Increased expression of BubR1 protects against aneuploidy and cancer and extends healthy lifespan

Nature Cell Biology

Volumn 15, Issue 1, 2013, Pages 96-102

  Baker, Darren J ^a,b   Dawlaty, Meelad M ^b   Wijshake, Tobias ^a,c   Jeganathan, Karthik B ^a   Malureanu, Liviu ^a,b   Van Ree, Janine H ^a   Crespo Diaz, Ruben ^a   Reyes, Santiago ^a   Seaburg, Lauren ^b   Shapiro, Virginia ^b   Behfar, Atta ^a   Terzic, Andre ^a   Van De Sluis, Bart ^c   Van Deursen, Jan M ^a,b  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BUB1 RELATED PROTEIN; K RAS PROTEIN;

AGING; ANEUPLOIDY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BUBR1 GENE; CANCER INCIDENCE; CANCER PREVENTION; CANCER RESISTANCE; CANCER SURVIVAL; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CATARACT; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; FEMALE; GENE FUNCTION; GENE OVEREXPRESSION; GENOMICS; HEART FAILURE; KIDNEY FIBROSIS; LIFESPAN; MALE; MOUSE; NEPHROSCLEROSIS; NONHUMAN; ONCOGENE K RAS; OSTEOPOROSIS; PRIORITY JOURNAL; TRANSGENE;

9,10-DIMETHYL-1,2-BENZANTHRACENE; AGING; ANEUPLOIDY; ANIMALS; CELL COUNT; CELLS, CULTURED; CHROMOSOMAL INSTABILITY; FEMALE; GENE EXPRESSION; LIFE EXPECTANCY; LUNG NEOPLASMS; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE, SKELETAL; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; SKIN NEOPLASMS; STEM CELLS;

MUS;

EID: 84871717211     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2643     Document Type: Article

References (52)

