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Infection Toxoplasma Gondii Susceptibility During Neutrophil CXCR2 Deficiency Confers Impaired Neutrophil Recruitment and Increased Susceptibility During Toxoplasma gondii Infection This information is current as of September 24, 2021. Laura Del Rio, Soumaya Bennouna, Jesus Salinas and Eric Y. Denkers J Immunol 2001; 167:6503-6509; ; doi: 10.4049/jimmunol.167.11.6503 http://www.jimmunol.org/content/167/11/6503 Downloaded from References This article cites 56 articles, 36 of which you can access for free at: http://www.jimmunol.org/content/167/11/6503.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 24, 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. CXCR2 Deficiency Confers Impaired Neutrophil Recruitment and Increased Susceptibility During Toxoplasma gondii Infection1 Laura Del Rio,† Soumaya Bennouna,* Jesus Salinas,† and Eric Y. Denkers*2 Neutrophil migration to the site of infection is a critical early step in host immunity to microbial pathogens, in which chemokines and their receptors play an important role. In this work, mice deficient in expression of the chemokine receptor CXCR2 were infected with Toxoplasma gondii and the outcome was monitored. Gene-deleted animals displayed completely defective neutrophil recruitment, which was apparent at 4 h and sustained for at least 36 h. KitW/KitW-v animals also displayed defective polymor- phonuclear leukocyte migration, suggesting mast cells as one source of chemokines driving the response. Tachyzoite infection and ؊/؊ replication were accelerated in CXCR2 animals, resulting in establishment of higher cyst numbers in the brain relative to Downloaded from wild-type controls. Furthermore, serum and spleen cell IFN-␥ levels in infected, gene-deleted mice were reduced 60–75% relative to infected normal animals, and spleen cell TNF-␣ was likewise reduced by ϳ50%. These results highlight an important role for CXCR2 in neutrophil migration, which may be important for early control of infection and induction of immunity during Toxoplasma infection. The Journal of Immunology, 2001, 167: 6503–6509. he CXC chemokine IL-8 is an important chemoattractant tions worldwide. In situations of immunodeficiency and during http://www.jimmunol.org/ and activator of neutrophils (1–3). In humans, there are congenital infection, Toxoplasma emerges as a major opportunistic T two high-affinity receptors for IL-8, designated CXCR1 pathogen that can be lethal if not appropriately treated (13, 14). T. and CXCR2 (4, 5). Although mice do not possess a homologous gondii is well known as a potent type 1 cytokine inducer, and while IL-8 gene, they express a CXCR with similarity to human CXCR2 these cytokines are required to survive infection, their overproduc- which is expressed predominantly on neutrophils. The murine re- tion can lead to pathology and death (15–23). ceptor binds several IL-8-like CXC chemokines, most notably We and others recently reported a requirement for neutrophils in 3 macrophage inflammatory protein (MIP) -2 and KC (6). early resistance to T. gondii (24–27). Although these cells display Recently, mice with a targeted deletion of CXCR2, also known microbicidal activity through phagocytosis and release of super- as murine IL-8R homolog (IL-8RL), were constructed (7). The oxides and peroxides, it is also clear that PMN can serve as a by guest on September 24, 2021 animals display defective neutrophil migration in response to thio- source of several proinflammatory cytokines during infection. For glycolate, although the killing function of intracellular and extra- the case of Toxoplasma, PMN release IL-12 and TNF-␣, as well as cellular bacteria remains intact. In a model of urinary tract infec- chemokines such as MIP-1␣ and MIP-1␤, in response to parasite tion, transepithelial polymorphonuclear leukocyte (PMN) stimulation (25, 28, 29). In an in vitro model of infection, migration is defective, resulting in bacteremia and systemic dis- tachyzoites induced recruitment of large neutrophil numbers into ease (8–10). The murine IL-8R homolog has also been implicated the peritoneal cavity within4hofinjection (30). The PMN were in increased susceptibility during infections with pathogens such as Candida albicans and Legionella pneumophila (11, 12), but its found to be the major source of IL-12 in this model system, and role during protozoan infection has hitherto remained unexplored. Ab-mediated neutrophil depletion resulted in early death of the In our laboratory, we use the intracellular protozoan Toxo- animals, associated with defective type 1 cytokine responses (24). plasma gondii as a model to study initiation of immunity and early These results, and similar findings by others (31–36), led us to host