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Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

General Review Article

Epithelial Barrier Dysfunction Induced by Hypoxia in the Respiratory System

Author(s): Yapeng Hou, Yan Ding, Yanhong Liu, Xiaoyong Xie, Yong Cui* and Hongguang Nie*

Volume 26, Issue 41, 2020

Page: [5310 - 5316] Pages: 7

DOI: 10.2174/1381612826666200825165434

Price: $65

Abstract

A steady and continuous supply of oxygen is important for humans, since an excess or deficiency in oxygen levels may result in the death of cells, tissues, or organisms. As a mechanical barrier against pathogens, the respiratory epithelium is always exposed to hypoxia in some detrimental external environments and/or pathologic states. The barrier function is accordingly impaired as a result of the disrupted cell composition ratio, ion transport, and tight junctions in a hypoxia-inducible factor-dependent or independent way. Hypoxia has been identified as an element of the primary or secondary pathogenic factors of many respiratory diseases. Still, the relationship between hypoxia and epithelial barrier dysfunction is not fully understood. Thus, we summarized recent researches on epithelial barrier dysfunction induced by hypoxia in the respiratory system, aiming to explore the possible therapeutic targets in hypoxia-related respiratory system diseases.

Keywords: Hypoxia, respiratory barrier dysfunction, hypoxia-inducible factor, ion transport, tight junctions, epithelial barrier.

[1]
Semenza GL. Oxygen sensing, homeostasis, and disease. N Engl J Med 2011; 365(6): 537-47.
[http://dx.doi.org/10.1056/NEJMra1011165] [PMID: 21830968]
[2]
Wang GL, Semenza GL. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci USA 1993; 90(9): 4304-8.
[http://dx.doi.org/10.1073/pnas.90.9.4304] [PMID: 8387214]
[3]
Serocki M, Bartoszewska S, Janaszak-Jasiecka A, Ochocka RJ, Collawn JF, Bartoszewski R. miRNAs regulate the HIF switch during hypoxia: a novel therapeutic target. Angiogenesis 2018; 21(2): 183-202.
[http://dx.doi.org/10.1007/s10456-018-9600-2] [PMID: 29383635]
[4]
Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 1995; 92(12): 5510-4.
[http://dx.doi.org/10.1073/pnas.92.12.5510] [PMID: 7539918]
[5]
Urrutia AA, Aragonés J. HIF oxygen sensing pathways in lung biology. Biomedicines 2018; 6(2): 6.
[http://dx.doi.org/10.3390/biomedicines6020068] [PMID: 29882755]
[6]
Gerovac BJ, Valencia M, Baumlin N, Salathe M, Conner GE, Fregien NL. Submersion and hypoxia inhibit ciliated cell differentiation in a notch-dependent manner. Am J Respir Cell Mol Biol 2014; 51(4): 516-25.
[http://dx.doi.org/10.1165/rcmb.2013-0237OC] [PMID: 24754775]
[7]
Song HA, Kim YS, Cho HJ, et al. Hypoxia modulates epithelial permeability via regulation of vascular endothelial growth factor in airway epithelia. Am J Respir Cell Mol Biol 2017; 57(5): 527-35.
[http://dx.doi.org/10.1165/rcmb.2016-0080OC] [PMID: 28598679]
[8]
Whitsett JA. Airway epithelial differentiation and mucociliary clearance. Ann Am Thorac Soc 2018; 15(Suppl. 3): S143-8.
[http://dx.doi.org/10.1513/AnnalsATS.201802-128AW] [PMID: 30431340]
[9]
Randell SH. Airway epithelial stem cells and the pathophysiology of chronic obstructive pulmonary disease. Proc Am Thorac Soc 2006; 3(8): 718-25.
[http://dx.doi.org/10.1513/pats.200605-117SF] [PMID: 17065380]
[10]
Rock JR, Randell SH, Hogan BLM. Airway basal stem cells: a perspective on their roles in epithelial homeostasis and remodeling. Dis Model Mech 2010; 3(9-10): 545-56.
