1,181
Views
17
CrossRef citations to date
0
Altmetric
Research Paper

Aquaporin 5 regulates cigarette smoke induced emphysema by modulating barrier and immune properties of the epithelium

, , , , , , , , , , , & show all
Article: e25248 | Received 17 Mar 2013, Accepted 01 Jun 2013, Published online: 03 Jun 2013

References

  • Mannino DM, Buist AS. Global burden of COPD: risk factors, prevalence, and future trends. Lancet 2007; 370:765 - 73; http://dx.doi.org/10.1016/S0140-6736(07)61380-4; PMID: 17765526
  • Podowski M, Calvi C, Metzger S, Misono K, Poonyagariyagorn H, Lopez-Mercado A, et al. Angiotensin receptor blockade attenuates cigarette smoke-induced lung injury and rescues lung architecture in mice. J Clin Invest 2012; 122:229 - 40; http://dx.doi.org/10.1172/JCI46215; PMID: 22182843
  • Balamayooran G, Batra S, Cai S, Mei J, Worthen GS, Penn AL, et al. Role of CXCL5 in leukocyte recruitment to the lungs during secondhand smoke exposure. Am J Respir Cell Mol Biol 2012; 47:104 - 11; http://dx.doi.org/10.1165/rcmb.2011-0260OC; PMID: 22362385
  • Burke WM, Roberts CM, Bryant DH, Cairns D, Yeates M, Morgan GW, et al. Smoking-induced changes in epithelial lining fluid volume, cell density and protein. Eur Respir J 1992; 5:780 - 4; PMID: 1499700
  • Forteza RM, Casalino-Matsuda SM, Falcon NS, Valencia Gattas M, Monzon ME. Hyaluronan and layilin mediate loss of airway epithelial barrier function induced by cigarette smoke by decreasing E-cadherin. J Biol Chem 2012; 287:42288 - 98; http://dx.doi.org/10.1074/jbc.M112.387795; PMID: 23048036
  • Shaykhiev R, Otaki F, Bonsu P, Dang DT, Teater M, Strulovici-Barel Y, et al. Cigarette smoking reprograms apical junctional complex molecular architecture in the human airway epithelium in vivo. Cell Mol Life Sci 2011; 68:877 - 92; http://dx.doi.org/10.1007/s00018-010-0500-x; PMID: 20820852
  • Heijink IH, Brandenburg SM, Postma DS, van Oosterhout AJM. Cigarette smoke impairs airway epithelial barrier function and cell-cell contact recovery. Eur Respir J 2012; 39:419 - 28; http://dx.doi.org/10.1183/09031936.00193810; PMID: 21778164
  • Gangl K, Reininger R, Bernhard D, Campana R, Pree I, Reisinger J, et al. Cigarette smoke facilitates allergen penetration across respiratory epithelium. Allergy 2009; 64:398 - 405; http://dx.doi.org/10.1111/j.1398-9995.2008.01861.x; PMID: 19120070
  • Van Miert E, Dumont X, Bernard A. CC16 as a marker of lung epithelial hyperpermeability in an acute model of rats exposed to mainstream cigarette smoke. Toxicol Lett 2005; 159:115 - 23; http://dx.doi.org/10.1016/j.toxlet.2005.05.007; PMID: 16165332
  • Olivera DS, Boggs SE, Beenhouwer C, Aden J, Knall C. Cellular mechanisms of mainstream cigarette smoke-induced lung epithelial tight junction permeability changes in vitro. Inhal Toxicol 2007; 19:13 - 22; http://dx.doi.org/10.1080/08958370600985768; PMID: 17127639
  • Rusznak C, Sapsford RJ, Devalia JL, Justin John R, Hewitt EL, Lamont AG, et al. Cigarette smoke potentiates house dust mite allergen-induced increase in the permeability of human bronchial epithelial cells in vitro. Am J Respir Cell Mol Biol 1999; 20:1238 - 50; http://dx.doi.org/10.1165/ajrcmb.20.6.3226; PMID: 10340943
  • Nocker RE, Schoonbrood DF, van de Graaf EA, Hack CE, Lutter R, Jansen HM, et al. Interleukin-8 in airway inflammation in patients with asthma and chronic obstructive pulmonary disease. Int Arch Allergy Immunol 1996; 109:183 - 91; http://dx.doi.org/10.1159/000237218; PMID: 8563494
