Yersinia enterocolitica targets cells of the innate and adaptive immune system by injection of Yops in a mouse infection model

PLoS Pathogens

Volumn 5, Issue 8, 2009, Pages

  Köberle, Martin ^a   Klein Günther, Annegret ^a   Schütz, Monika ^a   Fritz, Michaela ^a   Berchtold, Susanne ^a   Tolosa, Eva ^b,c   Autenrieth, Ingo B ^a   Bohn, Erwin ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2 INTEGRIN; BETA LACTAMASE; BETA1 INTEGRIN; CD19 ANTIGEN; CD23 ANTIGEN; CD3 ANTIGEN; CD69 ANTIGEN; COMPLEMENT COMPONENT C3D RECEPTOR; FLUORESCENT DYE; GAMMA INTERFERON RECEPTOR; GLYCOPROTEIN P 15095; HYBRID PROTEIN; PROTEIN P55; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR; YERSINIA OUTER PROTEIN E; OUTER MEMBRANE PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; BACTERIAL STRAIN; CELL CULTURE; CONTROLLED STUDY; DENDRITIC CELL; EPITHELIUM CELL; HUMAN; HUMAN CELL; INNATE IMMUNITY; LEUKOCYTE; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; SPLEEN; SPLEEN CELL; TARGET CELL; YERSINIA ENTEROCOLITICA; YERSINIOSIS; ANIMAL; C57BL MOUSE; CELL LINE; DISEASE MODEL; FEMALE; GENE SILENCING; GENETICS; HELA CELL; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MALE; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; PATHOGENICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; YERSINIA INFECTION;

MUS; YERSINIA; YERSINIA ENTEROCOLITICA;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; CELL LINE, TRANSFORMED; DISEASE MODELS, ANIMAL; FEMALE; GENE SILENCING; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; LEUKOCYTES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; YERSINIA ENTEROCOLITICA; YERSINIA INFECTIONS;

EID: 70049090384     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000551     Document Type: Article

References (67)

