Skip to main content

Myosin Class XIV And Other Myosins In Protists

  • Chapter
Myosins

Part of the book series: Proteins and Cell Regulation ((PROR,volume 7))

Abstract

Myosins are actin-based molecular motors that convert chemical energy released by ATP hydrolysis into directed movement along tracks of actin filaments. They are found in eukaryotes and are implicated in a number of important cell functions, such as nuclear and cell division, transport of molecules, vesicles, and organelles, signal transduction, and motility. The myosin superfamily was previously described as containing at least 18 different classes with class XIV reported to be specific to apicomplexan parasites and subdivided into two subclasses. But a recent reassessment of myosin phylogeny and classification incorporating a number of novel sequences uncovered by several genome sequencing initiatives has expanded the known repertoire of myosin heavy chains from apicomplexans and other protists. It established six new myosin classes, three of which are restricted to alveolates (XXII, XXIII, XXIV), and showed that class XIV encompasses myosins of both apicomplexans and ciliates and is subdivided into four subclasses. Moreover, several sequences include protein domains (ATS1-like, WD40) previously unknown to be associated with myosin motors. In this chapter, we discuss the current classification of myosin heavy chains with particular emphasis on the apicomplexan myosins. Most of them have not yet been studied experimentally and we discuss their possible function based on their classification and their protein domains.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abrahamsen, M.S. et al. (2004). Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science, 304(5669), 441–5.

    Article  PubMed  CAS  Google Scholar 

  • Adl, S.M. et al. (2005). The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol, 52(5), 399–451.

    Article  PubMed  Google Scholar 

  • Barragan, A. and Sibley, L.D. (2003). Migration of Toxoplasma gondii across biological barriers. Trends Microbiol., 11(9), 426–30.

    Article  PubMed  CAS  Google Scholar 

  • Baum, J., Papenfuss, A.T., Baum, B., Speed, T.P. and Cowman, A.F. (2006a). Regulation of apicomplexan actin-based motility. Nat Rev Microbiol 4(8), 621–8.

    Article  CAS  Google Scholar 

  • Baum, J. et al. (2006b). A conserved molecular motor drives cell invasion and gliding motility across malaria life cycle stages and other apicomplexan parasites. J Biol Chem 281(8), 5197–208.

    Article  CAS  Google Scholar 

  • Berg, J.S., Powell, B.C. and Cheney, R.E. (2001). A millennial myosin census. Mol Biol Cell 12(4), 780–94.

    PubMed  CAS  Google Scholar 

  • Bergman, L.W. et al. (2003). Myosin A tail domain interacting protein (MTIP) localizes to the inner membrane complex of Plasmodium sporozoites. J Cell Sci 116(Pt 1), 39–49.

    Google Scholar 

  • Bhattacharya, D., Yoon, H.S. and Hackett, J.D. (2004). Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays, 26(1), 50–60.

    Article  PubMed  Google Scholar 

  • Bosch, J. et al. (2006). Structure of the MTIP–MyoA complex, a key component of the malaria parasite invasion motor. Proc Natl Acad Sci USA 103(13), 4852–7.

    Article  PubMed  CAS  Google Scholar 

  • Buscaglia, C.A., Coppens, I., Hol, W.G. and Nussenzweig, V. (2003). Sites of interaction between aldolase and thrombospondin-related anonymous protein in plasmodium. Mol Biol Cell, 14(12), 4947–57.

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith, T. (2000). Membrane heredity and early chloroplast evolution. Trends Plant Sci 5(4), 174–82.

    Article  PubMed  CAS  Google Scholar 

  • Chaparro-Olaya, J. et al. (2005). Plasmodium falciparum myosins: transcription and translation during asexual parasite development. Cell Motil Cytoskeleton 60(4), 200–13.

    Google Scholar 

  • Chen, Z.Y. et al. (1996). Molecular cloning and domain structure of human myosin-VIIa, the gene product defective in Usher syndrome 1B. Genomics 36(3), 440–8.

    Article  PubMed  CAS  Google Scholar 

  • Chen, Z.Y. et al. (2001). Myosin-VIIb, a novel unconventional myosin, is a constituent of microvilli in transporting epithelia. Genomics 72(3), 285–96.

    Article  PubMed  CAS  Google Scholar 

  • Chishti, A.H. et al. (1998). The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem Sci 23(8), 281–2.

