Role of the Parasite and Host Cytoskeleton in Apicomplexa Parasitism

Cell Host and Microbe

Volumn 5, Issue 6, 2009, Pages 602-611

  Frénal, Karine ^a   Soldati Favre, Dominique ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

CELLBIO; MICROBIO

Indexed keywords

ACTIN; TUBULIN;

APICOMPLEXA; CELL DIVISION; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL SURVIVAL; CRYPTOSPORIDIUM; CYTOSKELETON; ERYTHROCYTE MEMBRANE; HOST PARASITE INTERACTION; MICROBIAL DIVERSITY; MICROTUBULE; MOLECULAR MECHANICS; NONHUMAN; PARASITISM; PARASITOSIS; PLASMODIUM; PRIORITY JOURNAL; PROTEIN MODIFICATION; REVIEW;

ACTINS; ANIMALS; APICOMPLEXA; CYTOSKELETON; HOST-PARASITE INTERACTIONS; MODELS, BIOLOGICAL; TUBULIN;

APICOMPLEXA;

EID: 67649415132     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2009.05.013     Document Type: Review

References (93)

1. Allen M.L., Dobrowolski J.M., Muller H., Sibley L.D., and Mansour T.E. Cloning and characterization of actin depolymerizing factor from Toxoplasma gondii. Mol. Biochem. Parasitol. 88 (1997) 43-52
2. Barragan A., and Sibley L.D. Migration of Toxoplasma gondii across biological barriers. Trends Microbiol. 11 (2003) 426-430
3. Baum J., Papenfuss A.T., Baum B., Speed T.P., and Cowman A.F. Regulation of apicomplexan actin-based motility. Nat. Rev. Microbiol. 4 (2006) 621-628
4. Baum J., Tonkin C.J., Paul A.S., Rug M., Smith B.J., Gould S.B., Richard D., Pollard T.D., and Cowman A.F. A malaria parasite formin regulates actin polymerization and localizes to the parasite-erythrocyte moving junction during invasion. Cell Host Microbe 3 (2008) 188-198
5. Besteiro S., Michelin A., Poncet J., Dubremetz J.F., and Lebrun M. Export of a Toxoplasma gondii rhoptry neck protein complex at the host cell membrane to form the moving junction during invasion. PLoS Pathog. 5 (2009) e1000309
6. Bhavsar A.P., Guttman J.A., and Finlay B.B. Manipulation of host-cell pathways by bacterial pathogens. Nature 449 (2007) 827-834
7. Bishop R., Musoke A., Morzaria S., Gardner M., and Nene V. Theileria: intracellular protozoan parasites of wild and domestic ruminants transmitted by ixodid ticks. Parasitology 129 (2004) S271-S283
8. Black M.W., Arrizabalaga G., and Boothroyd J.C. Ionophore-resistant mutants of Toxoplasma gondii reveal host cell permeabilization as an early event in egress. Mol. Cell. Biol. 20 (2000) 9399-9408
9. Borowski H., Clode P.L., and Thompson R.C. Active invasion and/or encapsulation? A reappraisal of host-cell parasitism by Cryptosporidium. Trends Parasitol. 24 (2008) 509-516
10. Bradley P.J., Ward C., Cheng S.J., Alexander D.L., Coller S., Coombs G.H., Dunn J.D., Ferguson D.J., Sanderson S.J., Wastling J.M., and Boothroyd J.C. Proteomic analysis of rhoptry organelles reveals many novel constituents for host-parasite interactions in Toxoplasma gondii. J. Biol. Chem. 280 (2005) 34245-34258
11. Buscaglia C.A., Coppens I., Hol W.G., and Nussenzweig V. Sites of interaction between aldolase and thrombospondin-related anonymous protein in plasmodium. Mol. Biol. Cell 14 (2003) 4947-4957
12. Chandramohanadas R., Davis P.H., Beiting D.P., Harbut M.B., Darling C., Velmourougane G., Lee M.Y., Greer P.A., Roos D.S., and Greenbaum D.C. Apicomplexan parasites co-opt host calpains to facilitate their escape from infected cells. Science 324 (2009) 794-797
13. Chen X.M., Huang B.Q., Splinter P.L., Orth J.D., Billadeau D.D., McNiven M.A., and LaRusso N.F. Cdc42 and the actin-related protein/neural Wiskott-Aldrich syndrome protein network mediate cellular invasion by Cryptosporidium parvum. Infect. Immun. 72 (2004) 3011-3021
