Korean J Urol.  2015 Jun;56(6):412-421. 10.4111/kju.2015.56.6.412.

Cell-based therapy for kidney disease

Affiliations
  • 1Wake Forest Institute for Regenerative Medicine, Wake Forest School of Medicine, Medical Center Boulevard, Winston-Salem, NC, USA. jyoo@wakehealth.edu
  • 2Department of Urology, Yonsei University Wonju College of Medicine, Wonju, Korea.

Abstract

The prevalence of renal disease continues to increase worldwide. When normal kidney is injured, the damaged renal tissue undergoes pathological and physiological events that lead to acute and chronic kidney diseases, which frequently progress to end stage renal failure. Current treatment of these renal pathologies includes dialysis, which is incapable of restoring full renal function. To address this issue, cell-based therapy has become a potential therapeutic option to treat renal pathologies. Recent development in cell therapy has demonstrated promising therapeutic outcomes, in terms of restoration of renal structure and function impaired by renal disease. This review focuses on the cell therapy approaches for the treatment of kidney diseases, including various cell sources used, as well recent advances made in preclinical and clinical studies.

Keyword

Acute kidney injury; Cell- and tissue-based therapy; Chronic kidney failure; Clinical trial; Evaluation studies

MeSH Terms

Cell- and Tissue-Based Therapy/*methods
Fetal Stem Cells/transplantation
Humans
Kidney/cytology
Kidney Diseases/*therapy
Pluripotent Stem Cells/transplantation
Stem Cell Transplantation/methods

Cited by  1 articles

Hypoxic Preconditioned Mesenchymal Stromal Cell Therapy in a Rat Model of Renal Ischemia-reperfusion Injury: Development of Optimal Protocol to Potentiate Therapeutic Efficacy
Myoung Jin Jang, Dalsan You, Jin Young Park, Kyung Kim, Joomin Aum, Chunwoo Lee, Geehyun Song, Ha Chul Shin, Nayoung Suh, Yong Man Kim, Choung-Soo Kim
Int J Stem Cells. 2018;11(2):157-167.    doi: 10.15283/ijsc18073.


