Update on the role of innate immune receptors during Brucella abortus infection

Veterinary Immunology and Immunopathology

Volumn 148, Issue 1-2, 2012, Pages 129-135

  Oliveira, Sérgio C ^a   de Almeida, Leonardo A ^a   Carvalho, Natalia B ^a   Oliveira, Fernanda S ^a   Lacerda, Thaís L S ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Brucella abortus; Innate immunity; MyD88; TLR signaling; TRIF

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 6; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 2;

ARTICLE; BACTERIAL CLEARANCE; BRUCELLA ABORTUS; BRUCELLOSIS; CELL MATURATION; CYTOKINE RESPONSE; CYTOSOL; DENDRITIC CELL; IMMUNE EVASION; IMMUNOCOMPETENT CELL; IMMUNOSENSOR; IN VIVO STUDY; INNATE IMMUNITY; INTRACELLULAR SIGNALING; NONHUMAN;

ANIMALS; BRUCELLA ABORTUS; BRUCELLOSIS, BOVINE; CATTLE; IMMUNITY, INNATE; MYELOID DIFFERENTIATION FACTOR 88; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

BACTERIA (MICROORGANISMS); BRUCELLA; BRUCELLA MELITENSIS BIOVAR ABORTUS; MUS;

EID: 84864139889     PISSN: 01652427     EISSN: 18732534     Source Type: Journal    
DOI: 10.1016/j.vetimm.2011.05.036     Document Type: Article

References (89)

1. Ablasser A., Bauernfeind F., Hartmann G., Latz E., Fitzgerald K.A., Hornung V. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat. Immunol. 2009, 10(10):1065-1072.
2. Akira S. TLR signaling. Curr. Top. Microbiol. Immunol. 2006, 311:1-16.
3. Akira S., Takeda K., Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2001, 2(8):675-680.
4. Albiger B., Dahlberg S., Henriques-Normark B., Normark S. Role of the innate immune system in host defence against bacterial infections: focus on the Toll-like receptors. J. Intern. Med. 2007, 261(6):511-528.
5. Allen C.A., Adams L.G., Ficht T.A. Transposon-derived Brucella abortus rough mutants are attenuated and exhibit reduced intracellular survival. Infect. Immun. 1998, 66(3):1008-1016.
6. Andersen-Nissen E., Smith K.D., Strobe K.L., Barrett S.L., Cookson B.T., Logan S.M., Aderem A. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc. Natl. Acad. Sci. U.S.A. 2005, 102(26):9247-9252.
7. Arellano-Reynoso B., Lapaque N., Salcedo S., Briones G., Ciocchini A.E., Ugalde R., Moreno E., Moriyon I., Gorvel J.P. Cyclic beta-1,2-glucan is a Brucella virulence factor required for intracellular survival. Nat. Immunol. 2005, 6(6):618-625.
8. Auerbuch V., Brockstedt D.G., Meyer-Morse N., O'Riordan M., Portnoy D.A. Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J. Exp. Med. 2004, 200(4):527-533.
9. Barquero-Calvo E., Chaves-Olarte E., Weiss D.S., Guzman-Verri C., Chacon-Diaz C., Rucavado A., Moriyon I., Moreno E. Brucella abortus uses a stealthy strategy to avoid activation of the innate immune system during the onset of infection. PLoS One 2007, 2(7):e631.
10. Barquero-Calvo E., Conde-Alvarez R., Chacon-Diaz C., Quesada-Lobo L., Martirosyan A., Guzman-Verri C., Iriarte M., Mancek-Keber M., Jerala R., Gorvel J.P., Moriyon I., Moreno E., Chaves-Olarte E. The differential interaction of Brucella and ochrobactrum with innate immunity reveals traits related to the evolution of stealthy pathogens. PLoS One 2009, 4(6):e5893.
