Skip to main content
Top
Published in: Inflammation 6/2016

01-12-2016 | ORIGINAL ARTICLE

Maresin 1 Maintains the Permeability of Lung Epithelial Cells In Vitro and In Vivo

Authors: Lin Chen, Hong Liu, Yaxin Wang, Haifa Xia, Jie Gong, Bo Li, Shanglong Yao, You Shang

Published in: Inflammation | Issue 6/2016

Login to get access

Abstract

Previous reports showed that Maresin 1 (MaR1) possessed organ protection effects and could attenuate acute lung injury. Here, we aim to figure out whether MaR1 can maintain the permeability of lung epithelial cells by regulating the expression of tight junction protein during lung injury. Monolayer of murine lung epithelial cells was stimulated by lipopolysaccharide (LPS) with or without MaR1 and the permeability was evaluated. The expression of Claudin-1 and ZO-1 in lung epithelial cells was analyzed by immunofluorescence staining and western blotting. MaR1 was given to the mice after LPS induced acute lung injury. The permeability of lung was assessed by Evans Blue extravasation, lung wet/dry ratio and protein concentration in bronchoalveolar lavage fluid. Lung injury score was also evaluated. The expression of Claudin-1 and ZO-1 in the lung was analyzed by immunofluorescence staining. Results showed that MaR1 maintained the permeability of lung epithelial cells and upregulated the expression of Claudin-1 and ZO-1 after LPS stimulation. In acute lung injury mice, MaR1 upregulated the expression of Claudin-1 and ZO-1, decreased lung permeability, and reduced lung injury. In summary, this study suggests that MaR1 can maintain the permeability of lung epithelial cells by upregulating the expression of Claudin-1 and ZO-1 in acute lung injury.
Literature
1.
go back to reference Piantadosi, C.A., and D.A. Schwartz. 2004. The acute respiratory distress syndrome. Annals of Internal Medicine 141: 460–470.CrossRefPubMed Piantadosi, C.A., and D.A. Schwartz. 2004. The acute respiratory distress syndrome. Annals of Internal Medicine 141: 460–470.CrossRefPubMed
2.
go back to reference Rubenfeld, G.D., E. Caldwell, E. Peabody, J. Weaver, D.P. Martin, M. Neff, E.J. Stern, and L.D. Hudson. 2005. Incidence and outcomes of acute lung injury. New England Journal of Medicine 353: 1685–1693.CrossRefPubMed Rubenfeld, G.D., E. Caldwell, E. Peabody, J. Weaver, D.P. Martin, M. Neff, E.J. Stern, and L.D. Hudson. 2005. Incidence and outcomes of acute lung injury. New England Journal of Medicine 353: 1685–1693.CrossRefPubMed
3.
go back to reference Gropper, M.A., and J. Wiener-Kronish. 2008. The epithelium in acute lung injury/acute respiratory distress syndrome. Current Opinion in Critical Care 14: 11–15.CrossRefPubMed Gropper, M.A., and J. Wiener-Kronish. 2008. The epithelium in acute lung injury/acute respiratory distress syndrome. Current Opinion in Critical Care 14: 11–15.CrossRefPubMed
4.
go back to reference Smith, L.S., J.J. Zimmerman, and T.R. Martin. 2013. Mechanisms of acute respiratory distress syndrome in children and adults: a review and suggestions for future research. Pediatric Critical Care Medicine 14: 631–643.CrossRefPubMed Smith, L.S., J.J. Zimmerman, and T.R. Martin. 2013. Mechanisms of acute respiratory distress syndrome in children and adults: a review and suggestions for future research. Pediatric Critical Care Medicine 14: 631–643.CrossRefPubMed
5.
go back to reference Shen, L., C.R. Weber, and J.R. Turner. 2008. The tight junction protein complex undergoes rapid and continuous molecular remodeling at steady state. Journal of Cell Biology 181: 683–695.CrossRefPubMedPubMedCentral Shen, L., C.R. Weber, and J.R. Turner. 2008. The tight junction protein complex undergoes rapid and continuous molecular remodeling at steady state. Journal of Cell Biology 181: 683–695.CrossRefPubMedPubMedCentral
6.
