Structural Differences Explain Diverse Functions of Actins

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Malaria parasites have two actin isoforms, which are among the most divergent within the actin family that comprises highly conserved proteins, essential in all eukaryotic cells. In Plasmodium, actin is indispensable for motility and, thus, the infectivity of the deadly parasite. Yet, actin filaments have not been observed in vivo in these pathogens. Here, we show that the two Plasmodium actins differ from each other in both monomeric and filamentous form and that actin I cannot replace actin II during male gametogenesis. Whereas the major isoform actin I cannot form stable filaments alone, the mosquito-stage-specific actin II readily forms long filaments that have dimensions similar to canonical actins. A chimeric actin I mutant that forms long filaments in vitro also rescues gametogenesis in parasites lacking actin II. Both Plasmodium actins rapidly hydrolyze ATP and form short oligomers in the presence of ADP, which is a fundamental difference to all other actins characterized to date. Structural and functional differences in the two Plasmodium actin isoforms compared both to each other and to canonical actins reveal how the polymerization properties of eukaryotic actins have evolved along different avenues.

Vyšlo v časopise: Structural Differences Explain Diverse Functions of Actins. PLoS Pathog 10(4): e32767. doi:10.1371/journal.ppat.1004091
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004091

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Zdroje

1. PollardTD, CooperJA (2009) Actin, a central player in cell shape and movement. Science 326: 1208–1212.

2. DominguezR, HolmesKC (2011) Actin structure and function. Annu Rev Biophys 40: 169–186.

3. HermanIM (1993) Actin isoforms. Curr Opin Cell Biol 5: 48–55.

4. García-SalcedoJA, Pérez-MorgaD, GijónP, DilbeckV, PaysE, et al. (2004) A differential role for actin during the life cycle of Trypanosoma brucei. EMBO J 23: 780–789.

5. SchülerH, MatuschewskiK (2006) Plasmodium motility: actin not actin' like actin. Trends Parasitol 22: 146–147.

6. SibleyLD (1995) Invasion of vertebrate cells by Toxoplasma gondii. Trends Cell Biol 5: 129–132.

7. HeintzelmanMB (2006) Cellular and molecular mechanics of gliding locomotion in eukaryotes. Int Rev Cytol 251: 79–129.

8. MeissnerM, FergusonDJ, FrischknechtF (2013) Invasion factors of apicomplexan parasites: essential or redundant? Curr Opin Microbiol 16: 438–444.

9. Kuhni-BoghenborK, MaM, LemgruberL, CyrklaffM, FrischknechtF, et al. (2012) Actin-mediated plasma membrane plasticity of the intracellular parasite Theileria annulata. Cell Microbiol 14: 1867–1879.

10. ShawMK (1999) Theileria parva: sporozoite entry into bovine lymphocytes is not dependent on the parasite cytoskeleton. Exp Parasitol 92: 24–31.

11. KudryashevM, LepperS, BaumeisterW, CyrklaffM, FrischknechtF (2010) Geometric constrains for detecting short actin filaments by cryogenic electron tomography. PMC Biophys 3: 6.

12. Sidén-KiamosI, LouisC, MatuschewskiK (2012) Evidence for filamentous actin in ookinetes of a malarial parasite. Mol Biochem Parasitol 181: 186–189.

13. AngrisanoF, RiglarDT, SturmA, VolzJC, DelvesMJ, et al. (2012) Spatial localisation of actin filaments across developmental stages of the malaria parasite. PLoS One 7: e32188.

14. WetzelDM, HåkanssonS, HuK, RoosD, SibleyLD (2003) Actin filament polymerization regulates gliding motility by apicomplexan parasites. Mol Biol Cell 14: 396–406.

15. SahooN, BeattyW, HeuserJ, SeptD, SibleyLD (2006) Unusual kinetic and structural properties control rapid assembly and turnover of actin in the parasite Toxoplasma gondii. Mol Biol Cell 17: 895–906.

16. SchmitzS, GraingerM, HowellS, CalderLJ, GaebM, et al. (2005) Malaria parasite actin filaments are very short. J Mol Biol 349: 113–125.

17. SchülerH, MuellerAK, MatuschewskiK (2005) Unusual properties of Plasmodium falciparum actin: new insights into microfilament dynamics of apicomplexan parasites. FEBS Lett 579: 655–660.

18. SkillmanKM, MaCI, FremontDH, DiraviyamK, CooperJA, et al. (2013) The unusual dynamics of parasite actin result from isodesmic polymerization. Nat Commun 4: 2285.

