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Open Access 01-12-2022 | Acute Kidney Injury | Research

Extracellular vesicles for ischemia/reperfusion injury-induced acute kidney injury: a systematic review and meta-analysis of data from animal models

Authors: Xia-Qing Li, Jin-Feng Liu, Han Liu, Yu Meng

Published in: Systematic Reviews | Issue 1/2022

Abstract

Background

Acute kidney injury (AKI) induced by ischemia/reperfusion injury significantly contribute to the burden of end-stage renal disease. Extracellular vesicles (EVs), especially for stem/progenitor cell-derived EVs (stem/progenitor cell-EVs), have emerged as a promising therapy for ischemia/reperfusion injury-induced AKI. However, their regulatory effects remain poorly understood, and their therapeutic efficiency in clinical trials is controversial. Here, we performed this systematic review and meta-analysis to assess the stem/progenitor cell-EV efficacy in treating ischemia/reperfusion injury-induced AKI in preclinical rodent models.

Methods

A literature search was performed in PubMed, Embase, Scopus, and Web of Science to identify controlled studies about the therapeutic efficiency of stem/progenitor cell-EVs on ischemia/reperfusion injury-induced AKI rodent models. The level of SCr, an indicator of renal function, was regarded as the primary outcome. Meta-regression analysis was used to reveal the influential factors of EV therapy. Sensitivity analysis, cumulative meta-analysis, and assessment of publication bias were also performed in our systematic review and meta-analysis. A standardized mean difference (SMD) was used as the common effect size between stem/progenitor cell-EV-treated and control groups, with values of 0.2, 0.5, 0.8, and 1.0 defined as small, medium, large, and very large effect sizes, respectively.

Results

A total of 30 studies with 985 ischemia/reperfusion injury-induced AKI rodent models were included. The pooled results showed that EV injection could lead to a remarkable sCr reduction compared with the control group (SMD, − 3.47; 95%CI, − 4.15 to − 2.80; P < 0.001). Meanwhile, the EV treatment group had lower levels of BUN (SMD, − 3.60; 95%CI, − 4.25 to − 2.94; P < 0.001), indexes for tubular and endothelial injury, renal fibrosis (fibrosis score and α-SMA), renal inflammation (TNF-α, IL-1β, iNOS, and CD68 + macrophages), but higher levels of indexes for tubular proliferation, angiogenesis-related VEGF, and reactive oxygen species. However, our meta-regression analysis did not identify significant associations between sCr level and cell origins of EVs, injection doses, delivery routes, and therapy and outcome measurement time (all P values > 0.05). Significant publication bias was observed (Egger’s test, P < 0.001).

Conclusion

Stem/progenitor cell-EVs are effective in improving renal function in rodent ischemia/reperfusion injury-induced AKI model. These vesicles may help (i) reduce cell apoptosis and stimulate cell proliferation, (ii) ameliorate inflammatory injury and renal fibrosis, (iii) promote angiogenesis, and (iv) inhibit oxidative stress. However, the current systematic review and meta-analysis did not identify significant influential factors associated with treatment effects. More preclinical studies and thoughtfully designed animal studies are needed in the future.

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Moreth K, Frey H, Hubo M, Zeng-Brouwers J, Nastase MV, Hsieh LT, Haceni R, Pfeilschifter J, Iozzo RV, Schaefer L. Biglycan-triggered TLR-2- and TLR-4-signaling exacerbates the pathophysiology of ischemic acute kidney injury. Matrix Biol. 2014;35:143–51.PubMedPubMedCentralCrossRef

Perico N, Cattaneo D, Sayegh MH, Remuzzi G. Delayed graft function in kidney transplantation. Lancet (London, England). 2004;364(9447):1814–27.CrossRef

Wang C, Zhu G, He W, Yin H, Lin F, Gou X, Li X. BMSCs protect against renal ischemia-reperfusion injury by secreting exosomes loaded with miR-199a-5p that target BIP to inhibit endoplasmic reticulum stress at the very early reperfusion stages. FASEB J. 2019;33(4):5440–56.PubMedCrossRef

Martin-Sole O, Rodo J, Garcia-Aparicio L, Blanch J, Cusi V, Albert A. Effects of platelet-rich plasma (PRP) on a model of renal ischemia-reperfusion in rats. PLoS ONE. 2016;11(8): e0160703.PubMedPubMedCentralCrossRef

