The Salmonella deubiquitinase Ssel inhibits selective autophagy of cytosolic aggregates

PLoS Pathogens

Volumn 8, Issue 6, 2012, Pages

  Mesquita, Francisco S ^a   Thomas, Mair ^a   Sachse, Martin ^b   Santos, António J M ^a   Figueira, Rita ^a   Holden, David W ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; DEUBIQUITINASE SSEL; PROTEIN P62; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; PROTEINASE; UBIQUITIN;

AGGRESOME; ARTICLE; AUTOPHAGY; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL COMPARTMENTALIZATION; CELL STRESS; CELL VACUOLE; CONTROLLED STUDY; CYTOPLASM; CYTOSOL; EPITHELIUM CELL; GENE MUTATION; HOST; IMMUNOCOMPETENT CELL; MACROPHAGE; NONHUMAN; PATHOGENICITY ISLAND; PROTEIN AGGREGATION; PROTEIN DEGRADATION; SALMONELLA ENTERICA; SALMONELLA PATHOGENICITY ISLAND 2; SALMONELLOSIS; TYPE III SECRETION SYSTEM; UBIQUITINATION; ANIMAL; CELL LINE; CONFOCAL MICROSCOPY; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; HUMAN; IMMUNOBLOTTING; IMMUNOELECTRON MICROSCOPY; IMMUNOPRECIPITATION; METABOLISM; MOUSE; PARASITOLOGY;

BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA;

ANIMALS; AUTOPHAGY; BACTERIAL PROTEINS; CELL LINE; CYTOSOL; ENDOPEPTIDASES; EPITHELIAL CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MACROPHAGES; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MICROSCOPY, IMMUNOELECTRON; SALMONELLA ENTERICA; SALMONELLA INFECTIONS; UBIQUITIN; VACUOLES;

EID: 84864060156     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002743     Document Type: Article

References (69)

