Streptococcal M protein promotes IL-10 production by cGAS-independent activation of the STING signaling pathway

PLoS Pathogens

Volumn 14, Issue 3, 2018, Pages

  Movert, Elin ^a   Lienard, Julia ^a   Valfridsson, Christine ^a   Nordström, Therése ^b,c   Johansson Lindbom, Bengt ^a   Carlsson, Fredric ^a,b  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c MALMÖ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; BACTERIAL PROTEIN; BETA INTERFERON; FIBRINOGEN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; MYELOID DIFFERENTIATION FACTOR 88; STREPTOCOCCAL M PROTEIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; CARRIER PROTEIN; INTERFERON; MB21D1 PROTEIN, MOUSE; MEMBRANE PROTEIN; MPYS PROTEIN, MOUSE; NUCLEOTIDYLTRANSFERASE; OUTER MEMBRANE PROTEIN;

ANIMAL CELL; ARTICLE; BACTERIAL GENE; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; INFLAMMATION; MACROPHAGE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RADIOIMMUNOASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SORTASE A GENE; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; GENETICS; HOST PATHOGEN INTERACTION; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; MOUSE; PHYSIOLOGY; STREPTOCOCCUS INFECTION; STREPTOCOCCUS PYOGENES;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; CARRIER PROTEINS; CELLS, CULTURED; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; INTERFERON TYPE I; INTERLEUKIN-10; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; NUCLEOTIDYLTRANSFERASES; SIGNAL TRANSDUCTION; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES;

EID: 85044824499     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006969     Document Type: Article

References (55)

