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Published in: Medical Microbiology and Immunology 6/2017

Open Access 01-12-2017 | Review

Immune response against rickettsiae: lessons from murine infection models

Author: Anke Osterloh

Published in: Medical Microbiology and Immunology | Issue 6/2017

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Abstract

Rickettsiae are small intracellular bacteria that can cause life-threatening febrile diseases. Rickettsioses occur worldwide with increasing incidence. Therefore, a vaccine is highly desired. A prerequisite for the development of a vaccine is the knowledge of the immune response against these bacteria, in particular protective immunity. In recent years murine models of rickettsial infections have been established, and the study of immune response against rickettsiae in mice provided many new insights into protective and pathological immune reactions. This review summarizes the current knowledge about immune mechanisms in protection and pathology in rickettsial infections.
Literature
1.
go back to reference Mediannikov O, Nguyen TT, Bell-Sakyi L, Padmanabhan R, Fournier PE, Raoult D (2014) High quality draft genome sequence and description of Occidentia massiliensis gen. nov., sp. nov., a new member of the family Rickettsiaceae. Stand Genomic Sci 9:9. doi:10.1186/1944-3277-9-9 PubMedPubMedCentralCrossRef Mediannikov O, Nguyen TT, Bell-Sakyi L, Padmanabhan R, Fournier PE, Raoult D (2014) High quality draft genome sequence and description of Occidentia massiliensis gen. nov., sp. nov., a new member of the family Rickettsiaceae. Stand Genomic Sci 9:9. doi:10.​1186/​1944-3277-9-9 PubMedPubMedCentralCrossRef
2.
go back to reference Sekeyova Z, Roux V, Raoult D (2001) Phylogeny of Rickettsia spp. inferred by comparing sequences of ‘gene D’, which encodes an intracytoplasmic protein. Int J Syst Evol Microbiol 51(Pt 4):1353–1360PubMedCrossRef Sekeyova Z, Roux V, Raoult D (2001) Phylogeny of Rickettsia spp. inferred by comparing sequences of ‘gene D’, which encodes an intracytoplasmic protein. Int J Syst Evol Microbiol 51(Pt 4):1353–1360PubMedCrossRef
3.
go back to reference Mansueto P, Vitale G, Cascio A, Seidita A, Pepe I, Carroccio A, di Rosa S, Rini GB, Cillari E, Walker DH (2012) New insight into immunity and immunopathology of Rickettsial diseases. Clin Dev Immunol 2012:967852. doi:10.1155/2012/967852 PubMedCrossRef Mansueto P, Vitale G, Cascio A, Seidita A, Pepe I, Carroccio A, di Rosa S, Rini GB, Cillari E, Walker DH (2012) New insight into immunity and immunopathology of Rickettsial diseases. Clin Dev Immunol 2012:967852. doi:10.​1155/​2012/​967852 PubMedCrossRef
7.
go back to reference Winkler HH, Miller ET (1982) Phospholipase A and the interaction of Rickettsia prowazekii and mouse fibroblasts (L-929 cells). Infect Immun 38(1):109–113PubMedPubMedCentral Winkler HH, Miller ET (1982) Phospholipase A and the interaction of Rickettsia prowazekii and mouse fibroblasts (L-929 cells). Infect Immun 38(1):109–113PubMedPubMedCentral
8.
go back to reference Silverman DJ, Santucci LA, Meyers N, Sekeyova Z (1992) Penetration of host cells by Rickettsia rickettsii appears to be mediated by a phospholipase of rickettsial origin. Infect Immun 60(7):2733–2740PubMedPubMedCentral Silverman DJ, Santucci LA, Meyers N, Sekeyova Z (1992) Penetration of host cells by Rickettsia rickettsii appears to be mediated by a phospholipase of rickettsial origin. Infect Immun 60(7):2733–2740PubMedPubMedCentral
9.
go back to reference Walker DH, Feng HM, Popov VL (2001) Rickettsial phospholipase A2 as a pathogenic mechanism in a model of cell injury by typhus and spotted fever group rickettsiae. Am J Trop Med Hyg 65(6):936–942PubMedCrossRef Walker DH, Feng HM, Popov VL (2001) Rickettsial phospholipase A2 as a pathogenic mechanism in a model of cell injury by typhus and spotted fever group rickettsiae. Am J Trop Med Hyg 65(6):936–942PubMedCrossRef
10.
go back to reference Renesto P, Dehoux P, Gouin E, Touqui L, Cossart P, Raoult D (2003) Identification and characterization of a phospholipase D-superfamily gene in rickettsiae. J Infect Dis 188(9):1276–1283. doi:10.1086/379080 PubMedCrossRef Renesto P, Dehoux P, Gouin E, Touqui L, Cossart P, Raoult D (2003) Identification and characterization of a phospholipase D-superfamily gene in rickettsiae. J Infect Dis 188(9):1276–1283. doi:10.​1086/​379080 PubMedCrossRef
12.
go back to reference Silverman DJ, Bond SB (1984) Infection of human vascular endothelial cells by Rickettsia rickettsii. J Infect Dis 149(2):201–206PubMedCrossRef Silverman DJ, Bond SB (1984) Infection of human vascular endothelial cells by Rickettsia rickettsii. J Infect Dis 149(2):201–206PubMedCrossRef
13.
go back to reference Hackstadt T (1996) The biology of rickettsiae. Infect Agents Dis 5(3):127–143PubMed Hackstadt T (1996) The biology of rickettsiae. Infect Agents Dis 5(3):127–143PubMed
14.
