The centrosome and mitotic spindle apparatus in cancer and senescence

Cell Cycle

Volumn 9, Issue 22, 2010, Pages 4469-4473

  Schmidt, Stephan ^a   Essmann, Frank ^d   Cirstea, Ion C ^a   Kuck, Fabian ^a   Thakur, Harish C ^a   Singh, Madhurendra ^a   Kletke, Anja ^a   Jänicke, Reiner U ^b   Wiek, Constanze ^b   Hanenberg, Helmut ^b,c   Ahmadian, M Reza ^a   Schulze Osthoff, Klaus ^d   Nürnberg, Bernd ^d   Piekorz, Roland P ^a  

^a Institut fuer Biochemie und Molekularbiologie I   (Germany)

^b UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Cancer; Centrosome; Kinetochore; Mitotic checkpoint; p53; Senescence

Indexed keywords

CELL PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1; PROTEIN P53; TOXIC SUBSTANCE; TRANSFORMING ACIDIC COILED COIL PROTEIN; UNCLASSIFIED DRUG;

CARCINOGENESIS; CELL AGING; CELL STRESS; CENTROMERE; CENTROSOME; MITOSIS; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SPINDLE CELL;

EID: 78649804198     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.22.13684     Document Type: Review

References (62)

1. Nigg EA. Origins and consequences of centrosome aberrations in human cancers. Int J Cancer 2006; 119:2717-23.
2. Khodjakov A, Rieder CL. The nature of cell cycle checkpoints: Facts and fallacies. J Biol 2009; 8:88.
3. Doxsey S, Zimmerman W, Mikule K. Centrosome control of the cell cycle. Trends Cell Biol 2005; 15:303-11.
4. Sluder G. Two-way traffic: Centrosomes and the cell cycle. Nat Rev Mol Cell Biol 2005; 6:743-8.
5. Boveri T. Zur Frage der Entstehung maligner Tumoren. Gustav Fischer Verlag, Jena 1914.
6. Gergely F, Basto R. Multiple centrosomes: Together they stand, divided they fall. Genes Dev 2008; 22:2291-6.
7. Weaver BA, Silk AD, Montagna C, Verdier-Pinard P, Cleveland DW. Aneuploidy acts both oncogenically and as a tumor suppressor. Cancer Cell 2007; 11:25-36.
8. Basto R, Brunk K, Vinadogrova T, Peel N, Franz A, Khodjakov A, et al. Centrosome amplification can initiate tumorigenesis in flies. Cell 2008; 133:1032-42.
9. Castellanos E, Dominguez P, Gonzalez C. Centrosome dysfunction in Drosophila neural stem cells causes tumors that are not due to genome instability. Curr Biol 2008; 18:1209-14.
10. Klonisch T, Wiechec E, Hombach-Klonisch S, Ande SR, Wesselborg S, Schulze-Osthoff K, et al. Cancer stem cell markers in common cancers: Therapeutic implications. Trends Mol Med 2008; 14:450-60.
11. Zyss D, Gergely F. Centrosome function in cancer: guilty or innocent? Trends Cell Biol 2009; 19:334-46.
12. Gergely F. Centrosomal TACCtics. Bioessays 2002; 24:915-25.
13. Peset I, Vernos I. The TACC proteins: TACC-ling microtubule dynamics and centrosome function. Trends Cell Biol 2008; 18:379-88.
14. Gomez-Baldo L, Schmidt S, Maxwell CA, Bonifaci N, Gabaldon T, Vidalain PO, et al. TACC3-TSC2 maintains nuclear envelope structure and controls cell division. Cell Cycle 2010; 9:1143-55.
15. Samereier M, Baumann O, Meyer I, Graf R. Analysis of Dictyostelium TACC reveals differential interactions with CP224 and unusual dynamics of Dictyostelium microtubules. Cell Mol Life Sci 2010; In press.
16. Still IH, Vettaikkorumakankauv AK, DiMatteo A, Liang P. Structure-function evolution of the transforming acidic coiled coil genes revealed by analysis of phylogenetically diverse organisms. BMC Evol Biol 2004; 4:16.
17. Cassimeris L, Morabito J. TOGp, the human homolog of XMAP215/Dis1, is required for centrosome integrity, spindle pole organization and bipolar spindle assembly. Mol Biol Cell 2004; 15:1580-90.
18. Gergely F, Draviam VM, Raff JW. The ch-TOG/ XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev 2003; 17:336-41.
19. Schneider L, Essmann F, Kletke A, Rio P, Hanenberg H, Wetzel W, et al. The transforming acidic coiled coil 3 protein is essential for spindle-dependent chromosome alignment and mitotic survival. J Biol Chem 2007; 282:29273-83.
