Enhancing maturity in 3D kidney micro-tissues through clonogenic cell combinations and endothelial integration.
clonogenic epithelial‐like cells
clonogenic mesenchymal‐like cells
co‐culture
kidney micro‐tissues
Journal
Journal of cellular and molecular medicine
ISSN: 1582-4934
Titre abrégé: J Cell Mol Med
Pays: England
ID NLM: 101083777
Informations de publication
Date de publication:
Jun 2024
Jun 2024
Historique:
revised:
09
05
2024
received:
07
12
2023
accepted:
11
05
2024
medline:
31
5
2024
pubmed:
31
5
2024
entrez:
31
5
2024
Statut:
ppublish
Résumé
As an advance laboratory model, three-dimensional (3D) organoid culture has recently been recruited to study development, physiology and abnormality of kidney tissue. Micro-tissues derived from primary renal cells are composed of 3D epithelial structures representing the main characteristics of original tissue. In this research, we presented a simple method to isolate mouse renal clonogenic mesenchymal (MLCs) and epithelial-like cells (ELCs). Then we have done a full characterization of MLCs using flow cytometry for surface markers which showed that more than 93% of cells expressed these markers (Cd44, Cd73 and Cd105). Epithelial and stem/progenitor cell markers characterization also performed for ELC cells and upregulating of these markers observed while mesenchymal markers expression levels were not significantly increased in ELCs. Each of these cells were cultured either alone (ME) or in combination with human umbilical vein endothelial cells (HUVECs) (MEH; with an approximate ratio of 10:5:2) to generate more mature kidney structures. Analysis of 3D MEH renal micro-tissues (MEHRMs) indicated a significant increase in renal-specific gene expression including Aqp1 (proximal tubule), Cdh1 (distal tubule), Umod (loop of Henle), Wt1, Podxl and Nphs1 (podocyte markers), compared to those groups without endothelial cells, suggesting greater maturity of the former tissue. Furthermore, ex ovo transplantation showed greater maturation in the constructed 3D kidney.
Substances chimiques
Biomarkers
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e18453Subventions
Organisme : Royan Institute for Stem Cell Biology and Technology
Informations de copyright
© 2024 The Author(s). Journal of Cellular and Molecular Medicine published by Foundation for Cellular and Molecular Medicine and John Wiley & Sons Ltd.
Références
M. Services and N. E. Survey. US renal data system 2018 annual data report: epidemiology of kidney disease in the United States. Am J Kidney Dis. 2019;73:8‐10. doi:10.1053/j.ajkd.2019.01.001
Santoro D, Caccamo D, Lucisano S, et al. Interplay of vitamin D, erythropoiesis, and the renin‐angiotensin system. Biomed Res Int. 2015;2015:1‐11. doi:10.1155/2015/145828
Ahmadi A, Rad NK, Ezzatizadeh V, Moghadasali R. Kidney regeneration: stem cells as a new trend. Curr Stem Cell Res Ther. 2019;15(3):263‐283. doi:10.2174/1574888x15666191218094513
Ding W, Yousefi K, Shehadeh LA. Isolation, characterization, and high throughput extracellular flux analysis of mouse primary renal tubular epithelial cells. J Vis Exp. 2018;136:1‐10. doi:10.3791/57718
Khoshdel Rad N, Aghdami N, Moghadasali R. Cellular and molecular mechanisms of kidney development: from the embryo to the kidney organoid. Front Cell Dev Biol. 2020;8:1‐16. doi:10.3389/fcell.2020.00183
Brasile L, Henry N, Orlando G, Stubenitsky B. Potentiating renal regeneration using mesenchymal stem cells. Transplantation. 2019;103(2):307‐313. doi:10.1097/TP.0000000000002455
Munro DAD, Hohenstein P, Davies JA. Cycles of vascular plexus formation within the nephrogenic zone of the developing mouse kidney. Sci Rep. 2017;7:1‐13. doi:10.1038/s41598-017-03808-4
Mugford JW, Sipilä P, Mcmahon JA, Mcmahon AP. Osr1 expression demarcates a multi‐potent population of intermediate mesoderm that undergoes progressive restriction to an Osr1‐dependent nephron progenitor compartment within the mammalian kidney. Dev Biol. 2008;324(1):88‐98. doi:10.1016/j.ydbio.2008.09.010.Osr1
Yousef Yengej FA, Jansen J, Rookmaaker MB, Verhaar MC, Clevers H. Kidney organoids and tubuloids. Cells. 2020;9(6):1‐20. doi:10.3390/cells9061326
Kang HM, Lim JH, Noh KH, et al. Effective reconstruction of functional organotypic kidney spheroid for in vitro nephrotoxicity studies. Sci Rep. 2019;9(1):1‐17. doi:10.1038/s41598-019-53855-2
Khoshdel Rad N, Ahmadi A, Moghadasali R. Kidney organoids: current knowledge and future directions. Cell Tissue Res. 2022;387(2):207‐224. doi:10.1007/s00441-021-03565-x
Schutgens F, Rookmaaker MB, Margaritis T, et al. Tubuloids derived from human adult kidney and urine for personalized disease modeling. Nat Biotechnol. 2019;37(3):303‐313. doi:10.1038/s41587-019-0048-8
Oliver JA, Barasch J, Yang J, Herzlinger D, Al‐Awqati Q. Metanephric mesenchyme contains embryonic renal stem cells. Am J Physiol Ren Physiol. 2002;283(4):52‐54. doi:10.1152/ajprenal.00375.2001
Bussolati B, Bruno S, Grange C, et al. Isolation of renal progenitor cells from adult human kidney. Am J Pathol. 2005;166(2):545‐555. doi:10.1016/S0002-9440(10)62276-6
Kamiyama M, Garner MK, Farragut KM, Kobori H. The establishment of a primary culture system of proximal tubule segments using specific markers from normal mouse kidneys. Int J Mol Sci. 2012;13(4):5098‐5111. doi:10.3390/ijms13045098
Terryn S, Jouret F, Vandenabeele F, et al. A primary culture of mouse proximal tubular cells, established on collagen‐coated membranes. Am J Physiol Ren Physiol. 2007;293(2):F476‐F485. doi:10.1152/ajprenal.00363.2006
Tang MJ, Suresh KR, Tannen RL. Carbohydrate metabolism by primary cultures of rabbit proximal tubules. Am J Phys. 1989;256(3):C532‐C539. doi:10.1152/ajpcell.1989.256.3.c532
Gesek FA, Wolff DW, Strandhoy JW. Improved separation method for rat proximal and distal renal tubules. Am J Phys. 1987;253:f358. doi:10.1152/ajprenal.1987.253.2
Vinay P, Gougoux A, Lemieux G. Isolation of a pure suspension of rat proximal tubules. Am J Phys. 1981;10(4):f403. doi:10.1152/ajprenal.1981.241.4
Taub M, Chuman L, Saier MH, Sato G. Growth of Madin‐Darby canine kidney epithelial cell (MDCK) line in hormone‐supplemented, serum‐free medium. Proc Natl Acad Sci USA. 1979;76(7):3338‐3342. doi:10.1073/pnas.76.7.3338
Chung SD, Alavl N, Livingston D, Hiller S, Taub M. Characterization of primary rabbit kidney cultures that express proximal tubule functions in a hormonally defined medium. J Cell Biol. 1982;95(1):118‐126. doi:10.1083/jcb.95.1.118
Rubera I, Tauc M, Bidet M, et al. Chloride currents in primary cultures of rabbit proximal and distal convoluted tubules. Am J Phys. 1998;275(5):44‐45. doi:10.1152/ajprenal.1998.275.5.f651
Inoue CN, Kondo Y, Ohnuma S, Morimoto T, Nishio T, Iinuma K. Use of cultured tubular cells isolated from human urine for investigation of renal transporter. Clin Nephrol. 2000;53(2):90‐98.
