Plasmodium falciparum coronin organizes arrays of parallel actin filaments potentially guiding directional motility in invasive malaria parasites

Malaria Journal

Volumn 14, Issue 1, 2015, Pages

  Olshina, Maya A ^a,b   Angrisano, Fiona ^a,b   Marapana, Danushka S ^a,b   Riglar, David T ^a,b,h   Bane, Kartik ^c   Wong, Wilson ^a,b   Catimel, Bruno ^a,d   Yin, Meng Xin ^e   Holmes, Andrew B ^e   Frischknecht, Friedrich ^c   Kovar, David R ^f   Baum, Jake ^a,b,g  

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

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d ROYAL MELBOURNE HOSPITAL   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f UNIVERSITY OF CHICAGO   (United States)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

^h HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Actin; Coronin; Gliding motility; Merozoite; Plasmodium; Tight junction

Indexed keywords

ACTIN BINDING PROTEIN; BINDING PROTEIN; CORONIN PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPID; UNCLASSIFIED DRUG; CORONIN PROTEINS; PROTOZOAL PROTEIN;

ACTIN FILAMENT; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; GEOGRAPHIC DISTRIBUTION; MOLECULAR DYNAMICS; NONHUMAN; PARASITE DEVELOPMENT; PARASITE IDENTIFICATION; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; SEDIMENTATION; SPECIES INVASION; TOTAL INTERNAL REFLECTION FLUORESCENCE MICROSCOPY; ANIMAL; CHEMISTRY; ERYTHROCYTE; HUMAN; MALARIA FALCIPARUM; METABOLISM; MOLECULAR MODEL; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; RABBIT;

ACTIN CYTOSKELETON; ANIMALS; ERYTHROCYTES; HUMANS; MALARIA, FALCIPARUM; MICROFILAMENT PROTEINS; MODELS, MOLECULAR; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RABBITS;

EID: 84937556188     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/s12936-015-0801-5     Document Type: Article

References (80)