1. Galan JE, Curtiss R 3rd, (1989) Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci U S A 86: 6383-6387.
2. Ochman H, Soncini FC, Solomon F, Groisman EA, (1996) Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci U S A 93: 7800-7804.
3. Helaine S, Thompson JA, Watson KG, Liu M, Boyle C, et al. (2010) Dynamics of intracellular bacterial replication at the single cell level. Proc Natl Acad Sci U S A 107: 3746-3751.
4. Haraga A, Ohlson MB, Miller SI, (2008) Salmonellae interplay with host cells. Nat Rev Microbiol 6: 53-66.
5. Hicks SW, Galan JE, (2010) Hijacking the host ubiquitin pathway: structural strategies of bacterial E3 ubiquitin ligases. Curr Opin Microbiol 13: 41-46.
6. Rytkonen A, Holden DW, (2007) Bacterial interference of ubiquitination and deubiquitination. Cell Host Microbe 1: 13-22.
7. Rytkonen A, Poh J, Garmendia J, Boyle C, Thompson A, et al. (2007) SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc Natl Acad Sci U S A 104: 3502-3507.
8. Dupont N, Lacas-Gervais S, Bertout J, Paz I, Freche B, et al. (2009) Shigella phagocytic vacuolar membrane remnants participate in the cellular response to pathogen invasion and are regulated by autophagy. Cell Host Microbe 6: 137-149.
9. Collins CA, De Maziere A, van Dijk S, Carlsson F, Klumperman J, et al. (2009) Atg5-independent sequestration of ubiquitinated mycobacteria. PLoS Pathog 5: e1000430.
10. Fujita KI, Srinivasula SM, (2011) TLR4-mediated autophagy in macrophages is a p62-dependent type of selective autophagy of aggresome-like induced structures (ALIS). Autophagy 7: 552-554.
11. Szeto J, Kaniuk NA, Canadien V, Nisman R, Mizushima N, et al. (2006) ALIS are stress-induced protein storage compartments for substrates of the proteasome and autophagy. Autophagy 2: 189-199.
12. Ivanov SS, Roy CR, (2009) Modulation of ubiquitin dynamics and suppression of DALIS formation by the Legionella pneumophila Dot/Icm system. Cell Microbiol 11: 261-278.
13. Canadien V, Tan T, Zilber R, Szeto J, Perrin AJ, et al. (2005) Cutting edge: microbial products elicit formation of dendritic cell aggresome-like induced structures in macrophages. J Immunol 174: 2471-2475.
14. Fujita K, Maeda D, Xiao Q, Srinivasula SM, (2011) Nrf2-mediated induction of p62 controls Toll-like receptor-4-driven aggresome-like induced structure formation and autophagic degradation. Proc Natl Acad Sci U S A 108: 1427-1432.
15. Yoshikawa Y, Ogawa M, Hain T, Yoshida M, Fukumatsu M, et al. (2009) Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat Cell Biol 11: 1233-1240.
16. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, et al. (2005) Escape of intracellular Shigella from autophagy. Science 307: 727-731.
17. Mostowy S, Sancho-Shimizu V, Hamon M, Simeone R, Brosch R, et al. (2011) p62 and NDP52 target Intracytosolic Shigella and Listeria to different autophagy pathways. J Biol Chem 286: 26987-26995.
18. Birmingham CL, Brumell JH, (2006) Autophagy recognizes intracellular Salmonella enterica serovar Typhimurium in damaged vacuoles. Autophagy 2: 156-158.
19. Kageyama S, Omori H, Saitoh T, Sone T, Guan JL, et al. (2011) The LC3 recruitment mechanism is separate from Atg9L1-dependent membrane formation in the autophagic response against Salmonella. Mol Biol Cell 22: 2290-2300.
20. Thurston TL, Ryzhakov G, Bloor S, von Muhlinen N, Randow F, (2009) The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat Immunol 10: 1215-1221.
21. Salcedo SP, Holden DW, (2003) SseG, a virulence protein that targets Salmonella to the Golgi network. EMBO J 22: 5003-5014.
22. Garcia-del Portillo F, Finlay BB, (1995) Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors. J Cell Biol 129: 81-97.
23. Meresse S, Unsworth KE, Habermann A, Griffiths G, Fang F, et al. (2001) Remodelling of the actin cytoskeleton is essential for replication of intravacuolar Salmonella. Cell Microbiol 3: 567-577.
24. Guignot J, Caron E, Beuzon C, Bucci C, Kagan J, et al. (2004) Microtubule motors control membrane dynamics of Salmonella-containing vacuoles. J Cell Sci 117: 1033-1045.
25. Guignot J, Servin AL, (2008) Maintenance of the Salmonella-containing vacuole in the juxtanuclear area: a role for intermediate filaments. Microb Pathog 45: 415-422.
26. Bernal-Bayard J, Ramos-Morales F, (2009) Salmonella type III secretion effector SlrP is an E3 ubiquitin ligase for mammalian thioredoxin. J Biol Chem 284: 27587-27595.
27. Quezada CM, Hicks SW, Galan JE, Stebbins CE, (2009) A family of Salmonella virulence factors functions as a distinct class of autoregulated E3 ubiquitin ligases. Proc Natl Acad Sci U S A 106: 4864-4869.
28. Cirillo DM, Valdivia RH, Monack DM, Falkow S, (1998) Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microbiol 30: 175-188.
29. Waterman SR, Holden DW, (2003) Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol 5: 501-511.
30. Garcia-del Portillo F, Zwick MB, Leung KY, Finlay BB, (1993) Intracellular replication of Salmonella within epithelial cells is associated with filamentous structures containing lysosomal membrane glycoproteins. Infect Agents Dis 2: 227-231.
31. Kuhle V, Hensel M, (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.
32. Beuzon CR, Meresse S, Unsworth KE, Ruiz-Albert J, Garvis S, et al. (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19: 3235-3249.
33. Brumell JH, Tang P, Zaharik ML, Finlay BB, (2002) Disruption of the Salmonella-containing vacuole leads to increased replication of Salmonella enterica serovar typhimurium in the cytosol of epithelial cells. Infect Immun 70: 3264-3270.
34. Schroeder N, Henry T, de Chastellier C, Zhao W, Guilhon AA, et al. (2010) The virulence protein SopD2 regulates membrane dynamics of Salmonella-containing vacuoles. PLoS Pathog 6: e1001002.
35. Ruiz-Albert J, Yu XJ, Beuzon CR, Blakey AN, Galyov EE, et al. (2002) Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane. Mol Microbiol 44: 645-661.