1. Carapetis JR, Steer AC, Mulholland EK, Weber M, The global burden of group A streptococcal diseases. Lancet Infect Dis. 2005;5(11):685–94. doi: 10.1016/S1473-3099(05)70267-X 16253886
2. Smeesters PR, McMillan DJ, Sriprakash KS, The streptococcal M protein: a highly versatile molecule. Trends Microbiol. 2010;18(6):275–82. doi: 10.1016/j.tim.2010.02.007 20347595
3. Cunningham MW, Pathogenesis of group A streptococcal infections. Clin Microbiol Rev. 2000;13(3):470–511. 10885988
4. Mosser DM, Edwards JP, Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008;8(12):958–69. doi: 10.1038/nri2448 19029990
5. Goldmann O, Lengeling A, Bose J, Bloecker H, Geffers R, Chhatwal GS, et al. The role of the MHC on resistance to group a streptococci in mice. J Immunol. 2005;175(6):3862–72. 16148132
6. Goldmann O, Rohde M, Chhatwal GS, Medina E, Role of macrophages in host resistance to group A streptococci. Infect Immun. 2004;72(5):2956–63. doi: 10.1128/IAI.72.5.2956-2963.2004 15102808
7. Evans TJ, The role of macrophages in septic shock. Immunobiology. 1996;195(4–5):655–9. doi: 10.1016/S0171-2985(96)80029-5 8933164
8. Goldmann O, von Kockritz-Blickwede M, Holtje C, Chhatwal GS, Geffers R, Medina E, Transcriptome analysis of murine macrophages in response to infection with Streptococcus pyogenes reveals an unusual activation program. Infect Immun. 2007;75(8):4148–57. doi: 10.1128/IAI.00181-07 17526748
9. Kole A, He J, Rivollier A, Silveira DD, Kitamura K, Maloy KJ, et al. Type I IFNs regulate effector and regulatory T cell accumulation and anti-inflammatory cytokine production during T cell-mediated colitis. J Immunol. 2013;191(5):2771–9. doi: 10.4049/jimmunol.1301093 23913971
10. Lienard J, Movert E, Valfridsson C, Sturegard E, Carlsson F, ESX-1 exploits type I IFN-signalling to promote a regulatory macrophage phenotype refractory to IFNgamma-mediated autophagy and growth restriction of intracellular mycobacteria. Cell Microbiol. 2016;18(10):1471–85. doi: 10.1111/cmi.12594 27062290
11. McNab FW, Ewbank J, Howes A, Moreira-Teixeira L, Martirosyan A, Ghilardi N, et al. Type I IFN induces IL-10 production in an IL-27-independent manner and blocks responsiveness to IFN-gamma for production of IL-12 and bacterial killing in Mycobacterium tuberculosis-infected macrophages. J Immunol. 2014;193(7):3600–12. doi: 10.4049/jimmunol.1401088 25187652
12. Teles RM, Graeber TG, Krutzik SR, Montoya D, Schenk M, Lee DJ, et al. Type I interferon suppresses type II interferon-triggered human anti-mycobacterial responses. Science. 2013;339(6126):1448–53. doi: 10.1126/science.1233665 23449998
13. Gratz N, Hartweger H, Matt U, Kratochvill F, Janos M, Sigel S, et al. Type I interferon production induced by Streptococcus pyogenes-derived nucleic acids is required for host protection. PLoS Pathog. 2011;7(5):e1001345. doi: 10.1371/journal.ppat.1001345 21625574
14. Castiglia V, Piersigilli A, Ebner F, Janos M, Goldmann O, Dambock U, et al. Type I Interferon Signaling Prevents IL-1beta-Driven Lethal Systemic Hyperinflammation during Invasive Bacterial Infection of Soft Tissue. Cell Host Microbe. 2016;19(3):375–87. doi: 10.1016/j.chom.2016.02.003 26962946
15. Carlsson F, Sandin C, Lindahl G, Human fibrinogen bound to Streptococcus pyogenes M protein inhibits complement deposition via the classical pathway. Mol Microbiol. 2005;56(1):28–39. doi: 10.1111/j.1365-2958.2005.04527.x 15773976
16. Sandin C, Carlsson F, Lindahl G, Binding of human plasma proteins to Streptococcus pyogenes M protein determines the location of opsonic and non-opsonic epitopes. Mol Microbiol. 2006;59(1):20–30. doi: 10.1111/j.1365-2958.2005.04913.x 16359315
17. Areschoug T, Waldemarsson J, Gordon S, Evasion of macrophage scavenger receptor A-mediated recognition by pathogenic streptococci. Eur J Immunol. 2008;38(11):3068–79. doi: 10.1002/eji.200838457 18924218
18. Whitnack E, Beachey EH, Inhibition of complement-mediated opsonization and phagocytosis of Streptococcus pyogenes by D fragments of fibrinogen and fibrin bound to cell surface M protein. J Exp Med. 1985;162(6):1983–97. 3906018
