Whole Chromosome Instability Caused by Bub1 Insufficiency Drives Tumorigenesis through Tumor Suppressor Gene Loss of Heterozygosity

Cancer Cell

Volumn 16, Issue 6, 2009, Pages 475-486

  Baker, Darren J ^a   Jin, Fang ^a   Jeganathan, Karthik B ^a   van Deursen, Jan M ^a,b  

^a Mayo Clinic   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

CELLCYCLE; DNA

Indexed keywords

APC PROTEIN; BUB1 PROTEIN; NUCLEIC ACID BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P53; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ANEUPLOIDY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CHROMOSOMAL INSTABILITY; CHROMOSOME LOSS; CHROMOSOME SEGREGATION; COLON CARCINOGENESIS; COLON TUMOR; CONTROLLED STUDY; GENETIC PREDISPOSITION; HETEROZYGOSITY LOSS; KNOCKOUT MOUSE; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROTEIN DEPLETION; PROTEIN EXPRESSION; THYMUS LYMPHOMA; TUMOR SUPPRESSOR GENE;

MUS;

EID: 70749158525     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2009.10.023     Document Type: Article

References (44)

1. Baker D.J., Perez-Terzic C., Jin F., Pitel K., Niederlander N.J., Jeganathan K., Yamada S., Reyes S., Rowe L., Hiddinga H.J., et al. Opposing roles for p16Ink4a and p19Arf in senescence and ageing caused by BubR1 insufficiency. Nat. Cell Biol. 10 (2008) 825-836
2. Bracken A.P., Ciro M., Cocito A., and Helin K. E2F target genes: unraveling the biology. Trends Biochem. Sci. 29 (2004) 409-417
3. Chi Y.H., Ward J.M., Cheng L.I., Yasunaga J., and Jeang K.T. Spindle assembly checkpoint and p53 deficiencies cooperate for tumorigenesis in mice. Int. J. Cancer 124 (2009) 1483-1489
4. Di Cristofano A., and Pandolfi P.P. The multiple roles of PTEN in tumor suppression. Cell 100 (2000) 387-390
5. Di Cristofano A., De Acetis M., Koff A., Cordon-Cardo C., and Pandolfi P.P. Pten and p27KIP1 cooperate in prostate cancer tumor suppression in the mouse. Nat. Genet. 27 (2001) 222-224
6. Dobles M., Liberal V., Scott M.L., Benezra R., and Sorger P.K. Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2. Cell 101 (2000) 635-645
7. Fodde R., Kuipers J., Rosenberg C., Smits R., Kielman M., Gaspar C., van Es J.H., Breukel C., Wiegant J., Giles R.H., and Clevers H. Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat. Cell Biol. 3 (2001) 433-438
8. German J., and Alhadeff B. Analysis of sister-chromatid exchanges. Curr. Protoc. Hum. Genet. Chapter 8 (2001) Unit 8.6
9. Hawkins C.A., Bergstralh E.J., Lieber M.M., and Zincke H. Influence of DNA ploidy and adjuvant treatment on progression and survival in patients with pathologic stage T3 (PT3) prostate cancer after radical retropubic prostatectomy. Urology 46 (1995) 356-364
10. Holland A.J., and Cleveland D.W. Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat. Rev. Mol. Cell Biol. 10 (2009) 478-487
11. Hu N., Gutsmann A., Herbert D.C., Bradley A., Lee W.H., and Lee E.Y. Heterozygous Rb-1 delta 20/+mice are predisposed to tumors of the pituitary gland with a nearly complete penetrance. Oncogene 9 (1994) 1021-1027
12. Isaac C.E., Francis S.M., Martens A.L., Julian L.M., Seifried L.A., Erdmann N., Binne U.K., Harrington L., Sicinski P., Berube N.G., et al. The retinoblastoma protein regulates pericentric heterochromatin. Mol. Cell. Biol. 26 (2006) 3659-3671
13. Iwanaga Y., Chi Y.H., Miyazato A., Sheleg S., Haller K., Peloponese Jr. J.M., Li Y., Ward J.M., Benezra R., and Jeang K.T. Heterozygous deletion of mitotic arrest-deficient protein 1 (MAD1) increases the incidence of tumors in mice. Cancer Res. 67 (2007) 160-166
14. Jacks T., Fazeli A., Schmitt E.M., Bronson R.T., Goodell M.A., and Weinberg R.A. Effects of an Rb mutation in the mouse. Nature 359 (1992) 295-300
15. Jacks T., Remington L., Williams B.O., Schmitt E.M., Halachmi S., Bronson R.T., and Weinberg R.A. Tumor spectrum analysis in p53-mutant mice. Curr. Biol. 4 (1994) 1-7
16. Jeganathan K., Malureanu L., Baker D.J., Abraham S.C., and van Deursen J.M. Bub1 mediates cell death in response to chromosome missegregation and acts to suppress spontaneous tumorigenesis. J. Cell Biol. 179 (2007) 255-267
17. Kalitsis P., Fowler K.J., Griffiths B., Earle E., Chow C.W., Jamsen K., and Choo K.H. Increased chromosome instability but not cancer predisposition in haploinsufficient Bub3 mice. Genes Chromosomes Cancer 44 (2005) 29-36
18. Kaplan K.B., Burds A.A., Swedlow J.R., Bekir S.S., Sorger P.K., and Nathke I.S. A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat. Cell Biol. 3 (2001) 429-432
