Smoking and microRNA dysregulation: A cancerous combination

Trends in Molecular Medicine

Volumn 20, Issue 1, 2014, Pages 36-47

  Momi, Navneet ^a   Kaur, Sukhwinder ^a   Rachagani, Satyanarayana ^a   Ganti, Apar K ^a,b   Batra, Surinder K ^a,c  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b VA NEBRASKA WESTERN IOWA HEALTH CARE SYSTEM   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Cancer; Diagnostic; Epigenetics; MiRNA; Signaling; Smoking

Indexed keywords

BIOLOGICAL MARKER; CETUXIMAB; CISPLATIN; DOCETAXEL; DOXORUBICIN; ETOPOSIDE; GEFITINIB; MICRORNA; PACLITAXEL;

BIOGENESIS; DRUG TARGETING; EPIGENETICS; HEAD AND NECK SQUAMOUS CELL CARCINOMA; LUNG CANCER; PANCREAS CANCER; REVIEW; SIGNAL TRANSDUCTION; SMOKING; UTERINE CERVIX CANCER;

CANCER; DIAGNOSTIC; EPIGENETICS; MIRNA; SIGNALING; SMOKING;

ANIMALS; DRUG RESISTANCE, NEOPLASM; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MICRORNAS; NEOPLASMS; RADIATION TOLERANCE; SIGNAL TRANSDUCTION; SMOKING;

EID: 84891372058     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2013.10.005     Document Type: Review

References (122)