19. Svensson C, Klementsson H, Andersson M, Pipkorn U, Alkner U, Persson CG, Glucocorticoid-induced attenuation of mucosal exudation of fibrinogen and bradykinins in seasonal allergic rhinitis. Allergy. 1994;49(3):177–83. 8198250
20. Loof TG, Goldmann O, Gessner A, Herwald H, Medina E, Aberrant inflammatory response to Streptococcus pyogenes in mice lacking myeloid differentiation factor 88. Am J Pathol. 2010;176(2):754–63. doi: 10.2353/ajpath.2010.090422 20019195
21. Lawrence T, Natoli G, Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol. 2011;11(11):750–61. doi: 10.1038/nri3088 22025054
22. Diner EJ, Burdette DL, Wilson SC, Monroe KM, Kellenberger CA, Hyodo M, et al. The innate immune DNA sensor cGAS produces a noncanonical cyclic dinucleotide that activates human STING. Cell Rep. 2013;3(5):1355–61. doi: 10.1016/j.celrep.2013.05.009 23707065
23. Suschak JJ, Wang S, Fitzgerald KA, Lu S, A cGAS-Independent STING/IRF7 Pathway Mediates the Immunogenicity of DNA Vaccines. J Immunol. 2016;196(1):310–6. doi: 10.4049/jimmunol.1501836 26590319
24. Vance RE, Cytosolic DNA Sensing: The Field Narrows. Immunity. 2016;45(2):227–8. doi: 10.1016/j.immuni.2016.08.006 27533006
25. Gray EE, Winship D, Snyder JM, Child SJ, Geballe AP, Stetson DB, The AIM2-like Receptors Are Dispensable for the Interferon Response to Intracellular DNA. Immunity. 2016;45(2):255–66. doi: 10.1016/j.immuni.2016.06.015 27496731
26. Chen Q, Sun L, Chen ZJ, Regulation and function of the cGAS-STING pathway of cytosolic DNA sensing. Nat Immunol. 2016;17(10):1142–9. doi: 10.1038/ni.3558 27648547
27. Wassermann R, Gulen MF, Sala C, Perin SG, Lou Y, Rybniker J, et al. Mycobacterium tuberculosis Differentially Activates cGAS- and Inflammasome-Dependent Intracellular Immune Responses through ESX-1. Cell Host Microbe. 2015;17(6):799–810. doi: 10.1016/j.chom.2015.05.003 26048138
28. Watson RO, Bell SL, MacDuff DA, Kimmey JM, Diner EJ, Olivas J, et al. The Cytosolic Sensor cGAS Detects Mycobacterium tuberculosis DNA to Induce Type I Interferons and Activate Autophagy. Cell Host Microbe. 2015;17(6):811–9. doi: 10.1016/j.chom.2015.05.004 26048136
29. Wiens KE, Ernst JD, The Mechanism for Type I Interferon Induction by Mycobacterium tuberculosis is Bacterial Strain-Dependent. PLoS Pathog. 2016;12(8):e1005809. doi: 10.1371/journal.ppat.1005809 27500737
30. Mishalian I, Ordan M, Peled A, Maly A, Eichenbaum MB, Ravins M, et al. Recruited macrophages control dissemination of group A Streptococcus from infected soft tissues. J Immunol. 2011;187(11):6022–31. doi: 10.4049/jimmunol.1101385 22025550
31. Valderrama JA, Riestra AM, Gao NJ, LaRock CN, Gupta N, Ali SR, et al. Group A streptococcal M protein activates the NLRP3 inflammasome. Nat Microbiol. 2017. doi: 10.1038/s41564-017-0005-6 28784982
32. Pahlman LI, Morgelin M, Eckert J, Johansson L, Russell W, Riesbeck K, et al. Streptococcal M protein: a multipotent and powerful inducer of inflammation. J Immunol. 2006;177(2):1221–8. 16818781
33. Hancz D, Westerlund E, Bastiat-Sempe B, Sharma O, Valfridsson C, Meyer L, et al. Inhibition of Inflammasome-Dependent Interleukin 1beta Production by Streptococcal NAD+-Glycohydrolase: Evidence for Extracellular Activity. MBio. 2017;8(4). doi: 10.1128/mBio.00756-17 28720729
34. Price JD, Schaumburg J, Sandin C, Atkinson JP, Lindahl G, Kemper C, Induction of a regulatory phenotype in human CD4+ T cells by streptococcal M protein. J Immunol. 2005;175(2):677–84. 16002662
35. Kemper C, Leung M, Stephensen CB, Pinkert CA, Liszewski MK, Cattaneo R, et al. Membrane cofactor protein (MCP; CD46) expression in transgenic mice. Clin Exp Immunol. 2001;124(2):180–9. doi: 10.1046/j.1365-2249.2001.01458.x 11422193
36. Monroe KM, McWhirter SM, Vance RE, Induction of type I interferons by bacteria. Cell Microbiol. 2010;12(7):881–90. doi: 10.1111/j.1462-5822.2010.01478.x 20482555