go back to reference Coyne, C.B., T.M. Gambling, R.C. Boucher, J.L. Carson, and L.G. Johnson. 2003. Role of claudin interactions in airway tight junctional permeability. American Journal of Physiology - Lung Cellular and Molecular Physiology 285: L1166–L1178.CrossRefPubMed Coyne, C.B., T.M. Gambling, R.C. Boucher, J.L. Carson, and L.G. Johnson. 2003. Role of claudin interactions in airway tight junctional permeability. American Journal of Physiology - Lung Cellular and Molecular Physiology 285: L1166–L1178.CrossRefPubMed
7.
go back to reference Xie, W., H. Wang, L. Wang, C. Yao, R. Yuan, and Q. Wu. 2013. Resolvin D1 reduces deterioration of tight junction proteins by upregulating HO-1 in LPS-induced mice. Laboratory Investigation 93: 991–1000.CrossRefPubMed Xie, W., H. Wang, L. Wang, C. Yao, R. Yuan, and Q. Wu. 2013. Resolvin D1 reduces deterioration of tight junction proteins by upregulating HO-1 in LPS-induced mice. Laboratory Investigation 93: 991–1000.CrossRefPubMed
8.
go back to reference Miyoshi, K., S. Yanagi, K. Kawahara, M. Nishio, H. Tsubouchi, Y. Imazu, R. Koshida, N. Matsumoto, A. Taguchi, S. Yamashita, A. Suzuki, and M. Nakazato. 2013. Epithelial Pten controls acute lung injury and fibrosis by regulating alveolar epithelial cell integrity. American Journal of Respiratory and Critical Care Medicine 187: 262–275.CrossRefPubMed Miyoshi, K., S. Yanagi, K. Kawahara, M. Nishio, H. Tsubouchi, Y. Imazu, R. Koshida, N. Matsumoto, A. Taguchi, S. Yamashita, A. Suzuki, and M. Nakazato. 2013. Epithelial Pten controls acute lung injury and fibrosis by regulating alveolar epithelial cell integrity. American Journal of Respiratory and Critical Care Medicine 187: 262–275.CrossRefPubMed
9.
go back to reference Serhan, C.N., N. Chiang, and J. Dalli. 2015. The resolution code of acute inflammation: novel pro-resolving lipid mediators in resolution. Seminars in Immunology 27: 200–215.CrossRefPubMedPubMedCentral Serhan, C.N., N. Chiang, and J. Dalli. 2015. The resolution code of acute inflammation: novel pro-resolving lipid mediators in resolution. Seminars in Immunology 27: 200–215.CrossRefPubMedPubMedCentral
10.
go back to reference Borgeson, E., A.M. Johnson, Y.S. Lee, A. Till, G.H. Syed, S.T. Ali-Shah, P.J. Guiry, J. Dalli, R.A. Colas, C.N. Serhan, K. Sharma, and C. Godson. 2015. Lipoxin A4 attenuates obesity-induced adipose inflammation and associated liver and kidney disease. Cell Metabolism 22: 125–137.CrossRefPubMedPubMedCentral Borgeson, E., A.M. Johnson, Y.S. Lee, A. Till, G.H. Syed, S.T. Ali-Shah, P.J. Guiry, J. Dalli, R.A. Colas, C.N. Serhan, K. Sharma, and C. Godson. 2015. Lipoxin A4 attenuates obesity-induced adipose inflammation and associated liver and kidney disease. Cell Metabolism 22: 125–137.CrossRefPubMedPubMedCentral
11.
go back to reference Kain, V., K.A. Ingle, R.A. Colas, J. Dalli, S.D. Prabhu, C.N. Serhan, M. Joshi, and G.V. Halade. 2015. Resolvin D1 activates the inflammation resolving response at splenic and ventricular site following myocardial infarction leading to improved ventricular function. Journal of Molecular and Cellular Cardiology 84: 24–35.CrossRefPubMedPubMedCentral Kain, V., K.A. Ingle, R.A. Colas, J. Dalli, S.D. Prabhu, C.N. Serhan, M. Joshi, and G.V. Halade. 2015. Resolvin D1 activates the inflammation resolving response at splenic and ventricular site following myocardial infarction leading to improved ventricular function. Journal of Molecular and Cellular Cardiology 84: 24–35.CrossRefPubMedPubMedCentral
12.