11. Barrionuevo P., Cassataro J., Delpino M.V., Zwerdling A., Pasquevich K.A., Garcia Samartino C., Wallach J.C., Fossati C.A., Giambartolomei G.H. Brucella abortus inhibits major histocompatibility complex class II expression and antigen processing through interleukin-6 secretion via Toll-like receptor 2. Infect. Immun. 2008, 76(1):250-262.
12. Bieger C.D., Nierlich D.P. Distribution of 5'-triphosphate termini on the mRNA of Escherichia coli. J. Bacteriol. 1989, 171(1):141-147.
13. Bourhis L.L., Werts C. Role of Nods in bacterial infection. Microbes Infect. 2007, 9(5):629-636.
14. Campos M.A., Rosinha G.M., Almeida I.C., Salgueiro X.S., Jarvis B.W., Splitter G.A., Qureshi N., Bruna-Romero O., Gazzinelli R.T., Oliveira S.C. Role of Toll-like receptor 4 in induction of cell-mediated immunity and resistance to Brucella abortus infection in mice. Infect. Immun. 2004, 72(1):176-186.
15. Cardoso P.G., Macedo G.C., Azevedo V., Oliveira S.C. Brucella spp noncanonical LPS: structure, biosynthesis, and interaction with host immune system. Microb. Cell Fact. 2006, 5:13.
16. Carrero J.A., Calderon B., Unanue E.R. Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J. Exp. Med. 2004, 200(4):535-540.
17. Celli J., de Chastellier C., Franchini D.M., Pizarro-Cerda J., Moreno E., Gorvel J.P. Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J. Exp. Med. 2003, 198(4):545-556.
18. Chiu Y.H., Macmillan J.B., Chen Z.J. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 2009, 138(3):576-591.
19. Choi Y.J., Im E., Pothoulakis C., Rhee S.H. TRIF modulates TLR5-dependent responses by inducing proteolytic degradation of TLR5. J. Biol. Chem. 2010, 285(28):21382-21390.
20. Cirl C., Wieser A., Yadav M., Duerr S., Schubert S., Fischer H., Stappert D., Wantia N., Rodriguez N., Wagner H., Svanborg C., Miethke T. Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/interleukin-1 receptor domain-containing proteins. Nat. Med. 2008, 14(4):399-406.
21. Copin R., De Baetselier P., Carlier Y., Letesson J.J., Muraille E. MyD88-dependent activation of B220-CD11b+LY-6C+ dendritic cells during Brucella melitensis infection. J. Immunol. 2007, 178(8):5182-5191.
22. Corbel M.J. Brucellosis: an overview. Emerg. Infect. Dis. 1997, 3(2):213-221.
23. de Jong M.F., Rolan H.G., Tsolis R.M. Innate immune encounters of the (Type) 4th kind: Brucella. Cell. Microbiol. 2010, 12(9):1195-1202.
24. de Weerd N.A., Samarajiwa S.A., Hertzog P.J. Type I interferon receptors: biochemistry and biological functions. J. Biol. Chem. 2007, 282(28):20053-20057.
25. Decker T., Muller M., Stockinger S. The yin and yang of type I interferon activity in bacterial infection. Nat. Rev. Immunol. 2005, 5(9):675-687.
26. Dornand J., Gross A., Lafont V., Liautard J., Oliaro J., Liautard J.P. The innate immune response against Brucella in humans. Vet. Microbiol. 2002, 90(1-4):383-394.
27. 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(3):279-285.
28. Fitzgerald K.A., Rowe D.C., Barnes B.J., Caffrey D.R., Visintin A., Latz E., Monks B., Pitha P.M., Golenbock D.T. LPS-TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF. J. Exp. Med. 2003, 198(7):1043-1055.
29. Forestier C., Deleuil F., Lapaque N., Moreno E., Gorvel J.P. Brucella abortus lipopolysaccharide in murine peritoneal macrophages acts as a down-regulator of T cell activation. J. Immunol. 2000, 165(9):5202-5210.
