Reorganization of the Endosomal System in -Infected Cells: The Ultrastructure of -Induced Tubular Compartments

English version České info

Salmonella enterica is an invasive, facultative intracellular bacterial pathogen. Within mammalian host cells, Salmonella inhabits a specialized membrane-bound compartment, the Salmonella-containing vacuole (SCV), redirects host cell vesicular transport and massively remodels the endosomal system. These activities depend on the function of a type III secretion system and its translocated effector proteins. Intracellular Salmonella induces several types of tubular compartments termed Salmonella-induced tubules (SIT), but the biogenesis and biological function of SIT is only partially understood. Our work combines live cell imaging with correlative light and electron microscopy to provide ultrastructural insight into SIT. We report that SIT emerge as single membrane tubules that convert into double membrane tubules entrapping cytosol and cytoskeletal filaments. Labeling of the endosomal compartment and cytochemistry demonstrate that the space between inner and outer SIT membrane is composed of internalized material and connected to Salmonella within the SCV. The effector proteins SseF and SseG translocated by intracellular Salmonella are essential for the conversion of single to double membrane SIT. These findings challenge current models for the intracellular lifestyle of Salmonella and the composition of its intracellular habitat.

Vyšlo v časopise: Reorganization of the Endosomal System in -Infected Cells: The Ultrastructure of -Induced Tubular Compartments. PLoS Pathog 10(9): e32767. doi:10.1371/journal.ppat.1004374
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004374

Souhrn

Zdroje

1. Schaible UE, Haas A, editors (2009) Intracellular Niches for Microbes: A Pathogens Guide Through the Host Cell. Weinheim: Wiley-VCH.

2. FigueiraR, HoldenDW (2012) Functions of the Salmonella pathogenicity island 2 (SPI-2) type III secretion system effectors. Microbiology 158 : 1147–1161.

3. IbarraJA, Steele-MortimerO (2009) Salmonella -⁠ the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell Microbiol 11 : 1579–1586.

4. Garcia-del PortilloF, FinlayBB (1995) Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors. J Cell Biol 129 : 81–97.

5. SalcedoSP, HoldenDW (2003) SseG, a virulence protein that targets Salmonella to the Golgi network. EMBO J 22 : 5003–5014.

6. DrecktrahD, KnodlerLA, HoweD, Steele-MortimerO (2007) Salmonella trafficking is defined by continuous dynamic interactions with the endolysosomal system. Traffic 8 : 212–225.

7. KuhleV, AbrahamsGL, HenselM (2006) Intracellular Salmonella enterica redirect exocytic transport processes in a Salmonella pathogenicity island 2-dependent manner. Traffic 7 : 716–730.

8. Garcia-del PortilloF, ZwickMB, LeungKY, FinlayBB (1993) Salmonella induces the formation of filamentous structures containing lysosomal membrane glycoproteins in epithelial cells. Proc Natl Acad Sci U S A 90 : 10544–10548.

9. RajashekarR, LieblD, SeitzA, HenselM (2008) Dynamic remodeling of the endosomal system during formation of Salmonella-induced filaments by intracellular Salmonella enterica. Traffic 9 : 2100–2116.

10. DrecktrahD, Levine-WilkinsonS, DamT, WinfreeS, KnodlerLA, et al. (2008) Dynamic behavior of Salmonella-induced membrane tubules in epithelial cells. Traffic 9 : 2117–2129.

11. MotaLJ, RamsdenAE, LiuM, CastleJD, HoldenDW (2009) SCAMP3 is a component of the Salmonella-induced tubular network and reveals an interaction between bacterial effectors and post-Golgi trafficking. Cell Microbiol 11 : 1236–1253.

12. SchroederN, HenryT, de ChastellierC, ZhaoW, GuilhonAA, et al. (2010) The virulence protein SopD2 regulates membrane dynamics of Salmonella-containing vacuoles. PLoS Pathog 6: e1001002.

