ArticleKidney international2024
A genetically inducible endothelial niche enables vascularization of human kidney organoids with multilineage maturation and emergence of renin expressing cells.
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29 citing papers in PubMed.
- Generation of the functionally enhanced proximal tubular cells from human iPSC-derived kidney organoids.Experimental & molecular medicine · 2026Article
- Angiogenesis in Lung Regeneration and Aging.Arteriosclerosis, thrombosis, and vascular biology · 2026Review
- Bridging Kidney Organoid Innovation and Regenerative Medicine: Current Advances and Future Directions.Cell proliferation · 2026Review
- Synthetic developmental engineering of human liver organogenesis.Development (Cambridge, England) · 2026Review
- Kidney organoid vascularization: current advancements in the field.Regenerative therapy · 2026Article
- Disease modelling with in vitro vascularised organoids.Disease models & mechanisms · 2026Review
- Developmentally inspired synthetic kidney engineering.Nature biotechnology · 2026Review
- Living Tissues by Design: The Rise of Hybrid Models in Biofabrication.Journal of functional biomaterials · 2026Review
- Progress in stem cell-based embryo models and their applications in developmental biology and biomedicine.Nature reviews. Molecular cell biology · 2026Review
- Splice modulation of COL4A5 reinstates collagen IV assembly in an organoid model of Alport syndrome.JCI insight · 2026Article
- Vascularization and maturation of kidney organoids: a comprehensive review of technological trends and challenges.Journal of artificial organs : the official journal of the Japanese Society for Artificial Organs · 2026Review
- Development and Transformation of Veterinary Experimental In Vitro Models: From 2D Culture to 3D Organoids.Animals : an open access journal from MDPI · 2026Review
- Advances and continuing challenges in differentiation of stem cells to human kidney tissue.Nature reviews. Nephrology · 2026Review
- The role of the vascular niche in regulating kidney tubulointerstitial fibrosis.Kidney international · 2026Review
- Advances and future perspectives of kidney organoid technology in renal disease research and clinical translation.Frontiers in medicine · 2026Review
- Coordinated Development of Immune Cell Populations in Vascularized Skin Organoids from Human Induced Pluripotent Stem Cells.Advanced healthcare materials · 2025Article
- Multiscale Construction, Evaluation, and Application of Organoids.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2025Review
- From Cells to Organoids: Approaches, Regulatory Mechanisms, Applications, and Challenges of Organoids.Cells · 2025Review
- The kidney stroma in development and disease.Nature reviews. Nephrology · 2025Review
- Zonal endothelial cell heterogeneity underlies murine renal vascular development.Angiogenesis · 2025Article
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Authors and funding
29 authors.
Joseph C MaggioreDepartment of Cell Biology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA; Center for Integrative Organ Systems, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Ryan LeGrawDepartment of Pathology, Division of Experimental Pathology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA; Pittsburgh Liver Research Center, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Aneta PrzepiorskiDepartment of Cell Biology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Jeremy VelazquezDepartment of Pathology, Division of Experimental Pathology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA; Pittsburgh Liver Research Center, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Christopher ChaneyDepartment of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas, USA; Hamon Center for Regenerative Science and Medicine, University of Texas Southwestern Medical Center, Dallas, Texas, USA; Department of Internal Medicine, Division of Nephrology, University of Texas Southwestern Medical Center, Dallas, Texas, USA.
Thitinee VanichapolDepartment of Molecular Medicine and Pathology, University of Auckland, Auckland, New Zealand.
Evan StreeterDepartment of Cell Biology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA; Center for Integrative Organ Systems, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Zainab AlmuallimDepartment of Cell Biology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA; Center for Integrative Organ Systems, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Akira OdaDepartment of Pediatrics, School of Medicine, University of Pittsburgh, Pittsburgh Pennsylvania, USA.
Takuto ChibaDepartment of Pediatrics, School of Medicine, University of Pittsburgh, Pittsburgh Pennsylvania, USA.
Anne Silva-BarbosaDepartment of Pediatrics, School of Medicine, University of Pittsburgh, Pittsburgh Pennsylvania, USA.
