396
Views
1
CrossRef citations to date
0
Altmetric
Review

Glomerulus-on-a-Chip: Current Insights and Future Potential Towards Recapitulating Selectively Permeable Filtration Systems

, ORCID Icon, , &
Pages 85-101 | Published online: 10 Mar 2022

References

  • Levin A, Tonelli M, Bonventre J, et al. Global kidney health 2017 and beyond: a roadmap for closing gaps in care, research, and policy. Lancet Lond Engl. 2017;390:1888–1917. doi:10.1016/S0140-6736(17)30788-2
  • Levin A, Hemmelgarn B, Culleton B, et al. Guidelines for the management of chronic kidney disease. Can Med Assoc J. 2008;179:1154–1162. doi:10.1503/cmaj.080351
  • Cheung AK, Chang TI, Cushman WC, et al. Executive summary of the KDIGO 2021 clinical practice guideline for the management of blood pressure in chronic kidney disease. Kidney Int. 2021;99:559–569. doi:10.1016/j.kint.2020.10.026
  • Jacobs–Cachá C, Vergara A, García–Carro C, et al. Challenges in primary focal segmental glomerulosclerosis diagnosis: from the diagnostic algorithm to novel biomarkers. Clin Kidney J. 2021;14:482–491. doi:10.1093/ckj/sfaa110
  • Jang HM, Baek HS, Park SH, et al. Clinical characteristics and long-term prognosis of Alport syndrome: a retrospective single-center study. Child Kidney Dis. 2020;24:91–97. doi:10.3339/jkspn.2020.24.2.91
  • Ruggenenti P, Ruggiero B, Cravedi P, et al. Rituximab in steroid-dependent or frequently relapsing idiopathic nephrotic syndrome. J Am Soc Nephrol. 2014;25:850–863. doi:10.1681/ASN.2013030251
  • Bagga A, Sinha A. Individualizing treatment of steroid-resistant nephrotic syndrome: registries to the fore. Clin J Am Soc Nephrol. 2020;15:920–922. doi:10.2215/CJN.08080520
  • de Jong PE, Curhan GC. Screening, monitoring, and treatment of albuminuria: public health perspectives. J Am Soc Nephrol. 2006;17:2120–2126. doi:10.1681/ASN.2006010097
  • Abbate M, Zoja C, Remuzzi G. How does proteinuria cause progressive renal damage? J Am Soc Nephrol. 2006;17:2974–2984. doi:10.1681/ASN.2006040377
  • Gaitonde DY, Cook DL, Rivera IM. Chronic kidney disease: detection and evaluation. Am Fam Physician. 2017;96:776–783.
  • Shankland SJ, Pippin JW, Reiser J, Mundel P. Podocytes in culture: past, present, and future. Kidney Int. 2007;72:26–36. doi:10.1038/sj.ki.5002291
  • Krtil J, Pláteník J, Kazderová M, Tesař V, Zima T. Culture methods of glomerular podocytes. Kidney Blood Press Res. 2007;30:162–174. doi:10.1159/000102520
  • Lal MA, Young KW, Andag U. Targeting the podocyte to treat glomerular kidney disease. Drug Discov Today. 2015;20:1228–1234. doi:10.1016/j.drudis.2015.06.003
  • Lee HW, Khan SQ, Faridi MH, et al. A podocyte-based automated screening assay identifies protective small molecules. J Am Soc Nephrol. 2015;26:2741–2752. doi:10.1681/ASN.2014090859
  • Jefferson JA, Pippin JW, Shankland SJ. Experimental models of membranous nephropathy. Drug Discov Today Dis Models. 2010;7:27–33. doi:10.1016/j.ddmod.2010.11.001
  • Foster MH. Optimizing the translational value of animal models of glomerulonephritis: insights from recent murine prototypes. Am J Physiol-Ren Physiol. 2016;311:F487–F495. doi:10.1152/ajprenal.00275.2016
  • Cianciolo RE, Jennette JC. Glomerulonephritis in animal models and human medicine: discovery, pathogenesis, and diagnostics. Toxicol Pathol. 2018;46:898–903. doi:10.1177/0192623318800714
  • Bomback AS, Appel GB, Gipson DS, et al. Improving clinical trials for anticomplement therapies in complement-mediated glomerulopathies: report of a scientific workshop sponsored by the National Kidney Foundation. Am J Kidney Dis. 2021. doi:10.1053/j.ajkd.2021.07.025
