Kidney Regeneration: Stem Cells as a New Trend

Author(s): Amin Ahmadi, Niloofar K. Rad, Vahid Ezzatizadeh, Reza Moghadasali*

Journal Name: Current Stem Cell Research & Therapy

Volume 15 , Issue 3 , 2020

Become EABM
Become Reviewer


Renal disease is a major worldwide public health problem that affects one in ten people. Renal failure is caused by the irreversible loss of the structural and functional units of kidney (nephrons) due to acute and chronic injuries. In humans, new nephrons (nephrogenesis) are generated until the 36th week of gestation and no new nephron develops after birth. However, in rodents, nephrogenesis persists until the immediate postnatal period. The postnatal mammalian kidney can partly repair their nephrons. The kidney uses intrarenal and extra-renal cell sources for maintenance and repair. Currently, it is believed that dedifferentiation of surviving tubular epithelial cells and presence of resident stem cells have important roles in kidney repair. Many studies have shown that stem cells obtained from extra-renal sites such as the bone marrow, adipose and skeletal muscle tissues, in addition to umbilical cord and amniotic fluid, have potential therapeutic benefits. This review discusses the main mechanisms of renal regeneration by stem cells after a kidney injury.

Keywords: Kidney regeneration, end-stage renal diseases, acute kidney injury, chronic kidney injury, stem cells, nephrogenesis.

Hartman HA, Lai HL, Patterson LT. Cessation of renal morphogenesis in mice. Dev Biol 2007; 310(2): 379-87.
[] [PMID: 17826763]
Hopkins C, Li J, Rae F, Little MH. Stem cell options for kidney disease. J Pathol 2009; 217(2): 265-81.
[] [PMID: 19058290]
Humphreys B, Duffield J, Bonventre J. Renal stem cells in recovery from acute kidney injury Minerva urologica e nefrologica= The Italian journal of urology and nephrology 2006 58(4): 329-7.
Moghadasali R, Hajinasrollah M, Argani H, et al. Autologous transplantation of mesenchymal stromal cells tends to prevent progress of interstitial fibrosis in a rhesus Macaca mulatta monkey model of chronic kidney disease. Cytotherapy 2015; 17(11): 1495-505.
[] [PMID: 26341479]
Duffield JS, Bonventre JV. Kidney tubular epithelium is restored without replacement with bone marrow-derived cells during repair after ischemic injury. Kidney Int 2005; 68(5): 1956-61.
[] [PMID: 16221175]
Bataille A, Galichon P, Wetzstein M, et al. Evaluation of the ability of bone marrow derived cells to engraft the kidney and promote renal tubular regeneration in mice following exposure to cisplatin. Ren Fail 2016; 38(4): 521-9.
[] [PMID: 26905096]
Duffield JS, Park KM, Hsiao LL, et al. Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J Clin Invest 2005; 115(7): 1743-55.
[] [PMID: 16007251]
Lin F, Moran A, Igarashi P. Intrarenal cells, not bone marrow-derived cells, are the major source for regeneration in postischemic kidney. J Clin Invest 2005; 115(7): 1756-64.
[] [PMID: 16007252]
Westhoff JH, Schildhorn C, Jacobi C, et al. Telomere shortening reduces regenerative capacity after acute kidney injury. J Am Soc Nephrol 2010; 21(2): 327-36.
[] [PMID: 19959722]
Song J, Czerniak S, Wang T, et al. Characterization and fate of telomerase-expressing epithelia during kidney repair. J Am Soc Nephrol 2011; 22(12): 2256-65.
[] [PMID: 22021716]
Humphreys BD, Czerniak S, DiRocco DP, Hasnain W, Cheema R, Bonventre JV. Repair of injured proximal tubule does not involve specialized progenitors. Proc Natl Acad Sci USA 2011; 108(22): 9226-31.
[] [PMID: 21576461]
Humphreys BD, Valerius MT, Kobayashi A, et al. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2008; 2(3): 284-91.
[] [PMID: 18371453]
Skvarca LB, Han HI, Espiritu EB, et al. dmm.Enhancing acute kidney injury regeneration by promoting cellular dedifferentiation in zebrafish. In:Disease models & mechanisms:. 2019; p. 037390.
Berger K, Moeller MJ. Mechanisms of epithelial repair and regeneration after acute kidney injurySeminars in nephrology. Elsevier 2014.
