Shattered and stitched chromosomes-chromothripsis and chromoanasynthesis-manifestations of a new chromosome crisis?

Genes Chromosomes and Cancer

Volumn 51, Issue 11, 2012, Pages 975-981

  Righolt, Christiaan ^a,b   Mai, Sabine ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BONE CANCER; CANCER GENETICS; CHROMOANASYNTHESIS; CHROMOSOME ANALYSIS; CHROMOSOME DISORDER; CHROMOSOME REARRANGEMENT; CHROMOTHRIPSIS; HUMAN; MONTE CARLO METHOD; PRIORITY JOURNAL;

CELL LINE, TUMOR; CHROMOSOME BREAKAGE; GENE REARRANGEMENT; GENOME, HUMAN; HUMANS; MODELS, GENETIC; MONTE CARLO METHOD; NEOPLASMS; TERMINOLOGY AS TOPIC;

EID: 84865995513     PISSN: 10452257     EISSN: 10982264     Source Type: Journal    
DOI: 10.1002/gcc.21981     Document Type: Article

References (59)

1. Akavia UD, Litvin O, Kim J, Sanchez-Garcia F, Kotliar D, Causton HC, Pochanard P, Mozes E, Garraway LA, Pe'er D. 2010. An integrated approach to uncover drivers of cancer. Cell 143: 1005-1017.
2. Berger MF, Lawrence MS, Demichelis F, Drier Y, Cibulskis K, Sivachenko AY, Sboner A, Esgueva R, Pflueger D, Sougnez C, Onofrio R, Carter SL, Park K, Habegger L, Ambrogio L, Fennell T, Parkin M, Saksena G, Voet D, Ramos AH, Pugh TJ, Wilkinson J, Fisher S, Winckler W, Mahan S, Ardlie K, Baldwin J, Simons JW, Kitabayashi N, MacDonald TY, Kantoff PW, Chin L, Gabriel SB, Gerstein MB, Golub TR, Meyerson M, Tewari A, Lander ES, Getz G, Rubin MA, Garraway LA. 2011. The genomic complexity of primary human prostate cancer. Nature 470: 214-220.
3. Bickmore WA, Teague P. 2002. Influences of chromosome size, gene density and nuclear position on the frequency of constitutional translocations in the human population. Chromosome Res 10: 707-715.
4. Boveri T. 1914. Zur Frage der Entstehung maligner Tumoren. Jena: Fischer.
5. Boveri T. 1929. The Origin of Malignant Tumors. Translated by Marcella Boveri. Baltimore: The Williams & Wilkens Company.
6. Carvalho CM, Ramocki MB, Pehlivan D, Franco LM, Gonzaga-Jauregui C, Fang P, McCall A, Pivnick EK, Hines-Dowell S, Seaver LH, Friehling L, Lee S, Smith R, Del Gaudio D, Withers M, Liu P, Cheung SW, Belmont JW, Zoghbi HY, Hastings PJ, Lupski JR. 2011. Inverted genomic segments and complex triplication rearrangements are mediated by inverted repeats in the human genome. Nat Genet 43: 1074-1081.
7. Chen JM, Férec C, Cooper DN. 2012. Transient hypermutability, chromothripsis and replication-based mechanisms in the generation of concurrent clustered mutations. Mutat Res 750:52-79.
8. Chiang C, Jacobsen JC, Ernst C, Hanscom C, Heilbut A, Blumenthal I, Mills RE, Kirby A, Lindgren AM, Rudiger SR, McLaughlan CJ, Bawden CS, Reid SJ, Faull RL, Snell RG, Hall IM, Shen Y, Ohsumi TK, Borowsky ML, Daly MJ, Lee C, Morton CC, MacDonald ME, Gusella JF, Talkowski ME. 2012. Complex reorganization and predominant non-homologous repair following chromosomal breakage in karyotypically balanced germline rearrangements and transgenic integration. Nat Genet 44: 390-397, S1.
