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Mycoplasma Pneumonia During the Pathogenesis of Murine Responses Antigen-Pulsed Bone Marrow−Derived and Pulmonary Dendritic Cells Promote Th2 Cell Responses and Immunopathology in Lungs during the Pathogenesis of Murine This information is current as Mycoplasma Pneumonia of September 24, 2021. Nicole A. Dobbs, Xia Zhou, Mark Pulse, Lisa M. Hodge, Trenton R. Schoeb and Jerry W. Simecka J Immunol 2014; 193:1353-1363; Prepublished online 27 June 2014; Downloaded from doi: 10.4049/jimmunol.1301772 http://www.jimmunol.org/content/193/3/1353 http://www.jimmunol.org/ References This article cites 72 articles, 26 of which you can access for free at: http://www.jimmunol.org/content/193/3/1353.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision by guest on September 24, 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 © 2014 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Antigen-Pulsed Bone Marrow–Derived and Pulmonary Dendritic Cells Promote Th2 Cell Responses and Immunopathology in Lungs during the Pathogenesis of Murine Mycoplasma Pneumonia Nicole A. Dobbs,* Xia Zhou,† Mark Pulse,‡ Lisa M. Hodge,‡ Trenton R. Schoeb,x and Jerry W. Simecka‡ Mycoplasmas are a common cause of pneumonia in humans and animals, and attempts to create vaccines have not only failed to generate protective host responses, but they have exacerbated the disease. Mycoplasma pulmonis causes a chronic inflammatory lung disease resulting from a persistent infection, similar to other mycoplasma respiratory diseases. Using this model, Th1 subsets Downloaded from promote resistance to mycoplasma disease and infection, whereas Th2 responses contribute to immunopathology. The purpose of the present study was to evaluate the capacity of cytokine-differentiated dendritic cell (DC) populations to influence the generation of protective and/or pathologic immune responses during M. pulmonis respiratory disease in BALB/c mice. We hypothesized that intratracheal inoculation of mycoplasma Ag–pulsed bone marrow–derived DCs could result in the generation of protective T cell responses during mycoplasma infection. However, intratracheal inoculation (priming) of mice with Ag-pulsed DCs resulted in enhanced pathology in the recipient mice when challenged with mycoplasma. Inoculation of immunodeficient SCID mice with Ag- http://www.jimmunol.org/ pulsed DCs demonstrated that this effect was dependent on lymphocyte responses. Similar results were observed when mice were primed with Ag-pulsed pulmonary, but not splenic, DCs. Lymphocytes generated in uninfected mice after the transfer of either Ag-pulsed bone marrow–derived DCs or pulmonary DCs were shown to be IL-13+ Th2 cells, known to be associated with immunopathology. Thus, resident pulmonary DCs most likely promote the development of immunopathology in mycoplasma disease through the generation of mycoplasma-specific Th2 responses. Vaccination strategies that disrupt or bypass this process could potentially result in a more effective vaccination. The Journal of Immunology, 2014, 193: 1353–1363. ycoplasmas are underrecognized mucosal pathogens in problem in animals, causing a significant economic impact on humans with a profound impact on healthcare owing to livestock, poultry, and other food animals (9). Mycoplasma pul- by guest on September 24, 2021 M the number of urogential and respiratory diseases they monis causes a naturally occurring murine respiratory disease and cause (1–3). The common human respiratory pathogen Myco- is an excellent animal model of M. pneumoniae, allowing for the plasma pneumoniae is a frequent cause of community-acquired characterization of immune responses during the pathogenesis of pneumonia. It is responsible for up to 30% of all cases of pneu- mycoplasma respiratory disease (10). Both M. pulmonis and M. monia in the United States, in which 100,000 cases result in pneumoniae respiratory infections cause rhinitis, otitis media, hospitalization (4–7). Mycoplasma disease is also associated with laryngotracheitis, and bronchopneumonia. In terms of histopa- the exacerbation of other respiratory diseases, such as asthma (8). thology, both diseases are characterized by chronic inflammation, Additionally, mycoplasma respiratory infections are a major consisting of the accumulation of lymphocytes and macrophages along the respiratory airway (5, 11–14). Furthermore, several studies demonstrate that a component of mycoplasma respiratory *Division of Infectious