19. Keramaris E., Ruzhynsky V.A., Callaghan S.M., Wong E., Davis R.J., Flavell R., Slack R.S., and Park D.S. Required roles of Bax and JNKs in central and peripheral nervous system death of retinoblastoma-deficient mice. J. Biol. Chem. 283 (2008) 405-415
20. Kops G.J., Foltz D.R., and Cleveland D.W. Lethality to human cancer cells through massive chromosome loss by inhibition of the mitotic checkpoint. Proc. Natl. Acad. Sci. USA 101 (2004) 8699-8704
21. Lee E.Y., Chang C.Y., Hu N., Wang Y.C., Lai C.C., Herrup K., Lee W.H., and Bradley A. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359 (1992) 288-294
22. Lengauer C., Kinzler K.W., and Vogelstein B. Genetic instability in colorectal cancers. Nature 386 (1997) 623-627
23. Luo J., Solimini N.L., and Elledge S.J. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 136 (2009) 823-837
24. Luongo C., Moser A.R., Gledhill S., and Dove W.F. Loss of Apc+ in intestinal adenomas from Min mice. Cancer Res. 54 (1994) 5947-5952
25. Meraldi P., and Sorger P.K. A dual role for Bub1 in the spindle checkpoint and chromosome congression. EMBO J. 24 (2005) 1621-1633
26. Michel L.S., Liberal V., Chatterjee A., Kirchwegger R., Pasche B., Gerald W., Dobles M., Sorger P.K., Murty V.V., and Benezra R. MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 409 (2001) 355-359
27. Michor F., Iwasa Y., Vogelstein B., Lengauer C., and Nowak M.A. Can chromosomal instability initiate tumorigenesis?. Semin. Cancer Biol. 15 (2005) 43-49
28. Moser A.R., Pitot H.C., and Dove W.F. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 247 (1990) 322-324
29. Papp B., Pal C., and Hurst L.D. Dosage sensitivity and the evolution of gene families in yeast. Nature 424 (2003) 194-197
30. Park J.H., Walls J.E., Galvez J.J., Kim M., Abate-Shen C., Shen M.M., and Cardiff R.D. Prostatic intraepithelial neoplasia in genetically engineered mice. Am. J. Pathol. 161 (2002) 727-735
31. Perera D., Tilston V., Hopwood J.A., Barchi M., Boot-Handford R.P., and Taylor S.S. Bub1 maintains centromeric cohesion by activation of the spindle checkpoint. Dev. Cell 13 (2007) 566-579
32. Podsypanina K., Ellenson L.H., Nemes A., Gu J., Tamura M., Yamada K.M., Cordon-Cardo C., Catoretti G., Fisher P.E., and Parsons R. Mutation of Pten/Mmac1 in mice causes neoplasia in multiple organ systems. Proc. Natl. Acad. Sci. USA 96 (1999) 1563-1568
33. Rao C.V., Yang Y.M., Swamy M.V., Liu T., Fang Y., Mahmood R., Jhanwar-Uniyal M., and 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 102 (2005) 4365-4370
34. Ricke R.M., van Ree J.H., and van Deursen J.M. Whole chromosome instability and cancer: a complex relationship. Trends Genet. 24 (2008) 457-466
35. Schliekelman M., Cowley D.O., O'Quinn R., Oliver T.G., Lu L., Salmon E.D., and Van Dyke T. Impaired Bub1 function in vivo compromises tension-dependent checkpoint function leading to aneuploidy and tumorigenesis. Cancer Res. 69 (2009) 45-54
36. Shichiri M., Yoshinaga K., Hisatomi H., Sugihara K., and Hirata Y. Genetic and epigenetic inactivation of mitotic checkpoint genes hBUB1 and hBUBR1 and their relationship to survival. Cancer Res. 62 (2002) 13-17
37. Sotillo R., Hernando E., Diaz-Rodriguez E., Teruya-Feldstein J., Cordon-Cardo C., Lowe S.W., and Benezra R. Mad2 overexpression promotes aneuploidy and tumorigenesis in mice. Cancer Cell 11 (2007) 9-23
38. Torres E.M., Sokolsky T., Tucker C.M., Chan L.Y., Boselli M., Dunham M.J., and Amon A. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317 (2007) 916-924
39. Torres E.M., Williams B.R., and Amon A. Aneuploidy: cells losing their balance. Genetics 179 (2008) 737-746
40. Wang L.D., Zhou Q., Wei J.P., Yang W.C., Zhao X., Wang L.X., Zou J.X., Gao S.S., Li Y.X., and Yang C. Apoptosis and its relationship with cell proliferation, p53, Waf1p21, bcl-2 and c-myc in esophageal carcinogenesis studied with a high-risk population in northern China. World J. Gastroenterol. 4 (1998) 287-293
41. Weaver B.A., and Cleveland D.W. Aneuploidy: instigator and inhibitor of tumorigenesis. Cancer Res. 67 (2007) 10103-10105
42. Weaver B.A., Silk A.D., Montagna C., Verdier-Pinard P., and Cleveland D.W. Aneuploidy acts both oncogenically and as a tumor suppressor. Cancer Cell 11 (2007) 25-36
43. Williams B.R., Prabhu V.R., Hunter K.E., Glazier C.M., Whittaker C.A., Housman D.E., and Amon A. Aneuploidy affects proliferation and spontaneous immortalization in mammalian cells. Science 322 (2008) 703-709
44. Yuen K.W., Montpetit B., and Hieter P. The kinetochore and cancer: what's the connection?. Curr. Opin. Cell Biol. 17 (2005) 576-582