STING-Dependent Type I IFN Production Inhibits Cell-Mediated Immunity to Listeria monocytogenes

PLoS Pathogens

Volumn 10, Issue 1, 2014, Pages

  Archer, Kristina A ^a   Durack, Juliana ^a   Portnoy, Daniel A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CYCLIC DIADENOSINE PHOSPHATE; DINUCLEOSIDE PHOSPHATE; MEMBRANE PROTEIN; MPYS PROTEIN, MOUSE;

ANIMAL; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LISTERIA MONOCYTOGENES; LISTERIOSIS; MOUSE; PATHOLOGY;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; DINUCLEOSIDE PHOSPHATES; GENE EXPRESSION REGULATION; IMMUNITY, CELLULAR; INTERFERON-BETA; LISTERIA MONOCYTOGENES; LISTERIOSIS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT;

EID: 84893817803     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003861     Document Type: Article

References (59)

1. Harty JT, Tvinnereim AR, White DW, (2000) CD8+ T cell effector mechanisms in resistance to infection. Annual review of immunology 18: 275-308.
2. Pamer EG, (2004) Immune responses to Listeria monocytogenes. Nat Rev Immunol 4: 812-823.
3. Schenten D, Medzhitov R, (2011) The control of adaptive immune responses by the innate immune system. Advances in immunology 109: 87-124.
4. Witte CE, Archer KA, Rae CS, Sauer JD, Woodward JJ, et al. (2012) Innate immune pathways triggered by Listeria monocytogenes and their role in the induction of cell-mediated immunity. Advances in immunology 113: 135-156.
5. Leber JH, Crimmins GT, Raghavan S, Meyer-Morse NP, Cox JS, et al. (2008) Distinct TLR- and NLR-mediated transcriptional responses to an intracellular pathogen. PLoS Pathog 4: e6.
6. Cossart P, Toledo-Arana A, (2008) Listeria monocytogenes, a unique model in infection biology: an overview. Microbes and infection/Institut Pasteur 10: 1041-1050.
7. O'Riordan M, Yi CH, Gonzales R, Lee KD, Portnoy DA, (2002) Innate recognition of bacteria by a macrophage cytosolic surveillance pathway. Proc Natl Acad Sci U S A 99: 13861-13866.
8. Barber GN, (2011) Innate immune DNA sensing pathways: STING, AIMII and the regulation of interferon production and inflammatory responses. Current opinion in immunology 23: 10-20.
9. Barker JR, Koestler BJ, Carpenter VK, Burdette DL, Waters CM, et al. (2013) STING-dependent recognition of cyclic di-AMP mediates type I interferon responses during Chlamydia trachomatis infection. mBio 4: e00018-00013.
10. Zhang X, Shi H, Wu J, Sun L, Chen C, et al. (2013) Cyclic GMP-AMP Containing Mixed Phosphodiester Linkages Is An Endogenous High-Affinity Ligand for STING. Molecular cell 51: 226-235.
11. Burdette DL, Monroe KM, Sotelo-Troha K, Iwig JS, Eckert B, et al. (2011) STING is a direct innate immune sensor of cyclic di-GMP. Nature 478: 515-518.
12. Ishikawa H, Ma Z, Barber GN, (2009) STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461: 788-792.
13. McWhirter SM, Barbalat R, Monroe KM, Fontana MF, Hyodo M, et al. (2009) A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J Exp Med 206: 1899-1911.
14. Crimmins GT, Herskovits AA, Rehder K, Sivick KE, Lauer P, et al. (2008) Listeria monocytogenes multidrug resistance transporters activate a cytosolic surveillance pathway of innate immunity. Proc Natl Acad Sci U S A 105: 10191-10196.
15. Woodward JJ, Iavarone AT, Portnoy DA, (2010) c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328: 1703-1705.
16. Jin L, Hill KK, Filak H, Mogan J, Knowles H, et al. (2011) MPYS is required for IFN response factor 3 activation and type I IFN production in the response of cultured phagocytes to bacterial second messengers cyclic-di-AMP and cyclic-di-GMP. Journal of immunology 187: 2595-2601.
