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Review

A guiding torch at the poles: the multiple roles of spindle microtubule-organizing centers during cell division

ORCID Icon & ORCID Icon
Pages 1405-1421 | Received 22 Jan 2020, Accepted 29 Mar 2020, Published online: 13 May 2020

References

  • Prosser SL, Pelletier L. Mitotic spindle assembly in animal cells: a fine balancing act. Nat Rev Mol Cell Biol. 2017;18(3):187–201.
  • Winey M, Bloom K. Mitotic spindle form and function. Genetics. 2012;190:1197–1224.
  • Meraldi P. Centrosomes in spindle organization and chromosome segregation: a mechanistic view. Chromosome Res. 2016;24:19–34.
  • Wu J, Akhmanova A. Microtubule-organizing centers. Annu Rev Cell Dev Biol. 2017;33:51–75.
  • Valerio-Santiago M, Monje-Casas F. Tem1 localization to the spindle pole bodies is essential for mitotic exit and impairs spindle checkpoint function. J Cell Biol. 2011;192:599–614.
  • Baro B, Queralt E, Monje-Casas F. Regulation of mitotic exit in saccharomyces cerevisiae. Methods Mol Biol. 2017;1505:3–17.
  • Visintin R, Hwang ES, Amon A. Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus. Nature. 1999;398:818–823.
  • Shou W, Seol JH, Shevchenko A, et al. Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex. Cell. 1999;97:233–244.
  • Visintin R, Amon A. Regulation of the mitotic exit protein kinases Cdc15 and Dbf2. Mol Biol Cell. 2001;12:2961–2974.
  • Magidson V, Chang F, Khodjakov A. Regulation of cytokinesis by spindle-pole bodies. Nat Cell Biol. 2006;8(8):891–893.
  • Elserafy M, Saric M, Neuner A, et al. Molecular mechanisms that restrict yeast centrosome duplication to one event per cell cycle. Curr Biol. 2014;24:1456–1466.
  • Lengefeld J, Hotz M, Rollins M, et al. Budding yeast wee1 distinguishes spindle pole bodies to guide their pattern of age-dependent segregation. Nat Cell Biol. 2017;19:941–951.
  • Tamborrini D, Juanes MA, Ibanes S, et al. Recruitment of the mitotic exit network to yeast centrosomes couples septin displacement to actomyosin constriction. Nat Commun. 2018;9:4308.
  • Powers BL, Hall MC. Re-examining the role of Cdc14 phosphatase in reversal of Cdk phosphorylation during mitotic exit. J Cell Sci. 2017;130:2673–2681.
  • Shirk K, Jin H, Giddings TH Jr., et al. The Aurora kinase Ipl1 is necessary for spindle pole body cohesion during budding yeast meiosis. J Cell Sci. 2011;124:2891–2896.
  • Kim S, Meyer R, Chuong H, et al. Dual mechanisms prevent premature chromosome segregation during meiosis. Genes Dev. 2013;27:2139–2146.
  • Nakamura TS, Numajiri Y, Okumura Y, et al. Dynamic localization of a yeast development-specific PP1 complex during prospore membrane formation is dependent on multiple localization signals and complex formation. Mol Biol Cell. 2017;28:3881–3895.
  • Hinchcliffe EH, Miller FJ, Cham M, et al. Requirement of a centrosomal activity for cell cycle progression through G1 into S phase. Science. 2001;291:1547–1550.
  • Khodjakov A, Rieder CL. Centrosomes enhance the fidelity of cytokinesis in vertebrates and are required for cell cycle progression. J Cell Biol. 2001;153:237–242.
  • Matsumoto Y, Maller JL. A centrosomal localization signal in cyclin E required for Cdk2-independent S phase entry. Science. 2004;306:885–888.
  • Pascreau G, Eckerdt F, Churchill ME, et al. Discovery of a distinct domain in cyclin A sufficient for centrosomal localization independently of Cdk binding. Proc Natl Acad Sci U S A. 2010;107:2932–2937.
  • Krämer A, Mailand N, Lukas C, et al. Centrosome-associated Chk1 prevents premature activation of cyclin-B-Cdk1 kinase. Nat Cell Biol. 2004;6:884–891.
  • Hirota T, Kunitoku N, Sasayama T, et al. Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells. Cell. 2003;114:585–598.
  • Golsteyn RM, Mundt KE, Fry AM, et al. Cell cycle regulation of the activity and subcellular localization of Plk1, a human protein kinase implicated in mitotic spindle function. J Cell Biol. 1995;129:1617–1628.
