The pattern recognition receptors Nod1 and Nod2 account for neutrophil recruitment to the lungs of mice infected with Legionella pneumophila

Microbes and Infection

Volumn 12, Issue 11, 2010, Pages 819-827

  Frutuoso, Mariana S ^a   Hori, Juliana I ^a   Pereira, Marcelo S F ^a   Junior, Djalma S L ^a   Sônego, Fabiane ^a   Kobayashi, Koichi S ^b   Flavell, Richard A ^c   Cunha, Fernando Q ^a   Zamboni, Dario S ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b HARVARD MEDICAL SCHOOL   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Legionella pneumophila; Neutrophils; Nod1; Nod2

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CYTOKINE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PATTERN RECOGNITION RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL MUTATION; CELL INFILTRATION; CELL INTERACTION; CELL MUTANT; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HOST; IMMUNE RESPONSE; INNATE IMMUNITY; LEGIONELLA PNEUMOPHILA; LUNG; LUNG INFECTION; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; SECRETORY PATHWAY;

ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; LUNG; MALE; MICE; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; NOD1 SIGNALING ADAPTOR PROTEIN; NOD2 SIGNALING ADAPTOR PROTEIN; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RECEPTORS, PATTERN RECOGNITION; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); LEGIONELLA PNEUMOPHILA; MURINAE; MUS;

EID: 77957752777     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2010.05.006     Document Type: Article

References (51)

