Origins and Evolution of the Actin Cytoskeleton

  • Francisco Rivero
  • Fatima Cvrčková
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 607)


The presence of a complex cytoskeletal system is a hallmark feature of eukaryotic cells, distinguishing them from their prokaryotic (bacterial or archaeal) “cousins”. No extant prokaryote studied so far possesses obvious homologues of major cytoskeletal proteins shared universally among eukaryotes, such as e.g., actin or tubulin. However, several proteins exhibiting limited sequence similarity with certain cytoskeletal components, as well as the ability to form filaments, have been found.1–3 These include, among others, relatives of actin and actin-associated proteins that will be discussed in detail below, the FtsZ family of bacterial and archaeal tubulin-related proteins participating in cell division4 and an intermediate filament-like protein (crescentin) from Caulobacter. 5


Actin Filament Actin Cytoskeleton Myosin Head Curr Opin Cell Biol Eukaryotic Lineage 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Doolittle RF, York AL. Bacterial actins? An evolutionary perspective. BioEssays 2002; 24:293–296.PubMedCrossRefGoogle Scholar
  2. 2.
    Egelman EH. Actin’s prokaryotic homologs. Curr Opin Struct Biol 2003; 13:244–248.PubMedCrossRefGoogle Scholar
  3. 3.
    Margolin W. Bacterial shape: Concave coiled coils curve Caulobacter. Curr Biol 2004; 14:R242–R244.PubMedCrossRefGoogle Scholar
  4. 4.
    Bramhill D. Bacterial cell division. Annu Rev Cell Dev Biol 1997; 13:395–424.PubMedCrossRefGoogle Scholar
  5. 5.
    Ausmees N, Kuhn JR, Jacobs-Wagner C. The bacterial cytoskeleton: An intermediate filament-like function in cell shape. Cell 2003; 115:705–713.PubMedCrossRefGoogle Scholar
  6. 6.
    Gupta RS, Golding GB. The origin of the eukaryotic cell. Trends Biochem Sci 1996; 21:166–171.PubMedGoogle Scholar
  7. 7.
    Horiike T, Hamada K, Shinozawa T. Origin of eukaryotic cell nuclei by symbiosis of Archaea in Bacteria supported by the newly clarified origin of functional genes. Genes Genet Syst 2002; 77:369–376.PubMedCrossRefGoogle Scholar
  8. 8.
    Rivera MC, Lake JA. The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 2004; 431:152–155.PubMedCrossRefGoogle Scholar
  9. 9.
    Rivera MC, Jain R, Moore JE et al. Genomic evidence for two functionally distinct gene classes. Proc Natl Acad Sci USA 1998; 95:6239–6244.PubMedCrossRefGoogle Scholar
  10. 10.
    Li JY, Wu CF. Perspectives on the origin of microfilaments, microtubules, the relevant chaperonin system and cytoskeletal motors — a commentary on the spirochaete origin of flagella. Cell Res 2003; 13:219–227.PubMedCrossRefGoogle Scholar
  11. 11.
    Hartman H, Fedorov A. The origin of the eukaryotic cell: A genomic investigation. Proc Natl Acad Sci USA 2002; 99:16128–16133.CrossRefGoogle Scholar
  12. 12.
    Cvrcková F, Bavlnka B, Rivero F. Evolutionarily conserved modules in actin nucleation: Lessons from Dictyostelium discoideum and plants. Protoplasma 2004; 224:15–31.PubMedGoogle Scholar
  13. 13.
    Mitchison TJ. Evolution of a dynamic cytoskeleton. Philos Trans R Soc Lond B Biol Sci 1995; 349:299–304.PubMedCrossRefGoogle Scholar
  14. 14.
    Small JV, Stradal T, Vignal E et al. The lamellipodium: Where motility begins. Trends Cell Biol 2002; 12:112–120.PubMedCrossRefGoogle Scholar
  15. 15.
    Bader MF, Doussau F, Chasserot-Golaz S et al. Coupling actin and membrane dynamics during calcium-regulated exocytosis: A role for Rho and ARF GTPases. Biochim Biophys Acta 2004; 1742:37–49.PubMedCrossRefGoogle Scholar
  16. 16.
    Goldberg MB. Actin-based motility of intracellular microbial pathogens. Microbiol Mol Biol Rev 2001; 65:595–626.PubMedCrossRefGoogle Scholar
  17. 17.
    Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003; 112:453–465.PubMedCrossRefGoogle Scholar
  18. 18.
    Pruyne D, Legesse-Miller A, Gao L et al. Mechanisms of polarized growth and organelle segregation in yeast. Annu Rev Cell Dev Biol 2004; 20:559–591.PubMedCrossRefGoogle Scholar
  19. 19.
