Efficient Derivation of Functional Human Airway Epithelium from Pluripotent Stem Cells via Temporal Regulation of Wnt Signaling

Cell Stem Cell

Volumn 20, Issue 6, 2017, Pages 844-857.e6

  McCauley, Katherine B ^a,b   Hawkins, Finn ^a,b   Serra, Maria ^a,b   Thomas, Dylan C ^a   Jacob, Anjali ^a,b   Kotton, Darrell N ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

airway epithelium; cystic fibrosis; directed differentiation; disease modeling; human pluripotent stem cells; lung development; lung epithelium; Wnt signaling

Indexed keywords

FORSKOLIN; HOMEOBOX PROTEIN NKX 2.1; NKX2-1 PROTEIN, HUMAN;

AIRWAY EPITHELIUM CELL; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE EDITING; HUMAN; HUMAN CELL; IN VIVO STUDY; INDUCED PLURIPOTENT STEM CELL; MOUSE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; RESPIRATORY FUNCTION; WNT SIGNALING; CYTOLOGY; METABOLISM; ORGANOID; RESPIRATORY MUCOSA;

HUMANS; INDUCED PLURIPOTENT STEM CELLS; ORGANOIDS; RESPIRATORY MUCOSA; THYROID NUCLEAR FACTOR 1; WNT SIGNALING PATHWAY;

EID: 85016519790     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2017.03.001     Document Type: Article

References (52)

