Hypoxia-induced cystic fibrosis transmembrane conductance regulator dysfunction is a universal mechanism underlying reduced mucociliary transport in sinusitis.
CFTR
airway surface liquid
chronic rhinosinusitis
chronic sinusitis
functional microanatomy
glutathione
hypoxia
mucociliary transport
optical coherence tomography
patch clamp
periciliary liquid
potential difference
rabbit sinusitis
sinusitis
Journal
International forum of allergy & rhinology
ISSN: 2042-6984
Titre abrégé: Int Forum Allergy Rhinol
Pays: United States
ID NLM: 101550261
Informations de publication
Date de publication:
11 Dec 2023
11 Dec 2023
Historique:
revised:
30
10
2023
received:
07
08
2022
accepted:
29
11
2023
medline:
11
12
2023
pubmed:
11
12
2023
entrez:
11
12
2023
Statut:
aheadofprint
Résumé
Hypoxia due to sinus obstruction is a major pathogenic mechanism leading to sinusitis. The objective of the current study is to define the electrophysiologic characteristics of hypoxia in vitro and in vivo. Cystic fibrosis bronchoepithelial cells expressing wild-type cystic fibrosis transmembrane conductance regulator (CFTR) and human sinonasal epithelial cells were exposed to 1% or atmospheric O Ussing chamber (p < 0.05), whole-cell (p < 0.001), and single channel patch-clamp (p < 0.0001) showed significant inhibition of Cl Hypoxia induces severe CFTR dysfunction via free radical production causing reduced MCT in vitro and in vivo. Improved oxygenation is critical to reducing the impact of persistent mucociliary dysfunction.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIDDK NIH HHS
ID : 5P30DK072482-05
Pays : United States
Organisme : NIEHS NIH HHS
ID : 5UO1 ES026458
Pays : United States
Organisme : NIEHS NIH HHS
ID : 3UO1 ES026458 03S1
Pays : United States
Organisme : NIEHS NIH HHS
ID : 5UO1 ES027697
Pays : United States
Organisme : NCCIH NIH HHS
ID : R21AT012234-01
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL133006-05
Pays : United States
Organisme : NHLBI NIH HHS
ID : HL107142-05
Pays : United States
Informations de copyright
© 2023 ARS-AAOA, LLC.
Références
Wanner A, Salathe M, O'Riordan TG. Mucociliary clearance in the airways. Am J Respir Crit Care Med. 1996;154:1868-1902.
Robinson M, Bye PT. Mucociliary clearance in cystic fibrosis. Pediatr Pulmonol. 2002;33:293-306.
Wine JJ, Joo NS. Submucosal glands and airway defense. Proc Am Thorac Soc. 2004;1:47-53.
Hariri BM, Cohen NA. New insights into upper airway innate immunity. Am J Rhinol Allergy. 2016;30:319-323.
Sisson JH, Stoner JA, Ammons BA, Wyatt TA. All-digital image capture and whole-field analysis of ciliary beat frequency. J Microsc. 2003;211:103-111.
Alexander NS, Blount A, Zhang S, et al. Cystic fibrosis transmembrane conductance regulator modulation by the tobacco smoke toxin acrolein. Laryngoscope. 2012;122:1193-1197.
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.
Cho DY, Woodworth BA. Acquired cystic fibrosis transmembrane conductance regulator deficiency. Adv Otorhinolaryngol. 2016;79:78-85.
Blount A, Zhang S, Chestnut M, et al. Transepithelial ion transport is suppressed in hypoxic sinonasal epithelium. Laryngoscope. 2011;121:1929-1934.
Moller W, Haussinger K, Ziegler-Heitbrock L, Heyder J. Mucociliary and long-term particle clearance in airways of patients with immotile cilia. Respir Res. 2006;7:10.
Chaaban MR, Kejner A, Rowe SM, Woodworth BA. Cystic fibrosis chronic rhinosinusitis: a comprehensive review. Am J Rhinol Allergy. 2013;27:387-395.
Illing EA, Woodworth BA. Management of the upper airway in cystic fibrosis. Curr Opin Pulm Med. 2014;20:623-631.
Virgin FW, Rowe SM, Wade MB, et al. Extensive surgical and comprehensive postoperative medical management for cystic fibrosis chronic rhinosinusitis. Am J Rhinol Allergy. 2012;26:70-75.
Tipirneni KE, Woodworth BA. Medical and surgical advancements in the management of cystic fibrosis chronic rhinosinusitis. Curr Otorhinolaryngol Rep. 2017;5:24-34.
Cho DY, Zhang S, Lazrak A, et al. LPS decreases CFTR open probability and mucociliary transport through generation of reactive oxygen species. Redox Biol. 2021;43:101998.