go back to reference Heinzen RA (2003) Rickettsial actin-based motility: behavior and involvement of cytoskeletal regulators. Ann N Y Acad Sci 990:535–547PubMedCrossRef Heinzen RA (2003) Rickettsial actin-based motility: behavior and involvement of cytoskeletal regulators. Ann N Y Acad Sci 990:535–547PubMedCrossRef
17.
go back to reference Radulovic S, Price PW, Beier MS, Gaywee J, Macaluso JA, Azad A (2002) Rickettsia-macrophage interactions: host cell responses to Rickettsia akari and Rickettsia typhi. Infect Immun 70(5):2576–2582PubMedPubMedCentralCrossRef Radulovic S, Price PW, Beier MS, Gaywee J, Macaluso JA, Azad A (2002) Rickettsia-macrophage interactions: host cell responses to Rickettsia akari and Rickettsia typhi. Infect Immun 70(5):2576–2582PubMedPubMedCentralCrossRef
18.
go back to reference Walker DH, Popov VL, Wen J, Feng HM (1994) Rickettsia conorii infection of C3H/HeN mice. A model of endothelial-target rickettsiosis. Lab Invest 70(3):358–368PubMed Walker DH, Popov VL, Wen J, Feng HM (1994) Rickettsia conorii infection of C3H/HeN mice. A model of endothelial-target rickettsiosis. Lab Invest 70(3):358–368PubMed
19.
go back to reference Pongponratn E, Maneerat Y, Chaisri U, Wilairatana P, Punpoowong B, Viriyavejakul P, Riganti M (1998) Electron-microscopic examination of Rickettsia tsutsugamushi-infected human liver. Trop Med Int Health 3(3):242–248PubMedCrossRef Pongponratn E, Maneerat Y, Chaisri U, Wilairatana P, Punpoowong B, Viriyavejakul P, Riganti M (1998) Electron-microscopic examination of Rickettsia tsutsugamushi-infected human liver. Trop Med Int Health 3(3):242–248PubMedCrossRef
20.
go back to reference Walker DH, Harrison A, Henderson F, Murphy FA (1977) Identification of Rickettsia rickettsii in a guinea pig model by immunofluorescent and electron microscopic techniques. Am J Pathol 86(2):343–358PubMedPubMedCentral Walker DH, Harrison A, Henderson F, Murphy FA (1977) Identification of Rickettsia rickettsii in a guinea pig model by immunofluorescent and electron microscopic techniques. Am J Pathol 86(2):343–358PubMedPubMedCentral
22.
go back to reference McDade JE, Stakebake JR, Gerone PJ (1969) Plaque assay system for several species of Rickettsia. J Bacteriol 99(3):910–912PubMedPubMedCentral McDade JE, Stakebake JR, Gerone PJ (1969) Plaque assay system for several species of Rickettsia. J Bacteriol 99(3):910–912PubMedPubMedCentral
23.
go back to reference Wike DA, Tallent G, Peacock MG, Ormsbee RA (1972) Studies of the rickettsial plaque assay technique. Infect Immun 5(5):715–722PubMedPubMedCentral Wike DA, Tallent G, Peacock MG, Ormsbee RA (1972) Studies of the rickettsial plaque assay technique. Infect Immun 5(5):715–722PubMedPubMedCentral
24.
go back to reference Hanson B (1987) Improved plaque assay for Rickettsia tsutsugamushi. Am J Trop Med Hyg 36(3):631–638PubMedCrossRef Hanson B (1987) Improved plaque assay for Rickettsia tsutsugamushi. Am J Trop Med Hyg 36(3):631–638PubMedCrossRef
25.
go back to reference Policastro PF, Peacock MG, Hackstadt T (1996) Improved plaque assays for Rickettsia prowazekii in Vero 76 cells. J Clin Microbiol 34(8):1944–1948PubMedPubMedCentral Policastro PF, Peacock MG, Hackstadt T (1996) Improved plaque assays for Rickettsia prowazekii in Vero 76 cells. J Clin Microbiol 34(8):1944–1948PubMedPubMedCentral
27.
31.
go back to reference Parker RT, Menon PG, Merideth AM, Snyder MJ, Woodward TE (1954) Persistence of Rickettsia rickettsii in a patient recovered from Rocky Mountain spotted fever. J Immunol 73(6):383–386PubMed Parker RT, Menon PG, Merideth AM, Snyder MJ, Woodward TE (1954) Persistence of Rickettsia rickettsii in a patient recovered from Rocky Mountain spotted fever. J Immunol 73(6):383–386PubMed
32.
go back to reference Hove MG, Walker DH (1995) Persistence of rickettsiae in the partially viable gangrenous margins of amputated extremities 5 to 7 weeks after onset of Rocky Mountain spotted fever. Arch Pathol Lab Med 119(5):429–431PubMed Hove MG, Walker DH (1995) Persistence of rickettsiae in the partially viable gangrenous margins of amputated extremities 5 to 7 weeks after onset of Rocky Mountain spotted fever. Arch Pathol Lab Med 119(5):429–431PubMed
35.
