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Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

Research Article

Smoking is Associated with Lung Adenocarcinoma and Lung Squamous Cell Carcinoma Progression through Inducing Distinguishing lncRNA Alterations in Different Genders

Author(s): Bing Liu, Yuan Liu, Jingfeng Zou, Menglin Zou and Zhenshun Cheng*

Volume 22, Issue 8, 2022

Published on: 27 July, 2021

Page: [1541 - 1550] Pages: 10

DOI: 10.2174/1871520621666210727115147

Price: $65

Abstract

Background: Smoking participates in pathogenesis of lung cancer. Long non-coding RNAs (lncRNAs) play some specific roles during development of lung cancers.

Objective: To investigate effects of smoking on lncRNA alterations in lung cancer.

Methods: There are 522 lung adenocarcinoma (LUAD) and 504 lung squamous cell carcinoma (LUSC) participants. Clinical and lncRNA genetic data were downloaded from The Cancer Genome Atlas (TCGA) database. LncRNA alterations were analyzed in lung cancer patients. Smoking category and packs were evaluated. Correlations between smoking and LncRNA alterations were analyzed. Kaplan-Meier analysis was performed to determine overall survival and disease free survival.

Results: There are more non-smokers in LUSC than in LUAD. In both LUAD and LUSC, smoking could increase total mutation counts and fraction of copy number alterations. Smoking index positively correlated with total mutations in LUAD, but not in LUSC. Smoking could trigger lncRNA alterations both in LUAD and LUSC. Smoking regulated different lncRNA between male and female. EXOC3-AS1 and LINC00603 alterations were positively correlated with smoking index in male LUAD smokers. In female LUAD smokers, smoking index was positively correlated with SNHG15, TP53TG1 and LINC01600 and negatively with LINC00609 and PTCSC3. In both male and female LUSC patients, smoking increased or decreased several lncRNA alterations. DGCR5 alteration increased in male LUSC than in female LUSC patients. In female LUSC patients, LOH12CR2 alteration was positively correlated with smoking index.

Conclusion: Smoking promoted LUAD and LUSC development by affecting different lncRNA alterations in different genders.

Keywords: Smoking, lncRNA alteration, lung cancer, correlation, squamous cell carcinoma, TCGA.