  • Li M, Corbelli A, Watanabe S, et al. Three-dimensional podocyte–endothelial cell co-cultures: assembly, validation, and application to drug testing and intercellular signaling studies. Eur J Pharm Sci. 2016;86:1–12. doi:10.1016/j.ejps.2016.02.013
  • Li M, Alfieri CM, Morello W, et al. Assessment of increased glomerular permeability associated with recurrent focal segmental glomerulosclerosis using an in vitro model of the glomerular filtration barrier. J Nephrol. 2020;33:747–755. doi:10.1007/s40620-019-00683-2
  • Yang SH, Choi JW, Huh D, et al. Roles of fluid shear stress and retinoic acid in the differentiation of primary cultured human podocytes. Exp Cell Res. 2017;354:48–56. doi:10.1016/j.yexcr.2017.03.026
  • Van Norman GA. Limitations of animal studies for predicting toxicity in clinical trials. JACC Basic Transl Sci. 2019;4:845–854. doi:10.1016/j.jacbts.2019.10.008
  • Ebefors K, Lassén E, Anandakrishnan N, Azeloglu EU, Daehn IS. Modeling the glomerular filtration barrier and intercellular crosstalk. Front Physiol. 2021;12. doi:10.3389/fphys.2021.689083
  • Groff K, Bachli E, Lansdowne M, Capaldo T. Review of evidence of environmental impacts of animal research and testing. Environments. 2014;1:14–30. doi:10.3390/environments1010014
  • Morizane R, Lam AQ, Freedman BS, Kishi S, Valerius MT, Bonventre JV. Nephron organoids derived from human pluripotent stem cells model kidney development and injury. Nat Biotechnol. 2015;33:1193–1200. doi:10.1038/nbt.3392
  • Takasato M, Er PX, Chiu HS, Little MH. Generation of kidney organoids from human pluripotent stem cells. Nat Protoc. 2016;11:1681–1692. doi:10.1038/nprot.2016.098
  • Taguchi A, Nishinakamura R. Higher-order kidney organogenesis from pluripotent stem cells. Cell Stem Cell. 2017;21:730–746.e6. doi:10.1016/j.stem.2017.10.011
  • Low JH, Li P, Chew EGY, et al. Generation of human PSC-derived kidney organoids with patterned nephron segments and a de novo vascular network. Cell Stem Cell. 2019;25:373–387.e9. doi:10.1016/j.stem.2019.06.009
  • Uchimura K, Wu H, Yoshimura Y, Humphreys BD. Human pluripotent stem cell-derived kidney organoids with improved collecting duct maturation and injury modeling. Cell Rep. 2020;33:108514. doi:10.1016/j.celrep.2020.108514
  • Tsujimoto H, Kasahara T, Sueta S, et al. A modular differentiation system maps multiple human kidney lineages from pluripotent stem cells. Cell Rep. 2020;31:107476. doi:10.1016/j.celrep.2020.03.040
  • Huh D, Matthews BD, Mammoto A, Montoya-Zavala M, Hsin HY, Ingber DE. Reconstituting organ-level lung functions on a chip. Science. 2010;328:1662–1668. doi:10.1126/science.1188302
  • Pauty J, Usuba R, Cheng IG, et al. A vascular endothelial growth factor-dependent sprouting angiogenesis assay based on an in vitro human blood vessel model for the study of anti-angiogenic drugs. EBioMedicine. 2018;27:225–236. doi:10.1016/j.ebiom.2017.12.014
  • Kimura H, Sakai Y, Fujii T. Organ/body-on-a-chip based on microfluidic technology for drug discovery. Drug Metab Pharmacokinet. 2018;33:43–48. doi:10.1016/j.dmpk.2017.11.003
  • Deng J, Wei W, Chen Z, et al. Engineered liver-on-a-chip platform to mimic liver functions and its biomedical applications: a review. Micromachines. 2019;10:676. doi:10.3390/mi10100676
  • Bang S, Jeong S, Choi N, Kim HN. Brain-on-a-chip: a history of development and future perspective. Biomicrofluidics. 2019;13:051301. doi:10.1063/1.5120555
  • Cho KW, Lee WH, Kim BS, Kim DH. Sensors in heart-on-a-chip: a review on recent progress. Talanta. 2020;219:121269. doi:10.1016/j.talanta.2020.121269
