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Published in: Inflammation 2/2016

Open Access 01-04-2016 | Original Article

CXCR3 May Help Regulate the Inflammatory Response in Acute Lung Injury via a Pathway Modulated by IL-10 Secreted by CD8 + CD122+ Regulatory T Cells

Authors: Li Nie, Wei Wu, Zhibing Lu, Gangyan Zhu, Juan Liu

Published in: Inflammation | Issue 2/2016

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Abstract

The aim of this study is to investigate the role of CXCR3 and IL-10 in lipopolysaccharide (LPS)-induced acute lung injury (ALI). ALI was induced by LPS injection (10 mg/kg) via the tail vein in C57BL/6 mice. Mice were sacrificed after 2 or 12 h to examine the levels of inflammatory cytokines in bronchoalveolar lavage fluid (BALF) and histopathologic assessments. At 12 h after LPS injection, mice exhibited more severe lung infiltration by CD8+ T cell and less infiltration by CD8+CD122+ regulatory T cells than at 2 h after LPS challenge or in the control (mice not exposed to LPS). At 12 h, IFN-γ, CXCR3, and CXCL10 were significantly higher in the lungs. IL-10 in the lungs was significantly lower. CXCR3 may help to recruit CD8+ T cells and promotes IFN-γ and CXCL10 release. Such effects could be inhibited by IL-10 secreted by CD8+CD122+ regulatory T cells.
Literature
1.
2.
go back to reference Nie, L., R. Xiang, W. Zhou, B. Lu, D. Cheng, and J. Gao. 2008. Attenuation of acute lung inflammation induced by cigarette smoke in CXCR3 knockout mice. Respiratory Research 9: 82.CrossRefPubMedPubMedCentral Nie, L., R. Xiang, W. Zhou, B. Lu, D. Cheng, and J. Gao. 2008. Attenuation of acute lung inflammation induced by cigarette smoke in CXCR3 knockout mice. Respiratory Research 9: 82.CrossRefPubMedPubMedCentral
3.
go back to reference Ware, L.B. 2006. Pathophysiology of acute lung injury and the acute respiratory distress syndrome. Seminars in Respiratory and Critical Care Medicine 27: 337–349.CrossRefPubMed Ware, L.B. 2006. Pathophysiology of acute lung injury and the acute respiratory distress syndrome. Seminars in Respiratory and Critical Care Medicine 27: 337–349.CrossRefPubMed
4.
go back to reference Shapiro, H., I. Kaqan, M. Shalita-chesner, J. Singer, and P. Singer. 2010. Inhaled aerosolized insulin: a “topical” anti-inflammatory treatment for acute lung injury and respiratory distress syndrome? Inflammation 33: 315–319.CrossRefPubMed Shapiro, H., I. Kaqan, M. Shalita-chesner, J. Singer, and P. Singer. 2010. Inhaled aerosolized insulin: a “topical” anti-inflammatory treatment for acute lung injury and respiratory distress syndrome? Inflammation 33: 315–319.CrossRefPubMed
5.
go back to reference Sun, J., Z.B. Han, W. Liao, S.G. Yang, Z. Yang, J. Yu, et al. 2001. Intrapulmonary delivery of human umbilical cord mesenchymal stem cells attenuates acute lung injury by expanding CD4+CD25+ Forkhead Boxp3 (FOXP3)+ regulatory T cells and balancing anti- and pro-inflammatory factors. Cellular Physiology and Biochemistry 27: 587–596.CrossRef Sun, J., Z.B. Han, W. Liao, S.G. Yang, Z. Yang, J. Yu, et al. 2001. Intrapulmonary delivery of human umbilical cord mesenchymal stem cells attenuates acute lung injury by expanding CD4+CD25+ Forkhead Boxp3 (FOXP3)+ regulatory T cells and balancing anti- and pro-inflammatory factors. Cellular Physiology and Biochemistry 27: 587–596.CrossRef
6.
go back to reference Endharti, A.T., M. Rifa’l, Z. Shi, Y. Fukuoka, Y. Nakahara, Y. Kawamoto, et al. 2005. Cutting edge: CD8 + CD122+ regulatory T cells produce IL-10 to suppress IFN-gamma production and proliferation of CD8+ T cells. Journal of Immunology 175: 7093–7097.CrossRef Endharti, A.T., M. Rifa’l, Z. Shi, Y. Fukuoka, Y. Nakahara, Y. Kawamoto, et al. 2005. Cutting edge: CD8 + CD122+ regulatory T cells produce IL-10 to suppress IFN-gamma production and proliferation of CD8+ T cells. Journal of Immunology 175: 7093–7097.CrossRef
7.
go back to reference Liu, L., M.K. Callahan, D. Huang, and R.M. Ransohoff. 2005. Chemokine receptor CXCR3: an unexpected enigma. Current Topics in Developmental Biology 68: 149–181.CrossRefPubMed Liu, L., M.K. Callahan, D. Huang, and R.M. Ransohoff. 2005. Chemokine receptor CXCR3: an unexpected enigma. Current Topics in Developmental Biology 68: 149–181.CrossRefPubMed
