Kidney Bioengineering for Transplantation.
Journal
Transplantation
ISSN: 1534-6080
Titre abrégé: Transplantation
Pays: United States
ID NLM: 0132144
Informations de publication
Date de publication:
01 09 2023
01 09 2023
Historique:
medline:
23
8
2023
pubmed:
1
2
2023
entrez:
31
1
2023
Statut:
ppublish
Résumé
The kidney is an important organ for maintenance of homeostasis in the human body. As renal failure progresses, renal replacement therapy becomes necessary. However, there is a chronic shortage of kidney donors, creating a major problem for transplantation. To solve this problem, many strategies for the generation of transplantable kidneys are under investigation. Since the first reports describing that nephron progenitors could be induced from human induced pluripotent stem cells, kidney organoids have been attracting attention as tools for studying human kidney development and diseases. Because the kidney is formed through the interactions of multiple renal progenitors, current studies are investigating ways to combine these progenitors derived from human induced pluripotent stem cells for the generation of transplantable kidney organoids. Other bioengineering strategies, such as decellularization and recellularization of scaffolds, 3-dimensional bioprinting, interspecies blastocyst complementation and progenitor replacement, and xenotransplantation, also have the potential to generate whole kidneys, although each of these strategies has its own challenges. Combinations of these approaches will lead to the generation of bioengineered kidneys that are transplantable into humans.
Identifiants
pubmed: 36717963
doi: 10.1097/TP.0000000000004526
pii: 00007890-990000000-00324
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1883-1894Informations de copyright
Copyright © 2023 Wolters Kluwer Health, Inc. All rights reserved.
Déclaration de conflit d'intérêts
The authors declare no conflicts of interest.
Références
Boris B, Caroline AP, Andrew SL, et al. Global, regional, and national burden of chronic kidney disease, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet. 2020;395:709–733.
Kobayashi A, Valerius MT, Mugford JW, et al. Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell. 2008;3:169–181.
Humphreys BD, Lin SL, Kobayashi A, et al. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol. 2010;176:85–97.
Kobayashi A, Mugford JW, Krautzberger AM, et al. Identification of a multipotent self-renewing stromal progenitor population during mammalian kidney organogenesis. Stem Cell Rep. 2014;3:650–662.
Costantini F, Kopan R. Patterning a complex organ: branching morphogenesis and nephron segmentation in kidney development. Dev Cell. 2010;18:698–712.
Taguchi A, Nishinakamura R. Nephron reconstitution from pluripotent stem cells. Kidney Int. 2015;87:894–900.
Taguchi A, Kaku Y, Ohmori T, et al. Redefining the in vivo origin of metanephric nephron progenitors enables generation of complex kidney structures from pluripotent stem cells. Cell Stem Cell. 2014;14:53–67.
Morizane R, Lam AQ, Freedman BS, et al. Nephron organoids derived from human pluripotent stem cells model kidney development and injury. Nat Biotechnol. 2015;33:1193–1200.
Takasato M, Er PX, Chiu HS, et al. Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis. Nature. 2015;526:564–568.
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.
Tanigawa S, Islam M, Sharmin S, et al. Organoids from nephrotic disease-derived iPSCs identify impaired NEPHRIN localization and slit diaphragm formation in kidney podocytes. Stem Cell Rep. 2018;11:727–740.
van den Berg CW, Ritsma L, Avramut MC, et al. Renal subcapsular transplantation of PSC-derived kidney organoids induces neo-vasculogenesis and significant glomerular and tubular maturation in vivo. Stem Cell Rep. 2018;10:751–765.
Taguchi A, Nishinakamura R. Higher-order kidney organogenesis from pluripotent stem cells. Cell Stem Cell. 2017;21:730–746.e6.
Tsujimoto H, Kashihara T, Sueta SI, et al. A modular differentiation system maps multiple human kidney lineages from pluripotent stem cells. Cell Rep. 2020;31:107476.