  • Donkers JM, Eslami Amirabadi H, van de Steeg E. Intestine-on-a-chip: next level in vitro research model of the human intestine. Curr Opin Toxicol. 2021;25:6–14. doi:10.1016/j.cotox.2020.11.002
  • Shinohara M, Arakawa H, Oda Y, et al. Co-culture with hiPS-derived intestinal cells enhanced human hepatocyte functions in a pneumatic-pressure-driven two-organ microphysiological system. Sci Rep. 2021;11:5437. doi:10.1038/s41598-021-84861-y
  • Sharmin S, Taguchi A, Kaku Y, et al. Human induced pluripotent stem cell–derived podocytes mature into vascularized glomeruli upon experimental transplantation. J Am Soc Nephrol. 2016;27:1778–1791. doi:10.1681/ASN.2015010096
  • Zhou M, Zhang X, Wen X, et al. Development of a functional glomerulus at the organ level on a chip to mimic hypertensive nephropathy. Sci Rep. 2016;6:31771. doi:10.1038/srep31771
  • Wang L, Tao T, Su W, Yu H, Yu Y, Qin J. A disease model of diabetic nephropathy in a glomerulus-on-a-chip microdevice. Lab Chip. 2017;17:1749–1760. doi:10.1039/C7LC00134G
  • Musah S, Mammoto A, Ferrante TC, et al. Mature induced-pluripotent-stem-cell-derived human podocytes reconstitute kidney glomerular-capillary-wall function on a chip. Nat Biomed Eng. 2017;1:0069. doi:10.1038/s41551-017-0069
  • Petrosyan A, Cravedi P, Villani V, et al. A glomerulus-on-a-chip to recapitulate the human glomerular filtration barrier. Nat Commun. 2019;10:3656. doi:10.1038/s41467-019-11577-z
  • Iampietro C, Bellucci L, Arcolino FO, et al. Molecular and functional characterization of urine‐derived podocytes from patients with Alport syndrome. J Pathol. 2020;252:88–100. doi:10.1002/path.5496
  • Xie R, Korolj A, Liu C, et al. h-FIBER: microfluidic topographical hollow fiber for studies of glomerular filtration barrier. ACS Cent Sci. 2020;6:903–912. doi:10.1021/acscentsci.9b01097
  • Roye Y, Bhattacharya R, Mou X, Zhou Y, Burt MA, Musah S. A personalized glomerulus chip engineered from stem cell-derived epithelium and vascular endothelium. Micromachines. 2021;12:967. doi:10.3390/mi12080967
  • Kanwar YS, Venkatachalam MA. Ultrastructure of glomerulus and juxtaglomerular apparatus. Compr Physiol. 2011:3–40. doi:10.1002/cphy.cp080101
  • Scott RP, Quaggin SE. The cell biology of renal filtration. J Cell Biol. 2015;209:199–210. doi:10.1083/jcb.201410017
  • Satchell SC, Braet F. Glomerular endothelial cell fenestrations: an integral component of the glomerular filtration barrier. Am J Physiol - Ren Physiol. 2009;296:F947–F956. doi:10.1152/ajprenal.90601.2008
  • Kawasaki Y, Hosoyamada Y, Miyaki T, et al. Three-dimensional architecture of glomerular endothelial cells revealed by FIB-SEM tomography. Front Cell Dev Biol. 2021;9. doi:10.3389/fcell.2021.653472
  • Miner JH. Renal basement membrane components. Kidney Int. 1999;56:2016–2024. doi:10.1046/j.1523-1755.1999.00785.x
  • Lennon R, Randles MJ, Humphries MJ. The importance of podocyte adhesion for a healthy glomerulus. Front Endocrinol. 2014;5. doi:10.3389/fendo.2014.00160
  • Ichimura K, Kakuta S, Kawasaki Y, et al. Morphological process of podocyte development revealed by block-face scanning electron microscopy. J Cell Sci. 2016:jcs.187815. doi:10.1242/jcs.187815
  • Miyaki T, Kawasaki Y, Hosoyamada Y, et al. Three-dimensional imaging of podocyte ultrastructure using FE-SEM and FIB-SEM tomography. Cell Tissue Res. 2020;379:245–254. doi:10.1007/s00441-019-03118-3
  • Ruotsalainen V, Ljungberg P, Wartiovaara J, et al. Nephrin is specifically located at the slit diaphragm of glomerular podocytes. Proc Natl Acad Sci U S A. 1999;96:7962–7967. doi:10.1073/pnas.96.14.7962
