Genomics of chromophobe renal cell carcinoma: Implications from a rare tumor for pan-cancer studies

Oncoscience

Volumn 2, Issue 2, 2015, Pages 81-90

  Rathmell, Kimryn W ^d   Chen, Fengju ^a   Creighton, Chad J ^a,b,c  

^a Dan L Duncan Cancer Center   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

ChRCC; Chromophobe; Genomics; Kidney cancer; Mitochondria; TCGA; TERT

Indexed keywords

EID: 84958535301     PISSN: None     EISSN: 23314737     Source Type: Journal    
DOI: 10.18632/oncoscience.130     Document Type: Article

References (50)

1. Davis C, Ricketts C, Wang M, Yang L, Cherniack A, Shen H, Buhay C, Kang H, Kim S, Fahey C, Hacker K, Bhanot G, Gordenin D, Chu A, Gunaratne P, Biehl M, et al. The somatic genomic landscape of chromophobe renal cell carcinoma. Cancer Cell. 2014; 26(3):319-330.
2. Huang FW, Hodis E, Xu MJ, Kryukov GV, Chin L and Garraway LA. Highly recurrent TERT promoter mutations in human melanoma. Science. 2013; 339(6122):957-959.
3. Heidenreich B, Rachakonda P, Hemminki K and Kumar R. TERT promoter mutations in cancer development. Curr Opin Genet Dev. 2013; 24C:30-37.
4. Storkel S, Eble JN, Adlakha K, Amin M, Blute ML, Bostwick DG, Darson M, Delahunt B and Iczkowski K. Classification of renal cell carcinoma: Workgroup No. 1. Union Internationale Contre le Cancer (UICC) and the American Joint Committee on Cancer (AJCC). Cancer. 1997; 80(5):987-989.
5. Amin MB, Amin MB, Tamboli P, Javidan J, Stricker H, de-Peralta Venturina M, Deshpande A and Menon M. Prognostic impact of histologic subtyping of adult renal epithelial neoplasms: an experience of 405 cases. Am J Surg Pathol. 2002; 26(3):281-291.
6. Przybycin CG, Cronin AM, Darvishian F, Gopalan A, Al-Ahmadie HA, Fine SW, Chen YB, Bernstein M, Russo P, Reuter VE and Tickoo SK. Chromophobe renal cell carcinoma: a clinicopathologic study of 203 tumors in 200 patients with primary resection at a single institution. Am J Surg Pathol. 2011; 35(7):962-970.
7. Speicher MR, Schoell B, du Manoir S, Schrock E, Ried T, Cremer T, Storkel S, Kovacs A and Kovacs G. Specific loss of chromosomes 1, 2, 6, 10, 13, 17, and 21 in chromophobe renal cell carcinomas revealed by comparative genomic hybridization. Am J Pathol. 1994; 145(2):356-364.
8. Schmidt LS, Warren MB, Nickerson ML, Weirich G, Matrosova V, Toro JR, Turner ML, Duray P, Merino M, Hewitt S, Pavlovich CP, Glenn G, Greenberg CR, Linehan WM and Zbar B. Birt-Hogg-Dube syndrome, a genodermatosis associated with spontaneous pneumothorax and kidney neoplasia, maps to chromosome 17p11.2. Am J Hum Genet. 2001; 69(4):876-882.
9. Nagy A, Zoubakov D, Stupar Z and Kovacs G. Lack of mutation of the folliculin gene in sporadic chromophobe renal cell carcinoma and renal oncocytoma. Int J Cancer. 2004; 109(3):472-475.
10. Gad S, Lefevre SH, Khoo SK, Giraud S, Vieillefond A, Vasiliu V, Ferlicot S, Molinie V, Denoux Y, Thiounn N, Chretien Y, Mejean A, Zerbib M, Benoit G, Herve JM, Allegre G, et al. Mutations in BHD and TP53 genes, but not in HNF1beta gene, in a large series of sporadic chromophobe renal cell carcinoma. Br J Cancer. 2007; 96(2):336-340.
11. Shuch B, Ricketts CJ, Vocke CD, Komiya T, Middelton LA, Kauffman EC, Merino MJ, Metwalli AR, Dennis P and Linehan WM. Germline PTEN Mutation Cowden Syndrome: An Under-Appreciated Form of Hereditary Kidney Cancer. The Journal of urology. 2013.
12. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, Bignell GR, Bolli N, Borg A, Borresen-Dale AL, Boyault S, Burkhardt B, Butler AP, Caldas C, Davies HR, Desmedt C, et al. Signatures of mutational processes in human cancer. Nature. 2013; 500(7463):415-421.
13. Cancer Genome Atlas N. Comprehensive molecular portraits of human breast tumours. Nature. 2012; 490(7418):61-70.
14. Thoenes W, Storkel S and Rumpelt HJ. Human chromophobe cell renal carcinoma. Virchows Archiv B, Cell pathology including molecular pathology. 1985; 48(3):207-217.