17. Sauer JD, Sotelo-Troha K, von Moltke J, Monroe KM, Rae CS, et al. (2011) The N-Ethyl-N-Nitrosourea-Induced Goldenticket Mouse Mutant Reveals an Essential Function of Sting in the In Vivo Interferon Response to Listeria monocytogenes and Cyclic Dinucleotides. Infect Immun 79: 688-694.
18. Ebensen T, Libanova R, Schulze K, Yevsa T, Morr M, et al. (2011) Bis-(3′,5′)-cyclic dimeric adenosine monophosphate: Strong Th1/Th2/Th17 promoting mucosal adjuvant. Vaccine 29: 5210-5220.
19. Ebensen T, Schulze K, Riese P, Link C, Morr M, et al. (2007) The bacterial second messenger cyclic diGMP exhibits potent adjuvant properties. Vaccine 25: 1464-1469.
20. Karaolis DK, Means TK, Yang D, Takahashi M, Yoshimura T, et al. (2007) Bacterial c-di-GMP is an immunostimulatory molecule. J Immunol 178: 2171-2181.
21. Bahjat KS, Liu W, Lemmens EE, Schoenberger SP, Portnoy DA, et al. (2006) Cytosolic entry controls CD8+-T-cell potency during bacterial infection. Infect Immun 74: 6387-6397.
22. Berche P, Gaillard JL, Sansonetti PJ, (1987) Intracellular growth of Listeria monocytogenes as a prerequisite for in vivo induction of T cell-mediated immunity. J Immunol 138: 2266-2271.
23. von Koenig CH, Finger H, Hof H, (1982) Failure of killed Listeria monocytogenes vaccine to produce protective immunity. Nature 297: 233-234.
24. Harty JT, Bevan MJ, (1995) Specific immunity to Listeria monocytogenes in the absence of IFN gamma. Immunity 3: 109-117.
25. Edelson BT, Unanue ER, (2002) MyD88-dependent but Toll-like receptor 2-independent innate immunity to Listeria: no role for either in macrophage listericidal activity. Journal of immunology 169: 3869-3875.
26. Kursar M, Mittrucker HW, Koch M, Kohler A, Herma M, et al. (2004) Protective T cell response against intracellular pathogens in the absence of Toll-like receptor signaling via myeloid differentiation factor 88. International immunology 16: 415-421.
27. Seki E, Tsutsui H, Tsuji NM, Hayashi N, Adachi K, et al. (2002) Critical roles of myeloid differentiation factor 88-dependent proinflammatory cytokine release in early phase clearance of Listeria monocytogenes in mice. Journal of immunology 169: 3863-3868.
28. Way SS, Kollmann TR, Hajjar AM, Wilson CB, (2003) Cutting edge: protective cell-mediated immunity to Listeria monocytogenes in the absence of myeloid differentiation factor 88. J Immunol 171: 533-537.
29. Chen H, Sun H, You F, Sun W, Zhou X, et al. (2011) Activation of STAT6 by STING is critical for antiviral innate immunity. Cell 147: 436-446.
30. Ishikawa H, Barber GN, (2008) STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455: 674-678.
31. Condotta SA, Richer MJ, Badovinac VP, Harty JT, (2012) Probing CD8 T cell responses with Listeria monocytogenes infection. Advances in immunology 113: 51-80.
32. 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 pathogens 5: e1000355.
33. Keppler SJ, Rosenits K, Koegl T, Vucikuja S, Aichele P, (2012) Signal 3 cytokines as modulators of primary immune responses during infections: the interplay of type I IFN and IL-12 in CD8 T cell responses. PLoS One 7: e40865.
34. Thompson LJ, Kolumam GA, Thomas S, Murali-Krishna K, (2006) Innate inflammatory signals induced by various pathogens differentially dictate the IFN-I dependence of CD8 T cells for clonal expansion and memory formation. J Immunol 177: 1746-1754.
35. 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.
36. Huang L, Lemos HP, Li L, Li M, Chandler PR, et al. (2012) Engineering DNA nanoparticles as immunomodulatory reagents that activate regulatory T cells. Journal of immunology 188: 4913-4920.
37. Huang L, Li L, Lemos H, Chandler PR, Pacholczyk G, et al. (2013) Cutting Edge: DNA Sensing via the STING Adaptor in Myeloid Dendritic Cells Induces Potent Tolerogenic Responses. Journal of immunology 191: 3509-13.
