levi Z, Fireman Z, Fuerst F, Goel A, Boland CR (2009) Microsatellite instability, MLH1 promoter methylation, and BRAF mutation analysis in sporadic colorectal cancers of different ethnic groups in Israel. Cancer 115:760–769. doi:10.1002/cncr.24019

    Article  CAS  Google Scholar 

  • Vlaykova T, Mitkova A, Stancheva G, Kadiyska T, Gulubova M, Yovchev Y, Cirovski G, Chilingirov P, Damyanov D, Kremensky I, Mitev V, Kaneva R (2011) Microsatellite instability and promoter hypermethylation of MLH1 and MSH2 in patients with sporadic colorectal cancer. J BUON 16:265–273

    CAS  Google Scholar 

  • Voelkel K, Krug HF, Diabate S (2003) Formation of reactive oxygen species in rat epithelial cells upon stimulation with fly ash. J Biosci 28:51–55. doi:10.1007/BF02970131

    Article  CAS  Google Scholar 

  • Wang YC, Lu YP, Tseng RC, Lin RK, Chang JW, Chen JT, Shih CM, Chen CY (2003) Inactivation of hMLH1 and hMSH2 by promoter methylation in primary non-small cell lung tumors and matched sputum samples. J Clin Invest 111:887–895. doi:10.1172/JCI200315475

    Article  CAS  Google Scholar 

  • Yeager ME, Golpon HA, Voelkel NF, Tuder RM (2002) Microsatellite mutational analysis of endothelial cells within plexiform lesions from patients with familial, pediatric, and sporadic pulmonary hypertension. Chest 121:61S

    Google Scholar 

  • Zhang J, Smith KR (2003) Indoor air pollution: a global health concern. Br Med Bull 68:209–225. doi:10.1093/bmb/ldg029

    Article  CAS  Google Scholar 

  • Zighelboim I, Goodfellow PJ, Gao F, Gibb RK, Powell MA, Rader JS, Mutch DG (2007) Microsatellite instability and epigenetic inactivation of MLH1 and outcome of patients with endometrial carcinomas of the endometrioid type. J Clin Oncol 25:2042–2048. doi:10.1200/JCO.2006.08.2107

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The study was supported by funds received from Central Pollution Control Board under the Ministry of Environment and Forests, Government of India and Council of Scientific and Industrial Research, India.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Manas Ranjan Ray.

Additional information

Responsible Editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mukherjee, B., Dutta, A., Chowdhury, S. et al. Reduction of DNA mismatch repair protein expression in airway epithelial cells of premenopausal women chronically exposed to biomass smoke. Environ Sci Pollut Res 21, 2826–2836 (2014). https://doi.org/10.1007/s11356-013-2218-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-013-2218-4

Keywords

Navigation