Escherichia coli α-Hemolysin Counteracts the Anti-Virulence Innate Immune Response Triggered by the Rho GTPase Activating Toxin CNF1 during Bacteremia

PLoS Pathogens

Volumn 11, Issue 3, 2015, Pages 1-20

  Diabate, Mamady ^a,b,c   Munro, Patrick ^a,b   Garcia, Elsa ^a,b   Jacquel, Arnaud ^a,b   Michel, Gregory ^a,b   Obba, Sandrine ^a,b   Goncalves, Diogo ^a,b   Luci, Carmelo ^b,d   Marchetti, Sandrine ^a,b   Demon, Dieter ^e   Degos, Clara ^f   Bechah, Yassina ^g   Mege, Jean Louis ^g   Lamkanfi, Mohamed ^e   Auberger, Patrick ^a,b   Gorvel, Jean Pierre ^f   Stuart, Lynda Maria ^h   Landraud, Luce ^a,b,c   Lemichez, Emmanuel ^a,b   Boyer, Laurent ^a,b  

^a CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c CENTRE HOSPITALIER UNIVERSITAIRE DE NICE   (France)

^d INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^e GHENT UNIVERSITY   (Belgium)

^f AIX MARSEILLE UNIVERSITY   (France)

^g AIX MARSEILLE UNIVERSITÉ   (France)

^h BENAROYA RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA HEMOLYSIN; ASC PROTEIN; CXCL9 CHEMOKINE; CYTOTOXIC NECROTIZING FACTOR 1; EOTAXIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 2; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MACROPHAGE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN; RAC PROTEIN; RANTES; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG; VIRULENCE FACTOR; BACTERIAL TOXIN; ESCHERICHIA COLI PROTEIN; HEMOLYSIN; HLYA PROTEIN, E COLI;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTEREMIA; BACTERIAL CHROMOSOME; BACTERIAL LOAD; BACTERIAL STRAIN; CONTROLLED STUDY; ENZYME ASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FEMALE; IMMUNOBLOTTING; INNATE IMMUNITY; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; DISEASE MODEL; ESCHERICHIA COLI INFECTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOGENICITY; VIRULENCE;

ESCHERICHIA COLI; MAMMALIA; MUS;

ANIMALS; BACTEREMIA; BACTERIAL TOXINS; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; FEMALE; HEMOLYSIN PROTEINS; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; INTERLEUKIN-1BETA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; VIRULENCE; VIRULENCE FACTORS;

EID: 84926461954     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004732     Document Type: Article

References (53)