Ishani A, Xue JL, Himmelfarb J, Eggers PW, Kimmel PL, Molitoris BA, Collins AJ. Acute kidney injury increases risk of ESRD among elderly. J Am Soc Nephrol. 2009;20(1):223–8.PubMedPubMedCentralCrossRef

Waikar SS, Liu KD, Chertow GM. Diagnosis, epidemiology and outcomes of acute kidney injury. Clin J Am Soc Nephrol. 2008;3(3):844–61.PubMedCrossRef

Fan H, Yang HC, You L, Wang YY, He WJ, Hao CM. The histone deacetylase, SIRT1, contributes to the resistance of young mice to ischemia/reperfusion-induced acute kidney injury. Kidney Int. 2013;83(3):404–13.PubMedCrossRef

Cantaluppi V, Biancone L, Quercia A, Deregibus MC, Segoloni G, Camussi G. Rationale of mesenchymal stem cell therapy in kidney injury. Am J Kidney Dis. 2013;61(2):300–9.PubMedCrossRef

Fazekas B, Griffin MD. Mesenchymal stromal cell-based therapies for acute kidney injury: progress in the last decade. Kidney Int. 2020;97(6):1130–40.PubMedCrossRef

10.

Chen YT, Sun CK, Lin YC, Chang LT, Chen YL, Tsai TH, Chung SY, Chua S, Kao YH, Yen CH, 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.PubMedPubMedCentralCrossRef

11.

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(3):201–8.CrossRef

12.

Staal FJ, Baum C, Cowan C, Dzierzak E, Hacein-Bey-Abina S, Karlsson S, Lapidot T, Lemischka I, Mendez-Ferrer S, Mikkers H, et al. Stem cell self-renewal: lessons from bone marrow, gut and iPS toward clinical applications. Leukemia. 2011;25(7):1095–102.PubMedCrossRef

13.

L PK, Kandoi S, Misra R, S V, K R, Verma RS. The mesenchymal stem cell secretome: a new paradigm towards cell-free therapeutic mode in regenerative medicine. Cytokine Growth Factor Rev. 2019;46:1–9.

14.

Meng Y, Eirin A, Zhu XY, Tang H, Chanana P, Lerman A, van Wijnen AJ, Lerman LO. Obesity-induced mitochondrial dysfunction in porcine adipose tissue-derived mesenchymal stem cells. J Cell Physiol. 2018;233(8):5926–36.PubMedPubMedCentralCrossRef

15.

Bonventre JV. Microvesicles from mesenchymal stromal cells protect against acute kidney injury. J Am Soc Nephrol. 2009;20(5):927–8.PubMedCrossRef

16.

Bruno S, Grange C, Deregibus MC, Calogero RA, Saviozzi S, Collino F, Morando L, Busca A, Falda M, Bussolati B, et al. Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol. 2009;20(5):1053–67.PubMedPubMedCentralCrossRef

17.

Song L, Tang S, Han X, Jiang Z, Dong L, Liu C, Liang X, Dong J, Qiu C, Wang Y, et al. KIBRA controls exosome secretion via inhibiting the proteasomal degradation of Rab27a. Nat Commun. 2019;10(1):1639.PubMedPubMedCentralCrossRef

18.

van Balkom BW, Pisitkun T, Verhaar MC, Knepper MA. Exosomes and the kidney: prospects for diagnosis and therapy of renal diseases. Kidney Int. 2011;80(11):1138–45.PubMedPubMedCentralCrossRef

19.

Mathieu M, Martin-Jaular L, Lavieu G, Thery C. Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication. Nat Cell Biol. 2019;21(1):9–17.PubMedCrossRef

20.

Tkach M, Thery C. Communication by extracellular vesicles: where we are and where we need to go. Cell. 2016;164(6):1226–32.PubMedCrossRef

21.

Eirin A, Zhu XY, Puranik AS, Tang H, McGurren KA, van Wijnen AJ, Lerman A, Lerman LO. Mesenchymal stem cell-derived extracellular vesicles attenuate kidney inflammation. Kidney Int. 2017;92(1):114–24.PubMedPubMedCentralCrossRef

22.

Eirin A, Zhu XY, Krier JD, Tang H, Jordan KL, Grande JP, Lerman A, Textor SC, Lerman LO. 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.PubMedCrossRef

23.

Rani S, Ryan AE, Griffin MD, Ritter T. Mesenchymal stem cell-derived extracellular vesicles: toward cell-free therapeutic applications. Mol Ther. 2015;23(5):812–23.PubMedPubMedCentralCrossRef

24.

Lv LL, Feng Y, Tang TT, Liu BC. New insight into the role of extracellular vesicles in kidney disease. J Cell Mol Med. 2019;23(2):731–9.PubMedCrossRef

25.

Wu XQ, Tian XY, Wang ZW, Wu X, Wang JP, Yan TZ. miR-191 secreted by platelet-derived microvesicles induced apoptosis of renal tubular epithelial cells and participated in renal ischemia-reperfusion injury via inhibiting CBS. Cell Cycle. 2019;18(2):119–29.PubMedPubMedCentralCrossRef

26.

Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339: b2535.CrossRef

27.

Alzahrani FA. Melatonin improves therapeutic potential of mesenchymal stem cells-derived exosomes against renal ischemia-reperfusion injury in rats. Am J Transl Res. 2019;11(5):2887–907.PubMedPubMedCentral

28.

Burger D, Vinas JL, Akbari S, Dehak H, Knoll W, Gutsol A, Carter A, Touyz RM, Allan DS, Burns KD. Human endothelial colony-forming cells protect against acute kidney injury: role of exosomes. Am J Pathol. 2015;185(8):2309–23.PubMedCrossRef

29.

Cantaluppi V, Gatti S, Medica D, Figliolini F, Bruno S, Deregibus MC, Sordi A, Biancone L, Tetta C, Camussi G. Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney Int. 2012;82(4):412–27.PubMedCrossRef

30.

Cao H, Cheng Y, Gao H, Zhuang J, Zhang W, Bian Q, Wang F, Du Y, Li Z, Kong D, et al. In vivo tracking of mesenchymal stem cell-derived extracellular vesicles improving mitochondrial function in renal ischemia-reperfusion injury. ACS Nano. 2020;14(4):4014–26.PubMedCrossRef

31.

Choi HY, Moon SJ, Ratliff BB, Ahn SH, Jung A, Lee M, Lee S, Lim BJ, Kim BS, Plotkin MD, et al. Microparticles from kidney-derived mesenchymal stem cells act as carriers of proangiogenic signals and contribute to recovery from acute kidney injury. PLoS ONE. 2014;9(2): e87853.PubMedPubMedCentralCrossRef

32.

Collino F, Lopes JA, Correa S, Abdelhay E, Takiya CM, Wendt CHC, de Miranda KR, Vieyra A, Lindoso RS. Adipose-derived mesenchymal stromal cells under hypoxia: changes in extracellular vesicles secretion and improvement of renal recovery after ischemic injury. Cell Physiol Biochem. 2019;52(6):1463–83.PubMed

33.

Collino F, Lopes JA, Tapparo M, Tortelote GG, Kasai-Brunswick TH, Lopes GMC, et al. Extracellular vesicles derived from induced pluripotent stem cells promote renoprotection in acute kidney injury model. Cells. 2020;9(2):453.

34.

Gatti S, Bruno S, Deregibus MC, Sordi A, Cantaluppi V, Tetta C, Camussi G. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrol Dial Transplant. 2011;26(5):1474–83.PubMedCrossRef

35.

Gu D, Zou X, Ju G, Zhang G, Bao E, Zhu Y. Mesenchymal stromal cells derived extracellular vesicles ameliorate acute renal ischemia reperfusion injury by inhibition of mitochondrial fission through miR-30. Stem Cells Int. 2016;2016:2093940.PubMedPubMedCentralCrossRef

36.

Ju GQ, Cheng J, Zhong L, Wu S, Zou XY, Zhang GY, Gu D, Miao S, Zhu YJ, Sun J, et al. Microvesicles derived from human umbilical cord mesenchymal stem cells facilitate tubular epithelial cell dedifferentiation and growth via hepatocyte growth factor induction. PLoS ONE. 2015;10(3): e0121534.PubMedPubMedCentralCrossRef

37.

Kilpinen L, Impola U, Sankkila L, Ritamo I, Aatonen M, Kilpinen S, et al. Extracellular membrane vesicles from umbilical cord blood-derived MSC protect against ischemic acute kidney injury, a feature that is lost after inflammatory conditioning. J Extracell Vesicles. 2013;2:21927.

