IL-1R signaling enables bystander cells to overcome bacterial blockade of host protein synthesis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 24, 2015, Pages 7557-7562

  Copenhaver, Alan M ^a   Casson, Cierra N ^a   Nguyen, Hieu T ^a   Duda, Matthew M ^a   Shin, Sunny ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

IL 1; IL 1R; L. pneumophila; TNF; Type IV secretion system

Indexed keywords

INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 12; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR; AUTACOID; CD86 ANTIGEN; CD86 PROTEIN, MOUSE; CYTOKINE; IL1R1 PROTEIN, MOUSE; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR TYPE I; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL VIRULENCE; BYSTANDER EFFECT; CELL ELONGATION; CELL POPULATION; CYTOSOL; HOST CELL; IMMUNE RESPONSE; IMMUNE SYSTEM; LEGIONELLA PNEUMOPHILA; LUNG INFECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TRANSLATION INITIATION; TYPE IV SECRETION SYSTEM; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DEFICIENCY; FEMALE; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; LEGIONNAIRE DISEASE; MACROPHAGE; MALE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; VIRULENCE;

BACTERIA (MICROORGANISMS); LEGIONELLA PNEUMOPHILA;

ANIMALS; ANTIGENS, CD86; CYTOKINES; FEMALE; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; INTERLEUKIN-1; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN-1 TYPE I; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; VIRULENCE;

EID: 84932600749     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1501289112     Document Type: Article

References (53)