1. Lewis B.P., et al. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
2. Yue D., et al. Survey of computational algorithms for microRNA target prediction. Curr. Genomics 2009, 10:478-492.
3. Iorio M.V., Croce C.M. MicroRNAs in cancer: small molecules with a huge impact. J. Clin. Oncol. 2009, 27:5848-5856.
4. Schembri F., et al. MicroRNAs as modulators of smoking-induced gene expression changes in human airway epithelium. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2319-2324.
5. Blakely T., et al. The association of active smoking with multiple cancers: national census-cancer registry cohorts with quantitative bias analysis. Cancer Causes Control 2013, 24:1243-1255.
6. Momi N., et al. Nicotine/cigarette smoke promotes metastasis of pancreatic cancer through α7nAChR-mediated MUC4 upregulation. Oncogene 2012, 32:1384-1395.
7. Tobacco Smoke and Involuntary Smoking. IARC Monogr Eval Carcinog Risks Hum. 2004, 83:161-264. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans.
8. Winter J., Diederichs S. MicroRNA biogenesis and cancer. Methods Mol. Biol. 2011, 676:3-22.
9. Yi R., et al. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 2003, 17:3011-3016.
10. Lin S.L., et al. Asymmetry of intronic pre-miRNA structures in functional RISC assembly. Gene 2005, 356:32-38.
11. Calin G.A., et al. Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:15524-15529.
12. Volinia S., et al. Reprogramming of miRNA networks in cancer and leukemia. Genome Res. 2010, 20:589-599.
13. Wang J., et al. TransmiR: a transcription factor-microRNA regulation database. Nucleic Acids Res. 2010, 38:D119-D122.
14. Szafranska-Schwarzbach A.E., et al. Development of a miRNA-based diagnostic assay for pancreatic ductal adenocarcinoma. Exp. Rev. Mol. Diagn. 2011, 11:249-257.
15. La Conti J.J., et al. Tissue and serum microRNAs in the Kras(G12D) transgenic animal model and in patients with pancreatic cancer. PLoS ONE 2011, 6:e20687.
16. Ozcan S. MiR-30 family and EMT in human fetal pancreatic islets. Islets 2009, 1:283-285.
17. Sureban S.M., et al. DCAMKL-1 regulates epithelial-mesenchymal transition in human pancreatic cells through a miR-200a-dependent mechanism. Cancer Res. 2011, 71:2328-2338.
18. Hao J., et al. MicroRNA 421 suppresses DPC4/Smad4 in pancreatic cancer. Biochem. Biophys. Res. Commun. 2011, 406:552-557.
19. Lu Z., et al. miR-301a as an NF-κB activator in pancreatic cancer cells. EMBO J. 2011, 30:57-67.
20. Ohuchida K., et al. MicroRNA expression as a predictive marker for gemcitabine response after surgical resection of pancreatic cancer. Ann. Surg. Oncol. 2011, 18:2381-2387.
21. Preis M., et al. MicroRNA-10b expression correlates with response to neoadjuvant therapy and survival in pancreatic ductal adenocarcinoma. Clin. Cancer Res. 2011, 17:5812-5821.
22. Zheng Z.M., Wang X. Regulation of cellular miRNA expression by human papillomaviruses. Biochim. Biophys. Acta 2011, 1809:668-677.
23. Li B., et al. Reduced miR-34a expression in normal cervical tissues and cervical lesions with high-risk human papillomavirus infection. Int. J. Gynecol. Cancer 2010, 20:597-604.
24. Li Y., et al. High-risk human papillomavirus reduces the expression of microRNA-218 in women with cervical intraepithelial neoplasia. J. Int. Med. Res. 2010, 38:1730-1736.
25. Muralidhar B., et al. Functional evidence that Drosha overexpression in cervical squamous cell carcinoma affects cell phenotype and microRNA profiles. J. Pathol. 2011, 224:496-507.
26. Tian R.Q., et al. MicroRNA-372 is down-regulated and targets cyclin-dependent kinase 2 (CDK2) and cyclin A1 in human cervical cancer, which may contribute to tumorigenesis. J. Biol. Chem. 2011, 286:25556-25563.
27. Li J.H., et al. MicroRNA miR-886-5p inhibits apoptosis by down-regulating Bax expression in human cervical carcinoma cells. Gynecol. Oncol. 2011, 120:145-151.
28. Lajer C.B., et al. The role of miRNAs in human papilloma virus (HPV)-associated cancers: bridging between HPV-related head and neck cancer and cervical cancer. Br. J. Cancer 2012, 106:1526-1534.
29. Hsu C.M., et al. Circulating miRNA is a novel marker for head and neck squamous cell carcinoma. Tumour Biol. 2012, 33:1933-1942.
30. Bourguignon L.Y., et al. Stem cell marker (Nanog) and Stat-3 signaling promote microRNA-21 expression and chemoresistance in hyaluronan/CD44-activated head and neck squamous cell carcinoma cells. Oncogene 2012, 31:149-160.
31. Chen Z., et al. Down-regulation of the microRNA-99 family members in head and neck squamous cell carcinoma. Oral Oncol. 2012, 48:686-691.
32. Nohata N., et al. miR-1 as a tumor suppressive microRNA targeting TAGLN2 in head and neck squamous cell carcinoma. Oncotarget 2011, 2:29-42.
