MicroRNAs as potential signatures of environmental exposure or effect: A systematic review

Environmental Health Perspectives

Volumn 123, Issue 5, 2015, Pages 399-411

  Vrijens, Karen ^a   Bollati, Valentina ^b   Nawrot, Tim S ^a,c  

^a HASSELT UNIVERSITY   (Belgium)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; ALUMINUM SULFATE; ARSENIC; CHEMICAL AGENT; CIGARETTE SMOKE; CYCLONITE; DIETHYLSTILBESTROL; ENDOCRINE DISRUPTOR; MICRORNA; MICRORNA 10B; MICRORNA 128; MICRORNA 135B; MICRORNA 142; MICRORNA 143; MICRORNA 146A; MICRORNA 149; MICRORNA 155; MICRORNA 181A; MICRORNA 203; MICRORNA 205; MICRORNA 206; MICRORNA 21; MICRORNA 222; MICRORNA 223; MICRORNA 340; MICRORNA 638; MICRORNA 9; MICRORNA 92B; NANOPARTICLE; PERFLUOROOCTANOIC ACID; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; MESSENGER RNA;

AIR POLLUTION; CELL PROLIFERATION; DOWN REGULATION; ENVIRONMENTAL EXPOSURE; GENE EXPRESSION; GENETIC ASSOCIATION; HUMAN; OXIDATIVE STRESS; PARTICULATE MATTER; PRIORITY JOURNAL; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; SMOKING; SYSTEMATIC REVIEW; UPREGULATION; ANALYSIS;

BIOMARKERS; ENVIRONMENTAL EXPOSURE; HUMANS; MICRORNAS; RNA, MESSENGER;

EID: 84929466417     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1408459     Document Type: Review

References (180)

1. Ambros V. 2004. The functions of animal microRNAs. Nature 431(7006):350–355.
2. Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X, et al. 2003. A uniform system for microRNA annotation. RNA 9(3):277–279.
3. Avissar-Whiting M, Veiga KR, Uhl KM, Maccani MA, Gagne LA, Moen EL, et al. 2010. Bisphenol A exposure leads to specific microRNA alterations in placental cells. Reprod Toxicol 29(4):401–406.
4. Badrnya S, Baumgartner R, Assinger A. 2014. Smoking alters circulating plasma microvesicle pattern and microRNA signatures. Thromb Haemost 112(1):128–136.
5. Bai S, Nasser MW, Wang B, Hsu SH, Datta J, Kutay H, et al. 2009. MicroRNA-122 inhibits tumorigenic properties of hepatocellular carcinoma cells and sensitizes these cells to sorafenib. J Biol Chem 284(46):32015–32027.
6. Balansky R, Longobardi M, Ganchev G, Iltcheva M, Nedyalkov N, Atanasov P, et al. 2013. Transplacental clastogenic and epigenetic effects of gold nanoparticles in mice. Mutat Res 751–752:42–48.
7. Beezhold K, Liu J, Kan H, Meighan T, Castranova V, Shi X, et al. 2011. miR-190-mediated downregulation of PHLPP contributes to arsenic-induced Akt activation and carcinogenesis. Toxicol Sci 123(2):411-420.
8. Bisso A, Faleschini M, Zampa F, Capaci V, de Santa J, Santarpia L, et al. 2013. Oncogenic miR-181a/b affect the DNA damage response in aggressive breast cancer. Cell Cycle 12(11):1679–1687.
9. Bleck B, Grunig G, Chiu A, Liu M, Gordon T, Kazeros A, et al. 2013. MicroRNA-375 regulation of thymic stromal lymphopoietin by diesel exhaust particles and ambient particulate matter in human bronchial epithelial cells. J Immunol 190(7):3757–3763.
10. Bollati V, Marinelli B, Apostoli P, Bonzini M, Nordio F, Hoxha M, et al. 2010. Exposure to metal-rich particulate matter modifies the expression of candidate microRNAs in peripheral blood leukocytes. Environ Health Perspect 118:763–768; doi:10.1289/ehp.0901300.
11. Bourdon JA, Saber AT, Halappanavar S, Jackson PA, Wu D, Hougaard KS, et al. 2012. Carbon black nanoparticle intratracheal installation results in large and sustained changes in the expression of miR-135b in mouse lung. Environ Mol Mutagen 53(6):462–468.
12. Brunekreef B, Holgate ST. 2002. Air pollution and health. Lancet 360:1233–1242.
13. Busk PK, Cirera S. 2010. MicroRNA profiling in early hypertrophic growth of the left ventricle in rats. Biochem Biophys Res Commun 396(4):989–993.
14. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, et al. 2005. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med 353(17):1793–1801.
15. Camacho IA, Nagarkatti M, Nagarkatti PS. 2004. Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on maternal immune response during pregnancy. Arch Toxicol 78(5):290–300.
16. Caramuta S, Egyházi S, Rodolfo M, Witten D, Hansson J, Larsson C, et al. 2010. MicroRNA expression profiles associated with mutational status and survival in malignant melanoma. J Invest Dermatol 130(8):2062–2070.
17. Castranova V. 2011. Overview of current toxicological knowledge of engineered nanoparticles. J Occup Environ Med 53(6 suppl):S14–S17.
18. Ceccatelli R, Faass O, Schlumpf M, Lichtensteiger W. 2006. Gene expression and estrogen sensitivity in rat uterus after developmental exposure to the polybrominated diphenylether PBDE 99 and PCB. Toxicology 220(2–3):104–116.
