Human embryonic stem cells suffer from centrosomal amplification

Stem Cells

Volumn 29, Issue 1, 2011, Pages 46-56

  Holubcová, Zuzana ^a   Matula, Pavel ^a   Sedláčková, Miroslava ^a   Vinarský, Vladimír ^a,b   Doležalová, Dáša ^a,b   Bárta, Tomáš ^a,b   Dvořák, Petr ^a,b   Hampl, Aleš ^a,b  

^a MASARYK UNIVERSITY   (Czech Republic)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

Author keywords

Aurora A; CDK; Centrosome; Chromosome; Genomic instability; Human embryonic stem cells

Indexed keywords

AURORA A KINASE; CYCLIN DEPENDENT KINASE 2;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL CYCLE; CELL DIFFERENTIATION; CENTROSOME; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; MITOSIS; MOUSE; NONHUMAN; PLOIDY; REGULATORY MECHANISM; RISK FACTOR; STEM CELL EXPANSION;

ANEUPLOIDY; CELL DIFFERENTIATION; CELL LINE; CENTROSOME; CHROMOSOMAL INSTABILITY; CYCLIN-DEPENDENT KINASE 2; EMBRYONIC STEM CELLS; HUMANS; MITOSIS; PROTEIN-SERINE-THREONINE KINASES;

EID: 79951816916     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.549     Document Type: Article

References (61)

