Comprehensive exploration of novel chimeric transcripts in clear cell renal cell carcinomas using whole transcriptome analysis

Genes Chromosomes and Cancer

Volumn 53, Issue 12, 2014, Pages 1018-1032

  Gotoh, Masahiro ^a   Ichikawa, Hitoshi ^a   Arai, Eri ^a   Chiku, Suenori ^b   Sakamoto, Hiromi ^a   Fujimoto, Hiroyuki ^c   Hiramoto, Masaki ^d   Nammo, Takao ^d   Yasuda, Kazuki ^d   Yoshida, Teruhiko ^a   Kanai, Yae ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b MIZUHO INFORMATION AND RESEARCH INSTITUTE   (Japan)

^c NATIONAL CANCER CENTER HOSPITAL   (Japan)

^d NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; ONCOPROTEIN;

ADULT; AGED; COHORT ANALYSIS; FEMALE; GENE EXPRESSION PROFILING; GENE FUSION; GENETICS; HUMAN; KIDNEY CARCINOMA; KIDNEY TUMOR; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, RENAL CELL; COHORT STUDIES; FEMALE; GENE EXPRESSION PROFILING; GENE FUSION; HUMANS; KIDNEY NEOPLASMS; MALE; MIDDLE AGED; ONCOGENE PROTEINS, FUSION; RNA, MESSENGER;

EID: 84907952394     PISSN: 10452257     EISSN: 10982264     Source Type: Journal    
DOI: 10.1002/gcc.22211     Document Type: Article

References (53)

