Genomics and epigenomics of renal cell carcinoma

Seminars in Cancer Biology

Volumn 23, Issue 1, 2013, Pages 10-17

  Maher, Eamonn R ^a,b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b BIRMINGHAM WOMEN S HOSPITAL   (United Kingdom)

Author keywords

Epigenetics; Methylation; Mutation; Oncogenes; Renal cell carcinoma; Tumour suppressor gene

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 2; MICRORNA; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN; WNT PROTEIN;

ATTITUDE TO HEALTH; CANCER DIAGNOSIS; CANCER GENETICS; CANCER GROWTH; CANCER PROGNOSIS; CANCER RISK; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CCND1 GENE; CHROMOSOME 3P; CHROMOSOME ABERRATION; CHROMOSOME LOSS; CHROMOSOME MAP; CLINICAL ASSESSMENT; CLINICAL FEATURE; COPY NUMBER VARIATION; DNA METHYLATION; EARLY DIAGNOSIS; EPAS1 GENE; EPIGENETICS; FAMILIAL CANCER; FAMILY HISTORY; FH GENE; FLCN GENE; GENE EXPRESSION; GENE FUNCTION; GENE INACTIVATION; GENE LOCUS; GENE MUTATION; GENE SILENCING; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC VARIABILITY; GENOMICS; HIF2 GENE; HISTOPATHOLOGY; HUMAN; ITPR2 GENE; KIDNEY CANCER; KIDNEY CARCINOMA; MET GENE; MOLECULAR DIAGNOSIS; MOLECULAR PATHOLOGY; MOLECULARLY TARGETED THERAPY; PERSONALIZED MEDICINE; RARE DISEASE; REVIEW; SDHB GENE; SDHD GENE; SOMATIC MUTATION; TRANSLATIONAL RESEARCH; TUMOR SUPPRESSOR GENE; VHL GENE; VON HIPPEL LINDAU DISEASE; WNT SIGNALING PATHWAY;

CARCINOMA, RENAL CELL; EPIGENOMICS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC PREDISPOSITION TO DISEASE; GENOMICS; GERM-LINE MUTATION; HUMANS; KIDNEY NEOPLASMS; MICRORNAS; TRANSLATIONAL MEDICAL RESEARCH; TUMOR MARKERS, BIOLOGICAL;

EID: 84873084354     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2012.06.003     Document Type: Review

References (92)

