Organization and function of an actin cytoskeleton in Plasmodium falciparum gametocytes

Cellular Microbiology

Volumn 17, Issue 2, 2015, Pages 207-225

  Hliscs, Marion ^a,b   Millet, Coralie ^a,b   Dixon, Matthew W ^a,b   Siden Kiamos, Inga ^c   Mcmillan, Paul ^a,b   Tilley, Leann ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CYTOCHALASIN D; F ACTIN; FORMIN 1; JASPAMIDE; METHENAMINE; TUBULIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; APICOPLAST; ARTICLE; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; GAMETOCYTE; IMMUNOELECTRON MICROSCOPY; MICROTUBULE; MITOCHONDRION; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; CHEMISTRY; METABOLISM; MICROSCOPY; PROTEIN MULTIMERIZATION;

PLASMODIUM FALCIPARUM;

ACTIN CYTOSKELETON; MICROSCOPY; PLASMODIUM FALCIPARUM; PROTEIN MULTIMERIZATION;

EID: 84921502509     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12359     Document Type: Article

References (81)

1. Aikawa, M., and Beaudoin, R.L. (1969) Effects of chloroquine on the morphology of the erythrocytic stages of Plasmodium gallinaceum. Am J Trop Med Hyg 18: 166-181.
2. Andenmatten, N., Egarter, S., Jackson, A.J., Jullien, N., Herman, J.P., and Meissner, M. (2013) Conditional genome engineering in Toxoplasma gondii uncovers alternative invasion mechanisms. Nat Methods 10: 125-127.
3. Andreadaki, M., Morgan, R.N., Deligianni, E., Kooij, T.W., Santos, J.M., Spanos, L., etal. (2014) Genetic crosses and complementation reveal essential functions for the Plasmodium stage-specific actin2 in sporogonic development. Cell Microbiol 16: 751-767.
4. Angrisano, F., Delves, M.J., Sturm, A., Mollard, V., McFadden, G.I., Sinden, R.E., and Baum, J. (2012a) A GFP-actin reporter line to explore microfilament dynamics across the malaria parasite lifecycle. Mol Biochem Parasitol 182: 93-96.
5. Angrisano, F., Riglar, D.T., Sturm, A., Volz, J.C., Delves, M.J., Zuccala, E.S., etal. (2012b) Spatial localisation of actin filaments across developmental stages of the malaria parasite. PLoS ONE 7: e32188.
6. Baum, J., Papenfuss, A.T., Baum, B., Speed, T.P., and Cowman, A.F. (2006) Regulation of apicomplexan actin-based motility. Nat Rev Microbiol 4: 621-628.
7. Baum, J., Tonkin, C.J., Paul, A.S., Rug, M., Smith, B.J., Gould, S.B., etal. (2008) A malaria parasite formin regulates actin polymerization and localizes to the parasite-erythrocyte moving junction during invasion. Cell Host Microbe 3: 188-198.
8. Bubb, M.R., Senderowicz, A.M., Sausville, E.A., Duncan, K.L., and Korn, E.D. (1994) Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J Biol Chem 269: 14869-14871.
9. Clemen, C.S., Rybakin, V., and Eichinger, L. (2008) The coronin family of proteins. Subcell Biochem 48: 1-5.
10. Cooper, J.A. (1987) Effects of cytochalasin and phalloidin on actin. J Cell Biol 105: 1473-1478.
11. Cooper, J.A., and Sept, D. (2008) New insights into mechanism and regulation of actin capping protein. Int Rev Cell Mol Biol 267: 183-206.
12. Cowman, A.F., Berry, D., and Baum, J. (2012) The cellular and molecular basis for malaria parasite invasion of the human red blood cell. J Cell Biol 198: 961-971.
13. De Vos, K.J., Allan, V.J., Grierson, A.J., and Sheetz, M.P. (2005) Mitochondrial function and actin regulate dynamin-related protein 1-dependent mitochondrial fission. Curr Biol 15: 678-683.
14. Dearnley, M.K., Yeoman, J.A., Hanssen, E., Kenny, S., Turnbull, L., Whitchurch, C.B., etal. (2012) Origin, composition, organization and function of the inner membrane complex of Plasmodium falciparum gametocytes. J Cell Sci 125: 2053-2063.
15. Deligianni, E., Morgan, R.N., Bertuccini, L., Kooij, T.W., Laforge, A., Nahar, C., etal. (2011) Critical role for a stage-specific actin in male exflagellation of the malaria parasite. Cell Microbiol 13: 1714-1730.
16. Dixon, M.W., Dearnley, M.K., Hanssen, E., Gilberger, T., and Tilley, L. (2012) Shape-shifting gametocytes: how and why does P.falciparum go banana-shaped? Trends Parasitol 28: 471-478.
17. Dobrowolski, J.M., and Sibley, L.D. (1996) Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84: 933-939.