Graphical Abstract

[1]
Molina, J.R.; Yang, P.; Cassivi, S.D.; Schild, S.E.; Adjei, A.A. Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship. Mayo Clin. Proc., 2008, 83(5), 584-594.
[http://dx.doi.org/10.1016/S0025-6196(11)60735-0] [PMID: 18452692]
[2]
Doll, R.; Hill, A.B. Smoking and carcinoma of the lung; preliminary report. BMJ, 1950, 2(4682), 739-748.
[http://dx.doi.org/10.1136/bmj.2.4682.739] [PMID: 14772469]
[3]
Auerbach, O.; Stout, A.P.; Hammond, E.C.; Garfinkel, L. Changes in bronchial epithelium in relation to cigarette smoking and in relation to lung cancer. N. Engl. J. Med., 1961, 265, 253-267.
[http://dx.doi.org/10.1056/NEJM196108102650601] [PMID: 13685078]
[4]
Hu, X.; Duan, L.; Liu, H.; Zhang, L. Long noncoding RNA LINC01296 induces non-small cell lung cancer growth and progression through sponging miR-5095. Am. J. Transl. Res., 2019, 11(2), 895-903.
[5]
Weston, R.E.; Roberts, M. Lung Cancer and Smoking in Switzerland. Lancet, 1965, 1(7394), 1057-1058.
[6]
Torre, L.A.; Bray, F.; Siegel, R.L.; Ferlay, J.; Lortet-Tieulent, J.; Jemal, A. Global cancer statistics, 2012. CA Cancer J. Clin., 2015, 65(2), 87-108.
[http://dx.doi.org/10.3322/caac.21262] [PMID: 25651787]
[7]
Doll, R.; Hill, A.B. Smoking and carcinoma of the lung. Preliminary report. 1950. Bull. World Health Organ., 1999, 77(1), 84-93.
[8]
Parkin, D.M.; Pisani, P.; Lopez, A.D.; Masuyer, E. At least one in seven cases of cancer is caused by smoking. Global estimates for 1985. Int. J. Cancer, 1994, 59(4), 494-504.
[http://dx.doi.org/10.1002/ijc.2910590411] [PMID: 7960219]
[9]
Gallagher, C.J.; Ahn, K.; Knipe, A.L.; Dyer, A.M.; Richie, J.P., Jr; Lazarus, P.; Muscat, J.E. Association between haplotypes of manganese superoxide dismutase (SOD2), smoking, and lung cancer risk. Free Radic. Biol. Med., 2009, 46(1), 20-24.
[http://dx.doi.org/10.1016/j.freeradbiomed.2008.09.018] [PMID: 18930810]
[10]
Peluso, M.E.; Munnia, A.; Srivatanakul, P.; Jedpiyawongse, A.; Sangrajrang, S.; Ceppi, M.; Godschalk, R.W.; van Schooten, F.J.; Boffetta, P. DNA adducts and combinations of multiple lung cancer at-risk alleles in environmentally exposed and smoking subjects. Environ. Mol. Mutagen., 2013, 54(6), 375-383.
[http://dx.doi.org/10.1002/em.21788] [PMID: 23797975]
[11]
Yang, J.; Shen, Y.; Liu, B.; Tong, Y. Promoter methylation of BRMS1 correlates with smoking history and poor survival in non-small cell lung cancer patients. Lung Cancer, 2011, 74(2), 305-309.
[http://dx.doi.org/10.1016/j.lungcan.2011.03.002] [PMID: 21726917]
[12]
Esteller, M. Non-coding RNAs in human disease. Nat. Rev. Genet., 2011, 12(12), 861-874.
[http://dx.doi.org/10.1038/nrg3074] [PMID: 22094949]
[13]
Cao, J. The functional role of long non-coding RNAs and epigenetics. Biol. Proced. Online, 2014, 16, 11.
[http://dx.doi.org/10.1186/1480-9222-16-11] [PMID: 25276098]
[14]
Bassett, A.R.; Akhtar, A.; Barlow, D.P.; Bird, A.P.; Brockdorff, N.; Duboule, D.; Ephrussi, A.; Ferguson-Smith, A.C.; Gingeras, T.R.; Haerty, W.; Higgs, D.R.; Miska, E.A.; Ponting, C.P. Considerations when investigating lncRNA function in vivo. eLife, 2014, 3e03058