Reference

1. Jha V, Garcia-Garcia G. Global kidney disease - Authors' reply. Lancet. 2013; 382:1244.
2. Bellomo R, Kellum JA, Ronco C. Acute kidney injury. Lancet. 2012; 380:756–766.
3. Chawla LS, Eggers PW, Star RA, Kimmel PL. Acute kidney injury and chronic kidney disease as interconnected syndromes. N Engl J Med. 2014; 371:58–66.
4. National Kidney and Urologic Diseases Information Clearinghouse (NKUDIC). Kidney disease statistics for the United States. Bethesda (MD): NKUDIC;2012.
5. Bussolati B, Hauser PV, Carvalhosa R, Camussi G. Contribution of stem cells to kidney repair. Curr Stem Cell Res Ther. 2009; 4:2–8.
6. Aboushwareb T, Atala A. Stem cells in urology. Nat Clin Pract Urol. 2008; 5:621–631.
7. Jansen J, Fedecostante M, Wilmer MJ, van den Heuvel LP, Hoenderop JG, Masereeuw R. Biotechnological challenges of bioartificial kidney engineering. Biotechnol Adv. 2014; 32:1317–1327.
8. Humes HD, Buffington DA, MacKay SM, Funke AJ, Weitzel WF. Replacement of renal function in uremic animals with a tissue-engineered kidney. Nat Biotechnol. 1999; 17:451–455.
9. Davenport A, Gura V, Ronco C, Beizai M, Ezon C, Rambod E. A wearable haemodialysis device for patients with end-stage renal failure: a pilot study. Lancet. 2007; 370:2005–2010.
10. Wang PC, Takezawa T. Reconstruction of renal glomerular tissue using collagen vitrigel scaffold. J Biosci Bioeng. 2005; 99:529–540.
11. Lu SH, Lin Q, Liu YN, Gao Q, Hao T, Wang Y, et al. Self-assembly of renal cells into engineered renal tissues in collagen/Matrigel scaffold in vitro. J Tissue Eng Regen Med. 2012; 6:786–792.
12. Guimaraes-Souza NK, Yamaleyeva LM, AbouShwareb T, Atala A, Yoo JJ. In vitro reconstitution of human kidney structures for renal cell therapy. Nephrol Dial Transplant. 2012; 27:3082–3090.
13. Yoo JJ, Ashkar S, Atala A. Creation of functional kidney structures with excretion of kidney-like fluid in vivo. Pediatrics. 1996; 98:suppl. 605.
14. Kim SS, Park HJ, Han J, Choi CY, Kim BS. Renal tissue reconstitution by the implantation of renal segments on biodegradable polymer scaffolds. Biotechnol Lett. 2003; 25:1505–1508.
15. Lanza RP, Chung HY, Yoo JJ, Wettstein PJ, Blackwell C, Borson N, et al. Generation of histocompatible tissues using nuclear transplantation. Nat Biotechnol. 2002; 20:689–696.
16. Williams D. Benefit and risk in tissue engineering. Materialstoday. 2004; 7:24–29.
17. Eirin A, Lerman LO. Mesenchymal stem cell treatment for chronic renal failure. Stem Cell Res Ther. 2014; 5:83.
18. Rosenberg ME. Cell-based therapies in kidney disease. Kidney Int Suppl (2011). 2013; 3:364–367.
19. Li Y, Wingert RA. Regenerative medicine for the kidney: stem cell prospects & challenges. Clin Transl Med. 2013; 2:11.
20. Hendry CE, Little MH. Reprogramming the kidney: a novel approach for regeneration. Kidney Int. 2012; 82:138–146.
21. Reilly RF, Bulger RE, Kriz W. Structural-functional relationships in the kidney. In : Schiffer RW, editor. Diseases of the kidney and urinary tract. Philadelphia (PA): Lippincott Williams & Wilkins;2007. p. 2–53.
22. Strutz F, Zeisberg M, Renziehausen A, Raschke B, Becker V, van Kooten C, et al. TGF-beta 1 induces proliferation in human renal fibroblasts via induction of basic fibroblast growth factor (FGF-2). Kidney Int. 2001; 59:579–592.
23. Phillips AO, Steadman R. Diabetic nephropathy: the central role of renal proximal tubular cells in tubulointerstitial injury. Histol Histopathol. 2002; 17:247–252.
24. Helbert MJ, Dauwe S, De Broe ME. Flow cytometric immunodissection of the human nephron in vivo and in vitro. Exp Nephrol. 1999; 7:360–376.
25. Cummings BS, Lasker JM, Lash LH. Expression of glutathione-dependent enzymes and cytochrome P450s in freshly isolated and primary cultures of proximal tubular cells from human kidney. J Pharmacol Exp Ther. 2000; 293:677–685.
26. Qi W, Johnson DW, Vesey DA, Pollock CA, Chen X. Isolation, propagation and characterization of primary tubule cell culture from human kidney. Nephrology (Carlton). 2007; 12:155–159.
27. Presnell SC, Bruce AT, Wallace SM, Choudhury S, Genheimer CW, Cox B, et al. Isolation, characterization, and expansion methods for defined primary renal cell populations from rodent, canine, and human normal and diseased kidneys. Tissue Eng Part C Methods. 2011; 17:261–273.