9. Cho KR, Vogelstein B. 1992. Genetic alterations in the adenoma-Carcinoma sequence. Cancer 70(6 Suppl): 1727-1731.
10. Crasta K, Ganem NJ, Dagher R, Lantermann AB, Ivanova EV, Pan Y, Nezi L, Protopopov A, Chowdhury D, Pellman D. 2012. DNA breaks and chromosome pulverization from errors in mitosis. Nature 482: 53-58.
11. Cremer T, Cremer C. 2001. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2: 292-301.
12. Cremer T, Cremer M. 2010. Chromosome territories. Cold Spring Harb Perspect Biol 2: a003889.
13. Darai-Ramqvist E, Diaz de Ståhl T, Sandlund A, Mantripragada K, Klein G, Dumanski J, Imreh S, Kost-Alimova M. 2006. Array-CGH and multipoint FISH to decode complex chromosomal rearrangements. BMC Genomics 7: 330.
14. Darai-Ramqvist E, Sandlund A, Müller S, Klein G, Imreh S, Kost-Alimova M. 2008. Segmental duplications and evolutionary plasticity at tumor chromosome break-prone regions. Genome Res 18: 370-379.
15. Folle GA. 2008. Nuclear architecture, chromosome domains and genetic damage. Mutat Res 658: 172-183.
16. Gadji M, Vallente R, Klewes L, Righolt C, Wark L, Kongruttanachok N, Knecht H, Mai S. 2011. Nuclear remodeling as a mechanism for genomic instability in cancer. Adv Cancer Res 112: 77-126.
17. Gazave E, Gautier P, Gilchrist S, Bickmore WA. 2005. Does radial nuclear organisation influence DNA damage? Chromosome Res 13: 377-388.
18. Gebre-Medhin S, Broberg K, Jonson T, Gorunova L, von Steyern FV, Brosjö O, Jin Y, Gisselsson D, Panagopoulos I, Mandahl N, Mertens F. 2009. Telomeric associations correlate with telomere length reduction and clonal chromosome aberrations in giant cell tumor of bone. Cytogenet Genome Res 124: 121-127.
19. Gisselsson D, Jonson T, Petersén A, Strömbeck B, Dal Cin P, Höglund M, Mitelman F, Mertens F, Mandahl N. 2001. Telomere dysfunction triggers extensive DNA fragmentation and evolution of complex chromosome abnormalities in human malignant tumors. Proc Natl Acad Sci USA 98: 12683-12688.
20. Gisselsson D, Lv M, Tsao SW, Man C, Jin C, Höglund M, Kwong YL, Jin Y. 2005. Telomere-mediated mitotic disturbances in immortalized ovarian epithelial cells reproduce chromosomal losses and breakpoints from ovarian carcinoma. Genes Chromosomes Cancer 42: 22-33.
21. Guffei A, Sarkar R, Klewes L, Righolt C, Knecht H, Mai S. 2010. Dynamic chromosomal rearrangements in Hodgkin's lymphoma are due to ongoing three-dimensional nuclear remodeling and breakage-bridge-fusion cycles. Haematologica 95: 2038-2046.
22. Haltrich I, Kost-Alimova M, Kovács G, Dobos M, Klein G, Fekete G, Imreh S. Multipoint interphase FISH in childhood T-acute lymphoblastic leukemia detects subpopulations that carry different chromosome 3 aberrations. 2007. Cancer Genet Cytogenet 172: 54-60.
23. Hanahan D, Weinberg RA. 2000. The hallmarks of cancer. Cell 100: 57-70.
24. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: The next generation. Cell 144: 646-674.
25. Johansson B, Fioretos T, Mitelman F. 2002. Cytogenetic and molecular genetic evolution of chronic myeloid leukemia. Acta Haematol 107: 76-94.
