Advertisement

Chromosome Research

, Volume 24, Issue 1, pp 35–51 | Cite as

Centrosomes in the DNA damage response—the hub outside the centre

  • Lisa I. Mullee
  • Ciaran G. Morrison
Review

Abstract

Here, we review how DNA damage affects the centrosome and how centrosomes communicate with the DNA damage response (DDR) apparatus. We discuss how several proteins of the DDR are found at centrosomes, including the ATM, ATR, CHK1 and CHK2 kinases, the BRCA1 ubiquitin ligase complex and several members of the poly(ADP-ribose) polymerase family. Stereotypical centrosome organisation, in which two centriole barrels are orthogonally arranged in a roughly toroidal pericentriolar material (PCM), is strongly affected by exposure to DNA-damaging agents. We describe the genetic dependencies and mechanisms for how the centrioles lose their close association, and the PCM both expands and distorts after DNA damage. Another consequence of genotoxic stress is that centrosomes undergo duplication outside the normal cell cycle stage, meaning that centrosome amplification is commonly seen after DNA damage. We discuss several potential mechanisms for how centrosome numbers become dysregulated after DNA damage and explore the links between the DDR and the PLK1- and separase-dependent mechanisms that drive centriole separation and reduplication. We also describe how centrosome components, such as centrin2, are directly involved in responding to DNA damage. This review outlines current questions on the involvement of centrosomes in the DDR.

