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Finn Hawkins, … , Brian R. Davis, Darrell N. Kotton
Published May 2, 2017
Citation Information: J Clin Invest. 2017;127(6):2277-2294. https://doi.org/10.1172/JCI89950.
Citation Information: J Clin Invest. 2017;127(6):2277-2294. https://doi.org/10.1172/JCI89950.
Abstract
It has been postulated that during human fetal development, all cells of the lung epithelium derive from embryonic, endodermal, NK2 homeobox 1–expressing (NKX2-1+) precursor cells. However, this hypothesis has not been formally tested owing to an inability to purify or track these progenitors for detailed characterization. Here we have engineered and developmentally differentiated NKX2-1GFP reporter pluripotent stem cells (PSCs) in vitro to generate and isolate human primordial lung progenitors that express NKX2-1 but are initially devoid of differentiated lung lineage markers. After sorting to purity, these primordial lung progenitors exhibited lung epithelial maturation. In the absence of mesenchymal coculture support, this NKX2-1+ population was able to generate epithelial-only spheroids in defined 3D cultures. Alternatively, when recombined with fetal mouse lung mesenchyme, the cells recapitulated epithelial-mesenchymal developing lung interactions. We imaged these progenitors in real time and performed time-series global transcriptomic profiling and single-cell RNA sequencing as they moved through the earliest moments of lung lineage specification. The profiles indicated that evolutionarily conserved, stage-dependent gene signatures of early lung development are expressed in primordial human lung progenitors and revealed a CD47hiCD26lo cell surface phenotype that allows their prospective isolation from untargeted, patient-specific PSCs for further in vitro differentiation and future applications in regenerative medicine.
Authors
Finn Hawkins, Philipp Kramer, Anjali Jacob, Ian Driver, Dylan C. Thomas, Katherine B. McCauley, Nicholas Skvir, Ana M. Crane, Anita A. Kurmann, Anthony N. Hollenberg, Sinead Nguyen, Brandon G. Wong, Ahmad S. Khalil, Sarah X.L. Huang, Susan Guttentag, Jason R. Rock, John M. Shannon, Brian R. Davis, Darrell N. Kotton
Total citations by year
Citation information
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The in vivo genetic program of murine primordial lung epithelial progenitors
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Nature Communications | 2020 |
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Reconstructed Single-Cell Fate Trajectories Define Lineage Plasticity Windows during Differentiation of Human PSC-Derived Distal Lung Progenitors
K Hurley, J Ding, C Villacorta-Martin, MJ Herriges, A Jacob, M Vedaie, KD Alysandratos, YL Sun, C Lin, RB Werder, J Huang, AA Wilson, A Mithal, G Mostoslavsky, I Oglesby, IS Caballero, SH Guttentag, F Ahangari, N Kaminski, A Rodriguez-Fraticelli, F Camargo, Z Bar-Joseph, DN Kotton |
Cell Stem Cell | 2020 |
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Self-organization of organoids from endoderm-derived cells
A Lewis, R Keshara, YH Kim, A Grapin-Botton |
Journal of Molecular Medicine | 2020 |
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Generation of Complete Multi−Cell Type Lung Organoids From Human Embryonic and Patient‐Specific Induced Pluripotent Stem Cells for Infectious Disease Modeling and Therapeutics Validation
SL Leibel, RN McVicar, AM Winquist, WD Niles, EY Snyder |
Current Protocols in Stem Cell Biology | 2020 |
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Single-cell expression profiles of ACE2 and TMPRSS2 reveals potential vertical transmission and fetus infection of SARS-CoV-2
M Lü, L Qiu, G Jia, R Guo, Q Leng |
Aging | 2020 |
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Derivation of Airway Basal Stem Cells from Human Pluripotent Stem Cells
Hawkins FJ, Suzuki S, Beermann ML, Barillà C, Wang R, Villacorta-Martin C, Berical A, Jean JC, Suer JL, Matte T, Simone-Roach C, Tang Y, Schlaeger TM, Crane AM, Matthias N, Huang SX, Randell SH, Wu J, Spence JR, Carraro G, Stripp BR, Rab A, Sorsher EJ, Horani A, Brody SL, Davis BR, Kotton DN |
Cell Stem Cell | 2020 |
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Cell Biology and Translational Medicine, Volume 7: Stem Cells and Therapy: Emerging Approaches
K Turksen |
2019 | |
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Engraftment and proliferation potential of embryonic lung tissue cells in irradiated mice with emphysema
K Shiraishi, S Shichino, T Tsukui, S Hashimoto, S Ueha, K Matsushima |
Scientific Reports | 2019 |
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Circulating Truncated Alpha-1 Antitrypsin Glycoprotein in Patient Plasma Retains Anti-Inflammatory Capacity
EP Reeves, DM Dunlea, K McQuillan, CA ODwyer, TP Carroll, R Saldova, PR Akepati, MR Wormald, OJ McElvaney, V Shutchaidat, M Henry, P Meleady, J Keenan, DC Liberti, DN Kotton, PM Rudd, AA Wilson, NG McElvaney |
Journal of immunology (Baltimore, Md. : 1950) | 2019 |
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Challenges Facing Airway Epithelial Cell-Based Therapy for Cystic Fibrosis
A Berical, RE Lee, SH Randell, F Hawkins |
Frontiers in pharmacology | 2019 |
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Derivation of self-renewing lung alveolar epithelial type II cells from human pluripotent stem cells
A Jacob, M Vedaie, DA Roberts, DC Thomas, C Villacorta-Martin, KD Alysandratos, F Hawkins, DN Kotton |
Nature Protocols | 2019 |
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In Vitro Disease Modeling of Hermansky-Pudlak Syndrome Type 2 Using Human Induced Pluripotent Stem Cell-Derived Alveolar Organoids
Y Korogi, S Gotoh, S Ikeo, Y Yamamoto, N Sone, K Tamai, S Konishi, T Nagasaki, H Matsumoto, I Ito, TF Chen-Yoshikawa, H Date, M Hagiwara, I Asaka, A Hotta, M Mishima, T Hirai |
Stem Cell Reports | 2019 |
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Efficient Differentiation of Mouse Induced Pluripotent Stem Cells into Alveolar Epithelium Type II with a BRD4 Inhibitor
T Momozane, E Fukui, S Funaki, M Fujii, Y Kinehara, E Ito, S Miyagawa, Y Ohno, Y Sawa, M Okumura, Y Shintani |
Stem Cells International | 2019 |
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Stem cell-based Lung-on-Chips: The best of both worlds?
