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Research Article

ATAD5 suppresses centrosome over-duplication by regulating UAF1 and ID1

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Pages 1952-1968 | Received 28 Nov 2019, Accepted 10 May 2020, Published online: 28 Jun 2020

References

  • Doxsey S, McCollum D, Theurkauf W. Centrosomes in cellular regulation. Annu Rev Cell Dev Biol. 2005;21(1):411–434.
  • Nam HJ, Naylor RM, van Deursen JM. Centrosome dynamics as a source of chromosomal instability. Trends Cell Biol. 2015;25:65–73.
  • Fu J, Hagan IM, Glover DM. The centrosome and its duplication cycle. Cold Spring Harb Perspect Biol. 2015;7:a015800.
  • Gonczy P. Centrosomes and cancer: revisiting a long-standing relationship. Nat Rev Cancer. 2015;15:639–652.
  • Nigg EA, Cajanek L, Arquint C. The centrosome duplication cycle in health and disease. FEBS Lett. 2014;588:2366–2372.
  • Vitre BD, Cleveland DW. Centrosomes, chromosome instability (CIN) and aneuploidy. Curr Opin Cell Biol. 2012;24:809–815.
  • Hemerly AS, Prasanth SG, Siddiqui K, et al. Orc1 controls centriole and centrosome copy number in human cells. Science. 2009;323(5915):789–793.
  • Prasanth SG, Prasanth KV, Siddiqui K, et al. Human Orc2 localizes to centrosomes, centromeres and heterochromatin during chromosome inheritance. EMBO J. 2004;23(13):2651–2663.
  • Xu X, Huang S, Zhang B, et al. DNA replication licensing factor Cdc6 and Plk4 kinase antagonistically regulate centrosome duplication via Sas-6. Nat Commun. 2017;8(1):15164.
  • Ferguson RL, Maller JL. Cyclin E-dependent localization of MCM5 regulates centrosome duplication. J Cell Sci. 2008;121(19):3224–3232.
  • Bang SW, Ko MJ, Kang S, et al. Human TopBP1 localization to the mitotic centrosome mediates mitotic progression. Exp Cell Res. 2011;317(7):994–1004.
  • Perk J, Iavarone A, Benezra R. Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer. 2005;5(8):603–614.
  • Hasskarl J, Duensing S, Manuel E, et al. The helix-loop-helix protein ID1 localizes to centrosomes and rapidly induces abnormal centrosome numbers. Oncogene. 2004;23:1930–1938.
  • Manthey C, Mern DS, Gutmann A, et al. Elevated endogenous expression of the dominant negative basic helix-loop-helix protein ID1 correlates with significant centrosome abnormalities in human tumor cells. BMC Cell Biol. 2010;11:2.
  • Hasskarl J, Mern DS, Munger K. Interference of the dominant negative helix-loop-helix protein ID1 with the proteasomal subunit S5A causes centrosomal abnormalities. Oncogene. 2008;27:1657–1664.
  • Man C, Rosa J, Yip YL, et al. Id1 overexpression induces tetraploidization and multiple abnormal mitotic phenotypes by modulating aurora A. Mol Biol Cell. 2008;19:2389–2401.
  • Jung JK, Jang SW, Kim JM. A novel role for the deubiquitinase USP1 in the control of centrosome duplication. Cell Cycle. 2016;15:584–592.
  • Williams SA, Maecker HL, French DM, et al. USP1 deubiquitinates ID proteins to preserve a mesenchymal stem cell program in osteosarcoma. Cell. 2011;146:918–930.
  • Kubota T, Myung K, Donaldson AD. Is PCNA unloading the central function of the Elg1/ATAD5 replication factor C-like complex? Cell Cycle. 2013;12:2570–2579.
  • Fox JT, Lee KY, Myung K. Dynamic regulation of PCNA ubiquitylation/deubiquitylation. FEBS Lett. 2011;585:2780–2785.
  • Bellaoui M, Chang M, Ou J, et al. Elg1 forms an alternative RFC complex important for DNA replication and genome integrity. EMBO J. 2003;22:4304–4313.
  • Ben-Aroya S, Koren A, Liefshitz B, et al. ELG1, a yeast gene required for genome stability, forms a complex related to replication factor C. Proc Natl Acad Sci U S A. 2003;100:9906–9911.
  • Kanellis P, Agyei R, Durocher D. Elg1 forms an alternative PCNA-interacting RFC complex required to maintain genome stability. Curr Biol. 2003;13:1583–1595.
  • Banerjee S, Myung K. Increased genome instability and telomere length in the elg1-deficient Saccharomyces cerevisiae mutant are regulated by S-phase checkpoints. Eukaryot Cell. 2004;3:1557–1566.