Uchimura K, Wu H, Yoshimura Y, et al. Human pluripotent stem cell-derived kidney organoids with improved collecting duct maturation and injury modeling. Cell Rep. 2020;33:108514.
Tanigawa S, Tanaka E, Miike K, et al. Generation of the organotypic kidney structure by integrating pluripotent stem cell-derived renal stroma. Nat Commun. 2022;13:611.
Wu H, Uchimura K, Donnelly EL, et al. Comparative analysis and refinement of human PSC-derived kidney organoid differentiation with single-cell transcriptomics. Cell Stem Cell. 2018;23:869–881.e8.
Rizki-Safitri A, Gupta N, Hiratsuka K, et al. Live functional assays reveal longitudinal maturation of transepithelial transport in kidney organoids. Front Cell Dev Biol. 2022;10:978888.
Gupta N, Matsumoto T, Hiratsuka K, et al. Modeling injury and repair in kidney organoids reveals that homologous recombination governs tubular intrinsic repair. Sci Transl Med. 2022;14:eabj4772.
Yokote S, Matsunari H, Iwai S, et al. Urine excretion strategy for stem cell-generated embryonic kidneys. Proc Natl Acad Sci USA. 2015;112:12980–12985.
Bohnenpoll T, Feraric S, Nattkemper M, et al. Diversification of cell lineages in ureter development. J Am Soc Nephrol. 2017;28:1792–1801.
Badylak SF, Weiss DJ, Caplan A, et al. Engineered whole organs and complex tissues. Lancet. 2012;379:943–952.
Stephen FB, Doris T, Korkut U. Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Annu Rev Biomed Eng. 2011;13:27–53.
Lu TY, Lin B, Kim J, et al. Repopulation of decellularized mouse heart with human induced pluripotent stem cell-derived cardiovascular progenitor cells. Nat Commun. 2013;4:2307.
Shimoda H, Yagi H, Higashi H, et al. Decellularized liver scaffolds promote liver regeneration after partial hepatectomy. Sci Rep. 2019;9:12543.
Ott HC, Clippinger B, Conrad C, et al. Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med. 2010;16:927–933.
Caralt M, Uzarski JS, Lacob S, et al. Optimization and critical evaluation of decellularization strategies to develop renal extracellular matrix scaffolds as biological templates for organ engineering and transplantation. Am J Transplant. 2015;15:64–75.
Ross EA, Williams MJ, Hamazaki T, et al. Embryonic stem cells proliferate and differentiate when seeded into kidney scaffolds. J Am Soc Nephrol. 2009;20:2338–2347.
Remuzzi A, Figliuzzi M, Bonandrini B, et al. Experimental evaluation of kidney regeneration by organ scaffold recellularization. Sci Rep. 2017;7:43502.
Song JJ, Guyette JP, Glipin SE, et al. Regeneration and experimental orthotopic transplantation of a bioengineered kidney. Nat Med. 2013;19:646–651.
Ko KW, Park SY, Lee EH, et al. Integrated bioactive scaffold with polydeoxyribonucleotide and stem-cell-derived extracellular vesicles for kidney regeneration. ACS Nano. 2021;27:7575–7585.
Huling J, Min S, Kim DS, et al. Kidney regeneration with biomimetic vascular scaffolds based on vascular corrosion casts. Acta Biomater. 2019;95:328–336.
Poornejad N, Buckmiller E, Schaumann L, et al. Re-epithelialization of whole porcine kidneys with renal epithelial cells. J Tissue Eng. 2017;8:2041731417718802041731417718809.
Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol. 2014;32:773–785.
McGivern S, Boutouil H, AI-Kharusi G, et al. Translational application of 3D bioprinting for cartilage tissue engineering. Bioengineering. 2021;8:144.
Skardal A, Mack D, Kapetanovic E, et al. Bioprinted amniotic fluid-derived stem cells accelerate healing of large skin wounds. Stem Cells Transl Med. 2012;11:792–802.
