Route of Infection Determines the Impact of Type I Interferons on Innate Immunity to Listeria monocytogenes

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Kernbauer, Elisabeth ^a,c   Maier, Verena ^a   Rauch, Isabella ^a   Müller, Mathias ^b   Decker, Thomas ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERFERON; ALPHA BETA INTERFERON RECEPTOR; IFNAR1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COUNT; BACTERIAL IMMUNITY; CELL DEATH; CONTROLLED STUDY; CYTOKINE PRODUCTION; HEPATITIS; INFLAMMATORY INFILTRATE; INTERFERON PRODUCTION; INTESTINE INFECTION; LETHALITY; LISTERIOSIS; LIVER CELL; MOLECULAR SIZE; MOUSE; NONHUMAN; PERITONITIS; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; FEMALE; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; INTRAPERITONEAL DRUG ADMINISTRATION; INTRAVENOUS DRUG ADMINISTRATION; KNOCKOUT MOUSE; LISTERIA MONOCYTOGENES; MALE; MICROBIOLOGY; PHYSIOLOGY;

ANIMALIA; BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES; MUS;

ANIMALS; CELLS, CULTURED; FEMALE; IMMUNITY, INNATE; INJECTIONS, INTRAPERITONEAL; INJECTIONS, INTRAVENOUS; INTERFERON TYPE I; LISTERIA MONOCYTOGENES; LISTERIOSIS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTOR, INTERFERON ALPHA-BETA; SIGNAL TRANSDUCTION;

EID: 84879199318     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065007     Document Type: Article

References (43)

1. Vazquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Dominguez-Bernal G, et al. (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14: 584-640.
2. Hamon M, Bierne H, Cossart P, (2006) Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol 4: 423-434.
3. Decker T, Muller M, Stockinger S, (2005) The yin and yang of type I interferon activity in bacterial infection. Nat Rev Immunol 5: 675-687.
4. Rauch I, Müller M, Decker T, (2013) The regulation of inflammation by interferons and their STATs. Jak-Stat 96-95.
5. Auerbuch V, Brockstedt DG, Meyer-Morse N, O'Riordan M, Portnoy DA, (2004) Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J Exp Med 200: 527-533.
6. Carrero JA, Calderon B, Unanue ER, (2004) Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J Exp Med 200: 535-540.
7. O'Connell RM, Saha SK, Vaidya SA, Bruhn KW, Miranda GA, et al. (2004) Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J Exp Med 200: 437-445.
8. Zwaferink H, Stockinger S, Hazemi P, Lemmens-Gruber R, Decker T, (2008) IFN-beta increases listeriolysin O-induced membrane permeabilization and death of macrophages. J Immunol 180: 4116-4123.
9. Carrero JA, Calderon B, Unanue ER, (2006) Lymphocytes are detrimental during the early innate immune response against Listeria monocytogenes. J Exp Med 203: 933-940.
10. Dai WJ, Kohler G, Brombacher F, (1997) Both innate and acquired immunity to Listeria monocytogenes infection are increased in IL-10-deficient mice. J Immunol 158: 2259-2267.
11. Rayamajhi M, Humann J, Penheiter K, Andreasen K, Lenz LL, (2010) Induction of IFN-alphabeta enables Listeria monocytogenes to suppress macrophage activation by IFN-gamma. J Exp Med 207: 327-337.
12. Czuprynski CJ, Faith NG, Steinberg H, (2003) A/J mice are susceptible and C57BL/6 mice are resistant to Listeria monocytogenes infection by intragastric inoculation. Infect Immun 71: 682-689.
13. Cossart P, (2011) Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. Proc Natl Acad Sci U S A 108: 19484-19491.
14. Muller U, Steinhoff U, Reis LF, Hemmi S, Pavlovic J, et al. (1994) Functional role of type I and type II interferons in antiviral defense. Science 264: 1918-1921.
15. Arnaud M, Chastanet A, Debarbouille M, (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70: 6887-6891.
16. Chakraborty T, Leimeister-Wachter M, Domann E, Hartl M, Goebel W, et al. (1992) Coordinate regulation of virulence genes in Listeria monocytogenes requires the product of the prfA gene. J Bacteriol 174: 568-574.
17. Wollert T, Pasche B, Rochon M, Deppenmeier S, van den Heuvel J, et al. (2007) Extending the host range of Listeria monocytogenes by rational protein design. Cell 129: 891-902.
18. Lingnau A, Domann E, Hudel M, Bock M, Nichterlein T, et al. (1995) Expression of the Listeria monocytogenes EGD inlA and inlB genes, whose products mediate bacterial entry into tissue culture cell lines, by PrfA-dependent and-independent mechanisms. Infect Immun 63: 3896-3903.
19. Stockinger S, Kastner R, Kernbauer E, Pilz A, Westermayer S, et al. (2009) Characterization of the interferon-producing cell in mice infected with Listeria monocytogenes. PLoS Pathog 5: e1000355.
20. Cabanes D, Lecuit M, Cossart P, (2008) Animal models of Listeria infection. Curr Protoc Microbiol Chapter 9: Unit9B 1.
21. Stockinger S, Reutterer B, Schaljo B, Schellack C, Brunner S, et al. (2004) IFN regulatory factor 3-dependent induction of type I IFNs by intracellular bacteria is mediated by a TLR- and Nod2-independent mechanism. J Immunol 173: 7416-7425.
22. Kernbauer E, Maier V, Stoiber D, Strobl B, Schneckenleithner C, et al. (2012) Conditional Stat1 Ablation Reveals the Importance of Interferon Signaling for Immunity to Listeria monocytogenes Infection. PLoS Pathog 8: e1002763.
23. Monk IR, Casey PG, Hill C, Gahan CG, (2010) Directed evolution and targeted mutagenesis to murinize Listeria monocytogenes internalin A for enhanced infectivity in the murine oral infection model. BMC Microbiol 10: 318.
24. Pron B, Boumaila C, Jaubert F, Berche P, Milon G, et al. (2001) Dendritic cells are early cellular targets of Listeria monocytogenes after intestinal delivery and are involved in bacterial spread in the host. Cell Microbiol 3: 331-340.
25. Niesel DW, Hess CB, Cho YJ, Klimpel KD, Klimpel GR, (1986) Natural and recombinant interferons inhibit epithelial cell invasion by Shigella spp. Infect Immun 52: 828-833.
26. Bukholm G, Berdal BP, Haug C, Degre M, (1984) Mouse fibroblast interferon modifies Salmonella typhimurium infection in infant mice. Infect Immun 45: 62-66.
27. Vadia S, Arnett E, Haghighat AC, Wilson-Kubalek EM, Tweten RK, et al. (2011) The Pore-Forming Toxin Listeriolysin O Mediates a Novel Entry Pathway of L. monocytogenes into Human Hepatocytes. PLoS Pathog 7: e1002356.
28. Huang S, Hendriks W, Althage A, Hemmi S, Bluethmann H, et al. (1993) Immune response in mice that lack the interferon-gamma receptor. Science 259: 1742-1745.
29. Harty JT, Bevan MJ, (1995) Specific immunity to Listeria monocytogenes in the absence of IFN gamma. Immunity 3: 109-117.
30. Reutterer B, Stockinger S, Pilz A, Soulat D, Kastner R, et al. (2008) Type I IFN are host modulators of strain-specific Listeria monocytogenes virulence. Cell Microbiol 10: 1116-1129.
31. Pentecost M, Otto G, Theriot JA, Amieva MR, (2006) Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion. PLoS Pathog 2: e3.
32. Chiba S, Nagai T, Hayashi T, Baba Y, Nagai S, et al. (2011) Listerial invasion protein internalin B promotes entry into ileal Peyer's patches in vivo. Microbiol Immunol 55: 123-129.
33. Pentecost M, Kumaran J, Ghosh P, Amieva MR, (2010) Listeria monocytogenes internalin B activates junctional endocytosis to accelerate intestinal invasion. PLoS Pathog 6: e1000900.
34. Rayamajhi M, Humann J, Kearney S, Hill KK, Lenz LL, (2010) Antagonistic crosstalk between type I and II interferons and increased host susceptibility to bacterial infections. Virulence 1: 418-422.
35. Carrero JA, Unanue ER, (2007) Impact of lymphocyte apoptosis on the innate immune stages of infection. Immunol Res 38: 333-341.
36. Pfeffer K, Matsuyama T, Kundig TM, Wakeham A, Kishihara K, et al. (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.
37. Dalrymple SA, Lucian LA, Slattery R, McNeil T, Aud DM, et al. (1995) Interleukin-6-deficient mice are highly susceptible to Listeria monocytogenes infection: correlation with inefficient neutrophilia. Infect Immun 63: 2262-2268.
38. Pietras EM, Miller LS, Johnson CT, O'Connell RM, Dempsey PW, et al. (2011) A MyD88-dependent IFNgammaR-CCR2 signaling circuit is required for mobilization of monocytes and host defense against systemic bacterial challenge. Cell Res 21: 1068-1079.
39. Gough DJ, Messina NL, Clarke CJ, Johnstone RW, Levy DE, (2012) Constitutive type I interferon modulates homeostatic balance through tonic signaling. Immunity 36: 166-174.
40. Stockinger S, Materna T, Stoiber D, Bayr L, Steinborn R, et al. (2002) Production of type I IFN sensitizes macrophages to cell death induced by Listeria monocytogenes. J Immunol 169: 6522-6529.
41. Navarini AA, Recher M, Lang KS, Georgiev P, Meury S, et al. (2006) Increased susceptibility to bacterial superinfection as a consequence of innate antiviral responses. Proc Natl Acad Sci U S A 103: 15535-15539.
42. Rogers HW, Callery MP, Deck B, Unanue ER, (1996) Listeria monocytogenes induces apoptosis of infected hepatocytes. J Immunol 156: 679-684.
43. Pamer EG, (2004) Immune responses to Listeria monocytogenes. Nat Rev Immunol 4: 812-823.