38.
go back to reference Feng HM, Wen J, Walker DH (1993) Rickettsia australis infection: a murine model of a highly invasive vasculopathic rickettsiosis. Am J Pathol 142(5):1471–1482PubMedPubMedCentral Feng HM, Wen J, Walker DH (1993) Rickettsia australis infection: a murine model of a highly invasive vasculopathic rickettsiosis. Am J Pathol 142(5):1471–1482PubMedPubMedCentral
39.
go back to reference Anderson GW Jr, Osterman JV (1980) Host defenses in experimental rickettsialpox: genetics of natural resistance to infection. Infect Immun 28(1):132–136PubMedPubMedCentral Anderson GW Jr, Osterman JV (1980) Host defenses in experimental rickettsialpox: genetics of natural resistance to infection. Infect Immun 28(1):132–136PubMedPubMedCentral
40.
go back to reference Papp S, Moderzynski K, Rauch J, Heine L, Kuehl S, Richardt U, Mueller H, Fleischer B, Osterloh A (2016) Liver necrosis and lethal systemic inflammation in a murine model of Rickettsia typhi Infection: role of neutrophils, macrophages and NK cells. PLoS Negl Trop Dis 10(8):e0004935. doi:10.1371/journal.pntd.0004935 PubMedPubMedCentralCrossRef Papp S, Moderzynski K, Rauch J, Heine L, Kuehl S, Richardt U, Mueller H, Fleischer B, Osterloh A (2016) Liver necrosis and lethal systemic inflammation in a murine model of Rickettsia typhi Infection: role of neutrophils, macrophages and NK cells. PLoS Negl Trop Dis 10(8):e0004935. doi:10.​1371/​journal.​pntd.​0004935 PubMedPubMedCentralCrossRef
42.
go back to reference Groves MG, Kelly DJ (1989) Characterization of factors determining Rickettsia tsutsugamushi pathogenicity for mice. Infect Immun 57(5):1476–1482PubMedPubMedCentral Groves MG, Kelly DJ (1989) Characterization of factors determining Rickettsia tsutsugamushi pathogenicity for mice. Infect Immun 57(5):1476–1482PubMedPubMedCentral
43.
go back to reference Groves MG, Osterman JV (1978) Host defenses in experimental scrub typhus: genetics of natural resistance to infection. Infect Immun 19(2):583–588PubMedPubMedCentral Groves MG, Osterman JV (1978) Host defenses in experimental scrub typhus: genetics of natural resistance to infection. Infect Immun 19(2):583–588PubMedPubMedCentral
45.
go back to reference Moderzynski K, Heine L, Rauch J, Papp S, Kuehl S, Richardt U, Fleischer B, Osterloh A (2017) Cytotoxic effector functions of T cells are not required for protective immunity against fatal Rickettsia typhi infection in a murine model of infection: role of TH1 and TH17 cytokines in protection and pathology. PLoS Negl Trop Dis 11(2):e0005404. doi:10.1371/journal.pntd.0005404 PubMedPubMedCentralCrossRef Moderzynski K, Heine L, Rauch J, Papp S, Kuehl S, Richardt U, Fleischer B, Osterloh A (2017) Cytotoxic effector functions of T cells are not required for protective immunity against fatal Rickettsia typhi infection in a murine model of infection: role of TH1 and TH17 cytokines in protection and pathology. PLoS Negl Trop Dis 11(2):e0005404. doi:10.​1371/​journal.​pntd.​0005404 PubMedPubMedCentralCrossRef
49.
go back to reference Walker DH, Popov VL, Feng HM (2000) Establishment of a novel endothelial target mouse model of a typhus group rickettsiosis: evidence for critical roles for gamma interferon and CD8 T lymphocytes. Lab Invest 80(9):1361–1372PubMedCrossRef Walker DH, Popov VL, Feng HM (2000) Establishment of a novel endothelial target mouse model of a typhus group rickettsiosis: evidence for critical roles for gamma interferon and CD8 T lymphocytes. Lab Invest 80(9):1361–1372PubMedCrossRef
51.
go back to reference Eisemann CS, Nypaver MJ, Osterman JV (1984) Susceptibility of inbred mice to rickettsiae of the spotted fever group. Infect Immun 43(1):143–148PubMedPubMedCentral Eisemann CS, Nypaver MJ, Osterman JV (1984) Susceptibility of inbred mice to rickettsiae of the spotted fever group. Infect Immun 43(1):143–148PubMedPubMedCentral
52.
53.
go back to reference Feng HM, Whitworth T, Olano JP, Popov VL, Walker DH (2004) Fc-dependent polyclonal antibodies and antibodies to outer membrane proteins A and B, but not to lipopolysaccharide, protect SCID mice against fatal Rickettsia conorii infection. Infect Immun 72(4):2222–2228PubMedPubMedCentralCrossRef Feng HM, Whitworth T, Olano JP, Popov VL, Walker DH (2004) Fc-dependent polyclonal antibodies and antibodies to outer membrane proteins A and B, but not to lipopolysaccharide, protect SCID mice against fatal Rickettsia conorii infection. Infect Immun 72(4):2222–2228PubMedPubMedCentralCrossRef
54.
go back to reference Clifton DR, Rydkina E, Huyck H, Pryhuber G, Freeman RS, Silverman DJ, Sahni SK (2005) Expression and secretion of chemotactic cytokines IL-8 and MCP-1 by human endothelial cells after Rickettsia rickettsii infection: regulation by nuclear transcription factor NF-kappaB. Int J Med Microbiol 295(4):267–278PubMedCrossRef Clifton DR, Rydkina E, Huyck H, Pryhuber G, Freeman RS, Silverman DJ, Sahni SK (2005) Expression and secretion of chemotactic cytokines IL-8 and MCP-1 by human endothelial cells after Rickettsia rickettsii infection: regulation by nuclear transcription factor NF-kappaB. Int J Med Microbiol 295(4):267–278PubMedCrossRef
55.
