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Klp10A modulates the localization of centriole-associated proteins during Drosophila male gametogenesis

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Pages 3432-3441 | Received 25 Jul 2016, Accepted 10 Oct 2016, Published online: 16 Nov 2016

References

  • Bettencourt Dias M, Glover DM. Centrosome biogenesis and function: Centrosomics brings new understanding. Nat Rev Mol Cell Biol 2007; 8:451-63; PMID:17505520; http://dx.doi.org/10.1038/nrm2180
  • Winey M, O'Toole E. Centriole structure. Philos Trans R Soc Lond B Biol Sci 2014; 369:20130457-20130457; PMID:25047611; http://dx.doi.org/10.1098/rstb.2013.0457
  • Conduit PT, Richens JH, Wainman A, Holder J, Vicente CC, Pratt MB, Dix CI, Novak ZA, Dobbie IM, Schermelleh L, Raff JW. A molecular mechanism of mitotic centrosome assembly in Drosophila. eLife 2014; 3:e03399; PMID:25149451; http://dx.doi.org/10.7554/eLife.03399
  • Conduit PT, Wainman A, Raff JW. Centrosome function and assembly in animal cells. Nat Rev Mol Cell Biol 2015; 16:611-24; PMID:26373263; http://dx.doi.org/10.1038/nrm4062
  • Fu J, Lipinszki Z, Rangone H, Min M, Mykura C, Chao-Chu J, Schneider S, Dzhindzhev NS, Gottardo M, Riparbelli MG, et al. Conserved molecular interactions in centriole-to-centrosome conversion. Nat Cell Biol 2016; 18:87-99; PMID:26595382; http://dx.doi.org/10.1038/ncb3274
  • Conduit PT, Wainman A, Raff JW. Centrosome function and assembly in animal cells. Nat Rev Mol Cell Biol 2015; 16:611-624; PMID:26373263; http://dx.doi.org/10.1038/nrm4062
  • Jana SC, Marteil G. Bettencourt-Dias M.mMapping molecules to structure: unveiling secrets of centriole and cilia assembly with near-atomic resolution. Curr Opin Cell Biol 2014; 26:96-106; PMID:24529251; http://dx.doi.org/10.1016/j.ceb.2013.12.001
  • Izquierdo D, Wang WJ, Uryu K, Tsou MF. Stabilization of cartwheel-less centrioles for duplication requires CEP295-mediated centriole-to-centrosome conversion. Cell Rep 2014; 8:957-65; PMID:25131205; http://dx.doi.org/10.1016/j.celrep.2014.07.022
  • Wang WJ, Soni RK, Uryu K, Bryan Tsou MF. The conversion of centrioles to centrosomes: essential coupling of duplication with segregation. J Cell Biol 2011; 193:727-739; PMID:21576395; http://dx.doi.org/10.1083/jcb.201101109
  • Fu J, Glover DM. Structured illumination of the interface between centriole and peri-centriolar material. Open Biol 2012; 2:120104; PMID:22977736; http://dx.doi.org/10.1098/rsob.120104
  • Lawo S, Hasegan M, Gupta GD, Pelletier L. Subdiffraction imaging of centrosomes reveals higher-order organizational features of pericentriolar material. Nat Cell Biol 2012; 14:1148-58; PMID:23086237; http://dx.doi.org/10.1038/ncb2591
  • Mennella V, Keszthelyi B, McDonald KL, Chhun B, Kan F, Rogers GC, Huang B, Agard DA. Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat Cell Biol 2012; 14:1159-68; PMID:23086239; http://dx.doi.org/10.1038/ncb2597
  • Sonnen KF, Schermelleh L, Leonhardt H, Nigg EA. 3D-structured illumination microscopy provides novel insight into architecture of human centrosomes. Biol Open 2012; 1:965-76; PMID:23213374; http://dx.doi.org/10.1242/bio.20122337
  • Rodrigues–Martins A, Riparbelli M, Callaini G, Glover DM, Bettencourt–Dias M. From centriole biogenesis to cellular function: centrioles are essential for cell division at critical developmental stages. Cell Cycle 2008; 7:11-6; PMID:18196975; http://dx.doi.org/10.4161/cc.7.1.5226
  • Gottardo M, Callaini G, Riparbelli MG. The Drosophila centriole - conversion of doublets into triplets within the stem cell niche. J Cell Sci 2015; 128:2437-42; PMID:26092937; http://dx.doi.org/10.1242/jcs.172627
  • Hirono M. Cartwheel assembly. Phil Trans R Soc B 2014; 369:20130458; PMID:25047612
  • Tates AD. Cytodifferentiation during spermatogenesis in Drosophila melanogaster: an electron microscopy study. PhD thesis, 1971, Rijksunivrsiteit de Leiden, The Netherlands.
