The Centrosome pp 285-305 | Cite as

Mechanisms and Consequences of Centrosome Clustering in Cancer Cells

Chapter

Abstract

Ever since initially proposed by Theodor Boveri in 1914, centrosome abnormalities have been accused to be involved in the induction of chromosomal instability and tumorigenesis. New evidence especially on a mechanism termed centrosomal clustering now again supports Boveri's idea and adds fuel to the old debate on a mechanistic link between supernumerary centrosomes and malignant transformation. On top, inhibiting centrosome clustering might well turn out to be one of the long sought after possibilities to specifically interfere with tumor cells while leaving healthy tissues untouched.

Keywords

Spindle Pole Spindle Assembly Checkpoint Centrosome Amplification Centrosome Duplication Stem Cell Division 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgment

We apologize to those authors whose work is not cited because of space limitations. This work was supported by the Deutsche Forschungsgemeinschaft, the Deutsche Krebshilfe, the Deutsche José Carreras Leukämie-Stiftung and the Interdisciplinary Research Program of the National Center for Tumor Diseases Heidelberg.

References

  1. Adams RR et al (2001) Human INCENP colocalizes with the Aurora-B/AIRK2 kinase on chromosomes and is overexpressed in tumour cells. Chromosoma 110:65–74PubMedGoogle Scholar
  2. Altieri DC (2003) Survivin, versatile modulation of cell division and apoptosis in cancer. Oncogene 22:8581–8589PubMedGoogle Scholar
  3. Anderhub SJ, Krämer A, Maier B (2012) Centrosome amplification in tumorigenesis. Cancer Lett. 322:8–17Google Scholar
  4. Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, Mann M (2003) Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426:570–574PubMedGoogle Scholar
  5. Arquint C, Sonnen KF, Stierhof YD, Nigg EA (2012) Cell cycle-regulated expression of STIL controls centriole numbers in human cells. J Cell Sci 125:1342–1452PubMedGoogle Scholar
  6. Baker DJ, Jin F, Jeganathan KB, van Deursen JM (2009) Whole chromosome instability caused by Bub1 insufficiency drives tumorigenesis through tumor suppressor gene loss of heterozygosity. Cancer Cell 16:475–486PubMedGoogle Scholar
  7. Barr FA, Sillje HH, Nigg EA (2004) Polo-like kinases and the orchestration of cell division. Nat Rev Mol Cell Biol 5:429–440PubMedGoogle Scholar
  8. Basto R et al (2008) Centrosome amplification can initiate tumorigenesis in flies. Cell 133:1032–1042PubMedGoogle Scholar
  9. Bettencourt-Dias M et al (2005) SAK/PLK4 is required for centriole duplication and flagella development. Curr Biol 15:2199–2207PubMedGoogle Scholar
  10. Birkbak NJ et al. (2011) Paradoxical relationship between chromosomal instability and survival outcome in cancer. Cancer Res. (epub ahead of print)Google Scholar
  11. Bischoff JR et al (1998) A homologue of Drosophila aurora kinase is oncogenic and amplified in human colorectal cancers. EMBO J 17:3052–3065PubMedGoogle Scholar
  12. Bornens M (2002) Centrosome composition and microtubule anchoring mechanisms. Curr Opin Cell Biol 14:25–34PubMedGoogle Scholar
  13. Boveri T (1929) The origin of malignant tumors. Williams and Wilkins, BaltimoreGoogle Scholar
  14. Boyarchuk Y, Salic A, Dasso M, Arnaoutov A (2007) Bub1 is essential for assembly of the functional inner centromere. J Cell Biol 176:919–928PubMedGoogle Scholar
  15. Breuer M et al (2010) HURP permits MTOC sorting for robust meiotic spindle bipolarity, similar to extra centrosome clustering in cancer cells. J Cell Biol 191:1251–1260PubMedGoogle Scholar