14. Chen X.M., Splinter P.L., Tietz P.S., Huang B.Q., Billadeau D.D., and LaRusso N.F. Phosphatidylinositol 3-kinase and frabin mediate Cryptosporidium parvum cellular invasion via activation of Cdc42. J. Biol. Chem. 279 (2004) 31671-31678
15. Chen X.M., O'Hara S.P., Huang B.Q., Splinter P.L., Nelson J.B., and LaRusso N.F. Localized glucose and water influx facilitates Cryptosporidium parvum cellular invasion by means of modulation of host-cell membrane protrusion. Proc. Natl. Acad. Sci. USA 102 (2005) 6338-6343
16. Cooke B.M., Mohandas N., and Coppel R.L. Malaria and the red blood cell membrane. Semin. Hematol. 41 (2004) 173-188
17. Coppens I., Dunn J.D., Romano J.D., Pypaert M., Zhang H., Boothroyd J.C., and Joiner K.A. Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell 125 (2006) 261-274
18. Courret N., Darche S., Sonigo P., Milon G., Buzoni-Gatel D., and Tardieux I. CD11c- and CD11b-expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood 107 (2006) 309-316
19. Cowman A.F., and Crabb B.S. Invasion of red blood cells by malaria parasites. Cell 124 (2006) 755-766
20. Crabb B.S., Cooke B.M., Reeder J.C., Waller R.F., Caruana S.R., Davern K.M., Wickham M.E., Brown G.V., Coppel R.L., and Cowman A.F. Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 89 (1997) 287-296
21. Delbac F., Sanger A., Neuhaus E.M., Stratmann R., Ajioka J.W., Toursel C., Herm-Götz A., Tomavo S., Soldati T., and Soldati D. Toxoplasma gondii myosins B/C: one gene, two tails, two localizations, and a role in parasite division. J. Cell Biol. 155 (2001) 613-623
22. Dobbelaere D.A., and Küenzi P. The strategies of the Theileria parasite: a new twist in host-pathogen interactions. Curr. Opin. Immunol. 16 (2004) 524-530
23. Dobrowolski J.M., and Sibley L.D. Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84 (1996) 933-939
24. Dobrowolski J.M., Carruthers V.B., and Sibley L.D. Participation of myosin in gliding motility and host cell invasion by Toxoplasma gondii. Mol. Microbiol. 26 (1997) 163-173
25. Dobrowolski J.M., Niesman I.R., and Sibley L.D. 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 (1997) 253-262
26. Dubey J.P. The history of Toxoplasma gondii-the first 100 years. J. Eukaryot. Microbiol. 55 (2008) 467-475
27. Elliott D.A., and Clark D.P. Cryptosporidium parvum induces host cell actin accumulation at the host-parasite interface. Infect. Immun. 68 (2000) 2315-2322
28. Elliott D.A., Coleman D.J., Lane M.A., May R.C., Machesky L.M., and Clark D.P. Cryptosporidium parvum infection requires host cell actin polymerization. Infect. Immun. 69 (2001) 5940-5942
29. Foth B.J., Goedecke M.C., and Soldati D. New insights into myosin evolution and classification. Proc. Natl. Acad. Sci. USA 103 (2006) 3681-3686
30. Gaskins E., Gilk S., DeVore N., Mann T., Ward G., and Beckers C. Identification of the membrane receptor of a class XIV myosin in Toxoplasma gondii. J. Cell Biol. 165 (2004) 383-393
31. Goldszmid R.S., Coppens I., Lev A., Caspar P., Mellman I., and Sher A. Host ER-parasitophorous vacuole interaction provides a route of entry for antigen cross-presentation in Toxoplasma gondii-infected dendritic cells. J. Exp. Med. 206 (2009) 399-410
32. Gonzalez V., Combe A., David V., Malmquist N.A., Delorme V., Leroy C., Blazquez S., Ménard R., and Tardieux I. Host cell entry by apicomplexa parasites requires actin polymerization in the host cell. Cell Host Microbe 5 (2009) 259-272
33. Gordon J.L., and Sibley L.D. Comparative genome analysis reveals a conserved family of actin-like proteins in apicomplexan parasites. BMC Genomics 6 (2005) 179
34. Gordon J.L., Beatty W.L., and Sibley L.D. A novel actin-related protein is associated with daughter cell formation in Toxoplasma gondii. Eukaryot. Cell 7 (2008) 1500-1512
