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Carver Chair in Pulmonary Research"},{"name":"American Society of Gene and Cell Therapy Career Development Award"},{"DOI":"10.13039\/100001100","name":"Boomer Esiason Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100001100","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Vertex Mentored Research Innovation Award"},{"name":"WellsLee Foundation"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,9,9]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>A fundamental challenge for cystic fibrosis (CF) gene therapy is ensuring sufficient transduction of airway epithelia to achieve therapeutic correction. Hypertonic saline (HTS) is frequently administered to people with CF to enhance mucus clearance. HTS transiently disrupts epithelial cell tight junctions, but its ability to improve gene transfer has not been investigated. Here, we asked if increasing the concentration of NaCl enhances the transduction efficiency of three gene therapy vectors: adenovirus, AAV, and lentiviral vectors. Vectors formulated with 3\u20137% NaCl exhibited markedly increased transduction for all three platforms, leading to anion channel correction in primary cultures of human CF epithelial cells and enhanced gene transfer in mouse and pig airways in vivo. The mechanism of transduction enhancement involved tonicity but not osmolarity or pH. Formulating vectors with a high ionic strength solution is a simple strategy to greatly enhance efficacy and immediately improve preclinical or clinical applications.<\/jats:p>","DOI":"10.1093\/nar\/gkae640","type":"journal-article","created":{"date-parts":[[2024,7,9]],"date-time":"2024-07-09T17:49:00Z","timestamp":1720547340000},"page":"9369-9383","source":"Crossref","is-referenced-by-count":9,"title":["High ionic strength vector formulations enhance gene transfer to airway epithelia"],"prefix":"10.1093","volume":"52","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2717-9138","authenticated-orcid":false,"given":"Ashley\u00a0L","family":"Cooney","sequence":"first","affiliation":[{"name":"University of Iowa, Stead Family Department of Pediatrics ; Iowa City , IA 52242 , USA"},{"name":"University of Iowa, Pappajohn Biomedical Institute ; Iowa City , IA 52242 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura\u00a0Marquez","family":"Loza","sequence":"additional","affiliation":[{"name":"University of Iowa, Stead Family Department of Pediatrics ; Iowa City , IA 52242 , USA"},{"name":"University of Iowa, Pappajohn Biomedical Institute ; Iowa City , IA 52242 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kenan","family":"Najdawi","sequence":"additional","affiliation":[{"name":"University of Iowa, Stead Family Department of Pediatrics ; Iowa City , IA 52242 , USA"},{"name":"University of Iowa, Pappajohn Biomedical Institute ; Iowa City , IA 52242 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian\u00a0M","family":"Brommel","sequence":"additional","affiliation":[{"name":"University of Iowa, Stead Family Department of Pediatrics ; Iowa City , IA 52242 , USA"},{"name":"University of Iowa, Pappajohn Biomedical Institute ; Iowa City , IA 52242 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4067-577X","authenticated-orcid":false,"suffix":"Jr.","given":"Paul\u00a0B","family":"McCray","sequence":"additional","affiliation":[{"name":"University of Iowa, Stead Family Department of Pediatrics ; Iowa City , IA 52242 , USA"},{"name":"University of Iowa, Pappajohn Biomedical Institute ; Iowa City , IA 52242 , USA"},{"name":"University of Iowa, Center for Gene Therapy ; Iowa City , IA 52242 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrick\u00a0L","family":"Sinn","sequence":"additional","affiliation":[{"name":"University of Iowa, Stead Family Department of Pediatrics ; Iowa City , IA 52242 , USA"},{"name":"University of Iowa, Pappajohn Biomedical Institute ; Iowa City , IA 52242 , USA"},{"name":"University of Iowa, Center for Gene Therapy ; Iowa City , IA 52242 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,7,30]]},"reference":[{"key":"2024090904010008500_B1","doi-asserted-by":"crossref","first-page":"e88730","DOI":"10.1172\/jci.insight.88730","article-title":"Lentiviral-mediated