Keywords

Centriole Centrosome PCM Checkpoint Cancer ATM CHK1 PLK1 

Abbreviations

Aki1

Akt kinase-interacting protein

ADP

Adenosine diphosphate ribose

Ana2

Anastral spindle 2

AKAP

A-kinase-anchoring protein

APC/C

Anaphase-promoting complex/cyclosome

ATM

Ataxia telangiectasia, mutated

ATR

ATM-Rad3 related

ATRIP

ATR-interacting protein

BARD1

BRCA1-associated RING domain protein 1

BRCA

Breast cancer-associated gene

CDC

Cell division cycle

CDK

Cyclin-dependent kinase

CDK5RAP2

CDK5 regulatory subunit-associated protein 2

CEP164

Centrosomal protein 164 kDa

CHK

Checkpoint kinase

C-NAP1

Centrosomal NEK2-associated protein 1

DDR

DNA damage response

DNA-PK

DNA-dependent protein kinase

DNA-PKcs

DNA-PK catalytic subunit

DSB

Double-strand break

ES

Embryonic stem

γ-TURC

γ-tubulin ring complex

γ-TUSC

γ-tubulin small complex

GFP

Green fluorescent protein

HR

Homologous recombination

hTERT-RPE1

Human telomerase reverse transcriptase- retinal pigment epithelial

IR

Ionising radiation

MCPH

Microcephaly

Miki

Mitotic kinetics regulator

MRE11

Meiotic recombination 11

MRN

MRE11-RAD50-NBS1 complex

MTOC

Microtubule-organising centre

NBS1

Nijmegen breakage syndrome 1

NEK/NRK

NIMA-related kinase

NER

Nucleotide excision repair

NHEJ

Non-homologous end joining

NIMA

Never in mitosis A

OLA1

Obg-like ATPase 1

OMIM

Online Mendelian inheritance in man

PARP

Poly(ADP-ribose) polymerase

PCM

Pericentriolar material

PCNT

Pericentrin

PIKK

Phosphoinositide 3-kinase related protein kinase

PLK

Polo-like kinase

RNAi

RNA interference

SAS-5/6

Spindle assembly abnormal protein 5/6 homolog

SCC

Sister chromatid cohesion protein

SCL

Stem cell leukaemia

SGO1

Shugosin 1

sSGO1

Short shugoshin 1

siRNA

Short interfering RNA

SMC

Structural maintenance of chromosomes

ssDNA

Single-stranded DNA

STIL

SCL-interrupting locus protein

UV

Ultraviolet

XPA

Xeroderma pigmentosum complementation group A

XPC

Xeroderma pigmentosum group complementation C

Notes

Acknowledgments

We thank Alicja Antonczak for the critical reading of the manuscript. LIM received a Travelling Studentship from the National University of Ireland. Work in CGM’s laboratory is supported by Science Foundation Ireland Principal Investigator award 10/IN.1/B2972.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Agircan FG, Schiebel E (2014) Sensors at centrosomes reveal determinants of local separase activity. PLoS Genet 10, e1004672PubMedCentralPubMedCrossRefGoogle Scholar
  2. Agircan FG, Schiebel E, Mardin BR (2014) Separate to operate: control of centrosome positioning and separation. Philos Trans R Soc Lond B Biol Sci 369:20130461PubMedCentralPubMedCrossRefGoogle Scholar
  3. Alderton GK, Joenje H, Varon R, Borglum AD, Jeggo PA, O’Driscoll M (2004) Seckel syndrome exhibits cellular features demonstrating defects in the ATR-signalling pathway. Hum Mol Genet 13:3127–3138PubMedCrossRefGoogle Scholar
  4. Alderton GK, Galbiati L, Griffith E, Surinya KH, Neitzel H, Jackson AP, Jeggo PA, O’Driscoll M (2006) Regulation of mitotic entry by microcephalin and its overlap with ATR signalling. Nat Cell Biol 8:725–733PubMedCrossRefGoogle Scholar
  5. Alliegro MC, Alliegro MA (2008) Centrosomal RNA correlates with intron-poor nuclear genes in Spisula oocytes. Proc Natl Acad Sci U S A 105:6993–6997PubMedCentralPubMedCrossRefGoogle Scholar
  6. Antonczak AK, Mullee LI, Wang Y, Comartin D, Inoue T, Pelletier L, Morrison CG (2015) Opposing effects of pericentrin and microcephalin on the pericentriolar material regulate CHK1 activation in the DNA damage response. Oncogene, in pressGoogle Scholar
  7. Araki M, Masutani C, Takemura M, Uchida A, Sugasawa K, Kondoh J, Ohkuma Y, Hanaoka F (2001) Centrosome protein centrin 2/caltractin 1 is part of the xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair. J Biol Chem 276:18665–18672PubMedCrossRefGoogle Scholar
  8. Arquint C, Sonnen KF, Stierhof YD, Nigg EA (2012) Cell-cycle-regulated expression of STIL controls centriole number in human cells. J Cell Sci 125:1342–1352PubMedCrossRefGoogle Scholar
  9. Arquint C, Gabryjonczyk AM, Nigg EA (2014) Centrosomes as signalling centres. Philos Trans R Soc Lond B Biol Sci 369:20130464PubMedCentralPubMedCrossRefGoogle Scholar
  10. Augustin A, Spenlehauer C, Dumond H, Menissier-De Murcia J, Piel M, Schmit AC, Apiou F, Vonesch JL, Kock M, Bornens M, De Murcia G (2003) PARP-3 localizes preferentially to the daughter centriole and interferes with the G1/S cell cycle progression. J Cell Sci 116:1551–1562PubMedCrossRefGoogle Scholar
  11. Bahe S, Stierhof YD, Wilkinson CJ, Leiss F, Nigg EA (2005) Rootletin forms centriole-associated filaments and functions in centrosome cohesion. J Cell Biol 171:27–33PubMedCentralPubMedCrossRefGoogle Scholar
  12. Balczon R, Bao L, Zimmer WE, Brown K, Zinkowski RP, Brinkley BR (1995) Dissociation of centrosome replication events from cycles of DNA synthesis and mitotic division in hydroxyurea-arrested Chinese hamster ovary cells. J Cell Biol 130:105–115PubMedCrossRefGoogle Scholar
  13. Barbelanne M, Tsang WY (2014) Molecular and cellular basis of autosomal recessive primary microcephaly. BioMed Res Int 2014:547986PubMedCentralPubMedCrossRefGoogle Scholar
  14. Barr AR, Kilmartin JV, Gergely F (2010) CDK5RAP2 functions in centrosome to spindle pole attachment and DNA damage response. J Cell Biol 189:23–39PubMedCentralPubMedCrossRefGoogle Scholar
  15. Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov A, Raff JW (2006) Flies without centrioles. Cell 125:1375–1386PubMedCrossRefGoogle Scholar
  16. Batchelor E, Loewer A, Lahav G (2009) The ups and downs of p53: understanding protein dynamics in single cells. Nat Rev Cancer 9:371–377PubMedCentralPubMedCrossRefGoogle Scholar
  17. Bazzi H, Anderson KV (2014) Acentriolar mitosis activates a p53-dependent apoptosis pathway in the mouse embryo. Proc Natl Acad Sci U S A 111:E1491–E1500PubMedCentralPubMedCrossRefGoogle Scholar