McCormick J, Hoffman K, Thompson H, et al. Differential chloride secretory capacity in transepithelial ion transport properties in chronic rhinosinusitis. Am J Rhinol Allergy. 2020;34:830-837.
Banks C, Freeman L, Cho DY, Woodworth BA. Acquired cystic fibrosis transmembrane conductance regulator dysfunction. World J Otorhinolaryngol Head Neck Surg. 2018;4:193-199.
Virgin FW, Azbell C, Schuster D, et al. Exposure to cigarette smoke condensate reduces calcium activated chloride channel transport in primary sinonasal epithelial cultures. Laryngoscope. 2010;120:1465-1469.
Cohen NA, Zhang S, Sharp DB, et al. Cigarette smoke condensate inhibits transepithelial chloride transport and ciliary beat frequency. Laryngoscope. 2009;119:2269-2274.
MacEachran DP, Stanton BA, O'Toole GA. Cif is negatively regulated by the TetR family repressor CifR. Infect Immun. 2008;76:3197-3206.
MacEachran DP, Ye S, Bomberger JM, et al. The Pseudomonas aeruginosa secreted protein PA2934 decreases apical membrane expression of the cystic fibrosis transmembrane conductance regulator. Infect Immun. 2007;75:3902-3912.
Bebok Z, Tousson A, Schwiebert LM, Venglarik CJ. Improved oxygenation promotes CFTR maturation and trafficking in MDCK monolayers. Am J Physiol Cell Physiol. 2001;280:C135-C145.
Bebok Z, Varga K, Hicks JK, et al. Reactive oxygen nitrogen species decrease cystic fibrosis transmembrane conductance regulator expression and cAMP-mediated Cl- secretion in airway epithelia. J Biol Chem. 2002;277:43041-43049.
Worlitzsch D, Tarran R, Ulrich M, et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest. 2002;109:317-325.
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.
Aanaes K, Rickelt LF, Johansen HK, et al. Decreased mucosal oxygen tension in the maxillary sinuses in patients with cystic fibrosis. J Cyst Fibros. 2011;10:114-120.
Tipirneni KE, Grayson JW, Zhang S, et al. Assessment of acquired mucociliary clearance defects using micro-optical coherence tomography. Int Forum Allergy Rhinol. 2017;7:920-925.
Gruenert DC, Willems M, Cassiman JJ, Frizzell RA. Established cell lines used in cystic fibrosis research. J Cyst Fibros. 2004;3(Suppl 2):191-196.
Farrell PM, White TB, Howenstine MS, et al. Diagnosis of cystic fibrosis in screened populations. J Pediatr. 2017;181S:S33-S44. e32.
Bhargave G, Woodworth BA, Xiong G, Wolfe SG, Antunes MB, Cohen NA. Transient receptor potential vanilloid type 4 channel expression in chronic rhinosinusitis. Am J Rhinol. 2008;22:7-12.
Woodworth BA, Antunes MB, Bhargave G, Palmer JN, Cohen NA. Murine tracheal and nasal septal epithelium for air-liquid interface cultures: a comparative study. Am J Rhinol. 2007;21:533-537.
Antunes MB, Woodworth BA, Bhargave G, et al. Murine nasal septa for respiratory epithelial air-liquid interface cultures. BioTechniques. 2007;43:195-196. 198, 200 passim.
Woodworth BA, Tamashiro E, Bhargave G, Cohen NA, Palmer JN. An in vitro model of Pseudomonas aeruginosa biofilms on viable airway epithelial cell monolayers. Am J Rhinol. 2008;22:235-238.
Zhang S, Fortenberry JA, Cohen NA, Sorscher EJ, Woodworth BA. Comparison of vectorial ion transport in primary murine airway and human sinonasal air-liquid interface cultures, models for studies of cystic fibrosis, and other airway diseases. Am J Rhinol Allergy. 2009;23:149-152.
Dean N, Ranganath NK, Jones B, et al. Porcine nasal epithelial cultures for studies of cystic fibrosis sinusitis. Int Forum Allergy Rhinol. 2014;4:565-570.
Kumar P, Nagarajan A, Uchil PD. Analysis of cell viability by the lactate dehydrogenase assay. Cold Spring Harb Protoc. 2018;2018. doi:10.1101/pdb.prot095497
Cho DY, Zhang S, Lazrak A, et al. Resveratrol and ivacaftor are additive G551D CFTR-channel potentiators: therapeutic implications for cystic fibrosis sinus disease. Int Forum Allergy Rhinol. 2019;9:100-105.