20. Yao R, Natsume Y, Noda T. TACC3 is required for the proper mitosis of sclerotome mesenchymal cells during formation of the axial skeleton. Cancer Sci 2007; 98:555-62.
21. Hubner NC, Bird AW, Cox J, Splettstoesser B, Bandilla P, Poser I, et al. Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J Cell Biol 189:739-54.
22. Kinoshita K, Noetzel TL, Pelletier L, Mechtler K, Drechsel DN, Schwager A, et al. Aurora A phosphorylation of TACC3/maskin is required for centrosome- dependent microtubule assembly in mitosis. J Cell Biol 2005; 170:1047-55.
23. LeRoy PJ, Hunter JJ, Hoar KM, Burke KE, Shinde V, Ruan J, et al. Localization of human TACC3 to mitotic spindles is mediated by phosphorylation on Ser558 by Aurora A: a novel pharmacodynamic method for measuring Aurora A activity. Cancer Res 2007; 67:5362-70.
24. Lin CH, Hu CK, Shih HM. Clathrin heavy chain mediates TACC3 targeting to mitotic spindles to ensure spindle stability. J Cell Biol 189:1097-105.
25. Piekorz RP, Hoffmeyer A, Duntsch CD, McKay C, Nakajima H, Sexl V, et al. The centrosomal protein TACC3 is essential for hematopoietic stem cell function and genetically interfaces with p53-regulated apoptosis. EMBO J 2002; 21:653-64.
26. Still IH, Hamilton M, Vince P, Wolfman A, Cowell JK. Cloning of TACC1, an embryonically expressed, potentially transforming coiled coil containing gene, from the 8p11 breast cancer amplicon. Oncogene 1999; 18:4032-8.
27. Still IH, Vince P, Cowell JK. The third member of the transforming acidic coiled coil-containing gene family, TACC3, maps in 4p16, close to translocation breakpoints in multiple myeloma, and is upregulated in various cancer cell lines. Genomics 1999; 58:165-70.
28. Cully M, Shiu J, Piekorz RP, Muller WJ, Done SJ, Mak TW. Transforming acidic coiled coil 1 promotes transformation and mammary tumorigenesis. Cancer Res 2005; 65:10363-70.
29. Jung CK, Jung JH, Park GS, Lee A, Kang CS, Lee KY. Expression of transforming acidic coiled-coil containing protein 3 is a novel independent prognostic marker in non-small cell lung cancer. Pathol Int 2006; 56:503-9.
30. Kiemeney LA, Sulem P, Besenbacher S, Vermeulen SH, Sigurdsson A, Thorleifsson G, et al. A sequence variant at 4p16.3 confers susceptibility to urinary bladder cancer. Nat Genet 2010; 42:415-9.
31. Lauffart B, Vaughan MM, Eddy R, Chervinsky D, DiCioccio RA, Black JD, et al. Aberrations of TACC1 and TACC3 are associated with ovarian cancer. BMC Womens Health 2005; 5:8.
32. Duncan CG, Killela PJ, Payne CA, Lampson B, Chen WC, et al. Integrated genomic analyses identify ERRFl1 and TACC3 as glioblastoma-targeted genes. Oncotarget 2010; 1:265-77.
33. Hayflick L, Moorhead PS. The serial cultivation of human diploid cell strains. Exp Cell Res 1961; 25:585-621.
34. Campisi J, d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 2007; 8:729-40.
35. Ben-Porath I, Weinberg RA. The signals and pathways activating cellular senescence. Int J Biochem Cell Biol 2005; 37:961-76.
36. Collado M, Serrano M. The power and the promise of oncogene-induced senescence markers. Nat Rev Cancer 2006; 6:472-6.
37. Chuaire-Noack L, et al. The dual role of senescence in tumorigenesis. Int J Morphol 2010; 28:37-50.
38. Demidenko ZN, Blagosklonny MV. Growth stimulation leads to cellular senescence when the cell cycle is blocked. Cell Cycle 2008; 7:3355-61.
39. Demidenko ZN, Zubova SG, Bukreeva EI, Pospelov VA, Pospelova TV, Blagosklonny MV. Rapamycin decelerates cellular senescence. Cell Cycle 2009; 8:1888-95.
40. Korotchkina LG, Leontieva OV, Bukreeva EI, Demidenko ZN, Gudkov AV, Blagosklonny MV. The choice between p53-induced senescence and quiescence is determined in part by the mTOR pathway. Aging (Albany NY) 2:344-52.
