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Non-Lytic, Actin-Based Exit of Intracellular Parasites from Intestinal Cells

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The intestine is a common site for invasion by intracellular pathogens, but little is known about how pathogens restructure and exit intestinal cells in vivo. The natural microsporidian parasite N. parisii invades intestinal cells of the nematode C. elegans, progresses through its life cycle, and then exits cells in a transmissible spore form. Here we show that N. parisii causes rearrangements of host actin inside intestinal cells as part of a novel parasite exit strategy. First, we show that N. parisii infection causes ectopic localization of the normally apical-restricted actin to the basolateral side of intestinal cells, where it often forms network-like structures. Soon after this actin relocalization, we find that gaps appear in the terminal web, a conserved cytoskeletal structure that could present a barrier to exit. Reducing actin expression creates terminal web gaps in the absence of infection, suggesting that infection-induced actin relocalization triggers gap formation. We show that terminal web gaps form at a distinct stage of infection, precisely timed to precede spore exit, and that all contagious animals exhibit gaps. Interestingly, we find that while perturbations in actin can create these gaps, actin is not required for infection progression or spore formation, but actin is required for spore exit. Finally, we show that despite large numbers of spores exiting intestinal cells, this exit does not cause cell lysis. These results provide insight into parasite manipulation of the host cytoskeleton and non-lytic escape from intestinal cells in vivo.

Vyšlo v časopise: Non-Lytic, Actin-Based Exit of Intracellular Parasites from Intestinal Cells. PLoS Pathog 7(9): e32767. doi:10.1371/journal.ppat.1002227
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002227

Souhrn

The intestine is a common site for invasion by intracellular pathogens, but little is known about how pathogens restructure and exit intestinal cells in vivo. The natural microsporidian parasite N. parisii invades intestinal cells of the nematode C. elegans, progresses through its life cycle, and then exits cells in a transmissible spore form. Here we show that N. parisii causes rearrangements of host actin inside intestinal cells as part of a novel parasite exit strategy. First, we show that N. parisii infection causes ectopic localization of the normally apical-restricted actin to the basolateral side of intestinal cells, where it often forms network-like structures. Soon after this actin relocalization, we find that gaps appear in the terminal web, a conserved cytoskeletal structure that could present a barrier to exit. Reducing actin expression creates terminal web gaps in the absence of infection, suggesting that infection-induced actin relocalization triggers gap formation. We show that terminal web gaps form at a distinct stage of infection, precisely timed to precede spore exit, and that all contagious animals exhibit gaps. Interestingly, we find that while perturbations in actin can create these gaps, actin is not required for infection progression or spore formation, but actin is required for spore exit. Finally, we show that despite large numbers of spores exiting intestinal cells, this exit does not cause cell lysis. These results provide insight into parasite manipulation of the host cytoskeleton and non-lytic escape from intestinal cells in vivo.

Zdroje

1. HybiskeKStephensRS 2008 Exit strategies of intracellular pathogens. Nat Rev Microbiol 6 99 110

2. HybiskeKStephensRS 2007 Mechanisms of host cell exit by the intracellular bacterium Chlamydia. Proc Natl Acad Sci U S A 104 11430 11435

3. HamonMBierneHCossartP 2006 Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol 4 423 434

4. HagedornMRohdeKHRussellDGSoldatiT 2009 Infection by tubercular mycobacteria is spread by nonlytic ejection from their amoeba hosts. Science 323 1729 1733

5. StammLMPakMAMorisakiJHSnapperSBRottnerK 2005 Role of the WASP family proteins for Mycobacterium marinum actin tail formation. Proc Natl Acad Sci U S A 102 14837 14842

6. McGheeJD 2007 The C. elegans intestine. WormBook 1 36

7. Gravato-NobreMJHodgkinJ 2005 Caenorhabditis elegans as a model for innate immunity to pathogens. Cell Microbiol 7 741 751

8. IrazoquiJEUrbachJMAusubelFM 2010 Evolution of host innate defence: insights from Caenorhabditis elegans and primitive invertebrates. Nat Rev Immunol 10 47 58

9. TroemelERFelixMAWhitemanNKBarriereAAusubelFM 2008 Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans. PLoS Biol 6 2736 2752

10. HodgkinJPartridgeFA 2008 Caenorhabditis elegans meets microsporidia: the nematode killers from Paris. PLoS Biol 6 2634 2637

11. TexierCVidauCViguesBEl AlaouiHDelbacF 2010 Microsporidia: a model for minimal parasite-host interactions. Curr Opin Microbiol 13 443 449

12. WilliamsBA 2009 Unique physiology of host-parasite interactions in microsporidia infections. Cell Microbiol 11 1551 1560

13. KeelingPJFastNM 2002 Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu Rev Microbiol 56 93 116

14. KatinkaMDDupratSCornillotEMetenierGThomaratF 2001 Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414 450 453

15. DidierESMaddryJABrindleyPJStovallMEDidierPJ 2005 Therapeutic strategies for human microsporidia infections. Expert Rev Anti Infect Ther 3 419 434