26. Kloosterman WP, Guryev V, van Roosmalen M, Duran KJ, de Bruijn E, Bakker SC, Letteboer T, van Nesselrooij B, Hochstenbach R, Poot M, Cuppen E. 2011a. Chromothripsis as a mechanism driving complex de novo structural rearrangements in the germline. Hum Mol Genet 20: 1916-1924.
27. Kloosterman WP, Hoogstraat M, Paling O, Tavakoli-Yaraki M, Renkens I, Vermaat JS, van Roosmalen MJ, van Lieshout S, Nijman IJ, Roessingh W, van 't Slot R, van de Belt J, Guryev V, Koudijs M, Voest E, Cuppen E. 2011b. Chromothripsis is a common mechanism driving genomic rearrangements in primary and metastatic colorectal cancer. Genome Biol 12: R103.
28. Kuschak TI, Taylor C, McMillan-Ward E, Israels S, Henderson DW, Mushinski JF, Wright JA, Mai S. 1999. The ribonucleotide reductase R2 gene is a non-transcribed target of c-Myc-induced genomic instability. Gene 238: 351-365.
29. Kuschak TI, Kuschak BC, Taylor CL, Wright JA, Wiener F, Mai S. 2002. c-Myc initiates illegitimate replication of the ribonucleotide reductase R2 gene. Oncogene 21: 909-920.
30. Lapuk AV, Wu C, Wyatt AW, McPherson A, McConeghy BJ, Brahmbhatt S, Mo F, Zoubeidi A, Anderson S, Bell RH, Haegert A, Shukin R, Wang Y, Fazli L, Hurtado-Coll A, Jones EC, Hach F, Hormozdiari F, Hajiresouliha I, Boutros PC, Bristow RG, Zhao Y, Marra MA, Fanjul A, Maher CA, Chinnaiyan AM, Rubin MA, Beltran H, Sahinalp SC, Gleave ME, Volik SV, Collins CC. 2012. From sequence to molecular pathology, and a mechanism driving the neuroendocrine phenotype in prostate cancer. J Pathol 227: 286-297
31. Lichter P, Cremer T, Borden J, Manuelidis L, Ward DC. 1988. Delineation of individual human chromosomes in metaphase and interphase cells by in situ suppression hybridization using recombinant DNA libraries. Hum Genet 80: 224-234.
32. Liu P, Erez A, Nagamani SC, Dhar SU, Kolodziejska KE, Dharmadhikari AV, Cooper ML, Wiszniewska J, Zhang F, Withers MA, Bacino CA, Campos-Acevedo LD, Delgado MR, Freedenberg D, Garnica A, Grebe TA, Hernández-Almaguer D, Immken L, Lalani SR, McLean SD, Northrup H, Scaglia F, Strathearn L, Trapane P, Kang SH, Patel A, Cheung SW, Hastings PJ, Stankiewicz P, Lupski JR, Bi W. 2011. Chromosome catastrophes involve replication mechanisms generating complex genomic rearrangements. Cell 146: 889-903.
33. Louis SF, Vermolen BJ, Garini Y, Young IT, Guffei A, Lichtensztejn Z, Kuttler F, Chuang TC, Moshir S, Mougey V, Chuang AY, Kerr PD, Fest T, Boukamp P, Mai S. 2005. c-Myc induces chromosomal rearrangements through telomere and chromosome remodeling in the interphase nucleus. Proc Natl Acad Sci USA 102: 9613-9618.
34. Mailankody S, Mena E, Yuan CM, Balakumaran A, Kuehl WM, Landgren O. 2010. Molecular and biologic markers of progression in monoclonal gammopathy of undetermined significance to multiple myeloma. Leuk Lymphoma 51: 2159-2170.
35. Magrangeas F, Avet-Loiseau H, Munshi NC, Minvielle S. 2011. Chromothripsis identifies a rare and aggressive entity among newly diagnosed multiple myeloma patients. Blood 118: 675-678.
36. Maher CA, Wilson RK. 2012. Chromothripsis and human disease: Piecing together the shattering process. Cell 148: 29-32.
