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Published in: Lung 4/2011

01-08-2011

Effects of Downregulation of Aquaporin1 by Peptidoglycan and Lipopolysaccharide via MAPK Pathways in MeT-5A Cells

Authors: Lihua Liu, Canmao Xie

Published in: Lung | Issue 4/2011

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Abstract

This study was designed to investigate the signaling pathway involved in aquaporin1 (AQP1) expression caused by peptidoglycan (PGN) from Staphylococcus aureus and lipopolysaccharide (LPS) in human pleural mesothelial cell lines (MeT-5A) in vitro. RT-PCR, immunoblot analysis, and immunofluorescence assay were used to determine the relative mRNA and protein levels of AQP1 caused by PGN and LPS in MeT-5A cells. Activation of MAPKs by PGN and LPS was reflected by detecting the phosphorylation constituents of extracellular signal-regulated kinase 1/2 (ERK1/2), c-Jun N-terminal kinase (JNK), and p38 using immunoblot. MAPKs inhibitors were used to determine the effects of PGN- and LPS-induced AQP1 expression by immunoblot. AQP1 transcription and protein expression were decreased by PGN and LPS in dose- and time-dependent manners in MeT-5A cells. Both PGN and LPS activated p38/ERK/JNK pathways in MeT-5A cells. Furthermore, downregulation of AQP1 expression by LPS was blocked by SB203580, SP600125, and PD98059, which are inhibitors of p38, JNK, and ERK1/2, respectively. In contrast, downregulation of AQP1 expression by PGN was blocked only by SB203580, not by SP600125 or PD98059, underlying the importance of p38 MAPK in the downregulation of AQP1 expression by PGN in MeT-5A cells. AQP1 expression was decreased by both PGN and LPS in dose- and time-dependent manners in MeT-5A cells. AQP1 expression was down-regulated by PGN via p38 MAPK pathway, while AQP1 expression was down-regulated by LPS via p38/JNK/ERK pathways.
Literature
1.
go back to reference Nielsen S, Smith BL, Christensen EI, Agre P (1993) Distribution of the aquaporin chip in secretory and resorptive epithelia and capillary endothelia. Proc Natl Acad Sci USA 90:7275–7279PubMedCrossRef Nielsen S, Smith BL, Christensen EI, Agre P (1993) Distribution of the aquaporin chip in secretory and resorptive epithelia and capillary endothelia. Proc Natl Acad Sci USA 90:7275–7279PubMedCrossRef
2.
go back to reference Borok Z, Verkman AS (2002) Lung edema clearance: 20 years of progress: invited review: role of aquaporin water channels in fluid transport in lung and airways. J Appl Physiol 93:2199–2206PubMed Borok Z, Verkman AS (2002) Lung edema clearance: 20 years of progress: invited review: role of aquaporin water channels in fluid transport in lung and airways. J Appl Physiol 93:2199–2206PubMed
3.
4.
go back to reference Song Y, Fukuda N, Bai C, Ma T, Matthay MA, Verkman AS (2000) Role of aquaporins in alveolar fluid clearance in neonatal and adult lung, and in oedema formation following acute lung injury: studies in transgenic aquaporin null mice. J Physiol 525(Pt 3):771–779PubMedCrossRef Song Y, Fukuda N, Bai C, Ma T, Matthay MA, Verkman AS (2000) Role of aquaporins in alveolar fluid clearance in neonatal and adult lung, and in oedema formation following acute lung injury: studies in transgenic aquaporin null mice. J Physiol 525(Pt 3):771–779PubMedCrossRef
5.
go back to reference Song Y, Ma T, Matthay MA, Verkman AS (2000) Role of aquaporin-4 in airspace-to-capillary water permeability in intact mouse lung measured by a novel gravimetric method. J Gen Physiol 115:17–27PubMedCrossRef Song Y, Ma T, Matthay MA, Verkman AS (2000) Role of aquaporin-4 in airspace-to-capillary water permeability in intact mouse lung measured by a novel gravimetric method. J Gen Physiol 115:17–27PubMedCrossRef
6.