37. Manca C, Tsenova L, Bergtold A, Freeman S, Tovey M, Musser JM, et al. Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha /beta. Proc Natl Acad Sci U S A. 2001;98(10):5752–7. doi: 10.1073/pnas.091096998 11320211
38. Manzanillo PS, Shiloh MU, Portnoy DA, Cox JS, Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe. 2012;11(5):469–80. doi: 10.1016/j.chom.2012.03.007 22607800
39. Stanley SA, Johndrow JE, Manzanillo P, Cox JS, The Type I IFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J Immunol. 2007;178(5):3143–52. 17312162
40. Auerbuch V, Brockstedt DG, Meyer-Morse N, O'Riordan M, Portnoy DA, Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J Exp Med. 2004;200(4):527–33. doi: 10.1084/jem.20040976 15302899
41. Carrero JA, Calderon B, Unanue ER, Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J Exp Med. 2004;200(4):535–40. doi: 10.1084/jem.20040769 15302900
42. O'Connell RM, Saha SK, Vaidya SA, Bruhn KW, Miranda GA, Zarnegar B, et al. Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J Exp Med. 2004;200(4):437–45. doi: 10.1084/jem.20040712 15302901
43. Andrade WA, Firon A, Schmidt T, Hornung V, Fitzgerald KA, Kurt-Jones EA, et al. Group B Streptococcus Degrades Cyclic-di-AMP to Modulate STING-Dependent Type I Interferon Production. Cell Host Microbe. 2016;20(1):49–59. doi: 10.1016/j.chom.2016.06.003 27414497
44. Mancuso G, Midiri A, Biondo C, Beninati C, Zummo S, Galbo R, et al. Type I IFN signaling is crucial for host resistance against different species of pathogenic bacteria. J Immunol. 2007;178(5):3126–33. 17312160
45. Kamegaya T, Kuroda K, Hayakawa Y, Identification of a Streptococcus pyogenes SF370 gene involved in production of c-di-AMP. Nagoya J Med Sci. 2011;73(1–2):49–57. 21614937
46. Woodward JJ, Iavarone AT, Portnoy DA, c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science. 2010;328(5986):1703–5. doi: 10.1126/science.1189801 20508090
47. Madden JC, Ruiz N, Caparon M, Cytolysin-mediated translocation (CMT): a functional equivalent of type III secretion in gram-positive bacteria. Cell. 2001;104(1):143–52. 11163247
48. Gratz N, Siller M, Schaljo B, Pirzada ZA, Gattermeier I, Vojtek I, et al. Group A streptococcus activates type I interferon production and MyD88-dependent signaling without involvement of TLR2, TLR4, and TLR9. J Biol Chem. 2008;283(29):19879–87. doi: 10.1074/jbc.M802848200 18480050
49. Hertzen E, Johansson L, Wallin R, Schmidt H, Kroll M, Rehn AP, et al. M1 protein-dependent intracellular trafficking promotes persistence and replication of Streptococcus pyogenes in macrophages. J Innate Immun. 2010;2(6):534–45. doi: 10.1159/000317635 20798480
50. Miller L, Gray L, Beachey E, Kehoe M, Antigenic variation among group A streptococcal M proteins. Nucleotide sequence of the serotype 5 M protein gene and its relationship with genes encoding types 6 and 24 M proteins. J Biol Chem. 1988;263(12):5668–73. 3281944
51. Johnsson E, Berggard K, Kotarsky H, Hellwage J, Zipfel PF, Sjobring U, et al. Role of the hypervariable region in streptococcal M proteins: binding of a human complement inhibitor. J Immunol. 1998;161(9):4894–901. 9794423
52. Kotarsky H, Thern A, Lindahl G, Sjobring U, Strain-specific restriction of the antiphagocytic property of group A streptococcal M proteins. Infect Immun. 2000;68(1):107–12. 10603375
53. Lienard J, Carlsson F, Murine Mycobacterium marinum Infection as a Model for Tuberculosis. Methods Mol Biol. 2017;1535:301–15. doi: 10.1007/978-1-4939-6673-8_20 27914088
54. Peiser L, Gough PJ, Kodama T, Gordon S, Macrophage class A scavenger receptor-mediated phagocytosis of Escherichia coli: role of cell heterogeneity, microbial strain, and culture conditions in vitro. Infect Immun. 2000;68(4):1953–63. 10722588
55. Kotarsky H, Hellwage J, Johnsson E, Skerka C, Svensson HG, Lindahl G, et al. Identification of a domain in human factor H and factor H-like protein-1 required for the interaction with streptococcal M proteins. J Immunol. 1998;160(7):3349–54. 9531294