go back to reference Li, H., Z. Wu, D. Feng, J. Gong, C. Yao, Y. Wang, S. Yuan, S. Yao, and Y. Shang. 2014. BML-111, a lipoxin receptor agonist, attenuates ventilator-induced lung injury in rats. Shock 41: 311–316.CrossRefPubMed Li, H., Z. Wu, D. Feng, J. Gong, C. Yao, Y. Wang, S. Yuan, S. Yao, and Y. Shang. 2014. BML-111, a lipoxin receptor agonist, attenuates ventilator-induced lung injury in rats. Shock 41: 311–316.CrossRefPubMed
13.
go back to reference Gong, J., S. Guo, H.B. Li, S.Y. Yuan, Y. Shang, and S.L. Yao. 2012. BML-111, a lipoxin receptor agonist, protects haemorrhagic shock-induced acute lung injury in rats. Resuscitation 83: 907–912.CrossRefPubMed Gong, J., S. Guo, H.B. Li, S.Y. Yuan, Y. Shang, and S.L. Yao. 2012. BML-111, a lipoxin receptor agonist, protects haemorrhagic shock-induced acute lung injury in rats. Resuscitation 83: 907–912.CrossRefPubMed
14.
go back to reference Serhan, C.N., R. Yang, K. Martinod, K. Kasuga, P.S. Pillai, T.F. Porter, S.F. Oh, and M. Spite. 2009. Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions. The Journal of Experimental Medicine 206: 15–23.CrossRefPubMedPubMedCentral Serhan, C.N., R. Yang, K. Martinod, K. Kasuga, P.S. Pillai, T.F. Porter, S.F. Oh, and M. Spite. 2009. Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions. The Journal of Experimental Medicine 206: 15–23.CrossRefPubMedPubMedCentral
15.
go back to reference Krishnamoorthy, N., P.R. Burkett, J. Dalli, R.E. Abdulnour, R. Colas, S. Ramon, R.P. Phipps, N.A. Petasis, V.K. Kuchroo, C.N. Serhan, and B.D. Levy. 2015. Cutting edge: maresin-1 engages regulatory T cells to limit type 2 innate lymphoid cell activation and promote resolution of lung inflammation. Journal of Immunology 194: 863–867.CrossRef Krishnamoorthy, N., P.R. Burkett, J. Dalli, R.E. Abdulnour, R. Colas, S. Ramon, R.P. Phipps, N.A. Petasis, V.K. Kuchroo, C.N. Serhan, and B.D. Levy. 2015. Cutting edge: maresin-1 engages regulatory T cells to limit type 2 innate lymphoid cell activation and promote resolution of lung inflammation. Journal of Immunology 194: 863–867.CrossRef
16.
go back to reference Akagi, D., M. Chen, R. Toy, A. Chatterjee, and M.S. Conte. 2015. Systemic delivery of proresolving lipid mediators resolvin D2 and maresin 1 attenuates intimal hyperplasia in mice. The FASEB Journal 29: 2504–2513.CrossRefPubMedPubMedCentral Akagi, D., M. Chen, R. Toy, A. Chatterjee, and M.S. Conte. 2015. Systemic delivery of proresolving lipid mediators resolvin D2 and maresin 1 attenuates intimal hyperplasia in mice. The FASEB Journal 29: 2504–2513.CrossRefPubMedPubMedCentral
17.
go back to reference Gong, J., Z.Y. Wu, H. Qi, L. Chen, H.B. Li, B. Li, C.Y. Yao, Y.X. Wang, J. Wu, S.Y. Yuan, S.L. Yao, and Y. Shang. 2014. Maresin 1 mitigates LPS-induced acute lung injury in mice. British Journal of Pharmacology 171: 3539–3550.CrossRefPubMedPubMedCentral Gong, J., Z.Y. Wu, H. Qi, L. Chen, H.B. Li, B. Li, C.Y. Yao, Y.X. Wang, J. Wu, S.Y. Yuan, S.L. Yao, and Y. Shang. 2014. Maresin 1 mitigates LPS-induced acute lung injury in mice. British Journal of Pharmacology 171: 3539–3550.CrossRefPubMedPubMedCentral
18.