  • Holland AJ, Fachinetti D, Da Cruz S, et al. Polo-like kinase 4 controls centriole duplication but does not directly regulate cytokinesis. Mol Biol Cell. 2012;23:1838–1845.
  • Bruinsma W, Raaijmakers JA, Medema RH. Switching polo-like kinase-1 on and off in time and space. Trends Biochem Sci. 2012;37:534–542.
  • Schmucker S, Sumara I. Molecular dynamics of PLK1 during mitosis. Mol Cell Oncol. 2014;1:e954507.
  • Macurek L, Lindqvist A, Lim D, et al. Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature. 2008;455:119–123.
  • Seki A, Coppinger JA, Jang CY, et al. Bora and the kinase Aurora a cooperatively activate the kinase Plk1 and control mitotic entry. Science. 2008;320:1655–1658.
  • Bruinsma W, Aprelia M, Kool J, et al. Spatial separation of Plk1 phosphorylation and activity. Front Oncol. 2015;5:132.
  • Rapley J, Baxter JE, Blot J, et al. Coordinate regulation of the mother centriole component nlp by nek2 and plk1 protein kinases. Mol Cell Biol. 2005;25:1309–1324.
  • Mardin BR, Agircan FG, Lange C, et al. Plk1 controls the Nek2A-PP1gamma antagonism in centrosome disjunction. Curr Biol. 2011;21:1145–1151.
  • Kiyomitsu T, Cheeseman IM. Chromosome- and spindle-pole-derived signals generate an intrinsic code for spindle position and orientation. Nat Cell Biol. 2012;14:311–317.
  • Kratz AS, Barenz F, Richter KT, et al. Plk4-dependent phosphorylation of STIL is required for centriole duplication. Biol Open. 2015;4:370–377.
  • Ohta M, Ashikawa T, Nozaki Y, et al. Direct interaction of Plk4 with STIL ensures formation of a single procentriole per parental centriole. Nat Commun. 2014;5:5267.
  • Bury L, Coelho PA, Simeone A, et al. Plk4 and aurora A cooperate in the initiation of acentriolar spindle assembly in mammalian oocytes. J Cell Biol. 2017;216:3571–3590.
  • Coelho PA, Bury L, Sharif B, et al. Spindle formation in the mouse embryo requires Plk4 in the absence of centrioles. Dev Cell. 2013;27:586–597.
  • Ohta M, Watanabe K, Ashikawa T, et al. Bimodal binding of STIL to Plk4 controls proper centriole copy number. Cell Rep. 2018;23:3160–9 e4.
  • Cunha-Ferreira I, Rodrigues-Martins A, Bento I, et al. The SCF/Slimb ubiquitin ligase limits centrosome amplification through degradation of SAK/PLK4. Curr Biol. 2009;19:43–49.
  • Holland AJ, Lan W, Niessen S, et al. Polo-like kinase 4 kinase activity limits centrosome overduplication by autoregulating its own stability. J Cell Biol. 2010;188:191–198.
  • Montenegro Gouveia S, Zitouni S, Kong D, et al. PLK4 is a microtubule-associated protein that self-assembles promoting de novo MTOC formation. J Cell Sci. 2018;132(4):jcs219501.
  • Song MH, Liu Y, Anderson DE, et al. Protein phosphatase 2A-SUR-6/B55 regulates centriole duplication in C. elegans by controlling the levels of centriole assembly factors. Dev Cell. 2011;20:563–571.
  • Kitagawa D, Fluckiger I, Polanowska J, et al. PP2A phosphatase acts upon SAS-5 to ensure centriole formation in C. elegans embryos. Dev Cell. 2011;20:550–562.
  • Enos SJ, Dressler M, Gomes BF, et al. Phosphatase PP2A and microtubule-mediated pulling forces disassemble centrosomes during mitotic exit. Biol Open. 2018;7(1): bio029777.
  • Boudreau V, Chen R, Edwards A, et al. PP2A-B55/SUR-6 collaborates with the nuclear lamina for centrosome separation during mitotic entry. Mol Biol Cell. 2019;30:876–886.
  • Wlodarchak N, Xing Y. PP2A as a master regulator of the cell cycle. Crit Rev Biochem Mol Biol. 2016;51:162–184.
  • Peel N, Iyer J, Naik A, et al. Protein phosphatase 1 down regulates ZYG-1 levels to limit centriole duplication. PLoS Genet. 2017;13:e1006543.