  • Richman-Eisenstat JB, Jorens PG, Hébert CA, Ueki I, Nadel JA. Interleukin-8: an important chemoattractant in sputum of patients with chronic inflammatory airway diseases. [T.] Am J Physiol 1993; 264:L413 - 8; PMID: 8476069
  • Qiu Y, Zhu J, Bandi V, Atmar RL, Hattotuwa K, Guntupalli KK, et al. Biopsy neutrophilia, neutrophil chemokine and receptor gene expression in severe exacerbations of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2003; 168:968 - 75; http://dx.doi.org/10.1164/rccm.200208-794OC; PMID: 12857718
  • Morrison D, Strieter RM, Donnelly SC, Burdick MD, Kunkel SL, MacNee W. Neutrophil chemokines in bronchoalveolar lavage fluid and leukocyte-conditioned medium from nonsmokers and smokers. Eur Respir J 1998; 12:1067 - 72; http://dx.doi.org/10.1183/09031936.98.12051067; PMID: 9863998
  • Jeyaseelan S, Manzer R, Young SK, Yamamoto M, Akira S, Mason RJ, et al. Induction of CXCL5 during inflammation in the rodent lung involves activation of alveolar epithelium. Am J Respir Cell Mol Biol 2005; 32:531 - 9; http://dx.doi.org/10.1165/rcmb.2005-0063OC; PMID: 15778492
  • MacNee W, Wiggs B, Belzberg AS, Hogg JC. The effect of cigarette smoking on neutrophil kinetics in human lungs. N Engl J Med 1989; 321:924 - 8; http://dx.doi.org/10.1056/NEJM198910053211402; PMID: 2779614
  • O’Donnell R, Breen D, Wilson S, Djukanovic R. Inflammatory cells in the airways in COPD. Thorax 2006; 61:448 - 54; http://dx.doi.org/10.1136/thx.2004.024463; PMID: 16648353
  • Di Stefano A, Capelli A, Lusuardi M, Balbo P, Vecchio C, Maestrelli P, et al. Severity of airflow limitation is associated with severity of airway inflammation in smokers. Am J Respir Crit Care Med 1998; 158:1277 - 85; http://dx.doi.org/10.1164/ajrccm.158.4.9802078; PMID: 9769292
  • MacNee W. Pathogenesis of chronic obstructive pulmonary disease. Proc Am Thorac Soc 2005; 2:258 - 66, discussion 290-1; http://dx.doi.org/10.1513/pats.200504-045SR; PMID: 16267346
  • Ofulue AF, Ko M. Effects of depletion of neutrophils or macrophages on development of cigarette smoke-induced emphysema. Am J Physiol 1999; 277:L97 - 105; PMID: 10409235
  • Hautamaki RD, Kobayashi DK, Senior RM, Shapiro SD. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 1997; 277:2002 - 4; http://dx.doi.org/10.1126/science.277.5334.2002; PMID: 9302297
  • Profita M, Sala A, Bonanno A, Riccobono L, Ferraro M, La Grutta S, et al. Chronic obstructive pulmonary disease and neutrophil infiltration: role of cigarette smoke and cyclooxygenase products. Am J Physiol Lung Cell Mol Physiol 2010; 298:L261 - 9; http://dx.doi.org/10.1152/ajplung.90593.2008; PMID: 19897740
  • Le A, Zielinski R, He C, Crow MT, Biswal S, Tuder RM, et al. Pulmonary epithelial neuropilin-1 deletion enhances development of cigarette smoke-induced emphysema. Am J Respir Crit Care Med 2009; 180:396 - 406; http://dx.doi.org/10.1164/rccm.200809-1483OC; PMID: 19520907
  • Ning Y, Ying B, Han S, Wang B, Wang X, Wen F. Polymorphisms of aquaporin5 gene in chronic obstructive pulmonary disease in a Chinese population. Swiss Med Wkly 2008; 138:573 - 8; PMID: 18853286
  • Hansel NN, Sidhaye V, Rafaels NM, Gao L, Gao P, Williams R, et al. Aquaporin 5 polymorphisms and rate of lung function decline in chronic obstructive pulmonary disease. PLoS One 2010; 5:e14226; http://dx.doi.org/10.1371/journal.pone.0014226; PMID: 21151978