1. Bellusci, S., Grindley, J., Emoto, H., Itoh, N., Hogan, B., Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 124 (1997), 4867–4878.
2. Bilodeau, M., Shojaie, S., Ackerley, C., Post, M., Rossant, J., Identification of a proximal progenitor population from murine fetal lungs with clonogenic and multilineage differentiation potential. Stem Cell Reports 3 (2014), 634–649.
3. Cardoso, W.V., Itoh, A., Nogawa, H., Mason, I., Brody, J.S., FGF-1 and FGF-7 induce distinct patterns of growth and differentiation in embryonic lung epithelium. Dev. Dyn. 208 (1997), 398–405.
4. Chen, F., Desai, T.J., Qian, J., Niederreither, K., Lü, J., Cardoso, W.V., Inhibition of Tgf beta signaling by endogenous retinoic acid is essential for primary lung bud induction. Development 134 (2007), 2969–2979.
5. Chen, F., Cao, Y., Qian, J., Shao, F., Niederreither, K., Cardoso, W.V., A retinoic acid-dependent network in the foregut controls formation of the mouse lung primordium. J. Clin. Invest. 120 (2010), 2040–2048.
6. Crane, A.M., Kramer, P., Bui, J.H., Chung, W.J., Li, X.S., Gonzalez-Garay, M.L., Hawkins, F., Liao, W., Mora, D., Choi, S., et al. Targeted correction and restored function of the CFTR gene in cystic fibrosis induced pluripotent stem cells. Stem Cell Reports 4 (2015), 569–577.
7. De Langhe, S.P., Sala, F.G., Del Moral, P.-M., Fairbanks, T.J., Yamada, K.M., Warburton, D., Burns, R.C., Bellusci, S., Dickkopf-1 (DKK1) reveals that fibronectin is a major target of Wnt signaling in branching morphogenesis of the mouse embryonic lung. Dev. Biol. 277 (2005), 316–331.
8. Dekkers, J.F., Wiegerinck, C.L., de Jonge, H.R., Bronsveld, I., Janssens, H.M., de Winter-de Groot, K.M., Brandsma, A.M., de Jong, N.W.M., Bijvelds, M.J.C., Scholte, B.J., et al. A functional CFTR assay using primary cystic fibrosis intestinal organoids. Nat. Med. 19 (2013), 939–945.
9. Dye, B.R., Hill, D.R., Ferguson, M.A., Tsai, Y.H., Nagy, M.S., Dyal, R., Wells, J.M., Mayhew, C.N., Nattiv, R., Klein, O.D., et al. In vitro generation of human pluripotent stem cell derived lung organoids. eLife, 4, 2015, e05098.
10. Firth, A.L., Dargitz, C.T., Qualls, S.J., Menon, T., Wright, R., Singer, O., Gage, F.H., Khanna, A., Verma, I.M., Generation of multiciliated cells in functional airway epithelia from human induced pluripotent stem cells. Proc. Natl. Acad. Sci. USA 111 (2014), E1723–E1730.
11. Fuerer, C., Nusse, R., Lentiviral vectors to probe and manipulate the Wnt signaling pathway. PLoS ONE, 5, 2010, e9370.
12. Goss, A.M., Tian, Y., Tsukiyama, T., Cohen, E.D., Zhou, D., Lu, M.M., Yamaguchi, T.P., Morrisey, E.E., Wnt2/2b and beta-catenin signaling are necessary and sufficient to specify lung progenitors in the foregut. Dev. Cell 17 (2009), 290–298.
13. Gotoh, S., Ito, I., Nagasaki, T., Yamamoto, Y., Konishi, S., Korogi, Y., Matsumoto, H., Muro, S., Hirai, T., Funato, M., et al. Generation of alveolar epithelial spheroids via isolated progenitor cells from human pluripotent stem cells. Stem Cell Reports 3 (2014), 394–403.
14. Green, M.D., Chen, A., Nostro, M.-C., d'Souza, S.L., Schaniel, C., Lemischka, I.R., Gouon-Evans, V., Keller, G., Snoeck, H.-W., Generation of anterior foregut endoderm from human embryonic and induced pluripotent stem cells. Nat. Biotechnol. 29 (2011), 267–272.
15. Harris-Johnson, K.S., Domyan, E.T., Vezina, C.M., Sun, X., beta-Catenin promotes respiratory progenitor identity in mouse foregut. Proc. Natl. Acad. Sci. USA 106 (2009), 16287–16292.
16. Hashimoto, S., Chen, H., Que, J., Brockway, B.L., Drake, J.A., Snyder, J.C., Randell, S.H., Stripp, B.R., β-Catenin-SOX2 signaling regulates the fate of developing airway epithelium. J. Cell Sci. 125 (2012), 932–942.
17. Hawkins, F., Kramer, P., Jacob, A., Driver, I., Thomas, D.C., McCauley, K.B., Skvir, N., Crane, A.M., Kurmann, A.A., Hollenberg, A.N., et al. Prospective isolation of NKX2-1-expressing human lung progenitors derived from pluripotent stem cells. J. Clin. Invest., 2017, 10.1172/JCI89950 Published online May 2, 2017.
18. Huang, S.X.L., Islam, M.N., O'Neill, J., Hu, Z., Yang, Y.-G., Chen, Y.-W., Mumau, M., Green, M.D., Vunjak-Novakovic, G., Bhattacharya, J., Snoeck, H.-W., Efficient generation of lung and airway epithelial cells from human pluripotent stem cells. Nat. Biotechnol. 32 (2014), 84–91.
19. Huang, S.X.L., Green, M.D., de Carvalho, A.T., Mumau, M., Chen, Y.-W., D'Souza, S.L., Snoeck, H.-W., The in vitro generation of lung and airway progenitor cells from human pluripotent stem cells. Nat. Protoc. 10 (2015), 413–425.
20. Hyatt, B.A., Shangguan, X., Shannon, J.M., FGF-10 induces SP-C and Bmp4 and regulates proximal-distal patterning in embryonic tracheal epithelium. Am. J. Physiol. Lung Cell. Mol. Physiol. 287 (2004), L1116–L1126.
21. Ikeda, K., Clark, J.C., Shaw-White, J.R., Stahlman, M.T., Boutell, C.J., Whitsett, J.A., Gene structure and expression of human thyroid transcription factor-1 in respiratory epithelial cells. J. Biol. Chem. 270 (1995), 8108–8114.
22. Kim, B.R., Van de Laar, E., Cabanero, M., Tarumi, S., Hasenoeder, S., Wang, D., Virtanen, C., Suzuki, T., Bandarchi, B., Sakashita, S., et al. SOX2 and PI3K cooperate to induce and stabilize a squamous-committed stem cell injury state during lung squamous cell carcinoma pathogenesis. PLoS Biol., 14, 2016, e1002581.
23. Konishi, S., Gotoh, S., Tateishi, K., Yamamoto, Y., Korogi, Y., Nagasaki, T., Matsumoto, H., Muro, S., Hirai, T., Ito, I., et al. Directed induction of functional multi-ciliated cells in proximal airway epithelial spheroids from human pluripotent stem cells. Stem Cell Reports 6 (2016), 18–25.
24. Kurmann, A.A., Serra, M., Hawkins, F., Rankin, S.A., Mori, M., Astapova, I., Ullas, S., Lin, S., Bilodeau, M., Rossant, J., et al. Regeneration of thyroid function by transplantation of differentiated pluripotent stem cells. Cell Stem Cell 17 (2015), 527–542.
25. Li, C., Li, A., Li, M., Xing, Y., Chen, H., Hu, L., Tiozzo, C., Anderson, S., Taketo, M.M., Minoo, P., Stabilized beta-catenin in lung epithelial cells changes cell fate and leads to tracheal and bronchial polyposis. Dev. Biol. 334 (2009), 97–108.
26. Liu, Y., Hogan, B.L.M., Differential gene expression in the distal tip endoderm of the embryonic mouse lung. Gene Expr. Patterns 2 (2002), 229–233.
27. Liu, Y., Jiang, H., Crawford, H.C., Hogan, B.L.M., Role for ETS domain transcription factors Pea3/Erm in mouse lung development. Dev. Biol. 261 (2003), 10–24.
28. Longmire, T.A., Ikonomou, L., Hawkins, F., Christodoulou, C., Cao, Y., Jean, J.C., Kwok, L.W., Mou, H., Rajagopal, J., Shen, S.S., et al. Efficient derivation of purified lung and thyroid progenitors from embryonic stem cells. Cell Stem Cell 10 (2012), 398–411.
29. Mootha, V.K., Lindgren, C.M., Eriksson, K.-F., Subramanian, A., Sihag, S., Lehar, J., Puigserver, P., Carlsson, E., Ridderstråle, M., Laurila, E., et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34 (2003), 267–273.
30. Mou, H., Zhao, R., Sherwood, R., Ahfeldt, T., Lapey, A., Wain, J., Sicilian, L., Izvolsky, K., Musunuru, K., Cowan, C., Rajagopal, J., Generation of multipotent lung and airway progenitors from mouse ESCs and patient-specific cystic fibrosis iPSCs. Cell Stem Cell 10 (2012), 385–397.
31. Mou, H., Vinarsky, V., Tata, P.R., Brazauskas, K., Choi, S.H., Crooke, A.K., Zhang, B., Solomon, G.M., Turner, B., Bihler, H., et al. Dual SMAD signaling inhibition enables long-term expansion of diverse epithelial basal cells. Cell Stem Cell 19 (2016), 217–231.
32. Mucenski, M.L., Wert, S.E., Nation, J.M., Loudy, D.E., Huelsken, J., Birchmeier, W., Morrisey, E.E., Whitsett, J.A., beta-Catenin is required for specification of proximal/distal cell fate during lung morphogenesis. J. Biol. Chem. 278 (2003), 40231–40238.
33. Okubo, T., Hogan, B.L.M., Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J. Biol., 3, 2004, 11.
34. Phelps, D.S., Floros, J., Localization of surfactant protein synthesis in human lung by in situ hybridization. Am. Rev. Respir. Dis. 137 (1988), 939–942.
35. Ramasamy, S.K., Mailleux, A.A., Gupte, V.V., Mata, F., Sala, F.G., Veltmaat, J.M., Del Moral, P.M., De Langhe, S., Parsa, S., Kelly, L.K., et al. Fgf10 dosage is critical for the amplification of epithelial cell progenitors and for the formation of multiple mesenchymal lineages during lung development. Dev. Biol. 307 (2007), 237–247.