1. Mancini V., Battaglia M., Ditonno P., Palazzo S., Lastilla G., Montironi R., et al. Current insights in renal cell cancer pathology. Urologic Oncology 2008, 26:225-238.
2. Foster K., Prowse A., van den Berg A., Fleming S., Hulsbeek M.M., Crossey P.A., et al. Somatic mutations of the von Hippel-Lindau disease tumour suppressor gene in non-familial clear cell renal carcinoma. Human Molecular Genetics 1994, 3:2169-2173.
3. Gnarra J.R., Tory K., Weng Y., Schmidt L., Wei M.H., Li H., et al. Mutations of the VHL tumour suppressor gene in renal carcinoma. Nature Genetics 1994, 7:85-90.
4. Banks R.E., Tirukonda P., Taylor C., Hornigold N., Astuti D., Cohen D., et al. Genetic and epigenetic analysis of von Hippel-Lindau (VHL) gene alterations and relationship with clinical variables in sporadic renal cancer. Cancer Research 2006, 66:2000-2011.
5. Maher E.R. Genetics of familial renal cancers. Nephron Experimental Nephrology 2011, 118:e21-e26.
6. Maxwell P.H., Wiesener M.S., Chang G.W., Clifford S.C., Vaux E.C., Cockman M.E., et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999, 399:271-275.
7. Semenza G.L. Oxygen sensing, homeostasis, and disease. New England Journal of Medicine 2011, 365:537-547.
8. Clague J., Lin J., Cassidy A., Matin S., Tannir N.M., Tamboli P., et al. Family history and risk of renal cell carcinoma: results from a case-control study and systematic meta-analysis. Cancer Epidemiology, Biomarkers and Prevention 2009, 18:801-807.
9. Purdue M.P., Johansson M., Zelenika D., Toro J.R., Scelo G., Moore L.E., et al. Genome-wide association study of renal cell carcinoma identifies two susceptibility loci on 2p21 and 11q13.3. Nature Genetics 2011, 43:60-65.
10. Kondo K., Klco J., Nakamura E., Lechpammer M., Kaelin W.G. Inhibition of HIF is necessary for tumor suppression by the von Hippel-Lindau protein. Cancer Cell 2002, 1:237-246.
11. Gordan J.D., Lal P., Dondeti V.R., Letrero R., Parekh K.N., Oquendo C.E., et al. HIF-alpha effects on c-Myc distinguish two subtypes of sporadic VHL-deficient clear cell renal carcinoma. Cancer Cell 2008, 14:435-446.
12. Zatyka M., da Silva N.F., Clifford S.C., Morris M.R., Wiesener M.S., Eckardt K.U., et al. Identification of cyclin D1 and other novel targets for the von Hippel-Lindau tumor suppressor gene by expression array analysis and investigation of cyclin D1 genotype as a modifier in von Hippel-Lindau disease. Cancer Research 2002, 62:3803-3811.
13. Wu X., Scelo G., Purdue M.P., Rothman N., Johansson M., Ye Y., et al. A genome-wide association study identifies a novel susceptibility locus for renal cell carcinoma on 12p11.23. Human Molecular Genetics 2011, [Nov 1, Epub ahead of print].
14. Adams K.F., Leitzmann M.F., Albanes D., Kipnis V., Moore S.C., Schatzkin A., Chow W.H. Body size and renal cell cancer incidence in a large US cohort study. American Journal of Epidemiology 2008, 168:268-277.
15. Bennett K.L., Mester J., Eng C. Germline epigenetic regulation of KILLIN in Cowden and Cowden-like syndrome. JAMA 2010, 304:2724-2731.
16. Bennett K.L., Campbell R., Ganapathi S., Zhou M., Rini B., Ganapathi R., et al. Germline and somatic DNA methylation and epigenetic regulation of KILLIN in renal cell carcinoma. Genes, Chromosomes and Cancer 2011, 50:654-661.
17. Zbar B., Brauch H., Talmadge C., Linehan M. Loss of alleles of loci on the short arm of chromosome 3 in renal cell carcinoma. Nature 1987, 327:721-724.
18. Kovacs G., Erlandsson R., Boldog F., Ingvarsson S., Müller-Brechlin R., Klein G., Sümegi J. Consistent chromosome 3p deletion and loss of heterozygosity in renal cell carcinoma. Proceedings of the National Academy of Sciences of the United States of America 1988, 85:1571-1575.
19. Seizinger B.R., Rouleau G.A., Ozelius L.J., Lane A.H., Farmer G.E., Lamiell J.M., et al. von Hippel-Lindau disease maps to the region of chromosome 3 associated with renal cell carcinoma. Nature 1988, 332:268-269.
