Precision nephrotoxicity testing using 3D in vitro models.

3D culture model Drug toxicity testing Human primary renal cells Nephrotoxicity Precision medicine

Journal

Cell & bioscience
ISSN: 2045-3701
Titre abrégé: Cell Biosci
Pays: England
ID NLM: 101561195

Informations de publication

Date de publication:
21 Dec 2023
Historique:
received: 04 04 2023
accepted: 15 12 2023
medline: 22 12 2023
pubmed: 22 12 2023
entrez: 22 12 2023
Statut: epublish

Résumé

Nephrotoxicity is a significant concern during the development of new drugs or when assessing the safety of chemicals in consumer products. Traditional methods for testing nephrotoxicity involve animal models or 2D in vitro cell cultures, the latter of which lack the complexity and functionality of the human kidney. 3D in vitro models are created by culturing human primary kidney cells derived from urine in a 3D microenvironment that mimics the fluid shear stresses of the kidney. Thus, 3D in vitro models provide more accurate and reliable predictions of human nephrotoxicity compared to existing 2D models. In this review, we focus on precision nephrotoxicity testing using 3D in vitro models with human autologous urine-derived kidney cells as a promising approach for evaluating drug safety.

Identifiants

pubmed: 38129901
doi: 10.1186/s13578-023-01187-0
pii: 10.1186/s13578-023-01187-0
doi:

Types de publication

Journal Article Review

Langues

eng

Pagination

231

Subventions

Organisme : NIAID NIH HHS
ID : R21 AI152832
Pays : United States
Organisme : NIAID NIH HHS
ID : R03 AI165170
Pays : United States

Informations de copyright

© 2023. The Author(s).