1. Baker, D. J. et al. BubR1 insuf-ciency causes early onset of aging-associated phenotypes and infertility in mice. Nat. Genet. 36, 744-749 (2004).
2. Lampson, M. A. & Kapoor, T. M. The human mitotic checkpoint protein BubR1 regulates chromosome-spindle attachments. Nat. Cell Biol. 7, 93-98 (2005).
3. Malureanu, L. A. et al. BubR1 N terminus acts as a soluble inhibitor of cyclin B degradation by APC/C(Cdc20) in interphase. Dev. Cell 16, 118-131 (2009).
4. Matsumoto, T. et al. Aging-associated vascular phenotype in mutant mice with low levels of BubR1. Stroke 38, 1050-1056 (2007).
5. Hartman, T. K., Wengenack, T. M., Poduslo, J. F. & van Deursen, J. M. Mutant mice with small amounts of BubR1 display accelerated age-related gliosis. Neurobiol. Aging 28, 921-927 (2007).
6. Baker, D. J. et al. Opposing roles for p16Ink4a and p19Arf in senescence and ageing caused by BubR1 insuf-ciency. Nat. Cell Biol. 10, 825-836 (2008).
7. Matsuura, S. et al. Monoallelic BUB1B mutations and defective mitotic-spindle checkpoint in seven families with premature chromatid separation (PCS) syndrome. Am. J. Med. Genet. A 140, 358-367 (2006).
8. Hanks, S. et al. Constitutional aneuploidy and cancer predisposition caused by biallelic mutations in BUB1B. Nat. Genet. 36, 1159-1161 (2004).
9. Burtner, C. R. & Kennedy, B. K. Progeria syndromes and ageing: what is the connection? Nat. Rev. Mol. Cell Biol. 11, 567-578 (2010).
10. Sotillo, R. et al. Mad2 overexpression promotes aneuploidy and tumorigenesis in mice. Cancer Cell 11, 9-23 (2007).
11. Van Ree, J. H., Jeganathan, K. B., Malureanu, L. & van Deursen, J. M. Overex-pression of the E2 ubiquitin-conjugating enzyme UbcH10 causes chromosome missegregation and tumor formation. J. Cell Biol. 188, 83-100 (2010).
12. Ricke, R. M., Jeganathan, K. B. & van Deursen, J. M. Bub1 overexpression induces aneuploidy and tumor formation through Aurora B kinase hyperactivation. J. Cell Biol. 193, 1049-1064 (2011).
13. Serrano, M. et al. Role of the INK4a locus in tumor suppression and cell mortality. Cell 85, 27-37 (1996).
14. Johnson, L. et al. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 410, 1111-1116 (2001).
15. Schvartzman, J. M., Sotillo, R. & Benezra, R. Mitotic chromosomal instability and cancer: mouse modelling of the human disease. Nat. Rev. Cancer 10, 102-115 (2010).
16. Holland, A. J. & Cleveland, D. W. Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat. Rev. Mol. Cell Biol. 10, 478-487 (2009).
17. Baker, D. J., Jin, F., Jeganathan, K. B. & van Deursen, J. M. Whole chromosome instability caused by Bub1 insuf-ciency drives tumorigenesis through tumor suppressor gene loss of heterozygosity. Cancer Cell 16, 475-486 (2009).
18. Saavedra, H. I. et al. The RAS oncogene induces genomic instability in thyroid PCCL3 cells via the MAPK pathway. Oncogene 19, 3948-3954 (2000).
19. Sudakin, V., Chan, G. K. & Yen, T. J. Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J. Cell Biol. 154, 925-936 (2001).
20. Babu, J. R. et al. Rae1 is an essential mitotic checkpoint regulator that cooperates with Bub3 to prevent chromosome missegregation. J. Cell Biol. 160, 341-353 (2003).
21. Krishnamurthy, J. et al. Ink4a/Arf expression is a biomarker of aging. J. Clin. Invest. 114, 1299-1307 (2004).
22. Herbig, U., Jobling, W. A., Chen, B. P., Chen, D. J. & Sedivy, J. M. Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol. Cell 14, 501-513 (2004).
23. Matheu, A. et al. Delayed ageing through damage protection by the Arf/p53 pathway. Nature 448, 375-379 (2007).
24. Lukas, C. et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol. 13, 243-253 (2011).
25. Janssen, A., van der Burg, M., Szuhai, K., Kops, G. J. & Medema, R. H. Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations. Science 333, 1895-1898 (2011).
26. Vijg, J. & Campisi, J. Puzzles, promises and a cure for ageing. Nature 454, 1065-1071 (2008).
27. Baker, D. J. et al. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 479, 232-236 (2011).
28. Lushnikova, T., Bouska, A., Odvody, J., Dupont, W. D. & Eischen, C. M. Aging mice have increased chromosome instability that is exacerbated by elevated Mdm2 expression. Oncogene 30, 4622-4631 (2011).
29. Bergmann, O. et al. Evidence for cardiomyocyte renewal in humans. Science 324, 98-102 (2009).
30. Holland, A. J. & Cleveland, D. W. Losing balance: the origin and impact of aneuploidy in cancer. EMBO Rep. 13, 501-514 (2012).
31. Pfau, S. J. & Amon, A. Chromosomal instability and aneuploidy in cancer: from yeast to man. EMBO Rep. 13, 515-527 (2012).
32. Baker, D. J. et al. Early aging-associated phenotypes in Bub3/Rae1 haploinsuf-cient mice. J. Cell Biol. 172, 529-540 (2006).
33. Li, H., Mitchell, J. R. & Hasty, P. DNA double-strand breaks: a potential causative factor for mammalian aging? Mech. Ageing Dev. 129, 416-424(2008).
34. Morimoto, R. I. Proteotoxic stress and inducible chaperone networks in neurodegen-erative disease and aging. Genes Dev. 22, 1427-1438 (2008).
35. Fang, Y. et al. BubR1 is involved in regulation of DNA damage responses. Oncogene 25, 3598-3605 (2006).
36. Miyamoto, T. et al. Insuf-ciency of BUBR1, a mitotic spindle checkpoint reg-ulator, causes impaired ciliogenesis in vertebrates. Hum. Mol. Genet. 20, 2058-2070 (2011).
37. Malureanu, L. et al. Cdc20 hypomorphic mice fail to counteract de novo synthesis of cyclin B1 in mitosis. J. Cell Biol. 191, 313-329 (2010).
38. Kim, A. H. et al. A centrosomal Cdc20-APC pathway controls dendrite morphogenesis in postmitotic neurons. Cell 136, 322-336 (2009).
39. Yang, Y. et al. A Cdc20-APC ubiquitin signaling pathway regulates presynaptic differentiation. Science 326, 575-578 (2009).
40. Conover, C. A. & Bale, L. K. Loss of pregnancy-associated plasma protein A extends lifespan in mice. Aging Cell 6, 727-729 (2007).
41. Van Ree, J., Zhou, W., Li, M. & van Deursen, J. M. Transgenesis in mouse embryonic stem cells. Methods Mol. Biol. 693, 143-162 (2011).
42. Wang, C., Li, Q., Redden, D. T., Weindruch, R. & Allison, D. B. Statistical methods for testing effects on ̀maximum lifespan'. Mech. Ageing Dev. 125, 629-632 (2004).
43. Kasper, L. H. et al. CREB binding protein interacts with nucleoporin-specific FG repeats that activate transcription and mediate NUP98-HOXA9 oncogenicity. Mol. Cell Biol. 19, 764-776 (1999).
44. Jeganathan, K., Malureanu, L., Baker, D. J., Abraham, S. C. & van Deursen, J. M. Bub1 mediates cell death in response to chromosome missegregation and acts to suppress spontaneous tumorigenesis. J. Cell Biol. 179, 255-267 (2007).
45. Bayani, J. & Squire, J. A. Fluorescence in situ hybridization (FISH). Curr. Protoc. Cell Biol. 1-51 (2004).
46. Nath, K. A., Croatt, A. J., Warner, G. M. & Grande, J. P. Genetic de-ciency of Smad3 protects against murine ischemic acute kidney injury. Am. J. Physiol. Renal. Physiol. 301, F436-F442 (2011).
47. Ameri, A., Kurachi, S., Sueishi, K., Kuwahara, M. & Kurachi, K. Myocardial-brosis in mice with overexpression of human blood coagulation factor IX. Blood 101, 1871-1873 (2003).
48. Conboy, I. M., Conboy, M. J., Smythe, G. M. & Rando, T. A. Notch-mediated restora-tion of regenerative potential to aged muscle. Science 302, 1575-1577 (2003).
49. Sherwood, R. I. et al. Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle. Cell 119, 543-554 (2004).
50. Liu, X. K. et al. Genetic disruption of Kir6.2, the pore-forming subunit of ATP-sensitive KC channel, predisposes to catecholamine-induced ventricular dysrhythmia. Diabetes 53 (Suppl. 3), S165-S168 (2004).
51. Oh, H. et al. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc. Natl Acad. Sci. USA 100, 12313-12318 (2003).
52. Pajerowski, A. G. et al. Adult hematopoietic stem cells require NKAP for maintenance and survival. Blood 116, 2684-2693 (2010).