Pericentromeric instability and spontaneous emergence of human neoacrocentric and minute chromosomes in the alternative pathway of telomere lengthening

Cancer Research

Volumn 68, Issue 19, 2008, Pages 8146-8155

  Gagos, Sarantis ^a,e   Chiourea, Maria ^a   Christodoulidou, Agni ^a   Apostolou, Eftichia ^a   Raftopoulou, Christina ^a   Deustch, Samuel ^b   Jefford, Charles Edward ^c   Irminger Finger, Irmgard ^c   Shay, Jerry W ^d   Antonarakis, Stylianos E ^b  

^a BIOMEDICAL RESEARCH FOUNDATION   (Greece)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^c GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e NONE   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

TELOMERASE;

ARTICLE; CANCER CELL CULTURE; CENTROMERE; CHROMOSOMAL INSTABILITY; CHROMOSOME 21; CHROMOSOME STRUCTURE; CONTROLLED STUDY; ENZYME INHIBITION; FLUORESCENCE IN SITU HYBRIDIZATION; GAMMA IRRADIATION; GENETIC RECOMBINATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; SISTER CHROMATID; TELOMERE;

CELL PROLIFERATION; CENTROMERE; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATIONS; CHROMOSOME BREAKAGE; CYTOGENETIC ANALYSIS; HCT116 CELLS; HELA CELLS; HT29 CELLS; HUMANS; SIGNAL TRANSDUCTION; TELOMERASE; TELOMERE; TUMOR CELLS, CULTURED;

EID: 54249154250     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-0945     Document Type: Article

References (42)