go back to reference King LS, Nielsen S, Agre P (1997) Aquaporins in complex tissues. I. Developmental patterns in respiratory and glandular tissues of rat. Am J Physiol 273:C1541–C1548PubMed King LS, Nielsen S, Agre P (1997) Aquaporins in complex tissues. I. Developmental patterns in respiratory and glandular tissues of rat. Am J Physiol 273:C1541–C1548PubMed
7.
go back to reference Effros RM, Darin C, Jacobs ER, Rogers RA, Krenz G, Schneeberger EE (1997) Water transport and the distribution of aquaporin-1 in pulmonary air spaces. J Appl Physiol 83:1002–1016PubMed Effros RM, Darin C, Jacobs ER, Rogers RA, Krenz G, Schneeberger EE (1997) Water transport and the distribution of aquaporin-1 in pulmonary air spaces. J Appl Physiol 83:1002–1016PubMed
8.
go back to reference Song Y, Yang B, Matthay MA, Ma T, Verkman AS (2000) Role of aquaporin water channels in pleural fluid dynamics. Am J Physiol Cell Physiol 279:C1744–C1750PubMed Song Y, Yang B, Matthay MA, Ma T, Verkman AS (2000) Role of aquaporin water channels in pleural fluid dynamics. Am J Physiol Cell Physiol 279:C1744–C1750PubMed
9.
go back to reference Zhang W, Zitron E, Homme M, Kihm L, Morath C, Scherer D, Hegge S, Thomas D, Schmitt CP, Zeier M, Katus H, Karle C, Schwenger V (2007) Aquaporin-1 channel function is positively regulated by protein kinase C. J Biol Chem 282:20933–20940PubMedCrossRef Zhang W, Zitron E, Homme M, Kihm L, Morath C, Scherer D, Hegge S, Thomas D, Schmitt CP, Zeier M, Katus H, Karle C, Schwenger V (2007) Aquaporin-1 channel function is positively regulated by protein kinase C. J Biol Chem 282:20933–20940PubMedCrossRef
10.
go back to reference Jiang J, Hu J, Bai C (2003) Role of aquaporin and sodium channel in pleural water movement. Respir Physiol Neurobiol 139:83–88PubMedCrossRef Jiang J, Hu J, Bai C (2003) Role of aquaporin and sodium channel in pleural water movement. Respir Physiol Neurobiol 139:83–88PubMedCrossRef
11.
go back to reference Otterbach F, Callies R, Kimmig R, Schmid KW, Bankfalvi A (2008) Aquaporin 1 expression in invasive breast carcinomas. Pathologe 29(Suppl 2):357–362PubMedCrossRef Otterbach F, Callies R, Kimmig R, Schmid KW, Bankfalvi A (2008) Aquaporin 1 expression in invasive breast carcinomas. Pathologe 29(Suppl 2):357–362PubMedCrossRef
12.
go back to reference Papadopoulos MC, Saadoun S, Verkman AS (2008) Aquaporins and cell migration. Pflugers Arch 456:693–700PubMedCrossRef Papadopoulos MC, Saadoun S, Verkman AS (2008) Aquaporins and cell migration. Pflugers Arch 456:693–700PubMedCrossRef
13.
go back to reference Verkman AS (2008) Mammalian aquaporins: diverse physiological roles and potential clinical significance. Expert Rev Mol Med 10:e13PubMedCrossRef Verkman AS (2008) Mammalian aquaporins: diverse physiological roles and potential clinical significance. Expert Rev Mol Med 10:e13PubMedCrossRef
14.
go back to reference Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS (2005) Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434:786–792PubMedCrossRef Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS (2005) Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434:786–792PubMedCrossRef
15.
