c-MYC delays prometaphase by direct transactivation of MAD2 and BubR1: Identification of mechanisms underlying c-MYC-induced DNA damage and chromosomal instability

Cell Cycle

Volumn 6, Issue 3, 2007, Pages 339-352

  Menssen, Antje ^a   Epanchintsev, Alexey ^a   Rezaei, Nousin ^a   Lodygin, Dmitri ^a   Jung, Peter ^a   Verdoodt, Berlinda ^a   Diebold, Joachim ^b   Hermeking, Heiko ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

BubR1; c MYC; Cell cycle; Chromosomal instability; DNA damage response; MAD2; Mitosis; Spindle assembly checkpoint

Indexed keywords

ANAPHASE PROMOTING COMPLEX; BUB1 RELATED PROTEIN; DOUBLE STRANDED DNA; HISTONE H2AX; MYC PROTEIN; PROTEIN MAD2;

ALLELE; ANEUPLOIDY; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE G2 PHASE; CELL STRAIN MCF 7; CHROMOSOMAL INSTABILITY; COLORECTAL CANCER; CONTROLLED STUDY; CORRELATION ANALYSIS; DAUGHTER CELL; DEREGULATION; DIPLOIDY; DNA DAMAGE; DNA REPLICATION; DNA STRAND BREAKAGE; E BOX ELEMENT; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRON; MICROSATELLITE INSTABILITY; MITOSIS INHIBITION; MITOSIS SPINDLE; NONHUMAN; ONCOGENE; PROMETAPHASE; PROTEIN EXPRESSION; RAT; TRANSACTIVATION; TUMOR BIOPSY;

EID: 33847013757     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.6.3.3808     Document Type: Article

References (52)