1. Swanson M.S., Hammer B.K. Legionella pneumophila pathogesesis: a fateful journey from amoebae to macrophages. Annu. Rev. Microbiol. 2000, 54:567-613.
2. Diederen B.M. Legionella spp. and Legionnaires' disease. J. Infect. 2008, 56:1-12.
3. Friedman H., Yamamoto Y., Klein T.W. Legionella pneumophila pathogenesis and immunity. Semin. Pediatr. Infect. Dis. 2002, 13:273-279.
4. Carratala J., Gudiol F., Pallares R., Dorca J., Verdaguer R., Ariza J., Manresa F. Risk factors for nosocomial Legionella pneumophila pneumonia. Am. J. Respir. Crit. Care Med. 1994, 149:625-629.
5. Gutzeit M.F., Lauer S.J., Dunne W.M., Kelly K.J., Chusid M.J. Fatal Legionella pneumonitis in a neutropenic leukemic child. Pediatr. Infect. Dis. J. 1987, 6:68-69.
6. Winn W.C., Myerowitz R.L. The pathology of the Legionella pneumonias. A review of 74 cases and the literature. Hum. Pathol. 1981, 12:401-422.
7. Fuse E.T., Tateda K., Kikuchi Y., Matsumoto T., Gondaira F., Azuma A., Kudoh S., Standiford T.J., Yamaguchi K. Role of Toll-like receptor 2 in recognition of Legionella pneumophila in a murine pneumonia model. J. Med. Microbiol. 2007, 56:305-312.
8. Hawn T.R., Smith K.D., Aderem A., Skerrett S.J. Myeloid differentiation primary response gene (88)- and toll-like receptor 2-deficient mice are susceptible to infection with aerosolized Legionella pneumophila. J. Infect. Dis. 2006, 193:1693-1702.
9. Hawn T.R., Berrington W.R., Smith I.A., Uematsu S., Akira S., Aderem A., Smith K.D., Skerrett S.J. Altered inflammatory responses in TLR5-deficient mice infected with Legionella pneumophila. J. Immunol. 2007, 179:6981-6987.
10. Skerrett S.J., Martin T.R. Intratracheal interferon-gamma augments pulmonary defenses in experimental legionellosis. Am. J. Respir. Crit. Care Med. 1994, 149:50-58.
11. Tateda K., Moore T.A., Newstead M.W., Tsai W.C., Zeng X., Deng J.C., Chen G., Reddy R., Yamaguchi K., Standiford T.J. Chemokine-dependent neutrophil recruitment in a murine model of Legionella pneumonia: potential role of neutrophils as immunoregulatory cells. Infect. Immun. 2001, 69:2017-2024.
12. Tateda K., Moore T.A., Deng J.C., Newstead M.W., Zeng X., Matsukawa A., Swanson M.S., Yamaguchi K., Standiford T.J. Early recruitment of neutrophils determines subsequent T1/T2 host responses in a murine model of Legionella pneumophila pneumonia. J. Immunol. 2001, 166:3355-3361.
13. Fitzgeorge R.B., Featherstone A.S., Baskerville A. Effects of polymorphonuclear leucocyte depletion on the pathogenesis of experimental Legionnaires' disease. Br. J. Exp. Pathol. 1988, 69:105-112.
14. Horwitz M.A., Silverstein S.C. Interaction of the legionnaires' disease bacterium (Legionella pneumophila) with human phagocytes. II. Antibody promotes binding of L. pneumophila to monocytes but does not inhibit intracellular multiplication. J. Exp. Med. 1981, 153:398-406.
15. Weinbaum D.L., Bailey J., Benner R.R., Pasculle A.W., Dowling J.N. The contribution of human neutrophils and serum to host defense against Legionella micdadei. J. Infect. Dis. 1983, 148:510-517.
16. Sporri R., Joller N., Hilbi H., Oxenius A. A novel role for neutrophils as critical activators of NK cells. J. Immunol. 2008, 181:7121-7130.
17. Brieland J.K., Remick D.G., LeGendre M.L., Engleberg N.C., Fantone J.C. In vivo regulation of replicative Legionella pneumophila lung infection by endogenous interleukin-12. Infect. Immun. 1998, 66:65-69.
18. Nash T.W., Libby D.M., Horwitz M.A. IFN-gamma-activated human alveolar macrophages inhibit the intracellular multiplication of Legionella pneumophila. J. Immunol. 1988, 140:3978-3981.
19. Ensminger A.W., Isberg R.R. Legionella pneumophila Dot/Icm translocated substrates: a sum of parts. Curr. Opin. Microbiol. 2009, 12:67-73.
20. Ninio S., Roy C.R. Effector proteins translocated by Legionella pneumophila: strength in numbers. Trends Microbiol. 2007, 15:372-380.
21. Coers J., Kagan J.C., Matthews M., Nagai H., Zuckman D.M., Roy C.R. Identification of Icm protein complexes that play distinct roles in the biogenesis of an organelle permissive for Legionella pneumophila intracellular growth. Mol. Microbiol. 2000, 38:719-736.
22. Matthews M., Roy C.R. Identification and subcellular localization of the Legionella pneumophila IcmX protein: a factor essential for establishment of a replicative organelle in eukaryotic host cells. Infect. Immun. 2000, 68:3971-3982.
23. Roy C.R., Berger K.H., Isberg R.R. Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol. Microbiol. 1998, 28:663-674.
24. Kanneganti T.D., Lamkanfi M., Nunez G. Intracellular NOD-like receptors in host defense and disease. Immunity 2007, 27:549-559.
25. Franchi L., Eigenbrod T., Munoz-Planillo R., Nunez G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol. 2009, 10:241-247.
26. Franchi L., Warner N., Viani K., Nunez G. Function of Nod-like receptors in microbial recognition and host defense. Immunol. Rev. 2009, 227:106-128.
27. Masumoto J., Yang K., Varambally S., Hasegawa M., Tomlins S.A., Qiu S., Fujimoto Y., Kawasaki A., Foster S.J., Horie Y., Mak T.W., Nunez G., Chinnaiyan A.M., Fukase K., Inohara N. Nod1 acts as an intracellular receptor to stimulate chemokine production and neutrophil recruitment in vivo. J. Exp. Med. 2006, 203:203-213.
