Rapid expansion of human epithelial stem cells suitable for airway tissue engineering

American Journal of Respiratory and Critical Care Medicine

Volumn 194, Issue 2, 2016, Pages 156-168

  Butler, Colin R ^a   Hynds, Robert E ^a   Gowers, Kate H C ^a   Lee, Dani Do Hyang ^b   Brown, James M ^a   Crowley, Claire ^b   Teixeira, Vitor H ^a   Smith, Claire M ^b   Urbani, Luca ^b   Hamilton, Nicholas J ^a   Thakrar, Ricky M ^a   Booth, Helen L ^c   Birchall, Martin A ^d   De Coppi, Paolo ^b   Giangreco, Adam ^a   O'Callaghan, Christopher ^b   Janes, Sam M ^a,c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON HOSPITALS   (United Kingdom)

^d ROYAL NATIONAL THROAT NOSE AND EAR HOSPITAL   (United Kingdom)

Author keywords

Adult stem cells; Epithelium; Respiratory mucosa; Tissue engineering; Trachea

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; RHO KINASE; TELOMERASE;

AIRWAY EPITHELIAL CELL; ANGIOGENESIS; ARTICLE; BRONCHOSCOPY; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CILIARY MOTILITY; ENZYME INHIBITION; EPITHELIUM BASAL CELL; FEEDER CELL; FLOW CYTOMETRY; GENE EXPRESSION; GOBLET CELL; HETEROTOPIC TRANSPLANTATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VITRO STUDY; KARYOTYPE; KARYOTYPING; MUCOCILIARY CLEARANCE; MULTIPLEX LIGATION DEPENDENT PROBE AMPLIFICATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL; TELOMERE LENGTH; TISSUE ENGINEERING; CELL CULTURE; EPITHELIUM CELL; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; PHYSIOLOGY; PROCEDURES; RESPIRATORY MUCOSA; RESPIRATORY TRACT DISEASES;

CELL DIFFERENTIATION; CELLS, CULTURED; EPITHELIAL CELLS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MUCOCILIARY CLEARANCE; POLYMERASE CHAIN REACTION; RESPIRATORY MUCOSA; RESPIRATORY TRACT DISEASES; STEM CELLS; TISSUE ENGINEERING;

EID: 84988938994     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201507-1414OC     Document Type: Article

References (63)

