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Infection Trichuris Muris Failure to Expel in an Altered Th1/Th2

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Infection Trichuris Muris Failure to Expel in an Altered Th1/Th2 Absence of CC Chemokine Ligand 2 Results in an Altered Th1/Th2 Cytokine Balance and Failure to Expel Trichuris muris Infection This information is current as Matthew L. deSchoolmeester, Matthew C. Little, Barrett J. of September 29, 2021. Rollins and Kathryn J. Else J Immunol 2003; 170:4693-4700; ; doi: 10.4049/jimmunol.170.9.4693 http://www.jimmunol.org/content/170/9/4693 Downloaded from References This article cites 47 articles, 24 of which you can access for free at: http://www.jimmunol.org/content/170/9/4693.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 29, 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 © 2003 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Absence of CC Chemokine Ligand 2 Results in an Altered Th1/Th2 Cytokine Balance and Failure to Expel Trichuris muris Infection1 Matthew L. deSchoolmeester,2* Matthew C. Little,* Barrett J. Rollins,† and Kathryn J. Else* Despite a growing understanding of the role of cytokines in immunity to intestinal helminth infections, the importance of che- mokines has been neglected. As a chemokine with both chemoattractive properties and an ability to shape the quality of the adaptive immune response, CC chemokine ligand 2 (CCL2) was investigated as an attractive candidate for controlling resistance to these types of infection, which require highly polarized Th cell responses. We show here for the first time that CCL2 plays an important role in the development of resistance to infection by the gastrointestinal nematode Trichuris muris. Thus, in the absence of CCL2, worm expulsion does not occur, and the lymph node draining the site of infection becomes a Th1-promoting environ- ment. Elevated levels of IL-12 are produced by polarizing APCs, and the composition of the APC environment itself is perturbed, Downloaded from with reduced numbers of macrophages. The Journal of Immunology, 2003, 170: 4693–4700. richuris muris is a natural mouse model of the gastrointes- moattractant protein-1, was originally described as being chemo- tinal nematode parasite Trichuris trichiura, one of the most tactic for monocytes (11–13), but is now known to also be che- T prevalent human helminth infections worldwide. Strain motactic for human NK cells (14, 15), memory T cells (16), and variation in the mouse gives a spectrum of phenotypes varying basophils (17). In the mouse, CCL2 is a functional monocyte che- http://www.jimmunol.org/ from resistant strains such as BALB/c and C57BL/6, in which the moattractant in vivo (18–22), and CCL2-deficient mice are unable parasite is quickly expelled, to a completely susceptible strain such to recruit monocytes to sites of inflammation in a number of mod- as AKR, in which fecund adult worms survive in the intestine for els, including to the peritoneum after thioglycolate administration many weeks or months (1). It is now well established that a Th2- (23). Importantly with regard to the development of a Th2-biased dominated immune response, characterized by the production of immune response, CCL2 causes a decrease in IL-12 production IL-4, IL-5, IL-9, and IL-13, is an absolute requirement for worm from activated macrophages and monocytes (24, 25). Furthermore, expulsion (2–5), and the development of a Th1 response associated the stimulation of naive T cells from OVA-specific TCR trans- with high levels of IFN-␥ and IL-12 leads to host susceptibility (6, genic mice in the presence of CCL2 induces IL-4 production and 7). For example, blocking the interaction of IL-4 with the IL-4R using the development of a Th2 phenotype (26, 27), and CCL2 stimu- by guest on September 29, 2021 an anti-IL-4R Ab induces susceptibility in normally resistant lates IL-4 production from Th2-differentiated cells, suggesting a BALB/K mice, whereas injection of an IL-4 complex into susceptible possible positive feedback mechanism for the maintenance or en- AKR mice causes worm expulsion (2). BALB/K mice also become hancement of Th2 responses (28). Analysis of the CCL2-deficient susceptible to infection following administration of IL-12 (7). Despite mouse revealed an inability to mount a Th2 response following this knowledge, the expulsion mechanism responsible for the elimi- OVA sensitization and challenge (29). Interestingly, this was not due nation of T. muris from its host is not yet understood, although the to abnormal T cell migration, suggesting a role for CCL2 in adaptive roles of mast cells, eosinophils, Ab, and CD4ϩ T cell-mediated cy- immunity