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Open Life Sciences

formerly Central European Journal of Biology

Editor-in-Chief: Ratajczak, Mariusz


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Volume 5, Issue 1

Issues

Volume 10 (2015)

CLERC and centrosomal leucine-rich repeat proteins

Yoshinori Muto / Yukio Okano
Published Online: 2010-01-30 | DOI: https://doi.org/10.2478/s11535-009-0061-x

Abstract

The centrosome functions as the microtubule-organizing center and plays a vital role in organizing spindle poles during mitosis. Recently, we identified a centrosomal protein called CLERC (Centrosomal leucine-rich repeat and coiled-coil containing protein) which is a human ortholog of Chlamydomonas Vfl1 protein. The bibliography as well as database searches provided evidence that the human proteome contains at least seven centrosomal leucine-rich repeat proteins including CLERC. CLERC and four other centrosomal leucine-rich repeat proteins contain the SDS22-like leucine-rich repeat motifs, whereas the remaining two proteins contain the RI-like and the cysteine-containing leucine-rich repeat motifs. Individual leucine-rich repeat motifs are highly conserved and present in evolutionarily diverse organisms. Here, we provide an overview of CLERC and other centrosomal leucine-rich repeat proteins, their structures, their evolutionary relationships, and their functional properties.

Keywords: Centrosome; CLERC; Leucine-rich repeat; SDS22-like; Chlamydomonas; Centriolin; CEP97; LRRC6; Seahorse

  • [1] Wilson E.B., The cell in development and inheritance, Macmillan & co., ltd., 1896 Google Scholar

  • [2] Chretien D., Buendia B., Fuller S.D., Karsenti E., Reconstruction of the centrosome cycle from cryoelectron micrographs, J. Struct. Biol., 1997, 120, 117–133 http://dx.doi.org/10.1006/jsbi.1997.3928CrossrefGoogle Scholar

  • [3] Piel M., Meyer P., Khodjakov A., Rieder C.L., Bornens M., The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells, J. Cell Biol., 2000, 149, 317–330 http://dx.doi.org/10.1083/jcb.149.2.317CrossrefGoogle Scholar

  • [4] Bobinnec Y., Khodjakov A., Mir L.M., Rieder C.L., Edde B., Bornens M., Centriole disassembly in vivo and its effect on centrosome structure and function in vertebrate cells, J. Cell Biol., 1998, 143, 1575–1589 http://dx.doi.org/10.1083/jcb.143.6.1575CrossrefGoogle Scholar

  • [5] Bornens M., Centrosome composition and microtubule anchoring mechanisms, Curr. Opin. Cell Biol., 2002, 14, 25–34 http://dx.doi.org/10.1016/S0955-0674(01)00290-3CrossrefGoogle Scholar

  • [6] Fukasawa K., Introduction. Centrosome, Oncogene, 2002, 21, 6140–6145 http://dx.doi.org/10.1038/sj.onc.1205771CrossrefGoogle Scholar

  • [7] Rieder C.L., Faruki S., Khodjakov A., The centrosome in vertebrates: more than a microtubule-organizing center, Trends Cell Biol., 2001, 11, 413–419 http://dx.doi.org/10.1016/S0962-8924(01)02085-2CrossrefGoogle Scholar

  • [8] Zhong X., Pfeifer G.P., Xu X., Microcephalin encodes a centrosomal protein, Cell Cycle, 2006, 5, 457–458 CrossrefGoogle Scholar

  • [9] Doxsey S., Zimmerman W., Mikule K., Centrosome control of the cell cycle, Trends Cell Biol., 2005, 15, 303–311 http://dx.doi.org/10.1016/j.tcb.2005.04.008CrossrefGoogle Scholar

  • [10] Andersen J.S., Wilkinson C.J., Mayor T., Mortensen P., Nigg E.A., Mann M., Proteomic characterization of the human centrosome by protein correlation profiling, Nature, 2003, 426, 570–574 http://dx.doi.org/10.1038/nature02166CrossrefGoogle Scholar