  16. Brinkley BR (2001) Managing the centrosome numbers game: from chaos to stability in cancer cell division. Trends Cell Biol 11:18–21PubMedGoogle Scholar
  17. Brito DA, Rieder CL (2009) The ability to survive mitosis in the presence of microtubule poisons differs significantly between human nontransformed (RPE-1) and cancer (U2OS, HeLa) cells. Cell Motil. Cytoskeleton 66:437–447PubMedGoogle Scholar
  18. Carmena M, Earnshaw WC (2003) The cellular geography of aurora kinases. Nat Rev Mol Cell Biol 4:842–854PubMedGoogle Scholar
  19. Carter SL et al (2006) A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nat Genet 38:1043–1048PubMedGoogle Scholar
  20. Castellanos E, Dominguez P, Gonzalez C (2008) Centrosome dysfunction in Drosophila neural stem cell causes tumors that are not due to genome instability. Curr Biol 18:1209–1214PubMedGoogle Scholar
  21. Castiel A, Visochek L, Mittelman L, Dantzer F, Izraeli S, Cohen-Armon M (2011) A phenanthrene derived PARP inhibitor is an extra-centrosomes de-clustering agent exclusively eradicating human cancer cells. BMC Cancer 11:412PubMedGoogle Scholar
  22. Caussinus E, Gonzalez C (2005) Induction of tumor growth by altered stem-cell asymmetric division in Drosophila melanogaster. Nat Genet 37:1125–1129PubMedGoogle Scholar
  23. Chang P, Jacobson MK, Mitchison TJ (2004) Poly(ADP-ribose) is required for spindle assembly and structure. Nature 432:645–649PubMedGoogle Scholar
  24. Chang JL et al (2006) Borealin/Dasra B is a cell cycle-regulated chromosomal passenger protein and its nuclear accumulation is linked to poor prognosis for human gastric cancer. Exp Cell Res 312:962–973PubMedGoogle Scholar
  25. Charrasse S et al (1995) Characterization of the cDNA and pattern of expression of a new gene over-expressed in human hepatomas and colonic tumors. Eur J Biochem 234:406–413PubMedGoogle Scholar
  26. Chen JG, Horwitz SB (2002) Differential mitotic responses to microtubule-stabilizing and -destabilizing drugs. Cancer Res 62:1935–1938PubMedGoogle Scholar
  27. Cizmecioglu O, Arnold M, Bahtz R, Settele F, Ehret L, Haselmann-Weiss U, Antony C, Hoffmann I (2010) Cep152 acts as a scaffold for recruitment of Plk4 and CPAP to the centrosome. J Cell Biol 191:731–739PubMedGoogle Scholar
  28. Dai J, Kataneva AV, Higgins JMG (2009) Studies of haspin-depleted cells reveal that spindle-pole integrity in mitosis requires chromosome cohesion. J Cell Sci 122:4168–4176PubMedGoogle Scholar
  29. De S, Cipriano R, Jackson MW, Stark GR (2009) Overexpression of kinesins mediates docetaxel resistance in breast cancer cells. Cancer Res 69:8035–8042PubMedGoogle Scholar
  30. Diaz-Rodriguez E, Sotillo R, Schvartzman J-M, Benezra R (2008) Hec1 overexpression hyperactivates the mitotic checkpoint and induces tumor formation in vivo. Proc. Natl. Acad. Sci. USA 105:16719–16724PubMedGoogle Scholar
  31. Doxsey SJ, Stein P, Evans L, Calarco PD, Kirschner M (1994) Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 76:639–650PubMedGoogle Scholar
  32. Duncan AW et al (2010) The ploidy conveyor of mature hepatocytes as a source of genetic variation. Nature 467:707–711PubMedGoogle Scholar
  33. Dzhindzhev NS et al (2010) Asterless is a scaffold for the onset of centriole assembly. Nature 467:714–718PubMedGoogle Scholar
  34. Einarson MB, Cukierman E, Compton DA, Golemis EA (2004) Human enhancer of invasion-cluster, a coiled-coil protein required for passage through mitosis. Mol Cell Biol 24:3957–3971PubMedGoogle Scholar
  35. Epstein SS, Andrea J, Joshi S, Mantel N (1967) Hepatocarcinogenicity of griseofulvin following parenteral administration to infant mice. Cancer Res 27:1900–1906PubMedGoogle Scholar