18. 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: 253-262.
19. Ecker, A., Lakshmanan, V., Sinnis, P., Coppens, I., and Fidock, D.A. (2011) Evidence that mutant PfCRT facilitates the transmission to mosquitoes of chloroquine-treated Plasmodium gametocytes. J Infect Dis 203: 228-236.
20. Egarter, S., Andenmatten, N., Jackson, A.J., Whitelaw, J.A., Pall, G., Black, J.A., etal. (2014) The Toxoplasma acto-myoA motor complex is important but not essential for gliding motility and host cell invasion. PLoS ONE 9: e91819.
21. Evangelista, M., Zigmond, S., and Boone, C. (2003) Formins: signaling effectors for assembly and polarization of actin filaments. J Cell Sci 116: 2603-2611.
22. Fivelman, Q.L., McRobert, L., Sharp, S., Taylor, C.J., Saeed, M., Swales, C.A., etal. (2007) Improved synchronous production of Plasmodium falciparum gametocytes in vitro. Mol Biochem Parasitol 154: 119-123.
23. Foley, M., Deady, L.W., Ng, K., Cowman, A.F., and Tilley, L. (1994) Photoaffinity labeling of chloroquine-binding proteins in Plasmodium falciparum. J Biol Chem 269: 6955-6961.
24. Ganter, M., Schuler, H., and Matuschewski, K. (2009) Vital role for the Plasmodium actin capping protein (CP) beta-subunit in motility of malaria sporozoites. Mol Microbiol 74: 1356-1367.
25. Goode, B.L., Drubin, D.G., and Barnes, G. (2000) Functional cooperation between the microtubule and actin cytoskeletons. Curr Opin Cell Biol 12: 63-71.
26. Gordon, J.L., and Sibley, L.D. (2005) Comparative genome analysis reveals a conserved family of actin-like proteins in apicomplexan parasites. BMC Genomics 6: 179.
27. Gould, S.B., Tham, W.H., Cowman, A.F., McFadden, G.I., and Waller, R.F. (2008) Alveolins, a new family of cortical proteins that define the protist infrakingdom Alveolata. Mol Biol Evol 25: 1219-1230.
28. Gruring, C., Heiber, A., Kruse, F., Ungefehr, J., Gilberger, T.W., and Spielmann, T. (2011) Development and host cell modifications of Plasmodium falciparum blood stages in four dimensions. Nat Commun 2: 165.
29. Hadley, T.J., Erkmen, Z., Kaufman, B.M., Futrovsky, S., McGuinnis, M.H., Graves, P., etal. (1986) Factors influencing invasion of erythrocytes by Plasmodium falciparum parasites: the effects of an N-acetyl glucosamine neoglycoprotein and an anti-glycophorin A antibody. Am J Trop Med Hyg 35: 898-905.
30. Hanssen, E., Carlton, P., Deed, S., Klonis, N., Sedat, J., DeRisi, J., and Tilley, L. (2010) Whole cell imaging reveals novel modular features of the exomembrane system of the malaria parasite, Plasmodium falciparum. Int J Parasitol 40: 123-134.
31. Hu, K., Johnson, J., Florens, L., Fraunholz, M., Suravajjala, S., DiLullo, C., etal. (2006) Cytoskeletal components of an invasion machine - the apical complex of Toxoplasma gondii. PLoS Pathog 2: e13.
32. Ignatev, A., Bhargav, S.P., Vahokoski, J., Kursula, P., and Kursula, I. (2012) The lasso segment is required for functional dimerization of the Plasmodium formin 1 FH2 domain. PLoS ONE 7: e33586.
33. Ishihama, Y., Oda, Y., Tabata, T., Sato, T., Nagasu, T., Rappsilber, J., and Mann, M. (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4: 1265-1272.
34. Jacot, D., Daher, W., and Soldati-Favre, D. (2013) Toxoplasma gondii myosin F, an essential motor for centrosomes positioning and apicoplast inheritance. EMBO J 32: 1702-1716.
35. Kaverina, I., Rottner, K., and Small, J.V. (1998) Targeting, capture, and stabilization of microtubules at early focal adhesions. J Cell Biol 142: 181-190.
36. Kim, K., McCully, M.E., Bhattacharya, N., Butler, B., Sept, D., and Cooper, J.A. (2007) Structure/function analysis of the interaction of phosphatidylinositol 4, 5-bisphosphate with actin-capping protein: implications for how capping protein binds the actin filament. J Biol Chem 282: 5871-5879.
37. Knight, A., and Sinden, R.E. (1982) The purification of gametocytes of Plasmodium falciparum and P.yoelii nigeriensis by colloidal silica (Percoll) gradient centrifugation. Trans R Soc Trop Med Hyg 76: 503-509.
