The Role of MicroRNAs in Lung Cancer: Implications for Diagnosis and Therapy

Author(s): Parisa Naeli, Fatemeh Yousefi, Younes Ghasemi, Amir Savardashtaki*, Hamed Mirzaei*

Journal Name: Current Molecular Medicine

Volume 20 , Issue 2 , 2020

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer

Abstract:

Lung cancer is the first cause of cancer death in the world due to its high prevalence, aggressiveness, late diagnosis, lack of effective treatment and poor prognosis. It also shows high rate of recurrence, metastasis and drug resistance. All these problems highlight the urgent needs for developing new strategies using noninvasive biomarkers for early detection, metastasis and recurrence of disease. MicroRNAs (miRNAs) are a class of small noncoding RNAs that regulate gene expression post-transcriptionally. These molecules found to be abnormally expressed in increasing number of human disease conditions including cancer. miRNAs could be detected in body fluids such as blood, serum, urine and sputum, which leads us towards the idea of using them as non-invasive biomarker for cancer detection and monitoring cancer treatment and recurrence. miRNAs are found to be deregulated in lung cancer initiation and progression and could regulate lung cancer cell proliferation and invasion. In this review, we summarized recent progress and discoveries in microRNAs regulatory role in lung cancer initiation and progression. In addition, the role of microRNAs in EGFR signaling pathway regulation is discussed briefly.

Keywords: Lung cancer, microRNA, biomarker, diagnosis, therapy, cell death, biomarkers.

[1]
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin 2019; 69: 7-34.
[http://dx.doi.org/10.3322/caac.21551]
[2]
Travis WD, Brambilla E, Burke AP, Marx A, Nicholson AG. Introduction to The 2015 World Health Organization Classification of Tumors of the Lung, Pleura, Thymus, and Heart. J Thorac Oncol 2015; 10: 1240-2.
[http://dx.doi.org/10.1097/JTO.0000000000000663]
[3]
Mirzaei HR, Sahebkar A, Salehi R, et al. Boron neutron capture therapy: Moving toward targeted cancer therapy. J Cancer Res Ther 2016; 12: 520-5.
[http://dx.doi.org/10.4103/0973-1482.176167]
[4]
Mirzaei HR, Mirzaei H, Lee SY, Hadjati J, Till BG. Prospects for chimeric antigen receptor (CAR) gammadelta T cells: A potential game changer for adoptive T cell cancer immunotherapy. Cancer Lett 2016; 380: 413-23.
[http://dx.doi.org/10.1016/j.canlet.2016.07.001]
[5]
Mirzaei H, Sahebkar A, Sichani LS, et al. Therapeutic application of multipotent stem cells. J Cell Physiol 2018; 233: 2815-23.
[http://dx.doi.org/10.1002/jcp.25990]
[6]
Mirzaei H, Sahebkar A, Jaafari MR, et al. PiggyBac as a novel vector in cancer gene therapy: current perspective. Cancer Gene Ther 2016; 23: 45-7.
[http://dx.doi.org/10.1038/cgt.2015.68]
[7]
Moradian Tehrani R, Verdi J, Noureddini M, et al. Mesenchymal stem cells: A new platform for targeting suicide genes in cancer 2018; 233: pp.. 3831-45.
[http://dx.doi.org/10.1002/jcp.26094]
[8]
Mirzaei H, Salehi H, Oskuee RK, et al. The therapeutic potential of human adipose-derived mesenchymal stem cells producing CXCL10 in a mouse melanoma lung metastasis model. Cancer Lett 2018; 419: 30-9.
[http://dx.doi.org/10.1016/j.canlet.2018.01.029]
[9]
Hashemi Goradel N, Ghiyami-Hour F, Jahangiri S, et al. Nanoparticles as new tools for inhibition of cancer angiogenesis 2018; 233: pp.. 2902-10.
[http://dx.doi.org/10.1002/jcp.26029]
[10]
Cheng L, Alexander RE, Maclennan GT, et al. Molecular pathology of lung cancer: key to personalized medicine. Mod Pathol 2012; 25: 347-69.
[http://dx.doi.org/10.1038/modpathol.2011.215]
[11]
Wangari-Talbot J, Hopper-Borge E. Drug resistance mechanisms in non-small cell lung carcinoma. J Cancer Res Updates 2013; 2: 265-82.
[12]
Noone AM, Cronin KA, Altekruse SF, et al. Cancer incidence and survival trends by subtype using data from the surveillance epidemiology and end results program, 1992-2013. Cancer Epidemiol Biomarkers Prev 2017; 26: 632-41.
[http://dx.doi.org/10.1158/1055-9965.EPI-16-0520]
[13]
Sigismund S, Avanzato D, Lanzetti L. Emerging functions of the EGFR in cancer. Mol Oncol 2018; 12: 3-20.
[http://dx.doi.org/10.1002/1878-0261.12155]
[14]
Vallath S, Hynds RE, Succony L, Janes SM, Giangreco A. Targeting EGFR signalling in chronic lung disease: therapeutic challenges and opportunities. Eur Respir J 2014; 44: 513-22.