  • Unnersjö-Jess D, Scott L, Blom H, Brismar H. Super-resolution stimulated emission depletion imaging of slit diaphragm proteins in optically cleared kidney tissue. Kidney Int. 2016;89:243–247. doi:10.1038/ki.2015.308
  • Artelt N, Siegerist F, Ritter AM, et al. Comparative analysis of podocyte foot process morphology in three species by 3D super-resolution microscopy. Front Med. 2018;5:292. doi:10.3389/fmed.2018.00292
  • Myers BD, Guasch A. Selectivity of the glomerular filtration barrier in healthy and nephrotic humans. Am J Nephrol. 1993;13:311–317. doi:10.1159/000168645
  • Grahammer F, Wigge C, Schell C, et al. A flexible, multilayered protein scaffold maintains the slit in between glomerular podocytes. JCI Insight. 2016;1:9. doi:10.1172/jci.insight.86177
  • Lawrence MG, Altenburg MK, Sanford R, et al. Permeation of macromolecules into the renal glomerular basement membrane and capture by the tubules. Proc Natl Acad Sci U S A. 2017;114:2958–2963. doi:10.1073/pnas.1616457114
  • Schlöndorff D, Wyatt CM, Campbell KN. Revisiting the determinants of the glomerular filtration barrier: what goes round must come round. Kidney Int. 2017;92:533–536. doi:10.1016/j.kint.2017.06.003
  • Andreucci VE, Herrera-Acosta J, Rector FC, Seldin DW. Effective glomerular filtration pressure and single nephron filtration rate during hydropenia, elevated ureteral pressure, and acute volume expansion with isotonic saline. J Clin Invest. 1971;50:2230–2234. doi:10.1172/JCI106719
  • Benzing T, Salant D. Insights into glomerular filtration and albuminuria. N Engl J Med. 2021;384:1437–1446. doi:10.1056/NEJMra1808786
  • Pollak MR, Quaggin SE, Hoenig MP, Dworkin LD. The glomerulus: the sphere of influence. Clin J Am Soc Nephrol. 2014;9:1461–1469. doi:10.2215/CJN.09400913
  • Brenner BM, Bohrer MP, Baylis C, Deen WM. Determinants of glomerular permselectivity: insights derived from observations in vivo. Kidney Int. 1977;12:229–237. doi:10.1038/ki.1977.107
  • Vehaskari VM, Root ER, Germuth FG, Robson AM. Glomerular charge and urinary protein excretion: effects of systemic and intrarenal polycation infusion in the rat. Kidney Int. 1982;22:127–135. doi:10.1038/ki.1982.144
  • Holthöfer H. Molecular architecture of the glomerular slit diaphragm: lessons learnt for a better understanding of disease pathogenesis. Nephrol Dial Transplant. 2007;22:2124–2128. doi:10.1093/ndt/gfm344
  • Martin CE, Jones N. Nephrin signaling in the podocyte: an updated view of signal regulation at the slit diaphragm and beyond. Front Endocrinol. 2018;9. doi:10.3389/fendo.2018.00302
  • Butt L, Unnersjö-Jess D, Höhne M, et al. A molecular mechanism explaining albuminuria in kidney disease. Nat Metab. 2020;2:461–474. doi:10.1038/s42255-020-0204-y
  • Haas M, Rastaldi MP, Fervenza FC. Histologic classification of glomerular diseases: clinicopathologic correlations, limitations exposed by validation studies, and suggestions for modification. Kidney Int. 2014;85:779–793. doi:10.1038/ki.2013.375
  • Hebert LA, Parikh S, Prosek J, Nadasdy T, Rovin BH. Differential diagnosis of glomerular disease: a systematic and inclusive approach. Am J Nephrol. 2013;38:253–266. doi:10.1159/000354390
  • Sethi S, Fervenza FC. Standardized classification and reporting of glomerulonephritis. Nephrol Dial Transplant. 2019;34:193–199. doi:10.1093/ndt/gfy220
  • Kim P, Kwon KW, Park MC, Lee SH, Kim SM, Suh KY. Correspondence and requests for materials should be addressed. 2008.