go back to reference Kaplanski G, Teysseire N, Farnarier C, Kaplanski S, Lissitzky JC, Durand JM, Soubeyrand J, Dinarello CA, Bongrand P (1995) IL-6 and IL-8 production from cultured human endothelial cells stimulated by infection with Rickettsia conorii via a cell-associated IL-1 alpha-dependent pathway. J Clin Invest 96(6):2839–2844. doi:10.1172/JCI118354 PubMedPubMedCentralCrossRef Kaplanski G, Teysseire N, Farnarier C, Kaplanski S, Lissitzky JC, Durand JM, Soubeyrand J, Dinarello CA, Bongrand P (1995) IL-6 and IL-8 production from cultured human endothelial cells stimulated by infection with Rickettsia conorii via a cell-associated IL-1 alpha-dependent pathway. J Clin Invest 96(6):2839–2844. doi:10.​1172/​JCI118354 PubMedPubMedCentralCrossRef
57.
go back to reference Bechah Y, Capo C, Raoult D, Mege JL (2008) Infection of endothelial cells with virulent Rickettsia prowazekii increases the transmigration of leukocytes. J Infect Dis 197(1):142–147. doi:10.1086/523649 PubMedCrossRef Bechah Y, Capo C, Raoult D, Mege JL (2008) Infection of endothelial cells with virulent Rickettsia prowazekii increases the transmigration of leukocytes. J Infect Dis 197(1):142–147. doi:10.​1086/​523649 PubMedCrossRef
58.
go back to reference Baggiolini M, Clark-Lewis I (1992) Interleukin-8, a chemotactic and inflammatory cytokine. FEBS Lett 307(1):97–101PubMedCrossRef Baggiolini M, Clark-Lewis I (1992) Interleukin-8, a chemotactic and inflammatory cytokine. FEBS Lett 307(1):97–101PubMedCrossRef
59.
go back to reference Harada A, Sekido N, Akahoshi T, Wada T, Mukaida N, Matsushima K (1994) Essential involvement of interleukin-8 (IL-8) in acute inflammation. J Leukoc Biol 56(5):559–564PubMed Harada A, Sekido N, Akahoshi T, Wada T, Mukaida N, Matsushima K (1994) Essential involvement of interleukin-8 (IL-8) in acute inflammation. J Leukoc Biol 56(5):559–564PubMed
61.
go back to reference Li A, Dubey S, Varney ML, Dave BJ, Singh RK (2003) IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis. J Immunol 170(6):3369–3376PubMedCrossRef Li A, Dubey S, Varney ML, Dave BJ, Singh RK (2003) IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis. J Immunol 170(6):3369–3376PubMedCrossRef
65.
go back to reference Sporn LA, Lawrence SO, Silverman DJ, Marder VJ (1993) E-selectin-dependent neutrophil adhesion to Rickettsia rickettsii-infected endothelial cells. Blood 81(9):2406–2412PubMed Sporn LA, Lawrence SO, Silverman DJ, Marder VJ (1993) E-selectin-dependent neutrophil adhesion to Rickettsia rickettsii-infected endothelial cells. Blood 81(9):2406–2412PubMed
66.
go back to reference Valbuena G, Walker DH (2004) Effect of blocking the CXCL9/10-CXCR3 chemokine system in the outcome of endothelial-target rickettsial infections. Am J Trop Med Hyg 71(4):393–399PubMed Valbuena G, Walker DH (2004) Effect of blocking the CXCL9/10-CXCR3 chemokine system in the outcome of endothelial-target rickettsial infections. Am J Trop Med Hyg 71(4):393–399PubMed
67.
go back to reference Elices MJ, Osborn L, Takada Y, Crouse C, Luhowskyj S, Hemler ME, Lobb RR (1990) VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site. Cell 60(4):577–584PubMedCrossRef Elices MJ, Osborn L, Takada Y, Crouse C, Luhowskyj S, Hemler ME, Lobb RR (1990) VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site. Cell 60(4):577–584PubMedCrossRef
68.
go back to reference Sporn LA, Marder VJ (1996) Interleukin-1 alpha production during Rickettsia rickettsii infection of cultured endothelial cells: potential role in autocrine cell stimulation. Infect Immun 64(5):1609–1613PubMedPubMedCentral Sporn LA, Marder VJ (1996) Interleukin-1 alpha production during Rickettsia rickettsii infection of cultured endothelial cells: potential role in autocrine cell stimulation. Infect Immun 64(5):1609–1613PubMedPubMedCentral
72.
go back to reference Rydkina E, Sahni A, Baggs RB, Silverman DJ, Sahni SK (2006) Infection of human endothelial cells with spotted Fever group rickettsiae stimulates cyclooxygenase 2 expression and release of vasoactive prostaglandins. Infect Immun 74(9):5067–5074. doi:10.1128/IAI.00182-06 PubMedPubMedCentralCrossRef Rydkina E, Sahni A, Baggs RB, Silverman DJ, Sahni SK (2006) Infection of human endothelial cells with spotted Fever group rickettsiae stimulates cyclooxygenase 2 expression and release of vasoactive prostaglandins. Infect Immun 74(9):5067–5074. doi:10.​1128/​IAI.​00182-06 PubMedPubMedCentralCrossRef
73.
