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

Volumn 22, Issue 3, 1998, Pages 200-209

  Clifford, Steven C ^a,b   Prowse, Amanda H ^b,d   Affara, Nabeel A ^b   Buys, Charles H C M ^c   Maher, Eamonn R ^a,b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

^d FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ARTICLE; CHROMOSOME BREAKAGE; CHROMOSOME INACTIVATION; CHROMOSOME LOSS; CLEAR CELL CARCINOMA; GENE DELETION; GENE FREQUENCY; GENE MUTATION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; KIDNEY CARCINOMA; METHYLATION; PATHOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; VON HIPPEL LINDAU DISEASE;

EID: 0031776704     PISSN: 10452257     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1098-2264(199807)22:3<200::aid-gcc5>3.0.co;2-%23     Document Type: Article

References (47)

1. Cairns P, Tokino K, Eby Y, Sidransky D (1995) Localization of tumor-suppressor loci on chromosome-9 in primary human renal-cell carcinomas. Cancer Res 55:224-227.
2. Catchpoole D, Lam WWK, Valler D, Temple IK, Joyce JA, Reik W, Schofield PN, Maher ER (1997) Epigenetic modification and hypermethylation at H19 locus in Beckvvith-Wiedemann syndrome. J Med Genet 34:353-359.
3. Chen F, Kishida T, Duh FM, Renbaum P, Orcutt ML, Schmidt L, Zhar B (1995) Suppression of growth of renal carcinoma cells by the von Hippel-Lindau tumor suppressor gene. Cancer Res 55:4804-4807.
4. Crossey PA, Richards FM, Foster K, Green JS, Prowse A, Latif F, Lerman MI, Zbar B, Affara NA, Ferguson-Smith MA, Maher ER (1994) Identification of intragenic mutations in the von Hippel-Lindau disease tumour suppressor gene and correlation with disease phenotype. Hum Mol Genet 3:1303-1308
5. Druck T, Kastury K, Hadaczek P, Podolski J, Toloczko A, Sikorski A, Ohta M, laforgia S, Lasota J, McCue P, Lubinski J, Huebner K (1995) Loss of heterozygosity at the familial t(3-8) locus in most clear cell renal carcinomas. Cancer Res 55:5348-53.
6. Ferguson-Smith AC, Sasaki H, Cattanach BM, Surani A (1994) A parental-origin-specific epigenetic modification of the mouse H19 gene. Nature 362:751-755.
7. Foster K, Prowse A, van den Berg A, Fleming S, Hulsbeek MMF, Crossey PA, Richards FM, Cairns P, Affara NA, Ferguson-Smith MA, Buys CHCM, Maher ER (1994a) Somatic mutations of the von Hippel-Lindau disease tumour suppressor gene in nonfamilial clear cell renal carcinoma. Hum Mol Genet 3:2169-2173.
8. Foster K, Crossey PA, Cairns P, Hetherington JW, Richards FM, Jones MH, Bentley K, Affara NA, Ferguson-Smith MA, Maher ER (1994b) Molecular genetic investigation of sporadic renal cell carcinoma: Analysis of allele loss on chromosomes 3p, 5q, 11p, 17 and 22. Br J Cancer 69:230-234.
9. Ganly PS, Rabbitts PH (1991) Polymerase chain reaction (PCR) for detection of HindIII polymorphism at the D3F15S2 locus. Nucleic Acids Res 19:3758.
10. Gnarra JR, Tory K, Weng Y, Schmidt L, Wei MH, Li H, Latif F, Liu S, Chen F, Duh FM, Lubensky I, Duan DR, Florence C, Pozattti R, Walther MM, Bander NH, Grossman HB, Brauch H, Pomer S, Brooks JD, Isaacs WB, Lerman MI, Zbar B, Linehan WM (1994) Mutations of the VHL tumor suppressor gene in renal carcinoma. Nature Genet 7:85-90.
11. Hadaczek P, Podolski J, Toloczko A, Kurzawski G, Sikorski A, Rabbits P, Huebner K, Lubinski J (1996) Losses at 3p common deletion sites in subtypes of kidney tumours - Histopathological correlations. Virchows Archiv 429:37-42.
12. Herman JG, Latif K, Weng YK, Lerman MI, Zbar B, Liu S, Samid D, Duan DSR, Gnarra JR, Linehan WM, Baylin SB (1994) Silencing of the VHL tumor suppressor gene by DNA methylation in renal carcinomas. Proc Natl Acad Sci USA 91:9700-9704.
13. Iliopoulos O, Kibel A, Gray S, Kaelin WG Jr (1995) Tumour suppression by the human von Hippel-Lindau gene product. Nature Med 1:822-882.