19. DobrowolskiJM, NiesmanIR, SibleyLD (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.

20. FieldSJ, PinderJC, CloughB, DluzewskiAR, WilsonRJ, et al. (1993) Actin in the merozoite of the malaria parasite, Plasmodium falciparum. Cell Motil Cytoskeleton 25: 43–48.

21. WesselingJG, de ReeJM, PonnuduraiT, SmitsMA, SchoenmakersJG (1988) Nucleotide sequence and deduced amino acid sequence of a Plasmodium falciparum actin gene. Mol Biochem Parasitol 27: 313–320.

22. WesselingJG, SmitsMA, SchoenmakersJG (1988) Extremely diverged actin proteins in Plasmodium falciparum. Mol Biochem Parasitol 30: 143–153.

23. DeligianniE, MorganRN, BertucciniL, KooijTW, LaforgeA, et al. (2011) Critical role for a stage-specific actin in male exflagellation of the malaria parasite. Cell Microbiol 13: 1714–1730.

24. AndreadakiM, MorganRN, DeligianniE, KooijTW, SantosJM, et al. (2014) Genetic crosses and complementation reveal essential functions for the Plasmodium stage-specific actin2 in sporogonic development. Cell Microbiol [epub ahead of print].

25. LindnerSE, SwearingenKE, HarupaA, VaughanAM, SinnisP, et al. (2013) Total and putative surface proteomics of malaria parasite salivary gland sporozoites. Mol Cell Proteomics 12: 1127–1143.

26. SchmitzS, SchaapIA, KleinjungJ, HarderS, GraingerM, et al. (2010) Malaria parasite actin polymerization and filament structure. J Biol Chem 285: 36577–36585.

27. HohnM, TangG, GoodyearG, BaldwinPR, HuangZ, et al. (2007) SPARX, a new environment for Cryo-EM image processing. J Struct Biol 157: 47–55.

28. FujiiT, IwaneAH, YanagidaT, NambaK (2010) Direct visualization of secondary structures of F-actin by electron cryomicroscopy. Nature 467: 724–728.

29. EgelmanEH (2000) A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy 85: 225–234.

30. SachseC, ChenJZ, CoureuxPD, StroupeME, FandrichM, et al. (2007) High-resolution electron microscopy of helical specimens: a fresh look at tobacco mosaic virus. J Mol Biol 371: 812–835.

31. KursulaI, KursulaP, GanterM, PanjikarS, MatuschewskiK, et al. (2008) Structural basis for parasite-specific functions of the divergent profilin of Plasmodium falciparum. Structure 16: 1638–1648.

32. BaumJ, TonkinCJ, PaulAS, RugM, SmithBJ, et al. (2008) A malaria parasite formin regulates actin polymerization and localizes to the parasite-erythrocyte moving junction during invasion. Cell Host Microbe 3: 188–198.

33. WongW, SkauCT, MarapanaDS, HanssenE, TaylorNL, et al. (2011) Minimal requirements for actin filament disassembly revealed by structural analysis of malaria parasite actin-depolymerizing factor 1. Proc Natl Acad Sci U S A 108: 9869–9874.

34. WongW, WebbAI, OlshinaMA, InfusiniG, TanYH, 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.

35. SattlerJM, GanterM, HliscsM, MatuschewskiK, SchülerH (2011) Actin regulation in the malaria parasite. Eur J Cell Biol 90: 966–971.

36. IgnatevA, BhargavSP, VahokoskiJ, KursulaP, KursulaI (2012) The lasso segment is required for functional dimerization of the Plasmodium formin 1 FH2 domain. PLoS ONE 7: e33586.

37. SchülerH, MuellerAK, MatuschewskiK (2005) A Plasmodium actin-depolymerizing factor that binds exclusively to actin monomers. Mol Biol Cell 16: 4013–4023.

38. SinghBK, SattlerJM, ChatterjeeM, HuttuJ, SchülerH, et al. (2011) Crystal structures explain functional differences in the two actin depolymerization factors of the malaria parasite. J Biol Chem 286: 28256–28264.

39. McLaughlinPJ, GoochJT, MannherzHG, WeedsAG (1993) Structure of gelsolin segment 1-actin complex and the mechanism of filament severing. Nature 364: 685–692.

40. BhargavSP, VahokoskiJ, KumpulaEP, KursulaI (2013) Crystallization and preliminary structural characterization of the two actin isoforms of the malaria parasite. Acta Crystallogr Sect F Struct Biol Cryst Commun 69: 1171–1176.

41. MatsuuraY, StewartM, KawamotoM, KamiyaN, SaekiK, et al. (2000) Structural basis for the higher Ca(2+)-activation of the regulated actin-activated myosin ATPase observed with Dictyostelium/Tetrahymena actin chimeras. J Mol Biol 296: 579–595.