Kusaba T, Lalli M, Kramann R, Kobayashi A, Humphreys BD. Differentiated kidney epithelial cells repair injured proximal tubule. Proc Natl Acad Sci USA 2014; 111(4): 1527-32.
[] [PMID: 24127583]
Berger K, Bangen J-M, Hammerich L, et al. Origin of regenerating tubular cells after acute kidney injury. Proc Natl Acad Sci USA 2014; 111(4): 1533-8.
[] [PMID: 24474779]
Zou X, Kwon SH, Jiang K, et al. Renal scattered tubular-like cells confer protective effects in the stenotic murine kidney mediated by release of extracellular vesicles. Sci Rep 2018; 8(1): 1263.
[] [PMID: 29352176]
Sagrinati C, Netti GS, Mazzinghi B, et al. Isolation and characterization of multipotent progenitor cells from the Bowman’s capsule of adult human kidneys. J Am Soc Nephrol 2006; 17(9): 2443-56.
[] [PMID: 16885410]
Lindgren D, Boström A-K, Nilsson K, et al. Isolation and characterization of progenitor-like cells from human renal proximal tubules. Am J Pathol 2011; 178(2): 828-37.
[] [PMID: 21281815]
Maeshima A, Yamashita S, Nojima Y. Identification of renal progenitor-like tubular cells that participate in the regeneration processes of the kidney. J Am Soc Nephrol 2003; 14(12): 3138-46.
[] [PMID: 14638912]
Kim K, Lee KM, Han DJ, Yu E, Cho YM. Adult stem cell-like tubular cells reside in the corticomedullary junction of the kidney. Int J Clin Exp Pathol 2008; 1(3): 232-41.
[PMID: 18784815]
Langworthy M, Zhou B, de Caestecker M, Moeckel G, Baldwin HS. NFATc1 identifies a population of proximal tubule cell progenitors. J Am Soc Nephrol 2009; 20(2): 311-21.
[] [PMID: 19118153]
Maeshima A, Sakurai H, Nigam SK. Adult kidney tubular cell population showing phenotypic plasticity, tubulogenic capacity, and integration capability into developing kidney. J Am Soc Nephrol 2006; 17(1): 188-98.
[] [PMID: 16338966]
Angelotti ML, Ronconi E, Ballerini L, et al. Characterization of renal progenitors committed toward tubular lineage and their regenerative potential in renal tubular injury. Stem Cells 2012; 30(8): 1714-25.
[] [PMID: 22628275]
Oliver JA, Maarouf O, Cheema FH, Martens TP, Al-Awqati Q. The renal papilla is a niche for adult kidney stem cells. J Clin Invest 2004; 114(6): 795-804.
[] [PMID: 15372103]
Oliver JA, Klinakis A, Cheema FH, et al. Proliferation and migration of label-retaining cells of the kidney papilla. J Am Soc Nephrol 2009; 20(11): 2315-27.
[] [PMID: 19762493]
Yamashita S, Maeshima A, Nojima Y. Involvement of renal progenitor tubular cells in epithelial-to-mesenchymal transition in fibrotic rat kidneys. J Am Soc Nephrol 2005; 16(7): 2044-51.
[] [PMID: 15888566]
Iwatani H, Ito T, Imai E, et al. Hematopoietic and nonhematopoietic potentials of Hoechst(low)/side population cells isolated from adult rat kidney. Kidney Int 2004; 65(5): 1604-14.
[] [PMID: 15086898]
Challen GA, Bertoncello I, Deane JA, Ricardo SD, Little MH. Kidney side population reveals multilineage potential and renal functional capacity but also cellular heterogeneity. J Am Soc Nephrol 2006; 17(7): 1896-912.
[] [PMID: 16707564]
Bussolati B, Bruno S, Grange C, et al. Isolation of renal progenitor cells from adult human kidney. Am J Pathol 2005; 166(2): 545-55.
[] [PMID: 15681837]
Grange C, Moggio A, Tapparo M, Porta S, Camussi G, Bussolati B. Protective effect and localization by optical imaging of human renal CD133+ progenitor cells in an acute kidney injury model. Physiol Rep 2014; 2(5)e12009
[] [PMID: 24793983]
Aggarwal S, Grange C, Iampietro C, Camussi G, Bussolati B. Human CD133+ renal progenitor cells induce erythropoietin production and limit fibrosis after acute tubular injury. Sci Rep 2016; 6: 37270.
