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Listeria Monocytogenes and Tuberculosis Mycobacterium Intracellular Pathogens Involved in Controlling Infections with the Recept

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Listeria Monocytogenes and Tuberculosis Mycobacterium Intracellular Pathogens Involved in Controlling Infections with the Recept The Journal of Immunology The Lymphotoxin ␤ Receptor Is Critically Involved in Controlling Infections with the Intracellular Pathogens Mycobacterium tuberculosis and Listeria monocytogenes1 Stefan Ehlers,2* Christoph Ho¨lscher,* Stefanie Scheu,† Christine Tertilt,† Thomas Hehlgans,‡ Johanna Suwinski,* Robert Endres,† and Klaus Pfeffer3† Containment of intracellularly viable microorganisms requires an intricate cooperation between macrophages and T cells, the most potent mediators known to date being IFN-␥ and TNF. To identify novel mechanisms involved in combating intracellular infections, experiments were performed in mice with selective defects in the lymphotoxin (LT)/LT␤R pathway. When mice deficient in LT␣ or LT␤ were challenged intranasally with Mycobacterium tuberculosis, they showed a significant increase in bacterial loads in lungs and livers compared with wild-type mice, suggesting a role for LT␣␤ heterotrimers in resistance to ␣ ␤ ␤ infection. Indeed, mice deficient in the receptor for LT 1 2 heterotrimers (LT R-knockout (KO) mice) also had significantly higher numbers of M. tuberculosis in infected lungs and exhibited widespread pulmonary necrosis already by day 35 after intranasal infection. Furthermore, LT␤R-KO mice were dramatically more susceptible than wild-type mice to i.p. infection with Listeria monocytogenes. Compared with wild-type mice, LT␤R-KO mice had similar transcript levels of TNF and IFN-␥ and recruited similar numbers of CD3؉ T cells inside granulomatous lesions in M. tuberculosis-infected lungs. Flow cytometry revealed that the LT␤R is expressed on pulmonary macrophages obtained after digestion of M. tuberculosis-infected lungs. LT␤R-KO mice showed delayed expression of inducible NO synthase protein in granuloma macrophages, implicating deficient macrophage ac- tivation as the most likely cause for enhanced susceptibility of these mice to intracellular infections. Since LIGHT-KO mice proved ␣ ␤ to be equally resistant to M. tuberculosis infection as wild-type mice, these data demonstrate that signaling of LT 1 2 heterotri- mers via the LT␤R is an essential prerequisite for containment of intracellular pathogens. The Journal of Immunology, 2003, 170: 5210–5218. ycobacterium tuberculosis currently is the number one counter pathogens capable of surviving intracellularly need to be bacterial killer in the world. Eight to 10 million people reprogrammed by specific T cells, essentially via TNF and IFN-␥, M worldwide newly develop tuberculosis every year and to become fully competent in antibacterial functions, a process in for at least one-third of these patients the disease is lethal (1). which NO and superoxide generation act both as signaling and as These numbers are likely to rise with the emergence of multidrug- effector molecules (7). The concept of the activated macrophage resistant strains of M. tuberculosis and the increase of coinfection was originally established in the murine model of Listeria mono- with HIV. It is thus imperative to define the mechanisms that en- cytogenes infection which has since become a standard experimen- able the host to effectively contain M. tuberculosis infection to tal system for identifying the roles of newly discovered cells and enlist them in novel therapeutic strategies. mediators in response to intracellular pathogens (8, 9). Animal models have been instrumental in elucidating the mech- In addition, antibacterially inefficient host cells may need to be anisms of both protection and pathology in response to M. tuber- lysed and new effector cells, such as granulocytes and macro- culosis infection (2). In particular, the use of gene-targeted mice phages, must be recruited and activated to engulf and destroy the has provided incontrovertible evidence that an efficient coopera- released microorganisms (10–12). In the case of persistent myco- tion between T cells and macrophages is critical for control of bacteria, the close interaction of T cells and macrophages is facilitated infection (3–6). This is primarily because macrophages which en- in an organized microenvironment called granulomas, which at the same time serves as a physical barrier to dissemination of bacteria *Division of Molecular Infection Biology, Research Center Borstel, Borstel, Ger- released from incompetent macrophages (13). Therefore, granulomas many; †Institute of Medical Microbiology, Immunology and Hygiene, Technical Uni- are highly dynamic structures which are composed of effector cells versity, Munich, Germany; and ‡Institute of Pathology, University of Regensburg, that are chronically recruited and activated by stimuli such as chemo- Regensburg, Germany kines and IFN-␥- and TNF-mediated processes (14, 15). Received for publication August 8, 2002. Accepted for publication March 10, 2003. Lymphotoxin (LT)4 ␣,LT␤, and the recently identified TNF The costs of publication of this article were defrayed in part by the payment of page family member LIGHT (homologous to lymphotoxins, exhibits in- charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. ducible expression, and competes with HSV glycoprotein D for 1 This work was supported in part by Deutsche Forschungsgemeinschaft Grants SFB HVEM, a receptor expressed by T lymphocytes) along with the 391-B3, SFB 576-A6, and Pf 259/2-5/6 (to K.P.), Deutsche Forschungsgemeinschaft Grant SFB 367-C9 (to S.E.), and a research grant (Host Defense against Infections) from the University of Lu¨beck (to S.E.). 