Overproduction of TNF-α by CD8+ Type 1 Cells and Down-Regulation of IFN-γ Production by CD4+ Th1 Cells Contribute to Toxic Shock-Like Syndrome in an Animal Model of Fatal Monocytotropic Ehrlichiosis

Journal of Immunology

Volumn 172, Issue 3, 2004, Pages 1786-1800

  Ismail, Nahed ^a   Soong, Lynn ^a,b   McBride, Jere W ^a   Valbuena, Gustavo ^a   Olano, Juan P ^a   Feng, Hui Min ^a   Walker, David H ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; DOWN REGULATION; EHRLICHIA; EHRLICHIA CHAFFEENSIS; EHRLICHIA MURIS; EHRLICHIOSIS; IMMUNOPATHOLOGY; IXODES; LETHALITY; LIVER INJURY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN; TH1 CELL; TOXIC SHOCK SYNDROME;

EID: 1642525700     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.172.3.1786     Document Type: Article

References (55)

1. Olano, J. P., and D. H. Walker. 2002. Human ehrlichioses. Med. Clin. North Am. 86:375.
2. Walker, D. H., and J. S. Dumler. 1997. Human monocytotic and granulocytic ehrlichioses: discovery and diagnosis of emerging tick-borne infections and the critical role of the pathologist. Arch. Pathol. Lab. Med. 121:785.
3. Dumler, J. S., and D. H. Walker. 2001. Tick-borne ehrlichiosis. Lancet 21:478.
4. Paddock, C. D., D. P. Suchard, K. L. Grumbach, W. K. Hadley, R. L. Kerschmann, N. W. Abbey, J. E. Dawson, B. E. Anderson, K. G. Sims, J. S. Dumler, et al. 1993. Brief report: fatal seronegative ehrlichiosis in a patient with HIV infection. N. Engl. J. Med. 329:1164.
5. Fishbein, D. B., J. E. Dawson, and L. E. Robinson. 1994. Human ehrlichiosis in the United States, 1985 to 1990. Ann. Intern. Med. 120:736.
6. Childs, J. E., J. McQuiston, J. W. Summer, J. A. Comer, R. E. Massung, S. M. Standaert, and C. D. Paddock. 1994. Human monocytic ehrlichiosis due to Ehrlichia chaffeensis: how do we count the cases? In Rickettsiae and Rickettsial Diseases at the Turn of the Third Millenium. D. Raoult and P. Brouqui, eds. Elsevier, Paris, p. 287.
7. Fichtenbaum, C. J., L. R. Peterson, and G. J. Weil. 1993. Ehrlichiosis presenting as a life-threatening illness with features of the toxic shock syndrome. Am. J. Med. 95:351.
8. Winslow, G. M., E. Yager, K. Shilo, D. N. Collins, and F. K. Chu. 1998. Infection of the laboratory mouse with the intracellular pathogen Ehrlichia chaffeenis. Infect. Immun. 66:3892.
9. Li, J. S., E. Yager, M. Reilly, C. Freeman, G. R. Reddy, A. A. Reilly, F. K. Chu, and M. Winslow. 2001. Outer membrane protein-specific monoclonal antibodies protect SCID mice from fatal infection by the obligate intracellular bacterial pathogen Ehrlichia chaffeensis. J. Immunol. 166:1855.
10. Ganta, R. R., M. J. Wilkerson, C. Cheng, A. M. Rokey, and S. K. Chapes. 2002. Persistent Ehrlichia chaffeensis infection occurs in the absence of functional major histocompatibility complex class II genes. Infect. Immun. 70:380.
11. Shibata, S., M. Kawahara, Y. Rikihisa, H. Fujita, Y. Watanabe, C. Suto, and T. Ito. 2000. New Ehrlichia species closely related to Ehrlichia chaffeensis isolated from Ixodes ovatus ticks in Japan. J. Clin. Microbiol. 38:1331.
12. Sotomayor, E. A., V. L. Popov, H-M. Feng, D. H. Walker, and J. P. Olano. 2001. Animal model of fatal human monocytotropic ehrlichiosis. Am. J. Pathol. 158:757.
13. Kawahara, M., T. Ito, C. Suto, S. Shibata, Y. Rikihisa. K. Hata, and K. Hirai. 1999. Comparison of Ehrlichia muris strains isolated from wild mice and ticks and serologic survey of humans and animals with E. muris as antigen. J. Clin. Microbiol. 37:1123.
14. Sumner, J. W., G. A. Storch, R. S. Buller, A. M. Liddell, S. L. Stockham, Y. Rikihisa, S. Messenger, and C. D. Paddock. 2000. PCR amplification and phylogenetic analysis of groESL operon sequences from Ehrlichia ewingii and Ehrlichia muris. J. Clin. Microbiol. 38:2746.
