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Cited by 60Renal and related cancersPluripotent Stem Cells Research3D Printing in Biomedical Research

A genetically inducible endothelial niche enables vascularization of human kidney organoids with multilineage maturation and emergence of renin expressing cells

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Maggiore, Joseph C., LeGraw, Ryan, Przepiorski, Aneta, Velazquez, Jeremy, Chaney, Christopher, Vanichapol, Thitinee, Streeter, Evan, Almuallim, Zainab +21 more·2024·Kidney International
DOI 10.1016/j.kint.2024.05.026PMC PMC11912416

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Abstract

Abstract Vascularization plays a critical role in organ maturation and cell type development. Drug discovery, organ mimicry, and ultimately transplantation in a clinical setting thereby hinges on achieving robust vascularization of in vitro engineered organs. Here, focusing on human kidney organoids, we overcome this hurdle by combining an inducible ETS translocation variant 2 ( ETV2 ) human induced pluripotent stem cell (iPSC) line, which directs endothelial fate, with a non-transgenic iPSC line in suspension organoid culture. The resulting human kidney organoids show extensive vascularization by endothelial cells with an identity most closely related to endogenous kidney endothelia. Vascularized organoids also show increased maturation of nephron structures including more mature podocytes with improved marker expression, foot process interdigitation, an associated fenestrated endothelium, and the presence of renin + 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. Furthermore, this approach is orthogonal to native tissue differentiation paths, hence readily adaptable to other organoid systems and thus has the potential for a broad impact on basic and translational organoid studies. Translational Statement Developing therapies for patients with kidney diseases relies on a morphologically and physiologically representative in vitro model. Human kidney organoids are an attractive model to recapitulate kidney physiology, however, they are limited by the absence of a vascular network and mature cell populations. In this work, we have generated a genetically inducible endothelial niche that, when combined with an established kidney organoid protocol, induces the maturation of a robust endothelial cell network, induces a more mature podocyte population, and induces the emergence a functional renin population. This advance significantly increases the clinical relevance of human kidney organoids for etiological studies of kidney disease and future regenerative medicine strategies. Graphical Abstract Genetically engineered endothelial niche induces mature cell populations in human kidney organoids

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Authors
Maggiore, J. C., LeGraw, R., Przepiorski, A., Velazquez, J., Chaney, C., Vanichapol, T., Streeter, E., Almuallim, Z., Oda, A., Chiba, T., Silva-Barbosa, A., Franks, J., Hislop, J., Hill, A., Wu, H., Pfister, K., Howden, S. E., Watkins, S. C., Little, M. H., Humphreys, B. D., Kiani, S., Watson, A., Stolz, D. B., Davidson, A. J., Carroll, T., Cleaver, O., Sims-Lucas, S., Ebrahimkhani, M. R., & Hukriede, N. A.
Affiliations
  • University of Pittsburgh (US)
  • The University of Texas Southwestern Medical Center (US)
  • University of Auckland (NZ)
  • Murdoch Children's Research Institute (AU)
  • The University of Melbourne (AU)
  • Washington University in St. Louis (US)
Corresponding author
  • Ebrahimkhani, Mo R.
  • Hukriede, Neil A.
ORCID
Venue
Kidney International
Publisher
Elsevier BV
Published
2024-12
Volume
106
Issue
6
Pages
1086-1100
ISSN
0085-2538 (ISSN-L)
DOI
10.1016/j.kint.2024.05.026
PMC
PMC11912416
OpenAlex
W4399770652
Cited by
60
References
2
Citations by year
2026: 27 · 2025: 24 · 2024: 9
FWCI
8.17
Type
journal article
Language
en
Open access
Licence
Locations
  • Kidney International (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
  • Digital Commons@Becker (Washington University School of Medicine) (submittedVersion, cc-by-nc-nd)
  • Minerva Access (University of Melbourne) (submittedVersion, cc-by-nc-nd)
Funders
National Institutes of Health
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Renal and related cancers
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
  • Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
Keywords
kidney organoids, organoid vascularization, ETV2, induced pluripotent stem cells, endothelial differentiation, nephron maturation, glomerular endothelium, renin-producing cells, organoid maturation, organoid transplantation

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