20. Limon J., Mrózek K., Heim S., Elfving P., Nedoszytko B., Babińska M., et al. On the significance of trisomy 7 and sex chromosome loss in renal cell carcinoma. Cancer Genetics and Cytogenetics 1990, 49:259-263.
21. Sanchez Y., el-Naggar A., Pathak S., Killary A.M. A tumor suppressor locus within 3p14-p12 mediates rapid cell death of renal cell carcinoma in vivo. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:3383-3387.
22. Wilke C.M., Guo S.W., Hall B.K., Boldog F., Gemmill R.M., Chandrasekharappa S.C., et al. Multicolor FISH mapping of YAC clones in 3p14 and identification of a YAC spanning both FRA3B and the t(3;8) associated with hereditary renal cell carcinoma. Genomics 1994, 22:319-326.
23. Lubinski J., Hadaczek P., Podolski J., Toloczko A., Sikorski A., McCue P., et al. Common regions of deletion in chromosome regions 3p12 and 3p14 2 in primary clear cell renal carcinomas. Cancer Research 1994, 54:3710-3713.
24. van den Berg A., Dijkhuizen T., Draaijers T.G., Hulsbeek M.M., Maher E.R., van den Berg E., et al. Analysis of multiple renal cell adenomas and carcinomas suggests allelic loss at 3p21 to be a prerequisite for malignant development. Genes, Chromosomes and Cancer 1997, 19:228-232.
25. van den Berg E., van der Hout A.H., Oosterhuis J.W., Störkel S., Dijkhuizen T., Dam A., et al. Cytogenetic analysis of epithelial renal-cell tumors: relationship with a new histopathological classification. International Journal of Cancer 1993, 55:223-227.
26. Clifford S.C., Prowse A.H., Affara N.A., Buys C.H., Maher E.R. Inactivation of the von Hippel-Lindau (VHL) tumour suppressor gene and allelic losses at chromosome arm 3p in primary renal cell carcinoma: evidence for a VHL-independent pathway in clear cell renal tumourigenesis. Genes, Chromosomes and Cancer 1998, 22:200-209.
27. Ogawa O., Kakehi Y., Ogawa K., Koshiba M., Sugiyama T., Yoshida O. Allelic loss at chromosome 3p characterizes clear cell phenotype of renal cell carcinoma. Cancer Research 1991, 51:949-953.
28. Hughson M.D., Johnson L.D., Silva F.G., Kovacs G. Nonpapillary and papillary renal cell carcinoma: a cytogenetic and phenotypic study. Modern Pathology 1993, 6:449-456.
29. Herbers J., Schullerus D., Müller H., Kenck C., Chudek J., Weimer J., et al. Significance of chromosome arm 14q loss in nonpapillary renal cell carcinomas. Genes, Chromosomes and Cancer 1997, 19:29-35.
30. Macher-Goeppinger S., Roth W., Wagener N., Hohenfellner M., Penzel R., Haferkamp A., et al. Molecular heterogeneity of TFE3 activation in renal cell carcinomas. Modern Pathology 2011, [October 28]. 10.1038/modpathol.2011.169.
31. Beroukhim R., Brunet J.P., Di Napoli A., Mertz K.D., Seeley A., Pires M.M., et al. Patterns of gene expression and copy-number alterations in von-Hippel Lindau disease-associated and sporadic clear cell carcinoma of the kidney. Cancer Research 2009, 69:4674-4681.
32. Dalgliesh G.L., Furge K., Greenman C., Chen L., Bignell G., Butler A., et al. Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature 2010, 463:360-363.
33. Matsuda D., Khoo S.K., Massie A., Iwamura M., Chen J., Petillo D., et al. Identification of copy number alterations and its association with pathological features in clear cell and papillary RCC. Cancer Letters 2008, 272:260-267.
34. Yusenko M.V., Kuiper R.P., Boethe T., Ljungberg B., van Kessel A.G., Kovacs G. High-resolution DNA copy number and gene expression analyses distinguish chromophobe renal cell carcinomas and renal oncocytomas. BMC Cancer 2009, 9:152.
35. Shuib S., Wei W., Sur H., Morris M.R., McMullan D., Rattenberry E., et al. Copy number profiling in von Hippel-Lindau disease renal cell carcinoma. Genes, Chromosomes and Cancer 2011, 50:479-488.
36. Koski T.A., Lehtonen H.J., Jee K.J., Ninomiya S., Joosse S.A., Vahteristo P., et al. Array comparative genomic hybridization identifies a distinct DNA copy number profile in renal cell cancer associated with hereditary leiomyomatosis and renal cell cancer. Genes, Chromosomes and Cancer 2009, 48:544-551.
