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Model of Fatal Monocytotropic Ehrlichiosis Toxic Shock-Like 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 This information is current as Model of Fatal Monocytotropic Ehrlichiosis of September 29, 2021. Nahed Ismail, Lynn Soong, Jere W. McBride, Gustavo Valbuena, Juan P. Olano, Hui-Min Feng and David H. Walker J Immunol 2004; 172:1786-1800; ; Downloaded from doi: 10.4049/jimmunol.172.3.1786 http://www.jimmunol.org/content/172/3/1786 http://www.jimmunol.org/ References This article cites 53 articles, 31 of which you can access for free at: http://www.jimmunol.org/content/172/3/1786.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision by guest on September 29, 2021 • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2004 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Overproduction of TNF-␣ by CD8؉ Type 1 Cells and Down-Regulation of IFN-␥ Production by CD4؉ Th1 Cells Contribute to Toxic Shock-Like Syndrome in an Animal Model of Fatal Monocytotropic Ehrlichiosis1 Nahed Ismail,* Lynn Soong,*†‡§ Jere W. McBride,*‡ Gustavo Valbuena,* Juan P. Olano,*†‡ Hui-Min Feng,* and David H. Walker2*‡§ Human monocytotropic ehrlichiosis (HME) is an emerging, life-threatening, infectious disease caused by Ehrlichia chaffeensis,an obligate intracellular bacterium that lacks cell wall LPS. We have previously developed an animal model of severe HME using a strain of Ehrlichia isolated from Ixodes ovatus ticks (IOE). To understand the basis of susceptibility to severe monocytotropic Downloaded from ehrlichiosis, we compared low and high doses of the highly virulent IOE strain and the less virulent Ehrlichia muris strain that are closely related to E. chaffeensis in C57BL/6 mice. Lethal infections caused by high or low doses of IOE were accompanied by extensive liver damage, extremely elevated levels of TNF-␣ in the serum, high frequency of Ehrlichia-specific, TNF-␣-producing CD8؉ T cells in the spleen, decreased Ehrlicha-specific CD4؉ T cell proliferation, low IL-12 levels in the spleen, and a 40-fold decrease in the number of IFN-␥-producing CD4؉ Th1 cells. All groups contained negligible numbers of IL-4-producing cells in ؉ ؉ the spleen. Transfer of Ehrlichia-specific polyclonal Abs and IFN-␥-producing Ehrlichia-specific CD4 and CD8 type 1 cells http://www.jimmunol.org/ protected naive mice against lethal IOE challenge. Interestingly, infection with high dose E. muris provided protection against rechallenge with a lethal dose of IOE. Cross-protection was associated with substantial expansion of IFN-␥-producing CD4؉ and ,CD8؉ cells, but not TNF-␣-producing CD8؉ T cells, a high titer of IgG2a, and a low serum level of TNF-␣. In conclusion -uncontrolled TNF-␣ production by CD8؉ T cells together with a weak CD4؉ Th1 cell response are associated with immunopa thology and failure to clear IOE in the fatal model of HME. The Journal of Immunology, 2004, 172: 1786–1800. uman monocytotropic ehrlichiosis (HME)3 is an emerg- suggested that humoral immune responses play an important role ing, tick-borne, zoonotic disease caused by infection of during infections with E. chaffeensis and other related Ehrlichia H monocytes by the obligately intracellular bacterium, spp. (8). Although immunocompetent mice are generally resistant by guest on September 29, 2021 Ehrlichia chaffeensis (1–3). Infection of humans with E. chaffeen- to infection with E. chaffeensis, SCID mice are highly susceptible, sis results in a spectrum of clinical manifestations, ranging from developing persistent and fatal infection. Transfer of immune se- fatal to self-limited disease. In immunocompromised individuals, rum obtained from immunocompetent C57BL/6 mice as well as such as those infected with HIV (4) or treated with immunosup- Abs specific to the 28-kDa major outer membrane proteins of E. pressive drugs, E. chaffeensis infection can result in a severe, life- chaffeensis to C57BL/6 SCID mice provide significant, but tran- threatening disease. Immunocompetent individuals who do not re- sient, protection from disease (9). As infection of SCID mice with Ն ceive doxycycline treatment until 8 days after the onset of E. chaffeensis results in fatal disease with pathology that does not symptoms are also at increased risk of developing fatal HME. Se- mimic the histopathological findings in HME, SCID mice may not vere cases of HME are often comparable in severity to Rocky be a suitable model to