BMI-1 extends proliferative potential of human bronchial epithelial cells while retaining their mucociliary differentiation capacity

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 312, Issue 2, 2016, Pages L258-L267

  Munye, Mustafa M ^a   Shoemark, Amelia ^b   Hirst, Robert A ^c   Delhove, Juliette M ^a   Sharp, Tyson V ^d   McKay, Tristan R ^e   O’Callaghan, Christopher ^a   Baines, Deborah L ^f   Howe, Steven J ^a   Hart, Stephen L ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ROYAL BROMPTON AND HAREFIELD NHS FOUNDATION TRUST   (United Kingdom)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^e MANCHESTER METROPOLITAN UNIVERSITY   (United Kingdom)

^f ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Air liquid interface; Airway model; Lung; Mucociliary differentiation; Primary ciliary dyskinesia

Indexed keywords

BMI1 PROTEIN; DNAH5 PROTEIN; MUCIN; MUCIN 5AC; MUCIN 5B; PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; AXONEMAL DYNEIN; BMI1 PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DNAH5 PROTEIN, HUMAN; DYNEIN ADENOSINE TRIPHOSPHATASE;

ARTICLE; BASAL CELL; BRONCHUS EPITHELIUM; CELL DIFFERENTIATION; CELL DIVISION; CELL KINETICS; CELL PROLIFERATION; CELL ULTRASTRUCTURE; CILIARY MOTILITY; CONTROLLED STUDY; EPITHELIUM BASAL CELL; HUMAN; HUMAN CELL; KARYOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BIOLOGICAL MODEL; BRONCHUS; CELL SHAPE; CILIUM; CYTOLOGY; ELECTROPHYSIOLOGY; EPITHELIUM CELL; GENE SILENCING; GENETIC TRANSDUCTION; HEK293 CELL LINE; IMPEDANCE; KARTAGENER SYNDROME; KARYOTYPING; METABOLISM; MICROTUBULE; MOUSE; MUCUS; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE;

ANIMALS; AXONEMAL DYNEINS; BRONCHI; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SHAPE; CILIA; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DYNEINS; ELECTRIC IMPEDANCE; ELECTROPHYSIOLOGICAL PHENOMENA; EPITHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; KARTAGENER SYNDROME; KARYOTYPING; MICE; MICROTUBULES; MODELS, BIOLOGICAL; MUCUS; PHENOTYPE; POLYCOMB REPRESSIVE COMPLEX 1; TRANSDUCTION, GENETIC;

EID: 85012060314     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00471.2016     Document Type: Article

References (29)