1. Cowman AF, Berry D, Baum J (2012) The cellular and molecular basis for malaria parasite invasion of the human red blood cell. J Cell Biol 198:961-971
2. Prudencio M, Rodriguez A, Mota MM (2006) The silent path to thousands of merozoites: the Plasmodium liver stage. Nat Rev Microbiol 4:849-856
3. Baum J, Gilberger T-W, Frischknecht F, Meissner M (2008) Host-cell invasion by malaria parasites: insights from Plasmodium and Toxoplasma. Trends Parasitol 24:557-563
4. Morrissette NS, Sibley LD (2002) Cytoskeleton of apicomplexan parasites. Microbiol Mol Biol Rev 66:21-38
5. Frénal K, Polonais V, Marq J-B, Stratmann R, Limenitakis J, Soldati-Favre D (2010) Functional dissection of the apicomplexan glideosome molecular architecture. Cell Host Microbe 8:343-357
6. Pinder JC, Fowler RE, Dluzewski AR, Bannister LH, Lavin FM, Mitchell GH et al (1998) Actomyosin motor in the merozoite of the malaria parasite, Plasmodium falciparum: implications for red cell invasion. J Cell Sci 111:1831-1839
7. Jewett TJ, Sibley LD (2003) Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in apicomplexan parasites. Mol Cell 11:885-894
8. Wang J, Morris AJ, Tolan DR, Pagliaro L (1996) The molecular nature of the F-actin binding activity of aldolase revealed with site-directed mutants. J Biol Chem 271:6861-6865
9. Kudryashev M, Lepper S, Baumeister W, Cyrklaff M, Frischknecht F (2010) Geometric constrains for detecting short actin filaments by cryogenic electron tomography. PMC Biophys 3:6
10. Angrisano F, Riglar DT, Sturm A, Volz JC, Delves MJ, Zuccala ES et al (2012) Spatial localisation of actin filaments across developmental stages of the malaria parasite. PLoS One 7:e32188
11. Shen B, Sibley LD (2014) Toxoplasma aldolase is required for metabolism but dispensable for host-cell invasion. Proc Natl Acad Sci USA 111:3567-3572
12. Egarter S, Andenmatten N, Jackson AJ, Whitelaw JA, Pall G, Black JA et al (2014) The Toxoplasma Acto-MyoA motor complex is important but not essential for gliding motility and host cell invasion. PLoS One 9:e91819
13. Miller LH, Aikawa M, Johnson JG, Shiroishi T (1979) Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation. J Exp Med 149:172-184
14. Mizuno Y, Makioka A, Kawazu S, Kano S, Kawai S, Akaki M et al (2002) Effect of jasplakinolide on the growth, invasion, and actin cytoskeleton of Plasmodium falciparum. Parasitol Res 88:844-848
15. Schuler H, Matuschewski K (2006) Regulation of apicomplexan microfilament dynamics by a minimal set of actin-binding proteins. Traffic 7:1433-1439
16. Baum J, Papenfuss AT, Baum B, Speed TP, Cowman AF (2006) Regulation of apicomplexan actin-based motility. Nat Rev Microbiol 4:621-628
17. Olshina MA, Wong W, Baum J (2012) Holding back the microfilament - structural insights into actin and the actin-monomer-binding proteins of apicomplexan parasites. IUBMB Life 64:370-377
18. Baum J, Tonkin CJ, Paul AS, Rug M, Smith BJ, Gould SB et al (2008) A malaria parasite formin regulates actin polymerization and localizes to the parasite-erythrocyte moving junction during invasion. Cell Host Microb 3:188-198
19. Kursula I, Kursula P, Ganter M, Panjikar S, Matuschewski K, Schuler H (2008) Structural basis for parasite-specific functions of the divergent profilin of Plasmodium falciparum. Structure 16:1638-1648
20. Wong W, Webb AI, Olshina MA, Infusini G, Tan YH, Hanssen E et al (2014) A mechanism for actin filament severing by malaria parasite actin depolymerizing factor 1 via a low affinity binding interface. J Biol Chem 289:4043-4054
21. Singh BK, Sattler JM, Chatterjee M, Huttu J, Schüler H, Kursula I (2011) Crystal structures explain functional differences in the two actin depolymerization factors of the malaria parasite. J Biol Chem 286:28256-28264
22. Makkonen M, Bertling E, Chebotareva NA, Baum J, Lappalainen P (2013) Mammalian and malaria parasite cyclase-associated proteins catalyze nucleotide exchange on G-actin through a conserved mechanism. J Biol Chem 288:984-994
23. Hliscs M, Sattler JM, Tempel W, Artz JD, Dong A, Hui R et al (2010) Structure and function of a G-actin sequestering protein with a vital role in malaria oocyst development inside the mosquito vector. J Biol Chem 285:11572-11583
24. Ganter M, Rizopoulos Z, Schuler H, Matuschewski K (2015) Pivotal and distinct role for Plasmodium actin capping protein alpha during blood infection of the malaria parasite. Mol Microbiol 96:84-94
25. Tardieux I, Liu X, Poupel O, Parzy D, Dehoux P, Langsley G (1998) A Plasmodium falciparum novel gene encoding a coronin-like protein which associates with actin filaments. FEBS Lett 441:251-256
26. Uetrecht AC, Bear JE (2006) Coronins: the return of the crown. Trends Cell Biol 16:421-426
27. Eckert C, Hammesfahr B, Kollmar M (2011) A holistic phylogeny of the coronin gene family reveals an ancient origin of the tandem-coronin, defines a new subfamily, and predicts protein function. BMC Evol Biol 11:268