37. Maher E.R., Yates J.R., Ferguson-Smith M.A. Statistical analysis of the two stage mutation model in von Hippel-Lindau disease, and in sporadic cerebellar haemangioblastoma and renal cell carcinoma. Journal of Medical Genetics 1990, 27:311-314.
38. Young A.C., Craven R.A., Cohen D., Taylor C., Booth C., Harnden P., et al. Analysis of VHL gene alterations and their relationship to clinical parameters in sporadic conventional renal cell carcinoma. Clinical Cancer Research 2009, 15:7582-7592.
39. Mandriota S.J., Turner K.J., Davies D.R., Murray P.G., Morgan N.V., Sowter H.M., et al. HIF activation identifies early lesions in VHL kidneys: evidence for site-specific tumor suppressor function in the nephron. Cancer Cell 2002, 1:459-468.
40. Morris M.R., Hughes D.J., Tian Y.M., Ricketts C.J., Lau K.W., Gentle D., et al. Mutation analysis of hypoxia-inducible factors HIF1A and HIF2A in renal cell carcinoma. Anticancer Research 2009, 29:4337-4343.
41. Shen C., Beroukhim R., Schumacher S.E., Zhou J., Chang M., Signoretti S., Kaelin W.G. Genetic and functional studies implicate HIF1α as a 14q kidney cancer suppressor gene. Cancer Discovery 2011, 1:222-235.
42. Chen J., Lui W-O., Vos M.D., Clark G.J., Takahashi M., et al. The t(1;3) breakpoint-spanning genes LSAMP and NORE1 are involved in clear cell renal cell carcinomas. Cancer Cell 2003, 4:405-413.
43. Kuiper R.P., Vreede L., Venkatachalam R., Ricketts C., Kamping E., Verwiel E., et al. The tumor suppressor gene FBXW7 is disrupted by a constitutional t(3;4)(q21;q31) in a patient with renal cell cancer. Cancer Genetics and Cytogenetics 2009, 195:105-111.
44. Schmidt L., Duh F.M., Chen F., Kishida T., Glenn G., Choyke P., et al. Germline and somatic mutations in the tyrosine kinase domain of the MET proto-oncogene in papillary renal carcinomas. Nature Genetics 1997, 16:68-73.
45. Zhao J., Yart A., Frigerio S., Perren A., Schraml P., Weisstanner C., et al. Sporadic human renal tumors display frequent allelic imbalances and novel mutations of the HRPT2 gene. Oncogene 2007, 26:3440-3449.
46. Varela I., Tarpey P., Raine K., Huang D., Ong C.K., Stephens P., et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 2011, 469:539-542.
47. van Haaften G., Dalgliesh G.L., Davies H., Chen L., Bignell G., Greenman C., et al. Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer. Nature Genetics 2009, 41:521-523.
48. Gui Y., Guo G., Huang Y., Hu X., Tang A., Gao S., et al. Frequent mutations of chromatin remodeling genes in transitional cell carcinoma of the bladder. Nature Genetics 2011, 43:875-878.
49. Jankowska A.M., Makishima H., Tiu R.V., Szpurka H., Huang Y., Traina F., et al. Mutational spectrum analysis of chronic myelomonocytic leukemia includes genes associated with epigenetic regulation: UTX, EZH2, and DNMT3A. Blood 2011, 118:3932-3941.
50. Tsai M.C., Wang J.K., Chang H.Y. Tumor suppression by the histone demethylase UTX. Cell Cycle 2010, 9:2043-2044.
51. Jensen L.R., Amende M., Gurok U., Moser B., Gimmel V., Tzschach A., et al. Mutations in the JARID1C gene, which is involved in transcriptional regulation and chromatin remodeling, cause X-linked mental retardation. American Journal of Human Genetics 2005, 76:227-236.
52. Niu X., Zhang T., Liao L., Zhou L., Lindner D.J., Zhou M., et al. The von Hippel-Lindau tumor suppressor protein regulates gene expression and tumor growth through histone demethylase JARID1C. Oncogene 2011, [July 4]. 10.1038/onc.2011.266.
53. Duns G., van den Berg E., van Duivenbode I., Osinga J., Hollema H., Hofstra R.M., Kok K. Histone methyltransferase gene SETD2 is a novel tumor suppressor gene in clear cell renal cell carcinoma. Cancer Research 2010, 70:4287-4291.
54. Wilson B.G., Roberts C.W. SWI/SNF nucleosome remodellers and cancer. Nature Reviews Cancer 2011, 11:481-492.
55. Xia W., Nagase S., Montia A.G., Kalachikov S.M., Keniry M., Su T., et al. BAF180 is a critical regulator of p21 induction and a tumor suppressor mutated in breast cancer. Cancer Research 2008, 68:1667-1674.