1. Janeway CA, Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197-216.
2. Vance RE, Isberg RR, Portnoy DA (2009) Patterns of pathogenesis: Discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6(1):10-21.
3. Krachler AM, Woolery AR, Orth K (2011) Manipulation of kinase signaling by bacterial pathogens. J Cell Biol 195(7):1083-1092.
4. Roy CR, Mocarski ES (2007) Pathogen subversion of cell-intrinsic innate immunity. Nat Immunol 8(11):1179-1187.
5. Viboud GI, Bliska JB (2005) Yersinia outer proteins: Role in modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol 59:69-89.
6. Marra A, Blander SJ, Horwitz MA, Shuman HA (1992) Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages. Proc Natl Acad Sci USA 89(20):9607-9611.
7. Berger KH, Isberg RR (1993) Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol Microbiol 7(1):7-19.
8. Hubber A, Roy CR (2010) Modulation of host cell function by Legionella pneumophila type IV effectors. Annu Rev Cell Dev Biol 26:261-283.
9. Belyi Y, Tabakova I, Stahl M, Aktories K (2008) Lgt: a family of cytotoxic glucosyltransferases produced by Legionella pneumophila. J Bacteriol 190(8):3026-3035.
10. Shen X, et al. (2009) Targeting eEF1A by a Legionella pneumophila effector leads to inhibition of protein synthesis and induction of host stress response. Cell Microbiol 11(6):911-926.
11. Belyi Y, et al. (2006) Legionella pneumophila glucosyltransferase inhibits host elongation factor 1A. Proc Natl Acad Sci USA 103(45):16953-16958.
12. Barry KC, Fontana MF, Portman JL, Dugan AS, Vance RE (2013) IL-1α signaling initiates the inflammatory response to virulent Legionella pneumophila in vivo. J Immunol 190(12):6329-6339.
13. Fontana MF, et al. (2011) Secreted bacterial effectors that inhibit host protein synthesis are critical for induction of the innate immune response to virulent Legionella pneumophila. PLoS Pathog 7(2):e1001289.
14. Ivanov SS, Roy CR (2013) Pathogen signatures activate a ubiquitination pathway that modulates the function of the metabolic checkpoint kinase mTOR. Nat Immunol 14(12):1219-1228.
15. McCusker KT, Braaten BA, Cho MW, Low DA (1991) Legionella pneumophila inhibits protein synthesis in Chinese hamster ovary cells. Infect Immun 59(1):240-246.
16. Shin S, et al. (2008) Type IV secretion-dependent activation of host MAP kinases induces an increased proinflammatory cytokine response to Legionella pneumophila. PLoS Pathog 4(11):e1000220.
17. Spörri R, Joller N, Albers U, Hilbi H, Oxenius A (2006) MyD88-dependent IFN-gamma production by NK cells is key for control of Legionella pneumophila infection. J Immunol 176(10):6162-6171.
18. LeibundGut-Landmann S, Weidner K, Hilbi H, Oxenius A (2011) Nonhematopoietic cells are key players in innate control of bacterial airway infection. J Immunol 186(5): 3130-3137.
19. Casson CN, et al. (2013) Caspase-11 activation in response to bacterial secretion systems that access the host cytosol. PLoS Pathog 9(6):e1003400.
20. Fontana MF, Shin S, Vance RE (2012) Activation of host mitogen-activated protein kinases by secreted Legionella pneumophila effectors that inhibit host protein translation. Infect Immun 80(10):3570-3575.
21. Asrat S, Dugan AS, Isberg RR (2014) The frustrated host response to Legionella pneumophila is bypassed by MyD88-dependent translation of pro-inflammatory cytokines. PLoS Pathog 10(7):e1004229.
22. Copenhaver AM, et al. (2014) Alveolar macrophages and neutrophils are the primary reservoirs for Legionella pneumophila and mediate cytosolic surveillance of type IV secretion. Infect Immun 82(10):4325-4336.
23. Knapp T, Hare E, Feng L, Zlokarnik G, Negulescu P (2003) Detection of beta-lactamase reporter gene expression by flow cytometry. Cytometry A 51(2):68-78.
24. Ren T, Zamboni DS, Roy CR, Dietrich WF, Vance RE (2006) Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2(3):e18.
25. Zamboni DS, et al. (2006) The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat Immunol 7(3):318-325.
26. Molofsky AB, et al. (2006) Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J Exp Med 203(4):1093-1104.
27. Case CL, et al. (2013) Caspase-11 stimulates rapid flagellin-independent pyroptosis in response to Legionella pneumophila. Proc Natl Acad Sci USA 110(5):1851-1856.
28. Belyi Y, Jank T, Aktories K (2013) Cytotoxic glucosyltransferases of Legionella pneumophila. Curr Top Microbiol Immunol 376:211-226.
29. Kohase M, May LT, Tamm I, Vilcek J, Sehgal PB (1987) A cytokine network in human diploid fibroblasts: Interactions of beta-interferons, tumor necrosis factor, platelet-derived growth factor, and interleukin-1. Mol Cell Biol 7(1):273-280.
30. Dinarello CA (1996) Biologic basis for interleukin-1 in disease. Blood 87(6):2095-2147.
31. Mascarenhas DPA, Pereira MSF, Manin GZ, Hori JI, Zamboni DS (2015) Interleukin 1 receptor-driven neutrophil recruitment accounts to MyD88-dependent pulmonary clearance of legionella pneumophila infection in vivo. J Infect Dis 211(2):322-330.
32. Demuth A, Goebel W, Beuscher HU, Kuhn M (1996) Differential regulation of cytokine and cytokine receptor mRNA expression upon infection of bone marrow-derived macrophages with Listeria monocytogenes. Infect Immun 64(9):3475-3483.
33. Shimizu K, et al. (2015) IL-1 receptor type 2 suppresses collagen-induced arthritis by inhibiting IL-1 signal on macrophages. J Immunol 194(7):3156-3168.
34. Fontana MF, Vance RE (2011) Two signal models in innate immunity. Immunol Rev 243(1):26-39.
35. Franchi L, et al. (2012) NLRC4-driven production of IL-1β discriminates between pathogenic and commensal bacteria and promotes host intestinal defense. Nat Immunol 13(5):449-456.
36. Dreux M, et al. (2012) Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host Microbe 12(4):558-570.
37. Dolowschiak T, et al. (2010) Potentiation of epithelial innate host responses by intercellular communication. PLoS Pathog 6(11):e1001194.
38. Patel SJ, King KR, Casali M, Yarmush ML (2009) DNA-triggered innate immune responses are propagated by gap junction communication. Proc Natl Acad Sci USA 106(31):12867-12872.
39. Kasper CA, et al. (2010) Cell-cell propagation of NF-κB transcription factor and MAP kinase activation amplifies innate immunity against bacterial infection. Immunity 33(5):804-816.
40. Ablasser A, et al. (2013) Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature 503(7477):530-534.
41. Christian DA, et al. (2014) Use of transgenic parasites and host reporters to dissect events that promote interleukin-12 production during toxoplasmosis. Infect Immun 82(10):4056-4067.
42. Pang IK, Ichinohe T, Iwasaki A (2013) IL-1R signaling in dendritic cells replaces pattern-recognition receptors in promoting CD8+ T cell responses to influenza A virus. Nat Immunol 14(3):246-253.
43. Yrlid U, Wick MJ (2000) Salmonella-induced apoptosis of infected macrophages results in presentation of a bacteria-encoded antigen after uptake by bystander dendritic cells. J Exp Med 191(4):613-624.
44. Trunk G, Oxenius A (2012) Innate instruction of CD4+ T cell immunity in respiratory bacterial infection. J Immunol 189(2):616-628.
45. Stevenson FT, Torrano F, Locksley RM, Lovett DH (1992) Interleukin 1: The patterns of translation and intracellular distribution support alternative secretory mechanisms. J Cell Physiol 152(2):223-231.
46. Rathinam VAK, Vanaja SK, Fitzgerald KA (2012) Regulation of inflammasome signaling. Nat Immunol 13(4):333-342.
47. Ikejima T, Okusawa S, Ghezzi P, van der Meer JW, Dinarello CA (1990) Interleukin-1 induces tumor necrosis factor (TNF) in human peripheral blood mononuclear cells in vitro and a circulating TNF-like activity in rabbits. J Infect Dis 162(1):215-223.
48. th Ed.
49. Feeley JC, et al. (1979) Charcoal-yeast extract agar: Primary isolation medium for Legionella pneumophila. J Clin Microbiol 10(4):437-441.
50. Nogueira CV, et al. (2009) Rapid pathogen-induced apoptosis: A mechanism used by dendritic cells to limit intracellular replication of Legionella pneumophila. PLoS Pathog 5(6):e1000478.
51. Neild A, Murata T, Roy CR (2005) Processing and major histocompatibility complex class II presentation of Legionella pneumophila antigens by infected macrophages. Infect Immun 73(4):2336-2343.
52. Engel P, et al. (1994) The B7-2 (B20) costimulatory molecule expressed by monocytes and activated B lymphocytes is the CD86 differentiation antigen. Blood 81:1402-1407.
53. Inaba K, et al. (1992) Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 176:1693-1702.