go back to reference Walker TS, Brown JS, Hoover CS, Morgan DA (1990) Endothelial prostaglandin secretion: effects of typhus rickettsiae. J Infect Dis 162(5):1136–1144PubMedCrossRef Walker TS, Brown JS, Hoover CS, Morgan DA (1990) Endothelial prostaglandin secretion: effects of typhus rickettsiae. J Infect Dis 162(5):1136–1144PubMedCrossRef
74.
go back to reference Zimmerman GA, McIntyre TM, Prescott SM, Stafforini DM (2002) The platelet-activating factor signaling system and its regulators in syndromes of inflammation and thrombosis. Crit Care Med 30(5 Suppl):S294–S301PubMedCrossRef Zimmerman GA, McIntyre TM, Prescott SM, Stafforini DM (2002) The platelet-activating factor signaling system and its regulators in syndromes of inflammation and thrombosis. Crit Care Med 30(5 Suppl):S294–S301PubMedCrossRef
75.
go back to reference Sporn LA, Haidaris PJ, Shi RJ, Nemerson Y, Silverman DJ, Marder VJ (1994) Rickettsia rickettsii infection of cultured human endothelial cells induces tissue factor expression. Blood 83(6):1527–1534PubMed Sporn LA, Haidaris PJ, Shi RJ, Nemerson Y, Silverman DJ, Marder VJ (1994) Rickettsia rickettsii infection of cultured human endothelial cells induces tissue factor expression. Blood 83(6):1527–1534PubMed
77.
go back to reference Sporn LA, Sahni SK, Lerner NB, Marder VJ, Silverman DJ, Turpin LC, Schwab AL (1997) Rickettsia rickettsii infection of cultured human endothelial cells induces NF-kappaB activation. Infect Immun 65(7):2786–2791PubMedPubMedCentral Sporn LA, Sahni SK, Lerner NB, Marder VJ, Silverman DJ, Turpin LC, Schwab AL (1997) Rickettsia rickettsii infection of cultured human endothelial cells induces NF-kappaB activation. Infect Immun 65(7):2786–2791PubMedPubMedCentral
78.
go back to reference Shi RJ, Simpson-Haidaris PJ, Lerner NB, Marder VJ, Silverman DJ, Sporn LA (1998) Transcriptional regulation of endothelial cell tissue factor expression during Rickettsia rickettsii infection: involvement of the transcription factor NF-kappaB. Infect Immun 66(3):1070–1075PubMedPubMedCentral Shi RJ, Simpson-Haidaris PJ, Lerner NB, Marder VJ, Silverman DJ, Sporn LA (1998) Transcriptional regulation of endothelial cell tissue factor expression during Rickettsia rickettsii infection: involvement of the transcription factor NF-kappaB. Infect Immun 66(3):1070–1075PubMedPubMedCentral
79.
go back to reference Clifton DR, Goss RA, Sahni SK, van Antwerp D, Baggs RB, Marder VJ, Silverman DJ, Sporn LA (1998) NF-kappa B-dependent inhibition of apoptosis is essential for host cellsurvival during Rickettsia rickettsii infection. Proc Natl Acad Sci USA 95(8):4646–4651PubMedPubMedCentralCrossRef Clifton DR, Goss RA, Sahni SK, van Antwerp D, Baggs RB, Marder VJ, Silverman DJ, Sporn LA (1998) NF-kappa B-dependent inhibition of apoptosis is essential for host cellsurvival during Rickettsia rickettsii infection. Proc Natl Acad Sci USA 95(8):4646–4651PubMedPubMedCentralCrossRef
80.
go back to reference Walker DH, Hudnall SD, Szaniawski WK, Feng HM (1999) Monoclonal antibody-based immunohistochemical diagnosis of rickettsialpox: the macrophage is the principal target. Mod Pathol 12(5):529–533PubMed Walker DH, Hudnall SD, Szaniawski WK, Feng HM (1999) Monoclonal antibody-based immunohistochemical diagnosis of rickettsialpox: the macrophage is the principal target. Mod Pathol 12(5):529–533PubMed
81.
go back to reference Nelyubov MV (2002) Astrakhan scrub typhus: time course of infectious process according to electron microscopy findings. Bull Exp Biol Med 134(4):374–375PubMedCrossRef Nelyubov MV (2002) Astrakhan scrub typhus: time course of infectious process according to electron microscopy findings. Bull Exp Biol Med 134(4):374–375PubMedCrossRef
85.
86.
87.
go back to reference Nathan C, Xie QW (1994) Regulation of biosynthesis of nitric oxide. J Biol Chem 269(19):13725–13728PubMed Nathan C, Xie QW (1994) Regulation of biosynthesis of nitric oxide. J Biol Chem 269(19):13725–13728PubMed
88.
go back to reference Kamijo R, Harada H, Matsuyama T, Bosland M, Gerecitano J, Shapiro D, Le J, Koh SI, Kimura T, Green SJ et al (1994) Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science 263(5153):1612–1615PubMedCrossRef Kamijo R, Harada H, Matsuyama T, Bosland M, Gerecitano J, Shapiro D, Le J, Koh SI, Kimura T, Green SJ et al (1994) Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science 263(5153):1612–1615PubMedCrossRef
89.