  • Fritz-Niggli H. Meiosis and spermatid formation in non-irradiated and irradiated male germ cells in Drosophila melanogaster. Rev Suisse Zool 1972; Suppl:245-65; PMID:4625128
  • Riparbelli MG, Callaini G, Megraw TL. Assembly and persistence of primary cilia in dividing Drosophila spermatocytes. Dev Cell 2012; 23:425-32; PMID:22898783
  • Gottardo M, Callaini G, Riparbelli MG. Aurora A inhibition by MNL8054 promotes centriole elongation during Drosophila male meiosis. Cell Cycle 2015; 14:2844-52; PMID:25785740
  • Kim S, Tsiokas L. Cilia and cell cycle re-entry: more than a coincidence. Cell Cycle 2011; 10:2683-90; PMID:21814045
  • Kobayashi T, Dynlacht BD. Regulating the transition from centriole to basal body. J Cell Biol 2011; 193:435-44; PMID:21536747
  • Gottardo M, Callaini G, Riparbelli MG. The cilium-like region of the Drosophila spermatocyte: an emerging flagellum? J Cell Sci 2013; 126:5441-52; PMID:24105264
  • Fu J, Hagan IM, Glover DM. The centrosome and its duplication cycle. Cold Spring Harb Perspect Biol 2015; 7:a015800; PMID:25646378
  • Rogers GC, Rogers SL, Schwimmer TA, Ems-McClung SC, Walczak CE, Vale RD, Scholey JM, Sharp DJ. Two mitotic kinesins cooperate to drive sister chromatid separation during anaphase. Nature 2004; 427:364-70; PMID:14681690
  • Goshima G, Vale RD. Cell cycle-dependent dynamics and regulation of mitotic kinesins in Drosophila S2 cells. Mol Biol Cell 2005; 16:3896-907; PMID:15958489
  • Mennella V, Rogers GC, Rogers SL, Buster DW, Vale RD, Sharp DJ. Functionally distinct kinesin-13 family members cooperate to regulate microtubule dynamics during interphase. Nat Cell Biol 2005; 7:235-45; PMID:15723056
  • Delgehyr N, Rangone H, Fu J, Mao G, Tom B, Riparbelli MG, Callaini G, Glover DM. Klp10A, a microtubule-depolymerizing kinesin-13, cooperates with CP110 to control Drosophila centriole length. Curr Biol 2012; 22:502-9; PMID:22365849
  • Franz A, Roque H, Saurya S, Dobbelaere J, Raff JW. CP110 exhibits novel regulatory activities during centriole assembly in Drosophila. J Cell Biol 2013; 203:785-99; PMID:24297749
  • Woodruff JB, Wueseke O, Hyman AA. Pericentriolar material structure and dynamics. Philos Trans R Soc Lond B Biol Sci 2014; 369:20130459; PMID:25047613
  • Lerit DA, Jordan HA, Poulton JS, Fagerstrom CJ, Galletta BJ, Peifer M, Rusan NM. Interphase centrosome organization by the PLP-Cnn scaffold is required for centrosome function. J Cell Biol 2015; 210:79-97; PMID:26150390
  • Bettencourt-Dias M, Rodrigues-Martins A, Carpenter L, Riparbelli M, Lehmann L, Gatt MK, Carmo N, Balloux F, Callaini G, Glover DM. SAK/PLK4 is required for centriole duplication and flagella development. Curr Biol 2005; 15:2199-207; PMID:16326102; http://dx.doi.org/10.1016/j.cub.2005.11.042
  • Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov AL, Raff JW. Flies without centrioles. Cell 2006; 125:1375-86; PMID:16814722; http://dx.doi.org/10.1016/j.cell.2006.05.025
  • Novak ZA, Wainman A, Gartenmann L, Raff JW. Cdk1 phosphorylates Drosophila Sas-4 to recruit Polo to daughter centrioles and convert them to centrosomes. Dev Cell 2016; 37:545-57; PMID:27326932; http://dx.doi.org/10.1016/j.devcel.2016.05.022