[http://dx.doi.org/10.1242/dmm.006031] [PMID: 20699479]
[11]
Thomas B, Rutman A, Hirst RA, et al. Ciliary dysfunction and ultrastructural abnormalities are features of severe asthma. J Allergy Clin Immunol 2010; 126(4): 722-729.e2.
[http://dx.doi.org/10.1016/j.jaci.2010.05.046] [PMID: 20673980]
[12]
Wang W, Ji HL. Epithelial sodium and chloride channels and asthma. Chin Med J (Engl) 2015; 128(16): 2242-9.
[http://dx.doi.org/10.4103/0366-6999.162494] [PMID: 26265620]
[13]
Heijink IH, Noordhoek JA, Timens W, van Oosterhout AJ, Postma DS. Abnormalities in airway epithelial junction formation in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2014; 189(11): 1439-42.
[http://dx.doi.org/10.1164/rccm.201311-1982LE] [PMID: 24881942]
[14]
Magnani ND, Dada LA, Queisser MA, et al. HIF and HOIL-1L-mediated PKCζ degradation stabilizes plasma membrane Na,K-ATPase to protect against hypoxia-induced lung injury. Proc Natl Acad Sci USA 2017; 114(47): E10178-86.
[http://dx.doi.org/10.1073/pnas.1713563114] [PMID: 29109255]
[15]
Kasper M, Haroske G. Alterations in the alveolar epithelium after injury leading to pulmonary fibrosis. Histol Histopathol 1996; 11(2): 463-83.
[PMID: 8861769]
[16]
Sulkowska M. Morphological studies of the lungs in chronic hypobaric hypoxia. Pol J Pathol 1997; 48(4): 225-34.
[PMID: 9529928]
[17]
Torres-Capelli M, Marsboom G, Li QOY, et al. Role of Hif2α oxygen sensing pathway in bronchial epithelial club cell proliferation. Sci Rep 2016; 6: 25357.
[http://dx.doi.org/10.1038/srep25357] [PMID: 27150457]
[18]
Polosukhin VV, Cates JM, Lawson WE, et al. Hypoxia-inducible factor-1 signalling promotes goblet cell hyperplasia in airway epithelium. J Pathol 2011; 224(2): 203-11.
[http://dx.doi.org/10.1002/path.2863] [PMID: 21557221]
[19]
Rock JR, Gao X, Xue Y, Randell SH, Kong YY, Hogan BLM. Notch-dependent differentiation of adult airway basal stem cells. Cell Stem Cell 2011; 8(6): 639-48.
[http://dx.doi.org/10.1016/j.stem.2011.04.003] [PMID: 21624809]
[20]
Gustafsson MV, Zheng X, Pereira T, et al. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 2005; 9(5): 617-28.
[http://dx.doi.org/10.1016/j.devcel.2005.09.010] [PMID: 16256737]
[21]
de Jong PM, van Sterkenburg MAJA, Kempenaar JA, Dijkman JH, Ponec M. Serial culturing of human bronchial epithelial cells derived from biopsies. In Vitro Cell Dev Biol Anim 1993; 29 A: pp. (5)379-87.
[http://dx.doi.org/10.1007/BF02633985] [PMID: 7686141]
[22]
Ustiyan V, Wert SE, Ikegami M, et al. Foxm1 transcription factor is critical for proliferation and differentiation of Clara cells during development of conducting airways. Dev Biol 2012; 370(2): 198-212.
[http://dx.doi.org/10.1016/j.ydbio.2012.07.028] [PMID: 22885335]
[23]
Xu R, Zhou J, Du XZ, et al. The role of the XBP-1/AGR2 signaling pathway in the regulation of airway Mucin5ac hypersecretion under hypoxia. Exp Cell Res 2019; 382(1)111442
[http://dx.doi.org/10.1016/j.yexcr.2019.05.023] [PMID: 31128106]
[24]
Mylonis I, Chachami G, Samiotaki M, et al. Identification of MAPK phosphorylation sites and their role in the localization and activity of hypoxia-inducible factor-1alpha. J Biol Chem 2006; 281(44): 33095-106.