33. Zhang L., et al. MicroRNA-135b acts as a tumor promoter by targeting the hypoxia-inducible factor pathway in genetically defined mouse model of head and neck squamous cell carcinoma. Cancer Lett. 2013, 331:230-238.
34. Datta J., et al. microRNA-107 functions as a candidate tumor-suppressor gene in head and neck squamous cell carcinoma by downregulation of protein kinase Cvare. Oncogene 2012, 31:4045-4053.
35. Kinoshita T., et al. Tumor suppressive microRNA-133a regulates novel targets: moesin contributes to cancer cell proliferation and invasion in head and neck squamous cell carcinoma. Biochem. Biophys. Res. Commun. 2012, 418:378-383.
36. Kinoshita T., et al. Tumor suppressive microRNA-218 inhibits cancer cell migration and invasion through targeting laminin-332 in head and neck squamous cell carcinoma. Oncotarget 2012, 3:1386-1400.
37. Weber B., et al. Methylation of human microRNA genes in normal and neoplastic cells. Cell Cycle 2007, 6:1001-1005.
38. Watanabe K., et al. Genome structure-based screening identified epigenetically silenced microRNA associated with invasiveness in non-small-cell lung cancer. Int. J. Cancer 2012, 130:2580-2590.
39. Fazi F., et al. Epigenetic silencing of the myelopoiesis regulator microRNA-223 by the AML1/ETO oncoprotein. Cancer Cell 2007, 12:457-466.
40. Lujambio A., et al. A microRNA DNA methylation signature for human cancer metastasis. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:13556-13561.
41. Esteller M. Epigenetic gene silencing in cancer: the DNA hypermethylome. Hum. Mol. Genet. 2007, 16:R50-R59.
42. Li A., et al. Pancreatic cancers epigenetically silence SIP1 and hypomethylate and overexpress miR-200a/200b in association with elevated circulating miR-200a and miR-200b levels. Cancer Res. 2010, 70:5226-5237.
43. Saito Y., et al. Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 2006, 9:435-443.
44. Fabbri M., et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:15805-15810.
45. Duursma A.M., et al. miR-148 targets human DNMT3b protein coding region. RNA 2008, 14:872-877.
46. Scott G.K., et al. Rapid alteration of microRNA levels by histone deacetylase inhibition. Cancer Res. 2006, 66:1277-1281.
47. O'Hara S.P., et al. NFκB p50-CCAAT/enhancer-binding protein β (C/EBPβ)-mediated transcriptional repression of microRNA let-7i following microbial infection. J. Biol. Chem. 2010, 285:216-225.
48. Noonan E.J., et al. miR-449a targets HDAC-1 and induces growth arrest in prostate cancer. Oncogene 2009, 28:1714-1724.
49. Tuddenham L., et al. The cartilage specific microRNA-140 targets histone deacetylase 4 in mouse cells. FEBS Lett. 2006, 580:4214-4217.
50. McCabe M.T., et al. Cancer DNA methylation: molecular mechanisms and clinical implications. Clin. Cancer Res. 2009, 15:3927-3937.
51. Benetti R., et al. A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases. Nat. Struct. Mol. Biol. 2008, 15:998.
52. Jones J.G., et al. Increased alveolar epithelial permeability in cigarette smokers. Lancet 1980, 1:66-68.
53. Pleasance E.D., et al. A small-cell lung cancer genome with complex signatures of tobacco exposure. Nature 2010, 463:184-190.
54. Mathis C., et al. Human bronchial epithelial cells exposed in vitro to cigarette smoke at the air-liquid interface resemble bronchial epithelium from human smokers. Am. J. Physiol. Lung Cell. Mol. Physiol. 2013, 304:L489-L503.
55. Huang W., Li M.D. Differential allelic expression of dopamine D1 receptor gene (DRD1) is modulated by microRNA miR-504. Biol. Psychiatry 2009, 65:702-705.
56. Seike M., et al. MiR-21 is an EGFR-regulated anti-apoptotic factor in lung cancer in never-smokers. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:12085-12090.
57. Wong D.W., et al. The EML4-ALK fusion gene is involved in various histologic types of lung cancers from nonsmokers with wild-type EGFR and KRAS. Cancer 2009, 115:1723-1733.
58. Calin G.A., et al. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:2999-3004.
59. Yanaihara N., et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006, 9:189-198.
60. Izzotti A., et al. Chemoprevention of genome, transcriptome, and proteome alterations induced by cigarette smoke in rat lung. Eur. J. Cancer 2005, 41:1864-1874.
61. Duan R., et al. Single nucleotide polymorphism associated with mature miR-125a alters the processing of pri-miRNA. Hum. Mol. Genet. 2007, 16:1124-1131.
62. Landi M.T., et al. MicroRNA expression differentiates histology and predicts survival of lung cancer. Clin. Cancer Res. 2010, 16:430-441.