[] [PMID: 27853265]
Lazzeri E, Crescioli C, Ronconi E, et al. Regenerative potential of embryonic renal multipotent progenitors in acute renal failure. J Am Soc Nephrol 2007; 18(12): 3128-38.
[] [PMID: 17978305]
Burmeister DM, McIntyre MK, Montgomery RK, Gómez BI, Dubick MA. Isolation and Characterization of Multipotent CD24+ Cells From the Renal Papilla of Swine. Front Med (Lausanne) 2018; 5: 250.
[] [PMID: 30283781]
Bruno S, Bussolati B, Grange C, et al. Isolation and characterization of resident mesenchymal stem cells in human glomeruli. Stem Cells Dev 2009; 18(6): 867-80.
[] [PMID: 19579288]
Ranghino A, Bruno S, Bussolati B, et al. The effects of glomerular and tubular renal progenitors and derived extracellular vesicles on recovery from acute kidney injury. Stem Cell Res Ther 2017; 8(1): 24.
[] [PMID: 28173878]
Rangel EB, Gomes SA, Dulce RA, et al. C-kit(+) cells isolated from developing kidneys are a novel population of stem cells with regenerative potential. Stem Cells 2013; 31(8): 1644-56.
[] [PMID: 23733311]
Rangel EB, Gomes SA, Kanashiro-Takeuchi R, et al. Kidney-derived c-kit+ progenitor/stem cells contribute to podocyte recovery in a model of acute proteinuria. Sci Rep 2018; 8(1): 14723.
[] [PMID: 30283057]
Dekel B, Zangi L, Shezen E, et al. Isolation and characterization of nontubular sca-1+lin- multipotent stem/progenitor cells from adult mouse kidney. J Am Soc Nephrol 2006; 17(12): 3300-14.
[] [PMID: 17093069]
Rinkevich Y, Montoro DT, Contreras-Trujillo H, et al. In vivo clonal analysis reveals lineage-restricted progenitor characteristics in mammalian kidney development, maintenance, and regeneration. Cell Rep 2014; 7(4): 1270-83.
[] [PMID: 24835991]
Kumar S, Liu J, Pang P, et al. Sox9 activation highlights a cellular pathway of renal repair in the acutely injured mammalian kidney. Cell Rep 2015; 12(8): 1325-38.
[] [PMID: 26279573]
Kang HM, Huang S, Reidy K, Han SH, Chinga F, Susztak K. Sox9-positive progenitor cells play a key role in renal tubule epithelial regeneration in mice. Cell Rep 2016; 14(4): 861-71.
[] [PMID: 26776520]
Eng DG, Sunseri MW, Kaverina NV, Roeder SS, Pippin JW, Shankland SJ. Glomerular parietal epithelial cells contribute to adult podocyte regeneration in experimental focal segmental glomerulosclerosis. Kidney Int 2015; 88(5): 999-1012.
[] [PMID: 25993321]
Leuning DG, Reinders ME, Li J, et al. Clinical-Grade Isolated Human Kidney Perivascular Stromal Cells as an Organotypic Cell Source for Kidney Regenerative Medicine. Stem Cells Transl Med 2017; 6(2): 405-18.
[] [PMID: 28191776]
Rota C, Morigi M, Cerullo D, et al. Therapeutic potential of stromal cells of non-renal or renal origin in experimental chronic kidney disease. Stem Cell Res Ther 2018; 9(1): 220.
[] [PMID: 30107860]
Tögel F, Hu Z, Weiss K, Isaac J, Lange C, Westenfelder C. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol 2005; 289(1): F31-42.
[] [PMID: 15713913]
Semedo P, Correa-Costa M, Antonio Cenedeze M, et al. Mesenchymal stem cells attenuate renal fibrosis through immune modulation and remodeling properties in a rat remnant kidney model. Stem Cells 2009; 27(12): 3063-73.
[] [PMID: 19750536]
Qi S, Wu D. Bone marrow-derived mesenchymal stem cells protect against cisplatin-induced acute kidney injury in rats by inhibiting cell apoptosis. Int J Mol Med 2013; 32(6): 1262-72.
