Novel therapeutic perspectives for crescentic glomerulonephritis through targeting parietal epithelial cell activation and proliferation

References

• Trimarchi H. Crescents in primary glomerulonephritis: a pattern of injury with dissimilar actors. A pathophysiologic perspective. Pediatr Nephrol. 2022 Jun;37(6):1205–1214.
   PubMed Web of Science ®Google Scholar
• Anguiano L, Kain R, Anders HJ. The glomerular crescent: triggers, evolution, resolution, and implications for therapy. Curr Opin Nephrol Hypertens. 2020 May;29(3):302–309.
   PubMed Web of Science ®Google Scholar
• Shankland SJ, Smeets B, Pippin JW, et al. The emergence of the glomerular parietal epithelial cell. Nat Rev Nephrol. 2014 Mar;10(3):158–173.
   PubMed Web of Science ®Google Scholar
• Sethi S, Haas M, Markowitz GS, et al. Mayo clinic/renal pathology society consensus report on pathologic classification, diagnosis, and reporting of GN. J Am Soc Nephrol. 2016 May;27(5):1278–1287.
   PubMed Web of Science ®Google Scholar
• Smeets B, Uhlig S, Fuss A, et al. Tracing the origin of glomerular extracapillary lesions from parietal epithelial cells. J Am Soc Nephrol. 2009 Dec;20(12):2604–2615.
   PubMed Web of Science ®Google Scholar
• Wong MN, Tharaux PL, Grahammer F, et al. Parietal epithelial cell dysfunction in crescentic glomerulonephritis. Cell Tissue Res. 2021 Aug;385(2):345–354.
   PubMed Web of Science ®Google Scholar
• Su H, Chen S, He FF, et al. New insights into glomerular parietal epithelial cell activation and its signaling pathways in glomerular diseases. Biomed Res Int. 2015;2015:318935.
   PubMed Web of Science ®Google Scholar
• Moeller MJ, Smeets B. Role of parietal epithelial cells in kidney injury: the case of rapidly progressing glomerulonephritis and focal and segmental glomerulosclerosis. Nephron Exp Nephrol. 2014;126(2):97.
   PubMedGoogle Scholar
• Al Hussain T, Al Mana H, Hussein MH, et al. Podocyte and parietal epithelial cell interactions in health and disease. Adv Anat Pathol. 2017 Jan;24(1):24–34.
   PubMed Web of Science ®Google Scholar
• Smeets B, Moeller MJ. Parietal epithelial cells and podocytes in glomerular diseases. Semin Nephrol. 2012 Jul;32(4):357–367.
   PubMed Web of Science ®Google Scholar
• Appel D, Kershaw DB, Smeets B, et al. Recruitment of podocytes from glomerular parietal epithelial cells. J Am Soc Nephrol. 2009 Feb;20(2):333–343.
   PubMed Web of Science ®Google Scholar
• Poulsom R, Little MH. Parietal epithelial cells regenerate podocytes. J Am Soc Nephrol. 2009 Feb;20(2):231–233.
   PubMed Web of Science ®Google Scholar
• McAdoo SP, Pusey CD. Anti-glomerular basement membrane disease. Clin J Am Soc Nephrol. 2017 Jul 7;12(7):1162–1172.
   PubMed Web of Science ®Google Scholar
• KDIGO. 2021 clinical practice guideline for the management of glomerular diseases. Kidney Int. 2021 Oct;100(4s):S1–s276.
   PubMedGoogle Scholar
• Morita T, Suzuki Y, Churg J. Structure and development of the glomerular crescent. Am J Pathol. 1973 Sep;72(3):349–368.
   PubMed Web of Science ®Google Scholar
• Singh SK, Jeansson M, Quaggin SE. New insights into the pathogenesis of cellular crescents. Curr Opin Nephrol Hypertens. 2011 May;20(3):258–262.
   PubMed Web of Science ®Google Scholar
• Ryu M, Migliorini A, Miosge N, et al. Plasma leakage through glomerular basement membrane ruptures triggers the proliferation of parietal epithelial cells and crescent formation in non-inflammatory glomerular injury. J Pathol. 2012 Dec;228(4):482–494.