  18. Beck C, Robert I, Reina-San-Martin B, Schreiber V, Dantzer F (2014) Poly(ADP-ribose) polymerases in double-strand break repair: focus on PARP1, PARP2 and PARP3. Exp Cell Res 329:18–25PubMedCrossRefGoogle Scholar
  19. Bobinnec Y, Khodjakov A, Mir LM, Rieder CL, Edde B, Bornens M (1998) Centriole disassembly in vivo and its effect on centrosome structure and function in vertebrate cells. J Cell Biol 143:1575–1589PubMedCentralPubMedCrossRefGoogle Scholar
  20. Bornens M (2002) Centrosome composition and microtubule anchoring mechanisms. Curr Opin Cell Biol 14:25–34PubMedCrossRefGoogle Scholar
  21. Bourke E, Dodson H, Merdes A, Cuffe L, Zachos G, Walker M, Gillespie D, Morrison CG (2007) DNA damage induces Chk1-dependent centrosome amplification. EMBO Rep 8:603–609PubMedCentralPubMedCrossRefGoogle Scholar
  22. Bourke E, Brown JA, Takeda S, Hochegger H, Morrison CG (2010) DNA damage induces Chk1-dependent threonine-160 phosphorylation and activation of Cdk2. Oncogene 29:616–624PubMedCrossRefGoogle Scholar
  23. Boutros R, Ducommun B (2008) Asymmetric localization of the CDC25B phosphatase to the mother centrosome during interphase. Cell Cycle 7:401–406PubMedCrossRefGoogle Scholar
  24. Brown CR, Doxsey SJ, White E, Welch WJ (1994) Both viral (adenovirus E1B) and cellular (hsp 70, p53) components interact with centrosomes. J Cell Physiol 160:47–60PubMedCrossRefGoogle Scholar
  25. Brown JA, Bourke E, Liptrot C, Dockery P, Morrison CG (2010) MCPH1/BRIT1 limits ionizing radiation-induced centrosome amplification. Oncogene 29:5537–5544PubMedCrossRefGoogle Scholar
  26. Brownlee CW, Rogers GC (2013) Show me your license, please: deregulation of centriole duplication mechanisms that promote amplification. Cell Mol Life Sci 70:1021–1034PubMedCrossRefGoogle Scholar
  27. Cabral G, Sans SS, Cowan CR, Dammermann A (2013) Multiple mechanisms contribute to centriole separation in C. elegans. Curr Biol 23:1380–1387PubMedCentralPubMedCrossRefGoogle Scholar
  28. Cajanek L, Nigg EA (2014) Cep164 triggers ciliogenesis by recruiting Tau tubulin kinase 2 to the mother centriole. Proc Natl Acad Sci U S A 111:E2841–E2850PubMedCentralPubMedCrossRefGoogle Scholar
  29. Cazales M, Schmitt E, Montembault E, Dozier C, Prigent C, Ducommun B (2005) CDC25B phosphorylation by Aurora-A occurs at the G2/M transition and is inhibited by DNA damage. Cell Cycle 4:1233–1238PubMedCrossRefGoogle Scholar
  30. Chavali PL, Putz M, Gergely F (2014) Small organelle, big responsibility: the role of centrosomes in development and disease. Philos Trans R Soc Lond B Biol Sci 369:20130468PubMedCentralPubMedCrossRefGoogle Scholar
  31. Chestukhin A, Pfeffer C, Milligan S, DeCaprio JA, Pellman D (2003) Processing, localization, and requirement of human separase for normal anaphase progression. Proc Natl Acad Sci U S A 100:4574–4579PubMedCentralPubMedCrossRefGoogle Scholar
  32. Chouinard G, Clement I, Lafontaine J, Rodier F, Schmitt E (2013) Cell cycle-dependent localization of CHK2 at centrosomes during mitosis. Cell Div 8:7PubMedCentralPubMedCrossRefGoogle Scholar
  33. Ciccia A, Elledge SJ (2010) The DNA damage response: making it safe to play with knives. Mol Cell 40:179–204PubMedCentralPubMedCrossRefGoogle Scholar
  34. Conroy PC, Saladino C, Dantas TJ, Lalor P, Dockery P, Morrison CG (2012) C-NAP1 and rootletin restrain DNA damage-induced centriole splitting and facilitate ciliogenesis. Cell Cycle 11:3769–3778PubMedCentralPubMedCrossRefGoogle Scholar
  35. Cunha-Ferreira I, Rodrigues-Martins A, Bento I, Riparbelli M, Zhang W, Laue E, Callaini G, Glover DM, Bettencourt-Dias M (2009) The SCF/Slimb ubiquitin ligase limits centrosome amplification through degradation of SAK/PLK4. Curr Biol 19:43–49PubMedCrossRefGoogle Scholar
  36. Dammermann A, Merdes A (2002) Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J Cell Biol 159:255–266PubMedCentralPubMedCrossRefGoogle Scholar
  37. Dantas TJ, Wang Y, Lalor P, Dockery P, Morrison CG (2011) Defective nucleotide excision repair with normal centrosome structures and functions in the absence of all vertebrate centrins. J Cell Biol 193:307–318PubMedCentralPubMedCrossRefGoogle Scholar
  38. Dantas TJ, Daly OM, Morrison CG (2012) Such small hands: the roles of centrins/caltractins in the centriole and in genome maintenance. Cell Mol Life Sci 69:2979–2997PubMedCrossRefGoogle Scholar
  39. De Souza CP, Ellem KA, Gabrielli BG (2000) Centrosomal and cytoplasmic Cdc2/cyclin B1 activation precedes nuclear mitotic events. Exp Cell Res 257:11–21PubMedCrossRefGoogle Scholar
  40. Dictenberg JB, Zimmerman W, Sparks CA, Young A, Vidair C, Zheng Y, Carrington W, Fay FS, Doxsey SJ (1998) Pericentrin and gamma-tubulin form a protein complex and are organized into a novel lattice at the centrosome. J Cell Biol 141:163–174PubMedCentralPubMedCrossRefGoogle Scholar
  41. Dodson H, Wheatley SP, Morrison CG (2007) Involvement of centrosome amplification in radiation-induced mitotic catastrophe. Cell Cycle 6:364–370PubMedCrossRefGoogle Scholar
  42. Douthwright S, Sluder G (2014) Link between DNA damage and centriole disengagement/reduplication in untransformed human cells. J Cell Physiol 229:1427–1436PubMedCentralPubMedCrossRefGoogle Scholar
  43. Dutertre S, Cazales M, Quaranta M, Froment C, Trabut V, Dozier C, Mirey G, Bouche JP, Theis-Febvre N, Schmitt E, Monsarrat B, Prigent C, Ducommun B (2004) Phosphorylation of CDC25B by Aurora-A at the centrosome contributes to the G2-M transition. J Cell Sci 117:2523–2531PubMedCrossRefGoogle Scholar
  44. Firat-Karalar EN, Rauniyar N, Yates JR 3rd, Stearns T (2014) Proximity interactions among centrosome components identify regulators of centriole duplication. Curr Biol 24:664–670PubMedCentralPubMedCrossRefGoogle Scholar
