c-Myc-dependent formation of Robertsonian translocation chromosomes in mouse cells

Neoplasia

Volumn 9, Issue 7, 2007, Pages 578-588

  Guffei, Amanda ^a   Lichtensztejn, Zelda ^a   Silva, Amanda Gonçalves Dos Santos ^a,b   Louis, Sherif F ^a   Caporali, Andrea ^a,c,d   Mai, Sabine ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF PARMA   (Italy)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

c Myc; Centromere; Genomic instability; Nuclear organization; Robertsonian chromosome

Indexed keywords

ANIMAL CELL; ARTICLE; CENTROMERE; INTERPHASE; LYMPHOCYTE; MOUSE; MOUSE STRAIN; NONHUMAN; ONCOGENE C MYC; PLASMACYTOMA; PRIORITY JOURNAL; ROBERTSONIAN CHROMOSOME TRANSLOCATION; TELOMERE;

EID: 34547219101     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.07355     Document Type: Article

References (55)

1. Nesbit CE, Tersak JM, and Prochownik EV (1999). MYC oncogenes and human neoplastic disease. Oncogene 18, 3004-3016 (Review).
2. Popescu NC and Zimonjic DB (2002). Chromosome-mediated alterations of the MYC gene in human cancer. J Cell Mol Med 6, 151-159 (Review).
3. Arvanitis C and Felsher DW (2006). Conditional transgenic models define how MYC initiates and maintains tumorigenesis. Semin Cancer Biol 16, 313-317 (Epub 2006 Jul 21).
4. Lutz W, Leon J, and Eilers M (2002). Contributions of Myc to tumorigenesis. Biochim Biophys Acta 1602, 61-71 (Review).
5. Kuttler F and Mai S (2006). c-Myc, genomic instability and disease. In Vol 1: Genome Dynamics. Genome and Disease. J-N Volff (Ed). Karger Publishers, Würzburg, Germany, pp. 171-191.
6. Vita M and Henriksson M (2006). The Myc oncoprotein as a therapeutic target for human cancer. Semin Cancer Biol 16, 318-330 (Review; Epub 2006 Aug 3).
7. Mai S and Mushinski JF (2003). c-Myc-induced genomic instability. J Environ Pathol Toxicol Oncol 22, 179-199 (Review).
8. Oster SK, Ho CS, Soucie EL, and Penn LZ (2002). The myc oncogene: MarvelouslY Complex. Adv Cancer Res 84, 81-154 (Review).
9. Frank SR, Parisi T, Taubert S, Fernandez P, Fuchs M, Chan HM, Livingston DM, and Amati B (2003). MYC recruits the TIP60 histone acetyltransferase complex to chromatin. EMBO Rep 4, 575-580.
10. Knoepfler PS, Zhang XY, Cheng PF, Gafken PR, McMahon SB, and Eisenman RN (2006). Myc influences global chromatin structure. EMBO J 25, 2723-2734 (Epub 2006 May 25).
11. 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.
12. Mai S and Garini Y (2005). Oncogenic remodeling of the three-dimensional organization of the interphase nucleus: c-Myc induces telomeric aggregates whose formation precedes chromosomal rearrangements. Cell Cycle 4, 1327-1331 (Epub 2005 Oct 5).
13. Mai S and Garini Y (2006). The significance of telomeric aggregates in the interphase nuclei of tumor cells. J Cell Biochem 97, 904-915 (Review).
14. 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.
15. Gropp A, Winking H, Redi C, Capanna E, Britton-Davidian J, and Noack G (1982). Robertsonian karyotype variation in wild house mice from Rhaeto-Lombardia. Cytogenet Cell Genet 34, 67-77.
16. Gazave E, Catalan J, Ramalhinho Mda G, Mathias Mda L, Nunes AC, Dumas D, Britton-Davidian J, and Auffray JC (2003). The non-random occurrence of Robertsonian fusion in the house mouse. Genet Res 81, 33-42.
17. Garagna S, Marziliano N, Zuccotti M, Searle JB, Capanna E, and Redi CA (2001). Pericentromeric organization at the fusion point of mouse Robertsonian translocation chromosomes. Proc Natl Acad Sci USA 98, 171-175.
18. Capanna E and Castiglia R (2004). Chromosomes and speciation in Mus musculus domesticus. Cytogenet Genome Res 105, 375-384.
19. Sarkar R, Guffei A, Vermolen BJ, Garini Y, and Mai S (2007). Alterations in centromere positions in immortalized and malignant mouse lymphocytes. Cytometry Part A 71 (6), 386-392.
20. Fest T, Mougey V, Dalstein V, Hagerty M, Milette D, Silva S, and Mai S (2002). c-MYC overexpression in Ba/F3 cells simultaneously elicits genomic instability and apoptosis. Oncogene 21, 2981-2990.
21. Fest T, Guffei A, Williams G, Silva S, and Mai S (2005). Uncoupling of genomic instability and tumorigenesis in a mouse model of Burkitt's lymphoma expressing a conditional box II-deleted Myc protein. Oncogene 24, 2944-2953.
22. Caporali A, Wark L, and Mai S (2007). Telomeric aggregates and end-to-end chromosomal fusions require my box II. Oncogene 26, 1398-1406 (Epub 2006 Sep 4).
23. Mai S, Hanley-Hyde J, Rainey GJ, Kuschak TI, Paul JT, Littlewood TD, Mischak H, Stevens LM, Henderson DW, and Mushinski JF (1999). Chromosomal and extrachromosomal instability of the cyclin D2 gene is induced by Myc overexpression. Neoplasia 1, 241-252.
24. Fukasawa K, Wiener F, Vande Woude GF, and Mai S (1997). Genomic instability and apoptosis are frequent in p53 deficient young mice. Oncogene 11, 1295-1302.
25. Kim SH, McQueen PG, Lichtman MK, Shevach EM, Parada LA, and Misteli T (2004). Spatial genome organization during T-cell differentiation. Cytogenet Genome Res 105, 292-301.