phenotypic correction of cystic fibrosis pigs","volume":"1","author":"Cooney","year":"2016","journal-title":"JCI Insight"},{"key":"2024090904010008500_B2","doi-asserted-by":"crossref","first-page":"9591","DOI":"10.1093\/nar\/gky773","article-title":"Widespread airway distribution and short-term phenotypic correction of cystic fibrosis pigs following aerosol delivery of piggyBac\/adenovirus","volume":"46","author":"Cooney","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"2024090904010008500_B3","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1165\/rcmb.2019-0006OC","article-title":"A novel AAV-mediated gene delivery system corrects CFTR function in pigs","volume":"61","author":"Cooney","year":"2019","journal-title":"Am. J. Respir. Cell Mol. Biol."},{"key":"2024090904010008500_B4","doi-asserted-by":"crossref","first-page":"538","DOI":"10.3390\/genes9110538","article-title":"Cystic Fibrosis gene therapy: looking back, looking forward","volume":"9","author":"Cooney","year":"2018","journal-title":"Genes (Basel)"},{"key":"2024090904010008500_B5","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1186\/1465-9921-11-84","article-title":"Lysophosphatidylcholine as an adjuvant for lentiviral vector mediated gene transfer to airway epithelium: effect of acyl chain length","volume":"11","author":"Cmielewski","year":"2010","journal-title":"Respir. Res."},{"key":"2024090904010008500_B6","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1165\/ajrcmb.22.2.3938","article-title":"Increasing epithelial junction permeability enhances gene transfer to airway epithelia In vivo","volume":"22","author":"Wang","year":"2000","journal-title":"Am. J. Respir. Cell Mol. Biol."},{"key":"2024090904010008500_B7","doi-asserted-by":"crossref","first-page":"9818","DOI":"10.1128\/JVI.72.12.9818-9826.1998","article-title":"Influence of cell polarity on retrovirus-mediated gene transfer to differentiated human airway epithelia","volume":"72","author":"Wang","year":"1998","journal-title":"J. Virol."},{"key":"2024090904010008500_B8","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1165\/rcmb.2004-0410OC","article-title":"Viscoelastic gel formulations enhance airway epithelial gene transfer with viral vectors","volume":"32","author":"Sinn","year":"2005","journal-title":"Am. J. Respir. Cell Mol. Biol."},{"key":"2024090904010008500_B9","doi-asserted-by":"crossref","first-page":"918036","DOI":"10.1155\/2011\/918036","article-title":"Perfluorochemical liquid-adenovirus suspensions enhance gene delivery to the distal lung","volume":"2011","author":"Kazzaz","year":"2011","journal-title":"Pulm. Med."},{"key":"2024090904010008500_B10","doi-asserted-by":"crossref","first-page":"1444","DOI":"10.1183\/09031936.02.00017202","article-title":"Hypertonic saline increases tight junction permeability in airway epithelium","volume":"20","author":"Hogman","year":"2002","journal-title":"Eur. Respir. J."},{"key":"2024090904010008500_B11","doi-asserted-by":"crossref","first-page":"S2","DOI":"10.1258\/JRSM.2011.S11101","article-title":"Mechanisms and applications of hypertonic saline","volume":"104","author":"Elkins","year":"2011","journal-title":"J. R. Soc. Med."},{"key":"2024090904010008500_B12","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1055\/s-2007-981650","article-title":"Rationale for hypertonic saline therapy for cystic fibrosis lung disease","volume":"28","author":"Tarran","year":"2007","journal-title":"Semin. Respir. Crit. Care Med."},{"key":"2024090904010008500_B13","first-page":"115","article-title":"An in vitro model of differentiated human airway epithelia. Methods for establishing primary cultures","volume":"188","author":"Karp","year":"2002","journal-title":"Methods Mol. Biol."},{"key":"2024090904010008500_B14","doi-asserted-by":"crossref","first-page":"1034","DOI":"10.1038\/sj.gt.3301197","article-title":"A simple method for the rapid generation of recombinant adenovirus vectors","volume":"7","author":"Anderson","year":"2000","journal-title":"Gene Ther."},{"key":"2024090904010008500_B15","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1007\/978-1-4939-7116-9_5","article-title":"Lentiviral vectors pseudotyped with filoviral glycoproteins","volume":"1628","author":"Sinn","year":"2017","journal-title":"Methods Mol. Biol."