  36. Ferguson RL, Maller JL (2010) Centrosomal localization of cyclin E-Cdk2 is required for initiation of DNA synthesis. Curr Biol 20:856–860PubMedGoogle Scholar
  37. Ferretti C et al (2010) Expression of the kinetochore protein Hec1 during the cell cycle in normal and cancer cells and its regulation by the pRb pathway. Cell Cycle 9:4147–4182Google Scholar
  38. Fielding AB, Lim S, Montgomery K, Dobreva I, Dedhar S (2011) A critical role of integrin-linked kinase, ch-TOG and TACC3 in centrosome clustering in cancer cells. Oncogene 30:521–534PubMedGoogle Scholar
  39. Fukasawa K (2007) Oncogenes and tumour suppressors take on centrosomes. Nat Rev Cancer 7:911–924PubMedGoogle Scholar
  40. Ganem NJ, Godinho SA, Pellman D (2009) A mechanism linking extra centrosomes to chromosomal instability. Nature 460:278–282PubMedGoogle Scholar
  41. Gould RR, Borisy GG (1977) The pericentriolar material in Chinese hamster ovary cells nucleates microtubule formation. J Cell Biol 73:601–615PubMedGoogle Scholar
  42. Grinberg-Rashi H et al (2009) The expression of three genes in primary non-small cell lung cancer is associated with metastatic spread to the brain. Clin Cancer Res 15:1755–1761PubMedGoogle Scholar
  43. Grisham LM, Wilson L, Bensch KG (1973) Antimitotic action of griseofulvin does not involve disruption of microtubules. Nature 244:294–296PubMedGoogle Scholar
  44. Guidotti J-E et al (2003) Liver cell polyploidization: a pivotal role for binuclear hepatocytes. J Biol Chem 278:19095–19101PubMedGoogle Scholar
  45. Gull K, Trinci APJ (1973) Griseofulvin inhibits fungal mitosis. Nature 244:292–294PubMedGoogle Scholar
  46. Habedanck R, Stierhof YD, Wilkinson CJ, Nigg EA (2005) The Polo kinase Plk4 functions in centriole duplication. Nat Cell Biol 7:1140–1146PubMedGoogle Scholar
  47. Hannigan G, Troussard AA, Dedhar S (2005) Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat Rev Cancer 5:51–63PubMedGoogle Scholar
  48. Hatch EM, Kulukian A, Holland AJ, Cleveland DW, Stearns T (2010) Cep152 interacts with Plk4 and is required for centriole duplication. J Cell Biol 191:721–729PubMedGoogle Scholar
  49. Hayama S et al (2006) Activation of CDCA1-KNTC2, members of centromere protein complex, involved in pulmonary carcinogenesis. Cancer Res 66:10339–10348PubMedGoogle Scholar
  50. Hori T et al (2008) CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell 135:1039–1052PubMedGoogle Scholar
  51. Huang H et al (2007) Tripin/hSgo2 recruits MCAK to the inner centromere to correct defective kinetochore attachments. J Cell Biol 177:413–424PubMedGoogle Scholar
  52. Hung LY, Chen HL, Chang CW, Li BR, Tang TK (2004) Identification of a novel microtubule-destabilizing motif in CPAP that binds to tubulin heterodimers and inhibits microtubule assembly. Mol Biol Cell 15:2697–2706PubMedGoogle Scholar
  53. Indjeian VB, Stern BM, Murray AW (2005) The centromeric protein Sgo1 is required to sense lack of tension on mitotic chromosomes. Science 307:130–133PubMedGoogle Scholar
  54. Ishikawa K et al (2008) Mitotic centromere-associated kinesin is a novel marker for prognosis and lymph node metastasis in colorectal cancer. Br J Cancer 98:1824–1829PubMedGoogle Scholar
  55. Jackman M, Lindon C, Nigg EA, Pines J (2003) Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nat Cell Biol 5:143–148PubMedGoogle Scholar
  56. Kalra J et al (2009) QLT0267, a small molecule inhibitor targeting integrin-linked kinase (ILK), and docetaxel can combine to produce synergistic interactions linked to enhanced cytotoxicity, reductions in P-AKT levels, altered F-actin architecture and improved treatment outcomes in an orthotopic breast cancer model. Breast Cancer Res 11:R25PubMedGoogle Scholar
