Generation of proximal tubule-enhanced kidney organoids from human pluripotent stem cells

Jessica M. Vanslambrouck, Ker Sin Tan, Sophia Mah, Melissa H. Little

Published: 2023-09-27 DOI: 10.1038/s41596-023-00880-1

human pluripotent stem cells

kidney organoids

proximal tubules

nephron functionality

transporters expression

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Freedman, B. S. et al. Modelling kidney disease with CRISPR-mutant kidney organoids derived from human pluripotent epiblast spheroids. Nat. Commun. 6, 8715 (2015).
Morizane, R. et al. Nephron organoids derived from human pluripotent stem cells model kidney development and injury. Nat. Biotechnol. 33, 1193–1200 (2015).
Taguchi, A. & Nishinakamura, R. Higher-order kidney organogenesis from pluripotent stem cells. Cell Stem Cell 21, 730–746 e736 (2017).
Takasato, M. et al. Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis. Nature 526, 564–568 (2015).
Toyohara, T. et al. Cell therapy using human induced pluripotent stem cell-derived renal progenitors ameliorates acute kidney injury in mice. Stem Cells Transl. Med. 4, 980–992 (2015).
Vanslambrouck, J. M. et al. Enhanced metanephric specification to functional proximal tubule enables toxicity screening and infectious disease modelling in kidney organoids. Nat. Commun. 13, 5943 (2022).
Howden, S. E., Vanslambrouck, J. M., Wilson, S. B., Tan, K. S. & Little, M. H. Reporter-based fate mapping in human kidney organoids confirms nephron lineage relationships and reveals synchronous nephron formation. EMBO Rep. http://doi.org/10.15252/embr.201847483 (2019).
Takasato, M. et al. Directing human embryonic stem cell differentiation towards a renal lineage generates a self-organizing kidney. Nat. Cell Biol. 16, 118–126 (2014).
Takasato, M., Er, P. X., Chiu, H. S. & Little, M. H. Generation of kidney organoids from human pluripotent stem cells. Nat. Protoc. 11, 1681–1692 (2016).
Howden, S. E. & Little, M. H. Generating kidney organoids from human pluripotent stem cells using defined conditions. Methods Mol. Biol. 2155, 183–192 (2020).
Tanigawa, S., Taguchi, A., Sharma, N., Perantoni, A. O. & Nishinakamura, R. Selective in vitro propagation of nephron progenitors derived from embryos and pluripotent stem cells. Cell Rep. 15, 801–813 (2016).
de Bakker, B. S., van den Hoff, M. J. B., Vize, P. D. & Oostra, R. J. The pronephros; a fresh perspective. Integr. Comp. Biol. 59, 29–47 (2019).
Georgas, K. M., Chiu, H. S., Lesieur, E., Rumballe, B. A. & Little, M. H. Expression of metanephric nephron-patterning genes in differentiating mesonephric tubules. Dev. Dyn. 240, 1600–1612 (2011).
Mugford, J. W., Sipila, P., Kobayashi, A., Behringer, R. R. & McMahon, A. P. Hoxd11 specifies a program of metanephric kidney development within the intermediate mesoderm of the mouse embryo. Dev. Biol. 319, 396–405 (2008).
Tiedemann, K., Welling, L. W. & Basto, P. Structural and functional comparison of mesonephric and metanephric proximal tubules. Pediatr. Nephrol. 1, 297–305 (1987).
Dressler, G. R. Advances in early kidney specification, development and patterning. Development 136, 3863–3874 (2009).
Brown, A. C. et al. Role for compartmentalization in nephron progenitor differentiation. Proc. Natl Acad. Sci. USA 110, 4640–4645 (2013).
Brown, A. C., Muthukrishnan, S. D. & Oxburgh, L. A synthetic niche for nephron progenitor cells. Dev. Cell 34, 229–241 (2015).
Li, Z. et al. 3D culture supports long-term expansion of mouse and human nephrogenic progenitors. Cell Stem Cell 19, 516–529 (2016).
