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Origin and Evolution of the Centrosome

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Eukaryotic Membranes and Cytoskeleton

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 607))

Abstract

In this brief account we specifically address the question of how the plasma membrane-associated basal body/axoneme of the unicellular ancestor of eukaryotes has evolved into the centrosome organelle through the several attempts to multicellularity. We propose that the connection between the flagellar apparatus and the nucleus has been a critical feature for leading to the centriole-based centrosome of metazoa, the Spindle Pole Body of fungi, or to the absence of any centrosome in seed plants. We further suggest that the evolution of this connection could be reflected in the evolution of the centrin proteins. We then review evidence showing that the evolution of the centrosome-based tubulin network has been correlated with the evolution of the cortical actin-based cleavage apparatus. Finally we argue that this coevolution had a major impact on the cell individuation process and on the evolution of multicellular organisms. We conclude that only the metazoan lineage evolved multicellularity without loosing the ancestral association of three basic cellular functions of the basal body/ axoneme or the derived centrosome organelle, namely sensation, motion and division.

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References

  1. Mitchell DR. Speculations on the evolution of 9+2 organelles and the role of central pair microtubules. Biol Cell 2004; 96(9):691–6.

    Article  PubMed  CAS  Google Scholar 

  2. Mitchell DR. The evolution of eukaryotic cilia and flagella as motile and sensory organelles. In: Gáspár Jékely, ed. Origins ansd Evolution of Eukaryotic Endomembranes and Cytoskeleton. 2006, (Eureka.com).

    Google Scholar 

  3. Jékely G, Arendt D. Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. Bioessays 2006; 28(2):191–8.

    Article  PubMed  Google Scholar 

  4. Jékely G. Origin of eukaryotic endomembranes — A critical evaluation of different model scenarios. In: Gáspár Jékely, ed. Origins and Evolution of Eukaryotic Endomembranes and Cytoskeleton. Austin: Landes Bioscience, 2007, (Eurekah.com).

    Google Scholar 

  5. Baroin A, Perasso R, Qu L et al. Partial phylogeny of the unicellular eukaryotes based on rapid sequencing of a portion of 28S ribosomal RNA. Proc Natl Acad Sci US 1988; 85(10):3474–8.

    Article  CAS  Google Scholar 

  6. Gull K. Protist tubulins: New arrivals, evolutionary relationships and insights to cytoskeletal function. Curr Opin Microbiol 2001; 4(4):427–32.

    Article  PubMed  CAS  Google Scholar 

  7. Gull K. The biology of kinetoplastid parasites: Insights and challenges from genomics and post-genomics. Int J Parasitol 2001; 31(5–6):443–52.

    Article  PubMed  CAS  Google Scholar 

  8. Azimzadeh J, Bornens M. The centrosome in evolution. In: Nigg EA, ed. Centrosomes in Development and Disease. Weinheim: Wiley-VCH, 2004:93–122.

    Chapter  Google Scholar 

  9. Bray D, Duke T. Conformational spread: The propagation of allosteric states in large multiprotein complexes. Annu Rev Biophys Biomol Struct 2004; 33:53–73.

    Article  PubMed  CAS  Google Scholar 

  10. Janicki C. Centrioles and kinetosomes: Form, function, and evolution. In: Chapman MJ, Colan MF, Margulis L, eds. The Quarterly Review of Biology. 2000; 75(4):409–29, (1915, quoted).

    Google Scholar 

  11. Salisbury JL. The lost neuromotor apparatus of Chlamydomonas rediscovered. J Protozool 1988; 35(4):574–7.

    PubMed  CAS  Google Scholar 

  12. Bornens M. Is the centriole bound to the nuclear membrane? Nature 1977; 270(5632): 80–2.

    Article  PubMed  CAS  Google Scholar 

  13. Morris NR. Nuclear migration. From fungi to the mammalian brain. J Cell Biol 2000; 148(6):1097–101.

    Article  PubMed  CAS  Google Scholar 

  14. Reinsch S, Gonczy P. Mechanisms of nuclear positioning. J Cell Sci 1998; 111:2283–2295.

    PubMed  CAS  Google Scholar 

  15. Tanaka T, Serneo FF, Higgins C et al. Lisl and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 2004; 165(5):709–21.

