AKI recovery induced by mesenchymal stromal cell- derived extracellular vesicles carrying micrornas

Journal of the American Society of Nephrology

Volumn 26, Issue 10, 2015, Pages 2349-2360

  Collino, Federica ^a,b   Bruno, Stefania ^b   Incarnato, Danny ^b   Dettori, Daniela ^b   Neri, Francesco ^b   Provero, Paolo ^b,d   Pomatto, Margherita ^a   Oliviero, Salvatore ^b   Tetta, Ciro ^b,c   Quesenberry, Peter J ^e   Camussi, Giovanni ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c FRESENIUS MEDICAL CARE   (Germany)

^d SAN RAFFAELE HOSPITAL   (Italy)

^e BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; DROSHA PROTEIN; FATTY ACID; GLYCEROL; LENTIVIRUS VECTOR; MICRORNA; RIBONUCLEASE III; UNCLASSIFIED DRUG;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL TRANSPLANTATION; CLINICAL EVALUATION; CONTROLLED STUDY; CONVALESCENCE; DOWN REGULATION; EXOSOME; FATTY ACID METABOLISM; FEMALE; GENE EXPRESSION PROFILING; GENE ONTOLOGY; GENE OVEREXPRESSION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC TRANSDUCTION; INFLAMMATION; INTERNALIZATION; KIDNEY TUBULE CELL; MESENCHYMAL STROMA CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REGENERATIVE ABILITY; REGENERATIVE MEDICINE; RNA SEQUENCE; SCID MOUSE; SEQUENCE ANALYSIS; UPREGULATION; WILD TYPE; ACUTE KIDNEY INJURY; ANIMAL; EVALUATION STUDY; ULTRASTRUCTURE;

ACUTE KIDNEY INJURY; ANIMALS; EXTRACELLULAR VESICLES; FEMALE; MESENCHYMAL STROMAL CELLS; MICE; MICRORNAS;

EID: 84942893757     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014070710     Document Type: Article

References (48)

