Telomere-centromere-driven genomic instability contributes to karyotype evolution in a mouse model of melanoma

Neoplasia

Volumn 12, Issue 1, 2010, Pages 11-19

  Gonçalves Dos Santos Silva, Amanda ^a   Graves, Herbert Alexander ^b   Guffei, Amanda ^b   Ricca, Tatiana Iervolino ^a   Mortara, Renato Arruda ^a   Jasiulionis, Miriam Galvonas ^a   Mai, Sabine ^b  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENICITY; CELL ADHESION; CELL AGGREGATION; CELL TRANSFORMATION; CENTROMERE; CHROMOSOME ABERRATION; CONTROLLED STUDY; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENOMIC INSTABILITY; IN VITRO STUDY; KARYOTYPE EVOLUTION; MALIGNANT TRANSFORMATION; MELANOCYTE; MELANOMA; MELANOMA CELL; METAPHASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; ROBERTSONIAN CHROMOSOME TRANSLOCATION; TELOMERE; UTERINE CERVIX CARCINOMA IN SITU;

EID: 73949133378     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.91004     Document Type: Article

References (67)

1. Hussein MR (2004). Genetic pathways to melanoma tumorigenesis. J Clin Pathol 57, 797-801.
2. Lengauer C, Kinzler KW, and Vogelstein B (1998). Genetic instabilities in human cancers. Nature 396, 643-649.
3. Hussein MR, Sun M, Roggero E, Sudilovsky EC, Tuthill RJ, Wood GS, and Sudilovsky O (2002). Loss of heterozygosity, microsatellite instability, and mismatch repair protein alterations in the radial growth phase of cutaneous malignant melanomas. Mol Carcinog 34, 35-44.
4. Albertson DG, Collins C, McCormick F, and Gray JW (2003). Chromosome aberrations in solid tumors. Nat Genet 34, 369-376.
5. Gebhart E and Liehr T (2000). Patterns of genomic imbalances in human solid tumors. Int J Oncol 16, 383-399.
6. Bayani J, Selvarajah S, Maire G, Vukovic B, Al-Romaih K, Zielenska M, and Squire JA (2007). Genomic mechanisms and measurement of structural and numerical instability in cancer cells. Semin Cancer Biol 17, 5-18.
7. Yuen KW, Montpetit B, and Hieter P (2005). The kinetochore and cancer: what's the connection? Curr Opin Cell Biol 17, 576-582.
8. Storchova Z and Pellman D (2004). From polyploidy to aneuploidy, genome instability and cancer. Nat Rev Mol Cell Biol 5, 45-54.
9. Henikoff S, Ahmad K, and Malik HS (2001). The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293, 1098-1102.
10. Shaw CJ and Lupski JR (2004). Implications of human genome architecture for rearrangement-based disorders: the genomic basis of disease. Hum Mol Genet 1, R57-R64.
11. Gonçalves Dos Santos Silva A, Sarkar R, Harizanova J, Guffei A, Mowat M, Garini Y, and Mai S (2008). Centromeres in cell division, evolution, nuclear organization and disease. J Cell Biochem 104, 2040-2058.
12. Yue Y, Grossmann B, Ferguson-Smith M, Yang F, and Haaf T (2005). Comparative cytogenetics of human chromosome 3q21.3 reveals a hot spot for ectopic recombination in hominoid evolution. Genomics 85, 36-47.
13. Jamet D, Marzin Y, Douet-Guilbert N, Morel F, Le Bris MJ, Herry A, Banzakour S, Bourquard P, Morice P, Abgrall JF, et al. (2005). Jumping translocations in multiple myeloma. Cancer Genet Cytogenet 161, 159-163.
14. Chantot-Bastaraud S, Ravel C, Berthaut I, McElreavey K, Bouchard P, Mandelbaum J, and Siffroi JP (2007). Sperm-FISH analysis in a pericentric chromosome 1 inversion, 46,XY,inv(1)(p22q42), associated with infertility. Mol Hum Reprod 13, 55-59.
15. Collodel G, Moretti E, Capitani S, Piomboni P, Anichini C, Estenoz M, and Baccetti B (2006). TEM, FISH and molecular studies in infertile men with pericentric inversion of chromosome 9. Andrologia 38, 122-127.