    Article  PubMed  CAS  Google Scholar 

  16. Taxis C, Keller P, Kavagiou Z et al. Spore number control and breeding in Saccharomyces cerevisiae: A key role for a self-organizing system. J Cell Biol 2005; 171(4):627–40.

    Article  PubMed  CAS  Google Scholar 

  17. King N. The unicellularancestry of animal development. Dev Cell 2004; 7:313–325

    Article  PubMed  CAS  Google Scholar 

  18. Gross JD. Developmental decisions in Dictyostelium discoideum. Microbiol Rev 1994; 58(3):330–51.

    PubMed  CAS  Google Scholar 

  19. Buss LW. Evolution, development, and the units of selection. Proc Natl Acad Sci USA 1983; 80:1387–1391.

    Article  PubMed  CAS  Google Scholar 

  20. Hoops HJ, Witman GB. Basal bodies and associated structures are not required for normal flagellar motion or phototaxis in the green alga Chlorogonium elongatum. J Cell Biol 1985; 100(l):297–309.

    Article  PubMed  CAS  Google Scholar 

  21. Bastin P, Pullen TJ, Sherwin T et al. Protein transport and flagellum assembly dynamics revealed by analysis of the paralysed trypanosome mutant snl-1. J Cell Sci 1999; 112(Pt 21):3769–77.

    PubMed  CAS  Google Scholar 

  22. Gull K. Host-parasite interactions and trypanosome morphogenesis: A flagellar pocketful of goodies. Curr Opin Microbiol 2003; 6(4):365–70.

    Article  PubMed  CAS  Google Scholar 

  23. Cavalier-Smith T. Only six kingdoms of life. Proc Roy Soc Lond 2004; B271:1251–1262.

    Article  Google Scholar 

  24. Richards TA, Cavalier-Smith T. Myosin domain evolution and the primary divergence of eukaryotes. Nature 2005; 436(7054):1113–8.

    Article  PubMed  CAS  Google Scholar 

  25. Brickmann H, Philippe H. The diversity of eukaryotes and the root of the eukaryotic tree. In: Gáspár Jékely, ed. Origins and Evolution of Eukaryotic Endomembranes and Cytoskeleton. Austin: Landes Bioscience, 2006, (Eurekah.com).

    Google Scholar 

  26. Hartman H, Fedorov A. The origin of the eukaryotic cell: A genomic investigation. Proc Natl Acad Sci US 2002; 99(3): 1420–5, (Erratum in: Proc Natl Acad Sci USA. 2002; 99(7):4752).

    Article  CAS  Google Scholar 

  27. Salisbury JL, Baron AT, Sanders MA. The centrin-based cytoskeleton of Chlamydomonas reinhardtii: Distribution in interphase and mitotic cells. J Cell Biol 1988; 107(2):635–41.

    Article  PubMed  CAS  Google Scholar 

  28. Geimer S, Melkonian M. The ultrastructure of the Chlamydomonas reinhardtii basal apparatus: Identification of an early marker of radial asymmetry inherent in the basal body. J Cell Sci 2004; 117(13):2663–74.

    Article  PubMed  CAS  Google Scholar 

  29. Huang B, Watterson DM, Lee VD et al. Purification and characterization of a basal body-associated Ca(2+)-binding protein. J Cell Biol 1988; 107:121–131.

    Article  PubMed  CAS  Google Scholar 

  30. Spang A, Courtney I, Grein K et al. The Cdc31p-binding protein Karlp is a component of the half bridge of the yeast spindle pole body. J Cell Biol 1995; 128(5):863–77.

    Article  PubMed  CAS  Google Scholar 

  31. Paoletti A, Bordes N, Haddad R et al. Fission yeast cdc31p is a component of the half-bridge and controls SPB duplication. Mol Biol Cell 2003; 14(7):2793–808.

    Article  PubMed  CAS  Google Scholar 

  32. Salisbury JL, Suino KM, Busby R et al. Centrin-2 is required for centriole duplication in mammalian cells. Curr Biol 2002; 12(15):1287–92.

    Article  PubMed  CAS  Google Scholar 

  33. Koblenz B, Schoppmeier J, Grunow A et al. Centrin deficiency in Chlamydomonas causes defects in basal body replication, segregation and maturation. J Cell Sci 2003; 116(13):2635–46.