[] [PMID: 24126885]
Behr L, Hekmati M, Fromont G, et al. Intra renal arterial injection of autologous mesenchymal stem cells in an ovine model in the postischemic kidney. Nephron, Physiol 2007; 107(3): 65-76.
[] [PMID: 17940346]
Cavaglieri R, Martini D, Sogayar M, Noronha I. Mesenchymal stem cells delivered at the subcapsule of the kidney ameliorate renal disease in the rat remnant kidney modelTransplantation proceedings. Elsevier 2009.
Kunter U, Rong S, Djuric Z, et al. Transplanted mesenchymal stem cells accelerate glomerular healing in experimental glomerulonephritis. J Am Soc Nephrol 2006; 17(8): 2202-12.
[] [PMID: 16790513]
Morigi M, Imberti B, Zoja C, et al. Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure. J Am Soc Nephrol 2004; 15(7): 1794-804.
[] [PMID: 15213267]
Morigi M, Introna M, Imberti B, et al. Human bone marrow mesenchymal stem cells accelerate recovery of acute renal injury and prolong survival in mice. Stem Cells 2008; 26(8): 2075-82.
[] [PMID: 18499895]
Eliopoulos N, Zhao J, Bouchentouf M, et al. Human marrow-derived mesenchymal stromal cells decrease cisplatin renotoxicity in vitro and in vivo and enhance survival of mice post-intraperitoneal injection. Am J Physiol Renal Physiol 2010; 299(6): F1288-98.
[] [PMID: 20844023]
Moghadasali R, Azarnia M, Hajinasrollah M, et al. Intra-renal arterial injection of autologous bone marrow mesenchymal stromal cells ameliorates cisplatin-induced acute kidney injury in a rhesus Macaque mulatta monkey model. Cytotherapy 2014; 16(6): 734-49.
[] [PMID: 24801377]
Tögel F, Weiss K, Yang Y, Hu Z, Zhang P, Westenfelder C. Vasculotropic, paracrine actions of infused mesenchymal stem cells are important to the recovery from acute kidney injury. Am J Physiol Renal Physiol 2007; 292(5): F1626-35.
[] [PMID: 17213465]
Ninichuk V, Gross O, Segerer S, et al. Multipotent mesenchymal stem cells reduce interstitial fibrosis but do not delay progression of chronic kidney disease in collagen4A3-deficient mice. Kidney Int 2006; 70(1): 121-9.
[] [PMID: 16723981]
Eirin A, Zhu XY, Krier JD, et al. Adipose tissue-derived mesenchymal stem cells improve revascularization outcomes to restore renal function in swine atherosclerotic renal artery stenosis. Stem Cells 2012; 30(5): 1030-41.
[] [PMID: 22290832]
Morigi M, Rota C, Montemurro T, et al. Life-sparing effect of human cord blood-mesenchymal stem cells in experimental acute kidney injury. Stem Cells 2010; 28(3): 513-22.
Zhou Y, Xu H, Xu W, et al. Exosomes released by human umbilical cord mesenchymal stem cells protect against cisplatin-induced renal oxidative stress and apoptosis in vivo and in vitro. Stem Cell Res Ther 2013; 4(2): 34.
[] [PMID: 23618405]
De Coppi P, Bartsch G Jr, Siddiqui MM, et al. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 2007; 25(1): 100-6.
[] [PMID: 17206138]
Kaneko Y, Hayashi T, Yu S, et al. Human amniotic epithelial cells express melatonin receptor MT1, but not melatonin receptor MT2: a new perspective to neuroprotection. J Pineal Res 2011; 50(3): 272-80.
[] [PMID: 21269327]
Hauser PV, De Fazio R, Bruno S, et al. Stem cells derived from human amniotic fluid contribute to acute kidney injury recovery. Am J Pathol 2010; 177(4): 2011-21.
[] [PMID: 20724594]
Perin L, Giuliani S, Jin D, et al. Renal differentiation of amniotic fluid stem cells. Cell Prolif 2007; 40(6): 936-48.
[] [PMID: 18021180]
Perin L, Sedrakyan S, Giuliani S, et al. Protective effect of human amniotic fluid stem cells in an immunodeficient mouse model of acute tubular necrosis. PLoS One 2010; 5(2)e9357
[] [PMID: 20195358]
George SK, Abolbashari M, Kim T-H, et al. Effect of human amniotic fluid stem cells on kidney function in a model of chronic kidney disease. Tissue Eng Part A 2019; 25(21-22): 1493-503.