1. Humphreys BD, Valerius MT, Kobayashi A, Mugford JW, Soeung S, Duffield JS, McMahon AP, Bonventre JV: Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2: 284-291, 2008.
2. 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 18: 2486-2496, 2007.
3. Bruno S, Grange C, Deregibus MC, Calogero RA, Saviozzi S, Collino F, Morando L, Busca A, Falda M, Bussolati B, Tetta C, Camussi G: Mesenchymal stemcell-derivedmicrovesicles protect against acute tubular injury. J Am Soc Nephrol 20: 1053-1067, 2009.
4. Bruno S, Grange C, Collino F, Deregibus MC, Cantaluppi V, Biancone L, Tetta C, Camussi G: Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PLoS ONE 7: e33115, 2012.
5. He J, Wang Y, Sun S, Yu M, Wang C, Pei X, Zhu B, Wu J, Zhao W: Bone marrow stem cells-derived microvesicles protect against renal injury in the mouse remnant kidney model. Nephrology (Carlton) 17: 493-500, 2012.
6. Akers JC, Gonda D, Kim R, Carter BS, Chen CC: Biogenesis of extracellular vesicles (EV): Exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J Neurooncol 113: 1-11, 2013.
7. Lee Y, El-Andaloussi S, Wood MJ: Exosomes and microvesicles: Extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet 21: R125-R134, 2012.
8. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, Ratajczak MZ: Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: Evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20: 847-856, 2006.
9. Aliotta JM, Pereira M, Amaral A, Sorokina A, Igbinoba Z, Hasslinger A, El-Bizri R, Rounds SI, Quesenberry PJ, Klinger JR: Induction of pulmonary hypertensive changes by extracellular vesicles from monocrotalinetreated mice. Cardiovasc Res 100: 354-362, 2013.
10. Kim HS, Choi DY, Yun SJ, Choi SM, Kang JW, Jung JW, Hwang D, Kim KP, Kim DW: Proteomic analysis of microvesicles derived from human mesenchymal stem cells. J Proteome Res 11: 839-849, 2012.
11. Collino F, Deregibus MC, Bruno S, Sterpone L, Aghemo G, Viltono L, Tetta C, Camussi G: Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS ONE 5: e11803, 2010.
12. Maluf DG, Dumur CI, Suh JL, Scian MJ, King AL, Cathro H, Lee JK, Gehrau RC, Brayman KL, Gallon L, Mas VR: The urine microRNA profile may help monitor post-transplant renal graft function. Kidney Int 85: 439-449, 2014.
13. Kong YW, Ferland-McCollough D, Jackson TJ, Bushell M:microRNAs in cancer management. Lancet Oncol 13: e249-e258, 2012.
14. Blelloch R, Gutkind JS: Epigenetics, noncoding RNAs, and cell signaling- crossroads in the regulation of cell fate decisions. Curr Opin Cell Biol 25: 149-151, 2013.
15. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL, Tait JF, Tewari M: Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A 108: 5003-5008, 2011.
16. Quesenberry PJ, Goldberg LR, Aliotta JM, Dooner MS, Pereira MG, Wen S, Camussi G: Cellular phenotype and extracellular vesicles: Basic and clinical considerations. Stem Cells Dev 23: 1429-1436, 2014.
17. Cech TR, Steitz JA: The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157: 77-94, 2014.
18. Bartel DP: MicroRNAs: Target recognition and regulatory functions. Cell 136: 215-233, 2009.
19. Han J, Lee Y, Yeom KH, Kim YK, Jin H, Kim VN: The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 18: 3016-3027, 2004.
20. Leisegang MS, Martin R, Ramírez AS, Bohnsack MT: Exportin t and Exportin 5: tRNA andmiRNA biogenesis - And beyond. Biol Chem 393: 599-604, 2012.
21. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO: Exosomemediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659, 2007.
22. Yuan A, Farber EL, Rapoport AL, Tejada D, Deniskin R, Akhmedov NB, Farber DB: Transfer of microRNAs by embryonic stem cell microvesicles. PLoS ONE 4: e4722, 2009.
23. Xin H, Li Y, Buller B, Katakowski M, Zhang Y, Wang X, Shang X, Zhang ZG, Chopp M: Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells 30: 1556-1564, 2012.
24. Jinek M, Doudna JA: A three-dimensional view of the molecular machinery of RNA interference. Nature 457: 405-412, 2009.
25. Merritt WM, Bar-Eli M, Sood AK: The dicey role of Dicer: Implications for RNAi therapy. Cancer Res 70: 2571-2574, 2010.
26. Volk N, Shomron N: Versatility of MicroRNA biogenesis. PLoS ONE 6: e19391, 2011.
27. Xie M, Steitz JA: Versatile microRNA biogenesis in animals and their viruses. RNA Biol 11: 673-681, 2014.