30. Franchi L., Park J.H., Shaw M.H., Marina-Garcia N., Chen G., Kim Y.G., Nunez G. Intracellular NOD-like receptors in innate immunity, infection and disease. Cell. Microbiol. 2008, 10(1):1-8.
31. Fretin D., Fauconnier A., Kohler S., Halling S., Leonard S., Nijskens C., Ferooz J., Lestrate P., Delrue R.M., Danese I., Vandenhaute J., Tibor A., DeBolle X., Letesson J.J. The sheathed flagellum of Brucella melitensis is involved in persistence in a murine model of infection. Cell. Microbiol. 2005, 7(5):687-698.
32. Giambartolomei G.H., Zwerdling A., Cassataro J., Bruno L., Fossati C.A., Philipp M.T. Lipoproteins, not lipopolysaccharide, are the key mediators of the proinflammatory response elicited by heat-killed Brucella abortus. J. Immunol. 2004, 173(7):4635-4642.
33. Golding B., Scott D.E., Scharf O., Huang L.Y., Zaitseva M., Lapham C., Eller N., Golding H. Immunity and protection against Brucella abortus. Microbes Infect. 2001, 3(1):43-48.
34. Gorvel J.P. Brucella: a Mr. " Hide" converted into Dr. Jekyll. Microbes Infect. 2008, 10(9):1010-1013.
35. Henry T., Kirimanjeswara G.S., Ruby T., Jones J.W., Peng K., Perret M., Ho L., Sauer J.D., Iwakura Y., Metzger D.W., Monack D.M. Type I IFN signaling constrains IL-17A/F secretion by gammadelta T cells during bacterial infections. J. Immunol. 2010, 184(7):3755-3767.
36. Hornung V., Ellegast J., Kim S., Brzozka K., Jung A., Kato H., Poeck H., Akira S., Conzelmann K.K., Schlee M., Endres S., Hartmann G. 5'-Triphosphate RNA is the ligand for RIG-I. Science 2006, 314(5801):994-997.
37. Huang L.Y., Aliberti J., Leifer C.A., Segal D.M., Sher A., Golenbock D.T., Golding B. Heat-killed Brucella abortus induces TNF and IL-12p40 by distinct MyD88-dependent pathways: TNF, unlike IL-12p40 secretion, is Toll-like receptor 2 dependent. J. Immunol. 2003, 171(3):1441-1446.
38. Huang L.Y., Ishii K.J., Akira S., Aliberti J., Golding B. Th1-like cytokine induction by heat-killed Brucella abortus is dependent on triggering of TLR9. J. Immunol. 2005, 175(6):3964-3970.
39. Ishii K.J., Akira S. Innate immune recognition of, and regulation by, DNA. Trends Immunol. 2006, 27(11):525-532.
40. Ishikawa H., Barber G.N. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008, 455(7213):674-678.
41. Iwasaki A., Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 2004, 5(10):987-995.
42. Janeway C.A., Medzhitov R. Innate immune recognition. Annu. Rev. Immunol. 2002, 20:197-216.
43. Kanakaraj P., Schafer P.H., Cavender D.E., Wu Y., Ngo K., Grealish P.F., Wadsworth S.A., Peterson P.A., Siekierka J.J., Harris C.A., Fung-Leung W.P. Interleukin (IL)-1 receptor-associated kinase (IRAK) requirement for optimal induction of multiple IL-1 signaling pathways and IL-6 production. J. Exp. Med. 1998, 187(12):2073-2079.
44. Kawai T., Akira S. The roles of TLRs, RLRs and NLRs in pathogen recognition. Int. Immunol. 2009, 21(4):317-337.
45. Lacerda T.L., Cardoso P.G., Augusto de Almeida L., Camargo I.L., Afonso D.A., Trant C.C., Macedo G.C., Campos E., Cravero S.L., Salcedo S.P., Gorvel J.P., Oliveira S.C. Inactivation of formyltransferase (wbkC) gene generates a Brucella abortus rough strain that is attenuated in macrophages and in mice. Vaccine 2010, 28(34):5627-5634.