37. Mai S. 1994. Overexpression of c-myc precedes amplification of the gene encoding dihydrofolate reductase. Gene 148: 253-260.
38. Mai S. 2010. Initiation of telomere-mediated chromosomal rearrangements in cancer. J Cell Biochem 109: 1095-1102.
39. Mai S, 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.
40. Mai S, Garini Y. 2006. The significance of telomeric aggregates in the interphase nuclei of tumor cells. J Cell Biochem 97: 904-915.
41. Mai S, Imreh S. 2007. Non-random genomic instability in cancer: A fact, not an illusion. Semin Cancer Biol 17: 1-4.
42. Mai S, Hanley-Hyde J, Fluri M. 1996. c-Myc overexpression associated DHFR gene amplification in hamster, rat, mouse and human cell lines. Oncogene 12: 277-288.
43. Mai S, Hanley-Hyde J, Rainey GJ, Kuschak TI, Paul JT, Littlewood TD, Mischak H, Stevens LM, Henderson DW, Mushinski JF. 1999. Chromosomal and extrachromosomal instability of the cyclin D2 gene is induced by Myc overexpression. Neoplasia 1: 241-252.
44. Meaburn KJ, Misteli T, Soutoglou E. 2007. Spatial genome organization in the formation of chromosomal translocations. Semin Cancer Biol 17: 80-90.
45. Molenaar JJ, Koster J, Zwijnenburg DA, van Sluis P, Valentijn LJ, van der Ploeg I, Hamdi M, van Nes J, Westerman BA, van Arkel J, Ebus ME, Haneveld F, Lakeman A, Schild L, Molenaar P, Stroeken P, van Noesel MM, Ora I, Santo EE, Caron HN, Westerhout EM, Versteeg R. 2012. Sequencing of neuroblastoma identifies chromothripsis and defects in neuritogenesis genes. Nature 483: 589-593.
46. Petersson C, Pandis N, Rizou H, Mertens F, Dietrich CU, Adeyinka A, Idvall I, Bondeson L, Georgiou G, Ingvar C, Heim S, Mitelman F. 1997. Karyotypic abnormalities in fibroadenomas of the breast. Int J Cancer 70: 282-286.
47. Rausch T, Jones DT, Zapatka M, Stütz AM, Zichner T, Weischenfeldt J, Jäger N, Remke M, Shih D, Northcott PA, Pfaff E, Tica J, Wang Q, Massimi L, Witt H, Bender S, Pleier S, Cin H, Hawkins C, Beck C, von Deimling A, Hans V, Brors B, Eils R, Scheurlen W, Blake J, Benes V, Kulozik AE, Witt O, Martin D, Zhang C, Porat R, Merino DM, Wasserman J, Jabado N, Fontebasso A, Bullinger L, Rücker FG, Döhner K, Döhner H, Koster J, Molenaar JJ, Versteeg R, Kool M, Tabori U, Malkin D, Korshunov A, Taylor MD, Lichter P, Pfister SM, Korbel JO. 2012. Genome sequencing of pediatric medulloblastoma links catastrophic DNA rearrangements with TP53 mutations. Cell 148: 59-71.
48. Sachs RK, Hlatky LR, Trask BJ. 2000. Radiation-produced chromosome aberrations: Colourful clues. Trends Genet 16: 143-146.
49. Selvarajah S, Yoshimoto M, Park PC, Maire G, Paderova J, Bayani J, Lim G, Al-Romaih K, Squire JA, Zielenska M. 2006. The breakage-fusion-bridge (BFB) cycle as a mechanism for generating genetic heterogeneity in osteosarcoma. Chromosoma 115: 459-467.
50. Selvarajah S, Yoshimoto M, Maire G, Paderova J, Bayani J, Squire JA, Zielenska M. 2007. Identification of cryptic microaberrations in osteosarcoma by high-definition oligonucleotide array comparative genomic hybridization. Cancer Genet Cytogenet 179: 52-61.