  • Gale BK, Jafek AR, Lambert CJ, et al. A review of current methods in microfluidic device fabrication and future commercialization prospects. Inventions. 2018;3:60. doi:10.3390/inventions3030060
  • Deguchi S, Tsuda M, Kosugi K, et al. Usability of polydimethylsiloxane-based microfluidic devices in pharmaceutical research using human hepatocytes. ACS Biomater Sci Eng. 2021;7:3648–3657. doi:10.1021/acsbiomaterials.1c00642
  • Zhang J, Wei X, Zeng R, Xu F, Li X. Stem cell culture and differentiation in microfluidic devices toward organ-on-a-chip. Future Sci OA. 2017;3:FSO187. doi:10.4155/fsoa-2016-0091
  • Wu Q, Liu J, Wang X, et al. Organ-on-a-chip: recent breakthroughs and future prospects. Biomed Eng OnLine. 2020;19:9. doi:10.1186/s12938-020-0752-0
  • Quirós-Solano WF, Gaio N, Stassen OMJA, et al. Microfabricated tuneable and transferable porous PDMS membranes for Organs-on-Chips. Sci Rep. 2018;8:13524. doi:10.1038/s41598-018-31912-6
  • Apel P, Blonskaya I, Dmitriev S, Orelovitch O, Sartowska B. Structure of polycarbonate track-etch membranes: origin of the “paradoxical” pore shape. J Membr Sci. 2006;282:393–400. doi:10.1016/j.memsci.2006.05.045
  • Kim MY, Li DJ, Pham LK, Wong BG, Hui EE. Microfabrication of high-resolution porous membranes for cell culture. J Membr Sci. 2014;452:460–469. doi:10.1016/j.memsci.2013.11.034
  • Ikeda K, Nagata S, Okitsu T, Takeuchi S. Cell fiber-based three-dimensional culture system for highly efficient expansion of human induced pluripotent stem cells. Sci Rep. 2017;7:2850. doi:10.1038/s41598-017-03246-2
  • Kruegel J, Rubel D, Gross O. Alport syndrome—insights from basic and clinical research. Nat Rev Nephrol. 2013;9:170–178. doi:10.1038/nrneph.2012.259
  • Nozu K, Nakanishi K, Abe Y, et al. A review of clinical characteristics and genetic backgrounds in Alport syndrome. Clin Exp Nephrol. 2019;23:158–168. doi:10.1007/s10157-018-1629-4
  • Chittiprol S, Chen P, Petrovic-Djergovic D, Eichler T, Ransom RF. Marker expression, behaviors, and responses vary in different lines of conditionally immortalized cultured podocytes. Am J Physiol - Ren Physiol. 2011;301:F660–F671. doi:10.1152/ajprenal.00234.2011
  • Agarwal S, Sudhini YR, Reiser J, Altintas MM. From infancy to fancy: a glimpse into the evolutionary journey of podocytes in culture. Kidney360. 2021;2:385–397. doi:10.34067/KID.0006492020
  • Ciampi O, Iacone R, Longaretti L, et al. Generation of functional podocytes from human induced pluripotent stem cells. Stem Cell Res. 2016;17:130–139. doi:10.1016/j.scr.2016.06.001
  • Yoshimura Y, Taguchi A, Tanigawa S, et al. Manipulation of nephron-patterning signals enables selective induction of podocytes from human pluripotent stem cells. J Am Soc Nephrol. 2019;30:304–321. doi:10.1681/ASN.2018070747
  • Bejoy J, Qian ES, Woodard LE. Accelerated protocol for the differentiation of podocytes from human pluripotent stem cells. STAR Protoc. 2021;2:100898. doi:10.1016/j.xpro.2021.100898