15. Tickoo SK, Lee MW, Eble JN, Amin M, Christopherson T, Zarbo RJ and Amin MB. Ultrastructural observations on mitochondria and microvesicles in renal oncocytoma, chromophobe renal cell carcinoma, and eosinophilic variant of conventional (clear cell) renal cell carcinoma. Am J Surg Pathol. 2000; 24(9):1247-1256.
16. The_Cancer_Genome_Atlas_Research_Network. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature. 2013; 499(7456):43-49.
17. Shen H and Laird PW. Interplay between the cancer genome and epigenome. Cell. 2013; 153(1):38-55.
18. Prasad SR, Narra VR, Shah R, Humphrey PA, Jagirdar J, Catena JR, Dalrymple NC and Siegel CL. Segmental disorders of the nephron: histopathological and imaging perspective. The British journal of radiology. 2007; 80(956):593-602.
19. Cheval L, Pierrat F, Rajerison R, Piquemal D and Doucet A. Of mice and men: divergence of gene expression patterns in kidney. PloS one. 2012; 7(10):e46876.
20. Hoadley K, Yau C, Wolf D, Cherniack A, Tamborero D, Ng S, Leiserson M, Niu B, McLellan M, Uzunangelov V, Zhang J, Kandoth C, Akbani R, Shen H, Omberg L, Chu A, et al. Multiplatform Analysis of 12 Cancer Types Reveals Molecular Classification within and across Tissues of Origin. Cell. 2014; 158(4):929-944.
21. Perou C, Sørlie T, Eisen M, van de Rijn M, Jeffrey S, Rees C, Pollack J, Ross D, Johnsen H, Akslen L, Fluge O, Pergamenschikov A, Williams C, Zhu S, Lønning P, Børresen-Dale A, et al. Molecular portraits of human breast tumours. Nature. 2000; 406(6797):747-752.
22. Williams A, Higgins J, Zhao H, Ljunberg B and Brooks J. CD 9 and vimentin distinguish clear cell from chromophobe renal cell carcinoma. BMC Clin Pathol. 2009; 9:9.
23. FANTOM_Consortium_and_the_RIKEN_PMI_and_ CLST_(DGT), Forrest A, Kawaji H, Rehli M, Baillie J, de Hoon M, Lassmann T, Itoh M, Summers K, Suzuki H, Daub C, Kawai J, Heutink P, Hide W, Freeman T, Lenhard B, et al. A promoter-level mammalian expression atlas. Nature. 2014; 507(7493):462-470.
24. Linehan W, Srinivasan R and Schmidt L. The genetic basis of kidney cancer: a metabolic disease. Nat Rev Urol. 2010; 7(5):277-285.
25. Linehan W and Rathmell W. Kidney cancer. Urol Oncol. 2012; 30(6):948-951.
26. Linehan W and Ricketts C. The metabolic basis of kidney cancer. Semin Cancer Biol. 2013; 23(1):46-55.
27. Tong W, Sourbier C, Kovtunovych G, Jeong S, Vira M, Ghosh M, Romero V, Sougrat R, Vaulont S, Viollet B, Kim Y, Lee S, Trepel J, Srinivasan R, Bratslavsky G, Yang Y, et al. The glycolytic shift in fumarate-hydratase-deficient kidney cancer lowers AMPK levels, increases anabolic propensities and lowers cellular iron levels. Cancer Cell. 2011; 20(3):315-327.
28. Gameiro P, Yang JM, AM, Pérez-Carro R, Baker R, Wang Z, Arreola A, Rathmell W, Olumi A, López-Larrubia P, Stephanopoulos G and Iliopoulos O. In vivo HIF-mediated reductive carboxylation is regulated by citrate levels and sensitizes VHL-deficient cells to glutamine deprivation. Cell Metab. 2013; 17(3):372-385.
29. Ho C, Chen S, Ho K, Chan W, Leung Y, Cheng K, Wong K, Cheung M and Wong K. Dual-tracer PET/CT in renal angiomyolipoma and subtypes of renal cell carcinoma. Clin Nucl Med. 2012; 37(11):1075-1082.
30. Amin MB, Paner GP, Alvarado-Cabrero I, Young AN, Stricker HJ, Lyles RH and Moch H. Chromophobe renal cell carcinoma: histomorphologic characteristics and evaluation of conventional pathologic prognostic parameters in 145 cases. Am J Surg Pathol. 2008; 32(12):1822-1834.
31. Klomp JA, Petillo D, Niemi NM, Dykema KJ, Chen J, Yang XJ, Saaf A, Zickert P, Aly M, Bergerheim U, Nordenskjold M, Gad S, Giraud S, Denoux Y, Yonneau L, Mejean A, et al. Birt-Hogg-Dube renal tumors are genetically distinct from other renal neoplasias and are associated with up-regulation of mitochondrial gene expression. BMC medical genomics. 2010; 3:59.
32. Simonnet H, Demont J, Pfeiffer K, Guenaneche L, Bouvier R, Brandt U, Schagger H and Godinot C. Mitochondrial complex I is deficient in renal oncocytomas. Carcinogenesis. 2003; 24(9):1461-1466.
