Protein Trafficking through the Endosomal System Prepares Intracellular Parasites for a Home Invasion

English version České info

Toxoplasma (toxoplasmosis) and Plasmodium (malaria) use unique secretory organelles for migration, cell invasion, manipulation of host cell functions, and cell egress. In particular, the apical secretory micronemes and rhoptries of apicomplexan parasites are essential for successful host infection. New findings reveal that the contents of these organelles, which are transported through the endoplasmic reticulum (ER) and Golgi, also require the parasite endosome-like system to access their respective organelles. In this review, we discuss recent findings that demonstrate that these parasites reduced their endosomal system and modified classical regulators of this pathway for the biogenesis of apical organelles.

Vyšlo v časopise: Protein Trafficking through the Endosomal System Prepares Intracellular Parasites for a Home Invasion. PLoS Pathog 9(10): e32767. doi:10.1371/journal.ppat.1003629
Kategorie: Review
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003629

Souhrn

Zdroje

1. WHO (2012) World malaria report. Available: http://www.who.int/malaria/publications/world_malaria_report_2012/en/index.html. Accessed 2 October 2013.

2. LuftBJ, RemingtonJS (1992) Toxoplasmic encephalitis in AIDS. Clin Infect Dis 15: 211–222.

3. KafsackBF, PenaJD, CoppensI, RavindranS, BoothroydJC, et al. (2009) Rapid membrane disruption by a perforin-like protein facilitates parasite exit from host cells. Science 323: 530–533.

4. CarruthersVB, TomleyFM (2008) Microneme proteins in apicomplexans. Subcell Biochem 47: 33–45.

5. BradleyPJ, WardC, ChengSJ, AlexanderDL, CollerS, et al. (2005) Proteomic analysis of rhoptry organelles reveals many novel constituents for host-parasite interactions in Toxoplasma gondii. J Biol Chem 280: 34245–3458.

6. ShenB, SibleyLD (2012) The moving junction, a key portal to host cell invasion by apicomplexan parasites. Curr Opin Microbiol 15: 449–455.

7. AlexanderDL, MitalJ, WardGE, BradleyP, BoothroydJC (2005) Identification of the moving junction complex of Toxoplasma gondii: a collaboration between distinct secretory organelles. PLoS Pathog 1: e17 doi:10.1371/journal.ppat.0010017

8. BoothroydJC, DubremetzJF (2008) Kiss and spit: the dual roles of Toxoplasma rhoptries. Nat Rev Microbiol 6: 79–88.

9. HunterCA, SibleyLD (2012) Modulation of innate immunity by Toxoplasma gondii virulence effectors. Nat Rev Microbiol 10: 766–778.

10. CounihanNA, KalanonM, CoppelRL, de Koning-WardTF (2013) Plasmodium rhoptry proteins: why order is important. Trends Parasitol 29: 228–236.

11. Tufet-BayonaM, JanseCJ, KhanSM, WatersAP, SindenRE, et al. (2009) Localisation and timing of expression of putative Plasmodium berghei rhoptry proteins in merozoites and sporozoites. Mol Biochem Parasitol 166: 22–31.

12. ShawMK, TilneyLG, MusokeAJ (1991) Theileria parva sporozoites into bovine lymphocytes: evidence for MHC class I involvement. J Cell Biol 113: 87–101.

13. DacksJB, FieldMC (2007) Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode. J Cell Sci 120: 2977–2985.

14. EliasM, BrighouseA, Gabernet-CastelloC, FieldMC, DacksJB (2012) Sculpting the endomembrane system in deep time: high resolution phylogenetics of Rab GTPases. J Cell Sci 125: 2500–2508.

15. KremerK, KaminD, RittwegerE, WilkesJ, FlammerH, et al. (2013) An overexpression screen of Toxoplasma gondii Rab-GTPases reveals distinct transport routes to the micronemes. PLoS Pathog 9: e1003213 doi:10.1371/journal.ppat.1003213

16. MellmanI, SimonsK (1992) The Golgi complex: in vitro veritas? Cell 68: 829–840.

17. RothmanJE, OrciL (1992) Molecular dissection of the secretory pathway. Nature 355: 409–415.

18. HagerKM, StriepenB, TilneyLG, RoosDS (1999) The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. J Cell Sci 112: 2631–2638.

19. SchrevelJ, Asfaux-FoucherG, HopkinsJM, RobertV, BourgouinC, et al. (2008) Vesicle trafficking during sporozoite development in Plasmodium berghei: ultrastructural evidence for a novel trafficking mechanism. Parasitology 135: 1–12.

20. MogelsvangS, MarshBJ, LadinskyMS, HowellKE (2004) Predicting function from structure: 3D structure studies of the mammalian Golgi complex. Traffic 5: 338–345.

21. HeCY (2007) Golgi biogenesis in simple eukaryotes. Cell Microbiol 9: 566–572.

22. PelletierL, SternCA, PypaertM, SheffD, NgoHM, et al. (2002) Golgi biogenesis in Toxoplasma gondii. Nature 418: 548–552.

23. JoinerKA, RoosDS (2002) Secretory traffic in the eukaryotic parasite Toxoplasma gondii: less is more. J Cell Biol 157: 557–563.

24. HoppeHC, NgoHM, YangM, JoinerKA (2000) Targeting to rhoptry organelles of Toxoplasma gondii involves evolutionarily conserved mechanisms. Nat Cell Biol 2: 449–456.

25. NgoMH, HoppeHC, JoinerKA (2000) Differential sorting and post-secretory targeting of proteins in parasitic invasion. Trends Cell Biol 10: 67–72.

26. BannisterLH, HopkinsJM, FowlerRE, KrishnaS, MitchellGH (2000) Ultrastructure of ROP development in Plasmodium falciparum erythrocytic schizonts. Parasitology 121: 273–287.