   PubMed Web of Science ®Google Scholar
• Han Y, Tian L, Ma F, et al. Pharmacological inhibition of protease-activated receptor-2 reduces crescent formation in rat nephrotoxic serum nephritis. Clin Exp Pharmacol Physiol. 2019 May;46(5):456–464.
   PubMed Web of Science ®Google Scholar
• Sicking EM, Fuss A, Uhlig S, et al. Subtotal ablation of parietal epithelial cells induces crescent formation. J Am Soc Nephrol. 2012 Apr;23(4):629–640.
   PubMed Web of Science ®Google Scholar
• Ohse T, Chang AM, Pippin JW, et al. A new function for parietal epithelial cells: a second glomerular barrier. Am J Physiol Renal Physiol. 2009 Dec;297(6):F1566–74.
   PubMed Web of Science ®Google Scholar
• Smeets B, Kuppe C, Sicking EM, et al. Parietal epithelial cells participate in the formation of sclerotic lesions in focal segmental glomerulosclerosis. J Am Soc Nephrol. 2011 Jul;22(7):1262–1274.
   PubMed Web of Science ®Google Scholar
• Bariéty J, Bruneval P. Activated parietal epithelial cells or dedifferentiated podocytes in FSGS: can we make the difference? Kidney Int. 2006 Jan;69(1):194.
   PubMed Web of Science ®Google Scholar
• Ohse T, Pippin JW, Chang AM, et al. The enigmatic parietal epithelial cell is finally getting noticed: a review. Kidney Int. 2009 Dec;76(12):1225–1238.
   PubMed Web of Science ®Google Scholar
• Eymael J, Sharma S, Loeven MA, et al. CD44 is required for the pathogenesis of experimental crescentic glomerulonephritis and collapsing focal segmental glomerulosclerosis. Kidney Int. 2018 Mar;93(3):626–642.
   PubMed Web of Science ®Google Scholar
• Kim S, Kim YH, Choi KH, et al. Glomerular epithelial CD44 expression and segmental sclerosis in IgA nephropathy. Clin Exp Nephrol. 2016 Dec;20(6):871–877.
   PubMed Web of Science ®Google Scholar
• Zhao X, Chen X, Chima A, et al. Albumin induces CD44 expression in glomerular parietal epithelial cells by activating extracellular signal-regulated kinase 1/2 pathway. J Cell Physiol. 2019 May;234(5):7224–7235.
   PubMed Web of Science ®Google Scholar
• Miesen L, Steenbergen E, Smeets B. Parietal cells-new perspectives in glomerular disease. Cell Tissue Res. 2017 Jul;369(1):237–244.
   PubMed Web of Science ®Google Scholar
• Roeder SS, Barnes TJ, Lee JS, et al. Activated ERK1/2 increases CD44 in glomerular parietal epithelial cells leading to matrix expansion. Kidney Int. 2017 Apr;91(4):896–913.
   PubMed Web of Science ®Google Scholar
• Roeder SS, Stefanska A, Eng DG, et al. Changes in glomerular parietal epithelial cells in mouse kidneys with advanced age. Am J Physiol Renal Physiol. 2015 Jul 15;309(2):F164–78.
   PubMed Web of Science ®Google Scholar
• Chen A, Lee K, D’Agati VD, et al. Bowman’s capsule provides a protective niche for podocytes from cytotoxic CD8+ T cells. J Clin Invest. 2018 Aug 1;128(8):3413–3424.
   PubMed Web of Science ®Google Scholar
• Valiño-Rivas L, Baeza-Bermejillo C, Gonzalez-Lafuente L, et al. CD74 in kidney disease. Front Immunol. 2015;6:483.
   PubMed Web of Science ®Google Scholar
• Djudjaj S, Lue H, Rong S, et al. Macrophage migration inhibitory factor mediates proliferative GN via CD74. J Am Soc Nephrol. 2016 Jun;27(6):1650–1664.
