Adhesins and Host Serum Factors Drive Yop Translocation by Yersinia into Professional Phagocytes during Animal Infection

PLoS Pathogens

Volumn 9, Issue 6, 2013, Pages

  Maldonado Arocho, Francisco J ^a   Green, Carlos ^b   Fisher, Michael L ^b,c   Paczosa, Michelle K ^b   Mecsas, Joan ^a,b  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Sackler School of Graduate Biomedical Sciences   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; COMPLEMENT; UNCLASSIFIED DRUG; YERSINIA OUTER PROTEIN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; BACTERIAL TRANSLOCATION; BACTERIUM ADHERENCE; HOST CELL; MOUSE; MUTANT; NONHUMAN; PHAGOCYTE; PHAGOCYTOSIS; SERUM FACTOR; SPLEEN CELL; T LYMPHOCYTE; YERSINIA INFECTION; YERSINIA PSEUDOTUBERCULOSIS;

ADHESINS, BACTERIAL; ANIMALS; COMPLEMENT SYSTEM PROTEINS; MICE; PHAGOCYTES; PROTEIN TRANSPORT; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTIONS;

ANIMALIA; BACTERIA (MICROORGANISMS); MUS; YERSINIA; YERSINIA PSEUDOTUBERCULOSIS;

EID: 84879529562     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003415     Document Type: Article

References (65)