19. Chang S, Wang RH, Akagi K, Kim KA, Martin BK, Cavallone L, et al. 2011. Tumor suppressor BRCA1 epigenetically controls oncogenic microRNA-155. Nat Med 17(10):1275–1282.
20. Cheng L, Sharples RA, Scicluna BJ, Hill AF. 2014. Exosomes provide a protective and enriched source of miRNA for biomarker profiling compared to intracellular and cell-free blood. J Extracell Vesicles 3:23743; doi:10.3402/jev.v3.23743.
21. Cheng Y, Liu X, Zhang S, Lin Y, Yang J, Zhang C. 2009. MicroRNA-21 protects against the H2O2-induced injury on cardiac myocytes via its target gene PDCD4. J Mol Cell Cardiol 47(1):5–14.
22. Cheng Y, Zhang C. 2010. MicroRNA-21 in cardiovascular disease. J Cardiovasc Transl Res 3(3):251–255.
23. Chevrier J, Gunier RB, Bradman A, Holland NT, Calafat AM, Eskenazi B, et al. 2013. Maternal urinary bisphenol A during pregnancy and maternal and neonatal thyroid function in the CHAMACOS study. Environ Health Perspect 121:138–144; doi:10.1289/ehp.1205092.
24. Cho NH, Chan JC, Jang HC, Lim S, Kim HL, Choi SH. 2009. Cigarette smoking is an independent risk factor for type 2 diabetes: a four-year communitybased prospective study. Clin Endocrinol (Oxf) 71(5):679–685.
25. Clay CC, Maniar-Hew K, Gerriets JE, Wang TT, Postlethwait EM, Evans MJ, et al. 2014. Early life ozone exposure results in dysregulated innate immune function and altered microRNA expression in airway epithelium. PLoS One 9(3):e90401; doi:10.1371/journal.pone.0090401.
26. Contreras J, Rao DS. 2012. MicroRNAs in inflammation and immune responses. Leukemia 26(3):404–413.
27. Dai Y, Sui W, Lan H, Yan Q, Huang H, Huang Y. 2009. Comprehensive analysis of microRNA expression patterns in renal biopsies of lupus nephritis patients. Rheumatol Int 29(7):749–754.
28. Davis JL, Wani AH, O’Neal BR, Hansen LD. 2004. RDX biodegradation column study: comparison of electron donors for biologically induced reductive transformation in groundwater. J Hazard Mater 112(1–2):45–54.
29. Deng Q, Huang S, Zhang X, Zhang W, Feng J, Wang T, et al. 2014. Plasma microRNA expression and micronuclei frequency in workers exposed to polycyclic aromatic hydrocarbons. Environ Health Perspect 122:719–725; doi:10.1289/ehp.1307080.
30. D’hulst AI, Bracke KR, Maes T, De Bleecker JL, Pauwels RA, Joos GF, et al. 2006. Role of tumour necrosis factor-α receptor P75 in cigarette smoke–induced pulmonary inflammation and emphysema. Eur Respir J 28:102–112.
31. Djuranovic S, Nahvi A, Green R. 2011. A parsimonious model for gene regulation by miRNAs. Science 331(6017):550–553.
32. Dulout FN, Grillo CA, Seoane AI, Maderna CR, Nilsson R, Vahter M, et al. 1996. Chromosomal aberrations in peripheral blood lymphocytes from native Andean women and children from northwestern Argentina exposed to arsenic in drinking water. Mutat Res 370(3–4):151–158.
33. Earle JS, Luthra R, Romans A, Abraham R, Ensor J, Yao H, et al. 2010. Association of microRNA expression with microsatellite instability status in colorectal adenocarcinoma. J Mol Diagn 12(4):433–440.
34. Etheridge A, Lee I, Hood L, Galas D, Wang K. 2011. Extracellular microRNA: a new source of biomarkers. Mutat Res 717(1–2):85–90.
35. Eyholzer M, Schmid S, Schardt JA, Haefliger S, Mueller BU, Pabst T. 2010. Complexity of miR-223 regulation by CEBPA in human AML. Leuk Res 34(5):672–676.
36. Faith RE, Luster MI. 1979. Investigations on the effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on parameters of various immune functions. Ann NY Acad Sci 320:564–571.
37. Feitelson MA, Lee J. 2007. Hepatitis B virus integration, fragile sites, and hepatocarcinogenesis. Cancer Lett 252(2):157–170.
38. Fendorf S, Michael HA, van Geen A. 2010. Spatial and temporal variations of groundwater arsenic in South and Southeast Asia. Science 328(5982):1123–1127.
39. Ferretti E, De Smaele E, Po A, Di Marcotullio L, Tosi E, Espinola MS, et al. 2009. MicroRNA profiling in human medulloblastoma. Int J Cancer 124(3):568–577.
40. Fossati S, Baccarelli A, Zanobetti A, Hoxha M, Vokonas PS, Wright RO, et al. 2014. Ambient particulate air pollution and microRNAs in elderly men. Epidemiology 25(1):68–78.
41. Fry RC, Rager JE, Bauer R, Sebastian E Peden DB, Jaspers I, et al. 2014. Air toxics and epigenetic effects: ozone altered microRNAs in the sputum of human subjects. Am J Physiol Lung Cell Mol Physiol 306(12):L1129–L1137.
42. Fulgenzi A, Vietti D, Ferrero ME. 2014. Aluminium involvement in neurotoxicity. Biomed Res Int 2014:758323; doi:10.1155/2014/758323.
43. Gambardella S, Rinaldi F, Lepore SM, Viola A, Loro E, Angelini C, et al. 2010. Overexpression of microRNA-206 in the skeletal muscle from myotonic dystrophy type 1 patients. J Transl Med 8:48; doi:10.1186/1479-5876-8-48.