   PubMed Web of Science ®Google Scholar
• Farr L, Ghosh S, Moonah S. Role of MIF Cytokine/CD74 receptor pathway in protecting against injury and promoting repair. Front Immunol. 2020;11:1273.
   PubMed Web of Science ®Google Scholar
• Shi X, Leng L, Wang T, et al. CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity. 2006 Oct;25(4):595–606.
   PubMed Web of Science ®Google Scholar
• Su H, Na N, Zhang X, et al. The biological function and significance of CD74 in immune diseases. Inflamm Res. 2017 Mar;66(3):209–216.
   PubMed Web of Science ®Google Scholar
• Yoo SA, Leng L, Kim BJ, et al. MIF allele-dependent regulation of the MIF coreceptor CD44 and role in rheumatoid arthritis. Proc Natl Acad Sci U S A. 2016 Dec 6;113(49):E7917–e7926.
   PubMed Web of Science ®Google Scholar
• Smeets B, Miesen L, Shankland SJ. CD9 is a novel target in glomerular diseases typified by parietal epithelial cell activation. Am J Kidney Dis. 2020 May;75(5):812–814.
   PubMed Web of Science ®Google Scholar
• Reyes R, Cardeñes B, Machado-Pineda Y, et al. Tetraspanin CD9: a key regulator of cell adhesion in the immune system. Front Immunol. 2018;9:863.
   PubMed Web of Science ®Google Scholar
• Lazareth H, Henique C, Lenoir O, et al. The tetraspanin CD9 controls migration and proliferation of parietal epithelial cells and glomerular disease progression. Nat Commun. 2019 Jul 24;10(1):3303.
   PubMedGoogle Scholar
• Kabgani N, Grigoleit T, Schulte K, et al. Primary cultures of glomerular parietal epithelial cells or podocytes with proven origin. PLoS One. 2012;7(4):e34907.
   PubMed Web of Science ®Google Scholar
• Hemler ME. Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol. 2005 Oct;6(10):801–811.
   PubMed Web of Science ®Google Scholar
• Shi W, Fan H, Shum L, et al. The tetraspanin CD9 associates with transmembrane TGF-alpha and regulates TGF-alpha-induced EGF receptor activation and cell proliferation. J Cell Biol. 2000 Feb 7;148(3):591–602.
   PubMed Web of Science ®Google Scholar
• Iwamoto R, Higashiyama S, Mitamura T, et al. Heparin-binding EGF-like growth factor, which acts as the diphtheria toxin receptor, forms a complex with membrane protein DRAP27/CD9, which up-regulates functional receptors and diphtheria toxin sensitivity. Embo J. 1994 May 15;13(10):2322–2330.
   PubMed Web of Science ®Google Scholar
• Jeibmann A, Halama K, Witte HT, et al. Involvement of CD9 and PDGFR in migration is evolutionarily conserved from Drosophila glia to human glioma. J Neurooncol. 2015 Sep;124(3):373–383.
   PubMed Web of Science ®Google Scholar
• Fogo AB, Lusco MA, Najafian B, et al. AJKD atlas of renal pathology: pauci-immune necrotizing crescentic glomerulonephritis. Am J Kidney Dis. 2016 Nov;68(5):e31–e32.
   PubMed Web of Science ®Google Scholar
• McGregor JL. Current perspective on antithrombin drugs. Pathophysiol Haemost Thromb. 2002;32(Suppl 3):29–35.
   PubMedGoogle Scholar
• Drew AF, Tucker HL, Liu H, et al. Crescentic glomerulonephritis is diminished in fibrinogen-deficient mice. Am J Physiol Renal Physiol. 2001 Dec;281(6):F1157–63.
   PubMed Web of Science ®Google Scholar
• Trejo J. Protease-activated receptors: new concepts in regulation of G protein-coupled receptor signaling and trafficking. J Pharmacol Exp Ther. 2003 Nov;307(2):437–442.
