Beneficial effects of systemically administered human muse cells in adriamycin nephropathy

Journal of the American Society of Nephrology

Volumn 28, Issue 10, 2017, Pages 2946-2960

  Uchida, Nao ^a   Kushida, Yoshihiro ^a   Kitada, Masaaki ^a   Wakao, Shohei ^a   Kumagai, Naonori ^a   Kuroda, Yasumasa ^a   Kondo, Yoshiaki ^b   Hirohara, Yukari ^a,c   Kure, Shigeo ^a   Chazenbalk, Gregorio ^d   Dezawa, Mari ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NIHON UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Life Science Institute   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CREATININE; ORGANIC CATION TRANSPORTER 3; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; VON WILLEBRAND FACTOR; DOXORUBICIN;

ADHERENT CELL; ADRIAMYCIN-INDUCED NEPHROPATHY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CREATININE CLEARANCE; ENDOTHELIUM CELL; GLOMERULOSCLEROSIS; HUMAN; HUMAN CELL; INDUCED PLURIPOTENT STEM CELL; KIDNEY FUNCTION; MESANGIUM CELL; MOUSE; MUSE CELL; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN URINE LEVEL; RENAL PROTECTION; ANIMAL; BAGG ALBINO MOUSE; CELL MOTION; CHEMICALLY INDUCED; EVALUATION STUDY; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; KIDNEY FUNCTION TEST; REGENERATION; SCID MOUSE; STEM CELL TRANSPLANTATION;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; DOXORUBICIN; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; HUMANS; KIDNEY FUNCTION TESTS; MICE, INBRED BALB C; MICE, SCID; REGENERATION; STEM CELL TRANSPLANTATION;

EID: 85030478810     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2016070775     Document Type: Article

References (41)