    Article  PubMed  CAS  Google Scholar 

  • Dawson, S.C. and Pace, N.R. (2002). Novel kingdom-level eukaryotic diversity in anoxic environments. Proc Natl Acad Sci USA 99(12), 8324–9.

    Article  PubMed  CAS  Google Scholar 

  • Delbac, F. et al. (2001). Toxoplasma gondii myosins B/C: one gene, two tails, two localizations, and a role in parasite division. J Cell Biol 155(4), 613–23.

    Article  PubMed  CAS  Google Scholar 

  • Dobrowolski, J. and Sibley, L.D. (1997). The role of the cytoskeleton in host cell invasion by Toxoplasma gondii. Behring Inst Mitt 99, 90–6.

    PubMed  Google Scholar 

  • Dobrowolski, J.M., Niesman, I.R. and Sibley, L.D. (1997). Actin in the parasite Toxoplasma gondii is encoded by a single copy gene, ACT1 and exists primarily in a globular form. Cell Motil Cytoskeleton 37(3), 253–62.

    Article  PubMed  CAS  Google Scholar 

  • Dobrowolski, J.M. and Sibley, L.D. (1996). Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84(6), 933–9.

    Article  PubMed  CAS  Google Scholar 

  • Eisen, J.A. et al. (2006). Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol 4(9), e286.

    Google Scholar 

  • El-Sayed, N.M. et al. (2005). The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309(5733), 409–15.

    Article  PubMed  CAS  Google Scholar 

  • Endo, T., Yagita, K., Yasuda, T. and Nakamura, T. (1988). Detection and localization of actin in Toxoplasma gondii. Parasitol Res 75(2), 102–6.

    Article  PubMed  CAS  Google Scholar 

  • Forney, J.R., Vaughan, D.K., Yang, S. and Healey, M.C. (1998). Actin-dependent motility in Cryptosporidium parvum sporozoites. J Parasitol 84(5), 908–13.

    Article  PubMed  CAS  Google Scholar 

  • Foth, B.J., Goedecke, M.C. and Soldati, D. (2006). New insights into myosin evolution and classification. Proc Natl Acad Sci USA 103(10), 3681–6.

    Article  PubMed  CAS  Google Scholar 

  • Fowler, R.E., Margos, G. and Mitchell, G.H. (2004). The cytoskeleton and motility in apicomplexan invasion. Adv Parasitol 56, 213–63.

    Article  PubMed  Google Scholar 

  • Gardner, M.J. et al. (2002). Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419(6906), 498–511.

    Google Scholar 

  • Gaskins, E. et al. (2004). Identification of the membrane receptor of a class XIV myosin in Toxoplasma gondii. J Cell Biol 165(3), 383–93.

    Article  PubMed  CAS  Google Scholar 

  • Goodson, H.V. and Dawson, S.C. (2006). Multiplying myosins. Proc Natl Acad Sci USA 103(10), 3498–9.

    Article  PubMed  CAS  Google Scholar 

  • Green, J.L. et al. (2006). The MTIP–myosin A complex in blood stage malaria parasites. J Mol Biol 355(5), 933–41.

    Article  PubMed  CAS  Google Scholar 

  • Gubbels, M.J., Vaishnava, S., Boot, N., Dubremetz, J.F. and Striepen, B. (2006). A MORN-repeat protein is a dynamic component of the Toxoplasma gondii cell division apparatus. J Cell Sci 119(Pt 11), 2236–45.

    Article  PubMed  CAS  Google Scholar 

  • Hakansson, S., Morisaki, H., Heuser, J. and Sibley, L.D. (1999). Time-lapse video microscopy of gliding motility in Toxoplasma gondii reveals a novel, biphasic mechanism of cell locomotion. Mol Biol Cell 10(11), 3539–47.

    PubMed  CAS  Google Scholar 

  • Harper, J.T., Waanders, E. and Keeling, P.J. (2005). On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. Int J Syst Evol Microbiol 55(Pt 1), 487–96.

    Google Scholar 

  • Heintzelman, M.B. (2004). Actin and myosin in Gregarina polymorpha. Cell Motil Cytoskeleton 58(2), 83–95.

    Article  PubMed  CAS  Google Scholar 

  • Heintzelman, M.B. and Schwartzman, J.D. (1997). A novel class of unconventional myosins from Toxoplasma gondii. J Mol Biol 271(1), 139–46.