1. Boveri T. Zur Frage der Entstehung maligner Tumoren. Jena: Gustav Fischer Verlag 1914.
2. von Hansemann D. Über asymmetrische Zellteilung in Epithelkrebsen und deren biologische Bedeutung. Virchows Arch Patholog Anat 1890; 119:299-326.
3. Rajagopalan H, Lengauer C. Aneuploidy and cancer. Nature 2004; 432:338-41.
4. Lengauer C. Aneuploidy and genetic instability in cancer. Semin Cancer Biol 2005; 15:1.
5. Cahill DP, da Costa LT, Carson-Walter EB, Kinzler KW, Vogelstein B, Lengauer C. Characterization of MAD2B and other mitotic spindle checkpoint genes. Genomics 1999; 58:181-7.
6. Hernando E, Orlow I, Liberal V, Nohales G, Benezra R, Cordon-Cardo C. Molecular analyses of the mitotic checkpoint components hsMAD2, hBUB1 and hBUB3 in human cancer. Int J Cancer 2001; 95:223-7.
7. Wang Z, Cummins JM, Shen D, Cahill DP, Jallepalli PV, Wang TL, Parsons DW, Traverso G, Awad M, Silliman N, Ptak J, Szabo S, Willson JK, Markowitz SD, Goldberg ML, Karess R, Kinzler KW, Vogelstein B, Velculescu VE, Lengauer C. Three classes of genes mutated in colorectal cancers with chromosomal instability. Cancer Res 2004; 64:2998-3001.
8. Mai S, Mushinski JF. c-Myc-induced genomic instability. J Environ Pathol Toxicol Oncol 2003; 22:179-99.
9. Felsher DW, Bishop JM. Transient excess of MYC activity can elicit genomic instability and tumorigenesis. Proc Natl Acad Sci USA 1999; 96:3940-4.
10. Boxer RB, Jang JW, Sintasath L, Chodosh LA. Lack of sustained regression of c-MYC-induced mammary adenocarcinomas following brief or prolonged MYC inactivation. Cancer Cell 2004; 6:577-86.
11. Oster SK, Ho CS, Soucie EL, Penn LZ. The myc oncogene: MarvelouslY Complex. Adv Cancer Res 2002; 84:81-154.
12. Patel JH, Loboda AP, Showe MK, Showe LC, McMahon SB. Analysis of genomic targets reveals complex functions of MYC. Nat Rev Cancer 2004; 4:562-8.
13. Menssen A, Hermeking H. Characterization of the c-MYC-regulated transcriptome by SAGE: identification and analysis of c-MYC target genes. Proc Natl Acad Sci USA 2002; 99:6274-9.
14. Kops GJ, Weaver BA, Cleveland DW. On the road to cancer: aneuploidy and the mitotic checkpoint. Nat Rev Cancer 2005; 5:773-85.
15. Nasmyth K. How Do so Few Control so Many? Cell 2005; 120:739-46.
16. Fang G, Yu H, Kirschner MW. The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation. Genes Dev 1998; 12:1871-83.
17. Michel LS, Liberal V, Chatterjee A, Kirchwegger R, Pasche B, Gerald W, Dobles M, Sorger PK, Murty VV, Benezra R. MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 2001; 409:355-9.
18. Mao Y, Abrieu A, Cleveland DW. Activating and silencing the mitotic checkpoint through CENP-E-dependent activation/inactivation of BubR1. Cell 2003; 114:87-98.
19. Hernando E, Nahle Z, Juan G, Diaz-Rodriguez E, Alaminos M, Hemann M, Michel L, Mittal V, Gerald W, Benezra R, Lowe SW, Cordon-Cardo C. Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control. Nature 2004; 430:797-802.
20. Hermeking H, Rago C, Schuhmacher M, Li Q, Barrett JF, Obaya AJ, O'Connell BC, Mateyak MK, Tam W, Kohlhuber F, Dang CV, Sedivy JM, Eick D, Vogelstein B, Kinzler KW. Identification of CDK4 as a target of c-MYC. Proc Natl Acad Sci USA 2000; 97:2229-34.
21. Yu J, Zhang L, Hwang PM, Rago C, Kinzler KW, Vogelstein B. Identification and classification of p53-regulated genes. Proc Natl Acad Sci USA 1999; 96:14517-22.
22. Archidiacono N, Antonacci R, Marzella R, Finelli P, Lonoce A, Rocchi M. Comparative mapping of human alphoid sequences in great apes using fluorescence in situ hybridization. Genomics 1995; 25:477-84.
23. Brummelkamp TR, Bernards R, Agami R. Stable suppression of tumorigenicity by virus-mediated RNA interference. Cancer Cell 2002; 2:243-7.
24. van de Wetering M, Oving I, Muncan V, Pon Fong MT, Brantjes H, van Leenen D, Holstege FC, Brummelkamp TR, Agami R, Clevers H. Specific inhibition of gene expression using a stably integrated, inducible small-interfering-RNA vector. EMBO Rep 2003; 4:609-15.
25. Frank SR, Schroeder M, Fernandez P, Taubert S, Amati B. Binding of c-Myc to chromatin mediates mitogen-induced acetylation of histone H4 and gene activation. Genes Dev 2001; 15:2069-82.
26. Haggerty TJ, Zeller KI, Osthus RC, Wonsey DR, Dang CV. A strategy for identifying transcription factor binding sites reveals two classes of genomic c-Myc target sites. Proc Natl Acad Sci USA 2003; 100:5313-8.
27. Musacchio A, Hardwick KG. The spindle checkpoint: structural insights into dynamic signaling. Nat Rev Mol Cell Biol 2002; 3:731-41.
28. Cahill DP, Lengauer C, Yu J, Riggins GJ, Willson JK, Markowitz SD, Kinzler KW, Vogelstein B. Mutations of mitotic checkpoint genes in human cancers. Nature 1998; 392:300-3.