1. Arai E, Kanai Y. 2010. Genetic and epigenetic alterations during renal carcinogenesis. Int J Clin Exp Pathol 4:58-73.
2. Arai E, Kanai Y, Ushijima S, Fujimoto H, Mukai K, Hirohashi S. 2006. Regional DNA hypermethylation and DNA methyltransferase (DNMT) 1 protein overexpression in both renal tumors and corresponding nontumorous renal tissues. Int J Cancer 119:288-296.
3. Baldewijns MM, van Vlodrop IJ, Vermeulen PB, Soetekouw PM, van Engeland M, de Bruïne AP. 2010. VHL and HIF signalling in renal cell carcinogenesis. J Pathol 221:125-138.
4. Bava FA, Eliscovich C, Ferreira PG, Miñana B, Ben-Dov C, Guigó R, Valcárcel J, Méndez R. 2013. CPEB1 coordinates alternative 3′-UTR formation with translational regulation. Nature 495:121-125.
5. Caldeira J, Simões-Correia J, Paredes J, Pinto MT, Sousa S, Corso G, Marrelli D, Roviello F, Pereira PS, Weil D, Oliveira C, Casares F, Seruca R. 2012. CPEB1, a novel gene silenced in gastric cancer: A Drosophila approach. Gut 61:1115-1123.
6. Cantile M, Marra L, Franco R, Ascierto P, Liguori G, De Chiara A, Botti G. 2013. Molecular detection and targeting of EWSR1 fusion transcripts in soft tissue tumors. Med Oncol 30:412.
7. Chan WK, Bhalla AD, Le Hir H, Nguyen LS, Huang L, Gécz J, Wilkinson MF. 2009. A UPF3-mediated regulatory switch that maintains RNA surveillance. Nat Struct Mol Biol 16:747-753.
8. Clark J, Lu YJ, Sidhar SK, Parker C, Gill S, Smedley D, Hamoudi R, Linehan WM, Shipley J, Cooper CS. 1997. Fusion of splicing factor genes PSF and NonO (p54nrb) to the TFE3 gene in papillary renal cell carcinoma. Oncogene 15:2233-2239.
9. Coutinho-Camillo CM, Salaorni S, Sarkis AS, Nagai MA. 2006. Differentially expressed genes in the prostate cancer cell line LNCaP after exposure to androgen and anti-androgen. Cancer Genet Cytogenet 166:130-138.
10. Dalgliesh GL, Furge K, Greenman C, Chen L, Bignell G, Butler A, Davies H, Edkins S, Hardy C, Latimer C, Teague J, Andrews J, Barthorpe S, Beare D, Buck G, Campbell PJ, Forbes S, Jia M, Jones D, Knott H, Kok CY, Lau KW, Leroy C, Lin ML, McBride DJ, Maddison M, Maguire S, McLay K, Menzies A, Mironenko T, Mulderrig L, Mudie L, O'Meara S, Pleasance E, Rajasingham A, Shepherd R, Smith R, Stebbings L, Stephens P, Tang G, Tarpey PS, Turrell K, Dykema KJ, Khoo SK, Petillo D, Wondergem B, Anema J, Kahnoski RJ, Teh BT, Stratton MR, Futreal PA. 2010. Systematic sequencing of renal carcinoma reveals inactivation of histone-modifying genes. Nature 463:360-363.
11. Davies JA, Buchman VL, Krylova O, Ninkina NN. 1997. Molecular cloning and expression pattern of rpr-1, a resiniferatoxin-binding, phosphotriesterase-related protein, expressed in rat kidney tubules. FEBS Lett 410:378-382.
12. Debelenko LV, Raimondi SC, Daw N, Shivakumar BR, Huang D, Nelson M, Bridge JA. 2011. Renal cell carcinoma with novel VCL-ALK fusion: New representative of ALK-associated tumor spectrum. Mod Pathol 24:430-442.
13. Eble JN, Togashi K, Pisani P. 2004. Renal cell carcinoma. In: Eble JN, Sauter G, Epstein JI, Sesterhenn IA, editors. World Health Organization classification of tumours. Pathology and genetics. Tumours of the urinary system and male genital organs. Lyon: IARC, pp. 10-43.
14. Fuhrman SA, Lasky LC, Limas, C. 1982. Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol 6:655-663.
15. Gimm O, Chi H, Dahia PL, Perren A, Hinze R, Komminoth P, Dralle H, Reynolds PR, Eng C. 2001. Somatic mutation and germline variants of MINPP1, a phosphatase gene located in proximity to PTEN on 10q23.3, in follicular thyroid carcinomas. J Clin Endocrinol Metab 86:1801-1805.
16. Green WM, Yonescu R, Morsberger L, Morris K, Netto GJ, Epstein JI, Illei PB, Allaf M, Ladanyi M, Griffin CA, Argani P. 2013. Utilization of a TFE3 break-apart FISH assay in a renal tumor consultation service. Am J Surg Pathol 37:1150-1163.