46. Lapaque N., Moriyon I., Moreno E., Gorvel J.P. Brucella lipopolysaccharide acts as a virulence factor. Curr. Opin. Microbiol. 2005, 8(1):60-66.
47. Lapaque N., Muller A., Alexopoulou L., Howard J.C., Gorvel J.P. Brucella abortus induces Irgm3 and Irga6 expression via type-I IFN by a MyD88-dependent pathway, without the requirement of TLR2, TLR4, TLR5 and TLR9. Microb. Pathog. 2009, 47(6):299-304.
48. Lapaque N., Takeuchi O., Corrales F., Akira S., Moriyon I., Howard J.C., Gorvel J.P. Differential inductions of TNF-alpha and IGTP, IIGP by structurally diverse classic and non-classic lipopolysaccharides. Cell. Microbiol. 2006, 8(3):401-413.
49. Lilo S., Zheng Y., Bliska J.B. Caspase-1 activation in macrophages infected with Yersinia pestis KIM requires the type III secretion system effector YopJ. Infect. Immun. 2008, 76(9):3911-3923.
50. Lippmann J., Rothenburg S., Deigendesch N., Eitel J., Meixenberger K., van Laak V., Slevogt H., N'Guessan P.D., Hippenstiel S., Chakraborty T., Flieger A., Suttorp N., Opitz B. IFNbeta responses induced by intracellular bacteria or cytosolic DNA in different human cells do not require ZBP1 (DLM-1/DAI). Cell. Microbiol. 2008, 10(12):2579-2588.
51. Lye E., Dhanji S., Calzascia T., Elford A.R., Ohashi P.S. IRAK-4 kinase activity is required for IRAK-4-dependent innate and adaptive immune responses. Eur. J. Immunol. 2008, 38(3):870-876.
52. Macedo G.C., Magnani D.M., Carvalho N.B., Bruna-Romero O., Gazzinelli R.T., Oliveira S.C. Central role of MyD88-dependent dendritic cell maturation and proinflammatory cytokine production to control Brucella abortus infection. J. Immunol. 2008, 180(2):1080-1087.
53. Mancuso G., Midiri A., Biondo C., Beninati C., Zummo S., Galbo R., Tomasello F., Gambuzza M., Macri G., Ruggeri A., Leanderson T., Teti G. Type I IFN signaling is crucial for host resistance against different species of pathogenic bacteria. J. Immunol. 2007, 178(5):3126-3133.
54. Martinon F., Burns K., Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol. Cell 2002, 10(2):417-426.
55. Medzhitov R., Preston-Hurlburt P., Janeway C.A. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 1997, 388(6640):394-397.
56. Monroe K.M., McWhirter S.M., Vance R.E. Induction of type I interferons by bacteria. Cell. Microbiol. 2010, 12(7):881-890.
57. Muller A.J., Hoffmann C., Galle M., Van Den Broeke A., Heikenwalder M., Falter L., Misselwitz B., Kremer M., Beyaert R., Hardt W.D. The S. Typhimurium effector SopE induces caspase-1 activation in stromal cells to initiate gut inflammation. Cell Host Microbe 2009, 6(2):125-136.
58. Nagarajan U.M., Prantner D., Sikes J.D., Andrews C.W., Goodwin A.M., Nagarajan S., Darville T. Type I interferon signaling exacerbates Chlamydia muridarum genital infection in a murine model. Infect. Immun. 2008, 76(10):4642-4648.
59. O'Connell R.M., Saha S.K., Vaidya S.A., Bruhn K.W., Miranda G.A., Zarnegar B., Perry A.K., Nguyen B.O., Lane T.F., Taniguchi T., Miller J.F., Cheng G. Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J. Exp. Med. 2004, 200(4):437-445.