28. Chan KT, Creed SJ, Bear JE (2011) Unraveling the enigma: progress towards understanding the coronin family of actin regulators. Trends Cell Biol 21:481-488
29. Appleton BA, Wu P, Wiesmann C (2006) The crystal structure of murine coronin-1: a regulator of actin cytoskeletal dynamics in lymphocytes. Structure 14:87-96
30. Gatfield J, Albrecht I, Zanolari B, Steinmetz MO, Pieters J (2005) Association of the leukocyte plasma membrane with the actin cytoskeleton through coiled coil-mediated trimeric coronin 1 molecules. Mol Biol Cell 16:2786-2798
31. Kammerer RA, Kostrewa D, Progias P, Honnappa S, Avila D, Lustig A et al (2005) A conserved trimerization motif controls the topology of short coiled coils. Proc Natl Acad Sci USA 102:13891-13896
32. Salamun J, Kallio JP, Daher W, Soldati-Favre D, Kursula I (2014) Structure of Toxoplasma gondii coronin, an actin-binding protein that relocalizes to the posterior pole of invasive parasites and contributes to invasion and egress. FASEB J 28:4729-4747
33. Spudich JA, Watt S (1971) The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J Biol Chem 246:4866-4871
34. Wachsstock DH, Schwartz WH, Pollard TD (1993) Affinity of alpha-actinin for actin determines the structure and mechanical properties of actin filament gels. Biophys J 65:205-214
35. Neirynck K, Waterschoot D, Vandekerckhove J, Ampe C, Rommelaere H (2006) Actin interacts with CCT via discrete binding sites: a binding transition-release model for CCT-mediated actin folding. J Mol Biol 355:124-138
36. de Chaumont F, Dallongeville S, Chenouard N, Herve N, Pop S, Provoost T et al (2012) Icy: an open bioimage informatics platform for extended reproducible research. Nat Methods 9:690-696
37. Kovar DR, Kuhn JR, Tichy AL, Pollard TD (2003) The fission yeast cytokinesis formin Cdc12p is a barbed end actin filament capping protein gated by profilin. J Cell Biol 161:875-887
38. Neidt EM, Skau CT, Kovar DR (2008) The cytokinesis formins from the nematode worm and fission yeast differentially mediate actin filament assembly. J Biol Chem 283:23872-23883
39. Boyle MJ, Wilson DW, Richards JS, Riglar DT, Tetteh KK, Conway DJ et al (2010) Isolation of viable Plasmodium falciparum merozoites to define erythrocyte invasion events and advance vaccine and drug development. Proc Natl Acad Sci USA 107:14378-14383
40. Baum J, Richard D, Healer J, Rug M, Krnajski Z, Gilberger T-W et al (2006) A conserved molecular motor drives cell invasion and gliding motility across malaria life cycle stages and other apicomplexan parasites. J Biol Chem 281:5197-5208
41. Riglar DT, Richard D, Wilson DW, Boyle MJ, Dekiwadia C, Turnbull L et al (2011) Super-resolution dissection of coordinated events during malaria parasite invasion of the human erythrocyte. Cell Host Microbe 9:9-20
42. Lambros C, Vanderberg JP (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65:418-420
43. Boyle MJ, Richards JS, Gilson PR, Chai W, Beeson JG (2010) Interactions with heparin-like molecules during erythrocyte invasion by Plasmodium falciparum merozoites. Blood 115:4559-4568
44. Richard D, MacRaild CA, Riglar DT, Chan J-A, Foley M, Baum J et al (2010) Interaction between Plasmodium falciparum apical membrane antigen 1 and the rhoptry neck protein complex defines a key step in the erythrocyte invasion process of malaria parasites. J Biol Chem 285:14815-14822
45. Conway SJ, Gardiner J, Grove SJ, Johns MK, Lim ZY, Painter GF et al (2010) Synthesis and biological evaluation of phosphatidylinositol phosphate affinity probes. Org Biomol Chem 8:66-76
46. Catimel B, Kapp E, Yin MX, Gregory M, Wong LS, Condron M et al (2013) The PI(3)P interactome from a colon cancer cell. J Proteomics 82:35-51
47. Diaz SA, Martin SR, Grainger M, Howell SA, Green JL, Holder AA (2014) Plasmodium falciparum aldolase and the C-terminal cytoplasmic domain of certain apical organellar proteins promote actin polymerization. Mol Biochem Parasitol 197:9-14
48. Chan KT, Roadcap DW, Holoweckyj N, Bear JE (2012) Coronin 1C harbours a second actin-binding site that confers co-operative binding to F-actin. Biochem J 444:89-96
49. Gandhi M, Jangi M, Goode BL (2010) Functional surfaces on the actin-binding protein coronin revealed by systematic mutagenesis. J Biol Chem 285:34899-34908
50. Skau CT, Courson DS, Bestul AJ, Winkelman JD, Rock RS, Sirotkin V et al (2011) Actin filament bundling by fimbrin is important for endocytosis, cytokinesis, and polarization in fission yeast. J Biol Chem 286:26964-26977
51. Xu J, Wirtz D, Pollard TD (1998) Dynamic cross-linking by alpha-actinin determines the mechanical properties of actin filament networks. J Biol Chem 273:9570-9576
52. Falzone TT, Lenz M, Kovar DR, Gardel ML (2012) Assembly kinetics determine the architecture of alpha-actinin crosslinked F-actin networks. Nat Commun 3:861
53. Goode BL, Wong JJ, Butty AC, Peter M, McCormack AL, Yates JR et al (1999) Coronin promotes the rapid assembly and cross-linking of actin filaments and may link the actin and microtubule cytoskeletons in yeast. J Cell Biol 144:83-98