[] [PMID: 30829146]
Rota C, Imberti B, Pozzobon M, et al. Human amniotic fluid stem cell preconditioning improves their regenerative potential. Stem Cells Dev 2012; 21(11): 1911-23.
[] [PMID: 22066606]
Baulier E, Favreau F, Le Corf A, et al. Amniotic fluid-derived mesenchymal stem cells prevent fibrosis and preserve renal function in a preclinical porcine model of kidney transplantation. Stem Cells Transl Med 2014; 3(7): 809-20.
[] [PMID: 24797827]
Chade AR, Zhu X, Lavi R, et al. Endothelial progenitor cells restore renal function in chronic experimental renovascular disease. Circulation 2009; 119(4): 547-57.
[] [PMID: 19153272]
Chade AR, Zhu XY, Krier JD, et al. Endothelial progenitor cells homing and renal repair in experimental renovascular disease. Stem Cells 2010; 28(6): 1039-47.
[] [PMID: 20506499]
Patschan D, Krupincza K, Patschan S, Zhang Z, Hamby C, Goligorsky MS. Dynamics of mobilization and homing of endothelial progenitor cells after acute renal ischemia: modulation by ischemic preconditioning. Am J Physiol Renal Physiol 2006; 291(1): F176-85.
[] [PMID: 16478972]
Eirin A, Zhu X-Y, Ebrahimi B, et al. Intrarenal delivery of mesenchymal stem cells and endothelial progenitor cells attenuates hypertensive cardiomyopathy in experimental renovascular hypertension. Cell Transplant 2015; 24(10): 2041-53.
[] [PMID: 25420012]
Pavyde E, Maciulaitis R, Mauricas M, et al. Skeletal muscle-derived stem/progenitor cells: a potential strategy for the treatment of acute kidney injury. Stem Cells Int 2016; 20169618480
[] [PMID: 27069485]
Yeagy BA, Harrison F, Gubler M-C, Koziol JA, Salomon DR, Cherqui S. Kidney preservation by bone marrow cell transplantation in hereditary nephropathy. Kidney Int 2011; 79(11): 1198-206.
[] [PMID: 21248718]
Bi B, Schmitt R, Israilova M, Nishio H, Cantley LG. Stromal cells protect against acute tubular injury via an endocrine effect. J Am Soc Nephrol 2007; 18(9): 2486-96.
[] [PMID: 17656474]
Moghadasali R, Mutsaers HA, Azarnia M, et al. Mesenchymal stem cell-conditioned medium accelerates regeneration of human renal proximal tubule epithelial cells after gentamicin toxicity. Exp Toxicol Pathol 2013; 65(5): 595-600.
[] [PMID: 22727565]
Reis LA, Borges FT, Simões MJ, Borges AA, Sinigaglia-Coimbra R, Schor N. Bone marrow-derived mesenchymal stem cells repaired but did not prevent gentamicin-induced acute kidney injury through paracrine effects in rats. PLoS One 2012; 7(9)e44092
[] [PMID: 22970165]
Bruno S, Grange C, Deregibus MC, et al. Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol 2009; 20(5): 1053-67.
[] [PMID: 19389847]
Bruno S, Grange C, Collino F, et al. Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PLoS One 2012; 7(3)e33115
[] [PMID: 22431999]
Mansoori-Moghadam Z, Totonchi M, Hesaraki M, Aghdami N, Baharvand H, Moghadasali R. Programming of ES cells and reprogramming of fibroblasts into renal lineage-like cells. Exp Cell Res 2019; 379(2): 225-34.
[] [PMID: 30981668]
Hoshina A, Kawamoto T, Sueta S-I, et al. Development of new method to enrich human iPSC-derived renal progenitors using cell surface markers. Sci Rep 2018; 8(1): 6375.
[] [PMID: 29686294]
Toyohara T, Mae S, Sueta S, et al. 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.
[] [PMID: 26198166]
Ahmadi A, Moghadasali R, Ezzatizadeh V, et al. Transplantation of Mouse Induced Pluripotent Stem Cell-Derived Podocytes in a Mouse Model of Membranous Nephropathy Attenuates Proteinuria. Sci Rep 2019; 9(1): 15467.
