Culture and analysis of kidney tubuloids and perfused tubuloid cells-on-a-chip.
Adolescent
Adult
Aged
Aged, 80 and over
Animals
Cell Fractionation
Child
Child, Preschool
Electric Impedance
Female
Fluorescent Dyes
/ chemistry
Humans
Infant
Kidney Tubules
/ growth & development
Lab-On-A-Chip Devices
Male
Membrane Transport Proteins
/ metabolism
Microfluidics
Middle Aged
Organoids
/ growth & development
Perfusion
Rats
Tissue Culture Techniques
/ methods
Young Adult
Journal
Nature protocols
ISSN: 1750-2799
Titre abrégé: Nat Protoc
Pays: England
ID NLM: 101284307
Informations de publication
Date de publication:
04 2021
04 2021
Historique:
received:
07
03
2020
accepted:
04
12
2020
pubmed:
7
3
2021
medline:
5
5
2021
entrez:
6
3
2021
Statut:
ppublish
Résumé
Advanced in vitro kidney models are of great importance to the study of renal physiology and disease. Kidney tubuloids can be established from primary cells derived from adult kidney tissue or urine. Tubuloids are three-dimensional multicellular structures that recapitulate tubular function and have been used to study infectious, malignant, metabolic, and genetic diseases. For tubuloids to more closely represent the in vivo kidney, they can be integrated into an organ-on-a-chip system that has a more physiological tubular architecture and allows flow and interaction with vasculature or epithelial and mesenchymal cells from other organs. Here, we describe a detailed protocol for establishing tubuloid cultures from tissue and urine (1-3 weeks), as well as for generating and characterizing tubuloid cell-derived three-dimensional tubular structures in a perfused microfluidic multi-chip platform (7 d). The combination of the two systems yields a powerful in vitro tool that better recapitulates the complexity of the kidney tubule with donor-specific properties.
Identifiants
pubmed: 33674788
doi: 10.1038/s41596-020-00479-w
pii: 10.1038/s41596-020-00479-w
doi:
Substances chimiques
Fluorescent Dyes
0
Membrane Transport Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2023-2050Références
Saran, R., Robinson, B., Abbott, K. C. & Agodoa, L. Y. US Renal Data System 2018 Annual Data Report: epidemiology of kidney disease in the United States. Am. J. Kidney Dis. 73, A7–A8 (2019).
pubmed: 30798791
pmcid: 6620109
doi: 10.1053/j.ajkd.2019.01.001
Clevers, H. & Watt, F. M. Defining adult stem cells by function, not by phenotype. Annu. Rev. Biochem. 87, 1015–1027 (2018).
pubmed: 29494240
doi: 10.1146/annurev-biochem-062917-012341
Post, Y. & Clevers, H. Defining adult stem cell function at its simplest: the ability to replace lost cells through mitosis. Cell Stem Cell 25, 174–183 (2019).
pubmed: 31374197
doi: 10.1016/j.stem.2019.07.002
Clevers, H. Modeling development and disease with organoids. Cell 165, 1586–1597 (2016).
pubmed: 27315476
doi: 10.1016/j.cell.2016.05.082
Rossi, G., Manfrin, A. & Lutolf, M. P. Progress and potential in organoid research. Nat. Rev. Genet. 19, 671–687 (2018).
pubmed: 30228295
doi: 10.1038/s41576-018-0051-9
Lancaster, M. A. & Huch, M. Disease modelling in human organoids. Dis. Model. Mech. 12, dmm03934 (2019).
Yousef Yengej, F. A., Jansen, J., Rookmaaker, M. B., Verhaar, M. C. & Clevers, H. Kidney organoids and tubuloids. Cells 9, 1–20 (2020).
doi: 10.3390/cells9061326
Sato, T. et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262–265 (2009).
pubmed: 19329995
doi: 10.1038/nature07935
Schutgens, F. et al. Tubuloids derived from human adult kidney and urine for personalized disease modeling. Nat. Biotechnol. 37, 303–313 (2019).
pubmed: 30833775
doi: 10.1038/s41587-019-0048-8
Little, M., Georgas, K., Pennisi, D. & Wilkinson, L. Kidney development: two tales of tubulogenesis. Curr. Top. Dev. Biol. 90, 193–229 (2010).
pubmed: 20691850
doi: 10.1016/S0070-2153(10)90005-7
Little, M. H., Kumar, S. V. & Forbes, T. Recapitulating kidney development: progress and challenges. Semin. Cell Dev. Biol. 91, 153–168 (2019).
pubmed: 30184476
doi: 10.1016/j.semcdb.2018.08.015
Barker, N. et al. Lgr5
pubmed: 22999937
doi: 10.1016/j.celrep.2012.08.018
Brown, D., Lee, R. & Bonventre, J. V. Redistribution of villin to proximal tubule basolateral membranes after ischemia and reperfusion. Am. J. Physiol. 273, 1003–1012 (1997).