Tanigawa, S., Sharma, N., Hall, M. D., Nishinakamura, R. & Perantoni, A. O. Preferential propagation of competent SIX2+ nephronic progenitors by LIF/ROCKi treatment of the metanephric mesenchyme. Stem Cell Rep. 5, 435–447 (2015).
Chung, E., Deacon, P. & Park, J. S. Notch is required for the formation of all nephron segments and primes nephron progenitors for differentiation. Development 144, 4530–4539 (2017).
Duvall, K. et al. Revisiting the role of Notch in nephron segmentation confirms a role for proximal fate selection during mouse and human nephrogenesis. Development http://doi.org/10.1242/dev.200446 (2022).
Surendran, K. et al. The contribution of Notch1 to nephron segmentation in the developing kidney is revealed in a sensitized Notch2 background and can be augmented by reducing Mint dosage. Dev. Biol. 337, 386–395 (2010).
Ryan, M. J. et al. HK-2: an immortalized proximal tubule epithelial cell line from normal adult human kidney. Kidney Int. 45, 48–57 (1994).
Racusen, L. C. et al. Cell lines with extended in vitro growth potential from human renal proximal tubule: characterization, response to inducers, and comparison with established cell lines. J. Lab. Clin. Med. 129, 318–329 (1997).
Orosz, D. E. et al. Growth, immortalization, and differentiation potential of normal adult human proximal tubule cells. Vitr. Cell Dev. Biol. Anim. 40, 22–34 (2004).
Wieser, M. et al. hTERT alone immortalizes epithelial cells of renal proximal tubules without changing their functional characteristics. Am. J. Physiol. Ren. Physiol. 295, F1365–F1375 (2008).
Chandrasekaran, V. et al. Generation and characterization of iPSC-derived renal proximal tubule-like cells with extended stability. Sci. Rep. 11, 11575 (2021).
Kaminski, M. M. et al. Direct reprogramming of fibroblasts into renal tubular epithelial cells by defined transcription factors. Nat. Cell Biol. 18, 1269–1280 (2016).
Kandasamy, K. et al. Prediction of drug-induced nephrotoxicity and injury mechanisms with human induced pluripotent stem cell-derived cells and machine learning methods. Sci. Rep. 5, 12337 (2015).
Narayanan, K. et al. Human embryonic stem cells differentiate into functional renal proximal tubular-like cells. Kidney Int. 83, 593–603 (2013).
Heussner, A. H. & Dietrich, D. R. Primary porcine proximal tubular cells as an alternative to human primary renal cells in vitro: an initial characterization. BMC Cell Biol. 14, 55 (2013).
Jenkinson, S. E. et al. The limitations of renal epithelial cell line HK-2 as a model of drug transporter expression and function in the proximal tubule. Pflug. Arch. 464, 601–611 (2012).
Khundmiri, S. J., Chen, L., Lederer, E. D., Yang, C. R. & Knepper, M. A. Transcriptomes of major proximal tubule cell culture models. J. Am. Soc. Nephrol. 32, 86–97 (2021).
Duan, Y. et al. Shear-induced reorganization of renal proximal tubule cell actin cytoskeleton and apical junctional complexes. Proc. Natl Acad. Sci. USA 105, 11418–11423 (2008).
Frohlich, E. M., Zhang, X. & Charest, J. L. The use of controlled surface topography and flow-induced shear stress to influence renal epithelial cell function. Integr. Biol. 4, 75–83 (2012).
Jang, K. K. et al. Variable susceptibility of intestinal organoid-derived monolayers to SARS-CoV-2 infection. PLoS Biol. 20, e3001592 (2022).
Ng, C. P., Zhuang, Y., Lin, A. W. H. & Teo, J. C. M. A fibrin-based tissue-engineered renal proximal tubule for bioartificial kidney devices: development, characterization and in vitro transport study. Int. J. Tissue Eng. 2013, 319476 (2013).
Secker, P. F., Luks, L., Schlichenmaier, N. & Dietrich, D. R. RPTEC/TERT1 cells form highly differentiated tubules when cultured in a 3D matrix. ALTEX 35, 223–234 (2018).