  • Sacco SD, Lemley KV, Sedrakyan S, et al. A novel source of cultured podocytes. PLoS One. 2013;8(12):e81812. doi:10.1371/journal.pone.0081812
  • Kleinman HK, Martin GR. Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol. 2005;15:378–386. doi:10.1016/j.semcancer.2005.05.004
  • Li Y, Meng H, Liu Y, Lee BP. Fibrin gel as an injectable biodegradable scaffold and cell carrier for tissue engineering. Sci World J. 2015;2015:1–10. doi:10.1155/2015/685690
  • Antoine EE, Vlachos PP, Rylander MN. Review of collagen I hydrogels for bioengineered tissue microenvironments: characterization of mechanics, structure, and transport. Tissue Eng Part B Rev. 2014;20:683–696. doi:10.1089/ten.teb.2014.0086
  • Yoshida F, Yuzawa Y, Shigematsu H, et al. Nephrotic syndrome with massive accumulation of type I and type III collagen in the glomeruli. Intern Med. 1993;32:171–176. doi:10.2169/internalmedicine.32.171
  • Nagata M, Nakayama K, Terada Y, Hoshi S, Watanabe T. Cell cycle regulation and differentiation in the human podocyte lineage. Am J Pathol. 1998;153:1511–1520. doi:10.1016/S0002-9440(10)65739-2
  • McCaffrey JC, Webb NJ, Poolman TM, et al. Glucocorticoid therapy regulates podocyte motility by inhibition of Rac1. Sci Rep. 2017;7:6725. doi:10.1038/s41598-017-06810-y
  • Yaoita E, Yoshida Y, Nameta M, Takimoto H, Fujinaka H. Induction of interdigitating cell processes in podocyte culture. Kidney Int. 2018;93:519–524. doi:10.1016/j.kint.2017.06.031
  • Doi K, Kimura H, Wada T, et al. A novel method for successful induction of interdigitating process formation in conditionally immortalized podocytes from mice, rats, and humans. Biochem Biophys Res Commun. 2021;570:47–52. doi:10.1016/j.bbrc.2021.07.029
  • Yaoita E, Nameta M, Yoshida Y, Fujinaka H. Dynamic changes of podocytes caused by fibroblast growth factor 2 in culture. Cell Tissue Res. 2021;386:117–126. doi:10.1007/s00441-021-03511-x
  • Kikkawa Y, Virtanen I, Miner JH. Mesangial cells organize the glomerular capillaries by adhering to the G domain of laminin α5 in the glomerular basement membrane. J Cell Biol. 2003;161:187–196. doi:10.1083/jcb.200211121
  • Vaughan MR, Quaggin SE. How do mesangial and endothelial cells form the glomerular tuft? J Am Soc Nephrol. 2008;19:24–33. doi:10.1681/ASN.2007040471
  • Scindia YM, Deshmukh US, Bagavant H. Mesangial pathology in glomerular disease: targets for therapeutic intervention. Adv Drug Deliv Rev. 2010;62:1337–1343. doi:10.1016/j.addr.2010.08.011
  • Ballesteros Hernando J, Ramos Gómez M, Díaz Lantada A. Modeling living cells within microfluidic systems using cellular automata models. Sci Rep. 2019;9:14886. doi:10.1038/s41598-019-51494-1
  • Sung JH, Wang Y, Shuler ML. Strategies for using mathematical modeling approaches to design and interpret multi-organ microphysiological systems (MPS). APL Bioeng. 2019;3:021501. doi:10.1063/1.5097675