44. Gao W, He HW, Wang ZM, Zhao H, Lian XQ, Wang YS, et al. 2012. Plasma levels of lipometabolism- related miR-122 and miR-370 are increased in patients with hyperlipidemia and associated with coronary artery disease. Lipids Health Dis 11:55; doi:10.1186/1476-511X-11-55.
45. Gao W, Yu Y, Cao H, Shen H, Li X, Pan S, et al. 2010. Deregulated expression of miR-21, miR-143 and miR-181a in non small cell lung cancer is related to clinicopathologic characteristics or patient prognosis. Biomed Pharmacother 64(6):399–408.
46. Garcia-Reyero N, Habib T, Pirooznia M, Gust KA, Gong P, Warner C, et al. 2011. Conserved toxic responses across divergent phylogenetic lineages: a meta-analysis of the neurotoxic effects of RDX among multiple species using toxicogenomics. Ecotoxicology 20(3):580–594.
47. Genovesi LA, Carter KW, Gottardo NG, Giles KM, Dallas PB. 2011. Integrated analysis of miRNA and mRNA expression in childhood medulloblastoma compared with neural stem cells. PloS one 6(9):e23935; doi:10.1371/journal.pone.0023935.
48. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. 2008. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359(1):61–73.
49. Graff JW, Powers LS, Dickson AM, Kim J, Reisetter AC, Hassan IH, et al. 2012. Cigarette smoking decreases global microRNA expression in human alveolar macrophages. PloS One 7(8):e44066; doi:10.1371/journal.pone.0044066.
50. Greco S, Fasanaro P, Castelvecchio S, D’Alessandra Y, Arcelli D, Di Donato M, et al. 2012. MicroRNA dysregulation in diabetic ischemic heart failure patients. Diabetes 61(6):1633–1641.
51. Greenberg ER, Barnes AB, Resseguie L, Barrett JA, Burnside S, Lanza LL, et al. 1984. Breast cancer in mothers given diethylstilbestrol in pregnancy. N Engl J Med 311(22):1393–1398.
52. Guida M, Marra M, Zullo F, Guida M, Trifuoggi M, Biffali E, et al. 2013. Association between exposure to dioxin-like polychlorinated biphenyls and miR-191 expression in human peripheral blood mononuclear cells. Mutat Res 753(1):36–41.
53. Halappanavar S, Nikota J, Wu D, Williams A, Yauk CL, Stampfli M. 2013. IL-1 receptor regulates microRNA- 135b expression in a negative feedback mechanism during cigarette smoke-induced inflammation. J Immunol 190(7):3679–3686.
54. Henke JI, Goergen D, Zheng J, Song Y, Schüttler CG, Fehr C, et al. 2008. microRNA-122 stimulates translation of hepatitis C virus RNA. EMBO J 27(24):3300–3310.
55. Herberth G, Bauer M, Gasch M, Hinz D, Röder S, Olek S, et al. 2013. Maternal and cord blood miR-223 expression associates with prenatal tobacco smoke exposure and low regulatory T-cell numbers. J Allergy Clin Immunol 133(2):543–550.
56. Holsapple MP, Farland WH, Landry TD, Monteiro- Riviere NA, Carter JM, Walker NJ, et al. 2005. Research strategies for safety evaluation of nanomaterials, part II: toxicological and safety evaluation of nanomaterials, current challenges and data needs. Toxicol Sci 88(1):12–17.
57. Hu Y, Li P, Hao S, Liu L, Zhao J, Hou Y. 2009. Differential expression of microRNAs in the placentae of Chinese patients with severe pre-eclampsia. Clin Chem Lab Med 47(8):923–929.
58. Huang Y, Dai Y, Zhang J, Wang C, Li D, Cheng J, et al. 2012. Circulating microRNAs as potential biomarkers for smoking-related interstitial fibrosis. Biomarkers 17(5):435–440.
59. Hulsmans M, Sinnaeve P, Van der Schueren B, Mathieu C, Janssens S, Holvoet P. 2012. Decreased miR-181a expression in monocytes of obese patients is associated with the occurrence of metabolic syndrome and coronary artery disease. J Clin Endocrinol Metab 97(7):E1213–E1218.
60. Izzotti A, Calin GA, Steele VE, Croce CM, De Flora S. 2009. Relationships of microRNA expression in mouse lung with age and exposure to cigarette smoke and light. FASEB J 23(9):3243–3250.
61. Izzotti A, Larghero P, Longobardi M, Cartiglia C, Camoirano A, Steele VE, et al. 2011. Dose- responsiveness and persistence of microRNA expression alterations induced by cigarette smoke in mouse lung. Mutat Res 717(1–2):9–16.
62. Izzotti A, Pulliero A. 2014. The effects of environmental chemical carcinogens on the microRNA machinery. Int J Hyg Environ Health 217(6):601–627.
63. Jardim MJ, Fry RC, Jaspers I, Dailey L, Diaz-Sanchez D. 2009. Disruption of microRNA expression in human airway cells by diesel exhaust particles is linked to tumorigenesis-associated pathways. Environ Health Perspect 117:1745–1751; doi:10.1289/ehp.0900756.
64. Ji R, Cheng Y, Yue J, Yang J, Liu X, Chen H, et al. 2007. MicroRNA expression signature and antisensemediated depletion reveal an essential role of MicroRNA in vascular neointimal lesion formation. Circ Res 100(11):1579–1588.