  • Wang K, Feng YL, Wen FQ, Chen XR, Ou XM, Xu D, et al. Decreased expression of human aquaporin-5 correlated with mucus overproduction in airways of chronic obstructive pulmonary disease. Acta Pharmacol Sin 2007; 28:1166 - 74; http://dx.doi.org/10.1111/j.1745-7254.2007.00608.x; PMID: 17640479
  • Sidhaye VK, Chau E, Srivastava V, Sirimalle S, Balabhadrapatruni C, Aggarwal NR, et al. A novel role for aquaporin-5 in enhancing microtubule organization and stability. PLoS One 2012; 7:e38717; http://dx.doi.org/10.1371/journal.pone.0038717; PMID: 22715407
  • Sussan TE, Rangasamy T, Blake DJ, Malhotra D, El-Haddad H, Bedja D, et al. Targeting Nrf2 with the triterpenoid CDDO-imidazolide attenuates cigarette smoke-induced emphysema and cardiac dysfunction in mice. Proc Natl Acad Sci U S A 2009; 106:250 - 5; http://dx.doi.org/10.1073/pnas.0804333106; PMID: 19104057
  • Janssens JP, Pache JC, Nicod LP. Physiological changes in respiratory function associated with ageing. Eur Respir J 1999; 13:197 - 205; http://dx.doi.org/10.1183/09031936.99.14614549; PMID: 10836348
  • Chalkley HW, Cornfield J, Park H. A Method for Estimating Volume-Surface Ratios. Science 1949; 110:295 - 7; http://dx.doi.org/10.1126/science.110.2856.295; PMID: 17838566
  • Choe K-H, Taraseviciene-Stewart L, Scerbavicius R, Gera L, Tuder RM, Voelkel NF. Methylprednisolone causes matrix metalloproteinase-dependent emphysema in adult rats. Am J Respir Crit Care Med 2003; 167:1516 - 21; http://dx.doi.org/10.1164/rccm.200210-1207OC; PMID: 12522028
  • Harvey CJ, Thimmulappa RK, Sethi S, Kong X, Yarmus L, Brown RH, et al. Targeting Nrf2 signaling improves bacterial clearance by alveolar macrophages in patients with COPD and in a mouse model. Sci Transl Med 2011; 3:78ra32; http://dx.doi.org/10.1126/scitranslmed.3002042; PMID: 21490276
  • Sidhaye VK, Schweitzer KS, Caterina MJ, Shimoda L, King LS. Shear stress regulates aquaporin-5 and airway epithelial barrier function. Proc Natl Acad Sci U S A 2008; 105:3345 - 50; http://dx.doi.org/10.1073/pnas.0712287105; PMID: 18305162
  • Yamamoto K, Ferrari JD, Cao Y, Ramirez MI, Jones MR, Quinton LJ, et al. Type I alveolar epithelial cells mount innate immune responses during pneumococcal pneumonia. J Immunol 2012; 189:2450 - 9; http://dx.doi.org/10.4049/jimmunol.1200634; PMID: 22844121
  • Raina S, Preston GM, Guggino WB, Agre P. Molecular cloning and characterization of an aquaporin cDNA from salivary, lacrimal, and respiratory tissues. J Biol Chem 1995; 270:1908 - 12; http://dx.doi.org/10.1074/jbc.270.4.1908; PMID: 7530250
  • Zemans RL, Colgan SP, Downey GP. Transepithelial migration of neutrophils: mechanisms and implications for acute lung injury. Am J Respir Cell Mol Biol 2009; 40:519 - 35; http://dx.doi.org/10.1165/rcmb.2008-0348TR; PMID: 18978300
  • Reutershan J, Ley K. Bench-to-bedside review: acute respiratory distress syndrome - how neutrophils migrate into the lung. Crit Care 2004; 8:453 - 61; http://dx.doi.org/10.1186/cc2881; PMID: 15566616
  • Guth AM, Janssen WJ, Bosio CM, Crouch EC, Henson PM, Dow SW. Lung environment determines unique phenotype of alveolar macrophages. Am J Physiol Lung Cell Mol Physiol 2009; 296:L936 - 46; http://dx.doi.org/10.1152/ajplung.90625.2008; PMID: 19304907
  • Janssen WJ, Barthel L, Muldrow A, Oberley-Deegan RE, Kearns MT, Jakubzick C, et al. Fas determines differential fates of resident and recruited macrophages during resolution of acute lung injury. Am J Respir Crit Care Med 2011; 184:547 - 60; http://dx.doi.org/10.1164/rccm.201011-1891OC; PMID: 21471090