Xu, Y. et al. Adult human kidney organoids originate from CD24+ cells and represent an advanced model for adult polycystic kidney disease. Nat. Genet. 54, 1690–1701 (2022).
Aceves, J. O. et al. 3D proximal tubule-on-chip model derived from kidney organoids with improved drug uptake. Sci. Rep. 12, 14997 (2022).
Homan, K. A. et al. Bioprinting of 3D convoluted renal proximal tubules on perfusable chips. Sci. Rep. 6, 34845 (2016).
Schutgens, F. et al. Tubuloids derived from human adult kidney and urine for personalized disease modeling. Nat. Biotechnol. 37, 303–313 (2019).
Weber, E. J. et al. Development of a microphysiological model of human kidney proximal tubule function. Kidney Int. 90, 627–637 (2016).
Lin, N. Y. C. et al. Renal reabsorption in 3D vascularized proximal tubule models. Proc. Natl Acad. Sci. USA 116, 5399–5404 (2019).
Kumar, S. V. et al. Kidney micro-organoids in suspension culture as a scalable source of human pluripotent stem cell-derived kidney cells. Development http://doi.org/10.1242/dev.172361 (2019).
Lam, A. Q. et al. Rapid and efficient differentiation of human pluripotent stem cells into intermediate mesoderm that forms tubules expressing kidney proximal tubular markers. J. Am. Soc. Nephrol. 25, 1211–1225 (2014).
Taguchi, A. et al. Redefining the in vivo origin of metanephric nephron progenitors enables generation of complex kidney structures from pluripotent stem cells. Cell Stem Cell 14, 53–67 (2014).
Wilson, S. B. et al. DevKidCC allows for robust classification and direct comparisons of kidney organoid datasets. Genome Med. 14, 19 (2022).
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 e868 (2018).
Combes, A. N., Zappia, L., Er, P. X., Oshlack, A. & Little, M. H. Single-cell analysis reveals congruence between kidney organoids and human fetal kidney. Genome Med. 11, 3 (2019).
Subramanian, A. et al. Single cell census of human kidney organoids shows reproducibility and diminished off-target cells after transplantation. Nat. Commun. 10, 5462 (2019).
Das, A. et al. Stromal-epithelial crosstalk regulates kidney progenitor cell differentiation. Nat. Cell Biol. 15, 1035–1044 (2013).
England, A. R. et al. Identification and characterization of cellular heterogeneity within the developing renal interstitium. Development http://doi.org/10.1242/dev.190108 (2020).
Lindstrom, N. O. et al. Integrated beta-catenin, BMP, PTEN, and Notch signalling patterns the nephron. eLife 3, e04000 (2015).
Nielsen, R., Christensen, E. I. & Birn, H. Megalin and cubilin in proximal tubule protein reabsorption: from experimental models to human disease. Kidney Int. 89, 58–67 (2016).
Yasujima, T., Ohta, K. Y., Inoue, K., Ishimaru, M. & Yuasa, H. Evaluation of 4′,6-diamidino-2-phenylindole as a fluorescent probe substrate for rapid assays of the functionality of human multidrug and toxin extrusion proteins. Drug Metab. Dispos. 38, 715–721 (2010).
Vanslambrouck, J. M. et al. A toolbox to characterize human induced pluripotent stem cell-derived kidney cell types and organoids. J. Am. Soc. Nephrol. 30, 1811–1823 (2019).
Carcamo-Orive, I. et al. Analysis of transcriptional variability in a large human iPSC library reveals genetic and non-genetic determinants of heterogeneity. Cell Stem Cell 20, 518–532 e519 (2017).
Volpato, V. & Webber, C. Addressing variability in iPSC-derived models of human disease: guidelines to promote reproducibility. Dis. Model Mech. http://doi.org/10.1242/dmm.042317 (2020).

Generation of proximal tubule-enhanced kidney organoids from human pluripotent stem cells

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