Sld5 Ensures Centrosomal Resistance to Congression Forces by Preserving Centriolar Satellites

REFERENCES

• Wood KW, Sakowicz R, Goldstein LS, Cleveland DW. 1997. CENP-E is a plus end-directed kinetochore motor required for metaphase chromosome alignment. Cell 91:357–366. https://doi.org/10.1016/S0092-8674(00)80419-5.
   PubMed Web of Science ®Google Scholar
• Goshima G, Vale RD. 2003. The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. J Cell Biol 162:1003–1016. https://doi.org/10.1083/jcb.200303022.
   PubMed Web of Science ®Google Scholar
• Kops GJ, Saurin AT, Meraldi P. 2010. Finding the middle ground: how kinetochores power chromosome congression. Cell Mol Life Sci 67:2145–2161. https://doi.org/10.1007/s00018-010-0321-y.
   PubMed Web of Science ®Google Scholar
• Walczak CE, Cai S, Khodjakov A. 2010. Mechanisms of chromosome behaviour during mitosis. Nat Rev Mol Cell Biol 11:91–102. https://doi.org/10.1038/nrm2832.
   PubMed Web of Science ®Google Scholar
• Skibbens RV, Skeen VP, Salmon ED. 1993. Directional instability of kinetochore motility during chromosome congression and segregation in mitotic newt lung cells: a push-pull mechanism. J Cell Biol 122:859–875. https://doi.org/10.1083/jcb.122.4.859.
   PubMed Web of Science ®Google Scholar
• Kapoor TM, Lampson MA, Hergert P, Cameron L, Cimini D, Salmon ED, McEwen BF, Khodjakov A. 2006. Chromosomes can congress to the metaphase plate before biorientation. Science 311:388–391. https://doi.org/10.1126/science.1122142.
   PubMed Web of Science ®Google Scholar
• Su X, Arellano-Santoyo H, Portran D, Gaillard J, Vantard M, Thery M, Pellman D. 2013. Microtubule-sliding activity of a kinesin-8 promotes spindle assembly and spindle-length control. Nat Cell Biol 15:948–957. https://doi.org/10.1038/ncb2801.
   PubMed Web of Science ®Google Scholar
• Rieder CL, Salmon ED. 1994. Motile kinetochores and polar ejection forces dictate chromosome position on the vertebrate mitotic spindle. J Cell Biol 124:223–233. https://doi.org/10.1083/jcb.124.3.223.
   PubMed Web of Science ®Google Scholar
• Wandke C, Barisic M, Sigl R, Rauch V, Wolf F, Amaro AC, Tan CH, Pereira AJ, Kutay U, Maiato H, Meraldi P, Geley S. 2012. Human chromokinesins promote chromosome congression and spindle microtubule dynamics during mitosis. J Cell Biol 198:847–863. https://doi.org/10.1083/jcb.201110060.
   PubMed Web of Science ®Google Scholar
• Iemura K, Tanaka K. 2015. Chromokinesin Kid and kinetochore kinesin CENP-E differentially support chromosome congression without end-on attachment to microtubules. Nat Commun 6:6447. https://doi.org/10.1038/ncomms7447.
   PubMed Web of Science ®Google Scholar
• Shrestha RL, Draviam VM. 2013. Lateral to end-on conversion of chromosome-microtubule attachment requires kinesins CENP-E and MCAK. Curr Biol 23:1514–1526. https://doi.org/10.1016/j.cub.2013.06.040.
   PubMed Web of Science ®Google Scholar
• Cai S, O'Connell CB, Khodjakov A, Walczak CE. 2009. Chromosome congression in the absence of kinetochore fibres. Nat Cell Biol 11:832–838. https://doi.org/10.1038/ncb1890.
   PubMed Web of Science ®Google Scholar
• Levesque AA, Compton DA. 2001. The chromokinesin Kid is necessary for chromosome arm orientation and oscillation, but not congression, on mitotic spindles. J Cell Biol 154:1135–1146. https://doi.org/10.1083/jcb.200106093.
   PubMed Web of Science ®Google Scholar
• McDonald HB, Stewart RJ, Goldstein LS. 1990. The kinesin-like ncd protein of Drosophila is a minus end-directed microtubule motor. Cell 63:1159–1165. https://doi.org/10.1016/0092-8674(90)90412-8.