    Szymanski DB. Breaking the WAVE complex: The point of Arabidopsis trichomes. Curr Opin Plant Biol 2005; 8:103–112.PubMedCrossRefGoogle Scholar
  20. 20.
    Baluska F, Salaj J, Mathur J et al. Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol 2000; 227:618–632.PubMedCrossRefGoogle Scholar
  21. 21.
    Ringli C, Baumberger N, Diet A et al. ACTIN2 is essential for bulge site selection and tip growth during root hair development of Arabidopsis. Plant Physiol 2002; 129:1464–1472.PubMedCrossRefGoogle Scholar
  22. 22.
    Vidali L, McKenna ST, Hepler PK. Actin polymerization is essential for pollen tube growth. Mol Biol Cell 2001; 12:2534–2545.PubMedGoogle Scholar
  23. 23.
    Mathur J, Hulskamp M. Microtubules and microfilaments in cell morphogenesis in higher plants. Curr Biol 2002; 12:R669–R676.PubMedCrossRefGoogle Scholar
  24. 24.
    Field C, Li R, Oegema K. Cytokinesis in eukaryotes: A mechanistic comparison. Curr Opin Cell Biol 1999; 11:68–90.PubMedCrossRefGoogle Scholar
  25. 25.
    Hales KG, Bi E, Wu JQ et al. Cytokinesis: An emerging unified theory for eukaryotes? Curr Opin Cell Biol 1999; 11:717–725.PubMedCrossRefGoogle Scholar
  26. 26.
    Lénárt P, Bacher CP, Daigle N et al. A contractile nuclear actin network drives chromosome congression in oocytes. Nature 2005; 436:812–818.PubMedCrossRefGoogle Scholar
  27. 27.
    Bamburg JR, Drubin DG. Actin depolymerizing factor (ADF)/cofilin. In: Kreis T, Vale R, eds. Guidebook to the Cytoskeletal and Motor Proteins. Oxford: Oxford University Press, 1999:19–23.Google Scholar
  28. 28.
    Paavilainen VO, Bertling E, Falck S et al. Regulation of cytoskeletal dynamics by actin-monomer-binding proteins. Trends Cell Biol 2004; 14:386–394.PubMedCrossRefGoogle Scholar
  29. 29.
    McCurdy DW, Kovar DR, Staiger CJ. Actin and actin-binding proteins in higher plants. Protoplasma 2001; 215:89–104.PubMedCrossRefGoogle Scholar
  30. 30.
    Frankel S. Arps, divergent members. In: Kreis T, Vale R, eds. Guidebook to the Cytoskeletal and Motor Proteins. Oxford: Oxford University Press, 1999:49–52.Google Scholar
  31. 31.
    van den Ent F, Amos LA, Löwe J. Prokaryotic origin of the actin cytoskeleton. Nature 2001; 413:39–44.PubMedCrossRefGoogle Scholar
  32. 32.
    Jones LJ, Carballido-Lopez R, Errington J. Control of cell shape in bacteria: Helical, actin-like filaments in Bacillus subtilis. Cell 2001; 104:913–922.PubMedCrossRefGoogle Scholar
  33. 33.
    Pollard TD. Profilins. In: Kreis T, Vale R, eds. Guidebook to the Cytoskeletal and Motor Proteins. Oxford: Oxford University Press, 1999:117–120.Google Scholar
  34. 34.
    dos Remedios GC, Chhabra D, Kekic M et al. Actin binding proteins: Regulation of cytoskeletal microfilaments. Physiol Rev 2003; 83:433–473.PubMedGoogle Scholar
  35. 35.
    Rivero F, Eichinger L. The microfilament system of Dictysotelium discoideum. In: Loomis WF, Kuspa A, eds. Dictyostelium Genomics. Norfolk: Horizon Bioscience, 2005:125–171.Google Scholar
  36. 36.
    Koonin EV, Aravind L. Dynein light chains of the Roadblock/LC7 group belong to an ancient protein superfamily implicated in NTPase regulation. Curr Biol 2000; 10:R774–R776.PubMedCrossRefGoogle Scholar
  37. 37.
    Kurzbauer R, Teis D, de Araujo ME et al. Crystal structure of the pl4/MPl scaffolding complex: How a twin couple attaches mitogen-activated protein kinase signaling to late endosomes. Proc Natl Acad Sci USA 2004; 101:10984–10989.PubMedCrossRefGoogle Scholar
  38. 38.
    Maciver SK, Hussey P. The ADF/cofilin family: Actin-remodeling proteins. Genome Biol 2002; 3:R3007.CrossRefGoogle Scholar
  39. 39.
    Van Troys M, Vanderkerckhove J, Ampe C. Structural modules in actin-binding proteins: Towards a new clasification. Biochim Biophys Acta 1999; 1448:323–348.PubMedCrossRefGoogle Scholar
  40. 40.