go back to reference Koide N, Mu MM, Hassan F, Islam S, Tumurkhuu G, Dagvadorj J, Naiki Y, Mori I, Yoshida T, Yokochi T (2007) Lipopolysaccharide enhances interferon-gamma-induced nitric oxide (NO) production in murine vascular endothelial cells via augmentation of interferon regulatory factor-1 activation. J Endotoxin Res 13(3):167–175. doi:10.1177/0968051907080894 PubMedCrossRef Koide N, Mu MM, Hassan F, Islam S, Tumurkhuu G, Dagvadorj J, Naiki Y, Mori I, Yoshida T, Yokochi T (2007) Lipopolysaccharide enhances interferon-gamma-induced nitric oxide (NO) production in murine vascular endothelial cells via augmentation of interferon regulatory factor-1 activation. J Endotoxin Res 13(3):167–175. doi:10.​1177/​0968051907080894​ PubMedCrossRef
90.
go back to reference Turco J, Winkler HH (1986) Gamma-interferon-induced inhibition of the growth of Rickettsia prowazekii in fibroblasts cannot be explained by the degradation of tryptophan or other amino acids. Infect Immun 53(1):38–46PubMedPubMedCentral Turco J, Winkler HH (1986) Gamma-interferon-induced inhibition of the growth of Rickettsia prowazekii in fibroblasts cannot be explained by the degradation of tryptophan or other amino acids. Infect Immun 53(1):38–46PubMedPubMedCentral
91.
go back to reference Feng HM, Walker DH (2000) Mechanisms of intracellular killing of Rickettsia conorii in infected human endothelial cells, hepatocytes, and macrophages. Infect Immun 68(12):6729–6736PubMedPubMedCentralCrossRef Feng HM, Walker DH (2000) Mechanisms of intracellular killing of Rickettsia conorii in infected human endothelial cells, hepatocytes, and macrophages. Infect Immun 68(12):6729–6736PubMedPubMedCentralCrossRef
92.
go back to reference Billings AN, Feng HM, Olano JP, Walker DH (2001) Rickettsial infection in murine models activates an early anti-rickettsial effect mediated by NK cells and associated with production of gamma interferon. Am J Trop Med Hyg 65(1):52–56PubMedCrossRef Billings AN, Feng HM, Olano JP, Walker DH (2001) Rickettsial infection in murine models activates an early anti-rickettsial effect mediated by NK cells and associated with production of gamma interferon. Am J Trop Med Hyg 65(1):52–56PubMedCrossRef
93.
go back to reference Mazurier F, Fontanellas A, Salesse S, Taine L, Landriau S, Moreau-Gaudry F, Reiffers J, Peault B, Di Santo JP, de Verneuil H (1999) A novel immunodeficient mouse model–RAG2 x common cytokine receptor gamma chain double mutants–requiring exogenous cytokine administration for human hematopoietic stem cell engraftment. J Interferon Cytokine Res 19(5):533–541. doi:10.1089/107999099313983 PubMedCrossRef Mazurier F, Fontanellas A, Salesse S, Taine L, Landriau S, Moreau-Gaudry F, Reiffers J, Peault B, Di Santo JP, de Verneuil H (1999) A novel immunodeficient mouse model–RAG2 x common cytokine receptor gamma chain double mutants–requiring exogenous cytokine administration for human hematopoietic stem cell engraftment. J Interferon Cytokine Res 19(5):533–541. doi:10.​1089/​107999099313983 PubMedCrossRef
94.
go back to reference Rollwagen FM (1988) Role of natural killer cells in the early clearance of Rickettsia typhi in mice. Adv Exp Med Biol 239:163–168PubMedCrossRef Rollwagen FM (1988) Role of natural killer cells in the early clearance of Rickettsia typhi in mice. Adv Exp Med Biol 239:163–168PubMedCrossRef
95.
go back to reference Kenyon RH, Pedersen CE Jr (1980) Immune responses to Rickettsia akari infection in congenitally athymic nude mice. Infect Immun 28(2):310–313PubMedPubMedCentral Kenyon RH, Pedersen CE Jr (1980) Immune responses to Rickettsia akari infection in congenitally athymic nude mice. Infect Immun 28(2):310–313PubMedPubMedCentral
97.
go back to reference Dumler JS, Taylor JP, Walker DH (1991) Clinical and laboratory features of murine typhus in south Texas, 1980 through 1987. JAMA 266(10):1365–1370PubMedCrossRef Dumler JS, Taylor JP, Walker DH (1991) Clinical and laboratory features of murine typhus in south Texas, 1980 through 1987. JAMA 266(10):1365–1370PubMedCrossRef
98.
go back to reference Fournier PE, Jensenius M, Laferl H, Vene S, Raoult D (2002) Kinetics of antibody responses in Rickettsia africae and Rickettsia conorii infections. Clin Diagn Lab Immunol 9(2):324–328PubMedPubMedCentral Fournier PE, Jensenius M, Laferl H, Vene S, Raoult D (2002) Kinetics of antibody responses in Rickettsia africae and Rickettsia conorii infections. Clin Diagn Lab Immunol 9(2):324–328PubMedPubMedCentral
99.
go back to reference Feng H, Popov VL, Yuoh G, Walker DH (1997) Role of T lymphocyte subsets in immunity to spotted fever group Rickettsiae. J Immunol 158(11):5314–5320PubMed Feng H, Popov VL, Yuoh G, Walker DH (1997) Role of T lymphocyte subsets in immunity to spotted fever group Rickettsiae. J Immunol 158(11):5314–5320PubMed
100.