60. O'Neill L.A., Bowie A.G. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 2007, 7(5):353-364.
61. Oliveira S.C., Splitter G.A. CD8+ type 1 CD44hi CD45 RBlo T lymphocytes control intracellular Brucella abortus infection as demonstrated in major histocompatibility complex class I- and class II-deficient mice. Eur. J. Immunol. 1995, 25(9):2551-2557.
62. Pandey A.K., Yang Y., Jiang Z., Fortune S.M., Coulombe F., Behr M.A., Fitzgerald K.A., Sassetti C.M., Kelliher M.A. NOD2, RIP2 and IRF5 play a critical role in the type I interferon response to Mycobacterium tuberculosis. PLoS Pathog. 2009, 5(7):e1000500.
63. Park J.H., Kim Y.G., McDonald C., Kanneganti T.D., Hasegawa M., Body-Malapel M., Inohara N., Nunez G. RICK/RIP2 mediates innate immune responses induced through Nod1 and Nod2 but not TLRs. J. Immunol. 2007, 178(4):2380-2386.
64. Pasquevich K.A., Garcia Samartino C., Coria L.M., Estein S.M., Zwerdling A., Ibanez A.E., Barrionuevo P., Oliveira F.S., Carvalho N.B., Borkowski J., Oliveira S.C., Warzecha H., Giambartolomei G.H., Cassataro J. The protein moiety of Brucella abortus outer membrane protein 16 is a new bacterial pathogen-associated molecular pattern that activates dendritic cells in vivo, induces a Th1 immune response, and is a promising self-adjuvanting vaccine against systemic and oral acquired brucellosis. J. Immunol. 2010, 184(9):5200-5212.
65. Pei J., Turse J.E., Ficht T.A. Evidence of Brucella abortus OPS dictating uptake and restricting NF-kappaB activation in murine macrophages. Microbes Infect. 2008, 10(6):582-590.
66. Philpott D.J., Girardin S.E. The role of Toll-like receptors and Nod proteins in bacterial infection. Mol. Immunol. 2004, 41(11):1099-1108.
67. Pizarro-Cerda J., Meresse S., Parton R.G., van der Goot G., Sola-Landa A., Lopez-Goni I., Moreno E., Gorvel J.P. Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect. Immun. 1998, 66(12):5711-5724.
68. Porte F., Naroeni A., Ouahrani-Bettache S., Liautard J.P. Role of the Brucella suis lipopolysaccharide O antigen in phagosomal genesis and in inhibition of phagosome-lysosome fusion in murine macrophages. Infect. Immun. 2003, 71(3):1481-1490.
69. Prantner D., Darville T., Nagarajan U.M. Stimulator of IFN gene is critical for induction of IFN-beta during Chlamydia muridarum infection. J. Immunol. 2010, 184(5):2551-2560.
70. Qiu H., Fan Y., Joyee A.G., Wang S., Han X., Bai H., Jiao L., Van Rooijen N., Yang X. Type I IFNs enhance susceptibility to Chlamydia muridarum lung infection by enhancing apoptosis of local macrophages. J. Immunol. 2008, 181(3):2092-2102.
71. Radhakrishnan G.K., Yu Q., Harms J.S., Splitter G.A. Brucella TIR domain-containing protein mimics properties of the Toll-like receptor adaptor protein TIRAP. J. Biol. Chem. 2009, 284(15):9892-9898.
72. Radhakrishnan G.K., Splitter G.A. Biochemical and functional analysis of TIR domain containing protein from Brucella melitensis. Biochem. Biophys. Res. Commun. 2010, 397(1):59-63.
73. Salcedo S.P., Marchesini M.I., Lelouard H., Fugier E., Jolly G., Balor S., Muller A., Lapaque N., Demaria O., Alexopoulou L., Comerci D.J., Ugalde R.A., Pierre P., Gorvel J.P. Brucella control of dendritic cell maturation is dependent on the TIR-containing protein Btp1. PLoS Pathog. 2008, 4(2):e21.