17. Guo G, Gui Y, Gao S, Tang A, Hu X, Huang Y, Jia W, Li Z, He M, Sun L, Song P, Sun X, Zhao X, Yang S, Liang C, Wan S, Zhou F, Chen C, Zhu J, Li X, Jian M, Zhou L, Ye R, Huang P, Chen J, Jiang T, Liu X, Wang Y, Zou J, Jiang Z, Wu R, Wu S, Fan F, Zhang Z, Liu L, Yang R, Liu X, Wu H, Yin W, Zhao X, Liu Y, Peng H, Jiang B, Feng Q, Li C, Xie J, Lu J, Kristiansen K, Li Y, Zhang X, Li S, Wang J, Yang H, Cai Z, Wang J. 2012. Frequent mutations of genes encoding ubiquitin-mediated proteolysis pathway components in clear cell renal cell carcinoma. Nat Genet 44:17-19.
18. Helmlinger D, Hardy S, Abou-Sleymane G, Eberlin A, Bowman AB, Gansmüller A, Picaud S, Zoghbi HY, Trottier Y, Tora L, Devys D. 2006. Glutamine-expanded ataxin-7 alters TFTC/STAGA recruitment and chromatin structure leading to photoreceptor dysfunction. PLoS Biol 4:e67.
19. Jarjanazi H, Kiefer J, Savas S, Briollais L, Tuzmen S, Pabalan N, Ibrahim-Zada I, Mousses S, Ozcelik H. 2008. Discovery of genetic profiles impacting response to chemotherapy: Application to gemcitabine. Hum Mutat 29:461-467.
20. Karras JR, Paisie CA, Huebner K. 2014. Replicative Stress and the FHIT Gene: Roles in tumor suppression, genome stability and prevention of carcinogenesis. Cancers (Basel) 6:1208-1219.
21. Keller W, Minvielle-Sebastia L. 1997. A comparison of mammalian and yeast pre-mRNA 3′-end processing. Curr Opin Cell Biol 9:329-336.
22. Kohno T, Ichikawa H, Totoki Y, Yasuda K, Hiramoto M, Nammo T, Sakamoto H, Tsuta K, Furuta K, Shimada Y, Iwakawa R, Ogiwara H, Oike T, Enari M, Schetter AJ, Okayama H, Haugen A, Skaug V, Chiku S, Yamanaka I, Arai Y, Watanabe S, Sekine I, Ogawa S, Harris CC, Tsuda H, Yoshida T, Yokota J, Shibata T. 2012. KIF5B-RET fusions in lung adenocarcinoma. Nat Med 18:375-377.
23. Kondo A, Hashimoto S, Yano H, Nagayama K, Mazaki Y, Sabe H. 2000. A new paxillin-binding protein, PAG3/Papalpha/KIAA0400, bearing an ADP-ribosylation factor GTPase-activating protein activity, is involved in paxillin recruitment to focal adhesions and cell migration. Mol Biol Cell 11:1315-1327.
24. Lamesch P, Li N, Milstein S, Fan C, Hao T, Szabo G, Hu Z, Venkatesan K, Bethel G, Martin P, Rogers J, Lawlor S, McLaren S, Dricot A, Borick H, Cusick ME, Vandenhaute J, Dunham I, Hill DE, Vidal M. 2007. hORFeome v3.1: A resource of human open reading frames representing over 10, 000 human genes. Genomics 89:307-315.
25. Li A, Liu Z, Lezon-Geyda K, Sarkar S, Lannin D, Schulz V, Krop I, Winer E, Harris L, Tuck D. 2011. GPHMM: An integrated hidden Markov model for identification of copy number alteration and loss of heterozygosity in complex tumor samples using whole genome SNP arrays. Nucleic Acids Res 39:4928-4941.
26. Li H, Wang J, Mor G, Sklar J. 2008. A neoplastic gene fusion mimics trans-splicing of RNAs in normal human cells. Science 321:1357-1361.
27. Liu Q, Zhao XY, Bai RZ, Liang SF, Nie CL, Yuan Z, Wang CT, Wu Y, Chen LJ, Wei YQ. 2009. Induction of tumor inhibition and apoptosis by a candidate tumor suppressor gene DRR1 on 3p21.1. Oncol Rep 22:1069-1075.
28. Ljungberg B, Campbell SC, Choi HY, Jacqmin D, Lee JE, Weikert S, Kiemeney LA. 2011. The epidemiology of renal cell carcinoma. Eur Urol 60:615-621.
29. Loewy AD, Niles KM, Anastasio N, Watkins D, Lavoie J, Lerner-Ellis JP, Pastinen T, Trasler JM, Rosenblatt DS. 2009. Epigenetic modification of the gene for the vitamin B(12) chaperone MMACHC can result in increased tumorigenicity and methionine dependence. Mol Genet Metab 96:261-267.
30. Mariño-Enríquez A, Ou WB, Weldon CB, Fletcher JA, Pérez-Atayde AR. 2011. ALK rearrangement in sickle cell trait-associated renal medullary carcinoma. Genes Chromosomes Cancer 50:146-153.
31. Matsui C, Kaieda S, Ikegami T, Mimori-Kiyosue Y. 2008. Identification of a link between the SAMP repeats of adenomatous polyposis coli tumor suppressor and the Src homology 3 domain of DDEF. J Biol Chem 283:33006-33020.
32. McNerney ME, Brown CD, Wang X, Bartom ET, Karmakar S, Bandlamudi C, Yu S, Ko J, Sandall BP, Stricker T, Anastasi J, Grossman RL, Cunningham JM, Le Beau MM, White KP. 2013. CUX1 is a haploinsufficient tumor suppressor gene on chromosome 7 frequently inactivated in acute myeloid leukemia. Blood 121:975-983.