14. Kamb A, Gruis NA, Weaverfeldhaus J, Liu QY, Harshman K, Tavtigian SV, Stockert E, Day RS, Johnson BE, Skolnick MH (1994) A cell-cycle regulator potentially involved in genesis of many tumor types. Science 264:436-440.
15. Killary AM, Wolf ME, Giambernardi TA, Naylor SL (1992) Definition of a tumor suppressor locus within human chromosome-3p21-p22. Proc Natl Acad Sci USA 89:10877-10881.
16. Kok K, Osinga J, Carnt B, Davis MB, Vanderhout AH, Vanderveen AY, Landsvater RM, Deleij LFMH, Berendsen HH, Postmus PE, Poppema S, Buys CHCM (1987) Deletion of a DNA sequence at the chromosomal region 3p21 in all major types of lung cancer. Nature 330:578-581.
17. Kok K, van den Berg A, Veldhuis PMFJ, van der Veen AY, Kranke M, Schoenmakers EFPM, Hulsbeek MMF, van der Hout AH, de Leij L, van der Veen W, Buys CHCM (1994) A homozygous deletion in a small cell lung cancer cell line involving a 3p21 region with a marked instability in YACs. Cancer Res 54:4183-7.
18. Kok K, van den Berg A, Veldhuis PMJF, Franke M, Buys CHCM (1945) The genomic structure of the UBE1L gene. Gene Express 4:163-175.
19. Kok K, Naylor SL, Buys CHCM (1997) Deletions of the the short arm of chromosome 3 in solid tumours and the search for suppressor genes. Adv Cancer Res 71:27-92.
20. Kondo M, Suzuki H, Ueda R, Osada H, Takagi K, Takahashi T, Takahashi T (1995) Frequent loss of imprinting of the H19 gene is often associated with its overexpression in human lung cancers. Oncogene 10:1193-1198.
21. Kovacs G, Frisch S (1989) Clonal chromosome-abnormalities in tumor-cells from patients with sporadic renal-cell carcinomas. Cancer Res 49:651-659.
22. Laird PW, Jaenisch R (1994) DNA methylation and cancer. Hum Mol Genet 3:1487-1495.
23. Latif F, Tory K, Gnarra J, Yao M, Duh FM, Orcutt ML, Stackhouse T, Kuzmin I, Modi W, Geil L, Schmidt L, Zhou FW, Li H, Wei MH, Chen F, Glenn G, Choyke P, Walther MM, Weng YK, Duan DSR, Dean M, Glavac D, Richards FM, Crossey PA, Ferguson-Smith MA, Lepaslier D, Chumakov I, Cohen D, Chinault AC, Maher ER, Linehan WM, Zbar B, Lerman MI (1993) Isolation of the von Hippel-Lindau disease tumour suppressor gene. Science 260:1317-1320.
24. Lubinski J, Hadaczek P, Podolski J, Toloczko A, Sikorski A, McCue P, Druck T, Huebner K (1994) Common regions of deletion in chromosome regions 3p12 and 3p14.2 in primary clear-cell renal carcinomas. Cancer Res 54:3710-3713.
25. Merlo A, Herman JG, Mao L, Lee DJ, Gabrielson E, Burger PC, Baylin SB, Sidransky D (1995) 5′ CpG island methylation is associated with transcriptional silencing of the tumor-suppressor p16/cdkn2/mts1 in human cancers. Nature Med 1:686-692.
26. Morita R, Ishikawa J, Tsutsumi M, Hikiji K, Tsukada Y, Kamidono S, Maeda S, Nakamura Y (1991) Allelotype of renal-cell carcinoma. Cancer Res 51:820-823.
27. Moulton T, Crenshaw T, Hao Y, Moosikasuwan J, Lin N, Dembitzer F, Hensle T, Weiss L, McMorrow L, Loew T, Kraus W, Gerald W, Tycko B (1994) Epigenetic lesions at the H19 locus in Wilms' tumour patients. Nature Genet 7:440-447.
28. Ohta M, Inoue H, Cotticelli MG, Kastury K, Baffa R, Palazzo J, Siprashvili Z, Mori M, Mccue P, Druck T, Croce CM, Huebner K (1996) The FHIT gene spanning the chromosome 3p14 2 fragile site and renal carcinoma-associated t(3;8) breakpoint is abnormal in digestive tract cancers. Cell 84:587-597.
29. Presti JC, Rao PH, Chen Q, Reuter VE, Li FP, Fair WR, Jhanwar SC (1991) Histopathological cytogenetic and molecular characterization of renal cortical tumors. Cancer Res 51:1544-1552.
30. Prowse AH, Webster AR, Richards FM, Richard S, Olschwang S, Resche F, Affara NA, Maher ER (1997) Somatic inactivation of the VHL gene in von Hippel-Lindau disease tumors. Am J Hum Genet 60:765-771
31. Reik W, Bron K, Schneid H, Le Bouc Y, Bickmore W, Maher ER (1995) Imprinting mutations in the Beckwith-Wiedemann syndrome suggested by an altered imprinting pattern in the IGF2-H19 domain. Hum Mol Genet 4:2379-2385.