[http://dx.doi.org/10.1183/09031936.00146413]
[15]
Vafadar A, Shabaninejad Z, Movahedpour A, et al. Long non-coding rnas: epigenetic regulators in cancer. Curr Pharm Des 2019. Epub ahead of print
[http://dx.doi.org/10.2174/1381612825666190830161528]
[16]
Shabaninejad Z, Vafadar A, Movahedpour A, et al. Circular RNAs in cancer: new insights into functions and implications in ovarian cancer. J Ovarian Res 2019; 12: 1-12.
[http://dx.doi.org/10.1186/s13048-019-0558-5]
[17]
Gholamin S, Mirzaei H. GD2-targeted immunotherapy and potential value of circulating microRNAs in neuroblastoma. 2018; 233: pp.. 866-79.
[http://dx.doi.org/10.1002/jcp.25793]
[18]
O’Brien J, Hayder H, Zayed Y, Peng C. Overview of MicroRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol (Lausanne) 2018; 9: 402.
[http://dx.doi.org/10.3389/fendo.2018.00402]
[19]
Seok H, Ham J, Jang ES, Chi SW. MicroRNA target recognition: insights from transcriptome-wide non-canonical interactions. Mol Cells 2016; 39: 375-81.
[http://dx.doi.org/10.14348/molcells.2016.0013]
[20]
Jamali L, Tofigh R, Tutunchi S, et al. Circulating microRNAs as diagnostic and therapeutic biomarkers in gastric and esophageal cancers 2018; 233: pp.. 8538-50.
[http://dx.doi.org/10.1002/jcp.26850]
[21]
Iqbal MA, Arora S, Prakasam G, Calin GA, Syed MA. MicroRNA in lung cancer: role, mechanisms, pathways and therapeutic relevance. Mol Aspects Med 2018; pii: S0098-2997(18): 30065-7.
[http://dx.doi.org/10.1016/j.mam.2018.07.003]
[22]
Dong F, Xu T, Shen Y, et al. Dysregulation of miRNAs in bladder cancer: altered expression with aberrant biogenesis procedure. Oncotarget 2017; 8: 27547-68.
[http://dx.doi.org/10.18632/oncotarget.15173]
[23]
Tsai HP, Huang SF, Li CF, Chien HT, Chen SC. Differential microRNA expression in breast cancer with different onset age. PLoS One 2018; 13: e0191195
[http://dx.doi.org/10.1371/journal.pone.0191195]
[24]
Pileczki V, Cojocneanu-Petric R, Maralani M, Neagoe IB, Sandulescu R. MicroRNAs as regulators of apoptosis mechanisms in cancer. Clujul Med 2016; 89: 50-5.
[25]
Yao S. MicroRNA biogenesis and their functions in regulating stem cell potency and differentiation. Biol Proced Online 2016; 18: 8.
[http://dx.doi.org/10.1186/s12575-016-0037-y]
[26]
Lawrie CH, Gal S, Dunlop HM, et al. Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br J Haematol 2008; 141: 672-5.
[http://dx.doi.org/10.1111/j.1365-2141.2008.07077.x]
[27]
Wang K. The Ubiquitous Existence of MicroRNA in Body Fluids. Clin Chem 2017; 63: 784-5.
[http://dx.doi.org/10.1373/clinchem.2016.267625]
[28]
Lee Y, Kim M, Han J, et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004; 23: 4051-60.
[http://dx.doi.org/10.1038/sj.emboj.7600385]
[29]
Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 2006; 13: 1097-101.
[http://dx.doi.org/10.1038/nsmb1167]
[30]
Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 2003; 17: 3011-6.
[http://dx.doi.org/10.1101/gad.1158803]
[31]
Shabaninejad Z, Yousefi F, Movahedpour A, et al. Electrochemical-based biosensors for microRNA detection: Nanotechnology comes into view. Anal Biochem 2019.113349
[http://dx.doi.org/10.1016/j.ab.2019.113349]
[32]
Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136: 215-33.
[http://dx.doi.org/10.1016/j.cell.2009.01.002]
[33]
Calin GA, Dumitru CD, Shimizu M, et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2002; 99: 15524-9.
[http://dx.doi.org/10.1073/pnas.242606799]
[34]
Peng Y, Croce CM. The role of MicroRNAs in human cancer. Signal Transduct Target Ther 2016; 1: 15004.
[http://dx.doi.org/10.1038/sigtrans.2015.4]
[35]
Zhang B, Pan X, Cobb GP, Anderson TA. microRNAs as oncogenes and tumor suppressors. Dev Biol 2007; 302: 1-12.
[http://dx.doi.org/10.1016/j.ydbio.2006.08.028]
[36]
Croce CM. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 2009; 10: 704-14.
[http://dx.doi.org/10.1038/nrg2634]
[37]
Hill DA, Ivanovich J, Priest JR, et al. DICER1 mutations in familial pleuropulmonary blastoma. Science 2009; 325: 965.