   PubMed Web of Science ®Google Scholar
• Lok SWY, Yiu WH, Li H, et al. The PAR-1 antagonist vorapaxar ameliorates kidney injury and tubulointerstitial fibrosis. Clin Sci (Lond). 2020 Nov 13;134(21):2873–2891.
   PubMed Web of Science ®Google Scholar
• Palygin O, Ilatovskaya DV, Staruschenko A. Protease-activated receptors in kidney disease progression. Am J Physiol Renal Physiol. 2016 Dec 1;311(6):F1140–f1144.
   PubMed Web of Science ®Google Scholar
• Fang X, Liao R, Yu Y, et al. Thrombin induces secretion of multiple cytokines and expression of protease-activated receptors in mouse mast cell line. Mediators Inflamm. 2019;2019:4952131.
   PubMed Web of Science ®Google Scholar
• Cunningham MA, Rondeau E, Chen X, et al. Protease-activated receptor 1 mediates thrombin-dependent, cell-mediated renal inflammation in crescentic glomerulonephritis. J Exp Med. 2000 Feb 7;191(3):455–462.
   PubMed Web of Science ®Google Scholar
• Morrow DA, Braunwald E, Bonaca MP, et al. Vorapaxar in the secondary prevention of atherothrombotic events. N Engl J Med. 2012 Apr 12;366(15):1404–1413.
   PubMed Web of Science ®Google Scholar
• Tricoci P, Huang Z, Held C, et al. Thrombin-receptor antagonist vorapaxar in acute coronary syndromes. N Engl J Med. 2012 Jan 5;366(1):20–33.
   PubMed Web of Science ®Google Scholar
• Rothmeier AS, Ruf W. Protease-activated receptor 2 signaling in inflammation. Semin Immunopathol. 2012 Jan;34(1):133–149.
   PubMed Web of Science ®Google Scholar
• Vesey DA, Suen JY, Seow V, et al. PAR2-induced inflammatory responses in human kidney tubular epithelial cells. Am J Physiol Renal Physiol. 2013 Mar 15;304(6):F737–50.
   PubMed Web of Science ®Google Scholar
• Kanke T, Takizawa T, Kabeya M, et al. Physiology and pathophysiology of proteinase-activated receptors (PARs): PAR-2 as a potential therapeutic target. J Pharmacol Sci. 2005 Jan;97(1):38–42.
   PubMed Web of Science ®Google Scholar
• Flanc RS, Ma FY, Tesch GH, et al. A pathogenic role for JNK signaling in experimental anti-GBM glomerulonephritis. Kidney Int. 2007 Sep;72(6):698–708.
   PubMed Web of Science ®Google Scholar
• Ma FY, Flanc RS, Tesch GH, et al. Blockade of the c-Jun amino terminal kinase prevents crescent formation and halts established anti-GBM glomerulonephritis in the rat. Lab Invest. 2009 Apr;89(4):470–484.
   PubMed Web of Science ®Google Scholar
• De Borst MH, Prakash J, Melenhorst WB, et al. Glomerular and tubular induction of the transcription factor c-Jun in human renal disease. J Pathol. 2007 Oct;213(2):219–228.
   PubMed Web of Science ®Google Scholar
• Moussa L, Apostolopoulos J, Davenport P, et al. Protease-activated receptor-2 augments experimental crescentic glomerulonephritis. Am J Pathol. 2007 Sep;171(3):800–808.
   PubMed Web of Science ®Google Scholar
• Amos LA, Ma FY, Tesch GH, et al. ASK1 inhibitor treatment suppresses p38/JNK signalling with reduced kidney inflammation and fibrosis in rat crescentic glomerulonephritis. J Cell Mol Med. 2018 Sep;22(9):4522–4533.
   PubMed Web of Science ®Google Scholar
• Kawaguchi N, Zhang TT, Nakanishi T. Involvement of CXCR4 in normal and abnormal development. Cells. 2019 Feb 20;8(2):185.
   PubMed Web of Science ®Google Scholar
• Rizzo P, Novelli R, Rota C, et al. The role of angiotensin II in parietal epithelial cell proliferation and crescent formation in glomerular diseases. Am J Pathol. 2017 Nov;187(11):2441–2450.
