Air toxics and epigenetic effects: Ozone altered microRNAs in the sputum of human subjects

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 306, Issue 12, 2014, Pages

  Fry, Rebecca C ^a,b,c   Rager, Julia E ^a   Bauer, Rebecca ^b   Sebastian, Elizabeth ^a   Peden, David B ^b,d   Jaspers, Ilona ^b,d   Alexis, Neil E ^b,d  

^a University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c IL   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Air pollution; Epigenetics; Humans; MicroRNA; Ozone

Indexed keywords

MICRORNA; MICRORNA 132; MICRORNA 143; MICRORNA 145; MICRORNA 199A; MICRORNA 199B 5P; MICRORNA 222; MICRORNA 223; MICRORNA 25; MICRORNA 424; MICRORNA 582 5P; OZONE; UNCLASSIFIED DRUG;

ADULT; AIR POLLUTANT; ARTICLE; CORRELATION ANALYSIS; EPIGENETICS; EXPOSURE; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; HUMAN; HUMAN EXPERIMENT; IMMUNE RESPONSE; INFLAMMATION; MALE; MICROARRAY ANALYSIS; NORMAL HUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPUTUM;

AIR POLLUTION; EPIGENETICS; HUMANS; MICRORNA; OZONE;

ADOLESCENT; ADULT; AIR; AIR POLLUTANTS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION PROFILING; HUMANS; INFLAMMATION; MALE; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OZONE; RESPIRATORY SYSTEM; RNA, MESSENGER; YOUNG ADULT;

EID: 84902665815     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00348.2013     Document Type: Article

References (45)

