Human Endothelial Colony-Forming Cells Protect against Acute Kidney Injury Role of Exosomes

American Journal of Pathology

Volumn 185, Issue 8, 2015, Pages 2309-2323

  Burger, Dylan ^a   Viñas, Jose L ^a   Akbari, Shareef ^a   Dehak, Hajira ^a   Knoll, William ^a   Gutsol, Alex ^a   Carter, Anthony ^a   Touyz, Rhian M ^a,b   Allan, David S ^a   Burns, Kevin D ^a  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CREATININE; REACTIVE OXYGEN METABOLITE;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL INFILTRATION; COLONY FORMING CELL; CONTROLLED STUDY; CREATININE BLOOD LEVEL; ENDOTHELIAL COLONY FORMING CELL; ENDOTHELIUM CELL; EXOSOME; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; KIDNEY ISCHEMIA; KIDNEY TUBULE NECROSIS; MACROPHAGE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; UMBILICAL CORD BLOOD; UMBILICAL VEIN ENDOTHELIAL CELL; ACUTE KIDNEY INJURY; ANGIOGENESIS; ANIMAL; CELL PROLIFERATION; CYTOLOGY; METABOLISM; NONOBESE DIABETIC MOUSE; PHYSIOLOGY; STEM CELL;

ACUTE KIDNEY INJURY; ANIMALS; CELL PROLIFERATION; EXOSOMES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE; MICE, INBRED NOD; NEOVASCULARIZATION, PHYSIOLOGIC; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; STEM CELLS;

EID: 84937896090     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2015.04.010     Document Type: Article

References (53)