54. Asano S, Mishima M, Nishida E (2001) Coronin forms a stable dimer through its C-terminal coiled coil region: an implicated role in its localization to cell periphery. Genes Cells 6:225-235
55. Tempel M, Isenberg G, Sackmann E (1996) Temperature-induced sol-gel transition and microgel formation in alpha-actinin cross-linked actin networks: a rheological study. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 54:1802-1810
56. Higaki T, Kutsuna N, Sano T, Kondo N, Hasezawa S (2010) Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. Plant J 61:156-165
57. Khurana P, Henty JL, Huang S, Staiger AM, Blanchoin L, Staiger CJ (2010) Arabidopsis VILLIN1 and VILLIN3 have overlapping and distinct activities in actin bundle formation and turnover. Plant Cell 22:2727-2748
58. Bozdech Z, Zhu J, Joachimiak MP, Cohen FE, Pulliam B, DeRisi JL (2003) Expression profiling of the schizont and trophozoite stages of Plasmodium falciparum with a long-oligonucleotide microarray. Genome Biol 4:R9
59. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW et al (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511
60. Hodder AN, Crewther PE, Anders RF (2001) Specificity of the protective antibody response to apical membrane antigen 1. Infect Immun 69:3286-3294
61. Crewther PE, Culvenor JG, Silva A, Cooper JA, Anders RF (1990) Plasmodium falciparum: two antigens of similar size are located in different compartments of the rhoptry. Exp Parasitol 70:193-206
62. Triglia T, Healer J, Caruana SR, Hodder AN, Anders RF, Crabb BS et al (2000) Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species. Mol Microbiol 38:706-718
63. Wong W, Skau CT, Marapana DS, Hanssen E, Taylor NL, Riglar DT et al (2011) Minimal requirements for actin filament disassembly revealed by structural analysis of malaria parasite actin-depolymerizing factor 1. Proc Natl Acad Sci USA 108:9869-9874
64. Kauth CW, Woehlbier U, Kern M, Mekonnen Z, Lutz R, Mucke N et al (2006) Interactions between merozoite surface proteins 1, 6, and 7 of the malaria parasite Plasmodium falciparum. J Biol Chem 281:31517-31527
65. Tsujita K, Itoh T, Kondo A, Oyama M, Kozuka-Hata H, Irino Y et al (2010) Proteome of acidic phospholipid-binding proteins: spatial and temporal regulation of Coronin 1A by phosphoinositides. J Biol Chem 285:6781-6789
66. Catimel B, Schieber C, Condron M, Patsiouras H, Connolly L, Catimel J et al (2008) The PI(3,5)P2 and PI(4,5)P2 interactomes. J Proteome Res 7:5295-5313
67. Schüler H, Mueller A-K, Matuschewski K (2005) Unusual properties of Plasmodium falciparum actin: new insights into microfilament dynamics of apicomplexan parasites. FEBS Lett 579:655-660
68. Schmitz S, Schaap IA, Kleinjung J, Harder S, Grainger M, Calder L et al (2010) Malaria parasite actin polymerization and filament structure. J Biol Chem 285:36577-36585
69. Schmitz S, Grainger M, Howell S, Calder LJ, Gaeb M, Pinder JC et al (2005) Malaria parasite actin filaments are very short. J Mol Biol 349:113-125
70. Vahokoski J, Bhargav SP, Desfosses A, Andreadaki M, Kumpula EP, Martinez SM et al (2014) Structural differences explain diverse functions of Plasmodium actins. PLoS Pathog 10:e1004091
71. Skillman KM, Ma CI, Fremont DH, Diraviyam K, Cooper JA, Sept D et al (2013) The unusual dynamics of parasite actin result from isodesmic polymerization. Nat Commun 4:2285
72. Skillman KM, Diraviyam K, Khan A, Tang K, Sept D, Sibley LD (2011) Evolutionarily divergent, unstable filamentous actin is essential for gliding motility in apicomplexan parasites. PLoS Pathog 7:e1002280
73. Sahoo N, Beatty W, Heuser J, Sept D, Sibley LD (2006) Unusual kinetic and structural properties control rapid assembly and turnover of actin in the parasite Toxoplasma gondii. Mol Biol Cell 17:895-906
74. Field SJ, Pinder JC, Clough B, Dluzewski AR, Wilson RJ, Gratzer WB (1993) Actin in the merozoite of the malaria parasite, Plasmodium falciparum. Cell Motil Cytoskelet 25:43-48
75. Dobrowolski JM, Sibley LD (1996) Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84:933-939
76. Wetzel DM, Håkansson S, Hu K, Roos D, Sibley LD (2003) Actin filament polymerization regulates gliding motility by apicomplexan parasites. Mol Biol Cell 14:396-406
77. Bosch J, Turley S, Roach CM, Daly TM, Bergman LW, Hol WG (2007) The closed MTIP-myosin A-tail complex from the malaria parasite invasion machinery. J Mol Biol 372:77-88
78. Sheiner L, Santos JM, Klages N, Parussini F, Jemmely N, Friedrich N et al (2010) Toxoplasma gondii transmembrane microneme proteins and their modular design. Mol Microbiol 77:912-929
79. Oku T, Itoh S, Ishii R, Suzuki K, Nauseef WM, Toyoshima S et al (2005) Homotypic dimerization of the actin-binding protein p57/coronin-1 mediated by a leucine zipper motif in the C-terminal region. Biochem J 387:325-331
80. Galkin VE, Orlova A, Brieher W, Kueh HY, Mitchison TJ, Egelman EH (2008) Coronin-1A stabilizes F-actin by bridging adjacent actin protomers and stapling opposite strands of the actin filament. J Mol Biol 376:607-613