[] [PMID: 31664077]
Li Q, Tian SF, Guo Y, et al. Transplantation of induced pluripotent stem cell-derived renal stem cells improved acute kidney injury. Cell Biosci 2015; 5(1): 45.
[] [PMID: 26294957]
Wu HJ, Yiu WH, Wong DWL, et al. Human induced pluripotent stem cell-derived mesenchymal stem cells prevent adriamycin nephropathy in mice. Oncotarget 2017; 8(61): 103640-56.
[] [PMID: 29262590]
La Greca A, Solari C, Furmento V, et al. Extracellular vesicles from pluripotent stem cell-derived mesenchymal stem cells acquire a stromal modulatory proteomic pattern during differentiation. Exp Mol Med 2018; 50(9): 119.
[] [PMID: 30201949]
Li B, Leung JCK, Chan LYY, et al. Amelioration of Endoplasmic Reticulum Stress by Mesenchymal Stem Cells via Hepatocyte Growth Factor/c-Met Signaling in Obesity-Associated Kidney Injury. Stem Cells Transl Med 2019; 8(9): 898-910.
[] [PMID: 31054183]
Ko S-F, Chen Y-T, Wallace CG, et al. Inducible pluripotent stem cell-derived mesenchymal stem cell therapy effectively protected kidney from acute ischemia-reperfusion injury. Am J Transl Res 2018; 10(10): 3053-67.
[PMID: 30416650]
Shen W-C, Chou Y-H, Huang H-P, Sheen J-F, Hung S-C, Chen H-F. Induced pluripotent stem cell-derived endothelial progenitor cells attenuate ischemic acute kidney injury and cardiac dysfunction. Stem Cell Res Ther 2018; 9(1): 344.
[] [PMID: 30526689]
Luo J, Zhao X, Tan Z, Su Z, Meng F, Zhang M. Mesenchymal-like progenitors derived from human embryonic stem cells promote recovery from acute kidney injury via paracrine actions. Cytotherapy 2013; 15(6): 649-62.
[] [PMID: 23415919]
Geng X-D, Zheng W, Wu C-M, et al. Embryonic stem cells-loaded gelatin microcryogels slow progression of chronic kidney disease. Chin Med J (Engl) 2016; 129(4): 392-8.
[] [PMID: 26879011]
Lange C, Tögel F, Ittrich H, et al. Administered mesenchymal stem cells enhance recovery from ischemia/reperfusion-induced acute renal failure in rats. Kidney Int 2005; 68(4): 1613-7.
[] [PMID: 16164638]
Broekema M, Harmsen MC, van Luyn MJ, et al. Bone marrow-derived myofibroblasts contribute to the renal interstitial myofibroblast population and produce procollagen I after ischemia/reperfusion in rats. J Am Soc Nephrol 2007; 18(1): 165-75.
[] [PMID: 17135399]
Semedo P, Wang P, Andreucci T, et al. Mesenchymal stem cells ameliorate tissue damages triggered by renal ischemia and reperfusion injuryTransplantation proceedings. Elsevier 2007.
Hagiwara M, Shen B, Chao L, Chao J. Kallikrein-modified mesenchymal stem cell implantation provides enhanced protection against acute ischemic kidney injury by inhibiting apoptosis and inflammation. Hum Gene Ther 2008; 19(8): 807-19.
[] [PMID: 18554097]
Shi H, Patschan D, Dietz GP, Bähr M, Plotkin M, Goligorsky MS. Glial cell line-derived neurotrophic growth factor increases motility and survival of cultured mesenchymal stem cells and ameliorates acute kidney injury. Am J Physiol Renal Physiol 2008; 294(1): F229-35.
[] [PMID: 18003856]
Tögel F, Cohen A, Zhang P, Yang Y, Hu Z, Westenfelder C. Autologous and allogeneic marrow stromal cells are safe and effective for the treatment of acute kidney injury. Stem Cells Dev 2009; 18(3): 475-85.
[] [PMID: 18564903]
Gupta S, Verfaillie C, Chmielewski D, et al. Isolation and characterization of kidney-derived stem cells. J Am Soc Nephrol 2006; 17(11): 3028-40.
[] [PMID: 16988061]
Kitamura S, Yamasaki Y, Kinomura M, et al. Establishment and characterization of renal progenitor like cells from S3 segment of nephron in rat adult kidney. FASEB J 2005; 19(13): 1789-97.