42. DominguezR (2004) Actin-binding proteins–a unifying hypothesis. Trends Biochem Sci 29: 572–578.

43. SchuttCE, MyslikJC, RozyckiMD, GoonesekereNC, LindbergU (1993) The structure of crystalline profilin-beta-actin. Nature 365: 810–816.

44. GalkinVE, OrlovaA, SchröderGF, EgelmanEH (2010) Structural polymorphism in F-actin. Nat Struct Mol Biol 17: 1318–1323.

45. MurakamiK, YasunagaT, NoguchiTQ, GomibuchiY, NgoKX, et al. (2010) Structural basis for actin assembly, activation of ATP hydrolysis, and delayed phosphate release. Cell 143: 275–287.

46. OdaT, MaedaY (2010) Multiple Conformations of F-actin. Structure 18: 761–767.

47. HolmesKC, PoppD, GebhardW, KabschW (1990) Atomic model of the actin filament. Nature 347: 44–49.

48. OdaT, IwasaM, AiharaT, MaedaY, NaritaA (2009) The nature of the globular- to fibrous-actin transition. Nature 457: 441–445.

49. OtterbeinLR, GraceffaP, DominguezR (2001) The crystal structure of uncomplexed actin in the ADP state. Science 293: 708–711.

50. MortonWM, AyscoughKR, McLaughlinPJ (2000) Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat Cell Biol 2: 376–378.

51. SpectorI, ShochetNR, KashmanY, GroweissA (1983) Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science 219: 493–495.

52. Strzelecka-GolaszewskaH, MossakowskaM, WozniakA, MoraczewskaJ, NakayamaH (1995) Long-range conformational effects of proteolytic removal of the last three residues of actin. Biochem J 307: 527–534.

53. PfaendtnerJ, BranduardiD, ParrinelloM, PollardTD, VothGA (2009) Nucleotide-dependent conformational states of actin. Proc Natl Acad Sci U S A 106: 12723–12728.

54. PfaendtnerJ, LymanE, PollardTD, VothGA (2010) Structure and dynamics of the actin filament. J Mol Biol 396: 252–263.

55. KhaitlinaSY, Strzelecka-GolaszewskaH (2002) Role of the DNase-I-binding loop in dynamic properties of actin filament. Biophys J 82: 321–334.

56. KuznetsovaI, AntropovaO, TuroverovK, KhaitlinaS (1996) Conformational changes in subdomain I of actin induced by proteolytic cleavage within the DNase I-binding loop: energy transfer from tryptophan to AEDANS. FEBS Lett 383: 105–108.

57. VorobievS, StrokopytovB, DrubinDG, FriedenC, OnoS, et al. (2003) The structure of nonvertebrate actin: implications for the ATP hydrolytic mechanism. Proc Natl Acad Sci U S A 100: 5760–5765.

58. WegnerA (1976) Head to tail polymerization of actin. J Mol Biol 108: 139–150.

59. AttriAK, LewisMS, KornED (1991) The formation of actin oligomers studied by analytical ultracentrifugation. J Biol Chem 266: 6815–6824.

60. KooijTW, RauchMM, MatuschewskiK (2012) Expansion of experimental genetics approaches for Plasmodium berghei with versatile transfection vectors. Mol Biochem Parasitol 185: 19–26.

61. de BoerPA, CrossleyRE, RothfieldLI (1992) Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli. J Bacteriol 174: 63–70.

62. RayChaudhuriD, ParkJT (1992) Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature 359: 251–254.

63. MukherjeeA, DaiK, LutkenhausJ (1993) Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc Natl Acad Sci U S A 90: 1053–1057.

64. BorkP, SanderC, ValenciaA (1992) An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc Natl Acad Sci U S A 89: 7290–7294.

65. EscalanteAA, AyalaFJ (1995) Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes. Proc Natl Acad Sci U S A 92: 5793–5797.

66. MitchisonTJ (1995) Evolution of a dynamic cytoskeleton. Philos Trans R Soc Lond B Biol Sci 349: 299–304.

67. SchülerH, KarlssonR, SchuttCE, LindbergU (2006) The connection between actin ATPase and polymerization. Advances in Molecular and Cell Biology 37: 49–65.

68. van den EntF, AmosLA, LoweJ (2001) Prokaryotic origin of the actin cytoskeleton. Nature 413: 39–44.

69. SkillmanKM, DiraviyamK, KhanA, TangK, SeptD, et al. (2011) Evolutionarily divergent, unstable filamentous actin is essential for gliding motility in apicomplexan parasites. PLoS Pathog 7: e1002280.