[http://dx.doi.org/10.1126/science.1174334]
[38]
Diaz-Garcia CV, Agudo-Lopez A, Perez C, et al. DICER1, DROSHA and miRNAs in patients with non-small cell lung cancer: implications for outcomes and histologic classification. Carcinogenesis 2013; 34: 1031-8.
[http://dx.doi.org/10.1093/carcin/bgt022]
[39]
Karube Y, Tanaka H, Osada H, et al. Reduced expression of Dicer associated with poor prognosis in lung cancer patients. Cancer Sci 2005; 96: 111-5.
[http://dx.doi.org/10.1111/j.1349-7006.2005.00015.x]
[40]
Kumar MS, Lu J, Mercer KL, Golub TR, Jacks T. Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat Genet 2007; 39: 673-7.
[http://dx.doi.org/10.1038/ng2003]
[41]
Hata A, Kashima R. Dysregulation of microRNA biogenesis machinery in cancer. Crit Rev Biochem Mol Biol 2016; 51: 121-34.
[http://dx.doi.org/10.3109/10409238.2015.1117054]
[42]
Castro D, Moreira M, Gouveia AM, Pozza DH, De Mello RA. MicroRNAs in lung cancer. Oncotarget 2017; 8: 81679-85.
[http://dx.doi.org/10.18632/oncotarget.20955]
[43]
Zhang Y, Sui J, Shen X, et al. Differential expression profiles of microRNAs as potential biomarkers for the early diagnosis of lung cancer. Oncol Rep 2017; 37: 3543-53.
[http://dx.doi.org/10.3892/or.2017.5612]
[44]
Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006; 103: 2257-61.
[http://dx.doi.org/10.1073/pnas.0510565103]
[45]
Yanaihara N, Caplen N, Bowman E, et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006; 9: 189-98.
[http://dx.doi.org/10.1016/j.ccr.2006.01.025]
[46]
de Groot PM, Wu CC, Carter BW, Munden RF. The epidemiology of lung cancer. Transl Lung Cancer Res 2018; 7: 220-33.
[http://dx.doi.org/10.21037/tlcr.2018.05.06]
[47]
O’Keeffe LM, Taylor G, Huxley RR, Mitchell P, Woodward M, Peters SAE. Smoking as a risk factor for lung cancer in women and men: a systematic review and meta-analysis. BMJ Open 2018;. 8e021611
[http://dx.doi.org/10.1136/bmjopen-2018-021611]
[48]
Fujii T, Shimada K, Nakai T, Ohbayashi C. MicroRNAs in smoking-related carcinogenesis: biomarkers, functions, and therapy. J Clin Med 2018; 7(5): 98.
[http://dx.doi.org/10.3390/jcm7050098]
[49]
Advani J, Subbannayya Y, Patel K, et al. Long-term cigarette smoke exposure and changes in MiRNA expression and proteome in non-small-cell lung cancer. OMICS 2017; 21: 390-403.
[http://dx.doi.org/10.1089/omi.2017.0045]
[50]
Seike M, Goto A, Okano T, et al. MiR-21 is an EGFR-regulated anti-apoptotic factor in lung cancer in never-smokers. Proc Natl Acad Sci USA 2009; 106: 12085-90.
[http://dx.doi.org/10.1073/pnas.0905234106]
[51]
Jiang M, Li X, Quan X, Li X, Zhou B. Clinically correlated micrornas in the diagnosis of non-small cell lung cancer: a systematic review and meta-analysis. BioMed Res Int 2018; 20185930951
[http://dx.doi.org/10.1155/2018/5930951]
[52]
Huang J, Wu J, Li Y, et al. Deregulation of serum microRNA expression is associated with cigarette smoking and lung cancer. BioMed Res Int 2014; 2014: 364316
[http://dx.doi.org/10.1155/2014/364316]
[53]
Landi MT, Zhao Y, Rotunno M, et al. MicroRNA expression differentiates histology and predicts survival of lung cancer. Clin Cancer Res 2010; 16: 430-41.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-1736]
[54]
Raponi M, Dossey L, Jatkoe T, et al. MicroRNA classifiers for predicting prognosis of squamous cell lung cancer. Cancer Res 2009; 69: 5776-83.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-0587]
[55]
Bjaanaes MM, Halvorsen AR, Solberg S, et al. Unique microRNA-profiles in EGFR-mutated lung adenocarcinomas. Int J Cancer 2014; 135: 1812-21.
[http://dx.doi.org/10.1002/ijc.28828]
[56]
Mirzadeh Azad F, Naeli P, Malakootian M, et al. Two lung development-related microRNAs, miR-134 and miR-187, are differentially expressed in lung tumors. Gene 2016; 577: 221-6.
[http://dx.doi.org/10.1016/j.gene.2015.11.040]
[57]
Ulivi P, Petracci E, Marisi G, et al. Prognostic role of circulating mirnas in early-stage non-small cell lung cancer. J Clin Med 2019; 8(2): 131.