    Hatanaka H, Ogura K, Moriyama K et al. Tertiary structure of destrin and structural similartity between two actin-regulating protein families. Cell 1996; 85:1047–1055.PubMedCrossRefGoogle Scholar
  41. 41.
    Kwiatkowski DJ. Functions of gelsolin: Motility, signaling, apoptosis, cancer. Curr Opin Cell Biol 1999; 11:103–108.PubMedCrossRefGoogle Scholar
  42. 42.
    Bi X, Corpina RA, Goldberg J. Structure of the Sec23/24-Sarl prebudding complex of the COPII vesicle coat. Nature 2002; 419:271–277.PubMedCrossRefGoogle Scholar
  43. 43.
    Higgs HN, Pollard TD. Regulation of actin filament network formation through Arp2/3 complex: Activation by a diverse array of proteins. Annu Rev Biochem 2001; 70:649–676.PubMedCrossRefGoogle Scholar
  44. 44.
    Machesky LM, Gould KL. The Arp2/3 complex: A multifunctional actin organizer. Curr Opin Cell Biol 1999; 11:117–121.PubMedCrossRefGoogle Scholar
  45. 45.
    Beltzner CC, Pollard TD. Identification of functionally important residues of Arp2/3 complex by analysis of homology models from diverse species. J Mol Biol 2004; 336:551–565.PubMedCrossRefGoogle Scholar
  46. 46.
    Mathur J. The ARP2/3 complex: Giving plant cells a leading edge. BioEssays 2005; 27:377–387.PubMedCrossRefGoogle Scholar
  47. 47.
    Giaever G, Chu AM, Ni L et al. Functional profiling of the Saccharomyces cerevisiae genome. Nature 2002; 418:387–391.PubMedCrossRefGoogle Scholar
  48. 48.
    Evangelista M, Pruyne D, Amberg DC et al. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nature Cell Biol 2002; 4:32–41.PubMedCrossRefGoogle Scholar
  49. 49.
    Li F, Higgs HN. The mouse formin mDial is a potent actin nucleation factor regulated by autoinhibition. Curr Biol 2003; 13:1335–1340.PubMedCrossRefGoogle Scholar
  50. 50.
    Kovar DR, Kuhn JR, Tichy AL et al. The fission yeast cytokinesis formin Cdcl2p is a barbed end actin filament capping protein gated by profilin. J Cell Biol 2003; 161:885–887.CrossRefGoogle Scholar
  51. 51.
    Otomo T, Tomchick DR, Otomo C et al. Structural basis of actin filament nucleation and processive capping by a formin homology 2 domain. Nature 2005; 433:488–494.PubMedCrossRefGoogle Scholar
  52. 52.
    Michelot A, Guerin C, Huang S et al. The Formin Homology 1 domain modulates the actin nucleation and bundling activity of Arabidopsis FORMIN1. Plant Cell 2005; 17:2296–2313.PubMedCrossRefGoogle Scholar
  53. 53.
    Cvrcková F, Novotny M, Pícková D et al. Formin homology 2 domains occur in multiple contexts in angiosperms. BMC Genomics 2004; 5:44.PubMedCrossRefGoogle Scholar
  54. 54.
    Rivero F, Muramoto T, Meyer A-K et al. A comparative sequence analysis reveals a common GBD/FH3-FH1-FH2-DAD architecture in formins from Dictyostelium, fungi and metazoa. BMC Genomics 2005; 6:28.PubMedCrossRefGoogle Scholar
  55. 55.
    Higgs HN, Peterson KJ. Phylogenetic analysis of the formin homology 2 domain. Mol Biol Cell 2005; 16:1–13.PubMedCrossRefGoogle Scholar
  56. 56.
    Simpson AG, Roger AJ. The real ‘kingdoms’ of eukaryotes. Curr Biol 2004; 14:R693–R696.PubMedCrossRefGoogle Scholar
  57. 57.
    Wear MA, Cooper JA. Capping protein: New insights into mechanism and regulation. Trends Biochem Sci 2004; 29:418–428.PubMedCrossRefGoogle Scholar
  58. 58.
    Korenbaum E, Rivero F. Calponin homology domains at a glance. J Cell Sci 2002; 115:3543–3545.PubMedCrossRefGoogle Scholar
  59. 59.
    Tirnauer JS, Bierer BE. EB1 proteins regulate microtubule dynamics, cell polarity, and chromosome stability. J Cell Biol 2000; 149:761–766.PubMedCrossRefGoogle Scholar
  60. 60.
    van der Leij FR, Huijkman NC, Boomsma C et al. Genomics of the human carnitine acyltransferase genes. Mol Genet Metab 2000; 71:139–153.PubMedCrossRefGoogle Scholar
  61. 61.
