Crossref journal-article
Rockefeller University Press
Journal of Cell Biology (291)
Abstract

The capacity to migrate is fundamental to multicellular and single-celled life. Apicomplexan parasites, an ancient protozoan clade that includes malaria parasites (Plasmodium) and Toxoplasma, achieve remarkable speeds of directional cell movement. This rapidity is achieved via a divergent actomyosin motor system, housed within a narrow compartment that lies underneath the length of the parasite plasma membrane. How this motor functions at a mechanistic level during motility and host cell invasion is a matter of debate. Here, we integrate old and new insights toward refining the current model for the function of this motor with the aim of revitalizing interest in the mechanics of how these deadly pathogens move.

Bibliography

Tardieux, I., & Baum, J. (2016). Reassessing the mechanics of parasite motility and host-cell invasion. Journal of Cell Biology, 214(5), 507–515.

Authors 2
  1. Isabelle Tardieux (first)
  2. Jake Baum (additional)
References 108 Referenced 71
  1. {'key': '2023072310112206400_bib1', 'first-page': '285', 'article-title': 'Transmission and scanning electron microscopy of host cell entry by Toxoplasma gondii', 'volume': '87', 'author': 'Aikawa', 'year': '1977', 'journal-title': 'Am. J. Pathol.'} / Am. J. Pathol. / Transmission and scanning electron microscopy of host cell entry by Toxoplasma gondii by Aikawa (1977)
  2. 10.1083/jcb.77.1.72 / J. Cell Biol. / Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite by Aikawa (1978)
  3. 10.1371/journal.ppat.0010017 / PLoS Pathog. / Identification of the moving junction complex of Toxoplasma gondii: A collaboration between distinct secretory organelles by Alexander (2005)
  4. 10.1038/nm1350 / Nat. Med. / Quantitative imaging of Plasmodium transmission from mosquito to mammal by Amino (2006)
  5. 10.1038/nmeth.2301 / Nat. Methods. / Conditional genome engineering in Toxoplasma gondii uncovers alternative invasion mechanisms by Andenmatten (2013)
  6. 10.1371/journal.pone.0032188 / PLoS One. / Spatial localisation of actin filaments across developmental stages of the malaria parasite by Angrisano (2012)
  7. 10.1371/journal.pone.0035227 / PLoS One. / Gliding motility of Babesia bovis merozoites visualized by time-lapse video microscopy by Asada (2012)
  8. 10.1371/journal.ppat.1005710 / PLoS Pathog. / The actin filament-binding protein coronin regulates motility in Plasmodium sporozoites by Bane (2016)
  9. 10.1017/S0031182000047247 / Parasitology. / Structure and invasive behaviour of Plasmodium knowlesi merozoites in vitro by Bannister (1975)
  10. 10.1038/ncomms3552 / Nat. Commun. / Apical membrane antigen 1 mediates apicomplexan parasite attachment but is dispensable for host cell invasion by Bargieri (2013)
  11. 10.1371/journal.ppat.1004273 / PLoS Pathog. / Host cell invasion by apicomplexan parasites: The junction conundrum by Bargieri (2014)
  12. 10.1103/PhysRevE.90.042720 / Phys. Rev. E Stat. Nonlin. Soft Matter Phys. / Geometrical model for malaria parasite migration in structured environments by Battista (2014)
  13. 10.1126/science.1209875 / Science. / Biochemistry. Revealing a parasite’s invasive trick by Baum (2011)
  14. 10.1074/jbc.M509807200 / J. Biol. Chem. / A conserved molecular motor drives cell invasion and gliding motility across malaria life cycle stages and other apicomplexan parasites by Baum (2006)
  15. 10.1186/s12915-014-0108-y / BMC Biol. / The toxoplasma-host cell junction is anchored to the cell cortex to sustain parasite invasive force by Bichet (2014)
  16. 10.1038/nrmicro1800 / Nat. Rev. Microbiol. / Kiss and spit: The dual roles of Toxoplasma rhoptries by Boothroyd (2008)
  17. 10.1016/j.jsb.2015.02.008 / J. Struct. Biol. / The apicomplexan glideosome and adhesins - Structures and function by Boucher (2015)
  18. 10.1016/j.mib.2007.09.013 / Curr. Opin. Microbiol. / Rhoptries: An arsenal of secreted virulence factors by Bradley (2007)
