Regulation of apicomplexan actin-based motility

Nature Reviews Microbiology

Volumn 4, Issue 8, 2006, Pages 621-628

  Baum, Jake ^a   Papenfuss, Anthony T ^a   Baum, Buzz ^b   Speed, Terence P ^a   Cowman, Alan F ^a  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; ACTIN DEPOLYMERIZING FACTOR; ACTIN RELATED PROTEIN; ACTININ; CALPONIN; COFILIN; CYCLASE ASSOCIATED PROTEIN; CYTOSKELETON PROTEIN; F ACTIN; FASCIN; GELSOLIN; KHELLIN; MYOSIN; PROFILIN; REGULATOR PROTEIN; TALIN; THYMOSIN; TROPOMYOSIN; TROPONIN; UNCLASSIFIED DRUG; MOLECULAR MOTOR; PROTOZOAL PROTEIN;

ACTIN FILAMENT; ACTIN MYOSIN INTERACTION; ACTIN POLYMERIZATION; APICOMPLEXA; ARTICLE; CELL INVASION; CELL MOTILITY; CYTOSKELETON; DRUG TARGETING; GENE EXPRESSION; GENOME; HOST CELL; HOST PARASITE INTERACTION; INFECTION PREVENTION; LOCOMOTION; MICROBIAL METABOLISM; MICROBIAL MORPHOLOGY; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTOZOAL GENETICS; PROTOZOAL INFECTION; SIGNAL TRANSDUCTION; ANIMAL; CELL MOTION; GENE; PHYSIOLOGY; REVIEW;

ANIMALIA; APICOMPLEXA; PROTOZOA;

ACTINS; ANIMALS; APICOMPLEXA; CELL MOVEMENT; GENES, PROTOZOAN; MOLECULAR MOTOR PROTEINS; PROTOZOAN PROTEINS;

EID: 33747189218     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro1465     Document Type: Article

References (82)

