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Grahamii Bartonella Intraerythrocytic Mouse Cutting Edge: Antibody-Mediated Cessation of Hemotropic Infection by the Intraerythrocytic Mouse Pathogen Bartonella grahamii This information is current as of September 27, 2021. Jan Koesling, Toni Aebischer, Christine Falch, Ralf Schülein and Christoph Dehio J Immunol 2001; 167:11-14; ; doi: 10.4049/jimmunol.167.1.11 http://www.jimmunol.org/content/167/1/11 Downloaded from References This article cites 30 articles, 9 of which you can access for free at: http://www.jimmunol.org/content/167/1/11.full#ref-list-1 http://www.jimmunol.org/ Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication by guest on September 27, 2021 *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 © 2001 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. ● Cutting Edge: Antibody-Mediated Cessation of Hemotropic Infection by the Intraerythrocytic Mouse Pathogen Bartonella grahamii1 Jan Koesling,* Toni Aebischer,* Christine Falch,† Ralf Schu¨lein,†‡ and Christoph Dehio2†‡ studied in most detail in rats experimentally infected by Bar- The genus Bartonella includes important human-specific and tonella tribocorum (6). After residing in an unknown primary zoonotic pathogens which cause intraerythrocytic bacteremia niche, the onset of bacteremia in this model occurs 5–6 days Downloaded from in their mammalian reservoir host(s). It is accepted that cel- postinfection by a synchronous wave of bacterial adhesion and lular immunity plays a decisive role in the host’s defense invasion into mature erythrocytes. The intracellular bacteria against most intracellular bacteria. Bartonella sp. infection in replicate until reaching a steady number, which is sustained for the immunocompetent host typically leads to immunity against the remaining life span of the infected erythrocytes (eventually homologous challenge. The basis of this immunity, be it cellu- exceeding several weeks). The initial wave of erythrocyte in- lar or humoral, is unclear. In this study, the course of Bar- fection is followed by reinfection waves occurring in intervals tonella grahamii bacteremia in immunocompetent and immu- of 3–6 days. As found similarly in other animal models of Bar- http://www.jimmunol.org/ nocompromised mice was compared. In immunocompetent tonella infection (7–10), the phase of intraerythrocytic bactere- hosts, the bacteremia is transient and induces a strong hu- mia subsides spontaneously after a few months (typically 8–10 wk). moral immune response. In contrast, bacteremia persists in The infection triggers an immune response which confers protective immunocompromised B and T cell-deficient mice. Immune se- immunity as challenging convalescent animals with the same Bar- rum transfer beginning with day 6 postinfection to B cell-de- tonella strain does not result in reinfection (7, 10), whereas challeng- ficient mice unable to produce Igs converted the persistent bac- ing with a different Bartonella strain may again cause bacteremia (10). teremia to a transient course indistinguishable from that of However, the immune effector mechanism(s) mediating termination immunocompetent animals. These data demonstrate an essen- of Bartonella bacteremia are not yet elucidated. Both a humoral im- by guest on September 27, 2021 tial role for specific Abs in abrogating the intraerythrocytic mune response with high IgG titers (10) as well as a cellular immune response by T cell activation (8, 11–13) can be triggered by Bar- bacteremia of B. grahamii in mice. The Journal of Immunol- tonella infection. Classical studies of intracellular pathogens such as ogy, 2001, 167: 11–14. Listeria monocytogenes and Mycobacterium tuberculosis have pro- vided evidence for a critical role for cellular immunity in host defense wo Bartonella species, Bartonella bacilliformis and (14, 15). Therefore, cellular immune responses have long been con- Bartonella quintana, cause hemotropic infection in hu- sidered to be a hallmark of immunity to intracellular bacterial patho- T mans known as oroya fever (1) and trench fever (2), gens (16). However, erythrocytes cannot present Ags to the immune respectively. In the last decade, a number of Bartonella spp. system in a MHC-dependent way due to the lack of MHC on their naturally causing hemotropic infection in various mammals surface. Intraerythrocytic bartonellae should thus be hidden from a (i.e., cats, dogs, rats, and mice) have been associated with an respective cellular immune response. A growing body of evidence expanding spectrum of human diseases (3–5). The intraeryth- suggests that Ab can contribute to immunity against several other rocytic lifestyle appears to be the common parasitic strategy of intracellular pathogens (reviewed in Ref. 17), such as Salmonella (18, all Bartonella spp. in their respective mammalian reservoirs. 