Adaptable haemodynamic endothelial cells for organogenesis and tumorigenesis
Open accessAbstract
Endothelial cells adopt tissue-specific characteristics to instruct organ development and regeneration 1,2. This adaptability is lost in cultured adult endothelial cells, which do not vascularize tissues in an organotypic manner. Here, we show that transient reactivation of the embryonic-restricted ETS variant transcription factor 2 (ETV2)3 in mature human endothelial cells cultured in a serum-free three-dimensional matrix composed of a mixture of laminin, entactin and type-IV collagen (LEC matrix) 'resets' these endothelial cells to adaptable, vasculogenic cells, which form perfusable and plastic vascular plexi. Through chromatin remodelling, ETV2 induces tubulogenic pathways, including the activation of RAP1, which promotes the formation of durable lumens 4,5. In three-dimensional matrices-which do not have the constraints of bioprinted scaffolds-the 'reset' vascular endothelial cells (R-VECs) self-assemble into stable, multilayered and branching vascular networks within scalable microfluidic chambers, which are capable of transporting human blood. In vivo, R-VECs implanted subcutaneously in mice self-organize into durable pericyte-coated vessels that functionally anastomose to the host circulation and exhibit long-lasting patterning, with no evidence of malformations or angiomas. R-VECs directly interact with cells within three-dimensional co-cultured organoids, removing the need for the restrictive synthetic semipermeable membranes that are required for organ-on-chip systems, therefore providing a physiological platform for vascularization, which we call 'Organ-On-VascularNet'. R-VECs enable perfusion of glucose-responsive insulin-secreting human pancreatic islets, vascularize decellularized rat intestines and arborize healthy or cancerous human colon organoids. Using single-cell RNA sequencing and epigenetic profiling, we demonstrate that R-VECs establish an adaptive vascular niche that differentially adjusts and conforms to organoids and tumoroids in a tissue-specific manner. Our Organ-On-VascularNet model will permit metabolic, immunological and physiochemical studies and screens to decipher the crosstalk between organotypic endothelial cells and parenchymal cells for identification of determinants of endothelial cell heterogeneity, and could lead to advances in therapeutic organ repair and tumour targeting.
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This heterogeneity in treatment responses parallels variability in patient outcomes and has positioned cancer organoids as potential predictive tools for drug testing.
“This parallels the variability in patient outcomes observed in the clinic and have positioned cancer organoids as potential predictive tool for drug testing (Extensively reviewed in213).”
From Organoids (2022) · cites this paper as [213]
The Discussion (page unavailable) proposes co-cultures of malignant organoids as a platform for delivering chemotherapeutic agents and for pharmaceutical screening, supporting their potential use in drug testing. It does not report heterogeneous treatment responses, link those responses to variability in patient outcomes, or establish that organoids predict clinical outcomes. (LLM, conf=0.84)
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- Authors
- Palikuqi, B., Nguyen, D.-H. T., Li, G., Schreiner, R., Pellegata, A. F., Liu, Y., Redmond, D., Geng, F., Lin, Y., Gómez-Salinero, J. M., Yokoyama, M., Zumbo, P., Zhang, T., Kunar, B., Witherspoon, M., Han, T., Tedeschi, A. M., Scottoni, F., Lipkin, S. M., Dow, L., Elemento, O., Xiang, J. Z., Shido, K., Spence, J. R., Zhou, Q. J., Schwartz, R. E., De Coppi, P., Rabbany, S. Y., & Rafii, S.
- Affiliations
- Weill Cornell Medicine (US)
- University College London (GB)
- University of Michigan (US)
- Hofstra University (US)
- Corresponding author
- Rafii, Shahin
- ORCID
- Palikuqi, Brisa
- Nguyen, Duc-Huy T.
- Li, Ge
- Schreiner, Ryan
- Pellegata, Alessandro F.
- Liu, Ying
- Redmond, David
- Lin, Yang
- Gómez-Salinero, Jesus M.
- Yokoyama, Masataka
- Zumbo, Paul
- Zhang, Tuo
- Kunar, Balvir
- Scottoni, Federico
- Lipkin, Steven M.
- Dow, Lukas
- Elemento, Olivier
- Xiang, Jenny Z.
- Shido, Koji
- Spence, Jason R.
- Zhou, Qiao J.
- Schwartz, Robert E.
- De Coppi, Paolo
- Rabbany, Sina Y.
- Rafii, Shahin
- Venue
- Nature
- Published
- 2020-09-09
- Volume
- 585
- Issue
- 7825
- Pages
- 426-432
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC7480005
- OpenAlex
- W3083915852
- Cited by
- 259
- References
- 49
- Citations by year
- 2026: 34 · 2025: 48 · 2024: 43 · 2023: 40 · 2022: 49 · 2021: 39 · 2020: 5 · 2019: 1
- FWCI
- 10.42
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Nature (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Virtual Community of Pathological Anatomy (University of Castilla La Mancha) (submittedVersion)
- Funders
- U.S. Department of Defense
- Oak Foundation (W1095/OCAY-14-191)
- Eli Lilly and Company
- Starr Foundation (2014-023)
- Neuroendocrine Tumor Research Foundation
- New York State Stem Cell Science (C32596GG, C029156)
- National Institute for Health and Care Research (NIHRRP-2014-04-046)
- Great Ormond Street Hospital for Children
- National Tea Research Foundation
- National Institutes of Health (H2020, UL1TR002384)
- Weill Cornell Medical College (UL1TR002384)
- Horizon 2020 Framework Programme (668,294, INTENS 668294)
- Medical Research Council (MR/N028414/1)
- Biotechnology and Biological Sciences Research Council
- Japan Society for the Promotion of Science (20K08397)
- National Institute on Alcohol Abuse and Alcoholism (R01AA027327)
- National Institute on Aging (R01AG056298)
- National Heart, Lung, and Blood Institute (R01HL119872, R01HL128158, R01HL119215, R01HL115128, R01HL139056, R35HL150809)
- National Institute of Mental Health (F30MH115616)
- National Cancer Institute (R01CA194547, R01CA234614)
- National Institute of Allergy and Infectious Diseases (R21AI117213, U01AI138329, R01AI107301)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK095039, RC2DK114777, UC4DK116280, R01DK106253, R01DK121072, DP3DK111907, R03DK117252, K08DK101754, P30DK089503)
- National Center for Advancing Translational Sciences
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Keywords
- ETV2, vascular endothelial cells, organogenesis, carcinogenesis, vascularization, organoids, tumor organoids, vascular niche, Rap1, chromatin remodeling, three-dimensional matrix, pancreatic islets, colon organoids, endothelial heterogeneity, organ-on-a-chip
- MeSH terms
- RNA-Seq, Blood Vessels, Chromatin, Hemodynamics, Humans, Islets of Langerhans, Models, Biological, Neoplasms, Organ Specificity, Organoids, Transcription Factors, Cell Culture Techniques, Organogenesis, Endothelial Cells, Epigenesis, Genetic, Epigenomics, Single-Cell Analysis, Transcriptome, Human Umbilical Vein Endothelial Cells, Carcinogenesis, In Vitro Techniques
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