  • [11] Wilkinson C.J., Andersen J.S., Mann M., Nigg E.A., A proteomic approach to the inventory of the human centrosome, In: Nigg E.A., (Ed.), Centrosomes in Development and Disease, Wiley InterScience, Weinheim, 2005, 125–142 Google Scholar

  • [12] Gomez-Ferreria M.A., Rath U., Buster D.W., Chanda S.K., Caldwell J.S., Rines D.R., et al., Human cep192 is required for mitotic centrosome and spindle assembly, Curr. Biol., 2007, 17, 1960–1966 http://dx.doi.org/10.1016/j.cub.2007.10.019CrossrefGoogle Scholar

  • [13] Graser S., Stierhof Y.D., Nigg E.A., Cep68 and Cep215 (Cdk5rap2) are required for centrosome cohesion, J. Cell Sci., 2007, 120, 4321–4331 http://dx.doi.org/10.1242/jcs.020248CrossrefGoogle Scholar

  • [14] Gromley A., Jurczyk A., Sillibourne J., Halilovic E., Mogensen M., Groisman I., 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 http://dx.doi.org/10.1083/jcb.200301105CrossrefGoogle Scholar

  • [15] Guarguaglini G., Duncan P.I., Stierhof Y.D., Holmstrom T., Duensing S., Nigg E.A., The forkhead-associated domain protein Cep170 interacts with Polo-like kinase 1 and serves as a marker for mature centrioles, Mol. Biol. Cell, 2005, 16, 1095–1107 http://dx.doi.org/10.1091/mbc.E04-10-0939CrossrefGoogle Scholar

  • [16] Salisbury J.L., Suino K.M., Busby R., Springett M., Centrin-2 is required for centriole duplication in mammalian cells, Curr. Biol., 2002, 12, 1287–1292 http://dx.doi.org/10.1016/S0960-9822(02)01019-9CrossrefGoogle Scholar

  • [17] Strnad P., Leidel S., Vinogradova T., Euteneuer U., Khodjakov A., Gonczy P., Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle, Dev Cell, 2007, 13, 203–213 http://dx.doi.org/10.1016/j.devcel.2007.07.004CrossrefGoogle Scholar

  • [18] Xie Z., Moy L.Y., Sanada K., Zhou Y., Buchman J.J., Tsai L.H., Cep120 and TACCs Control Interkinetic Nuclear Migration and the Neural Progenitor Pool, Neuron, 2007, 56, 79–93 http://dx.doi.org/10.1016/j.neuron.2007.08.026CrossrefGoogle Scholar

  • [19] Zhao W.M., Seki A., Fang G., Cep55, a microtubule-bundling protein, associates with centralspindlin to control the midbody integrity and cell abscission during cytokinesis, Mol. Biol. Cell, 2006, 17, 3881–3896 http://dx.doi.org/10.1091/mbc.E06-01-0015CrossrefGoogle Scholar

  • [20] Zou C., Li J., Bai Y., Gunning W.T., Wazer D.E., Band V., et al., Centrobin: a novel daughter centriole-associated protein that is required for centriole duplication, J. Cell Biol., 2005, 171, 437–445 http://dx.doi.org/10.1083/jcb.200506185CrossrefGoogle Scholar

  • [21] Muto Y., Yoshioka T., Kimura M., Matsunami M., Saya H., Okano Y., An evolutionarily conserved leucine-rich repeat protein CLERC is a centrosomal protein required for spindle pole integrity, Cell Cycle, 2008, 7, 2738–2748 CrossrefGoogle Scholar

  • [22] Kobe B., Kajava A.V., The leucine-rich repeat as a protein recognition motif, Curr. Opin. Struct. Biol., 2001, 11, 725–732 http://dx.doi.org/10.1016/S0959-440X(01)00266-4CrossrefGoogle Scholar