[http://dx.doi.org/10.7554/eLife.03058] [PMID: 25124674]
[15]
Wang, Y.; Qian, C.Y.; Li, X.P.; Zhang, Y.; He, H.; Wang, J.; Chen, J.; Cui, J.J.; Liu, R.; Zhou, H.; Xiao, L.; Xu, X.J.; Zheng, Y.; Fu, Y.L.; Chen, Z.Y.; Chen, X.; Zhang, W.; Ye, C.C.; Zhou, H.H.; Yin, J.Y.; Liu, Z.Q. Genome-scale long noncoding RNA expression pattern in squamous cell lung cancer. Sci. Rep., 2015, 5, 11671.
[http://dx.doi.org/10.1038/srep11671] [PMID: 26159226]
[16]
Huang, N.S.; Chi, Y.Y.; Xue, J.Y.; Liu, M.Y.; Huang, S.; Mo, M.; Zhou, S.L.; Wu, J. Long non-coding RNA metastasis associated in lung adenocarcinoma transcript 1 (MALAT1) interacts with estrogen receptor and predicted poor survival in breast cancer. Oncotarget, 2016, 7(25), 37957-37965.
[http://dx.doi.org/10.18632/oncotarget.9364] [PMID: 27191888]
[17]
Enfield, K.S.; Pikor, L.A.; Martinez, V.D.; Lam, W.L. Mechanistic Roles of Noncoding RNAs in Lung Cancer Biology and Their Clinical Implications. Genet. Res. Int., 2012, 2012737416
[http://dx.doi.org/10.1155/2012/737416] [PMID: 22852089]
[18]
Liu, B.; Chen, Y.; Yang, J. LncRNAs are altered in lung squamous cell carcinoma and lung adenocarcinoma. Oncotarget, 2017, 8(15), 24275-24291.
[http://dx.doi.org/10.18632/oncotarget.13651] [PMID: 27903974]
[19]
Brownson, R.C.; Chang, J.C.; Davis, J.R. Gender and histologic type variations in smoking-related risk of lung cancer. Epidemiology, 1992, 3(1), 61-64.
[http://dx.doi.org/10.1097/00001648-199201000-00012] [PMID: 1313311]
[20]
Wang, D.; Yang, S.; Wang, H.; Wang, J.; Zhang, Q.; Zhou, S.; He, Y.; Zhang, H.; Deng, F.; Xu, H.; Zhong, S.; Fu, L.; Tang, J. The progress of circular RNAs in various tumors. Am. J. Transl. Res., 2018, 10(6), 1571-1582.
[21]
Juul, M.; Bertl, J.; Guo, Q.; Nielsen, M.M.; Świtnicki, M.; Hornshøj, H.; Madsen, T.; Hobolth, A.; Pedersen, J.S. Non-coding cancer driver candidates identified with a sample- and position-specific model of the somatic mutation rate. eLife, 2017, 6e21778
[http://dx.doi.org/10.7554/eLife.21778] [PMID: 28362259]
[22]
Tao, H.; Yang, J.J.; Zhou, X.; Deng, Z.Y.; Shi, K.H.; Li, J. Emerging role of long noncoding RNAs in lung cancer: Current status and future prospects. Respir. Med., 2016, 110, 12-19.
[http://dx.doi.org/10.1016/j.rmed.2015.10.006] [PMID: 26603340]
[23]
Thun, M.J.; Lally, C.A.; Flannery, J.T.; Calle, E.E.; Flanders, W.D.; Heath, C.W., Jr Cigarette smoking and changes in the histopathology of lung cancer. J. Natl. Cancer Inst., 1997, 89(21), 1580-1586.
[http://dx.doi.org/10.1093/jnci/89.21.1580] [PMID: 9362155]
[24]
Ahrendt, S.A.; Decker, P.A.; Alawi, E.A.; Zhu Yr, Y.R.; Sanchez-Cespedes, M.; Yang, S.C.; Haasler, G.B.; Kajdacsy-Balla, A.; Demeure, M.J.; Sidransky, D. Cigarette smoking is strongly associated with mutation of the K-ras gene in patients with primary adenocarcinoma of the lung. Cancer, 2001, 92(6), 1525-1530.