1. Smego RA, Frean J, Koornhof HJ (1999) Yersiniosis I: microbiological and clinicoepidemiological aspects of plague and non-plague Yersinia infections. Eur J Clin Microbiol Infect Dis 18: 1-15. (Pubitemid 29531147)
2. Koornhof HJ, Smego RA Jr, Nicol M (1999) Yersiniosis. II: The pathogenesis of Yersinia infections. Eur J Clin Microbiol Infect Dis 18: 87-112.
3. Cornelis GR (2002) Yersinia type III secretion: send in the effectors. J Cell Biol 158: 401-408. (Pubitemid 34851697)
4. Hueck CJ (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379-433. (Pubitemid 28270280)
5. Cornelis GR (2006) The type III secretion injectisome. Nat Rev Microbiol 4: 811-825.
6. Galan JE, Wolf-Watz H (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444: 567-573.
7. Edqvist PJ, Aili M, Liu J, Francis MS (2007) Minimal YopB and YopD translocator secretion by Yersinia is sufficient for Yop-effector delivery into target cells. Microbes Infect 9: 224-233. (Pubitemid 46228004)
8. Hakansson S, Bergman T, Vanooteghem JC, Cornelis G, Wolf Watz H (1993) YopB and YopD constitute a novel class of Yersinia Yop proteins. Infect Immun 61: 71-80. (Pubitemid 23015401)
9. Trulzsch K, Sporleder T, Igwe EI, Russmann H, Heesemann J (2004) Contribution of the major secreted yops of Yersinia enterocolitica O:8 to pathogenicity in the mouse infection model. Infect Immun 72: 5227-5234. (Pubitemid 39223408)
10. Boland A, Cornelis GR (1998) Role of YopP in suppression of tumor necrosis factor alpha release by macrophages during Yersinia infection. Infect Immun 66: 1878-1884. (Pubitemid 28194077)
11. Mukherjee S, Keitany G, Li Y, Wang Y, Ball HL, Goldsmith EJ, Orth K (2006) Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312: 1211-1214. (Pubitemid 43801146)
12. Thiefes A, Wolf A, Doerrie A, Grassl GA, Matsumoto K, Autenrieth I, Bohn E, Sakurai H, Niedenthal R, Resch K, Kracht M (2006) The Yersinia enterocolitica effector YopP inhibits host cell signalling by inactivating the protein kinase TAK1 in the IL-1 signalling pathway. EMBO Rep 7: 838-844. (Pubitemid 44275404)
13. Mittal R, Peak-Chew SY, McMahon HT (2006) Acetylation of MEK2 and I kappa B kinase (IKK) activation loop residues by YopJ inhibits signaling. Proc Natl Acad Sci U S A 103: 18574-18579. (Pubitemid 44913452)
14. Orth K, Xu Z, Mudgett MB, Bao ZQ, Palmer LE, Bliska JB, Mangel WF, Staskawicz B, Dixon JE (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290: 1594-1597.
15. Autenrieth SE, Soldanova I, Rosemann R, Gunst D, Zahir N, Kracht M, Ruckdeschel K, Wagner H, Borgmann S, Autenrieth IB (2007) Yersinia enterocolitica YopP inhibits MAP kinase-mediated antigen uptake in dendritic cells. Cell Microbiol 9: 425-437. (Pubitemid 46092169)
16. Bohn E, Muller S, Lauber J, Geffers R, Speer N, Spieth C, Krejci J, Manncke B, Buer J, Zell A, Autenrieth IB (2004) Gene expression patterns of epithelial cells modulated by pathogenicity factors of Yersinia enterocolitica. Cell Microbiol 6: 129-141. (Pubitemid 38111594)
17. Erfurth SE, Grobner S, Kramer U, Gunst DS, Soldanova I, Schaller M, Autenrieth IB, Borgmann S (2004) Yersinia enterocolitica induces apoptosis and inhibits surface molecule expression and cytokine production in murine dendritic cells. Infect Immun 72: 7045-7054. (Pubitemid 39552374)
18. Denecker G, Declercq W, Geuijen CA, Boland A, Benabdillah R, van Gurp M, Sory MP, Vandenabeele P, Cornelis GR (2001) Yersinia enterocolitica YopP-induced apoptosis of macrophages involves the apoptotic signaling cascade upstream of bid. J Biol Chem 276: 19706-19714. (Pubitemid 37411028)
19. Gröbner S, Autenrieth SE, Soldanova I, Gunst DS, Schaller M, Bohn E, Muller S, Leverkus M, Wesselborg S, Autenrieth IB, Borgmann S (2006) Yersinia YopP-induced apoptotic cell death in murine dendritic cells is partially independent from action of caspases and exhibits necrosis-like features. (2006) Yersinia YopP-induced apoptotic cell death in murine dendritic cells is partially independent from action of caspases and exhibits necrosis-like features. Apoptosis 11: 1959-1968.
20. Ruckdeschel K, Mannel O, Richter K, Jacobi CA, Trulzsch K, Rouot B, Heesemann J (2001) Yersinia outer protein P of Yersinia enterocolitica simultaneously blocks the nuclear factor-kappa B pathway and exploits lipopolysaccharide signaling to trigger apoptosis in macrophages. J Immunol 166: 1823-1831. (Pubitemid 32114668)
21. Viboud GI, Bliska JB (2005) Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol 59: 69-89.
22. Gerke C, Falkow S, Chien YH (2005) The adaptor molecules LAT and SLP-76 are specifically targeted by Yersinia to inhibit T cell activation. J Exp Med 201: 361-371. (Pubitemid 40229411)