    Article  PubMed  CAS  Google Scholar 

  • Heintzelman, M.B. and Schwartzman, J.D. (1999). Characterization of myosin-A and myosin-C: two class XIV unconventional myosins from Toxoplasma gondii. Cell Motil Cytoskeleton 44(1), 58–67.

    Article  PubMed  CAS  Google Scholar 

  • Heintzelman, M.B. and Schwartzman, J.D. (2001). Myosin diversity in Apicomplexa. J Parasitol 87(2), 429–32.

    PubMed  CAS  Google Scholar 

  • Herm-Gotz, A. et al. (2006). Functional and biophysical analyses of the class XIV Toxoplasma gondii Myosin D. J Muscle Res Cell Motil 27(2), 139–51.

    Article  PubMed  CAS  Google Scholar 

  • Herm-Gotz, A. et al. (2002). Toxoplasma gondii myosin A and its light chain: a fast, single-headed, plus-end-directed motor. Embo J 21(9), 2149–58.

    Article  PubMed  CAS  Google Scholar 

  • Hettmann, C. et al. (2000). A dibasic motif in the tail of a class XIV apicomplexan myosin is an essential determinant of plasma membrane localization. Mol Biol Cell 11(4), 1385–400.

    PubMed  CAS  Google Scholar 

  • Hosein, R.E., Williams, S.A. and Gavin, R.H. (2005). Directed motility of phagosomes in Tetrahymena thermophila requires actin and Myo1p, a novel unconventional myosin. Cell Motil Cytoskeleton 61(1), 49–60.

    Article  PubMed  CAS  Google Scholar 

  • Hu, K. et al. (2006). Cytoskeletal components of an invasion machine-the apical complex of Toxoplasma gondii. PLoS Pathog 2(2), e13.

    Google Scholar 

  • Hutchins, J.R. et al. (2004). Phosphorylation regulates the dynamic interaction of RCC1 with chromosomes during mitosis. Curr Biol 14(12), 1099–104.

    Article  PubMed  CAS  Google Scholar 

  • Jewett, T.J. and Sibley, L.D. (2003). Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in apicomplexan parasites. Mol Cell 11(4), 885–94.

    Article  PubMed  CAS  Google Scholar 

  • Jones, M.L., Kitson, E.L. and Rayner, J.C. (2006). Plasmodium falciparum erythrocyte invasion: a conserved myosin associated complex. Mol Biochem Parasitol 147(1), 74–84.

    Article  PubMed  CAS  Google Scholar 

  • Kappe, S.H., Buscaglia, C.A., Bergman, L.W., Coppens, I. and Nussenzweig, V. (2004). Apicomplexan gliding motility and host cell invasion: overhauling the motor model. Trends Parasitol 20(1), 13–6.

    Article  PubMed  CAS  Google Scholar 

  • Keeley, A. and Soldati, D. (2004). The glideosome: a molecular machine powering motility and host-cell invasion by Apicomplexa. Trends Cell Biol 14(10), 528–32.

    Article  PubMed  CAS  Google Scholar 

  • Keeling, P.J. et al. (2005). The tree of eukaryotes. Trends Ecol Evol 20(12), 670–6.

    Article  PubMed  Google Scholar 

  • King, C.A. (1981). Cell surface interaction of the protozoan Gregarina with concanavalin A beads - implications for models of gregarine gliding. Cell Biol Int Rep 5(3), 297–305.

    Article  PubMed  CAS  Google Scholar 

  • King, C.A. (1988). Cell motility of sporozoan protozoa. Parasitol Today 4(11), 315–9.

    Article  PubMed  CAS  Google Scholar 

  • Kirkpatrick, D. and Solomon, F. (1994). Overexpression of yeast homologs of the mammalian checkpoint gene RCC1 suppresses the class of alpha-tubulin mutations that arrest with excess microtubules. Genetics 137(2), 381–92.

    PubMed  CAS  Google Scholar 

  • Krendel, M., Osterweil, E.K. and Mooseker, M.S. (2007). Myosin 1E interacts with synaptojanin-1 and dynamin and is involved in endocytosis. FEBS Lett 581(4), 644–50.

    Article  PubMed  CAS  Google Scholar 

  • Le Roch, K.G. et al. (2004). Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Res 14(11), 2308–18.

