Kidney organoid systems for studies of immune-mediated kidney diseases: challenges and opportunities.
Immune cells
Immune cell–epithelial cell interaction
Immune-mediated kidney diseases
Kidney organoids
Tubuloids
Journal
Cell and tissue research
ISSN: 1432-0878
Titre abrégé: Cell Tissue Res
Pays: Germany
ID NLM: 0417625
Informations de publication
Date de publication:
Aug 2021
Aug 2021
Historique:
received:
03
04
2021
accepted:
23
06
2021
pubmed:
27
7
2021
medline:
19
2
2022
entrez:
26
7
2021
Statut:
ppublish
Résumé
Acute and chronic kidney diseases are major contributors to morbidity and mortality in the global population. Many nephropathies are considered to be immune-mediated with dysregulated immune responses playing an important role in the pathogenesis. At present, targeted approaches for many kidney diseases are still lacking, as the underlying mechanisms remain insufficiently understood. With the recent development of organoids-a three-dimensional, multicellular culture system, which recapitulates important aspects of human tissues-new opportunities to investigate interactions between renal cells and immune cells in the pathogenesis of kidney diseases arise. To date, kidney organoid systems, which reflect the structure and closer resemble critical aspects of the organ, have been established. Here, we highlight the recent advances in the development of kidney organoid models, including pluripotent stem cell-derived kidney organoids and primary epithelial cell-based tubuloids. The employment and further required advances of current organoid models are discussed to investigate the role of the immune system in renal tissue development, regeneration, and inflammation to identify targets for the development of novel therapeutic approaches of immune-mediated kidney diseases.
Identifiants
pubmed: 34309728
doi: 10.1007/s00441-021-03499-4
pii: 10.1007/s00441-021-03499-4
pmc: PMC8310776
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
457-473Subventions
Organisme : DFG
ID : CRC1192
Informations de copyright
© 2021. The Author(s).
Références
Allam R, Scherbaum CR, Darisipudi MN et al (2012) Histones from dying renal cells aggravate kidney injury via TLR2 and TLR4. J Am Soc Nephrol 23:1375–1388. https://doi.org/10.1681/ASN.2011111077
doi: 10.1681/ASN.2011111077
pubmed: 22677551
pmcid: 3402284
Almaani S, Meara A, Rovin BH (2017) Update on Lupus Nephritis. Clin J Am Soc Nephrol 12:825 LP – 835. https://doi.org/10.2215/CJN.05780616
Banas MC, Banas B, Hudkins KL et al (2008) TLR4 links podocytes with the innate immune system to mediate glomerular injury. J Am Soc Nephrol 19:704–713. https://doi.org/10.1681/ASN.2007040395
doi: 10.1681/ASN.2007040395
pubmed: 18256364
pmcid: 2390962
Banu N, Meyers CM (1999) IFN-γ and LPS differentially modulate class II MHC and B7–1 expression on murine renal tubular epithelial cells. Kidney Int 55:2250–2263. https://doi.org/10.1046/j.1523-1755.1999.00495.x
Bar-Ephraim YE, Kretzschmar K, Clevers H (2020) Organoids in immunological research. Nat Rev Immunol 20:279–293. https://doi.org/10.1038/s41577-019-0248-y
doi: 10.1038/s41577-019-0248-y
pubmed: 31853049
Beck LH, Bonegio RGB, Lambeau G et al (2009) M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N Engl J Med 361:11–21. https://doi.org/10.1056/NEJMoa0810457
doi: 10.1056/NEJMoa0810457
pubmed: 19571279
pmcid: 2762083
Berger K, Bangen JM, Hammerich L et al (2014) Origin of regenerating tubular cells after acute kidney injury. Proc Natl Acad Sci 111:1533 LP – 1538. https://doi.org/10.1073/pnas.1316177111
Berthoux F, Suzuki H, Thibaudin L et al (2012) Autoantibodies targeting galactose-deficient IgA1 associate with progression of IgA nephropathy. J Am Soc Nephrol 23:1579 LP – 1587. https://doi.org/10.1681/ASN.2012010053
Bishop GA, Waugh JA, Hall BM (1988) Expression of hla antigens on renal tubular cells in culture: II. Effect of increased hla antigen expression on tubular cell stimulation of lymphocyte activation and on their vulnerability to cell-mediated lysis. Transplantation 46:303–310. https://doi.org/10.1097/00007890-198808000-00022
doi: 10.1097/00007890-198808000-00022
pubmed: 2970135
Biton M, Haber AL, Rogel N et al (2018) T helper cell cytokines modulate intestinal stem cell renewal and differentiation. Cell 175:1307–1320.e22. https://doi.org/10.1016/j.cell.2018.10.008
Bohle A (1994) On the pathogenesis of chronic renal failure in primary glomerulopathies: A view from the interstitium. Exp Nephrol 2:205–210
pubmed: 8069656
Braun F, Homeyer I, Alachkar N, Huber TB (2021) Immune-mediated entities of (primary) focal segmental glomerulosclerosis. Cell Tissue Res. https://doi.org/10.1007/s00441-021-03454-3
doi: 10.1007/s00441-021-03454-3
pubmed: 34820703
pmcid: 8821047
Calandrini C, Schutgens F, Oka R et al (2020) An organoid biobank for childhood kidney cancers that captures disease and tissue heterogeneity. Nat Commun 11:1310. https://doi.org/10.1038/s41467-020-15155-6
doi: 10.1038/s41467-020-15155-6
pubmed: 32161258
pmcid: 7066173
Cantrell DA, Smith KA (1984) The interleukin-2 T-cell system: a new cell growth model. Science (80- ) 224:1312 LP – 1316. https://doi.org/10.1126/science.6427923
Cao Q, Wang Y, Zheng D et al (2010) IL-10/TGF-β–modified macrophages induce regulatory T cells and protect against adriamycin nephrosis. J Am Soc Nephrol 21:933 LP – 942. https://doi.org/10.1681/ASN.2009060592
Cattaneo CM, Dijkstra KK, Fanchi LF et al (2020) Tumor organoid–T-cell coculture systems. Nat Protoc 15:15–39. https://doi.org/10.1038/s41596-019-0232-9
doi: 10.1038/s41596-019-0232-9
pubmed: 31853056
Christensen SR, Shupe J, Nickerson K et al (2006) Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus. Immunity 25:417–428. https://doi.org/10.1016/j.immuni.2006.07.013
Chua CW, Shibata M, Lei M et al (2014) Single luminal epithelial progenitors can generate prostate organoids in culture. Nat Cell Biol 16:951–961. https://doi.org/10.1038/ncb3047
doi: 10.1038/ncb3047
pubmed: 25241035
pmcid: 4183706
Chung SA, Brown EE, Williams AH et al (2014) Lupus nephritis susceptibility loci in women with systemic lupus erythematosus. J Am Soc Nephrol 25:2859–2870. https://doi.org/10.1681/ASN.2013050446
doi: 10.1681/ASN.2013050446
pubmed: 24925725
pmcid: 4243339
Clevers H (2016) Modeling development and disease with organoids. Cell 165:1586–1597. https://doi.org/10.1016/j.cell.2016.05.082
Clynes R, Dumitru C, Ravetch JV (1998) Uncoupling of immune complex formation and kidney damage in autoimmune glomerulonephritis. Science (80- ) 279:1052 LP – 1054. https://doi.org/10.1126/science.279.5353.1052
Combes AN, Zappia L, Er PX et al (2019) Single-cell analysis reveals congruence between kidney organoids and human fetal kidney. Genome Med 11:3. https://doi.org/10.1186/s13073-019-0615-0
doi: 10.1186/s13073-019-0615-0
pubmed: 30674341
pmcid: 6345028
Cortes-Selva D, Ready A, Gibbs L et al (2019) IL-4 promotes stromal cell expansion and is critical for development of a type-2, but not a type 1 immune response. Eur J Immunol 49:428–442. https://doi.org/10.1002/eji.201847789
doi: 10.1002/eji.201847789
pubmed: 30575951
pmcid: 6953475
Couser WG (1988) Rapidly progressive glomerulonephritis: classification, pathogenetic mechanisms, and therapy. Am J Kidney Dis 11:449–464. https://doi.org/10.1016/S0272-6386(88)80079-9
doi: 10.1016/S0272-6386(88)80079-9
pubmed: 3287904
Cressman DE, Greenbaum LE, DeAngelis RA et al (1996) Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science (80- ) 274:1379 LP – 1383. https://doi.org/10.1126/science.274.5291.1379
DeAngelis RA, Markiewski MM, Kourtzelis I et al (2012) A complement–IL-4 regulatory circuit controls liver regeneration. J Immunol 188:641 LP – 648. https://doi.org/10.4049/jimmunol.1101925
Demmers MWHJ, Baan CC, van Beelen E et al (2013) Differential effects of activated human renal epithelial cells on T-cell migration. PLoS One 8:e64916–e64916. https://doi.org/10.1371/journal.pone.0064916
doi: 10.1371/journal.pone.0064916
pubmed: 23717673
pmcid: 3661561
Dijkstra KK, Cattaneo CM, Weeber F et al (2018) Generation of tumor-reactive t cells by co-culture of peripheral blood lymphocytes and tumor organoids. Cell 174:1586-1598.e12. https://doi.org/10.1016/j.cell.2018.07.009
doi: 10.1016/j.cell.2018.07.009
pubmed: 30100188
pmcid: 6558289
Disteldorf EM, Krebs CF, Paust HJ et al (2015) CXCL5 drives neutrophil recruitment in TH17-mediated GN. J Am Soc Nephrol 26:55 LP – 66. https://doi.org/10.1681/ASN.2013101061
Dong X, Swaminathan S, Bachman LA et al (2005) Antigen presentation by dendritic cells in renal lymph nodes is linked to systemic and local injury to the kidney. Kidney Int 68:1096–1108. https://doi.org/10.1111/j.1523-1755.2005.00502.x
doi: 10.1111/j.1523-1755.2005.00502.x
pubmed: 16105040
Eiraku M, Watanabe K, Matsuo-Takasaki M et al (2008) Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3:519–532. https://doi.org/10.1016/j.stem.2008.09.002
doi: 10.1016/j.stem.2008.09.002
pubmed: 18983967
Feng Y, Ren J, Gui Y et al (2018) Wnt/β-catenin-promoted macrophage alternative activation contributes to kidney fibrosis. J Am Soc Nephrol 29:182–193. https://doi.org/10.1681/ASN.2017040391
doi: 10.1681/ASN.2017040391
pubmed: 29021383
Ferenbach D, Hughes J (2008) Macrophages and dendritic cells: what is the difference? Kidney Int 74:5–7. https://doi.org/10.1038/ki.2008.189
Flach TL, Ng G, Hari A et al (2011) Alum interaction with dendritic cell membrane lipids is essential for its adjuvanticity. Nat Med 17:479–487. https://doi.org/10.1038/nm.2306
doi: 10.1038/nm.2306
pubmed: 21399646
Forbes TA, Howden SE, Lawlor K et al (2018) Patient-iPSC-derived kidney organoids show functional validation of a ciliopathic renal phenotype and reveal underlying pathogenetic mechanisms. Am J Hum Genet 102:816–831. https://doi.org/10.1016/j.ajhg.2018.03.014
Franklin BS, Mangan MS, Latz E (2016) Crystal formation in inflammation. Annu Rev Immunol 34:173–202. https://doi.org/10.1146/annurev-immunol-041015-055539
doi: 10.1146/annurev-immunol-041015-055539
pubmed: 26772211
Frasca L, Marelli-Berg F, Imami N et al (1998) Interferon-γ-treated renal tubular epithelial cells induce allospecific tolerance. Kidney Int 53:679–689. https://doi.org/10.1046/j.1523-1755.1998.00800.x
Freedman BS, Brooks CR, Lam AQ et al (2015) Modelling kidney disease with CRISPR-mutant kidney organoids derived from human pluripotent epiblast spheroids. Nat Commun 6:8715. https://doi.org/10.1038/ncomms9715
doi: 10.1038/ncomms9715
pubmed: 26493500
Gijzen L, Yousef Yengej FA, Schutgens F et al (2021) Culture and analysis of kidney tubuloids and perfused tubuloid cells-on-a-chip. Nat Protoc 16:2023–2050. https://doi.org/10.1038/s41596-020-00479-w
doi: 10.1038/s41596-020-00479-w
pubmed: 33674788
Goldwich A, Burkard M, Ölke M et al (2013) Podocytes are nonhematopoietic professional antigen-presenting cells. J Am Soc Nephrol 24:906–916. https://doi.org/10.1681/ASN.2012020133
doi: 10.1681/ASN.2012020133
pubmed: 23539760
pmcid: 3665387
Goodnow CC (2007) Multistep pathogenesis of autoimmune disease. Cell 130:25–35. https://doi.org/10.1016/j.cell.2007.06.033
Gottschalk C, Damuzzo V, Gotot J et al (2013) Batf3-dependent dendritic cells in the renal lymph node induce tolerance against circulating antigens. J Am Soc Nephrol 24:543 LP – 549. https://doi.org/10.1681/ASN.2012101022
Graham RR, Ortmann W, Rodine P et al (2007) Specific combinations of HLA-DR2 and DR3 class II haplotypes contribute graded risk for disease susceptibility and autoantibodies in human SLE. Eur J Hum Genet 15:823–830. https://doi.org/10.1038/sj.ejhg.5201827
doi: 10.1038/sj.ejhg.5201827
pubmed: 17406641
Grote D, Souabni A, Busslinger M, Bouchard M (2006) Pax2/8-regulated Gata3 expression is necessary for morphogenesis and guidance of the nephric duct in the developing kidney. Development 133:53 LP – 61. https://doi.org/10.1242/dev.02184
Hacker BC, Gomez JD, Batista CAS, Rafat M (2019) Growth and characterization of irradiated organoids from mammary glands. J vis Exp. https://doi.org/10.3791/59293.10.3791/59293
doi: 10.3791/59293.10.3791/59293
pubmed: 31475976
Haddad E, Moura IC, Arcos-Fajardo M et al (2003) Enhanced expression of the CD71 mesangial IgA1 receptor in Berger disease and Henoch-Schönlein nephritis: association between CD71 expression and IgA deposits. J Am Soc Nephrol 14:327 LP – 337. https://doi.org/10.1097/01.ASN.0000046961.04917.83
Hale LJ, Howden SE, Phipson B et al (2018) 3D organoid-derived human glomeruli for personalised podocyte disease modelling and drug screening. Nat Commun 9:5167. https://doi.org/10.1038/s41467-018-07594-z
doi: 10.1038/s41467-018-07594-z
pubmed: 30514835
pmcid: 6279764
Henny FC, Weening JJ, Baldwin WM et al (1986) Expression of HLA-DR antigens on peripheral blood T lymphocytes and renal graft tubular epithelial cells in association with rejection. Transplantation 42:479–483. https://doi.org/10.1097/00007890-198611000-00007
doi: 10.1097/00007890-198611000-00007
pubmed: 3024368
Hollywood JA, Przepiorski A, D’Souza RF et al (2020) Use of human induced pluripotent stem cells and kidney organoids to develop a cysteamine/mTOR Inhibition Combination Therapy for Cystinosis. J Am Soc Nephrol ASN.2019070712. https://doi.org/10.1681/ASN.2019070712
Homan KA, Gupta N, Kroll KT et al (2019) Flow-enhanced vascularization and maturation of kidney organoids in vitro. Nat Methods 16:255–262. https://doi.org/10.1038/s41592-019-0325-y
doi: 10.1038/s41592-019-0325-y
pubmed: 30742039
pmcid: 6488032
Hou W, Li S, Wu Y et al (2009) Inhibition of indoleamine 2, 3-dioxygenase-mediated tryptophan catabolism accelerates crescentic glomerulonephritis. Clin Exp Immunol 156:363–372. https://doi.org/10.1111/j.1365-2249.2009.03902.x
doi: 10.1111/j.1365-2249.2009.03902.x
pubmed: 19302241
pmcid: 2759486
Howden SE, Little MH (2020) Generating kidney organoids from human pluripotent stem cells using defined conditions BT-stem cells and tissue repair: methods and protocols. In: Kioussi C (ed). Springer US, New York, NY, pp 183–192
Hu W, Lin J, Lian X et al (2019) M2a and M2b macrophages predominate in kidney tissues and M2 subpopulations were associated with the severity of disease of IgAN patients. Clin Immunol 205:8–15. https://doi.org/10.1016/j.clim.2019.05.005
Huch M, Bonfanti P, Boj SF et al (2013) Unlimited in vitro expansion of adult bi-potent pancreas progenitors through the Lgr5/R-spondin axis. EMBO J 32:2708–2721. https://doi.org/10.1038/emboj.2013.204
Huch M, Gehart H, van Boxtel R et al (2015) Long-term culture of genome-stable bipotent stem cells from adult human liver. Cell 160:299–312. https://doi.org/10.1016/j.cell.2014.11.050
doi: 10.1016/j.cell.2014.11.050
pubmed: 25533785
pmcid: 4313365
Hume DA, Gordon S (1983) Mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80. Identification of resident macrophages in renal medullary and cortical interstitium and the juxtaglomerular complex. J Exp Med 157:1704–1709. https://doi.org/10.1084/jem.157.5.1704
doi: 10.1084/jem.157.5.1704
pubmed: 6854206
pmcid: 2186998
Jayme TS, Leung G, Wang A et al (2020) Human interleukin-4–treated regulatory macrophages promote epithelial wound healing and reduce colitis in a mouse model. Sci Adv 6:eaba4376. https://doi.org/10.1126/sciadv.aba4376
Kaissling B, Le Hir M (1994) Characterization and distribution of interstitial cell types in the renal cortex of rats. Kidney Int 45:709–720. https://doi.org/10.1038/ki.1994.95
Kang HM, Huang S, Reidy K et al (2016) Sox9-positive progenitor cells play a key role in renal tubule epithelial regeneration in mice. Cell Rep 14:861–871. https://doi.org/10.1016/j.celrep.2015.12.071
Karin M, Clevers H (2016) Reparative inflammation takes charge of tissue regeneration. Nature 529:307–315. https://doi.org/10.1038/nature17039
doi: 10.1038/nature17039
pubmed: 26791721
pmcid: 5228603
Kassianos AJ, Sampangi S, Wang X et al (2013) Human proximal tubule epithelial cells modulate autologous dendritic cell function. Nephrol Dial Transplant 28:303–312. https://doi.org/10.1093/ndt/gfs136
doi: 10.1093/ndt/gfs136
pubmed: 22610986
Kessler M, Hoffmann K, Brinkmann V et al (2015) The Notch and Wnt pathways regulate stemness and differentiation in human fallopian tube organoids. Nat Commun 6:8989. https://doi.org/10.1038/ncomms9989
doi: 10.1038/ncomms9989
pubmed: 26643275
Kluth DC, Ainslie C V, Pearce WP et al (2001) Macrophages transfected with adenovirus to express IL-4 reduce inflammation in experimental glomerulonephritis. J Immunol 166:4728 LP – 4736. https://doi.org/10.4049/jimmunol.166.7.4728
Kopp JB, Anders HJ, Susztak K et al (2020) Podocytopathies Nat Rev Dis Prim 6:68. https://doi.org/10.1038/s41572-020-0196-7
doi: 10.1038/s41572-020-0196-7
pubmed: 32792490
Krebs CF, Panzer U (2018) Plasticity and heterogeneity of Th17 in immune-mediated kidney diseases. J Autoimmun 87:61–68. https://doi.org/10.1016/j.jaut.2017.12.005
Krebs CF, Paust HJ, Krohn S et al (2016) Autoimmune renal disease is exacerbated by S1P-receptor-1-dependent intestinal Th17 cell migration to the kidney. Immunity 45:1078–1092. https://doi.org/10.1016/j.immuni.2016.10.020
doi: 10.1016/j.immuni.2016.10.020
pubmed: 27851911
pmcid: 6381450
Krebs CF, Reimers D, Zhao Y et al (2020) Pathogen-induced tissue-resident memory TH17 (TRM17) cells amplify autoimmune kidney disease. Sci Immunol 5:eaba4163. https://doi.org/10.1126/sciimmunol.aba4163
Krebs CF, Schmidt T, Riedel JH, Panzer U (2017) T helper type 17 cells in immune-mediated glomerular disease. Nat Rev Nephrol 13:647–659. https://doi.org/10.1038/nrneph.2017.112
doi: 10.1038/nrneph.2017.112
pubmed: 28781371
Krohn S, Nies JF, Kapffer S et al (2018) IL-17C/IL-17 receptor E signaling in CD4+ T cells promotes TH17 cell-driven glomerular inflammation. J Am Soc Nephrol 29:1210 LP – 1222. https://doi.org/10.1681/ASN.2017090949
Kumar S V, Er PX, Lawlor KT et al (2019) Kidney micro-organoids in suspension culture as a scalable source of human pluripotent stem cell-derived kidney cells. Development 146:dev172361. https://doi.org/10.1242/dev.172361
Kurts C, Panzer U, Anders HJ, Rees AJ (2013) The immune system and kidney disease: basic concepts and clinical implications. Nat Rev Immunol 13:738–753. https://doi.org/10.1038/nri3523
doi: 10.1038/nri3523
pubmed: 24037418
Lancaster MA, Louie CM, Silhavy JL et al (2009) Impaired Wnt–β-catenin signaling disrupts adult renal homeostasis and leads to cystic kidney ciliopathy. Nat Med 15:1046–1054. https://doi.org/10.1038/nm.2010
doi: 10.1038/nm.2010
pubmed: 19718039
pmcid: 2895985
Lancaster MA, Renner M, Martin CA et al (2013) Cerebral organoids model human brain development and microcephaly. Nature 501:373–379. https://doi.org/10.1038/nature12517
doi: 10.1038/nature12517
pubmed: 23995685
Lee AS, Tang C, Rao MS et al (2013) Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies. Nat Med 19:998–1004. https://doi.org/10.1038/nm.3267
doi: 10.1038/nm.3267
pubmed: 23921754
pmcid: 3967018
Lee PY, Kumagai Y, Li Y et al (2008) TLR7-dependent and FcgammaR-independent production of type I interferon in experimental mouse lupus. J Exp Med 205:2995–3006. https://doi.org/10.1084/jem.20080462
doi: 10.1084/jem.20080462
pubmed: 19047436
pmcid: 2605237
Leemans JC, Stokman G, Claessen N et al (2005) Renal-associated TLR2 mediates ischemia/reperfusion injury in the kidney. J Clin Invest 115:2894–2903. https://doi.org/10.1172/JCI22832
doi: 10.1172/JCI22832
pubmed: 16167081
pmcid: 1201659
Lemos DR, McMurdo M, Karaca G et al (2018) Interleukin-1β activates a MYC-dependent metabolic switch in kidney stromal cells necessary for progressive tubulointerstitial fibrosis. J Am Soc Nephrol 29:1690 LP – 1705. https://doi.org/10.1681/ASN.2017121283
Li S, Liu Y, He Y et al (2020) Podocytes present antigen to activate specific T cell immune responses in inflammatory renal disease. J Pathol 252:e5508. https://doi.org/10.1002/path.5508
Lin SL, Castaño AP, Nowlin BT et al (2009) Bone marrow Ly6C high monocytes are selectively recruited to injured kidney and differentiate into functionally distinct populations. J Immunol 183:6733 LP – 6743. https://doi.org/10.4049/jimmunol.0901473
Lindemans CA, Calafiore M, Mertelsmann AM et al (2015) Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature 528:560–564. https://doi.org/10.1038/nature16460
doi: 10.1038/nature16460
pubmed: 26649819
pmcid: 4720437
Little M, Georgas K, Pennisi D, Wilkinson L (2010) Chapter Five—Kidney development: two tales of tubulogenesis. In: Koopman PBT-CT in DB (ed) Organogenesis in development. Academic Press pp 193–229
Little MH, Combes AN (2019) Kidney organoids: accurate models or fortunate accidents. Genes Dev 33:1319–1345. https://doi.org/10.1101/gad.329573.119
doi: 10.1101/gad.329573.119
pubmed: 31575677
pmcid: 6771389
Liu B, Yang Y, Dai J et al (2006) TLR4 up-regulation at protein or gene level is pathogenic for lupus-like autoimmune disease. J Immunol 177:6880 LP – 6888. https://doi.org/10.4049/jimmunol.177.10.6880
Liu P, Lassén E, Nair V et al (2017) Transcriptomic and proteomic profiling provides insight into mesangial cell function in IgA nephropathy. J Am Soc Nephrol 28:2961–2972. https://doi.org/10.1681/ASN.2016101103
doi: 10.1681/ASN.2016101103
pubmed: 28646076
pmcid: 5619958
Lugli N, Kamileri I, Keogh A et al (2016) R-spondin 1 and noggin facilitate expansion of resident stem cells from non-damaged gallbladders. EMBO Rep 17:769–779. https://doi.org/10.15252/embr.201642169
Lukacs-Kornek V, Burgdorf S, Diehl L et al (2008) The kidney-renal lymph node-system contributes to cross-tolerance against innocuous circulating antigen. J Immunol 180:706 LP – 715. https://doi.org/10.4049/jimmunol.180.2.706
Molyneux K, Wimbury D, Pawluczyk I et al (2017) β1,4-galactosyltransferase 1 is a novel receptor for IgA in human mesangial cells. Kidney Int 92:1458–1468. https://doi.org/10.1016/j.kint.2017.05.002
Monteil V, Kwon H, Prado P et al (2020) Inhibition of SARS-CoV-2 infections in engineered human tissues using clinical-grade soluble human ACE2. Cell 181:905–913.e7. https://doi.org/10.1016/j.cell.2020.04.004
Morizane R, Lam AQ, Freedman BS et al (2015) Nephron organoids derived from human pluripotent stem cells model kidney development and injury. Nat Biotechnol 33:1193–1200. https://doi.org/10.1038/nbt.3392
doi: 10.1038/nbt.3392
pubmed: 26458176
pmcid: 4747858
Moura IC, Arcos-Fajardo M, Gdoura A et al (2005) Engagement of transferrin receptor by polymeric IgA1: evidence for a positive feedback loop involving increased receptor expression and mesangial cell proliferation in iga nephropathy. J Am Soc Nephrol 16:2667 LP – 2676. https://doi.org/10.1681/ASN.2004111006
Munroe ME, James JA (2015) Genetics of lupus nephritis: clinical implications. Semin Nephrol 35:396–409. https://doi.org/10.1016/j.semnephrol.2015.08.002
doi: 10.1016/j.semnephrol.2015.08.002
pubmed: 26573543
pmcid: 4653095
Murray I, Paolini MA (2020) Histology, kidney and gloerulus. In: StatPearls Publ. https://www.ncbi.nlm.nih.gov/books/NBK554544/
Nagata M, Nakayama K, Terada Y et al (1998) Cell cycle regulation and differentiation in the human podocyte lineage. Am J Pathol 153:1511–1520. https://doi.org/10.1016/S0002-9440(10)65739-2
doi: 10.1016/S0002-9440(10)65739-2
pubmed: 9811343
pmcid: 1853414
Naji A, Menier C, Morandi F et al (2014) Binding of HLA-G to ITIM-bearing Ig-like transcript 2 receptor suppresses B cell responses. J Immunol 192:1536 LP – 1546. https://doi.org/10.4049/jimmunol.1300438
Nelson PJ, Rees AJ, Griffin MD et al (2012) The renal mononuclear phagocytic system. J Am Soc Nephrol 23:194 LP – 203. https://doi.org/10.1681/ASN.2011070680
Ng G, Sharma K, Ward SM et al (2008) Receptor-independent, direct membrane binding leads to cell-surface lipid sorting and Syk kinase activation in dendritic cells. Immunity 29:807–818. https://doi.org/10.1016/j.immuni.2008.09.013
doi: 10.1016/j.immuni.2008.09.013
pubmed: 18993083
pmcid: 2642965
Niu Z, Zhang P, Tong Y (2015) Value of HLA-DR genotype in systemic lupus erythematosus and lupus nephritis: a meta-analysis. Int J Rheum Dis 18:17–28. https://doi.org/10.1111/1756-185X.12528
Olaru F, Wang X-P, Luo W et al (2013) Proteolysis breaks tolerance toward Intact α345(IV) collagen, eliciting novel anti–glomerular basement membrane autoantibodies specific for α345NC1 hexamers. J Immunol 190:1424 LP – 1432. https://doi.org/10.4049/jimmunol.1202204
Paust HJ, Turner JE, Riedel JH et al (2012) Chemokines play a critical role in the cross-regulation of Th1 and Th17 immune responses in murine crescentic glomerulonephritis. Kidney Int 82:72–83. https://doi.org/10.1038/ki.2012.101
doi: 10.1038/ki.2012.101
pubmed: 22495297
Pedchenko V, Bondar O, Fogo AB et al (2010) Molecular architecture of the goodpasture autoantigen in anti-GBM nephritis. N Engl J Med 363:343–354. https://doi.org/10.1056/NEJMoa0910500
doi: 10.1056/NEJMoa0910500
pubmed: 20660402
pmcid: 4144421
Petrosyan A, Cravedi P, Villani V et al (2019) A glomerulus-on-a-chip to recapitulate the human glomerular filtration barrier. Nat Commun 10:3656. https://doi.org/10.1038/s41467-019-11577-z
doi: 10.1038/s41467-019-11577-z
pubmed: 31409793
pmcid: 6692336
Poladia DP, Kish K, Kutay B et al (2006) Role of fibroblast growth factor receptors 1 and 2 in the metanephric mesenchyme. Dev Biol 291:325–339. https://doi.org/10.1016/j.ydbio.2005.12.034
Praga M, González E (2010) Acute interstitial nephritis. Kidney Int 77:956–961. https://doi.org/10.1038/ki.2010.89
Price AE, Shamardani K, Lugo KA et al (2018) A map of toll-like receptor expression in the intestinal epithelium reveals distinct spatial, cell type-specific, and temporal patterns. Immunity 49:560-575.e6. https://doi.org/10.1016/j.immuni.2018.07.016
doi: 10.1016/j.immuni.2018.07.016
pubmed: 30170812
pmcid: 6152941
Przepiorski A, Sander V, Tran T et al (2018) A simple bioreactor-based method to generate kidney organoids from pluripotent stem cells. Stem Cell Reports 11:470–484. https://doi.org/10.1016/j.stemcr.2018.06.018
doi: 10.1016/j.stemcr.2018.06.018
pubmed: 30033089
pmcid: 6092837
Qi F, Adair A, Ferenbach D et al (2008) Depletion of cells of monocyte lineage prevents loss of renal microvasculature in murine kidney transplantation. Transplantation 86:
Rewa O, Bagshaw SM (2014) Acute kidney injury—epidemiology, outcomes and economics. Nat Rev Nephrol 10:193–207. https://doi.org/10.1038/nrneph.2013.282
doi: 10.1038/nrneph.2013.282
pubmed: 24445744
Riedel JH, Turner JE, Panzer U (2021) T helper cell trafficking in autoimmune kidney diseases. Cell Tissue Res. https://doi.org/10.1007/s00441-020-03403-6
doi: 10.1007/s00441-020-03403-6
pubmed: 33598825
pmcid: 8523400
Rogoz A, Reis BS, Karssemeijer RA, Mucida D (2015) A 3-D enteroid-based model to study T-cell and epithelial cell interaction. J Immunol Methods 421:89–95. https://doi.org/10.1016/j.jim.2015.03.014
Ruiz-Ortega M, Rayego-Mateos S, Lamas S et al (2020) Targeting the progression of chronic kidney disease. Nat Rev Nephrol 16:269–288. https://doi.org/10.1038/s41581-019-0248-y
doi: 10.1038/s41581-019-0248-y
pubmed: 32060481
Sachs N, Papaspyropoulos A, Zomer-van Ommen DD et al (2019) Long-term expanding human airway organoids for disease modeling. EMBO J 38:e100300. https://doi.org/10.15252/embj.2018100300
Sampangi S, Wang X, Beagley KW et al (2015) Human proximal tubule epithelial cells modulate autologous B-cell function. Nephrol Dial Transplant 30:1674–1683. https://doi.org/10.1093/ndt/gfv242
doi: 10.1093/ndt/gfv242
pubmed: 26058593
Sato T, Vries RG, Snippert HJ et al (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459:262–265. https://doi.org/10.1038/nature07935
doi: 10.1038/nature07935
pubmed: 19329995
Schene IF, Joore IP, Oka R et al (2020) Prime editing for functional repair in patient-derived disease models. Nat Commun 11:5352. https://doi.org/10.1038/s41467-020-19136-7
doi: 10.1038/s41467-020-19136-7
pubmed: 33097693
pmcid: 7584657
Schreurs RRCE, Baumdick ME, Sagebiel AF et al (2019) Human fetal TNF-α;-cytokine-producing CD4
doi: 10.1016/j.immuni.2018.12.010
pubmed: 30770246
Schutgens F, Rookmaaker MB, Margaritis T et al (2019) Tubuloids derived from human adult kidney and urine for personalized disease modeling. Nat Biotechnol 37:303–313. https://doi.org/10.1038/s41587-019-0048-8
doi: 10.1038/s41587-019-0048-8
pubmed: 30833775
Segerer S, Heller F, Lindenmeyer MT et al (2008) Compartment specific expression of dendritic cell markers in human glomerulonephritis. Kidney Int 74:37–46. https://doi.org/10.1038/ki.2008.99
Shankland SJ, Pippin JW, Duffield JS (2014) Progenitor cells and podocyte regeneration. Semin Nephrol 34:418–428. https://doi.org/10.1016/j.semnephrol.2014.06.008
doi: 10.1016/j.semnephrol.2014.06.008
pubmed: 25217270
pmcid: 4163204
Shao DD, Suresh R, Vakil V et al (2008) Pivotal advance: Th-1 cytokines inhibit, and Th-2 cytokines promote fibrocyte differentiation. J Leukoc Biol 83:1323–1333. https://doi.org/10.1189/jlb.1107782
doi: 10.1189/jlb.1107782
pubmed: 18332234
Smith KD (2009) Toll-like receptors in kidney disease. Curr Opin Nephrol Hypertens 18:189–196. https://doi.org/10.1097/MNH.0b013e32832a1d5f
doi: 10.1097/MNH.0b013e32832a1d5f
pubmed: 19352178
pmcid: 2896868
Sommer AG, Rozelle SS, Sullivan S et al (2012) Generation of human induced pluripotent stem cells from peripheral blood using the STEMCCA lentiviral vector. J vis Exp 4327. https://doi.org/10.3791/4327
Soos TJ, Sims TN, Barisoni L et al (2006) CX3CR1+ interstitial dendritic cells form a contiguous network throughout the entire kidney. Kidney Int 70:591–596. https://doi.org/10.1038/sj.ki.5001567
Spence JR, Mayhew CN, Rankin SA et al (2011) Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 470:105–109. https://doi.org/10.1038/nature09691
doi: 10.1038/nature09691
pubmed: 21151107
Stanley JC, Deng H (2020) Progress in pathogenesis of immunoglobin a nephropathy. Cureus 12:e8789–e8789. https://doi.org/10.7759/cureus.8789
doi: 10.7759/cureus.8789
pubmed: 32724739
pmcid: 7381842
Starke A, Lindenmeyer MT, Segerer S et al (2010) Renal tubular PD-L1 (CD274) suppresses alloreactive human T-cell responses. Kidney Int 78:38–47. https://doi.org/10.1038/ki.2010.97
doi: 10.1038/ki.2010.97
pubmed: 20393451
Stein M, Keshav S, Harris N, Gordon S (1992) Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med 176:287–292. https://doi.org/10.1084/jem.176.1.287
doi: 10.1084/jem.176.1.287
pubmed: 1613462
Stern JB, Smith KA (1986) Interleukin-2 induction of T-cell G1 progression and c-myb expression. Science (80- ) 233:203 LP – 206. https://doi.org/10.1126/science.3523754
Stout RD, Suttles J (2004) Functional plasticity of macrophages: reversible adaptation to changing microenvironments. J Leukoc Biol 76:509–513. https://doi.org/10.1189/jlb.0504272
doi: 10.1189/jlb.0504272
pubmed: 15218057
Taguchi A, Kaku Y, Ohmori T et al (2014) 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. https://doi.org/10.1016/j.stem.2013.11.010
Taguchi A, Nishinakamura R (2017) Higher-order kidney organogenesis from pluripotent stem cells. Cell Stem Cell 21:730–746.e6. https://doi.org/10.1016/j.stem.2017.10.011
Takahashi K, Tanabe K, Ohnuki M et al (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872. https://doi.org/10.1016/j.cell.2007.11.019
Takasato M, Er PX, Chiu HS et al (2015) Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis. Nature 526:564–568. https://doi.org/10.1038/nature15695
doi: 10.1038/nature15695
pubmed: 26444236
Takebe T, Sekine K, Enomura M et al (2013) Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 499:481–484. https://doi.org/10.1038/nature12271
doi: 10.1038/nature12271
pubmed: 23823721
Tamouza H, Vende F, Tiwari M et al (2007) Transferrin receptor engagement by polymeric IgA1 induces receptor expression and mesangial cell proliferation: role in IgA nephropathy. In: Contributions to nephrology. pp 144–147
Tanigawa S, Islam M, Sharmin S et al (2018) Organoids from nephrotic disease-derived iPSCs identify impaired NEPHRIN localization and slit diaphragm formation in kidney podocytes. Stem Cell Reports 11:727–740. https://doi.org/10.1016/j.stemcr.2018.08.003
Tecklenborg J, Clayton D, Siebert S, Coley SM (2018) The role of the immune system in kidney disease. Clin Exp Immunol 192:142–150. https://doi.org/10.1111/cei.13119
doi: 10.1111/cei.13119
pubmed: 29453850
pmcid: 5904695
Thongboonkerd V (2019) Proteomics of crystal–cell interactions: a model for kidney stone research. Cells 8
Tojo M, Hamashima Y, Hanyu A et al (2005) The ALK-5 inhibitor A-83–01 inhibits Smad signaling and epithelial-to-mesenchymal transition by transforming growth factor-β. Cancer Sci 96:791–800. https://doi.org/10.1111/j.1349-7006.2005.00103.x
Tomas NM, Beck LH Jr, Meyer-Schwesinger C et al (2014) Thrombospondin type-1 domain-containing 7A in idiopathic membranous nephropathy. N Engl J Med 371:2277–2287. https://doi.org/10.1056/NEJMoa1409354
doi: 10.1056/NEJMoa1409354
pubmed: 25394321
pmcid: 4278759
Tomas NM, Huber TB, Hoxha E (2021) Perspectives in membranous nephropathy. Cell Tissue Res. https://doi.org/10.1007/s00441-021-03429-4
doi: 10.1007/s00441-021-03429-4
pubmed: 33864499
pmcid: 8052535
Torres Á, Muñoz K, Nahuelpán Y et al (2020) Intraglomerular monocyte/macrophage infiltration and macrophage–myofibroblast transition during diabetic nephropathy is regulated by the A2B Adenosine Receptor. Cells 9
Tsuboi N, Yoshikai Y, Matsuo S et al (2002) Roles of toll-like receptors in C-C chemokine production by renal tubular epithelial cells. J Immunol 169:2026 LP – 2033. https://doi.org/10.4049/jimmunol.169.4.2026
van den Berg CW, Ritsma L, Avramut MC et al (2018) Renal subcapsular transplantation of PSC-derived kidney organoids induces neo-vasculogenesis and significant glomerular and tubular maturation in vivo. Stem Cell Reports 10:751–765. https://doi.org/10.1016/j.stemcr.2018.01.041
Vernon MA, Mylonas KJ, Hughes J (2010) Macrophages and renal fibrosis. Semin Nephrol 30:302–317. https://doi.org/10.1016/j.semnephrol.2010.03.004
Voehringer D, Reese TA, Huang X et al (2006) Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system. J Exp Med 203:1435–1446. https://doi.org/10.1084/jem.20052448
doi: 10.1084/jem.20052448
pubmed: 16702603
pmcid: 2118302
Wang F, Yin J, Lin Y et al (2020) IL-17C has a pathogenic role in kidney ischemia/reperfusion injury. Kidney Int 97:1219–1229. https://doi.org/10.1016/j.kint.2020.01.015
doi: 10.1016/j.kint.2020.01.015
pubmed: 32331702
Wang Y, Wang Y, Cai Q et al (2008) By homing to the kidney, activated macrophages potently exacerbate renal injury. Am J Pathol 172:1491–1499. https://doi.org/10.2353/ajpath.2008.070825
doi: 10.2353/ajpath.2008.070825
pubmed: 18467704
pmcid: 2408410
Wanner N, Hartleben B, Herbach N et al (2014) Unraveling the role of podocyte turnover in glomerular aging and injury. J Am Soc Nephrol 25:707 LP – 716. https://doi.org/10.1681/ASN.2013050452
Watanabe K, Ueno M, Kamiya D et al (2007) A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 25:681–686. https://doi.org/10.1038/nbt1310
doi: 10.1038/nbt1310
pubmed: 17529971
Weeber F, van de Wetering M, Hoogstraat M et al (2015) Preserved genetic diversity in organoids cultured from biopsies of human colorectal cancer metastases. Proc Natl Acad Sci 112:13308 LP – 13311. https://doi.org/10.1073/pnas.1516689112
Wilkinson R, Wang X, Roper KE, Healy H (2011) Activated human renal tubular cells inhibit autologous immune responses. Nephrol Dial Transplant 26:1483–1492. https://doi.org/10.1093/ndt/gfq677
doi: 10.1093/ndt/gfq677
pubmed: 21045077
Wolfs TGAM, Buurman WA, van Schadewijk A et al (2002) In vivo expression of toll-like receptor 2 and 4 by renal epithelial cells: IFN-γ and TNF-α mediated up-regulation during inflammation. J Immunol 168:1286 LP – 1293. https://doi.org/10.4049/jimmunol.168.3.1286
Workalemahu G, Foerster M, Kroegel C (2004) Expression and synthesis of fibroblast growth factor-9 in human γδ T-lymphocytes. Response to isopentenyl pyrophosphate and TGF-β1/IL-15. J Leukoc Biol 75:657–663. https://doi.org/10.1189/jlb.0902471
Wu H, Chen G, Wyburn KR et al (2007) TLR4 activation mediates kidney ischemia/reperfusion injury. J Clin Invest 117:2847–2859. https://doi.org/10.1172/JCI31008
doi: 10.1172/JCI31008
pubmed: 17853945
pmcid: 1974864
Wu H, Uchimura K, Donnelly EL et al (2018) Comparative analysis and refinement of human PSC-derived kidney organoid differentiation with single-cell transcriptomics. Cell Stem Cell 23:869–881.e8. https://doi.org/10.1016/j.stem.2018.10.010
Wuthrich RP, Yui MA, Mazoujian G et al (1989) Enhanced MHC class II expression in renal proximal tubules precedes loss of renal function in MRL/lpr mice with lupus nephritis. Am J Pathol 134:45–51
pubmed: 2492404
pmcid: 1879559
Wysocki J, Ye M, Hassler L et al (2021) A novel soluble ACE2 variant with prolonged duration of action neutralizes SARS-CoV-2 infection in human kidney organoids. J Am Soc Nephrol 32:795 LP – 803. https://doi.org/10.1681/ASN.2020101537
Xu J, Lamouille S, Derynck R (2009) TGF-β-induced epithelial to mesenchymal transition. Cell Res 19:156–172. https://doi.org/10.1038/cr.2009.5
doi: 10.1038/cr.2009.5
pubmed: 19153598
Xu R, Li Q, Liu R et al (2017) Association analysis of the MHC in lupus bephritis. J Am Soc Nephrol 28:3383–3394. https://doi.org/10.1681/ASN.2016121331
doi: 10.1681/ASN.2016121331
pubmed: 28754791
pmcid: 5661284
Yellin MJ, D’Agati V, Parkinson G et al (1997) Immunohistologic analysis of renal CD40 and CD40L expression in lupus nephritis and other glomerulonephritides. Arthritis Rheum 40:124–134. https://doi.org/10.1002/art.1780400117
Yousef Yengej FA, Jansen J Rookmaaker MB, et al (2020) Kidney organoids and tubuloids. Cells 9
Yuan DH, Jia Y, Hassan OM et al (2020) LPS-treated podocytes polarize naive CD4(+) T Cells into Th17 and treg cells. Biomed Res Int 2020:8587923. https://doi.org/10.1155/2020/8587923
doi: 10.1155/2020/8587923
pubmed: 32509873
pmcid: 7251438
Zea AH, Stewart T, Ascani J et al (2016) Activation of the IL-2 receptor in podocytes: a potential mechanism for podocyte injury in idiopathic nephrotic syndrome? PLoS ONE 11:e0157907–e0157907. https://doi.org/10.1371/journal.pone.0157907
doi: 10.1371/journal.pone.0157907
pubmed: 27389192
pmcid: 4936730
Zhou T, Benda C, Dunzinger S et al (2012) Generation of human induced pluripotent stem cells from urine samples. Nat Protoc 7:2080–2089. https://doi.org/10.1038/nprot.2012.115
doi: 10.1038/nprot.2012.115
pubmed: 23138349
Zhou T, Benda C, Duzinger S et al (2011) Generation of induced pluripotent stem cells from urine. J Am Soc Nephrol 22:1221 LP – 1228. https://doi.org/10.1681/ASN.2011010106
Zimmerman KA, Song CJ, Li Z et al (2019) Tissue-resident macrophages promote renal cystic disease. J Am Soc Nephrol 30:1841 LP – 1856. https://doi.org/10.1681/ASN.2018080810