65. Jiang W, Zhang Y, Meng F, Lian B, Chen X, Yu X, et al. 2013. Identification of active transcription factor and miRNA regulatory pathways in Alzheimer’s disease. Bioinformatics 29(20):2596–2602.
66. Jin L, Hu WL, Jiang CC, Wang JX, Han CC, Chu P, et al. 2011. MicroRNA-149*, a p53-responsive microRNA, functions as an oncogenic regulator in human melanoma. Proc Natl Acad Sci USA 108(38):15840–15845.
67. Ju X, Li D, Shi Q, Hou H, Sun N, Shen B. 2009. Differential microRNA expression in childhood B-cell precursor acute lymphoblastic leukemia. Pediatr Hematol Oncol 26(1):1–10.
68. Kang JH, Kondo F, Katayama Y. 2006. Human exposure to bisphenol A. Toxicology 226(2–3):79–89.
69. Kim K, Lee HC, Park JL, Kim M, Kim SY, Noh SM, et al. 2011. Epigenetic regulation of microRNA-10b and targeting of oncogenic MAPRE1 in gastric cancer. Epigenetics 6(6):740–751.
70. Kim KH, Jahan SA, Kabir E. 2011. A review of diseases associated with household air pollution due to the use of biomass fuels. J Hazard Mater 192(2):425–431.
71. Kim WJ, Terada N, Nomura T, Takahashi R, Lee SD, Park JH, et al. 2002. Effect of formaldehyde on the expression of adhesion molecules in nasal microvascular endothelial cells: the role of formaldehyde in the pathogenesis of sick building syndrome. Clin Exp Allergy 32(2):287–295.
72. Kin K, Miyagawa S, Fukushima S, Shirakawa Y, Torikai K, Shimamura K, et al. 2012. Tissue- and plasma-specific microRNA signatures for atherosclerotic abdominal aortic aneurysm. J Am Heart Assoc 1(5):e000745; doi:10.1161/JAHA.112.000745.
73. Kong AP, Xiao K, Choi KC, Wang G, Chan MH, Ho CS, et al. 2012. Associations between microRNA (miR-21, 126, 155 and 221), albuminuria and heavy metals in Hong Kong Chinese adolescents. Clin Chim Acta 413(13–14):1053–1057.
74. Kong W, He L, Richards EJ, Challa S, Xu CX, Permuth-Wey J, et al. 2014. Upregulation of miRNA- 155 promotes tumour angiogenesis by targeting VHL and is associated with poor prognosis and triplenegative breast cancer. Oncogene 33(6):679–689.
75. Kumar V, Gill KD. 2009. Aluminium neurotoxicity: neurobehavioural and oxidative aspects. Arch Toxicol 83(11):965–978.
76. Lau P, de Strooper B. 2010. Dysregulated microRNAs in neurodegenerative disorders. Semin Cell Dev Biol 21(7):768–773.
77. Lee RC, Feinbaum RL, Ambros V. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5):843–854.
78. Leucci, E, Zriwil, A, Gregersen LH, Jensen KT, Obad S, Bellan C, et al. 2012. Inhibition of miR-9 de-represses HuR and DICER1 and impairs Hodgkin lymphoma tumour outgrowth in vivo. Oncogene 31(49):5081–5089.
79. Levänen B, Bhakta NR, Torregrosa Paredes P, Barbeau R, Hiltbrunner S, Pollack JL, et al. 2013. Altered microRNA profiles in bronchoalveolar lavage fluid exosomes in asthmatic patients. J Allergy Clin Immunol 131(3):894–903.
80. Li GY, Lee HY, Shin HS, Kim HY, Lim CH, Lee BH. 2007. Identification of gene markers for formaldehyde exposure in humans. Environ Health Perspect 115:1460–1466; doi:10.1289/ehp.10180.
81. Li X, Liu Y, Song G, Liu N. 2012a. A microarray for microRNA profiling in spermatozoa from adult men living in an environmentally polluted site. Bull Environ Contam Toxicol 89(6):1111–1114.
82. Li X, Shi Y, Wei Y, Ma X, Li Y, Li R. 2012b. Altered expression profiles of microRNAs upon arsenic exposure of human umbilical vein endothelial cells. Environ Toxicol Pharmacol 34(2):381–387.
83. Liang P, Lv C, Jiang B, Long X, Zhang P, Zhang M, et al. 2012. MicroRNA profiling in denatured dermis of deep burn patients. Burns 38(4):534–540.
84. Liu C, Duan W, Li R, Xu S, Zhang L, Chen C, et al. 2013. Exposure to bisphenol A disrupts meiotic progression during spermatogenesis in adult rats through estrogen-like activity. Cell Death Dis 4:e676; doi:10.1038/cddis.2013.203.
85. Liu XX, Li XJ, Zhang B, Liang YJ, Zhou CX, Cao DX, et al. 2011. MicroRNA-26b is underexpressed in human breast cancer and induces cell apoptosis by targeting SLC7A11. FEBS Lett 585(9):1363–1367.
86. Lukiw WJ, Alexandrov PN. 2012. Regulation of complement factor H (CFH) by multiple miRNAs in Alzheimer’s disease (AD) brain. Mol Neurobiol 46(1):11–19.
87. Lukiw WJ, Dua P, Pogue AI, Eicken C, Hill JM. 2011. Upregulation of micro RNA-146a (miRNA-146a), a marker for inflammatory neurodegeneration, in sporadic Creutzfeldt-Jakob disease (sCJD) and Gerstmann-Straussler-Scheinker (GSS) syndrome. J Toxicol Environ Health A 74(22–24):1460–1468.