Mitsuzawa S, Ikeguchi R, Aoyama T, et al. The efficacy of a scaffold-free bio 3D conduit developed from autologous dermal fibroblasts on peripheral nerve regeneration in a canine ulnar nerve injury model: a preclinical proof-of-concept study. Cell Transplant. 2019;28:1231–1241.
Liu N, Ye X, Yao B, et al. Advances in 3D bioprinting technology for cardiac tissue engineering and regeneration. Bioactive Mater. 2021;6:1388–1401.
Peired AJ, Mazzinghi B, Chiara LD, et al. Bioengineering strategies for nephrologists: kidney was not built in a day. Expert Opin Biol Ther. 2020;20:467–480.
King SM, Higgins JW, Nino CR, et al. 3D proximal tubule tissues recapitulate key aspects of renal physiology to enable nephrotoxicity testing. Front Physiol. 2017;8:123.
Singh NK, Han W, Nam SA, et al. Three-dimensional cell-printing of advanced renal tubular tissue analogue. Biomaterials. 2020;232:119734.
Homan KA, Kolesky DB, Skylar-Scott MA, et al. Bioprinting of 3D convoluted renal proximal tubules on perfusable chips. Sci Rep. 2016;6:34845.
Lin NYC, Homan KA, Robinson SS, et al. Renal reabsorption in 3D vascularized proximal tubule models. Proc Natl Acad Sci USA. 2019;116:5399–5404.
Lawlor KT, Vanslambrouck JM, Higgins JW, et al. Cellular extrusion bioprinting improves kidney organoid reproducibility and conformation. Nat Mater. 2021;20:260–271.
Nishinakamura R, Matsumoto Y, Nakao K, et al. Murine homolog of SALL1 is essential for ureteric bud invasion in kidney development. Development. 2001;128:3105–3115.
Goto T, Hara H, Sanbo M, et al. Generation of pluripotent stem cell-derived mouse kidneys in Sall1-targeted anephric rats. Nat Commun. 2019;10:451.
Yamaguchi T, Sato H, Kato-Itoh M, et al. Interspecies organogenesis generates autologous functional islets. Nature. 2017;542:191–196.
Wu J, Platero-Luengo A, Sakurai M, et al. Interspecies chimerism with mammalian pluripotent stem cells. Cell. 2017;168:473–486.
Tan T, Wu J, Si C, et al. Chimeric contribution of human extended pluripotent stem cells to monkey embryos ex vivo. Cell. 2021;184:35892020–35892032.
Clark AT, Brivanlou A, Fu J, et al. Human embryo research, stem cell-derived embryo models and in vitro gametogenesis: considerations leading to the revised ISSCR guidelines. Stem Cell Rep. 2021;16:1416–1424.
Fujimoto T, Yamanaka S, Tajiri S, et al. Generation of human renal vesicles in mouse organ niche using nephron progenitor cell replacement system. Cell Rep. 2020;32:108130.
Kobayashi A, Valerius MT, Mugford JW, et al. Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell. 2008;3:169–181.
Wu S, Wu Y, Capecchi MR. Motoneurons and oligodendrocytes are sequentially generated from neural stem cells but do not appear to share common lineage-restricted progenitors in vivo. Development. 2006;133:581–590.
Saito Y, Yamanaka S, Matsumoto N, et al. Generation of functional chimeric kidney containing exogenous progenitor-derived stroma and nephron via a conditional empty niche. Cell Rep. 2022;39:110933.
Pascual J, Zamora J, Pirsch JD. A systematic review of kidney transplantation from expanded criteria donors. Am J Kidney Dis. 2008;52:553–586.
Hamed MO, Chen Y, Pasea L, et al. Early graft loss after kidney transplantation: risk factors and consequences. Am J Transplant. 2015;15:1632–1643.
Summers DM, Johnson RJ, Hudson A, et al. Effect of donor age and cold storage time on outcome in recipients of kidneys donated after circulatory death in the UK: a cohort study. Lancet. 2013;381:727–734.
Kaths JM, Cen JY, Chun YM, et al. Continuous normothermic ex vivo kidney perfusion is superior to brief normothermic perfusion following static cold storage in donation after circulatory death pig kidney transplantation. Am J Transplant. 2017;17:957–969.
