Interplay between histopathological alterations, cigarette smoke and chemopreventive agents in defining microRNA profiles in mouse lung

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 717, Issue 1-2, 2011, Pages 17-24

  Izzotti, Alberto ^a   Larghero, Patrizia ^a   Balansky, Roumen ^b   Pfeffer, Ulrich ^c   Steele, Vernon E ^d   de Flora, Silvio ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b National Oncology Center Bulgaria   (Bulgaria)

^c UNIVERSITY OF GENOA   (Italy)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Chemopreventive agents; Cigarette smoke; Lung carcinogenesis; MicroRNAs

Indexed keywords

ACETYLCYSTEINE; CIGARETTE SMOKE; MICRORNA; PHENETHYL ISOTHIOCYANATE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER INVASION; CANCER PREVENTION; CELL COMMUNICATION; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; GENE EXPRESSION PROFILING; HISTOPATHOLOGY; INFLAMMATION; LUNG; LUNG ADENOMA; LUNG ALVEOLUS CELL CARCINOMA; LUNG CARCINOGENESIS; LUNG TUMOR; METASTASIS; MOUSE; NEWBORN; NONHUMAN; ONCOGENE; PNEUMONIA; PRIORITY JOURNAL; STEM CELL; TUMOR SUPPRESSOR GENE; TUMOR VASCULARIZATION; UNDIFFERENTIATED STEM CELL;

ANIMALS; ANTICARCINOGENIC AGENTS; FEMALE; GENE EXPRESSION PROFILING; HUMANS; LUNG; LUNG NEOPLASMS; MICE; PNEUMONIA; PREGNANCY; PRINCIPAL COMPONENT ANALYSIS; RATS; SMOKE; SMOKING; TOBACCO; TOBACCO SMOKE POLLUTION;

MUS; RATTUS;

EID: 82755161957     PISSN: 00275107     EISSN: 09218262     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2010.10.003     Document Type: Article

References (62)