[] [PMID: 16260649]
Chen J, Park HC, Addabbo F, et al. Kidney-derived mesenchymal stem cells contribute to vasculogenesis, angiogenesis and endothelial repair. Kidney Int 2008; 74(7): 879-89.
[] [PMID: 18596729]
Lin F, Igarashi P. Searching for stem/progenitor cells in the adult mouse kidney. J Am Soc Nephrol 2003; 14(12): 3290-2.
[] [PMID: 14638929]
Lin F, Cordes K, Li L, et al. Hematopoietic stem cells contribute to the regeneration of renal tubules after renal ischemia-reperfusion injury in mice. J Am Soc Nephrol 2003; 14(5): 1188-99.
[] [PMID: 12707389]
Behr L, Hekmati M, Lucchini A, et al. Evaluation of the effect of autologous mesenchymal stem cell injection in a large-animal model of bilateral kidney ischaemia reperfusion injury. Cell Prolif 2009; 42(3): 284-97.
[] [PMID: 19438896]
Herrera MB, Bussolati B, Bruno S, Fonsato V, Romanazzi GM, Camussi G. Mesenchymal stem cells contribute to the renal repair of acute tubular epithelial injury. Int J Mol Med 2004; 14(6): 1035-41.
[] [PMID: 15547670]
Herrera MB, Bussolati B, Bruno S, et al. Exogenous mesenchymal stem cells localize to the kidney by means of CD44 following acute tubular injury. Kidney Int 2007; 72(4): 430-41.
[] [PMID: 17507906]
Iwasaki M, Adachi Y, Minamino K, et al. Mobilization of bone marrow cells by G-CSF rescues mice from cisplatin-induced renal failure, and M-CSF enhances the effects of G-CSF. J Am Soc Nephrol 2005; 16(3): 658-66.
[] [PMID: 15689404]
Imberti B, Morigi M, Tomasoni S, et al. Insulin-like growth factor-1 sustains stem cell mediated renal repair. J Am Soc Nephrol 2007; 18(11): 2921-8.
[] [PMID: 17942965]
Hishikawa K, Marumo T, Miura S, et al. Musculin/MyoR is expressed in kidney side population cells and can regulate their function. J Cell Biol 2005; 169(6): 921-8.
[] [PMID: 15967813]
Morigi M, Buelli S, Angioletti S, et al. In response to protein load podocytes reorganize cytoskeleton and modulate endothelin-1 gene: implication for permselective dysfunction of chronic nephropathies. Am J Pathol 2005; 166(5): 1309-20.
[] [PMID: 15855633]
Kinomura M, Kitamura S, Tanabe K, et al. Amelioration of cisplatin-induced acute renal injury by renal progenitor-like cells derived from the adult rat kidney. Cell Transplant 2008; 17(1-2): 143-58.
[] [PMID: 18468244]
Roufosse C, Bou-Gharios G, Prodromidi E, et al. Bone marrow-derived cells do not contribute significantly to collagen I synthesis in a murine model of renal fibrosis. J Am Soc Nephrol 2006; 17(3): 775-82.
[] [PMID: 16467445]
Fang T-C, Alison MR, Cook HT, Jeffery R, Wright NA, Poulsom R. Proliferation of bone marrow-derived cells contributes to regeneration after folic acid-induced acute tubular injury. J Am Soc Nephrol 2005; 16(6): 1723-32.
[] [PMID: 15814835]
Fang TC, Otto WR, Rao J, et al. Haematopoietic lineage-committed bone marrow cells, but not cloned cultured mesenchymal stem cells, contribute to regeneration of renal tubular epithelium after HgCl 2 -induced acute tubular injury. Cell Prolif 2008; 41(4): 575-91.
[] [PMID: 18616694]
Fang TC, Otto WR, Jeffery R, et al. Exogenous bone marrow cells do not rescue non-irradiated mice from acute renal tubular damage caused by HgCl2, despite establishment of chimaerism and cell proliferation in bone marrow and spleen. Cell Prolif 2008; 41(4): 592-606.
[] [PMID: 18699966]
Yen TH, Alison MR, Cook HT, et al. The cellular origin and proliferative status of regenerating renal parenchyma after mercuric chloride damage and erythropoietin treatment. Cell Prolif 2007; 40(2): 143-56.