2 Address correspondence and reprint requests to Dr. Stefan Ehlers, Division of Mo- 4 Abbreviations used in this paper: LT, lymphotoxin; HVEM, herpesvirus entry me- lecular Infection Biology, Research Center Borstel, Parkallee 22, D-23845 Borstel, diator; LIGHT, ligand homologous to LTs, exhibits inducible expression, competes Germany. E-mail address: [email protected] with HSV glycoprotein D for HVEM, a receptor expressed by T lymphocytes; iNOS, 3 Current address: Institute of Medical Microbiology and Virology, Universita¨tsstrasse 1, inducible NO synthase; KO, knockout; BM, bone marrow; IKK, inhibitor of ␬B D-40225 Du¨sseldorf, Germany. kinase. Copyright © 2003 by The American Association of Immunologists, Inc. 0022-1767/03/$02.00 The Journal of Immunology 5211 prototype cytokine TNF may be defined as a core group of cyto- dilutions of the cultures on Middlebrook 7H10 agar plates followed by kines clustered within the growing TNF superfamily (16–19). The incubation at 37°C. Before infection of experimental animals, stock solu- specific cell surface receptors for the ligands of the TNF core fam- tions of M. tuberculosis were briefly sonicated and diluted in PBS. Pul- ␤ monary infection was performed by intranasal instillation. Mice were anes- ily are TNFRp55, TNFRp75, LT R and herpesvirus entry medi- thetized by i.p. injection of 1.25% ketamine (Bayer, Leverkusen, Germany) ator (HVEM) that reveal overlapping, but distinct ligand interac- and 0.025% Rompun (WDT, Garbsen, Germany) to fully suppress swal- ␮ tions (16, 20, 21). TNF3 binds to the TNFRp55 and TNFRp75, lowing reflexes. Intranasal instillation was performed by applying 20 lof 4 whereas LT␣ engages the TNFRp55, TNFRp75, and HVEM as a suspension containing 1–2.5 ϫ 10 CFU of M. tuberculosis/ml to the 3 nares of anesthetized mice. Actual inoculum size was determined 24 h after homotrimer (16, 20, 22). In combination with the membrane- infection by determining the bacterial load in the lungs of infected mice ␤ ␣ ␣ ␤ ␤ bound LT ,LT binds as the LT 1 2 heterotrimer to the LT R and is indicated in the figure legends. Bacterial loads in infected organs ␣ (16, 21, 23, 24). TNF3,LT 3 in concert with the TNFRp55, were were evaluated at different time points after infection with M. tuberculosis shown to be of critical importance for the host defense against to follow the course of infection. Lungs and livers of sacrificed animals intracellularly replicating bacterial pathogens and for the forma- (four to five mice per group) were removed and weighed aseptically and homogenized in distilled water. Ten-fold serial dilutions of organ homog- tion and maintenance of fully differentiated granulomas (25–31). enates were plated in duplicates onto Middlebrook 7H10 agar plates con- In contrast, the detailed role of the LT␤R and its cognate ligands taining 10% OADC and incubated at 37°C for 3 wk. Colonies on plates in antimicrobial resistance and granuloma formation has remained were enumerated and results expressed as log10 CFU per organ. unexplored. Infections with Listeria monocytogenes were performed as described ␤ previously (26). Briefly, overnight cultures of L. monocytogenes (ATCC To ascertain the functional relevance of the LT R for the im- strain 43251) were grown in brain-heart infusion (Difco), adjusted to an mune defense against intracellular microorganisms, we investi- OD of 0.75, and serially diluted in medium. Titrated numbers of L. mono- gated the course of infection in two infection models (M. tuber- cytogenes were i.p. inoculated in a volume of 350 ␮l into the mice. The culosis and L. monocytogenes) in mice deficient for the LT␤R, dose of bacteria was checked by plating 10-␮l aliquots of a serial 10-fold LT␣,LT␤, or LIGHT. Collectively, the results of this comprehen- dilution on Columbia blood agar plates and counting the CFU after over- ␣ ␤ ␤ night incubation at 37°C. Livers and spleens were removed 2 days after sive study indicate that LT 1 2 signaling via the LT Ronmac- infection, organ homogenates prepared, and bacterial counts determined as rophages is essential for controlling the infection with both above. pathogens. Histology and immunohistology Materials and Methods One lung lobe per mouse was fixed in 4% Formalin-PBS, set in paraffin Mice blocks, and sectioned (2–3 ␮m). Histology was performed using standard protocols for H&E staining and for acid-fast staining. For immunohistol- LT␤R-knockout (KO) (21), TNFRp55-KO (25), and LT␣-KO (32) were ogy, tissue sections were deparaffinized, placed in 10 mM sodium citrate ␤ N5 backcross generations to C57BL/6; LT -KO (23) were N10 backcrosses buffer (pH 6.0), and pressure-cooked for exactly 1.5 min. After blocking to C57BL/6.
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