1. Calin G.A., Croce C.M. MicroRNA-cancer connection: the beginning of a new tale. Cancer Res. 2006, 66:7390-7394.
2. Calin G.A., Sevignani C., Dumitru C.D., Hyslop T., Noch E., Yendamuri S., Shimizu M., Rattan S., Bullrich F., Negrini M., Croce C.M. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancer. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:2999-3004.
3. Wu X., Piper-Hunter M.G., Crawford M., Nuovo G.J., Marsh C.B., Otterson G.A., Nana-Sinkam S.P. MicroRNAs in the pathogenesis of lung cancer. J. Thorac. Oncol. 2009, 4:1028-1034.
4. Qi Z.W., Xu W., Habib N., Xu R. Potential uses of microRNA in lung cancer diagnosis, prognosis, and therapy. Curr. Cancer Drug Targets 2009, 9:572-594.
5. Izzotti I.A, Calin G.A., Arrigo P., Steele V.E., Croce C.M., De Flora S. Downregulation of microRNA expression in the lungs of rats exposed to cigarette smoke. FASEB J. 2009, 23:806-812.
6. Izzotti A., Bagnasco M., Cartiglia C., Longobardi M., Camoirano A., Tampa E., Lubet R.A., De Flora S. Modulation of multigene expression and proteome profiles by chemopreventive agents. Mutat. Res. 2005, 591:212-223.
7. Izzotti A., Bagnasco M., Cartiglia C., Longobardi M., Balansky R.M., Merello A., Lubet R.A., De Flora S. Chemoprevention of genome, transcriptome, and proteome alterations induced by cigarette smoke in rat lung. Eur. J. Cancer 2005, 41:1864-1874.
8. Izzotti A., Calin G.A., Steele V.E., Croce C.M., De Flora S. Relationships of microRNA expression in mouse lung with age and exposure to cigarette smoke and light. FASEB J. 2009, 23:3243-3250.
9. Schembri F., Sridhar S., Perdomo C., Gustafson A.M., Zhang X., Ergun A., Lu J., Liu G., Zhang X., Bowers J., Vaziri C., Ott K., Sensinger K., Collins J.J., Brody J.S., Getts R., Lenburg M.E., Spira A. MicroRNAs as modulators of smoking-induced gene expression changes in human airway epithelium. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2319-2324.
10. Izzotti A., Calin G.A., Steele V.E., Cartiglia C., Longobardi M., Croce C.M., De Flora S. Chemoprevention of cigarette smoke-induced alterations of microRNA expression in rat lung. Cancer Prev. Res. 2010, 3:62-72.
11. Izzotti A., Larghero P., Cartiglia C., Longobardi M., Pfeffer U., Steele V.E., De Flora S. Modulation of microRNA expression by budesonide, phenethyl isothiocyanate, and cigarette smoke in mouse liver and lung. Carcinogenesis 2010, 31:894-901.
12. D'Agostini F., Mastracci L., Izzotti A., Balansky R., Pennisi T.M., Steele V.E., De Flora S. Modulation by phenethyl isothiocyanate and budesonide of molecular and histopathological alterations induced by environmental cigarette smoke in mice. Cancer Prev. Res. 2009, 2:546-556.
13. Liu X., Sempere L.F., Galimberti F., Freemantle S.J., Black C., Dragnev K.H., Ma Y., Fiering S., Memoli V., Li H., DiRenzo J., Korc M., Cole C.N., Bak M., Kauppinen S., Dmitrovsky E. Uncovering growth-suppressive MicroRNAs in lung cancer. Clin. Cancer Res. 2009, 15:1177-1183.
14. Melkamu T., Zhang X., Tan J., Zeng Y., Kassie F. Alteration of microRNA expression in vinyl carbamate-induced mouse lung tumors and modulation by the chemopreventive agent indole-3-carbinol. Carcinogenesis 2010, 31:252-258.
15. Balansky R., Ganchev G., Iltcheva M., Steele V.E., De Flora S. Prevention of cigarette smoke-induced lung cancer in mice by budesonide, phenethyl isothiocyanate, and N-acetylcysteine. Int. J. Cancer 2009, 126:1047-1054.
16. Balansky R., Ganchev G., Iltcheva M., Steele V.E., De Flora S. Prenatal N-acetylcysteine prevents cigarette smoke-induced lung cancer in neonatal mice. Carcinogenesis 2009, 30:1398-1401.