8.
go back to reference Groom, J.R., and A.D. Luster. 2011. CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunology and Cell Biology 89: 207–215.CrossRefPubMed Groom, J.R., and A.D. Luster. 2011. CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunology and Cell Biology 89: 207–215.CrossRefPubMed
9.
go back to reference Uppaluri, R., K.C. Sheehan, L. Wang, J.D. Bui, J.J. Brotman, B. Lu, et al. 2008. Prolongation of cardiac and islet allograft survival by a blocking hamster anti-mouse CXCR3 monoclonal antibody. Transplantation 86: 137–147.CrossRefPubMedPubMedCentral Uppaluri, R., K.C. Sheehan, L. Wang, J.D. Bui, J.J. Brotman, B. Lu, et al. 2008. Prolongation of cardiac and islet allograft survival by a blocking hamster anti-mouse CXCR3 monoclonal antibody. Transplantation 86: 137–147.CrossRefPubMedPubMedCentral
10.
go back to reference Winkler, A.E., J.J. Brotman, M.E. Pittman, N.P. Judd, J.S. Jr Lewis, R.D. Schreiber, et al. 2011. CXCR3 enhances a T-cell-dependent epidermal proliferative response and promotes skin tumorigenesis. Cancer Research 71: 5707–5716.CrossRefPubMedPubMedCentral Winkler, A.E., J.J. Brotman, M.E. Pittman, N.P. Judd, J.S. Jr Lewis, R.D. Schreiber, et al. 2011. CXCR3 enhances a T-cell-dependent epidermal proliferative response and promotes skin tumorigenesis. Cancer Research 71: 5707–5716.CrossRefPubMedPubMedCentral
11.
go back to reference Muller, M., S. Carter, M.J. Hofer, and I.L. Campbell. 2010. Review: the chemokine receptor CXCR3 and its ligands CXCL9, CXCL10 and CXCL11 in neuroimmunity—a tale of conflict and conundrum. Neuropathology and Applied Neurobiology 36: 368–387.CrossRefPubMed Muller, M., S. Carter, M.J. Hofer, and I.L. Campbell. 2010. Review: the chemokine receptor CXCR3 and its ligands CXCL9, CXCL10 and CXCL11 in neuroimmunity—a tale of conflict and conundrum. Neuropathology and Applied Neurobiology 36: 368–387.CrossRefPubMed
12.
go back to reference Nakajima, C., T. Mukai, N. Yamaguchi, Y. Morimoto, W.R. Park, M. Iwasaki, et al. 2002. Induction of the chemokine receptor CXCR3 on TCR-stimulated T cells: dependence on the release from persistent TCR-triggering and requirement for IFN-gamma stimulation. European Journal of Immunology 32: 1792–1801.CrossRefPubMed Nakajima, C., T. Mukai, N. Yamaguchi, Y. Morimoto, W.R. Park, M. Iwasaki, et al. 2002. Induction of the chemokine receptor CXCR3 on TCR-stimulated T cells: dependence on the release from persistent TCR-triggering and requirement for IFN-gamma stimulation. European Journal of Immunology 32: 1792–1801.CrossRefPubMed
13.
go back to reference Grumelli, S., D.B. Corry, L.Z. Song, L. Song, L. Green, J. Huh, et al. 2004. An immune basis for lung parenchymal destruction in chronic obstructive pulmonary disease and emphysema. PLoS Medicine l: e8.CrossRef Grumelli, S., D.B. Corry, L.Z. Song, L. Song, L. Green, J. Huh, et al. 2004. An immune basis for lung parenchymal destruction in chronic obstructive pulmonary disease and emphysema. PLoS Medicine l: e8.CrossRef
14.
go back to reference Ichikawa, A., K. Kuba, M. Morita, S. Chida, H. Tezuka, H. Hara, et al. 2013. CXCL10-CXCR3 enhances the development of neurophil-mediated fulminant lung injury of viral and nonviral origin. American Journal of Respiratory and Critical Care Medicine 187: 65–77.CrossRefPubMedPubMedCentral Ichikawa, A., K. Kuba, M. Morita, S. Chida, H. Tezuka, H. Hara, et al. 2013. CXCL10-CXCR3 enhances the development of neurophil-mediated fulminant lung injury of viral and nonviral origin. American Journal of Respiratory and Critical Care Medicine 187: 65–77.CrossRefPubMedPubMedCentral
15.
go back to reference D’Ambrosio, D., M. Mariani, P. Panina-Bordignon, and F. Sinigaglia. 2001. Chemokines and their receptors guiding T lymphocyte recruitment in lung inflammation. American Journal of Respiratory and Critical Care Medicine 164: 1266–1275.CrossRefPubMed D’Ambrosio, D., M. Mariani, P. Panina-Bordignon, and F. Sinigaglia. 2001. Chemokines and their receptors guiding T lymphocyte recruitment in lung inflammation. American Journal of Respiratory and Critical Care Medicine 164: 1266–1275.CrossRefPubMed