  45. Fletcher L, Cerniglia GJ, Nigg EA, Yend TJ, Muschel RJ (2004) Inhibition of centrosome separation after DNA damage: a role for Nek2. Radiat Res 162:128–135PubMedCrossRefGoogle Scholar
  46. Fry AM, Meraldi P, Nigg EA (1998) A centrosomal function for the human Nek2 protein kinase, a member of the NIMA family of cell cycle regulators. EMBO J 17:470–481PubMedCentralPubMedCrossRefGoogle Scholar
  47. Fu J, Glover DM (2012) Structured illumination of the interface between centriole and peri-centriolar material. Open Biol 2:120104PubMedCentralPubMedCrossRefGoogle Scholar
  48. Fukasawa K, Choi T, Kuriyama R, Rulong S, Vande Woude GF (1996) Abnormal centrosome amplification in the absence of p53. Science 271:1744–1747PubMedCrossRefGoogle Scholar
  49. Furnari B, Rhind N, Russell P (1997) Cdc25 mitotic inducer targeted by chk1 DNA damage checkpoint kinase. Science 277:1495–1497PubMedCrossRefGoogle Scholar
  50. Ganem NJ, Godinho SA, Pellman D (2009) A mechanism linking extra centrosomes to chromosomal instability. Nature 460:278–282PubMedCentralPubMedCrossRefGoogle Scholar
  51. Gimenez-Abian JF, Diaz-Martinez LA, Beauchene NA, Hsu WS, Tsai HJ, Clarke DJ (2010) Determinants of Rad21 localization at the centrosome in human cells. Cell Cycle 9:1759–1763PubMedCrossRefGoogle Scholar
  52. Godinho SA, Pellman D (2014) Causes and consequences of centrosome abnormalities in cancer. Philos Trans R Soc Lond B Biol Sci 369:20130467PubMedCentralPubMedCrossRefGoogle Scholar
  53. Golan A, Pick E, Tsvetkov L, Nadler Y, Kluger H, Stern DF (2010) Centrosomal Chk2 in DNA damage responses and cell cycle progression. Cell Cycle 9:2647–2656PubMedCentralPubMedCrossRefGoogle Scholar
  54. Gorr IH, Boos D, Stemmann O (2005) Mutual inhibition of separase and Cdk1 by two-step complex formation. Mol Cell 19:135–141PubMedCrossRefGoogle Scholar
  55. Graser S, Stierhof YD, Lavoie SB, Gassner OS, Lamla S, Le Clech M, Nigg EA (2007) Cep164, a novel centriole appendage protein required for primary cilium formation. J Cell Biol 179:321–330PubMedCentralPubMedCrossRefGoogle Scholar
  56. Gregson HC, Schmiesing JA, Kim JS, Kobayashi T, Zhou S, Yokomori K (2001) A potential role for human cohesin in mitotic spindle aster assembly. J Biol Chem 276:47575–47582PubMedCrossRefGoogle Scholar
  57. Griffith E, Walker S, Martin CA, Vagnarelli P, Stiff T, Vernay B, Al Sanna N, Saggar A, Hamel B, Earnshaw WC, Jeggo PA, Jackson AP, O’Driscoll M (2008) Mutations in pericentrin cause Seckel syndrome with defective ATR-dependent DNA damage signaling. Nat Genet 40:232–236PubMedCentralPubMedCrossRefGoogle Scholar
  58. Gruber R, Zhou Z, Sukchev M, Joerss T, Frappart PO, Wang ZQ (2011) MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nat Cell Biol 13:1325–1334PubMedCrossRefGoogle Scholar
  59. Guan J, Ekwurtzel E, Kvist U, Yuan L (2008) Cohesin protein SMC1 is a centrosomal protein. Biochem Biophys Res Commun 372:761–764PubMedCrossRefGoogle Scholar
  60. Guichard P, Chretien D, Marco S, Tassin AM (2010) Procentriole assembly revealed by cryo-electron tomography. EMBO J 29:1565–1572PubMedCentralPubMedCrossRefGoogle Scholar
  61. Hsu LC, White RL (1998) BRCA1 is associated with the centrosome during mitosis. Proc Natl Acad Sci U S A 95:12983–12988PubMedCentralPubMedCrossRefGoogle Scholar
  62. Hsu LC, Doan TP, White RL (2001) Identification of a gamma-tubulin-binding domain in BRCA1. Cancer Res 61:7713–7718PubMedGoogle Scholar
  63. Hut HM, Lemstra W, Blaauw EH, Van Cappellen GW, Kampinga HH, Sibon OC (2003) Centrosomes split in the presence of impaired DNA integrity during mitosis. Mol Biol Cell 14:1993–2004PubMedCentralPubMedCrossRefGoogle Scholar
  64. Inanc B, Dodson H, Morrison CG (2010) A centrosome-autonomous signal that involves centriole disengagement permits centrosome duplication in G2 phase after DNA damage. Mol Biol Cell 21:3866–3877PubMedCentralPubMedCrossRefGoogle Scholar
  65. Jackman M, Lindon C, Nigg EA, Pines J (2003) Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nat Cell Biol 5:143–148PubMedCrossRefGoogle Scholar
  66. Jackson SP, Bartek J (2009) The DNA-damage response in human biology and disease. Nature 461:1071–1078PubMedCentralPubMedCrossRefGoogle Scholar
  67. Jeffers LJ, Coull BJ, Stack SJ, Morrison CG (2008) Distinct BRCT domains in Mcph1/Brit1 mediate ionizing radiation-induced focus formation and centrosomal localization. Oncogene 27:139–144PubMedCrossRefGoogle Scholar
  68. Jilani Y, Lu S, Lei H, Karnitz LM, Chadli A (2015) UNC45A localizes to centrosomes and regulates cancer cell proliferation through ChK1 activation. Cancer Lett 357:114–120PubMedCentralPubMedCrossRefGoogle Scholar
  69. Kanai M, Uchida M, Hanai S, Uematsu N, Uchida K, Miwa M (2000) Poly(ADP-ribose) polymerase localizes to the centrosomes and chromosomes. Biochem Biophys Res Commun 278:385–389PubMedCrossRefGoogle Scholar
  70. Kanai M, Tong WM, Sugihara E, Wang ZQ, 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 23:2451–2462PubMedCentralPubMedCrossRefGoogle Scholar
  71. Karlsson-Rosenthal C, Millar JB (2006) Cdc25: mechanisms of checkpoint inhibition and recovery. Trends Cell Biol 16:285–292PubMedCrossRefGoogle Scholar
  72. Katsura M, Tsuruga T, Date O, Yoshihara T, Ishida M, Tomoda Y, Okajima M, Takaku M, Kurumizaka H, Kinomura A, Mishima HK, Miyagawa K (2009) The ATR-Chk1 pathway plays a role in the generation of centrosome aberrations induced by Rad51C dysfunction. Nucleic Acids Res 37:3959–3968PubMedCentralPubMedCrossRefGoogle Scholar
  73. Kawamura K, Morita N, Domiki C, Fujikawa-Yamamoto K, Hashimoto M, Iwabuchi K, Suzuki K (2006) Induction of centrosome amplification in p53 siRNA-treated human fibroblast cells by radiation exposure. Cancer Sci 97:252–258PubMedCrossRefGoogle Scholar
  74. Kenney J, Karsenti E, Gowen B, Fuller SD (1997) Three-dimensional reconstruction of the mammalian centriole from cryoelectron micrographs: the use of common lines for orientation and alignment. J Struct Biol 120:320–328PubMedCrossRefGoogle Scholar