   PubMed Web of Science ®Google Scholar
• Benigni A, Morigi M, Rizzo P, et al. Inhibiting angiotensin-converting enzyme promotes renal repair by limiting progenitor cell proliferation and restoring the glomerular architecture. Am J Pathol. 2011 Aug;179(2):628–638.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Jiang SM, Ma YP, et al. Expression of the intrarenal angiotensin receptor and the role of renin-angiotensin system inhibitors in IgA nephropathy. Mol Cell Biochem. 2019 Mar;453(1–2):103–110.
   PubMed Web of Science ®Google Scholar
• Urushihara M, Ohashi N, Miyata K, et al. Addition of angiotensin II type 1 receptor blocker to CCR2 antagonist markedly attenuates crescentic glomerulonephritis. Hypertension. 2011 Mar;57(3):586–593.
   PubMed Web of Science ®Google Scholar
• Kinoshita Y, Kondo S, Urushihara M, et al. Angiotensin II type I receptor blockade suppresses glomerular renin-angiotensin system activation, oxidative stress, and progressive glomerular injury in rat anti-glomerular basement membrane glomerulonephritis. Transl Res. 2011 Oct;158(4):235–248.
   PubMed Web of Science ®Google Scholar
• Bollée G, Flamant M, Schordan S, et al. Epidermal growth factor receptor promotes glomerular injury and renal failure in rapidly progressive crescentic glomerulonephritis. Nat Med. 2011 Sep 25;17(10):1242–1250.
   PubMed Web of Science ®Google Scholar
• Flamant M, Bollée G, Hénique C, et al. Epidermal growth factor: a new therapeutic target in glomerular disease. Nephrol Dial Transplant. 2012 Apr;27(4):1297–1304.
   PubMed Web of Science ®Google Scholar
• Harris R. EGFR signaling in podocytes at the root of glomerular disease. Nat Med. 2011 Oct 11;17(10):1188–1189.
   PubMed Web of Science ®Google Scholar
• Dai Y, Gu L, Yuan W, et al. Podocyte-specific deletion of signal transducer and activator of transcription 3 attenuates nephrotoxic serum-induced glomerulonephritis. Kidney Int. 2013 Nov;84(5):950–961.
   PubMed Web of Science ®Google Scholar
• Hénique C, Papista C, Guyonnet L, et al. Update on crescentic glomerulonephritis. Semin Immunopathol. 2014 Jul;36(4):479–490.
   PubMed Web of Science ®Google Scholar
• Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell. 2000 Oct 13;103(2):211–225.
   PubMed Web of Science ®Google Scholar
• Hir ML, Keller C, Eschmann V, et al. Podocyte bridges between the tuft and Bowman’s capsule: an early event in experimental crescentic glomerulonephritis. J Am Soc Nephrol. 2001 Oct;12(10):2060–2071.
   PubMed Web of Science ®Google Scholar
• Changsirikulchai S, Hudkins KL, Goodpaster TA, et al. Platelet-derived growth factor-D expression in developing and mature human kidneys. Kidney Int. 2002 Dec;62(6):2043–2054.
   PubMed Web of Science ®Google Scholar
• Rönnstrand L, Arvidsson AK, Kallin A, et al. SHP-2 binds to Tyr763 and Tyr1009 in the PDGF beta-receptor and mediates PDGF-induced activation of the Ras/MAP kinase pathway and chemotaxis. Oncogene. 1999 Jun 24;18(25):3696–3702.
   PubMed Web of Science ®Google Scholar
• Floege J, Eitner F, Alpers CE. A new look at platelet-derived growth factor in renal disease. J Am Soc Nephrol. 2008 Jan;19(1):12–23.
   PubMed Web of Science ®Google Scholar
• Hudkins KL, Gilbertson DG, Carling M, et al. Exogenous PDGF-D is a potent mesangial cell mitogen and causes a severe mesangial proliferative glomerulopathy. J Am Soc Nephrol. 2004 Feb;15(2):286–298.