[http://dx.doi.org/10.1002/1097-0142(20010915)92:6<1525:AID-CNCR1478>3.0.CO;2-H] [PMID: 11745231]
[25]
Gou, L.Y.; Niu, F.Y.; Wu, Y.L.; Zhong, W.Z. Differences in driver genes between smoking-related and non-smoking-related lung cancer in the Chinese population. Cancer, 2015, 121(Suppl. 17), 3069-3079.
[http://dx.doi.org/10.1002/cncr.29531] [PMID: 26331813]
[26]
Sun, S.; Schiller, J.H.; Gazdar, A.F. Lung cancer in never smokers--a different disease. Nat. Rev. Cancer, 2007, 7(10), 778-790.
[http://dx.doi.org/10.1038/nrc2190] [PMID: 17882278]
[27]
Hotta, K.; Kiura, K.; Takigawa, N.; Kuyama, S.; Segawa, Y.; Yonei, T.; Gemba, K.; Aoe, K.; Shibayama, T.; Matsuo, K.; Kamei, H.; Fujiwara, Y.; Bessho, A.; Moritaka, T.; Sugimoto, K.; Tabata, M.; Ueoka, H.; Tanimoto, M. Sex difference in the influence of smoking status on the responsiveness to gefitinib monotherapy in adenocarcinoma of the lung: Okayama Lung Cancer Study Group experience. J. Cancer Res. Clin. Oncol., 2009, 135(1), 117-123.
[http://dx.doi.org/10.1007/s00432-008-0431-1] [PMID: 18618142]
[28]
Scagliotti, G.V.; Longo, M.; Novello, S. Nonsmall cell lung cancer in never smokers. Curr. Opin. Oncol., 2009, 21(2), 99-104.
[http://dx.doi.org/10.1097/CCO.0b013e328321049e] [PMID: 19532009]
[29]
Lee, Y.J.; Kim, J.H.; Kim, S.K.; Ha, S.J.; Mok, T.S.; Mitsudomi, T.; Cho, B.C. Lung cancer in never smokers: change of a mindset in the molecular era. Lung Cancer, 2011, 72(1), 9-15.
[http://dx.doi.org/10.1016/j.lungcan.2010.12.013] [PMID: 21272954]
[30]
Bavarva, J.H.; Tae, H.; McIver, L.; Garner, H.R. Nicotine and oxidative stress induced exomic variations are concordant and overrepresented in cancer-associated genes. Oncotarget, 2014, 5(13), 4788-4798.
[http://dx.doi.org/10.18632/oncotarget.2033] [PMID: 24947164]
[31]
Yavorski, J.M.; Blanck, G. Smoking correlates with increased cytoskeletal protein-related coding region mutations in the lung and head and neck datasets of the cancer genome atlas. Physiol. Rep., 2016, 4(24)e13045
[http://dx.doi.org/10.14814/phy2.13045] [PMID: 28039401]
[32]
Huang, Y.T.; Lin, X.; Liu, Y.; Chirieac, L.R.; McGovern, R.; Wain, J.; Heist, R.; Skaug, V.; Zienolddiny, S.; Haugen, A.; Su, L.; Fox, E.A.; Wong, K.K.; Christiani, D.C. Cigarette smoking increases copy number alterations in nonsmall-cell lung cancer. Proc. Natl. Acad. Sci. USA, 2011, 108(39), 16345-16350.
[http://dx.doi.org/10.1073/pnas.1102769108] [PMID: 21911369]
[33]
Massion, P.P.; Zou, Y.; Chen, H.; Jiang, A.; Coulson, P.; Amos, C.I.; Wu, X.; Wistuba, I.; Wei, Q.; Shyr, Y.; Spitz, M.R. Smoking-related genomic signatures in non-small cell lung cancer. Am. J. Respir. Crit. Care Med., 2008, 178(11), 1164-1172.
[http://dx.doi.org/10.1164/rccm.200801-142OC] [PMID: 18776155]
[34]
Yang, Y.; Li, H.; Hou, S.; Hu, B.; Liu, J.; Wang, J. The noncoding RNA expression profile and the effect of lncRNA AK126698 on cisplatin resistance in non-small-cell lung cancer cell. PLoS One, 2013, 8(5)e65309
[http://dx.doi.org/10.1371/journal.pone.0065309] [PMID: 23741487]
[35]
Yang, Y.R.; Zang, S.Z.; Zhong, C.L.; Li, Y.X.; Zhao, S.S.; Feng, X.J. Increased expression of the lncRNA PVT1 promotes tumorigenesis in non-small cell lung cancer. Int. J. Clin. Exp. Pathol., 2014, 7(10), 6929-6935.
[36]
Wang, H.M.; Lu, J.H.; Chen, W.Y.; Gu, A.Q. Upregulated lncRNA-UCA1 contributes to progression of lung cancer and is closely related to clinical diagnosis as a predictive biomarker in plasma. Int. J. Clin. Exp. Med., 2015, 8(7), 11824-11830.
[37]
Gong, W.J.; Yin, J.Y.; Li, X.P.; Fang, C.; Xiao, D.; Zhang, W.; Zhou, H.H.; Li, X.; Liu, Z.Q. Association of well-characterized lung cancer lncRNA polymorphisms with lung cancer susceptibility and platinum-based chemotherapy response. Tumour Biol., 2016, 37(6), 8349-8358.
[http://dx.doi.org/10.1007/s13277-015-4497-5] [PMID: 26729200]
[38]
Shen, L.; Chen, L.; Wang, Y.; Jiang, X.; Xia, H.; Zhuang, Z. Long noncoding RNA MALAT1 promotes brain metastasis by inducing epithelial-mesenchymal transition in lung cancer. J. Neurooncol., 2015, 121(1), 101-108.
[http://dx.doi.org/10.1007/s11060-014-1613-0] [PMID: 25217850]
[39]
Liu, X.H.; Liu, Z.L.; Sun, M.; Liu, J.; Wang, Z.X.; De, W. The long non-coding RNA HOTAIR indicates a poor prognosis and promotes metastasis in non-small cell lung cancer. BMC Cancer, 2013, 13, 464.
[http://dx.doi.org/10.1186/1471-2407-13-464] [PMID: 24103700]
[40]
Zhao, R.; Sun, F.; Bei, X.; Wang, X.; Zhu, Y.; Jiang, C.; Zhao, F.; Han, B.; Xia, S. Upregulation of the long non-coding RNA FALEC promotes proliferation and migration of prostate cancer cell lines and predicts prognosis of PCa patients. Prostate, 2017, 77(10), 1107-1117.
[http://dx.doi.org/10.1002/pros.23367] [PMID: 28585762]
[41]
Collin, G.B.; Hubmacher, D.; Charette, J.R.; Hicks, W.L.; Stone, L.; Yu, M.; Naggert, J.K.; Krebs, M.P.; Peachey, N.S.; Apte, S.S.; Nishina, P.M. Disruption of murine Adamtsl4 results in zonular fiber detachment from the lens and in retinal pigment epithelium dedifferentiation. Hum. Mol. Genet., 2015, 24(24), 6958-6974.
[42]
Wu, X.; Ruan, L.; Yang, Y.; Mei, Q. Identification of crucial regulatory relationships between long non-coding RNAs and protein-coding genes in lung squamous cell carcinoma. Mol. Cell. Probes, 2016, 30(3), 146-152.
[http://dx.doi.org/10.1016/j.mcp.2016.02.009] [PMID: 26928440]
[43]
Wan, L.; Sun, M.; Liu, G.J.; Wei, C.C.; Zhang, E.B.; Kong, R.; Xu, T.P.; Huang, M.D.; Wang, Z.X. Long Noncoding RNA PVT1 Promotes Non-Small Cell Lung Cancer Cell Proliferation through Epigenetically Regulating LATS2 Expression. Mol. Cancer Ther., 2016, 15(5), 1082-1094.
[http://dx.doi.org/10.1158/1535-7163.MCT-15-0707] [PMID: 26908628]
[44]
Chen, W.; Zhu, H.; Yin, L.; Wang, T.; Wu, J.; Xu, J.; Tao, H.; Liu, J.; He, X. lncRNA-PVT1 Facilitates Invasion Through Upregulation of MMP9 in Nonsmall Cell Lung Cancer Cell. DNA Cell Biol., 2017, 36(9), 787-793.
[http://dx.doi.org/10.1089/dna.2017.3725] [PMID: 28731781]
[45]