  • Riparbelli MG, Gottardo M, Glover DM, Callaini G. Inhibition of Polo kinase by BI2536 affects centriole separation during Drosophila male meiosis. Cell Cycle 2014; 13:2064-72; PMID:24802643; http://dx.doi.org/10.4161/cc.29083
  • Kohlmaier G, Loncarek J, Meng X, McEwen BF, Mogensen MM, Spektor A, Dynlacht BD, Khodjakov A, Gonczy P. Overly long centrioles and defective cell division upon excess of the SAS-4-related protein CPAP. Curr Biol 2009; 19:1012-8; PMID:19481460; http://dx.doi.org/10.1016/j.cub.2009.05.018
  • Schmidt TI, Kleylein-Sohn J, Westendorf J, Le Clech M, Lavoie SB, Stierhof YD, Nigg EA. Control of centriole length by CPAP and CP110. Curr Biol 2009; 19:1005-11; PMID:19481458; http://dx.doi.org/10.1016/j.cub.2009.05.016
  • Tang CJ, Fu RH, Wu KS, Hsu WB, Tang TK. CPAP is a cell-cycle regulated protein that controls centriole length. Nat Cell Biol 2009; 11:825-31; PMID:19503075; http://dx.doi.org/10.1038/ncb1889
  • Kleylein-Sohn J, Westendorf J, Le Clech M, Habedanck R, Stierhof YD, Nigg EA. Plk4-induced centriole biogenesis in human cells. Dev Cell 2007; 13:190-202; PMID:17681131; http://dx.doi.org/10.1016/j.devcel.2007.07.002
  • Rodrigues-Martins A, Riparbelli M, Callaini G, Glover DM, Bettencourt-Dias M. Revisiting the role of the mother centriole in centriole biogenesis. Science 2007; 316:1046-50; PMID:17463247; http://dx.doi.org/10.1126/science.1142950
  • Bornens M, Gönczy P. Centrosomes back in the limelight. Phil Trans R Soc B Biol Sci 2014; 369:20130452; http://dx.doi.org/10.1098/rstb.2013.0452
  • Nigg EA, Stearns TT. The centrosome cycle: centriole biogenesis, duplication and inherent asymmetries. Nat Cell Biol 2011; 13:1154-60; PMID:21968988; http://dx.doi.org/10.1038/ncb2345
  • Callaini G, Whitfield WG, Riparbelli MG. Centriole and centrosome dynamics during the embryonic cell cycles that follow the formation of the cellular blastoderm in Drosophila. Exp Cell Res 1997; 234:183-90; PMID:9223385; http://dx.doi.org/10.1006/excr.1997.3618
  • Martinez-Campos M, Basto R, Baker J, Kernan M, Raff JW. The Drosophila pericentrin-like protein is essential for cilia/flagella function, but appears to be dispensable for mitosis. J. Cell Biol 2004; 165:673-83; PMID:15184400; http://dx.doi.org/10.1083/jcb.200402130
  • Galletta BJ, Guillen RX, Fagerstrom CJ, Brownlee CW, Lerit DA, Megraw TL, Rogers GC, Rusan NM. Drosophila pericentrin requires interaction with calmodulin for its function at centrosomes and neuronal basal bodies but not at sperm basal bodies. Mol Biol Cell 2014; 25:2682-94; PMID:25031429; http://dx.doi.org/10.1091/mbc.E13-10-0617
  • Galletta BJ, Jacobs KC, Fagerstrom CJ, Rusan NM. Asterless is required for centriole length control and sperm development. J Cell Biol 2016; 213:435-50; PMID:27185836; http://dx.doi.org/10.1083/jcb.201501120
  • Purohit A, Tynan SH, Vallee R, Doxsey SJ. Direct interaction of pericentrin with cytoplasmic dynein light intermediate chain contributes to mitotic spindle organization. J Cell Biol 1999; 147:481-92; PMID:10545494; http://dx.doi.org/10.1083/jcb.147.3.481
  • Young A, Dictenberg JB, Purohit A, Tuft R, Doxsey SJ. Cytoplasmic dynein-mediated assembly of pericentrin and gamma tubulin onto centrosomes. Mol Biol Cell 2000; 11:2047-56; PMID:10848628; http://dx.doi.org/10.1091/mbc.11.6.2047