35. Gould S.B., Tham W.H., Cowman A.F., McFadden G.I., and Waller R.F. Alveolins, a new family of cortical proteins that define the protist infrakingdom Alveolata. Mol. Biol. Evol. 25 (2008) 1219-1230
36. Gubbels M.J., Vaishnava S., Boot N., Dubremetz J.F., and Striepen B. A MORN-repeat protein is a dynamic component of the Toxoplasma gondii cell division apparatus. J. Cell Sci. 119 (2006) 2236-2245
37. Halonen S.K., and Weidner E. Overcoating of Toxoplasma parasitophorous vacuoles with host cell vimentin type intermediate filaments. J. Eukaryot. Microbiol. 41 (1994) 65-71
38. Hu K. Organizational changes of the daughter basal complex during the parasite replication of Toxoplasma gondii. PLoS Pathog. 4 (2008) e10
39. Hu K., Roos D.S., and Murray J.M. A novel polymer of tubulin forms the conoid of Toxoplasma gondii. J. Cell Biol. 156 (2002) 1039-1050
40. Hu K., Johnson J., Florens L., Fraunholz M., Suravajjala S., DiLullo C., Yates J., Roos D.S., and Murray J.M. Cytoskeletal components of an invasion machine-the apical complex of Toxoplasma gondii. PLoS Pathog. 2 (2006) e13
41. Jewett T.J., and Sibley L.D. Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in apicomplexan parasites. Mol. Cell 11 (2003) 885-894
42. Johnson T.M., Rajfur Z., Jacobson K., and Beckers C.J. Immobilization of the type XIV myosin complex in Toxoplasma gondii. Mol. Biol. Cell 18 (2007) 3039-3046
43. Kafsack B.F., Pena J.D., Coppens I., Ravindran S., Boothroyd J.C., and Carruthers V.B. Rapid membrane disruption by a perforin-like protein facilitates parasite exit from host cells. Science 323 (2009) 530-533
44. Kappe S.H., Buscaglia C.A., Bergman L.W., Coppens I., and Nussenzweig V. Apicomplexan gliding motility and host cell invasion: overhauling the motor model. Trends Parasitol. 20 (2004) 13-16
45. Keeley A., and Soldati D. The glideosome: a molecular machine powering motility and host-cell invasion by Apicomplexa. Trends Cell Biol. 14 (2004) 528-532
46. Khater E.I., Sinden R.E., and Dessens J.T. A malaria membrane skeletal protein is essential for normal morphogenesis, motility, and infectivity of sporozoites. J. Cell Biol. 167 (2004) 425-432
47. King C.A. Cell motility of sporozoan protozoa. Parasitol. Today 4 (1988) 315-319
48. Lambert H., Hitziger N., Dellacasa I., Svensson M., and Barragan A. Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination. Cell. Microbiol. 8 (2006) 1611-1623
49. Lambert H., Vutova P.P., Adams W.C., Lore K., and Barragan A. The Toxoplasma gondii-shuttling function of dendritic cells is linked to the parasite genotype. Infect. Immun. 77 (2009) 1679-1688
50. Lavine M.D., and Arrizabalaga G. Exit from host cells by the pathogenic parasite Toxoplasma gondii does not require motility. Eukaryot. Cell 7 (2008) 131-140
51. Magowan C., Coppel R.L., Lau A.O., Moronne M.M., Tchernia G., and Mohandas N. Role of the Plasmodium falciparum mature-parasite-infected erythrocyte surface antigen (MESA/PfEMP-2) in malarial infection of erythrocytes. Blood 86 (1995) 3196-3204
52. Mann T., Gaskins E., and Beckers C. Proteolytic processing of TgIMC1 during maturation of the membrane skeleton of Toxoplasma gondii. J. Biol. Chem. 277 (2002) 41240-41246
53. Martin A.M., Liu T., Lynn B.C., and Sinai A.P. The Toxoplasma gondii parasitophorous vacuole membrane: transactions across the border. J. Eukaryot. Microbiol. 54 (2007) 25-28
54. Matsubayashi M., Takase H., Kimata I., Nakagawa H., Tani H., Sasai K., and Baba E. Electron microscopic observation of cytoskeletal frame structures and detection of tubulin on the apical region of Cryptosporidium parvum sporozoites. Parasitology 135 (2008) 295-301