[http://dx.doi.org/10.1074/jbc.M605058200] [PMID: 16954218]
[25]
Minet E, Arnould T, Michel G, et al. ERK activation upon hypoxia: involvement in HIF-1 activation. FEBS Lett 2000; 468(1): 53-8.
[http://dx.doi.org/10.1016/S0014-5793(00)01181-9] [PMID: 10683440]
[26]
Pan J, Yeger H, Ratcliffe P, Bishop T, Cutz E. Hyperplasia of pulmonary neuroepithelial bodies (NEB) in lungs of prolyl hydroxylase -1(PHD-1) deficient mice. Adv Exp Med Biol 2012; 758: 149-55.
[http://dx.doi.org/10.1007/978-94-007-4584-1_21] [PMID: 23080156]
[27]
Sui P, Wiesner DL, Xu J, et al. Pulmonary neuroendocrine cells amplify allergic asthma responses. Science 2018; 360(6393): 360.
[http://dx.doi.org/10.1126/science.aan8546] [PMID: 29599193]
[28]
Hogan BLM, Barkauskas CE, Chapman HA, et al. Repair and regeneration of the respiratory system: complexity, plasticity, and mechanisms of lung stem cell function. Cell Stem Cell 2014; 15(2): 123-38.
[http://dx.doi.org/10.1016/j.stem.2014.07.012] [PMID: 25105578]
[29]
Groenman F, Unger S, Post M. The molecular basis for abnormal human lung development. Biol Neonate 2005; 87(3): 164-77.
[http://dx.doi.org/10.1159/000082595] [PMID: 15591817]
[30]
Gassmann M, Fandrey J, Bichet S, et al. Oxygen supply and oxygen-dependent gene expression in differentiating embryonic stem cells. Proc Natl Acad Sci USA 1996; 93(7): 2867-72.
[http://dx.doi.org/10.1073/pnas.93.7.2867] [PMID: 8610133]
[31]
Fischer B, Bavister BD. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil 1993; 99(2): 673-9.
[http://dx.doi.org/10.1530/jrf.0.0990673] [PMID: 8107053]
[32]
Pimton P, Lecht S, Stabler CT, Johannes G, Schulman ES, Lelkes PI. Hypoxia enhances differentiation of mouse embryonic stem cells into definitive endoderm and distal lung cells. Stem Cells Dev 2015; 24(5): 663-76.
[http://dx.doi.org/10.1089/scd.2014.0343] [PMID: 25226206]
[33]
Yee M, Gelein R, Mariani TJ, Lawrence BP, O’Reilly MA. The oxygen environment at birth specifies the population of alveolar epithelial stem cells in the adult lung. Stem Cells 2016; 34(5): 1396-406.
[http://dx.doi.org/10.1002/stem.2330] [PMID: 26891117]
[34]
Zheng D, Limmon GV, Yin L, et al. Regeneration of alveolar type I and II cells from Scgb1a1-expressing cells following severe pulmonary damage induced by bleomycin and influenza. PLoS One 2012; 7(10)e48451
[http://dx.doi.org/10.1371/journal.pone.0048451] [PMID: 23119022]
[35]
Yee M, Domm W, Gelein R, et al. Alternative progenitor lineages regenerate the adult lung depleted of alveolar epithelial type 2 cells. Am J Respir Cell Mol Biol 2017; 56(4): 453-64.
[http://dx.doi.org/10.1165/rcmb.2016-0150OC] [PMID: 27967234]
[36]
Yee M, Buczynski BW, O’Reilly MA. Neonatal hyperoxia stimulates the expansion of alveolar epithelial type II cells. Am J Respir Cell Mol Biol 2014; 50(4): 757-66.