  • Zemans RL, Briones N, Campbell M, McClendon J, Young SK, Suzuki T, et al. Neutrophil transmigration triggers repair of the lung epithelium via β-catenin signaling. Proc Natl Acad Sci U S A 2011; 108:15990 - 5; http://dx.doi.org/10.1073/pnas.1110144108; PMID: 21880956
  • Garibaldi BT, D’Alessio FR, Mock JR, Files DC, Chau E, Eto Y, et al. Regulatory T cells reduce acute lung injury fibroproliferation by decreasing fibrocyte recruitment. Am J Respir Cell Mol Biol 2013; 48:35 - 43; http://dx.doi.org/10.1165/rcmb.2012-0198OC; PMID: 23002097
  • Chin AC, Parkos CA. Neutrophil transepithelial migration and epithelial barrier function in IBD: potential targets for inhibiting neutrophil trafficking. Ann N Y Acad Sci 2006; 1072:276 - 87; http://dx.doi.org/10.1196/annals.1326.018; PMID: 17057207
  • Sydora BC, Macfarlane SM, Walker JW, Dmytrash AL, Churchill TA, Doyle J, et al. Epithelial barrier disruption allows nondisease-causing bacteria to initiate and sustain IBD in the IL-10 gene-deficient mouse. Inflamm Bowel Dis 2007; 13:947 - 54; http://dx.doi.org/10.1002/ibd.20155; PMID: 17427241
  • Cork MJ, Danby SG, Vasilopoulos Y, Hadgraft J, Lane ME, Moustafa M, et al. Epidermal barrier dysfunction in atopic dermatitis. J Invest Dermatol 2009; 129:1892 - 908; http://dx.doi.org/10.1038/jid.2009.133; PMID: 19494826
  • Jakasa I, Koster ES, Calkoen F, McLean WH, Campbell LE, Bos JD, et al. Skin barrier function in healthy subjects and patients with atopic dermatitis in relation to filaggrin loss-of-function mutations. J Invest Dermatol 2011; 131:540 - 2; http://dx.doi.org/10.1038/jid.2010.307; PMID: 20962854
  • Palmer CN, Irvine AD, Terron-Kwiatkowski A, Zhao Y, Liao H, Lee SP, et al. Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis. Nat Genet 2006; 38:441 - 6; http://dx.doi.org/10.1038/ng1767; PMID: 16550169
  • Elias PM, Schmuth M. Abnormal skin barrier in the etiopathogenesis of atopic dermatitis. Curr Opin Allergy Clin Immunol 2009; 9:437 - 46; http://dx.doi.org/10.1097/ACI.0b013e32832e7d36; PMID: 19550302
  • Landsman L, Jung S. Lung macrophages serve as obligatory intermediate between blood monocytes and alveolar macrophages. J Immunol 2007; 179:3488 - 94; PMID: 17785782
  • D’Alessio FR, Tsushima K, Aggarwal NR, West EE, Willett MH, Britos MF, et al. CD4+CD25+Foxp3+ Tregs resolve experimental lung injury in mice and are present in humans with acute lung injury. J Clin Invest 2009; 119:2898 - 913; http://dx.doi.org/10.1172/JCI36498; PMID: 19770521
  • Jaye DL, Parkos CA. Neutrophil migration across intestinal epithelium. Ann N Y Acad Sci 2000; 915:151 - 61; http://dx.doi.org/10.1111/j.1749-6632.2000.tb05238.x; PMID: 11193572
  • Herold S, Mayer K, Lohmeyer J. Acute lung injury: how macrophages orchestrate resolution of inflammation and tissue repair. Front Immunol 2011; 2:65; http://dx.doi.org/10.3389/fimmu.2011.00065; PMID: 22566854
  • Ariel A, Maridonneau-Parini I, Rovere-Querini P, Levine JS, Mühl H. Macrophages in inflammation and its resolution. Front Immunol 2012; 3:324; http://dx.doi.org/10.3389/fimmu.2012.00324; PMID: 23125842
  • Kang BH, Crapo JD, Wegner CD, Letts LG, Chang LY. Intercellular adhesion molecule-1 expression on the alveolar epithelium and its modification by hyperoxia. Am J Respir Cell Mol Biol 1993; 9:350 - 5; http://dx.doi.org/10.1165/ajrcmb/9.4.350; PMID: 8104434
  • Burns AR, Takei F, Doerschuk CM. Quantitation of ICAM-1 expression in mouse lung during pneumonia. J Immunol 1994; 153:3189 - 98; PMID: 7916369