go back to reference Gong, J., H. Liu, J. Wu, H. Qi, Z.Y. Wu, H.Q. Shu, H.B. Li, L. Chen, Y.X. Wang, B. Li, M. Tang, Y.D. Ji, S.Y. Yuan, S.L. Yao, and Y. Shang. 2015. Maresin 1 prevents lipopolysaccharide-induced neutrophil survival and accelerates resolution of acute lung injury. Shock 44: 371–380.CrossRefPubMed Gong, J., H. Liu, J. Wu, H. Qi, Z.Y. Wu, H.Q. Shu, H.B. Li, L. Chen, Y.X. Wang, B. Li, M. Tang, Y.D. Ji, S.Y. Yuan, S.L. Yao, and Y. Shang. 2015. Maresin 1 prevents lipopolysaccharide-induced neutrophil survival and accelerates resolution of acute lung injury. Shock 44: 371–380.CrossRefPubMed
19.
go back to reference Wang, Y., R. Li, L. Chen, W. Tan, Z. Sun, H. Xia, B. Li, Y. Yu, J. Gong, M. Tang, Y. Ji, S. Yuan, Shanglong Yao, and Y. Shang. 2015. Maresin 1 inhibits epithelial-to-mesenchymal transition in vitro and attenuates bleomycin induced lung fibrosis in vivo. Shock 44: 496–502.CrossRefPubMed Wang, Y., R. Li, L. Chen, W. Tan, Z. Sun, H. Xia, B. Li, Y. Yu, J. Gong, M. Tang, Y. Ji, S. Yuan, Shanglong Yao, and Y. Shang. 2015. Maresin 1 inhibits epithelial-to-mesenchymal transition in vitro and attenuates bleomycin induced lung fibrosis in vivo. Shock 44: 496–502.CrossRefPubMed
20.
go back to reference Kilkenny, C., W. Browne, I.C. Cuthill, M. Emerson, D.G. Altman, and NC3Rs Reporting Guidelines Working Group. 2010. Animal research: reporting in vivo experiments: the ARRIVE guidelines. British Journal of Pharmacology 160: 1577–1579.CrossRefPubMedPubMedCentral Kilkenny, C., W. Browne, I.C. Cuthill, M. Emerson, D.G. Altman, and NC3Rs Reporting Guidelines Working Group. 2010. Animal research: reporting in vivo experiments: the ARRIVE guidelines. British Journal of Pharmacology 160: 1577–1579.CrossRefPubMedPubMedCentral
21.
go back to reference Matute-Bello, G., G. Downey, B.B. Moore, S.D. Groshong, M.A. Matthay, A.S. Slutsky, W.M. Kuebler, and Acute Lung Injury in Animals Study Group. 2011. An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals. American Journal of Respiratory Cell and Molecular Biology 44: 725–738.CrossRefPubMed Matute-Bello, G., G. Downey, B.B. Moore, S.D. Groshong, M.A. Matthay, A.S. Slutsky, W.M. Kuebler, and Acute Lung Injury in Animals Study Group. 2011. An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals. American Journal of Respiratory Cell and Molecular Biology 44: 725–738.CrossRefPubMed
22.
go back to reference Abdulnour, R.E., J. Dalli, J.K. Colby, N. Krishnamoorthy, J.Y. Timmons, S.H. Tan, R.A. Colas, N.A. Petasis, C.N. Serhan, and B.D. Levy. 2014. Maresin 1 biosynthesis during platelet-neutrophil interactions is organ-protective. Proceedings of the National Academy of Science 111: 16526–16531.CrossRef Abdulnour, R.E., J. Dalli, J.K. Colby, N. Krishnamoorthy, J.Y. Timmons, S.H. Tan, R.A. Colas, N.A. Petasis, C.N. Serhan, and B.D. Levy. 2014. Maresin 1 biosynthesis during platelet-neutrophil interactions is organ-protective. Proceedings of the National Academy of Science 111: 16526–16531.CrossRef
23.
go back to reference Matthay, M.A., and G.A. Zimmerman. 2005. Acute lung injury and the acute respiratory distress syndrome: four decades of inquiry into pathogenesis and rational management. American Journal of Respiratory Cell and Molecular Biology 33: 319–327.CrossRefPubMedPubMedCentral Matthay, M.A., and G.A. Zimmerman. 2005. Acute lung injury and the acute respiratory distress syndrome: four decades of inquiry into pathogenesis and rational management. American Journal of Respiratory Cell and Molecular Biology 33: 319–327.CrossRefPubMedPubMedCentral
24.