go back to reference Fang R, Ismail N, Soong L, Popov VL, Whitworth T, Bouyer DH, Walker DH (2007) Differential interaction of dendritic cells with Rickettsia conorii: impact on host susceptibility to murine spotted fever rickettsiosis. Infect Immun 75(6):3112–3123. doi:10.1128/IAI.00007-07 PubMedPubMedCentralCrossRef Fang R, Ismail N, Soong L, Popov VL, Whitworth T, Bouyer DH, Walker DH (2007) Differential interaction of dendritic cells with Rickettsia conorii: impact on host susceptibility to murine spotted fever rickettsiosis. Infect Immun 75(6):3112–3123. doi:10.​1128/​IAI.​00007-07 PubMedPubMedCentralCrossRef
101.
go back to reference Feng HM, Popov VL, Walker DH (1994) Depletion of gamma interferon and tumor necrosis factor alpha in mice with Rickettsia conorii-infected endothelium: impairment of rickettsicidal nitric oxide production resulting in fatal, overwhelming rickettsial disease. Infect Immun 62(5):1952–1960PubMedPubMedCentral Feng HM, Popov VL, Walker DH (1994) Depletion of gamma interferon and tumor necrosis factor alpha in mice with Rickettsia conorii-infected endothelium: impairment of rickettsicidal nitric oxide production resulting in fatal, overwhelming rickettsial disease. Infect Immun 62(5):1952–1960PubMedPubMedCentral
102.
go back to reference Fossiez F, Djossou O, Chomarat P, Flores-Romo L, Ait-Yahia S, Maat C, Pin JJ, Garrone P, Garcia E, Saeland S, Blanchard D, Gaillard C, Das Mahapatra B, Rouvier E, Golstein P, Banchereau J, Lebecque S (1996) T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J Exp Med 183(6):2593–2603PubMedCrossRef Fossiez F, Djossou O, Chomarat P, Flores-Romo L, Ait-Yahia S, Maat C, Pin JJ, Garrone P, Garcia E, Saeland S, Blanchard D, Gaillard C, Das Mahapatra B, Rouvier E, Golstein P, Banchereau J, Lebecque S (1996) T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J Exp Med 183(6):2593–2603PubMedCrossRef
103.
go back to reference Jovanovic DV, Di Battista JA, Martel-Pelletier J, Jolicoeur FC, He Y, Zhang M, Mineau F, Pelletier JP (1998) IL-17 stimulates the production and expression of proinflammatory cytokines, IL-beta and TNF-alpha, by human macrophages. J Immunol 160(7):3513–3521PubMed Jovanovic DV, Di Battista JA, Martel-Pelletier J, Jolicoeur FC, He Y, Zhang M, Mineau F, Pelletier JP (1998) IL-17 stimulates the production and expression of proinflammatory cytokines, IL-beta and TNF-alpha, by human macrophages. J Immunol 160(7):3513–3521PubMed
105.
go back to reference Sylvester J, Liacini A, Li WQ, Zafarullah M (2004) Interleukin-17 signal transduction pathways implicated in inducing matrix metalloproteinase-3, -13 and aggrecanase-1 genes in articular chondrocytes. Cell Signal 16(4):469–476PubMedCrossRef Sylvester J, Liacini A, Li WQ, Zafarullah M (2004) Interleukin-17 signal transduction pathways implicated in inducing matrix metalloproteinase-3, -13 and aggrecanase-1 genes in articular chondrocytes. Cell Signal 16(4):469–476PubMedCrossRef
106.
go back to reference Koenders MI, Lubberts E, Oppers-Walgreen B, van den Bersselaar L, Helsen MM, Di Padova FE, Boots AM, Gram H, Joosten LA, van den Berg WB (2005) Blocking of interleukin-17 during reactivation of experimental arthritis prevents joint inflammation and bone erosion by decreasing RANKL and interleukin-1. Am J Pathol 167(1):141–149. doi:10.1016/S0002-9440(10)62961-6 PubMedPubMedCentralCrossRef Koenders MI, Lubberts E, Oppers-Walgreen B, van den Bersselaar L, Helsen MM, Di Padova FE, Boots AM, Gram H, Joosten LA, van den Berg WB (2005) Blocking of interleukin-17 during reactivation of experimental arthritis prevents joint inflammation and bone erosion by decreasing RANKL and interleukin-1. Am J Pathol 167(1):141–149. doi:10.​1016/​S0002-9440(10)62961-6 PubMedPubMedCentralCrossRef
107.
go back to reference Kao CY, Chen Y, Thai P, Wachi S, Huang F, Kim C, Harper RW, Wu R (2004) IL-17 markedly up-regulates beta-defensin-2 expression in human airway epithelium via JAK and NF-kappaB signaling pathways. J Immunol 173(5):3482–3491PubMedCrossRef Kao CY, Chen Y, Thai P, Wachi S, Huang F, Kim C, Harper RW, Wu R (2004) IL-17 markedly up-regulates beta-defensin-2 expression in human airway epithelium via JAK and NF-kappaB signaling pathways. J Immunol 173(5):3482–3491PubMedCrossRef
108.
go back to reference Liang SC, Tan XY, Luxenberg DP, Karim R, Dunussi-Joannopoulos K, Collins M, Fouser LA (2006) Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 203(10):2271–2279. doi:10.1084/jem.20061308 PubMedPubMedCentralCrossRef Liang SC, Tan XY, Luxenberg DP, Karim R, Dunussi-Joannopoulos K, Collins M, Fouser LA (2006) Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 203(10):2271–2279. doi:10.​1084/​jem.​20061308 PubMedPubMedCentralCrossRef
109.