Jonathan FranksCenter for Biologic Imaging, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Joshua HislopPittsburgh Liver Research Center, University of Pittsburgh, Pittsburgh, Pennsylvania, USA; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Alex HillDepartment of Pathology, Division of Experimental Pathology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA; Pittsburgh Liver Research Center, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Haojia WuDivision of Nephrology, Department of Medicine, School of Medicine, Washington University in St. Louis, St. Louis, Missouri, USA.
Katherine PfisterDepartment of Pediatrics, School of Medicine, University of Pittsburgh, Pittsburgh Pennsylvania, USA.
Sara E HowdenMurdoch Children's Research Institute, Melbourne, Victoria, Australia.
Simon C WatkinsCenter for Biologic Imaging, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Melissa H LittleMurdoch Children's Research Institute, Melbourne, Victoria, Australia; Department of Anatomy and Neuroscience, The University of Melbourne, Melbourne, Victoria, Australia; Department of Paediatrics, The University of Melbourne, Melbourne, Victoria, Australia.
Benjamin D HumphreysDivision of Nephrology, Department of Medicine, School of Medicine, Washington University in St. Louis, St. Louis, Missouri, USA; Department of Developmental Biology, School of Medicine, Washington University in St. Louis, St. Louis, Missouri, USA.
Samira KianiDepartment of Pathology, Division of Experimental Pathology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA; Pittsburgh Liver Research Center, University of Pittsburgh, Pittsburgh, Pennsylvania, USA; Center for Biologic Imaging, University of Pittsburgh, Pittsburgh, Pennsylvania, USA; McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Alan WatsonCenter for Biologic Imaging, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Donna B StolzCenter for Biologic Imaging, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Alan J DavidsonDepartment of Molecular Medicine and Pathology, University of Auckland, Auckland, New Zealand.
Tom CarrollDepartment of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas, USA; Hamon Center for Regenerative Science and Medicine, University of Texas Southwestern Medical Center, Dallas, Texas, USA; Department of Internal Medicine, Division of Nephrology, University of Texas Southwestern Medical Center, Dallas, Texas, USA.
Ondine CleaverDepartment of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas, USA.
Sunder Sims-LucasDepartment of Pediatrics, School of Medicine, University of Pittsburgh, Pittsburgh Pennsylvania, USA.
Mo R EbrahimkhaniDepartment of Pathology, Division of Experimental Pathology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA; Pittsburgh Liver Research Center, University of Pittsburgh, Pittsburgh, Pennsylvania, USA; Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas, USA; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, Pennsylvania, USA. Electronic address: mo.ebr@pitt.edu.
Neil A HukriedeDepartment of Cell Biology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA; Center for Integrative Organ Systems, University of Pittsburgh, Pittsburgh, Pennsylvania, USA. Electronic address: hukriede@pitt.edu.
Funding
Pittsburgh Liver Research CenterP30DK120531 · NIDDK · UNIVERSITY OF PITTSBURGH AT PITTSBURGH · PI CLAUDETTE Marie ST CROIX · 2019 to 2026
$10.9MApplication of Progenitor Niche Signals to Ex Vivo NephrogenesisRC2DK125960 · NIDDK · ROGOSIN INSTITUTE · PI CARROLL, THOMAS JOSEPH, CLEAVER, ONDINE B · 2021 to 2025
$7.4MCellular Approaches to Tissue Engineering/RegenerationT32EB001026 · NIBIB · UNIVERSITY OF PITTSBURGH AT PITTSBURGH · PI DUNCAN, ANDREW W, MONGA, SATDARSHAN SINGH · 2003 to 2024