Soo, J. Y. C., Jansen, J., Masereeuw, R. & Little, M. H. Advances in predictive in vitro models of drug-induced nephrotoxicity. Nat. Rev. Nephrol. 14, 378–393 (2018).
pubmed: 29626199
pmcid: 6013592
doi: 10.1038/s41581-018-0003-9
Jouan, E., Le Vee, M., Denizot, C., Da Violante, G. & Fardel, O. The mitochondrial fluorescent dye rhodamine 123 is a high-affinity substrate for organic cation transporters (OCTs) 1 and 2. Fundam. Clin. Pharmacol. 28, 65–77 (2014).
pubmed: 22913740
doi: 10.1111/j.1472-8206.2012.01071.x
Calandrini, C. et al. An organoid biobank for childhood kidney cancers that captures disease and tissue heterogeneity. Nat. Commun. 11, 1310 (2020).
Jamalpoor, A. et al. Cysteamine-bicalutamide combination treatment restores alpha-ketoglutarate and corrects proximal tubule phenotype in cystinosis. Preprint at bioRxiv https://doi.org/10.1101/2020.02.10.941799 (2020).
Park, S. E., Georgescu, A. & Huh, D. Organoids-on-a-chip. Science 364, 960–965 (2019).
pubmed: 31171693
pmcid: 7764943
doi: 10.1126/science.aaw7894
Yu, F., Hunziker, W. & Choudhury, D. Engineering microfluidic organoid-on-a-chip platforms. Micromachines 10, 1–12 (2019).
doi: 10.3390/mi10030165
Moisan, A. et al. Mechanistic investigations of diarrhea toxicity induced by Anti-HER2/3 combination therapy. Mol. Cancer Ther. 17, 1464–1474 (2018).
pubmed: 29654069
doi: 10.1158/1535-7163.MCT-17-1268
Petrosyan, A. et al. A glomerulus-on-a-chip to recapitulate the human glomerular filtration barrier. Nat. Commun. 10, 3656 (2019).
pubmed: 31409793
pmcid: 6692336
doi: 10.1038/s41467-019-11577-z
van Duinen, V. et al. Perfused 3D angiogenic sprouting in a high-throughput in vitro platform. Angiogenesis 22, 157–165 (2019).
pubmed: 30171498
doi: 10.1007/s10456-018-9647-0
Wevers, N. R. et al. A perfused human blood-brain barrier on-a-chip for high-throughput assessment of barrier function and antibody transport. Fluids Barriers CNS 15, 23 (2018).
pubmed: 30165870
pmcid: 6117964
doi: 10.1186/s12987-018-0108-3
Yetkin-Arik, B. et al. Endothelial tip cells in vitro are less glycolytic and have a more flexible response to metabolic stress than non-tip cells. Sci. Rep. 9, 1–17 (2019).
doi: 10.1038/s41598-019-46503-2
Gijzen, L. et al. An intestine-on-a-chip model of plug-and-play modularity to study inflammatory processes. SLAS Technol. 25, 585–597 (2020).
pubmed: 32576063
pmcid: 7684793
doi: 10.1177/2472630320924999
Vormann, M. K. et al. Nephrotoxicity and kidney transport assessment on 3D perfused proximal tubules. AAPS J. 20, 1–11 (2018).
doi: 10.1208/s12248-018-0248-z
Kramer, B. et al. Interstitial flow recapitulates gemcitabine chemoresistance in a 3D microfluidic pancreatic ductal adenocarcinoma model by induction of multidrug resistance proteins. Int. J. Mol. Sci. 20, 4647 (2019).
van Duinen, V. et al. Robust and scalable angiogenesis assay of perfused 3D human iPSC-derived endothelium for anti-angiogenic drug screening. Int. J. Mol. Sci. 21, 4804 (2020).
pmcid: 7370283
doi: 10.3390/ijms21134804
Naumovska, E. et al. Direct on-chip differentiation of intestinal tubules from induced pluripotent stem cells. Int. J. Mol. Sci. 21, 1–15 (2020).
doi: 10.3390/ijms21144964
Post, Y. et al. Snake venom gland organoids. Cell 180, 233–247.e21 (2020).
pubmed: 31978343
doi: 10.1016/j.cell.2019.11.038
Trietsch, S. J. et al. Membrane-free culture and real-time barrier integrity assessment of perfused intestinal epithelium tubes. Nat. Commun. 8, 262 (2017).
pubmed: 28811479
pmcid: 5557798
doi: 10.1038/s41467-017-00259-3
Poussin, C. 3D human microvessel-on-a-chip model for studying monocyte-to-endothelium adhesion under flow—application in systems toxicology. ALTEX 37, 47–63 (2019).
pubmed: 31445503
Vriend, J. et al. Flow stimulates drug transport in a human kidney proximal tubule-on-a-chip independent of primary cilia. Biochim. Biophys. Acta Gen. Subj. 1864, 129433 (2020).
