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Myosin B of Plasmodium falciparum (PfMyoB): in silico prediction of its three-dimensional structure and its possible interaction with MTIP

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Abstract

The mobility and invasion strategy of Plasmodium falciparum is governed by a protein complex known as the glideosome, which contains an actin-myosin motor. It has been shown that myosin A of the parasite (PfMyoA) is the myosin of the glideosome, and the interaction of PfMyoA with myosin tail domain interacting protein (MTIP) determines its correct location and its ability to function in the complex. Because PfMyoA and myosin B of P. falciparum (PfMyoB) share high sequence identity, are both small proteins without a tail domain, belong to the class XIV myosins, and are expressed in late schizonts and merozoites, we suspect that these myosins may have similar or redundant functions. Therefore, this work examined the structural similarity between PfMyoA and PfMyoB and performed a molecular docking between PfMyoB and MTIP. Three-dimensional (3D) models obtained for PfMyoA and PfMyoB achieved high scores in the structural validation programs used, and their superimposition revealed high structural similarity, supporting the hypothesis of possible similar functions for these two proteins. The 3D interaction models obtained and energy values found suggested that interaction between PfMyoB and MTIP is possible. Given the apparent abundance of PfMyoA relative to PfMyoB in the parasite, we believe that the interaction between PfMyoB and MTIP would only be detectable in specific cellular environments because under normal circumstances, it would be masked by the interaction between PfMyoA and MTIP.

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References

  • Andenmatten N, Egarter S, Jackson AJ, Jullien N, Herman JP et al (2013) Conditional genome engineering in Toxoplasma gondii uncovers alternative invasion mechanisms. Nat Methods 10(2):125–127

    Article  CAS  PubMed  Google Scholar 

  • Andrusier N, Nussinov R, Wolfson HJ (2007) FireDock: fast interaction refinement in molecular docking. Proteins 69(1):139–159

    Article  CAS  PubMed  Google Scholar 

  • Bassen DM, Hou Y, Bowser SS, Banavali NK (2016) Maintenance of electrostatic stabilization in altered tubulin lateral contacts may facilitate formation of helical filaments in foraminifera. Sci Rep 6:31723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergeron B (2003) Bioinformatics computing. Prentice Hall, New Jersey

    Google Scholar 

  • Bergman LW, Kaiser K, Fujioka H, Coppens I, Daly TM et al (2003) Myosin A tail domain interacting protein (MTIP) localizes to the inner membrane complex of Plasmodium sporozoites. J Cell Sci 116:39–49

    Article  CAS  PubMed  Google Scholar 

  • Bird JE, Takagi Y, Billington N, Strub MP, Sellers JR et al (2014) Chaperone-enhanced purification of unconventional myosin 15, a molecular motor specialized for stereocilia protein trafficking. Proc Natl Acad Sci U S A 111(34):12390–12395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bosch J, Turley S, Daly TM, Bogh SM, Villasmil ML et al (2006) Structure of the MTIP-MyoA complex, a key component of the malaria parasite invasion motor. Proc Natl Acad Sci U S A 103:4852–4857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bosch J, Turley S, Roach CM, Daly TM, Bergman LW et al (2007) The closed MTIP-myosin A-tail complex from the malaria parasite invasion machinery. J Mol Biol 372:77–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaparro-Olaya J, Dluzewski AR, Margos G, Wasserman MM, Mitchell GH et al (2003) The multiple myosins of malaria: the smallest malaria myosin, Plasmodium falciparum myosin-B (Pfmyo-B) is expressed in mature schizonts and merozoites. Europ J Protistol 39:423–427

    Article  Google Scholar 

  • Chaparro-Olaya J, Margos G, Coles DJ, Dluzewski AR, Mitchell GH et al (2005) Plasmodium falciparum myosins: transcription and translation during asexual parasite development. Cell Motil Cytoskeleton 60(4):200–213

    Article  CAS  PubMed  Google Scholar 

  • Colovos C, Yeates TO (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci 2(9):1511–1519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crawley SW, Liburd J, Shaw K, Jung Y, Smith SP, Côté GP (2011) Identification of calmodulin and MlcC as light chains for Dictyostelium myosin-I isozymes. Biochemistry 50(30):6579–6588

    Article  CAS  PubMed  Google Scholar 

  • Dobrowolski JM, Sibley LD (1996) Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84:933–939

    Article  CAS  PubMed  Google Scholar 

  • Dobrowolski JM, Carruthers VB, Sibley LD (1997) Participation of myosin in gliding motility and host cell invasion by Toxoplasma gondii. Mol Microbiol 26(1):163–173