go back to reference Lucas, R., A.D. Verin, S.M. Black, and J.D. Catravas. 2009. Regulators of endothelial and epithelial barrier integrity and function in acute lung injury. Biochemical Pharmacology 77: 1763–1772.CrossRefPubMedPubMedCentral Lucas, R., A.D. Verin, S.M. Black, and J.D. Catravas. 2009. Regulators of endothelial and epithelial barrier integrity and function in acute lung injury. Biochemical Pharmacology 77: 1763–1772.CrossRefPubMedPubMedCentral
25.
go back to reference Zemans, R.L., S.P. Colgan, and G.P. Downey. 2009. Transepithelial migration of neutrophils: mechanisms and implications for acute lung injury. American Journal of Respiratory Cell and Molecular Biology 40: 519–535.CrossRefPubMed Zemans, R.L., S.P. Colgan, and G.P. Downey. 2009. Transepithelial migration of neutrophils: mechanisms and implications for acute lung injury. American Journal of Respiratory Cell and Molecular Biology 40: 519–535.CrossRefPubMed
26.
go back to reference Broermann, A., M. Winderlich, H. Block, M. Frye, J. Rossaint, A. Zarbock, G. Cagna, R. Linnepe, D. Schulte, A.F. Nottebaum, and D. Vestweber. 2011. Dissociation of VE-PTP from VE-cadherin is required for leukocyte extravasation and for VEGF-induced vascular permeability in vivo. The Journal of Experimental Medicine 208: 2393–2401.CrossRefPubMedPubMedCentral Broermann, A., M. Winderlich, H. Block, M. Frye, J. Rossaint, A. Zarbock, G. Cagna, R. Linnepe, D. Schulte, A.F. Nottebaum, and D. Vestweber. 2011. Dissociation of VE-PTP from VE-cadherin is required for leukocyte extravasation and for VEGF-induced vascular permeability in vivo. The Journal of Experimental Medicine 208: 2393–2401.CrossRefPubMedPubMedCentral
27.
go back to reference Fang, X., A.P. Neyrinck, M.A. Matthay, and J.W. Lee. 2010. Allogeneic human mesenchymal stem cells restore epithelial protein permeability in cultured human alveolar type II cells by secretion of angiopoietin-1. The Journal of Biological Chemistry 285: 26211–26222.CrossRefPubMedPubMedCentral Fang, X., A.P. Neyrinck, M.A. Matthay, and J.W. Lee. 2010. Allogeneic human mesenchymal stem cells restore epithelial protein permeability in cultured human alveolar type II cells by secretion of angiopoietin-1. The Journal of Biological Chemistry 285: 26211–26222.CrossRefPubMedPubMedCentral
28.
go back to reference Van Itallie, C.M., and J.M. Anderson. 2006. Claudins and epithelial paracellular transport. Annual Review of Physiology 68: 403–429.CrossRefPubMed Van Itallie, C.M., and J.M. Anderson. 2006. Claudins and epithelial paracellular transport. Annual Review of Physiology 68: 403–429.CrossRefPubMed
29.
go back to reference Schlingmann, B., S.A. Molina, and M. Koval. 2015. Claudins: gatekeepers of lung epithelial function. Seminars in Cell and Developmental Biology 42: 47–57.CrossRefPubMedPubMedCentral Schlingmann, B., S.A. Molina, and M. Koval. 2015. Claudins: gatekeepers of lung epithelial function. Seminars in Cell and Developmental Biology 42: 47–57.CrossRefPubMedPubMedCentral
30.
go back to reference Chen, Y.H., Q. Lu, D.A. Goodenough, and B. Jeansonne. 2002. Nonreceptor tyrosine kinase c-Yes interacts with occludin during tight junction formation in canine kidney epithelial cells. Molecular Biology of the Cell 13: 1227–1237.CrossRefPubMedPubMedCentral Chen, Y.H., Q. Lu, D.A. Goodenough, and B. Jeansonne. 2002. Nonreceptor tyrosine kinase c-Yes interacts with occludin during tight junction formation in canine kidney epithelial cells. Molecular Biology of the Cell 13: 1227–1237.CrossRefPubMedPubMedCentral
31.
go back to reference Nagaoka, K., T. Udagawa, and J.D. Richter. 2012. CPEB-mediated ZO-1 mRNA localization is required for epithelial tight-junction assembly and cell polarity. Nature Communications 3: 675.CrossRefPubMedPubMedCentral Nagaoka, K., T. Udagawa, and J.D. Richter. 2012. CPEB-mediated ZO-1 mRNA localization is required for epithelial tight-junction assembly and cell polarity. Nature Communications 3: 675.CrossRefPubMedPubMedCentral
32.