38.

Li L, Wang R, Jia Y, Rong R, Xu M, Zhu T. Exosomes derived from mesenchymal stem cells ameliorate renal ischemic-reperfusion injury through inhibiting inflammation and cell apoptosis. Front Med (Lausanne). 2019;6:269.CrossRef

39.

Lin KC, Yip HK, Shao PL, Wu SC, Chen KH, Chen YT, Yang CC, Sun CK, Kao GS, Chen SY, et al. Combination of adipose-derived mesenchymal stem cells (ADMSC) and ADMSC-derived exosomes for protecting kidney from acute ischemia-reperfusion injury. Int J Cardiol. 2016;216:173–85.PubMedCrossRef

40.

Liu Y, Cui J, Wang H, Hezam K, Zhao X, Huang H, Chen S, Han Z, Han ZC, Guo Z, et al. Enhanced therapeutic effects of MSC-derived extracellular vesicles with an injectable collagen matrix for experimental acute kidney injury treatment. Stem Cell Res Ther. 2020;11(1):161.PubMedPubMedCentralCrossRef

41.

Ranghino A, Bruno S, Bussolati B, Moggio A, Dimuccio V, Tapparo M, Biancone L, Gontero P, Frea B, Camussi G. 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.PubMedPubMedCentralCrossRef

42.

Shen B, Liu J, Zhang F, Wang Y, Qin Y, Zhou Z, Qiu J, Fan Y. CCR2 positive exosome released by mesenchymal stem cells suppresses macrophage functions and alleviates ischemia/reperfusion-induced renal injury. Stem Cells Int. 2016;2016:1240301.PubMedPubMedCentralCrossRef

43.

Vinas JL, Burger D, Zimpelmann J, Haneef R, Knoll W, Campbell P, Gutsol A, Carter A, Allan DS, Burns KD. Transfer of microRNA-486-5p from human endothelial colony forming cell-derived exosomes reduces ischemic kidney injury. Kidney Int. 2016;90(6):1238–50.PubMedCrossRef

44.

Vinas JL, Spence M, Gutsol A, Knoll W, Burger D, Zimpelmann J, Allan DS, Burns KD. Receptor-ligand interaction mediates targeting of endothelial colony forming cell-derived exosomes to the kidney after ischemic injury. Sci Rep. 2018;8(1):16320.PubMedPubMedCentralCrossRef

45.

Wang R, Lin M, Li L, Li L, Qi G, Rong R, Xu M, Zhu T. Bone marrow mesenchymal stem cell-derived exosome protects kidney against ischemia reperfusion injury in rats. Zhonghua Yi Xue Za Zhi. 2014;94(42):3298–303.PubMed

46.

Wu X, Yan T, Wang Z, Wu X, Cao G, Zhang C, Tian X, Wang J. Micro-vesicles derived from human Wharton’s Jelly mesenchymal stromal cells mitigate renal ischemia-reperfusion injury in rats after cardiac death renal transplantation. J Cell Biochem. 2018;119(2):1879–88.PubMedCrossRef

47.

Yuan X, Li D, Chen X, Han C, Xu L, Huang T, Dong Z, Zhang M. Extracellular vesicles from human-induced pluripotent stem cell-derived mesenchymal stromal cells (hiPSC-MSCs) protect against renal ischemia/reperfusion injury via delivering specificity protein (SP1) and transcriptional activating of sphingosine kinase 1 and inhibiting necroptosis. Cell Death Dis. 2017;8(12):3200.PubMedPubMedCentralCrossRef

48.

Yu L, Liu S, Wang C, Zhang C, Wen Y, Zhang K, Chen S, Huang H, Liu Y, Wu L, et al. Embryonic stem cell-derived extracellular vesicles promote the recovery of kidney injury. Stem Cell Res Ther. 2021;12(1):379.PubMedPubMedCentralCrossRef

49.

Zhang G, Zou X, Miao S, Chen J, Du T, Zhong L, Ju G, Liu G, Zhu Y. The anti-oxidative role of micro-vesicles derived from human Wharton-Jelly mesenchymal stromal cells through NOX2/gp91(phox) suppression in alleviating renal ischemia-reperfusion injury in rats. PLoS ONE. 2014;9(3): e92129.PubMedPubMedCentralCrossRef

50.