    Article  CAS  PubMed  Google Scholar 

  • Douse CH, Green JL, Salgado PS, Simpson PJ, Thomas JC et al (2012) Regulation of the Plasmodium motor complex: phosphorylation of myosin A tail-interacting protein (MTIP) loosens its grip on MyoA. J Bioll Chem 287(44):36968–36977

    Article  CAS  Google Scholar 

  • Douse CH, Vrielink N, Wenlin Z, Cota E, Tate EW (2015) Targeting a dynamic protein–protein interaction: fragment screening against the malaria myosin A motor complex. ChemMedChem 10(1):134–143

    Article  CAS  PubMed  Google Scholar 

  • Farrow RE, Green J, Katsimitsoulia Z, Taylor WR, Holder AA et al (2011) The mechanism of erythrocyte invasion by the malarial parasite, Plasmodium falciparum. Semin Cell Dev Biol 22(9):953–960

    Article  CAS  PubMed  Google Scholar 

  • Foth BJ, Goedecke MC, Soldati D (2006) New insights into myosin evolution and classification. Proc Natl Acad Sci U S A 103(10):3681–3686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frénal K, Marq JB, Jacot D, Polonais V, Soldati-Favre D (2014) Plasticity between MyoC-and MyoA-glideosomes: an example of functional compensation in Toxoplasma gondii invasion. PLoS Pathog 10(11):e1004504

    Article  PubMed  PubMed Central  Google Scholar 

  • Gan HH, Perlow RA, Roy S, Ko J, Wu M et al (2002) Analysis of protein sequence/structure similarity relationships. Biophys J 83(5):2781–2791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green JL, Martin SR, Fielden J, Ksagoni A, Grainger M et al (2006) The MTIP–myosin A complex in blood stage malaria parasites. J Mol Biol 355:933–941

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Heissler SM, Sellers JR (2014) Myosin light chains: teaching old dogs new tricks. BioArchitecture 4(6):169–188

    Article  PubMed  Google Scholar 

  • Herm-Götz A, Delbac F, Weiss S, Nyitrai M, Stratmann R et al (2006) Functional and biophysical analyses of the class XIV Toxoplasma gondii myosin D. J Muscle Res Cell Motil 27(2):139–151

    Article  PubMed  Google Scholar 

  • Hettmann C, Herm A, Geiter A, Frank B, Schwarz E 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):1385–1400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones DT (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292:195–202

    Article  CAS  PubMed  Google Scholar 

  • Khamrui S, Turley S, Pardon E, Steyaert J, Fan E et al (2013) The structure of the D3 domain of Plasmodium falciparum myosin tail interacting protein MTIP in complex with a nanobody. Mol Biochem Parasitol 190(2):87–91

    Article  CAS  PubMed  Google Scholar 

  • Koch M, Baum J (2016) The mechanics of malaria parasite invasion of the human erythrocyte—towards a reassessment of the host cell contribution. Cell Microbiol 18(3):319–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krieger E, Vriend G (2014) YASARA view—molecular graphics for all devices—from smartphones to workstations. Bioinformatics 30(20):2981–2982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK—a program to check the stereochemical quality of protein structures. J App Cryst 26:283–291

    Article  CAS  Google Scholar 

  • Luo J, Vallen EA, Dravis C, Tcheperegine SE, Drees B et al (2004) Identification and functional analysis of the essential and regulatory light chains of the only type II myosin Myo1p in Saccharomyces cerevisiae. J Cell Biol 165(6):843–855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meissner M, Schlüter D, Soldati D (2002) Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science 298(5594):837–840

    Article  CAS  PubMed  Google Scholar 

  • Mermall V, Post PL, Mooseker MS (1998) Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 279(5350):527–533

    Article  CAS  PubMed  Google Scholar 

  • Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK et al (2009) Autodock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem 16:2785–2791

    Article  Google Scholar 

  • Nebl T, Prieto JH, Kapp E, Smith BJ, Williams MJ et al (2011) Quantitative in vivo analyses reveal calcium-dependent phosphorylation sites and identifies a novel component of the Toxoplasma invasion motor complex. PLoS Pathog 7(9):e1002222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okumura T, Sasamura T, Inatomi M, Hozumi S, Nakamura M et al (2015) Class I myosins have overlapping and specialized functions in left-right asymmetric development in Drosophila. Genetics 199(4):1183–1199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM et al (2004) UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605–1612

    Article  CAS  PubMed  Google Scholar 

  • Pinder JC, Fowler RE, Dluzewski AR, Bannister LH, Lavin FM et al (1998) Actomyosin motor in the merozoite of the malaria parasite, Plasmodium falciparum: implications for red cell invasion. J Cell Sci 111(13):1831–1839