Références

Kwiatkowska E, Domański L, Dziedziejko V, Kajdy A, Stefańska K, Kwiatkowski S. The mechanism of drug nephrotoxicity and the methods for preventing kidney damage. Int J Mol Sci. 2021;22(11):6109.
pubmed: 34204029 pmcid: 8201165 doi: 10.3390/ijms22116109
Ostermann M, Zarbock A, Goldstein S, Kashani K, Macedo E, Murugan R, Bell M, Forni L, Guzzi L, Joannidis M, Kane-Gill SL, Legrand M, Mehta R, Murray PT, Pickkers P, Plebani M, Prowle J, Ricci Z, Rimmele T, Rosner M, Shaw AD, Kellum JA, Ronco C. Recommendations on acute kidney injury biomarkers from the acute disease quality initiative consensus conference: a consensus statement. JAMA Netw Open. 2020;3(10):e2019209.
pubmed: 33021646 doi: 10.1001/jamanetworkopen.2020.19209
Mehta RL, Pascual MT, Soroko S, Savage BR, Himmelfarb J, Ikizler TA, Paganini EP, Chertow GM, Program to Improve Care in Acute Renal Disease. Spectrum of acute renal failure in the intensive care unit: the PICARD experience. Kidney Int. 2004;66(4):1613–21.
pubmed: 15458458 doi: 10.1111/j.1523-1755.2004.00927.x
Stevens PE, Levin A, Kidney Disease: Improving Global Outcomes Chronic Kidney Disease Guideline Development Work Group Members. Evaluation and management of chronic kidney disease: synopsis of the kidney disease: improving global outcomes 2012 clinical practice guideline. Ann Intern Med. 2013;158(11):825–30.
pubmed: 23732715 doi: 10.7326/0003-4819-158-11-201306040-00007
van Renterghem AWJ, van de Haar J, Voest EE. Functional precision oncology using patient-derived assays: bridging genotype and phenotype. Nat Rev Clin Oncol. 2023. https://doi.org/10.1038/s41571-023-00745-2 .
doi: 10.1038/s41571-023-00745-2 pubmed: 36914745
Guo H, Deng N, Dou L, Ding H, Criswell T, Atala A, Furdui CM, Zhang Y. 3-D human renal tubular organoids generated from urine-derived stem cells for nephrotoxicity screening. ACS Biomater Sci Eng. 2020;6(12):6701–9.
pubmed: 33320634 pmcid: 8118570 doi: 10.1021/acsbiomaterials.0c01468
Yu P, Duan Z, Liu S, Pachon I, Ma J, Hemstreet GP, Zhang Y. Drug-induced nephrotoxicity assessment in 3D cellular models. Micromachines. 2021;13(1):3.
pubmed: 35056167 pmcid: 8780064 doi: 10.3390/mi13010003
Ding H, George S, Leng XI, Ihnat M, Ma J-X, Jiang G, Margolis D, Dumond J, Zhang Y. Silk fibers assisted long-term 3D culture of human primary urinary stem cells via inhibition of senescence-associated genes: potential use in the assessment of chronic mitochondrial toxicity. Mater Today Adv. 2022;15:100261.
pubmed: 36212078 pmcid: 9542430 doi: 10.1016/j.mtadv.2022.100261
Ding H, Jambunathan K, Jiang G, Margolis DM, Leng I, Ihnat M, Ma J-X, Mirsalis J, Zhang Y. 3D spheroids of human primary urine-derived stem cells in the assessment of drug-induced mitochondrial toxicity. Pharmaceutics. 2022;14(5):1042.
pubmed: 35631624 pmcid: 9145543 doi: 10.3390/pharmaceutics14051042
Soo JY, Jansen J, Masereeuw R, Little MH. Advances in predictive in vitro models of drug-induced nephrotoxicity. Nat Rev Nephrol. 2018;14(6):378–93.
pubmed: 29626199 pmcid: 6013592 doi: 10.1038/s41581-018-0003-9
Graf BW, Boppart SA. Imaging and analysis of three-dimensional cell culture models. Methods Mol Biol. 2010;591:211–27.
pubmed: 19957133 pmcid: 3699323 doi: 10.1007/978-1-60761-404-3_13
Welten M, Pavlovska G, Chen Y, Teruoka Y, Fisher M, Bangs F, Towers M, Tickle C. 3D expression patterns of cell cycle genes in the developing chick wing and comparison with expression patterns of genes implicated in digit specification. Dev Dyn. 2011;240(5):1278–88.
pubmed: 21509900 doi: 10.1002/dvdy.22633
Tse HM, Gardner G, Dominguez-Bendala J, Fraker CA. The importance of proper oxygenation in 3D culture. Front Bioeng Biotechnol. 2021;9:634403.
pubmed: 33859979 pmcid: 8042214 doi: 10.3389/fbioe.2021.634403
Bédard P, Gauvin S, Ferland K, Caneparo C, Pellerin È, Chabaud S, Bolduc S. Innovative human three-dimensional tissue-engineered models as an alternative to animal testing. Bioengineering. 2020;7(3):115.
pubmed: 32957528 pmcid: 7552665 doi: 10.3390/bioengineering7030115
Choudhury MI, Li Y, Mistriotis P, Vasconcelos ACN, Dixon EE, Yang J, Benson M, Maity D, Walker R, Martin L, Koroma F, Qian F, Konstantopoulos K, Woodward OM, Sun SX. Kidney epithelial cells are active mechano-biological fluid pumps. Nat Commun. 2022;13(1):2317.
pubmed: 35484146 pmcid: 9050750 doi: 10.1038/s41467-022-29988-w
Bharadwaj S, Liu G, Shi Y, Wu R, Yang B, He T, Fan Y, Lu X, Zhou X, Liu H, Atala A, Rohozinski J, Zhang Y. Multipotential differentiation of human urine-derived stem cells: potential for therapeutic applications in urology. Stem Cells. 2013;31(9):1840–56.
pubmed: 23666768 doi: 10.1002/stem.1424