   PubMed Web of Science ®Google Scholar
• Oshimori N, Ohsugi M, Yamamoto T. 2006. The Plk1 target Kizuna stabilizes mitotic centrosomes to ensure spindle bipolarity. Nat Cell Biol 8:1095–1101. https://doi.org/10.1038/ncb1474.
   PubMed Web of Science ®Google Scholar
• Logarinho E, Maffini S, Barisic M, Marques A, Toso A, Meraldi P, Maiato H. 2012. CLASPs prevent irreversible multipolarity by ensuring spindle-pole resistance to traction forces during chromosome alignment. Nat Cell Biol 14:295–303. https://doi.org/10.1038/ncb2423.
   PubMed Web of Science ®Google Scholar
• Kim K, Rhee K. 2011. The pericentriolar satellite protein CEP90 is crucial for integrity of the mitotic spindle pole. J Cell Sci 124:338–347. https://doi.org/10.1242/jcs.078329.
   PubMed Web of Science ®Google Scholar
• Lopes CA, Prosser SL, Romio L, Hirst RA, O'Callaghan C, Woolf AS, Fry AM. 2011. Centriolar satellites are assembly points for proteins implicated in human ciliopathies, including oral-facial-digital syndrome 1. J Cell Sci 124:600–612. https://doi.org/10.1242/jcs.077156.
   PubMed Web of Science ®Google Scholar
• Kubo A, Sasaki H, Yuba-Kubo A, Tsukita S, Shiina N. 1999. Centriolar satellites: molecular characterization, ATP-dependent movement toward centrioles and possible involvement in ciliogenesis. J Cell Biol 147:969–980. https://doi.org/10.1083/jcb.147.5.969.
   PubMed Web of Science ®Google Scholar
• Dmowski M, Fijalkowska IJ. 2017. Diverse roles of Dpb2, the non-catalytic subunit of DNA polymerase epsilon. Curr Genet 63:983–987. https://doi.org/10.1007/s00294-017-0706-7.
   PubMed Web of Science ®Google Scholar
• Zou L, Elledge SJ. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542–1548. https://doi.org/10.1126/science.1083430.
   PubMed Web of Science ®Google Scholar
• Knockleby J, Lee H. 2010. Same partners, different dance: involvement of DNA replication proteins in centrosome regulation. Cell Cycle 9:4487–4491. https://doi.org/10.4161/cc.9.22.14047.
   PubMed Web of Science ®Google Scholar
• Prasanth SG, Prasanth KV, Siddiqui K, Spector DL, Stillman B. 2004. Human Orc2 localizes to centrosomes, centromeres and heterochromatin during chromosome inheritance. EMBO J 23:2651–2663. https://doi.org/10.1038/sj.emboj.7600255.
   PubMed Web of Science ®Google Scholar
• Ferguson RL, Maller JL. 2008. Cyclin E-dependent localization of MCM5 regulates centrosome duplication. J Cell Sci 121:3224–3232. https://doi.org/10.1242/jcs.034702.
   PubMed Web of Science ®Google Scholar
• Ferguson RL, Pascreau G, Maller JL. 2010. The cyclin A centrosomal localization sequence recruits MCM5 and Orc1 to regulate centrosome reduplication. J Cell Sci 123:2743–2749. https://doi.org/10.1242/jcs.073098.
   PubMed Web of Science ®Google Scholar
• Prasanth SG, Prasanth KV, Stillman B. 2002. Orc6 involved in DNA replication, chromosome segregation, and cytokinesis. Science 297:1026–1031. https://doi.org/10.1126/science.1072802.
   PubMed Web of Science ®Google Scholar
• Hemerly AS, Prasanth SG, Siddiqui K, Stillman B. 2009. Orc1 controls centriole and centrosome copy number in human cells. Science 323:789–793. https://doi.org/10.1126/science.1166745.
   PubMed Web of Science ®Google Scholar
• Chang YP, Wang G, Bermudez V, Hurwitz J, Chen XS. 2007. Crystal structure of the GINS complex and functional insights into its role in DNA replication. Proc Natl Acad Sci U S A 104:12685–12690. https://doi.org/10.1073/pnas.0705558104.