1. Blum B, Benvenisty N. The tumorigenicity of diploid and aneuploid human pluripotent stem cells. Cell Cycle 2009;8:3822-3830.
2. Draper JS, Smith K, Gokhale P et al. Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat Biotechnol 2004;22:53-54. (Pubitemid 38057956)
3. Maitra A, Arking DE, Shivapurkar N et al. Genomic alterations in cultured human embryonic stem cells. Nat Genet 2005;37:1099-1103. (Pubitemid 41486662)
4. Mitalipova MM, Rao RR, Hoyer DM et al. Preserving the genetic integrity of human embryonic stem cells. Nat Biotechnol 2005;23:19-20. (Pubitemid 41724618)
5. Schvartzman J, Sotillo R, Benezra R. Mitotic chromosomal instability and cancer: Mouse modelling of the human disease. Nat Rev Cancer 2010;10:102-115.
6. D'Assoro AB, Barrett SL, Folk C et al. Amplified centrosomes in breast cancer: A potential indicator of tumor aggressiveness. Breast Cancer Res Treat 2002;75:25-34.
7. Pihan GA, Wallace J, Zhou Y et al. Centrosome abnormalities and chromosome instability occur together in pre-invasive carcinomas. Cancer Res 2003;63:1398-1404. (Pubitemid 36348723)
8. Chng WJ, Braggio E, Mulligan G et al. The centrosome index is a powerful prognostic marker in myeloma and identifies a cohort of patients that might benefit from aurora kinase inhibition. Blood 2008;111:1603-1609. (Pubitemid 351213451)
9. Alieva IB, Uzbekov RE. The centrosome is a polyfunctional multiprotein cell complex. Biochemistry (Mosc) 2008;73:626-643. (Pubitemid 351931560)
10. Meraldi P, Nigg EA. The centrosome cycle. FEBS Lett 2002;521:9-13. (Pubitemid 34628448)
11. Nigg EA. Centrosome duplication: Of rules and licenses. Trends Cell Biol 2007;17:215-221. (Pubitemid 46679244)
12. Rusan NM, Rogers GC. Centrosome function: Sometimes less is more. Traffic 2009;10:472-481.
13. Schatten H. The mammalian centrosome and its functional significance. Histochem Cell Biol 2008;129:667-686.
14. Ganem NJ, Godinho SA, Pellman D. A mechanism linking extra centrosomes to chromosomal instability. Nature 2009;460:278-282.
15. Silkworth WT, Nardi IK, Scholl LM et al. Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome mis-segregation in cancer cells. Plos One 2009;4:e6564.
16. Adewumi O, Aflatoonian B, Ahrlund-Richter L et al. Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol 2007;25:803-816. (Pubitemid 47052190)
17. Manfredi MG, Ecsedy JA, Meetze KA et al. Antitumor activity of MLN8054, an orally active small-molecule inhibitor of Aurora A kinase. Proc Natl Acad Sci USA 2007;104:4106-4111. (Pubitemid 47181586)
18. Krystof V, McNae IW, Walkinshaw MD et al. Antiproliferative activity of olomoucine II, a novel 2,6,9-trisubstituted purine cyclin-dependent kinase inhibitor. Cell Mol Life Sci 2005;62:1763-1771.
19. Frelinger AL, Du XP, Plow EF et al. Monoclonal antibodies to ligand-occupied conformers of integrin alpha IIb beta 3 (glycoprotein IIb-IIIa) alter receptor affinity, specificity, and function. J Biol Chem 1991;266:17106-17111. (Pubitemid 21907912)
20. Reverte CG, Benware A, Jones CW et al. Perturbing integrin function inhibits microtubule growth from centrosomes, spindle assembly, and cytokinesis. J Cell Biol 2006;174:491-497. (Pubitemid 44231861)
21. Matula P, Maška M, Danek O et al. Software for the Acquisition and Analysis of 3D Images of Cells in Fluorescence Microscopy: Proceedings of the IEEE International Symposium on Biomedical Imaging, Boston, IEEE New York. 2009:1138-1141. Available at http://cbia.fi.muni.cz/acquiarium/.
22. Lingle WL, Salisbury JL. Altered centrosome structure is associated with abnormal mitoses in human breast tumors. Am J Pathol 1999;155:1941-1951.
23. Baker DEC, Harrison NJ, Maltby E et al. Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat Biotechnol 2007;25:207-215.
24. Amit M, Shariki C, Margulets V et al. Feeder layer- and serum-free culture of human embryonic stem cells. Biol Reprod 2004;70:837-845. (Pubitemid 38233724)
25. Draper JS, Moore HD, Ruban LN et al. Culture and characterization of human embryonic stem cells. Stem Cells Dev 2004;13:325-336. (Pubitemid 39223282)
26. Xu C, Inokuma MS, Denham J et al. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 2001;19:971-974. (Pubitemid 32947578)
27. Guarguaglini G, Duncan PI, Stierhof YD et al. The forkhead-associated domain protein Cep170 interacts with Polo-like kinase 1 and serves as a marker for mature centrioles. Mol Biol Cell 2005;16:1095-1107. (Pubitemid 40349548)
28. Meraldi P, Honda R, Nigg EA. Aurora-A overexpression reveals tetraploidization as a major route to centrosome amplification in p53-/- cells. EMBO J 2002;21:483-492. (Pubitemid 34174030)
29. Katayama H, Brinkley WR, Sen S. The Aurora kinases: Role in cell transformation and tumorigenesis. Cancer Metastasis Rev 2003;22:451-464. (Pubitemid 36791899)
30. Yamamoto Y, Eguchi S, Junpei A et al. Intercellular centrosome number is correlated with the copy number of chromosomes in bladder cancer. Cancer Genet Cytogenet 2009;191:38-42.