1. Martin GS, Mannino DM, Eaton S, Moss M, The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med. 2003; 348: 1546–1554. 12700374
2. Russo TA, Johnson JR, Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J Infect Dis. 2000; 181: 1753–1754. 10823778
3. Wiles TJ, Kulesus RR, Mulvey MA, Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp Mol Pathol. 2008; 85: 11–19. doi: 10.1016/j.yexmp.2008.03.007 18482721
4. Leimbach A, Hacker J, Dobrindt U E, coli as an all-rounder: the thin line between commensalism and pathogenicity. Curr Top Microbiol Immunol. 2013; 358: 3–32. doi: 10.1007/82_2012_303 23340801
5. Hannan TJ, Totsika M, Mansfield KJ, Moore KH, Schembri MA, et al. Host-pathogen checkpoints and population bottlenecks in persistent and intracellular uropathogenic Escherichia coli bladder infection. FEMS Microbiol Rev. 2012; 36: 616–648. doi: 10.1111/j.1574-6976.2012.00339.x 22404313
6. Welch RA, Burland V, Plunkett G, Redford P, Roesch P, et al. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A. 2002; 99: 17020–17024. 12471157
7. Nagy G, Altenhoefer A, Knapp O, Maier E, Dobrindt U, et al. Both alpha-haemolysin determinants contribute to full virulence of uropathogenic Escherichia coli strain 536. Microbes Infect. 2006; 8: 2006–2012. 16787757
8. Alteri CJ, Mobley HL, Escherichia coli physiology and metabolism dictates adaptation to diverse host microenvironments. Curr Opin Microbiol. 2012; 15: 3–9. doi: 10.1016/j.mib.2011.12.004 22204808
9. Dubois D, Delmas J, Cady A, Robin F, Sivignon A, et al. Cyclomodulins in urosepsis strains of Escherichia coli. J Clin Microbiol. 2010; 48: 2122–2129. doi: 10.1128/JCM.02365-09 20375237
10. Smith YC, Rasmussen SB, Grande KK, Conran RM, O'Brien AD Hemolysin of Uropathogenic Escherichia coli Evokes Extensive Shedding of the Uroepithelium and Hemorrhage in Bladder Tissue Within the First 24 Hours After Intraurethral Inoculation of Mice. Infect Immun. 2008;
11. Rippere-Lampe KE, Lang M, Ceri H, Olson M, Lockman HA, et al. Cytotoxic necrotizing factor type 1-positive Escherichia coli causes increased inflammation and tissue damage to the prostate in a rat prostatitis model. Infect Immun. 2001; 69: 6515–6519. 11553597
12. Real JM, Munro P, Buisson-Touati C, Lemichez E, Boquet P, et al. Specificity of immunomodulator secretion in urinary samples in response to infection by alpha-hemolysin and CNF1 bearing uropathogenic Escherichia coli. Cytokine. 2007; 37: 22–25. 17382555
13. Linhartova I, Bumba L, Masin J, Basler M, Osicka R, et al. RTX proteins: a highly diverse family secreted by a common mechanism. FEMS Microbiol Rev. 2010; 34: 1076–1112. doi: 10.1111/j.1574-6976.2010.00231.x 20528947
14. Welch RA Pore-forming cytolysins of gram-negative bacteria. Mol Microbiol. 1991; 5: 521–528. 2046545
15. Bhakdi S, Bayley H, Valeva A, Walev I, Walker B, et al. Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins. Arch Microbiol. 1996; 165: 73–79. 8593102
16. Gadeberg OV, Orskov I, Rhodes JM, Cytotoxic effect of an alpha-hemolytic Escherichia coli strain on human blood monocytes and granulocytes in vitro. Infect Immun. 1983; 41: 358–364. 6345395
17. Gur C, Coppenhagen-Glazer S, Rosenberg S, Yamin R, Enk J, et al. Natural Killer Cell-Mediated Host Defense against Uropathogenic E. coli Is Counteracted by Bacterial HemolysinA-Dependent Killing of NK Cells. Cell Host Microbe. 2013; 14: 664–674. doi: 10.1016/j.chom.2013.11.004 24331464
18. Wiles TJ, Mulvey MA, The RTX pore-forming toxin alpha-hemolysin of uropathogenic Escherichia coli: progress and perspectives. Future Microbiol. 2013; 8: 73–84. doi: 10.2217/fmb.12.131 23252494
19. Landraud L, Gibert M, Popoff MR, Boquet P, Gauthier M, Expression of cnf1 by Escherichia coli J96 involves a large upstream DNA region including the hlyCABD operon, and is regulated by the RfaH protein. Mol Microbiol. 2003; 47: 1653–1667. 12622819
20. Leeds JA, Welch RA, RfaH enhances elongation of Escherichia coli hlyCABD mRNA. J Bacteriol. 1996; 178: 1850–1857. 8606157
21. Aktories K, Barbieri J, Bacterial cytotoxins: targeting eukaryotic switches. Nat Rev Micro. 2005; 3: 397–410. 15821726
22. Galan JE, Common themes in the design and function of bacterial effectors. Cell Host Microbe. 2009; 5: 571–579. doi: 10.1016/j.chom.2009.04.008 19527884
23. Bruno VM, Hannemann S, Lara-Tejero M, Flavell RA, Kleinstein SH, et al. Salmonella Typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog. 2009; 5: e1000538. doi: 10.1371/journal.ppat.1000538 19662166
24. Munro P, Flatau G, Doye A, Boyer L, Oregioni O, et al. Activation and proteasomal degradation of rho GTPases by cytotoxic necrotizing factor-1 elicit a controlled inflammatory response. J Biol Chem. 2004; 279: 35849–35857. 15152002
25. Lemonnier M, Landraud L, Lemichez E, Rho GTPase-activating bacterial toxins: from bacterial virulence regulation to eukaryotic cell biology. FEMS Microbiol Rev. 2007; 31: 515–534. 17680807