  57. Kanai M, Tong W-M, Sugihara E, Wang Z-Q, Fukasawa K, Miwa M (2003) Involvement of poly(ADP-ribose) polymerase 1 and poly(ADP-ribosyl)ation in regulation of centrosome function. Mol Cell Biol 23:2451–2462PubMedGoogle Scholar
  58. Karna P et al (2011) A novel microtubule-modulating noscapinoid triggers apoptosis by inducing spindle multipolarity via centrosome amplification and declustering. Cell Death Differ 18:632–644PubMedGoogle Scholar
  59. Kawashima SA, Tsukahara T, Langegger M, Hauf S, Kitajima TS, Watanabe Y (2007) Shugoshin enables tension-generating attachment of kinetochores by loading Aurora to centromeres. Genes Dev 21:420–435PubMedGoogle Scholar
  60. Kawashima SA, Yamagishi Y, Honda T, Ishiguro K, Watanabe Y (2010) Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science 327:172–177PubMedGoogle Scholar
  61. Kelly AE, Ghenoiu C, Xue JZ, Zierhut C, Kimura H, Funabiki H (2010) Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase aurora B. Science 330:235–239PubMedGoogle Scholar
  62. Kitagawa D, Kohlmaier G, Keller D, Strnad P, Balestra FR, Fluckiger I, Gönczy P (2011) Spindle positioning in human cells relies on proper centriole formation and on the microcephaly proteins CPAP and STIL. J Cell Sci 124:3884–3893PubMedGoogle Scholar
  63. Kleylein-Sohn J, Westendorf J, Le Clech M, Habedanck R, Stierhof YD, Nigg EA (2007) Plk4-induced centriole biogenesis in human cells. Dev Cell 13:190–202PubMedGoogle Scholar
  64. Koffa MD, Casanova CM, Santarella R, Kocher T, Wilm M, Mattaj IW (2006) HURP is part of a Ran-dependent complex involved in spindle formation. Curr Biol 16:743–754PubMedGoogle Scholar
  65. Kops GJ, Foltz DR, Cleveland DW (2004) Lethality to human cancer cells through massive chromosome loss by inhibition of the mitotic checkpoint. Proc. Natl. Acad. Sci. USA 101:8699–8704PubMedGoogle Scholar
  66. Koutsami MK et al (2006) Centrosome abnormalities are frequently observed in non-small-cell lung cancer and are associated with aneuploidy and cyclin E overexpression. J. Pathol. 209:512–521PubMedGoogle Scholar
  67. Krämer A, Neben K, Ho AD (2002) Centrosome replication, genomic instability and cancer. Leukemia 16:767–775PubMedGoogle Scholar
  68. Krämer A et al (2003) Centrosome aberrations as a possible mechanism for chromosomal instability in non-Hodgkin’s lymphoma. Leukemia 17:2207–2213PubMedGoogle Scholar
  69. Kuriyama R, Borisy GG (1981) Centriole cycle in Chinese hamster ovary cells as determined by whole-mount electron microscopy. J Cell Biol 91:814–821PubMedGoogle Scholar
  70. Kwiatkowski N et al (2010) Small-molecule kinase inhibitors provide insight into Mps1 cell cycle function. Nat Chem Biol 6:359–368PubMedGoogle Scholar
  71. Kwon M et al (2008) Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes. Genes Dev 22:2189–2203PubMedGoogle Scholar
  72. Lawo S et al (2009) HAUS, the 8-subunit complex, regulates centrosome and spindle integrity. Curr Biol 19:1–11Google Scholar
  73. Leber B et al. Proteins required for centrosome clustering in cancer cells. Sci. Transl. Med. 2, 32ra38 (2010)Google Scholar
  74. Leidel S, Delattre M, Cerutti L, Baumer K, Gönczy P (2005) SAS-6 defines a protein family required for centrosome duplication in C. elegans and in human cells. Nat Cell Biol 7:115–125PubMedGoogle Scholar