32. Roche J, Whisenat E, Boldog F, Loeb D, Vance JM, Drabkin H (1994) Dinucleotidc repeats flanking the renal carcinoma break-point at 3p14. 2. Hum Mol Genet 3:215.
33. Sanchez Y, Elnaggar A, Pathak S, Killary AM (1993) A tumor-suppressor locus within 3p14-p12 mediates rapid cell-death of renal-cell carcinoma in-vivo. Proc Natl Acad Sci USA 91:3383-3387.
34. Schmidt L, Duh FM, Chen F, Kishida T, Glenn G, Choyke P, Scherer SW, Zhuang Z, Lubensky I, Dean M, Allikmets R, Chidambaram A, Bergerheim UR, Feltis JT, Casadevall C, Zamarron A, Richard S, Lips CJM, McCellan MW, Lap-Chee T, Geil L, Orcutt ML, Stackhouse T, Lipan J, Slife L, Branch H, Decker J, Niehans G, Hughson MD, Moch H, Lerman MI, Linehan WM, Zbar B (1997) Germline and somatic mutations in the tyrosine kinase domain of the MRT proto-oncogene in papillary renal carcinomas. Nature Genet 16:68-73.
35. Seizinger BR, Klinger HP, Junien C, Nakamura Y, le Beau M, Cavanee W, Emanuel B, Ponder B, Naylor S, Mitelman F, Louis D, Menon A, Newsham I, Decker J, Kaelbling M, Henry I, Deimling AN (1991) Report of the committee on chromosome and gene loss in human neoplasia. Cytogenet Cell Genet 58:1080-1096.
36. Shimizu M, Yokota J, Mori N, Shuin T, Shinoda M, Terada M, Oshimura M (1990) Introduction of normal chromosome-3p modulates the tumorigenicity of a human renal cell carcinoma cell-line YCR. Oncogene 5:185-194.
37. Shuin T, Kondo K, Torigoe S, Kishida T, Kubota Y, Hosaka M, Nagashima Y, Kitamura H, Latif F, Zbar B, Lerman MI, Yao M (1994) Frequent somatic mutations and loss of heterozygosity of the von Hippel-Lindau tumor suppressor gene in primary human renal cell carcinomas. Cancer Res 54:2852-2855.
38. Steenman MJC, Rainier S, Dobry CJ, Grundy P, Horon I, Feinberg AP (1994) Loss of imprinting of IGF2 is linked to reduced expression and abnormal methylation of H19 in Wilms tumour. Nature Genet 7:433-9.
39. Thoenes W, Storkel S. Rumpelt HJ (1986) Histopathology and classification of renal cell tumors (adenomas oncocytomas and carcinomas). The basic cytological and histopathological elements and their use for diagnostics. Path Res Pract 181:125-143.
40. Thrash-Bingham CA, Greenberg RE, Howard S, Bruzel A, Bremer M, Goll A, Salazar H, Freed JJ, Tartof KD (1995) Comprehensive allelotyping of human renal-cell carcinomas using microsatellite DNA probes. Proc Natl Acad Sci USA 92:2854-2858.
41. van den Berg A, Buys CHCM (1997) Involvement of multiple loci on chromosome 3 in renal cell cancer development. Genes Chromosomes Cancer 17:1-18.
42. van den Berg A, Hulsbeek MMF, Dejong D, Kok K, Veldhuis PMJF, Roche J, Buys CHCM (1996) Major role for a 3p21 region and lack of involvement of the t(3-8) breakpoint region in the development of renal-cell carcinoma suggested by loss of heterozygosity analysis. Genes Chromosomes Cancer 15:64-72.
43. van den Berg A, Dijkhuizen T, Draaijers TC, Hulsheek MMF, Maher ER, van den Berg E, Storkel S, Buys CHCM (1997) Analysis of multiple renal cell adenomas and carcinomas suggests allelic loss at3p21 to be a prerequisite for malignant development. Genes Chromosomes Cancer 19:228-232.
44. van der Hout AH, Van den Berg E, Van der Vlies P, Dijkhuizen T, Oosterhuis JW, De Jong B, Buys CHCM (1993) Loss of heterozygosity at the short arm of chromosome 3 in renal cell cancer correlates with cytological tumour type. Int J Cancer 53:353-357.
45. Weissenbach J, Gyapay G, Dib C, Vignal A, Mirissette J, Millaseau P, Vayssieix G, Lathrop M (1992) A second generation linkage map of the human genome. Nature 359:794-801.
46. Wilhelm M, Bugert P, Kenck C, Staehler G, Kovacs G (1995) Terminal deletion of chromosome 3p sequences in nonpapillary renal cell carcinomas: A breakpoint cluster between loci D3S1285 and D3S1603. Cancer Res 55:5383-5385.
47. Zbar B, Brauch H, Talmadge C, Linehan M (1987) Loss of alleles of loci on the short arm of chromosome-3 in renal-cell carcinoma. Nature 327:721-724.