88. Lukiw WJ, Pogue AI. 2007. Induction of specific micro RNA (miRNA) species by ROS-generating metal sulfates in primary human brain cells. J Inorg Biochem 101(9):1265–1269.
89. Lv SQ, Kim YH, Giulio F, Shalaby T, Nobusawa S, Yang H, et al. 2012. Genetic alterations in microRNAs in medulloblastomas. Brain Pathol 22(2):230–239.
90. Ma L, Young J, Prabhala, Pan E, Mestdagh P, Muth D, et al. 2010. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 12(3):247–256.
91. Maccani MA, Avissar-Whiting M, Banister CE, McGonnigal B, Padbury JF, Marsit CJ. 2010. Maternal cigarette smoking during pregnancy is associated with downregulation of miR-16, miR-21, and miR-146a in the placenta. Epigenetics 5(7):583–589.
92. Maccani MA, Padbury JF, Marsit CJ. 2011. miR-16 and miR-21 expression in the placenta is associated with fetal growth. PLoS One 6(6):e21210; doi:10.1371/journal.pone.0021210.
93. Marcucci G, Radmacher MD, Maharry K, Mrózek K, Ruppert AS, Paschka P, et al. 2008. MicroRNA expression in cytogenetically normal acute myeloid leukemia. N Engl J Med 358(18):1919–1928.
94. Marczylo EL, Amoako AA, Konje JC, Gant TW, Marczylo TH. 2012. Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern? Epigenetics 7(5):432–439.
95. Miller MR, Shaw CA, Langrish JP. 2012. From particles to patients: oxidative stress and the cardiovascular effects of air pollution. Future Cardiol 8(4):577–602.
96. Miller TE, Ghoshal K, Ramaswamy B, Roy S, Datta J, Shapiro CL, et al. 2008. MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1. J Biol Chem 283(44):29897–29903.
97. Mittendorf R. 1995. Teratogen update: carcinogenesis and teratogenesis associated with exposure to diethylstilbestrol (DES) in utero. Teratology 51(6):435–445.
98. Motta V, Angelici L, Nordio F, Bollati V, Fossati S, Frascati F, et al. 2013. Integrative analysis of miRNA and inflammatory gene expression after acute particulate matter exposure. Toxicol Sci 132(2):307–316.
99. Murchison EP, Hannon GJ. 2004. miRNAs on the move: miRNA biogenesis and the RNAi machinery. Curr Opin Cell Biol 16(3):223–229.
100. Nagano T, Higashisaka K, Kunieda A, Iwahara Y, Tanaka K, Nagano K, et al. 2013. Liver-specific microRNAs as biomarkers of nanomaterial-induced liver damage. Nanotechnology 24(40):405102; doi:10.1088/0957-4484/24/40/405102.
101. Nagel R, le Sage C, Diosdado B, van der Waal M, Oude Vrielink JA, Bolijn A, et al. 2008. Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancer. Cancer Res 68(14):5795–5802.
102. Nakanishi H, Taccioli C, Palatini J, Fernandez-Cymering C, Cui R, Kim T, et al. 2014. Loss of miR-125b-1 contributes to head and neck cancer development by dysregulating TACSTD2 and MAPK pathway. Oncogene 33(6):702–712.
103. Nana-Sinkam SP, Hunter MG, Nuovo GJ, Schmittgen TD, Gelinas R, Galas D, et al. 2009. Integrating the microRNome into the study of lung disease. Am J Respir Crit Care Med 179(1):4–10.
104. Nel A, Xia T, Mädler L, Li N. 2006. Toxic potential of materials at the nanolevel. Science 311(5761):622–627.
105. Ohlsson Teague EM, Van der Hoek KH, Van der Hoek MB, Perry N, Wagaarachchi P, Robertson SA, et al. 2009. MicroRNA-regulated pathways associated with endometriosis. Mol Endocrinol 23(2):265–275.
106. Ota D, Mimori K, Yokobori T, Iwatsuki M, Kataoka A, Masuda N, et al. 2011. Identification of recurrence- related microRNAs in the bone marrow of breast cancer patients. Int J Oncol 38(4):955–962.
107. Overton JH, Kimbell JS, Miller FJ. 2001. Dosimetry modeling of inhaled formaldehyde: the human respiratory tract. Toxicol Sci 64(1):122–134.
108. Pallante P, Visone R, Ferracin M, Ferraro A, Berlingieri MT, Troncone G, et al. 2006. MicroRNA deregulation in human thyroid papillary carcinomas. Endocr Relat Cancer 13(2):497–508.
109. Palma CA, Al Sheikha D, Lim TK, Bryant A, Vu TT, Jayaswal V, et al. 2014. MicroRNA-155 as an inducer of apoptosis and cell differentiation in Acute Myeloid Leukaemia. Mol Cancer 13(1):79; doi:10.1186/1476-4598-13-79.
110. Perkins DO, Jeffries CD, Jarskog LF, Thomson JM, Woods K, Newman MA, et al. 2007. microRNA expression in the prefrontal cortex of individuals with schizophrenia and schizoaffective disorder. Genome Biol 8(2):R27; doi:10.1186/gb-2007-8-2-r27.
111. Pogue AI, Li YY, Cui JG, Zhao Y, Kruck TP, Percy ME, et al. 2009. Characterization of an NF-κBregulated, miRNA-146a-mediated down-regulation of complement factor H (CFH) in metal-sulfatestressed human brain cells. J Inorg Biochem 103(11):1591–1595.
112. Polikepahad S, Knight JM, Naghavi AO, Oplt T, Creighton CJ, Shaw C, et al. 2010. Proinflammatory role for let-7 microRNAS in experimental asthma. J Biol Chem 285(39):30139–30149.