17. De Flora S., D'Agostini F., Balansky R., Camoirano A., Cartiglia C., Longobardi M., Travaini G., Steele V.E., Pesce C., Izzotti A. High susceptibility of neonatal mice to molecular, biochemical and cytogenetical alterations induced by environmental cigarette smoke and light. Mutat. Res. 2008, 659:137-146.
18. Balansky R., Ganchev G., Iltcheva M., Steele V.E., D'Agostini F., De Flora S. Potent carcinogenicity of cigarette smoke in mice exposed early in life. Carcinogenesis 2007, 28:2236-2243.
19. Park S.Y., Lee J.H., Ha M., Nam J.W., Kim V.N. MiR-29 miRNAs activate p53 by targeting p85 alpha and CDC42. Nat. Struct. Mol. Biol. 2009, 16:23-29.
20. Duan R., Pak C., Jin P. Single nucleotide polymorphism associated with mature miR-125a alters the processing of pri-miRNA. Hum. Mol. Gen. 2007, 16:1124-1131.
21. Zhou L., Qi X., Potashkin J.A., Abdul-Karim F.W., Gorodeski G.I. MicroRNAs miR-186 and miR-150 down-regulate expression of the pro-apoptotic purinergic P2X7 receptor by activation of instability sites at the 3'-untranslated region of the gene that decrease steady-state levels of the transcript. J. Biol. Chem. 2008, 283:28274-28286.
22. D'Agostini F., Balansky R., Izzotti A., Lubet R.A., Kelloff G.J., De Flora S. Modulation of apoptosis by cigarette smoke and cancer chemopreventive agents in the respiratory tract of rats. Carcinogenesis 2001, 22:375-380.
23. Wang X.H., Qian R.Z., Zhang W., Chen S.F., Jin H.M., Hu R.M. MicroRNA-320 expression in myocardial microvascular endothelial cells and its relationship with insulin-like growth factor-1 in type 2 diabetic rats. Clin. Exp. Pharmacol. Physiol. 2009, 36:181-188.
24. Izzotti A., Balansky R., Cartiglia C., Camoirano A., Longobardi M., De Flora S. Genomic and transcriptional alterations in mouse fetus liver after transplacental exposure to cigarette smoke. FASEB J. 2003, 17:1127-1129. (full text available online, 22 April 2003).
25. Schoolmeesters A., Eklund T., Leake D., Vermeulen A., Smith Q., Force Aldred S., Fedorov Y. Functional profiling reveals critical role for miRNA in differentiation of human mesenchymal stem cells. PLoS ONE 2009, 4:e5605.
26. Izzotti A., D'Agostini F., Larghero P., Cartiglia C., Travaini G., Balansky R., Steele V.E., De Flora S. Upregulation of stem cell antigen-1 in the lung of neonatal mice exposed to environmental cigarette smoke. Oncol. Rep. 2009, 22:469-474.
27. Tian Y., Luo A., Cai Y., Su Q., Ding F., Chen H., Liu Z. MicroRNA-10b promotes migration and invasion through KLF4 in human esophageal cancer cell lines. J. Biol. Chem. 2010, 285:7986-7994.
28. Hummel R., Hussey D.J., Haier J. MicroRNAs: predictors and modifiers of chemo- and radiotherapy in different tumour types. Eur. J. Cancer 2010, 46:298-311.
29. Izzotti A., Cartiglia C., Longobardi M., Balansky R., D'Agostini F., Lubet R.A., De Flora S. Alterations of gene expression in skin and lung of mice exposed to light and cigarette smoke. FASEB J. 2004, 18:1559-1561. (Full text published online, 2 August 2004).
30. Duisters R.F., Tijsen A.J., Schroen B., Leenders J.J., Lentink V., van der Made I., Herias V., van Leeuwen R.E., Schellings M.W., Barenbrug P., Maessen J.G., Heymans S., Pinto Y.M., Creemers E.E. MiR-133 and miR-30 regulate connective tissue growth factor: implications for a role of microRNAs in myocardial matrix remodelling. Circ. Res. 2009, 104:170-178.