13. BrumellJH, GoosneyDL, FinlayBB (2002) SifA, a type III secreted effector of Salmonella typhimurium, directs Salmonella-induced filament (Sif) formation along microtubules. Traffic 3 : 407–415.

14. KuhleV, JäckelD, HenselM (2004) Effector proteins encoded by Salmonella pathogenicity island 2 interfere with the microtubule cytoskeleton after translocation into host cells. Traffic 5 : 356–370.

15. BeuzonCR, MeresseS, UnsworthKE, Ruiz-AlbertJ, GarvisS, et al. (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19 : 3235–3249.

16. HuotariJ, HeleniusA (2011) Endosome maturation. EMBO J 30 : 3481–3500.

17. AschBB, MedinaD, BrinkleyBR (1979) Microtubules and actin-containing filaments of normal, preneoplastic, and neoplastic mouse mammary epithelial cells. Cancer Res 39 : 893–907.

18. EllismanMH, DeerinckTJ, ShuX, SosinskyGE (2012) Picking faces out of a crowd: genetic labels for identification of proteins in correlated light and electron microscopy imaging. Methods Cell Biol 111 : 139–155.

19. ZhangY, HenselM (2013) Evaluation of nanoparticles as endocytic tracers in cellular microbiology. Nanoscale 5 : 9296–9309.

20. SandellJH, MaslandRH (1988) Photoconversion of some fluorescent markers to a diaminobenzidine product. J Histochem Cytochem 36 : 555–559.

21. RajashekarR, LieblD, ChikkaballiD, HenselM (2014) Analyses of Salmonella enterica SPI2 effector protein functions in remodelling the host cell endosomal system. submitted

22. KnappPE, SwansonJA (1990) Plasticity of the tubular lysosomal compartment in macrophages. J Cell Sci 95 : 433–439.

23. RubinszteinDC, ShpilkaT, ElazarZ (2012) Mechanisms of autophagosome biogenesis. Curr Biol 22: R29–34.

24. CemmaM, BrumellJH (2012) Interactions of pathogenic bacteria with autophagy systems. Curr Biol 22: R540–545.

25. BirminghamCL, BrumellJH (2006) Autophagy recognizes intracellular Salmonella enterica serovar Typhimurium in damaged vacuoles. Autophagy 2 : 156–158.

26. WildP, FarhanH, McEwanDG, WagnerS, RogovVV, et al. (2011) Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333 : 228–233.

27. FujitaN, MoritaE, ItohT, TanakaA, NakaokaM, et al. (2013) Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J Cell Biol 203 : 115–128.

28. KabeyaY, MizushimaN, UenoT, YamamotoA, KirisakoT, et al. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19 : 5720–5728.

29. TanidaI, WaguriS (2010) Measurement of autophagy in cells and tissues. Methods Mol Biol 648 : 193–214.

30. BirminghamCL, SmithAC, BakowskiMA, YoshimoriT, BrumellJH (2006) Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J Biol Chem 281 : 11374–11383.

31. ShpilkaT, WeidbergH, PietrokovskiS, ElazarZ (2011) Atg8: an autophagy-related ubiquitin-like protein family. Genome Biol 12 : 226.

32. MizushimaN, YamamotoA, HatanoM, KobayashiY, KabeyaY, et al. (2001) Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 152 : 657–668.

33. Hamacher-BradyA, BradyNR, LogueSE, SayenMR, JinnoM, et al. (2007) Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ 14 : 146–157.

34. SteinmanRM, BrodieSE, CohnZA (1976) Membrane flow during pinocytosis. A stereologic analysis. J Cell Biol 68 : 665–687.

35. KuhleV, HenselM (2002) SseF and SseG are translocated effectors of the type III secretion system of Salmonella pathogenicity island 2 that modulate aggregation of endosomal compartments. Cell Microbiol 4 : 813–824.

36. MüllerP, ChikkaballiD, HenselM (2012) Functional dissection of SseF, a membrane-integral effector protein of intracellular Salmonella enterica. PLoS ONE 7: e35004.