  19. 10.1016/S0166-6851(00)00280-2 / Mol. Biochem. Parasitol. / Induction of secretion and surface capping of microneme proteins in Eimeria tenella by Bumstead (2000)
  20. 10.1091/mbc.E03-06-0355 / Mol. Biol. Cell. / Sites of interaction between aldolase and thrombospondin-related anonymous protein in plasmodium by Buscaglia (2003)
  21. 10.1007/978-0-387-78267-6_2 / Subcell. Biochem. / Microneme proteins in apicomplexans by Carruthers (2008)
  22. 10.1126/science.1257998 / Science. / Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution by Chen (2014)
  23. 10.1016/j.ceb.2016.03.007 / Curr. Opin. Cell Biol. / Role of the ER and Golgi in protein export by Apicomplexa by Coffey (2016)
  24. 10.1016/j.pt.2013.03.003 / Trends Parasitol. / Plasmodium rhoptry proteins: Why order is important by Counihan (2013)
  25. 10.1083/jcb.201206112 / J. Cell Biol. / The cellular and molecular basis for malaria parasite invasion of the human red blood cell by Cowman (2012)
  26. {'key': '2023072310112206400_bib26', 'first-page': '4', 'article-title': 'The progressive movement of gregarines', 'volume': '54', 'author': 'Crawley', 'year': '1902', 'journal-title': 'Proc Natl Acad Sci Philadelphia.'} / Proc Natl Acad Sci Philadelphia. / The progressive movement of gregarines by Crawley (1902)
  27. 10.1016/j.bpj.2014.07.010 / Biophys. J. / Quantitation of malaria parasite-erythrocyte cell-cell interactions using optical tweezers by Crick (2014)
  28. 10.1111/cmi.12498 / Cell. Microbiol. / The aspartyl protease TgASP5 mediates the export of the Toxoplasma GRA16 and GRA24 effectors into host cells by Curt-Varesano (2016)
  29. 10.1084/jem.20062405 / J. Exp. Med. / Cryoelectron tomography reveals periodic material at the inner side of subpellicular microtubules in apicomplexan parasites by Cyrklaff (2007)
  30. 10.1016/j.mib.2009.06.008 / Curr. Opin. Microbiol. / Mechanisms controlling glideosome function in apicomplexans by Daher (2009)
  31. 10.1016/j.bpj.2014.05.024 / Biophys. J. / Membrane-wrapping contributions to malaria parasite invasion of the human erythrocyte by Dasgupta (2014)
  32. 10.1126/science.1162912 / Science. / Stretching single talin rod molecules activates vinculin binding by del Rio (2009)
  33. 10.1016/S0092-8674(00)81071-5 / Cell. / Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite by Dobrowolski (1996)
  34. 10.1128/mBio.00557-15 / MBio. / Toxoplasma actin is required for efficient host cell invasion by Drewry (2015)
  35. 10.1126/science.803712 / Science. / Invasion of erythrocytes by malaria merozoites by Dvorak (1975)
  36. 10.1371/journal.pone.0091819 / PLoS One / The toxoplasma Acto-MyoA motor complex is important but not essential for gliding motility and host cell invasion by Egarter (2014)
  37. 10.1038/368113a0 / Nature. / Single myosin molecule mechanics: Piconewton forces and nanometre steps by Finer (1994)
  38. 10.1016/j.chom.2010.09.002 / Cell Host Microbe. / Functional dissection of the apicomplexan glideosome molecular architecture by Frénal (2010)
  39. {'key': '2023072310112206400_bib39', 'first-page': '201', 'article-title': 'Shape, movement in situ and locomotion of plasmodial ookinetes', 'volume': '23', 'author': 'Freyvogel', 'year': '1966', 'journal-title': 'Acta Trop.'} / Acta Trop. / Shape, movement in situ and locomotion of plasmodial ookinetes by Freyvogel (1966)
  40. 10.1002/(SICI)1097-0169(1996)34:2<152::AID-CM6>3.0.CO;2-D / Cell Motil. Cytoskeleton. / Kinematic analysis of Toxoplasma gondii motility by Frixione (1996)
  41. 10.1083/jcb.200311137 / J. Cell Biol. / Identification of the membrane receptor of a class XIV myosin in Toxoplasma gondii by Gaskins (2004)
  42. 10.1016/j.chom.2009.01.011 / Cell Host Microbe. / Host cell entry by apicomplexa parasites requires actin polymerization in the host cell by Gonzalez (2009)
  43. 10.1093/molbev/msq321 / Mol. Biol. Evol. / Ciliate pellicular proteome identifies novel protein families with characteristic repeat motifs that are common to alveolates by Gould (2011)