    Google Scholar 

  • Le Roch, K.G. et al. (2003). Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301(5639), 1503–8.

    Google Scholar 

  • Lew, A.E., Dluzewski, A.R., Johnson, A.M. and Pinder, J.C. (2002). Myosins of Babesia bovis: molecular characterisation, erythrocyte invasion, and phylogeny. Cell Motil Cytoskeleton 52(4), 202–20.

    Article  PubMed  CAS  Google Scholar 

  • Matuschewski, K., Mota, M.M., Pinder, J.C., Nussenzweig, V. and Kappe, S.H. (2001). Identification of the class XIV myosins Pb-MyoA and Py-MyoA and expression in Plasmodium sporozoites. Mol Biochem Parasitol 112(1), 157–61.

    Article  PubMed  CAS  Google Scholar 

  • Meissner, M., Schluter, D. and Soldati, D. (2002). Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science 298(5594), 837–40.

    Google Scholar 

  • Morrissette, N.S. and Sibley, L.D. (2002). Cytoskeleton of apicomplexan parasites. Microbiol Mol Biol Rev 66(1), 21–38; table of contents.

    Google Scholar 

  • Morton, C.J. and Campbell, I.D. (1994). SH3 domains. Molecular ’Velcro’. Curr Biol 4(7), 615–7.

    CAS  Google Scholar 

  • Oliver, T.N., Berg, J.S. and Cheney, R.E. (1999). Tails of unconventional myosins. Cell Mol Life Sci 56(3–4), 243–57.

    Google Scholar 

  • Opitz, C. and Soldati, D. (2002). ‘The glideosome’: a dynamic complex powering gliding motion and host cell invasion by Toxoplasma gondii. Mol Microbiol 45(3), 597–604.

    Google Scholar 

  • Pain, A. et al. (2005). Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. Science 309(5731), 131–3.

    Google Scholar 

  • Poupel, O. and Tardieux, I. (1999). Toxoplasma gondii motility and host cell invasiveness are drastically impaired by jasplakinolide, a cyclic peptide stabilizing F-actin. Microbes Infect 1(9), 653–62.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Russell, D.G. and Sinden, R.E. (1981). The role of the cytoskeleton in the motility of coccidian sporozoites. J Cell Sci 50, 345–59.

    PubMed  CAS  Google Scholar 

  • Sahoo, N., Beatty, W., Heuser, J., Sept, D. and Sibley, L.D. (2006). Unusual kinetic and structural properties control rapid assembly and turnover of actin in the parasite Toxoplasma gondii. Mol Biol Cell 17(2), 895–906.

    Article  PubMed  CAS  Google Scholar 

  • Schmitz, S. et al. (2005). Malaria parasite actin filaments are very short. J Mol Biol 349(1), 113–25.

    Article  PubMed  CAS  Google Scholar 

  • Schuler, H., Mueller, A.K. and Matuschewski, K. (2005). Unusual properties of Plasmodium falciparum actin: new insights into microfilament dynamics of apicomplexan parasites. FEBS Lett 579(3), 655–60.

    Article  PubMed  CAS  Google Scholar 

  • Schwartzman, J.D. and Pfefferkorn, E.R. (1983). Immunofluorescent localization of myosin at the anterior pole of the coccidian, Toxoplasma gondii. J Protozool 30(4), 657–61.

    PubMed  CAS  Google Scholar 

  • Sellers, J.R. (2000). Myosins: a diverse superfamily. Biochim Biophys Acta 1496(1), 3–22.

    Article  PubMed  CAS  Google Scholar 

  • Shaw, M.K. and Tilney, L.G. (1999). Induction of an acrosomal process in Toxoplasma gondii: visualization of actin filaments in a protozoan parasite. Proc Natl Acad Sci USA 96(16), 9095–9.

    Article  PubMed  CAS  Google Scholar 

  • Shields, C.M. et al. (2003). Saccharomyces cerevisiae Ats1p interacts with Nap1p, a cytoplasmic protein that controls bud morphogenesis. Curr Genet 44(4), 184–94.

    Article  PubMed  CAS  Google Scholar 

  • Siden-Kiamos, I., Pinder, J.C. and Louis, C. (2006). Involvement of actin and myosins in Plasmodium berghei ookinete motility. Mol Biochem Parasitol 150(2), 308–17.