31. Mitomo S., Maesawa C., Ogasawara S., Iwaya T., Shibazaki M., Yashima-Abo A., Kotani K., Oikawa H., Sakurai E., Izutsu N., Kato K., Komatsu H., Ikeda K., Wakabayashi G., Masuda T. Downregulation of miR-138 is associated with overexpression of human telomerase reverse transcriptase protein in human anaplastic thyroid carcinoma cell lines. Cancer Sci. 2008, 99:280-286.
32. Zhao X., Yang L., Hu J., Ruan J. MiR-138 might reverse multidrug resistance of leukemia cells. Leuk. Res. 2010, 34:1078-1082.
33. Du L., Schageman J.J., Subauste M.C., Saber B., Hammond S.M., Prudkin L., Wistuba I.I., Ji L., Roth J.A., Minna J.D., Pertsemlidis A. MiR-93, miR-98, and miR-197 regulate expression of tumor suppressor gene FUS1. Mol. Cancer Res. 2009, 7:1234-1243.
34. Lebanony D., Benjamin H., Gilad S., Ezagouri M., Dov A., Ashkenazi K., Gefen N., Izraeli S., Rechavi G., Pass H., Nonaka D., Li J., Spector Y., Rosenfeld N., Chajut A., Cohen D., Aharonov R., Mansukhani M. Diagnostic assay based on hsa-miR-205 expression distinguishes squamous from nonsquamous non-small-cell lung carcinoma. J. Clin. Oncol. 2009, 27:2030-2037.
35. Markou A., Tsaroucha E.G., Kaklamanis L., Fotinou M., Georgoulias V., Lianidou E.S. Prognostic value of mature microRNA-21 and microRNA-205 overexpression in non-small cell lung cancer by quantitative real-time RT-PCR. Clin. Chem. 2008, 54:1696-1704.
36. He X.Y., Chen J.X., Zhang Z., Li C.L., Peng Q.L., Peng H.M. The let-7a microRNA protects from growth of lung carcinoma by suppression of k-Ras and c-Myc in nude mice. J. Cancer Res. Clin. Oncol. 2010, 136:1023-1028.
37. Takamizawa J., Konishi H., Yanagisawa K., Tomida S., Osada H., Endoh H., Harano T., Yatabe Y., Nagino M., Nimura Y., Mitsudomi T., Takahashi T. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res. 2004, 64:3753-3756.
38. Qian S., Ding J.Y., Xie R., An J.H., Ao X.J., Zhao Z.G., Sun J.G., Duan Y.Z., Chen Z.T., Zhu B., MicroRNA expression profile of bronchioalveolar stem cells from mouse lung. Biochem. Biophys. Res. Commun. 2008, 377:668-673.
39. Kim S.Y., Kim A.Y., Lee H.W., Son Y.H., Lee G.Y., Lee J.W., Lee Y.S., Kim J.B. MiR-27a is a negative regulator of adipocyte differentiation via suppressing PPARgamma expression. Biochem. Biophys. Res. Commun. 2010, 392:323-328.
40. Jennewein C., von Knethen A., Schmid T., Bruene B. MicroRNA-27b contributes tolipopolysaccharide-mediated peroxisome proliferator-activated receptor {gamma}(PPAR{gamma}) mRNA destabilization. J. Biol. Chem. 2010, 285:11846-11853.
41. Izzotti A., Cartiglia C., Longobardi M., Bagnasco M., Merello A., You M., Lubet R.A., De Flora S. Gene expression in the lung of p53 mutant mice exposed to cigarette smoke. Cancer Res. 2004, 64:8566-8572.
42. Li M.Y., Yuan H., Ma L.T., Kong A.W., Hsin M.K., Yip J., Underwood M.J., Chen G.G. Roles of PPAR{alpha} and PPAR{gamma} in the development of non-small cell lung cancer. Am. J. Respir. Cell. Mol. Biol. 2010, (January). (Epub ahead of print).
43. Chhabra R., Adlakha Y.K., Hariharan M., Scaria V., Saini N. Upregulation of miR-23a-27a-24-2 cluster induces caspase-dependent and -independent apoptosis in human embryonic kidney cells. PLoS ONE 2009, 4:e5848.
44. Bellon M., Lepelletier Y., Hermine O., Nicot C. Deregulation of microRNA involved in hematopoiesis and the immune response in HTLV-I adult T-cell leukaemia. Blood 2009, 113:4914-4917.
45. Al-Shibli K.I., Donnem T., Al-Saad S., Persson M., Bremnes R.M., Busund L.T. Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin. Cancer Res. 2008, 14:5220-5527.
46. Dixon-McIver A., East P., Mein C.A., Cazier J.B., Molloy G., Chaplin T., Andrew Lister T., Young B.D., Debernardi S. Distinctive patterns of microRNA expression associated with karyotype in acute myeloid leukaemia. PLoS ONE 2008, 3:e2141.