Kaths JM, Echeverri J, Chun YM, et al. Continuous normothermic ex vivo kidney perfusion improves graft function in donation after circulatory death pig kidney transplantation. Transplantation. 2017;101:754–763.
Hamar M, Urbanellis P, Kaths MJ, et al. Normothermic ex vivo kidney perfusion reduces warm ischemic injury of porcine kidney grafts retrieved after circulatory death. Transplantation. 2018;102:1262–1270.
Mazilescu LI, Urbanellis P, Kim SJ, et al. Normothermic ex vivo kidney perfusion for human kidney transplantation: first North American results. Transplantation. 2022;106:1852–1859.
Cypel M, Yeung JC, Liu M, et al. Normothermic ex vivo lung perfusion in clinical lung transplantation. N Engl J Med. 2011;364:1431–1440.
Eshmuminov D, Becker D, Borrego LB, et al. An integrated perfusion machine preserves injured human livers for 1 week. Nat Biotechnol. 2020;38:189–198.
Brasile L, Henry N, Orlando G, et al. Potentiating renal regeneration using mesenchymal stem cells. Transplantation. 2019;103:307–313.
Brasile L, Stubenitsky BM, Booster MH, et al. Overcoming severe renal ischemia- the role of ex vivo warm perfusion. Transplantation. 2002;73:897–901.
Lange C, Togel F, Ittrich H, et al. Administered mesenchymal stem cells enhance recovery form ischemia/reperfusion-induced acute renal failure in rats. Kidney Int. 2005;68:1613–1617.
Bonventre JV. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J Am Soc Nephrol. 2003;14:S55–S61.
McCully JD, Cowan DB, Pacak CA, et al. Injection of isolated mitochondria during early reperfusion for cardioprotection. Am J Physiol Heart Circ Physiol. 2009;296:H94–H105.
Blitzer D, Guariento A, Doulamis IP, et al. Delayed transplantation of autologous mitochondria for cardioprotection in a porcine model. Ann Thorac Surg. 2020;109:711–719.
McCully JD, Cowan DB, Emani SM, et al. Mitochondrial transplantation: from animal models to clinical use in humans. Mitochondrion. 2017;34:127–134.
Emani SM, McCully JD. Mitochondrial transplantation: applications for pediatric patients with congenital heart disease. Transl Pediatr. 2018;7:169–175.
Emani SM, Piekarski BL, Harrild D, et al. Autologous mitochondrial transplantation for dysfunction after ischemia-reperfusion injury. J Thorac Cardiovasc Surg. 2017;154:286–289.
Bertero E, Maack C, O’Rourke B. Mitochondrial transplantation in humans: “magical” cure or cause for concern? J Clin Investig. 2018;128:5191–5194.
Doulamis IP, Guariento A, Duignan T, et al. Mitochondrial transplantation by intra-arterial injection for acute kidney injury. Am J Physiol Renal Physiol. 2020;319:403–413.
Pacak CA, Preble JM, Kondo H, et al. Actin-dependent mitochondrial internalization in cardiomyocytes: evidence for rescue of mitochondrial function. Biol Open. 2015;4:622–626.
Cowan DB, Yao R, Thedsanamoorthy JK, et al. Transit and integration of extracellular mitochondria in human heart cells. Sci Rep. 2017;7:17450.
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.
Wang L, Tao T, Su W, et al. A disease model of diabetic nephropathy in a glomerulus-on-a-chip microdevice. Lab Chip. 2017;17:1749–1760.
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.
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.
Raghavan V, Rbaibi Y, Postor-Soler NM, et al. Stress-dependent regulation of apical endocytosis in proximal renal tubule cells mediated by primary cilia. Proc Natl Acad Sci USA. 2014;111:8506–8511.
Maggiorani D, Dissard R, Belloy M, et al. Shear stress-induced alteration of epithelial organization in human renal tubular cells. PLoS One. 2015;10:e0131416.