  75. Levine DS, Sanchez CA, Rabinovitch PS, Reid BJ (1991) Formation of the tetraploid intermediate is associated with the development of cells with more than four centrioles in the elastase-simian virus 40 tumor antigen transgenic mouse model of pancreatic cancer. Proc. Natl. Acad. Sci. USA 88:6427–6431PubMedGoogle Scholar
  76. Lingle WL, Salisbury JL (1999) Altered centrosome structure is associated with abnormal mitoses in human breast tumors. Am J Pathol 155:1941–1951PubMedGoogle Scholar
  77. Lingle WL, Lutz WH, Ingle JN, Maihle NJ, Salisbury JL (1998) Centrosome hypertrophy in human breast tumors: implications for genomic stability and cell polarity. Proc. Natl. Acad. Sci. USA 95:2950–2955PubMedGoogle Scholar
  78. Liu D, Vader G, Vromans MJM, Lampson MA, Lens SMA (2009) Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 323:1350–1353PubMedGoogle Scholar
  79. Löffler H et al (2011) Cep63 recruits Cdk1 to the centrosome: implications for regulation of mitotic entry, centrosome amplification, and genome maintenance. Cancer Res 71:2129–2139PubMedGoogle Scholar
  80. Loo DS (2006) Systemic antifungal agents: an update of established and new therapies. Adv Dermatol 22:101–124PubMedGoogle Scholar
  81. Nakamura Y et al (2007) Clinicopathological and biological significance of mitotic centromere-associated kinesin overexpression in human gastric cancer. Br J Cancer 97:543–549PubMedGoogle Scholar
  82. Neben K, Giesecke C, Schweizer S, Ho AD, Krämer A (2003) Centrosome aberrations in acute myeloid leukemia are correlated with cytogenetic risk profile. Blood 101:289–291PubMedGoogle Scholar
  83. Nguyen CL, McLaughlin-Drubin ME, Münger K (2008) Delocalization of the microtubule motor dynein from mitotic spindles by the human papillomavirus E7 oncoprotein is not sufficient for induction of multipolar mitoses. Cancer Res 68:8715–8722PubMedGoogle Scholar
  84. Nguyen HG et al (2009) Deregulated Aurora-B induced tetraploidy promotes tumorigenesis. FASEB J. 23:2741–2748PubMedGoogle Scholar
  85. Nguyen M-H et al (2010) Phosphorylation and activation of cell division cycle associated 5 by mitogen-activated protein kinase play a crucial role in human lung carcinogenesis. Cancer Res 70:5337–5347PubMedGoogle Scholar
  86. Nigg EA (2002) Centrosome aberrations: cause or consequence of cancer progression? Nat Rev Cancer 2:815–825PubMedGoogle Scholar
  87. Nigg EA, Raff JW (2009) Centrioles, centrosomes, and cilia in health and disease. Cell 139:663–678PubMedGoogle Scholar
  88. Panda D, Rathinasamy K, Santra MK, Wilson L (2005) Kinetic suppression of microtubule dynamic instability by griseofulvin: implications for its possible use in the treatment of cancer. Proc. Natl. Acad. Sci. USA 102:9878–9883PubMedGoogle Scholar
  89. Peset I, Vernos I (2008) The TACC proteins: TACC-ling microtubule dynamics and centrosome function. Trends Cell Biol 18:379–388PubMedGoogle Scholar
  90. Pihan GA, Purohit A, Wallace J (1998) Centrosome defects and genetic instability in malignant tumors. Cancer Res 58:3974–3985PubMedGoogle Scholar
  91. Pihan GA, Purohit A, Wallace J, Malhotra R, Liotta L, Doxsey SJ (2001) Centrosome defects can account for cellular and genetic changes that characterize prostate cancer progression. Cancer Res 61:2212–2219PubMedGoogle Scholar
  92. Putkey FR et al (2002) Unstable kinetochore-microtubule capture and chromosomal instability following deletion of CENP-E. Dev Cell 3:351–365PubMedGoogle Scholar
  93. Quintyne NJ, Reing JE, Hoffelder DR, Gollin SM, Saunders WS (2005) Spindle multipolarity is prevented by centrosomal clustering. Science 307:127–129PubMedGoogle Scholar
  94. Rebacz B et al (2007) Identification of griseofulvin as an inhibitor of centrosomal clustering in a phenotype-based screen. Cancer Res 67:6342–6350PubMedGoogle Scholar