1. Kotloff RM, Thabut G. Lung transplantation. Am J Respir Crit Care Med 2011;184:159-171.
2. Ren X, Ott HC. On the road to bioartificial organs. Pflugers Arch 2014; 466:1847-1857.
3. Macchiarini P, Jungebluth P, Go T, Asnaghi MA, Rees LE, Cogan TA, Dodson A, Martorell J, Bellini S, Parnigotto PP, et al. Clinical transplantation of a tissue-engineered airway. Lancet 2008;372: 2023-2030.
4. Elliott MJ, De Coppi P, Speggiorin S, Roebuck D, Butler CR, Samuel E, Crowley C, McLaren C, Fierens A, Vondrys D, et al. Stem-cell-based, tissue engineered tracheal replacement in a child: a 2-year follow-up study. Lancet 2012;380:994-1000.
5. Delaere P, Vranckx J, Verleden G, De Leyn P, Van Raemdonck D; Leuven Tracheal Transplant Group. Tracheal allotransplantation after withdrawal of immunosuppressive therapy. N Engl J Med 2010;362:138-145.
6. Crowley C, Birchall M, Seifalian AM. Trachea transplantation: from laboratory to patient. J Tissue Eng Regen Med 2015;9:357-367.
7. Brouwer KM, Hoogenkamp HR, Daamen WF, van Kuppevelt TH. Regenerative medicine for the respiratory system: distant future or tomorrow's treatment? Am J Respir Crit Care Med 2013;187: 468-475.
8. Jungebluth P, Alici E, Baiguera S, Le Blanc K, Blomberg P, Bozóky B, Crowley C, Einarsson O, Grinnemo KH, Gudbjartsson T, et al. Tracheobronchial transplantation with a stem-cell-seeded bioartificial nanocomposite: a proof-of-concept study. Lancet 2011;378:1997-2004.
9. Delaere PR, Vranckx JJ, Den Hondt M; Leuven Tracheal Transplant Group. Tracheal allograft after withdrawal of immunosuppressive therapy. N Engl J Med 2014;370:1568-1570.
10. Hamilton N, Bullock AJ, Macneil S, Janes SM, Birchall M. Tissue engineering airway mucosa: a systematic review. Laryngoscope 2014;124:961-968.
11. Fishman JM, Wiles K, Lowdell MW, De Coppi P, Elliott MJ, Atala A, Birchall MA. Airway tissue engineering: an update. Expert Opin Biol Ther 2014;14:1477-1491.
12. Kotton DN. Next-generation regeneration: the hope and hype of lung stem cell research. Am J Respir Crit Care Med 2012;185: 1255-1260.
13. Hogan BL, Barkauskas CE, Chapman HA, Epstein JA, Jain R, Hsia CC, Niklason L, Calle E, Le A, Randell SH, et al. Repair and regeneration of the respiratory system: complexity, plasticity, and mechanisms of lung stem cell function. Cell Stem Cell 2014;15:123-138.
14. Santacruz JF, Mehta AC. Airway complications and management after lung transplantation: ischemia, dehiscence, and stenosis. Proc Am Thorac Soc 2009;6:79-93.
15. Berg M, Ejnell H, Kovács A, Nayakawde N, Patil PB, Joshi M, Aziz L, Ra° dberg G, Hajizadeh S, Olausson M, et al. Replacement of a tracheal stenosis with a tissue-engineered human trachea using autologous stem cells: a case report. Tissue Eng Part A 2014;20:389-397.
16. Hamilton NJ, Kanani M, Roebuck DJ, Hewitt RJ, Cetto R, Culme-Seymour EJ, Toll E, Bates AJ, Comerford AP, McLaren CA, et al. Tissue-engineered tracheal replacement in a child: a 4-year follow-up study. Am J Transplant 2015;15:2750-2757.
17. Fulcher ML, Gabriel S, Burns KA, Yankaskas JR, Randell SH. Well-differentiated human airway epithelial cell cultures. Methods Mol Med 2005;107:183-206.
18. Araya J, Cambier S, Markovics JA, Wolters P, Jablons D, Hill A, Finkbeiner W, Jones K, Broaddus VC, Sheppard D, et al. Squamous metaplasia amplifies pathologic epithelial-mesenchymal interactions in COPD patients. J Clin Invest 2007;117:3551-3562.
19. Gray TE, Guzman K, Davis CW, Abdullah LH, Nettesheim P. Mucociliary differentiation of serially passaged normal human tracheobronchial epithelial cells. Am J Respir Cell Mol Biol 1996;14:104-112.
20. Ghosh M, Ahmad S, Jian A, Li B, Smith RW, Helm KM, Seibold MA, Groshong SD, White CW, Reynolds SD. Human tracheobronchial basal cells: normal versus remodeling/repairing phenotypes in vivo and in vitro. Am J Respir Cell Mol Biol 2013;49:1127-1134.
21. Rheinwald JG, Green H. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 1975;6:331-343.
22. Chapman S, Liu X, Meyers C, Schlegel R, McBride AA. Human keratinocytes are efficiently immortalized by a Rho kinase inhibitor. J Clin Invest 2010;120:2619-2626.