19), Mycobacterium (20), Legionella (21), Brucella (22), and Plas- The process of erythrocyte parasitism by Bartonella has been modium (23). A better understanding of the host immune response(s) interfering with Bartonella infections may facilitate the design of strategies to control these emerging pathogens. To this end, we have *Department of Molecular Biology, Max Planck Institute for Infection Biology, Ber- established a mouse model of transient Bartonella bacteremia in wild- lin, Germany; †Department of Infection Biology, Max Planck Institute for Biology, type and persistent bacteremia in B cell-deficient strains. Further by ‡ Tubingen, Germany; and Department of Molecular Microbiology, Biozentrum of the immune serum transfer we formally demonstrate that Abs are re- University of Basel, Basel, Switzerland quired for immune control of intraerythrocytic Bartonella infection Received for publication February 7, 2001. Accepted for publication May 7, 2001. in mice. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. 1 This work was supported by Deutsche Forschungsgemeinschaft Grant De 539/4-1 Materials and Methods and Swiss National Science Foundation Grant 3100-061777.00/1 (both to C.D.). Mice, bacteria, and infection 2 Address correspondence and reprint requests to Dr. Christoph Dehio, Department of Molecular Microbiology, Biozentrum of the University of Basel, Klingelbergstrasse Six- to 8-wk-old female BALB/c mice were purchased from Harlan and 70, CH-4056 Basel, Switzerland. E-mail address: [email protected] Winkelmann (Borchen, Germany), C57BL/6 from Bundesinstitut fu¨r Copyright © 2001 by The American Association of Immunologists 0022-1767/01/$02.00 ● 12 CUTTING EDGE: Ab-MEDIATED CESSATION OF Bartonella INFECTION gesundheitlichen Verbraucherschutz und Veterina¨rmedizin (Berlin, Ger- many), C57BL/6-IghϪ/Ϫ (IghϪ/Ϫ) and C57BL/6-Rag1Ϫ/Ϫ (RagϪ/Ϫ) mice from The Jackson Laboratory (Bar Harbor, ME). A Bartonella isolate from field-vole (strain IBS 376, generously provided by Yves Pie´mont, Stras- bourg, France) was identified as B. grahamii by sequence analysis of the citrate synthase gene (gltA) as previously described (24). Bacteria were cultivated on Columbia blood agar with 5% defibrinated sheep blood 3 ϫ 9 (CB-agar) at 35°C and 5% CO2 for 7 days, and 2 10 CFU suspended in 200 ␮l PBS were injected i.v. Bacteremia was analyzed by plating citrate blood samples previously frozen at Ϫ80°C on CB-agar and CFU enumeration. Serum transfer experiments Serum was obtained from blood pooled from 20 C57BL/6 mice. Normal serum was collected from naive mice and immune serum from mice 40–82 days postinfection. To increase the Ig concentration, serum precipitation was performed with 45% ammonium sulfate (25). The precipitate was di- alyzed against PBS. On days 6, 11, 18, and 32 postinfection, 1 mg protein of normal or immune serum precipitate within 300 ␮l PBS or PBS alone was injected i.v. into B. grahamii-infected mice. ELISA Downloaded from Ab titers were determined colorimetrically by solid-phase ELISA essen- tially as described (26), except that B. grahamii whole cell lysate was used for Ag coating of microtiter plates. In brief, dilutions of serum samples were added into Ag-coated microtiter plates. For detection, HRP-conju- gated rat anti-mouse IgG1 or IgG2a (Nordic, Tilburg, The Netherlands) and orthophenyldiamine-supplemented peroxide were used. Absorbance was measured at 492 nm. http://www.jimmunol.org/ Intraeythrocytic bacteria The gentamicin protection assay was performed as described previously (6). Blood smears were stained by SpotTest acridine orange stain as specified by the manufacturer (Difco, Detroit, MI) and fluorescent in- traerythrocytic bacteria were visualized by a Leica DM IRBE inverted fluorescence microscope (Leica, Deerfield, IL) using filter block GFP. Results and Discussion B. grahamii has been isolated from the blood of various small by guest on September 27, 2021 woodland mammals
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