[http://dx.doi.org/10.3390/jcm8020131]
[58]
Lebanony D, Benjamin H, Gilad S, et al. Diagnostic assay based on hsa-miR-205 expression distinguishes squamous from nonsquamous non-small-cell lung carcinoma. J Clin Oncol 2009; 27: 2030-7.
[http://dx.doi.org/10.1200/JCO.2008.19.4134]
[59]
Bishop JA, Benjamin H, Cholakh H, Chajut A, Clark DP, Westra WH. Accurate classification of non-small cell lung carcinoma using a novel microRNA-based approach. Clin Cancer Res 2010; 16: 610-9.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-2638]
[60]
Lu S, Kong H, Hou Y, et al. Two plasma microRNA panels for diagnosis and subtype discrimination of lung cancer. Lung Cancer 2018; 123: 44-51.
[http://dx.doi.org/10.1016/j.lungcan.2018.06.027]
[61]
Hu Y, Wang L, Gu J, Qu K, Wang Y. Identification of microRNA differentially expressed in three subtypes of non-small cell lung cancer and in silico functional analysis. Oncotarget 2017; 8: 74554-66.
[http://dx.doi.org/10.18632/oncotarget.20218]
[62]
Takamizawa J, Konishi H, Yanagisawa K, et al. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res 2004; 64: 3753-6.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-0637]
[63]
Kumar MS, Erkeland SJ, Pester RE, et al. Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proc Natl Acad Sci USA 2008; 105: 3903-8.
[http://dx.doi.org/10.1073/pnas.0712321105]
[64]
Johnson SM, Grosshans H, Shingara J, et al. RAS is regulated by the let-7 microRNA family. Cell 2005; 120: 635-47.
[http://dx.doi.org/10.1016/j.cell.2005.01.014]
[65]
Lee ST, Chu K, Oh HJ, et al. Let-7 microRNA inhibits the proliferation of human glioblastoma cells. J Neurooncol 2011; 102: 19-24.
[http://dx.doi.org/10.1007/s11060-010-0286-6]
[66]
Yu F, Yao H, Zhu P, et al. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 2007; 131: 1109-23.
[http://dx.doi.org/10.1016/j.cell.2007.10.054]
[67]
Chang TC, Zeitels LR, Hwang HW, et al. Lin-28B transactivation is necessary for Myc-mediated let-7 repression and proliferation. Proc Natl Acad Sci USA 2009; 106: 3384-9.
[http://dx.doi.org/10.1073/pnas.0808300106]
[68]
Zhou Y, Liang H, Liao Z, et al. miR-203 enhances let-7 biogenesis by targeting LIN28B to suppress tumor growth in lung cancer. Sci Rep 2017; 7: 42680.
[http://dx.doi.org/10.1038/srep42680]
[69]
Levine AJ, Hu W, Feng Z. The P53 pathway: what questions remain to be explored? Cell Death Differ 2006; 13: 1027-36.
[http://dx.doi.org/10.1038/sj.cdd.4401910]
[70]
Williams AB, Schumacher B. p53 in the DNA-damage-repair process. Cold Spring Harb Perspect Med 2016; 6(5 ) a026070
[71]
He L, He X, Lim LP, et al. A microRNA component of the p53 tumour suppressor network. Nature 2007; 447: 1130-4.
[http://dx.doi.org/10.1038/nature05939]
[72]
Raver-Shapira N, Marciano E, Meiri E, et al. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 2007; 26: 731-43.
[http://dx.doi.org/10.1016/j.molcel.2007.05.017]
[73]
Hunten S, Siemens H, Kaller M, Hermeking H. The p53/microRNA network in cancer: experimental and bioinformatics approaches. Adv Exp Med Biol 2013; 774: 77-101.
[http://dx.doi.org/10.1007/978-94-007-5590-1_5]
[74]
Li Y, Guessous F, Zhang Y, et al. MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res 2009; 69: 7569-76.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-0529]
[75]
Guessous F, Zhang Y, Kofman A, et al. microRNA-34a is tumor suppressive in brain tumors and glioma stem cells. Cell Cycle 2010; 9: 1031-6.
[http://dx.doi.org/10.4161/cc.9.6.10987]
[76]
Slabakova E, Culig Z, Remsik J, Soucek K. Alternative mechanisms of miR-34a regulation in cancer. Cell Death Dis 2017.8e3100
[http://dx.doi.org/10.1038/cddis.2017.495]
[77]
Migliore C, Petrelli A, Ghiso E, et al. MicroRNAs impair MET-mediated invasive growth. Cancer Res 2008; 68: 10128-36.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-2148]
[78]
Kasinski AL, Slack FJ. miRNA-34 prevents cancer initiation and progression in a therapeutically resistant K-ras and p53-induced mouse model of lung adenocarcinoma. Cancer Res 2012; 72: 5576-87.
[http://dx.doi.org/10.1158/0008-5472.CAN-12-2001]
[79]
Daugaard I, Knudsen A, Kjeldsen TE, Hager H, Hansen LL. The association between miR-34 dysregulation and distant metastases formation in lung adenocarcinoma. Exp Mol Pathol 2017; 102: 484-91.