through control of Th cell differentiation as well as in innate totoxicity are known not to be essential individually (8–10). immunity through effects on monocyte recruitment. Recently, an increasing number of chemokines have been shown With regard to models of infection, CCL2 is produced in re- to play important roles in shaping the adaptive immune response in sponse to the intestinal nematode, Trichinella spiralis, with ex- addition to their widely detailed chemotactic properties. The CC pression found in the serum and locally at the site of infection, in chemokine ligand (CCL)2,3 previously defined as monocyte che- the jejunum (30–32). CCL2-deficient mice are resistant to Leish- mania major infection, a model that requires a Th1 immune re- sponse for resolution (29), and the induction of lung granulomas *Department of Immunology, Microbiology, and Development, University of Manchester School of Biological Sciences, Manchester, United Kingdom; and †De- by Schistosoma mansonii egg Ag results in elevated levels of partment of Adult Oncology, Dana-Farber Cancer Institute, Harvard Medical School, CCL2 in whole lung tissue (33). A number of reports detail CCL2 Boston, MA 02115 being produced in human and mouse intestinal mucosa and asso- Received for publication November 11, 2002. Accepted for publication February ciated tissues (34, 35), leading to increased IL-4 and decreased 24, 2003. IL-12 production. Furthermore, human lamina propria macro- The costs of publication of this article were defrayed in part by the payment of page phages, endothelial cells, and intestinal epithelial cells (36) and mouse charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. mesenteric lymph node (MLN) cells and Peyer’s patch cells (35) all 1 This work was supported by Wellcome Trust Grant 044494/Z (to M.L.D., M.C.L., have the potential to make CCL2. Therefore, it was decided to further and K.J.E.). investigate the role of this chemokine in intestinal infection. 2 Address correspondence and reprint requests to Dr. Matthew deSchoolmeester, De- It is reported here that mice naturally resistant to T. muris pro- partment of Immunology, Microbiology, and Development, University of Manchester duce higher levels of CCL2 than susceptible mice following in- School of Biological Sciences, 3.239 Stopford Building, Manchester, U.K. M13 9PT. E-mail address: [email protected] fection, and significantly, CCL2-deficient animals are totally un- 3 Abbreviations used in this paper: CCL, CC chemokine ligand; CCU, cecal crypt able to expel T. muris infection. This susceptible phenotype is units; E/S, excretory/secretory; MLN, mesenteric lymph node; p.i., postinfection. associated with a reduced Th2 response, characterized by low IL-4 Copyright © 2003 by The American Association of Immunologists, Inc. 0022-1767/03/$02.00 4694 CCL2-DEFICIENT MICE ARE SUSCEPTIBLE TO T. muris INFECTION and high IFN-␥ and IL-12. Macrophage recruitment to the large binding sites in the sections were blocked using 20% normal rat serum intestine and local draining node (MLN) was also decreased in the (Sigma-Aldrich) in PBS for1hatroom temperature. Endogenous avidin CCL2-deficient mouse, and relatively fewer CD4ϩ cells were and biotin binding sites were blocked using a commercial kit according to the manufacturer’s instructions (Vector Laboratories, Burlingame, CA). present in the MLN. The sections were incubated with either 4 ␮g/ml biotinylated rat anti- mouse f4/80 mAb (Caltag Laboratories, Burlingame, CA) or 5 ␮g/ml bi- Materials and Methods otinylated rat anti-mouse CD4 mAb (BD Biosciences) in PBS for1hat Animals room temperature. Alternatively, a number of sections were incubated in parallel with the appropriate biotinylated isotype control Abs (BD Bio- Ϫ Ϫ Breeding pairs of SCYA2 / (CCL2-deficient) (23, 37) were provided by sciences). A Vectastain Elite avidin-biotin-peroxidase complex kit fol- B. Rollins (Dana-Farber Cancer Institute, Boston, MA) and bred in-house lowed by a 3,3Ј-diaminobenzidine chromagen kit were then used according at University of Manchester. The appropriate control mice, C57BL/6, as to the manufacturer’s instructions (Vector Laboratories). Sections were well as AKR and BALB/c mice were purchased from Harlan U.K. (Bic- counterstained in Harris’ hematoxylin solution and mounted in Aquamount ester, U.K.). Male mice were used in all experiments. Mice were infected aqueous mounting medium (BDH Laboratory Supplies). The number of with T. muris when 8–10 wk old. positively stained cells per 20 crypt units was assessed in triplicate by light microscopy after randomization and blinding. Parasite Flow cytometry The maintenance of T.
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