1. M. James, J. Bouchard, J. Ho, S. Klarenbach, J.P. LaFrance, C. Rigatto, R. Wald, M. Zappitelli, and N. Pannu Canadian Society of Nephrology commentary on the 2012 KDIGO clinical practice guideline for acute kidney injury Am J Kidney Dis 61 2013 673 685
2. J.V. Bonventre, and L. Yang Cellular pathophysiology of ischemic acute kidney injury J Clin Invest 121 2011 4210 4221
3. D.P. Basile The endothelial cell in ischemic acute kidney injury: implications for acute and chronic function Kidney Int 72 2007 151 156
4. C.J. Liang, W.C. Shen, F.B. Chang, V.C. Wu, S.H. Wang, G.H. Young, J.S. Tsai, Y.C. Tseng, Y.S. Peng, and Y.L. Chen Endothelial progenitor cells derived from Wharton's jelly of human umbilical cord attenuate ischemic acute kidney injury by increasing vascularization and decreasing apoptosis, inflammation, and fibrosis Cell Transplant 2014 [Epub ahead of print] http://dx.doi.org/10.3727/096368914X681720
5. M. Morigi, and A. Benigni Mesenchymal stem cells and kidney repair Nephrol Dial Transplant 28 2013 788 793
6. D. Patschan, S. Patschan, and G.A. Muller Endothelial progenitor cells in acute ischemic kidney injury: strategies for increasing the cells' renoprotective competence Int J Nephrol 2011 2011 828369
7. F.E. Togel, and C. Westenfelder Kidney protection and regeneration following acute injury: progress through stem cell therapy Am J Kidney Dis 60 2012 1012 1022
8. E.J. Suuronen, S. Wong, V. Kapila, G. Waghray, S.C. Whitman, T.G. Mesana, and M. Ruel Generation of CD133+ cells from CD133- peripheral blood mononuclear cells and their properties Cardiovasc Res 70 2006 126 135
9. D. Burger, A. Gutsol, A. Carter, D.S. Allan, R.M. Touyz, and K.D. Burns Human cord blood CD133+ cells exacerbate ischemic acute kidney injury in mice Nephrol Dial Transplant 27 2012 3781 3789
10. S.V. Brodsky, T. Yamamoto, T. Tada, B. Kim, J. Chen, F. Kajiya, and M.S. Goligorsky Endothelial dysfunction in ischemic acute renal failure: rescue by transplanted endothelial cells Am J Physiol Renal Physiol 282 2002 F1140 F1149
11. M.C. Yoder, L.E. Mead, D. Prater, T.R. Krier, K.N. Mroueh, F. Li, R. Krasich, C.J. Temm, J.T. Prchal, and D.A. Ingram Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals Blood 109 2007 1801 1809
12. B.J. Oh, D.K. Kim, B.J. Kim, K.-S. Yoon, S.G. Park, K.S. Park, M.-S. Lee, K.-W. Kim, and J.H. Kim Differences in donor CXCR4 expression levels are correlated with functional capacity and therapeutic outcome of angiogenic treatment with endothelial colony forming cells Biochem Biophys Res Commun 398 2010 627 633
13. P.R. Baraniak, and T.C. McDevitt Stem cell paracrine actions and tissue regeneration Regen Med 5 2010 121 143
14. V. Cantaluppi, S. Gatti, D. Medica, F. Figliolini, S. Bruno, M.C. Deregibus, A. Sordi, L. Biancone, C. Tetta, and G. Camussi Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells Kidney Int 82 2012 412 427
15. S. Bruno, C. Grange, F. Collino, M.C. Deregibus, V. Cantaluppi, L. Biancone, C. Tetta, and G. Camussi Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury PLoS One 7 2012 e33115
16. S. Bruno, C. Grange, M.C. Deregibus, R.A. Calogero, S. Saviozzi, F. Collino, L. Morando, A. Busca, M. Falda, B. Bussolati, C. Tetta, and G. Camussi Mesenchymal stem cell-derived microvesicles protect against acute tubular injury J Am Soc Nephrol 20 2009 1053 1067
17. M.B. Sanchez, S. Bruno, C. Grange, M. Tapparo, V. Cantaluppi, C. Tetta, and G. Camussi Human liver stem cells and derived extracellular vesicles improve recovery in a murine model of acute kidney injury Stem Cell Res Ther 5 2014 124
18. J. Sun, Y. Li, G.M. Graziani, L. Filion, and D.S. Allan E-selectin mediated adhesion and migration of endothelial colony forming cells is enhanced by SDF-1alpha/CXCR4 PLoS One 8 2013 e60890
19. rd Edition 2006 Springer New York, NY 985