[http://dx.doi.org/10.1016/j.yexmp.2017.05.012]
[80]
Xiao W, Zhong Y, Wu L, Yang D, Ye S, Zhang M. Prognostic value of microRNAs in lung cancer: A systematic review and meta-analysis. Mol Clin Oncol 2019; 10: 67-77.
[81]
Zhan B, Lu D, Luo P, Wang B. Prognostic value of expression of MicroRNAs in non-small cell lung cancer: a systematic review and meta-analysis. Clin Lab 2016; 62: 2203-11.
[http://dx.doi.org/10.7754/Clin.Lab.2016.160426]
[82]
Saadatpour Z, Rezaei A, Ebrahimnejad H, et al. Imaging techniques: new avenues in cancer gene and cell therapy. Cancer Gene Ther 2017; 24: 1-5.
[http://dx.doi.org/10.1038/cgt.2016.61]
[83]
Saadatpour Z, Bjorklund G, Chirumbolo S, et al. Molecular imaging and cancer gene therapy. Cancer Gene Ther 2016. Epub ahead of print
[http://dx.doi.org/10.1038/cgt.2016.62]
[84]
Keshavarzi M, Sorayayi S, Jafar Rezaei M, et al. MicroRNAs-based imaging techniques in cancer diagnosis and therapy 2017; 118: 4121-8.
[85]
Movahedpour A, Ahmadi N, Ghasemi Y, Savardashtaki A, Shabaninejad Z. Circulating microRNAs as potential diagnostic biomarkers and therapeutic targets in prostate cancer: Current status and future perspectives. J Cell Biochem 2019; 120: 16316-29.
[http://dx.doi.org/10.1002/jcb.29053]
[86]
Mitchell PS, Parkin RK, Kroh EM, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 2008; 105: 10513-8.
[http://dx.doi.org/10.1073/pnas.0804549105]
[87]
Gyoba J, Shan S, Roa W, Bedard EL. Diagnosing lung cancers through examination of Micro-RNA biomarkers in blood, plasma, serum and sputum: a review and summary of current literature. Int J Mol Sci 2016; 17: 494.
[http://dx.doi.org/10.3390/ijms17040494]
[88]
Rabinowits G, Gercel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer 2009; 10: 42-6.
[http://dx.doi.org/10.3816/CLC.2009.n.006]
[89]
Zheng D, Haddadin S, Wang Y, et al. Plasma microRNAs as novel biomarkers for early detection of lung cancer. Int J Clin Exp Pathol 2011; 4: 575-86.
[90]
Wozniak MB, Scelo G, Muller DC, Mukeria A, Zaridze D, Brennan P. Circulating MicroRNAs as non-invasive biomarkers for early detection of non-small-cell lung cancer. PLoS One 2015; 10: e0125026
[http://dx.doi.org/10.1371/journal.pone.0125026]
[91]
Xie Y, Todd NW, Liu Z, et al. Altered miRNA expression in sputum for diagnosis of non-small cell lung cancer. Lung Cancer 2010; 67: 170-6.
[http://dx.doi.org/10.1016/j.lungcan.2009.04.004]
[92]
Yu L, Todd NW, Xing L, et al. Early detection of lung adenocarcinoma in sputum by a panel of microRNA markers. Int J Cancer 2010; 127: 2870-8.
[http://dx.doi.org/10.1002/ijc.25289]
[93]
Xing L, Todd NW, Yu L, Fang H, Jiang F. Early detection of squamous cell lung cancer in sputum by a panel of microRNA markers. Mod Pathol 2010; 23: 1157-64.
[http://dx.doi.org/10.1038/modpathol.2010.111]
[94]
Le HB, Zhu WY, Chen DD, et al. Evaluation of dynamic change of serum miR-21 and miR-24 in pre- and post-operative lung carcinoma patients. Med Oncol 2012; 29: 3190-7.
[http://dx.doi.org/10.1007/s12032-012-0303-z]
[95]
Leidinger P, Keller A, Backes C, Huwer H, Meese E. MicroRNA expression changes after lung cancer resection: a follow-up study. RNA Biol 2012; 9: 900-10.
[http://dx.doi.org/10.4161/rna.20107]
[96]
Aiso T, Ohtsuka K, Ueda M, et al. Serum levels of candidate microRNA diagnostic markers differ among the stages of non-small-cell lung cancer. Oncol Lett 2018; 16: 6643-51.
[http://dx.doi.org/10.3892/ol.2018.9464]
[97]
Zhu Y, Li T, Chen G, et al. Identification of a serum microRNA expression signature for detection of lung cancer, involving miR-23b, miR-221, miR-148b and miR-423-3p. Lung Cancer 2017; 114: 6-11.
[http://dx.doi.org/10.1016/j.lungcan.2017.10.002]
[98]
Leng Q, Lin Y, Jiang F, et al. A plasma miRNA signature for lung cancer early detection. Oncotarget 2017; 8: 111902-11.