[http://dx.doi.org/10.1165/rcmb.2013-0207OC] [PMID: 24188066]
[37]
Saini Y, Harkema JR, LaPres JJ. HIF1alpha is essential for normal intrauterine differentiation of alveolar epithelium and surfactant production in the newborn lung of mice. J Biol Chem 2008; 283(48): 33650-7.
[http://dx.doi.org/10.1074/jbc.M805927200] [PMID: 18801745]
[38]
Zhang H, Okamoto M, Panzhinskiy E, Zawada WM, Das M. PKCδ/midkine pathway drives hypoxia-induced proliferation and differentiation of human lung epithelial cells. Am J Physiol Cell Physiol 2014; 306(7): C648-58.
[http://dx.doi.org/10.1152/ajpcell.00351.2013] [PMID: 24500281]
[39]
Nordin SL, Jovic S, Kurut A, et al. High expression of midkine in the airways of patients with cystic fibrosis. Am J Respir Cell Mol Biol 2013; 49(6): 935-42.
[http://dx.doi.org/10.1165/rcmb.2013-0106OC] [PMID: 23815177]
[40]
Reynolds PR, Mucenski ML, Le Cras TD, Nichols WC, Whitsett JA. Midkine is regulated by hypoxia and causes pulmonary vascular remodeling. J Biol Chem 2004; 279(35): 37124-32.
[http://dx.doi.org/10.1074/jbc.M405254200] [PMID: 15197188]
[41]
Matsui H, Grubb BR, Tarran R, et al. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 1998; 95(7): 1005-15.
[http://dx.doi.org/10.1016/S0092-8674(00)81724-9] [PMID: 9875854]
[42]
Pezzulo AA, Tang XX, Hoegger MJ, et al. Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 2012; 487(7405): 109-13.
[http://dx.doi.org/10.1038/nature11130] [PMID: 22763554]
[43]
Mall M, Grubb BR, Harkema JR, O’Neal WK, Boucher RC. Increased airway epithelial Na+ absorption produces cystic fibrosis-like lung disease in mice. Nat Med 2004; 10(5): 487-93.
[http://dx.doi.org/10.1038/nm1028] [PMID: 15077107]
[44]
Rafii B, Tanswell AK, Otulakowski G, Pitkänen O, Belcastro-Taylor R, O’Brodovich H. O2-induced ENaC expression is associated with NF-kappaB activation and blocked by superoxide scavenger. Am J Physiol 1998; 275(4): L764-70.
[PMID: 9755109]
[45]
Woodworth BA. Resveratrol ameliorates abnormalities of fluid and electrolyte secretion in a hypoxia-Induced model of acquired CFTR deficiency. Laryngoscope 2015; 125(Suppl. 7): S1-S13.
[http://dx.doi.org/10.1002/lary.25335] [PMID: 25946147]
[46]
Dada LA, Chandel NS, Ridge KM, Pedemonte C, Bertorello AM, Sznajder JI. Hypoxia-induced endocytosis of Na,K-ATPase in alveolar epithelial cells is mediated by mitochondrial reactive oxygen species and PKC-zeta. J Clin Invest 2003; 111(7): 1057-64.
[http://dx.doi.org/10.1172/JCI16826] [PMID: 12671055]
[47]
Gille T, Randrianarison-Pellan N, Goolaerts A, et al. Hypoxia-induced inhibition of epithelial Na(+) channels in the lung. Role of Nedd4-2 and the ubiquitin-proteasome pathway. Am J Respir Cell Mol Biol 2014; 50(3): 526-37.
[http://dx.doi.org/10.1165/rcmb.2012-0518OC] [PMID: 24093724]
[48]
Mairbäurl H. Role of alveolar epithelial sodium transport in high altitude pulmonary edema (HAPE). Respir Physiol Neurobiol 2006; 151(2-3): 178-91.