38. Korobova, F., Ramabhadran, V., and Higgs, H.N. (2013) An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. Science 339: 464-467.
39. Kovar, D.R., Harris, E.S., Mahaffy, R., Higgs, H.N., and Pollard, T.D. (2006) Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 124: 423-435.
40. Kudryashev, M., Lepper, S., Stanway, R., Bohn, S., Baumeister, W., Cyrklaff, M., and Frischknecht, F. (2010) Positioning of large organelles by a membrane-associated cytoskeleton in Plasmodium sporozoites. Cell Microbiol 12: 362-371.
41. Lambros, C., and Vanderberg, J.P. (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65: 418-420.
42. Lawrence, G., Cheng, Q.Q., Reed, C., Taylor, D., Stowers, A., Cloonan, N., etal. (2000) Effect of vaccination with 3 recombinant asexual-stage malaria antigens on initial growth rates of Plasmodium falciparum in non-immune volunteers. Vaccine 18: 1925-1931.
43. Lazarus, M.D., Schneider, T.G., and Taraschi, T.F. (2008) A new model for hemoglobin ingestion and transport by the human malaria parasite Plasmodium falciparum. J Cell Sci 121: 1937-1949.
44. Lin, D.C., Tobin, K.D., Grumet, M., and Lin, S. (1980) Cytochalasins inhibit nuclei-induced actin polymerization by blocking filament elongation. J Cell Biol 84: 455-460.
45. McMillan, P.J., Millet, C., Batinovic, S., Maiorca, M., Hanssen, E., Kenny, S., etal. (2013) Spatial and temporal mapping of the PfEMP1 export pathway in Plasmodium falciparum. Cell Microbiol 15: 1401-1418.
46. Mizuno, Y., Makioka, A., Kawazu, S., Kano, S., Kawai, S., Akaki, M., etal. (2002) Effect of jasplakinolide on the growth, invasion, and actin cytoskeleton of Plasmodium falciparum. Parasitol Res 88: 844-848.
47. Mueller, C., Klages, N., Jacot, D., Santos, J.M., Cabrera, A., Gilberger, T.W., etal. (2013) The Toxoplasma protein ARO mediates the apical positioning of rhoptry organelles, a prerequisite for host cell invasion. Cell Host Microbe 13: 289-301.
48. Munter, S., Sabass, B., Selhuber-Unkel, C., Kudryashev, M., Hegge, S., Engel, U., etal. (2009) Plasmodium sporozoite motility is modulated by the turnover of discrete adhesion sites. Cell Host Microbe 6: 551-562.
49. Okamoto, N., Spurck, T.P., Goodman, C.D., and McFadden, G.I. (2009) Apicoplast and mitochondrion in gametocytogenesis of Plasmodium falciparum. Eukaryot Cell 8: 128-132.
50. Pollard, T.D., and Borisy, G.G. (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453-465.
51. Pollard, T.D., and Cooper, J.A. (2009) Actin, a central player in cell shape and movement. Science 326: 1208-1212.
52. Pruyne, D., Evangelista, M., Yang, C., Bi, E., Zigmond, S., Bretscher, A., and Boone, C. (2002) Role of formins in actin assembly: nucleation and barbed-end association. Science 297: 612-615.
53. Rupp, I., Sologub, L., Williamson, K.C., Scheuermayer, M., Reininger, L., Doerig, C., etal. (2011) Malaria parasites form filamentous cell-to-cell connections during reproduction in the mosquito midgut. Cell Res 21: 683-696.
54. Sattler, J.M., Ganter, M., Hliscs, M., Matuschewski, K., and Schuler, H. (2011) Actin regulation in the malaria parasite. Eur J Cell Biol 90: 966-971.
55. Schatten, H., Sibley, L.D., and Ris, H. (2003) Structural evidence for actin-like filaments in Toxoplasma gondii using high-resolution low-voltage field emission scanning electron microscopy. Microsc Microanal 9: 330-335.
56. Schermelleh, L., Carlton, P.M., Haase, S., Shao, L., Winoto, L., Kner, P., etal. (2008) Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320: 1332-1336.
57. Schuler, H., and Matuschewski, K. (2006) Regulation of apicomplexan microfilament dynamics by a minimal set of actin-binding proteins. Traffic 7: 1433-1439.
58. 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: 655-660.
59. 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: 9095-9099.
60. Shaw, M.K., Compton, H.L., Roos, D.S., and Tilney, L.G. (2000) Microtubules, but not actin filaments, drive daughter cell budding and cell division in Toxoplasma gondii. J Cell Sci 113 (Part 7): 1241-1254.