27. BannisterLH, HopkinsJM, DluzewskiAR, MargosG, WilliamsIT, et al. (2003) Plasmodium falciparum apical membrane antigen 1 (PfAMA-1) is translocated within micronemes along subpellicular microtubules during merozoite development. J Cell Sci 116: 3825–3834.

28. JoinerKA, RoosDS (2002) Secretory traffic in the eukaryotic parasite Toxoplasma gondii: less is more. J Cell Biol 157: 557–563.

29. HoppeHC, NgoHM, YangM, JoinerKA (2000) Targeting to rhoptry organelles of Toxoplasma gondii involves evolutionarily conserved mechanisms. Nat Cell Biol 2: 449–456.

30. NgoMH, HoppeHC, JoinerKA (2000) Differential sorting and post-secretory targeting of proteins in parasitic invasion. Trends Cell Biol 10: 67–72.

31. HarperJM, HuynhMH, CoppensI, ParussiniF, MorenoS, et al. (2006) A cleavable propeptide influences Toxoplasma infection by facilitating the trafficking and secretion of the TgMIC2-M2AP invasion complex. Mol Biol Cell 17: 4551–4563.

32. El HajjH, PapoinJ, CérèdeO, Garcia-RéguetN, SoêteM, et al. (2008) Molecular signals in the trafficking of Toxoplasma gondii protein MIC3 to the micronemes. Eukaryot Cell 7: 1019–1028.

33. BrydgesSD, HarperJM, ParussiniF, CoppensI, CarruthersVB (2008) A transient forward-targeting element for microneme-regulated secretion in Toxoplasma gondii. Biol Cell 100: 253–264.

34. ParussiniF, CoppensI, ShahPP, DiamondSL, CarruthersVB (2010) Cathepsin L occupies a vacuolar compartment and is a protein maturase within the endo/exocytic system of Toxoplasma gondii. Mol Microbiol 76: 1340–1357.

35. DubremetzJF (2007) Rhoptries are major players in Toxoplasma gondii invasion and host cell interaction. Cell Microbiol 9: 841–848.

36. YangM, CoppensI, WormsleyS, BaevovaP, HoppeHC, et al. (2004) The Plasmodium falciparum Vps4 homolog mediates multivesicular body formation. J Cell Sci 117: 3831–3838.

37. RichardD, KatsLM, LangerC, BlackCG, MitriK, et al. (2009) Identification of rhoptry trafficking determinants and evidence for a novel sorting mechanism in the malaria parasite Plasmodium falciparum. PLoS Pathog 5: e1000328 doi:10.1371/journal.ppat.1000328

38. QueX, NgoH, LawtonJ, GrayM, LiuQ, et al. (2002) The cathepsin B of Toxoplasma gondii, toxopain-1, is critical for parasite invasion and rhoptry protein processing. J Biol Chem 277: 25791–25797.

39. DouZ, CoppensI, CarruthersVB (2013) Non-canonical maturation of two papain-family proteases in Toxoplasma gondii. J Biol Chem 288: 3523–3534.

40. MarksMS, HeijnenHF, RaposoG (2013) Lysosome-related organelles: unusual compartments become mainstream. Curr Opin Cell Biol 25: 495–505.

41. SheinerL, Soldati-FavreD (2008) Protein trafficking inside Toxoplasma gondii. Traffic 9: 636–646.

42. KatsLM, CookeBM, CoppelRL, BlackCG (2007) Protein trafficking to apical organelles of malaria parasites-building an invasion machine. Traffic 9: 176–186.

43. TopolskaAE, LidgettA, TrumanD, FujiokaH, CoppelRL (2004) Characterization of a membrane-associated rhoptry protein of Plasmodium falciparum. J Biol Chem 279: 4648–4656.

44. BreinichMS, FergusonDJ, FothBJ, van DoorenGG, LebrunM, et al. (2009) A dynamin is required for the biogenesis of secretory organelles in Toxoplasma gondii. Curr Biol 19: 277–286.

45. SlovesPJ, DelhayeS, MouveauxT, WerkmeisterE, SlomiannyC, et al. (2012) Toxoplasma sortilin-like receptor regulates protein transport and is essential for apical secretory organelle biogenesis and host infection. Cell Host Microbe 11: 515–527.

46. HenneWM, BuchkovichNJ, EmrSD (2011) The ESCRT pathway. Dev Cell 21: 77–91.

47. LordC, BhandariD, MenonS, GhassemianM, NyczD, et al. (2011) Sequential interactions with Sec23 control the direction of vesicle traffic. Nature 473: 181–186.

48. LigeB, RomanoJD, SampelsV, SondaS, JoinerKA, et al. (2012) Introduction of caveolae structural proteins into the protozoan Toxoplasma results in the formation of heterologous caveolae but not caveolar endocytosis. PLoS ONE 7: e51773 doi:10.1371/journal.pone.0051773

49. FomovskaA, HuangQ, El BissatiK, MuiEJ, WitolaWH, et al. (2012) Novel N-benzoyl-2-hydroxybenzamide disrupts unique parasite secretory pathway. Antimicrob Agents Chemother 56: 2666–2682.

50. MirandaK, PaceDA, CintronR, RodriguesJC, FangJ, et al. (2010) Characterization of a novel organelle in Toxoplasma gondii with similar composition and function to the plant vacuole. Mol Microbiol 76: 1358–1375.

51. FranciaME, WicherS, PaceDA, SullivanJ, MorenoSN, et al. (2011) Toxoplasma gondii protein with homology to intracellular type Na+/H+ exchangers is important for osmoregulation and invasion. Exp Cell Res 317: 1382–1396.