1. Mota LJ, Cornelis GR, (2005) The bacterial injection kit: type III secretion systems. Ann Med 37: 234-249.
2. Marketon MM, DePaolo RW, DeBord KL, Jabri B, Schneewind O, (2005) Plague bacteria target immune cells during infection. Science 309: 1739-1741.
3. Durand EA, Maldonado-Arocho FJ, Castillo C, Walsh RL, Mecsas J, (2010) The presence of professional phagocytes dictates the number of host cells targeted for Yop translocation during infection. Cell Microbiol 12: 1064-1082.
4. Köberle M, Klein-Günther A, Schütz M, Fritz M, Berchtold S, et al. (2009) Yersinia enterocolitica targets cells of the innate and adaptive immune system by injection of Yops in a mouse infection model. PLoS Pathog 5: e1000551.
5. Grosdent N, Maridonneau-Parini I, Sory MP, Cornelis GR, (2002) Role of Yops and adhesins in resistance of Yersinia enterocolitica to phagocytosis. Infect Immun 70: 4165-4176.
6. Paquette N, Conlon J, Sweet C, Rus F, Wilson L, et al. (2012) Serine/threonine acetylation of TGFbeta-activated kinase (TAK1) by Yersinia pestis YopJ inhibits innate immune signaling. Proc Natl Acad Sci U S A 109: 12710-12715.
7. Songsungthong W, Higgins MC, Rolan HG, Murphy JL, Mecsas J, (2010) ROS-inhibitory activity of YopE is required for full virulence of Yersinia in mice. Cell Microbiol 12: 988-1001.
8. Trosky JE, Liverman AD, Orth K, (2008) Yersinia outer proteins: Yops. Cell Microbiol 10: 557-565.
9. Viboud GI, Bliska JB, (2005) Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol 59: 69-89.
10. Bliska JB, Copass MC, Falkow S, (1993) The Yersinia pseudotuberculosis adhesin YadA mediates intimate bacterial attachment to and entry into HEp-2 cells. Infect Immun 61: 3914-3921.
11. Mejía E, Bliska JB, Viboud GI, (2008) Yersinia controls type III effector delivery into host cells by modulating Rho activity. PLoS Pathog 4: e3.
12. Kang PJ, Hauser AR, Apodaca G, Fleiszig SM, Wiener-Kronish J, et al. (1997) Identification of Pseudomonas aeruginosa genes required for epithelial cell injury. Mol Microbiol 24: 1249-1262.
13. Kenny B, DeVinney R, Stein M, Reinscheid DJ, Frey EA, et al. (1997) Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91: 511-520.
14. Zahavi EE, Lieberman JA, Donnenberg MS, Nitzan M, Baruch K, et al. (2011) Bundle-forming pilus retraction enhances enteropathogenic Escherichia coli infectivity. Mol Biol Cell 22: 2436-2447.
15. Comolli JC, Hauser AR, Waite L, Whitchurch CB, Mattick JS, et al. (1999) Pseudomonas aeruginosa gene products PilT and PilU are required for cytotoxicity in vitro and virulence in a mouse model of acute pneumonia. Infect Immun 67: 3625-3630.
16. Tsang TM, Felek S, Krukonis ES, (2010) Ail binding to fibronectin facilitates Yersinia pestis binding to host cells and Yop delivery. Infect Immun 78: 3358-3368.
17. Handley SA, Newberry RD, Miller VL, (2005) Yersinia enterocolitica invasin-dependent and invasin-independent mechanisms of systemic dissemination. Infect Immun 73: 8453-8455.
18. Marra A, Isberg RR, (1997) Invasin-dependent and invasin-independent pathways for translocation of Yersinia pseudotuberculosis across the Peyer's patch intestinal epithelium. Infect Immun 65: 3412-3421.
19. Pepe JC, Wachtel MR, Wagar E, Miller VL, (1995) Pathogenesis of defined invasion mutants of Yersinia enterocolitica in a BALB/c mouse model of infection. Infect Immun 63: 4837-4848.
20. Felek S, Krukonis ES, (2009) The Yersinia pestis Ail protein mediates binding and Yop delivery to host cells required for plague virulence. Infect Immun 77: 825-836.
21. Kirjavainen V, Jarva H, Biedzka-Sarek M, Blom AM, Skurnik M, et al. (2008) Yersinia enterocolitica serum resistance proteins YadA and ail bind the complement regulator C4b-binding protein. PLoS Pathog 4: e1000140.
22. Biedzka-Sarek M, Salmenlinna S, Gruber M, Lupas AN, Meri S, et al. (2008) Functional mapping of YadA- and Ail-mediated binding of human factor H to Yersinia enterocolitica serotype O:3. Infect Immun 76: 5016-5027.
23. Miller VL, Falkow S, (1988) Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect Immun 56: 1242-1248.
24. Isberg RR, Voorhis DL, Falkow S, (1987) Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell 50: 769-778.
25. Heise T, Dersch P, (2006) Identification of a domain in Yersinia virulence factor YadA that is crucial for extracellular matrix-specific cell adhesion and uptake. Proc Natl Acad Sci U S A 103: 3375-3380.
26. Han YW, Miller VL, (1997) Reevaluation of the virulence phenotype of the inv yadA double mutants of Yersinia pseudotuberculosis. Infect Immun 65: 327-330.
27. Marra A, Isberg RR, (1996) Analysis of the role of invasin during Yersinia pseudotuberculosis infection of mice. Ann N Y Acad Sci 797: 290-292.
28. Mecsas J, Bilis I, Falkow S, (2001) Identification of attenuated Yersinia pseudotuberculosis strains and characterization of an orogastric infection in BALB/c mice on day 5 postinfection by signature-tagged mutagenesis. Infect Immun 69: 2779-2787.
29. Hudson KJ, Bouton AH, (2006) Yersinia pseudotuberculosis adhesins regulate tissue-specific colonization and immune cell localization in a mouse model of systemic infection. Infect Immun 74: 6487-6490.
30. Barnes PD, Bergman MA, Mecsas J, Isberg RR, (2006) Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine. J Exp Med 203: 1591-1601.
31. Fällman M, Andersson K, Håkansson S, Magnusson KE, Stendahl O, et al. (1995) Yersinia pseudotuberculosis inhibits Fc receptor-mediated phagocytosis in J774 cells. Infect Immun 63: 3117-3124.
32. Lee VT, Mazmanian SK, Schneewind O, (2001) A program of Yersinia enterocolitica type III secretion reactions is activated by specific signals. J Bacteriol 183: 4970-4978.
33. Ricklin D, Hajishengallis G, Yang K, Lambris JD, (2010) Complement: a key system for immune surveillance and homeostasis. Nat Immunol 11: 785-797.