56. Burrows A.E., Smogorzewska A., Elledge S.J. Polybromo-associated BRG1-associated factor components BRD7 and BAF180 are critical regulators of p53 required for induction of replicative senescence. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:14280-14285.
57. Kulis M., Esteller M. DNA methylation and cancer. Advances in Genetics 2010, 70:27-56.
58. Issa J.-P.J., Kantarjian H.M. Targeting DNA methylation. Clinical Cancer Research 2009, 15:3938-3946.
59. Herman J.G., Latif F., Weng Y., Lerman M.I., Zbar B., Liu S., et al. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:9700-9704.
60. Morrissey C., Martinez A., Zatyka M., Agathanggelou A., Honorio S., Astuti D., et al. Epigenetic inactivation of the RASSF1A 3p21.3 tumor suppressor gene in both clear cell and papillary renal cell carcinoma. Cancer Research 2001, 61:7277-7281.
61. Dreijerink K., Braga E., Kuzmin I., Geil L., Duh F.M., Angeloni D., et al. The candidate tumor suppressor gene, RASSF1A, from human chromosome 3p21.3 is involved in kidney tumorigenesis. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:7504-7509.
62. Morris M.R., Maher E.R. Epigenetics of renal cell carcinoma: the path towards new diagnostics and therapeutics. Genome Medicine 2010, 2:59.
63. Awakura Y., Nakamura E., Ito N., Kamoto T., Ogawa O. Methylation-associated silencing of TU3A in human cancers. International Journal of Oncology 2008, 33(October (4)):893-899.
64. Zhang Q., Ying J., Li J., Fan Y., Poon F.F., Ng K.M., et al. Aberrant promoter methylation of DLEC1, a critical 3p22 tumor suppressor for renal cell carcinoma, is associated with more advanced tumor stage. Journal of Urology 2010, 184:731-737.
65. Kvasha S., Gordiyuk V., Kondratov A., Ugryn D., Zgonnyk Y.M., Rynditch A.V., Vozianov A.F. Hypermethylation of the 5'CpG island of the FHIT gene in clear cell renal carcinomas. Cancer Letters 2008, 265:250-257.
66. Awakura Y., Nakamura E., Ito N., Kamoto T., Ogawa O. Methylation-associated silencing of SFRP1 in renal cell carcinoma. Oncology Reports 2008, 20:1257-1263.
67. Gumz M.L., Zou H., Kreinest P.A., Childs A.C., Belmonte L.S., LeGrand S.N., et al. Secreted frizzled-related protein 1 loss contributes to tumor phenotype of clear cell renal cell carcinoma. Clinical Cancer Research 2007, 13:4740-4749.
68. Morris M.R., Ricketts C., Gentle D., Abdulrahman M., Clarke N., Brown M., et al. Identification of candidate tumour suppressor genes frequently methylated in renal cell carcinoma. Oncogene 2010, 29:2104-2117.
69. Hirata H., Hinoda Y., Nakajima K., Kawamoto K., Kikuno N., Ueno K., et al. Wnt antagonist DKK1 acts as a tumor suppressor gene that induces apoptosis and inhibits proliferation in human renal cell carcinoma. International Journal of Cancer 2010, 10.1002/ijc.25507.
70. Morris M.R., Gentle D., Abdulrahman M., Maina E.N., Gupta K., Banks R.E., et al. Tumor suppressor activity and epigenetic inactivation of hepatocyte growth factor activator inhibitor type 2/SPINT2 in papillary and clear cell renal cell carcinoma. Cancer Research 2005, 65:4598-4606.
71. Choi H., Chun Y.S., Kim T.Y., Park J.W. HIF-2alpha enhances beta-catenin/TCF-driven transcription by interacting with beta-catenin. Cancer Research 2010, 70:10101-10111.
72. Morais C., Gobe G., Johnson D.W., Healy H. The emerging role of nuclear factor kappa B in renal cell carcinoma. International Journal of Biochemistry and Cell Biology 2011, 43:1537-1549.
73. Furge K.A., Chen J., Koeman J., Swiatek P., Dykema K., Lucin K., et al. Detection of DNA copy number changes and oncogenic signalling abnormalities from gene expression data reveals MYC activation in high-grade papillary renal cell carcinoma. Cancer Research 2007, 67:3171-3176.
74. Youssef Y.M., White N.M., Grigull J., Krizova A., Samy C., Mejia-Guerrero S., et al. Accurate molecular classification of kidney cancer subtypes using microRNA signature. European Urology 2011, 59:721-730.