28. Kashiwagi E, Tonomura Y, Kondo C, Masuno K, Fujisawa K, Tsuchiya N, Matsushima S, Torii M, Takasu N, Izawa T, Kuwamura M, Yamate J: Involvement of neutrophil gelatinase-associated lipocalin and osteopontin in renal tubular regeneration and interstitial fibrosis after cisplatin-induced renal failure. Exp Toxicol Pathol 66: 301-311, 2014.
29. Sörensen-Zender I, Rong S, Susnik N, Lange J, Gueler F, Degen JL, Melk A, Haller H, Schmitt R: Role of fibrinogen in acute ischemic kidney injury. Am J Physiol Renal Physiol 305: F777-F785, 2013.
30. 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 32: 1262-1272, 2013.
31. Kim JH, Park DJ, Yun JC, Jung MH, Yeo HD, Kim HJ, Kim DW, Yang JI, Lee GW, Jeong SH, Roh GS, Chang SH: Human adipose tissue-derived mesenchymal stem cells protect kidneys from cisplatin nephrotoxicity in rats. Am J Physiol Renal Physiol 302: F1141-F1150, 2012.
32. Zhou Y, Xu H, Xu W, Wang B, Wu H, Tao Y, Zhang B, Wang M, Mao F, Yan Y, Gao S, Gu H, Zhu W, Qian H: Exosomes released by human umbilical cord mesenchymal stem cells protect against cisplatin-induced renal oxidative stress and apoptosis in vivo and in vitro. StemCell Res Ther 4: 34, 2013.
33. Del-Tatto M, Ng T, Aliotta JM, Colvin GA, Dooner MS, Berz D, Dooner GJ, Papa EF, Hixson DC, Ramratnam B, Aswad BI, Sears EH, Reagan J, Quesenberry PJ: Marrow cell genetic phenotype change induced by human lung cancer cells. Exp Hematol 39: 1072-1080, 2011.
34. Tomasoni S, Longaretti L, Rota C, MorigiM, Conti S, Gotti E, Capelli C, Introna M, Remuzzi G, Benigni A: Transfer of growth factor receptor mRNA via exosomes unravels the regenerative effect of mesenchymal stem cells. Stem Cells Dev 22: 772-780, 2013.
35. Lindoso RS, Collino F, Bruno S, Araujo DS, Sant'Anna JF, Tetta C, Provero P, Quesenberry PJ, Vieyra A, Einicker-Lamas M, Camussi G: Extracellular vesicles released from mesenchymal stromal cells modulate miRNA in renal tubular cells and inhibit ATP depletion injury. Stem Cells Dev 23: 1809-1819, 2014.
36. Negishi K, Noiri E, Sugaya T, Li S, Megyesi J, Nagothu K, Portilla D: A role of liver fatty acid-binding protein in cisplatin-induced acute renal failure. Kidney Int 72: 348-358, 2007 37.
37. Da-Costa MR, Pizzatti L, Lindoso RS, Sant'Anna JF, DuRocher B, Abdelhay E, Vieyra A: Mechanisms of kidney repair by human mesenchymal stromal cells after ischemia: A comprehensive view using labelfree MS(E). Proteomics 14: 1480-1493, 2014.
38. Fang Y, Tian X, Bai S, Fan J, Hou W, Tong H, Li D: Autologous transplantation of adipose-derived mesenchymal stem cells ameliorates streptozotocin-induced diabetic nephropathy in rats by inhibiting oxidative stress, pro-inflammatory cytokines and the p38 MAPK signaling pathway. Int J Mol Med 30: 85-92, 2012.
39. Guo Y, Xiao L, Sun L, Liu F: Wnt/beta-catenin signaling: A promising new target for fibrosis diseases. Physiol Res 61: 337-346, 2012.
40. Gonçalves JG, de Bragança AC, Canale D, Shimizu MH, Sanches TR, Moysés RM, Andrade L, Seguro AC, Volpini RA: Vitamin D deficiency aggravates chronic kidney disease progression after ischemic acute kidney injury. PLoS ONE 9: e107228, 2014.
41. Ying Y, Kim J, Westphal SN, Long KE, Padanilam BJ: Targeted deletion of p53 in the proximal tubule prevents ischemic renal injury [published online ahead of print May 22, 2014]. J Am Soc Nephrol.doi:ASN. 2013121270.
42. Oskowitz AZ, Penfornis P, Tucker A, Prockop DJ, Pochampally R: Drosha regulates hMSCs cell cycle progression through a miRNA independent mechanism. Int J Biochem Cell Biol 43: 1563-1572, 2011.
43. Aagaard L, Amarzguioui M, Sun G, Santos LC, Ehsani A, Prydz H, Rossi JJ: A facile lentiviral vector system for expression of doxycyclineinducible shRNAs: Knockdown of the pre-miRNA processing enzyme Drosha. Mol Ther 15: 938-945, 2007.
44. Bruno S, Collino F, Deregibus MC, Grange C, Tetta C, Camussi G: Microvesicles derived from human bone marrow mesenchymal stem cells inhibit tumor growth. Stem Cells Dev 22: 758-771, 2013.
45. Grange C, Tapparo M, Bruno S, Chatterjee D, Quesenberry PJ, Tetta C, Camussi G: Biodistribution of mesenchymal stem cell-derived extracellular vesicles in a model of acute kidney injury monitored by optical imaging. Int J Mol Med 33: 1055-1063, 2014.
46. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL: TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14: R36, 2013.
47. Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L: Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31: 46-53, 2013.
48. Huang W, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57, 2009.