55. Meissner M., Schlüter D., and Soldati D. Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science 298 (2002) 837-840
56. Morrissette N.S., and Roos D.S. Toxoplasma gondii: a family of apical antigens associated with the cytoskeleton. Exp. Parasitol. 89 (1998) 296-303
57. Morrissette N.S., and Sibley L.D. Cytoskeleton of apicomplexan parasites. Microbiol. Mol. Biol. Rev. 66 (2002) 21-38
58. Morrissette N.S., and Sibley L.D. Disruption of microtubules uncouples budding and nuclear division in Toxoplasma gondii. J. Cell Sci. 115 (2002) 1017-1025
59. Morrissette N.S., Mitra A., Sept D., and Sibley L.D. Dinitroanilines bind alpha-tubulin to disrupt microtubules. Mol. Biol. Cell 15 (2004) 1960-1968
60. Moudy R., Manning T.J., and Beckers C.J. The loss of cytoplasmic potassium upon host cell breakdown triggers egress of Toxoplasma gondii. J. Biol. Chem. 276 (2001) 41492-41501
61. Nishi M., Hu K., Murray J.M., and Roos D.S. Organellar dynamics during the cell cycle of Toxoplasma gondii. J. Cell Sci. 121 (2008) 1559-1568
62. Pei X., Guo X., Coppel R., Bhattacharjee S., Haldar K., Gratzer W., Mohandas N., and An X. The ring-infected erythrocyte surface antigen (RESA) of Plasmodium falciparum stabilizes spectrin tetramers and suppresses further invasion. Blood 110 (2007) 1036-1042
63. Pei X., Guo X., Coppel R., Mohandas N., and An X. Plasmodium falciparum erythrocyte membrane protein 3 (PfEMP3) destabilizes erythrocyte membrane skeleton. J. Biol. Chem. 282 (2007) 26754-26758
64. Pinder J.C., Fowler R.E., Dluzewski A.R., Bannister L.H., Lavin F.M., Mitchell G.H., Wilson R.J., and Gratzer W.B. Actomyosin motor in the merozoite of the malaria parasite, Plasmodium falciparum: implications for red cell invasion. J. Cell Sci. 111 (1998) 1831-1839
65. Plattner F., Yarovinsky F., Romero S., Didry D., Carlier M.F., Sher A., and Soldati-Favre D. Toxoplasma profilin is essential for host cell invasion and TLR11-dependent induction of an interleukin-12 response. Cell Host Microbe 3 (2008) 77-87
66. Pomel S., Luk F.C., and Beckers C.J. Host cell egress and invasion induce marked relocations of glycolytic enzymes in Toxoplasma gondii tachyzoites. PLoS Pathog. 4 (2008) e1000188
67. Poupel O., and Tardieux I. Toxoplasma gondii motility and host cell invasiveness are drastically impaired by jasplakinolide, a cyclic peptide stabilizing F-actin. Microbes Infect. 1 (1999) 653-662
68. Poupel O., Boleti H., Axisa S., Couture-Tosi E., and Tardieux I. Toxofilin, a novel actin-binding protein from Toxoplasma gondii, sequesters actin monomers and caps actin filaments. Mol. Biol. Cell 11 (2000) 355-368
69. Radtke K., Döhner K., and Sodeik B. Viral interactions with the cytoskeleton: a hitchhiker's guide to the cell. Cell. Microbiol. 8 (2006) 387-400
70. Russell D.G., and Sinden R.E. The role of the cytoskeleton in the motility of coccidian sporozoites. J. Cell Sci. 50 (1981) 345-359
71. Sahoo N., Beatty W., Heuser J., Sept D., and Sibley L.D. Unusual kinetic and structural properties control rapid assembly and turnover of actin in the parasite Toxoplasma gondii. Mol. Biol. Cell 17 (2006) 895-906
72. Sanders P.R., Cantin G.T., Greenbaum D.C., Gilson P.R., Nebl T., Moritz R.L., Yates III J.R., Hodder A.N., and Crabb B.S. Identification of protein complexes in detergent-resistant membranes of Plasmodium falciparum schizonts. Mol. Biochem. Parasitol. 154 (2007) 148-157
73. Schmitz S., Grainger M., Howell S., Calder L.J., Gaeb M., Pinder J.C., Holder A.A., and Veigel C. Malaria parasite actin filaments are very short. J. Mol. Biol. 349 (2005) 113-125
74. Schneider I., Haller D., Kullmann B., Beyer D., Ahmed J.S., and Seitzer U. Identification, molecular characterization and subcellular localization of a Theileria annulata parasite protein secreted into the host cell cytoplasm. Parasitol. Res. 101 (2007) 1471-1482