  • Barton WW, Wilcoxen SE, Christensen PJ, Paine R 3rd. Association of ICAM-1 with the cytoskeleton in rat alveolar epithelial cells in primary culture. Am J Physiol 1996; 271:L707 - 18; PMID: 8944713
  • Di Stefano A, Caramori G, Ricciardolo FL, Capelli A, Adcock IM, Donner CF. Cellular and molecular mechanisms in chronic obstructive pulmonary disease: an overview. Clin Exp Allergy 2004; 34:1156 - 67; http://dx.doi.org/10.1111/j.1365-2222.2004.02030.x; PMID: 15298554
  • Shibata Y, Nakamura H, Kato S, Tomoike H. Cellular detachment and deformation induce IL-8 gene expression in human bronchial epithelial cells. J Immunol 1996; 156:772 - 7; PMID: 8543832
  • Borok Z, Lubman RL, Danto SI, Zhang XL, Zabski SM, King LS, et al. Keratinocyte growth factor modulates alveolar epithelial cell phenotype in vitro: expression of aquaporin 5. Am J Respir Cell Mol Biol 1998; 18:554 - 61; http://dx.doi.org/10.1165/ajrcmb.18.4.2838; PMID: 9533944
  • Shen Y, Wang Y, Chen Z, Wang D, Wang X, Jin M, et al. Role of aquaporin 5 in antigen-induced airway inflammation and mucous hyperproduction in mice. J Cell Mol Med 2011; 15:1355 - 63; http://dx.doi.org/10.1111/j.1582-4934.2010.01103.x; PMID: 20550619
  • Lorenowicz MJ, Fernandez-Borja M, van Stalborch AM, van Sterkenburg MA, Hiemstra PS, Hordijk PL. Microtubule dynamics and Rac-1 signaling independently regulate barrier function in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 2007; 293:L1321 - 31; http://dx.doi.org/10.1152/ajplung.00443.2006; PMID: 17827248
  • Königshoff M, Eickelberg O. WNT signaling in lung disease: a failure or a regeneration signal?. Am J Respir Cell Mol Biol 2010; 42:21 - 31; http://dx.doi.org/10.1165/rcmb.2008-0485TR; PMID: 19329555
  • Kneidinger N, Yildirim AÖ, Callegari J, Takenaka S, Stein MM, Dumitrascu R, et al. Activation of the WNT/β-catenin pathway attenuates experimental emphysema. Am J Respir Crit Care Med 2011; 183:723 - 33; http://dx.doi.org/10.1164/rccm.200910-1560OC; PMID: 20889911
  • Manna SK, Rangasamy T, Wise K, Sarkar S, Shishodia S, Biswal S, et al. Long term environmental tobacco smoke activates nuclear transcription factor-kappa B, activator protein-1, and stress responsive kinases in mouse brain. Biochem Pharmacol 2006; 71:1602 - 9; http://dx.doi.org/10.1016/j.bcp.2006.02.014; PMID: 16569398
  • Aggarwal NR, D’Alessio FR, Tsushima K, Files DC, Damarla M, Sidhaye VK, et al. Moderate oxygen augments lipopolysaccharide-induced lung injury in mice. Am J Physiol Lung Cell Mol Physiol 2010; 298:L371 - 81; http://dx.doi.org/10.1152/ajplung.00308.2009; PMID: 20034961
  • Yoshida T, Mett I, Bhunia AK, Bowman J, Perez M, Zhang L, et al. Rtp801, a suppressor of mTOR signaling, is an essential mediator of cigarette smoke-induced pulmonary injury and emphysema. Nat Med 2010; 16:767 - 73; http://dx.doi.org/10.1038/nm.2157; PMID: 20473305
  • Davenpeck KL, Chrest FJ, Sterbinsky SA, Bickel CA, Bochner BS. Carboxyfluorescein diacetate labeling does not affect adhesion molecule expression or function in human neutrophils or eosinophils. J Immunol Methods 1995; 188:79 - 89; http://dx.doi.org/10.1016/0022-1759(95)00206-5; PMID: 8551041
  • D’Alessio FR, Tsushima K, Aggarwal NR, Mock JR, Eto Y, Garibaldi BT, et al. Resolution of experimental lung injury by monocyte-derived inducible nitric oxide synthase. J Immunol 2012; 189:2234 - 45; http://dx.doi.org/10.4049/jimmunol.1102606; PMID: 22844117