go back to reference Du H, Xie C, He Q, Deng X (2007) Increased expression of aquaporin-1 on the pleura of rats with a tuberculous pleural effusion. Lung 185:325–336PubMedCrossRef Du H, Xie C, He Q, Deng X (2007) Increased expression of aquaporin-1 on the pleura of rats with a tuberculous pleural effusion. Lung 185:325–336PubMedCrossRef
17.
go back to reference Smith JA, Mullerworth MH, Westlake GW, Tatoulis J (1991) Empyema thoracis: 14-year experience in a teaching center. Ann Thorac Surg 51:39–42PubMedCrossRef Smith JA, Mullerworth MH, Westlake GW, Tatoulis J (1991) Empyema thoracis: 14-year experience in a teaching center. Ann Thorac Surg 51:39–42PubMedCrossRef
18.
go back to reference Bryant RE, Salmon CJ (1996) Pleural empyema. Clin Infect Dis 22(747–762):763–764 Bryant RE, Salmon CJ (1996) Pleural empyema. Clin Infect Dis 22(747–762):763–764
19.
21.
go back to reference Hage CA, Abdul-Mohammed K, Antony VB (2004) Pathogenesis of pleural infection. Respirology 9:12–15PubMedCrossRef Hage CA, Abdul-Mohammed K, Antony VB (2004) Pathogenesis of pleural infection. Respirology 9:12–15PubMedCrossRef
22.
go back to reference Kaminska B (2005) MAPK signalling pathways as molecular targets for anti-inflammatory therapy–from molecular mechanisms to therapeutic benefits. Biochim Biophys Acta 1754:253–262PubMed Kaminska B (2005) MAPK signalling pathways as molecular targets for anti-inflammatory therapy–from molecular mechanisms to therapeutic benefits. Biochim Biophys Acta 1754:253–262PubMed
23.
go back to reference Hommes DW, Peppelenbosch MP, van Deventer SJ (2003) Mitogen activated protein (MAP) kinase signal transduction pathways and novel anti-inflammatory targets. Gut 52:144–151PubMedCrossRef Hommes DW, Peppelenbosch MP, van Deventer SJ (2003) Mitogen activated protein (MAP) kinase signal transduction pathways and novel anti-inflammatory targets. Gut 52:144–151PubMedCrossRef
24.
go back to reference Umenishi F, Schrier RW (2003) Hypertonicity-induced aquaporin-1 (AQP1) expression is mediated by the activation of MAPK pathways and hypertonicity-responsive element in the AQP1 gene. J Biol Chem 278(18):15765–15770PubMedCrossRef Umenishi F, Schrier RW (2003) Hypertonicity-induced aquaporin-1 (AQP1) expression is mediated by the activation of MAPK pathways and hypertonicity-responsive element in the AQP1 gene. J Biol Chem 278(18):15765–15770PubMedCrossRef
25.
go back to reference Yatsushige H, Ostrowski RP, Tsubokawa T, Colohan A, Zhang JH (2007) Role of c-Jun N-terminal kinase in early brain injury after subarachnoid hemorrhage. J Neurosci Res 85:1436–1448PubMedCrossRef Yatsushige H, Ostrowski RP, Tsubokawa T, Colohan A, Zhang JH (2007) Role of c-Jun N-terminal kinase in early brain injury after subarachnoid hemorrhage. J Neurosci Res 85:1436–1448PubMedCrossRef
26.
go back to reference Hussain T, Nasreen N, Lai Y, Bellew BF, Antony VB, Mohammed KA (2008) Innate immune responses in murine pleural mesothelial cells: toll-like receptor-2 dependent induction of beta-defensin-2 by staphylococcal peptidoglycan. Am J Physiol Lung Cell Mol Physiol 295:L461–L470PubMedCrossRef Hussain T, Nasreen N, Lai Y, Bellew BF, Antony VB, Mohammed KA (2008) Innate immune responses in murine pleural mesothelial cells: toll-like receptor-2 dependent induction of beta-defensin-2 by staphylococcal peptidoglycan. Am J Physiol Lung Cell Mol Physiol 295:L461–L470PubMedCrossRef
27.