26. Boyer L, Magoc L, Dejardin S, Cappillino M, Paquette N, et al. Pathogen-derived effectors trigger protective immunity via activation of the Rac2 enzyme and the IMD or Rip kinase signaling pathway. Immunity. 2011; 35: 536–549. doi: 10.1016/j.immuni.2011.08.015 22018470
27. Keestra AM, Winter MG, Auburger JJ, Frassle SP, Xavier MN, et al. Manipulation of small Rho GTPases is a pathogen-induced process detected by NOD1. Nature. 2013; 496: 233–237. doi: 10.1038/nature12025 23542589
28. Jones JD, Dangl JL, The plant immune system. Nature. 2006; 444: 323–329. 17108957
29. Stuart LM, Paquette N, Boyer L, Effector-triggered versus pattern-triggered immunity: how animals sense pathogens. Nat Rev Immunol. 2013; 13: 199–206. doi: 10.1038/nri3398 23411798
30. Broz P, Monack DM, Molecular mechanisms of inflammasome activation during microbial infections. Immunol Rev. 2011; 243: 174–190. doi: 10.1111/j.1600-065X.2011.01041.x 21884176
31. Keller M, Ruegg A, Werner S, Beer HD, Active caspase-1 is a regulator of unconventional protein secretion. Cell. 2008; 132: 818–831. doi: 10.1016/j.cell.2007.12.040 18329368
32. Kostura MJ, Tocci MJ, Limjuco G, Chin J, Cameron P, et al. Identification of a monocyte specific pre-interleukin 1 beta convertase activity. Proc Natl Acad Sci U S A. 1989; 86: 5227–5231. 2787508
33. Friebel A, Ilchmann H, Aepfelbacher M, Ehrbar K, Machleidt W, et al. SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell. J Biol Chem. 2001; 276: 34035–34040. 11440999
34. Lara-Tejero M, Sutterwala FS, Ogura Y, Grant EP, Bertin J, et al. Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J Exp Med. 2006; 203: 1407–1412. 16717117
35. Muller AJ, Hoffmann C, Galle M, Van Den Broeke A, Heikenwalder M, et al. The S. Typhimurium effector SopE induces caspase-1 activation in stromal cells to initiate gut inflammation. Cell Host Microbe. 2009; 6: 125–136. doi: 10.1016/j.chom.2009.07.007 19683679
36. Dinarello CA, Interleukin-1 beta, interleukin-18, and the interleukin-1 beta converting enzyme. Ann N Y Acad Sci. 1998; 856: 1–11. 9917859
37. Garlanda C, Dinarello CA, Mantovani A, The interleukin-1 family: back to the future. Immunity. 2013; 39: 1003–1018. doi: 10.1016/j.immuni.2013.11.010 24332029
38. Franchi L, Munoz-Planillo R, Nunez G, Sensing and reacting to microbes through the inflammasomes. Nat Immunol. 2012; 13: 325–332. doi: 10.1038/ni.2231 22430785
39. Petrilli V, Dostert C, Muruve DA, Tschopp J, The inflammasome: a danger sensing complex triggering innate immunity. Curr Opin Immunol. 2007; 19: 615–622. 17977705
40. Sansonetti PJ, The innate signaling of dangers and the dangers of innate signaling. Nat Immunol. 2006; 7: 1237–1242. 17110939
41. Vance RE, Isberg RR, Portnoy DA, Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe. 2009; 6: 10–21. doi: 10.1016/j.chom.2009.06.007 19616762
42. Xu H, Yang J, Gao W, Li L, Li P, et al. Innate immune sensing of bacterial modifications of Rho GTPases by the Pyrin inflammasome. Nature. 2014;
43. Wang X, Parashar K, Sitaram A, Bliska JB, The GAP Activity of Type III Effector YopE Triggers Killing of Yersinia in Macrophages. PLoS Pathog. 2014; 10: e1004346. doi: 10.1371/journal.ppat.1004346 25165815
44. Caprioli A, Falbo V, Ruggeri FM, Minelli F, Orskov I, et al. Relationship between cytotoxic necrotizing factor production and serotype in hemolytic Escherichia coli. J Clin Microbiol. 1989; 27: 758–761. 2656748
45. Yamamoto S, Tsukamoto T, Terai A, Kurazono H, Takeda Y, et al. Distribution of virulence factors in Escherichia coli isolated from urine of cystitis patients. Microbiol Immunol. 1995; 39: 401–404. 8551971
46. Finlay BB, McFadden G, Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell. 2006; 124: 767–782. 16497587
47. Pumplin N, Voinnet O, RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat Rev Microbiol. 2013; 11: 745–760. doi: 10.1038/nrmicro3120 24129510
48. Mulvey MA, Schilling JD, Hultgren SJ, Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect Immun. 2001; 69: 4572–4579. 11402001
49. Doye A, Boyer L, Mettouchi A, Lemichez E, Ubiquitin-mediated proteasomal degradation of Rho proteins by the CNF1 toxin. Methods Enzymol. 2006; 406: 447–456. 16472677
50. Lemonnier M, Bouet JY, Libante V, Lane D, Disruption of the F plasmid partition complex in vivo by partition protein SopA. Mol Microbiol. 2000; 38: 493–505. 11069673
51. Jacquel A, Obba S, Boyer L, Dufies M, Robert G, et al. Autophagy is required for CSF-1-induced macrophagic differentiation and acquisition of phagocytic functions. Blood. 2012; 119: 4527–4531. doi: 10.1182/blood-2011-11-392167 22452982
52. Kuida K, Lippke JA, Ku G, Harding MW, Livingston DJ, et al. Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science. 1995; 267: 2000–2003. 7535475
53. Smith SN, Hagan EC, Lane MC, Mobley HL, Dissemination and systemic colonization of uropathogenic Escherichia coli in a murine model of bacteremia. MBio. 2010; 1: