Prospective isolation of NKX2-1-expressing human lung progenitors derived from pluripotent stem cells

Journal of Clinical Investigation

Volumn 127, Issue 6, 2017, Pages 2277-2294

  Hawkins, Finn ^a,b   Kramer, Philipp ^c   Jacob, Anjali ^a,b   Driver, Ian ^d   Thomas, Dylan C ^a   McCauley, Katherine B ^a,b   Skvir, Nicholas ^a   Crane, Ana M ^c   Kurmann, Anita A ^a,e   Hollenberg, Anthony N ^e   Nguyen, Sinead ^a   Wong, Brandon G ^f   Khalil, Ahmad S ^f,g   Huang, Sarah X L ^c,h   Guttentag, Susan ⁱ   Rock, Jason R ^d   Shannon, John M ^j   Davis, Brian R ^c   Kotton, Darrell N ^a,b  

^a BOSTON MEDICAL CENTER   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f Boston University   (United States)

^g HARVARD UNIVERSITY   (United States)

^h Department of Medicine   (United States)

ⁱ MONROE CARELL JR CHILDREN S HOSPITAL AT VANDERBILT   (United States)

^j CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD47 ANTIGEN; DIPEPTIDYL PEPTIDASE IV; ENHANCED GREEN FLUORESCENT PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX2-1; UNCLASSIFIED DRUG; NUCLEAR PROTEIN; THYROID NUCLEAR FACTOR 1; TRANSCRIPTOME;

ARTICLE; CELL DIFFERENTIATION; CELL ENGINEERING; CELL ISOLATION; CELL SELECTION; CELL SURFACE; COCULTURE; CONTROLLED STUDY; EMBRYO; FETUS; FETUS LUNG MATURATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LUNG DEVELOPMENT; LUNG EPITHELIUM; MESENCHYME; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN EXPRESSION; RNA SEQUENCE; SINGLE CELL ANALYSIS; TRANSCRIPTOMICS; ANIMAL; CELL CULTURE; CELL SEPARATION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; INDUCED PLURIPOTENT STEM CELL; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELL SEPARATION; CELLS, CULTURED; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 85020209962     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI89950     Document Type: Article

References (61)

1. Kimura S, et al. The T/ebp null mouse: thyroidspecific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev. 1996;10(1):60-69.
2. Lazzaro D, Price M, de Felice M, Di Lauro R. The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development. 1991;113(4):1093-1104.
3. Minoo P, Su G, Drum H, Bringas P, Kimura S. Defects in tracheoesophageal and lung morphogenesis in Nkx2.1(-/-) mouse embryos. Dev Biol. 1999;209(1):60-71.
4. Coraux C, et al. Embryonic stem cells generate airway epithelial tissue. Am J Respir Cell Mol Biol. 2005;32(2):87-92.
5. Wang D, Haviland DL, Burns AR, Zsigmond E, Wetsel RA. A pure population of lung alveolar epithelial type II cells derived from human embryonic stem cells. Proc Natl Acad Sci USA. 2007;104(11):4449-4454.
6. Van Haute L, De Block G, Liebaers I, Sermon K, De Rycke M. Generation of lung epitheliallike tissue from human embryonic stem cells. Respir Res. 2009;10:105.
7. Green MD, et al. Generation of anterior foregut endoderm from human embryonic and induced pluripotent stem cells. Nat Biotechnol. 2011;29(3):267-272.
8. Longmire TA, et al. Efficient derivation of purified lung and thyroid progenitors from embryonic stem cells. Cell Stem Cell. 2012;10(4):398-411.
9. Huang SX, et al. Efficient generation of lung and airway epithelial cells from human pluripotent stem cells. Nat Biotechnol. 2014;32(1):84-91.
10. Firth AL, et al. Generation of multiciliated cells in functional airway epithelia from human induced pluripotent stem cells. Proc Natl Acad Sci U S A. 2014;111(17):E1723-E1730.
11. Mou H, et al. Generation of multipotent lung and airway progenitors from mouse ESCs and patient-specific cystic fibrosis iPSCs. Cell Stem Cell. 2012;10(4):385-397.
12. Hawkins F, Rankin SA, Kotton DN, Zorn AM. The genetic programs regulating embryonic lung development and induced pluripotent stem cell differentiation. In: Jobe AH, Whitsett JA, Abman SH, eds. Fetal and Neonatal Lung Development: Clinical Correlates and Technologies for the Future. Cambridge: Cambridge University Press; 2016:ix-x.
13. Hawkins F, Kotton DN. Embryonic and induced pluripotent stem cells for lung regeneration. Ann Am Thorac Soc. 2015;12 Suppl 1:S50-S53.
14. Wong AP, et al. Directed differentiation of human pluripotent stem cells into mature airway epithelia expressing functional CFTR protein. Nat Biotechnol. 2012;30(9):876-882.
15. Dye BR, et al. In vitro generation of human pluripotent stem cell derived lung organoids. Elife. 2015;4:e05098.
16. Gotoh S, et al. Generation of alveolar epithelial spheroids via isolated progenitor cells from human pluripotent stem cells. Stem Cell Reports. 2014;3(3):394-403.
17. Goulburn AL, et al. A targeted NKX2.1 human embryonic stem cell reporter line enables identification of human basal forebrain derivatives. Stem Cells. 2011;29(3):462-473.
18. Crane AM, et al. Targeted correction and restored function of the CFTR gene in cystic fibrosis induced pluripotent stem cells. Stem Cell Reports. 2015;4(4):569-577.
19. Kurmann AA, et al. Regeneration of thyroid function by transplantation of differentiated pluripotent stem cells. Cell Stem Cell. 2015;17(5):527-542.
20. Kim JE, et al. Investigating synapse formation and function using human pluripotent stem cell-derived neurons. Proc Natl Acad Sci USA. 2011;108(7):3005-3010.
21. Ma L, et al. Human embryonic stem cell-derived GABA neurons correct locomotion deficits in quinolinic acid-lesioned mice. Cell Stem Cell. 2012;10(4):455-464.
22. Rishniw M, et al. Molecular aspects of esophageal development. Ann N Y Acad Sci. 2011;1232:309-315.
23. Shannon JM, Hyatt BA. Epithelial-mesenchymal interactions in the developing lung. Annu Rev Physiol. 2004;66:625-645.
24. Shannon JM. Induction of alveolar type II cell differentiation in fetal tracheal epithelium by grafted distal lung mesenchyme. Dev Biol. 1994;166(2):600-614.
25. Shannon JM, Nielsen LD, Gebb SA, Randell SH. Mesenchyme specifies epithelial differentiation in reciprocal recombinants of embryonic lung and trachea. Dev Dyn. 1998;212(4):482-494.
26. Herriges JC, et al. Genome-scale study of transcription factor expression in the branching mouse lung. Dev Dyn. 2012;241(9):1432-1453.
27. Maeda Y, Davé V, Whitsett JA. Transcriptional control of lung morphogenesis. Physiol Rev. 2007;87(1):219-244.
28. Millien G, et al. Characterization of the midforegut transcriptome identifies genes regulated during lung bud induction. Gene Expr Patterns. 2008;8(2):124-139.
29. Vukicevic S, Helder MN, Luyten FP. Developing human lung and kidney are major sites for synthe-sis of bone morphogenetic protein-3 (osteogenin). J Histochem Cytochem. 1994;42(7):869-875.
30. Takahashi H, Ikeda T. Transcripts for two members of the transforming growth factorbeta superfamily BMP-3 and BMP-7 are expressed in developing rat embryos. Dev Dyn. 1996;207(4):439-449.
31. Keegan CE, Herman JP, Karolyi IJ, O'Shea KS, Camper SA, Seasholtz AF. Differential expression of corticotropin-releasing hormone in developing mouse embryos and adult brain. Endocrinology. 1994;134(6):2547-2555.