20. S.R. Dunn, Z. Qi, E.P. Bottinger, M.D. Breyer, and K. Sharma Utility of endogenous creatinine clearance as a measure of renal function in mice Kidney Int 65 2004 1959 1967
21. C.W. Yang, C. Li, J.Y. Jung, S.J. Shin, B.S. Choi, S.W. Lim, B.K. Sun, Y.S. Kim, J. Kim, Y.S. Chang, and B.K. Bang Preconditioning with erythropoietin protects against subsequent ischemia-reperfusion injury in rat kidney FASEB J 17 2003 1754 1755
22. T. Yoshida, H. Sugiura, M. Mitobe, K. Tsuchiya, S. Shirota, S. Nishimura, S. Shiohira, H. Ito, K. Nobori, S.R. Gullans, T. Akiba, and K. Nitta ATF3 protects against renal ischemia-reperfusion injury J Am Soc Nephrol 19 2008 217 224
23. D. Burger, D.G. Kwart, A.C. Montezano, N.C. Read, C.R. Kennedy, C.S. Thompson, and R.M. Touyz Microparticles induce cell cycle arrest through redox-sensitive processes in endothelial cells: implications in vascular senescence J Am Heart Assoc 1 2012 e001842
24. D. Burger, A.C. Montezano, N. Nishigaki, Y. He, A. Carter, and R.M. Touyz Endothelial microparticle formation by angiotensin II is mediated via Ang II receptor type I/NADPH oxidase/Rho kinase pathways targeted to lipid rafts Arterioscler Thromb Vasc Biol 31 2011 1898 1907
25. D.C. Fernandes, J. Wosniak Jr., L.A. Pescatore, M.A. Bertoline, M. Liberman, F.R. Laurindo, and C.X. Santos Analysis of DHE-derived oxidation products by HPLC in the assessment of superoxide production and NADPH oxidase activity in vascular systems Am J Physiol Cell Physiol 292 2007 C413 C422
26. J. Wang, S. Chen, X. Ma, C. Cheng, X. Xiao, J. Chen, S. Liu, B. Zhao, and Y. Chen Effects of endothelial progenitor cell-derived microvesicles on hypoxia/reoxygenation-induced endothelial dysfunction and apoptosis Oxid Med Cell Longev 2013 2013 572729
27. M. Ostrowski, N.B. Carmo, S. Krumeich, I. Fanget, G. Raposo, A. Savina, C.F. Moita, K. Schauer, A.N. Hume, R.P. Freitas, B. Goud, P. Benaroch, N. Hacohen, M. Fukuda, C. Desnos, M.C. Seabra, F. Darchen, S. Amigorena, L.F. Moita, and C. Thery Rab27a and Rab27b control different steps of the exosome secretion pathway Nat Cell Biol 12 2010 19 30 supp 11-13
28. D. Burger, J.F. Thibodeau, C.E. Holterman, K.D. Burns, R.M. Touyz, and C.R. Kennedy Urinary podocyte microparticles identify pre-albuminuric diabetic glomerular injury J Am Soc Nephrol 25 2014 1401 1407
29. C. Gardiner, Y.J. Ferreira, R.A. Dragovic, C.W. Redman, and I.L. Sargent Extracellular vesicle sizing and enumeration by nanoparticle tracking analysis J Extracell Vesicles 2 2013 19671
30. D. Burger, M. Lei, N. Geoghegan-Morphet, X. Lu, A. Xenocostas, and Q. Feng Erythropoietin protects cardiomyocytes from apoptosis via up-regulation of endothelial nitric oxide synthase Cardiovasc Res 72 2006 51 59
31. E.I. Christensen, H. Birn, T. Storm, K. Weyer, and R. Nielsen Endocytic receptors in the renal proximal tubule Physiology (Bethesda) 27 2012 223 236
32. S.K. Jo, S.A. Sung, W.Y. Cho, K.J. Go, and H.K. Kim Macrophages contribute to the initiation of ischaemic acute renal failure in rats Nephrol Dial Transplant 21 2006 1231 1239
33. D.J. Oh, B. Dursun, Z. He, L. Lu, T.S. Hoke, D. Ljubanovic, S. Faubel, and C.L. Edelstein Fractalkine receptor (CX3CR1) inhibition is protective against ischemic acute renal failure in mice Am J Physiol Renal Physiol 294 2008 F264 F271
34. C. Thery, M. Ostrowski, and E. Segura Membrane vesicles as conveyors of immune responses Nat Rev Immunol 9 2009 581 593
35. H. Sugimoto, K. Shikata, K. Hirata, K. Akiyama, M. Matsuda, M. Kushiro, Y. Shikata, N. Miyatake, M. Miyasaka, and H. Makino Increased expression of intercellular adhesion molecule-1 (ICAM-1) in diabetic rat glomeruli: glomerular hyperfiltration is a potential mechanism of ICAM-1 upregulation Diabetes 46 1997 2075 2081