JC Nawroth, R Barrile, D Conegliano, S van Riet, PS Hiemstra, R Villenave |
Advanced Drug Delivery Reviews | 2019 |
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Generation of lung organoids from human pluripotent stem cells in vitro
AJ Miller, BR Dye, D Ferrer-Torres, DR Hill, AW Overeem, LD Shea, JR Spence |
Nature Protocols | 2019 |
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Reversal of Surfactant Protein B Deficiency in Patient Specific Human Induced Pluripotent Stem Cell Derived Lung Organoids by Gene Therapy
SL Leibel, A Winquist, I Tseu, J Wang, D Luo, S Shojaie, N Nathan, E Snyder, M Post |
Scientific Reports | 2019 |
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The Interferon-Inducible Proteoglycan Testican-2/SPOCK2 Functions as a Protective Barrier against Virus Infection of Lung Epithelial Cells
N Ahn, WJ Kim, N Kim, HW Park, SW Lee, JY Yoo, BR Williams |
Journal of virology | 2019 |
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Chemically-Defined, Xeno-Free, Scalable Production of hPSC-Derived Definitive Endoderm Aggregates with Multi-Lineage Differentiation Potential
A Sahabian, M Sgodda, O Naujok, R Dettmer, J Dahlmann, F Manstein, T Cantz, R Zweigerdt, U Martin, R Olmer |
Cells | 2019 |
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GATA6 suppression enhances lung specification from human pluripotent stem cells
Chia-Min Liao, Somdutta Mukherjee, Amita Tiyaboonchai, Jean Ann Maguire, Fabian L. Cardenas-Diaz, Deborah L. French, Paul Gadue |
Journal of Clinical Investigation | 2018 |
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Pulmonary Transplantation of Human iPSC-derived Macrophages Ameliorates Pulmonary Alveolar Proteinosis
C Happle, N Lachmann, M Ackermann, A Mirenska, G Göhring, K Thomay, A Mucci, M Hetzel, T Glomb, T Suzuki, C Chalk, S Glage, O Dittrich-Breiholz, B Trapnell, T Moritz, G Hansen |
American journal of respiratory and critical care medicine | 2018 |
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3D Modeling of Esophageal Development using Human PSC-Derived Basal Progenitors Reveals a Critical Role for Notch Signaling
Y Zhang, Y Yang, M Jiang, SX Huang, W Zhang, DA Alam, S Danopoulos, M Mori, YW Chen, R Balasubramanian, SM de Sousa Lopes, C Serra, M Bialecka, E Kim, S Lin, AL de Carvalho, PN Riccio, WV Cardoso, X Zhang, HW Snoeck, J Que |
Cell Stem Cell | 2018 |
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Human lung development: recent progress and new challenges
MZ Nikolić, D Sun, EL Rawlins |
Development (Cambridge, England) | 2018 |
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Single-Cell Transcriptomic Profiling of Pluripotent Stem Cell-Derived SCGB3A2+ Airway Epithelium
KB McCauley, KD Alysandratos, A Jacob, F Hawkins, IS Caballero, M Vedaie, W Yang, KJ Slovik, M Morley, G Carraro, S Kook, SH Guttentag, BR Stripp, EE Morrisey, DN Kotton |
Stem Cell Reports | 2018 |
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Derivation of Epithelial-Only Airway Organoids from Human Pluripotent Stem Cells: hPSC-derived Epithelial-Only Airway Organoids
KB McCauley, F Hawkins, DN Kotton |
Current Protocols in Stem Cell Biology | 2018 |
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Efficient Derivation of Functional Human Airway Epithelium from Pluripotent Stem Cells via Temporal Regulation of Wnt Signaling
KB McCauley, F Hawkins, M Serra, DC Thomas, A Jacob, DN Kotton |
Cell Stem Cell | 2017 |
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Pluripotent stem cell differentiation reveals distinct developmental pathways regulating lung- versus thyroid-lineage specification
M Serra, KD Alysandratos, F Hawkins, KB McCauley, A Jacob, J Choi, IS Caballero, M Vedaie, AA Kurmann, L Ikonomou, AN Hollenberg, JM Shannon, DN Kotton |
Development (Cambridge, England) | 2017 |
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Differentiation of Human Pluripotent Stem Cells into Functional Lung Alveolar Epithelial Cells
A Jacob, M Morley, F Hawkins, KB McCauley, JC Jean, H Heins, CL Na, TE Weaver, M Vedaie, K Hurley, A Hinds, SJ Russo, S Kook, W Zacharias, M Ochs, K Traber, LJ Quinton, A Crane, BR Davis, FV White, J Wambach, JA Whitsett, FS Cole, EE Morrisey, SH Guttentag, MF Beers, DN Kotton |
Cell Stem Cell | 2017 |
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Stem cell biology and regenerative medicine for neonatal lung diseases
M Kang, B Thébaud |
Pediatric Research | 2017 |
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