23. Alonso A, Bottini N, Bruckner S, Rahmouni S, Williams S, Schoenberger SP, Mustelin T (2004) Lck dephosphorylation at Tyr-394 and inhibition of T cell antigen receptor signaling by Yersinia phosphatase YopH. J Biol Chem 279: 4922-4928. (Pubitemid 38199088)
24. McDonald C, Vacratsis PO, Bliska JB, Dixon JE (2003) The Yersinia virulence factor YopM forms a novel protein complex with two cellular kinases. J Biol Chem. (Pubitemid 36799476)
25. Aili M, Telepnev M, Hallberg B, Wolf-Watz H, Rosqvist R (2003) In vitro GAP activity towards RhoA, Rac1 and Cdc42 is not a prerequisite for YopE induced HeLa cell cytotoxicity. Microb Pathog 34: 297-308.
26. Jacobi CA, Roggenkamp A, Rakin A, Zumbihl R, Leitritz L, Heesemann J (1998) In vitro and in vivo expression studies of yopE from Yersinia enterocolitica using the gfp reporter gene. Mol Microbiol 30: 865-882.
27. Sory MP, Boland A, Lambermont I, Cornelis GR (1995) Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc Natl Acad Sci U S A 92: 11998-12002. (Pubitemid 26013998)
28. Day JB, Ferracci F, Plano GV (2003) Injection of YopE and YopN into eukaryotic cells by Yersinia pestis yopN, tyeA, sycN, yscB and lcrG deletion mutants measured using a phosphorylatable peptide tag and phosphospecific antibodies. Mol Microbiol 47: 807-823. (Pubitemid 36114987)
29. Briones G, Hofreuter D, Galan JE (2006) Cre reporter system to monitor the injection of type III secreted proteins into host cells. Infect Immun 74: 1084-1090. (Pubitemid 43185545)
30. Marketon MM, DePaolo RW, DeBord KL, Jabri B, Schneewind O (2005) Plague bacteria target immune cells during infection. Science 309: 1739-1741. (Pubitemid 41285946)
31. Charpentier X, Oswald E (2004) Identification of the secretion and injection domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescence-based reporter. J Bacteriol 186: 5486-5495. (Pubitemid 39038151)
32. Geddes K, Cruz F, Heffron F (2007) Analysis of cells targeted by Salmonella type III secretion in vivo. PLoS Pathog 3: e196. doi:10.1371/journal. -ppat.0030196.
33. Zlokarnik G, Negulescu PA, Knapp TE, Mere L, Burres N, Feng L, Whitney M, Roemer K, Tsien RY (1998) Quantitation of transcription and clonal selection of single living cells with beta-lactamase as reporter. Science 279: 84-88. (Pubitemid 28079160)
34. Schmid Y, Grassl GA, Buhler OT, Skurnik M, Autenrieth IB, Bohn E (2004) Yersinia enterocolitica adhesin A induces production of interleukin-8 in epithelial cells. Infect Immun 72: 6780-6789. (Pubitemid 39552345)
35. Mejia E, Bliska JB, Viboud GI (2008) Yersinia controls type III effector delivery into host cells by modulating Rho activity. PLoS Pathog 4: e3. doi:10.1371/journal.ppat.0040003. (Pubitemid 351230889)
36. Autenrieth IB, Beer M, Bohn E, Kaufmann SHE, Heesemann J (1994) Immune responses to Yersinia enterocolitica in susceptible BALB/c and resistant C57BL/6 mice: an essential role for gamma interferon. Infect Immun 62: 2590-2599. (Pubitemid 24157094)
37. Autenrieth IB, Heesemann J (1992) In vivo neutralization of tumor necrosis factor alpha and interferon-gamma abrogates resistance to Yersinia enterocolitica in mice. Med Microbiol Immunol 181: 333-338.
38. Bohn E, Autenrieth IB (1996) IL-12 is essential for resistance against Yersinia enterocolitica by triggering IFN-gamma production in NK cells and CD4+ T cells. J Immunol 156: 1458-1468. (Pubitemid 26065856)
39. Bohn E, Schmitt E, Bielfeldt C, Noll A, Schulte R, et al. (1998) Ambiguous role of interleukin-12 in Yersinia enterocolitica infection in susceptible and resistant mouse strains. Infect Immun 66: 2213-2220. (Pubitemid 28194123)
40. Di Genaro MS, Waidmann M, Kramer U, Hitziger N, Bohn E, Autenrieth IB (2003) Attenuated Yersinia enterocolitica mutant strains exhibit differential virulence in cytokine-deficient mice: implications for the development of novel live carrier vaccines. Infect Immun 71: 1804-1812. (Pubitemid 36368709)
41. 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. (Pubitemid 34907296)
42. Isberg RR, Leong JM (1990) Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Immunity 60: 861-871. (Pubitemid 20086898)
43. Schulte R, Grassl GA, Preger S, Fessele S, Jacobi CA, Schaller M, Nelson PJ, Autenrieth IB (2000) Yersinia enterocolitica invasin protein triggers IL-8 production in epithelial cells via activation of Rel p65-p65 homodimers. FASEB J 2000 Aug ;14 (11):1471-84 14: 1471-1484. (Pubitemid 30636552)