[http://dx.doi.org/10.1016/j.resp.2005.11.001] [PMID: 16337225]
[49]
Planès C, Escoubet B, Blot-Chabaud M, Friedlander G, Farman N, Clerici C. Hypoxia downregulates expression and activity of epithelial sodium channels in rat alveolar epithelial cells. Am J Respir Cell Mol Biol 1997; 17(4): 508-18.
[http://dx.doi.org/10.1165/ajrcmb.17.4.2680] [PMID: 9376126]
[50]
Clerici C, Planès C. Gene regulation in the adaptive process to hypoxia in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 2009; 296(3): L267-74.
[http://dx.doi.org/10.1152/ajplung.90528.2008] [PMID: 19118091]
[51]
Pradervand S, Wang Q, Burnier M, et al. A mouse model for Liddle’s syndrome. J Am Soc Nephrol 1999; 10(12): 2527-33.
[PMID: 10589691]
[52]
Guimbellot JS, Fortenberry JA, Siegal GP, et al. Role of oxygen availability in CFTR expression and function. Am J Respir Cell Mol Biol 2008; 39(5): 514-21.
[http://dx.doi.org/10.1165/rcmb.2007-0452OC] [PMID: 18474670]
[53]
Longo LD. The biological effects of carbon monoxide on the pregnant woman, fetus, and newborn infant. Am J Obstet Gynecol 1977; 129(1): 69-103.
[http://dx.doi.org/10.1016/0002-9378(77)90824-9] [PMID: 561541]
[54]
Underner M, Peiffer G. Interpretation of exhaled CO levels in studies on smokin Rev Mal Respir 2010; 27(4): 293-300.
[http://dx.doi.org/10.1016/j.rmr.2009.09.004] [PMID: 20403540]
[55]
Cantin AM, Hanrahan JW, Bilodeau G, et al. Cystic fibrosis transmembrane conductance regulator function is suppressed in cigarette smokers. Am J Respir Crit Care Med 2006; 173(10): 1139-44.
[http://dx.doi.org/10.1164/rccm.200508-1330OC] [PMID: 16497995]
[56]
Kreindler JL, Jackson AD, Kemp PA, Bridges RJ, Danahay H. Inhibition of chloride secretion in human bronchial epithelial cells by cigarette smoke extract. Am J Physiol Lung Cell Mol Physiol 2005; 288(5): L894-902.
[http://dx.doi.org/10.1152/ajplung.00376.2004] [PMID: 15626749]
[57]
Dransfield MT, Wilhelm AM, Flanagan B, et al. Acquired cystic fibrosis transmembrane conductance regulator dysfunction in the lower airways in COPD. Chest 2013; 144(2): 498-506.
[http://dx.doi.org/10.1378/chest.13-0274] [PMID: 23538783]
[58]
Sloane PA, Shastry S, Wilhelm A, et al. A pharmacologic approach to acquired cystic fibrosis transmembrane conductance regulator dysfunction in smoking related lung disease. PLoS One 2012; 7(6)e39809
[http://dx.doi.org/10.1371/journal.pone.0039809] [PMID: 22768130]
[59]
Bartoszewska S, Kamysz W, Jakiela B, et al. miR-200b downregulates CFTR during hypoxia in human lung epithelial cells. Cell Mol Biol Lett 2017; 22: 23.
[http://dx.doi.org/10.1186/s11658-017-0054-0] [PMID: 29167681]
[60]
Blount A, Zhang S, Chestnut M, et al. Transepithelial ion transport is suppressed in hypoxic sinonasal epithelium. Laryngoscope 2011; 121(9): 1929-34.
[http://dx.doi.org/10.1002/lary.21921] [PMID: 22024847]
[61]
Zheng W, Kuhlicke J, Jäckel K, et al. Hypoxia inducible factor-1 (HIF-1)-mediated repression of cystic fibrosis transmembrane conductance regulator (CFTR) in the intestinal epithelium. FASEB J 2009; 23(1): 204-13.
[http://dx.doi.org/10.1096/fj.08-110221] [PMID: 18779379]
[62]
Greco S, Martelli F. MicroRNAs in hypoxia response. Antioxid Redox Signal 2014; 21(8): 1164-6.