   PubMed Web of Science ®Google Scholar
• Tallquist M, Kazlauskas A. PDGF signaling in cells and mice. Cytokine Growth Factor Rev. 2004 Aug;15(4):205–213.
   PubMed Web of Science ®Google Scholar
• van Roeyen CR, Eitner F, Boor P, et al. Induction of progressive glomerulonephritis by podocyte-specific overexpression of platelet-derived growth factor-D. Kidney Int. 2011 Dec;80(12):1292–1305.
   PubMed Web of Science ®Google Scholar
• D’Agati VD, Shankland SJ. Recognizing diversity in parietal epithelial cells. Kidney Int. 2019 Jul;96(1):16–19.
   PubMed Web of Science ®Google Scholar
• Zhang J, Hansen KM, Pippin JW, et al. De novo expression of podocyte proteins in parietal epithelial cells in experimental aging nephropathy. Am J Physiol Renal Physiol. 2012 Mar 1;302(5):F571–80.
   PubMed Web of Science ®Google Scholar
• Ronconi E, Sagrinati C, Angelotti ML, et al. Regeneration of glomerular podocytes by human renal progenitors. J Am Soc Nephrol. 2009 Feb;20(2):322–332.
   PubMed Web of Science ®Google Scholar
• Prochnicki A, Amann K, Wegner M, et al. Characterization of glomerular Sox9(+) cells in anti-glomerular basement membrane nephritis in the rat. Am J Pathol. 2018 Nov;188(11):2529–2541.
   PubMed Web of Science ®Google Scholar
• Jo A, Denduluri S, Zhang B, et al. The versatile functions of Sox9 in development, stem cells, and human diseases. Genes Dis. 2014 Dec;1(2):149–161.
   PubMedGoogle Scholar
• Lazareth H, Lenoir O, Tharaux PL. Parietal epithelial cells role in repair versus scarring after glomerular injury. Curr Opin Nephrol Hypertens. 2020 May;29(3):293–301.
   PubMed Web of Science ®Google Scholar
• Wrede C, Hegermann J, Mühlfeld C. Novel cell contact between podocyte microprojections and parietal epithelial cells analyzed by volume electron microscopy. Am J Physiol Renal Physiol. 2020 May 1;318(5):F1246–f1251.
   PubMed Web of Science ®Google Scholar
• Kaverina NV, Eng DG, Freedman BS, et al. Dual lineage tracing shows that glomerular parietal epithelial cells can transdifferentiate toward the adult podocyte fate. Kidney Int. 2019 Sep;96(3):597–611.
   PubMed Web of Science ®Google Scholar
• Zhang L, He S, Guo S, et al. Down-regulation of miR-34a alleviates mesangial proliferation in vitro and glomerular hypertrophy in early diabetic nephropathy mice by targeting GAS1. J Diabetes Complications. 2014 May-June;28(3):259–264.
   PubMed Web of Science ®Google Scholar
• Luna-Antonio BI, Rodriguez-Muñoz R, Namorado-Tonix C, et al. Gas1 expression in parietal cells of Bowman’s capsule in experimental diabetic nephropathy. Histochem Cell Biol. 2017 Jul;148(1):33–47.
   PubMed Web of Science ®Google Scholar
• Kann M, Bae E, Lenz MO, et al. WT1 targets Gas1 to maintain nephron progenitor cells by modulating FGF signals. Development. 2015 Apr 1;142(7):1254–1266.
   PubMed Web of Science ®Google Scholar
• Kaverina NV, Eng DG, Miner JH, et al. Parietal epithelial cell differentiation to a podocyte fate in the aged mouse kidney. Aging (Albany NY). 2020 Aug 28;12(17):17601–17624.
   PubMedGoogle Scholar
• Endlich N, Kliewe F, Kindt F, et al. The transcription factor Dach1 is essential for podocyte function. J Cell Mol Med. 2018 May;22(5):2656–2669.
   PubMed Web of Science ®Google Scholar
• Kliewe F, Kuss AW, Siegerist F, et al. Studies on the role of the transcription factor Tcf21 in the transdifferentiation of parietal epithelial cells into podocyte-like cells. Cell Physiol Biochem. 2021 Jun 19;55(S4):48–67.