   PubMed Web of Science ®Google Scholar
• Kamada K, Kubota Y, Arata T, Shindo Y, Hanaoka F. 2007. Structure of the human GINS complex and its assembly and functional interface in replication initiation. Nat Struct Mol Biol 14:388–396. https://doi.org/10.1038/nsmb1231.
   PubMed Web of Science ®Google Scholar
• Gouge CA, Christensen TW. 2010. Drosophila Sld5 is essential for normal cell cycle progression and maintenance of genomic integrity. Biochem Biophys Res Commun 400:145–150. https://doi.org/10.1016/j.bbrc.2010.08.033.
   PubMed Web of Science ®Google Scholar
• Vaziri C, Saxena S, Jeon Y, Lee C, Murata K, Machida Y, Wagle N, Hwang DS, Dutta A. 2003. A p53-dependent checkpoint pathway prevents rereplication. Mol Cell 11:997–1008. https://doi.org/10.1016/S1097-2765(03)00099-6.
   PubMed Web of Science ®Google Scholar
• Liu E, Lee AY, Chiba T, Olson E, Sun P, Wu X. 2007. The ATR-mediated S phase checkpoint prevents rereplication in mammalian cells when licensing control is disrupted. J Cell Biol 179:643–657. https://doi.org/10.1083/jcb.200704138.
   PubMed Web of Science ®Google Scholar
• Tatsumi Y, Sugimoto N, Yugawa T, Narisawa-Saito M, Kiyono T, Fujita M. 2006. Deregulation of Cdt1 induces chromosomal damage without rereplication and leads to chromosomal instability. J Cell Sci 119:3128–3140. https://doi.org/10.1242/jcs.03031.
   PubMed Web of Science ®Google Scholar
• Canitrot Y, Frechet M, Servant L, Cazaux C, Hoffmann JS. 1999. Overexpression of DNA polymerase beta: a genomic instability enhancer process. FASEB J 13:1107–1111.
   PubMed Web of Science ®Google Scholar
• Chan K, Houlbrook S, Zhang QM, Harrison M, Hickson ID, Dianov GL. 2007. Overexpression of DNA polymerase beta results in an increased rate of frameshift mutations during base excision repair. Mutagenesis 22:183–188. https://doi.org/10.1093/mutage/gel070.
   PubMed Web of Science ®Google Scholar
• Aparicio T, Guillou E, Coloma J, Montoya G, Mendez J. 2009. The human GINS complex associates with Cdc45 and MCM and is essential for DNA replication. Nucleic Acids Res 37:2087–2095. https://doi.org/10.1093/nar/gkp065.
   PubMed Web of Science ®Google Scholar
• Borel F, Lohez OD, Lacroix FB, Margolis RL. 2002. Multiple centrosomes arise from tetraploidy checkpoint failure and mitotic centrosome clusters in p53 and RB pocket protein-compromised cells. Proc Natl Acad Sci U S A 99:9819–9824. https://doi.org/10.1073/pnas.152205299.
   PubMed Web of Science ®Google Scholar
• Dodson H, Bourke E, Jeffers LJ, Vagnarelli P, Sonoda E, Takeda S, Earnshaw WC, Merdes A, Morrison C. 2004. Centrosome amplification induced by DNA damage occurs during a prolonged G2 phase and involves ATM. EMBO J 23:3864–3873. https://doi.org/10.1038/sj.emboj.7600393.
   PubMed Web of Science ®Google Scholar
• 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 21:3866–3877. https://doi.org/10.1091/mbc.E10-02-0124.
   PubMed Web of Science ®Google Scholar
• 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 14:1993–2004. https://doi.org/10.1091/mbc.E02-08-0510.
   PubMed Web of Science ®Google Scholar
• Dammermann A, Merdes A. 2002. Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J Cell Biol 159:255–266. https://doi.org/10.1083/jcb.200204023.
   PubMed Web of Science ®Google Scholar
• Lee MJ, Gergely F, Jeffers K, Peak-Chew SY, Raff JW. 2001. Msps/XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behaviour. Nat Cell Biol 3:643–649. https://doi.org/10.1038/35083033.
   PubMed Web of Science ®Google Scholar
• Guarguaglini G, Duncan PI, Stierhof YD, Holmstrom T, Duensing S, Nigg EA. 2005. The forkhead-associated domain protein Cep170 interacts with Polo-like kinase 1 and serves as a marker for mature centrioles. Mol Biol Cell 16:1095–1107. https://doi.org/10.1091/mbc.E04-10-0939.