  • Joukov V, Walter JC, De Nicolo A. The Cep192-organized aurora A-Plk1 cascade is essential for centrosome cycle and bipolar spindle assembly. Mol Cell. 2014;55:578–591.
  • Nasa I, Trinkle-Mulcahy L, Douglas P, et al. Recruitment of PP1 to the centrosomal scaffold protein CEP192. Biochem Biophys Res Commun. 2017;484:864–870.
  • Sankaran S, Crone DE, Palazzo RE, et al. Aurora-A kinase regulates breast cancer associated gene 1 inhibition of centrosome-dependent microtubule nucleation. Cancer Res. 2007;67:11186–11194.
  • Meraldi P, Nigg EA. Centrosome cohesion is regulated by a balance of kinase and phosphatase activities. J Cell Sci. 2001;114:3749–3757.
  • Saito RM, Perreault A, Peach B, van den Heuvel S, et al. The CDC-14 phosphatase controls developmental cell-cycle arrest in C. elegans. Nat Cell Biol. 2004;6:777–783.
  • Kaiser BK, Zimmerman ZA, Charbonneau H, et al. Disruption of centrosome structure, chromosome segregation, and cytokinesis by misexpression of human Cdc14A phosphatase. Mol Biol Cell. 2002;13:2289–2300.
  • Mocciaro A, Berdougo E, Zeng K, et al. Vertebrate cells genetically deficient for Cdc14A or Cdc14B retain DNA damage checkpoint proficiency but are impaired in DNA repair. J Cell Biol. 2010;189:631–639.
  • Mailand N, Lukas C, Kaiser BK, et al. Deregulated human Cdc14A phosphatase disrupts centrosome separation and chromosome segregation. Nat Cell Biol. 2002;4:317–322.
  • Clément A, Solnica-Krezel L, Gould KL. Functional redundancy between Cdc14 phosphatases in zebrafish ciliogenesis. Dev Dyn. 2012;241:1911–1921.
  • Schindler K, Schultz RM. The CDC14A phosphatase regulates oocyte maturation in mouse. Cell Cycle. 2009;8:1090–1098.
  • Kaiser BK, Nachury MV, Gardner BE, et al. Xenopus Cdc14 alpha/beta are localized to the nucleolus and centrosome and are required for embryonic cell division. BMC Cell Biol. 2004;5:27.
  • Krasinska L, de Bettignies G, Fisher D, et al. Regulation of multiple cell cycle events by Cdc14 homologues in vertebrates. Exp Cell Res. 2007;313:1225–1239.
  • Gromley A, Jurczyk A, Sillibourne J, et al. A novel human protein of the maternal centriole is required for the final stages of cytokinesis and entry into S phase. J Cell Biol. 2003;161:535–545.
  • Lanz MC, Dibitetto D, Smolka MB. DNA damage kinase signaling: checkpoint and repair at 30 years. Embo J. 2019;38:e101801.
  • Su TT. Cellular responses to DNA damage: one signal, multiple choices. Annu Rev Genet. 2006;40:187–208.
  • Villoria MT, Ramos F, Duenas E, et al. Stabilization of the metaphase spindle by Cdc14 is required for recombinational DNA repair. Embo J. 2017;36:79–101.
  • Pereira G, Hofken T, Grindlay J, et al. The Bub2p spindle checkpoint links nuclear migration with mitotic exit. Mol Cell. 2000;6:1–10.
  • Geymonat M, Spanos A, Smith SJ, et al. Control of mitotic exit in budding yeast. in vitro regulation of Tem1 GTPase by Bub2 and Bfa1. J Biol Chem. 2002;277:28439–28445.
  • Hu F, Wang Y, Liu D, et al. Regulation of the Bub2/Bfa1 GAP complex by Cdc5 and cell cycle checkpoints. Cell. 2001;107:655–665.
  • Valerio-Santiago M, de Los Santos-velazquez AI, Monje-Casas F. Inhibition of the mitotic exit network in response to damaged telomeres. PLoS Genet. 2013;9:e1003859.
  • Pereira G, Schiebel E. Kin4 kinase delays mitotic exit in response to spindle alignment defects. Mol Cell. 2005;19:209–221.
  • D’Aquino KE, Monje-Casas F, Paulson J, et al. The protein kinase Kin4 inhibits exit from mitosis in response to spindle position defects. Mol Cell. 2005;19:223–234.
  • Bardin AJ, Visintin R, Amon A. A mechanism for coupling exit from mitosis to partitioning of the nucleus. Cell. 2000;102:21–31.