16. Anton E, Blanco J, Egozcue J, and Vidal F (2005). Sperm studies in heterozygote inversion carriers: a review. Cytogenet Genome Res 111, 297-304.
17. Anelli L, Albano F, Zagaria A, Liso A, Cuneo A, Mancini M, Liso V, Rocchi M, and Specchia G (2004). Pericentric chromosome 8 inversion associated with the 5′RUNX1/3′CBFA2T1 gene in acute myeloid leukemia cases. Ann Hematol 84, 245-249.
18. Pedrazzini E, Cerretini R, Noriega MF, Narbaitz M, Palacios MF, Negri P, Bengió R, and Slavutsky I (2006). Inversions of chromosomes 2 and 6 in mantle cell lymphoma. Cytogenetic, FISH, and molecular studies. Cancer Genet Cytogenet 167, 164-167.
19. Mathew S, Dalton J, Riedley S, Spunt SL, and Hill DA (2002). Complex t(X;18)(p11.2;q11.2) with a pericentric inversion of the X chromosome in an adolescent boy with synovial sarcoma. Cancer Genet Cytogenet 132, 136-140.
20. Ulucan H, Akin R, Kösem M, and Gül D (2006). De novo pericentric inversion of chromosome 5 in a girl with mental retardation and unilateral ear malformation. Am J Med Genet A 140, 298-299.
21. Ramadevi AR, Naik U, Dutta U, Srikanth, and Prabhakara K (2002). De novo pericentric inversion of chromosome 4, inv(4)(p16q12) in a boy with piebaldism and mental retardation. Am J Med Genet 113, 190-192.
22. Bailey S and Murnane JP (2006). Telomeres, chromosome instability and cancer. Nucl Acid Res 34, 2408-2417.
23. Desmaze C, Soria JC, Freulet-Marriere MA, Mathieu N, and Sabatier L (2003). Telomere-driven genomic instability in cancer cells. Cancer Lett 194, 173-182.
24. Riha K, Heacock ML, and Shippen DE (2006). The role of the nonhomologous end-joining DNA double-strand break repair pathway in telomere biology. Annu Rev Genet 40, 237-277.
25. Louis SF, Vermolen BJ, Garini Y, Young IT, Guffei A, Lichtensztejn Z, Kuttler F, Chuang TC, Moshir S, Mougey V, et al. (2005). c-Myc induces chromosomal rearrangements through telomere and chromosome remodeling in the interphase nucleus. Proc Natl Acad Sci USA 102, 9613-9618.
26. Mai S and Garini Y (2005). Oncogenic remodeling of the threedimensional organization of the interphase nucleus: c-Myc induces telomeric aggregates whose formation precedes chromosomal rearrangements. Cell Cycle 4, 1327-1331.
27. Caporali A, Wark L, Vermolen BJ, Garini Y, and Mai S (2007). Telomeric aggregates and end-to-end chromosomal fusions require myc box II. Oncogene 26, 1398-1406.
28. Guffei A, Lichtensztejn Z, Gonçalves Dos Santos Silva A, Louis SF, Caporali A, and Mai S (2007). c-Myc-dependent formation of Robertsonian translocation chromosomes in mouse cells. Neoplasia 9, 578-588.
29. Foijer F, Draviam VM, and Sorger PK (2008). Studying chromosomal instability in the mouse. Biochim Biophys Acta 1786, 73-82.
30. Wu X and Pandolfi PP (2001). Mouse models for multistep tumorigenesis. Trends Cell Biol 11, S2-S9.
31. Oba-Shinjo SM, Correa M, Ricca TI, Molognoni F, Pinhal MA, Neves IA, Marie SK, Sampaio LO, Nader HB, Chammas R, et al. (2006). Melanocyte transformation associated with substrate adhesion impediment. Neoplasia 8, 231-241.
32. Bennett DC, Cooper PJ, and Hart IR (1987). A line of non-tumorigenic mouse melanocytes, syngeneic with the B16 melanoma and requiring a tumour promoter for growth. Int J Cancer 39, 414-418.