},{"key":"2024090904010008500_B16","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/j.omtn.2021.06.010","article-title":"Lentiviral vectors transduce lung stem cells without disrupting plasticity","volume":"25","author":"Cooney","year":"2021","journal-title":"Mol. Ther. 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Commun."},{"key":"2024090904010008500_B20","doi-asserted-by":"crossref","first-page":"e9909","DOI":"10.1371\/journal.pone.0009909","article-title":"Isoform-specific regulation and localization of the coxsackie and adenovirus receptor in human airway epithelia","volume":"5","author":"Excoffon","year":"2010","journal-title":"PLoS One"},{"key":"2024090904010008500_B21","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1186\/s13052-021-01117-1","article-title":"Hypertonic saline in people with cystic fibrosis: review of comparative studies and clinical practice","volume":"47","author":"Terlizzi","year":"2021","journal-title":"Ital. J. Pediatr."},{"key":"2024090904010008500_B22","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1038\/mt.2014.254","article-title":"Hybrid nonviral\/viral vector systems for improved piggyBac DNA transposon in vivo delivery","volume":"23","author":"Cooney","year":"2015","journal-title":"Mol. Ther."},{"key":"2024090904010008500_B23","doi-asserted-by":"crossref","first-page":"e171268","DOI":"10.1172\/JCI171268","article-title":"CFTR-rich ionocytes mediate chloride absorption across airway epithelia","volume":"133","author":"Lei","year":"2023","journal-title":"J. Clin. Invest."},{"key":"2024090904010008500_B24","doi-asserted-by":"crossref","first-page":"10558","DOI":"10.1093\/nar\/gkab788","article-title":"Functional correction of CFTR mutations in human airway epithelial cells using adenine base editors","volume":"49","author":"Krishnamurthy","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"2024090904010008500_B25","doi-asserted-by":"crossref","first-page":"4454","DOI":"10.1128\/JVI.78.9.4454-4462.2004","article-title":"The human membrane cofactor CD46 is a receptor for species B adenovirus serotype 3","volume":"78","author":"Sirena","year":"2004","journal-title":"J. Virol."},{"key":"2024090904010008500_B26","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1038\/gt.2017.78","article-title":"Novel GP64 envelope variants for improved delivery to human airway epithelial cells","volume":"24","author":"Sinn","year":"2017","journal-title":"Gene Ther."},{"key":"2024090904010008500_B27","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.omtm.2021.02.020","article-title":"Increased CFTR expression and function from an optimized lentiviral vector for cystic fibrosis gene therapy","volume":"21","author":"Marquez\u00a0Loza","year":"2021","journal-title":"Mol. Ther. Methods Clin. Dev."},{"key":"2024090904010008500_B28","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1089\/hum.2005.16.479","article-title":"Gene transfer to respiratory epithelia with lentivirus pseudotyped with Jaagsiekte sheep retrovirus envelope glycoprotein","volume":"16","author":"Sinn","year":"2005","journal-title":"Hum. Gene Ther."},{"key":"2024090904010008500_B29","doi-asserted-by":"crossref","first-page":"1221","DOI":"10.1182\/blood-2014-02-558163","article-title":"Baboon envelope pseudotyped LVs outperform VSV-G-LVs for gene transfer into early-cytokine-stimulated and resting HSCs","volume":"124","author":"Girard-Gagnepain","year":"2014","journal-title":"Blood"},{"key":"2024090904010008500_B30","doi-asserted-by":"crossref","first-page":"3865","DOI":"10.1073\/pnas.0813365106","article-title":"Directed evolution of adeno-associated virus to an infectious respiratory virus","volume":"106","author":"Excoffon","year":"2009","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"2024090904010008500_B31","doi-asserted-by":"crossref","first-page":"990","DOI":"10.1016\/j.ymthe.2004.08.009","article-title":"Dual therapeutic utility of proteasome modulating agents for pharmaco-gene therapy of the cystic fibrosis airway","volume":"10","author":"Zhang","year":"2004","journal-title":"Mol. Ther."