23. Liu X, Ory V, Chapman S, Yuan H, Albanese C, Kallakury B, Timofeeva OA, Nealon C, Dakic A, Simic V, et al. ROCK inhibitor and feeder cells induce the conditional reprogramming of epithelial cells. Am J Pathol 2012;180:599-607.
24. Suprynowicz FA, Upadhyay G, Krawczyk E, Kramer SC, Hebert JD, Liu X, Yuan H, Cheluvaraju C, Clapp PW, Boucher RC Jr, et al. Conditionally reprogrammed cells represent a stem-like state of adult epithelial cells. Proc Natl Acad Sci USA 2012;109:20035-20040.
25. Wang X, Yamamoto Y, Wilson LH, Zhang T, Howitt BE, Farrow MA, Kern F, Ning G, Hong Y, Khor CC, et al. Cloning and variation of ground state intestinal stem cells. Nature 2015;522:173-178.
26. Hynds RE, Butler CR, Gowers KH, Brown JM, Lee DD, Smith CM, Crowley C, Teixeira VH, Thakrar R, Hamilton N, et al. Rapid expansion of human airway epithelial cells for tissue engineering [abstract]. Presented at Stem Cells, Cell Therapies, and Bioengineering in Lung Biology and Lung Diseases, July 2015, Vermont.
27. Butler CR, Hynds RE, Gowers KH, Brown JM, Lee DD, Teixeira VH, Hamilton NJ, Birchall MA, O'Callaghan C, Janes SM. Co-culture-expanded human basal epithelial stem cells for application in tracheal tissue engineering. Lancet 2016;387:S23.
28. Crowley C, Klanrit P, Butler CR, Varanou A, Platé M, Hynds RE, Chambers RC, Seifalian AM, Birchall MA, Janes SM. Surface modification of a POSS-nanocomposite material to enhance cellular integration of a synthetic bioscaffold. Biomaterials 2016;83:283-293.
29. Mercer RR, Russell ML, Roggli VL, Crapo JD. Cell number and distribution in human and rat airways. Am J Respir Cell Mol Biol 1994;10:613-624.
30. Griscom NT, Wohl ME. Dimensions of the growing trachea related to age and gender. AJR Am J Roentgenol 1986;146:233-237.
31. Schouten JP, McElgunn CJ, Waaijer R, Zwijnenburg D, Diepvens F, Pals G. Relative quantification of 40 nucleic acid sequences by multiplex ligation-dependent probe amplification. Nucleic Acids Res 2002;30:e57.
32. Darnfors C, Flodin A, Andersson K, Caisander G, Lindqvist J, Hyllner J, Wahlströ m J, Sartipy P. High-resolution analysis of the subtelomeric regions of human embryonic stem cells. Stem Cells 2005;23:483-488.
33. Cawthon RM. Telomere measurement by quantitative PCR. Nucleic Acids Res 2002;30:e47.
34. Barrandon Y, Grasset N, Zaffalon A, Gorostidi F, Claudinot S, Droz-Georget SL, Nanba D, Rochat A. Capturing epidermal stemness for regenerative medicine. Semin Cell Dev Biol 2012;23:937-944.
35. Rock JR, Onaitis MW, Rawlins EL, Lu Y, Clark CP, Xue Y, Randell SH, Hogan BL. Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc Natl Acad Sci USA 2009;106: 12771-12775.
36. Teixeira VH, Nadarajan P, Graham TA, Pipinikas CP, Brown JM, Falzon M, Nye E, Poulsom R, Lawrence D, Wright NA, et al. Stochastic homeostasis in human airway epithelium is achieved by neutral competition of basal cell progenitors. eLife 2013;2:e00966.
37. Hackett NR, Shaykhiev R, Walters MS, Wang R, Zwick RK, Ferris B, Witover B, Salit J, Crystal RG. The human airway epithelial basal cell transcriptome. PLoS One 2011;6:e18378.
38. Hegab AE, Ha VL, Gilbert JL, Zhang KX, Malkoski SP, Chon AT, Darmawan DO, Bisht B, Ooi AT, Pellegrini M, et al. Novel stem/progenitor cell population from murine tracheal submucosal gland ducts with multipotent regenerative potential. Stem Cells 2011;29:1283-1293.
39. Arason AJ, Jonsdottir HR, Halldorsson S, Benediktsdottir BE, Bergthorsson JT, Ingthorsson S, Baldursson O, Sinha S, Gudjonsson T, Magnusson MK. deltaNp63 has a role in maintaining epithelial integrity in airway epithelium. PLoS One 2014;9:e88683.
40. Warner SM, Hackett TL, Shaheen F, Hallstrand TS, Kicic A, Stick SM, Knight DA. Transcription factor p63 regulates key genes and wound repair in human airway epithelial basal cells. Am J Respir Cell Mol Biol 2013;49:978-988.
41. Hynds RE, Giangreco A. Concise review: the relevance of human stem cell-derived organoid models for epithelial translational medicine. Stem Cells 2013;31:417-422.