[http://dx.doi.org/10.1089/ars.2014.6083] [PMID: 25098394]
[63]
Mutlu GM, Sznajder JI. Mechanisms of pulmonary edema clearance. Am J Physiol Lung Cell Mol Physiol 2005; 289(5): L685-95.
[http://dx.doi.org/10.1152/ajplung.00247.2005] [PMID: 16214819]
[64]
Suzuki S, Noda M, Sugita M, Ono S, Koike K, Fujimura S. Impairment of transalveolar fluid transport and lung Na(+)-K(+)-ATPase function by hypoxia in rats. J Appl Physiol 1999; 87(3): 962-8.
[http://dx.doi.org/10.1152/jappl.1999.87.3.962] [PMID: 10484564]
[65]
Carpenter TC, Schomberg S, Nichols C, Stenmark KR, Weil JV. Hypoxia reversibly inhibits epithelial sodium transport but does not inhibit lung ENaC or Na-K-ATPase expression. Am J Physiol Lung Cell Mol Physiol 2003; 284(1): L77-83.
[http://dx.doi.org/10.1152/ajplung.00181.2002] [PMID: 12388331]
[66]
Helenius IT, Dada LA, Sznajder JI. Role of ubiquitination in Na,K-ATPase regulation during lung injury. Proc Am Thorac Soc 2010; 7(1): 65-70.
[http://dx.doi.org/10.1513/pats.200907-082JS] [PMID: 20160150]
[67]
Gusarova GA, Dada LA, Kelly AM, et al. Alpha1-AMP-activated protein kinase regulates hypoxia-induced Na,K-ATPase endocytosis via direct phosphorylation of protein kinase C zeta. Mol Cell Biol 2009; 29(13): 3455-64.
[http://dx.doi.org/10.1128/MCB.00054-09] [PMID: 19380482]
[68]
Gusarova GA, Trejo HE, Dada LA, et al. Hypoxia leads to Na,K-ATPase downregulation via Ca(2+) release-activated Ca(2+) channels and AMPK activation. Mol Cell Biol 2011; 31(17): 3546-56.
[http://dx.doi.org/10.1128/MCB.05114-11] [PMID: 21730292]
[69]
Olson KR. Hydrogen sulfide as an oxygen sensor. Antioxid Redox Signal 2015; 22(5): 377-97.
[http://dx.doi.org/10.1089/ars.2014.5930] [PMID: 24801248]
[70]
Krause NC, Kutsche HS, Santangelo F, et al. Hydrogen sulfide contributes to hypoxic inhibition of airway transepithelial sodium absorption. Am J Physiol Regul Integr Comp Physiol 2016; 311(3): R607-17.
[http://dx.doi.org/10.1152/ajpregu.00177.2016] [PMID: 27440715]
[71]
Althaus M, Urness KD, Clauss WG, Baines DL, Fronius M. The gasotransmitter hydrogen sulphide decreases Na+ transport across pulmonary epithelial cells. Br J Pharmacol 2012; 166(6): 1946-63.
[http://dx.doi.org/10.1111/j.1476-5381.2012.01909.x] [PMID: 22352810]
[72]
Campbell HK, Maiers JL, DeMali KA. Interplay between tight junctions & adherens junctions. Exp Cell Res 2017; 358(1): 39-44.
[http://dx.doi.org/10.1016/j.yexcr.2017.03.061] [PMID: 28372972]
[73]
Fritzsching B, Zhou-Suckow Z, Trojanek JB, et al. Hypoxic epithelial necrosis triggers neutrophilic inflammation via IL-1 receptor signaling in cystic fibrosis lung disease. Am J Respir Crit Care Med 2015; 191(8): 902-13.
[http://dx.doi.org/10.1164/rccm.201409-1610OC] [PMID: 25607238]
[74]
Godfrey RW, Severs NJ, Jeffery PK. Structural alterations of airway epithelial tight junctions in cystic fibrosis: comparison of transplant and postmortem tissue. Am J Respir Cell Mol Biol 1993; 9(2): 148-56.