41. Demidenko ZN, Korotchkina LG, Gudkov AV, Blagosklonny MV. Paradoxical suppression of cellular senescence by p53. Proc Natl Acad Sci USA 107:9660-4.
42. Blagosklonny MV. Prolonged mitosis versus tetraploid checkpoint: how p53 measures the duration of mitosis. Cell Cycle 2006; 5:971-5.
43. Schneider L, Essmann F, Kletke A, Rio P, Hanenberg H, Schulze-Osthoff K, et al. TACC3 depletion sensitizes to paclitaxel-induced cell death and over-rides p21(WAF)-mediated cell cycle arrest. Oncogene 2008; 27:116-25.
44. Schmidt S, Schneider L, Essmann F, Cirstea IC, Kuck F, Kletke A, et al. The centrosomal protein TACC3 controls paclitaxel sensitivity by modulating a premature senescence program. Oncogene 2010; DOI:10.1038/onc.2010.354.
45. Huck JJ, Zhang M, McDonald A, Bowman D, Hoar KM, Stringer B, et al. MLN8054, an inhibitor of Aurora A kinase, induces senescence in human tumor cells both in vitro and in vivo. Mol Cancer Res 2010; 8:373-84.
46. Katayama H, Sasai K, Kawai H, Yuan ZM, Bondaruk J, Suzuki F, et al. Phosphorylation by aurora kinase A induces Mdm2-mediated destabilization and inhibition of p53. Nat Genet 2004; 36:55-62.
47. Dominguez-Brauer C, Brauer PM, Chen YJ, Pimkina J, Raychaudhuri P. Tumor suppression by ARF: Gatekeeper and caretaker. Cell Cycle 9:86-9.
48. Tritarelli A, Oricchio E, Ciciarello M, Mangiacasale R, Palena A, Lavia P, et al. p53 localization at centrosomes during mitosis and postmitotic checkpoint are ATM-dependent and require serine 15 phosphorylation. Mol Biol Cell 2004; 15:3751-7.
49. Vogel C, Kienitz A, Hofmann I, Muller R, Bastians H. Crosstalk of the mitotic spindle assembly check-point with p53 to prevent polyploidy. Oncogene 2004; 23:6845-53.
50. Gjoerup OV, Wu J, Chandler-Militello D, Williams GL, Zhao J, Schaffhausen B, et al. Surveillance mechanism linking Bub1 loss to the p53 pathway. Proc Natl Acad Sci USA 2007; 104:8334-9.
51. Maehara K, Takahashi K, Saitoh S. CENP-A reduction induces a p53-dependent cellular senescence response to protect cells from executing defective mitoses. Mol Cell Biol 2010; 30:2090-104.
52. Baker DJ, Jeganathan KB, Cameron JD, Thompson M, Juneja S, Kopecka A, et al. BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat Genet 2004; 36:744-9.
53. Baker DJ, Jeganathan KB, Malureanu L, Perez-Terzic C, Terzic A, van Deursen JM. Early aging-associated phenotypes in Bub3/Rae1 haploinsufficient mice. J Cell Biol 2006; 172:529-40.
54. Baker DJ, Chen J, van Deursen JM. The mitotic checkpoint in cancer and aging: What have mice taught us? Curr Opin Cell Biol 2005; 17:583-9.
55. Campisi J, Sedivy J. How does proliferative homeostasis change with age? What causes it and how does it contribute to aging? J Gerontol A Biol Sci Med Sci 2009; 64:164-6.
56. Jeyapalan JC, Ferreira M, Sedivy JM, Herbig U. Accumulation of senescent cells in mitotic tissue of aging primates. Mech Ageing Dev 2007; 128:36-44.
57. Yang D, McCrann DJ, Nguyen H, St. Hilaire C, DePinho RA, Jones MR, et al. Increased polyploidy in aortic vascular smooth muscle cells during aging is marked by cellular senescence. Aging Cell 2007; 6:257-60.
58. Görgün G, Calabrese E, Hideshima T, Ecsedy J, Perrone G, Mani M, et al. A novel Aurora-A kinase inhibitor MLN8237 induces cytotoxicity and cell cycle arrest in multiple myeloma. Blood 2010; 115:5202-13.
59. Prencipe M, Fitzpatrick P, Gorman S, Tosetto M, Klinger R, Furlong F, et al. Cellular senescence induced by aberrant MAD2 levels impacts on paclitaxel responsiveness in vitro. Br J Cancer 2009; 101:1900-8.
60. comet Induces cellular senescence through p21 accumulation and Mad2 disruption. Mol Cancer Res 2009; 7:371-82.
61. 1-S arrest. Nat Cell Biol 2007; 9:160-70.
62. Srsen V, Gnadt N, Dammermann A, Merdes A. Inhibition of centrosome protein assembly leads to p53-dependent exit from the cell cycle. J Cell Biol 2006; 174:625-30.