32. Emanuel RL, Torday JS, Asokananthan N, Sunday ME. Direct effects of corticotropin-releasing hormone and thyrotropin-releasing hormone on fetal lung explants. Peptides. 2000;21(12):1819-1829.
33. Simard M, Côté M, Provost PR, Tremblay Y. Expression of genes related to the hypothalamicpituitary- adrenal axis in murine fetal lungs in late gestation. Reprod Biol Endocrinol. 2010;8:134.
34. Provost PR, Tremblay Y. Genes involved in the adrenal pathway of glucocorticoid synthesis are transiently expressed in the developing lung. Endocrinology. 2005;146(5):2239-2245.
35. Herriges MJ, et al. Long noncoding RNAs are spatially correlated with transcription factors and regulate lung development. Genes Dev. 2014;28(12):1363-1379.
36. Herriges M, Morrisey EE. Lung development: orchestrating the generation and regeneration of a complex organ. Development. 2014;141(3):502-513.
37. Williams MC. Alveolar type I cells: molecular phenotype and development. Annu Rev Physiol. 2003;65:669-695.
38. Zorn AM, Wells JM. Vertebrate endoderm development and organ formation. Annu Rev Cell Dev Biol. 2009;25:221-251.
39. Rankin SA, Kormish J, Kofron M, Jegga A, Zorn AM. A gene regulatory network controlling hhex transcription in the anterior endoderm of the organizer. Dev Biol. 2011;351(2):297-310.
40. Perkins AS, Mercer JA, Jenkins NA, Copeland NG. Patterns of Evi-1 expression in embryonic and adult tissues suggest that Evi-1 plays an important regulatory role in mouse development. Development. 1991;111(2):479-487.
41. Attar MA, Bailie MB, Christensen PJ, Brock TG, Wilcoxen SE, Paine R. Induction of ICAM-1 expression on alveolar epithelial cells during lung development in rats and humans. Exp Lung Res. 1999;25(3):245-259.
42. Li Y, Linnoila RI. Multidirectional differentiation of Achaete-Scute homologue-1-defined progenitors in lung development and injury repair. Am J Respir Cell Mol Biol. 2012;47(6):768-775.
43. Metzger DE, Xu Y, Shannon JM. Elf5 is an epithelium- specific, fibroblast growth factor-sensitive transcription factor in the embryonic lung. Dev Dyn. 2007;236(5):1175-1192.
44. Lu MM, Li S, Yang H, Morrisey EE. Foxp4: a novel member of the Foxp subfamily of wingedhelix genes co-expressed with Foxp1 and Foxp2 in pulmonary and gut tissues. Mech Dev. 2002;119 Suppl 1:S197-S202.
45. Yu Y, et al. Gene expression profiling in human fetal liver and identification of tissue- and developmental-stage-specific genes through compiled expression profiles and efficient cloning of full-length cDNAs. Genome Res. 2001;11(8):1392-1403.
46. Wilson AA, et al. Emergence of a stage-dependent human liver disease signature with directed differentiation of alpha-1 antitrypsin-deficient iPS cells. Stem Cell Reports. 2015;4(5):873-885.
47. Trapnell C, et al. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat Biotechnol. 2014;32(4):381-386.
48. Shalek AK, et al. Single-cell transcriptomics reveals bimodality in expression and splicing in immune cells. Nature. 2013;498(7453):236-240.
49. Guo G, et al. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell. 2010;18(4):675-685.
50. Tang F, et al. Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis. Cell Stem Cell. 2010;6(5):468-478.
51. Buganim Y, et al. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell. 2012;150(6):1209-1222.
52. Lü J, Izvolsky KI, Qian J, Cardoso WV. Identification of FGF10 targets in the embryonic lung epithelium during bud morphogenesis. J Biol Chem. 2005;280(6):4834-4841.
53. Kho AT, et al. Transcriptomic analysis of human lung development. Am J Respir Crit Care Med. 2010;181(1):54-63.
54. Kido T, et al. CPM is a useful cell surface marker to isolate expandable bi-potential liver progenitor cells derived from human iPS cells. Stem Cell Reports. 2015;5(4):508-515.
55. Somers A, et al. Generation of transgenefree lung disease-specific human induced pluripotent stem cells using a single excisable lentiviral stem cell cassette. Stem Cells. 2010;28(10):1728-1740.
56. Sherwood RI, Chen TY, Melton DA. Transcriptional dynamics of endodermal organ formation. Dev Dyn. 2009;238(1):29-42.
57. Barclay AN, Van den Berg TK. The interaction between signal regulatory protein alpha (SIRPα) and CD47: structure, function, and therapeutic target. Annu Rev Immunol. 2014;32:25-50.
58. Herold S, et al. Alveolar epithelial cells direct monocyte transepithelial migration upon influenza virus infection: impact of chemokines and adhesion molecules. J Immunol. 2006;177(3):1817-1824.
59. Wade KC, et al. Gene induction during differentiation of human pulmonary type II cells in vitro. Am J Respir Cell Mol Biol. 2006;34(6):727-737.
60. Gonzales LW, Guttentag SH, Wade KC, Postle AD, Ballard PL. Differentiation of human pulmonary type II cells in vitro by glucocorticoid plus cAMP. Am J Physiol Lung Cell Mol Physiol. 2002;283(5):L940-L951.
61. Weaver M, Batts L, Hogan BL. Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev Biol. 2003;258(1):169-184.