[http://dx.doi.org/10.18632/oncotarget.22950]
[99]
Wee P, Wang Z. Epidermal growth factor receptor cell proliferation signaling pathways. Cancers (Basel) 2017; 9(5): 52.
[100]
Modjtahedi H, Essapen S. Epidermal growth factor receptor inhibitors in cancer treatment: advances, challenges and opportunities. Anticancer Drugs 2009; 20: 851-5.
[http://dx.doi.org/10.1097/CAD.0b013e3283330590]
[101]
Downward J, Yarden Y, Mayes E, et al. Close similarity of epidermal growth factor receptor and v-erb-B oncogene protein sequences. Nature 1984; 307: 521-7.
[http://dx.doi.org/10.1038/307521a0]
[102]
Hirsch FR, Varella-Garcia M, Bunn PA Jr, et al. Epidermal growth factor receptor in non-small-cell lung carcinomas: correlation between gene copy number and protein expression and impact on prognosis. J Clin Oncol 2003; 21: 3798-807.
[http://dx.doi.org/10.1200/JCO.2003.11.069]
[103]
Suzuki S, Dobashi Y, Sakurai H, Nishikawa K, Hanawa M, Ooi A. Protein overexpression and gene amplification of epidermal growth factor receptor in nonsmall cell lung carcinomas. An immunohistochemical and fluorescence in situ hybridization study. Cancer 2005; 103: 1265-73.
[http://dx.doi.org/10.1002/cncr.20909]
[104]
Liu TC, Jin X, Wang Y, Wang K. Role of epidermal growth factor receptor in lung cancer and targeted therapies. Am J Cancer Res 2017; 7: 187-202.
[105]
Han F, He J, Li F, et al. Emerging roles of MicroRNAs in EGFR-targeted therapies for lung cancer. BioMed Res Int 2015; 2015: 672759
[http://dx.doi.org/10.1155/2015/672759]
[106]
Dacic S, Kelly L, Shuai Y, Nikiforova MN. miRNA expression profiling of lung adenocarcinomas: correlation with mutational status. Mod Pathol 2010; 23: 1577-82.
[http://dx.doi.org/10.1038/modpathol.2010.152]
[107]
Foley NH, Bray IM, Tivnan A, et al. MicroRNA-184 inhibits neuroblastoma cell survival through targeting the serine/threonine kinase AKT2. Mol Cancer 2010; 9: 83.
[http://dx.doi.org/10.1186/1476-4598-9-83]
[108]
Chan LW, Wang FF, Cho WC. Genomic sequence analysis of EGFR regulation by microRNAs in lung cancer. Curr Top Med Chem 2012; 12: 920-6.
[http://dx.doi.org/10.2174/156802612800166747]
[109]
Petriella D, Galetta D, Rubini V, et al. Molecular profiling of thin-prep FNA samples in assisting clinical management of non-small-cell lung cancer. Mol Biotechnol 2013; 54: 913-9.
[http://dx.doi.org/10.1007/s12033-012-9640-6]
[110]
Webster RJ, Giles KM, Price KJ, Zhang PM, Mattick JS, Leedman PJ. Regulation of epidermal growth factor receptor signaling in human cancer cells by microRNA-7. J Biol Chem 2009; 284: 5731-41.
[http://dx.doi.org/10.1074/jbc.M804280200]
[111]
Chou YT, Lin HH, Lien YC, et al. EGFR promotes lung tumorigenesis by activating miR-7 through a Ras/ERK/Myc pathway that targets the Ets2 transcriptional repressor ERF. Cancer Res 2010; 70: 8822-31.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-0638]
[112]
Yamaguchi G, Takanashi M, Tanaka M, et al. Isolation of miRNAs that target EGFR mRNA in human lung cancer. Biochem Biophys Res Commun 2012; 420: 411-6.
[http://dx.doi.org/10.1016/j.bbrc.2012.03.008]
[113]
Wang LK, Hsiao TH, Hong TM, et al. MicroRNA-133a suppresses multiple oncogenic membrane receptors and cell invasion in non-small cell lung carcinoma. PLoS One 2014; 9: e96765
[http://dx.doi.org/10.1371/journal.pone.0096765]
[114]
Gomez GG, Wykosky J, Zanca C, Furnari FB, Cavenee WK. Therapeutic resistance in cancer: microRNA regulation of EGFR signaling networks. Cancer Biol Med 2013; 10: 192-205.
[115]
Guo YH, Zhang C, Shi J, et al. Abnormal activation of the EGFR signaling pathway mediates the downregulation of miR145 through the ERK1/2 in non-small cell lung cancer. Oncol Rep 2014; 31: 1940-6.
[http://dx.doi.org/10.3892/or.2014.3021]
[116]
Wu SG, Shih JY. Management of acquired resistance to EGFR TKI-targeted therapy in advanced non-small cell lung cancer. Mol Cancer 2018; 17: 38.
[http://dx.doi.org/10.1186/s12943-018-0777-1]
[117]
Weiss GJ, Bemis LT, Nakajima E, et al. EGFR regulation by microRNA in lung cancer: correlation with clinical response and survival to gefitinib and EGFR expression in cell lines. Ann Oncol 2008; 19: 1053-9.