1. Brookes S, Rowe J, Gutierrez Del Arroyo A, Bond J, Peters G. Contribution of p16(INK4a) to replicative senescence of human fibroblasts. Exp Cell Res 298: 549–559, 2004. doi:10.1016/j.yexcr.2004.04.035.
2. Butler CR, Hynds RE, Gowers KH, Lee DH, Brown JM, Crowley C, Teixeira VH, Smith CM, Urbani L, Hamilton NJ, Thakrar RM, Booth HL, Birchall MA, De Coppi P, Giangreco A, O’Callaghan C, Janes SM. Rapid expansion of human epithelial stem cells suitable for airway tissue engineering. Am J Respir Crit Care Med 194: 156–168, 2016. doi:10.1164/rccm.201507-1414OC.
3. Chu Q, Tousignant JD, Fang S, Jiang C, Eastman SJ, Chen LH, Cheng SH, Scheule RK. Binding and uptake of cationic lipid:pDNA complexes by polarized airway epithelial cells. Hum Gene Ther 10: 25–36, 1999. doi:10.1089/10430349950019165.
4. Cozens AL, Yezzi MJ, Kunzelmann K, Ohrui T, Chin L, Eng K, Finkbeiner WE, Widdicombe JH, Gruenert DC. CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol 10: 38–47, 1994. doi:10.1165/ajrcmb.10.1.7507342.
5. Fulcher ML, Gabriel SE, Olsen JC, Tatreau JR, Gentzsch M, Livanos E, Saavedra MT, Salmon P, Randell SH. Novel human bronchial epithelial cell lines for cystic fibrosis research. Am J Physiol Lung Cell Mol Physiol 296: L82–L91, 2009. doi:10.1152/ajplung.90314.2008.
6. Hirst RA, Rutman A, Williams G, O’Callaghan C. Ciliated air-liquid cultures as an aid to diagnostic testing of primary ciliary dyskinesia. Chest 138: 1441–1447, 2010. doi:10.1378/chest.10-0175.
7. Horani A, Brody SL, Ferkol TW, Shoseyov D, Wasserman MG, Ta-shma A, Wilson KS, Bayly PV, Amirav I, Cohen-Cymberknoh M, Dutcher SK, Elpeleg O, Kerem E. CCDC65 mutation causes primary ciliary dyskinesia with normal ultrastructure and hyperkinetic cilia. PLoS One 8: e72299, 2013. doi:10.1371/journal.pone.0072299.
8. Horani A, Ferkol TW, Shoseyov D, Wasserman MG, Oren YS, Kerem B, Amirav I, Cohen-Cymberknoh M, Dutcher SK, Brody SL, Elpeleg O, Kerem E. LRRC6 mutation causes primary ciliary dyskinesia with dynein arm defects. PLoS One 8: e59436, 2013. doi:10.1371/journal.pone.0059436.
9. Horani A, Nath A, Wasserman MG, Huang T, Brody SL. Rhoassociated protein kinase inhibition enhances airway epithelial Basal-cell proliferation and lentivirus transduction. Am J Respir Cell Mol Biol 49: 341–347, 2013. doi:10.1165/rcmb.2013-0046TE.
10. Hornef N, Olbrich H, Horvath J, Zariwala MA, Fliegauf M, Loges NT, Wildhaber J, Noone PG, Kennedy M, Antonarakis SE, Blouin JL, Bartoloni L, Nüsslein T, Ahrens P, Griese M, Kuhl H, Sudbrak R, Knowles MR, Reinhardt R, Omran H. DNAH5 mutations are a common cause of primary ciliary dyskinesia with outer dynein arm defects. Am J Respir Crit Care Med 174: 120–126, 2006. doi:10.1164/rccm.200601-084OC.
11. Hussain S, Ji Z, Taylor AJ, DeGraff LM, George M, Tucker CJ, Chang CH, Li R, Bonner JC, Garantziotis S. Multiwalled carbon nanotube functionalization with high molecular weight hyaluronan significantly reduces pulmonary injury. ACS Nano 10: 7675–7688, 2016. doi:10.1021/acsnano.6b03013.
12. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397: 164–168, 1999. doi:10.1038/16476.
13. Kesimer M, Kirkham S, Pickles RJ, Henderson AG, Alexis NE, Demaria G, Knight D, Thornton DJ, Sheehan JK. Tracheobronchial air-liquid interface cell culture: a model for innate mucosal defense of the upper airways? Am J Physiol Lung Cell Mol Physiol 296: L92–L100, 2009. doi:10.1152/ajplung.90388.2008.
14. Li Y, Yagi H, Onuoha EO, Damerla RR, Francis R, Furutani Y, Tariq M, King SM, Hendricks G, Cui C, Saydmohammed M, Lee DM, Zahid M, Sami I, Leatherbury L, Pazour GJ, Ware SM, Nakanishi T, Goldmuntz E, Tsang M, Lo CW. DNAH6 and its interactions with PCD genes in heterotaxy and primary ciliary dyskinesia. PLoS Genet 12: e1005821, 2016. doi:10.1371/journal.pgen.1005821.