  75. Kim MK, Dudognon C, Smith S (2012) Tankyrase 1 regulates centrosome function by controlling CPAP stability. EMBO Rep 13:724–732PubMedCentralPubMedCrossRefGoogle Scholar
  76. Kim SH, Park ER, Joo HY, Shen YN, Hong SH, Kim CH, Singh R, Lee KH, Shin HJ (2014) RRM1 maintains centrosomal integrity via CHK1 and CDK1 signaling during replication stress. Cancer Lett 346:249–256PubMedCrossRefGoogle Scholar
  77. Klingseisen A, Jackson AP (2011) Mechanisms and pathways of growth failure in primordial dwarfism. Genes Dev 25:2011–2024PubMedCentralPubMedCrossRefGoogle Scholar
  78. Ko MJ, Murata K, Hwang DS, Parvin JD (2006) Inhibition of BRCA1 in breast cell lines causes the centrosome duplication cycle to be disconnected from the cell cycle. Oncogene 25:298–303PubMedCrossRefGoogle Scholar
  79. Kodani A, Yu TW, Johnson JR, Jayaraman D, Johnson TL, Al-Gazali L, Sztriha L, Partlow JN, Kim H, Krup AL, Dammermann A, Krogan N, Walsh CA, Reiter JF (2015) Centriolar satellites assemble centrosomal microcephaly proteins to recruit CDK2 and promote centriole duplication. eLife 4Google Scholar
  80. Koledova Z, Kafkova LR, Kramer A, Divoky V (2010) DNA damage-induced degradation of Cdc25A does not lead to inhibition of Cdk2 activity in mouse embryonic stem cells. Stem Cells 28:450–461PubMedGoogle Scholar
  81. Kong X, Ball AR Jr, Sonoda E, Feng J, Takeda S, Fukagawa T, Yen TJ, Yokomori K (2009) Cohesin associates with spindle poles in a mitosis-specific manner and functions in spindle assembly in vertebrate cells. Mol Biol Cell 20:1289–1301PubMedCentralPubMedCrossRefGoogle Scholar
  82. Kramer A, Mailand N, Lukas C, Syljuasen RG, Wilkinson CJ, Nigg EA, Bartek J, Lukas J (2004) Centrosome-associated Chk1 prevents premature activation of cyclin-B-Cdk1 kinase. Nat Cell Biol 6:884–891PubMedCrossRefGoogle Scholar
  83. Kubo A, Tsukita S (2003) Non-membranous granular organelle consisting of PCM-1: subcellular distribution and cell-cycle-dependent assembly/disassembly. J Cell Sci 116:919–928PubMedCrossRefGoogle Scholar
  84. La Terra S, English CN, Hergert P, McEwen BF, Sluder G, Khodjakov A (2005) The de novo centriole assembly pathway in HeLa cells: cell cycle progression and centriole assembly/maturation. J Cell Biol 168:713–722PubMedCentralPubMedCrossRefGoogle Scholar
  85. Lambrus BG, Uetake Y, Clutario KM, Daggubati V, Snyder M, Sluder G, Holland AJ (2015) p53 protects against genome instability following centriole duplication failure. J Cell Biol 210:63–77PubMedCentralPubMedCrossRefGoogle Scholar
  86. Lawo S, Hasegan M, Gupta GD, Pelletier L (2012) Subdiffraction imaging of centrosomes reveals higher-order organizational features of pericentriolar material. Nat Cell Biol 14:1148–1158PubMedCrossRefGoogle Scholar
  87. Lee K, Rhee K (2012) Separase-dependent cleavage of pericentrin B is necessary and sufficient for centriole disengagement during mitosis. Cell Cycle 11:2476–2485PubMedCrossRefGoogle Scholar
  88. Lindqvist A, Kallstrom H, Lundgren A, Barsoum E, Rosenthal CK (2005) Cdc25B cooperates with Cdc25A to induce mitosis but has a unique role in activating cyclin B1-Cdk1 at the centrosome. J Cell Biol 171:35–45PubMedCentralPubMedCrossRefGoogle Scholar
  89. Loffler H, Bochtler T, Fritz B, Tews B, Ho AD, Lukas J, Bartek J, Kramer A (2007) DNA damage-induced accumulation of centrosomal Chk1 contributes to its checkpoint function. Cell Cycle 6:2541–2548PubMedCrossRefGoogle Scholar
  90. Loffler H, Fechter A, Liu FY, Poppelreuther S, Kramer A (2013) DNA damage-induced centrosome amplification occurs via excessive formation of centriolar satellites. Oncogene 32:2963–2972PubMedCrossRefGoogle Scholar
  91. Lotti LV, Ottini L, D’Amico C, Gradini R, Cama A, Belleudi F, Frati L, Torrisi MR, Mariani-Costantini R (2002) Subcellular localization of the BRCA1 gene product in mitotic cells. Genes Chromosomes Cancer 35:193–203PubMedCrossRefGoogle Scholar
  92. Lukas J, Lukas C, Bartek J (2011) More than just a focus: the chromatin response to DNA damage and its role in genome integrity maintenance. Nat Cell Biol 13:1161–1169PubMedCrossRefGoogle Scholar
  93. Mahjoub MR, Stearns T (2012) Supernumerary centrosomes nucleate extra cilia and compromise primary cilium signaling. Curr Biol 22:1628–1634PubMedCentralPubMedCrossRefGoogle Scholar
  94. Mardin BR, Agircan FG, Lange C, Schiebel E (2011) Plk1 controls the Nek2A-PP1gamma antagonism in centrosome disjunction. Curr Biol 21:1145–1151PubMedCrossRefGoogle Scholar
  95. Marshall WF, Rosenbaum JL (2000) Are there nucleic acids in the centrosome? Curr Top Dev Biol 49:187–205PubMedCrossRefGoogle Scholar
  96. Matsuo K, Ohsumi K, Iwabuchi M, Kawamata T, Ono Y, Takahashi M (2012) Kendrin is a novel substrate for separase involved in the licensing of centriole duplication. Curr Biol 22:915–921PubMedCrossRefGoogle Scholar
  97. Matsuyama M, Goto H, Kasahara K, Kawakami Y, Nakanishi M, Kiyono T, Goshima N, Inagaki M (2011) Nuclear Chk1 prevents premature mitotic entry. J Cell Sci 124:2113–2119PubMedCrossRefGoogle Scholar
  98. Matsuzawa A, Kanno S, Nakayama M, Mochiduki H, Wei L, Shimaoka T, Furukawa Y, Kato K, Shibata S, Yasui A, Ishioka C, Chiba N (2014) The BRCA1/BARD1-interacting protein OLA1 functions in centrosome regulation. Mol Cell 53:101–114PubMedCrossRefGoogle Scholar
  99. Mayor T, Stierhof YD, Tanaka K, Fry AM, Nigg EA (2000) The centrosomal protein C-Nap1 is required for cell cycle-regulated centrosome cohesion. J Cell Biol 151:837–846PubMedCentralPubMedCrossRefGoogle Scholar
  100. Mennella V, Keszthelyi B, McDonald KL, Chhun B, Kan F, Rogers GC, Huang B, Agard DA (2012) Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat Cell Biol 14:1159–1168PubMedCentralPubMedCrossRefGoogle Scholar
  101. Meraldi P, Honda R, Nigg EA (2002) Aurora-A overexpression reveals tetraploidization as a major route to centrosome amplification in p53−/− cells. EMBO J 21:483–492PubMedCentralPubMedCrossRefGoogle Scholar