},{"key":"2024090904010008500_B32","doi-asserted-by":"crossref","DOI":"10.1101\/2024.02.03.578756","article-title":"Prolonged airway explant culture enables study of health, disease, and viral pathogenesis","author":"Lee-Ferris","year":"2024"},{"key":"2024090904010008500_B33","doi-asserted-by":"crossref","first-page":"e88728","DOI":"10.1172\/jci.insight.88728","article-title":"CFTR gene transfer with AAV improves early cystic fibrosis pig phenotypes","volume":"1","author":"Steines","year":"2016","journal-title":"JCI Insight"},{"key":"2024090904010008500_B34","doi-asserted-by":"crossref","first-page":"e69","DOI":"10.1038\/mtna.2012.60","article-title":"Intrapulmonary versus nasal transduction of murine airways with GP64-pseudotyped viral vectors","volume":"2","author":"Oakland","year":"2013","journal-title":"Mol. Ther. Nucleic Acids"},{"key":"2024090904010008500_B35","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1056\/NEJMoa043900","article-title":"A controlled trial of long-term inhaled hypertonic saline in patients with cystic fibrosis","volume":"354","author":"Elkins","year":"2006","journal-title":"N. Engl. J. Med."},{"key":"2024090904010008500_B36","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1089\/hum.2015.001","article-title":"Optimization of recombinant adeno-associated virus-mediated expression for large transgenes, using a synthetic promoter and tandem array enhancers","volume":"26","author":"Yan","year":"2015","journal-title":"Hum. Gene Ther."},{"key":"2024090904010008500_B37","doi-asserted-by":"crossref","first-page":"2921","DOI":"10.1073\/pnas.1019752108","article-title":"Cystic fibrosis transmembrane conductance regulator with a shortened R domain rescues the intestinal phenotype of CFTR-\/- mice","volume":"108","author":"Ostedgaard","year":"2011","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"2024090904010008500_B38","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1038\/s41434-022-00332-7","article-title":"Effective viral-mediated lung gene therapy: is airway surface preparation necessary?","volume":"30","author":"McCarron","year":"2023","journal-title":"Gene Ther."},{"key":"2024090904010008500_B39","doi-asserted-by":"crossref","first-page":"1373","DOI":"10.1016\/S0169-409X(02)00145-X","article-title":"Barriers to and new approaches for gene therapy and gene delivery in cystic fibrosis","volume":"54","author":"Ferrari","year":"2002","journal-title":"Adv. Drug. Deliv. Rev."},{"key":"2024090904010008500_B40","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.omtm.2022.02.011","article-title":"Testing preexisting antibodies prior to AAV gene transfer therapy: rationale, lessons and future considerations","volume":"25","author":"Mendell","year":"2022","journal-title":"Mol. Ther. Methods Clin. Dev."},{"key":"2024090904010008500_B41","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1182\/blood-2013-01-306647","article-title":"Immune responses to AAV vectors: overcoming barriers to successful gene therapy","volume":"122","author":"Mingozzi","year":"2013","journal-title":"Blood"},{"key":"2024090904010008500_B42","doi-asserted-by":"crossref","first-page":"e143780","DOI":"10.1172\/JCI143780","article-title":"Overcoming innate immune barriers that impede AAV gene therapy vectors","volume":"131","author":"Muhuri","year":"2021","journal-title":"J. Clin. 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Sci."},{"key":"2024090904010008500_B46","doi-asserted-by":"crossref","first-page":"4698","DOI":"10.1128\/JVI.74.10.4698-4704.2000","article-title":"Retrovirus vectors bearing jaagsiekte sheep retrovirus Env transduce human cells by using a new receptor localized to chromosome 3p21.3","volume":"74","author":"Rai","year":"2000","journal-title":"J. Virol."},{"key":"2024090904010008500_B47","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1128\/MMBR.65.3.371-389.2001","article-title":"Receptors and entry cofactors for retroviruses include single and multiple transmembrane-spanning proteins as well as newly described glycophosphatidylinositol-anchored and secreted proteins","volume":"65","author":"Overbaugh","year":"2001","journal-title":"Microbiol. Mol. Biol. 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