33. Gasparre G, Hervouet E, de Laplanche E, Demont J, Pennisi LF, Colombel M, Mege-Lechevallier F, Scoazec JY, Bonora E, Smeets R, Smeitink J, Lazar V, Lespinasse J, Giraud S, Godinot C, Romeo G, et al. Clonal expansion of mutated mitochondrial DNA is associated with tumor formation and complex I deficiency in the benign renal oncocytoma. Hum Mol Genet. 2008; 17(7):986-995.
34. Mayr JA, Meierhofer D, Zimmermann F, Feichtinger R, Kogler C, Ratschek M, Schmeller N, Sperl W and Kofler B. Loss of complex I due to mitochondrial DNA mutations in renal oncocytoma. Clin Cancer Res. 2008; 14(8):2270-2275.
35. Larman TC, DePalma SR, Hadjipanayis AG, Cancer_ Genome_Atlas_Research_Network, Protopopov A, Zhang J, Gabriel SB, Chin L, Seidman CE, Kucherlapati R and Seidman JG. Spectrum of somatic mitochondrial mutations in five cancers. Proc Natl Acad Sci U S A. 2012; 109(35):14087-14091.
36. Hofhaus G and Attardi G. Efficient selection and characterization of mutants of a human cell line which are defective in mitochondrial DNA-encoded subunits of respiratory NADH dehydrogenase. Mol Cell Biol. 1995; 15(2):964-974.
37. Park J, Sharma L, Li H, Xiang R, Holstein D, Wu J, Lechleiter J, Naylor S, Deng J, Lu J and Bai Y. A heteroplasmic, not homoplasmic, mitochondrial DNA mutation promotes tumorigenesis via alteration in reactive oxygen species generation and apoptosis. Hum Mol Genet. 2009; 18(9):1578-1589.
38. Weinhold N, Jacobsen A, Schultz N, Sander C and Lee W. Genome-wide analysis of noncoding regulatory mutations in cancer. Nature genetics. 2014; 46(11):1160-1165.
39. Ward P and Thompson C. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell. 2012; 21(3):297-308.
40. Nik-Zainal S, Alexandrov LB, Wedge DC, Van Loo P, Greenman CD, Raine K, Jones D, Hinton J, Marshall J, Stebbings LA, Menzies A, Martin S, Leung K, Chen L, Leroy C, Ramakrishna M, et al. Mutational processes molding the genomes of 21 breast cancers. Cell. 2012; 149(5):979-993.
41. Yang L, Luquette L, Gehlenborg N, Xi R, Haseley P, Hsieh C, Zhang C, Ren X, Protopopov A, Chin L, Kucherlapati R, Lee C and Park P. Diverse mechanisms of somatic structural variations in human cancer genomes. Cell. 2013; 153(4):919-929.
42. Totoki Y, Tatsuno K, Covington K, Ueda H, Creighton C, Kato M, Tsuji S, Donehower L, Slagle B, Nakamura H, Yamamoto S, Shinbrot E, Hama N, Lehmkuhl M, Hosoda F, Arai Y, et al. Trans-ancestry mutational landscape of hepatocellular carcinoma genomes. Nature genetics. 2014; 46(12):1267-1273.
43. Y Chudnovsky, Adams A, Robbins P, Lin Q and Khavari P. Use of human tissue to assess the oncogenic activity of melanomaassociated mutations. Nat Genet. 2005; 37(7):745-749.
44. Weir B, Woo M, Getz G, Perner S, Ding L, Beroukhim R, Lin W, Province M, Kraja A, Johnson L, Shah K, Sato M, Thomas R, Barletta J, Borecki I, Broderick S, et al. Characterizing the cancer genome in lung adenocarcinoma. Nature. 2007; 450(7171):893-898.
45. Rafnar T, Sulem P, Stacey S, Geller F, Gudmundsson J, Sigurdsson A, Jakobsdottir M, Helgadottir H, Thorlacius S, Aben K, Blöndal T, Thorgeirsson T, Thorleifsson G, Kristjansson K, Thorisdottir K, Ragnarsson R, et al. Sequence variants at the TERT-CLPTM1L locus associate with many cancer types. Nature genetics. 2009; 41(2):221-227.
46. Fredriksson N, Ny L, Nilsson J and Larsson E. Systematic analysis of noncoding somatic mutations and gene expression alterations across 14 tumor types. Nature genetics. 2014; 46(12):1258-1263.
47. Zhao Y, Wang S, Popova E, Grigoryev S and Zhu J. Rearrangement of upstream sequences of the hTERT gene during cellular immortalization. Genes Chromosomes Cancer. 2009; 48(11):963-974.
48. International_Cancer_Genome_Consortium. International network of cancer genome projects. Nature. 2010; 464(7291):993-998.
49. Cancer_Genome_Atlas_Research_Network, Weinstein J, Collisson E, Mills G, Shaw K, Ozenberger B, Ellrott K, Shmulevich I, Sander C and Stuart J. The Cancer Genome Atlas Pan-Cancer analysis project. Nature genetics. 2013; 45(10):1113-1120.
50. Eisen MB, Spellman PT, Brown PO and Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA. 1998; 95:14863-14868.