15. Shibata, S., M. Kawahara, Y. Rikihisa, H. Fujita, Y. Watanabe, C. Suto, and T. Ito. 2000. New Ehrlichia species closely related to Ehrlichia Ehrlichia chaffeensis isolated from Ixodes avatus ticks in Japan. J. Clin. Microbiol. 38:1331.
16. Yu, X. J., X. F. Zhang, J. W. McBride, Y. Zhang, and D. H. Walker. 2001. Phylogenetic relationships of Anaplasma marginale and 'Ehrlichia platys' to other Ehrlichia species determined by GroEL amino acid sequences. Int. J. Syst. Evol. Microbiol. 51:1143.
17. McBride, J. W., X. J. Yu. and D. H. Walker. 2000. A conserved, transcriptionally active p28 multigene locus of Ehrlichia canis. Gene 254:245.
18. Ohashi, N., Y. Rikihisa, and A. Unver. 2001. Analysis of transcriptionally active gene clusters of major outer membrane protein multigene family in Ehrlichia canis and E. chaffeensis. Infect. Immun. 69:2083.
19. Alleman, A. R., A. F. Barbet, M. V. Bowie, H. L. Sorenson, S. J. Wong, and M. Belanger. 2000. Expression of a gene encoding the major antigenic protein 2 homolog of Ehrlichia chaffeensis and potential application for serodiagnosis. J. Clin. Microbiol. 38:3705.
20. Alleman, A. R., L. J. McSherry, A. F. Barbet, E. B. Breitschwerdt, H. L. Sorenson. M. V. Bowie, and M. Belanger. 2001. Recombinant major antigenic protein 2 of Ehrlichia canis: a potential diagnostic tool. J. Clin. Microbiol. 39:2494.
21. McBride, J. W., R. E. Corstvet, S. D. Gaunt SD, C. Boudreaux, T. Guedry, and D. H. Walker. 2003. Kinetics of antibody response to Ehrlichia canis immunoreactive proteins. Infect. Immun. 71:2516.
22. + T cells from murine spleen via nylon wool adherence and an optimized antibody cocktail. J. Immunol. Methods 258:55.
23. Favre, N., G. Bordmann, and W. Rudin. 1997. Comparison of cytokine measurements using ELISA, ELISPOT and semi-quantitative RT-PCR. J. Immunol. Methods 204:57.
24. Power, C. A., C. L. Grand, N. Ismail, N. C. Peters, D. P. Yurkowski, and P. A. Bretscher. 1999. A valid ELISPOT assay for enumeration of ex vivo, antigen-specific, IFN-γ-producing T cells. J. Immunol. Methods 227:99.
25. Huong, P. L., A. H. Kolk, T. A. Eggelte, C. P. Verstijnen, H. Gilis, and J. T. Hendriks. 1991. Measurement of antigen specific lymphocyte proliferation using 5-bromo-deoxyuridine incorporation: an easy and low cost alternative to radioactive thymidine incorporation. J. Immunol. Methods 140:243.
26. Hack, C. E., L. A. Aarden, and L. G. Thijs. 1997. Role of cytokine in sepsis. Adv. Immunol. 66:101.
27. Park, A. Y., B. D. Hondowicz, and P. Scott. 2000. IL-12 is required to maintain a Th1 response during Leishmania major infection. J. Immunol. 165:896.
28. Sypek, J. P., C. L. Chung, S. E. Mayor, J. M. Subramanyam, S. J. Goldman, D. S. Sieburth, S. F. Wolf, and R. G. Schaub. 1993. Resolution of cutaneous leishmaniasis: interleukin-12 initiates a protective T helper type I immune response. J. Exp. Med. 177:1797.
29. Leist, M., F. Gantner, I. Bohlinger, G. Tiegs, P. Germann, and A. Wendel. 1995. Tumor necrosis factor-induced hepatocyte apoptosis precedes liver failure in experimental murine shock models. Am. J. Pathol. 146:1220.
30. Leist, M., F. Gantner, I. Bohlinger, P. G. Germann, G. Tiegs, and A. Wendel. 1994. Murine hepatocyte apoptosis induced in vitro and in vivo by TNF-α requires transcriptional arrest. J. Immunol. 153:1778.
31. Bradham, C., J. Plumpe, M. Manns, D. Brenner, and C. Trautwein. 1998. Mechanisms of hepatic toxicity: TNF-induced liver injury. Am. J. Physiol. 275:G387.
32. Anthony, J. M., B. L. Rosa, Y. V. Gessel, A. Alcaraz, S. K. Bliss, E. J. Pearce, and E. Y. Denkers. 1999. Toxoplasma gondii and Schistosoma mansoni synergize to promote hepatocyte dysfunction associated with high levels of plasma TNF-α and early death in C57BL/6 mice. J. Immunol. 163:2089.