Bharadwaj S, Liu G, Shi Y, Markert C, Andersson KE, Atala A, Zhang Y. Characterization of urine-derived stem cells obtained from upper urinary tract for use in cell-based urological tissue engineering. Tissue Eng Part A. 2011;17(15–16):2123–32.
pubmed: 21513463 pmcid: 9836685 doi: 10.1089/ten.tea.2010.0637
Wan Q, Xiong G, Liu G, Shupe TD, Wei G, Zhang D, Liang D, Lu X, Atala A, Zhang Y. Urothelium with barrier function differentiated from human urine-derived stem cells for potential use in urinary tract reconstruction. Stem Cell Res Ther. 2018;9(1):304–304.
pubmed: 30409188 pmcid: 6225683 doi: 10.1186/s13287-018-1035-6
DesRochers TM, Suter L, Roth A, Kaplan DL. Bioengineered 3D human kidney tissue, a platform for the determination of nephrotoxicity. PLoS ONE. 2013;8(3):e59219.
pubmed: 23516613 pmcid: 3597621 doi: 10.1371/journal.pone.0059219
King SM, Higgins JW, Nino CR, Smith TR, Paffenroth EH, Fairbairn CE, Docuyanan A, Shah VD, Chen AE, Presnell SC, Nguyen DG. 3D proximal tubule tissues recapitulate key aspects of renal physiology to enable nephrotoxicity testing. Front Physiol. 2017;8:123.
pubmed: 28337147 pmcid: 5340751 doi: 10.3389/fphys.2017.00123
Vormann MK, Vriend J, Lanz HL, Gijzen L, van den Heuvel A, Hutter S, Joore J, Trietsch SJ, Stuut C, Nieskens TTG, Peters JGP, Ramp D, Caj M, Russel FGM, Jacobsen B, Roth A, Lu S, Polli JW, Naidoo AA, Vulto P, Masereeuw R, Wilmer MJ, Suter-Dick L. Implementation of a human renal proximal tubule on a chip for nephrotoxicity and drug interaction studies. J Pharm Sci. 2021;110(4):1601–14.
pubmed: 33545187 doi: 10.1016/j.xphs.2021.01.028
Vidal Yucha SE, Quackenbush D, Chu T, Lo F, Sutherland JJ, Kuzu G, Roberts C, Luna F, Barnes SW, Walker J, Kuss P. 3D, human renal proximal tubule (RPTEC-TERT1) organoids ‘tubuloids’ for translatable evaluation of nephrotoxins in high-throughput. PLoS ONE. 2022;17(11):e0277937.
pubmed: 36409750 pmcid: 9678317 doi: 10.1371/journal.pone.0277937
Digby JLM, Vanichapol T, Przepiorski A, Davidson AJ, Sander V. Evaluation of cisplatin-induced injury in human kidney organoids. Am J Physiol Renal Physiol. 2020;318(4):F971–8.
pubmed: 32150447 pmcid: 7395477 doi: 10.1152/ajprenal.00597.2019
Gu S, Wu G, Lu D, Meng G, Wang Y, Tang L, Zhang W. Nephrotoxicity assessment of Esculentoside A using human-induced pluripotent stem cell-derived organoids. Phytother Res. 2023. https://doi.org/10.1002/ptr.7721 .
doi: 10.1002/ptr.7721 pubmed: 37461256
Astashkina AI, Mann BK, Prestwich GD, Grainger DW. Comparing predictive drug nephrotoxicity biomarkers in kidney 3-D primary organoid culture and immortalized cell lines. Biomaterials. 2012;33(18):4712–21.
pubmed: 22475530 doi: 10.1016/j.biomaterials.2012.03.001
Astashkina AI, Mann BK, Prestwich GD, Grainger DW. A 3-D organoid kidney culture model engineered for high-throughput nephrotoxicity assays. Biomaterials. 2012;33(18):4700–11.
pubmed: 22444643 doi: 10.1016/j.biomaterials.2012.02.063
Fedecostante M, Westphal KGC, Buono MF, Sanchez Romero N, Wilmer MJ, Kerkering J, Baptista PM, Hoenderop JG, Masereeuw R. Recellularized native kidney scaffolds as a novel tool in nephrotoxicity screening. Drug Metab Dispos. 2018;46(9):1338–50.
pubmed: 29980578 doi: 10.1124/dmd.118.080721
Vormann MK, Gijzen L, Hutter S, Boot L, Nicolas A, van den Heuvel A, Vriend J, Ng CP, Nieskens TTG, van Duinen V, de Wagenaar B, Masereeuw R, Suter-Dick L, Trietsch SJ, Wilmer M, Joore J, Vulto P, Lanz HL. Nephrotoxicity and kidney transport assessment on 3D perfused proximal tubules. AAPS J. 2018;20(5):90.
pubmed: 30109442 doi: 10.1208/s12248-018-0248-z
Cohen A, Ioannidis K, Ehrlich A, Regenbaum S, Cohen M, Ayyash M, Tikva SS, Nahmias Y. Mechanism and reversal of drug-induced nephrotoxicity on a chip. Sci Transl Med. 2021;13(582):eabd6299.
pubmed: 33627489 pmcid: 8897043 doi: 10.1126/scitranslmed.abd6299
Jang KJ, Mehr AP, Hamilton GA, McPartlin LA, Chung S, Suh KY, Ingber DE. Human kidney proximal tubule-on-a-chip for drug transport and nephrotoxicity assessment. Integr Biol. 2013;5(9):1119–29.
doi: 10.1039/c3ib40049b
Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol. 2014;32(8):773–85.
pubmed: 25093879 doi: 10.1038/nbt.2958
Zhang YS, Yue K, Aleman J, Moghaddam KM, Bakht SM, Yang J, Jia W, Dell’Erba V, Assawes P, Shin SR, Dokmeci MR, Oklu R, Khademhosseini A. 3D bioprinting for tissue and organ fabrication. Ann Biomed Eng. 2017;45(1):148–63.
pubmed: 27126775 doi: 10.1007/s10439-016-1612-8
Cui X, Boland T, D’Lima DD, Lotz MK. Thermal inkjet printing in tissue engineering and regenerative medicine. Recent Pat Drug Deliv Formul. 2012;6(2):149–55.
pubmed: 22436025 pmcid: 3565591 doi: 10.2174/187221112800672949