  • Sikdar N, Banerjee S, Lee KY, et al. DNA damage responses by human ELG1 in S phase are important to maintain genomic integrity. Cell Cycle. 2009;8:3199–3207.
  • Bell DW, Sikdar N, Lee KY, et al. Predisposition to cancer caused by genetic and functional defects of mammalian Atad5. PLoS Genet. 2011;7:e1002245.
  • Maleva Kostovska I, Wang J, Bogdanova N, et al. Rare ATAD5 missense variants in breast and ovarian cancer patients. Cancer Lett. 2016;376:173–177.
  • Kuchenbaecker KB, Ramus SJ, Tyrer J, et al. Identification of six new susceptibility loci for invasive epithelial ovarian cancer. Nat Genet. 2015;47:164–171.
  • Park SH, Kang N, Song E, et al. ATAD5 promotes replication restart by regulating RAD51 and PCNA in response to replication stress. Nat Commun. 2019;10:5718.
  • Kubota T, Nishimura K, Kanemaki MT, et al. The Elg1 replication factor C-like complex functions in PCNA unloading during DNA replication. Mol Cell. 2013;50:273–280.
  • Lee KY, Fu H, Aladjem MI, et al. ATAD5 regulates the lifespan of DNA replication factories by modulating PCNA level on the chromatin. J Cell Biol. 2013;200:31–44.
  • Kang MS, Ryu E, Lee SW, et al. Regulation of PCNA cycling on replicating DNA by RFC and RFC-like complexes. Nat Commun. 2019;10:2420.
  • Shiomi Y, Nishitani H. Alternative replication factor C protein, Elg1, maintains chromosome stability by regulating PCNA levels on chromatin. Genes Cells. 2013;18:946–959.
  • Lee KY, Yang K, Cohn MA, et al. Human ELG1 regulates the level of ubiquitinated proliferating cell nuclear antigen (PCNA) through Its interactions with PCNA and USP1. J Biol Chem. 2010;285:10362–10369.
  • Cohn MA, Kee Y, Haas W, et al. UAF1 is a subunit of multiple deubiquitinating enzyme complexes. J Biol Chem. 2009;284:5343–5351.
  • Liang F, Longerich S, Miller AS, et al. Promotion of RAD51-mediated homologous DNA pairing by the RAD51AP1-UAF1 complex. Cell Rep. 2016;15:2118–2126.
  • Cohn MA, Kowal P, Yang K, et al. A UAF1-containing multisubunit protein complex regulates the Fanconi anemia pathway. Mol Cell. 2007;28:786–797.
  • Cukras S, Lee E, Palumbo E, et al. The USP1-UAF1 complex interacts with RAD51AP1 to promote homologous recombination repair. Cell Cycle. 2016;15:2636–2646.
  • Murai J, Yang K, Dejsuphong D, et al. The USP1/UAF1 complex promotes double-strand break repair through homologous recombination. Mol Cell Biol. 2011;31:2462–2469.
  • 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.
  • 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.
  • 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.
  • Park E, Kim JM, Primack B, et al. Inactivation of Uaf1 causes defective homologous recombination and early embryonic lethality in mice. Mol Cell Biol. 2013;33:4360–4370.
  • Strnad P, Leidel S, Vinogradova T, et al. Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle. Dev Cell. 2007;13:203–213.
  • Yoshiba S, Tsuchiya Y, Ohta M, et al. HsSAS-6-dependent cartwheel assembly ensures stabilization of centriole intermediates. J Cell Sci. 2019;132(12).
  • Vulprecht J, David A, Tibelius A, et al. STIL is required for centriole duplication in human cells. J Cell Sci. 2012;125:1353–1362.
  • Chang J, Cizmecioglu O, Hoffmann I, et al. PLK2 phosphorylation is critical for CPAP function in procentriole formation during the centrosome cycle. EMBO J. 2010;29:2395–2406.
  • Tang CJ, Fu RH, Wu KS, et al. CPAP is a cell-cycle regulated protein that controls centriole length. Nat Cell Biol. 2009;11:825–831.
  • Wessel SR, Mohni KN, Luzwick JW, et al. Functional analysis of the replication fork proteome identifies BET proteins as PCNA regulators. Cell Rep. 2019;28:3497–509 e4.
  • Hein MY, Hubner NC, Poser I, et al. A human interactome in three quantitative dimensions organized by stoichiometries and abundances. Cell. 2015;163:712–723.