Non-FcεR bearing mast cells secrete sufficient interleukin-4 to control Francisella tularensis replication within macrophages
► We utilize P815 mast cells and J774 macrophages as surrogates for primary mast cells and macrophages respectively. ► Mast cell activation by non-FcεR driven signals produces IL-4 and control intramacrophage LVS replication. ► Inhibition in vitro is preserved at ratios relevant to cellular infiltra...
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Published in | Cytokine (Philadelphia, Pa.) Vol. 55; no. 2; pp. 211 - 220 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier Ltd
01.08.2011
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Abstract | ► We utilize P815 mast cells and J774 macrophages as surrogates for primary mast cells and macrophages respectively. ► Mast cell activation by non-FcεR driven signals produces IL-4 and control intramacrophage LVS replication. ► Inhibition in vitro is preserved at ratios relevant to cellular infiltration following pulmonary challenge.
Mast cells have classically been implicated in the triggering of allergic and anaphylactic reactions. However, recent findings have elucidated the ability of these cells to selectively release a variety of cytokines leading to bacterial clearance through neutrophil and dendritic cell mobilization, and suggest an important role in innate host defenses. Our laboratory has established a primary bone marrow derived mast cell–macrophage co-culture system and found that mast cells mediated a significant inhibition of Francisella tularensis live vaccine strain (LVS) uptake and replication within macrophages through contact and the secreted product interleukin-4 (IL-4). In this study, we utilized P815 mast cells and J774 macrophages to further investigate whether mast cell activation by non-FcεR driven signals could produce IL-4 and control intramacrophage LVS replication. P815 supernatants collected upon activation by the mast cell activating peptide MP7, as well as P815 cells co-cultured with J774 macrophages, exhibited marked inhibition of bacterial uptake and replication, which correlated with the production of IL-4. The inhibition noted in vitro was titratable and preserved at ratios relevant to cellular infiltration events following pulmonary challenge. Collectively, our data suggest that both primary mast cell and P815 mast cell (lacking FcεR) secreted IL-4 can control intramacrophage Francisella replication. |
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AbstractList | ► We utilize P815 mast cells and J774 macrophages as surrogates for primary mast cells and macrophages respectively. ► Mast cell activation by non-FcεR driven signals produces IL-4 and control intramacrophage LVS replication. ► Inhibition in vitro is preserved at ratios relevant to cellular infiltration following pulmonary challenge.
Mast cells have classically been implicated in the triggering of allergic and anaphylactic reactions. However, recent findings have elucidated the ability of these cells to selectively release a variety of cytokines leading to bacterial clearance through neutrophil and dendritic cell mobilization, and suggest an important role in innate host defenses. Our laboratory has established a primary bone marrow derived mast cell–macrophage co-culture system and found that mast cells mediated a significant inhibition of Francisella tularensis live vaccine strain (LVS) uptake and replication within macrophages through contact and the secreted product interleukin-4 (IL-4). In this study, we utilized P815 mast cells and J774 macrophages to further investigate whether mast cell activation by non-FcεR driven signals could produce IL-4 and control intramacrophage LVS replication. P815 supernatants collected upon activation by the mast cell activating peptide MP7, as well as P815 cells co-cultured with J774 macrophages, exhibited marked inhibition of bacterial uptake and replication, which correlated with the production of IL-4. The inhibition noted in vitro was titratable and preserved at ratios relevant to cellular infiltration events following pulmonary challenge. Collectively, our data suggest that both primary mast cell and P815 mast cell (lacking FcεR) secreted IL-4 can control intramacrophage Francisella replication. Mast cells have classically been implicated in the triggering of allergic and anaphylactic reactions. However, recent findings have elucidated the ability of these cells to selectively release a variety of cytokines leading to bacterial clearance through neutrophil and dendritic cell mobilization, and suggest an important role in innate host defenses. Our laboratory has established a primary bone marrow derived mast cell-macrophage co-culture system and found that mast cells mediated a significant inhibition of Francisella tularensis LVS uptake and replication within macrophages through contact and the secreted product interleukin-4 (IL-4). In this study, we utilized P815 mast cells and J774 macrophages to further investigate whether mast cell activation by non-FcεR driven signals could produce IL-4 and control intramacrophage LVS replication. P815 supernatants collected upon activation by the mast cell activating peptide MP7, as well as P815 cells co-cultured with J774 macrophages, exhibited marked inhibition of bacterial uptake and replication, which correlated with the production of IL-4. The inhibition noted in vitro was titratable and preserved at ratios relevant to cellular infiltration events following