47. Choong M.L., Yang H.H., McNiece I. MicroRNA expression profiling during human cord blood-derived CD34 cell erythropoiesis. Exp. Hematol. 2007, 35:551-564.
48. Myatt S.S., Wang J., Monteiro L.J., Christian M., Ho K.K., Fusi L., Dina R.E., Brosens J.J., Ghaem-Maghami S., Lam E.W. Definition of microRNAs that repress expression of the tumor suppressor gene FOXO1 in endometrial cancer. Cancer Res. 2010, 70:367-377.
49. Guttilla I.K., White B.A. Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J. Biol. Chem. 2009, 284:23204-23216.
50. Cho W.C., Chow A.S., Au J.S. Restoration of tumour suppressor hsa-miR-145 inhibits cancer cell growth in lung adenocarcinoma patients with epidermal growth factor receptor mutation. Eur. J. Cancer 2009, 45:2197-2206.
51. Segura M.F., Hanniford D., Menendez S., Reavie L., Zou X., Alvarez-Diaz S., Zakrzewski J., Blochin E., Rose A., Bogunovic D., Polsky D., Wei J., Lee P., Belitskaya-Levy I., Bhardwaj N., Osman I., Hernando E. Aberrant miR-182 expression promotes melanoma metastasis by repressing FOXO3 and microphthalmia-associated transcription factor. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:1814-1819.
52. Mohri T., Nakajima M., Fukami T., Takamiya M., Aoki Y., Yokoi T. Human CYP2E1 is regulated by miR-378. Biochem. Pharmacol. 2010, 79:1045-1052.
53. Uematsu F., Kikuchi H., Motomiya M., Abe T., Ishioka C., Kanamaru R., Sagami I., Watanabe M. Human cytochrome P450IIE1 gene: DraI polymorphism and susceptibility to cancer. Tohoku J. Exp. Med. 1992, 168:113-117.
54. Kivistö K.T., Kroemer H.K., Eichelbaum M. The role of human cytochrome P450 enzymes in the metabolism of anticancer agents: implications for drug interactions. Br. J. Clin. Pharmacol. 1995, 40:523-530.
55. Wang S., Olson E.N. AngiomiRs-key regulators of angiogenesis. Curr. Opin. Genet. Dev. 2009, 19:205-211.
56. Lee D.Y., Deng Z., Wang C.H., Yang B.B. MicroRNA-378 promotes cell survival, tumor growth, and angiogenesis by targeting SuFu and Fus-1 expression. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:20350-20355.
57. Yamamoto Y., Kosaka N., Tanaka M., Koizumi F., Kanai Y., Mizutani T., Murakami Y., Kuroda M., Miyajima A., Kato T., Ochiya T. MicroRNA-500 as a potential diagnostic marker for hepatocellular carcinoma. Biomarkers 2009, 14:529-538.
58. Patnaik S.K., Kannisto E., Knudsen S., Yendamuri S. Evaluation of microRNA expression profiles that may predict recurrence of localized stage I non-small cell lung cancer after surgical resection. Cancer Res. 2010, 70:36-45.
59. Yao R., Wang Y., Lubet R.A., You M., D'Agostini F., Izzotti A., De Flora F. K-Ras mutations in lung tumors from p53 mutant mice exposed to cigarette smoke. Exp. Lung Res. 2005, 31:271-281.
60. Chen J.T., Cheng Y.W., Chou M.C., Sen-Lin T., Lai W.W., Ho W.L., Lee H. The correlation between aberrant connexin 43 mRNA expression induced by promoter methylation and nodal micrometastasis in non-small cell lung cancer. Clin. Cancer Res. 2003, 9:4200-4204.
61. De Flora S., Scarfì S., Izzotti A., D'Agostini F., Chang C.-C., Bagnasco M., De Flora A., Trosko J.E. Induction by 7, 12-dimethylbenz(a)anthracene of molecular and biochemical alterations in transformed human mammary epithelial stem cells, and protection by N-acetylcysteine. Int. J. Oncol. 2006, 29:521-529.
62. Xu G., Zhang Y., Jia H., Li J., Liu X., Engelhardt J.F., Wang Y. Cloning and identification of microRNAs in bovine alveolar macrophages. Mol. Cell. Biochem. 2009, 332:9-16.