  • [23] Takahashi N., Takahashi Y., Putnam F.W., Periodicity of leucine and tandem repetition of a 24-amino acid segment in the primary structure of leucine-rich alpha 2-glycoprotein of human serum, Proc. Natl. Acad. Sci. U.S.A., 1985, 82, 1906–1910 http://dx.doi.org/10.1073/pnas.82.7.1906CrossrefGoogle Scholar

  • [24] Kobe B., Deisenhofer J., The leucine-rich repeat: a versatile binding motif, Trends Biochem. Sci., 1994, 19, 415–421 http://dx.doi.org/10.1016/0968-0004(94)90090-6CrossrefGoogle Scholar

  • [25] Kobe B., Deisenhofer J., Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats, Nature, 1993, 366, 751–756 http://dx.doi.org/10.1038/366751a0CrossrefGoogle Scholar

  • [26] Kobe B., Kajava A.V., When protein folding is simplified to protein coiling: the continuum of solenoid protein structures, Trends Biochem. Sci., 2000, 25, 509–515 http://dx.doi.org/10.1016/S0968-0004(00)01667-4CrossrefGoogle Scholar

  • [27] Bella J., Hindle K.L., McEwan P.A., Lovell S.C., The leucine-rich repeat structure, Cell. Mol. Life Sci., 2008, 65, 2307–2333 http://dx.doi.org/10.1007/s00018-008-8019-0CrossrefGoogle Scholar

  • [28] Matsushima N., Tachi N., Kuroki Y., Enkhbayar P., Osaki M., Kamiya M., et al., Structural analysis of leucine-rich-repeat variants in proteins associated with human diseases, Cell. Mol. Life Sci., 2005, 62, 2771–2791 http://dx.doi.org/10.1007/s00018-005-5187-zCrossrefGoogle Scholar

  • [29] Hohenester E., Hussain S., Howitt J.A., Interaction of the guidance molecule Slit with cellular receptors, Biochem. Soc. Trans., 2006, 34, 418–421 http://dx.doi.org/10.1042/BST0340418CrossrefGoogle Scholar

  • [30] Matilla A., Radrizzani M., The Anp32 family of proteins containing leucine-rich repeats, Cerebellum, 2005, 4, 7–18 http://dx.doi.org/10.1080/14734220410019020CrossrefGoogle Scholar

  • [31] Liker E., Fernandez E., Izaurralde E., Conti E., The structure of the mRNA export factor TAP reveals a cis arrangement of a non-canonical RNP domain and an LRR domain, EMBO J., 2000, 19, 5587–5598 http://dx.doi.org/10.1093/emboj/19.21.5587CrossrefGoogle Scholar

  • [32] Price S.R., Evans P.R., Nagai K., Crystal structure of the spliceosomal U2B″-U2A′ protein complex bound to a fragment of U2 small nuclear RNA, Nature, 1998, 394, 645–650 http://dx.doi.org/10.1038/29234CrossrefGoogle Scholar

  • [33] Chen Y., Aulia S., Li L., Tang B.L., AMIGO and friends: an emerging family of brain-enriched, neuronal growth modulating, type I transmembrane proteins with leucine-rich repeats (LRR) and cell adhesion molecule motifs, Brain Res Rev, 2006, 51, 265–274 http://dx.doi.org/10.1016/j.brainresrev.2005.11.005CrossrefGoogle Scholar

  • [34] Ko J., Kim E., Leucine-rich repeat proteins of synapses, J. Neurosci. Res., 2007, 85, 2824–2832 http://dx.doi.org/10.1002/jnr.21306CrossrefGoogle Scholar

  • [35] Gay N.J., Gangloff M., Structure and function of Toll receptors and their ligands, Annu. Rev. Biochem., 2007, 76, 141–165 http://dx.doi.org/10.1146/annurev.biochem.76.060305.151318CrossrefGoogle Scholar

  • [36] Pancer Z., Cooper M.D., The evolution of adaptive immunity, Annu. Rev. Immunol., 2006, 24, 497–518 http://dx.doi.org/10.1146/annurev.immunol.24.021605.090542CrossrefGoogle Scholar

  • [37] Hocking A.M., Shinomura T., McQuillan D.J., Leucine-rich repeat glycoproteins of the extracellular matrix, Matrix Biol., 1998, 17, 1–19 http://dx.doi.org/10.1016/S0945-053X(98)90121-4CrossrefGoogle Scholar

  • [38] Nogales-Cadenas R., Abascal F., Diez-Perez J., Carazo J.M., Pascual-Montano A., CentrosomeDB: a human centrosomal proteins database, Nucl. Acids Res., 2009, 37, D175–D180 http://dx.doi.org/10.1093/nar/gkn815CrossrefGoogle Scholar

  • [39] Eddy S.R., Profile hidden Markov models, Bioinformatics, 1998, 14, 755–763 http://dx.doi.org/10.1093/bioinformatics/14.9.755CrossrefGoogle Scholar

  • [40] Kajava A.V., Structural diversity of leucine-rich repeat proteins, J. Mol. Biol., 1998, 277, 519–527 http://dx.doi.org/10.1006/jmbi.1998.1643CrossrefGoogle Scholar

  • [41] Schneider T.D., Stephens R.M., Sequence logos: a new way to display consensus sequences, Nucl. Acids Res., 1990, 18, 6097–6100 http://dx.doi.org/10.1093/nar/18.20.6097CrossrefGoogle Scholar

  • [42] Crooks G.E., Hon G., Chandonia J.M., Brenner S.E., WebLogo: a sequence logo generator, Genome Res., 2004, 14, 1188–1190 http://dx.doi.org/10.1101/gr.849004CrossrefGoogle Scholar

  • [43] Dutcher S.K., Elucidation of basal body and centriole functions in Chlamydomonas reinhardtii, Traffic, 2003, 4, 443–451 http://dx.doi.org/10.1034/j.1600-0854.2003.00104.xCrossrefGoogle Scholar

  • [44] Adams G.M., Wright R.L., Jarvik J.W., Defective temporal and spatial control of flagellar assembly in a mutant of Chlamydomonas reinhardtii with variable flagellar number, J. Cell Biol., 1985, 100, 955–964 http://dx.doi.org/10.1083/jcb.100.3.955CrossrefGoogle Scholar

  • [45] Silflow C.D., LaVoie M., Tam L.W., Tousey S., Sanders M., Wu W., et al., The Vfl1 Protein in Chlamydomonas localizes in a rotationally asymmetric pattern at the distal ends of the basal bodies, J. Cell Biol., 2001, 153, 63–74 http://dx.doi.org/10.1083/jcb.153.1.63CrossrefGoogle Scholar

  • [46] Keryer G., Ris H., Borisy G.G., Centriole distribution during tripolar mitosis in Chinese hamster ovary cells, J. Cell Biol., 1984, 98, 2222–2229 http://dx.doi.org/10.1083/jcb.98.6.2222CrossrefGoogle Scholar

  • [47] Sluder G., Rieder C.L., Centriole number and the reproductive capacity of spindle poles, J. Cell Biol., 1985, 100, 887–896 http://dx.doi.org/10.1083/jcb.100.3.887CrossrefGoogle Scholar

  • [48] Di Fiore B., Ciciarello M., Mangiacasale R., Palena A., Tassin A.M., Cundari E., et al., Mammalian RanBP1 regulates centrosome cohesion during mitosis, J. Cell Sci., 2003, 116, 3399–3411 http://dx.doi.org/10.1242/jcs.00624CrossrefGoogle Scholar

  • [49] Thein K.H., Kleylein-Sohn J., Nigg E.A., Gruneberg U., Astrin is required for the maintenance of sister chromatid cohesion and centrosome integrity, J. Cell Biol., 2007, 178, 345–354 http://dx.doi.org/10.1083/jcb.200701163CrossrefGoogle Scholar