Vriend J, Peters JGP, Nieskens TTG, et al. Flow stimulates drug transport in a human kidney proximal tubule-on-a-chip independent of primary cilia. Biochim Biophys Acta Gen Subj. 2020;1864:129433.
Homan KA, Gupta N, Kroll KT, et al. Flow-enhanced vascularization and maturation of kidney organoids in vitro. Nat Methods. 2019;16:255–262.
Hiratsuka K, Miyoshi T, Kroll KT, et al. Organoid-on-a-chip model of human ARPKD reveals mechanosensing pathomechanisms for drug discovery. Sci Adv. 2022;8:eabq0866.
Davenport A, Gura V, Ronco C, et al. A wearable haemodialysis device for patients with end-stage renal failure: a pilot study. Lancet. 2007;370:2005–2010.
Armignacco P, Lorenzin A, Neri M, et al. Wearable devices for blood purification: principles, miniaturization, and technical challenges. Semin Dial. 2015;28:125–130.
Gura V, Rivara MB, Bieber S, et al. A wearable artificial kidney for patients with end-stage renal disease. JCI Insight. 2016;1:e86397.
Fissell WH, Dubnisheva A, Eldridge A, et al. High-performance silicone nanopore hemofiltration membranes. J Membr Sci. 2009;326:58–63.
Salani M, Roy S, Fissell WH 4th. Innovations in wearable and implantable artificial kidneys. Am J Kidney Dis. 2018;72:745–751.
Griffith BP, Goerlich CE, Singh AK, et al. Genetically modified porcine-to-human cardiac xenotransplantation. N Engl J Med. 2022;387:35–44.
Porrett PM, Orandi BJ, Kumar V, et al. First clinical-grade porcine kidney xenotransplant using a human decedent model. Am J Transplant. 2022;22:1037–1053.
Adams AB, Kim SC, Martens GR, et al. Xenoantigen deletion and chemical immunosuppression can prolong renal xenograft survival. Ann Surg. 2018;268:564–573.
Elisseeff J, Badylak SF, Boeke JD. Immune and genome engineering as the future of transplantable tissue. N Engl J Med. 2021;385:2451–2462.
Brown BN, Ratner BD, Goodman SB, et al. Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine. Biomaterials. 2012;33:3792–3802.
Sadtler K, Sommerfeld SD, Wolf MT, et al. Proteomic composition and immunomodulatory properties of urinary bladder matrix scaffolds in homeostasis and injury. Semin Immunol. 2017;29:14–23.
Burzyn D, Kuswanto W, Kolodin D, et al. A special population of regulatory T cells potentiates muscle repair. Cell. 2013;155:1282–1295.
Hui SP, Sheng DZ, Sugimoto K, et al. Zebrafish regulatory T cells mediate organ-specific regenerative programs. Dev Cell. 2017;43:659–672.e5.
Geissler EK. The ONE study compares cell therapy products in organ transplantation: introduction to a review series on suppressive monocyte-derived cells. Transplant Res. 2012;1:11.
Raffin C, Vo LT, Bluestone JA. Treg cell-based therapies: challenges and perspectives. Nat Rev Immunol. 2020;20:158–172.
Orlando G, Murphy SV, Bussolati B, et al. Rethinking regenerative medicine from a transplant perspective (and vice versa). Transplantation. 2019;103:237–249.
Cossu G, Birchall M, Brown T, et al. Lancet Commission: stem cells and regenerative medicine. Lancet. 2018;391:883–910.
Daley GQ, Hyun I, Apperley JF, et al. Setting global standards for stem cell research and clinical translation: the 2016 ISSCR guidelines. Stem Cell Rep. 2016;6:787–797.
Lovell-Badge R, Anthony E, Barker RA, et al. ISSCR guidelines for stem cell research and clinical translation: the 2021 update. Stem Cell Rep. 2021;16:1398–1408.
Oxburgh L, Carroll TJ, Cleaver O, et al. (Re)building a kidney. J Am Soc Nephrol. 2017;28:1370–1378.