51. Selvarajah S, Yoshimoto M, Ludkovski O, Park PC, Bayani J, Thorner P, Maire G, Squire JA, Zielenska M. 2008. Genomic signatures of chromosomal instability and osteosarcoma progression detected by high resolution array CGH and interphase FISH. Cytogenet Genome Res 122: 5-15.
52. Shimizu N, Itoh N, Utiyama H, Wahl GM. 1998. Selective entrapment of extrachromosomally amplified DNA by nuclear budding and micronucleation during S phase. J Cell Biol 140: 1307-1320.
53. Sjöblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, Mandelker D, Leary RJ, Ptak J, Silliman N, Szabo S, Buckhaults P, Farrell C, Meeh P, Markowitz SD, Willis J, Dawson D, Willson JK, Gazdar AF, Hartigan J, Wu L, Liu C, Parmigiani G, Park BH, Bachman KE, Papadopoulos N, Vogelstein B, Kinzler KW, Velculescu VE. 2006. The consensus coding sequences of human breast and colorectal cancers. Science 314: 268-274.
54. Smith G, Taylor-Kashton C, Dushnicky L, Symons S, Wright J, Mai S. 2003. c-Myc-induced extrachromosomal elements carry active chromatin. Neoplasia 5: 110-120.
55. Stephens PJ, McBride DJ, Lin ML, Varela I, Pleasance ED, Simpson JT, Stebbings LA, Leroy C, Edkins S, Mudie LJ, Greenman CD, Jia M, Latimer C, Teague JW, Lau KW, Burton J, Quail MA, Swerdlow H, Churcher C, Natrajan R, Sieuwerts AM, Martens JW, Silver DP, Langerød A, Russnes HE, Foekens JA, Reis-Filho JS, van 't Veer L, Richardson AL, Børresen-Dale AL, Campbell PJ, Futreal PA, Stratton MR. 2009. Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature 462: 1005-1010.
56. Stephens PJ, Greenman CD, Fu B, Yang F, Bignell GR, Mudie LJ, Pleasance ED, Lau KW, Beare D, Stebbings LA, McLaren S, Lin ML, McBride DJ, Varela I, Nik-Zainal S, Leroy C, Jia M, Menzies A, Butler AP, Teague JW, Quail MA, Burton J, Swerdlow H, Carter NP, Morsberger LA, Iacobuzio-Donahue C, Follows GA, Green AR, Flanagan AM, Stratton MR, Futreal PA, Campbell PJ. 2011. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144: 27-40.
57. Stewénius Y, Gorunova L, Jonson T, Larsson N, Höglund M, Mandahl N, Mertens F, Mitelman F, Gisselsson D. 2005. Structural and numerical chromosome changes in colon cancer develop through telomere-mediated anaphase bridges, not through mitotic multipolarity. Proc Natl Acad Sci USA 102: 5541-5546.
58. Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, Nakamura Y, White R, Smits AM, Bos JL. 1988. Genetic alterations during colorectal-tumor development. N Engl J Med 319: 525-532.
59. Wood LD, Parsons DW, Jones S, Lin J, Sjöblom T, Leary RJ, Shen D, Boca SM, Barber T, Ptak J, Silliman N, Szabo S, Dezso Z, Ustyanksky V, Nikolskaya T, Nikolsky Y, Karchin R, Wilson PA, Kaminker JS, Zhang Z, Croshaw R, Willis J, Dawson D, Shipitsin M, Willson JK, Sukumar S, Polyak K, Park BH, Pethiyagoda CL, Pant PV, Ballinger DG, Sparks AB, Hartigan J, Smith DR, Suh E, Papadopoulos N, Buckhaults P, Markowitz SD, Parmigiani G, Kinzler KW, Velculescu VE, Vogelstein B. 2007. The genomic landscapes of human breast and colorectal cancers. Science 318: 1108-1113.