  44. 10.1016/j.ijpara.2012.09.009 / Int. J. Parasitol. / Evolution of apicomplexan secretory organelles by Gubbels (2012)
  45. 10.1091/mbc.10.11.3539 / Mol. Biol. Cell. / Time-lapse video microscopy of gliding motility in Toxoplasma gondii reveals a novel, biphasic mechanism of cell locomotion by Håkansson (1999)
  46. 10.1111/cmi.12132 / Cell. Microbiol. / Electron tomography of Plasmodium falciparum merozoites reveals core cellular events that underpin erythrocyte invasion by Hanssen (2013)
  47. 10.1128/mBio.01111-13 / MBio. / Shear forces enhance Toxoplasma gondii tachyzoite motility on vascular endothelium by Harker (2014)
  48. 10.1016/j.semcdb.2015.09.020 / Semin. Cell Dev. Biol. / Gliding motility in apicomplexan parasites by Heintzelman (2015)
  49. {'key': '2023072310112206400_bib49', 'first-page': '81', 'article-title': 'A cinematographic study of the penetration of cultured cells by Toxoplasma gondii', 'volume': '14', 'author': 'Hirai', 'year': '1966', 'journal-title': 'Jpn. J. Vet. Res.'} / Jpn. J. Vet. Res. / A cinematographic study of the penetration of cultured cells by Toxoplasma gondii by Hirai (1966)
  50. 10.7554/eLife.07789 / eLife. / Longitudinal analysis of Plasmodium sporozoite motility in the dermis reveals component of blood vessel recognition by Hopp (2015)
  51. 10.1016/S1097-2765(03)00113-8 / Mol. Cell. / Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in apicomplexan parasites by Jewett (2003)
  52. 10.1016/j.molbiopara.2006.01.009 / Mol. Biochem. Parasitol. / Plasmodium falciparum erythrocyte invasion: A conserved myosin associated complex by Jones (2006)
  53. 10.1111/cmi.12283 / Cell. Microbiol. / Quantitative analysis of Plasmodium ookinete motion in three dimensions suggests a critical role for cell shape in the biomechanics of malaria parasite gliding motility by Kan (2014)
  54. 10.1074/mcp.M116.058263 / Mol. Cell. Proteomics. / Proteomic analysis of the Plasmodium berghei gametocyte egressome and vesicular bioID of osmiophilic body proteins identifies MTRAP as an essential factor for parasite transmission by Kehrer (2016)
  55. 10.1016/0169-4758(88)90113-5 / Parasitol. Today (Regul. Ed.). / Cell motility of sporozoan protozoa by King (1988)
  56. 10.1111/cmi.12557 / Cell. Microbiol. / The mechanics of malaria parasite invasion of the human erythrocyte—towards a reassessment of the host cell contribution by Koch (2016)
  57. 10.1371/journal.ppat.1003213 / PLoS Pathog. / An overexpression screen of Toxoplasma gondii Rab-GTPases reveals distinct transport routes to the micronemes by Kremer (2013)
  58. 10.1186/1757-5036-3-6 / PMC Biophys. / Geometric constrains for detecting short actin filaments by cryogenic electron tomography by Kudryashev (2010)
  59. 10.1111/j.1462-5822.2012.01836.x / Cell. Microbiol. / Structural basis for chirality and directional motility of Plasmodium sporozoites by Kudryashev (2012)
  60. 10.2307/3277308 / J. Parasitol. / Penetration of erythrocytes by merozoites of mammalian and avian malarial parasites by Ladda (1969)
  61. 10.1038/ncomms5098 / Nat. Commun. / Plasticity and redundancy among AMA-RON pairs ensure host cell entry of Toxoplasma parasites by Lamarque (2014)
  62. 10.1371/journal.pone.0085763 / PLoS One. / Disruption of TgPHIL1 alters specific parameters of Toxoplasma gondii motility measured in a quantitative, three-dimensional live motility assay by Leung (2014)
  63. 10.1126/science.aab3500 / Science. / Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics by Li (2015)
  64. 10.1126/science.aad8857 / Science. / Visualizing the molecular sociology at the HeLa cell nuclear periphery by Mahamid (2016)
  65. 10.1038/nature14044 / Nature. / Theileria parasites secrete a prolyl isomerase to maintain host leukocyte transformation by Marsolier (2015)
  66. 10.1016/j.mib.2013.05.002 / Curr. Opin. Microbiol. / Invasion factors of apicomplexan parasites: Essential or redundant? by Meissner (2013)