  95. Ring D, Hubble R, Kirschner M (1982) Mitosis in a cell with multiple centrioles. J Cell Biol 94:549–556PubMedGoogle Scholar
  96. Roobol A, Gull K, Pogson CI (1977) Evidence that griseofulvin binds to a microtubule associated protein. FEBS Lett 75:149–153PubMedGoogle Scholar
  97. Ruchaud S, Carmena M, Earnshaw WC (2007) Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8:798–812PubMedGoogle Scholar
  98. Saxena A, Saffery R, Wong LH, Kalitsis P, Choo A (2002) Centromere proteins CENPA, CENPB, and BUB3 interact with poly(ADP-ribose) polymerase-1 protein and are poly(ADP-ribosyl)ated. J Biol Chem 277:26921–26926PubMedGoogle Scholar
  99. Schmitz J, Watrin E, Lénárt P, Mechtler K, Peters J-M (2007) Sororin is required for stable binding of cohesin to chromatin and for sister chromatid cohesion in interphase. Curr Biol 17:630–636PubMedGoogle Scholar
  100. Schockel L, Mockel M, Mayer B, Boos D, Stemmann O (2011) Cleavage of cohesin rings coordinates the separation of centrioles and chromatids. Nat Cell Biol 13:966–972PubMedGoogle Scholar
  101. Schvartzman J-M, Sotillo R, Benezra R (2010) Mitotic chromosomal instability and cancer: mouse modelling of the human disease. Nat Rev Cancer 10:102–115PubMedGoogle Scholar
  102. Shao S et al (2010) Centrosomal Nlp is an oncogenic protein that is gene-amplified in human tumors and causes spontaneous tumorigenesis in transgenic mice. J. Clin. Invest. 120:498–507PubMedGoogle Scholar
  103. Shimo A et al (2007) Elevated expression of protein regulator of cytokinesis 1, involved in the growth of breast cancer cells. Cancer Sci 98:174–181PubMedGoogle Scholar
  104. Silkworth WT, Nardi IK, Scholl LM, Cimini D (2009) Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome mis-segregation. in cancer cells. PLoS ONE 4:e6564PubMedGoogle Scholar
  105. Sillje HHW, Nagel S, Körner R, Nigg EA (2006) HURP is a Ran-importin β-related protein that stabilizes kinetochore microtubules in the vincinity of chromosomes. Curr Biol 16:731–742PubMedGoogle Scholar
  106. Sluder G, Thompson EA, Miller FJ, Hayes J, Rieder CL (1997) The checkpoint control for anaphase onset does not monitor excess numbers of spindle poles or bipolar spindle symmetry. J Cell Sci 110:421–429PubMedGoogle Scholar
  107. Sotillo R et al (2007) Mad2 overexpression promotes aneuploidy and tumorigenesis in mice. Cancer Cell 11:9–23PubMedGoogle Scholar
  108. Stearns T, Evans L, Kirschner M (1991) Gamma-tubulin is a highly conserved component of the centrosome. Cell 65:825–836PubMedGoogle Scholar
  109. Stevens NR, Dobbelaere J, Brunk K, Franz A, Raff JW (2010) Drosophila Ana2 is a conserved centriole duplication factor. J Cell Biol 188:313–323PubMedGoogle Scholar
  110. Strnad P, Gönczy P (2008) Mechanisms of procentriole formation. Trends Cell Biol 18:389–396PubMedGoogle Scholar
  111. Tang CJ et al (2011) The human microcephaly protein STIL interacts with CPAP and is required for procentriole formation. EMBO J 30:4790–4804PubMedGoogle Scholar
  112. Taylor S, Peters JM (2008) Polo and Aurora kinases: lessons derived from chemical biology. Curr Opin Cell Biol 20:77–84PubMedGoogle Scholar
  113. Thery M et al (2005) The extracellular matrix guides the orientation of the cell division axis. Nat Cell Biol 7:947–953PubMedGoogle Scholar
  114. Tsou MF, Stearns T (2006) Mechanism limiting centrosome duplication to once per cell cycle. Nature 442:947–951PubMedGoogle Scholar
  115. Tsou AP et al (2003) Identification of a novel cell cycle regulated gene, HURP, overexpressed in human hepatocellular carcinoma. Oncogene 22:298–307PubMedGoogle Scholar