75. Nakada C., Tsukamoto Y., Matsuura K., Nguyen T.L., Hijiya N., Uchida T., et al. Overexpression of miR-210, a downstream target of HIF1α, causes centrosome amplification in renal carcinoma cells. Journal of Pathology 2011, 224:280-288.
76. Neal C.S., Michael M.Z., Rawlings L.H., Van der Hoek M.B., Gleadle J.M. The VHL-dependent regulation of microRNAs in renal cancer. BMC Medicine 2010, 8(October 21):64.
77. Kaku H., Ito S., Ebara S., Ouchida M., Nasu Y., Tsushima T., et al. Positive correlation between allelic loss at chromosome 14q24-31 and poor prognosis of patients with renal cell carcinoma. Urology 2004, 64:176-181.
78. Klatte T., Rao P.N., de Martino M., LaRochelle J., Shuch B., Zomorodian N., et al. Cytogenetic profile predicts prognosis of patients with clear cell renal cell carcinoma. Journal of Clinical Oncology 2009, 27:746-753.
79. Sanjmyatav J., Junker K., Matthes S., Muehr M., Sava D., Sternal M., et al. Identification of genomic alterations associated with metastasis and cancer specific survival in clear cell renal cell carcinoma. Journal of Urology 2011, 186:2078-2083.
80. Battagli C., Uzzo R.G., Dulaimi E., Ibanez de Caceres I., Krassenstein R., Al-Saleem T., et al. Promoter hypermethylation of tumor suppressor genes in urine from kidney cancer patients. Cancer Research 2003, 63:8695-8699.
81. Hoque M.O., Begum S., Topaloglu O., Jeronimo C., Mambo E., Westra W.H., et al. Quantitative detection of promoter hypermethylation of multiple genes in the tumor, urine, and serum DNA of patients with renal cancer. Cancer Research 2004, 64:5511-5517.
82. Urakami S., Shiina H., Enokida H., Hirata H., Kawamoto K., Kawakami T., et al. Wnt antagonist family genes as biomarkers for diagnosis, staging, and prognosis of renal cell carcinoma using tumor and serum DNA. Clinical Cancer Research 2006, 12:6989-6997.
83. Yao M., Yoshida M., Kishida T., et al. VHL tumor suppressor gene alterations associated with good prognosis in sporadic clear-cell renal carcinoma. Journal of the National Cancer Institute 2002, 94:1569-1575.
84. Schraml P., Struckmann K., Hatz F., Sonnet S., Kully C., Gasser T., et al. VHL mutations and their correlation with tumour cell proliferation, microvessel density, and patient prognosis in clear cell renal cell carcinoma. Journal of Pathology 2002 Feb, 196(2):186-193.
85. Kim J.H., Jung C.W., Cho Y.H., Lee J., Lee S.H., Kim H.Y., et al. Somatic VHL alteration and its impact on prognosis in patients with clear cell renal cell carcinoma. Oncology Reports 2005, 13:859-864.
86. Choueiri T.K., Vaziri S.A., Jaeger E., Elson P., Wood L., Bhalla I.P., et al. von Hippel-Lindau gene status and response to vascular endothelial growth factor targeted therapy for metastatic clear cell renal cell carcinoma. Journal of Urology 2008, 180:860-865.
87. Rechsteiner M.P., von Teichman A., Nowicka A., Sulser T., Schraml P., Moch H. VHL gene mutations and their effects on hypoxia inducible factor HIFα: identification of potential driver and passenger mutations. Cancer Research 2011, 71:5500-5511.
88. Stillebroer A.B., Mulders P.F., Boerman O.C., Oyen W.J., Oosterwijk E. Carbonic anhydrase IX in renal cell carcinoma: implications for prognosis, diagnosis, and therapy. European Urology 2010, 58:75-83.
89. Furge K.A., Tan M.H., Dykema K., Kort E., Stadler W., Yao X., et al. Identification of deregulated oncogenic pathways in renal cell carcinoma: an integrated oncogenomic approach based on gene expression profiling. Oncogene 2007, 26:1346-1350.
90. Latif F., Tory K., Gnarra J., Yao M., Duh F.M., Orcutt M.L., et al. Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 1993, 260:1317-1320.
91. Huang da W., Sherman B.T., Zheng X., Yang J., Imamichi T., Stephens R., Lempicki R.A. Extracting biological meaning from large gene lists with DAVID. Current Protocols in Bioinformatics 2009, [chapter 13: unit 13.11].
92. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 2009, 4:44-57.