38. Abdullah Z, Schlee M, Roth S, Mraheil MA, Barchet W, et al. (2012) RIG-I detects infection with live Listeria by sensing secreted bacterial nucleic acids. The EMBO journal 31: 4153-4164.
39. Hagmann CA, Herzner AM, Abdullah Z, Zillinger T, Jakobs C, et al. (2013) RIG-I Detects Triphosphorylated RNA of Listeria monocytogenes during Infection in Non-Immune Cells. PLoS One 8: e62872.
40. Brzoza-Lewis KL, Hoth JJ, Hiltbold EM, (2012) Type I interferon signaling regulates the composition of inflammatory infiltrates upon infection with Listeria monocytogenes. Cellular immunology 273: 41-51.
41. Marshall HD, Urban SL, Welsh RM, (2011) Virus-induced transient immune suppression and the inhibition of T cell proliferation by type I interferon. Journal of virology 85: 5929-5939.
42. Ngoi SM, St Rose MC, Menoret AM, Smith DE, Tovey MG, et al. (2012) Presensitizing with a Toll-like receptor 3 ligand impairs CD8 T-cell effector differentiation and IL-33 responsiveness. Proceedings of the National Academy of Sciences of the United States of America 109: 10486-10491.
43. Monroe KM, McWhirter SM, Vance RE, (2010) Induction of type I interferons by bacteria. Cellular microbiology 12: 881-890.
44. 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.
45. 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.
46. Schwartz KT, Carleton JD, Quillin SJ, Rollins SD, Portnoy DA, et al. (2012) Hyperinduction of host beta interferon by a Listeria monocytogenes strain naturally overexpressing the multidrug efflux pump MdrT. Infection and immunity 80: 1537-1545.
47. Wilson EB, Yamada DH, Elsaesser H, Herskovitz J, Deng J, et al. (2013) Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science 340: 202-207.
48. Teijaro JR, Ng C, Lee AM, Sullivan BM, Sheehan KC, et al. (2013) Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science 340: 207-211.
49. Manzanillo PS, Shiloh MU, Portnoy DA, Cox JS, (2012) Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell host & microbe 11: 469-480.
50. Telesca C, Angelico M, Piccolo P, Nosotti L, Morrone A, et al. (2007) Interferon-alpha treatment of hepatitis D induces tuberculosis exacerbation in an immigrant. The Journal of infection 54: e223-226.
51. Berry MP, Graham CM, McNab FW, Xu Z, Bloch SA, et al. (2010) An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466: 973-977.
52. Diner EJ, Burdette DL, Wilson SC, Monroe KM, Kellenberger CA, et al. (2013) The Innate Immune DNA Sensor cGAS Produces a Noncanonical Cyclic Dinucleotide that Activates Human STING. Cell reports 3: 1355-1361.
53. Pearce EL, Shen H, (2007) Generation of CD8 T cell memory is regulated by IL-12. Journal of immunology 179: 2074-2081.
54. Sauer JD, Pereyre S, Archer KA, Burke TP, Hanson B, et al. (2011) Listeria monocytogenes engineered to activate the Nlrc4 inflammasome are severely attenuated and are poor inducers of protective immunity. Proceedings of the National Academy of Sciences of the United States of America 108: 12419-12424.
55. Bahjat KS, Meyer-Morse N, Lemmens EE, Shugart JA, Dubensky TW, et al. (2009) Suppression of cell-mediated immunity following recognition of phagosome-confined bacteria. PLoS pathogens 5: e1000568.
56. Badovinac VP, Porter BB, Harty JT, (2004) CD8+ T cell contraction is controlled by early inflammation. Nature immunology 5: 809-817.
57. Brockstedt DG, Giedlin MA, Leong ML, Bahjat KS, Gao Y, et al. (2004) Listeria-based cancer vaccines that segregate immunogenicity from toxicity. Proc Natl Acad Sci U S A 101: 13832-13837.
58. Witte CE, Whiteley AT, Burke TP, Sauer JD, Portnoy DA, et al. (2013) Cyclic di-AMP Is Critical for Listeria monocytogenes Growth, Cell Wall Homeostasis, and Establishment of Infection. mBio 4: e00282-13.
59. Portnoy DA, Jacks PS, Hinrichs DJ, (1988) Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167: 1459-1471.