go back to reference Umeda, K., T. Matsui, M. Nakayama, K. Furuse, H. Sasaki, M. Furuse, and S. Tsukita. 2004. Establishment and characterization of cultured epithelial cells lacking expression of ZO-1. The Journal of Biological Chemistry 279: 44785–44794.CrossRefPubMed Umeda, K., T. Matsui, M. Nakayama, K. Furuse, H. Sasaki, M. Furuse, and S. Tsukita. 2004. Establishment and characterization of cultured epithelial cells lacking expression of ZO-1. The Journal of Biological Chemistry 279: 44785–44794.CrossRefPubMed
33.
go back to reference Schamberger, A.C., N. Mise, J. Jia, E. Genoyer, A.O. Yildirim, S. Meiners, and O. Eickelberg. 2014. Cigarette smoke-induced disruption of bronchial epithelial tight junctions is prevented by transforming growth factor-beta. American Journal of Respiratory Cell and Molecular Biology 50: 1040–1052.CrossRefPubMed Schamberger, A.C., N. Mise, J. Jia, E. Genoyer, A.O. Yildirim, S. Meiners, and O. Eickelberg. 2014. Cigarette smoke-induced disruption of bronchial epithelial tight junctions is prevented by transforming growth factor-beta. American Journal of Respiratory Cell and Molecular Biology 50: 1040–1052.CrossRefPubMed
34.
go back to reference Grumbach, Y., N.V. Quynh, R. Chiron, and V. Urbach. 2009. LXA4 stimulates ZO-1 expression and transepithelial electrical resistance in human airway epithelial (16HBE14o-) cells. American Journal of Physiology. Lung Cellular and Molecular Physiology 296: L101–L108.CrossRefPubMed Grumbach, Y., N.V. Quynh, R. Chiron, and V. Urbach. 2009. LXA4 stimulates ZO-1 expression and transepithelial electrical resistance in human airway epithelial (16HBE14o-) cells. American Journal of Physiology. Lung Cellular and Molecular Physiology 296: L101–L108.CrossRefPubMed
35.
go back to reference Englert, J.A., A.A. Macias, D. Amador-Munoz, M. Pinilla Vera, C. Isabelle, J. Guan, B. Magaoay, M. Suarez Velandia, A. Coronata, A. Lee, L.E. Fredenburgh, D.J. Culley, G. Crosby, and R.M. Baron. 2015. Isoflurane ameliorates acute lung injury by preserving epithelial tight junction integrity. Anesthesiology 123: 377–388.CrossRefPubMedPubMedCentral Englert, J.A., A.A. Macias, D. Amador-Munoz, M. Pinilla Vera, C. Isabelle, J. Guan, B. Magaoay, M. Suarez Velandia, A. Coronata, A. Lee, L.E. Fredenburgh, D.J. Culley, G. Crosby, and R.M. Baron. 2015. Isoflurane ameliorates acute lung injury by preserving epithelial tight junction integrity. Anesthesiology 123: 377–388.CrossRefPubMedPubMedCentral
36.
go back to reference Krause, G., L. Winkler, S.L. Mueller, R.F. Haseloff, J. Piontek, and I.E. Blasig. 2008. Structure and function of claudins. Biochimica et Biophysica Acta 1778: 631–645.CrossRefPubMed Krause, G., L. Winkler, S.L. Mueller, R.F. Haseloff, J. Piontek, and I.E. Blasig. 2008. Structure and function of claudins. Biochimica et Biophysica Acta 1778: 631–645.CrossRefPubMed
37.
go back to reference LaFemina, M.J., K.M. Sutherland, T. Bentley, L.W. Gonzales, L. Allen, C.J. Chapin, D. Rokkam, K.A. Sweerus, L.G. Dobbs, P.L. Ballard, and J.A. Frank. 2014. Claudin-18 deficiency results in alveolar barrier dysfunction and impaired alveologenesis in mice. American Journal of Respiratory Cell and Molecular Biology 51: 550–558.CrossRefPubMedPubMedCentral LaFemina, M.J., K.M. Sutherland, T. Bentley, L.W. Gonzales, L. Allen, C.J. Chapin, D. Rokkam, K.A. Sweerus, L.G. Dobbs, P.L. Ballard, and J.A. Frank. 2014. Claudin-18 deficiency results in alveolar barrier dysfunction and impaired alveologenesis in mice. American Journal of Respiratory Cell and Molecular Biology 51: 550–558.CrossRefPubMedPubMedCentral
38.