33. McPherson A, Hormozdiari F, Zayed A, Giuliany R, Ha G, Sun MG, Griffith M, Heravi Moussavi A, Senz J, Melnyk N, Pacheco M, Marra MA, Hirst M, Nielsen TO, Sahinalp SC, Huntsman D, Shah SP. 2011. deFuse: An algorithm for gene fusion discovery in tumor RNA-Seq data. PLoS Comput Biol 7:e1001138.
34. Milne RL, Burwinkel B, Michailidou K, Arias-Perez JI, Zamora MP, Menéndez-Rodríguez P, Hardisson D, Mendiola M, González-Neira A, Pita G, Alonso MR, Dennis J, Wang Q, Bolla MK, Swerdlow A, Ashworth A, Orr N, Schoemaker M, Ko YD, Brauch H, Hamann U; The GENICA Network, Andrulis IL, Knight JA, Glendon G, Tchatchou S, Investigators K; Australian Ovarian Cancer Study Group, Matsuo K, Ito H, Iwata H, Tajima K, Li J, Brand JS, Brenner H, Dieffenbach AK, Arndt V, Stegmaier C, Lambrechts D, Peuteman G, Christiaens MR, Smeets A, Jakubowska A, Lubinski J, Jaworska-Bieniek K, Durda K, Hartman M, Hui M, Lim WY, Chan CW, Marme F, Yang R, Bugert P, Lindblom A, Margolin S, García-Closas M, Chanock SJ, Lissowska J, Figueroa JD, Bojesen SE, Nordestgaard BG, Flyger H, Hooning MJ, Kriege M, van den Ouweland AM, Koppert LB, Fletcher O, Johnson N, Dos-Santos-Silva I, Peto J, Zheng W, Deming-Halverson S, Shrubsole MJ, Long J, Chang-Claude J, Rudolph A, Seibold P, Flesch-Janys D, Winqvist R, Pylkäs K, Jukkola-Vuorinen A, Grip M, Cox A, Cross SS, Reed MW, Schmidt MK, Broeks A, Cornelissen S, Braaf L, Kang D, Choi JY, Park SK, Noh DY, Simard J, Dumont M, Goldberg MS, Labrèche F, Fasching PA, Hein A, Ekici AB, Beckmann MW, Radice P, Peterlongo P, Azzollini J, Barile M, Sawyer E, Tomlinson I, Kerin M, Miller N, Hopper JL, Schmidt DF, Makalic E, Southey MC, Teo SH, Yip CH, Sivanandan K, Tay WT, Shen CY, Hsiung CN, Yu JC, Hou MF, Guénel P, Truong T, Sanchez M, Mulot C, Blot W, Cai Q, Nevanlinna H, Muranen TA, Aittomäki K, Blomqvist C, Wu AH, Tseng CC, Van Den Berg D, Stram DO, Bogdanova N, Dörk T, Muir K, Lophatananon A, Stewart-Brown S, Siriwanarangsan P, Mannermaa A, Kataja V, Kosma VM, Hartikainen JM, Shu XO, Lu W, Gao YT, Zhang B, Couch FJ, Toland AE; TNBCC, Yannoukakos D, Sangrajrang S, McKay J, Wang X, Olson JE, Vachon C, Purrington K, Severi G, Baglietto L, Haiman CA, Henderson BE, Schumacher F, Le Marchand L, Devilee P, Tollenaar RA, Seynaeve C, Czene K, Eriksson M, Humphreys K, Darabi H, Ahmed S, Shah M, Pharoah PD, Hall P, Giles GG, Benítez J, Dunning AM, Chenevix-Trench G, Easton DF. Common non-synonymous SNPs associated with breast cancer susceptibility: Findings from the Breast Cancer Association Consortium. Hum Mol Genet (in press).
35. Pflueger D, Sboner A, Storz M, Roth J, Compérat E, Bruder E, Rubin MA, Schraml P, Moch H. 2013. Identification of molecular tumor markers in renal cell carcinomas with TFE3 protein expression by RNA sequencing. Neoplasia 15:1231-1240.
36. Rao Q, Williamson SR, Zhang S, Eble JN, Grignon DJ, Wang M, Zhou XJ, Huang W, Tan PH, Maclennan GT, Cheng L. 2013. TFE3 break-apart FISH has a higher sensitivity for Xp11.2 translocation-associated renal cell carcinoma compared with TFE3 or cathepsin K immunohistochemical staining alone: Expanding the morphologic spectrum. Am J Surg Pathol 37:804-815.
37. Ribeiro IP, Marques F, Caramelo F, Ferrão J, Prazeres H, Julião MJ, Rifi W, Savola S, de Melo JB, Baptista IP, Carreira IM. 2014. Genetic imbalances detected by multiplex ligation-dependent probe amplification in a cohort of patients with oral squamous cell carcinoma-the first step toward clinical personalized medicine. Tumour Biol 35:4687-4695.
38. Sato Y, Yoshizato T, Shiraishi Y, Maekawa S, Okuno Y, Kamura T, Shimamura T, Sato-Otsubo A, Nagae G, Suzuki H, Nagata Y, Yoshida K, Kon A, Suzuki Y, Chiba K, Tanaka H, Niida A, Fujimoto A, Tsunoda T, Morikawa T, Maeda D, Kume H, Sugano S, Fukayama M, Aburatani H, Sanada M, Miyano S, Homma Y, Ogawa S. 2013. Integrated molecular analysis of clear-cell renal cell carcinoma. Nat Genet 45:860-867.