37. BoucrotE, BeuzonCR, HoldenDW, GorvelJP, MeresseS (2003) Salmonella typhimurium SifA effector protein requires its membrane-anchoring C-terminal hexapeptide for its biological function. J Biol Chem 278 : 14196–14202.

38. KnoopsK, KikkertM, WormSH, Zevenhoven-DobbeJC, van der MeerY, et al. (2008) SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol 6: e226.

39. ReggioriF, MonastyrskaI, VerheijeMH, CaliT, UlasliM, et al. (2010) Coronaviruses Hijack the LC3-I-positive EDEMosomes, ER-derived vesicles exporting short-lived ERAD regulators, for replication. Cell Host Microbe 7 : 500–508.

40. Romero-BreyI, MerzA, ChiramelA, LeeJY, ChlandaP, et al. (2012) Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. PLoS Pathog 8: e1003056.

41. McGourtyK, ThurstonTL, MatthewsSA, PinaudL, MotaLJ, et al. (2012) Salmonella inhibits retrograde trafficking of mannose-6-phosphate receptors and lysosome function. Science 338 : 963–967.

42. PolsMS, van MeelE, OorschotV, ten BrinkC, FukudaM, et al. (2013) hVps41 and VAMP7 function in direct TGN to late endosome transport of lysosomal membrane proteins. Nat Commun 4 : 1361.

43. BoucrotE, HenryT, BorgJP, GorvelJP, MeresseS (2005) The intracellular fate of Salmonella depends on the recruitment of kinesin. Science 308 : 1174–1178.

44. OhlsonMB, HuangZ, AltoNM, BlancMP, DixonJE, et al. (2008) Structure and function of Salmonella SifA indicate that its interactions with SKIP, SseJ, and RhoA family GTPases induce endosomal tubulation. Cell Host Microbe 4 : 434–446.

45. WangX, LiD, QuD, ZhouD (2010) Involvement of TIP60 acetyltransferase in intracellular Salmonella replication. BMC Microbiol 10 : 228.

46. AuweterSD, BhavsarAP, de HoogCL, LiY, ChanYA, et al. (2011) Quantitative mass spectrometry catalogues Salmonella pathogenicity island-2 effectors and identifies their cognate host binding partners. J Biol Chem 286 : 24023–24035.

47. AbrahamsGL, MüllerP, HenselM (2006) Functional dissection of SseF, a type III effector protein involved in positioning the Salmonella-containing vacuole. Traffic 7 : 950–965.

48. DeiwickJ, SalcedoSP, BoucrotE, GillilandSM, HenryT, et al. (2006) The translocated Salmonella effector proteins SseF and SseG interact and are required to establish an intracellular replication niche. Infect Immun 74 : 6965–6972.

49. RamsdenAE, HoldenDW, MotaLJ (2007) Membrane dynamics and spatial distribution of Salmonella-containing vacuoles. Trends Microbiol 15 : 516–524.

50. SheaJE, HenselM, GleesonC, HoldenDW (1996) Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci U S A 93 : 2593–2597.

51. ValdiviaRH, FalkowS (1996) Bacterial genetics by flow cytometry: rapid isolation of Salmonella typhimurium acid-inducible promoters by differential fluorescence induction. Mol Microbiol 22 : 367–378.

52. LorkowskiM, Felipe-LopezA, DanzerCA, HansmeierN, HenselM (2014) Salmonella enterica invasion of polarized epithelial cells is a highly cooperative effort. Infect Immun 82 : 2657–2667.

53. KremerJR, MastronardeDN, McIntoshJR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116 : 71–76.

54. HenselM, SheaJE, WatermanSR, MundyR, NikolausT, et al. (1998) Genes encoding putative effector proteins of the type III secretion system of Salmonella Pathogenicity Island 2 are required for bacterial virulence and proliferation in macrophages. Mol Microbiol 30 : 163–174.

55. FungC, LockR, GaoS, SalasE, DebnathJ (2008) Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol Biol Cell 19 : 797–806.