Progenitor potential of lung epithelial organoid cells in a transplantation model
Lung progenitor cells are crucial for regeneration following injury, yet it is unclear whether lung progenitor cells can be functionally engrafted after transplantation. We transplanted organoid cells derived from alveolar type II (AT2) cells enriched by SCA1-negative status (SNO) or multipotent SCA...
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| Published in | Cell reports (Cambridge) Vol. 39; no. 2; p. 110662 |
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| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
12.04.2022
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| Subjects | |
| Online Access | Get full text |
| ISSN | 2211-1247 2211-1247 |
| DOI | 10.1016/j.celrep.2022.110662 |
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| Abstract | Lung progenitor cells are crucial for regeneration following injury, yet it is unclear whether lung progenitor cells can be functionally engrafted after transplantation. We transplanted organoid cells derived from alveolar type II (AT2) cells enriched by SCA1-negative status (SNO) or multipotent SCA1-positive progenitor cells (SPO) into injured mouse lungs. Transplanted SNO cells are retained in the alveolar regions, whereas SPO cells incorporate into airway and alveolar regions. Single-cell transcriptomics demonstrate that transplanted SNO cells are comparable to native AT2 cells. Transplanted SPO cells exhibit transcriptional hallmarks of alveolar and airway cells, as well as transitional cell states identified in disease. Transplanted cells proliferate after re-injury of recipient mice and retain organoid-forming capacity. Thus, lung epithelial organoid cells exhibit progenitor cell functions after reintroduction to the lung. This study reveals methods to interrogate lung progenitor cell potential and model transitional cell states relevant to pathogenic features of lung disease in vivo.
[Display omitted]
•Alveolar organoid cells engraft into the alveolar space•Transplanted lung alveolar cells have transcriptional signature of native AT2 cells•Transplanted alveolar cells proliferate and retain organoid-forming capacity•Organoid cells undergo changes to transitional cell states upon transplantation
Upon return to the lung via transplantation, lung epithelial progenitor cells from organoid cultures restore their native transcriptional state and retain progenitor cell function. Louie et al. show future cell-based therapies, reveal methods to interrogate lung progenitor cell potential, and model transitional cell states relevant to lung disease in vivo. |
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| AbstractList | Lung progenitor cells are crucial for regeneration following injury, yet it is unclear whether lung progenitor cells can be functionally engrafted after transplantation. We transplanted organoid cells derived from alveolar type II (AT2) cells enriched by SCA1-negative status (SNO) or multipotent SCA1-positive progenitor cells (SPO) into injured mouse lungs. Transplanted SNO cells are retained in the alveolar regions, whereas SPO cells incorporate into airway and alveolar regions. Single-cell transcriptomics demonstrate that transplanted SNO cells are comparable to native AT2 cells. Transplanted SPO cells exhibit transcriptional hallmarks of alveolar and airway cells, as well as transitional cell states identified in disease. Transplanted cells proliferate after re-injury of recipient mice and retain organoid-forming capacity. Thus, lung epithelial organoid cells exhibit progenitor cell functions after reintroduction to the lung. This study reveals methods to interrogate lung progenitor cell potential and model transitional cell states relevant to pathogenic features of lung disease
in vivo
.