go back to reference Li ZM, Ma JF, Wang LN (2007) Lipopolysaccharide influenced peritoneal mesothelial cells on the growth and expression of tumor necrosis factor through nuclear factor kappaB pathway. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 23:346–349PubMedCrossRef Li ZM, Ma JF, Wang LN (2007) Lipopolysaccharide influenced peritoneal mesothelial cells on the growth and expression of tumor necrosis factor through nuclear factor kappaB pathway. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 23:346–349PubMedCrossRef
28.
go back to reference Wu J, Yang X, Zhang YF, Wang YN, Liu M, Dong XQ, Fan JJ, Yu XQ (2010) Glucose-based peritoneal dialysis fluids downregulate toll-like receptors and trigger hyporesponsiveness to pathogen-associated molecular patterns in human peritoneal mesothelial cells. Clin Vaccine Immunol 17:757–763PubMedCrossRef Wu J, Yang X, Zhang YF, Wang YN, Liu M, Dong XQ, Fan JJ, Yu XQ (2010) Glucose-based peritoneal dialysis fluids downregulate toll-like receptors and trigger hyporesponsiveness to pathogen-associated molecular patterns in human peritoneal mesothelial cells. Clin Vaccine Immunol 17:757–763PubMedCrossRef
29.
go back to reference Lai KN, Leung JC, Metz CN, Lai FM, Bucala R, Lan HY (2003) Role for macrophage migration inhibitory factor in acute respiratory distress syndrome. J Pathol 199:496–508PubMedCrossRef Lai KN, Leung JC, Metz CN, Lai FM, Bucala R, Lan HY (2003) Role for macrophage migration inhibitory factor in acute respiratory distress syndrome. J Pathol 199:496–508PubMedCrossRef
30.
go back to reference Motulsky E, Koch P, Janssens S, Lienart M, Vanbellinghen AM, Bolaky N, Chan CC, Caspers L, Martin-Martinez MD, Xu H, Delporte C, Willermain F (2010) Aquaporin expression in blood-retinal barrier cells during experimental autoimmune uveitis. Mol Vis 16:602–610PubMed Motulsky E, Koch P, Janssens S, Lienart M, Vanbellinghen AM, Bolaky N, Chan CC, Caspers L, Martin-Martinez MD, Xu H, Delporte C, Willermain F (2010) Aquaporin expression in blood-retinal barrier cells during experimental autoimmune uveitis. Mol Vis 16:602–610PubMed
31.
go back to reference Su X, Song Y, Jiang J, Bai C (2004) The role of aquaporin-1 (AQP1) expression in a murine model of lipopolysaccharide-induced acute lung injury. Respir Physiol Neurobiol 142:1–11PubMedCrossRef Su X, Song Y, Jiang J, Bai C (2004) The role of aquaporin-1 (AQP1) expression in a murine model of lipopolysaccharide-induced acute lung injury. Respir Physiol Neurobiol 142:1–11PubMedCrossRef
32.
go back to reference Jiao G, Li E, Yu R (2002) Decreased expression of AQP1 and AQP5 in acute injured lungs in rats. Chin Med J (Engl) 115:963–967 Jiao G, Li E, Yu R (2002) Decreased expression of AQP1 and AQP5 in acute injured lungs in rats. Chin Med J (Engl) 115:963–967
33.
go back to reference Fischbarg J (2010) Fluid transport across leaky epithelia: central role of the tight junction and supporting role of aquaporins. Physiol Rev 90:1271–1290PubMedCrossRef Fischbarg J (2010) Fluid transport across leaky epithelia: central role of the tight junction and supporting role of aquaporins. Physiol Rev 90:1271–1290PubMedCrossRef
34.