  67. 10.1084/jem.149.1.172 / J. Exp. Med. / Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation by Miller (1979)
  68. 10.1242/jcs.108.6.2457 / J. Cell Sci. / Invasion of Toxoplasma gondii occurs by active penetration of the host cell by Morisaki (1995)
  69. 10.1128/MMBR.66.1.21-38.2002 / Microbiol. Mol. Biol. Rev. / Cytoskeleton of apicomplexan parasites by Morrissette (2002)
  70. 10.1016/j.chom.2009.11.007 / Cell Host Microbe. / Plasmodium sporozoite motility is modulated by the turnover of discrete adhesion sites by Münter (2009)
  71. 10.1371/journal.ppat.1002222 / PLoS Pathog. / Quantitative in vivo analyses reveal calcium-dependent phosphorylation sites and identifies a novel component of the Toxoplasma invasion motor complex by Nebl (2011)
  72. 10.1007/BF00927970 / Z. Parasitenkd. / Modes of entry of Toxoplasma gondii trophozoites into normal mouse peritoneal macrophage and HeLa cell monolayers. A phase-contrast microcinematographic study by Nguyen (1979)
  73. 10.1186/s12936-015-0801-5 / Malar. J. / Plasmodium falciparum coronin organizes arrays of parallel actin filaments potentially guiding directional motility in invasive malaria parasites by Olshina (2015)
  74. 10.1046/j.1365-2958.2002.03056.x / Mol. Microbiol. / ‘The glideosome’: A dynamic complex powering gliding motion and host cell invasion by Toxoplasma gondii by Opitz (2002)
  75. 10.1242/jcs.111.13.1831 / J. Cell Sci. / Actomyosin motor in the merozoite of the malaria parasite, Plasmodium falciparum: Implications for red cell invasion by Pinder (1998)
  76. 10.1021/acsnano.5b06417 / ACS Nano. / Coupling of retrograde flow to force production during malaria parasite migration by Quadt (2016)
  77. 10.1006/jsbi.2001.4396 / J. Struct. Biol. / Cryofracture electron microscopy of the ookinete pellicle of Plasmodium gallinaceum reveals the existence of novel pores in the alveolar membranes by Raibaud (2001)
  78. 10.1016/j.chom.2010.12.003 / Cell Host Microbe. / Super-resolution dissection of coordinated events during malaria parasite invasion of the human erythrocyte by Riglar (2011)
  79. 10.1242/jcs.177741 / J. Cell Sci. / Localisation-based imaging of malarial antigens during erythrocyte entry reaffirms a role for AMA1 but not MTRAP in invasion by Riglar (2016)
  80. 10.1242/jcs.50.1.345 / J. Cell Sci. / The role of the cytoskeleton in the motility of coccidian sporozoites by Russell (1981)
  81. 10.1016/0020-7519(82)90020-0 / Int. J. Parasitol. / Three-dimensional study of the intact cytoskeleton of coccidian sporozoites by Russell (1982)
  82. 10.1128/iai.20.3.739-743.1978 / Infect. Immun. / Effect of cytochalasin D on Toxoplasma gondii cell entry by Ryning (1978)
  83. 10.1091/mbc.E05-06-0512 / Mol. Biol. Cell. / Unusual kinetic and structural properties control rapid assembly and turnover of actin in the parasite Toxoplasma gondii by Sahoo (2006)
  84. {'key': '2023072310112206400_bib84', 'first-page': '340', 'article-title': 'Uber die Ursache der Fortschreitenden Bewegungder Gregarinen', 'volume': '58', 'author': 'Schewiakoff', 'year': '1894', 'journal-title': 'Z. Wiss. Zool.'} / Z. Wiss. Zool. / Uber die Ursache der Fortschreitenden Bewegungder Gregarinen by Schewiakoff (1894)
  85. 10.1016/j.jmb.2005.03.056 / J. Mol. Biol. / Malaria parasite actin filaments are very short by Schmitz (2005)
  86. 10.1016/S1471-4922(02)00015-6 / Trends Parasitol. / Cell invasion by Theileria sporozoites by Shaw (2003)
  87. 10.1073/pnas.1315156111 / Proc. Natl. Acad. Sci. USA. / Toxoplasma aldolase is required for metabolism but dispensable for host-cell invasion by Shen (2014)
  88. 10.1126/science.1094717 / Science. / Intracellular parasite invasion strategies by Sibley (2004)
  89. 10.1371/journal.ppat.1002280 / PLoS Pathog. / Evolutionarily divergent, unstable filamentous actin is essential for gliding motility in apicomplexan parasites by Skillman (2011)
  90. 10.1371/journal.ppat.1002280 / PLoS Pathog. / Evolutionarily divergent, unstable filamentous actin is essential for gliding motility in apicomplexan parasites by Skillman (2011)