44. Movilla N, Dosil M, Zheng Y, Bustelo XR (2001) How Vav proteins discriminate the GTPases Rac1 and RhoA from Cdc42. Oncogene 20: 8057-8065. (Pubitemid 34028330)
45. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y (2004) Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci U S A 101: 7618-7623. (Pubitemid 38658078)
46. Carniel E (2001) The Yersinia high-pathogenicity island: an iron-uptake island. Microbes Infect 3: 561-569.
47. Carniel E, Mercereau Puijalon O, Bonnefoy S (1989) The gene coding for the 190,000-dalton iron-regulated protein of Yersinia species is present only in the highly pathogenic strains. Infect Immun 57: 1211-1217. (Pubitemid 19087869)
48. Robins-Browne RM, Prpic JK (1985) Effects of iron and desferrioxamine on infections with Yersinia enterocolitica. Infect Immun 47: 774-779. (Pubitemid 15075874)
49. Gripenberg-Lerche C, Zhang L, Ahtonen P, Toivanen P, Skurnik M (2000) Construction of urease-negative mutants of Yersinia enterocolitica serotypes O:3 and o:8: role of urease in virulence and arthritogenicity. Infect Immun 68: 942-947. (Pubitemid 30056558)
50. Lee VT, Schneewind O (1999) Type III machines of pathogenic yersiniae secrete virulence factors into the extracellular milieu. Mol Microbiol 31: 1619-1629.
51. Ewald JH, Heesemann J, Rüdiger H, Autenrieth IB (1994) Interaction of polymorphonuclear leukocytes with Yersinia enterocolitica: role of the Yersinia virulence plasmid and modulation by the iron-chelator desferrioxamine B. J Infect Dis 170: 140-150. (Pubitemid 24186437)
52. Autenrieth IB, Bohn E, Ewald JH, Heesemann J (1995) Deferoxamine B but not deferoxamine G1 inhibits cytokine production in murine bone marrow macrophages. J Infect Dis 172: 490-496.
53. Allman D, Pillai S (2008) Peripheral B cell subsets. Curr Opin Immunol 20: 149-157.
54. 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. doi:10.1371/journal.ppat.0020086.
55. Oellerich MF, Jacobi CA, Freund S, Niedung K, Bach A, et al. (2007) Yersinia enterocolitica infection of mice reveals clonal invasion and abscess formation. Infect Immun 75: 3802-3811. (Pubitemid 47206277)
56. Adkins I, Köberle M, Grobner S, Bohn E, Autenrieth IB, Borgmann S (2007) Yersinia outer proteins E, H, P, and T differentially target the cytoskeleton and inhibit phagocytic capacity of dendritic cells. Int J Med Microbiol 297: 235-244. (Pubitemid 46830041)
57. Strauch E, Voigt I, Broll H, Appel B (2000) Use of a plasmid of a yersinia enterocolitica biogroup 1A strain for the construction of cloning vectors. J Biotechnol 79: 63-72. (Pubitemid 30160717)
58. Wiedig CA, Kramer U, Garbom S, Wolf-Watz H, Autenrieth IB (2005) Induction of CD8+ T cell responses by Yersinia vaccine carrier strains. Vaccine 23: 4984-4998. (Pubitemid 41267027)
59. Sarker MR, Carman RJ, McClane BA (1999) Inactivation of the gene (cpe) encoding Clostridium perfringens enterotoxin eliminates the ability of two cpe-positive C. perfringens type A human gastrointestinal disease isolates to affect rabbit ileal loops. Mol Microbiol 33: 946-958.
60. Heesemann J (1987) Chromosomal-encoded siderophores are required for mouse virulence of enteropathogenic Yersinia species. FEMS Microbiol Lett 48: 229-233.
61. Woestyn S, Allaoui A, Wattiau P, Cornelis GR (1994) YscN, the putative energizer of the Yersinia Yop secretion machinery. J Bacteriol 176: 1561-1569. (Pubitemid 24100204)
62. Heesemann J, Gross U, Schmidt N, Laufs R (1986) Immunochemical analysis of plasmid-encoded proteins released by enteropathogenic Yersinia sp. grown in calcium-deficient media. Infect Immun 54: 561-567. (Pubitemid 17171474)
63. Fässler R, Pfaff M, Murphy J, Noegel AA, Johansson S, Timpl R, Albrcht R (1995) Lack of beta 1 integrin gene in embryonic stem cells affects morphology, adhesion, and migration but not integration into the inner cell mass of blastocysts. J Cell Biol 128: 979-988.
64. Wennerberg K, Lohikangas L, Gullberg D, Pfaff M, Johansson S, Fässler R (1996) Beta 1 integrin-dependent and -independent polymerization of fibronectin. J Cell Biol 132: 227-238. (Pubitemid 26035087)
65. Pfaffl MW (2001) A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res 29: e45.
66. Pfeffer K, Matsuyama T, Kundig TM, Wakeham A, Kishihara K, Shahinian A, Wiegmann K, Ohashi PS, Krönke M, Mak TW (1993) Mice deficient for the 55 Kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell 73: 457-467. (Pubitemid 23143346)
67. Huang S, Hendriks W, Althage A, Hemmi S, Bluethmann H, Kamijo R, Vilcek J, Zinkernagel RM, Aguet M (1993) Immune response in mice that lack the interferon-gamma receptor [see comments]. Science 259: 1742-1745. (Pubitemid 23114659)