Homan KA, Kolesky DB, Skylar-Scott MA, Herrmann J, Obuobi H, Moisan A, Lewis JA. Bioprinting of 3D convoluted renal proximal tubules on perfusable chips. Sci Rep. 2016;6:34845.
pubmed: 27725720 pmcid: 5057112 doi: 10.1038/srep34845
Trondle K, Miotto G, Rizzo L, Pichler R, Koch F, Koltay P, Zengerle R, Lienkamp SS, Kartmann S, Zimmermann S. Deep learning-assisted nephrotoxicity testing with bioprinted renal spheroids. Int J Bioprint. 2022;8(2):528.
pubmed: 35702333 pmcid: 9186384 doi: 10.18063/ijb.v8i2.528
Yin L, Du G, Zhang B, Zhang H, Yin R, Zhang W, Yang SM. Efficient drug screening and nephrotoxicity assessment on co-culture microfluidic kidney chip. Sci Rep. 2020;10(1):6568.
pubmed: 32300186 pmcid: 7162892 doi: 10.1038/s41598-020-63096-3
Lee J, Kim S. Kidney-on-a-chip: a new technology for predicting drug efficacy, interactions, and drug-induced nephrotoxicity. Curr Drug Metab. 2018;19(7):577–83.
pubmed: 29521220 doi: 10.2174/1389200219666180309101844
Imaoka T, Yang J, Wang L, McDonald MG, Afsharinejad Z, Bammler TK, Van Ness K, Yeung CK, Rettie AE, Himmelfarb J, Kelly EJ. Microphysiological system modeling of ochratoxin A-associated nephrotoxicity. Toxicology. 2020;444:152582.
pubmed: 32905824 doi: 10.1016/j.tox.2020.152582
DesRochers TM, Kimmerling EP, Jandhyala DM, El-Jouni W, Zhou J, Thorpe CM, Leong JM, Kaplan DL. Effects of Shiga toxin type 2 on a bioengineered three-dimensional model of human renal tissue. Infect Immun. 2015;83(1):28–38.
pubmed: 25312954 doi: 10.1128/IAI.02143-14
Forbes TA, Howden SE, Lawlor K, Phipson B, Maksimovic J, Hale L, Wilson S, Quinlan C, Ho G, Holman K, Bennetts B, Crawford J, Trnka P, Oshlack A, Patel C, Mallett A, Simons C, Little MH. Patient-iPSC-derived kidney organoids show functional validation of a ciliopathic renal phenotype and reveal underlying pathogenetic mechanisms. Am J Hum Genet. 2018;102(5):816–31.
pubmed: 29706353 pmcid: 5986969 doi: 10.1016/j.ajhg.2018.03.014
Li Y, Oo ZY, Chang SY, Huang P, Eng KG, Zeng JL, Kaestli AJ, Gopalan B, Kandasamy K, Tasnim F, Zink D. An in vitro method for the prediction of renal proximal tubular toxicity in humans. Toxicol Res. 2013;2(5):352–65.
doi: 10.1039/c3tx50042j
Balzer MS, Rohacs T, Susztak K. How many cell types are in the kidney and what do they do? Annu Rev Physiol. 2022;84:507–31.
pubmed: 34843404 doi: 10.1146/annurev-physiol-052521-121841
Gupta N, Matsumoto T, Hiratsuka K, Garcia Saiz E, Galichon P, Miyoshi T, Susa K, Tatsumoto N, Yamashita M, Morizane R. Modeling injury and repair in kidney organoids reveals that homologous recombination governs tubular intrinsic repair. Sci Transl Med. 2022;14(634):eabj4772.
pubmed: 35235339 pmcid: 9161367 doi: 10.1126/scitranslmed.abj4772
Wilson SB, Howden SE, Vanslambrouck JM, Dorison A, Alquicira-Hernandez J, Powell JE, Little MH. DevKidCC allows for robust classification and direct comparisons of kidney organoid datasets. Genome Med. 2022;14(1):19.
pubmed: 35189942 pmcid: 8862535 doi: 10.1186/s13073-022-01023-z
Hale LJ, Howden SE, Phipson B, Lonsdale A, Er PX, Ghobrial I, Hosawi S, Wilson S, Lawlor KT, Khan S, Oshlack A, Quinlan C, Lennon R, Little MH. 3D organoid-derived human glomeruli for personalised podocyte disease modelling and drug screening. Nat Commun. 2018;9(1):5167.
pubmed: 30514835 pmcid: 6279764 doi: 10.1038/s41467-018-07594-z
Tekguc M, Gaal RCV, Uzel SGM, Gupta N, Riella LV, Lewis JA, Morizane R. Kidney organoids: a pioneering model for kidney diseases. Transl Res. 2022;250:1–17.
pubmed: 35750295 pmcid: 9691572 doi: 10.1016/j.trsl.2022.06.012
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(11):1193–200.
pubmed: 26458176 pmcid: 4747858 doi: 10.1038/nbt.3392
Chun J, Riella CV, Chung H, Shah SS, Wang M, Magraner JM, Ribas GT, Ribas HT, Zhang JY, Alper SL, Friedman DJ, Pollak MR. DGAT2 inhibition potentiates lipid droplet formation to reduce cytotoxicity in APOL1 kidney risk variants. J Am Soc Nephrol. 2022;33(5):889–907.
pubmed: 35232775 pmcid: 9063887 doi: 10.1681/ASN.2021050723
Diekjurgen D, Grainger DW. A murine ex vivo 3D kidney proximal tubule model predicts clinical drug-induced nephrotoxicity. Arch Toxicol. 2019;93(5):1349–64.
pubmed: 30863989 doi: 10.1007/s00204-019-02430-9
Choucha Snouber L, Jacques S, Monge M, Legallais C, Leclerc E. Transcriptomic analysis of the effect of ifosfamide on MDCK cells cultivated in microfluidic biochips. Genomics. 2012;100(1):27–34.
pubmed: 22580237 doi: 10.1016/j.ygeno.2012.05.001
Jenkinson SE, Chung GW, van Loon E, Bakar NS, Dalzell AM, Brown CD. The limitations of renal epithelial cell line HK-2 as a model of drug transporter expression and function in the proximal tubule. Pflugers Arch. 2012;464(6):601–11.
pubmed: 23014881 doi: 10.1007/s00424-012-1163-2