  • [50] Wang X., Yang Y., Duan Q., Jiang N., Huang Y., Darzynkiewicz Z., et al., sSgo1, a major splice variant of Sgo1, functions in centriole cohesion where it is regulated by Plk1, Dev. Cell, 2008, 14, 331–341 http://dx.doi.org/10.1016/j.devcel.2007.12.007CrossrefGoogle Scholar

  • [51] McDonald K., Morphew M.K., Improved preservation of ultrastructure in difficult-to-fix organisms by high pressure freezing and freeze substitution: I. Drosophila melanogaster and Strongylocentrotus purpuratus embryos, Microsc. Res. Tech., 1993, 24, 465–473 http://dx.doi.org/10.1002/jemt.1070240603CrossrefGoogle Scholar

  • [52] Moritz M., Braunfeld M.B., Fung J.C., Sedat J.W., Alberts B.M., Agard D.A., Three-dimensional structural characterization of centrosomes from early Drosophila embryos, J. Cell Biol., 1995, 130, 1149–1159 http://dx.doi.org/10.1083/jcb.130.5.1149CrossrefGoogle Scholar

  • [53] Perkins L.A., Hedgecock E.M., Thomson J.N., Culotti J.G., Mutant sensory cilia in the nematode Caenorhabditis elegans, Dev. Biol., 1986, 117, 456–487 http://dx.doi.org/10.1016/0012-1606(86)90314-3CrossrefGoogle Scholar

  • [54] Lee M.J., Gergely F., Jeffers K., Peak-Chew S.Y., Raff J.W., Msps/XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behaviour, Nat. Cell Biol., 2001, 3, 643–649 http://dx.doi.org/10.1038/35083033Google Scholar

  • [55] Andersen S.S., Spindle assembly and the art of regulating microtubule dynamics by MAPs and Stathmin/Op18, Trends Cell Biol., 2000, 10, 261–267 http://dx.doi.org/10.1016/S0962-8924(00)01786-4CrossrefGoogle Scholar

  • [56] Guasch G., Mack G.J., Popovici C., Dastugue N., Birnbaum D., Rattner J.B., et al., FGFR1 is fused to the centrosome-associated protein CEP110 in the 8p12 stem cell myeloproliferative disorder with t(8;9)(p12;q33), Blood, 2000, 95, 1788–1796 Google Scholar

  • [57] McCollum D., Gould K.L., Timing is everything: regulation of mitotic exit and cytokinesis by the MEN and SIN, Trends Cell Biol., 2001, 11, 89–95 http://dx.doi.org/10.1016/S0962-8924(00)01901-2CrossrefGoogle Scholar

  • [58] Vorobjev I.A., Chentsov Yu S., Centrioles in the cell cycle. I. Epithelial cells, J. Cell Biol., 1982, 93, 938–949 http://dx.doi.org/10.1083/jcb.93.3.938CrossrefGoogle Scholar

  • [59] Gromley A., Yeaman C., Rosa J., Redick S., Chen C.T., Mirabelle S., et al., Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission, Cell, 2005, 123, 75–87 http://dx.doi.org/10.1016/j.cell.2005.07.027CrossrefGoogle Scholar

  • [60] Paweletz N., On the function of the “Flemming body” during division of animal cells, Naturwissenschaften, 1967, 54, 533–535 http://dx.doi.org/10.1007/BF00627210CrossrefGoogle Scholar

  • [61] Fielding A.B., Schonteich E., Matheson J., Wilson G., Yu X., Hickson G.R., et al., Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis, EMBO J., 2005, 24, 3389–3399 http://dx.doi.org/10.1038/sj.emboj.7600803CrossrefGoogle Scholar

  • [62] Chen Z., Indjeian V.B., McManus M., Wang L., Dynlacht B.D., CP110, a cell cycle-dependent CDK substrate, regulates centrosome duplication in human cells, Dev. Cell, 2002, 3, 339–350 http://dx.doi.org/10.1016/S1534-5807(02)00258-7Google Scholar