34. Lambris JD, Ricklin D, Geisbrecht BV, (2008) Complement evasion by human pathogens. Nat Rev Microbiol 6: 132-142.
35. Ho DK, Riva R, Skurnik M, Meri S, (2012) The Yersinia pseudotuberculosis outer membrane protein Ail recruits the human complement regulatory protein factor H. J Immunol 189: 3593-3599.
36. Ebanks RO, Isenman DE, (1996) Mouse complement component C4 is devoid of classical pathway C5 convertase subunit activity. Mol Immunol 33: 297-309.
37. Marcus S, Esplin DW, Donaldson DM, (1954) Lack of bactericidal effect of mouse serum on a number of common microorganisms. Science 119: 877.
38. Isberg RR, Barnes P, (2001) Subversion of integrins by enteropathogenic Yersinia. J Cell Sci 114: 21-28.
39. Leo JC, Skurnik M, (2011) Adhesins of human pathogens from the genus Yersinia. Adv Exp Med Biol 715: 1-15.
40. El Tahir Y, Skurnik M, (2001) YadA, the multifaceted Yersinia adhesin. Int J Med Microbiol 291: 209-218.
41. McPhee JB, Mena P, Zhang Y, Bliska JB, (2012) Interleukin-10 induction is an important virulence function of the Yersinia pseudotuberculosis type III effector YopM. Infect Immun 80: 2519-2527.
42. Simonet M, Falkow S, (1992) Invasin expression in Yersinia pseudotuberculosis. Infect Immun 60: 4414-4417.
43. Eitel J, Dersch P, (2002) The YadA protein of Yersinia pseudotuberculosis mediates high-efficiency uptake into human cells under environmental conditions in which invasin is repressed. Infect Immun 70: 4880-4891.
44. Harmon DE, Davis AJ, Castillo C, Mecsas J, (2010) Identification and characterization of small-molecule inhibitors of Yop translocation in Yersinia pseudotuberculosis. Antimicrob Agents Chemother 54: 3241-3254.
45. Zlokarnik G, Negulescu PA, Knapp TE, Mere L, Burres N, et al. (1998) Quantitation of transcription and clonal selection of single living cells with beta-lactamase as reporter. Science 279: 84-88.
46. Hakansson S, Schesser K, Persson C, Galyov EE, Rosqvist R, et al. (1996) The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J 15: 5812-5823.
47. Akopyan K, Edgren T, Wang-Edgren H, Rosqvist R, Fahlgren A, et al. (2011) Translocation of surface-localized effectors in type III secretion. Proc Natl Acad Sci U S A 108: 1639-1644.
48. Bartra SS, Styer KL, O'Bryant DM, Nilles ML, Hinnebusch BJ, et al. (2008) Resistance of Yersinia pestis to complement-dependent killing is mediated by the Ail outer membrane protein. Infect Immun 76: 612-622.
49. Shapiro S, Beenhouwer DO, Feldmesser M, Taborda C, Carroll MC, et al. (2002) Immunoglobulin G monoclonal antibodies to Cryptococcus neoformans protect mice deficient in complement component C3. Infect Immun 70: 2598-2604.
50. Vogel CW, Fritzinger DC, (2010) Cobra venom factor: Structure, function, and humanization for therapeutic complement depletion. Toxicon 56: 1198-1222.
51. Rosso ML, Chauvaux S, Dessein R, Laurans C, Frangeul L, et al. (2008) Growth of Yersinia pseudotuberculosis in human plasma: impacts on virulence and metabolic gene expression. BMC Microbiol 8: 211.
52. Pisano F, Kochut A, Uliczka F, Geyer R, Stolz T, et al. (2012) In vivo-induced InvA-like autotransporters Ifp and InvC of Yersinia pseudotuberculosis promote interactions with intestinal epithelial cells and contribute to virulence. Infect Immun 80: 1050-1064.
53. Kim J, Ahn K, Min S, Jia J, Ha U, et al. (2005) Factors triggering type III secretion in Pseudomonas aeruginosa. Microbiology 151: 3575-3587.
54. Menard R, Sansonetti P, Parsot C, (1994) The secretion of the Shigella flexneri Ipa invasins is activated by epithelial cells and controlled by IpaB and IpaD. EMBO J 13: 5293-5302.
55. Zierler MK, Galan JE, (1995) Contact with cultured epithelial cells stimulates secretion of Salmonella typhimurium invasion protein InvJ. Infect Immun 63: 4024-4028.
56. Kolodziejek AM, Schnider DR, Rohde HN, Wojtowicz AJ, Bohach GA, et al. (2010) Outer membrane protein X (Ail) contributes to Yersinia pestis virulence in pneumonic plague and its activity is dependent on the lipopolysaccharide core length. Infect Immun 78: 5233-5243.
57. Hinnebusch BJ, Jarrett CO, Callison JA, Gardner D, Buchanan SK, et al. (2011) Role of the Yersinia pestis Ail protein in preventing a protective polymorphonuclear leukocyte response during bubonic plague. Infect Immun 79: 4984-4989.
58. Crimmins GT, Mohammadi S, Green ER, Bergman MA, Isberg RR, et al. (2012) Identification of MrtAB, an ABC transporter specifically required for Yersinia pseudotuberculosis to colonize the mesenteric lymph nodes. PLoS Pathog 8: e1002828.
59. Logsdon LK, Mecsas J, (2006) The proinflammatory response induced by wild-type Yersinia pseudotuberculosis infection inhibits survival of yop mutants in the gastrointestinal tract and Peyer's patches. Infect Immun 74: 1516-1527.
60. Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, et al. (2012) Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med 18: 1386-1393.
61. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, et al. (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535.
62. McDonald B, Urrutia R, Yipp BG, Jenne CN, Kubes P, (2012) Intravascular Neutrophil Extracellular Traps Capture Bacteria from the Bloodstream during Sepsis. Cell Host Microbe 12: 324-333.
63. Bergman MA, Loomis WP, Mecsas J, Starnbach MN, Isberg RR, (2009) CD8(+) T cells restrict Yersinia pseudotuberculosis infection: bypass of anti-phagocytosis by targeting antigen-presenting cells. PLoS Pathog 5: e1000573.
64. Balada-Llasat JM, Mecsas J, (2006) Yersinia has a tropism for B and T cell zones of lymph nodes that is independent of the type III secretion system. PLoS Pathog 2: e86.
65. Casutt-Meyer S, Renzi F, Schmaler M, Jann NJ, Amstutz M, et al. (2010) Oligomeric coiled-coil adhesin YadA is a double-edged sword. PLoS One 5: e15159.