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Plasticity between MyoC- and MyoA-Glideosomes: An Example of Functional Compensation in Invasion


Toxoplasma gondii can infect most warm-blooded animals, and is an important opportunistic pathogen for humans. This obligate intracellular parasite is able to invade virtually all nucleated cells, and as with most parasites of the Apicomplexa phylum, relies on a substrate-dependent gliding motility to actively penetrate into host cells and egress from infected cells. The conserved molecular machine (named glideosome) powering motility is located at the periphery of the parasite and involves the molecular motor, myosin A (MyoA). The glideosome exists in three flavors, exhibiting the same overall organization and sharing some common components while being spatially restricted to the central IMC, the apical cap and the basal pole of the parasite, respectively. The central and apical glideosomes are associated with MyoA (MyoA-glideosome) whereas the basal complex recruits myosin C (MyoC). Deleting components of the MyoC-glideosome uncovers the existence of complementary and compensatory mechanisms that ensure successful establishment of infection. This study highlights a higher degree of complexity and plasticity of the gliding machinery.


Vyšlo v časopise: Plasticity between MyoC- and MyoA-Glideosomes: An Example of Functional Compensation in Invasion. PLoS Pathog 10(11): e32767. doi:10.1371/journal.ppat.1004504
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004504

Souhrn

Toxoplasma gondii can infect most warm-blooded animals, and is an important opportunistic pathogen for humans. This obligate intracellular parasite is able to invade virtually all nucleated cells, and as with most parasites of the Apicomplexa phylum, relies on a substrate-dependent gliding motility to actively penetrate into host cells and egress from infected cells. The conserved molecular machine (named glideosome) powering motility is located at the periphery of the parasite and involves the molecular motor, myosin A (MyoA). The glideosome exists in three flavors, exhibiting the same overall organization and sharing some common components while being spatially restricted to the central IMC, the apical cap and the basal pole of the parasite, respectively. The central and apical glideosomes are associated with MyoA (MyoA-glideosome) whereas the basal complex recruits myosin C (MyoC). Deleting components of the MyoC-glideosome uncovers the existence of complementary and compensatory mechanisms that ensure successful establishment of infection. This study highlights a higher degree of complexity and plasticity of the gliding machinery.


Zdroje

1. InnesEA (2010) A brief history and overview of Toxoplasma gondii. Zoonoses Public Health 57: 1–7.

2. MorrissetteNS, SibleyLD (2002) Cytoskeleton of apicomplexan parasites. Microbiol Mol Biol Rev 66: 21–38 table of contents.

3. DubremetzJF, TorpierG (1978) Freeze fracture study of the pellicle of an eimerian sporozoite (Protozoa, Coccidia). J Ultrastruct Res 62: 94–109.

4. PorchetE, TorpierG (1977) [Freeze fracture study of Toxoplasma and Sarcocystis infective stages (author's transl)]. Z Parasitenkd 54: 101–124.

5. BeckJR, Rodriguez-FernandezIA, de LeonJC, HuynhMH, CarruthersVB, et al. (2010) A novel family of Toxoplasma IMC proteins displays a hierarchical organization and functions in coordinating parasite division. PLoS Pathog 6: e1001094.

6. NicholsBA, ChiappinoML (1987) Cytoskeleton of Toxoplasma gondii. J Protozool 34: 217–226.

7. HuK, JohnsonJ, FlorensL, FraunholzM, SuravajjalaS, et al. (2006) Cytoskeletal components of an invasion machine–the apical complex of Toxoplasma gondii. PLoS Pathog 2: e13.

8. HuK (2008) Organizational changes of the daughter basal complex during the parasite replication of Toxoplasma gondii. PLoS Pathog 4: e10.

9. OpitzC, SoldatiD (2002) 'The glideosome': a dynamic complex powering gliding motion and host cell invasion by Toxoplasma gondii. Mol Microbiol 45: 597–604.