go back to reference Steinfeld S, Cogan E, King LS, Agre P, Kiss R, Delporte C (2001) Abnormal distribution of aquaporin-5 water channel protein in salivary glands from Sjogren’s syndrome patients. Lab Invest 81:143–148PubMed Steinfeld S, Cogan E, King LS, Agre P, Kiss R, Delporte C (2001) Abnormal distribution of aquaporin-5 water channel protein in salivary glands from Sjogren’s syndrome patients. Lab Invest 81:143–148PubMed
35.
go back to reference Jwalitha S, Rajkumar VP, Jamboor KV (2010) Effect of down-regulation of aquaporins in human corneal endothelial and epithelial cell lines. Mol Vis 16:1538–1548 Jwalitha S, Rajkumar VP, Jamboor KV (2010) Effect of down-regulation of aquaporins in human corneal endothelial and epithelial cell lines. Mol Vis 16:1538–1548
36.
go back to reference Cheon IS, Woo SS, Kang SS, Im J, Yun CH, Chung DK, Park DK, Han SH (2008) Peptidoglycan-mediated IL-8 expression in human alveolar type II epithelial cells requires lipid raft formation and MAPK activation. Mol Immunol 45:1665–1673PubMedCrossRef Cheon IS, Woo SS, Kang SS, Im J, Yun CH, Chung DK, Park DK, Han SH (2008) Peptidoglycan-mediated IL-8 expression in human alveolar type II epithelial cells requires lipid raft formation and MAPK activation. Mol Immunol 45:1665–1673PubMedCrossRef
37.
go back to reference Dziarski R, Jin YP, Gupta D (1996) Differential activation of extracellular signal-regulated kinase (ERK) 1, ERK2, p38, and c-Jun NH2-terminal kinase mitogen-activated protein kinases by bacterial peptidoglycan. J Infect Dis 174:777–785PubMedCrossRef Dziarski R, Jin YP, Gupta D (1996) Differential activation of extracellular signal-regulated kinase (ERK) 1, ERK2, p38, and c-Jun NH2-terminal kinase mitogen-activated protein kinases by bacterial peptidoglycan. J Infect Dis 174:777–785PubMedCrossRef
38.
go back to reference Fragaki K, Kileztky C, Trentesaux C, Zahm JM, Bajolet O, Johnson M, Puchelle E (2006) Downregulation by a long-acting beta2-adrenergic receptor agonist and corticosteroid of Staphylococcus aureus-induced airway epithelial inflammatory mediator production. Am J Physiol Lung Cell Mol Physiol 291:L11–L18PubMedCrossRef Fragaki K, Kileztky C, Trentesaux C, Zahm JM, Bajolet O, Johnson M, Puchelle E (2006) Downregulation by a long-acting beta2-adrenergic receptor agonist and corticosteroid of Staphylococcus aureus-induced airway epithelial inflammatory mediator production. Am J Physiol Lung Cell Mol Physiol 291:L11–L18PubMedCrossRef
39.
go back to reference Lee HS, Kim HJ, Moon CS, Chong YH, Kang JL (2004) Inhibition of c-Jun NH2-terminal kinase or extracellular signal-regulated kinase improves lung injury. Respir Res 5:23PubMedCrossRef Lee HS, Kim HJ, Moon CS, Chong YH, Kang JL (2004) Inhibition of c-Jun NH2-terminal kinase or extracellular signal-regulated kinase improves lung injury. Respir Res 5:23PubMedCrossRef
40.
go back to reference Sun CY, Pei CQ, Zang BX, Wang L, Jin M (2010) The ability of hydroxysafflor yellow a to attenuate lipopolysaccharide-induced pulmonary inflammatory injury in mice. Phytother Res 24:1788–1795PubMedCrossRef Sun CY, Pei CQ, Zang BX, Wang L, Jin M (2010) The ability of hydroxysafflor yellow a to attenuate lipopolysaccharide-induced pulmonary inflammatory injury in mice. Phytother Res 24:1788–1795PubMedCrossRef
41.