Zhang G, Zou X, Huang Y, Wang F, Miao S, Liu G, Chen M, Zhu Y. Mesenchymal stromal cell-derived extracellular vesicles protect against acute kidney injury through anti-oxidation by enhancing Nrf2/ARE activation in rats. Kidney Blood Press Res. 2016;41(2):119–28.PubMedCrossRef

51.

Zhang ZY, Hou YP, Zou XY, Xing XY, Ju GQ, Zhong L, Sun J. Oct-4 enhanced the therapeutic effects of mesenchymal stem cell-derived extracellular vesicles in acute kidney injury. Kidney Blood Press Res. 2020;45(1):95–108.PubMedCrossRef

52.

Zou X, Zhang G, Cheng Z, Yin D, Du T, Ju G, Miao S, Liu G, Lu M, Zhu Y. Microvesicles derived from human Wharton’s Jelly mesenchymal stromal cells ameliorate renal ischemia-reperfusion injury in rats by suppressing CX3CL1. Stem Cell Res Ther. 2014;5(2):40.PubMedPubMedCentralCrossRef

53.

Zou X, Gu D, Xing X, Cheng Z, Gong D, Zhang G, Zhu Y. Human mesenchymal stromal cell-derived extracellular vesicles alleviate renal ischemic reperfusion injury and enhance angiogenesis in rats. Am J Transl Res. 2016;8(10):4289–99.PubMedPubMedCentral

54.

Zou X, Gu D, Zhang G, Zhong L, Cheng Z, Liu G, Zhu Y. NK cell regulatory property is involved in the protective role of MSC-derived extracellular vesicles in renal ischemic reperfusion injury. Hum Gene Ther. 2016;27(11):926–35.PubMedCrossRef

55.

Zhu G, Pei L, Lin F, Yin H, Li X, He W, Liu N, Gou X. Exosomes from human-bone-marrow-derived mesenchymal stem cells protect against renal ischemia/reperfusion injury via transferring miR-199a-3p. J Cell Physiol. 2019;234(12):23736–49.PubMedCrossRef

56.

Macleod MR, O’Collins T, Howells DW, Donnan GA. Pooling of animal experimental data reveals influence of study design and publication bias. Stroke. 2004;35(5):1203–8.PubMedCrossRef

57.

Cohen J. Statistical power analysis for the behavioral sciences. 2nd ed. NJ: Lawrence Erlbaum Associates; 1988. p. 567.

58.

Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–60.PubMedPubMedCentralCrossRef

59.

Eirin A, Zhu XY, Puranik AS, Woollard JR, Tang H, Dasari S, Lerman A, van Wijnen AJ, Lerman LO. Comparative proteomic analysis of extracellular vesicles isolated from porcine adipose tissue-derived mesenchymal stem/stromal cells. Sci Rep. 2016;6:36120.PubMedPubMedCentralCrossRef

60.

Zhang G, Wang D, Miao S, Zou X, Liu G, Zhu Y. Extracellular vesicles derived from mesenchymal stromal cells may possess increased therapeutic potential for acute kidney injury compared with conditioned medium in rodent models: A meta-analysis. Exp Ther Med. 2016;11(4):1519–25.PubMedPubMedCentralCrossRef

61.

Liu C, Wang J, Hu J, Fu B, Mao Z, Zhang H, Cai G, Chen X, Sun X. Extracellular vesicles for acute kidney injury in preclinical rodent models: a meta-analysis. Stem Cell Res Ther. 2020;11(1):11.PubMedPubMedCentralCrossRef

62.

Polichnowski AJ, Griffin KA, Licea-Vargas H, Lan R, Picken MM, Long J, Williamson GA, Rosenberger C, Mathia S, Venkatachalam MA, et al. Pathophysiology of unilateral ischemia-reperfusion injury: importance of renal counterbalance and implications for the AKI-CKD transition. Am J Physiol Renal Physiol. 2020;318(5):F1086–99.PubMedPubMedCentralCrossRef

63.

Zager RA, Johnson AC, Lund S. Uremia impacts renal inflammatory cytokine gene expression in the setting of experimental acute kidney injury. Am J Physiol Renal Physiol. 2009;297(4):F961-970.PubMedPubMedCentralCrossRef

64.

Xu Y, Wan J, Jiang D, Wu X. BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition in human renal proximal tubular epithelial cells. J Nephrol. 2009;22(3):403–10.PubMed

65.