pulmonary challenge. Collectively, our data suggest that both primary mast cell and P815 mast cell (lacking FcεR) secreted IL-4 can control intramacrophage Francisella replication. Mast cells have classically been implicated in the triggering of allergic and anaphylactic reactions. However, recent findings have elucidated the ability of these cells to selectively release a variety of cytokines leading to bacterial clearance through neutrophil and dendritic cell mobilization, and suggest an important role in innate host defenses. Our laboratory has established a primary bone marrow derived mast cell–macrophage co-culture system and found that mast cells mediated a significant inhibition of Francisella tularensis live vaccine strain (LVS) uptake and replication within macrophages through contact and the secreted product interleukin-4 (IL-4). In this study, we utilized P815 mast cells and J774 macrophages to further investigate whether mast cell activation by non-FcεR driven signals could produce IL-4 and control intramacrophage LVS replication. P815 supernatants collected upon activation by the mast cell activating peptide MP7, as well as P815 cells co-cultured with J774 macrophages, exhibited marked inhibition of bacterial uptake and replication, which correlated with the production of IL-4. The inhibition noted in vitro was titratable and preserved at ratios relevant to cellular infiltration events following pulmonary challenge. Collectively, our data suggest that both primary mast cell and P815 mast cell (lacking FcεR) secreted IL-4 can control intramacrophage Francisella replication. |
Author | Thathiah, Prea Chambers, James P. Sanapala, Shilpa Yu, Jieh-Juen Guentzel, M. Neal Murthy, Ashlesh K. Rodriguez, Annette R. Arulanandam, Bernard P. Forsthuber, Thomas G. |
AuthorAffiliation | South Texas Center for Emerging Infectious Diseases and Department of Biology, University of Texas at San Antonio, San Antonio, TX 78249 |
AuthorAffiliation_xml | – name: South Texas Center for Emerging Infectious Diseases and Department of Biology, University of Texas at San Antonio, San Antonio, TX 78249 |
Author_xml | – sequence: 1 givenname: Prea surname: Thathiah fullname: Thathiah, Prea – sequence: 2 givenname: Shilpa surname: Sanapala fullname: Sanapala, Shilpa – sequence: 3 givenname: Annette R. surname: Rodriguez fullname: Rodriguez, Annette R. – sequence: 4 givenname: Jieh-Juen surname: Yu fullname: Yu, Jieh-Juen – sequence: 5 givenname: Ashlesh K. surname: Murthy fullname: Murthy, Ashlesh K. – sequence: 6 givenname: M. Neal surname: Guentzel fullname: Guentzel, M. Neal – sequence: 7 givenname: Thomas G. surname: Forsthuber fullname: Forsthuber, Thomas G. – sequence: 8 givenname: James P. surname: Chambers fullname: Chambers, James P. – sequence: 9 givenname: Bernard P. surname: Arulanandam fullname: Arulanandam, Bernard P. email: BArulanandam@utsa.edu, Bernard.Arulanandam@utsa.edu |
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CitedBy_id | crossref_primary_10_1016_j_phymed_2020_153391 crossref_primary_10_1177_1753425916663639 crossref_primary_10_1177_0394632015621768 crossref_primary_10_1258_ebm_2012_011389 crossref_primary_10_1080_08820139_2019_1694939 crossref_primary_10_1093_femspd_ftv058 |
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Keywords | IL-4 Innate immunity Mast cells Respiratory infection Francisella tularensis |
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148 Saslaw (10.1016/j.cyto.2011.04.009_b0045) 1961; 107 Flesch lEA (10.1016/j.cyto.2011.04.009_b0165) 1990; 168 Metcalfe (10.1016/j.cyto.2011.04.009_b0005) 1997; 77 Galli (10.1016/j.cyto.2011.04.009_b0020) 1993; 328 Paul (10.1016/j.cyto.2011.04.009_b0125) 1987; 1 Higashijima (10.1016/j.cyto.2011.04.009_b0230) 1990; 265 Collazo (10.1016/j.cyto.2011.04.009_b0205) 2009; 77 Klinker (10.1016/j.cyto.2011.04.009_b0065) 1996; 51 Palomaki (10.1016/j.cyto.2011.04.009_b0240) 2006; 147 Furuno (10.1016/j.cyto.2011.04.009_b0085) 1996; 219 Telepnev (10.1016/j.cyto.2011.04.009_b0255) 2005; 38 |
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Snippet | ► We utilize P815 mast cells and J774 macrophages as surrogates for primary mast cells and macrophages respectively. ► Mast cell activation by non-FcεR driven... Mast cells have classically been implicated in the triggering of allergic and anaphylactic reactions. However, recent findings have elucidated the ability of... |
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SubjectTerms | anaphylaxis Animals bone marrow Bone Marrow Cells - cytology Bone Marrow Cells - immunology Bone Marrow Cells - physiology Cells, Cultured coculture Coculture Techniques Francisella tularensis Francisella tularensis - immunology Francisella tularensis - physiology IL-4 Innate immunity interleukin-4 Interleukin-4 - secretion macrophages Macrophages - cytology Macrophages - immunology Macrophages - microbiology Mast cells Mast Cells - cytology Mast Cells - immunology Mast Cells - secretion Mice Mice, Inbred C57BL Receptors, IgE - genetics Receptors, IgE - immunology Respiratory infection Tularemia - immunology Tumor Necrosis Factor-alpha - immunology |
Title | Non-FcεR bearing mast cells secrete sufficient interleukin-4 to control Francisella tularensis replication within macrophages |
URI | https://dx.doi.org/10.1016/j.cyto.2011.04.009 https://www.ncbi.nlm.nih.gov/pubmed/21565523 https://search.proquest.com/docview/874296702 https://pubmed.ncbi.nlm.nih.gov/PMC3155945 |
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