[] [PMID: 17472723]
Guillot P, Cook H, Pusey C, et al 2008; Transplantation of human fetal mesenchymal stem cells improves glomerulopathy in a collagen type Iα2‐deficient mouse The Journal of Pathology: A Journal of the Pathological Society of Great Britain and Ireland 214(5): 627-36.
Sugimoto H, Mundel TM, Sund M, Xie L, Cosgrove D, Kalluri R. Bone-marrow-derived stem cells repair basement membrane collagen defects and reverse genetic kidney disease. Proc Natl Acad Sci USA 2006; 103(19): 7321-6.
[] [PMID: 16648256]
Prodromidi EI, Poulsom R, Jeffery R, et al. Bone marrow-derived cells contribute to podocyte regeneration and amelioration of renal disease in a mouse model of Alport syndrome. Stem Cells 2006; 24(11): 2448-55.
[] [PMID: 16873763]
Imasawa T, Nagasawa R, Utsunomiya Y, et al. Bone marrow transplantation attenuates murine IgA nephropathy: role of a stem cell disorder. Kidney Int 1999; 56(5): 1809-17.
[] [PMID: 10571789]
Imasawa T, Utsunomiya Y. Stem cells in renal biology: bone marrow transplantation for the treatment of IgA nephropathy. Exp Nephrol 2002; 10(1): 51-8.
[] [PMID: 11803205]
Ezquer FE, Ezquer ME, Parrau DB, Carpio D, Yañez AJ, Conget PA. Systemic administration of multipotent mesenchymal stromal cells reverts hyperglycemia and prevents nephropathy in type 1 diabetic mice. Biol Blood Marrow Transplant 2008; 14(6): 631-40.
[] [PMID: 18489988]
Kunter U, Rong S, Boor P, et al. Mesenchymal stem cells prevent progressive experimental renal failure but maldifferentiate into glomerular adipocytes. J Am Soc Nephrol 2007; 18(6): 1754-64.
[] [PMID: 17460140]
Wong C-Y, Cheong S-K, Mok P-L, Leong C-F. Differentiation of human mesenchymal stem cells into mesangial cells in post-glomerular injury murine model. Pathology 2008; 40(1): 52-7.
[] [PMID: 18038316]
Challen GA, Little MH. A side order of stem cells: the SP phenotype. Stem Cells 2006; 24(1): 3-12.
[] [PMID: 16449630]
Li J, Deane JA, Campanale NV, Bertram JF, Ricardo SD. The contribution of bone marrow-derived cells to the development of renal interstitial fibrosis. Stem Cells 2007; 25(3): 697-706.
[] [PMID: 17170067]
Kim S-S, Park HJ, Han J, et al. Improvement of kidney failure with fetal kidney precursor cell transplantation. Transplantation 2007; 83(9): 1249-58.
[] [PMID: 17496543]
Choi S, Park M, Kim J, Hwang S, Park S, Lee Y. The role of mesenchymal stem cells in the functional improvement of chronic renal failure. Stem Cells Dev 2009; 18(3): 521-9.
[] [PMID: 18647091]
Eliopoulos N, Gagnon RF, Francois M, Galipeau J. Erythropoietin delivery by genetically engineered bone marrow stromal cells for correction of anemia in mice with chronic renal failure. J Am Soc Nephrol 2006; 17(6): 1576-84.
[] [PMID: 16672321]
Yokoo T, Ohashi T, Shen JS, et al. Human mesenchymal stem cells in rodent whole-embryo culture are reprogrammed to contribute to kidney tissues. Proc Natl Acad Sci USA 2005; 102(9): 3296-300.
[] [PMID: 15728383]
Semedo P, Palasio CG, Oliveira CD, et al. Early modulation of inflammation by mesenchymal stem cell after acute kidney injury. Int Immunopharmacol 2009; 9(6): 677-82.
[] [PMID: 19146993]
Caldas H, Fernandes I, Gerbi F, et al. Effect of whole bone marrow cell infusion in the progression of experimental chronic renal failureTransplantation proceedings. Elsevier 2008.

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2020
Page: [263 - 283]
Pages: 21
DOI: 10.2174/1574888X15666191218094513
Price: $65

Article Metrics

PDF: 18