75. Schüler H., and Matuschewski K. Regulation of apicomplexan microfilament dynamics by a minimal set of actin-binding proteins. Traffic 7 (2006) 1433-1439
76. Schüler H., Mueller A.K., and Matuschewski K. A Plasmodium actin-depolymerizing factor that binds exclusively to actin monomers. Mol. Biol. Cell 16 (2005) 4013-4023
77. Schüler H., Mueller A.K., and Matuschewski K. Unusual properties of Plasmodium falciparum actin: new insights into microfilament dynamics of apicomplexan parasites. FEBS Lett. 579 (2005) 655-660
78. Shaw M.K. Cell invasion by Theileria sporozoites. Trends Parasitol. 19 (2003) 2-6
79. Shaw M.K., and Tilney L.G. Induction of an acrosomal process in Toxoplasma gondii: visualization of actin filaments in a protozoan parasite. Proc. Natl. Acad. Sci. USA 96 (1999) 9095-9099
80. Shaw M.K., Compton H.L., Roos D.S., and Tilney L.G. Microtubules, but not actin filaments, drive daughter cell budding and cell division in Toxoplasma gondii. J. Cell Sci. 113 (2000) 1241-1254
81. Siden-Kiamos I., Pinder J.C., and Louis C. Involvement of actin and myosins in Plasmodium berghei ookinete motility. Mol. Biochem. Parasitol. 150 (2006) 308-317
82. Silva M.D., Cooke B.M., Guillotte M., Buckingham D.W., Sauzet J.P., Le Scanf C., Contamin H., David P., Mercereau-Puijalon O., and Bonnefoy S. A role for the Plasmodium falciparum RESA protein in resistance against heat shock demonstrated using gene disruption. Mol. Microbiol. 56 (2005) 990-1003
83. Soldati D., Foth B.J., and Cowman A.F. Molecular and functional aspects of parasite invasion. Trends Parasitol. 20 (2004) 567-574
84. Starnes G.L., Coincon M., Sygusch J., and Sibley L.D. Aldolase is essential for energy production and bridging adhesin-actin cytoskeletal interactions during parasite invasion of host cells. Cell Host Microbe 5 (2009) 353-364
85. Thompson R.C., Olson M.E., Zhu G., Enomoto S., Abrahamsen M.S., and Hijjawi N.S. Cryptosporidium and cryptosporidiosis. Adv. Parasitol. 59 (2005) 77-158
86. Tremp A.Z., Khater E.I., and Dessens J.T. IMC1b is a putative membrane skeleton protein involved in cell shape, mechanical strength, motility, and infectivity of malaria ookinetes. J. Biol. Chem. 283 (2008) 27604-27611
87. van Ooij C., Tamez P., Bhattacharjee S., Hiller N.L., Harrison T., Liolios K., Kooij T., Ramesar J., Balu B., Adams J., et al. The malaria secretome: from algorithms to essential function in blood stage infection. PLoS Pathog. 4 (2008) e1000084
88. Vanderberg J.P. Studies on the motility of Plasmodium sporozoites. J. Protozool. 21 (1974) 527-537
89. Vaughan A.M., Aly A.S., and Kappe S.H. Malaria parasite pre-erythrocytic stage infection: gliding and hiding. Cell Host Microbe 4 (2008) 209-218
90. Walker M.E., Hjort E.E., Smith S.S., Tripathi A., Hornick J.E., Hinchcliffe E.H., Archer W., and Hager K.M. Toxoplasma gondii actively remodels the microtubule network in host cells. Microbes Infect. 10 (2008) 1440-1449
91. Waller K.L., Nunomura W., An X., Cooke B.M., Mohandas N., and Coppel R.L. Mature parasite-infected erythrocyte surface antigen (MESA) of Plasmodium falciparum binds to the 30-kDa domain of protein 4.1 in malaria-infected red blood cells. Blood 102 (2003) 1911-1914
92. Wetzel D.M., Hakansson S., Hu K., Roos D., and Sibley L.D. Actin filament polymerization regulates gliding motility by apicomplexan parasites. Mol. Biol. Cell 14 (2003) 396-406
93. Wetzel D.M., Schmidt J., Kuhlenschmidt M.S., Dubey J.P., and Sibley L.D. Gliding motility leads to active cellular invasion by Cryptosporidium parvum sporozoites. Infect. Immun. 73 (2005) 5379-5387