1. Pollard, T. D. & Borisy, G. G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465 (2003).
2. Stevens, J. M., Galyov, E. E. & Stevens, M. P. Actin-dependent movement of bacterial pathogens. Nature Rev. Microbiol. 4, 91-101 (2006).
3. Morrissette, N. S. & Sibley, L. D. Cytoskeleton of apicomplexan parasites. Microbiol. Mol. Biol. Rev. 66, 21-38 (2002).
4. Soldati, D. & Meissner, M. Toxoplasma as a novel system for motility. Curr. Opin. Cell. Biol. 16, 32-40 (2004).
5. King, C. A. Cell motility of sporozoan protozoa. Parasitol. Today 4, 315-319 (1988).
6. Blackman, M. J. & Bannister, L. H. Apical organelles of Apicomplexa: biology and isolation by subcellular fractionation. Mol. Biochem. Parasitol. 117, 11-25 (2001).
7. Cowman, A. F. & Crabb, B. S. Invasion of human red blood cells by malaria parasites. Cell 124, 755-766 (2006).
8. Carruthers, V. B. & Sibley, L. D. Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur. J. Cell Biol. 73, 114-123 (1997).
9. Alexander, D. L., Mital, J., Ward, G. E., Bradley, P. & Boothroyd, J. C. Identification of the moving junction complex of Toxoplasma gondii: A collaboration between distinct secretory organelles. PLoS Pathog. 1, e 17 (2005).
10. Kappe, S. et al. Conservation of a gliding motility and cell invasion machinery in apicomplexan parasites. J. Cell Biol. 147, 937-944 (1999).
11. Baum, J. et al. A conserved molecular motor drives cell invasion and gliding motility across malaria lifecycle stages and other apicomplexan parasites. J. Biol. Chem. 281, 5197-5208 (2006).
12. Stewart, M. J. & Vanderberg, J. P. Malaria sporozoites leave behind trails of circumsporozoite protein during gliding motility. J. Protozool. 35, 389-393 (1988).
13. Russell, D. G. & Sinden, R. E. The role of the cytoskeleton in the motility of coccidian sporozoites. J. Cell Sci. 50, 345-359 (1981).
14. Ryning, F. W. & Remington, J. S. Effect of cytochalasin D on Toxoplasma gondii cell entry. Infect. Immun. 20, 739-743 (1978).
15. Wetzel, D. M., Schmidt, J., Kuhlenschmidt, M. S., Dubey, J. P. & Sibley, L. D. Gliding motility leads to active cellular invasion by Cryptosporidium parvum sporozoites. Infect. Immun. 73, 5379-5387 (2005).
16. Pinder, J. C. et al. Actomyosin motor in the merozoite of the malaria parasite, Plasmodium falciparum: Implications for red cell invasion. J. Cell Sci. 111, 1831-1839 (1998).
17. Dobrowolski, J. M., Carruthers, V. B. & Sibley, L. D. Participation of myosin in gliding motility and host cell invasion by Toxoplasma gondii. Mol. Microbiol. 26, 163-173 (1997).
18. Dobrowolski, J. M., Niesman, I. R. & 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, 253-262 (1997).
19. Patron, S. A. et al. Identification and purification of actin from the subpellicular network of Toxoplasma gondii tachyzoites. Int. J. Parasitol. 35, 883-894 (2005).
20. Trottein, F., Triglia, T. & Cowman, A. F. Molecular cloning of a gene from Plasmodium falciparum that codes for a protein sharing motifs found in adhesive molecules from mammals and plasmodia. Mol. Biochem. Parasitol. 74, 129-141 (1995).
21. Robson, K. J. et al. A highly conserved amino-acid sequence in thrombospondin, properdin and in proteins from sporozoites and blood stages of a human malaria parasite. Nature 335, 79-82 (1988).
22. Brossier, F. & Sibley, L. D. Toxoplasma gondii: Microneme protein MIC2. Int. J. Biochem. Cell Biol. 37, 2266-2272 (2005).
23. Spano, F. et al. Molecular cloning and expression analysis of a Cryptosporidium parvum gene encoding a new member of the thrombospondin family. Mol. Biochem. Parasitol. 92, 147-162 (1998).
24. Jewett, T. J. & Sibley, L. D. Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in apicomplexan parasites. Mol. Cell. 11, 885-894 (2003).
25. Buscaglia, C. A., Coppens, I., Hol, W. G. & Nussenzweig, V. Sites of interaction between aldolase and thrombospondin-related anonymous protein in plasmodium. Mol. Biol. Cell 14, 4947-4957 (2003).
26. Sultan, A. A. et al. TRAP is necessary for gliding motility and infectivity of plasmodium sporozoites. Cell 90, 511-522 (1997).
27. Yuda, M., Sakaida, H. & Chinzei, Y. Targeted disruption of the Plasmodium berghei CTRP gene reveals its essential role in malaria infection of the vector mosquito. J. Exp. Med. 190, 1711-1716 (1999).