42. Danahay H, Pessotti AD, Coote J, Montgomery BE, Xia D, Wilson A, Yang H, Wang Z, Bevan L, Thomas C, et al. Notch2 is required for inflammatory cytokine-driven goblet cell metaplasia in the lung. Cell Reports 2015;10:239-252.
43. Schamberger AC, Staab-Weijnitz CA, Mise-Racek N, Eickelberg O. Cigarette smoke alters primary human bronchial epithelial cell differentiation at the air-liquid interface. Sci Rep 2015;5:8163.
44. 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 2014;43:485-496.
45. Chilvers MA, Rutman A, O'Callaghan C. Functional analysis of cilia and ciliated epithelial ultrastructure in healthy children and young adults. Thorax 2003;58:333-338.
46. Keiser NW, Engelhardt JF. Gene delivery to the airway. Curr Protoc Hum Genet 2013;Chapter 13:Unit 13.9.
47. Engelhardt JF, Yankaskas JR, Wilson JM. In vivo retroviral gene transfer into human bronchial epithelia of xenografts. J Clin Invest 1992;90:2598-2607.
48. Avril-Delplanque A, Casal I, Castillon N, Hinnrasky J, Puchelle E, Pé ault B. Aquaporin-3 expression in human fetal airway epithelial progenitor cells. Stem Cells 2005;23:992-1001.
49. Hawkins F, Kotton DN. Embryonic and induced pluripotent stem cells for lung regeneration. Ann Am Thorac Soc 2015;12:S50-S53.
50. Bayart E, Cohen-Haguenauer O. Technological overview of iPS induction from human adult somatic cells. Curr Gene Ther 2013;13:73-92.
51. Serra M, Brito C, Correia C, Alves PM. Process engineering of human pluripotent stem cells for clinical application. Trends Biotechnol 2012;30:350-359.
52. Horani A, Nath A, Wasserman MG, Huang T, Brody SL. Rho-associated protein kinase inhibition enhances airway epithelial basal-cell proliferation and lentivirus transduction. Am J Respir Cell Mol Biol 2013;49:341-347.
53. Palechor-Ceron N, Suprynowicz FA, Upadhyay G, Dakic A, Minas T, Simic V, Johnson M, Albanese C, Schlegel R, Liu X. Radiation induces diffusible feeder cell factor(s) that cooperate with ROCK inhibitor to conditionally reprogram and immortalize epithelial cells. Am J Pathol 2013;183:1862-1870.
54. Ligaba SB, Khurana A, Graham G, Krawczyk E, Jablonski S, Petricoin EF, Glazer RI, Upadhyay G. Multifactorial analysis of conditional reprogramming of human keratinocytes. PLoS One 2015;10:e0116755.
55. Paul MK, Bisht B, Darmawan DO, Chiou R, Ha VL, Wallace WD, Chon AT, Hegab AE, Grogan T, Elashoff DA, et al. Dynamic changes in intracellular ROS levels regulate airway basal stem cell homeostasis through Nrf2-dependent Notch signaling. Cell Stem Cell 2014;15:199-214.
56. Hiyama E, Hiyama K. Telomere and telomerase in stem cells. Br J Cancer 2007;96:1020-1024.
57. Ramunas J, Yakubov E, Brady JJ, Corbel SY, Holbrook C, Brandt M, Stein J, Santiago JG, Cooke JP, Blau HM. Transient delivery of modified mRNA encoding TERT rapidly extends telomeres in human cells. FASEB J 2015;29:1930-1939.
58. Goldstein AS, Lawson DA, Cheng D, Sun W, Garraway IP, Witte ON. Trop2 identifies a subpopulation of murine and human prostate basal cells with stem cell characteristics. Proc Natl Acad Sci USA 2008; 105:20882-20887.
59. O'Connor NE, Mulliken JB, Banksschlegel S, Kehinde O, Green H. Grafting of burns with cultured epithelium prepared from autologous epidermal cells. Lancet 1981;1:75-78.
60. Gallico GG III, O'Connor NE, Compton CC, Kehinde O, Green H. Permanent coverage of large burn wounds with autologous cultured human epithelium. N Engl J Med 1984;311:448-451.
61. Pellegrini G, Traverso CE, Franzi AT, Zingirian M, Cancedda R, De Luca M. Long-term restoration of damaged corneal surfaces with autologous cultivated corneal epithelium. Lancet 1997;349:990-993.
62. Rama P, Matuska S, Paganoni G, Spinelli A, De Luca M, Pellegrini G. Limbal stem-cell therapy and long-term corneal regeneration. N Engl J Med 2010;363:147-155.
63. Sharma SM, Fuchsluger T, Ahmad S, Katikireddy KR, Armant M, Dana R, Jurkunas UV. Comparative analysis of human-derived feeder layers with 3T3 fibroblasts for the ex vivo expansion of human limbal and oral epithelium. Stem Cell Rev 2012;8:696-705.