29. Lengauer C, Kinzler KW, Vogelstein B. Genetic instability in colorectal cancers. Nature 1997; 386:623-7.
30. Vafa O, Wade M, Kern S, Beeche M, Pandita TK, Hampton GM, Wahl GM. c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol Cell 2002; 9:1031-44.
31. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, Schurra C, Garre M, Nuciforo PG, Bensimon A, Maestro R, Pelicci PG, d'Adda di Fagagna F. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006; 444:638-42.
32. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, Vassiliou LV, Kolettas E, Niforou K, Zoumpourlis VC, Takaoka M, Nakagawa H, Tort F, Fugger K, Johansson F, Sehested M, Andersen CL, Dyrskjot L, Orntoft T, Lukas J, Kittas C, Helleday T, Halazonetis TD, Bartek J, Gorgoulis VG. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006; 444:633-7.
33. Hermeking H, Funk JO, Reichert M, Ellwart JW, Eick D. Abrogation of p53-induced cell cycle arrest by c-Myc: evidence for an inhibitor of p21WAF1/CIP1/SDI1. Oncogene 1995; 11:1409-15.
34. Hermeking H, Eick D. Mediation of c-Myc-induced apoptosis by p53. Science 1994; 265:2091-3.
35. Kim HS, Park KH, Kim SA, Wen J, Park SW, Park B, Gham CW, Hyung WJ, Noh SH, Kim HK, Song SY. Frequent mutations of human Mad2, but not Bub1, in gastric cancers cause defective mitotic spindle checkpoint. Mutat Res 2005; 578:187-201.
36. Percy MJ, Myrie KA, Neeley CK, Azim JN, Ethier SP, Petty EM. Expression and mutational analyses of the human MAD2L1 gene in breast cancer cells. Genes Chromosomes Cancer 2000; 29:356-62.
37. Michel L, Benezra R, Diaz-Rodriguez E. MAD2 dependent mitotic checkpoint defects in tumorigenesis and tumor cell death: a double edged sword. Cell Cycle 2004; 3:990-2.
38. Rao CV, Yang YM, Swamy MV, Liu T, Fang Y, Mahmood R, Jhanwar-Uniyal M, Dai W. Colonic tumorigenesis in BubR1+/-ApcMin/+ compound mutant mice is linked to premature separation of sister chromatids and enhanced genomic instability. Proc Natl Acad Sci USA 2005; 102:4365-70.
39. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW. Identification of c-MYC as a target of the APC pathway. Science 1998; 281:1509-12.
40. Hanks S, Coleman K, Reid S, Plaja A, Firth H, Fitzpatrick D, Kidd A, Mehes K, Nash R, Robin N, Shannon N, Tolmie J, Swansbury J, Irrthum A, Douglas J, Rahman N. Constitutional aneuploidy and cancer predisposition caused by biallelic mutations in BUB1B. Nat Genet 2004; 36:1159-61.
41. Matsuura S, Matsumoto Y, Morishima K, Izumi H, Matsumoto H, Ito E, Tsutsui K, Kobayashi J, Tauchi H, Kajiwara Y, Hama S, Kurisu K, Tahara H, Oshimura M, Komatsu K, Ikeuchi T, Kajii T. Monoallelic BUB1B mutations and defective mitotic-spindle checkpoint in seven families with premature chromatid separation (PCS) syndrome. Am J Med Genet A 2006; 140:358-67.
42. Shin HJ, Baek KH, Jeon AH, Park MT, Lee SJ, Kang CM, Lee HS, Yoo SH, Chung DH, Sung YC, McKeon F, Lee CW. Dual roles of human BubR1, a mitotic checkpoint kinase, in the monitoring of chromosomal instability. Cancer Cell 2003; 4:483-97.
43. Syljuasen RG, Jensen S, Bartek J, Lukas J. Adaptation to the ionizing radiation-induced G2 checkpoint occurs in human cells and depends on checkpoint kinase 1 and Polo-like kinase 1 kinases. Cancer Res 2006; 66:10253-7.
44. Zeller KI, Zhao X, Lee CW, Chiu KP, Yao F, Yustein JT, Ooi HS, Orlov YL, Shahab A, Yong HC, Fu Y, Weng Z, Kuznetsov VA, Sung WK, Ruan Y, Dang CV, Wei CL. Global mapping of c-Myc binding sites and target gene networks in human B cells. Proc Natl Acad Sci USA 2006; 103:17834-9.
45. Koch HB, Zhang R, Verdoodt B, Bailey A, Zhang CD, Yates JR, Menssen A, Hermeking H. Large Scale identification of c-MYC-associated proteins with a combined TAP/MudPIT approach. Cell Cycle 2007; 6:205-17.
46. van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A, van der Horn K, Batlle E, Coudreuse D, Haramis AP, Tjon-Pon-Fong M, Moerer P, van den Born M, Soete G, Pals S, Eilers M, Medema R, Clevers H. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 2002; 111:241-50.
47. Pajic A, Spitkovsky D, Christoph B, Kempkes B, Schuhmacher M, Staege MS, Brielmeier M, Ellwart J, Kohlhuber F, Bornkamm GW, Polack A, Eick D. Cell cycle activation by cmyc in a burkitt lymphoma model cell line. Int J Cancer 2000; 87:787-93.
48. Supplemental information can be found at: www.landesbioscience.com/ supplement/ menssenCC6-3-sup.pdf
49. www.landesbioscience.com/supplement/ menssenCC6-3-sup2.mov
50. www.landesbioscience.com/supplement/ menssenCC6-3-sup3.mov
51. www.landesbioscience.com/supplement/ menssenCC6-3-sup4.mov
52. www.landesbioscience.com/supplement/ menssenCC6-3-sup5.mov