33. + T cell knockout, and normal C57BL/6 mice. Vet. Parasitol. 93:159.
34. Rikihisa, Y. 1991. The tribe Ehrlichieae and Ehrlichial diseases. Clin. Microbiol Rev. 4:286.
35. Dasch G. A., E. Weiss, J. C. Williams. 1990. Antigenic properties of the ehrlichiae and other rickettsiae. In Ehrlichiosis: A Vector Borne Illness of Animals And Humans. J. C. Williams and I. Kakoma, eds. Kluwer Academic. Boston, p. 323.
36. Miethke, T., C. Wahl, K. Heeg, B. Echtenacher, P. H. Krammer, and H. Wagner. 1992. T cell-mediated lethal shock triggered in mice by the superantigen staphylococcal enterotoxin B: critical role of tumor necrosis factor. J. Exp. Med. 175:91.
37. Henderson, B., S. Poole, and M. Wilson. 1996. Bacterial modulins: a novel class of virulence factors which cause host tissue pathology by inducing cytokine synthesis. Microbiol. Rev. 60:316.
38. Mordue, D. G., F. Monroy, M. La Regina, C. A. Dinarello, and L. D. Sibley. 2001. Acute toxoplasmosis leads to lethal overproduction of Th1 cytokines. J. Immunol. 167:4574.
39. Hodge-Defour, J., M. W. Marino, M. R. Horton, A. Jungbluth, M. D. Burdick. R. M. Stricter, P. W. Noble, C. A. Hunter, and E. Pure. 1998. Inhibition or interferon γ induced interleukin 12 production: a potential mechanism for the anti-inflammatory activities of tumor necrosis factor. Proc. Natl. Acad. Sci. USA 95:13806.
40. + T cells and accompanied by overproduction of IL-12, IFN-γ and TNF-α. J. Immunol. 157:798.
41. Schopf, L. R., K. F. Hoffmann, A. W. Cheever, J. F. Urban, and T. A. Wynn. 2002. IL-10 is critical for host resistance and survival during gastrointestinal helminth infection. J. Immunol. 168:2383.
42. + T cells during Mycobacterium tuberculosis infection. J. Immunol. 167:699.
43. + T-cell responses against malaria liver stages. Nat. Med. 8:166.
44. + T cells. Infect. Immun. 70:434.
45. Ismail, N., P. Olano, H. M. Feng, and D. H. Walker. 2002. Current status of immune mechanisms of killing of intracellular microorganisms. FEMS Microb. Lett. 207:111.
46. Unanue, E. R. 1997. Inter-relationships among macrophages, natural killer cells and neutrophils in early stages of Listeria resistance. Curr. Opin. Immunol. 9:35.
47. Feng, H. M., V. L. Popov, and D. H. Walker. 1994. Depletion of γ interferon and tumor necrosis factor a in mice with Rickettsia conorii-infected endothelium: impairment of rickettsicidal nitric oxide production resulting in fatal, overwhelming rickettsial disease. Infect. Immun. 62:1952.
48. Barnewall, R. E., and Y. Rikihisa. 1994. Abrogation of γ interferon-induced inhibition of Ehrlichia chaffeensis infection in human monocytes with iron-transferrin. Infect. Immun. 62:4804.
49. Barnewall, R. E., N. Ohashi, and Y. Rikihisa. 1999. Ehrlichia chaffeensis and E. sennetsu, but not the human granulocytic ehrlichiosis agent, colocalize with transferrin receptor and up-regulate tranferrin receptor mRNA by activating iron-responsive protein. Infect. Immun. 67:2258.
50. + cells but markedly decreased helper cell activity in mice lacking CD4. Nature 353:180.
51. Shedlock, D. J., J. K. Whitmire, J. Tan, A. S. MacDonald, R. Ahmed, and H. Shen. 2003. Role of CD4 T cell help and costimulation in CD8 T cell responses during Listeria monocytogenes infection. J. Immunol. 170:2053.
52. + T cells. J. Immunol. 167:560.3.
53. + T cell responses: the alternative approaches. Annu. Rev. Immunol. 15:297.
54. Erbe, D. V., E. R. Pfefferkorn, and M. W. Fanger. 1991. Functions of the various IgG Fe receptors in mediating killing of Toxoplasma gondii. J. Immunol. 146:3145.
55. Li, J. S., F. Chu, A. Reilly, and G. M. Winslow. 2002. Antibodies highly effective in SCID mice during infection by the intracellular bacterium Ehrlichia chaffeensis are of picomolar affinity and exhibit preferential epitope and isotype utilization. J. Immunol. 169:1419.