Upon return to the lung via transplantation, lung epithelial progenitor cells from organoid cultures restore their native transcriptional state and retain progenitor cell function. Louie et al. show future cell-based therapies, reveal methods to interrogate lung progenitor cell potential, and model transitional cell states relevant to lung disease
in vivo
. Lung progenitor cells are crucial for regeneration following injury, yet it is unclear whether lung progenitor cells can be functionally engrafted after transplantation. We transplanted organoid cells derived from alveolar type II (AT2) cells enriched by SCA1-negative status (SNO) or multipotent SCA1-positive progenitor cells (SPO) into injured mouse lungs. Transplanted SNO cells are retained in the alveolar regions, whereas SPO cells incorporate into airway and alveolar regions. Single-cell transcriptomics demonstrate that transplanted SNO cells are comparable to native AT2 cells. Transplanted SPO cells exhibit transcriptional hallmarks of alveolar and airway cells, as well as transitional cell states identified in disease. Transplanted cells proliferate after re-injury of recipient mice and retain organoid-forming capacity. Thus, lung epithelial organoid cells exhibit progenitor cell functions after reintroduction to the lung. This study reveals methods to interrogate lung progenitor cell potential and model transitional cell states relevant to pathogenic features of lung disease in vivo. Lung progenitor cells are crucial for regeneration following injury, yet it is unclear whether lung progenitor cells can be functionally engrafted after transplantation. We transplanted organoid cells derived from alveolar type II (AT2) cells enriched by SCA1-negative status (SNO) or multipotent SCA1-positive progenitor cells (SPO) into injured mouse lungs. Transplanted SNO cells are retained in the alveolar regions, whereas SPO cells incorporate into airway and alveolar regions. Single-cell transcriptomics demonstrate that transplanted SNO cells are comparable to native AT2 cells. Transplanted SPO cells exhibit transcriptional hallmarks of alveolar and airway cells, as well as transitional cell states identified in disease. Transplanted cells proliferate after re-injury of recipient mice and retain organoid-forming capacity. Thus, lung epithelial organoid cells exhibit progenitor cell functions after reintroduction to the lung. This study reveals methods to interrogate lung progenitor cell potential and model transitional cell states relevant to pathogenic features of lung disease in vivo.Lung progenitor cells are crucial for regeneration following injury, yet it is unclear whether lung progenitor cells can be functionally engrafted after transplantation. We transplanted organoid cells derived from alveolar type II (AT2) cells enriched by SCA1-negative status (SNO) or multipotent SCA1-positive progenitor cells (SPO) into injured mouse lungs. Transplanted SNO cells are retained in the alveolar regions, whereas SPO cells incorporate into airway and alveolar regions. Single-cell transcriptomics demonstrate that transplanted SNO cells are comparable to native AT2 cells. Transplanted SPO cells exhibit transcriptional hallmarks of alveolar and airway cells, as well as transitional cell states identified in disease. Transplanted cells proliferate after re-injury of recipient mice and retain organoid-forming capacity. Thus, lung epithelial organoid cells exhibit progenitor cell functions after reintroduction to the lung. This study reveals methods to interrogate lung progenitor cell potential and model transitional cell states relevant to pathogenic features of lung disease in vivo. Lung progenitor cells are crucial for regeneration following injury, yet it is unclear whether lung progenitor cells can be functionally engrafted after transplantation. We transplanted organoid cells derived from alveolar type II (AT2) cells enriched by SCA1-negative status (SNO) or multipotent SCA1-positive progenitor cells (SPO) into injured mouse lungs. Transplanted SNO cells are retained in the alveolar regions, whereas SPO cells incorporate into airway and alveolar regions. Single-cell transcriptomics demonstrate that transplanted SNO cells are comparable to native AT2 cells. Transplanted SPO cells exhibit transcriptional hallmarks of alveolar and airway cells, as well as transitional cell states identified in disease. Transplanted cells proliferate after re-injury of recipient mice and retain organoid-forming capacity. Thus, lung epithelial organoid cells exhibit progenitor cell functions after reintroduction to the lung. This study reveals methods to interrogate lung progenitor cell potential and model transitional cell states relevant to pathogenic features of lung disease in vivo. [Display omitted] •Alveolar organoid cells engraft into the alveolar space•Transplanted lung alveolar cells have transcriptional signature of native AT2 cells•Transplanted alveolar cells proliferate and retain organoid-forming capacity•Organoid cells undergo changes to transitional cell states upon transplantation Upon return to the lung via transplantation, lung epithelial progenitor cells from organoid cultures restore their native transcriptional state and retain progenitor cell function. Louie et al. show future cell-based therapies, reveal methods to interrogate lung progenitor cell potential, and model transitional cell states relevant to lung disease in vivo. |