16.
go back to reference Maeno, T., A.M. Houghton, P.A. Quintero, S. Grumelli, C.A. Owen, and S.D. Shapiro. 2007. CD8+ T cells are required for inflammation and destruction in cigarette smoke-induced emphysema in mice. Journal of Immunology 178: 8090–8096.CrossRef Maeno, T., A.M. Houghton, P.A. Quintero, S. Grumelli, C.A. Owen, and S.D. Shapiro. 2007. CD8+ T cells are required for inflammation and destruction in cigarette smoke-induced emphysema in mice. Journal of Immunology 178: 8090–8096.CrossRef
17.
go back to reference Shen, J., R. Wan, Z. Shen, J. Gao, X. Wang, L. Qian, et al. 2012. Chemokine receptor CXCR3 is involved in the acute pancreatitis-associated lung injury. Biomedicine Pharmacothe 66: 390–396.CrossRef Shen, J., R. Wan, Z. Shen, J. Gao, X. Wang, L. Qian, et al. 2012. Chemokine receptor CXCR3 is involved in the acute pancreatitis-associated lung injury. Biomedicine Pharmacothe 66: 390–396.CrossRef
18.
go back to reference Goodman, R.B., J. Pugin, J.S. Lee, and M.A. Matthay. 2003. Cytokine mediated inflammation in acute lung injury. Cytokine & Growth Factor Reviews 14: 523–535.CrossRef Goodman, R.B., J. Pugin, J.S. Lee, and M.A. Matthay. 2003. Cytokine mediated inflammation in acute lung injury. Cytokine & Growth Factor Reviews 14: 523–535.CrossRef
19.
go back to reference Gaddi, P.J., M.J. Crane, M. Kamanaka, R.A. Flavell, et al. 2012. IL-10 mediated regulation of liver inflammation during acute murine cytomegalovirus infection. PloS One 7: e42850.CrossRefPubMedPubMedCentral Gaddi, P.J., M.J. Crane, M. Kamanaka, R.A. Flavell, et al. 2012. IL-10 mediated regulation of liver inflammation during acute murine cytomegalovirus infection. PloS One 7: e42850.CrossRefPubMedPubMedCentral
20.
go back to reference Dennnis, K.L., N.R. Blatner, F. Gounari, and K. Khazaie. 2013. Current status of interleukin-10 and regulatory T-cells in cancer. Current Opinion in Oncology 25: 637–645.CrossRef Dennnis, K.L., N.R. Blatner, F. Gounari, and K. Khazaie. 2013. Current status of interleukin-10 and regulatory T-cells in cancer. Current Opinion in Oncology 25: 637–645.CrossRef
21.
go back to reference Bonfield, T.L., M.W. Konstan, P. Burfeind, J.R. Panuska, J.B. Hilliard, and M. Berger. 1995. Normal bronchial epithelial cells constitutively produce the anti-inflammatory cytokine interleukin-10, which is downregulated in cystic fibrosis. American Journal of Respiratory Cell and Molecular Biology 13: 257–261.CrossRefPubMed Bonfield, T.L., M.W. Konstan, P. Burfeind, J.R. Panuska, J.B. Hilliard, and M. Berger. 1995. Normal bronchial epithelial cells constitutively produce the anti-inflammatory cytokine interleukin-10, which is downregulated in cystic fibrosis. American Journal of Respiratory Cell and Molecular Biology 13: 257–261.CrossRefPubMed
22.
go back to reference Takanashi, S., Y. Hasegawa, Y. Kanehira, K. Yamamoto, K. Fujimoto, K. Satoh, et al. 1999. Interleukin-10 level in sputum is reduced in bronchial asthma, COPD and in smokers. The European Respiratory Journal 14: 309–314.CrossRefPubMed Takanashi, S., Y. Hasegawa, Y. Kanehira, K. Yamamoto, K. Fujimoto, K. Satoh, et al. 1999. Interleukin-10 level in sputum is reduced in bronchial asthma, COPD and in smokers. The European Respiratory Journal 14: 309–314.CrossRefPubMed
23.
go back to reference Shanley, T.P., N. Vasi, and A. Deneberg. 2000. Regulation of chemokine expression by IL-10 in lung inflammation. Cytokine 12: 1054–1064.CrossRefPubMed Shanley, T.P., N. Vasi, and A. Deneberg. 2000. Regulation of chemokine expression by IL-10 in lung inflammation. Cytokine 12: 1054–1064.CrossRefPubMed
Metadata
Title
CXCR3 May Help Regulate the Inflammatory Response in Acute Lung Injury via a Pathway Modulated by IL-10 Secreted by CD8 + CD122+ Regulatory T Cells
Authors
Li Nie
Wei Wu
Zhibing Lu
Gangyan Zhu
Juan Liu
Publication date
01-04-2016
Publisher
Springer US
Published in
Inflammation / Issue 2/2016
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-015-0276-0

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