31. Lingle WL, Lukasiewicz K, Salisbury JL. Deregulation of the centrosome cycle and the origin of chromosomal instability in cancer. Adv Exp Med Biol 2005;570:393-421. (Pubitemid 47413181)
32. Fukasawa K. Centrosome amplification, chromosome instability and cancer development. Cancer Lett 2005;230:6-19. (Pubitemid 41506955)
33. Zyss D, Gergely F. Centrosome function in cancer: Guilty or innocent? Trends Cell Biol 2009;19:334-346.
34. Rebollo E, Sampaio P, Januschke J et al. Functionally unequal centrosomes drive spindle orientation in asymmetrically dividing Drosophila neural stem cells. Dev Cell 2007;12:467-474.
35. Rusan NM, Peifer M. A role for a novel centrosome cycle in asymmetric cell division. J Cell Biol 2007;177:13-20. (Pubitemid 46588397)
36. Yamashita YM, Mahowald AP, Perlin JR et al. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 2007;315:518-521. (Pubitemid 46175756)
37. Wang X, Tsai J, Imai JH et al. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 2009;461:947-955.
38. Mantel C, Guo Y, Lee MR et al. Checkpoint-apoptosis uncoupling in human and mouse embryonic stem cells: A source of karyotypic instability. Blood 2007;109:4518-4527. (Pubitemid 46743423)
39. Fukasawa K. P53, cyclin-dependent kinase and abnormal amplification of centrosomes. Biochim Biophys Acta 2008;1786:15-23.
40. Fukasawa K, Choi T, Kuriyama R et al. Abnormal centrosome amplification in the absence of p53. Science 1996;271:1744-1747. (Pubitemid 26102826)
41. Bárta T, Vinarský V, Holubcová Z et al. Human embryonic stem cells are capable of executing G1/S checkpoint activation. Stem Cells 2010; 28:1143-1152.
42. Pugacheva EN, Roegiers F, Golemis EA. Interdependence of cell attachment and cell cycle signaling. Curr Opin Cell Biol 2006;18:507-515. (Pubitemid 44332913)
43. Zhou H, Kuang J, Zhong L et al. Tumour amplified kinase STK15/ BTAK induces centrosome amplification, aneuploidy and transformation. Nat Genet 1998;20:189-193. (Pubitemid 28455454)
44. Bischoff JR, Anderson L, Zhu Y et al. A homologue of Drosophila aurora kinase is oncogenic and amplified in human colorectal cancers. EMBO J 1998;17:3052-3065. (Pubitemid 28254378)
45. Liu Q, Ruderman JV. Aurora A, mitotic entry, and spindle bipolarity. Proc Natl Acad Sci USA 2006;103:5811-5816.
46. Sasayama T, Marumoto T, Kunitoku N et al. Over-expression of Aurora- A targets cytoplasmic polyadenylation element binding protein and promotes mRNA polyadenylation of Cdk1 and cyclin B1. Genes Cells 2005;10:627-638. (Pubitemid 40932344)
47. Hinchcliffe EH, Li C, Thompson EA et al. Requirement of Cdk2-cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science 1999;283:851-854.
48. Meraldi P, Lukas J, Fry AM et al. Centrosome duplication in mammalian somatic cells requires E2F and Cdk2-cyclin A. Nat Cell Biol 1999;1:88-93. (Pubitemid 129501949)
49. Lacey KR, Jackson PK, Stearns T. Cyclin-dependent kinase control of centrosome duplication. Proc Natl Acad Sci USA 1999;96:2817-2822. (Pubitemid 29148801)
50. Balczon R, Bao L, Zimmer WE et al. Dissociation of centrosome replication events from cycles of DNA synthesis and mitotic division in hydroxyurea-arrested Chinese hamster ovary cells. J Cell Biol 1995;130:105-115.
51. Mussman JG, Horn HF, Carroll PE et al. Synergistic induction of centrosome hyperamplification by loss of p53 and cyclin E overexpression. Oncogene 2000;19:1635-1646. (Pubitemid 30200965)
52. Stead E, White J, Faast R et al. Pluripotent cell division cycles are driven by ectopic Cdk2, cyclin A/E and E2F activities. Oncogene 2002;21:8320-8333. (Pubitemid 35477872)
53. Catalina P, Montes R, Ligero G et al. Human ESCs predisposition to karyotypic instability: Is a matter of culture adaptation or differential vulnerability among hESC lines due to inherent properties? Mol Cancer 2008;7:76-84.
54. Fabarius A, Giehl M, Frank O et al. Induction of centrosome and chromosome aberrations by imatinib in vitro. Leukemia 2005;19:1573-1578. (Pubitemid 43090401)
55. Giehl M, Fabarius A, Frank O et al. Centrosome aberrations in chronic myeloid leukemia correlate with stage of disease and chromosomal instability. Leukemia 2005;19:1192-1197. (Pubitemid 40946003)
56. Hsu L, Kapali M, DeLoia JA et al. Centrosome abnormalities in ovarian cancer. Int J Cancer 2005;113:746-751. (Pubitemid 40101255)
57. Giehl M, Leitner A, Haferlach C et al. Detection of centrosome aberrations in disease-unrelated cells from patients with tumor treated with tyrosine kinase inhibitors. Eur J Haematol 2010;85:139-148.
58. Heim S, Mandahl N, Mitelman F. Genetic convergence and divergence in tumor progression. Cancer Res 1988;48:5911-5916. (Pubitemid 18266774)
59. Quintyne NJ, Reing JE, Hoffelder DR et al. Spindle multipolarity is prevented by centrosomal clustering. Science 2005;307:127-129. (Pubitemid 40093495)
60. Basto R, Brunk K, Vinadogrova T et al. Centrosome amplification can initiate tumorigenesis in flies. Cell 2008;133:1032-1042. (Pubitemid 351787756)
61. Quyn AJ, Appleton PL, Carey FA et al. Spindle orientation bias in gut epithelial stem cell compartments is lost in precancerous tissue. Cell Stem Cell 2010;6:175-181.