  • Monje-Casas F, Amon A. Cell polarity determinants establish asymmetry in MEN signaling. Dev Cell. 2009;16:132–145.
  • Caydasi AK, Pereira G. Spindle alignment regulates the dynamic association of checkpoint proteins with yeast spindle pole bodies. Dev Cell. 2009;16:146–156.
  • Bertazzi DT, Kurtulmus B, Pereira G. The cortical protein Lte1 promotes mitotic exit by inhibiting the spindle position checkpoint kinase Kin4. J Cell Biol. 2011;193:1033–1048.
  • Falk JE, Chan LY, Amon A. Lte1 promotes mitotic exit by controlling the localization of the spindle position checkpoint kinase Kin4. Proc Natl Acad Sci U S A. 2011;108:12584–12590.
  • Chan LY, Amon A. Spindle position is coordinated with cell-cycle progression through establishment of mitotic exit-activating and -inhibitory zones. Mol Cell. 2010;39:444–454.
  • Serrano D, D’Amours D. When genome integrity and cell cycle decisions collide: roles of polo kinases in cellular adaptation to DNA damage. Syst Synth Biol. 2014;8:195–203.
  • Toczyski DP, Galgoczy DJ, Hartwell LH. CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell. 1997;90:1097–1106.
  • Rawal CC, Riccardo S, Pesenti C, et al. Reduced kinase activity of polo kinase Cdc5 affects chromosome stability and DNA damage response in S. cerevisiae. Cell Cycle. 2016;15:2906–2919.
  • Ratsima H, Serrano D, Pascariu M, et al. Centrosome-dependent bypass of the dna damage checkpoint by the polo kinase Cdc5. Cell Rep. 2016;14:1422–1434.
  • Löffler H, Fechter A, Liu FY, et al. DNA damage-induced centrosome amplification occurs via excessive formation of centriolar satellites. Oncogene. 2013;32:2963–2972.
  • Roninson IB, Broude EV, Chang BD. If not apoptosis, then what? treatment-induced senescence and mitotic catastrophe in tumor cells. Drug Resist Updat. 2001;4:303–313.
  • Takada S, Kelkar A, Theurkauf WE. Drosophila checkpoint kinase 2 couples centrosome function and spindle assembly to genomic integrity. Cell. 2003;113:87–99.
  • Hut HM, Lemstra W, Blaauw EH, et al. Centrosomes split in the presence of impaired DNA integrity during mitosis. Mol Biol Cell. 2003;14:1993–2004.
  • Smits VA, Klompmaker R, Arnaud L, et al. Polo-like kinase-1 is a target of the DNA damage checkpoint. Nat Cell Biol. 2000;2:672–676.
  • Bruinsma W, Aprelia M, Garcia-Santisteban I, et al. Inhibition of Polo-like kinase 1 during the DNA damage response is mediated through loss of aurora A recruitment by Bora. Oncogene. 2017;36:1840–1848.
  • Krystyniak A, Garcia-Echeverria C, Prigent C, et al. Inhibition of Aurora A in response to DNA damage. Oncogene. 2006;25:338–348.
  • Qin B, Gao B, Yu J, et al. Ataxia telangiectasia-mutated- and Rad3-related protein regulates the DNA damage-induced G2/M checkpoint through the Aurora A cofactor Bora protein. J Biol Chem. 2013;288:16139–16144.
  • Chan EH, Santamaria A, Sillje HH, et al. Plk1 regulates mitotic Aurora A function through betaTrCP-dependent degradation of hBora. Chromosoma. 2008;117:457–469.
  • Tavernier N, Noatynska A, Panbianco C, et al. Cdk1 phosphorylates SPAT-1/Bora to trigger PLK-1 activation and drive mitotic entry in C. elegans embryo. J Cell Biol. 2015;208:661–669.
  • Yata K, Lloyd J, Maslen S, et al. Plk1 and CK2 act in concert to regulate Rad51 during DNA double strand break repair. Mol Cell. 2012;45:371–383.
  • Mi J, Guo C, Brautigan DL, et al. Protein phosphatase-1alpha regulates centrosome splitting through Nek2. Cancer Res. 2007;67:1082–1089.
  • Zhang W, Fletcher L, Muschel RJ. The role of Polo-like kinase 1 in the inhibition of centrosome separation after ionizing radiation. J Biol Chem. 2005;280:42994–42999.
  • Petersen J, Nurse P. TOR signalling regulates mitotic commitment through the stress MAP kinase pathway and the Polo and Cdc2 kinases. Nat Cell Biol. 2007;9:1263–1272.