113. Pope CA III, Burnett RT, Turner MC, Cohen A, Krewski D, Jerrett M, et al. 2011. Lung cancer and cardiovascular disease mortality associated with ambient air pollution and cigarette smoke: shape of the exposure–response relationships. Environ Health Perspect 119:1616–1621; doi:10.1289/ehp.1103639.
114. Porta M, Zumeta E. 2002. Implementing the Stockholm Treaty on Persistent Organic Pollutants [Editorial]. Occup Environ Med 59(10):651–652.
115. Prokopec SD, Watson JD, Waggott DM, Smith AB, Wu AH, Okey AB, et al. 2013. Systematic evaluation of medium-throughput mRNA abundance platforms. RNA 19(1):51–62.
116. Qian ZR, Asa SL, Siomi H, Siomi MC, Yoshimoto K, Yamada S, et al. 2009. Overexpression of HMGA2 relates to reduction of the let-7 and its relationship to clinicopathological features in pituitary adenomas. Mod Pathol 22(3):431–441.
117. Qu P, Roberts J, Li Y, Albrecht M, Cummings OW, Eble JN, et al. 2009. Stat3 downstream genes serve as biomarkers in human lung carcinomas and chronic obstructive pulmonary disease. Lung Cancer 63:341–347.
118. Rager JE, Moeller BC, Doyle-Eisele M, Kracko D, Swenberg JA, Fry RC. 2013. Formaldehyde and epigenetic alterations: microRNA changes in the nasal epithelium of nonhuman primates. Environ Health Perspect 121:339–344; doi:10.1289/ehp.1205582.
119. Rager JE, Moeller BC, Miller SK, Kracko D, Doyle- Eisele M, Swenberg JA, et al. 2014. Formaldehyde- associated changes in microRNAs: tissue and temporal specificity in the rat nose, white blood cells, and bone marrow. Toxicol Sci 138(1):36–46.
120. Rager JE, Smeester L, Jaspers I, Sexton KG, Fry RC. 2011. Epigenetic changes induced by air toxics: formaldehyde exposure alters miRNA expression profiles in human lung cells. Environ Health Perspect 119:494–500; doi:10.1289/ehp.1002614.
121. Rahman MM, Qian ZR, Wang EL, Sultana R, Kudo E, Nakasono M, et al. 2009. Frequent overexpression of HMGA1 and 2 in gastroenteropancreatic neuroendocrine tumours and its relationship to let-7 downregulation. Br J Cancer 100(3):501–510.
122. Raitoharju E, Lyytikäinen LP, Levula M, Oksala N, Mennander A, Tarkka M, et al. 2011. miR-21, miR-210, miR-34a, and miR-146a/b are up-regulated in human atherosclerotic plaques in the Tampere Vascular Study. Atherosclerosis 219(1):211–217.
123. Ralfkiaer U, Hagedorn PH, Bangsgaard N, Løvendorf MB, Ahler CB, Svensson L, et al. 2011. Diagnostic microRNA profiling in cutaneous T-cell lymphoma (CTCL). Blood 118(22):5891–5900.
124. Rubin BS. 2011. Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol 127(1–2):27–34.
125. Saetrom P, Heale BS, Snøve O Jr, Aagaard L, Alluin J, Rossi JJ. 2007. Distance constraints between microRNA target sites dictate efficacy and cooperativity. Nucleic Acids Res. 35:2333–2342.
126. Sakurai M, Miki Y, Masuda M, Hata S, Shibahara Y, Hirakawa H, et al. 2012. LIN28: a regulator of tumor-suppressing activity of let-7 microRNA in human breast cancer. J Steroid Biochem Mol Biol 131(3–5):101–106.
127. Scapoli L, Palmieri A, Lo Muzio L, Pezzetti F, Rubini C, Girardi A, et al. 2010. MicroRNA expression profiling of oral carcinoma identifies new markers of tumor progression. Int J Immunopathol Pharmacol 23(4):1229–1234.
128. Schembri F, Sridhar S, Perdomo C, Gustafson AM, Zhang X, Ergun A, et al. 2009. MicroRNAs as modulators of smoking-induced gene expression changes in human airway epithelium. Proc Natl Acad Sci USA 106(7):2319–2324.
129. Schulte JH, Marschall T, Martin M, Rosenstiel P, Mestdagh P, Schlierf S, et al. 2010. Deep sequencing reveals differential expression of microRNAs in favorable versus unfavorable neuroblastoma. Nucleic Acids Res 38(17):5919–5928.
130. Seok J, Warren HS, Cuenca AG, Mindrinos MN, Baker HV, Xu W, et al. 2013. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci USA 110(9):3507–3512.
131. Shan ZX, Lin QX, Fu YH, Deng CY, Zhou ZL, Zhu JN, et al. 2009. Upregulated expression of miR-1/miR-206 in a rat model of myocardial infarction. Biochem Biophys Res Commun 381(4):597–601.
132. Shi L, Cheng Z, Zhang J, Li R, Zhao P, Fu Z, et al. 2008. hsa-mir-181a and hsa-mir-181b function as tumor suppressors in human glioma cells. Brain Res 1236:185–193.
133. Singh NP, Singh UP, Guan H, Nagarkatti P, Nagarkatti M. 2012. Prenatal exposure to TCDD triggers significant modulation of microRNA expression profile in the thymus that affects consequent gene expression. PLoS One 7(9):e45054; doi:10.1371/journal.pone.0045054.