Van der Hauwaert C, Savary G, Buob D, Leroy X, Aubert S, Flamand V, Hennino MF, Perrais M, Lo-Guidice JM, Broly F, Cauffiez C, Glowacki F. Expression profiles of genes involved in xenobiotic metabolism and disposition in human renal tissues and renal cell models. Toxicol Appl Pharmacol. 2014;279(3):409–18.
pubmed: 25036895 doi: 10.1016/j.taap.2014.07.007
Aschauer L, Carta G, Vogelsang N, Schlatter E, Jennings P. Expression of xenobiotic transporters in the human renal proximal tubule cell line RPTEC/TERT1. Toxicol Vitro. 2015;30(1 Pt A):95–105.
doi: 10.1016/j.tiv.2014.12.003
Aschauer L, Limonciel A, Wilmes A, Stanzel S, Kopp-Schneider A, Hewitt P, Lukas A, Leonard MO, Pfaller W, Jennings P. Application of RPTEC/TERT1 cells for investigation of repeat dose nephrotoxicity: a transcriptomic study. Toxicol Vitro. 2015;30(1 Pt A):106–16.
doi: 10.1016/j.tiv.2014.10.005
Takasato M, Er PX, Chiu HS, Maier B, Baillie GJ, Ferguson C, Parton RG, Wolvetang EJ, Roost MS, de Sousa Lopes SMC, Little MH. Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis. Nature. 2015;526(7574):564–8.
pubmed: 26444236 doi: 10.1038/nature15695
Gupta N, Susa K, Morizane R. Regenerative medicine, disease modeling, and drug discovery in human pluripotent stem cell-derived kidney tissue. Eur Med J Reprod Health. 2017;3(1):57–67.
pubmed: 31157117 pmcid: 6544146
Taguchi A, Kaku Y, Ohmori T, Sharmin S, Ogawa M, Sasaki H, Nishinakamura R. Redefining the in vivo origin of metanephric nephron progenitors enables generation of complex kidney structures from pluripotent stem cells. Cell Stem Cell. 2014;14(1):53–67.
pubmed: 24332837 doi: 10.1016/j.stem.2013.11.010
Toyohara T, Mae S, Sueta S, Inoue T, Yamagishi Y, Kawamoto T, Kasahara T, Hoshina A, Toyoda T, Tanaka H, Araoka T, Sato-Otsubo A, Takahashi K, Sato Y, Yamaji N, Ogawa S, Yamanaka S, Osafune K. Cell therapy using human induced pluripotent stem cell-derived renal progenitors ameliorates acute kidney injury in mice. Stem Cells Transl Med. 2015;4(9):980–92.
pubmed: 26198166 pmcid: 4542865 doi: 10.5966/sctm.2014-0219
Ungricht R, Guibbal L, Lasbennes MC, Orsini V, Beibel M, Waldt A, Cuttat R, Carbone W, Basler A, Roma G, Nigsch F, Tchorz JS, Hoepfner D, Hoppe PS. Genome-wide screening in human kidney organoids identifies developmental and disease-related aspects of nephrogenesis. Cell Stem Cell. 2022;29(1):160-175.e7.
pubmed: 34847364 doi: 10.1016/j.stem.2021.11.001
Karagiannis P, Takahashi K, Saito M, Yoshida Y, Okita K, Watanabe A, Inoue H, Yamashita JK, Todani M, Nakagawa M, Osawa M, Yashiro Y, Yamanaka S, Osafune K. Induced pluripotent stem cells and their use in human models of disease and development. Physiol Rev. 2019;99(1):79–114.
pubmed: 30328784 doi: 10.1152/physrev.00039.2017
Garreta E, Prado P, Tarantino C, Oria R, Fanlo L, Marti E, Zalvidea D, Trepat X, Roca-Cusachs P, Gavalda-Navarro A, Cozzuto L, Campistol JM, Izpisua Belmonte JC, Hurtado Del Pozo C, Montserrat N. Fine tuning the extracellular environment accelerates the derivation of kidney organoids from human pluripotent stem cells. Nat Mater. 2019;18(4):397–405.
pubmed: 30778227 pmcid: 9845070 doi: 10.1038/s41563-019-0287-6
Xia Y, Sancho-Martinez I, Nivet E, Rodriguez Esteban C, Campistol JM, Izpisua Belmonte JC. The generation of kidney organoids by differentiation of human pluripotent cells to ureteric bud progenitor-like cells. Nat Protoc. 2014;9(11):2693–704.
pubmed: 25340442 doi: 10.1038/nprot.2014.182
Schena FP, Nistor I, Curci C. Transcriptomics in kidney biopsy is an untapped resource for precision therapy in nephrology: a systematic review. Nephrol Dial Transplant. 2018;33(7):1094–102.
pubmed: 28992289 doi: 10.1093/ndt/gfx211
Low JH, Li P, Chew EGY, Zhou B, Suzuki K, Zhang T, Lian MM, Liu M, Aizawa E, Rodriguez Esteban C, Yong KSM, Chen Q, Campistol JM, Fang M, Khor CC, Foo JN, Izpisua Belmonte JC, Xia Y. Generation of human PSC-derived kidney organoids with patterned nephron segments and a de novo vascular network. Cell Stem Cell. 2019;25(3):373-387.e9.
pubmed: 31303547 pmcid: 6731150 doi: 10.1016/j.stem.2019.06.009
Shi Y, Liu G, Wu R, Mack DL, Sun XS, Maxwell J, Guan X, Atala A, Zhang Y. Differentiation capacity of human urine-derived stem cells to retain telomerase activity. Front Cell Dev Biol. 2022;10:890574.
pubmed: 35693947 pmcid: 9186504 doi: 10.3389/fcell.2022.890574
Luo S, Shao L, Geng R, Liu Q, Jiang W, Gong M, Zhang Y, He Y. Identification and biological characteristics of clear cell renal cell carcinoma associated urine-derived stem cells. Am J Transl Res. 2021;13(4):2143–62.
pubmed: 34017380 pmcid: 8129396