Baek G, Choi H, Kim Y, Lee HC, Choi C. Mesenchymal stem cell-derived extracellular vesicles as therapeutics and as a drug delivery platform. Stem Cells Transl Med. 2019;8(9):880–6.PubMedPubMedCentralCrossRef

66.

Du T, Zhou J, Chen WX, Zhang XL, Ji TY, Liu J, Rong L, Wang LD, Zhou RJ, Ding DG. Microvesicles derived from human umbilical cord mesenchymal stem cells ameliorate renal ischemia-reperfusion injury via delivery of miR-21. Cell Cycle. 2020;19(11):1285–97.PubMedPubMedCentralCrossRef

67.

Li Z, Deng X, Kang Z, Wang Y, Xia T, Ding N, Yin Y. Elevation of miR-21, through targeting MKK3, may be involved in ischemia pretreatment protection from ischemia-reperfusion induced kidney injury. J Nephrol. 2016;29(1):27–36.PubMedCrossRef

68.

Jeppesen DK, Fenix AM, Franklin JL, Higginbotham JN, Zhang Q, Zimmerman LJ, Liebler DC, Ping J, Liu Q, Evans R et al. Reassessment of exosome composition. Cell. 2019; 177(2):428–445 e418.

69.

Roberts TC, Blomberg KE, McClorey G, El Andaloussi S, Godfrey C, Betts C, Coursindel T, Gait MJ, Smith CI, Wood MJ. Expression analysis in multiple muscle groups and serum reveals complexity in the microRNA transcriptome of the mdx mouse with implications for therapy. Mol Ther Nucleic Acids. 2012;1: e39.PubMedPubMedCentralCrossRef

70.

Vagner T, Spinelli C, Minciacchi VR, Balaj L, Zandian M, Conley A, Zijlstra A, Freeman MR, Demichelis F, De S, et al. Large extracellular vesicles carry most of the tumour DNA circulating in prostate cancer patient plasma. J Extracell Vesicles. 2018;7(1):1505403.PubMedPubMedCentralCrossRef

71.

Kordelas L, Rebmann V, Ludwig AK, Radtke S, Ruesing J, Doeppner TR, Epple M, Horn PA, Beelen DW, Giebel B. MSC-derived exosomes: a novel tool to treat therapy-refractory graft-versus-host disease. Leukemia. 2014;28(4):970–3.PubMedCrossRef

72.

Nassar W, El-Ansary M, Sabry D, Mostafa MA, Fayad T, Kotb E, Temraz M, Saad AN, Essa W, Adel H. Umbilical cord mesenchymal stem cells derived extracellular vesicles can safely ameliorate the progression of chronic kidney diseases. Biomater Res. 2016;20:21.PubMedPubMedCentralCrossRef

73.

Harrell CR, Fellabaum C, Jovicic N, Djonov V, Arsenijevic N, Volarevic V. Molecular mechanisms responsible for therapeutic potential of mesenchymal stem cell-derived secretome. Cells. 2019;8(5):467.

74.

Eirin A, Riester SM, Zhu XY, Tang H, Evans JM, O’Brien D, van Wijnen AJ, Lerman LO. MicroRNA and mRNA cargo of extracellular vesicles from porcine adipose tissue-derived mesenchymal stem cells. Gene. 2014;551(1):55–64.PubMedPubMedCentralCrossRef

75.

Eirin A, Saad A, Woollard JR, Juncos LA, Calhoun DA, Tang H, Lerman A, Textor SC, Lerman LO. Glomerular hyperfiltration in obese african american hypertensive patients is associated with elevated urinary mitochondrial-DNA copy number. Am J Hypertens. 2017;30(11):1112–9.PubMedPubMedCentralCrossRef

Title: Extracellular vesicles for ischemia/reperfusion injury-induced acute kidney injury: a systematic review and meta-analysis of data from animal models
Authors: Xia-Qing Li
Jin-Feng Liu
Han Liu
Yu Meng
Publication date: 01-12-2022
Publisher: BioMed Central
Keywords: Acute Kidney Injury
Acute Kidney Injury
Published in: Systematic Reviews / Issue 1/2022
Electronic ISSN: 2046-4053
DOI: https://doi.org/10.1186/s13643-022-02003-5

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Extracellular vesicles for ischemia/reperfusion injury-induced acute kidney injury: a systematic review and meta-analysis of data from animal models

Abstract

Background

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

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