  91. 10.1038/ncomms3285 / Nat. Commun. / The unusual dynamics of parasite actin result from isodesmic polymerization by Skillman (2013)
  92. 10.1016/j.pt.2004.09.009 / Trends Parasitol. / Molecular and functional aspects of parasite invasion by Soldati (2004)
  93. 10.2307/3281974 / J. Parasitol. / Capping of immune complexes by sporozoites of Eimeria tenella by Speer (1985)
  94. 10.1073/pnas.1110303108 / Proc. Natl. Acad. Sci. USA. / Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion by Srinivasan (2011)
  95. 10.1111/j.1550-7408.1988.tb04115.x / J. Protozool. / Malaria sporozoites leave behind trails of circumsporozoite protein during gliding motility by Stewart (1988)
  96. 10.4269/ajtmh.1986.35.37 / Am. J. Trop. Med. Hyg. / Rhoptry secretion of membranous whorls by Plasmodium falciparum merozoites by Stewart (1986)
  97. 10.1038/ncb3350 / Nat. Cell Biol. / The molecular clutch model for mechanotransduction evolves by Swaminathan (2016)
  98. 10.2471/BLT.12.111732 / Bull. World Health Organ. / The global burden of congenital toxoplasmosis: A systematic review by Torgerson (2013)
  99. 10.1111/j.1550-7408.1974.tb03693.x / J. Protozool. / Studies on the motility of Plasmodium sporozoites by Vanderberg (1974)
  100. 10.1111/j.1462-5822.2004.00394.x / Cell. Microbiol. / Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion by Vlachou (2004)
  101. 10.1371/journal.ppat.1004670 / PLoS Pathog. / Revealing the sequence and resulting cellular morphology of receptor-ligand interactions during Plasmodium falciparum invasion of erythrocytes by Weiss (2015)
  102. 10.1016/0166-6851(88)90107-7 / Mol. Biochem. Parasitol. / Extremely diverged actin proteins in Plasmodium falciparum by Wesseling (1988)
  103. 10.1091/mbc.E02-08-0458 / Mol. Biol. Cell. / Actin filament polymerization regulates gliding motility by apicomplexan parasites by Wetzel (2003)
  104. 10.1016/S0140-6736(13)60024-0 / Lancet. / Malaria by White (2014)
  105. 10.7554/eLife.06974 / eLife. / Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites by Woo (2015)
  106. 10.1016/j.cell.2007.10.049 / Cell. / Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes by Yeoh (2007)
  107. 10.1371/journal.pone.0046160 / PLoS One. / Subcompartmentalisation of proteins in the rhoptries correlates with ordered events of erythrocyte invasion by the blood stage malaria parasite by Zuccala (2012)
  108. 10.1038/srep19766 / Sci. Rep. / Quantitative phospho-proteomics reveals the Plasmodium merozoite triggers pre-invasion host kinase modification of the red cell cytoskeleton by Zuccala (2016)
Dates
Type When
Created 9 years ago (Aug. 29, 2016, 9:18 a.m.)
Deposited 2 years, 1 month ago (July 23, 2023, 6:11 a.m.)
Indexed 3 weeks, 3 days ago (Aug. 6, 2025, 9:47 a.m.)
Issued 9 years ago (Aug. 29, 2016)
Published 9 years ago (Aug. 29, 2016)
Published Online 9 years ago (Aug. 29, 2016)
Published Print 9 years ago (Aug. 29, 2016)
Funders 3
  1. Wellcome Trust 10.13039/100004440 Wellcome
    Awards1
    1. 100993/Z/13/Z
  2. Fondation pour la Recherche Médicale 10.13039/501100002915

    Region: Europe

    pri (Trusts, charities, foundations (both public and private))

    Labels2
    1. Foundation for Medical Research
    2. FRM
    Awards1
    1. FRM-DEQ20100318279
  3. Fondation Innovations en Infectiologie 10.13039/100008656

    Region: Europe

    pri (Trusts, charities, foundations (both public and private))

    Labels4
    1. FINOVI Foundation
    2. Fondation Finovi
    3. Innovations in Infectiology Foundation
    4. Finovi

@article{Tardieux_2016, title={Reassessing the mechanics of parasite motility and host-cell invasion}, volume={214}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.201605100}, DOI={10.1083/jcb.201605100}, number={5}, journal={Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Tardieux, Isabelle and Baum, Jake}, year={2016}, month=aug, pages={507–515} }