  • Messier V, Zenklusen D, Michnick SW. A nutrient-responsive pathway that determines M phase timing through control of B-cyclin mRNA stability. Cell. 2013;153:1080–1093.
  • Nakashima A, Maruki Y, Imamura Y, et al. The yeast Tor signaling pathway is involved in G2/M transition via polo-kinase. PLoS One. 2008;3:e2223.
  • Searle JS, Schollaert KL, Wilkins BJ, et al. The DNA damage checkpoint and PKA pathways converge on APC substrates and Cdc20 to regulate mitotic progression. Nat Cell Biol. 2004;6:138–145.
  • Chauhan N, Visram M, Cristobal-Sarramian A, et al. Morphogenesis checkpoint kinase swe1 is the executor of lipolysis-dependent cell-cycle progression. Proc Natl Acad Sci U S A. 2015;112:E1077–85.
  • Cuyas E, Corominas-Faja B, Joven J, et al. Cell cycle regulation by the nutrient-sensing mammalian target of rapamycin (mTOR) pathway. Methods Mol Biol. 2014;1170:113–144.
  • Vazquez-Martin A, Oliveras-Ferraros C, Menendez JA. The active form of the metabolic sensor: AMP-activated protein kinase (AMPK) directly binds the mitotic apparatus and travels from centrosomes to the spindle midzone during mitosis and cytokinesis. Cell Cycle. 2009;8:2385–2398.
  • Vazquez-Martin A, Oliveras-Ferraros C, Cufi S, et al. Polo-like kinase 1 regulates activation of AMP-activated protein kinase (AMPK) at the mitotic apparatus. Cell Cycle. 2011;10(8):1295–1302.
  • Li Q-R, Yan X-M, Guo L, et al. AMPK regulates anaphase central spindle length by phosphorylation of KIF4A. J Mol Cell Biol. 2018;10(1):2–17.
  • Platani M, Trinkle-Mulcahy L, Porter M, et al. Mio depletion links mTOR regulation to Aurora A and Plk1 activation at mitotic centrosomes. J Cell Biol. 2015;210(1):45–62.
  • Vandame P, Spriet C, Trinel D, et al. The spatio-temporal dynamics of PKA activity profile during mitosis and its correlation to chromosome segregation. Cell Cycle. 2014;13:3232–3240.
  • Noree C, Monfort E, Shotelersuk V. Human asparagine synthetase associates with the mitotic spindle. Biol Open. 2018;7.
  • Culver C, Melvin A, Mudie S, et al. HIF-1alpha depletion results in SP1-mediated cell cycle disruption and alters the cellular response to chemotherapeutic drugs. Cell Cycle. 2011;10:1249–1260.
  • Hubbi ME, Kshitiz, Gilkes DM, et al. A nontranscriptional role for HIF-1alpha as a direct inhibitor of DNA replication. Sci Signal. 2013;6:ra10.
  • Strowitzki MJ, Cummins EP, Taylor CT. Protein hydroxylation by hypoxia-inducible factor (HIF) hydroxylases: unique or ubiquitous? Cells. 2019;8.
  • Moser SC, Bensaddek D, Ortmann B, et al. PHD1 links cell-cycle progression to oxygen sensing through hydroxylation of the centrosomal protein Cep192. Dev Cell. 2013;26:381–392.
  • Kim S, Dynlacht BD. Centrosomes tune in to metabolic state and turn on to oxygen. Dev Cell. 2013;26:325–326.
  • Mihajlovic AI, FitzHarris G. Segregating chromosomes in the mammalian oocyte. Curr Biol. 2018;28:R895–R907.
  • Jansen RP. RNA-cytoskeletal associations. Faseb J. 1999;13:455–466.
  • Ruzanov PV, Evdokimova VM, Korneeva NL, et al. Interaction of the universal mRNA-binding protein, p50, with actin: a possible link between mRNA and microfilaments. J Cell Sci. 1999;112(Pt 20):3487–3496.
  • Groisman I, Huang YS, Mendez R, et al. CPEB, maskin, and cyclin B1 mRNA at the mitotic apparatus: implications for local translational control of cell division. Cell. 2000;103:435–447.
  • Lambert JD, Nagy LM. Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages. Nature. 2002;420:682–686.
  • Kingsley EP, Chan XY, Duan Y, et al. Widespread RNA segregation in a spiralian embryo. Evol Dev. 2007;9:527–539.