   PubMed Web of Science ®Google Scholar
• Ishikawa H, Kubo A, Tsukita S, Tsukita S. 2005. Odf2-deficient mother centrioles lack distal/subdistal appendages and the ability to generate primary cilia. Nat Cell Biol 7:517–524. https://doi.org/10.1038/ncb1251.
   PubMed Web of Science ®Google Scholar
• Lawo S, Hasegan M, Gupta GD, Pelletier L. 2012. Subdiffraction imaging of centrosomes reveals higher-order organizational features of pericentriolar material. Nat Cell Biol 14:1148–1158. https://doi.org/10.1038/ncb2591.
   PubMed Web of Science ®Google Scholar
• Sharp DJ, Rogers GC, Scholey JM. 2000. Microtubule motors in mitosis. Nature 407:41–47. https://doi.org/10.1038/35024000.
   PubMed Web of Science ®Google Scholar
• Gorbsky GJ. 2013. Cohesion fatigue. Curr Biol 23:R986–R988. https://doi.org/10.1016/j.cub.2013.08.017.
   PubMed Web of Science ®Google Scholar
• Agircan FG, Schiebel E. 2014. Sensors at centrosomes reveal determinants of local separase activity. PLoS Genet 10:e1004672. https://doi.org/10.1371/journal.pgen.1004672.
   Google Scholar
• Yao X, Abrieu A, Zheng Y, Sullivan KF, Cleveland DW. 2000. CENP-E forms a link between attachment of spindle microtubules to kinetochores and the mitotic checkpoint. Nat Cell Biol 2:484–491. https://doi.org/10.1038/35019518.
   PubMed Web of Science ®Google Scholar
• Cai S, Weaver LN, Ems-McClung SC, Walczak CE. 2009. Kinesin-14 family proteins HSET/XCTK2 control spindle length by cross-linking and sliding microtubules. Mol Biol Cell 20:1348–1359. https://doi.org/10.1091/mbc.E08-09-0971.
   PubMed Web of Science ®Google Scholar
• Ganem NJ, Godinho SA, Pellman D. 2009. A mechanism linking extra centrosomes to chromosomal instability. Nature 460:278–282. https://doi.org/10.1038/nature08136.
   PubMed Web of Science ®Google Scholar
• Brinkley BR, Cox SM, Pepper DA, Wible L, Brenner SL, Pardue RL. 1981. Tubulin assembly sites and the organization of cytoplasmic microtubules in cultured mammalian cells. J Cell Biol 90:554–562. https://doi.org/10.1083/jcb.90.3.554.
   PubMed Web of Science ®Google Scholar
• Kubo A, Tsukita S. 2003. Non-membranous granular organelle consisting of PCM-1: subcellular distribution and cell-cycle-dependent assembly/disassembly. J Cell Sci 116:919–928. https://doi.org/10.1242/jcs.00282.
   PubMed Web of Science ®Google Scholar
• 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 32:3029–3040. https://doi.org/10.1038/emboj.2013.223.
   PubMed Web of Science ®Google Scholar
• MacNeill SA. 2010. Structure and function of the GINS complex, a key component of the eukaryotic replisome. Biochem J 425:489–500. https://doi.org/10.1042/BJ20091531.
   PubMed Web of Science ®Google Scholar
• Huang HK, Bailis JM, Leverson JD, Gomez EB, Forsburg SL, Hunter T. 2005. Suppressors of Bir1p (Survivin) identify roles for the chromosomal passenger protein Pic1p (INCENP) and the replication initiation factor Psf2p in chromosome segregation. Mol Cell Biol 25:9000–9015. https://doi.org/10.1128/MCB.25.20.9000-9015.2005.
   PubMed Web of Science ®Google Scholar
• Barkley LR, Song IY, Zou Y, Vaziri C. 2009. Reduced expression of GINS complex members induces hallmarks of pre-malignancy in primary untransformed human cells. Cell Cycle 8:1577–1588. https://doi.org/10.4161/cc.8.10.8535.
   PubMed Web of Science ®Google Scholar
• Ibarra A, Schwob E, Mendez J. 2008. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc Natl Acad Sci U S A 105:8956–8961. https://doi.org/10.1073/pnas.0803978105.
   PubMed Web of Science ®Google Scholar