Xiong G, Tang W, Zhang D, He D, Wei G, Atala A, Liang XJ, Bleyer AJ, Bleyer ME, Yu J, Aloi JA, Ma JX, Furdui CM, Zhang Y. Impaired regeneration potential in urinary stem cells diagnosed from the patients with diabetic nephropathy. Theranostics. 2019;9(14):4221–32.
pubmed: 31281543 pmcid: 6592174 doi: 10.7150/thno.34050
Jorgensen AM, Yoo JJ, Atala A. Solid organ bioprinting: strategies to achieve organ function. Chem Rev. 2020;120(19):11093–127.
pubmed: 32885956 pmcid: 8459198 doi: 10.1021/acs.chemrev.0c00145
Pins GD, Toner M, Morgan JR. Microfabrication of an analog of the basal lamina: biocompatible membranes with complex topographies. FASEB J. 2000;14(3):593–602.
pubmed: 10698975 doi: 10.1096/fasebj.14.3.593
Limongi T, Guzzi F, Parrotta E, Candeloro P, Scalise S, Lucchino V, Gentile F, Tirinato L, Coluccio ML, Torre B, Allione M, Marini M, Susa F, Fabrizio ED, Cuda G, Perozziello G. Microfluidics for 3D cell and tissue cultures: microfabricative and ethical aspects updates. Cells. 2022;11(10):1699.
pubmed: 35626736 pmcid: 9139493 doi: 10.3390/cells11101699
Wilmer MJ, Ng CP, Lanz HL, Vulto P, Suter-Dick L, Masereeuw R. Kidney-on-a-chip technology for drug-induced nephrotoxicity screening. Trends Biotechnol. 2016;34(2):156–70.
pubmed: 26708346 doi: 10.1016/j.tibtech.2015.11.001
Desrochers TM, Palma E, Kaplan DL. Tissue-engineered kidney disease models. Adv Drug Deliv Rev. 2014;69–70:67–80.
pubmed: 24361391 doi: 10.1016/j.addr.2013.12.002
Nomura M, Matsunami T, Kobayashi K, Uchibayashi T, Koshida K, Tanaka M, Namiki M, Mizuhara Y, Akiba T, Yokogawa K, Moritani S, Miyamoto K. Involvement of ABC transporters in chemosensitivity of human renal cell carcinoma, and regulation of MRP2 expression by conjugated bilirubin. Anticancer Res. 2005;25(4):2729–35.
pubmed: 16080518
Zarrintaj P, Saeb MR, Stadler FJ, Yazdi MK, Nezhad MN, Mohebbi S, Seidi F, Ganjali MR, Mozafari M. Human organs-on-chips: a review of the state-of-the-art, current prospects, and future challenges. Adv Biol. 2022;6(1):e2000526.
doi: 10.1002/adbi.202000526
Downes KJ, Hayes M, Fitzgerald JC, Pais GM, Liu J, Zane NR, Goldstein SL, Scheetz MH, Zuppa AF. Mechanisms of antimicrobial-induced nephrotoxicity in children. J Antimicrob Chemother. 2020;75(1):1–13.
pubmed: 31369087 doi: 10.1093/jac/dkz325
Lash LH. Diverse roles of mitochondria in renal injury from environmental toxicants and therapeutic drugs. Int J Mol Sci. 2021;22(8):4172.
pubmed: 33920653 pmcid: 8073222 doi: 10.3390/ijms22084172
Balakumar P, Rohilla A, Thangathirupathi A. Gentamicin-induced nephrotoxicity: do we have a promising therapeutic approach to blunt it? Pharmacol Res. 2010;62(3):179–86.
pubmed: 20434560 doi: 10.1016/j.phrs.2010.04.004
Abdel-Fattah MM, Elgendy A, Mohamed WR. Xanthenone, ACE2 activator, counteracted gentamicin-induced nephrotoxicity in rats: impact on oxidative stress and ACE2/Ang-(1–7) signaling. Life Sci. 2021;275:119387.
pubmed: 33774027 doi: 10.1016/j.lfs.2021.119387
Elyasi S, Khalili H, Dashti-Khavidaki S, Mohammadpour A. Vancomycin-induced nephrotoxicity: mechanism, incidence, risk factors and special populations: a literature review. Eur J Clin Pharmacol. 2012;68(9):1243–55.
pubmed: 22411630 doi: 10.1007/s00228-012-1259-9
Oktem F, Arslan MK, Ozguner F, Candir O, Yilmaz HR, Ciris M, Uz E. In vivo evidences suggesting the role of oxidative stress in pathogenesis of vancomycin-induced nephrotoxicity: protection by erdosteine. Toxicology. 2005;215(3):227–33.
pubmed: 16112787 doi: 10.1016/j.tox.2005.07.009
Luque Y, Louis K, Jouanneau C, Placier S, Esteve E, Bazin D, Rondeau E, Letavernier E, Wolfromm A, Gosset C, Boueilh A, Burbach M, Frere P, Verpont MC, Vandermeersch S, Langui D, Daudon M, Frochot V, Mesnard L. Vancomycin-associated cast nephropathy. J Am Soc Nephrol. 2017;28(6):1723–8.
pubmed: 28082518 pmcid: 5461798 doi: 10.1681/ASN.2016080867
Hall AM, Hendry BM, Nitsch D, Connolly JO. Tenofovir-associated kidney toxicity in HIV-infected patients: a review of the evidence. Am J Kidney Dis. 2011;57(5):773–80.
pubmed: 21435764 doi: 10.1053/j.ajkd.2011.01.022
Rodriguez-Novoa S, Labarga P, Soriano V, Egan D, Albalater M, Morello J, Cuenca L, Gonzalez-Pardo G, Khoo S, Back D, Owen A. Predictors of kidney tubular dysfunction in HIV-infected patients treated with tenofovir: a pharmacogenetic study. Clin Infect Dis. 2009;48(11):e108–16.
pubmed: 19400747 doi: 10.1086/598507
Liborio AB, Andrade L, Pereira LV, Sanches TR, Shimizu MH, Seguro AC. Rosiglitazone reverses tenofovir-induced nephrotoxicity. Kidney Int. 2008;74(7):910–8.
pubmed: 18563054 doi: 10.1038/ki.2008.252
Fanos V, Cataldi L. Amphotericin B-induced nephrotoxicity: a review. J Chemother. 2000;12(6):463–70.
pubmed: 11154026 doi: 10.1179/joc.2000.12.6.463