28. Dessens, J. T. et al. CTRP is essential for mosquito infection by malaria ookinetes. EMBO J. 18, 6221-6227 (1999).
29. Bergman, L. W. et al. Myosin A tail domain interacting protein (MTIP) localizes to the inner membrane complex of Plasmodium sporozoites. J. Cell Sci. 116, 39-49 (2003).
30. Bosch, J. et al. Structure of the MTIP-MyoA complex, a key component of the malaria parasite invasion motor. Proc. Natl Acad. Sci. USA 103, 4852-4857 (2006).
31. Green, J. L. et al. The MTIP-myosin A complex in blood stage malaria parasites. J. Mol. Biol. 355, 933-941 (2006).
32. Jones, M. L., Kitson, E. L. & Rayner, J. C. Plasmodium falciparum erythrocyte invasion: A conserved myosin associated complex. Mol. Biochem. Parasitol. 147, 74-84 (2006).
33. Gaskins, E. et al. Identification of the membrane receptor of a class XIV myosin in Toxoplasma gondii. J. Cell Biol. 165, 383-393 (2004).
34. Foth, B. J., Goedecke, M. C. & Soldati, D. New insights into myosin evolution and classification. Proc. Natl Acad. Sci. USA 103, 3681-3686 (2006).
35. Herm-Gotz, A. et al. Toxoplasma gondii myosin A and its light chain: A fast, single-headed, plus-end-directed motor. EMBO J. 21, 2149-2158 (2002).
36. Meissner, M., Schluter, D. & Soldati, D. Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science 298, 837-840 (2002).
37. Schmitz, S. et al. Malaria parasite actin filaments are very short. J. Mol. Biol. 349, 113-125 (2005).
38. Schuler, H., Mueller, A. K. & Matuschewski, K. Unusual properties of Plasmodium falciparum actin: New insights into microfilament dynamics of apicomplexan parasites. FEBS Lett. 579, 655-660 (2005).
39. Sahoo, N., Beatty W., Heuser, J., Sept, D. & Sibley, L. D. Unusual kinetic and structural properties control rapid assembly and turnover of actin in the parasite Toxoplasma gondii. Mol. Biol. Cell 17, 895-906 (2005).
40. Revenu, C., Athman, R., Robine, S. & Louvard, D. The co-workers of actin filaments: From cell structures to signals. Nature Rev. Mol. Cell. Biol. 5, 635-646 (2004).
41. Bannister, L. H. & Mitchell, G. H. The role of the cytoskeleton in Plasmodium falciparum merozoite biology: An electron-microscopic view. Ann. Trop. Med. Parasitol. 89, 105-111 (1995).
42. Shaw, M. K. & 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, 9095-9099 (1999).
43. Field, S. J. et al. Actin in the merozoite of the malaria parasite, Plasmodium falciparum. Cell Motil. Cytoskeleton 25, 43-48 (1993).
44. Mizuno, Y. et al. Effect of jasplakinolide on the growth, invasion, and actin cytoskeleton of Plasmodium falciparum. Parasitol. Res. 88, 844-848 (2002).
45. Wetzel, D. M., Hakansson, S., Hu, K., Roos. D. & Sibley, L. D. Actin filament polymerization regulates gliding motility by apicomplexan parasites. Mol. Biol. Cell 14, 396-406 (2003).
46. Wesseling, J. G., Smits, M. A & Schoenmakers, J. G. Extremely diverged actin proteins in Plasmodium falciparum. Mol. Biochem. Parasitol. 30, 143-153 (1988).
47. Kim, K., Gooze, L., Petersen, C., Gut, J. & Nelson, R. G. Isolation, sequence and molecular karyotype analysis of the actin gene of Cryptosporidium parvum. Mol. Biochem. Parasitol. 50, 105-113 (1992).
48. Wesseling, J. G. et al. Stage-specific expression and genomic organization of the actin genes of the malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 35, 167-176 (1989).
49. Kabsch, W., Mannherz, H. G., Suck, D., Pai, E. F. & Holmes, K. C. Atomic structure of the actin: DNase I complex. Nature 347, 37-44 (1990).
50. Dominguez, R. Actin-binding proteins - a unifying hypothesis. Trends Biochem. Sci. 29, 572-578 (2004).
51. Abrahamsen, M. S. et al. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304, 441-445 (2004).
52. Carlton, J. M. et al. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoeli. Nature 419, 512-519 (2002).
53. Gardner, M. J. et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498-511 (2002).
54. Pain, A et al. Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. Science 309, 131-133 (2005).
55. Gordon. J. L. & Sibley, L. D. Comparative genome analysis reveals a conserved family of actin-like proteins in apicomplexan parasites. BMC Genomics 6, 179 (2005).
56. Ivens, A. C. et al. The genome of the kinetoplastid parasite, Leishmania major. Science 309, 436-442 (2005).