28. Park J.H., Kim Y.G., Shaw M., Kanneganti T.D., Fujimoto Y., Fukase K., Inohara N., Nunez G. Nod1/RICK and TLR signaling regulate chemokine and antimicrobial innate immune responses in mesothelial cells. J. Immunol. 2007, 179:514-521.
29. Ferwerda G., Girardin S.E., Kullberg B.J., Le Bourhis L., de Jong D.J., Langenberg D.M., van Crevel R., Adema G.J., Ottenhoff T.H., Van der Meer J.W., Netea M.G. NOD2 and toll-like receptors are nonredundant recognition systems of Mycobacterium tuberculosis. PLoS Pathog. 2005, 1:279-285.
30. Benoit M., Bechah Y., Capo C., Murray P.J., Mege J.L., Desnues B. Role of the cytoplasmic pattern recognition receptor Nod2 in Coxiella burnetii infection. Clin. Microbiol. Infect. 2009.
31. Opitz B., Forster S., Hocke A.C., Maass M., Schmeck B., Hippenstiel S., Suttorp N., Krull M. Nod1-mediated endothelial cell activation by Chlamydophila pneumoniae. Circ. Res. 2005, 96:319-326.
32. Shimada K., Chen S., Dempsey P.W., Sorrentino R., Alsabeh R., Slepenkin A.V., Peterson E., Doherty T.M., Underhill D., Crother T.R., Arditi M. The NOD/RIP2 pathway is essential for host defenses against Chlamydophila pneumoniae lung infection. PLoS Pathog. 2009, 5:e1000379.
33. Berger K.H., Isberg R.R. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 1993, 7:7-19.
34. Zuckman D.M., Hung J.B., Roy C.R. Pore-forming activity is not sufficient for Legionella pneumophila phagosome trafficking and intracellular growth. Mol. Microbiol. 1999, 32:990-1001.
35. Ren T., Zamboni D.S., Roy C.R., Dietrich W.F., Vance R.E. Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog. 2006, 2:e18.
36. Chamaillard M., Hashimoto M., Horie Y., Masumoto J., Qiu S., Saab L., Ogura Y., Kawasaki A., Fukase K., Kusumoto S., Valvano M.A., Foster S.J., Mak T.W., Nunez G., Inohara N. An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat. Immunol. 2003, 4:702-707.
37. Kobayashi K.S., Chamaillard M., Ogura Y., Henegariu O., Inohara N., Nunez G., Flavell R.A. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005, 307:731-734.
38. Kobayashi K., Inohara N., Hernandez L.D., Galan J.E., Nunez G., Janeway C.A., Medzhitov R., Flavell R.A. RICK/Rip2/CARDIAK mediates signaling for receptors of the innate and adaptive immune systems. Nature 2002, 416:194-199.
39. Alves-Filho J.C., Freitas A., Souto F.O., Spiller F., Paula-Neto H., Silva J.S., Gazzinelli R.T., Teixeira M.M., Ferreira S.H., Cunha F.Q. Regulation of chemokine receptor by Toll-like receptor 2 is critical to neutrophil migration and resistance to polymicrobial sepsis. Proc. Natl. Acad. Sci. U S A 2009, 106:4018-4023.
40. Isberg R.R., Rankin S., Roy C.R., Swanson M.S., Berger K.H. Legionella pneumophila: factors involved in the route and response to an intracellular niche. Infect. Agents Dis. 1993, 2:220-223.
41. Ninio S., Zuckman-Cholon D.M., Cambronne E.D., Roy C.R. The Legionella IcmS-IcmW protein complex is important for Dot/Icm-mediated protein translocation. Mol. Microbiol. 2005, 55:912-926.
42. Shin S., Case C.L., Archer K.A., Nogueira C.V., Kobayashi K.S., Flavell R.A., Roy C.R., Zamboni D.S. Type IV secretion-dependent activation of host MAP kinases induces an increased proinflammatory cytokine response to Legionella pneumophila. PLoS Pathog. 2008, 4:e1000220.
43. Amer A., Franchi L., Kanneganti T.D., Body-Malapel M., Ozoren N., Brady G., Meshinchi S., Jagirdar R., Gewirtz A., Akira S., Nunez G. Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J. Biol. Chem. 2006, 281:35217-35223.
44. Case C.L., Shin S., Roy C.R. Asc and Ipaf Inflammasomes direct distinct pathways for caspase-1 activation in response to Legionella pneumophila. Infect. Immun. 2009, 77:1981-1991.
45. Molofsky A.B., Byrne B.G., Whitfield N.N., Madigan C.A., Fuse E.T., Tateda K., Swanson M.S. Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J. Exp. Med. 2006, 203:1093-1104.
46. Zamboni D.S., Kobayashi K.S., Kohlsdorf T., Ogura Y., Long E.M., Vance R.E., Kuida K., Mariathasan S., Dixit V.M., Flavell R.A., Dietrich W.F., Roy C.R. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat. Immunol. 2006, 7:318-325.
47. Archer K.A., Roy C.R. MyD88-dependent responses involving toll-like receptor 2 are important for protection and clearance of Legionella pneumophila in a mouse model of Legionnaires' disease. Infect. Immun. 2006, 74:3325-3333.
48. Nagai H., Cambronne E.D., Kagan J.C., Amor J.C., Kahn R.A., Roy C.R. A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc. Natl. Acad. Sci. U S A 2005, 102:826-831.
49. Kim Y.G., Park J.H., Shaw M.H., Franchi L., Inohara N., Nunez G. The cytosolic sensors Nod1 and Nod2 are critical for bacterial recognition and host defense after exposure to Toll-like receptor ligands. Immunity 2008, 28:246-257.
50. Silveira T.N., Zamboni D.S. Pore formation triggered by Legionella spp. is an Nlrc4 inflammasome-dependent host cell response that precedes pyroptosis. Infect. Immun. 2010, 78:1403-1413.
51. Viala J., Chaput C., Boneca I.G., Cardona A., Girardin S.E., Moran A.P., Athman R., Memet S., Huerre M.R., Coyle A.J., DiStefano P.S., Sansonetti P.J., Labigne A., Bertin J., Philpott D.J., Ferrero R.L. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 2004, 5:1166-1174.