63. Yu L., et al. Early detection of lung adenocarcinoma in sputum by a panel of microRNA markers. Int. J. Cancer 2010, 127:2870-2878.
64. Vosa U., et al. Identification of miR-374a as a prognostic marker for survival in patients with early-stage nonsmall cell lung cancer. Genes Chromosomes Cancer 2011, 50:812-822.
65. Kalscheuer S., et al. Differential expression of microRNAs in early-stage neoplastic transformation in the lungs of F344 rats chronically treated with the tobacco carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone. Carcinogenesis 2008, 29:2394-2399.
66. Puissegur M.P., et al. miR-210 is overexpressed in late stages of lung cancer and mediates mitochondrial alterations associated with modulation of HIF-1 activity. Cell Death Differ. 2011, 18:465-478.
67. Heegaard N.H., et al. Circulating micro-RNA expression profiles in early stage nonsmall cell lung cancer. Int. J. Cancer 2012, 130:1378-1386.
68. Wang Z.X., et al. Prognostic significance of serum miRNA-21 expression in human non-small cell lung cancer. J. Surg. Oncol. 2011, 104:847-851.
69. Liu X.G., et al. High expression of serum miR-21 and tumor miR-200c associated with poor prognosis in patients with lung cancer. Med. Oncol. 2012, 29:618-626.
70. Lu J., et al. MicroRNA expression profiles classify human cancers. Nature 2005, 435:834-838.
71. Amos C.I., et al. Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1. Nat. Genet. 2008, 40:616-622.
72. Hung R.J., et al. A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25. Nature 2008, 452:633-637.
73. Slebos R.J., et al. Relationship between K-ras oncogene activation and smoking in adenocarcinoma of the human lung. J. Natl. Cancer Inst. 1991, 83:1024-1027.
74. Le C.F., et al. TP53 and KRAS mutation load and types in lung cancers in relation to tobacco smoke: distinct patterns in never, former, and current smokers. Cancer Res. 2005, 65:5076-5083.
75. Mounawar M., et al. Patterns of EGFR, HER2, TP53, and KRAS mutations of p14arf expression in non-small cell lung cancers in relation to smoking history. Cancer Res. 2007, 67:5667-5672.
76. Chin L.J., et al. A SNP in a let-7 microRNA complementary site in the KRAS 3' untranslated region increases non-small cell lung cancer risk. Cancer Res. 2008, 68:8535-8540.
77. Lee Y.J., et al. Dose effect of cigarette smoking on frequency and spectrum of epidermal growth factor receptor gene mutations in Korean patients with non-small cell lung cancer. J. Cancer Res. Clin. Oncol. 2010, 136:1937-1944.
78. Izzotti A., et al. Downregulation of microRNA expression in the lungs of rats exposed to cigarette smoke. FASEB J. 2009, 23:806-812.
79. D'Alessio A.C., Szyf M. Epigenetic tete-a-tete: the bilateral relationship between chromatin modifications and DNA methylation. Biochem. Cell Biol. 2006, 84:463-476.
80. Kopelovich L., et al. The epigenome as a target for cancer chemoprevention. J. Natl. Cancer Inst. 2003, 95:1747-1757.
81. Belinsky S.A., et al. Aberrant promoter methylation in bronchial epithelium and sputum from current and former smokers. Cancer Res. 2002, 62:2370-2377.
82. Kim J.S., et al. Aberrant methylation of the FHIT gene in chronic smokers with early stage squamous cell carcinoma of the lung. Carcinogenesis 2004, 25:2165-2171.
83. Russo A.L., et al. Differential DNA hypermethylation of critical genes mediates the stage-specific tobacco smoke-induced neoplastic progression of lung cancer. Clin. Cancer Res. 2005, 11:2466-2470.
84. Vuillemenot B.R., et al. Gene promoter hypermethylation in mouse lung tumors. Mol. Cancer Res. 2006, 4:267-273.
85. Leng S., et al. Haplotypes of DNMT1 and DNMT3B are associated with mutagen sensitivity induced by benzo[a]pyrene diol epoxide among smokers. Carcinogenesis 2008, 29:1380-1385.
86. Liu H., et al. Cigarette smoke induces demethylation of prometastatic oncogene synuclein-γ in lung cancer cells by downregulation of DNMT3B. Oncogene 2007, 26:5900-5910.
87. Yang S.R., et al. Cigarette smoke induces proinflammatory cytokine release by activation of NF-κB and post-translational modifications of histone deacetylase in macrophages. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 291:L46-L57.
88. Tellez C.S., et al. EMT and stem cell-like properties associated with miR-205 and miR-200 epigenetic silencing are early manifestations during carcinogen-induced transformation of human lung epithelial cells. Cancer Res. 2011, 71:3087-3097.
89. Xi S., et al. Cigarette smoke mediates epigenetic repression of miR-487b during pulmonary carcinogenesis. J. Clin. Invest. 2013, 123:1241-1261.
90. Tessema M., et al. Concomitant promoter methylation of multiple genes in lung adenocarcinomas from current, former and never smokers. Carcinogenesis 2009, 30:1132-1138.
91. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
92. Kim D.H., et al. Promoter methylation of DAP-kinase: association with advanced stage in non-small cell lung cancer. Oncogene 2001, 20:1765-1770.
93. Hamilton M., et al. Effects of smoking on the pharmacokinetics of erlotinib. Clin. Cancer Res. 2006, 12:2166-2171.
94. Burnett J.C., et al. Current progress of siRNA/shRNA therapeutics in clinical trials. Biotechnol. J. 2011, 6:1130-1146.
95. Ebert M.S., et al. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat. Methods 2007, 4:721-726.
96. Krutzfeldt J., et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005, 438:685-689.
97. Lennox K.A., Behlke M.A. Chemical modification and design of anti-miRNA oligonucleotides. Gene Ther. 2011, 18:1111-1120.
98. Esau C., et al. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab. 2006, 3:87-98.
99. Henke J.I., et al. microRNA-122 stimulates translation of hepatitis C virus RNA. EMBO J. 2008, 27:3300-3310.
100. Zeisel M.B., et al. Host-targeting agents for prevention and treatment of chronic hepatitis C - perspectives and challenges. J. Hepatol. 2013, 58:375-384.
101. Trang P., et al. Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol. Ther. 2011, 19:1116-1122.
102. Ma L., et al. Expression of miR-122 mediated by adenoviral vector induces apoptosis and cell cycle arrest of cancer cells. Cancer Biol. Ther. 2010, 9:554-561.
103. Chen Y., et al. Nanoparticles modified with tumor-targeting scFv deliver siRNA and miRNA for cancer therapy. Mol. Ther. 2010, 18:1650-1656.
104. Wu Y., et al. MicroRNA delivery by cationic lipoplexes for lung cancer therapy. Mol. Pharm. 2011, 8:1381-1389.
105. Belinsky S.A., et al. Inhibition of DNA methylation and histone deacetylation prevents murine lung cancer. Cancer Res. 2003, 63:7089-7093.
106. Harris R.C., et al. EGF receptor ligands. Exp. Cell Res. 2003, 284:2-13.
107. Ishikawa N., et al. Increases of amphiregulin and transforming growth factor-α in serum as predictors of poor response to gefitinib among patients with advanced non-small cell lung cancers. Cancer Res. 2005, 65:9176-9184.
108. Blobel C.P. ADAMs: key components in EGFR signalling and development. Nat. Rev. Mol. Cell Biol. 2005, 6:32-43.
109. Lemjabbar H., et al. Tobacco smoke-induced lung cell proliferation mediated by tumor necrosis factor α-converting enzyme and amphiregulin. J. Biol. Chem. 2003, 278:26202-26207.
110. Toyooka S., et al. Mutational and epigenetic evidence for independent pathways for lung adenocarcinomas arising in smokers and never smokers. Cancer Res. 2006, 66:1371-1375.
111. Vasudevan K.M., et al. Suppression of PTEN expression by NF-κB prevents apoptosis. Mol. Cell. Biol. 2004, 24:1007-1021.
112. Holleman A., et al. miR-135a contributes to paclitaxel resistance in tumor cells both in vitro and in vivo. Oncogene 2011, 30:4386-4398.
113. Rui W., et al. Identification of microRNA profiles in docetaxel-resistant human non-small cell lung carcinoma cells (SPC-A1). J. Cell. Mol. Med. 2010, 14:206-214.
114. Xie L., et al. Cell-free miRNAs may indicate diagnosis and docetaxel sensitivity of tumor cells in malignant effusions. BMC Cancer 2010, 10:591.
115. Guo L., et al. Gene expression profiling of drug-resistant small cell lung cancer cells by combining microRNA and cDNA expression analysis. Eur. J. Cancer 2010, 46:1692-1702.
116. Wang X.C., et al. Expression and function of miRNA in postoperative radiotherapy sensitive and resistant patients of non-small cell lung cancer. Lung Cancer 2011, 72:92-99.
117. Zhang J.G., et al. MicroRNA-101 exerts tumor-suppressive functions in non-small cell lung cancer through directly targeting enhancer of zeste homolog 2. J. Thorac. Oncol. 2011, 6:671-678.
118. Galluzzi L., et al. miR-181a and miR-630 regulate cisplatin-induced cancer cell death. Cancer Res. 2010, 70:1793-1803.
119. Zhu W., et al. miR-497 modulates multidrug resistance of human cancer cell lines by targeting BCL2. Med. Oncol. 2012, 29:384-391.
120. Ceppi P., et al. Loss of miR-200c expression induces an aggressive, invasive, and chemoresistant phenotype in non-small cell lung cancer. Mol. Cancer Res. 2010, 8:1207-1216.
121. Nasser M.W., et al. Down-regulation of micro-RNA-1 (miR-1) in lung cancer. Suppression of tumorigenic property of lung cancer cells and their sensitization to doxorubicin-induced apoptosis by miR-1. J. Biol. Chem. 2008, 283:33394-33405.
122. Zhong M., et al. MicroRNAs reduce tumor growth and contribute to enhance cytotoxicity induced by gefitinib in non-small cell lung cancer. Chem. Biol. Interact. 2010, 184:431-438.