39. Shima Y, Kitabayashi I. 2011. Deregulated transcription factors in leukemia. Int J Hematol 94:134-141.
40. Sobin LH, Gospodarowicz M, Wittekind C. 2009. International Union Against Cancer (UICC). TNM classification of malignant tumors, 7th ed. New York: Wiley Periodicals.
41. Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, Fujiwara S, Watanabe H, Kurashina K, Hatanaka H, Bando M, Ohno S, Ishikawa Y, Aburatani H, Niki T, Sohara Y, Sugiyama Y, Mano H. 2007. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 448:561-566.
42. Sugawara E, Togashi Y, Kuroda N, Sakata S, Hatano S, Asaka R, Yuasa T, Yonese J, Kitagawa M, Mano H, Ishikawa Y, Takeuchi K. 2012. Identification of anaplastic lymphoma kinase fusions in renal cancer: Large-scale immunohistochemical screening by the intercalated antibody-enhanced polymer method. Cancer 118:4427-4436.
43. Takeuchi K, Soda M, Togashi Y, Suzuki R, Sakata S, Hatano S, Asaka R, Hamanaka W, Ninomiya H, Uehara H, Lim Choi Y, Satoh Y, Okumura S, Nakagawa K, Mano H, Ishikawa Y. 2012. RET, ROS1 and ALK fusions in lung cancer. Nat Med 18:378-381.
44. Tanuma N, Nomura M, Ikeda M, Kasugai I, Tsubaki Y, Takagaki K, Kawamura T, Yamashita Y, Sato I, Sato M, Katakura R, Kikuchi K, Shima H. 2009. Protein phosphatase Dusp26 associates with KIF3 motor and promotes N-cadherin-mediated cell-cell adhesion. Oncogene 28:752-761.
45. The Cancer Genome Atlas Research Network. 2013. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 499:43-49.
46. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, Lee C, Montie JE, Shah RB, Pienta KJ, Rubin MA, Chinnaiyan AM. 2005. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 310:644-648.
47. van Haaften G, Dalgliesh GL, Davies H, Chen L, Bignell G, Greenman C, Edkins S, Hardy C, O'Meara S, Teague J, Butler A, Hinton J, Latimer C, Andrews J, Barthorpe S, Beare D, Buck G, Campbell PJ, Cole J, Forbes S, Jia M, Jones D, Kok CY, Leroy C, Lin ML, McBride DJ, Maddison M, Maquire S, McLay K, Menzies A, Mironenko T, Mulderrig L, Mudie L, Pleasance E, Shepherd R, Smith R, Stebbings L, Stephens P, Tang G, Tarpey PS, Turner R, Turrell K, Varian J, West S, Widaa S, Wray P, Collins VP, Ichimura K, Law S, Wong J, Yuen ST, Leung SY, Tonon G, DePinho RA, Tai YT, Anderson KC, Kahnoski RJ, Massie A, Khoo SK, Teh BT, Stratton MR, Futreal PA. 2009. Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer. Nat Genet 41:521-523.
48. Varela I, Tarpey P, Raine K, Huang D, Ong CK, Stephens P, Davies H, Jones D, Lin ML, Teague J, Bignell G, Butler A, Cho J, Dalgliesh GL, Galappaththige D, Greenman C, Hardy C, Jia M, Latimer C, Lau KW, Marshall J, McLaren S, Menzies A, Mudie L, Stebbings L, Largaespada DA, Wessels LF, Richard S, Kahnoski RJ, Anema J, Tuveson DA, Perez-Mancera PA, Mustonen V, Fischer A, Adams DJ, Rust A, Chan-on W, Subimerb C, Dykema K, Furge K, Campbell PJ, Teh BT, Stratton MR, Futreal PA. 2011. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 469:539-542.
49. Wang L, Darling J, Zhang JS, Liu W, Qian J, Bostwick D, Hartmann L, Jenkins R, Bardenhauer W, Schutte J, Opalka B, Smith DI. 2000. Loss of expression of the DRR 1 gene at chromosomal segment 3p21.1 in renal cell carcinoma. Genes Chromosomes Cancer 27:1-10.
50. Yuan H, Qin F, Movassagh M, Park H, Golden W, Xie Z, Zhang P, Sklar J, Li H. 2013. A chimeric RNA characteristic of rhabdomyosarcoma in normal myogenesis process. Cancer Discov 3:1394-1403.
51. Yu G, Tseng GC, Yu YP, Gavel T, Nelson J, Wells A, Michalopoulos G, Kokkinakis D, Luo JH. 2006. CSR1 suppresses tumor growth and metastasis of prostate cancer. Am J Pathol 168:597-607.
52. Zhang J, Wan L, Dai X, Sun Y, Wei W. 2014. Functional characterization of Anaphase Promoting Complex/Cyclosome (APC/C) E3 ubiquitin ligases in tumorigenesis. Biochim Biophys Acta 1845:277-293.
53. Zhu ZH, Yu YP, Shi YK, Nelson JB, Luo JH. 2009. CSR1 induces cell death through inactivation of CPSF3. Oncogene 28:41-51.