36. Rawlins, E.L., Clark, C.P., Xue, Y., Hogan, B.L.M., The Id2+ distal tip lung epithelium contains individual multipotent embryonic progenitor cells. Development 136 (2009), 3741–3745.
37. Reynolds, S.D., Zemke, A.C., Giangreco, A., Brockway, B.L., Teisanu, R.M., Drake, J.A., Mariani, T., Di, P.Y., Taketo, M.M., Stripp, B.R., Conditional stabilization of β-catenin expands the pool of lung stem cells. Stem Cells 26 (2008), 1337–1346.
38. Rock, J.R., Onaitis, M.W., Rawlins, E.L., Lu, Y., Clark, C.P., Xue, Y., Randell, S.H., Hogan, B.L.M., Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc. Natl. Acad. Sci. USA 106 (2009), 12771–12775.
39. Sekine, K., Ohuchi, H., Fujiwara, M., Yamasaki, M., Yoshizawa, T., Sato, T., Yagishita, N., Matsui, D., Koga, Y., Itoh, N., Kato, S., Fgf10 is essential for limb and lung formation. Nat. Genet. 21 (1999), 138–141.
40. Shu, W., Guttentag, S., Wang, Z., Andl, T., Ballard, P., Lu, M.M., Piccolo, S., Birchmeier, W., Whitsett, J.A., Millar, S.E., Morrisey, E.E., Wnt/beta-catenin signaling acts upstream of N-myc, BMP4, and FGF signaling to regulate proximal-distal patterning in the lung. Dev. Biol. 283 (2005), 226–239.
41. Somers, A., Jean, J.-C., Sommer, C.A., Omari, A., Ford, C.C., Mills, J.A., Ying, L., Sommer, A.G., Jean, J.M., Smith, B.W., et al. Generation of transgene-free lung disease-specific human induced pluripotent stem cells using a single excisable lentiviral stem cell cassette. Stem Cells 28 (2010), 1728–1740.
42. ten Berge, D., Koole, W., Fuerer, C., Fish, M., Eroglu, E., Nusse, R., Wnt signaling mediates self-organization and axis formation in embryoid bodies. Cell Stem Cell 3 (2008), 508–518.
43. Tsao, P.N., Vasconcelos, M., Izvolsky, K.I., Qian, J., Lu, J., Cardoso, W.V., Notch signaling controls the balance of ciliated and secretory cell fates in developing airways. Development 136 (2009), 2297–2307.
44. Volckaert, T., Campbell, A., Dill, E., Li, C., Minoo, P., De Langhe, S., Localized Fgf10 expression is not required for lung branching morphogenesis but prevents differentiation of epithelial progenitors. Development 140 (2013), 3731–3742.
45. Wang, R., Ahmed, J., Wang, G., Hassan, I., Strulovici-Barel, Y., Hackett, N.R., Crystal, R.G., Down-regulation of the canonical Wnt β-catenin pathway in the airway epithelium of healthy smokers and smokers with COPD. PLoS ONE, 6, 2011, e14793.
46. Weaver, M., Yingling, J.M., Dunn, N.R., Bellusci, S., Hogan, B.L., Bmp signaling regulates proximal-distal differentiation of endoderm in mouse lung development. Development 126 (1999), 4005–4015.
47. Weaver, M., Dunn, N.R., Hogan, B.L., Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 127 (2000), 2695–2704.
48. Wilson, A.A., Murphy, G.J., Hamakawa, H., Kwok, L.W., Srinivasan, S., Hovav, A.-H., Mulligan, R.C., Amar, S., Suki, B., Kotton, D.N., Amelioration of emphysema in mice through lentiviral transduction of long-lived pulmonary alveolar macrophages. J. Clin. Invest. 120 (2010), 379–389.
49. Wong, A.P., Bear, C.E., Chin, S., Pasceri, P., Thompson, T.O., Huan, L.-J., Ratjen, F., Ellis, J., Rossant, J., Directed differentiation of human pluripotent stem cells into mature airway epithelia expressing functional CFTR protein. Nat. Biotechnol. 30 (2012), 876–882.
50. Xu, Y., Mizuno, T., Sridharan, A., Du, Y., Guo, M., Tang, J., Wikenheiser-Brokamp, K.A., Perl, A.T., Funari, V.A., Gokey, J.J., et al. Single-cell RNA sequencing identifies diverse roles of epithelial cells in idiopathic pulmonary fibrosis. JCI Insight, 1, 2016, e90558.
51. You, Y., Richer, E.J., Huang, T., Brody, S.L., Growth and differentiation of mouse tracheal epithelial cells: selection of a proliferative population. Am. J. Physiol. Lung Cell. Mol. Physiol. 283 (2002), L1315–L1321.
52. Zemke, A.C., Teisanu, R.M., Giangreco, A., Drake, J.A., Brockway, B.L., Reynolds, S.D., Stripp, B.R., beta-Catenin is not necessary for maintenance or repair of the bronchiolar epithelium. Am. J. Respir. Cell Mol. Biol. 41 (2009), 535–5430.