  • Lecuyer E, Yoshida H, Parthasarathy N, et al. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell. 2007;131:174–187.
  • Yaffe MP, Stuurman N, Vale RD. Mitochondrial positioning in fission yeast is driven by association with dynamic microtubules and mitotic spindle poles. Proc Natl Acad Sci U S A. 2003;100:11424–11428.
  • Fisk HA, Yaffe MP. Mutational analysis of Mdm1p function in nuclear and mitochondrial inheritance. J Cell Biol. 1997;138:485–494.
  • Dalton CM, Carroll J. Biased inheritance of mitochondria during asymmetric cell division in the mouse oocyte. J Cell Sci. 2013;126:2955–2964.
  • Katayama M, Zhong Z, Lai L, et al. Mitochondrial distribution and microtubule organization in fertilized and cloned porcine embryos: implications for developmental potential. Dev Biol. 2006;299:206–220.
  • Knabe W, Kuhn HJ. The role of microtubules and microtubule-organising centres during the migration of mitochondria. J Anat. 1996;189(Pt 2):383–391.
  • Maccari I, Zhao R, Peglow M, et al. Cytoskeleton rotation relocates mitochondria to the immunological synapse and increases calcium signals. Cell Calcium. 2016;60:309–321.
  • Morlino G, Barreiro O, Baixauli F, et al. Miro-1 links mitochondria and microtubule Dynein motors to control lymphocyte migration and polarity. Mol Cell Biol. 2014;34:1412–1426.
  • Ogbadoyi EO, Robinson DR, Gull K. A high-order trans-membrane structural linkage is responsible for mitochondrial genome positioning and segregation by flagellar basal bodies in trypanosomes. Mol Biol Cell. 2003;14:1769–1779.
  • Van Blerkom J. Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured mouse oocytes. Proc Natl Acad Sci U S A. 1991;88:5031–5035.
  • Sutterlin C, Colanzi A. The Golgi and the centrosome: building a functional partnership. J Cell Biol 2010; 188:621–8
  • Tormanen K, Ton C, Waring BM, et al. Function of golgi-centrosome proximity in RPE-1 cells. PLoS One. 2019;14:e0215215.
  • Orlofsky A. Positioning of the centrosome and golgi complex. Results Probl Cell Differ. 2019;67:127–200.
  • Saraste J, Prydz K. A new look at the functional organization of the golgi ribbon. Front Cell Dev Biol. 2019;7:171.
  • Hehnly H, Chen CT, Powers CM, et al. The centrosome regulates the Rab11- dependent recycling endosome pathway at appendages of the mother centriole. Curr Biol. 2012;22:1944–1950.
  • Brose L, Crest J, Tao L, et al. Polo kinase mediates the phosphorylation and cellular localization of Nuf/FIP3, a Rab11 effector. Mol Biol Cell. 2017;28:1435–1443.
  • Pelletier L, Yamashita YM. Centrosome asymmetry and inheritance during animal development. Curr Opin Cell Biol. 2012;24:541–546.
  • Pereira G, Tanaka TU, Nasmyth K, et al. Modes of spindle pole body inheritance and segregation of the Bfa1p-Bub2p checkpoint protein complex. Embo J. 2001;20:6359–6370.
  • Yamashita YM, Mahowald AP, Perlin JR, et al. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science. 2007;315:518–521.
  • Salzmann V, Chen C, Chiang CY, et al. Centrosome-dependent asymmetric inheritance of the midbody ring in Drosophila germline stem cell division. Mol Biol Cell. 2014;25:267–275.
  • Januschke J, Llamazares S, Reina J, et al. Drosophila neuroblasts retain the daughter centrosome. Nat Commun. 2011;2:243.
  • Izumi H, Kaneko Y. Evidence of asymmetric cell division and centrosome inheritance in human neuroblastoma cells. Proc Natl Acad Sci U S A. 2012;109:18048–18053.
  • Wang X, Tsai JW, Imai JH, et al. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature. 2009;461:947–955.
  • Manzano-Lopez J, Matellan L, Alvarez-Llamas A, et al. Asymmetric inheritance of spindle microtubule-organizing centres preserves replicative lifespan. Nat Cell Biol. 2019;21:952–965.
  • Denoth Lippuner A, Julou T, Barral Y. Budding yeast as a model organism to study the effects of age. FEMS Microbiol Rev. 2014;38:300–325.
  • Cheng J, Turkel N, Hemati N, et al. Centrosome misorientation reduces stem cell division during ageing. Nature. 2008;456:599–604.

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