16. KeelingPJLukerMAPalmerJD 2000 Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. Mol Biol Evol 17 23 31

17. LeeSCCorradiNByrnesEJ3rdTorres-MartinezSDietrichFS 2008 Microsporidia evolved from ancestral sexual fungi. Curr Biol 18 1675 1679

18. DidierESWeissLM 2006 Microsporidiosis: current status. Curr Opin Infect Dis 19 485 492

19. HigesMMartin-HernandezRBotiasCBailonEGGonzalez-PortoAV 2008 How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 10 2659 2669

20. ShawRWKM 1999 Fish Microsporidia. WittnerMWL  The Microsporidia and Microsporidiosis: ASM 418 446

21. TroemelER 2011 New Models of Microsporidiosis: Infections in Zebrafish, C. elegans, and Honey Bee. PLoS Pathog 7 e1001243

22. BromenshenkJJHendersonCBWickCHStanfordMFZulichAW 2010 Iridovirus and Microsporidian Linked to Honey Bee Colony Decline. PLoS One 5 e13181

23. MacQueenAJBaggettJJPerumovNBauerRAJanuszewskiT 2005 ACT-5 is an essential Caenorhabditis elegans actin required for intestinal microvilli formation. Mol Biol Cell 16 3247 3259

24. BossingerOFukushigeTClaeysMBorgonieGMcGheeJD 2004 The apical disposition of the Caenorhabditis elegans intestinal terminal web is maintained by LET-413. Dev Biol 268 448 456

25. HuskenKWiesenfahrtTAbrahamCWindofferRBossingerO 2008 Maintenance of the intestinal tube in Caenorhabditis elegans: the role of the intermediate filament protein IFC-2. Differentiation 76 881 896

26. TanMWMahajan-MiklosSAusubelFM 1999 Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci U S A 96 715 720

27. AballayAYorgeyPAusubelFM 2000 Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans. Curr Biol 10 1539 1542

28. LabrousseAChauvetSCouillaultCKurzCLEwbankJJ 2000 Caenorhabditis elegans is a model host for Salmonella typhimurium. Curr Biol 10 1543 1545

29. JiaKThomasCAkbarMSunQAdams-HuetB 2009 Autophagy genes protect against Salmonella typhimurium infection and mediate insulin signaling-regulated pathogen resistance. Proc Natl Acad Sci U S A 106 14564 14569

30. SatoTMushiakeSKatoYSatoKSatoM 2007 The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 448 366 369

31. LosFCKaoCYSmithamJMcDonaldKLHaC 2011 RAB-5 -⁠ and RAB-11-Dependent Vesicle-Trafficking Pathways Are Required for Plasma Membrane Repair after Attack by Bacterial Pore-Forming Toxin. Cell Host Microbe 9 147 157

32. Grimm-GunterEMRevenuCRamosSHurbainISmythN 2009 Plastin 1 binds to keratin and is required for terminal web assembly in the intestinal epithelium. Mol Biol Cell 20 2549 2562

33. TakemuraRMasakiTHirokawaN 1988 Developmental organization of the intestinal brush-border cytoskeleton. Cell Motil Cytoskeleton 9 299 311

34. KellerTC3rdConzelmanKAChasanRMoosekerMS 1985 Role of myosin in terminal web contraction in isolated intestinal epithelial brush borders. J Cell Biol 100 1647 1655

35. KellerTC3rdMoosekerMS 1982 Ca++-calmodulin-dependent phosphorylation of myosin, and its role in brush border contraction in vitro. J Cell Biol 95 943 959

36. CarberryKWiesenfahrtTWindofferRBossingerOLeubeRE 2009 Intermediate filaments in Caenorhabditis elegans. Cell Motil Cytoskeleton 66 852 864

37. BhavsarAPGuttmanJAFinlayBB 2007 Manipulation of host-cell pathways by bacterial pathogens. Nature 449 827 834

38. TsaousisADKunjiERGoldbergAVLucocqJMHirtRP 2008 A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453 553 556

39. AndersonRMMayRM 1982 Coevolution of hosts and parasites. Parasitology 85 Pt 2 411 426

40. FrankSA 1996 Models of parasite virulence. Q Rev Biol 71 37 78

41. ChalifouxLVMacKeyJCarvilleAShvetzDLinKC 1998 Ultrastructural morphology of Enterocytozoon bieneusi in biliary epithelium of rhesus macaques (Macaca mulatta). Vet Pathol 35 292 296

42. ConteasCNBerlinOGAshLRPruthiJS 2000 Therapy for human gastrointestinal microsporidiosis. Am J Trop Med Hyg 63 121 127

43. BrennerS 1974 The genetics of Caenorhabditis elegans. Genetics 77 71 94

44. PowellJRAusubelFM 2008 Models of Caenorhabditis elegans infection by bacterial and fungal pathogens. Methods Mol Biol 415 403 427

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2011 Číslo 9
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