Ramella NA, Schinella GR, Ferreira ST, et al. Human apolipoprotein A-I natural variants: molecular mechanisms underlying amyloidogenic propensity. PLoS One. 2012;7:e43755.
Liu L, Chu KK, Houser GH, et al. Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography. PLoS One. 2013;8:e54473.
Leung HM, Birket SE, Hyun C, et al. Intranasal micro-optical coherence tomography imaging for cystic fibrosis studies. Sci Transl Med. 2019;11:eaav3505.
Cho DY, Skinner D, Mackey C, et al. Herbal dry extract BNO 1011 improves clinical and mucociliary parameters in a rabbit model of chronic rhinosinusitis. Int Forum Allergy Rhinol. 2019;9:629-637.
Cho DY, Mackey C, Van Der Pol WJ, et al. Sinus microanatomy and microbiota in a rabbit model of rhinosinusitis. Front Cell Infect Microbiol. 2017;7:540.
Birket SE, Chu KK, Houser GH, et al. Combination therapy with cystic fibrosis transmembrane conductance regulator modulators augment the airway functional microanatomy. Am J Physiol Lung Cell Mol Physiol. 2016;310:L928-939.
Cho DY, Hoffman K, Skinner D, et al. Tolerance and pharmacokinetics of a ciprofloxacin-coated sinus stent in a preclinical model. Int Forum Allergy Rhinol. 2016;7:352-358.
Zhang S, Ranganath NK, Skinner D, et al. Marked repression of CFTR mRNA in the transgenic Cftr(tm1kth) mouse model. J Cyst Fibros. 2014;13:351-352.
Alexander NS, Hatch N, Zhang S, et al. Resveratrol has salutary effects on mucociliary transport and inflammation in sinonasal epithelium. Laryngoscope. 2011;121:1313-1319.
Virgin F, Zhang S, Schuster D, et al. The bioflavonoid compound, sinupret, stimulates transepithelial chloride transport in vitro and in vivo. Laryngoscope. 2010;120:1051-1056.
Brand JD, Lazrak A, Trombley JE, et al. Influenza-mediated reduction of lung epithelial ion channel activity leads to dysregulated pulmonary fluid homeostasis. JCI Insight. 2018;3:e123467.
Zhang S, Blount AC, McNicholas CM, et al. Resveratrol enhances airway surface liquid depth in sinonasal epithelium by increasing cystic fibrosis transmembrane conductance regulator open probability. PLoS One. 2013;8:e81589.
Cho DY, Zhang S, Skinner DF, et al. Ivacaftor restores delayed mucociliary transport caused by Pseudomonas aeruginosa-induced acquired cystic fibrosis transmembrane conductance regulator dysfunction in rabbit nasal epithelia. Int Forum Allergy Rhinol. 2022;12:690-698.
Cho DY, Skinner D, Zhang S, et al. Korean Red Ginseng aqueous extract improves markers of mucociliary clearance by stimulating chloride secretion. J Ginseng Res. 2021;45:66-74.
McCormick J, Cho DY, Lampkin B, et al. Ivacaftor improves rhinologic, psychologic, and sleep-related quality of life in G551D cystic fibrosis patients. Int Forum Allergy Rhinol. 2019;9:292-297.
Cho DY, Lim DJ, Mackey C, et al. Ivacaftor, a cystic fibrosis transmembrane conductance regulator potentiator, enhances ciprofloxacin activity against Pseudomonas aeruginosa. Am J Rhinol Allergy. 2019;33:129-136.
Zhang S, Skinner D, Hicks SB, et al. Sinupret activates CFTR and TMEM16A-dependent transepithelial chloride transport and improves indicators of mucociliary clearance. PLoS One. 2014;9:e104090.
Zhang S, Smith N, Schuster D, et al. Quercetin increases cystic fibrosis transmembrane conductance regulator-mediated chloride transport and ciliary beat frequency: therapeutic implications for chronic rhinosinusitis. Am J Rhinol Allergy. 2011;25:307-312.
Lim DJ, Skinner D, West JM, et al. In vitro evaluation of a novel oxygen-generating biomaterial for chronic rhinosinusitis therapy. Int Forum Allergy Rhinol. 2022;12:181-190.
Bridgeman MM, Marsden M, Selby C, Morrison D, MacNee W. Effect of N-acetyl cysteine on the concentrations of thiols in plasma, bronchoalveolar lavage fluid, and lung tissue. Thorax. 1994;49:670-675.
Schreiber J, Bohnsteen B, Rosahl W. Influence of mucolytic therapy on respiratory mechanics in patients with chronic obstructive pulmonary disease. Eur J Med Res. 2002;7:98-102.