resistance during microbial infection. Toxoplasmosis is a hypothesize that PMN, by virtue of their ability to rapidly migrate widespread parasitic infection among human and animal popula- to a site of infection and release proinflammatory cytokines, may be important immunoregulatory cells during the immune response to Toxoplasma. *Department of Microbiology and Immunology, College of Veterinary Medicine, In the present report, we examined the ability of CXCR2Ϫ/Ϫ Cornell University, Ithaca, NY 14853; and †Departamento de Patologia Animal (Mi- crobiologia e Immunologia), Facultad de Veterinaria, Universidad de Murcia, Murcia, mice to respond to T. gondii infection. Our results reveal a pro- Spain found defect in the ability of neutrophils to migrate into the peri- Received for publication June 8, 2001. Accepted for publication October 1, 2001. toneal cavity following tachyzoite inoculation. Production of The costs of publication of this article were defrayed in part by the payment of page proinflammatory cytokines, in particular TNF-␣ and IFN-␥, was charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. lower in CXCR2-deficient mice. The gene-deleted mice harbored more parasites in the peritoneal cavity during early infection and 1 This work was supported by National Institutes of Health Grant AI47888. L.D.R. was supported by Ministerio de Educacio´n y Cultura of Spain. greater brain cyst numbers during chronic infection. Mast cell- W W-v 2 Address correspondence and reprint requests to Dr. Eric Y. Denkers, Department of deficient (Kit /Kit ) mice also displayed a defective ability to Microbiology and Immunology, College of Veterinary Medicine, Cornell University, recruit PMN during early infection, suggesting that these cells Ithaca, NY 14853-6401. E-mail address: [email protected] serve as a major chemokine source involved in neutrophil recruit- 3 Abbreviations used in this paper: MIP, macrophage inflammatory protein; PMN, polymorphonuclear leukocyte; KO, knockout; STAg, soluble tachyzoite lysate Ag; ment. Our results suggest that CXCR2 is required for early WT, wild type; PEC, peritoneal exudate cell; IL-8Rh, IL-8R homolog. neutrophil recruitment, and that this chemokine receptor and its Copyright © 2001 by The American Association of Immunologists 0022-1767/01/$02.00 6504 CXCR2 DEFICIENCY DURING T. gondii INFECTION ligands play an important protective role in resistance to PECs Toxoplasma. Peritoneal exudate cells (PEC; 2 ϫ 105 per sample) collected by peritoneal lavage with 10 ml of PBS were cytospun (700 rpm for 5 min) onto glass microscope slides (VWR Scientific, Rochester, NY) using cytofunnels Materials and Methods (Thermo Shandon, Pittsburgh, PA). To determine the composition of PEC Mice and the number of parasites, differential counts were performed on Diff- Quick-stained (American Scientific Products, McGraw Park, IL) cytocen- Female BALB/c and 129/J mice (6–8 wk of age) were obtained from The trifuge slides. A minimum of 300 cells were counted per slide. Jackson Laboratory (Bar Harbor, ME). Heterozygous CXCR2 knockout (KO) mice (C.129S2(B6)-Cmkartm1/Mwm) were purchased from The Jack- Spleen cell culture son Laboratory and bred at the College of Veterinary Medicine animal Spleens were collected from mice 7 days after i.p. infection with 100 ME49 facility (Cornell University, Ithaca, NY). The KO animals were originally cysts. After gentle mashing, cells were suspended in complete DMEM engineered by homologous recombination of a defective CXCR2 gene into consisting of 10% FCS, 1 mM sodium pyruvate, 0.1 mM nonessential 129 embryonic stem cells, followed by transplantation into C57BL/6 blas- amino acids, 10 mM HEPES buffer, 100 U/ml penicillin, 0.1 mg/ml strep- tocysts. Resulting chimeric animals were backcrossed onto a BALB/c tomycin (all from Life Technologies), and 50 mM 2-ME (Sigma-Aldrich). background for 10 generations (7). After genotyping for the CXCR2 gene, The resulting single cell suspension was centrifuged for 7 min at 1,000 ϫ a colony of homozygous KO mice was established and used in the studies g, supernatant was decanted, and erythrocytes were lysed using erythrocyte described. Female KO animals were age-matched to wild-type (WT) con- W W-v ϩ/ϩ lysis buffer (Sigma-Aldrich). Cells were cultured (37°C; 5% CO2)indu- trols. Mast cell-deficient Kit /Kit and congenic normal WBB6F1 plicate wells of 96-well plates (Costar, Cambridge, MA) at a concentration littermates were obtained from The Jackson Laboratory. The mice were of 5 ϫ 106 cells/ml with medium or STAg (2 ␮g/ml). After 24 or 48 h, housed under specific pathogen-free conditions in the College of Veteri- supernatants were collected and stored at Ϫ20°C until assayed.
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