  • [63] Tsang W.Y., Spektor A., Luciano D.J., Indjeian V.B., Chen Z., Salisbury J.L., et al., CP110 cooperates with two calcium-binding proteins to regulate cytokinesis and genome stability, Mol. Biol. Cell, 2006, 17, 3423–3434 http://dx.doi.org/10.1091/mbc.E06-04-0371Google Scholar

  • [64] Spektor A., Tsang W.Y., Khoo D., Dynlacht B.D., Cep97 and CP110 suppress a cilia assembly program, Cell, 2007, 130, 678–690 http://dx.doi.org/10.1016/j.cell.2007.06.027CrossrefGoogle Scholar

  • [65] Wheatley D.N., Wang A.M., Strugnell G.E., Expression of primary cilia in mammalian cells, Cell Biol. Int., 1996, 20, 73–81 http://dx.doi.org/10.1006/cbir.1996.0011CrossrefGoogle Scholar

  • [66] Xue J.C., Goldberg E., Identification of a novel testis-specific leucine-rich protein in humans and mice, Biol. Reprod., 2000, 62, 1278–1284 http://dx.doi.org/10.1095/biolreprod62.5.1278CrossrefGoogle Scholar

  • [67] Morgan G.W., Denny P.W., Vaughan S., Goulding D., Jeffries T.R., Smith D.F., et al., An evolutionarily conserved coiled-coil protein implicated in polycystic kidney disease is involved in basal body duplication and flagellar biogenesis in Trypanosoma brucei, Mol. Cell. Biol., 2005, 25, 3774–3783 http://dx.doi.org/10.1128/MCB.25.9.3774-3783.2005CrossrefGoogle Scholar

  • [68] Sun Z., Amsterdam A., Pazour G.J., Cole D.G., Miller M.S., Hopkins N., A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney, Development, 2004, 131, 4085–4093 http://dx.doi.org/10.1242/dev.01240CrossrefGoogle Scholar

  • [69] Kishimoto N., Cao Y., Park A., Sun Z., Cystic kidney gene seahorse regulates cilia-mediated processes and Wnt pathways, Dev. Cell, 2008, 14, 954–961 http://dx.doi.org/10.1016/j.devcel.2008.03.010CrossrefGoogle Scholar

  • [70] Serluca F.C., Xu B., Okabe N., Baker K., Lin S.Y., Sullivan-Brown J., et al., Mutations in zebrafish leucine-rich repeat-containing six-like affect cilia motility and result in pronephric cysts, but have variable effects on left-right patterning, Development, 2009, 136, 1621–1631 http://dx.doi.org/10.1242/dev.020735CrossrefGoogle Scholar

  • [71] Oshimori N., Ohsugi M., Yamamoto T., The Plk1 target Kizuna stabilizes mitotic centrosomes to ensure spindle bipolarity, Nat. Cell Biol., 2006, 8, 1095–1101 http://dx.doi.org/10.1038/ncb1474CrossrefGoogle Scholar

  • [72] Pereira G., Hofken T., Grindlay J., Manson C., Schiebel E., The Bub2p spindle checkpoint links nuclear migration with mitotic exit, Mol. Cell, 2000, 6, 1–10 http://dx.doi.org/10.1016/S1097-2765(00)00002-2CrossrefGoogle Scholar

  • [73] Oshimori N., Li X., Ohsugi M., Yamamoto T., Cep72 regulates the localization of key centrosomal proteins and proper bipolar spindle formation, EMBO J., 2009, 28, 2066–2076 http://dx.doi.org/10.1038/emboj.2009.161CrossrefGoogle Scholar

About the article

Published Online: 2010-01-30

Published in Print: 2010-02-01


Citation Information: Open Life Sciences, Volume 5, Issue 1, Pages 1–10, ISSN (Online) 2391-5412, DOI: https://doi.org/10.2478/s11535-009-0061-x.

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