28. Baer PC, Geiger H. Human renal cells from the thick ascending limb and early distal tubule: characterization of primary isolated and cultured cells by reverse transcription polymerase chain reaction. Nephrology (Carlton). 2008; 13:316–321.
29. Sagrinati C, Netti GS, Mazzinghi B, Lazzeri E, Liotta F, Frosali F, et al. Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys. J Am Soc Nephrol. 2006; 17:2443–2456.
30. Bruno S, Camussi G. Isolation and characterization of resident mesenchymal stem cells in human glomeruli. Methods Mol Biol. 2012; 879:367–380.
31. Angelotti ML, Ronconi E, Ballerini L, Peired A, Mazzinghi B, Sagrinati C, et al. Characterization of renal progenitors committed toward tubular lineage and their regenerative potential in renal tubular injury. Stem Cells. 2012; 30:1714–1725.
32. 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; 14:3138–3146.
33. Kitamura S, Yamasaki Y, Kinomura M, Sugaya T, Sugiyama H, Maeshima Y, et al. Establishment and characterization of renal progenitor like cells from S3 segment of nephron in rat adult kidney. FASEB J. 2005; 19:1789–1797.
34. Lindgren D, Bostrom AK, Nilsson K, Hansson J, Sjolund J, Moller C, et al. Isolation and characterization of progenitor-like cells from human renal proximal tubules. Am J Pathol. 2011; 178:828–837.
35. Al-Awqati Q, Oliver JA. The kidney papilla is a stem cells niche. Stem Cell Rev. 2006; 2:181–184.
36. Bussolati B, Bruno S, Grange C, Buttiglieri S, Deregibus MC, Cantino D, et al. Isolation of renal progenitor cells from adult human kidney. Am J Pathol. 2005; 166:545–555.
37. Sallustio F, De Benedictis L, Castellano G, Zaza G, Loverre A, Costantino V, et al. TLR2 plays a role in the activation of human resident renal stem/progenitor cells. FASEB J. 2010; 24:514–525.
38. Smeets B, Boor P, Dijkman H, Sharma SV, Jirak P, Mooren F, et al. Proximal tubular cells contain a phenotypically distinct, scattered cell population involved in tubular regeneration. J Pathol. 2013; 229:645–659.
39. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A. 1981; 78:7634–7638.
40. Morizane R, Monkawa T, Itoh H. Differentiation of murine embryonic stem and induced pluripotent stem cells to renal lineage in vitro. Biochem Biophys Res Commun. 2009; 390:1334–1339.
41. Kim D, Dressler GR. Nephrogenic factors promote differentiation of mouse embryonic stem cells into renal epithelia. J Am Soc Nephrol. 2005; 16:3527–3534.
42. Steenhard BM, Isom KS, Cazcarro P, Dunmore JH, Godwin AR, St John PL, et al. Integration of embryonic stem cells in metanephric kidney organ culture. J Am Soc Nephrol. 2005; 16:1623–1631.
43. Vigneau C, Polgar K, Striker G, Elliott J, Hyink D, Weber O, et al. Mouse embryonic stem cell-derived embryoid bodies generate progenitors that integrate long term into renal proximal tubules in vivo. J Am Soc Nephrol. 2007; 18:1709–1720.
44. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006; 126:663–676.
45. Zhou T, Benda C, Dunzinger S, Huang Y, Ho JC, Yang J, et al. Generation of human induced pluripotent stem cells from urine samples. Nat Protoc. 2012; 7:2080–2089.
46. Song B, Smink AM, Jones CV, Callaghan JM, Firth SD, Bernard CA, et al. The directed differentiation of human iPS cells into kidney podocytes. PLoS One. 2012; 7:e46453.
47. Okita K, Nagata N, Yamanaka S. Immunogenicity of induced pluripotent stem cells. Circ Res. 2011; 109:720–721.
48. De Coppi P, Bartsch G Jr, Siddiqui MM, Xu T, Santos CC, Perin L, et al. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol. 2007; 25:100–106.
49. Perin L, Giuliani S, Jin D, Sedrakyan S, Carraro G, Habibian R, et al. Renal differentiation of amniotic fluid stem cells. Cell Prolif. 2007; 40:936–948.
50. Siegel N, Rosner M, Unbekandt M, Fuchs C, Slabina N, Dolznig H, et al. Contribution of human amniotic fluid stem cells to renal tissue formation depends on mTOR. Hum Mol Genet. 2010; 19:3320–3331.
51. Caplan AI, Bruder SP. Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol Med. 2001; 7:259–264.
52. Phinney DG, Prockop DJ. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair: current views. Stem Cells. 2007; 25:2896–2902.
53. Oliver J. Correlations of structure and function and mechanisms of recovery in acute tubular necrosis. Am J Med. 1953; 15:535–557.
54. Cuppage FE, Tate A. Repair of the nephron following injury with mercuric chloride. Am J Pathol. 1967; 51:405–429.
55. 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:F31–F42.