15. Liu X, Ory V, Chapman S, Yuan H, Albanese C, Kallakury B, Timofeeva OA, Nealon C, Dakic A, Simic V, Haddad BR, Rhim JS, Dritschilo A, Riegel A, McBride A, Schlegel R. ROCK inhibitor and feeder cells induce the conditional reprogramming of epithelial cells. Am J Pathol 180: 599–607, 2012. doi:10.1016/j.ajpath.2011.10.036.
16. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402–408, 2001. doi:10.1006/meth.2001.1262.
17. McKay TR, Camarasa MV, Iskender B, Ye J, Bates N, Miller D, Fitzsimmons JC, Foxler D, Mee M, Sharp TV, Aplin J, Brison DR, Kimber SJ. Human feeder cell line for derivation and culture of hESc/hiPSc. Stem Cell Res (Amst) 7: 154–162, 2011. doi:10.1016/j.scr.2011.04.005.
18. Milyavsky M, Shats I, Erez N, Tang X, Senderovich S, Meerson A, Tabach Y, Goldfinger N, Ginsberg D, Harris CC, Rotter V. Prolonged culture of telomerase-immortalized human fibroblasts leads to a premalignant phenotype. Cancer Res 63: 7147–7157, 2003.
19. Reynolds SD, Rios C, Wesolowska-Andersen A, Zhuang Y, Pinter M, Happoldt C, Hill CL, Lallier SW, Cosgrove GP, Solomon GM, Nichols DP, Seibold MA. Airway progenitor clone formation is enhanced by Y-27632-dependent changes in the transcriptome. Am J Respir Cell Mol Biol 55: 323–336, 2016. doi:10.1165/rcmb.2015-0274MA.
20. Rousseau K, Wickstrom C, Whitehouse DB, Carlstedt I, Swallow DM. New monoclonal antibodies to non-glycosylated domains of the secreted mucins MUC5B and MUC7. Hybrid Hybridomics 22: 293–299, 2003. doi:10.1089/153685903322538818.
21. Shoemark A, Dixon M, Beales PL, Hogg CL. Bardet Biedl syndrome: motile ciliary phenotype. Chest 147: 764–770, 2015. doi:10.1378/chest.13-2913.
22. Smith CM, Djakow J, Free RC, Djakow P, Lonnen R, Williams G, Pohunek P, Hirst RA, Easton AJ, Andrew PW, O’Callaghan C. ciliaFA: a research tool for automated, high-throughput measurement of ciliary beat frequency using freely available software. Cilia 1: 14, 2012. doi:10.1186/2046-2530-1-14.
23. Smith CM, Kulkarni H, Radhakrishnan P, Rutman A, Bankart MJ, Williams G, Hirst RA, Easton AJ, Andrew PW, O’Callaghan C. Ciliary dyskinesia is an early feature of respiratory syncytial virus infection. Eur Respir J 43: 485–496, 2014. doi:10.1183/09031936.00205312.
24. Suprynowicz FA, Upadhyay G, Krawczyk E, Kramer SC, Hebert JD, Liu X, Yuan H, Cheluvaraju C, Clapp PW, Boucher RC Jr, Kamonjoh CM, Randell SH, Schlegel R. Conditionally reprogrammed cells represent a stem-like state of adult epithelial cells. Proc Natl Acad Sci USA 109: 20035–20040, 2012. doi:10.1073/pnas.1213241109.
25. Torr E, Heath M, Mee M, Shaw D, Sharp TV, Sayers I. Expression of polycomb protein BMI-1 maintains the plasticity of basal bronchial epithelial cells. Physiol Rep 4: e12847, 2016. doi:10.14814/phy2.12847.
26. Tosoni K, Cassidy D, Kerr B, Land SC, Mehta A. Using drugs to probe the variability of trans-epithelial airway resistance. PLoS One 11: e0149550, 2016. doi:10.1371/journal.pone.0149550.
27. Wong AP, Bear CE, Chin S, Pasceri P, Thompson TO, Huan LJ, Ratjen F, Ellis J, Rossant J. Directed differentiation of human pluripotent stem cells into mature airway epithelia expressing functional CFTR protein. Nat Biotechnol 30: 876–882, 2012. doi:10.1038/nbt.2328.
28. Wong AP, Rossant J. Generation of lung epithelium from pluripotent stem cells. Curr Pathobiol Rep 1: 137–145, 2013. doi:10.1007/s40139-013-0016-9.
29. + transport processes across human lung epithelial cells. Br J Pharmacol 151: 1204–1215, 2007. doi:10.1038/sj.bjp.0707343.