[http://dx.doi.org/10.1093/annonc/mdn006]
[118]
Li B, Ren S, Li X, et al. MiR-21 overexpression is associated with acquired resistance of EGFR-TKI in non-small cell lung cancer. Lung Cancer 2014; 83: 146-53.
[http://dx.doi.org/10.1016/j.lungcan.2013.11.003]
[119]
Wang YS, Wang YH, Xia HP, Zhou SW, Schmid-Bindert G, Zhou CC. MicroRNA-214 regulates the acquired resistance to gefitinib via the PTEN/AKT pathway in EGFR-mutant cell lines. Asian Pac J Cancer Prev 2012; 13: 255-60.
[http://dx.doi.org/10.7314/APJCP.2012.13.1.255]
[120]
Zhong M, Ma X, Sun C, Chen L. MicroRNAs reduce tumor growth and contribute to enhance cytotoxicity induced by gefitinib in non-small cell lung cancer. Chem Biol Interact 2010; 184: 431-8.
[http://dx.doi.org/10.1016/j.cbi.2010.01.025]
[121]
Chen G, Umelo IA, Lv S, et al. miR-146a inhibits cell growth, cell migration and induces apoptosis in non-small cell lung cancer cells. PLoS One 2013; 8: e60317
[http://dx.doi.org/10.1371/journal.pone.0060317]
[122]
Chitty JL, Filipe EC, Lucas MC, Herrmann D, Cox TR, Timpson P. Recent advances in understanding the complexities of metastasis. F1000 Res 2018; 7 pii: . : F1000.
[123]
Roche J. The epithelial-to-mesenchymal transition in cancer. Cancers (Basel) 2018; 10: 52.
[124]
Bracken CP, Gregory PA, Khew-Goodall Y, Goodall GJ. The role of microRNAs in metastasis and epithelial-mesenchymal transition. Cell Mol Life Sci 2009; 66: 1682-99.
[http://dx.doi.org/10.1007/s00018-009-8750-1]
[125]
Wu SG, Chang TH, Liu YN, Shih JY. MicroRNA in lung cancer metastasis. Cancers (Basel) 2019; 11: E265
[126]
Huang TH, Wu F, Loeb GB, et al. Up-regulation of miR-21 by HER2/neu signaling promotes cell invasion. J Biol Chem 2009; 284: 18515-24.
[http://dx.doi.org/10.1074/jbc.M109.006676]
[127]
Chen Y, Knosel T, Kristiansen G, et al. Loss of PDCD4 expression in human lung cancer correlates with tumour progression and prognosis. J Pathol 2003; 200: 640-6.
[http://dx.doi.org/10.1002/path.1378]
[128]
Wang Q, Sun Z, Yang HS. Downregulation of tumor suppressor Pdcd4 promotes invasion and activates both beta-catenin/Tcf and AP-1-dependent transcription in colon carcinoma cells. Oncogene 2008; 27: 1527-35.
[http://dx.doi.org/10.1038/sj.onc.1210793]
[129]
Wang R, Wang ZX, Yang JS, Pan X, De W, Chen LB. MicroRNA-451 functions as a tumor suppressor in human non-small cell lung cancer by targeting ras-related protein 14 (RAB14). Oncogene 2011; 30: 2644-58.
[http://dx.doi.org/10.1038/onc.2010.642]
[130]
Sun M, Liu XH, Li JH, et al. MiR-196a is upregulated in gastric cancer and promotes cell proliferation by downregulating p27(kip1). Mol Cancer Ther 2012; 11: 842-52.
[http://dx.doi.org/10.1158/1535-7163.MCT-11-1015]
[131]
Liu XH, Lu KH, Wang KM, et al. MicroRNA-196a promotes non-small cell lung cancer cell proliferation and invasion through targeting HOXA5. BMC Cancer 2012; 12: 348.
[http://dx.doi.org/10.1186/1471-2407-12-348]
[132]
Chang CJ, Chen YL, Hsieh CH, et al. HOXA5 and p53 cooperate to suppress lung cancer cell invasion and serve as good prognostic factors in non-small cell lung cancer. J Cancer 2017; 8: 1071-81.
[http://dx.doi.org/10.7150/jca.17295]
[133]
Nagel R, le Sage C, Diosdado B, et al. Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancer. Cancer Res 2008; 68: 5795-802.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-0951]
[134]
Lowery AJ, Miller N, Devaney A, et al. MicroRNA signatures predict oestrogen receptor, progesterone receptor and HER2/neu receptor status in breast cancer. Breast Cancer Res 2009; 11: R27.
[http://dx.doi.org/10.1186/bcr2257]
[135]
Tong AW, Fulgham P, Jay C, et al. MicroRNA profile analysis of human prostate cancers. Cancer Gene Ther 2009; 16: 206-16.
[http://dx.doi.org/10.1038/cgt.2008.77]
[136]
Lin CW, Chang YL, Chang YC, et al. MicroRNA-135b promotes lung cancer metastasis by regulating multiple targets in the Hippo pathway and LZTS1. Nat Commun 2013; 4: 1877.