56. Hu J, Zhang L, Wang N, Ding R, Cui S, Zhu F, et al. Mesenchymal stem cells attenuate ischemic acute kidney injury by inducing regulatory T cells through splenocyte interactions. Kidney Int. 2013; 84:521–531.
57. Morigi M, Introna M, Imberti B, Corna D, Abbate M, Rota C, et al. Human bone marrow mesenchymal stem cells accelerate recovery of acute renal injury and prolong survival in mice. Stem Cells. 2008; 26:2075–2082.
58. Reis LA, Borges FT, Simoes 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:e44092.
59. Semedo P, Correa-Costa M, Antonio Cenedeze M, Maria Avancini Costa Malheiros D, Antonia dos Reis M, Shimizu MH, et al. Mesenchymal stem cells attenuate renal fibrosis through immune modulation and remodeling properties in a rat remnant kidney model. Stem Cells. 2009; 27:3063–3073.
60. Franquesa M, Herrero E, Torras J, Ripoll E, Flaquer M, Goma M, et al. Mesenchymal stem cell therapy prevents interstitial fibrosis and tubular atrophy in a rat kidney allograft model. Stem Cells Dev. 2012; 21:3125–3135.
61. Tomasoni S, Longaretti L, Rota C, Morigi M, Conti S, Gotti E, et al. Transfer of growth factor receptor mRNA via exosomes unravels the regenerative effect of mesenchymal stem cells. Stem Cells Dev. 2013; 22:772–780.
62. Xinaris C, Morigi M, Benedetti V, Imberti B, Fabricio AS, Squarcina E, et al. A novel strategy to enhance mesenchymal stem cell migration capacity and promote tissue repair in an injury specific fashion. Cell Transplant. 2013; 22:423–436.
63. 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; 115:1756–1764.
64. Prodromidi EI, Poulsom R, Jeffery R, Roufosse CA, Pollard PJ, Pusey CD, 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; 24:2448–2455.
65. Cornacchia F, Fornoni A, Plati AR, Thomas A, Wang Y, Inverardi L, et al. Glomerulosclerosis is transmitted by bone marrow-derived mesangial cell progenitors. J Clin Invest. 2001; 108:1649–1656.
66. Ikarashi K, Li B, Suwa M, Kawamura K, Morioka T, Yao J, et al. Bone marrow cells contribute to regeneration of damaged glomerular endothelial cells. Kidney Int. 2005; 67:1925–1933.
67. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem. 2006; 98:1076–1084.
68. Bruno S, Grange C, Deregibus MC, Calogero RA, Saviozzi S, Collino F, et al. Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol. 2009; 20:1053–1067.
69. Wang Y, He J, Pei X, Zhao W. Systematic review and meta-analysis of mesenchymal stem/stromal cells therapy for impaired renal function in small animal models. Nephrology (Carlton). 2013; 18:201–208.
70. Duffy MM, Ritter T, Ceredig R, Griffin MD. Mesenchymal stem cell effects on T-cell effector pathways. Stem Cell Res Ther. 2011; 2:34.
71. Camussi G, Deregibus MC, Tetta C. Paracrine/endocrine mechanism of stem cells on kidney repair: role of microvesicle-mediated transfer of genetic information. Curr Opin Nephrol Hypertens. 2010; 19:7–12.
72. Ke YH, He JW, Fu WZ, Zhang ZL. Identification of two novel mutations in the OCRL1 gene in two Chinese families with Lowe syndrome. Nephrology (Carlton). 2012; 17:20–25.
73. Ito T, Suzuki A, Imai E, Okabe M, Hori M. Bone marrow is a reservoir of repopulating mesangial cells during glomerular remodeling. J Am Soc Nephrol. 2001; 12:2625–2635.
74. 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; 25:697–706.
75. Thirabanjasak D, Tantiwongse K, Thorner PS. Angiomyeloproliferative lesions following autologous stem cell therapy. J Am Soc Nephrol. 2010; 21:1218–1222.
76. de Almeida DC, Donizetti-Oliveira C, Barbosa-Costa P, Origassa CS, Câmara NO. In search of mechanisms associated with mesenchymal stem cell-based therapies for acute kidney injury. Clin Biochem Rev. 2013; 34:131–144.
77. Chen YT, Sun CK, Lin YC, Chang LT, Chen YL, Tsai TH, et al. Adipose-derived mesenchymal stem cell protects kidneys against ischemia-reperfusion injury through suppressing oxidative stress and inflammatory reaction. J Transl Med. 2011; 9:51.
78. Donizetti-Oliveira C, Semedo P, Burgos-Silva M, Cenedeze MA, Malheiros DM, Reis MA, et al. Adipose tissue-derived stem cell treatment prevents renal disease progression. Cell Transplant. 2012; 21:1727–1741.
79. Kim JH, Park DJ, Yun JC, Jung MH, Yeo HD, Kim HJ, et al. Human adipose tissue-derived mesenchymal stem cells protect kidneys from cisplatin nephrotoxicity in rats. Am J Physiol Renal Physiol. 2012; 302:F1141–F1150.