Mayer J, Doubek M, Doubek J, Horky D, Scheer P, Stepanek M. Reduced nephrotoxicity of conventional amphotericin B therapy after minimal nephroprotective measures: animal experiments and clinical study. J Infect Dis. 2002;186(3):379–88.
pubmed: 12134234 doi: 10.1086/341662
Pabla N, Dong Z. Cisplatin nephrotoxicity: mechanisms and renoprotective strategies. Kidney Int. 2008;73(9):994–1007.
pubmed: 18272962 doi: 10.1038/sj.ki.5002786
Ikeda Y, Hamano H, Horinouchi Y, Miyamoto L, Hirayama T, Nagasawa H, Tamaki T, Tsuchiya K. Role of ferroptosis in cisplatin-induced acute nephrotoxicity in mice. J Trace Elem Med Biol. 2021;67:126798.
pubmed: 34087581 doi: 10.1016/j.jtemb.2021.126798
Morsy MA, El-Sheikh AAK, Abdel-Hafez SMN, Kandeel M, Abdel-Gaber SA. Paeonol protects against methotrexate-induced nephrotoxicity via upregulation of P-gp expression and inhibition of TLR4/NF-kappaB pathway. Front Pharmacol. 2022;13:774387.
pubmed: 35185559 pmcid: 8854802 doi: 10.3389/fphar.2022.774387
Song Y, Liu L, Liu B, Liu R, Chen Y, Li C, Liu G, Song Z, Lu C, Lu A, Liu Y. Interaction of nobiletin with methotrexate ameliorates 7-OH methotrexate-induced nephrotoxicity through endoplasmic reticulum stress-dependent PERK/CHOP signaling pathway. Pharmacol Res. 2021;165:105371.
pubmed: 33460792 doi: 10.1016/j.phrs.2020.105371
Ghannoum M, Roberts DM, Goldfarb DS, Heldrup J, Anseeuw K, Galvao TF, Nolin TD, Hoffman RS, Lavergne V, Meyers P, Gosselin S, Botnaru T, Mardini K, Wood DM, EXTRIP Workgroup. Extracorporeal treatment for methotrexate poisoning: systematic review and recommendations from the EXTRIP Workgroup. Clin J Am Soc Nephrol. 2022;17(4):602–22.
pubmed: 35236714 pmcid: 8993465 doi: 10.2215/CJN.08030621
Damiano S, Ciarcia R, Montagnaro S, Pagnini U, Garofano T, Capasso G, Florio S, Giordano A. Prevention of nephrotoxicity induced by cyclosporine-A: role of antioxidants. J Cell Biochem. 2015;116(3):364–9.
pubmed: 25418335 doi: 10.1002/jcb.25022
Damiano S, Trepiccione F, Ciarcia R, Scanni R, Spagnuolo M, Manco L, Borrelli A, Capasso C, Mancini R, Schiattarella A, Iervolino A, Zacchia E, Bata-Csere A, Florio S, Anastasio P, Pollastro R, Mancini A, Capasso G. A new recombinant MnSOD prevents the cyclosporine A-induced renal impairment. Nephrol Dial Transplant. 2013;28(8):2066–72.
pubmed: 23677648 doi: 10.1093/ndt/gft020
Wu HM, Lee SG, Oh CS, Kim SG. Hypergravity load modulates acetaminophen nephrotoxicity via endoplasmic reticulum stress in association with hepatic microRNA-122 expression. Int J Mol Sci. 2021;22(9):4901.
pubmed: 34063126 pmcid: 8124210 doi: 10.3390/ijms22094901
Park WY. Controversies in acetaminophen nephrotoxicity. Kidney Res Clin Pract. 2020;39(1):4–6.
pubmed: 32176973 pmcid: 7105628 doi: 10.23876/j.krcp.20.027
Awad DS, Ali RM, Mhaidat NM, Shotar AM. Zizyphus jujuba protects against ibuprofen-induced nephrotoxicity in rats. Pharm Biol. 2014;52(2):182–6.
pubmed: 24074058 doi: 10.3109/13880209.2013.821665
Xu W, Yang J, Gu X, Su W, Pu F, Xie Z, Jin K, Su W, Mao L. Mechanochemical prepared ibuprofen-Polygonatum sibiricum polysaccharide drug delivery system for enhanced bioactivity with reduced renal injury induced by NSAIDs. Drug Deliv. 2022;29(1):351–63.
pubmed: 35049408 pmcid: 8786252 doi: 10.1080/10717544.2022.2026533
Ommati MM, Niknahad H, Farshad O, Azarpira N, Heidari R. In vitro and in vivo evidence on the role of mitochondrial impairment as a mechanism of lithium-induced nephrotoxicity. Biol Trace Elem Res. 2021;199(5):1908–18.
pubmed: 32712907 doi: 10.1007/s12011-020-02302-9
Alsady M, Baumgarten R, Deen PM, de Groot T. Lithium in the kidney: friend and foe? J Am Soc Nephrol. 2016;27(6):1587–95.
pubmed: 26577775 doi: 10.1681/ASN.2015080907
Awdishu L, Atilano-Roque A, Tuey S, Joy MS. Identification of novel biomarkers for predicting kidney injury due to drugs using “Omic” strategies. Pharmgenomics Pers Med. 2020;13:687–705.
pubmed: 33293850 pmcid: 7719321
Koturbash I, Tolleson WH, Guo L, Yu D, Chen S, Hong H, Mattes W, Ning B. microRNAs as pharmacogenomic biomarkers for drug efficacy and drug safety assessment. Biomark Med. 2015;9(11):1153–76.
pubmed: 26501795 doi: 10.2217/bmm.15.89
Schofield AL, Brown JP, Brown J, Wilczynska A, Bell C, Glaab WE, Hackl M, Howell L, Lee S, Dear JW, Remes M, Reeves P, Zhang E, Allmer J, Norris A, Falciani F, Takeshita LY, Seyed Forootan S, Sutton R, Park BK, Goldring C. Systems analysis of miRNA biomarkers to inform drug safety. Arch Toxicol. 2021;95(11):3475–95.
pubmed: 34510227 pmcid: 8492583 doi: 10.1007/s00204-021-03150-9
Schraml E, Hackl M, Grillari J. MicroRNAs and toxicology: a love marriage. Toxicol Rep. 2017;4:634–6.
pubmed: 29214146 pmcid: 5695539 doi: 10.1016/j.toxrep.2017.11.001