go back to reference Ling WL, Wang LJ, Pong JC, Lau AS, Li JC (2013) A role for interleukin-17A in modulating intracellular survival of Mycobacterium bovis bacillus Calmette-Guerin in murine macrophages. Immunology 140(3):323–334. doi:10.1111/imm.12140 PubMedPubMedCentral Ling WL, Wang LJ, Pong JC, Lau AS, Li JC (2013) A role for interleukin-17A in modulating intracellular survival of Mycobacterium bovis bacillus Calmette-Guerin in murine macrophages. Immunology 140(3):323–334. doi:10.​1111/​imm.​12140 PubMedPubMedCentral
113.
go back to reference Stange J, Hepworth MR, Rausch S, Zajic L, Kuhl AA, Uyttenhove C, Renauld JC, Hartmann S, Lucius R (2012) IL-22 mediates host defense against an intestinal intracellular parasite in the absence of IFN-gamma at the cost of Th17-driven immunopathology. J Immunol 188(5):2410–2418. doi:10.4049/jimmunol.1102062 PubMedCrossRef Stange J, Hepworth MR, Rausch S, Zajic L, Kuhl AA, Uyttenhove C, Renauld JC, Hartmann S, Lucius R (2012) IL-22 mediates host defense against an intestinal intracellular parasite in the absence of IFN-gamma at the cost of Th17-driven immunopathology. J Immunol 188(5):2410–2418. doi:10.​4049/​jimmunol.​1102062 PubMedCrossRef
115.
go back to reference Trajkovic V, Stosic-Grujicic S, Samardzic T, Markovic M, Miljkovic D, Ramic Z, Mostarica Stojkovic M (2001) Interleukin-17 stimulates inducible nitric oxide synthase activation in rodent astrocytes. J Neuroimmunol 119(2):183–191PubMedCrossRef Trajkovic V, Stosic-Grujicic S, Samardzic T, Markovic M, Miljkovic D, Ramic Z, Mostarica Stojkovic M (2001) Interleukin-17 stimulates inducible nitric oxide synthase activation in rodent astrocytes. J Neuroimmunol 119(2):183–191PubMedCrossRef
118.
go back to reference Woodward TE (1982) Murine and epidemic typhus rickettsiae: how close is their relationship? Yale J Biol Med 55(3–4):335–341PubMedPubMedCentral Woodward TE (1982) Murine and epidemic typhus rickettsiae: how close is their relationship? Yale J Biol Med 55(3–4):335–341PubMedPubMedCentral
119.
go back to reference Jerrells TR, Jarboe DL, Eisemann CS (1986) Cross-reactive lymphocyte responses and protective immunity against other spotted fever group rickettsiae in mice immunized with Rickettsia conorii. Infect Immun 51(3):832–837PubMedPubMedCentral Jerrells TR, Jarboe DL, Eisemann CS (1986) Cross-reactive lymphocyte responses and protective immunity against other spotted fever group rickettsiae in mice immunized with Rickettsia conorii. Infect Immun 51(3):832–837PubMedPubMedCentral
120.
go back to reference Feng HM, Walker DH (2003) Cross-protection between distantly related spotted fever group rickettsiae. Vaccine 21(25–26):3901–3905PubMedCrossRef Feng HM, Walker DH (2003) Cross-protection between distantly related spotted fever group rickettsiae. Vaccine 21(25–26):3901–3905PubMedCrossRef
121.
go back to reference Valbuena G, Jordan JM, Walker DH (2004) T cells mediate cross-protective immunity between spotted fever group rickettsiae and typhus group rickettsiae. J Infect Dis 190(7):1221–1227. doi:10.1086/423819 PubMedCrossRef Valbuena G, Jordan JM, Walker DH (2004) T cells mediate cross-protective immunity between spotted fever group rickettsiae and typhus group rickettsiae. J Infect Dis 190(7):1221–1227. doi:10.​1086/​423819 PubMedCrossRef
124.
go back to reference Li Z, Diaz-Montero CM, Valbuena G, Yu XJ, Olano JP, Feng HM, Walker DH (2003) Identification of CD8 T-lymphocyte epitopes in OmpB of Rickettsia conorii. Infect Immun 71(7):3920–3926PubMedPubMedCentralCrossRef Li Z, Diaz-Montero CM, Valbuena G, Yu XJ, Olano JP, Feng HM, Walker DH (2003) Identification of CD8 T-lymphocyte epitopes in OmpB of Rickettsia conorii. Infect Immun 71(7):3920–3926PubMedPubMedCentralCrossRef
125.
go back to reference Hickman CJ, Stover CK, Joseph SW, Oaks EV (1991) Molecular cloning and sequence analysis of a Rickettsia tsutsugamushi 22 kDa antigen containing B- and T-cell epitopes. Microb Pathog 11(1):19–31PubMedCrossRef Hickman CJ, Stover CK, Joseph SW, Oaks EV (1991) Molecular cloning and sequence analysis of a Rickettsia tsutsugamushi 22 kDa antigen containing B- and T-cell epitopes. Microb Pathog 11(1):19–31PubMedCrossRef
Metadata
Title
Immune response against rickettsiae: lessons from murine infection models
Author
Anke Osterloh
Publication date
01-12-2017
Publisher
Springer Berlin Heidelberg
Published in
Medical Microbiology and Immunology / Issue 6/2017
Print ISSN: 0300-8584
Electronic ISSN: 1432-1831
DOI
https://doi.org/10.1007/s00430-017-0514-1

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