Diseases, Department of Internal Medicine, University of disease is immunopathologic, with lymphocyte responses re- Texas Southwestern Medical Center, Dallas, TX 75390; †Department of Ophthalmol- sponsible for the severity of the inflammatory disease (15–18). ogy, Xiangya Hospital of Central South University, Changsha 410008, China; Recent studies have revealed that pulmonary T cell populations ‡Department of Cell Biology and Immunology, University of North Texas Health Science Center, Fort Worth, TX 76107; and xDivision of Genomics, Department of are pivotal in determining the outcome of the mycoplasma in- Genetics, University of Alabama at Birmingham, Birmingham, AL 35294 fection. The depletion of Th cells results in less severe lung disease, Received for publication July 3, 2013. Accepted for publication May 22, 2014. demonstrating that a Th cell population mediates disease pathology This work was supported by Public Health Service Grants R01HL069431-01 and in the lung (19). Furthermore, additional studies indicate that Th2 R01AI042075 (to J.W.S.). The Flow Cytometry facility was supported by a shared cells are likely promote the development of immunopathology in instrument grant from the National Institutes of Health. mycoplasma disease (20, 21). However, adaptive immunity can Address correspondence and reprint requests to Dr. Jerry W. Simecka, Department of Cell Biology and Immunology, University of North Texas Health Science Center, still be beneficial by preventing dissemination of mycoplasma to 3500 Camp Bowie Boulevard, Fort Worth, TX 76107. E-mail address: jerry. extrapulmonary tissues and conferring resistance to infection and [email protected] disease (18). Th1 cell responses appear to lead to resistance and Abbreviations used in this article: BMDC, bone marrow–derived DC; DC, dendritic dampen the inflammatory responses to infection (20). Addition- cell; FSL-1, fibroblast-stimulating lipopeptide-1; G4DC, bone marrow–derived DC + + grown in the presence of GM-CSF plus IL-4; GMDC, bone marrow–derived DC ally, CD8 T cells and CD25 regulatory T cells also reduce the grown in the presence of GM-CSF; LRN, lower respiratory lymph node; T10DC, severity of inflammatory disease (19) (A. Odeh and J.W. Simecka, bone marrow–derived DC grown in the presence of GM-CSF plus IL-10 and TGF- unpublished results). Therefore, Th cells, as well as other T cell b1; WT, wild-type. populations, have conflicting roles when it comes to protection Copyright Ó 2014 by The American Association of Immunologists, Inc. 0022-1767/14/$16.00 and pathology of mycoplasma disease, and the mechanisms that www.jimmunol.org/cgi/doi/10.4049/jimmunol.1301772 1354 DCs PROMOTE MYCOPLASMA PNEUMONIA IMMUNOPATHOLOGY determine which arm of the immune response is activated are through the promotion of mycoplasma-specific Th2 responses. critical in the pathogenesis and outcome of mycoplasma respira- Vaccination strategies that disrupt or bypass this process could po- tory disease of the lower respiratory tract. tentially result in a more effective vaccination. Because of their central role in activation of T cell responses, APCs, that is, dendritic cells (DCs) and macrophages, may be Materials and Methods influential in the generation of harmful and/or beneficial pulmonary Mice immune responses, particularly with regard to the development of scid immune-mediated pathology or protection in mycoplasma pneu- BALB/cAnNHsd wild-type (WT) and SCID (BALB/cJHanHsd-Prkdc ) mice, tested to be virus- and mycoplasma-free, were obtained from Harlan monia (22–24). DCs are extremely potent APCs found in tissues Sprague Dawley (Indianapolis, IN). Mice were housed in sterile micro- and can activate both Th and cytotoxic T cells (25–31). However, isolator cages supplied with sterile bedding; food and water were provided studies suggest that the naive resident DCs in lungs are immature ad libitum. Female mice between 6 and 10 wk of age were used in the and are not as effective in Ag presentation (32, 33). In a recent study. All animal studies were reviewed and approved by the University of study, we demonstrated that in response to mycoplasma infec- North Texas Health Science Center Institutional Animal Care and Use Committee. tion pulmonary CD11c+ DCs, and not macrophages, were potent stimulators of mycoplasma-specific T cell responses in vitro (34). Bacterial growth conditions Furthermore, these DCs were colocalized with Th cells in the M. pulmonis
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