Auteurs

Pengfei Yu (P)

Wake Forest Institute for Regenerative Medicine, Wake Forest University Health Sciences, Winston-Salem, NC, USA.
The Fourth Department of Liver Disease, Beijing You An Hospital, Capital Medical University, Beijing, China.

Hainan Zhu (H)

Wake Forest Institute for Regenerative Medicine, Wake Forest University Health Sciences, Winston-Salem, NC, USA.

Carol Christine Bosholm (CC)

Wake Forest Institute for Regenerative Medicine, Wake Forest University Health Sciences, Winston-Salem, NC, USA.

Daniella Beiner (D)

Wake Forest Institute for Regenerative Medicine, Wake Forest University Health Sciences, Winston-Salem, NC, USA.

Zhongping Duan (Z)

The Fourth Department of Liver Disease, Beijing You An Hospital, Capital Medical University, Beijing, China.

Avinash K Shetty (AK)

Department of Pediatrics, Wake Forest University School of Medicine, Winston-Salem, NC, USA.

Steve S Mou (SS)

Department of Anesthesiology and Pediatrics, Wake Forest University School of Medicine, Winston-Salem, NC, USA.

Philip Adam Kramer (PA)

Department of Internal Medicine, Section on Gerontology and Geriatrics, Wake Forest University School of Medicine, Winston-Salem, NC, USA.

Luis F Barroso (LF)

Internal Medicine/Infectious Diseases, Wake Forest University Health Sciences, Winston-Salem, NC, USA.

Hongbing Liu (H)

Department of Pediatrics and The Tulane Hypertension and Renal Center of Excellence, Tulane University School of Medicine, Tulane Avenue, New Orleans, LA, USA.

Kun Cheng (K)

Division of Pharmacology and Pharmaceutical Sciences, School of Pharmacy, University of Missouri-Kansas City, 2464 Charlotte Street, Kansas City, MO, 64108, USA.

Michael Ihnat (M)

Department of Pharmaceutical Sciences, University of Oklahoma College of Pharmacy, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.

Matthew A Gorris (MA)

Division of Endocrinology and Metabolism at Wake Forest Baptist Health, Winston-Salem, NC, USA.

Joseph A Aloi (JA)

Division of Endocrinology and Metabolism at Wake Forest Baptist Health, Winston-Salem, NC, USA.

Jobira A Woldemichael (JA)

Division of Nephrology, Wake Forest University Health Sciences, Winston-Salem, NC, USA.

Anthony Bleyer (A)

Division of Nephrology, Wake Forest University Health Sciences, Winston-Salem, NC, USA.

Yuanyuan Zhang (Y)

Wake Forest Institute for Regenerative Medicine, Wake Forest University Health Sciences, Winston-Salem, NC, USA. yzhang@wakehealth.edu.

Classifications MeSH