[http://dx.doi.org/10.1165/ajrcmb/9.2.148] [PMID: 8338684]
[75]
Caraballo JC, Yshii C, Butti ML, et al. Hypoxia increases transepithelial electrical conductance and reduces occludin at the plasma membrane in alveolar epithelial cells via PKC-ζ and PP2A pathway. Am J Physiol Lung Cell Mol Physiol 2011; 300(4): L569-78.
[http://dx.doi.org/10.1152/ajplung.00109.2010] [PMID: 21257729]
[76]
Sheth P, Samak G, Shull JA, Seth A, Rao R. Protein phosphatase 2A plays a role in hydrogen peroxide-induced disruption of tight junctions in Caco-2 cell monolayers. Biochem J 2009; 421(1): 59-70.
[http://dx.doi.org/10.1042/BJ20081951] [PMID: 19356149]
[77]
Min HJ, Kim TH, Yoon JH, Kim CH. Hypoxia increases epithelial permeability in human nasal epithelia. Yonsei Med J 2015; 56(3): 825-31.
[http://dx.doi.org/10.3349/ymj.2015.56.3.825] [PMID: 25837192]
[78]
Jimenez FR, Lewis JB, Belgique ST, et al. Cigarette smoke and decreased oxygen tension inhibit pulmonary claudin-6 expression. Exp Lung Res 2016; 42(8-10): 440-52.
[http://dx.doi.org/10.1080/01902148.2016.1261309] [PMID: 27982694]
[79]
Saeedi BJ, Kao DJ, Kitzenberg DA, et al. HIF-dependent regulation of claudin-1 is central to intestinal epithelial tight junction integrity. Mol Biol Cell 2015; 26(12): 2252-62.
[http://dx.doi.org/10.1091/mbc.E14-07-1194] [PMID: 25904334]
[80]
Saatian B, Rezaee F, Desando S, et al. Interleukin-4 and interleukin-13 cause barrier dysfunction in human airway epithelial cells. Tissue Barriers 2013; 1(2)e24333
[http://dx.doi.org/10.4161/tisb.24333] [PMID: 24665390]
[81]
Nagashima A, Shinkai M, Shinoda M, et al. Clarithromycin suppresses chloride channel accessory 1 and inhibits interleukin-13-induced goblet cell hyperplasia in human bronchial epithelial cells. Antimicrob Agents Chemother 2016; 60(11): 6585-90.
[http://dx.doi.org/10.1128/AAC.01327-16] [PMID: 27550358]
[82]
Sajjan U, Wang Q, Zhao Y, Gruenert DC, Hershenson MB. Rhinovirus disrupts the barrier function of polarized airway epithelial cells. Am J Respir Crit Care Med 2008; 178(12): 1271-81.
[http://dx.doi.org/10.1164/rccm.200801-136OC] [PMID: 18787220]
[83]
Schamberger AC, Mise N, Jia J, et al. Cigarette smoke-induced disruption of bronchial epithelial tight junctions is prevented by transforming growth factor-β. Am J Respir Cell Mol Biol 2014; 50(6): 1040-52.
[http://dx.doi.org/10.1165/rcmb.2013-0090OC] [PMID: 24358952]
[84]
Cui Y, Li H, Wu S, et al. Formaldehyde impairs transepithelial sodium transport. Sci Rep 2016; 6: 35857.
[http://dx.doi.org/10.1038/srep35857] [PMID: 27762337]
[85]
Li Y, Chang J, Cui Y, et al. Novel mechanisms for crotonaldehyde-induced lung edema. Oncotarget 2017; 8(48): 83509-22.
[http://dx.doi.org/10.18632/oncotarget.17840] [PMID: 29137360]
[86]
Xian M, Ma S. Particulate matter 2.5 causes deficiency in barrier integrity in human nasal epithelial cells 2020; 12 56: 71.

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