134. Song MK, Park YK, Ryu JC. 2013. Polycyclic aromatic hydrocarbon (PAH)-mediated upregulation of hepatic microRNA-181 family promotes cancer cell migration by targeting MAPK phosphatase-5, regulating the activation of p38 MAPK. Toxicol Appl Pharmacol 273(1):130–139.
135. Soto AM, Brisken C, Schaeberle C, Sonnenschein C. 2013. Does cancer start in the womb? Altered mammary gland development and predisposition to breast cancer due to in utero exposure to endocrine disruptors. J Mammary Gland Biol Neoplasia 18(2):199–208.
136. Spira A, Beane J, Shah V, Liu G, Schembri F, Yang X, et al. 2004. Effects of cigarette smoke on the human airway epithelial cell transcriptome. Proc Natl Acad Sci USA 101(27):10143–10148.
137. Stánitz E, Juhász K, Tóth C, Gombos K, Natali PG, Ember I. 2013. Evaluation of MicroRNA expression pattern of gastric adenocarcinoma associated with socioeconomic, environmental and lifestyle factors in northwestern Hungary. Anticancer Res 33(8):3195–3200.
138. Steele G, Stehr-Green P, Welty E. 1986. Estimates of the biologic half-life of polychlorinated biphenyls in human serum [Letter]. N Engl J Med 314(14):926–927.
139. Sturchio E, Colombo T, Boccia P, Carucci N, Meconi C, Minoia C, et al. 2014. Arsenic exposure triggers a shift in microRNA expression. Sci Total Environ 472:672–680.
140. Sweeney LM, Okolica MR, Gut CP Jr, Gargas ML. 2012. Cancer mode of action, weight of evidence, and proposed cancer reference value for hexahydro- 1,3,5-trinitro-1,3,5-triazine (RDX). Regul Toxicol Pharmacol 64(2):205–224.
141. Takahashi K, Yokota S, Tatsumi N, Fukami T, Yokoi T, Nakajima M. 2013. Cigarette smoking substantially alters plasma microRNA profiles in healthy subjects. Toxicol Appl Pharmacol 272(1):154–160.
142. Takahashi O, Oishi S. 2000. Disposition of orally administered 2,2-bis(4-hydroxyphenyl)propane (bisphenol A) in pregnant rats and the placental transfer to fetuses. Environ Health Perspect 108:931–935.
143. Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H, et al. 2004. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res 64(11):3753–3756.
144. Thum T, Galuppo P, Wolf C, Fiedler J, Kneitz S, van Laake LW, et al. 2007. MicroRNAs in the human heart: a clue to fetal gene reprogramming in heart failure. Circulation 116(3):258–267.
145. Tilghman SL, Bratton MR, Segar HC, Martin EC, Rhodes LV, Li M, et al. 2012. Endocrine disruptor regulation of microRNA expression in breast carcinoma cells. PLoS One 7(3):e32754; doi:10.1371/journal.pone.0032754.
146. Tseng CH. 2008. Cardiovascular disease in arsenicexposed subjects living in the arseniasishyperendemic areas in Taiwan. Atherosclerosis 199(1):12–18.
147. Tsukimori K, Tokunaga S, Shibata S, Uchi H, Nakayama D, Ishimaru T, et al. 2008. Long-term effects of polychlorinated biphenyls and dioxins on pregnancy outcomes in women affected by the Yusho incident. Environ Health Perspect 116:626–630; doi:10.1289/ehp.10686.
148. Van Pottelberge GR, Mestdagh P, Bracke KR, Thas O, van Durme YM, Joos GF, et al. 2011. MicroRNA expression in induced sputum of smokers and patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 183(7):898–906.
149. van Rooij E, Sutherland LB, Qi X, Richardson JA, Hill J, Olson EN. 2007. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316(5824):575–579.
150. Vasudevan S, Tong Y, Steitz JA. 2007. Switching from repression to activation: microRNAs can up- regulate translation. Science 318(5858):1931–1934.
151. Voellenkle C, van Rooij J, Cappuzzello C, Greco S, Arcelli D, Di Vito L, et al. 2010. MicroRNA signatures in peripheral blood mononuclear cells of chronic heart failure patients. Physiol Genomics 42(3):420–426.
152. Vogt M, Munding J, Grüner M, Liffers ST, Verdoodt B, Hauk J, et al. 2011. Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Arch 458(3):313–322.
153. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, et al. 2006. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 103(7):2257–2261.
154. Waliszewski SM, Aguirre AA, Infanzon RM, Silva CS, Siliceo J. 2001. Organochlorine pesticide levels in maternal adipose tissue, maternal blood serum, umbilical blood serum, and milk from inhabitants of Veracruz, Mexico. Arch Environ Contam Toxicol 40(3):432–438.
155. Wang C, Yang C, Chen X, Yao B, Yang C, Zhu C, et al. 2011. Altered profile of seminal plasma microRNAs in the molecular diagnosis of male infertility. Clin Chem 57(12):1722–1731.
156. Wang F, Liu W, Jin Y, Wang F, Ma J. 2014. Prenatal and neonatal exposure to perfluorooctane sulfonic acid results in aberrant changes in miRNA expression profile and levels in developing rat livers. Environ Toxicol; doi:10.1002/tox.21949 [Online 13 January 2014].
157. Wang H, Zhang P, Chen W, Feng D, Jia Y, Xie L. 2012. Serum microRNA signatures identified by Solexa sequencing predict sepsis patients’ mortality: a prospective observational study. PLoS One 7(6):e38885; doi:10.1371/journal.pone.0038885.