80. Eirin A, Zhu XY, Krier JD, Tang H, Jordan KL, Grande JP, et al. Adipose tissue-derived mesenchymal stem cells improve revascularization outcomes to restore renal function in swine atherosclerotic renal artery stenosis. Stem Cells. 2012; 30:1030–1041.
81. Zhu XY, Urbieta-Caceres V, Krier JD, Textor SC, Lerman A, Lerman LO. Mesenchymal stem cells and endothelial progenitor cells decrease renal injury in experimental swine renal artery stenosis through different mechanisms. Stem Cells. 2013; 31:117–125.
82. Harari-Steinberg O, Metsuyanim S, Omer D, Gnatek Y, Gershon R, Pri-Chen S, et al. Identification of human nephron progenitors capable of generation of kidney structures and functional repair of chronic renal disease. EMBO Mol Med. 2013; 5:1556–1568.
83. Wang HJ, Varner A, AbouShwareb T, Atala A, Yoo JJ. Ischemia/reperfusion-induced renal failure in rats as a model for evaluating cell therapies. Ren Fail. 2012; 34:1324–1332.
84. Maxwell PH, Osmond MK, Pugh CW, Heryet A, Nicholls LG, Tan CC, et al. Identification of the renal erythropoietin-producing cells using transgenic mice. Kidney Int. 1993; 44:1149–1162.
85. Yamaleyeva LM, Guimaraes-Souza NK, Krane LS, Agcaoili S, Gyabaah K, Atala A, et al. Cell therapy with human renal cell cultures containing erythropoietin-positive cells improves chronic kidney injury. Stem Cells Transl Med. 2012; 1:373–383.
86. Kelley R, Werdin ES, Bruce AT, Choudhury S, Wallace SM, Ilagan RM, et al. Tubular cell-enriched subpopulation of primary renal cells improves survival and augments kidney function in rodent model of chronic kidney disease. Am J Physiol Renal Physiol. 2010; 299:F1026–F1039.
87. Hauser PV, De Fazio R, Bruno S, Sdei S, Grange C, Bussolati B, et al. Stem cells derived from human amniotic fluid contribute to acute kidney injury recovery. Am J Pathol. 2010; 177:2011–2021.
88. Rota C, Imberti B, Pozzobon M, Piccoli M, De Coppi P, Atala A, et al. Human amniotic fluid stem cell preconditioning improves their regenerative potential. Stem Cells Dev. 2012; 21:1911–1923.
89. Sedrakyan S, Da Sacco S, Milanesi A, Shiri L, Petrosyan A, Varimezova R, et al. Injection of amniotic fluid stem cells delays progression of renal fibrosis. J Am Soc Nephrol. 2012; 23:661–673.
90. Baulier E, Favreau F, Le Corf A, Jayle C, Schneider F, Goujon JM, 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; 3:809–820.
91. Lee PY, Chien Y, Chiou GY, Lin CH, Chiou CH, Tarng DC. Induced pluripotent stem cells without c-Myc attenuate acute kidney injury via downregulating the signaling of oxidative stress and inflammation in ischemia-reperfusion rats. Cell Transplant. 2012; 21:2569–2585.
92. Imberti B, Tomasoni S, Ciampi O, Pezzotta A, Derosas M, Xinaris C, et al. Renal progenitors derived from human iPSCs engraft and restore function in a mouse model of acute kidney injury. Sci Rep. 2015; 5:8826.
93. Reinders ME, de Fijter JW, Roelofs H, Bajema IM, de Vries DK, Schaapherder AF, et al. Autologous bone marrow-derived mesenchymal stromal cells for the treatment of allograft rejection after renal transplantation: results of a phase I study. Stem Cells Transl Med. 2013; 2:107–111.
94. Tan J, Wu W, Xu X, Liao L, Zheng F, Messinger S, et al. Induction therapy with autologous mesenchymal stem cells in living-related kidney transplants: a randomized controlled trial. JAMA. 2012; 307:1169–1177.
95. Perico N, Casiraghi F, Introna M, Gotti E, Todeschini M, Cavinato RA, et al. Autologous mesenchymal stromal cells and kidney transplantation: a pilot study of safety and clinical feasibility. Clin J Am Soc Nephrol. 2011; 6:412–422.
96. Reports Global Information Premium Market Research. Acute renal failure (ARF) (Acute Kidney Injury): pipeline review, H2 2014. Tokyo: H&I Co.;2014.
97. Ko IK, Abolbashari M, Huling J, Kim C, Mirmalek Sani SH, Moradi M, et al. Enhanced re-endothelialization of acellular kidney scaffolds for whole organ engineering via antibody conjugation of vasculatures. Technology. 2014; 2:243–253.
98. Kim IH, Ko IK, Atala A, Yoo JJ. Whole kidney engineering for clinical translation. Curr Opin Organ Transplant. 2015; 20:165–170.
99. Sullivan DC, Mirmalek-Sani SH, Deegan DB, Baptista PM, Aboushwareb T, Atala A, et al. Decellularization methods of porcine kidneys for whole organ engineering using a high-throughput system. Biomaterials. 2012; 33:7756–7764.
Full Text Links
  • KJU
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr