Transcriptome-wide analysis of UTRs in non-small cell lung cancer reveals cancer-related genes with SNV-induced changes on RNA secondary structure and miRNA target sites

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Sabarinathan, Radhakrishnan ^a   Wenzel, Anne ^a   Novotny, Peter ^a   Tang, Xiaojia ^b   Kalari, Krishna R ^b,c   Gorodkin, Jan ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b MAYO CLINIC   (United States)

^c MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; INITIATION FACTOR 2; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA; MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTOME;

ARTICLE; CLINICAL ARTICLE; ENZYME ACTIVATION; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE MAPPING; GENE MUTATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC PARAMETERS; GENETIC VARIABILITY; HUMAN; HUMAN TISSUE; LUNG NON SMALL CELL CANCER; MICRORNA TARGET SITE; ONCOGENE K RAS; RNA SECONDARY STRUCTURE; RNA STRUCTURE; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR CELL; UNTRANSLATED REGION; WILD TYPE;

CARCINOMA, NON-SMALL-CELL LUNG; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; GENES, NEOPLASM; HUMANS; LUNG NEOPLASMS; MICRORNAS; NUCLEIC ACID CONFORMATION; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA, MESSENGER; RNA, NEOPLASM; SOFTWARE; UNTRANSLATED REGIONS;

EID: 84897410906     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082699     Document Type: Article

References (67)

1. Meyerson M, Gabriel S, Getz G (2010) Advances in understanding cancer genomes through second-generation sequencing. Nat Rev Genet 11: 685-696. nrg2841 [pii];10.1038/nrg2841 [doi].
2. Hudson TJ, Anderson W, Artez A, Barker AD, Bell C, et al. (2010) International network of cancer genome projects. Nature 464: 993-998. nature08987 [pii];10.1038/nature08987 [doi].
3. Eberhard DA, Johnson BE, Amler LC, Goddard AD, Heldens SL, et al. (2005) Mutations in the epidermal growth factor receptor and in KRAS are predictive and prognostic indicators in patients with non-small-cell lung cancer treated with chemotherapy alone and in combination with erlotinib. J Clin Oncol 23: 5900-5909. JCO.2005.02.857 [pii];10.1200/JCO.2005.02.857 [doi].
4. Pao W, Wang TY, Riely GJ, Miller VA, Pan Q, et al. (2005) KRAS mutations and primary resistance of lung adenocarcinomas to gefitinib or erlotinib. PLoS Med 2: e17. 04-PLME-RA-0242R1 [pii];10.1371/journal.pmed.0020017 [doi].
5. Riely GJ, Marks J, Pao W (2009) KRAS mutations in non-small cell lung cancer. Proc Am Thorac Soc 6: 201-205. 6/2/201 [pii];10.1513/pats.200809-107LC [doi].
6. Kalari KR, Rossell D, Necela BM, Asmann YW, Nair A, et al. (2012) Deep Sequence Analysis of Non-Small Cell Lung Cancer: Integrated Analysis of Gene Expression, Alternative Splicing, and Single Nucleotide Variations in Lung Adenocarcinomas with and without Oncogenic KRAS Mutations. Front Oncol 2: 12. 10.3389/fonc.2012.00012 [doi].
7. Zhu Q, Ge D, Maia JM, Zhu M, Petrovski S, et al. (2011) A genome-wide comparison of the functional properties of rare and common genetic variants in humans. Am J Hum Genet 88: 458-468. S0002-9297(11)00100-5 [pii];10.1016/j.ajhg. 2011.03.008 [doi].
8. Chepelev I, Wei G, Tang Q, Zhao K (2009) Detection of single nucleotide variations in expressed exons of the human genome using RNA-Seq. Nucleic Acids Res 37: e106. gkp507 [pii];10.1093/nar/gkp507 [doi].
9. Nackley AG, Shabalina SA, Tchivileva IE, Satterfield K, Korchynskyi O, et al. (2006) Human catechol-O-methyltransferase haplotypes modulate protein expression by altering mRNA secondary structure. Science 314: 1930-1933. 314/5807/1930 [pii];10.1126/science.1131262 [doi].
10. Jambhekar A, Derisi JL (2007) Cis-acting determinants of asymmetric, cytoplasmic RNA transport. RNA 13: 625-642. 13/5/625 [pii];10.1261/rna.262607 [doi].
11. Martin KC, Ephrussi A (2009) mRNA localization: gene expression in the spatial dimension. Cell 136: 719-730. S0092-8674(09)00126-3 [pii];10.1016/j. cell.2009.01.044 [doi].
12. Andreassi C, Riccio A (2009) To localize or not to localize: mRNA fate is in 39 UTR ends. Trends Cell Biol 19: 465-474. S0962-8924(09)00141-X [pii];10.1016/j.tcb.2009.06.001 [doi].
13. Kaye JA, Rose NC, Goldsworthy B, Goga A, L'Etoile ND (2009) A 39UTR pumilio-binding element directs translational activation in olfactory sensory neurons. Neuron 61: 57-70. S0896-6273(08)00966-5 [pii];10.1016/j.neuron.2008.11. 012 [doi].
14. Fabian MR, Sonenberg N, Filipowicz W (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79: 351-379. 10.1146/annurev-biochem-060308-103103 [doi].
15. Reveal B, Yan N, Snee MJ, Pai CI, Gim Y, et al. (2010) BREs mediate both repression and activation of oskar mRNA translation and act in trans. Dev Cell 18: 496-502. S1534-5807(10)00050-X [pii];10.1016/j.devcel.2009.12.021 [doi].
16. Farazi TA, Spitzer JI, Morozov P, Tuschl T (2011) miRNAs in human cancer. J Pathol 223: 102-115. 10.1002/path.2806 [doi].
17. Martin JS, Halvorsen M, Davis-Neulander L, Ritz J, Gopinath C, et al. (2012) Structural effects of linkage disequilibrium on the transcriptome. RNA 18: 77-87. rna.029900.111 [pii];10.1261/rna.029900.111 [doi].
18. Halvorsen M, Martin JS, Broadaway S, Laederach A (2010) Disease-associated mutations that alter the RNA structural ensemble. PLoS Genet 6: e1001074. 10.1371/journal.pgen.1001074 [doi].
19. Aouacheria A, Navratil V, Lopez-Perez R, Gutierrez NC, Churkin A, et al. (2007) In silico whole-genome screening for cancer-related single-nucleotide polymorphisms located in human mRNA untranslated regions. BMC Genomics 8: 2. 1471-2164-8-2 [pii];10.1186/1471-2164-8-2 [doi].
20. Chatterjee S, Pal JK (2009) Role of 59- and 39-untranslated regions of mRNAs in human diseases. Biol Cell 101: 251-262. BC20080104 [pii];10.1042/ BC20080104 [doi].
21. Chin LJ, Ratner E, Leng S, Zhai R, Nallur S, et al. (2008) A SNP in a let-7 microRNA complementary site in the KRAS 39 untranslated region increases non-small cell lung cancer risk. Cancer Res 68: 8535-8540. 68/20/8535 [pii];10.1158/0008-5472.CAN-08-2129 [doi].
22. Bruno AE, Li L, Kalabus JL, Pan Y, Yu A, et al. (2012) miRdSNP: a database of disease-associated SNPs and microRNA target sites on 39UTRs of human genes. BMC Genomics 13: 44. 1471-2164-13-44 [pii];10.1186/1471-2164-13-44 [doi].
23. Gong J, Tong Y, Zhang HM, Wang K, Hu T, et al. (2012) Genome-wide identification of SNPs in microRNA genes and the SNP effects on microRNA target binding and biogenesis. Hum Mutat 33: 254-263. 10.1002/humu.21641 [doi].
24. Nicoloso MS, Sun H, Spizzo R, Kim H, Wickramasinghe P, et al. (2010) Single-nucleotide polymorphisms inside microRNA target sites influence tumor susceptibility. Cancer Res 70: 2789-2798. 0008-5472.CAN-09-3541 [pii];10.1158/0008-5472.CAN-09-3541 [doi].
25. Grover R, Sharathchandra A, Ponnuswamy A, Khan D, Das S (2011) Effect of mutations on the p53 IRES RNA structure: implications for de-regulation of the synthesis of p53 isoforms. RNA Biol 8: 132-142. 14260 [pii].
26. Barenboim M, Zoltick BJ, Guo Y, Weinberger DR (2010) MicroSNiPer: a web tool for prediction of SNP effects on putative microRNA targets. Hum Mutat 31: 1223-1232. 10.1002/humu.21349 [doi].
27. Bhattacharya A, Ziebarth JD, Cui Y (2013) SomamiR: a database for somatic mutations impacting microRNA function in cancer. Nucleic Acids Res 41: D977-D982. gks1138 [pii];10.1093/nar/gks1138 [doi].
28. Ziebarth JD, Bhattacharya A, Chen A, Cui Y (2012) PolymiRTS Database 2.0: linking polymorphisms in microRNA target sites with human diseases and complex traits. Nucleic Acids Res 40: D216-D221. gkr1026 [pii];10.1093/nar/gkr1026 [doi].
29. Sabarinathan R, Tafer H, Seemann SE, Hofacker IL, Stadler PF, et al. (2013) RNAsnp: efficient detection of local RNA secondary structure changes induced by SNPs. Hum Mutat 34: 546-556. 10.1002/humu.22273 [doi].
30. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20. S0092867404012607 [pii];10.1016/j.cell.2004.12.035 [doi].
31. Enright AJ, John B, Gaul U, Tuschl T, Sander C, et al. (2003) MicroRNA targets in Drosophila. Genome Biol 5: R1. 10.1186/gb-2003-5-1-r1 [doi];gb-2003-5-1-r1 [pii].
32. Croft L, Szklarczyk D, Jensen LJ, Gorodkin J (2012) Multiple independent analyses reveal only transcription factors as an enriched functional class associated with microRNAs. BMC Syst Biol 6: 90. 1752-0509-6-90 [pii];10.1186/1752-0509-6-90 [doi].
33. Chi SW, Zang JB, Mele A, Darnell RB (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460: 479-486. nature08170 [pii];10.1038/nature08170 [doi].
34. Johnson AD, Handsaker RE, Pulit SL, Nizzari MM, O'Donnell CJ, et al. (2008) SNAP: a web-based tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics 24: 2938-2939. btn564 [pii];10.1093/bioinformatics/ btn564 [doi].
35. Karolchik D, Hinrichs AS, Furey TS, Roskin KM, Sugnet CW, et al. (2004) The UCSC Table Browser data retrieval tool. Nucleic Acids Res 32: D493-D496. 10.1093/nar/gkh103 [doi];32/suppl-1/D493 [pii].
36. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, et al. (2011) COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 39: D945-D950. gkq929 [pii];10.1093/nar/gkq929 [doi].
37. Arikawa E, Quelhorst G, Han Y, Pan H, Yang J (2011) RT2 Profiler™ PCR Arrays: Pathway-focused gene expression profiling with qRT-PCR. SABiosciences.
38. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57: 289-300.
39. Seemann SE, et al. (2013) in prep.
40. Yao Z, Weinberg Z, Ruzzo WL (2006) CMfinder-a covariance model based RNA motif finding algorithm. Bioinformatics 22: 445-452. btk008 [pii];10.1093/ bioinformatics/btk008 [doi].
41. Washietl S, Hofacker IL, Stadler PF (2005) Fast and reliable prediction of noncoding RNAs. Proc Natl Acad Sci U S A 102: 2454-2459. 0409169102 [pii];10.1073/pnas.0409169102 [doi].
42. Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39: D152-D157. gkq1027 [pii];10.1093/nar/gkq1027 [doi].
43. Wenzel A, Akbasli E, Gorodkin J (2012) RIsearch: Fast RNA-RNA interaction search using a simplified nearest-neighbor energy model. Bioinformatics. bts519 [pii];10.1093/bioinformatics/bts519 [doi].
44. Yang JH, Li JH, Shao P, Zhou H, Chen YQ, et al. (2011) starBase: a database for exploring microRNA-mRNA interaction maps from Argonaute CLIP-Seq and Degradome-Seq data. Nucleic Acids Res 39: D202-D209. gkq1056 [pii];10.1093/nar/gkq1056 [doi].
45. Mestdagh P, Lefever S, Pattyn F, Ridzon D, Fredlund E, et al. (2011) The microRNA body map: dissecting microRNA function through integrative genomics. Nucleic Acids Res 39: e136. gkr646 [pii];10.1093/nar/gkr646 [doi].