26. Mai S and Wiener F (2002). Murine FISH. In FISH: A Practical Approach. B Beatty, S Mai, and J Squire (Eds). Oxford University Press, Oxford. pp. 55-67.
27. 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.
28. Solovei I, Schermelleh L, During K, Engelhardt A, Stein S, Cremer C, and Cremer T (2004). Differences in centromere positioning of cycling and postmitotic human cell types. Chromosoma 112, 410-423.
29. Weierich C, Brero A, Stein S, von Hase J, Cremer C, Cremer T, and Solovei I (2003). Three-dimensional arrangements of centromeres and telomeres in nuclei of human and murine lymphocytes. Chromosome Res 11, 485-502.
30. Friebe B, Zhang P, Linc G, and Gill BS (2005). Robertsonian translocations in wheat arise by centric misdivision of univalents at anaphase I and rejoining of broken centromeres during interkinesis of meiosis II. Cytogenet Genome Res 109, 293-297.
31. Mastromonaco GF, Coppola G, Crawshaw G, DiBerardino D, and King WA (2004). Identification of the homologue of the bovine Rob(1;29) in a captive gaur (Bos gaurus). Chromosome Res 12, 725-731.
32. Nachman MW and Searle JB (1995). Why is the house mouse karyotype so variable? Trends Ecol Evol 10, 397-402.
33. Gold JR and Gall GA (1975). Chromosome cytology and polymorphism in the California High Sierra golden trout (Salmo aguabonita). Can J Genet Cytol 17, 41-53.
34. Welborn J (2004). Acquired Robertsonian translocations are not rare events in acute leukemia and lymphoma. Cancer Genet Cytogenet 151, 14-35.
35. Jacobs PA (1981). Mutation rates of structural chromosome rearrangements in man. Am J Hum Genet 33, 44-54.
36. Nielsen J and Wohlert M (1991). Chromosome abnormalities found among 34,910 newborn children: results from a 13-year incidence study in Århus, Denmark. Hum Genet 87, 81-83.
37. Kim SR and Shaffer LG (2002). Robertsonian translocations: mechanisms of formation, aneuploidy, and uniparental disomy and diagnostic considerations. Genet Test 6, 163-168.
38. 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 myelogeneous leukemia. Cancer Genet Cytogenet 132, 79-80.
39. Padilla-Nash HM, Heselmeyer-Haddad K, Wangsa D, Zhang H, Ghadimi BM, Macville M, Augustus M, Schrock 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.
40. 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, 19 and 20 in osteosarcomas. Genes Chromosomes Cancer 36, 7-16.
41. 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.
42. Haigis KM and Dove WF (2003). A Robertsonian translocation suppresses a somatic recombination pathway to loss of heterozygosity. Nat Genet 33, 33-39 (Epub 2002 Nov 25).
43. 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.
44. Silva S, Wiener F, Klein G, and Janz S (2005). Location of Myc, Igh, and Igk on Robertsonian fusion chromosomes is inconsequential for Myc translocations and plasmacytoma development in mice, but Rb(6.15)-carrying tumors prefer Igk-Myc inversions over translocations. Genes Chromosomes Cancer 42, 416-426.
45. Meaburn KJ, Misteli T, and Soutoglou E (2007). Spatial genome organization in the formation of chromosomal translocations. Semin Cancer Biol 17, 80-90 (Epub 2006 Oct 26).
46. Kalitsis P, Griffiths B, and Choo AKH (2006). Mouse telocentric sequences reveal a high rate of homogenization and possible role in Robertsonian translocation. Proc Natl Acad Sci USA 103, 8786-8791.
47. Hecht F, Morgan R, and Hecht BK (1988). Robertsonian chromosome recombinations are rare in cancer. Cancer Genet Cytogenet 35, 79-81.
48. Slijepcevic P (1998). Telomeres and mechanisms of Robertsonian fusions. Chromosoma 107, 136-140.
49. Mai S, Fluri M, Siwarski D, and Huppi K (1996). Genomic instability in MycER-activated Rat1A-MycER cells. Chromosome Res 4, 365-371.
50. Felsher DW and Bishop JM (1999). Transient excess of MYC activity can elicit genomic instability and tumorigenesis. Proc Natl Acad Sci USA 96, 3940-3944.
51. McCormack SJ, Weaver Z, Deming S, Natarajan G, Torri J, Johnson MD, Liyanage M, Ried T, and Dickson RB (1998). Myc/p53 interactions in transgenic mouse mammary development, tumorigenesis and chromosomal instability. Oncogene 16, 2755-2766.
52. Vafa O, Wade M, Kern S, Beeche M, Pandita TK, Hampton GM, and Wahl GM (2002). c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol Cell 9, 1031-1044.
53. Karlsson A, Deb-Basu D, Cherry A, Turner S, Ford J, and Felsher DW (2003). Defective double-strand DNA break repair and chromosomal translocations by MYC overexpression. Proc Natl Acad Sci USA 100, 9974-9979 (Epub 2003 Aug 8).
54. Ray S, Atkuri KR, Deb-Basu D, Adler AS, Chang HY, Herzenberg LA, and Felsher DW (2006). MYC can induce DNA breaks in vivo and in vitro independent of reactive oxygen species. Cancer Res 66, 6598-6605.
55. Hande P, Slijepcevic P, Silver A, Bouffler S, van Buul P, Bryant P, and Lansdorp P (1999). Elongated telomeres in scid mice. Genomics 56, 221-223.