10. CarruthersV, BoothroydJC (2007) Pulling together: an integrated model of Toxoplasma cell invasion. Curr Opin Microbiol 10: 83–89.

11. Herm-GotzA, WeissS, StratmannR, Fujita-BeckerS, RuffC, et al. (2002) Toxoplasma gondii myosin A and its light chain: a fast, single-headed, plus-end-directed motor. Embo J 21: 2149–2158.

12. MeissnerM, SchluterD, SoldatiD (2002) Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science 298: 837–840.

13. NeblT, PrietoJH, KappE, SmithBJ, WilliamsMJ, et al. (2011) Quantitative in vivo analyses reveal calcium-dependent phosphorylation sites and identifies a novel component of the Toxoplasma invasion motor complex. PLoS Pathog 7: e1002222.

14. FrenalK, PolonaisV, MarqJB, StratmannR, LimenitakisJ, et al. (2010) Functional dissection of the apicomplexan glideosome molecular architecture. Cell Host Microbe 8: 343–357.

15. GaskinsE, GilkS, DeVoreN, MannT, WardG, et al. (2004) Identification of the membrane receptor of a class XIV myosin in Toxoplasma gondii. J Cell Biol 165: 383–393.

16. Rees-ChannerRR, MartinSR, GreenJL, BowyerPW, GraingerM, et al. (2006) Dual acylation of the 45 kDa gliding-associated protein (GAP45) in Plasmodium falciparum merozoites. Mol Biochem Parasitol 149: 113–116.

17. AndenmattenN, EgarterS, JacksonAJ, JullienN, HermanJP, et al. (2013) Conditional genome engineering in Toxoplasma gondii uncovers alternative invasion mechanisms. Nat Methods 10: 125–7.

18. EgarterS, AndenmattenN, JacksonAJ, WhitelawJA, PallG, 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.

19. FoxBA, RistucciaJG, GigleyJP, BzikDJ (2009) Efficient gene replacements in Toxoplasma gondii strains deficient for nonhomologous end joining. Eukaryot Cell 8: 520–529.

20. HuynhMH, CarruthersVB (2009) Tagging of endogenous genes in a Toxoplasma gondii strain lacking Ku80. Eukaryot Cell 8: 530–539.

21. JacotD, FrenalK, MarqJB, SharmaP, Soldati-FavreD (2014) Assessment of phosphorylation in Toxoplasma glideosome assembly and function. Cell Microbiol 16: 1518–32.

22. GajriaB, BahlA, BrestelliJ, DommerJ, FischerS, et al. (2008) ToxoDB: an integrated Toxoplasma gondii database resource. Nucleic Acids Res 36: D553–556.

23. DelbacF, SangerA, NeuhausEM, StratmannR, AjiokaJW, et al. (2001) Toxoplasma gondii myosins B/C: one gene, two tails, two localizations, and a role in parasite division. J Cell Biol 155: 613–623.

24. MaeshimaM (1992) Characterization of the major integral protein of vacuolar membrane. Plant Physiol 98: 1248–1254.

25. SazukaT, KetaS, ShiratakeK, YamakiS, ShibataD (2004) A proteomic approach to identification of transmembrane proteins and membrane-anchored proteins of Arabidopsis thaliana by peptide sequencing. DNA Res 11: 101–113.

26. RenJ, WenL, GaoX, JinC, XueY, et al. (2008) CSS-Palm 2.0: an updated software for palmitoylation sites prediction. Protein Eng Des Sel 21: 639–644.

27. LorestaniA, IveyFD, ThirugnanamS, BusbyMA, MarthGT, et al. (2012) Targeted proteomic dissection of Toxoplasma cytoskeleton sub-compartments using MORN1. Cytoskeleton (Hoboken) 69: 1069–1085.

28. ShenB, BrownKM, LeeTD, SibleyLD (2014) Efficient gene disruption in diverse strains of Toxoplasma gondii using CRISPR/CAS9. MBio 5: e01114–01114.

29. HakanssonS, MorisakiH, HeuserJ, SibleyLD (1999) Time-lapse video microscopy of gliding motility in Toxoplasma gondii reveals a novel, biphasic mechanism of cell locomotion. Mol Biol Cell 10: 3539–3547.

30. FrenalK, TayCL, MuellerC, BushellES, JiaY, et al. (2013) Global analysis of apicomplexan protein S-acyl transferases reveals an enzyme essential for invasion. Traffic 14: 895–911.

31. GubbelsMJ, VaishnavaS, BootN, DubremetzJF, StriepenB (2006) A MORN-repeat protein is a dynamic component of the Toxoplasma gondii cell division apparatus. J Cell Sci 119: 2236–2245.

32. HeaslipAT, DzierszinskiF, SteinB, HuK (2010) TgMORN1 is a key organizer for the basal complex of Toxoplasma gondii. PLoS Pathog 6: e1000754.

33. LorestaniA, SheinerL, YangK, RobertsonSD, SahooN, et al. (2010) A Toxoplasma MORN1 null mutant undergoes repeated divisions but is defective in basal assembly, apicoplast division and cytokinesis. PLoS One 5: e12302.

34. RoosDS, DonaldRG, MorrissetteNS, MoultonAL (1994) Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol 45: 27–63.

35. SoldatiD, KimK, KampmeierJ, DubremetzJF, BoothroydJC (1995) Complementation of a Toxoplasma gondii ROP1 knock-out mutant using phleomycin selection. Mol Biochem Parasitol 74: 87–97.

36. SheinerL, SantosJM, KlagesN, ParussiniF, JemmelyN, et al. (2010) Toxoplasma gondii transmembrane microneme proteins and their modular design. Mol Microbiol [epub ahead of print]

37. StolsL, GuM, DieckmanL, RaffenR, CollartFR, et al. (2002) A new vector for high-throughput, ligation-independent cloning encoding a tobacco etch virus protease cleavage site. Protein expression and purification 25: 8–15.

38. SoldatiD, BoothroydJC (1993) Transient transfection and expression in the obligate intracellular parasite Toxoplasma gondii. Science 260: 349–352.

39. DonaldRG, CarterD, UllmanB, RoosDS (1996) Insertional tagging, cloning, and expression of the Toxoplasma gondii hypoxanthine-xanthine-guanine phosphoribosyltransferase gene. Use as a selectable marker for stable transformation. J Biol Chem 271: 14010–14019.

40. DingM, ClaytonC, SoldatiD (2000) Toxoplasma gondii catalase: are there peroxisomes in toxoplasma? J Cell Sci 113: 2409–2419.

41. PlattnerF, YarovinskyF, RomeroS, DidryD, CarlierMF, et al. (2008) Toxoplasma profilin is essential for host cell invasion and TLR11-dependent induction of an interleukin-12 response. Cell Host Microbe 3: 77–87.

42. HettmannC, HermA, GeiterA, FrankB, SchwarzE, et al. (2000) A dibasic motif in the tail of a class XIV apicomplexan myosin is an essential determinant of plasma membrane localization. Mol Biol Cell 11: 1385–1400.

43. BrossierF, JewettTJ, LovettJL, SibleyLD (2003) C-terminal processing of the toxoplasma protein MIC2 is essential for invasion into host cells. J Biol Chem 278: 6229–6234.

44. ThompsonJD, HigginsDG, GibsonTJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680.

45. BolognaG, YvonC, DuvaudS, VeutheyAL (2004) N-Terminal myristoylation predictions by ensembles of neural networks. Proteomics 4: 1626–1632.

46. LupasA, Van DykeM, StockJ (1991) Predicting coiled coils from protein sequences. Science 252: 1162–1164.

47. AurrecoecheaC, HeigesM, WangH, WangZ, FischerS, et al. (2007) ApiDB: integrated resources for the apicomplexan bioinformatics resource center. Nucleic Acids Res 35: D427–430.

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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PLOS Pathogens


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