Khoshdel‐rad N, Zahmatkesh E, Moeinvaziri F. Promoting maturation of human pluripotent stem cell‐derived renal micro‐tissue by incorporation of endothelial and. Stem Cells Dev. 2021;30(8):428‐440. doi:10.1089/scd.2020.0189
Bahrehbar K, Khanjarpoor Malakhond M, Gholami S. Tracking of human embryonic stem cell‐derived mesenchymal stem cells in premature ovarian failure model mice. Biochem Biophys Res Commun. 2021;577:6‐11. doi:10.1016/j.bbrc.2021.08.063
Bahrehbar K, Gholami S, Nazari Z, Malakhond MK. Embryonic stem cells‐derived mesenchymal stem cells do not differentiate into ovarian cells but improve ovarian function in POF mice. Biochem Biophys Res Commun. 2022;635:92‐98. doi:10.1016/J.BBRC.2022.10.014
Willenbring H, Soto‐Gutierrez A. Transplantable liver organoids made from only three ingredients. Cell Stem Cell. 2013;13(2):139‐140. doi:10.1016/j.stem.2013.07.014
Moeinvaziri F, Shojaei A, Haghparast N, et al. Towards maturation of human otic hair cell–like cells in pluripotent stem cell–derived organoid transplants. Cell Tissue Res. 2021;386(2):321‐333. doi:10.1007/s00441-021-03510-y
Serban MA, Prestwich GD. Modular extracellular matrices: solutions for the puzzle. Methods. 2008;45(1):93‐98. doi:10.1016/j.ymeth.2008.01.010
Zahmatkesh E, Khoshdel‐Rad N, Mirzaei H, et al. Evolution of organoid technology: lessons learnt in co‐culture systems from developmental biology. Dev Biol. 2021;475:37‐53. doi:10.1016/j.ydbio.2021.03.001
Takebe T, Enomura M, Yoshizawa E, Kimura M, Koike H, Ueno Y. Vascularized and complex organ buds from diverse tissues via mesenchymal cell‐driven condensation. Stem Cells. 2015;16(5):556‐565. doi:10.1016/j.stem.2015.03.004.T
Takebe T, Sekine K, Kimura M, et al. Massive and reproducible production of liver buds entirely from human pluripotent stem cells. Cell Rep. 2017;21(10):2661‐2670. doi:10.1016/j.celrep.2017.11.005
Taguchi A, Nishinakamura R. Higher‐order kidney organogenesis from pluripotent stem cells. Cell Stem Cell. 2017;21(6):730‐746.e6. doi:10.1016/j.stem.2017.10.011
Yang WY, Chen LC, Jhuang YT, et al. Injection of hybrid 3D spheroids composed of podocytes, mesenchymal stem cells, and vascular endothelial cells into the renal cortex improves kidney function and replenishes glomerular podocytes. Bioeng Transl Med. 2021;6(2):1‐12. doi:10.1002/btm2.10212
Faria J, Ahmed S, Gerritsen KGF, Mihaila SM, Masereeuw R. Kidney‐based in vitro models for drug‐induced toxicity testing. Arch Toxicol. 2019;93(12):3397‐3418. doi:10.1007/s00204-019-02598-0
Garreta E, Prado P, Tarantino C, et al. Fine tuning the extracellular environment accelerates the derivation of kidney organoids from human pluripotent stem cells. Nat Mater. 2019;18(4):397‐405. doi:10.1038/s41563-019-0287-6
Xinaris C, Benedetti V, Novelli R, et al. Functional human podocytes generated in organoids from amniotic fluid stem cells. J Am Soc Nephrol. 2016;27(5):1400‐1411. doi:10.1681/ASN.2015030316
Sys GML, Lapeire L, Stevens N, et al. The in ovo CAM‐assay as a xenograft model for sarcoma. J Vis Exp. 2013;77:1‐7. doi:10.3791/50522
Holloway EM, Capeling MM, Spence JR. Biologically inspired approaches to enhance human organoid complexity. Development (Cambridge). 2019;146(8):1‐13. doi:10.1242/dev.166173
Dhimolea E, Maffini MV, Soto AM, Sonnenschein C. The role of collagen reorganization on mammary epithelial morphogenesis in a 3D culture model. Biomaterials. 2010;31(13):3622‐3630. doi:10.1016/j.biomaterials.2010.01.077
Hall MS, Alisafaei F, Ban E, et al. Fibrous nonlinear elasticity enables positive mechanical feedback between cells and ECMs. Proc Natl Acad Sci USA. 2016;113(49):14043‐14048. doi:10.1073/pnas.1613058113
Abdollahzadeh F, Khoshdel‐Rad N, Moghadasali R. Kidney development and function: ECM cannot be ignored. Differentiation. 2022;124:28‐42. doi:10.1016/J.DIFF.2022.02.001
Sachs N, Tsukamoto Y, Kujala P, Peters PJ, Clevers H. Intestinal epithelial organoids fuse to form self‐organizing tubes in floating collagen gels. Development. 2017;144(6):1107‐1112. doi:10.1242/dev.143933
Buchmann B, Engelbrecht LK, Fernandez P, et al. Mechanical plasticity of collagen directs branch elongation in human mammary gland organoids. Nat Commun. 2021;12(1):2759. doi:10.1038/s41467-021-22988-2
Emerman JT, Pitelka DR. Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes. In Vitro. 1977;13(5):316‐328. doi:10.1007/BF02616178