   PubMedGoogle Scholar
• Grouls S, Iglesias DM, Wentzensen N, et al. Lineage specification of parietal epithelial cells requires β-catenin/Wnt signaling. J Am Soc Nephrol. 2012 Jan;23(1):63–72.
   PubMed Web of Science ®Google Scholar
• Zhou D, Tan RJ, Fu H, et al. Wnt/β-catenin signaling in kidney injury and repair: a double-edged sword. Lab Invest. 2016 Feb;96(2):156–167.
   PubMed Web of Science ®Google Scholar
• Kato H, Susztak K. Repair problems in podocytes: wnt, Notch, and glomerulosclerosis. Semin Nephrol. 2012 Jul;32(4):350–356.
   PubMed Web of Science ®Google Scholar
• Shkreli M, Sarin KY, Pech MF, et al. Reversible cell-cycle entry in adult kidney podocytes through regulated control of telomerase and Wnt signaling. Nat Med. 2011 Dec 4;18(1):111–119.
   PubMed Web of Science ®Google Scholar
• Kietzmann L, Guhr SS, Meyer TN, et al. MicroRNA-193a regulates the transdifferentiation of human parietal epithelial cells toward a podocyte phenotype. J Am Soc Nephrol. 2015 Jun;26(6):1389–1401.
   PubMed Web of Science ®Google Scholar
• Discenza MT, He S, Lee TH, et al. WT1 is a modifier of the Pax2 mutant phenotype: cooperation and interaction between WT1 and Pax2. Oncogene. 2003 Nov 6;22(50):8145–8155.
   PubMed Web of Science ®Google Scholar
• Eng DG, Sunseri MW, Kaverina NV, et al. Glomerular parietal epithelial cells contribute to adult podocyte regeneration in experimental focal segmental glomerulosclerosis. Kidney Int. 2015 Nov;88(5):999–1012.
   PubMed Web of Science ®Google Scholar
• Gebeshuber CA, Kornauth C, Dong L, et al. Focal segmental glomerulosclerosis is induced by microRNA-193a and its downregulation of WT1. Nat Med. 2013 Apr;19(4):481–487.
   PubMed Web of Science ®Google Scholar
• Melica ME, Antonelli G, Semeraro R, et al. Differentiation of crescent-forming kidney progenitor cells into podocytes attenuates severe glomerulonephritis in mice. Sci Transl Med. 2022 Aug 10;14(657):eabg3277.
   PubMed Web of Science ®Google Scholar
• Anders HJ, Romagnani P, Mantovani A. Pathomechanisms: homeostatic chemokines in health, tissue regeneration, and progressive diseases. Trends Mol Med. 2014 Mar;20(3):154–165.
   PubMed Web of Science ®Google Scholar
• Romagnani P. Toward the identification of a “renopoietic system”? Stem Cells. 2009 Sep;27(9):2247–2253.
   PubMed Web of Science ®Google Scholar
• Mead AJ, Mullally A. Myeloproliferative neoplasm stem cells. Blood. 2017 Mar 23;129(12):1607–1616.
   PubMed Web of Science ®Google Scholar
• Chen J, Kao YR, Sun D, et al. Myelodysplastic syndrome progression to acute myeloid leukemia at the stem cell level. Nat Med. 2019 Jan;25(1):103–110.
   PubMed Web of Science ®Google Scholar
• Laubach JP, Moreau P, San-Miguel JF, et al. Panobinostat for the treatment of multiple myeloma. Clin Cancer Res. 2015 Nov 1;21(21):4767–4773.
   PubMed Web of Science ®Google Scholar
• Urushihara M, Kondo S, Kinoshita Y, et al. (Pro)renin receptor promotes crescent formation via the ERK1/2 and Wnt/β-catenin pathways in glomerulonephritis. Am J Physiol Renal Physiol. 2020 Oct 1;319(4):F571–f578.
   PubMed Web of Science ®Google Scholar