    Watanabe A, Yonemura I, Gonda K et al. Cloning and sequencing of the gene for a Tetrahymena fimbrin-like protein. J Biochem 2000; 127:85–94.PubMedGoogle Scholar
  62. 62.
    Mulder NJ, Apweiler R, Attwood TK et al. The InterPro Database, 2003 brings increased coverage and new features. Nucleic Acids Res 2003; 31:315–318.PubMedCrossRefGoogle Scholar
  63. 63.
    Vardar D, Chishti AH, Frank BS et al. Villin-type headpiece domains show a wide range of F-actin-binding affinities. Cell Motil Cytoskeleton 2002; 52:9–21.PubMedCrossRefGoogle Scholar
  64. 64.
    Hertzog M, van Heijenoort C, Didry D et al. The beta-thymosin/WH2 domain: Structural basis for the switch from inhibition to promotion of actin assembly. Cell 2004; 117:611–623.PubMedCrossRefGoogle Scholar
  65. 65.
    Quinlan ME, Heuser JE, Kerkhoff E et al. Drosophila Spire is an actin nucleation factor. Nature 2005; 433:382–388.PubMedCrossRefGoogle Scholar
  66. 66.
    Paunola E, Mattila PK, Lappalainen P. WH2 domain: A small versatile adapter for actin monomers. FEBS Lett 2002; 513:92–97.PubMedCrossRefGoogle Scholar
  67. 67.
    Ponting CP, Russell JB. Identification of distant homologues of fibroblast growth factors suggests a common ancestor for all beta-trefoil proteins. J Mol Biol 2000; 302:1041–1047.PubMedCrossRefGoogle Scholar
  68. 68.
    McCann RO, Craig SW. The I/LWEQ module: A conserved sequence that signifies F-actin binding in functionally diverse proteins from yeast to mammals. Proc Natl Acad Sci USA 1997; 94:5679–5684.PubMedCrossRefGoogle Scholar
  69. 69.
    Kull FJ, Sablin EP, Lau R et al. Crystal structure of the kinesin motor domain reveals a structural similarity to myosin. Nature 1996; 380:550–555.PubMedCrossRefGoogle Scholar
  70. 70.
    Kull FJ, Vale RD, Fletterick RJ. The case for a common ancestor: Kinesin and myosin motor proteins and G proteins. J Musc Res Cell Motil 1998; 19:877–886.CrossRefGoogle Scholar
  71. 71.
    Leipe DD, Wolf YI, Koonin EV et al. Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 2002; 317:41–72.PubMedCrossRefGoogle Scholar
  72. 72.
    Thompson RF, Langford GM. Myosin superfamily evolutionary history. Anat Rec 2002; 268:276–289.PubMedCrossRefGoogle Scholar
  73. 73.
    Hodge T, Cope MJ. A myosin family tree. J Cell Sci 2000; 113:3353–3354.PubMedGoogle Scholar
  74. 74.
    Richards TA, Cavalier-Smith T. Myosin domain evolution and the primary divergence of eukaryotes. Nature 2005; 436:1113–1118.PubMedCrossRefGoogle Scholar
  75. 75.
    Csete ME, Doyle JC. Reverse engineering of biological complexity. Science 2002; 295:1664–1668.PubMedCrossRefGoogle Scholar
  76. 76.
    Weaver AM, Young ME, Lee WL et al. Integration of signals to the Arp2/3 complex. Curr Opin Cell Biol 2003; 15:23–30.PubMedCrossRefGoogle Scholar
  77. 77.
    Deeks MJ, Hussey P, Davies B. Formins: Intermediates in signal transduction cascades that affect cytoskeletal reorganization. Trends Plant Sci 2002; 7:492–498.PubMedCrossRefGoogle Scholar
  78. 78.
    Johnson DI. Cdc42: An essential Rho-type GTPase controlling eukaryotic cell polarity. Microbiol Mol Biol Rev 1999; 63:54–105.PubMedGoogle Scholar
  79. 79.
    Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature 2002; 420:629–635.PubMedCrossRefGoogle Scholar
  80. 80.
    Sorokina EM, Chernoff J. Rho-GTPases: New members, new pathways. J Cell Biochem 2005; 94(2):225–231.PubMedCrossRefGoogle Scholar
  81. 81.
    Jekely G. Small GTPases and the evolution of the eukaryotic cell. BioEssays 2003; 25(11):1129–1138.PubMedCrossRefGoogle Scholar
  82. 82.
    Cotteret S, Chernoff J. The evolutionary history of effectors downstream of Cdc42 and Rac. Genome Biol 2002; 3:R0002.CrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2007

Authors and Affiliations

  1. 1.Center for Biochemistry and Center for Molecular Medicine Cologne, Medical FacultyUniversity of CologneKölnGermany
  2. 2.Department of Plant Physiology Faculty of SciencesCharles UniversityPragueCzechia

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