36. D. Patschan, S. Patschan, J.T. Wessels, J.U. Becker, S. David, E. Henze, M.S. Goligorsky, and G.A. Muller Epac-1 activator 8-O-cAMP augments renoprotective effects of syngeneic [corrected] murine EPCs in acute ischemic kidney injury Am J Physiol Renal Physiol 298 2010 F78 F85
37. D. Patschan, R. Backhaus, H.J. Elle, K. Schwarze, E. Henze, J.U. Becker, S. Patschan, and G.A. Muller Angiopoietin-2 modulates eEOC-mediated renoprotection in AKI in a dose-dependent manner J Nephrol 26 2013 667 674
38. S.S. Waikar, and J.V. Bonventre Can we rely on blood urea nitrogen as a biomarker to determine when to initiate dialysis? Clin J Am Soc Nephrol 1 2006 903 904
39. A. Tojo, K. Asaba, and M.L. Onozato Suppressing renal NADPH oxidase to treat diabetic nephropathy Expert Opin Ther Targets 11 2007 1011 1018
40. R.M. Touyz, A.M. Briones, M. Sedeek, D. Burger, and A.C. Montezano NOX isoforms and reactive oxygen species in vascular health Mol Interv 11 2011 27 35
41. M.Z. Ratajczak, M. Kucia, T. Jadczyk, N.J. Greco, W. Wojakowski, M. Tendera, and J. Ratajczak Pivotal role of paracrine effects in stem cell therapies in regenerative medicine: can we translate stem cell-secreted paracrine factors and microvesicles into better therapeutic strategies? Leukemia 26 2012 1166 1173
42. N. Imai, T. Kaur, M.E. Rosenberg, and S. Gupta Innovation in the treatment of uremia: proceedings from the Cleveland Clinic Workshop: cellular therapy of kidney diseases Semin Dial 22 2009 629 635
43. D. Burger, S. Schock, C.S. Thompson, A.C. Montezano, A.M. Hakim, and R.M. Touyz Microparticles: biomarkers and beyond Clin Sci (Lond) 124 2013 423 441
44. Y. Zhou, H. Xu, W. Xu, B. Wang, H. Wu, Y. Tao, B. Zhang, M. Wang, F. Mao, Y. Yan, S. Gao, H. Gu, W. Zhu, and H. Qian 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 4 2013 34
45. T. Katsuno, T. Ozaki, Y. Saka, K. Furuhashi, H. Kim, K. Yasuda, T. Yamamoto, W. Sato, N. Tsuboi, M. Mizuno, Y. Ito, E. Imai, S. Matsuo, and S. Maruyama Low serum cultured adipose tissue-derived stromal cells ameliorate acute kidney injury in rats Cell Transplant 22 2013 287 297
46. K. Yasuda, T. Ozaki, Y. Saka, T. Yamamoto, M. Gotoh, Y. Ito, Y. Yuzawa, S. Matsuo, and S. Maruyama Autologous cell therapy for cisplatin-induced acute kidney injury by using non-expanded adipose tissue-derived cells Cytotherapy 14 2012 1089 1100
47. D.P. Basile, M.D. Anderson, and T.A. Sutton Pathophysiology of acute kidney injury Compr Physiol 2 2012 1303 1353
48. B. Li, A. Cohen, T.E. Hudson, D. Motlagh, D.L. Amrani, and J.S. Duffield Mobilized human hematopoietic stem/progenitor cells promote kidney repair after ischemia/reperfusion injury Circulation 121 2010 2211 2220
49. L. Frangsmyr, V. Baranov, O. Nagaeva, U. Stendahl, L. Kjellberg, and L. Mincheva-Nilsson Cytoplasmic microvesicular form of Fas ligand in human early placenta: switching the tissue immune privilege hypothesis from cellular to vesicular level Mol Hum Reprod 11 2005 35 41
50. T.E. Ichim, Z. Zhong, S. Kaushal, X. Zheng, X. Ren, X. Hao, J.A. Joyce, H.H. Hanley, N.H. Riordan, J. Koropatnick, V. Bogin, B.R. Minev, W.P. Min, and R.H. Tullis Exosomes as a tumor immune escape mechanism: possible therapeutic implications J Transl Med 6 2008 37
51. S. Schrepfer, T. Deuse, H. Reichenspurner, M.P. Fischbein, R.C. Robbins, and M.P. Pelletier Stem cell transplantation: the lung barrier Transplant Proc 39 2007 573 576
52. Y. Takahashi, M. Nishikawa, H. Shinotsuka, Y. Matsui, S. Ohara, T. Imai, and Y. Takakura Visualization and in vivo tracking of the exosomes of murine melanoma B16-BL6 cells in mice after intravenous injection J Biotechnol 165 2013 77 84
53. N. Amariglio, A. Hirshberg, B.W. Scheithauer, Y. Cohen, R. Loewenthal, L. Trakhtenbrot, N. Paz, M. Koren-Michowitz, D. Waldman, L. Leider-Trejo, A. Toren, S. Constantini, and G. Rechavi Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient PLoS Med 6 2009 e1000029