1. Aggarwal S, Moggio A, Bussolati B: Concise review: Stem/progenitor cells for renal tissue repair: Current knowledge and perspectives. Stem Cells Transl Med 2: 1011-1019, 2013
2. Hickson LJ, Eirin A, Lerman LO: Challenges and opportunities for stem cell therapy in patientswith chronic kidney disease. Kidney Int 89: 767-778, 2016
3. Kuroda Y, Kitada M, Wakao S, Nishikawa K, Tanimura Y, Makinoshima H, Goda M, Akashi H, Inutsuka A, Niwa A, Shigemoto T, Nabeshima Y, Nakahata T, Nabeshima Y, Fujiyoshi Y, Dezawa M: Unique multipotent cells in adult human mesenchymal cell populations. Proc Natl Acad Sci USA 107: 8639-8643, 2010
4. Kuroda Y, Wakao S, Kitada M, Murakami T, Nojima M, Dezawa M: Isolation, culture and evaluation of multilineage-differentiating stressenduring (Muse) cells. Nat Protoc 8: 1391-1415, 2013
5. Alessio N, Özcan S, Tatsumi K, Murat A, Peluso G, DezawaM, Galderisi U: The secretome of MUSE cells contains factors that may play a role in regulation of stemness, apoptosis and immunomodulation. Cell Cycle 16: 33-44, 2017
6. Wakao S, Kitada M, Kuroda Y, Shigemoto T, Matsuse D, Akashi H, Tanimura Y, Tsuchiyama K, Kikuchi T, GodaM, Nakahata T, Fujiyoshi Y, Dezawa M: Multilineage-differentiating stress-enduring (Muse) cells are a primary source of induced pluripotent stem cells in human fibroblasts. Proc Natl Acad Sci USA 108: 9875-9880, 2011
7. Heneidi S, Simerman AA, Keller E, Singh P, Li X, Dumesic DA, Chazenbalk G: Awakened by cellular stress: Isolation and characterization of a novel population of pluripotent stem cells derived from human adipose tissue. PLoS One 8: E64752, 2013
8. Ogura F, Wakao S, Kuroda Y, Tsuchiyama K, Bagheri M, Heneidi S, Chazenbalk G, Aiba S, Dezawa M: Human adipose tissue possesses a unique population of pluripotent stem cells with nontumorigenic and low telomerase activities: Potential implications in regenerative medicine. Stem Cells Dev 23: 717-728, 2014
9. Kinoshita K, Kuno S, Ishimine H, Aoi N, Mineda K, Kato H, Doi K, Kanayama K, Feng J, Mashiko T, Kurisaki A, Yoshimura K: Therapeutic potential of adipose-derived SSEA-3-positive Muse cells for treating diabetic skin ulcers. Stem Cells Transl Med 4: 146-155, 2015
10. UchidaH, Morita T, Niizuma K, Kushida Y, Kuroda Y, Wakao S, SakataH, Matsuzaka Y, Mushiake H, Tominaga T, Borlongan CV, Dezawa M: Transplantation of unique subpopulation of fibroblasts, Muse cells, ameliorates experimental stroke possibly via robust neuronal differentiation. Stem Cells 34: 160-173, 2016
11. Iseki M, Kushida Y, Wakao S, Akimoto T, Mizuma M, Motoi F, Asada R, Shimizu S, Unno M, ChazenbalkG, DezawaM:Muse cells, nontumorigenic pluripotent-like stem cells, have liver regeneration capacity through specific homing and cell replacement in a mouse model of liver fibrosis. Cell Transplant 26: 821-840, 2017
12. Hori E, Hayakawa Y, Hayashi T, Hori S, Okamoto S, Shibata T, Kubo M, Horie Y, Sasahara M, Kuroda S: Mobilization of pluripotent multilineagedifferentiating stress-Enduring cells in ischemic stroke. J Stroke Cerebrovasc Dis 25: 1473-1481, 2016
13. Dezawa M: Muse cells provide the pluripotency of mesenchymal stem cells: Direct contribution of Muse cells to tissue regeneration. Cell Transplant 25: 849-861, 2016
14. Lee VW, Harris DC: Adriamycin nephropathy: A model of focal segmental glomerulosclerosis. Nephrology (Carlton) 16: 30-38, 2011
15. Zoja C, Garcia PB, Remuzzi G: The role of chemokines in progressive renal disease. Front Biosci (Landmark Ed) 14: 1815-1822, 2009
16. Eggenhofer E, Luk F, Dahlke MH, Hoogduijn MJ: The life and fate of mesenchymal stem cells. Front Immunol 5: 148, 2014
17. Batchelder CA, Lee CC, Matsell DG, Yoder MC, Tarantal AF: Renal ontogeny in the rhesus monkey (Macaca mulatta) and directed differentiation of human embryonic stem cells towards kidney precursors. Differentiation 78: 45-56, 2009
18. Yagi H, Soto-Gutierrez A, Parekkadan B, Kitagawa Y, Tompkins RG, Kobayashi N, Yarmush ML: Mesenchymal stem cells: Mechanisms of immunomodulation and homing. Cell Transplant 19: 667-679, 2010
19. LingW, Zhang J, Yuan Z, Ren G, Zhang L, Chen X, Rabson AB, Roberts AI, Wang Y, Shi Y: Mesenchymal stem cells use IDO to regulate immunity in tumor microenvironment. Cancer Res 74: 1576-1587, 2014
20. Ezquer ME, Ezquer FE, Arango-Rodríguez ML, Conget PA: MSC transplantation: A promising therapeutic strategy to manage the onset and progression of diabetic nephropathy. Biol Res 45: 289-296, 2012
21. Villanueva S, Ewertz E, Carrión F, Tapia A, Vergara C, Céspedes C, Sáez PJ, Luz P, Irarrázabal C, Carreño JE, Figueroa F, Vio CP: Mesenchymal stem cell injection ameliorates chronic renal failure in a rat model. Clin Sci (Lond) 121: 489-499, 2011