33. Mai S and Wiener F (2002). Murine FISH. FISH: A Practical Approach. B Beatty, S Mai, and J Squire (Eds.). Oxford, UK: Oxford University Press, pp. 55-67.
34. Garagna S, Zuccotti M, Thornhill A, Fernandez-Donoso R, Berrios S, Capanna E, and Redi CA (2001). Alteration of nuclear architecture in male germ cells of chromosomally derived subfertile mice. J Cell Sci 114, 4429-4434.
35. Schaefer LH, Schuster D, and Herz H (2001). Generalized approach for accelerated maximum likelihood based image restoration applied to three-dimensional fluorescence microscopy. J Microsc 204, 99-107.
36. Chuang TC, Moshir S, Garini Y, Chuang AY, Young IT, Vermolen B, van den Doel R, Mougey V, Perrin M, Braun M, et al. (2004). The three-dimensional organization of telomeres in the nucleus of mammalian cells. BMC Biol 3, 2-12.
37. Vermolen BJ, Garini Y, Mai S, Mougey V, Fest T, Chuang TC, Chuang AY, Wark L, and Young IT (2005). Characterizing the three-dimensional organization of telomeres. Cytometry A 67, 144-150.
38. Cleveland DW, Mao Y, and Sullivan KF (2003). Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112, 407-421.
39. Dalla Torre CA, Maciel RM, Pinheiro NA, Andrade JA, De Toledo SR, Villa LL, and Cerutti JM (2002). TRAP-silver staining, a highly sensitive assay for measuring telomerase activity in tumor tissue and cell lines. Braz J Med Biol Res 35, 65-68.
40. Correa M, Machado J Jr, Carneiro CR, Pesquero JB, Bader M, Travassos LR, Chammas R, and Jasiulionis MG (2005). Transient inflammatory response induced by apoptotic cells is an important mediator of melanoma cell engraftment and growth. Int J Cancer 114, 356-363.
41. Kanaya T, Kyo S, Takakura M, Ito H, Namiki M, and Inoue M (1998). hTERT is a critical determinant of telomerase activity in renal-cell carcinoma. Int J Cancer 78, 539-543.
42. Kolquist KA, Ellisen LW, Counter CM, Meyerson M, Tan LK, Weinberg RA, Haber DA, and Gerald WL (1998). Expression of TERT in early permalignant lesions and a subset of cells in normal tissues. Nat Genet 19, 182-186.
43. Soler D, Genescà A, Arnedo G, Egozcue J, and Tusell L (2005). Telomere dysfunction drives chromosomal instability in human mammary epithelial cells. Genes Chromosomes Cancer 44, 339-350.
44. Artandi SE, Chang S, Lee SL, Alson S, Gottlieb GJ, Chin L, and DePinho RA (2000). Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 406, 641-645.
45. Londoño-Vallejo JA (2008). Telomere instability and cancer. Biochimie 90, 73-82.
46. Raynaud CM, Sabatier L, Philipot O, Olaussen KA, and Soria JC (2008). Telomere length, telomeric proteins and genomic instability during the multistep carcinogenic process. Crit Rev Oncol Hematol 66, 99-117.
47. Meeker AK and Argani P (2004). Telomere shortening occurs early during breast tumorigenesis: a cause of chromosome destabilization underlying malignant transformation? J Mammary Gland Biol Neoplasia 9, 285-296.
48. vanHeek NT, Meeker AK, Kern SE, Yeo CJ, Lillemoe KD, Cameron JL, Offerhaus GJ, Hicks JL, Wilentz RE, Goggins MG, et al. (2002). Telomere shortening is nearly universal in pancreatic intraepithelial neoplasia. Am J Pathol 161, 1541-1547.
49. Joshua AM, Evans A, Van der Kwast T, Zielenska M, Meeker AK, Chinnaiyan A, and Squire JA (2008). Prostatic preneoplasia and beyond. Biochim Biophys Acta 1785, 156-181.
50. Vukovic B, Beheshti B, Park P, Lim G, Bayani J, Zielenska M, and Squire JA (2007). Correlating breakage-fusion-bridge events with the overall chromosomal instability and in vitro karyotype evolution in prostate cancer. Cytogenet Genome Res 116, 1-11.