    Article  PubMed  CAS  Google Scholar 

  34. Taillon BE, Adler SA, Suhan JP et al. Mutational analysis of centrin: An EF-hand protein associated with three distinct contractile fibers in the basal body apparatus of Chlamydomonas. J Cell Biol 1992; 119(6): 1613–24.

    Article  PubMed  CAS  Google Scholar 

  35. Araki M, Masutani C, Takemura M et al. Centrosome protein centrin 2/caltractin 1 is part of the Xeroderma Pigmentosum group C complex that initiates global genome nucleotide excision repair. J Biol Chem 2001; 276(22): 18665–72.

    Article  PubMed  CAS  Google Scholar 

  36. Fischer T, Rodriguez-Navarro S, Pereira G et al. Yeast centrin Cdc31 is linked to the nuclear mRNA export machinery. Nat Cell Biol 2004; 6(9):840–8.

    Article  PubMed  CAS  Google Scholar 

  37. He CY, Pypaert M, Warren G. Golgi duplication in Trypanosoma brucei requires Centrin2. Science 2005; 310(5751):1196–8.

    Article  PubMed  CAS  Google Scholar 

  38. Molinier J, Ramos C, Fritsch O et al. CENTRIN2 modulates homologous recombination and nucleotide excision repair in Arabidopsis. Plant Cell 2004; 16(6): 1633–43.

    Article  PubMed  CAS  Google Scholar 

  39. Nishi R, Okuda Y, Watanabe E et al. Centrin 2 stimulates nucleotide excision repair by interacting with xeroderma pigmentosum group C protein. Mol Cell Biol 2005; 25(13):5664–74.

    Article  PubMed  CAS  Google Scholar 

  40. Pulvermuller A, Giessl A, Heck M et al. Calcium-dependent assembly of centrin-G-protein complex in photoreceptor cells. Mol Cell Biol 2002; 22:2194–2203.

    Article  PubMed  CAS  Google Scholar 

  41. Sullivan DS, Biggins S, Rose MD. The yeast centrin, Cdc31p, and the interacting protein kinase, Kiclp, are required for cell integrity. J Cell Biol 1998; 143:751–765.

    Article  PubMed  CAS  Google Scholar 

  42. Lee VD, Huang B. Molecular cloning and centrosomal localization of human caltractin. Proc Natl Acad Sci USA 1993; 90(23): 11039–43.

    Article  PubMed  CAS  Google Scholar 

  43. Errabolu R, Sanders MA, Salisbury JL. Cloning of a cDNA encoding human centrin, an EF-hand protein of centrosomes and mitotic spindle poles. J Cell Sci 1994; 107(Pt 1):9–16.

    PubMed  CAS  Google Scholar 

  44. Wolfrum U, Salisbury JL. Expression of centrin isoforms in the mammalian retina. Exp Cell Res 1998; 242(l):10–7.

    Article  PubMed  CAS  Google Scholar 

  45. Hart PE, Glantz JN, Orth JD et al. Testis-specific murine centrin, Cetnl: Genomic characterization and evidence for retroposition of a gene encoding a centrosome protein. Genomics 1999; 60(2):111–20.

    Article  PubMed  CAS  Google Scholar 

  46. Laoukili J, Perret E, Middendorp S et al. Differential expression and cellular distribution of centrin isoforms during human ciliated cell differentiation in vitro. J Cell Sci 2000; 113(Pt 8):1355–64.

    PubMed  CAS  Google Scholar 

  47. Gavet O, Alvarez C, Gaspar P et al. Centrin4p, a novel mammalian centrin specifically expressed in ciliated cells. Mol Biol Cell 2003; 14(5):1818–34.

    Article  PubMed  CAS  Google Scholar 

  48. Middendorp S, Paoletti A, Schiebel E et al. Identification of a new mammalian centrin gene, more closely related to Saccharomyces cerevisiae CDC31 gene. Proc Natl Acad Sci US 1997; 94(17):9141–6.

    Article  CAS  Google Scholar 

  49. Ribichich KF, Gomes SL. Blastocladiella emersonii expresses a centrin similar to Chlamydomonas reinhardtii isoform not found in late-diverging fungi. FEBS Lett 2005; 579(20):4355–60.

    Article  PubMed  CAS  Google Scholar 

  50. Leidel S, Gonczy P. Centrosome duplication and nematodes: Recent insights from an old relationship. Dev Cell 2005; 9(3):317–25.