1. Alexis N, Urch B, Tarlo S, Corey P, Pengelly D, O'Byrne P, Silverman F. Cyclooxygenase metabolites play a different role in ozone-induced pulmonary function decline in asthmatics compared to normals. Inhal Toxicol 12: 1205-1224, 2000.
2. Alexis NE, Becker S, Bromberg PA, Devlin RB, Peden DB. Circulating cd11b expression correlates with the neutrophil response and airway mcd14 expression is enhanced following ozone exposure in humans. Clin Immunol 111: 126-131, 2004.
3. Alexis NE, Zhou H, Lay JC, Harris B, Hernandez ML, Lu TS, Bromberg PA, Diaz-Sanchez D, Devlin RB, Kleeberger SR, Peden DB. The glutathione-S-transferase mu 1 null genotype modulates ozone-induced airway inflammation in human subjects. J Allergy Clin Immunol 124: 1222-1228, 2009.
4. Alexis NE, Lay JC, Hazucha M, Harris B, Hernandez ML, Bromberg PA, Kehrl H, Diaz-Sanchez D, Kim C, Devlin RB, Peden DB. Lowlevel ozone exposure induces airways inflammation and modifies cell surface phenotypes in healthy humans. Inhal Toxicol 22: 593-600, 2010.
5. Alexis NE, Lay JC, Zhou H, Kim CS, Hernandez ML, Kehrl H, Hazucha MJ, Devlin RB, Diaz-Sanchez D, Peden DB. The glutathione-S-transferase mu 1 (gstm1) null genotype and increased neutrophil response to low-level ozone (0.06 ppm). J Allergy Clin Immunol 131: 610-612, 2013.
6. Allantaz F, Cheng DT, Bergauer T, Ravindran P, Rossier MF, Ebeling M, Badi L, Reis B, Bitter H, D'Asaro M, Chiappe A, Sridhar S, Pacheco GD, Burczynski ME, Hochstrasser D, Vonderscher J, Matthes T. Expression profiling of human immune cell subsets identifies miRNAmRNA regulatory relationships correlated with cell type specific expression. PLoS One 7: e29979, 2012.
7. Baccarelli A, Wright RO, Bollati V, Tarantini L, Litonjua AA, Suh HH, Zanobetti A, Sparrow D, Vokonas PS, Schwartz J. Rapid DNA methylation changes after exposure to traffic particles. Am J Respir Crit Care Med 179: 572-578, 2009.
8. Belinsky SA, Snow SS, Nikula KJ, Finch GL, Tellez CS, Palmisano WA. Aberrant cpg island methylation of the p16(ink4a) and estrogen receptor genes in rat lung tumors induced by particulate carcinogens. Carcinogenesis 23: 335-339, 2002.
9. Bollati V, Baccarelli A, Hou L, Bonzini M, Fustinoni S, Cavallo D, Byun HM, Jiang J, Marinelli B, Pesatori AC, Bertazzi PA, Yang AS. Changes in DNA methylation patterns in subjects exposed to low-dose benzene. Cancer Res 67: 876-880, 2007.
10. Bollati V, Marinelli B, Apostoli P, Bonzini M, Nordio F, Hoxha M, Pegoraro V, Motta V, Tarantini L, Cantone L, Schwartz J, Bertazzi PA, Baccarelli A. Exposure to metal-rich particulate matter modifies the expression of candidate microRNAs in peripheral blood leukocytes. Environ Health Perspect 118: 763-768, 2010.
11. Breton CV, Byun HM, Wenten M, Pan F, Yang A, Gilliland FD. Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. Am J Respir Crit Care Med 180: 462-467, 2009.
12. Calvano SE, Xiao W, Richards DR, Felciano RM, Baker HV, Cho RJ, Chen RO, Brownstein BH, Cobb JP, Tschoeke SK, Miller-Graziano C, Moldawer LL, Mindrinos MN, Davis RW, Tompkins RG, Lowry SF; Inflamm and Host Response to Injury Large Scale Collab. Res. Program. A network-based analysis of systemic inflammation in humans. Nature 437: 1032-1037, 2005.
13. Downey T. Analysis of a multifactor microarray study using Partek genomics solution. Methods Enzymol 411: 256-270, 2006.
14. Edgar R, Domrachev M, Lash AE. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210, 2002.
15. Farraj AK, Hazari MS, Haykal-Coates N, Lamb C, Winsett DW, Ge Y, Ledbetter AD, Carll AP, Bruno M, Ghio A, Costa DL. ST depression, arrhythmia, vagal dominance, and reduced cardiac micro-RNA in particulate-exposed rats. Am J Respir Cell Mol Biol 44: 185-196, 2011.
16. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of posttranscriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9: 102-114, 2008.
17. Fry RC, Rager JE, Zhou H, Zou B, Brickey JW, Ting J, Lay JC, Peden DB, Alexis NE. Individuals with increased inflammatory response to ozone demonstrate muted signaling of immune cell trafficking pathways. Respir Res 13: 89, 2012.
18. Izzotti A, Calin GA, Arrigo P, Steele VE, Croce CM, De Flora S. Downregulation of microRNA expression in the lungs of rats exposed to cigarette smoke. FASEB J 23: 806-812, 2009.
19. Jardim MJ, Fry RC, Jaspers I, Dailey L, Diaz-Sanchez D. Disruption of microRNA expression in human airway cells by diesel exhaust particles is linked to tumorigenesis-associated pathways. Environ Health Perspect 117: 1745-1751, 2009.
20. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet 8: 253-262, 2007.
21. Johnnidis JB, Harris MH, Wheeler RT, Stehling-Sun S, Lam MH, Kirak O, Brummelkamp TR, Fleming MD, Camargo FD. Regulation of progenitor cell proliferation and granulocyte function by miRNA-223. Nature 451: 1125-1129, 2008.