22. Ninichuk V, Gross O, Segerer S, Hoffmann R, Radomska E, Buchstaller A, Huss R, Akis N, Schlöndorff D, Anders HJ:Multipotentmesenchymal stem cells reduce interstitial fibrosis but do not delay progression of chronic kidney disease in collagen4A3-deficient mice. Kidney Int 70: 121-129, 2006
23. Arumugam TV, Phillips TM, Cheng A, Morrell CH, Mattson MP, Wan R: Age and energy intake interact to modify cell stress pathways and stroke outcome. Ann Neurol 67: 41-52, 2010
24. Song J, Finnerty CC, Herndon DN, Boehning D, Jeschke MG: Severe burn-induced endoplasmic reticulum stress and hepatic damage in mice. Mol Med 15: 316-320, 2009
25. Fulda S, Gorman AM, Hori O, Samali A: Cellular stress responses: Cell survival and cell death. Int J Cell Biol 2010: 214074, 2010
26. Huang XP, Sun Z, Miyagi Y, McDonald KinkaidH, Zhang L, Weisel RD, Li RK: Differentiation of allogeneic mesenchymal stem cells induces immunogenicity and limits their long-term benefits for myocardial repair. Circulation 122: 2419-2429, 2010
27. Gimeno ML, Fuertes F, Barcala Tabarrozzi AE, Attorressi AI, Cucchiani R, Corrales L, Oliveira TC, Sogayar MC, Labriola L, Dewey RA, Perone MJ: Pluripotent nontumorigenic adipose tissue-derived Muse cells have immunomodulatory capacity mediated by transforming frowth factor-beta1. Stem Cells Transl Med 6: 161-173, 2017
28. Novak ML, Koh TJ: Macrophage phenotypes during tissue repair. J Leukoc Biol 93: 875-881, 2013
29. Cho DI, Kim MR, Jeong HY, Jeong HC, Jeong MH, Yoon SH, Kim YS, Ahn Y: Mesenchymal stem cells reciprocally regulate the M1/M2 balance in mouse bone marrow-derived macrophages. Exp Mol Med 46: E70, 2014
30. Griffin SV, Petermann AT, Durvasula RV, Shankland SJ: Podocyte proliferation and differentiation in glomerular disease: Role of cell-cycle regulatory proteins. Nephrol Dial Transplant 18[Suppl 6]: Vi8-vi13, 2003
31. Guo JK, Cantley LG: Cellular maintenance and repair of the kidney. Annu Rev Physiol 72: 357-376, 2010
32. Sun YB, Qu X, Zhang X, Caruana G, Bertram JF, Li J: Glomerular endothelial cell injury and damage precedes that of podocytes in adriamycin-induced nephropathy. PLoS One 8: E55027, 2013
33. Wilkinson EL, Sidaway JE, Cross MJ: Cardiotoxic drugs Herceptin and doxorubicin inhibit cardiac microvascular endothelial cell barrier formation resulting in increased drug permeability. Biol Open 5: 1362-1370, 2016
34. Guerrot D, Dussaule JC, Kavvadas P, Boffa JJ, Chadjichristos CE, Chatziantoniou C: Progression of renal fibrosis: The underestimated role of endothelial alterations. Fibrogenesis Tissue Repair 5[Suppl 1]: S15, 2012
35. Nolan DJ, GinsbergM, Israely E, Palikuqi B, PoulosMG, James D, Ding BS, Schachterle W, Liu Y, Rosenwaks Z, Butler JM, Xiang J, Rafii A, Shido K, Rabbany SY, Elemento O, Rafii S: Molecular signatures of tissuespecific microvascular endothelial cell heterogeneity in organ maintenance and regeneration. Dev Cell 26: 204-219, 2013
36. Magnasco A, Corselli M, Bertelli R, Ibatici A, Peresi M, Gaggero G, Cappiello V, Chiavarina B, Mattioli G, Gusmano R, Ravetti JL, Frassoni F, Ghiggeri GM: Mesenchymal stem cells protective effect in adriamycin model of nephropathy. Cell Transplant 17: 1157-1167, 2008
37. Zoja C, Garcia PB, Rota C, Conti S, Gagliardini E, Corna D, Zanchi C, Bigini P, Benigni A, Remuzzi G, Morigi M: Mesenchymal stem cell therapy promotes renal repair by limiting glomerular podocyte and progenitor cell dysfunction in adriamycin-induced nephropathy. Am J Physiol Renal Physiol 303: F1370-F1381, 2012
38. Baulier E, Favreau F, Le Corf A, Jayle C, Schneider F, Goujon JM, Feraud O, Bennaceur-Griscelli A, Hauet T, Turhan AG: Amniotic fluidderived mesenchymal stem cells prevent fibrosis and preserve renal function in a preclinical porcine model of kidney transplantation. Stem Cells Transl Med 3: 809-820, 2014
39. Franquesa M, Herrero E, Torras J, Ripoll E, Flaquer M, Gomà M, Lloberas N, Anegon I, Cruzado JM, Grinyó JM, Herrero-Fresneda I: Mesenchymal stemcell therapy prevents interstitial fibrosis and tubular atrophy in a rat kidney allograft model. Stem Cells Dev 21: 3125-3135, 2012
40. Kunter U, Rong S, Djuric Z, Boor P, Müller-Newen G, Yu D, Floege J: Transplantedmesenchymal stemcells accelerate glomerular healing in experimental glomerulonephritis. J Am Soc Nephrol 17: 2202-2212, 2006
41. Kunter U, Rong S, Boor P, Eitner F, Müller-Newen G, Djuric Z, van Roeyen CR, Konieczny A, Ostendorf T, Villa L, Milovanceva-Popovska M, Kerjaschki D, Floege J:Mesenchymal stemcells prevent progressive experimental renal failure but maldifferentiate into glomerular adipocytes. J Am Soc Nephrol 18: 1754-1764, 2007