36. Freeman JA, Ohl ME, Miller SI, (2003) The Salmonella enterica serovar typhimurium translocated effectors SseJ and SifB are targeted to the Salmonella-containing vacuole. Infect Immun 71: 418-427.
37. Kuhle V, Jackel D, Hensel M, (2004) Effector proteins encoded by Salmonella pathogenicity island 2 interfere with the microtubule cytoskeleton after translocation into host cells. Traffic 5: 356-370.
38. Poh J, Odendall C, Spanos A, Boyle C, Liu M, et al. (2008) SteC is a Salmonella kinase required for SPI-2-dependent F-actin remodelling. Cell Microbiol 10: 20-30.
39. Dupont N, Temime-Smaali N, Lafont F, (2010) How ubiquitination and autophagy participate in the regulation of the cell response to bacterial infection. Biol Cell 102: 621-634.
40. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, et al. (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282: 24131-24145.
41. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, et al. (2004) Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 36: 585-595.
42. Delgado MA, Elmaoued RA, Davis AS, Kyei G, Deretic V, (2008) Toll-like receptors control autophagy. EMBO J 27: 1110-1121.
43. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, et al. (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4: 151-175.
44. Mizushima N, Yoshimori T, Levine B, (2010) Methods in mammalian autophagy research. Cell 140: 313-326.
45. Coombes BK, Lowden MJ, Bishop JL, Wickham ME, Brown NF, et al. (2007) SseL is a salmonella-specific translocated effector integrated into the SsrB-controlled salmonella pathogenicity island 2 type III secretion system. Infect Immun 75: 574-580.
46. Suzuki S, Tamai K, Watanabe M, Kyuuma M, Ono M, et al. (2011) AMSH is required to degrade ubiquitinated proteins in the central nervous system. Biochem Biophys Res Commun 408: 582-588.
47. Shi CS, Kehrl JH, (2010) TRAF6 and A20 Regulate Lysine 63-Linked Ubiquitination of Beclin-1 to Control TLR4-Induced Autophagy. Sci Signal 3: ra42.
48. Mazurkiewicz P, Thomas J, Thompson JA, Liu M, Arbibe L, et al. (2008) SpvC is a Salmonella effector with phosphothreonine lyase activity on host mitogen-activated protein kinases. Mol Microbiol 67: 1371-1383.
49. Necchi V, Sommi P, Ricci V, Solcia E, (2010) In vivo accumulation of Helicobacter pylori products, NOD1, ubiquitinated proteins and proteasome in a novel cytoplasmic structure. PLoS One 5: e9716.
50. Kaniuk NA, Lam GY, Ma C, Galindo-Mata E, Jones N, et al. (2010) Citrobacter rodentium Infection Induces MyD88-Dependent Formation of Ubiquitinated Protein Aggregates in the Intestinal Epithelium. J Innate Immun 3: 83-98.
51. Sarkar S, Krishna G, Imarisio S, Saiki S, O'Kane CJ, et al. (2008) A rational mechanism for combination treatment of Huntington's disease using lithium and rapamycin. Hum Mol Genet 17: 170-178.
52. Jia K, Hart AC, Levine B, (2007) Autophagy genes protect against disease caused by polyglutamine expansion proteins in Caenorhabditis elegans. Autophagy 3: 21-25.
53. Pierre P, (2005) Dendritic cells, DRiPs, and DALIS in the control of antigen processing. Immunol Rev 207: 184-190.
54. Lelouard H, Ferrand V, Marguet D, Bania J, Camosseto V, et al. (2004) Dendritic cell aggresome-like induced structures are dedicated areas for ubiquitination and storage of newly synthesized defective proteins. J Cell Biol 164: 667-675.
55. Auweter SD, Yu HB, Arena ET, Guttman JA, Finlay BB, (2011) Oxysterol-binding protein (OSBP) enhances replication of intracellular Salmonella and binds the Salmonella SPI-2 effector SseL via its N-terminus. Microbes Infect 14: 148-54.
56. Arena ET, Auweter SD, Antunes LC, Vogl AW, Han J, et al. (2011) The deubiquitinase activity of the Salmonella Pathogenicity Island 2 effector, SseL, prevents accumulation of cellular lipid droplets. Infect Immun 79: 4392-4400.
57. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, et al. (2009) Autophagy regulates lipid metabolism. Nature 458: 1131-1135.
58. Kubori T, Galan JE, (2003) Temporal regulation of salmonella virulence effector function by proteasome-dependent protein degradation. Cell 115: 333-342.
59. Patel JC, Hueffer K, Lam TT, Galan JE, (2009) Diversification of a Salmonella virulence protein function by ubiquitin-dependent differential localization. Cell 137: 283-294.
60. Deiwick J, Nikolaus T, Erdogan S, Hensel M, (1999) Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol 31: 1759-1773.
61. Hensel M, Shea JE, Waterman SR, Mundy R, Nikolaus T, 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.
62. Datsenko KA, Wanner BL, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645.
63. Racoosin EL, Swanson JA, (1989) Macrophage colony-stimulating factor (rM-CSF) stimulates pinocytosis in bone marrow-derived macrophages. J Exp Med 170: 1635-1648.
64. Karlsson K, Carlsson SR, (1998) Sorting of lysosomal membrane glycoproteins lamp-1 and lamp-2 into vesicles distinct from mannose 6-phosphate receptor/gamma-adaptin vesicles at the trans-Golgi network. J Biol Chem 273: 18966-18973.
65. Szeto J, Namolovan A, Osborne SE, Coombes BK, Brumell JH, (2009) Salmonella-containing vacuoles display centrifugal movement associated with cell-to-cell transfer in epithelial cells. Infect Immun 77: 996-1007.
66. Webb JL, Ravikumar B, Atkins J, Skepper JN, Rubinsztein DC, (2003) Alpha-Synuclein is degraded by both autophagy and the proteasome. J Biol Chem 278: 25009-25013.
67. Lossi NS, Rolhion N, Magee AI, Boyle C, Holden DW, (2008) The Salmonella SPI-2 effector SseJ exhibits eukaryotic activator-dependent phospholipase A and glycerophospholipid: cholesterol acyltransferase activity. Microbiology 154: 2680-2688.
68. Valdivia RH, Hromockyj AE, Monack D, Ramakrishnan L, Falkow S, (1996) Applications for green fluorescent protein (GFP) in the study of host-pathogen interactions. Gene 173: 47-52.
69. Slot JW, Geuze HJ, Gigengack S, Lienhard GE, James DE, (1991) Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J Cell Biol 113: 123-135.