1. Blasco MA. Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet 2005;6:611-22.
2. Bryan TM, Englezou A, Gupta J, Bacchetti S, Reddel RR. Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J 1995;14:4240-8.
3. Kim NW, Piatyszek MA, Prowse KR, et al. Specific association of human telomerase activity with immortal cells and cancer. Science 1994;26:2011-5.
4. Muntoni A, Reddel RR. The first molecular details of ALT in human tumor cells. Hum Mol Genet 2005;14:191-6.
5. Chang S, Khoo CM, Naylor ML, Maser RS, DePinho RA. Telomere-based crisis: functional differences between telomerase activation and ALT in tumor progression. Genes Dev 2003;17:88-100.
6. Rizki A, Lundblad V. Defects in mismatch repair promote telomerase-independent proliferation. Nature 2001;411:713-6.
7. Bechter OE, Zou Y, Walker W, Wright WE, Shay JW. Telomeric recombination in mismatch repair deficient human colon cancer cells after telomerase inhibition. Cancer Res 2004;64:3444-51.
8. Rajagopalan H, Jallepalli PV, Rago C, et al. Inactivation of hCDC4 can cause chromosomal instability. Nature 2004;428:77-81.
9. Hackett JA, Greider CW. Balancing instability: dual roles for telomerase and telomere dysfunction in tumorigenesis. Oncogene 2002;21:619-26.
10. Shay JW, Wright WE. Hallmarks of telomeres in ageing research. J Pathol 2007;211:114-23.
11. Gisselsson D, Pettersson L, Höglund M, et al. Chromosomal breakage-fusion-bridge events cause genetic intratumor heterogeneity. Proc Natl Acad Sci U S A 2000;97:5357-62.
12. Sabatier L, Ricoul M, Pottier G, Murnane JP. The loss of a single telomere can result in instability of multiple chromosomes in a human tumor cell line. Mol Cancer Res 2005;3:139-50.
13. Selvarajah S, Yoshimoto M, Park P, et al. The breakage-fusion-bridge (BFB) cycle as a mechanism for generating genetic heterogeneity in osteosarcoma. Chromosoma 2006;115:459-67.
14. Bailey SM, Brenneman MA, Goodwin EH. Frequent recombination in telomeric DNA may extend the proliferative life of telomerase-negative cells. Nucleic Acids Res 2004;16:3743-51.
15. Yeager TR, Neumann AA, Englezou A, Huschtscha LI, Noble JR, Reddel RR. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res 1999;59:4175-9.
16. Fasching CL, Neumann AA, Muntoni A, Yeager TR, Reddel RR. DNA damage induces alternative lengthening of telomeres (ALT) associated promyelocytic leukemia bodies that preferentially associate with linear telomeric DNA. Cancer Res 2007;67:7072-7.
17. Tarsounas M, Munoz P, Claas A, et al. Telomere maintenance requires the RAD51D recombination/ repair protein. Cell 2004;117:337-47.
18. Zhong Z, Jiang W, Cesare AJ, Neumann AA, Wadhwa R, Reddel RR. Disruption of telomere maintenance by depletion of the MRE11/RAD50/NBS1 complex in cells that use alternative lengthening of telomeres. J Biol Chem 2007;40:29314-22.
19. Trask BJ. Human Cytogenetics: 46 Chromosomes, 46 years and counting. Nat Rev Genet 2002;3:769-78.
20. Gagos S, Irminger-Finger I. Chromosome instability in neoplasia: chaotic roots to continuous growth. Int J Biochem Cell Biol 2005;37:1014-33.
21. Ford LP, Zou Y, Pongracz K, Gryaznov SM, Shay JW, Wright WE. Telomerase can inhibit the recombination-based pathway of telomere maintenance in human cells. J Biol Chem 2001;276:32198-203.
22. Barch JM, editor. The ACT Cytogenetics laboratory manual. 2nd ed. New York: Raven Press; 1991.
23. Guan Z, Giustetto M, Lombardas S, et al. Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 2002;111:483-93.
24. Coullin P, Andreo B, Charlieu JP, Candelier JJ, Pellestor F. Primed in situ (PRINS) labelling with Alu and satellite primers for rapid characterization of human chromosomes in hybrid cell lines. Chromosome Res 1997;5:307-12.
25. Hubbard TJP, Aken BL, Beal1 K, et al. Ensembl 2007. Nucleic Acids Res 2007;35:610-7. Available from http://www.ensembl.org.
26. Bailey SM, Cornforth MN, Kurimasa A, Chen DJ, Goodwin EH. Strand-Specific Postreplicative Processing of Mammalian Telomeres. Science 2001;293:2462-5.
27. Rogakou EP, Nieves-Neira W, Boon C, Pommier Y, Bonner WM. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 2000;275:9390-5.
28. Sugata N, Li S, Earnshaw WC, et al. Human CENP-H multimers colocalize with CENP-A and CENP-C at active centromere-kinetochore complexes. Hum Mol Genet 2000;9:2919-26.
29. Scheel C, Schaefer K, Jauch A, et al. Alternative lengthening of telomeres is associated with chromosomal instability in osteosarcomas. Oncogene 2001;20:3835-44.
30. Bayani J, Zielenska M, Pandita A, et al. Spectral karyotyping identifies recurrent complex rearrangements of chromosomes 8, 17, and 20 in osteosarcomas. Genes Chromosomes Cancer 2003;36:7-16.
31. Gisselsson D, Hoglund M, Mertens F, Mandahl N. Variable stability of chromosomes containing amplified a-satellite sequences in human mesenchymal tumours. Chromosoma 1999;108:271-7.
32. Dellaire G, Ching RW, Ahmed K, et al. Promyelocytic leukemia nuclear bodies behave as DNA damage sensors whose response to DNA double-strand breaks is regulated by NBS1 and the kinases ATM, Chk2, and ATR. J Cell Biol 2006;175:55-66.
33. Costanzo V, Robertson K, Bibikova M, et al. Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol Cell 2001;8:137-47.
34. Zhu XD, Niedernhofer L, Kuster B, Mann M, Hoeijmakers JHJ, de Lange T. ERCC1/XPF removes the 3′ overhang from uncapped telomeres and represses formation of telomeric DNA-containing double minute chromosomes. Mol Cell 2003;12:1489-98.
35. Cayuela ML, Flores JM, Blasco MA. The telomerase RNA component Terc is required for the tumour-promoting effects of Tert overexpression. EMBO Rep 2005;6:268-74.
36. Basu J, Willard HF. Artificial and engineered chromosomes: non-integrating vectors for gene therapy. Trends Mol Med 2005;11:251-8.
37. Lin CC, Meyne J, Sasi R, Moyzis RK. Apparent lack of telomere sequences on double minute chromosomes. Cancer Genet Cytogenet 1990;48:271-4.
38. Mitelman F. ISCN: an international system for human cytogenetic nomenclature. Basel: Karger; 1995.
39. Jackson SP. Sensing and repairing DNA doublestrand breaks. Carcinogenesis 2002;23:687-96.
40. Teng SC, Zakian VA. Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae . Mol Cell Biol 1999;19:8083-93.
41. Garcia-Cao M, O'Sullivan R, Peters AH, Jenuwein T, Blasco MA. Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat Genet 2004;36:94-9.
42. Cenci G, Ciapponi L, Gatti M. The mechanism of telomere protection: a comparison between Drosophila and humans. Chromosoma 2005;114:135-45.