Liu, H.; Li, J.; Koirala, P.; Ding, X.; Chen, B.; Wang, Y.; Wang, Z.; Wang, C.; Zhang, X.; Mo, Y.Y. Long non-coding RNAs as prognostic markers in human breast cancer. Oncotarget, 2016, 7(15), 20584-20596.
[http://dx.doi.org/10.18632/oncotarget.7828] [PMID: 26942882]
[46]
Ma, B.; Liao, T.; Wen, D.; Dong, C.; Zhou, L.; Yang, S.; Wang, Y.; Ji, Q. Long intergenic non-coding RNA 271 is predictive of a poorer prognosis of papillary thyroid cancer. Sci. Rep., 2016, 6, 36973.
[http://dx.doi.org/10.1038/srep36973] [PMID: 27833134]
[47]
Yang, H.; Liu, P.; Zhang, J.; Peng, X.; Lu, Z.; Yu, S.; Meng, Y.; Tong, W.M.; Chen, J. Long noncoding RNA MIR31HG exhibits oncogenic property in pancreatic ductal adenocarcinoma and is negatively regulated by miR-193b. Oncogene, 2016, 35(28), 3647-3657.
[http://dx.doi.org/10.1038/onc.2015.430] [PMID: 26549028]
[48]
Keenan, C.R.; Schuliga, M.J.; Stewart, A.G. Pro-inflammatory mediators increase levels of the noncoding RNA GAS5 in airway smooth muscle and epithelial cells. Can. J. Physiol. Pharmacol., 2015, 93(3), 203-206.
[http://dx.doi.org/10.1139/cjpp-2014-0391] [PMID: 25615620]
[49]
Dong, S.; Qu, X.; Li, W.; Zhong, X.; Li, P.; Yang, S.; Chen, X.; Shao, M.; Zhang, L. The long non-coding RNA, GAS5, enhances gefitinib-induced cell death in innate EGFR tyrosine kinase inhibitor-resistant lung adenocarcinoma cells with wide-type EGFR via downregulation of the IGF-1R expression. J. Hematol. Oncol., 2015, 8, 43.
[http://dx.doi.org/10.1186/s13045-015-0140-6] [PMID: 25925741]
[50]
Zhang, J.H.; Wei, H.W.; Yang, H.G. Long noncoding RNA SNHG15, a potential prognostic biomarker for hepatocellular carcinoma. Eur. Rev. Med. Pharmacol. Sci., 2016, 20(9), 1720-1724.
[51]
Chen, S.X.; Yin, J.F.; Lin, B.C.; Su, H.F.; Zheng, Z.; Xie, C.Y.; Fei, Z.H. Upregulated expression of long noncoding RNA SNHG15 promotes cell proliferation and invasion through regulates MMP2/MMP9 in patients with GC. Tumour Biol., 2016, 37(5), 6801-6812.
[http://dx.doi.org/10.1007/s13277-015-4404-0] [PMID: 26662309]
[52]
Yao, S.; Johnson, C.; Hu, Q.; Yan, L.; Liu, B.; Ambrosone, C.B.; Wang, J.; Liu, S. Differences in somatic mutation landscape of hepatocellular carcinoma in Asian American and European American populations. Oncotarget, 2016, 7(26), 40491-40499.
[http://dx.doi.org/10.18632/oncotarget.9636] [PMID: 27246981]
[53]
Wang, Z.; Rajaraman, P.; Melin, B.S.; Chung, C.C.; Zhang, W.; McKean-Cowdin, R.; Michaud, D.; Yeager, M.; Ahlbom, A.; Albanes, D.; Andersson, U.; Freeman, L.E.; Buring, J.E.; Butler, M.A.; Carreón, T.; Feychting, M.; Gapstur, S.M.; Gaziano, J.M.; Giles, G.G.; Hallmans, G.; Henriksson, R.; Hoffman-Bolton, J.; Inskip, P.D.; Kitahara, C.M.; Marchand, L.L.; Linet, M.S.; Li, S.; Peters, U.; Purdue, M.P.; Rothman, N.; Ruder, A.M.; Sesso, H.D.; Severi, G.; Stampfer, M.; Stevens, V.L.; Visvanathan, K.; Wang, S.S.; White, E.; Zeleniuch-Jacquotte, A.; Hoover, R.; Fraumeni, J.F.; Chatterjee, N.; Hartge, P.; Chanock, S.J. Further Confirmation of Germline Glioma Risk Variant rs78378222 in TP53 and Its Implication in Tumor Tissues via Integrative Analysis of TCGA Data. Hum. Mutat., 2015, 36(7), 684-688.