  116. Uehara R et al (2009) The augmin complex plays a critical role in spindle microtubule generation for mitotic progression and cytokinesis in human cells. Proc. Natl. Acad. Sci. USA 106:6998–7003PubMedGoogle Scholar
  117. Uzbekov R, Prigent C (2007) Clockwise or anticlockwise? Turning the centriole triplets in the right direction! FEBS Lett 581:1251–1254PubMedGoogle Scholar
  118. Vader G, Lens SM (2008) The Aurora kinase family in cell division and cancer. Biochim Biophys Acta 1786:60–72PubMedGoogle Scholar
  119. Vanoosthuyse V, Prykhozhij S, Hardwick KG (2007) Shugoshin 2 regulates localization of the chromosomal passenger proteins in fission yeast mitosis. Mol Biol Cell 18:1657–1669PubMedGoogle Scholar
  120. von Hansemann D (1890) Über asymmetrische Zellteilung in Epithelkrebsen und deren biologische Bedeutung. Virchows Arch. Patholog. Anat. 119, 299-326 (in German)Google Scholar
  121. Vulprecht J et al (2012) SIL is required for centriole duplication in human cells. J Cell Sci 125:1353–1362PubMedGoogle Scholar
  122. Wang X et al (2009) Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461:947–955PubMedGoogle Scholar
  123. Wang F et al (2010) Histone H3 Thr-3 phosphorylation by haspin positions aurora B at centromeres in mitosis. Science 330:231–235PubMedGoogle Scholar
  124. Weaver BA, Silk AD, Montagna C, Verdier-Pinard P, Cleveland DW (2007) Aneuploidy acts both oncogenically and as a tumor suppressor. Cancer Cell 11:25–36PubMedGoogle Scholar
  125. Weber K, Wehland J, Herzog W (1976) Griseofulvin interacts with microtubules both in vitro and in vivo. J Mol Biol 102:817–829PubMedGoogle Scholar
  126. Wehland J, Herzog W, Weber K (1977) Interaction of griseofulvin with microtubules, microtubule protein and tubulin. J Mol Biol 111:329–342PubMedGoogle Scholar
  127. Wei RR, Al-Bassam J, Harrison SC (2007) The Ndc80/HEC1 complex is a contact point for kinetochore-microtubule attachment. Nat Struct Mol Biol 14:54–59PubMedGoogle Scholar
  128. Wilkinson RW et al (2007) AZD1152, a selective inhibitor of Aurora B kinase, inhibits human tumor xenograft growth by inducing apoptosis. Clin Cancer Res 13:3682–3688PubMedGoogle Scholar
  129. Wong J, Fang G (2006) HURP controls spindle dynamics to promote proper interkinetochore tension and efficient kinetochore capture. J Cell Biol 173:879–891PubMedGoogle Scholar
  130. Wu G, Lin YT, Wei R, Chen Y, Shan Z, Lee WH (2008a) Hice1, a novel microtubule-associated protein required for maintenance of spindle integrity and chromosomal stability in human cells. Mol Cell Biol 28:3652–3662PubMedGoogle Scholar
  131. Wu G et al (2008b) Small molecule targeting the Hec1/Nek2 mitotic pathway suppresses tumor cell growth in culture and in animal. Cancer Res 68:8393–8399PubMedGoogle Scholar
  132. Yamagishi Y, Honda T, Tanno Y, Watanabe Y (2010) Two histone marks establish the inner centromere and chromosome bi-orientation. Science 330:239–243PubMedGoogle Scholar
  133. Yamashita YM, Mahowald AP, Perlin JR, Fuller MT (2007) Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315:518–521PubMedGoogle Scholar
  134. Yang Z, Loncarek J, Khodjakov A, Rieder CL (2008) Extra centrosomes and/or chromosomes prolong mitosis in human cells. Nat Cell Biol 10:748–751PubMedGoogle Scholar

Copyright information

© Humana Press, a part of Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Clinical Cooperation Unit Molecular Hematology/OncologyGerman Cancer Research Center and Department of Internal Medicine University of HeidelbergHeidelbergGermany

Personalised recommendations