70. DurerZA, KudryashovDS, SawayaMR, AltenbachC, HubbellW, et al. (2012) Structural states and dynamics of the D-loop in actin. Biophys J 103: 930–939.

71. PaceCN, HornG, HebertEJ, BechertJ, ShawK, et al. (2001) Tyrosine hydrogen bonds make a large contribution to protein stability. J Mol Biol 312: 393–404.

72. BaekK, LiuX, FerronF, ShuS, KornED, et al. (2008) Modulation of actin structure and function by phosphorylation of Tyr-53 and profilin binding. Proc Natl Acad Sci U S A 105: 11748–11753.

73. JungbluthA, EckerskornC, GerischG, LottspeichF, StockerS, et al. (1995) Stress-induced tyrosine phosphorylation of actin in Dictyostelium cells and localization of the phosphorylation site to tyrosine-53 adjacent to the DNase I binding loop. FEBS Lett 375: 87–90.

74. LiuX, ShuS, HongMS, YuB, KornED (2010) Mutation of actin Tyr-53 alters the conformations of the DNase I-binding loop and the nucleotide-binding cleft. J Biol Chem 285: 9729–9739.

75. KameyamaK, KishiY, YoshimuraM, KanzawaN, SameshimaM, et al. (2000) Tyrosine phosphorylation in plant bending. Nature 407: 37.

76. KandasamyMK, McKinneyEC, RoyE, MeagherRB (2012) Plant vegetative and animal cytoplasmic actins share functional competence for spatial development with protists. Plant Cell 24: 2041–2057.

77. PardeeJD, SpudichJA (1982) Purification of muscle actin. Methods Enzymol 85(Pt B): 164–181.

78. SchneiderCA, RasbandWS, EliceiriKW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675.

79. KabschW (2010) XDS. Acta Crystallogr D Biol Crystallogr 66: 125–132.

80. KursulaP (2004) XDSi: a graphical interface for the data processing program XDS. Journal of applied crystallography 37: 347–348.

81. McCoyAJ, Grosse-KunstleveRW, AdamsPD, WinnMD, StoroniLC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658–674.

82. IrobiE, BurtnickLD, UrosevD, NarayanK, RobinsonRC (2003) From the first to the second domain of gelsolin: a common path on the surface of actin? FEBS Lett 552: 86–90.

83. AfoninePV, Grosse-KunstleveRW, EcholsN, HeaddJJ, MoriartyNW, et al. (2012) Towards automated crystallographic structure refinement with phenix. refine. Acta Crystallographica Section D: Biological Crystallography 68: 352–367.

84. EmsleyP, CowtanK (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126–2132.

85. ChenVB, ArendallWB, HeaddJJ, KeedyDA, ImmorminoRM, et al. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12–21.

86. PettersenEF, GoddardTD, HuangCC, CouchGS, GreenblattDM, et al. (2004) UCSF Chimera–a visualization system for exploratory research and analysis. J Comput Chem 25: 1605–1612.

87. MindellJA, GrigorieffN (2003) Accurate determination of local defocus and specimen tilt in electron microscopy. J Struct Biol 142: 334–347.

88. TangG, PengL, BaldwinPR, MannDS, JiangW, et al. (2007) EMAN2: an extensible image processing suite for electron microscopy. J Struct Biol 157: 38–46.

89. DesfossesA, CiuffaR, GutscheI, SachseC (2014) SPRING - An image processing package for single-particle based helical reconstruction from electron cryomicrographs. J Struct Biol 185: 15–26.

90. EgelmanEH (2010) Reconstruction of helical filaments and tubes. Methods Enzymol 482: 167–183.

91. de Koning-WardTF, FidockDA, ThathyV, MenardR, van SpaendonkRM, et al. (2000) The selectable marker human dihydrofolate reductase enables sequential genetic manipulation of the Plasmodium berghei genome. Mol Biochem Parasitol 106: 199–212.

92. BillkerO, DechampsS, TewariR, WenigG, Franke-FayardB, et al. (2004) Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 117: 503–514.

93. JanseCJ, RamesarJ, WatersAP (2006) High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nat Protoc 1: 346–356.

94. DiederichsK, KarplusPA (1997) Improved R-factors for diffraction data analysis in macromolecular crystallography. Nat Struct Biol 4: 269–275.

95. WeissMS, HilgenfeldR (1997) On the use of the merging R factor as a quality indicator for X-ray data. Journal of applied crystallography 30: 203–205.

96. KarplusPA, DiederichsK (2012) Linking crystallographic model and data quality. Science 336: 1030–1033.