46. Ruepp A, Kowarsch A, Schmidl D, Buggenthin F, Brauner B, et al. (2010) PhenomiR: a knowledgebase for microRNA expression in diseases and biological processes. Genome Biol 11: R6. gb-2010-11-1-r6 [pii];10.1186/gb-2010-11-1-r6 [doi].
47. Tsang JS, Ebert MS, van OA (2010) Genome-wide dissection of microRNA functions and cotargeting networks using gene set signatures. Mol Cell 38: 140-153. S1097-2765(10)00241-8 [pii];10.1016/j.molcel.2010.03.007 [doi].
48. Ingenuity Systems (2005) IPA Network Generation Algorithm [white paper]. Available: http://www.ingenuity.com/wp-content/themes/ingenuitytheme/pdf/ipa/ IPA-netgen-algorithm-whitepaper.pdf Accessed: 2013 Nov 8.
49. Fontana W, Konings DA, Stadler PF, Schuster P (1993) Statistics of RNA secondary structures. Biopolymers 33: 1389-1404. 10.1002/bip.360330909 [doi]. (Pubitemid 23249156)
50. Walczak R, Westhof E, Carbon P, Krol A (1996) A novel RNA structural motif in the selenocysteine insertion element of eukaryotic selenoprotein mRNAs. RNA 2: 367-379. (Pubitemid 26371288)
51. Diwa A, Bricker AL, Jain C, Belasco JG (2000) An evolutionarily conserved RNA stem-loop functions as a sensor that directs feedback regulation of RNase E gene expression. Genes Dev 14: 1249-1260. (Pubitemid 30327505)
52. Chen XS, Brown CM (2012) Computational identification of new structured cis-regulatory elements in the 39-untranslated region of human protein coding genes. Nucleic Acids Res 40: 8862-8873. gks684 [pii];10.1093/nar/gks684 [doi].
53. Pesole G, Grillo G, Larizza A, Liuni S (2000) The untranslated regions of eukaryotic mRNAs: structure, function, evolution and bioinformatic tools for their analysis. Brief Bioinform 1: 236-249.
54. Mignone F, Gissi C, Liuni S, Pesole G (2002) Untranslated regions of mRNAs. Genome Biol 3: REVIEWS0004.
55. Pearson G, Robinson F, Beers GT, Xu BE, Karandikar M, et al. (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 22: 153-183. (Pubitemid 32458157)
56. Latreche L, Jean-Jean O, Driscoll DM, Chavatte L (2009) Novel structural determinants in human SECIS elements modulate the translational recoding of UGA as selenocysteine. Nucleic Acids Res 37: 5868-5880. gkp635 [pii];10.1093/nar/ gkp635 [doi].
57. Rollin J, Blechet C, Regina S, Tenenhaus A, Guyetant S, et al. (2009) The intracellular localization of ID2 expression has a predictive value in non small cell lung cancer. PLoS One 4: e4158. 10.1371/journal.pone.0004158 [doi].
58. Gochhait S, Bukhari SI, Bairwa N, Vadhera S, Darvishi K, et al. (2007) Implication of BRCA2 -26G>A 5′ untranslated region polymorphism in susceptibility to sporadic breast cancer and its modulation by p53 codon 72 Arg>Pro polymorphism. Breast Cancer Res 9: R71. bcr1780 [pii];10.1186/bcr1780 [doi].
59. Teresi RE, Zbuk KM, Pezzolesi MG, Waite KA, Eng C (2007) Cowden syndrome-affected patients with PTEN promoter mutations demonstrate abnormal protein translation. Am J Hum Genet 81: 756-767. S0002-9297(07)63051-1 [pii];10.1086/521051 [doi].
60. Martin JS, Halvorsen M, Davis-Neulander L, Ritz J, Gopinath C, et al. (2012) Structural effects of linkage disequilibrium on the transcriptome. RNA 18: 77-87. rna.029900.111 [pii];10.1261/rna.029900.111 [doi].
61. Wang Y, Zhang X, Li H, Yu J, Ren X (2013) The role of miRNA-29 family in cancer. Eur J Cell Biol 92: 123-128. S0171-9335(12)00188-4 [pii];10.1016/j.ejcb. 2012.11.004 [doi].
62. Iliopoulos D, Lindahl-Allen M, Polytarchou C, Hirsch HA, Tsichlis PN, et al. (2010) Loss of miR-200 inhibition of Suz12 leads to polycomb-mediated repression required for the formation and maintenance of cancer stem cells. Mol Cell 39: 761-772. S1097-2765(10)00623-4 [pii];10.1016/j.molcel.2010.08.013 [doi].
63. Haas U, Sczakiel G, Laufer SD (2012) MicroRNA-mediated regulation of gene expression is affected by disease-associated SNPs within the 3′-UTR via altered RNA structure. RNA Biol 9: 924-937. 20497 [pii];10.4161/rna.20497 [doi].
64. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E (2007) The role of site accessibility in microRNA target recognition. Nat Genet 39: 1278-1284. ng2135 [pii];10.1038/ng2135 [doi].
65. Mwenifumbo JC, Marra MA (2013) Cancer genome-sequencing study design. Nat Rev Genet 14: 321-332. nrg3445 [pii];10.1038/nrg3445 [doi].
66. Pleasance ED, Stephens PJ, O'Meara S, McBride DJ, Meynert A, et al. (2010) A small-cell lung cancer genome with complex signatures of tobacco exposure. Nature 463: 184-190. nature08629 [pii];10.1038/nature08629 [doi].
67. Sabarinathan R, Tafer H, Seemann SE, Hofacker IL, Stadler PF, et al. (2013) The RNAsnp web server: predicting SNP effects on local RNA secondary structure. Nucleic Acids Res. gkt291 [pii];10.1093/nar/gkt291 [doi].