74. Schroder K., Tschopp J. The inflammasomes. Cell 2010, 140(6):821-832.
75. Sengupta D., Koblansky A., Gaines J., Brown T., West A.P., Zhang D., Nishikawa T., Park S.G., Roop R.M., Ghosh S. Subversion of innate immune responses by Brucella through the targeted degradation of the TLR signaling adapter, MAL. J. Immunol. 2010, 184(2):956-964.
76. Stetson D.B., Medzhitov R. Type I interferons in host defense. Immunity 2006, 25(3):373-381.
77. Sutterwala F.S., Flavell R.A. NLRC4/IPAF: a CARD carrying member of the NLR family. Clin. Immunol. 2009, 130(1):2-6.
78. Suzuki N., Chen N.J., Millar D.G., Suzuki S., Horacek T., Hara H., Bouchard D., Nakanishi K., Penninger J.M., Ohashi P.S., Yeh W.C. IL-1 receptor-associated kinase 4 is essential for IL-18-mediated NK and Th1 cell responses. J. Immunol. 2003, 170(8):4031-4035.
79. Suzuki N., Suzuki S., Duncan G.S., Millar D.G., Wada T., Mirtsos C., Takada H., Wakeham A., Itie A., Li S., Penninger J.M., Wesche H., Ohashi P.S., Mak T.W., Yeh W.C. Severe impairment of interleukin-1 and Toll-like receptor signalling in mice lacking IRAK-4. Nature 2002, 416(6882):750-756.
80. Takaoka A., Wang Z., Choi M.K., Yanai H., Negishi H., Ban T., Lu Y., Miyagishi M., Kodama T., Honda K., Ohba Y., Taniguchi T. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007, 448(7152):501-505.
81. Takeuchi O., Akira S. Pattern recognition receptors and inflammation. Cell 2010, 140(6):805-820.
82. Thomas J.A., Allen J.L., Tsen M., Dubnicoff T., Danao J., Liao X.C., Cao Z., Wasserman S.A. Impaired cytokine signaling in mice lacking the IL-1 receptor-associated kinase. J. Immunol. 1999, 163(2):978-984.
83. Uematsu S., Akira S. Toll-like receptors and Type I interferons. J. Biol. Chem. 2007, 282(21):15319-15323.
84. Weiss D.S., Takeda K., Akira S., Zychlinsky A., Moreno E. MyD88, but not Toll-like receptors 4 and 2, is required for efficient clearance of Brucella abortus. Infect. Immun. 2005, 73(8):5137-5143.
85. Yamamoto M., Sato S., Hemmi H., Hoshino K., Kaisho T., Sanjo H., Takeuchi O., Sugiyama M., Okabe M., Takeda K., Akira S. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 2003, 301(5633):640-643.
86. Yamamoto M., Sato S., Hemmi H., Uematsu S., Hoshino K., Kaisho T., Takeuchi O., Takeda K., Akira S. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat. Immunol. 2003, 4(11):1144-1150.
87. Yang P., An H., Liu X., Wen M., Zheng Y., Rui Y., Cao X. The cytosolic nucleic acid sensor LRRFIP1 mediates the production of type I interferon via a beta-catenin-dependent pathway. Nat. Immunol. 2010, 11(6):487-494.
88. Yoneyama M., Fujita T. Structural mechanism of RNA recognition by the RIG-I-like receptors. Immunity 2008, 29(2):178-181.
89. Zwerdling A., Delpino M.V., Barrionuevo P., Cassataro J., Pasquevich K.A., Garcia Samartino C., Fossati C.A., Giambartolomei G.H. Brucella lipoproteins mimic dendritic cell maturation induced by Brucella abortus. Microbes Infect. 2008, 10(12-13):1346-1354.