Developmental diversity and unique sensitivity to injury of lung endothelial subtypes during postnatal growth
Summary: At birth, the lung is still immature, heightening susceptibility to injury but enhancing regenerative capacity. Angiogenesis drives postnatal lung development. Therefore, we profiled the transcriptional ontogeny and sensitivity to injury of pulmonary endothelial cells (EC) during early post...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-03-01
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| Series: | iScience |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004223001748 |
| _version_ | 1797904303564783616 |
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| author | Fabio Zanini Xibing Che Carsten Knutsen Min Liu Nina E. Suresh Racquel Domingo-Gonzalez Steve H. Dou Daoqin Zhang Gloria S. Pryhuber Robert C. Jones Stephen R. Quake David N. Cornfield Cristina M. Alvira |
| author_facet | Fabio Zanini Xibing Che Carsten Knutsen Min Liu Nina E. Suresh Racquel Domingo-Gonzalez Steve H. Dou Daoqin Zhang Gloria S. Pryhuber Robert C. Jones Stephen R. Quake David N. Cornfield Cristina M. Alvira |
| author_sort | Fabio Zanini |
| collection | DOAJ |
| description | Summary: At birth, the lung is still immature, heightening susceptibility to injury but enhancing regenerative capacity. Angiogenesis drives postnatal lung development. Therefore, we profiled the transcriptional ontogeny and sensitivity to injury of pulmonary endothelial cells (EC) during early postnatal life. Although subtype speciation was evident at birth, immature lung EC exhibited transcriptomes distinct from mature counterparts, which progressed dynamically over time. Gradual, temporal changes in aerocyte capillary EC (CAP2) contrasted with more marked alterations in general capillary EC (CAP1) phenotype, including distinct CAP1 present only in the early alveolar lung expressing Peg3, a paternally imprinted transcription factor. Hyperoxia, an injury that impairs angiogenesis induced both common and unique endothelial gene signatures, dysregulated capillary EC crosstalk, and suppressed CAP1 proliferation while stimulating venous EC proliferation. These data highlight the diversity, transcriptomic evolution, and pleiotropic responses to injury of immature lung EC, possessing broad implications for lung development and injury across the lifespan. |
| first_indexed | 2024-04-10T09:46:47Z |
| format | Article |
| id | doaj.art-b26cc1b660b54915931e23d68f0719cc |
| institution | Directory Open Access Journal |
| issn | 2589-0042 |
| language | English |
| last_indexed | 2024-04-10T09:46:47Z |
| publishDate | 2023-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj.art-b26cc1b660b54915931e23d68f0719cc2023-02-17T04:55:27ZengElsevieriScience2589-00422023-03-01263106097Developmental diversity and unique sensitivity to injury of lung endothelial subtypes during postnatal growthFabio Zanini0Xibing Che1Carsten Knutsen2Min Liu3Nina E. Suresh4Racquel Domingo-Gonzalez5Steve H. Dou6Daoqin Zhang7Gloria S. Pryhuber8Robert C. Jones9Stephen R. Quake10David N. Cornfield11Cristina M. Alvira12Prince of Wales Clinical School, Lowy Cancer Research Centre, University of New South Wales, Sydney, Kensington, NSW 2052, AustraliaCenter for Excellence in Pulmonary Biology, Stanford University School of Medicine, Stanford, CA 94305, USA; Division of Pulmonary, Asthma and Sleep Medicine, Department of Pediatrics, Stanford University School of Medicine, Stanford, CA 94305, USACenter for Excellence in Pulmonary Biology, Stanford University School of Medicine, Stanford, CA 94305, USA; Division of Critical Care Medicine, Department of Pediatrics, Stanford University School of Medicine, Stanford, CA 94305, USACenter for Excellence in Pulmonary Biology, Stanford University School of Medicine, Stanford, CA 94305, USA; Division of Critical Care Medicine, Department of Pediatrics, Stanford University School of Medicine, Stanford, CA 94305, USACenter for Excellence in Pulmonary Biology, Stanford University School of Medicine, Stanford, CA 94305, USA; Division of Pulmonary, Asthma and Sleep Medicine, Department of Pediatrics, Stanford University School of Medicine, Stanford, CA 94305, USACenter for