  102. Mikule K, Delaval B, Kaldis P, Jurcyzk A, Hergert P, Doxsey S (2007) Loss of centrosome integrity induces p38-p53-p21-dependent G1-S arrest. Nat Cell Biol 9:160–170PubMedCrossRefGoogle Scholar
  103. Moritz M, Braunfeld MB, Guenebaut V, Heuser J, Agard DA (2000) Structure of the gamma-tubulin ring complex: a template for microtubule nucleation. Nat Cell Biol 2:365–370PubMedCrossRefGoogle Scholar
  104. Mussman JG, Horn HF, Carroll PE, Okuda M, Tarapore P, Donehower LA, Fukasawa K (2000) Synergistic induction of centrosome hyperamplification by loss of p53 and cyclin E overexpression. Oncogene 19:1635–1646PubMedCrossRefGoogle Scholar
  105. Nakamura A, Arai H, Fujita N (2009) Centrosomal Aki1 and cohesin function in separase-regulated centriole disengagement. J Cell Biol 187:607–614PubMedCentralPubMedCrossRefGoogle Scholar
  106. Nam HJ, van Deursen JM (2014) Cyclin B2 and p53 control proper timing of centrosome separation. Nat Cell Biol 16:538–549PubMedCentralPubMedCrossRefGoogle Scholar
  107. Niida H, Katsuno Y, Banerjee B, Hande MP, Nakanishi M (2007) Specific role of Chk1 phosphorylations in cell survival and checkpoint activation. Mol Cell Biol 27:2572–2581PubMedCentralPubMedCrossRefGoogle Scholar
  108. Nishi R, Okuda Y, Watanabe E, Mori T, Iwai S, Masutani C, Sugasawa K, Hanaoka F (2005) Centrin 2 stimulates nucleotide excision repair by interacting with xeroderma pigmentosum group C protein. Mol Cell Biol 25:5664–5674PubMedCentralPubMedCrossRefGoogle Scholar
  109. Okada S, Ouchi T (2003) Cell cycle differences in DNA damage-induced BRCA1 phosphorylation affect its subcellular localization. J Biol Chem 278:2015–2020PubMedCrossRefGoogle Scholar
  110. Oliveira RA, Nasmyth K (2013) Cohesin cleavage is insufficient for centriole disengagement in Drosophila. Curr Biol 23:R601–R603PubMedCrossRefGoogle Scholar
  111. Oricchio E, Saladino C, Iacovelli S, Soddu S, Cundari E (2006) ATM is activated by default in mitosis, localizes at centrosomes and monitors mitotic spindle integrity. Cell Cycle 5:88–92PubMedCrossRefGoogle Scholar
  112. Ozaki Y, Matsui H, Asou H, Nagamachi A, Aki D, Honda H, Yasunaga S, Takihara Y, Yamamoto T, Izumi S, Ohsugi M, Inaba T (2012) Poly-ADP ribosylation of Miki by tankyrase-1 promotes centrosome maturation. Mol Cell 47:694–706PubMedCrossRefGoogle Scholar
  113. Pagan JK, Marzio A, Jones MJ, Saraf A, Jallepalli PV, Florens L, Washburn MP, Pagano M (2015) Degradation of Cep68 and PCNT cleavage mediate Cep215 removal from the PCM to allow centriole separation, disengagement and licensing. Nat Cell Biol 17:31–43PubMedCentralPubMedCrossRefGoogle Scholar
  114. Paintrand M, Moudjou M, Delacroix H, Bornens M (1992) Centrosome organization and centriole architecture: their sensitivity to divalent cations. J Struct Biol 108:107–128PubMedCrossRefGoogle Scholar
  115. Palazzo RE, Vogel JM, Schnackenberg BJ, Hull DR, Wu X (2000) Centrosome maturation. Curr Top Dev Biol 49:449–470PubMedCrossRefGoogle Scholar
  116. Pan YR, Lee EY (2009) UV-dependent interaction between Cep164 and XPA mediates localization of Cep164 at sites of DNA damage and UV sensitivity. Cell Cycle 8:655–664PubMedCrossRefGoogle Scholar
  117. Paoletti A, Moudjou M, Paintrand M, Salisbury JL, Bornens M (1996) Most of centrin in animal cells is not centrosome-associated and centrosomal centrin is confined to the distal lumen of centrioles. J Cell Sci 109(Pt 13):3089–3102PubMedGoogle Scholar
  118. Piane M, Della Monica M, Piatelli G, Lulli P, Lonardo F, Chessa L, Scarano G (2009) Majewski osteodysplastic primordial dwarfism type II (MOPD II) syndrome previously diagnosed as Seckel syndrome: report of a novel mutation of the PCNT gene. Am J Med Genet A 149A:2452–2456PubMedCrossRefGoogle Scholar
  119. Piel M, Meyer P, Khodjakov A, Rieder CL, Bornens M (2000) The respective contributions of the mother and daughter centrioles to centrosome activity and behaviour in vertebrate cells. J Cell Biol 149:317–330PubMedCentralPubMedCrossRefGoogle Scholar
  120. Prosser SL, Morrison CG (2015) Centrin2 regulates CP110 removal in primary cilium formation. J Cell Biol 208:693–701PubMedCentralPubMedCrossRefGoogle Scholar
  121. Prosser SL, Straatman KR, Fry AM (2009) Molecular dissection of the centrosome overduplication pathway in S-phase-arrested cells. Mol Cell Biol 29:1760–1773PubMedCentralPubMedCrossRefGoogle Scholar
  122. Prosser SL, Samant MD, Baxter JE, Morrison CG, Fry AM (2012) Oscillation of APC/C activity during cell cycle arrest promotes centrosome amplification. J Cell Sci 125:5353–5368PubMedCentralPubMedCrossRefGoogle Scholar
  123. Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, Galova M, Petronczki M, Gregan J, Cetin B, Mudrak I, Ogris E, Mechtler K, Pelletier L, Buchholz F, Shirahige K, Nasmyth K (2006) Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441:53–61PubMedCrossRefGoogle Scholar
  124. Riley T, Sontag E, Chen P, Levine A (2008) Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 9:402–412PubMedCrossRefGoogle Scholar
  125. Rogers GC, Rusan NM, Roberts DM, Peifer M, Rogers SL (2009) The SCF Slimb ubiquitin ligase regulates Plk4/Sak levels to block centriole reduplication. J Cell Biol 184:225–239PubMedCentralPubMedCrossRefGoogle Scholar
  126. Saladino C, Bourke E, Conroy PC, Morrison CG (2009) Centriole separation in DNA damage-induced centrosome amplification. Environ Mol Mutagen 50:725–732PubMedCrossRefGoogle Scholar
  127. Saladino C, Bourke E, Morrison CG (2012) Centrosomes, DNA damage and aneuploidy. In: Schatten H (ed) The centrosome: cell and molecular mechanisms of functions and dysfunctions in disease, 13. Humana Press, New York, pp 223–243CrossRefGoogle Scholar
  128. Sanchez Y, Wong C, Thoma RS, Richman R, Wu Z, Piwnica-Worms H, Elledge SJ (1997) Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science 277:1497–1501PubMedCrossRefGoogle Scholar