    Article  PubMed  CAS  Google Scholar 

  51. Grunow A, Lechtreck KF. Mitosis in Dunaliella bioculata (Chlorophyta): Centrin but not basal bodies are at the spindle poles. Journal of Phycology 2001; 37(6): 1030–1043.

    Article  Google Scholar 

  52. Daunderer C, Schliwa M, Graf R. Dictyostelium centrin-related protein (DdCrp), the most divergent member of the centrin family, possesses only two EF hands and dissociates from the centrosome during mitosis. Eur J Cell Biol 2001; 80(10):621–30.

    Article  PubMed  CAS  Google Scholar 

  53. Jaspersen SL, Giddings Jr TH, Winey M. Mps3p is a novel component of the yeast spindle pole body that interacts with the yeast centrin homologue Cdc31p. J Cell Biol 2002; 159(6):945–56.

    Article  PubMed  CAS  Google Scholar 

  54. Biggins S, Rose MD. Direct interaction between yeast spindle pole body components: Karlp is required for Cdc31p localization to the spindle pole body. J Cell Biol 1994; 125(4):843–52.

    Article  PubMed  CAS  Google Scholar 

  55. Kilmartin JV. Sfilp has conserved centrin-binding sites and an essential function in budding yeast spindle pole body duplication. J Cell Biol 2003; 162(7):1211–21.

    Article  PubMed  CAS  Google Scholar 

  56. Li S, Sandercock AM, Conduit P et al. Structural role of Sfilp-centrin filaments in budding yeast spindle pole body duplication. J Cell Biol 2006; 173(6):867–77.

    Article  PubMed  CAS  Google Scholar 

  57. Kallenbach RJ, Mazia D. Origin and maturation of centrioles in association with the nuclear envelope in hypertonic-stressed sea urchin eggs. Eur J Cell Biol 1982; 28(l):68–76.

    PubMed  CAS  Google Scholar 

  58. Adams IR, Kilmartin JV. Spindle pole body duplication: A model for centrosome duplication? Trends Cell Biol 2000; 10(8):329–35.

    Article  PubMed  CAS  Google Scholar 

  59. Middendorp S, Kuntziger T, Abraham Y et al. A role for centrin 3 in centrosome reproduction. J Cell Biol 2000; 148(3):405–16.

    Article  PubMed  CAS  Google Scholar 

  60. Pazour GJ, Agrin N, Leszyk J et al. Proteomic analysis of a eukaryotic cilium. J Cell Biol 2005; 170(l):103–13.

    Article  PubMed  CAS  Google Scholar 

  61. Lawrence C, Morris, Meagher R et al. Dyneins have run their course in plant lineage. Traffic 2001; 2(5):362–363.

    Article  PubMed  CAS  Google Scholar 

  62. Cowan CR, Hyman AA. Centrosomes direct cell polarity independently of microtubule assembly in C. elegans embryos. Nature 2004; 431(7004):92–6.

    Article  PubMed  CAS  Google Scholar 

  63. Avidor-Reiss T, Maer AM, Koundakjian E et al. Decoding cilia function: Defining specialized genes required for compartmentalized cilia biogenesis. Cell 2004; 117(4):527–39.

    Article  PubMed  CAS  Google Scholar 

  64. Szollosi A, Ris H, Szollosi D et al. A centriole-free Drosophila cell line. A high voltage EM study. Eur J Cell Biol 1986; 40(1): 100–4.

    PubMed  CAS  Google Scholar 

  65. Bettencourt-Dias M, Rodrigues-Martins A, Carpenter L et al. SAK/PLK4 is required for centriole duplication and flagella development. Curr Biol 2005; 15(24):2199–207.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. UMR 144-CNRS-lnstitut Curie, 75248, Paris Cedex 05, France

    Michel Bornens & Juliette Azimzadeh

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  1. Michel Bornens
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  2. Juliette Azimzadeh
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Correspondence to Michel Bornens .

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Bornens, M., Azimzadeh, J. (2007). Origin and Evolution of the Centrosome. In: Eukaryotic Membranes and Cytoskeleton. Advances in Experimental Medicine and Biology, vol 607. Springer, New York, NY. https://doi.org/10.1007/978-0-387-74021-8_10

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