Excellence in Pulmonary Biology, Stanford University School of Medicine, Stanford, CA 94305, USA; Division of Critical Care Medicine, Department of Pediatrics, Stanford University School of Medicine, Stanford, CA 94305, USACenter for Excellence in Pulmonary Biology, Stanford University School of Medicine, Stanford, CA 94305, USA; Division of Critical Care Medicine, Department of Pediatrics, Stanford University School of Medicine, Stanford, CA 94305, USACenter for Excellence in Pulmonary Biology, Stanford University School of Medicine, Stanford, CA 94305, USA; Division of Critical Care Medicine, Department of Pediatrics, Stanford University School of Medicine, Stanford, CA 94305, USADivision of Neonatology, Department of Pediatrics, University of Rochester Medical Center, Rochester, NY 14642, USADepartment of Bioengineering, Stanford University, Stanford, CA 94305, USADepartment of Bioengineering, Stanford University, Stanford, CA 94305, USA; Chan Zuckerberg Biohub, San Francisco, CA 94158, USA; Department of Applied Physics, Stanford University, Stanford, CA 94305, USACenter for Excellence in Pulmonary Biology, Stanford University School of Medicine, Stanford, CA 94305, USA; Division of Pulmonary, Asthma and Sleep Medicine, Department of Pediatrics, Stanford University School of Medicine, Stanford, CA 94305, USACenter for Excellence in Pulmonary Biology, Stanford University School of Medicine, Stanford, CA 94305, USA; Division of Critical Care Medicine, Department of Pediatrics, Stanford University School of Medicine, Stanford, CA 94305, USA; Corresponding authorSummary: At birth, the lung is still immature, heightening susceptibility to injury but enhancing regenerative capacity. Angiogenesis drives postnatal lung development. Therefore, we profiled the transcriptional ontogeny and sensitivity to injury of pulmonary endothelial cells (EC) during early postnatal life. Although subtype speciation was evident at birth, immature lung EC exhibited transcriptomes distinct from mature counterparts, which progressed dynamically over time. Gradual, temporal changes in aerocyte capillary EC (CAP2) contrasted with more marked alterations in general capillary EC (CAP1) phenotype, including distinct CAP1 present only in the early alveolar lung expressing Peg3, a paternally imprinted transcription factor. Hyperoxia, an injury that impairs angiogenesis induced both common and unique endothelial gene signatures, dysregulated capillary EC crosstalk, and suppressed CAP1 proliferation while stimulating venous EC proliferation. These data highlight the diversity, transcriptomic evolution, and pleiotropic responses to injury of immature lung EC, possessing broad implications for lung development and injury across the lifespan.http://www.sciencedirect.com/science/article/pii/S2589004223001748Developmental biologySystems biologyTranscriptomics |
| spellingShingle | Fabio Zanini Xibing Che Carsten Knutsen Min Liu Nina E. Suresh Racquel Domingo-Gonzalez Steve H. Dou Daoqin Zhang Gloria S. Pryhuber Robert C. Jones Stephen R. Quake David N. Cornfield Cristina M. Alvira Developmental diversity and unique sensitivity to injury of lung endothelial subtypes during postnatal growth iScience Developmental biology Systems biology Transcriptomics |
| title | Developmental diversity and unique sensitivity to injury of lung endothelial subtypes during postnatal growth |
| title_full | Developmental diversity and unique sensitivity to injury of lung endothelial subtypes during postnatal growth |
| title_fullStr | Developmental diversity and unique sensitivity to injury of lung endothelial subtypes during postnatal growth |
| title_full_unstemmed | Developmental diversity and unique sensitivity to injury of lung endothelial subtypes during postnatal growth |
| title_short | Developmental diversity and unique sensitivity to injury of lung endothelial subtypes during postnatal growth |
| title_sort | developmental diversity and unique sensitivity to injury of lung endothelial subtypes during postnatal growth |
| topic | Developmental biology Systems biology Transcriptomics |
| url | http://www.sciencedirect.com/science/article/pii/S2589004223001748 |
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