    CAS  PubMed  Google Scholar 

  • Prokhnevsky AI, Peremyslov VV, Dolja VV (2008) Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc Natl Acad Sci U S A 105(50):19744–19749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rhoads AR, Friedberg F (1997) Sequence motifs for calmodulin recognition. FASEB J 11:331–340

    CAS  PubMed  Google Scholar 

  • Richards TA, Cavalier-Smith T (2005) Myosin domain evolution and the primary divergence of eukaryotes. Nature 436(7054):1113–1118

    Article  CAS  PubMed  Google Scholar 

  • Schneidman-Duhovny D, Inbar Y, Nussinov R, Wolfson HJ (2005) PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res 33:W363–W367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwarz EC, Geissler H, Soldati T (1999) A potentially exhaustive screening strategy reveals two novel divergent myosins in Dictyostelium. Cell Biochem Biophys 30(3):413–435

    Article  CAS  PubMed  Google Scholar 

  • Sebé-Pedrós A, Grau-Bové X, Richards TA, Ruiz-Trillo I (2014) Evolution and classification of myosins, a paneukaryotic whole-genome approach. Genome Biol Evol 6(2):290–305

    Article  PubMed  PubMed Central  Google Scholar 

  • Sievers F, Higgins DG (2014) Clustal omega. Curr Protoc Bioinformatics 48:3.13.16

    Google Scholar 

  • Soldati T, Geissler H, Schwarz EC (1999) How many is enough? Exploring the myosin repertoire in the model eukaryote Dictyostelium discoideum. Cell Biochem Biophys 30(3):389–411

    Article  CAS  PubMed  Google Scholar 

  • Tan I, Yong J, Dong JM, Lim L, Leung T (2008) A tripartite complex containing MRCK modulates lamellar actomyosin retrograde flow. Cell 135(1):123–136

    Article  CAS  PubMed  Google Scholar 

  • Thomas JC, Green JL, Howson RI, Simpson P, Moss DK et al (2010) Interaction and dynamics of the Plasmodium falciparum MTIP–MyoA complex, a key component of the invasion motor in the malaria parasite. Mol BioSyst 6:494–498

    Article  CAS  PubMed  Google Scholar 

  • Venit T, Dzijak R, Kalendová A, Kahle M, Rohožková J et al (2013) Mouse nuclear myosin I knock-out shows interchangeability and redundancy of myosin isoforms in the cell nucleus. PLoS One 8(4):e61406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webb SE, Fowler RE, O’Shaughnessy C, Pinder JC, Dluzewski AR et al (1996) Contractile protein system in the asexual stages of the malaria parasite Plasmodium falciparum. Parasitology 112(5):451–457

    Article  CAS  PubMed  Google Scholar 

  • WHO (2015) World malaria report 2015. http://www.who.int/malaria/publications/world-malaria-report-2015/report/en/. Accessed 16 December 1996

  • Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res 35:W407–W410

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson CA, Kreychman J, Gerstein M (2000) Assessing annotation transfer for genomics: quantifying the relations between protein sequence, structure and function through traditional and probabilistic scores. J Mol Biol 297(1):233–249

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Yan R, Roy A, Xu D, Poisson J et al (2015) The I-TASSER Suite: protein structure and function prediction. Nat Methods 12(1):7–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yusuf NA, Green JL, Wall RJ, Knuepfer E, Moon RW et al (2015) The Plasmodium class XIV myosin, MyoB, has a distinct subcellular location in invasive and motile stages of the malaria parasite and an unusual light chain. J Biol Chem 290(19):12147–12164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by COLCIENCIAS (projects 110152128729 and 130834319109) and Universidad El Bosque (projects UB-271-2010 and PCI-2011-264). Funding organizations had no role in study design, data analysis, decision to publish, or preparation of the manuscript.

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  1. Instituto de Biología Molecular, Laboratorio de Parasitología Molecular, Vicerrectoría de Investigaciones, Universidad El Bosque, Edificio D. Segundo piso. Avenida Cra. 9 No. 131 A–02, Bogotá, Colombia

    Paula C. Hernández, Liliana Morales, Isabel C Castellanos & Jacqueline Chaparro-Olaya

  2. Laboratorio de Investigaciones Básicas en Bioquímica-LIBBIQ, Departamento de Química-Facultad de Ciencias, Universidad Nacional de Colombia, Bogotá, Colombia

    Moisés Wasserman

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  1. Paula C. Hernández
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Correspondence to Jacqueline Chaparro-Olaya.

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Hernández, P.C., Morales, L., Castellanos, I.C. et al. Myosin B of Plasmodium falciparum (PfMyoB): in silico prediction of its three-dimensional structure and its possible interaction with MTIP. Parasitol Res 116, 1373–1382 (2017). https://doi.org/10.1007/s00436-017-5417-y

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