$5.5MResource Development CoreU54DK137329 · NIDDK · UNIVERSITY OF PITTSBURGH AT PITTSBURGH · PI Gerard L Apodaca · 2023 to 2026
$4.8MRegulation of Renal Progenitor Cells in Regenerating KidneysR01DK069403 · NIDDK · UNIVERSITY OF PITTSBURGH AT PITTSBURGH · PI HUKRIEDE, NEIL A · 2006 to 2020
$4.8MTherapeutic Optimization of Productive Repair After Acute Kidney InjuryUC2DK126122 · NIDDK · UNIVERSITY OF PITTSBURGH AT PITTSBURGH · PI DAVIDSON, ALAN, DE CAESTECKER, MARK P. · 2020 to 2024
$3.2MMolecular regulation of Rho and Ras family GTPase activity controls vascular lumen formation.R01HL126518 · NHLBI · UT SOUTHWESTERN MEDICAL CENTER · PI CLEAVER, ONDINE B, DAVIS, GEORGE E · 2015 to 2023
$3.1MThe Role of Renal Interstitium in Kidney DevelopmentR01DK127634 · NIDDK · UT SOUTHWESTERN MEDICAL CENTER · PI CARROLL, THOMAS JOSEPH, PARK, JOO-SEOP · 2021 to 2024
$2.8MRecreating Human Developmental Hematopoietic Niches for Ex Vivo Biomanufacturing of Blood Stem CellsR01HL141805 · NHLBI · UNIVERSITY OF PITTSBURGH AT PITTSBURGH · PI Mo Reza Ebrahimkhani · 2019 to 2026
$2.6MIntegration of systems and synthetic biology to advance development of human tissues ex vivoR01EB028532 · NIBIB · UNIVERSITY OF PITTSBURGH AT PITTSBURGH · PI EBRAHIMKHANI, MO REZA · 2019 to 2022
$1.7MCRISPR logic circuits for safer and controllable gene therapiesR01EB024562 · NIBIB · UNIVERSITY OF PITTSBURGH AT PITTSBURGH · PI KIANI, SAMIRA · 2018 to 2021
$1.7MGenerating kidney organoids and mature renal cell types via directed iPSC differentiationUH3DK107344 · NIDDK · MURDOCH CHILDREN'S RESEARCH INSTITUTE · PI LITTLE, MELISSA HELEN · 2017 to 2019
$1.0MNHLBI NIH HHS R01 HL126518NHLBI NIH HHS R01 HL141805NIBIB NIH HHS R01 EB024562NIBIB NIH HHS R01 EB028532NIBIB NIH HHS T32 EB001026NIDDK NIH HHS F30 DK137453NIDDK NIH HHS P30 DK120531NIDDK NIH HHS R01 DK069403NIDDK NIH HHS R01 DK127634NIDDK NIH HHS R56 DK125960NIDDK NIH HHS RC2 DK125960NIDDK NIH HHS U54 DK137329NIDDK NIH HHS UC2 DK126122NIDDK NIH HHS UH2 DK107344NIDDK NIH HHS UH3 DK107344NIH HHS S10 OD016236NIH HHS S10 OD019973
Abstract
Vascularization plays a critical role in organ maturation and cell-type development. Drug discovery, organ mimicry, and ultimately transplantation hinge on achieving robust vascularization of in vitro engineered organs. Here, focusing on human kidney organoids, we overcame this hurdle by combining a human induced pluripotent stem cell (iPSC) line containing an inducible ETS translocation variant 2 (ETV2) (a transcription factor playing a role in endothelial cell development) that directs endothelial differentiation in vitro, with a non-transgenic iPSC line in suspension organoid culture. The resulting human kidney organoids show extensive endothelialization with a cellular identity most closely related to human kidney endothelia. Endothelialized kidney organoids also show increased maturation of nephron structures, an associated fenestrated endothelium with de novo formation of glomerular and venous subtypes, and the emergence of drug-responsive renin expressing cells. The creation of an engineered vascular niche capable of improving kidney organoid maturation and cell type complexity is a significant step forward in the path to clinical translation. Thus, incorporation of an engineered endothelial niche into a previously published kidney organoid protocol allowed the orthogonal differentiation of endothelial and parenchymal cell types, demonstrating the potential for applicability to other basic and translational organoid studies.
Indexed as
Cell DifferentiationEndothelial CellsInduced Pluripotent Stem CellsKidneyOrganoidsReninTranscription FactorsCell LineCell LineageHumansNeovascularization, PhysiologicETV2 protein, humanReninTranscription Factorsendothelialgenetic engineeringorganoidspodocytesreninscRNAseq
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