elucidate the immunological basis of resis- Mountain spotted fever or toxic shock syndrome (5–7). tance and susceptibility to infection by monocytotropic ehrlichiae. Little is known about the host factors that influence susceptibil- The role of the cell-mediated response in the host defense ity and resistance to severe HME, although some studies have against Ehrlichia is supported by the observations that intracellular killing of E. chaffeensis requires CD4ϩ T cell-dependent cellular Departments of *Pathology and †Microbiology and Immunology, ‡Sealy Center for effector mechanisms, including NO production by IFN-␥-activated § Vaccine Development, and Center for Biodefense and Emerging Infectious Diseases, macrophages, and granulomatous inflammation (10). However, the University of Texas Medical Branch, Galveston, TX 77555 roles of CD4ϩ and CD8ϩ T cells and their cytokines in host de- Received for publication October 24, 2003. Accepted for publication November 18, 2003. fense and pathogenesis of the disease are not yet defined. The costs of publication of this article were defrayed in part by the payment of page In the present study we have analyzed the immunopathological charges. This article must therefore be hereby marked advertisement in accordance mechanisms associated with susceptibility or resistance to ehrli- with 18 U.S.C. Section 1734 solely to indicate this fact. chial infection, using two ehrlichial strains that are phylogeneti- 1 This work was supported by Grant AI31431 from the National Institute of Allergy cally related to E. chaffeensis. The first one is a highly virulent and Infectious Diseases. ehrlichial strain isolated from Ixodes ovatus ticks (IOE) native to 2 Address correspondence and reprint requests to Dr. David H. Walker, Department of Pathology, Center for Biodefense and Emerging Infectious Diseases, 301 Univer- Japan (11) that causes fatal disease in immunocompetent mice sity Boulevard, Galveston, TX 77555-0609. E-mail address: [email protected] (12). The second organism is a mildly virulent strain (Ehrlichia 3 Abbreviations used in this paper: HME, human monocytotropic ehrlichiosis; EM/ muris) that causes mild and self-limited disease in immunocom- IOE, mice primed with high dose E. muris and rechallenged with high dose IOE; IOE, Ixodes ovatus Ehrlichia; MOI, multiplicity of infection; OMP, outer membrane pro- petent mice (13). Phylogenetic analysis supports the close rela- tein; p.i., postinfection. tionships among monocytotropic Ehrlichia spp., including E. Copyright © 2004 by The American Association of Immunologists, Inc. 0022-1767/04/$02.00 The Journal of Immunology 1787 chaffeensis, E. muris, and IOE (14–17). Additionally, serological preparations was determined using a bicinchoninic acid protein assay kit cross-reactions occur between closely related monocytotropic Ehr- (Pierce, Rockford, IL) and was used as the Ag in ELISPOT assay and lichia species (18–20), attributed mainly to a molecularly charac- ELISA. The uninfected cell lysates were prepared similarly and used as a negative control (mock Ag). For preparation of host cell-free IOE Ag, terized major outer membrane proteins (p28) of Ehrlichia and ma- IOE-infected spleens and livers were harvested from day 7 infected mice, jor antigenic protein 2, the P28 orthologue identified in E. and cell-free IOE Ags were prepared as previously described (21). Spleen ruminantium (18–20). and liver of naive mice were prepared as the E. muris-infected P388D1 In this study we assessed the course of infection and immune cells and were used as a negative control in all experiments using cell-free IOE Ags (mock Ag). responses in C57BL/6 mice susceptible to fatal infection with IOE, but resistant to severe disease caused by E. muris infection. We ELISPOT assays for Ag-specific, cytokine-producing T cells also investigated whether a primary infection with E. muris can Single-cell suspensions were obtained from the spleen of control and in- protect mice against rechallenge with virulent IOE and analyzed fected mice. CD4ϩ and CD8ϩ T cells were isolated by negative selection the immunological correlates of this cross-protection. We provide using mouse CD4 or CD8 subset enrichment columns (R&D Systems, in this report compelling evidence that infection with virulent IOE Minneapolis, MN), and the purity ranged from 80–90% as determined by causes overproduction of TNF-␣ by Ag-specific
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