  129. Sankaran S, Starita LM, Groen AC, Ko MJ, Parvin JD (2005) Centrosomal microtubule nucleation activity is inhibited by BRCA1-dependent ubiquitination. Mol Cell Biol 25:8656–8668PubMedCentralPubMedCrossRefGoogle Scholar
  130. Sato N, Mizumoto K, Nakamura M, Tanaka M (2000) Radiation-induced centrosome overduplication and multiple mitotic spindles in human tumor cells. Exp Cell Res 255:321–326PubMedCrossRefGoogle Scholar
  131. Savage KI, Harkin DP (2015) BRCA1, a ‘complex’ protein involved in the maintenance of genomic stability. FEBS J 282:630–646PubMedCrossRefGoogle Scholar
  132. Schmidt KN, Kuhns S, Neuner A, Hub B, Zentgraf H, Pereira G (2012) Cep164 mediates vesicular docking to the mother centriole during early steps of ciliogenesis. J Cell Biol 199:1083–1101PubMedCentralPubMedCrossRefGoogle Scholar
  133. 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 13:966–972PubMedCrossRefGoogle Scholar
  134. Schreiber V, Dantzer F, Ame JC, de Murcia G (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7:517–528PubMedCrossRefGoogle Scholar
  135. Shukla A, Kong D, Sharma M, Magidson V, Loncarek J (2015) Plk1 relieves centriole block to reduplication by promoting daughter centriole maturation. Nat Commun 6:8077PubMedCentralPubMedCrossRefGoogle Scholar
  136. Sibon OC, Kelkar A, Lemstra W, Theurkauf WE (2000) DNA-replication/DNA-damage-dependent centrosome inactivation in Drosophila embryos. Nat Cell Biol 2:90–95PubMedCrossRefGoogle Scholar
  137. Sir JH, Putz M, Daly O, Morrison CG, Dunning M, Kilmartin JV, Gergely F (2013) Loss of centrioles causes chromosomal instability in vertebrate somatic cells. J Cell Biol 203:747–756PubMedCentralPubMedCrossRefGoogle Scholar
  138. Sivasubramaniam S, Sun X, Pan YR, Wang S, Lee EY (2008) Cep164 is a mediator protein required for the maintenance of genomic stability through modulation of MDC1, RPA, and CHK1. Genes Dev 22:587–600PubMedCentralPubMedCrossRefGoogle Scholar
  139. Slaats GG, Ghosh AK, Falke LL, Le Corre S, Shaltiel IA, van de Hoek G, Klasson TD, Stokman MF, Logister I, Verhaar MC, Goldschmeding R, Nguyen TQ, Drummond IA, Hildebrandt F, Giles RH (2014) Nephronophthisis-associated CEP164 regulates cell cycle progression, apoptosis and epithelial-to-mesenchymal transition. PLoS Genet 10, e1004594PubMedCentralPubMedCrossRefGoogle Scholar
  140. Smith S, de Lange T (1999) Cell cycle dependent localization of the telomeric PARP, tankyrase, to nuclear pore complexes and centrosomes. J Cell Sci 112:3649–3656PubMedGoogle Scholar
  141. Smits VA, Klompmaker R, Arnaud L, Rijksen G, Nigg EA, Medema RH (2000) Polo-like kinase-1 is a target of the DNA damage checkpoint. Nat Cell Biol 2:672–676PubMedCrossRefGoogle Scholar
  142. Sonnen KF, Schermelleh L, Leonhardt H, Nigg EA (2012) 3D-structured illumination microscopy provides novel insight into architecture of human centrosomes. Biol Open 1:965–976PubMedCentralPubMedCrossRefGoogle Scholar
  143. Sorino C, Bruno T, Desantis A, Di Certo MG, Iezzi S, De Nicola F, Catena V, Floridi A, Chessa L, Passananti C, Cundari E, Fanciulli M (2013) Centrosomal Che-1 protein is involved in the regulation of mitosis and DNA damage response by mediating pericentrin (PCNT)-dependent Chk1 protein localization. J Biol Chem 288:23348–23357PubMedCentralPubMedCrossRefGoogle Scholar
  144. Staples CJ, Myers KN, Beveridge RD, Patil AA, Lee AJ, Swanton C, Howell M, Boulton SJ, Collis SJ (2012) The centriolar satellite protein Cep131 is important for genome stability. J Cell Sci 125:4770–4779PubMedCrossRefGoogle Scholar
  145. Staples CJ, Myers KN, Beveridge RD, Patil AA, Howard AE, Barone G, Lee AJ, Swanton C, Howell M, Maslen S, Skehel JM, Boulton SJ, Collis SJ (2014) Ccdc13 is a novel human centriolar satellite protein required for ciliogenesis and genome stability. J Cell Sci 127:2910–2919PubMedCrossRefGoogle Scholar
  146. Starita LM, Machida Y, Sankaran S, Elias JE, Griffin K, Schlegel BP, Gygi SP, Parvin JD (2004) BRCA1-dependent ubiquitination of gamma-tubulin regulates centrosome number. Mol Cell Biol 24:8457–8466PubMedCentralPubMedCrossRefGoogle Scholar
  147. Stevens NR, Roque H, Raff JW (2010) DSas-6 and Ana2 coassemble into tubules to promote centriole duplication and engagement. Dev Cell 19:913–919PubMedCentralPubMedCrossRefGoogle Scholar
  148. Sugasawa K, Ng JM, Masutani C, Iwai S, van der Spek PJ, Eker AP, Hanaoka F, Bootsma D, Hoeijmakers JH (1998) Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol Cell 2:223–232PubMedCrossRefGoogle Scholar
  149. Sugihara E, Kanai M, Saito S, Nitta T, Toyoshima H, Nakayama K, Nakayama KI, Fukasawa K, Schwab M, Saya H, Miwa M (2006) Suppression of centrosome amplification after DNA damage depends on p27 accumulation. Cancer Res 66:4020–4029PubMedCrossRefGoogle Scholar
  150. Suzuki K, Morimoto M, Yamauchi M, Yoshida H, Kodama S, Tsukamoto K, Watanabe M (2006) Non-specific detection of the centrosomes by antibodies recognizing phosphorylated ATM at serine 1981. Cell Cycle 5:1008–1009, author reply 1010PubMedCrossRefGoogle Scholar
  151. Takada S, Kelkar A, Theurkauf WE (2003) Drosophila checkpoint kinase 2 couples centrosome function and spindle assembly to genomic integrity. Cell 113:87–99PubMedCrossRefGoogle Scholar
  152. Tanenbaum ME, Medema RH (2010) Mechanisms of centrosome separation and bipolar spindle assembly. Dev Cell 19:797–806PubMedCrossRefGoogle Scholar
  153. Tarapore P, Fukasawa K (2002) Loss of p53 and centrosome hyperamplification. Oncogene 21:6234–6240PubMedCrossRefGoogle Scholar
  154. Tarapore P, Horn HF, Tokuyama Y, Fukasawa K (2001) Direct regulation of the centrosome duplication cycle by the p53-p21Waf1/Cip1 pathway. Oncogene 20:3173–3184PubMedCrossRefGoogle Scholar
  155. Tarapore P, Hanashiro K, Fukasawa K (2012) Analysis of centrosome localization of BRCA1 and its activity in suppressing centrosomal aster formation. Cell Cycle 11:2931–2946PubMedCentralPubMedCrossRefGoogle Scholar