51. Meeker AK, Hicks JL, Platz EA, March GE, Bennett CJ, Delannoy MJ, and De Marzo AM (2002). Telomere shortening is an early somatic DNA alteration in human prostate tumorigenesis. Cancer Res 62, 6405-6409.
52. Meeker AK, Hicks JL, Iacobuzio-Donahue CA, Montgomery EA, Westra WH, Chan TY, Ronnett BM, and De Marzo AM (2004). Telomere length abnormalities occur early in the initiation of epithelial carcinogenesis. Clin Cancer Res 10, 3317-3326.
53. Lantuejoul S, Soria JC, Morat L, Lorimier P, Moro-Sibilot D, Sabatier L, Brambilla C, and Brambilla E (2005). Telomere shortening and telomerase reverse transcriptase expression in preinvasive bronchial lesions. Clin Cancer Res 11, 2074-2082.
54. Gulmann C, Lantuejoul S, Grace A, Leader M, Patchett S, and Kay E (2005). Telomerase activity in proximal and distal gastric neoplastic and preneoplastic lesions using immunohistochemical detection of hTERT. Dig Liver Dis 37, 439-445.
55. Lancelin F, Anidjar M, Villette JM, Soliman A, Teillac P, Le Duc A, Fiet J, and Cussenot O (2000). Telomerase activity as a potential marker in preneoplastic bladder lesions. BJU Int 85, 526-531.
56. Chin K, de Solorzano CO, Knowles D, Jones A, Chou W, Rodriguez EG, Kuo WL, Ljung BM, Chew K, Myambo K, et al. (2004). In situ analysis of genome instability in breast cancer. Nat Genet 16, 984-988.
57. Kim M, Xu L, and Blackburn EH (2003). Catalytically active human telomerase mutants with allele-specific biological properties. Exp Cell Res 288, 277-287.
58. Zhu J, Wang H, Bishop JM, and Blackburn EH (1999). Telomerase extends the lifespan of virus-transformed human cells without net telomere lengthening. Proc Natl Acad Sci USA 96, 3723-3728.
59. Xu L and Blackburn EH (2007). Human cancer cells harbor T-stumps, a distinct class of extremely short telomeres. Mol Cell 28, 315-327.
60. Kim SR and Shaffer LG (2002). Robertsonian translocations: mechanisms of formation, aneuploidy, and uniparental disomy and diagnostic considerations. Genet Test 6, 163-168.
61. Nielsen J and Wohlert M (1991). Chromosome abnormalities found among 34,910 newborn children: results from a 13-year incidence study in Arhus, Denmark. Hum Genet 87, 81-83.
62. Jacobs PA (1981). Mutation rates of structural chromosome rearrangements in man. Am J Hum Genet 33, 44-54.
63. Welborn J (2004). Acquired Robertsonian translocations are not rare events in acute leukemia and lymphoma. Cancer Genet Cytogenet 151, 14-35.
64. Qian J, Xue Y, Sun J, Guo Y, Pan J, Wu Y, Wang W, and Yao L (2002). Constitutional Robertsonian translocations in (9;22)-positive chronic myelogenous leukemia. Cancer Genet Cytogenet 132, 79-80.
65. Bayani J, Zielenska M, Pandita A, Al-Romaih K, Karaskova J, Harrison K, Bridge JA, Sorensen P, Thorner P, and Squire JA (2003). Spectral karyotyping identifies recurrent complex rearrangements of chromosomes 8, 17, and 20 in osteosarcomas. Genes Chromosomes Cancer 36, 7-16.
66. Padilla-Nash HM, Heselmeyer-Haddad K, Wangsa D, Zhang H, Ghadimi BM, Macville M, Augustus M, Schröck E, Hilgenfeld E, and Ried T (2001). Jumping translocations are common in solid tumor cell lines and result in recurrent fusions of whole chromosome arms. Genes Chromosomes Cancer 30, 349-363.
67. Shimokawa T, Sakai M, Kojima Y, and Takeyama H (2004). Acute myelogeneous leukemia (M5a) that demonstrated chromosomal abnormality of Robertsonian 13;21 translocation at onset. Intern Med 43, 508-511.