61. Siden-Kiamos, I., Pinder, J.C., and Louis, C. (2006) Involvement of actin and myosins in Plasmodium berghei ookinete motility. Mol Biochem Parasitol 150: 308-317.
62. Siden-Kiamos, I., Schuler, H., Liakopoulos, D., and Louis, C. (2010) Arp1, an actin-related protein, in Plasmodium berghei. Mol Biochem Parasitol 173: 88-96.
63. Siden-Kiamos, I., Louis, C., and Matuschewski, K. (2012) Evidence for filamentous actin in ookinetes of a malarial parasite. Mol Biochem Parasitol 181: 186-189.
64. Sider, J.R., Mandato, C.A., Weber, K.L., Zandy, A.J., Beach, D., Finst, R.J., etal. (1999) Direct observation of microtubule-F-actin interaction in cell free lysates. J Cell Sci 112 (Part 12): 1947-1956.
65. Sinden, R.E. (1982) Gametocytogenesis of Plasmodium falciparum in vitro: an electron microscopic study. Parasitology 84: 1-11.
66. Sinden, R.E., Canning, E.U., Bray, R.S., and Smalley, M.E. (1978) Gametocyte and gamete development in Plasmodium falciparum. Proc R Soc Lond B Biol Sci 201: 375-399.
67. Skillman, K.M., Diraviyam, K., Khan, A., Tang, K., Sept, D., and Sibley, L.D. (2011) Evolutionarily divergent, unstable filamentous actin is essential for gliding motility in apicomplexan parasites. PLoS Pathog 7: e1002280.
68. Skillman, K.M., Daher, W., Ma, C.I., Soldati-Favre, D., and Sibley, L.D. (2012) Toxoplasma gondii profilin acts primarily to sequester G-actin while formins efficiently nucleate actin filament formation in vitro. Biochemistry 51: 2486-2495.
69. Skillman, K.M., Ma, C.I., Fremont, D.H., Diraviyam, K., Cooper, J.A., Sept, D., and Sibley, L.D. (2013) The unusual dynamics of parasite actin result from isodesmic polymerization. Nat Commun 4: 2285.
70. Smythe, W.A., Joiner, K.A., and Hoppe, H.C. (2008) Actin is required for endocytic trafficking in the malaria parasite Plasmodium falciparum. Cell Microbiol 10: 452-464.
71. Soldati, D., and Meissner, M. (2004) Toxoplasma as a novel system for motility. Curr Opin Cell Biol 16: 32-40.
72. Song, J., Worth, N.F., Rolfe, B.E., Campbell, G.R., and Campbell, J.H. (2000) Heterogeneous distribution of isoactins in cultured vascular smooth muscle cells does not reflect segregation of contractile and cytoskeletal domains. J Histochem Cytochem 48: 1441-1452.
73. Srinivasan, P., Beatty, W.L., Diouf, A., Herrera, R., Ambroggio, X., Moch, J.K., etal. (2011) Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion. Proc Natl Acad Sci USA 108: 13275-13280.
74. Tardieux, I., Liu, X., Poupel, O., Parzy, D., Dehoux, P., and Langsley, G. (1998) A Plasmodium falciparum novel gene encoding a coronin-like protein which associates with actin filaments. FEBS Lett 441: 251-256.
75. Tonkin, C.J., van Dooren, G.G., Spurck, T.P., Struck, N.S., Good, R.T., Handman, E., etal. (2004) Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol Biochem Parasitol 137: 13-21.
76. Vahakoski, J., Bhargav, S.P., Desfosses, A., Andreadaki, M., Esa-Pekka, K., Martinez, S.M., etal. (2014) Structural differences explain diverse functions of Plasmodium actins. PLoS Pathog 10: e1004091.
77. Wesseling, J.G., Snijders, P.J., van Someren, P., Jansen, J., Smits, M.A., and Schoenmakers, J.G. (1989) Stage-specific expression and genomic organization of the actin genes of the malaria parasite Plasmodium falciparum. Mol Biochem Parasitol 35: 167-176.
78. Westphal, M., Jungbluth, A., Heidecker, M., Muhlbauer, B., Heizer, C., Schwartz, J.M., etal. (1997) Microfilament dynamics during cell movement and chemotaxis monitored using a GFP-actin fusion protein. Curr Biol 7: 176-183.
79. 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: 396-406.
80. Yeoman, J.A., Hanssen, E., Maier, A.G., Klonis, N., Maco, B., Baum, J., etal. (2011) Tracking Glideosome-Associated Protein 50 reveals the development and organization of the inner membrane complex of Plasmodium falciparum. Eukaryot Cell 10: 556-564.
81. Zhang, Q., Huang, Y., Zhang, Y., Fang, X., Claes, A., Duchateau, M., etal. (2011) A critical role of perinuclear filamentous actin in spatial repositioning and mutually exclusive expression of virulence genes in malaria parasites. Cell Host Microbe 10: 451-463.