57. Baum, B. & Perrimon, N. Spatial control of the actin cytoskeleton in Drosophila epithelial cells. Nature Cell Biol. 3, 883-890 (2001).
58. Yarovinsky, F. et al. TLR 11 activation of dendritic cells by a protozoan profilin-like protein. Science 308, 1626-1629 (2005).
59. Fetterer, R. H., Miska, K. B., Jenkins, M. C. & Barfield, R. C. A conserved 19-kDa Eimeria tenella antigen is a profilin-like protein. J. Parasitol. 90, 1321-1328 (2004).
60. Bozdech, Z. et al. Expression profiling of the schizont and trophozoite stages of Plasmodium falciparum with a long-oligonucleotide microarray. Genome Biol. 4, R9 (2003).
61. Le Roch, K. G. et al. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301, 1503-1508 (2003).
62. Barnburg, J. R. Proteins of the ADF/cofilin family: Essential regulators of actin dynamics. Annu. Rev. Cell Dev. Biol. 15, 185-230 (1999).
63. Allen, M. L., Dobrowolski, J. M., Muller, H., Sibley, L. D. & Mansour, T. E. Cloning and characterization of actin depolymerizing factor from Toxoplasma gondii. Mol. Biochem. Parasitol. 88, 43-52 (1997).
64. Schuler, H., Mueller, A. K. & Matuschewski, K. A Plasmodium actin-depolymerizing factor that binds exclusively to actin monomers. Mol. Biol. Cell 16, 4013-4023 (2005).
65. Huang, T. Y., Dermardirossian, C. & Bokoch. G. M. Cofilin phosphatases and regulation of actin dynamics. Curr. Opin. Cell Biol. 18, 26-31 (2006).
66. Baum, B., Li, W. & Perrimon, N. A cyclase-associated protein regulates actin and cell polarity during Drosophila oogenesis and in yeast. Curr. BioL. 10, 964-973 (2000).
67. Balcer, H. I. et al. Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1. Curr. Biol. 13, 2159-2169 (2003).
68. Goodson, H. V. & Hawse, W. F. Molecular evolution of the actin family J. Cell Sci. 115, 2619-2622 (2002).
69. Quinlan, M. E., Heuser, J. E., Kerkhoff, E. & Mullins, R. D. Drosophila spire is an actin nucleation factor. Nature 433, 382-388 (2005).
70. Higgs, H. N. Formin proteins: A domain-based approach. Trends Biochem. Sci. 30, 342-353 (2005).
71. Tardieux, I. et al. A Plasmodium falciparum novel gene encoding a coronin-like protein which associates with actin filaments. FEBS Lett. 441, 251-256 (1998).
72. Poupel, O., Boleti, H., Axisa, S., Couture-Tosi, E. & Tardieux, I. Toxofilin, a novel actin-binding protein from Toxoplasma gondii, sequesters actin monomers and caps actin filaments. Mol. Biol. Cell 11, 355-368 (2000).
73. Carruthers, V. B. & Sibley, L. D. Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii. Mol. Microbiol. 31, 421-428 (1999).
74. Lovett, J. L. & Sibley, L. D. Intracellular calcium stores in Toxoplasma gondii govern invasion of host cells. J. Cell Sci. 116, 3009-3016 (2003).
75. Ward, P., Equinet, L., Packer, J. & Doerig, C. Protein kinases of the human malaria parasite Plasmodium falciparum: The kinome of a divergent eukaryote. BMC Genomics 5, 79 (2004).
76. Kieschnick, H., Wakefield, T., Narducci, C. A. & Beckers, C. Toxoplasma gondii attachment to host cells is regulated by a calmodulin-like domain protein kinase. J. Biol. Chem. 276, 12369-12377 (2001).
77. Siden-Kiamos, I. et al. Plasmodium berghei calcium-dependent protein kinase 3 is required for ookinete gliding motility and mosquito midgut invasion. Mol. Microbiol. 60, 1355-1363 (2006).
78. Ishino, T., Onto, Y., Chinrei, Y. & Yuda, M. A calcium-dependent protein kinase regulates Plasmodium ookinete access to the midgut epithelial cell. Mol. Microbiol. 59, 1175-1184 (2006).
79. Snow, R. W., Guerra, C. A., Noor, A. M., Myint, H. Y. & Hay, S. I. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434, 214-217 (2005).
80. Brossier, F., Jewett, T. J., Sibley, L. D. & Urban, S. A spatially localized rhomboid protease cleaves cell surface adhesins essential for invasion by Toxoplasma. Proc. Natl Acad. Sci. USA 102, 4146-4151 (2005).
81. Dowse, T. J., Pascall, J. C., Brown, K. D. & Soldati, D. Apicomplexan rhomboids have a potential role in microneme protein cleavage during host cell invasion. Int. J. Parasitol. 35, 747-756 (2005).
82. Beltzner, C. C. & Pollard, T. D. Identification of functionally important residues of Arp2/3 complex by analysis of homology models from diverse species. J. Mol. Biol. 336, 551-565 (2004).