22. Kim CS, Alexis NE, Rappold AG, Kehrl H, Hazucha MJ, Lay JC, Schmitt MT, Case M, Devlin RB, Peden DB, Diaz-Sanchez D. Lung function and inflammatory responses in healthy young adults exposed to 0.06 ppm ozone for 66 h. Am J Respir Crit Care Med 183: 1215-1221, 2011.
23. Lagos D, Pollar G, Henderson S, Gartrix G, Fabani M, Milne RSB, Gotch F, Boshoff C. Mir-132 regulates antiviral innate immunity through suppression of the p300 transcriptional co-activator. Nat Cell Biol 12: 513-530, 2010.
24. Lay JC, Alexis NE, Kleeberger SR, Roubey RA, Harris BD, Bromberg PA, Hazucha MJ, Devlin RB, Peden DB. Ozone enhances markers of innate immunity and antigen presentation on airway monocytes in healthy individuals. J Allergy Clin Immunol 120: 719-722, 2007.
25. Lindsay MA. MicroRNAs and the immune response. Trends Immunol 29: 343-351, 2008.
26. Lippmann M. Health effects of tropospheric ozone. Environ Sci Technol 25: 1954-1962, 1991.
27. Lippmann M. Health effects of tropospheric ozone: review of recent research findings and their implications to ambient air quality standards. J Expo Anal Environ Epidemiol 3: 103-129, 1993.
28. Liu J, Ballaney M, Al-alem U, Quan C, Jin X, Perera F, Chen LC, Miller RL. Combined inhaled diesel exhaust particles and allergen exposure alter methylation of T helper genes and IgE production in vivo. Toxicol Sci 102: 76-81, 2008.
29. Lu TX, Rothenberg ME. Diagnostic, functional, and therapeutic roles of microRNA in allergic diseases. J Allergy Clin Immunol 132: 3-13, 2013.
30. Madrigano J, Baccarelli A, Mittleman MA, Wright RO, Sparrow D, Vokonas PS, Tarantini L, Schwartz J. Prolonged exposure to particulate pollution, genes associated with glutathione pathways, and DNA methylation in a cohort of older men. Environ Health Perspect 119: 977-982, 2011.
31. Mattick JS, Makunin IV. Non-coding RNA. Hum Mol Genet 15: R17-R29, 2006.
32. Ollinger J, Bowen B, Wiedmann M, Boor KJ, Bergholz TM. Listeria monocytogenes sigmaB modulates Prfa-mediated virulence factor expression. Infect Immun 77: 2113-2124, 2009.
33. Papadopoulos GL, Reczko M, Simossis VA, Sethupathy P, BC, Hatzigeorgiou AG. The database of experimentally supported targets: A functional update of TarBase. Nucleic Acids Res 37: D155-D158, 2009.
34. Pavanello S, Bollati V, Pesatori AC, Kapka L, Bolognesi C, Bertazzi PA, Baccarelli A. Global and gene-specific promoter methylation changes are related to anti-B[a]PDE-DNA adduct levels and influence micronuclei levels in polycyclic aromatic hydrocarbon-exposed individuals. Int J Cancer 125: 1692-1697, 2009.
35. Pottelberge GR, Mestdagh P, Bracke KR, Thas O, Durme YM, Joos GF, Vandesompele J, Brusselle GG. MicroRNA expression in induced sputum of smokers and patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 183: 898-906, 2011.
36. Rager JE, Smeester L, Jaspers I, Sexton KG, Fry RC. Epigenetic changes induced by air toxics: formaldehyde exposure alters miRNA expression profiles in human lung cells. Environ Health Perspect 119: 494-500, 2011.
37. Rager JE, Moeller BC, Doyle-Eisele M, Kracko D, Swenberg JA, Fry RC. Formaldehyde and epigenetic alterations: microRNA changes in the nasal epithelium of nonhuman primates. Environ Health Perspect 121: 339-344, 2013.
38. Roa WH, Kim JO, Razzak R, Du H, Guo L, Singh R, Gazala S, Ghosh S, Wong E, Joy AA, Xing JZ, Bedard EL. Sputum microRNA profiling: a novel approach for the early detection of non-small cell lung cancer. Clin Invest Med 35: E271, 2012.
39. Sciuto AM, Phillips CS, Orzolek LD, Hege AI, Moran TS, Dillman JF 3rd. Genomic analysis of murine pulmonary tissue following carbonyl chloride inhalation. Chem Res Toxicol 18: 1654-1660, 2005.
40. Sood A, Petersen H, Blanchette CM, Meek P, Picchi MA, Belinsky SA, Tesfaigzi Y. Wood smoke exposure and gene promoter methylation are associated with increased risk for COPD in smokers. Am J Respir Crit Care Med 182: 1098-1104, 2010.
41. Storey JD. The positive false discovery rate: a Bayesian interpretation and the q-value. Ann Statist 31: 2013-2035, 2003.
42. Urbich C, Kuehbacher A, Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res 79: 581-588, 2008.
43. Xiao F, Zuo Z, Cia G, Kang S, Gao X, Li T. miRecords: an integrated resource for microRNA-target interactions. Nucleic Acids Res 37: D105-D110, 2009.
44. Yauk C, Polyzos A, Rowan-Carroll A, Somers CM, Godschalk RW, Van Schooten FJ, Berndt ML, Pogribny IP, Koturbash I, Williams A, Douglas GR, Kovalchuk O. Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. Proc Natl Acad Sci USA 105: 605-610, 2008.
45. Zhang AH, Bin HH, Pan XL, Xi XG. Analysis of p16 gene mutation, deletion and methylation in patients with arseniasis produced by indoor unventilated-stove coal usage in Guizhou, China. J Toxicol Environ Health 70: 970-975, 2007.