    Article  PubMed  CAS  Google Scholar 

  • Smith, J.J., Yakisich, J.S., Kapler, G.M., Cole, E.S. and Romero, D.P., (2004). A beta-tubulin mutation selectively uncouples nuclear division and cytokinesis in Tetrahymena thermophila. Eukaryot Cell 3(5), 1217–26.

    Article  PubMed  CAS  Google Scholar 

  • Smith, T.F., Gaitatzes, C., Saxena, K. and Neer, E.J. (1999). The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24(5), 181–5.

    Article  PubMed  CAS  Google Scholar 

  • Soldati, D., Foth, B.J. and Cowman, A.F. (2004). Molecular and functional aspects of parasite invasion. Trends Parasitol 20(12), 567–74.

    Article  PubMed  CAS  Google Scholar 

  • Soldati, D. and Meissner, M. (2004). Toxoplasma as a novel system for motility. Curr Opin Cell Biol 16(1), 32–40.

    Google Scholar 

  • Terrak, M., Wu, G., Stafford, W.F., Lu, R.C. and Dominguez, R. (2003). Two distinct myosin light chain structures are induced by specific variations within the bound IQ motifs-functional implications. Embo J 22(3), 362–71.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, R.F. and Langford, G.M. (2002). Myosin superfamily evolutionary history. Anat Rec 268(3), 276–89.

    Article  PubMed  CAS  Google Scholar 

  • Vale, R.D. (2003). The molecular motor toolbox for intracellular transport. Cell 112(4), 467–80.

    Article  PubMed  CAS  Google Scholar 

  • van Nocker, S. and Ludwig, P. (2003). The WD-repeat protein superfamily in Arabidopsis: conservation and divergence in structure and function. BMC Genomics 4(1), 50.

    Google Scholar 

  • Wall, M.A. et al. (1995). The structure of the G protein heterotrimer Gi alpha 1 beta 1 gamma 2. Cell 83(6), 1047–58.

    Article  PubMed  CAS  Google Scholar 

  • Weber, K.L., Sokac, A.M., Berg, J.S., Cheney, R.E. and Bement, W.M. (2004). A microtubule-binding myosin required for nuclear anchoring and spindle assembly. Nature, 431(7006): 325–9.

    Google Scholar 

  • Wetzel, D.M., Hakansson, S., Hu, K., Roos, D. and Sibley, L.D. (2003). Actin filament polymerization regulates gliding motility by apicomplexan parasites. Mol Biol Cell 14(2), 396–406.

    Article  PubMed  CAS  Google Scholar 

  • Wetzel, D.M., Schmidt, J., Kuhlenschmidt, M.S., Dubey, J.P. and Sibley, L.D. (2005). Gliding motility leads to active cellular invasion by Cryptosporidium parvum sporozoites. Infect Immun 73(9), 5379–87.

    Article  PubMed  CAS  Google Scholar 

  • Williams, S.A. and Gavin, R.H. (2005). Myosin genes in Tetrahymena. Cell Motil Cytoskeleton 61(4), 237–43.

    Article  PubMed  CAS  Google Scholar 

  • Williams, S.A., Hosein, R.E., Garces, J.A. and Gavin, R.H. (2000). MYO1, a novel, unconventional myosin gene affects endocytosis and macronuclear elongation in Tetrahymena thermophila. J Eukaryot Microbiol 47(6), 561–8.

    Article  PubMed  CAS  Google Scholar 

  • Yasuda, T., Yagita, K., Nakamura, T. and Endo, T. (1988). Immunocytochemical localization of actin in Toxoplasma gondii. Parasitol Res 75(2), 107–13.

    Article  PubMed  CAS  Google Scholar 

  • Yoon, H.S., Hackett, J.D., Pinto, G. and Bhattacharya, D. (2002). The single, ancient origin of chromist plastids. Proc Natl Acad Sci USA 99(24), 15507–12.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, C., Goldberg, M.W., Moore, W.J., Allen, T.D. and Clarke, P.R. (2002). Concentration of Ran on chromatin induces decondensation, nuclear envelope formation and nuclear pore complex assembly. Eur J Cell Biol 81(11), 623–33.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer

About this chapter

Cite this chapter

FrÉnal, K., Foth, B.J., Soldati, D. (2008). Myosin Class XIV And Other Myosins In Protists. In: Myosins. Proteins and Cell Regulation, vol 7. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6519-4_15

Download citation

Publish with us

Policies and ethics