[http://dx.doi.org/10.1002/humu.22799] [PMID: 25907361]
[54]
Nickerson, M.L.; Witte, N.; Im, K.M.; Turan, S.; Owens, C.; Misner, K.; Tsang, S.X.; Cai, Z.; Wu, S.; Dean, M.; Costello, J.C.; Theodorescu, D. Molecular analysis of urothelial cancer cell lines for modeling tumor biology and drug response. Oncogene, 2017, 36(1), 35-46.
[http://dx.doi.org/10.1038/onc.2016.172] [PMID: 27270441]
[55]
Skoulidis, F.; Byers, L.A.; Diao, L.; Papadimitrakopoulou, V.A.; Tong, P.; Izzo, J.; Behrens, C.; Kadara, H.; Parra, E.R.; Canales, J.R.; Zhang, J.; Giri, U.; Gudikote, J.; Cortez, M.A.; Yang, C.; Fan, Y.; Peyton, M.; Girard, L.; Coombes, K.R.; Toniatti, C.; Heffernan, T.P.; Choi, M.; Frampton, G.M.; Miller, V.; Weinstein, J.N.; Herbst, R.S.; Wong, K.K.; Zhang, J.; Sharma, P.; Mills, G.B.; Hong, W.K.; Minna, J.D.; Allison, J.P.; Futreal, A.; Wang, J.; Wistuba, I.I.; Heymach, J.V. Co-occurring genomic alterations define major subsets of KRAS-mutant lung adenocarcinoma with distinct biology, immune profiles, and therapeutic vulnerabilities. Cancer Discov., 2015, 5(8), 860-877.
[http://dx.doi.org/10.1158/2159-8290.CD-14-1236] [PMID: 26069186]
[56]
Diederichs, S.; Bartsch, L.; Berkmann, J.C.; Fröse, K.; Heitmann, J.; Hoppe, C.; Iggena, D.; Jazmati, D.; Karschnia, P.; Linsenmeier, M.; Maulhardt, T.; Möhrmann, L.; Morstein, J.; Paffenholz, S.V.; Röpenack, P.; Rückert, T.; Sandig, L.; Schell, M.; Steinmann, A.; Voss, G.; Wasmuth, J.; Weinberger, M.E.; Wullenkord, R. The dark matter of the cancer genome: aberrations in regulatory elements, untranslated regions, splice sites, non-coding RNA and synonymous mutations. EMBO Mol. Med., 2016, 8(5), 442-457.
[http://dx.doi.org/10.15252/emmm.201506055] [PMID: 26992833]
[57]
Diaz-Lagares, A.; Crujeiras, A.B.; Lopez-Serra, P.; Soler, M.; Setien, F.; Goyal, A.; Sandoval, J.; Hashimoto, Y.; Martinez-Cardús, A.; Gomez, A.; Heyn, H.; Moutinho, C.; Espada, J.; Vidal, A.; Paúles, M.; Galán, M.; Sala, N.; Akiyama, Y.; Martínez-Iniesta, M.; Farré, L.; Villanueva, A.; Gross, M.; Diederichs, S.; Guil, S.; Esteller, M. Epigenetic inactivation of the p53-induced long noncoding RNA TP53 target 1 in human cancer. Proc. Natl. Acad. Sci. USA, 2016, 113(47), E7535-E7544.
[http://dx.doi.org/10.1073/pnas.1608585113] [PMID: 27821766]
[58]
Sutherland, H.F.; Wadey, R.; McKie, J.M.; Taylor, C.; Atif, U.; Johnstone, K.A.; Halford, S.; Kim, U.J.; Goodship, J.; Baldini, A.; Scambler, P.J. Identification of a novel transcript disrupted by a balanced translocation associated with DiGeorge syndrome. Am. J. Hum. Genet., 1996, 59(1), 23-31.
[59]
Johnson, R.; Teh, C.H.; Jia, H.; Vanisri, R.R.; Pandey, T.; Lu, Z.H.; Buckley, N.J.; Stanton, L.W.; Lipovich, L. Regulation of neural macroRNAs by the transcriptional repressor REST. RNA, 2009, 15(1), 85-96.
[http://dx.doi.org/10.1261/rna.1127009] [PMID: 19050060]

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