  156. Thein KH, Kleylein-Sohn J, Nigg EA, Gruneberg U (2007) Astrin is required for the maintenance of sister chromatid cohesion and centrosome integrity. J Cell Biol 178:345–354PubMedCentralPubMedCrossRefGoogle Scholar
  157. Tibelius A, Marhold J, Zentgraf H, Heilig CE, Neitzel H, Ducommun B, Rauch A, Ho AD, Bartek J, Kramer A (2009) Microcephalin and pericentrin regulate mitotic entry via centrosome-associated Chk1. J Cell Biol 185:1149–1157PubMedCentralPubMedCrossRefGoogle Scholar
  158. Tollenaere MA, Mailand N, Bekker-Jensen S (2015) Centriolar satellites: key mediators of centrosome functions. Cell Mol Life Sci 72:11–23PubMedCrossRefGoogle Scholar
  159. Tritarelli A, Oricchio E, Ciciarello M, Mangiacasale R, Palena A, Lavia P, Soddu S, Cundari E (2004) p53 localization at centrosomes during mitosis and postmitotic checkpoint are ATM-dependent and require serine 15 phosphorylation. Mol Biol Cell 15:3751–3757PubMedCentralPubMedCrossRefGoogle Scholar
  160. Tsou MF, Stearns T (2006) Mechanism limiting centrosome duplication to once per cell cycle. Nature 442:947–951PubMedCrossRefGoogle Scholar
  161. Tsou MF, Wang WJ, George KA, Uryu K, Stearns T, Jallepalli PV (2009) Polo kinase and separase regulate the mitotic licensing of centriole duplication in human cells. Dev Cell 17:344–354PubMedCentralPubMedCrossRefGoogle Scholar
  162. Tsvetkov L, Xu X, Li J, Stern DF (2003) Polo-like kinase 1 and Chk2 interact and co-localize to centrosomes and the midbody. J Biol Chem 278:8468–8475PubMedCrossRefGoogle Scholar
  163. Uetake Y, Loncarek J, Nordberg JJ, English CN, La Terra S, Khodjakov A, Sluder G (2007) Cell cycle progression and de novo centriole assembly after centrosomal removal in untransformed human cells. J Cell Biol 176:173–182PubMedCentralPubMedCrossRefGoogle Scholar
  164. Uto K, Inoue D, Shimuta K, Nakajo N, Sagata N (2004) Chk1, but not Chk2, inhibits Cdc25 phosphatases by a novel common mechanism. EMBO J 23:3386–3396PubMedCentralPubMedCrossRefGoogle Scholar
  165. van Vugt MA, Smits VA, Klompmaker R, Medema RH (2001) Inhibition of Polo-like kinase-1 by DNA damage occurs in an ATM- or ATR-dependent fashion. J Biol Chem 276:41656–41660PubMedCrossRefGoogle Scholar
  166. Villumsen BH, Danielsen JR, Povlsen L, Sylvestersen KB, Merdes A, Beli P, Yang YG, Choudhary C, Nielsen ML, Mailand N, Bekker-Jensen S (2013) A new cellular stress response that triggers centriolar satellite reorganization and ciliogenesis. EMBO J 32:3029–3040PubMedCentralPubMedCrossRefGoogle Scholar
  167. Vorobjev IA, Chentsov Yu S (1982) Centrioles in the cell cycle. I. Epithelial cells. J Cell Biol 93:938–949PubMedCrossRefGoogle Scholar
  168. Wang X, Yang Y, Duan Q, Jiang N, Huang Y, Darzynkiewicz Z, Dai W (2008) sSgo1, a major splice variant of Sgo1, functions in centriole cohesion where it is regulated by PIk1. Dev Cell 14:331–341PubMedCentralPubMedCrossRefGoogle Scholar
  169. Wang WJ, Soni RK, Uryu K, Tsou MF (2011) The conversion of centrioles to centrosomes: essential coupling of duplication with segregation. J Cell Biol 193:727–739PubMedCentralPubMedCrossRefGoogle Scholar
  170. Wang CY, Huang EY, Huang SC, Chung BC (2015) DNA-PK/Chk2 induces centrosome amplification during prolonged replication stress. Oncogene 34:1263–1269PubMedCrossRefGoogle Scholar
  171. Wiese C, Zheng Y (2000) A new function for the gamma-tubulin ring complex as a microtubule minus-end cap. Nat Cell Biol 2:358–364PubMedCrossRefGoogle Scholar
  172. Wilsker D, Petermann E, Helleday T, Bunz F (2008) Essential function of Chk1 can be uncoupled from DNA damage checkpoint and replication control. Proc Natl Acad Sci U S A 105:20752–20757PubMedCentralPubMedCrossRefGoogle Scholar
  173. Wong RW, Blobel G (2008) Cohesin subunit SMC1 associates with mitotic microtubules at the spindle pole. Proc Natl Acad Sci U S A 105:15441–15445PubMedCentralPubMedCrossRefGoogle Scholar
  174. Wong YL, Anzola JV, Davis RL, Yoon M, Motamedi A, Kroll A, Seo CP, Hsia JE, Kim SK, Mitchell JW, Mitchell BJ, Desai A, Gahman TC, Shiau AK, Oegema K (2015) Reversible centriole depletion with an inhibitor of Polo-like kinase 4. Science 348:1155–1160PubMedCrossRefGoogle Scholar
  175. Woodruff JB, Wueseke O, Hyman AA (2014) Pericentriolar material structure and dynamics. Philos Trans R Soc Lond B Biol Sci 369:20130459PubMedCentralPubMedCrossRefGoogle Scholar
  176. Woodruff JB, Wueseke O, Viscardi V, Mahamid J, Ochoa SD, Bunkenborg J, Widlund PO, Pozniakovsky A, Zanin E, Bahmanyar S, Zinke A, Hong SH, Decker M, Baumeister W, Andersen JS, Oegema K, Hyman AA (2015) Centrosomes. Regulated assembly of a supramolecular centrosome scaffold in vitro. Science 348:808–812PubMedCrossRefGoogle Scholar
  177. Xu X, Weaver Z, Linke SP, Li C, Gotay J, Wang XW, Harris CC, Ried T, Deng CX (1999) Centrosome amplification and a defective G2-M cell cycle checkpoint induce genetic instability in BRCA1 exon 11 isoform-deficient cells. Mol Cell 3:389–395PubMedCrossRefGoogle Scholar
  178. Yang J, Adamian M, Li T (2006) Rootletin interacts with C-Nap1 and may function as a physical linker between the pair of centrioles/basal bodies in cells. Mol Biol Cell 17:1033–1040PubMedCentralPubMedCrossRefGoogle Scholar
  179. Zhang W, Fletcher L, Muschel RJ (2005) The role of Polo-like kinase 1 in the inhibition of centrosome separation after ionizing radiation. J Biol Chem 280:42994–42999PubMedCrossRefGoogle Scholar
  180. Zhang S, Hemmerich P, Grosse F (2007) Centrosomal localization of DNA damage checkpoint proteins. J Cell Biochem 101:451–465PubMedCrossRefGoogle Scholar
  181. Zheng Y, Wong ML, Alberts B, Mitchison T (1995) Nucleation of microtubule assembly by a gamma-tubulin-containing ring complex. Nature 378:578–583PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Centre for Chromosome Biology, School of Natural SciencesNational University of Ireland GalwayGalwayIreland

Personalised recommendations