Vulto, P. et al. Phaseguides: a paradigm shift in microfluidic priming and emptying. Lab Chip 11, 1596–1602 (2011).
pubmed: 21394334
doi: 10.1039/c0lc00643b
Van der Hauwaert, C. et al. Expression profiles of genes involved in xenobiotic metabolism and disposition in human renal tissues and renal cell models. Toxicol. Appl. Pharmacol. 279, 409–418 (2014).
pubmed: 25036895
doi: 10.1016/j.taap.2014.07.007
Wilmer, M. J. et al. Kidney-on-a-chip technology for drug-induced nephrotoxicity screening. Trends Biotechnol. 34, 156–170 (2015).
pubmed: 26708346
doi: 10.1016/j.tibtech.2015.11.001
Takasato, M. et al. Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis. Nature 526, 564–568 (2015).
pubmed: 26444236
doi: 10.1038/nature15695
Little, M. H. & Combes, A. N. Kidney organoids: accurate models or fortunate accidents. Genes Dev. 33, 1319–1345 (2019).
pubmed: 31575677
pmcid: 6771389
doi: 10.1101/gad.329573.119
Kumar, S. V. et al. Kidney micro-organoids in suspension culture as a scalable source of human pluripotent stem cell-derived kidney cells. Development 146, dev172361 (2019).
Wu, H. et al. Comparative analysis and refinement of human psc-derived kidney organoid differentiation with single-cell transcriptomics. Cell Stem Cell 23, 869–881.e8 (2018).
pubmed: 30449713
pmcid: 6324730
doi: 10.1016/j.stem.2018.10.010
Faria, J., Ahmed, S., Gerritsen, K. G. F., Mihaila, S. M. & Masereeuw, R. Kidney-based in vitro models for drug-induced toxicity testing. Arch. Toxicol. 93, 3397–3418 (2019).
pubmed: 31664498
doi: 10.1007/s00204-019-02598-0
Homan, K. A. et al. Flow-enhanced vascularization and maturation of kidney organoids in vitro. Nat. Methods 16, 255–262 (2019).
pubmed: 30742039
pmcid: 6488032
doi: 10.1038/s41592-019-0325-y
Jang, K.-J. et al. Human kidney proximal tubule-on-a-chip for drug transport and nephrotoxicity assessment. Integr. Biol. 5, 1119 (2013).
doi: 10.1039/c3ib40049b
Kolesky, D. B. et al. 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv. Mater. 26, 3124–3130 (2014).
pubmed: 24550124
doi: 10.1002/adma.201305506
Chung, H. H., Mireles, M., Kwarta, B. J. & Gaborski, T. R. Use of porous membranes in tissue barrier and co-culture models. Lab Chip 18, 1671–1689 (2018).
pubmed: 29845145
pmcid: 5997570
doi: 10.1039/C7LC01248A
Ashammakhi, N., Wesseling-Perry, K., Hasan, A., Elkhammas, E. & Zhang, Y. S. Kidney-on-a-chip: untapped opportunities. Kidney Int. 94, 1073–1086 (2018).
pubmed: 30366681
pmcid: 6408139
doi: 10.1016/j.kint.2018.06.034
Weber, E. J. et al. Development of a microphysiological model of human kidney proximal tubule function. Kidney Int. 90, 627–637 (2016).
pubmed: 27521113
pmcid: 4987715
doi: 10.1016/j.kint.2016.06.011
Zanetti, F. Kidney-on-a-chip. in Organ-on-a-Chip (eds Hoeng, J., Bovard, D. & Peitch, M. C.), Chap. 7 (Elsevier, 2019).
Musah, S. et al. Mature induced-pluripotent-stem-cell-derived human podocytes reconstitute kidney glomerular-capillary-wall function on a chip. Nat. Biomed. Eng. 176, 139–148 (2017).
Yin, L. et al. Efficient drug screening and nephrotoxicity assessment on co-culture microfluidic kidney chip. Sci. Rep. 10, 1–11 (2020).
Toepke, M. W. & Beebe, D. J. PDMS absorption of small molecules and consequences in microfluidic applications. Lab Chip 6, 1484–1486 (2006).
pubmed: 17203151
doi: 10.1039/b612140c
Ferenbach, D. A. & Bonventre, J. V. Acute kidney injury and chronic kidney disease: from the laboratory to the clinic. Nephrol. Ther. 12, S41–S48 (2016).
pubmed: 26972097
pmcid: 5475438
doi: 10.1016/j.nephro.2016.02.005
Huch, M. et al. Long-term culture of genome-stable bipotent stem cells from adult human liver. Cell 160, 299–312 (2015).
pubmed: 25533785
pmcid: 4313365
doi: 10.1016/j.cell.2014.11.050
Albadine, R. et al. PAX8 (+)/p63 (−) immunostaining pattern in renal collecting duct carcinoma (CDC). Am. J. Surg. Pathol. 34, 965–969 (2010).
pubmed: 20463571
pmcid: 3505675
doi: 10.1097/PAS.0b013e3181dc5e8a
Saito, K. et al. Hydronephrosis in the early stage of pregnancy after renal transplantation. Int. J. Urol. 13, 809–810 (2006).
pubmed: 16834667
doi: 10.1111/j.1442-2042.2006.01409.x
Cai, Z., Xin, J., Pollock, D. M. & Pollock, J. S. Shear stress-mediated NO production in inner medullary collecting duct cells. Am. J. Physiol. Ren. Physiol. 279, F270–F274 (2000).
doi: 10.1152/ajprenal.2000.279.2.F270