go back to reference Wray, C., Y. Mao, J. Pan, A. Chandrasena, F. Piasta, and J.A. Frank. 2009. Claudin-4 augments alveolar epithelial barrier function and is induced in acute lung injury. American Journal of Physiology. Lung Cellular and Molecular Physiology 297: L219–L227.CrossRefPubMedPubMedCentral Wray, C., Y. Mao, J. Pan, A. Chandrasena, F. Piasta, and J.A. Frank. 2009. Claudin-4 augments alveolar epithelial barrier function and is induced in acute lung injury. American Journal of Physiology. Lung Cellular and Molecular Physiology 297: L219–L227.CrossRefPubMedPubMedCentral
39.
go back to reference Cording, J., J. Berg, N. Kading, C. Bellmann, C. Tscheik, J.K. Westphal, S. Milatz, D. Günzel, H. Wolburg, J. Piontek, O. Huber, and I.E. Blasig. 2013. In tight junctions, claudins regulate the interactions between occludin, tricellulin and marvelD3, which, inversely, modulate claudin oligomerization. Journal of Cell Science 126: 554–564.CrossRefPubMed Cording, J., J. Berg, N. Kading, C. Bellmann, C. Tscheik, J.K. Westphal, S. Milatz, D. Günzel, H. Wolburg, J. Piontek, O. Huber, and I.E. Blasig. 2013. In tight junctions, claudins regulate the interactions between occludin, tricellulin and marvelD3, which, inversely, modulate claudin oligomerization. Journal of Cell Science 126: 554–564.CrossRefPubMed
40.
go back to reference Gan, H., G. Wang, Q. Hao, Q.J. Wang, and H. Tang. 2013. Protein kinase D promotes airway epithelial barrier dysfunction and permeability through down-regulation of claudin-1. The Journal of Biological Chemistry 288: 37343–37354.CrossRefPubMedPubMedCentral Gan, H., G. Wang, Q. Hao, Q.J. Wang, and H. Tang. 2013. Protein kinase D promotes airway epithelial barrier dysfunction and permeability through down-regulation of claudin-1. The Journal of Biological Chemistry 288: 37343–37354.CrossRefPubMedPubMedCentral
41.
go back to reference Ragupathy, S., F. Esmaeili, S. Paschoud, E. Sublet, S. Citi, and G. Borchard. 2014. Toll-like receptor 2 regulates the barrier function of human bronchial epithelial monolayers through atypical protein kinase C zeta, and an increase in expression of claudin-1. Tissue Barriers 2: e29166.CrossRefPubMedPubMedCentral Ragupathy, S., F. Esmaeili, S. Paschoud, E. Sublet, S. Citi, and G. Borchard. 2014. Toll-like receptor 2 regulates the barrier function of human bronchial epithelial monolayers through atypical protein kinase C zeta, and an increase in expression of claudin-1. Tissue Barriers 2: e29166.CrossRefPubMedPubMedCentral
42.
go back to reference Chatterjee, A., A. Sharma, M. Chen, R. Toy, G. Mottola, and M.S. Conte. 2014. The pro-resolving lipid mediator maresin 1 (MaR1) attenuates inflammatory signaling pathways in vascular smooth muscle and endothelial cells. PloS One 9: e113480.CrossRefPubMedPubMedCentral Chatterjee, A., A. Sharma, M. Chen, R. Toy, G. Mottola, and M.S. Conte. 2014. The pro-resolving lipid mediator maresin 1 (MaR1) attenuates inflammatory signaling pathways in vascular smooth muscle and endothelial cells. PloS One 9: e113480.CrossRefPubMedPubMedCentral
Metadata
Title
Maresin 1 Maintains the Permeability of Lung Epithelial Cells In Vitro and In Vivo
Authors
Lin Chen
Hong Liu
Yaxin Wang
Haifa Xia
Jie Gong
Bo Li
Shanglong Yao
You Shang
Publication date
01-12-2016
Publisher
Springer US
Published in
Inflammation / Issue 6/2016
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-016-0433-0

Other articles of this Issue 6/2016

Inflammation 6/2016 Go to the issue