  • Kawaguchi S-I, Zheng Y. Characterization of a Drosophila centrosome protein CP309 that shares homology with Kendrin and CG-NAP. Mol Biol Cell 2004; 15:37-45; PMID:14565985; http://dx.doi.org/10.1091/mbc.E03-03-0191
  • Cizmecioglu O, Arnold M, Bahtz R, Settele F, Ehret L, Haselmann-Weiss U, Antony C, Hoffmann I. Cep152 acts as a scaffold for recruitment of Plk4 and CPAP to the centrosome. J Cell Biol 2010; 191:731-9; PMID:21059844; http://dx.doi.org/10.1083/jcb.201007107
  • Dzhindzhev NS, Yu QD, Weiskopf K, Tzolovsky G, Cunha-Ferreira I, Riparbelli M, Rodrigues-Martins A, Bettencourt-Dias M, Callaini G, Glover DM. Asterless is a scaffold for the onset of centriole assembly. Nature 2010; 467:714-8; PMID:20852615; http://dx.doi.org/10.1038/nature09445
  • Hatch EM, Kulukian A, Holland AJ, Cleveland DW, Stearns T. Cep152 interacts with Plk4 and is required for centriole duplication. J Cell Biol 2010; 191:721-9; PMID:21059850; http://dx.doi.org/10.1083/jcb.201006049
  • Kim TS, Park JE, Shukla A, Choi S, Murugan RN, Lee JH, Ahn M, Rhee K, Bang JK, Kim BY. et al. Hierarchical recruitment of Plk4 and regulation of centriole biogenesis by two centrosomal scaffolds, Cep192 and Cep152. Proc Natl Acad Sci USA 2013; 110:E4849-57; PMID:24277814; http://dx.doi.org/10.1073/pnas.1319656110
  • Sonnen KF, Gabryjonczyk AM, Anselm E, Stierhof YD, Nigg EA. Human Cep192 and Cep152 cooperate in Plk4 recruitment and centriole duplication. J Cell Sci 2013; 126:3223-33; PMID:23641073; http://dx.doi.org/10.1242/jcs.129502
  • Klebba JE, Galletta BJ, Nye J, Plevock KM, Buster DW, Hollingsworth NA, Slep KC, Rusan NM, Rogers GC. Two polo-like kinase 4 binding domains in asterless perform distinct roles in regulating kinase stability. J Cell Biol 2015; 208:401-14; PMID:25688134; http://dx.doi.org/10.1083/jcb.201410105
  • Stevens NR, Raposo AA, Basto R, St Johnston D, Raff JW. From stem cell to embryo without centrioles. Curr Biol 2007; 17:1498-503; PMID:17716897; http://dx.doi.org/10.1016/j.cub.2007.07.060
  • Riparbelli MG, Callaini G. Male gametogenesis without centrioles. Dev Biol 2011; 349:427-43; PMID:20974123; http://dx.doi.org/10.1016/j.ydbio.2010.10.021
  • Gopalakrishnan J, Mennella V, Blachon S, Zhai B, Smith AH, Megraw TL, Nicastro D, Gygi SP, Agard DA, Avidor-Reiss T. Sas-4 provides a scaffold for cytoplasmic complexes and tethers them in a centrosome. Nat Commun 2011; 2:359; PMID:21694707; http://dx.doi.org/10.1038/ncomms1367
  • Novak ZA, Conduit PT, Wainman A, Raff JW. Asterless licenses daughter centrioles to duplicate for the first time in Drosophila embryos. Curr Biol 2014; 24:1276-82; PMID:24835456; http://dx.doi.org/10.1016/j.cub.2014.04.023
  • Peter A, Schottler P, Werner M, Beinert N, Dowe G, Burkert P, Mourkioti F, Dentzer L, He Y, Deak P, et al. Mapping and identification of essential gene functions on the X chromosome of Drosophila. EMBO Rep 2002; 3:34-8; PMID:11751581; http://dx.doi.org/10.1093/embo-reports/kvf012
  • Rodrigues-Martins A, Bettencourt-Dias M, Riparbelli M, Ferreira C, Ferreira I, Callaini G, Glover DM. DSAS-6 organizes a tube-like centriole precursor, and its absence suggests modularity in centriole assembly. Curr Biol 2007; 17:1465-72; PMID:17689959; http://dx.doi.org/10.1016/j.cub.2007.07.034

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