journal article·2024-10-01Open access

A perfusable, vascularized kidney organoid-on-chip model

Katharina T Kroll, Kimberly A Homan, Sebastien G M Uzel, Mariana M Mata, Kayla J Wolf, Jonathan E Rubins, Jennifer A Lewis

Biofabrication· Volume 16· Issue 4

Abstract

Abstract The ability to controllably perfuse kidney organoids would better recapitulate the native tissue microenvironment for applications ranging from drug testing to therapeutic use. Here, we report a perfusable, vascularized kidney organoid on chip model composed of two individually addressable channels embedded in an extracellular matrix (ECM). The channels are respectively seeded with kidney organoids and human umbilical vein endothelial cells that form a confluent endothelium (macrovessel). During perfusion, endogenous endothelial cells present within the kidney organoids migrate through the ECM towards the macrovessel, where they form lumen-on-lumen anastomoses that are supported by stromal-like cells. Once micro-macrovessel integration is achieved, we introduced fluorescently labeled dextran of varying molecular weight and red blood cells into the macrovessel, which are transported through the microvascular network to the glomerular epithelia within the kidney organoids. Our approach for achieving controlled organoid perfusion opens new avenues for generating other perfused human tissues.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Renal and related cancers · 3D Printing in Biomedical Research · Tissue Engineering and Regenerative Medicine

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (46)

Show source-provided references
1. US agency seeks to phase out animal testing10.1038/d41586-022-03569-9 ↗
2. Towards in vitro models for reducing or replacing the use of animals in drug testing10.1038/s41551-023-01154-7 ↗
3. A systematic review of in vitro models of drug-induced kidney injury10.1016/j.cotox.2021.06.001 ↗
4. Bioprinting of 3D convoluted renal proximal tubules on perfusable chips10.1038/srep34845 ↗
5. Human kidney proximal tubule-on-a-chip for drug transport and nephrotoxicity assessment10.1039/c3ib40049b ↗
6. Renal reabsorption in 3D vascularized proximal tubule models10.1073/pnas.1815208116 ↗
7. Mature induced-pluripotent-stem-cell-derived human podocytes reconstitute kidney glomerular-capillary-wall function on a chip10.1038/s41551-017-0069 ↗
8. A glomerulus-on-a-chip to recapitulate the human glomerular filtration barrier10.1038/s41467-019-11577-z ↗
9. Flow-enhanced vascularization and maturation of kidney organoids in vitro10.1038/s41592-019-0325-y ↗
10. Creating a kidney organoid-vasculature interaction model using a novel organ-on-chip system10.1038/s41598-022-24945-5 ↗
11. Organoid-on-a-chip model of human ARPKD reveals mechanosensing pathomechanisms for drug discovery10.1126/sciadv.abq0866 ↗
12. Immune-infiltrated kidney organoid-on-chip model for assessing T cell bispecific antibodies10.1073/pnas.2305322120 ↗
13. Human organs-on-chips for disease modelling, drug development and personalized medicine10.1038/s41576-022-00466-9 ↗
14. Advances in predictive in vitro models of drug-induced nephrotoxicity10.1038/s41581-018-0003-9 ↗
15. Generation of functioning nephrons by implanting human pluripotent stem cell-derived kidney progenitors10.1016/j.stemcr.2018.01.008 ↗
16. Renal subcapsular transplantation of PSC-derived kidney organoids induces neo-vasculogenesis and significant glomerular and tubular maturation in vivo10.1016/j.stemcr.2018.01.041 ↗
17. In vivo assessment of size-selective glomerular sieving in transplanted human induced pluripotent stem cell-derived kidney organoids10.1681/ASN.2019060573 ↗
18. Vasculogenesis in kidney organoids upon transplantation10.1038/s41536-022-00237-4 ↗
19. Vascularized organoids on a chip: strategies for engineering organoids with functional vasculature10.1039/D0LC01186J ↗
20. Three-dimensional bioprinting of thick vascularized tissues10.1073/pnas.1521342113 ↗
21. Biomanufacturing of organ-specific tissues with high cellular density and embedded vascular channels10.1126/sciadv.aaw2459 ↗
22. Biomanufacturing human tissues via organ building blocks10.1016/j.stem.2022.04.012 ↗
23. Nephron organoids derived from human pluripotent stem cells model kidney development and injury10.1038/nbt.3392 ↗
24. Generation of nephron progenitor cells and kidney organoids from human pluripotent stem cells10.1038/nprot.2016.170 ↗
25. Vascular wall shear stress: basic principles and methods
26. Measuring the density and viscosity of culture media for optimized computational fluid dynamics analysis of in vitro devices10.1016/j.jmbbm.2021.105024 ↗
27. A computational tool for quantitative analysis of vascular networks10.1371/journal.pone.0027385 ↗
28. Aminocaproic Acid
29. Endothelial cells and VEGF in vascular development10.1038/nature04479 ↗
30. In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract10.1038/nprot.2010.6 ↗
31. Mechanisms of vessel pruning and regression10.1016/j.devcel.2015.06.004 ↗
32. Endothelial signaling during development10.1038/nm0603-661 ↗
33. Molecular determinants of nephron vascular specialization in the kidney10.1038/s41467-019-12872-5 ↗
34. Vascular endothelial cell development and diversity10.1038/s41569-022-00770-1 ↗
35. Diversity within pericytes10.1046/j.1440-1681.2000.03343.x ↗
36. Pericytes: developmental, physiological pathological perspectives, problems and promises10.1016/j.devcel.2011.07.001 ↗
37. Integrin-mediated cell-matrix interaction in physiological and pathological blood vessel formation10.1155/2012/125278 ↗
38. Fluid shear stress threshold regulates angiogenic sprouting10.1073/pnas.1310842111 ↗
39. Transient support from fibroblasts is sufficient to drive functional vascularization in engineered tissues10.1002/adfm.202003777 ↗
40. KLF2 and KLF4 control endothelial identity and vascular integrity10.1172/jci.insight.91700 ↗
41. Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Krüppel-like factor (KLF2)10.1182/blood-2002-01-0046 ↗
42. Connexins in Vascular Physiology and Pathology10.1089/ars.2008.2115 ↗
43. Piezo1, a mechanically activated ion channel, is required for vascular development in mice10.1073/pnas.1409233111 ↗
44. Arterial specification of endothelial cells derived from human induced pluripotent stem cells in a biomimetic flow bioreactor10.1016/j.biomaterials.2015.02.121 ↗
45. Distinct roles of Ephrin-B2 forward and EphB4 reverse signaling in endothelial cells10.1161/01.ATV.0000055440.89758.C2 ↗
46. Draft version of paper data and code of manuscript: body mass and cell size shape the tolerance of fishes to low oxygen in a temperature-dependent manner10.5281/zenodo.6123770 ↗