[http://dx.doi.org/10.1038/ncomms2876]
[137]
Hayashita Y, Osada H, Tatematsu Y, et al. A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005; 65: 9628-32.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-2352]
[138]
Li J, Yang S, Yan W, et al. MicroRNA-19 triggers epithelial-mesenchymal transition of lung cancer cells accompanied by growth inhibition. Lab Invest 2015; 95: 1056-70.
[http://dx.doi.org/10.1038/labinvest.2015.76]
[139]
Yu YX, Wang Y, Liu H. Overexpression of PTEN suppresses non-small-cell lung carcinoma metastasis through inhibition of integrin alphaVbeta6 signaling. Am J Transl Res 2017; 9: 3304-14.
[140]
Li Y, Liu J, Fan Y, et al. Expression levels of microRNA-145 and microRNA-10b are associated with metastasis in non-small cell lung cancer. Cancer Biol Ther 2016; 17(3): 272-9.
[http://dx.doi.org/10.1080/15384047.2016.1139242]
[141]
Sheedy P, Medarova Z. The fundamental role of miR-10b in metastatic cancer. Am J Cancer Res 2018; 8: 1674-88.
[142]
Shi ZM, Wang L, Shen H, et al. Downregulation of miR-218 contributes to epithelial-mesenchymal transition and tumor metastasis in lung cancer by targeting Slug/ZEB2 signaling. Oncogene 2017; 36: 2577-88.
[http://dx.doi.org/10.1038/onc.2016.414]
[143]
Chen QY, Jiao DM, Yan L, et al. Comprehensive gene and microRNA expression profiling reveals miR-206 inhibits MET in lung cancer metastasis. Mol Biosyst 2015; 11: 2290-302.
[http://dx.doi.org/10.1039/C4MB00734D]
[144]
Zhang YJ, Xu F, Zhang YJ, Li HB, Han JC, Li L. miR-206 inhibits non small cell lung cancer cell proliferation and invasion by targeting SOX9. Int J Clin Exp Med 2015; 8: 9107-13.
[145]
Jiang SS, Fang WT, Hou YH, et al. Upregulation of SOX9 in lung adenocarcinoma and its involvement in the regulation of cell growth and tumorigenicity. Clin Cancer Res 2010; 16: 4363-73.
[http://dx.doi.org/10.1158/1078-0432.CCR-10-0138]
[146]
Cui R, Meng W, Sun HL, et al. MicroRNA-224 promotes tumor progression in nonsmall cell lung cancer. Proc Natl Acad Sci USA 2015; 112: E4288-97.
[http://dx.doi.org/10.1073/pnas.1502068112]
[147]
Su QL, Li SQ, Wang DN, Liu F, Yuan B. Effects of MicroRNA-10b on lung cancer cell proliferation and invasive metastasis and the underlying mechanism. Asian Pac J Trop Med 2014; 7: 364-7.
[http://dx.doi.org/10.1016/S1995-7645(14)60056-0]
[148]
Huang W, Li H, Luo R. The microRNA-1246 promotes metastasis in non-small cell lung cancer by targeting cytoplasmic polyadenylation element-binding protein 4. Diagn Pathol 2015; 10: 127.
[http://dx.doi.org/10.1186/s13000-015-0366-1]
[149]
Zhou R, Zhou X, Yin Z, et al. Tumor invasion and metastasis regulated by microRNA-184 and microRNA-574-5p in small-cell lung cancer. Oncotarget 2015; 6(42): 44609.
[http://dx.doi.org/10.18632/oncotarget.6338]
[150]
Li J, Tan Q, Yan M, et al. miRNA-200c inhibits invasion and metastasis of human non-small cell lung cancer by directly targeting ubiquitin specific peptidase 25. Mol Cancer 2014; 13: 166.
[http://dx.doi.org/10.1186/1476-4598-13-166]
[151]
Mutlu M, Raza U, Saatci O, Eyupoglu E, Yurdusev E, Sahin O. miR-200c: a versatile watchdog in cancer progression, EMT, and drug resistance. J Mol Med (Berl) 2016; 94: 629-44.
[http://dx.doi.org/10.1007/s00109-016-1420-5]
[152]
Lin J, Chen Y, Liu L, Shen A, Zheng W. MicroRNA-155-5p suppresses the migration and invasion of lung adenocarcinoma A549 cells by targeting Smad2. Oncol Lett 2018; 16: 2444-52.
[http://dx.doi.org/10.3892/ol.2018.8889]
[153]
Gonzalez DM, Medici D. Signaling mechanisms of the epithelial-mesenchymal transition. Sci Signal 2014; 7: re8.
[http://dx.doi.org/10.1126/scisignal.2005189]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 20
ISSUE: 2
Year: 2020
Page: [90 - 101]
Pages: 12
DOI: 10.2174/1566524019666191001113511
Price: $65

Article Metrics

PDF: 24
HTML: 7
EPUB: 1
PRC: 2