go back to reference Yao C, Purwanti N, Karabasil MR, Azlina A, Javkhlan P, Hasegawa T, Akamatsu T, Hosoi T, Ozawa K, Hosoi K (2010) Potential down-regulation of salivary gland AQP5 by LPS via cross-coupling of NF-kappaB and p-c-Jun/c-Fos. Am J Pathol 177:724–734PubMedCrossRef Yao C, Purwanti N, Karabasil MR, Azlina A, Javkhlan P, Hasegawa T, Akamatsu T, Hosoi T, Ozawa K, Hosoi K (2010) Potential down-regulation of salivary gland AQP5 by LPS via cross-coupling of NF-kappaB and p-c-Jun/c-Fos. Am J Pathol 177:724–734PubMedCrossRef
42.
go back to reference Dziarski R (2003) Recognition of bacterial peptidoglycan by the innate immune system. Cell Mol Life Sci 60:1793–1804PubMedCrossRef Dziarski R (2003) Recognition of bacterial peptidoglycan by the innate immune system. Cell Mol Life Sci 60:1793–1804PubMedCrossRef
43.
go back to reference Hajjar AM, Ernst RK, Tsai JH, Wilson CB, Miller SI (2002) Human toll-like receptor 4 recognizes host-specific LPS modifications. Nat Immunol 3:354–359PubMedCrossRef Hajjar AM, Ernst RK, Tsai JH, Wilson CB, Miller SI (2002) Human toll-like receptor 4 recognizes host-specific LPS modifications. Nat Immunol 3:354–359PubMedCrossRef
44.
go back to reference Erridge C, Pridmore A, Eley A, Stewart J, Poxton IR (2004) Lipopolysaccharides of Bacteroides fragilis, Chlamydia trachomatis and Pseudomonas aeruginosa signal via toll-like receptor 2. J Med Microbiol 53:735–740PubMedCrossRef Erridge C, Pridmore A, Eley A, Stewart J, Poxton IR (2004) Lipopolysaccharides of Bacteroides fragilis, Chlamydia trachomatis and Pseudomonas aeruginosa signal via toll-like receptor 2. J Med Microbiol 53:735–740PubMedCrossRef
45.
go back to reference Gon Y, Asai Y, Hashimoto S, Mizumura K, Jibiki I, Machino T, Ra C, Horie T (2004) A20 inhibits toll-like receptor 2- and 4-mediated interleukin-8 synthesis in airway epithelial cells. Am J Respir Cell Mol Biol 31:330–336PubMedCrossRef Gon Y, Asai Y, Hashimoto S, Mizumura K, Jibiki I, Machino T, Ra C, Horie T (2004) A20 inhibits toll-like receptor 2- and 4-mediated interleukin-8 synthesis in airway epithelial cells. Am J Respir Cell Mol Biol 31:330–336PubMedCrossRef
46.
go back to reference Raoust E, Balloy V, Garcia-Verdugo I, Touqui L, Ramphal R, Chignard M (2009) Pseudomonas aeruginosa LPS or flagellin are sufficient to activate TLR-dependent signaling in murine alveolar macrophages and airway epithelial cells. PLoS One 4:e7259PubMedCrossRef Raoust E, Balloy V, Garcia-Verdugo I, Touqui L, Ramphal R, Chignard M (2009) Pseudomonas aeruginosa LPS or flagellin are sufficient to activate TLR-dependent signaling in murine alveolar macrophages and airway epithelial cells. PLoS One 4:e7259PubMedCrossRef
Metadata
Title
Effects of Downregulation of Aquaporin1 by Peptidoglycan and Lipopolysaccharide via MAPK Pathways in MeT-5A Cells
Authors
Lihua Liu
Canmao Xie
Publication date
01-08-2011
Publisher
Springer-Verlag
Published in
Lung / Issue 4/2011
Print ISSN: 0341-2040
Electronic ISSN: 1432-1750
DOI
https://doi.org/10.1007/s00408-011-9288-1

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