| ArticleNumber | 110662 |
| Author | Lu, Emery Garcia-de-Alba, Carolina Shehaj, Andrea Paschini, Margherita Louie, Sharon M. Raby, Benjamin A. Moye, Aaron L. Bronson, Roderick T. Kim, Carla F. Wong, Irene G. Ararat, Erhan Lu, Bao |
| AuthorAffiliation | 2 Harvard Stem Cell Institute, Cambridge, MA 02138, USA 4 Division of Pulmonary Medicine, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USA 3 Department of Genetics, Harvard Medical School, Boston, MA 02115, USA 1 Stem Cell Program and Divisions of Hematology/Oncology, Boston Children’s Hospital, Boston, MA 02115, USA 5 Rodent Histopathology Core, Harvard Medical School, Boston, MA 02115, USA 6 These authors contributed equally 7 Lead contact |
| AuthorAffiliation_xml | – name: 5 Rodent Histopathology Core, Harvard Medical School, Boston, MA 02115, USA – name: 4 Division of Pulmonary Medicine, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USA – name: 3 Department of Genetics, Harvard Medical School, Boston, MA 02115, USA – name: 7 Lead contact – name: 1 Stem Cell Program and Divisions of Hematology/Oncology, Boston Children’s Hospital, Boston, MA 02115, USA – name: 6 These authors contributed equally – name: 2 Harvard Stem Cell Institute, Cambridge, MA 02138, USA |
| Author_xml | – sequence: 1 givenname: Sharon M. surname: Louie fullname: Louie, Sharon M. organization: Stem Cell Program and Divisions of Hematology/Oncology, Boston Children’s Hospital, Boston, MA 02115, USA – sequence: 2 givenname: Aaron L. surname: Moye fullname: Moye, Aaron L. organization: Stem Cell Program and Divisions of Hematology/Oncology, Boston Children’s Hospital, Boston, MA 02115, USA – sequence: 3 givenname: Irene G. orcidid: 0000-0001-5229-2111 surname: Wong fullname: Wong, Irene G. organization: Stem Cell Program and Divisions of Hematology/Oncology, Boston Children’s Hospital, Boston, MA 02115, USA – sequence: 4 givenname: Emery surname: Lu fullname: Lu, Emery organization: Stem Cell Program and Divisions of Hematology/Oncology, Boston Children’s Hospital, Boston, MA 02115, USA – sequence: 5 givenname: Andrea surname: Shehaj fullname: Shehaj, Andrea organization: Stem Cell Program and Divisions of Hematology/Oncology, Boston Children’s Hospital, Boston, MA 02115, USA – sequence: 6 givenname: Carolina orcidid: 0000-0001-9774-445X surname: Garcia-de-Alba fullname: Garcia-de-Alba, Carolina organization: Stem Cell Program and Divisions of Hematology/Oncology, Boston Children’s Hospital, Boston, MA 02115, USA – sequence: 7 givenname: Erhan orcidid: 0000-0003-1880-4827 surname: Ararat fullname: Ararat, Erhan organization: Stem Cell Program and Divisions of Hematology/Oncology, Boston Children’s Hospital, Boston, MA 02115, USA – sequence: 8 givenname: Benjamin A. surname: Raby fullname: Raby, Benjamin A. organization: Division of Pulmonary Medicine, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USA – sequence: 9 givenname: Bao surname: Lu fullname: Lu, Bao organization: Division of Pulmonary Medicine, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USA – sequence: 10 givenname: Margherita surname: Paschini fullname: Paschini, Margherita organization: Stem Cell Program and Divisions of Hematology/Oncology, Boston Children’s Hospital, Boston, MA 02115, USA – sequence: 11 givenname: Roderick T. surname: Bronson fullname: Bronson, Roderick T. organization: Rodent Histopathology Core, Harvard Medical School, Boston, MA 02115, USA – sequence: 12 givenname: Carla F. orcidid: 0000-0002-2366-9538 surname: Kim fullname: Kim, Carla F. email: carla.kim@childrens.harvard.edu organization: Stem Cell Program and Divisions of Hematology/Oncology, Boston Children’s Hospital, Boston, MA 02115, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35417699$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2022 The Authors Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved. |
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| Keywords | single-cell RNA sequencing CP: Stem cell research organoids airway transplantation alveolar lung epithelial cells lung progenitor cells lung stem cells lung regeneration |
| Language | English |
| License | This is an open access article under the CC BY-NC-ND license. Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS Conceptualization, S.M.L., A.L.M., I.G.W., and C.F.K.; methodology, S.M.L., A.L.M., I.G.W., and C.F.K.; software, A.L.M.; investigation, S.M.L., A.L.M., I.G.W., E.L., A.S., C.G.d.A., E.A., M.P., R.T.B., B.L., and B.A.R.; writing – original draft, S.M.L. and C.F.K.; writing – review & editing, S.M.L., A.L.M., I.G.W., E.L., and C.F.K.; visualization, S.M.L. and A.L.M.; funding acquisition, S.M.L., A.L.M., I.G.W., and C.F.K.; supervision, C.F.K. |
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| SubjectTerms | airway alveolar Animals Cell Differentiation Epithelial Cells Lung lung epithelial cells lung progenitor cells lung regeneration lung stem cells Mice Organoids single-cell RNA sequencing Spinocerebellar Ataxias Stem Cells transplantation |
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| Title | Progenitor potential of lung epithelial organoid cells in a transplantation model |
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