158. Wang J, Zhang Y, Zhang W, Jin Y, Dai J. 2012. Association of perfluorooctanoic acid with HDL cholesterol and circulating miR-26b and miR-199-3p in workers of a fluorochemical plant and nearby residents. Environ Sci Technol 46(17):9274–9281.
159. Wang X, Ha T, Liu L, Zou J, Zhang X, Kalbfleisch J, et al. 2013. Increased expression of microRNA- 146a decreases myocardial ischaemia/reperfusion injury. Cardiovasc Res 97(3):432–442.
160. Wang Y, Li Z, He C, Wang D, Yuan X, Chen J, et al. 2010. MicroRNAs expression signatures are associated with lineage and survival in acute leukemias. Blood Cells Mol Dis 44(3):191–197.
161. Weigelt K, Bergink V, Burgerhout KM, Pescatori M, Wijkhuijs A, Drexhage HA. 2013. Down-regulation of inflammation-protective microRNAs 146a and 212 in monocytes of patients with postpartum psychosis. Brain Behav Immun 29:147–155.
162. White NM, Bao TT, Grigull J, Youssef YM, Girgis A, Diamandis M, et al. 2011. miRNA profiling for clear cell renal cell carcinoma: biomarker discovery and identification of potential controls and consequences of miRNA dysregulation. J Urol 186(3):1077–1083.
163. Wild C. 2005. Complementing the genome with an “exposome”: the outstanding challenge of environmental exposure measurement in molecular epidemiology. Cancer Epidemiol Biomarkers Prev 14(8):1847–1850.
164. Williams AH, Valdez G, Moresi V, Qi X, McAnally J, Elliott JL, et al. 2009. MicroRNA-206 delays ALS progression and promotes regeneration of neuromuscular synapses in mice. Science 326(5959):1549–1554.
165. Wong KY, Liang R, So CC, Jin DY, Costello JF, Chim CS. 2011. Epigenetic silencing of MIR203 in multiple myeloma. Br J Haematol 154(5):569–578.
166. Wu J, Yang T, Li X, Yang Q, Liu R, Huang J, et al. 2013. Alteration of serum miR-206 and miR-133b is associated with lung carcinogenesis induced by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone. Toxicol Appl Pharmacol 267(3):238–246.
167. Wu ZS, Wu Q, Wang CQ, Wang XN, Huang J, Zhao JJ, et al. 2011. miR-340 inhibition of breast cancer cell migration and invasion through targeting of oncoprotein c-Met. Cancer 117(13):2842–2852.
168. Xi S, Yang M, Tao Y, Xu H, Shan J, Inchauste S, et al. 2010. Cigarette smoke induces C/EBP-β-mediated activation of miR-31 in normal human respiratory epithelia and lung cancer cells. PLoS One 5(10):e13764; doi:10.1371/journal.pone.0013764.
169. Xiao C, Calado DP, Galler G, Thai TH, Patterson HC, Wang J, et al. 2007. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 131(1):146–159.
170. Xu CC, Han WQ, Xiao B, Li NN, Zhu DL, Gao PJ. 2008. Differential expression of microRNAs in the aorta of spontaneously hypertensive rats [in Chinese]. Sheng Li Xue Bao 60(4):553–560.
171. Yamagishi M, Nakano K, Miyake A, Yamochi T, Kagami Y, Tsutsumi A, et al. 2012. Polycomb- mediated loss of miR-31 activates NIK-dependent NF-κB pathway in adult T cell leukemia and other cancers. Cancer Cell 21(1):121–135.
172. Yamamoto M, Singh A, Sava F, Pui M, Tebbutt SJ, Carlsten C. 2013. MicroRNA expression in response to controlled exposure to diesel exhaust: attenuation by the antioxidant N-acetylcysteine in a randomized crossover study. Environ Health Perspect 121:670–675; doi:10.1289/ehp.1205963.
173. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, et al. 2006. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer cell 9(3):189–198.
174. Yi C, Wang Q, Wang L, Huang Y, Li L, Liu L, et al. 2012. MiR-663, a microRNA targeting p21(WAF1/CIP1), promotes the proliferation and tumorigenesis of nasopharyngeal carcinoma. Oncogene 31(41):4421–4433.
175. Yuchuan H, Ya D, Jie Z, Jingqiu C, Yanrong L, Dongliang L, et al. 2014. Circulating miRNAs might be promising biomarkers to reflect the dynamic pathological changes in smoking-related interstitial fibrosis. Toxicol Ind Health 30 (2):182–191.
176. Zampetaki A, Kiechl S, Drozdov I, Willeit P, Mayr U, Prokopi M, et al. 2010. Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res 107(6):810–817.
177. Zhang B, Pan X. 2009. RDX induces aberrant expression of microRNAs in mouse brain and liver. Environ Health Perspect 117:231–240; doi:10.1289/ehp.11841.
178. Zhang JX, Song W, Chen ZH, Wei JH, Liao YJ, Lei J, et al. 2013. Prognostic and predictive value of a microRNA signature in stage II colon cancer: a microRNA expression analysis. Lancet Oncol 14(13):1295–1306.
179. Zhang Y, Pan T, Zhong X, Cheng C. 2014. Nicotine upregulates microRNA-21 and promotes TGF-β- dependent epithelial-mesenchymal transition of esophageal cancer cells. Tumour Biol 35(7):7063–7072.
180. Zhang Y, Yan LX, Wu QN, Du ZM, Chen J, Liao DZ, et al. 2011. miR-125b is methylated and functions as a tumor suppressor by regulating the ETS1 proto-oncogene in human invasive breast cancer. Cancer Res 71(10):3552–3562.