Exosome-mediated targeted delivery of miR-210 for angiogenic therapy after cerebral ischemia in mice

Journal of Nanobiotechnology - Tập 17 Số 1 - 2019
Huixin Zhang1, Jin Wu2, Jiahuan Wu1, Qi Fan3, Jingchao Zhou3, Junwen Wu3, Sichen Liu3, Jie Zang3, Jinhai Ye4, Ming Xiao5, Tian Tian1, Jun Gao1
1The Department of Neurobiology, Key Laboratory of Human Functional Genomics of Jiangsu, Nanjing Medical University, Nanjing, 211166, Jiangsu, China
2The Department of Neurology, The Second Affiliated Hospital of Nanjing Medical University, Nanjing, 210011, Jiangsu, China
3The School of Basic Medical Science, Nanjing Medical University, Nanjing, 211166, Jiangsu, China
4The Department of Oral and Maxillofacial Surgery, The Affiliated Stomatology Hospital of Nanjing Medical University, Nanjing Medical University, Nanjing, 210029, China
5Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, 211166, Jiangsu, China

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Neuhaus AA, Couch Y, Hadley G, Buchan AM. Neuroprotection in stroke: the importance of collaboration and reproducibility. Brain. 2017;140:2079–92.

Bai YY, Gao X, Wang YC, Peng XG, Chang D, Zheng S, Li C, Ju S. Image-guided pro-angiogenic therapy in diabetic stroke mouse models using a multi-modal nanoprobe. Theranostics. 2014;4:787–97.

Abumiya T, Fitridge R, Mazur C, Copeland BR, Koziol JA, Tschopp JF, Pierschbacher MD, del Zoppo GJ. Integrin alpha(IIb)beta(3) inhibitor preserves microvascular patency in experimental acute focal cerebral ischemia. Stroke. 2000;31:1402–9 (discussion 09-10).

Di Y, Lei Y, Yu F, Changfeng F, Song W, Xuming M. MicroRNAs expression and function in cerebral ischemia reperfusion injury. J Mol Neurosci. 2014;53:242–50.

Ambros V. The functions of animal microRNAs. Nature. 2004;431:350–5.

Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–97.

He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet. 2004;5:522–31.

Fasanaro P, Greco S, Lorenzi M, Pescatori M, Brioschi M, Kulshreshtha R, Banfi C, Stubbs A, Calin GA, Ivan M, et al. An integrated approach for experimental target identification of hypoxia-induced miR-210. J Biol Chem. 2009;284:35134–43.

Meng ZY, Kang HL, Duan W, Zheng J, Li QN, Zhou ZJ. MicroRNA-210 promotes accumulation of neural precursor cells around ischemic foci after cerebral ischemia by regulating the SOCS1-STAT3-VEGF-C pathway. J Am Heart Assoc. 2018;7:e005052.

Lou YL, Guo F, Liu F, Gao FL, Zhang PQ, Niu X, Guo SC, Yin JH, Wang Y, Deng ZF. miR-210 activates notch signaling pathway in angiogenesis induced by cerebral ischemia. Mol Cell Biochem. 2012;370:45–51.

Zeng L, Liu J, Wang Y, Wang L, Weng S, Tang Y, Zheng C, Cheng Q, Chen S, Yang GY. MicroRNA-210 as a novel blood biomarker in acute cerebral ischemia. Front Biosci (Elite Ed). 2011;3:1265–72.

Hu S, Huang M, Li Z, Jia F, Ghosh Z, Lijkwan MA, Fasanaro P, Sun N, Wang X, Martelli F, et al. MicroRNA-210 as a novel therapy for treatment of ischemic heart disease. Circulation. 2010;122:S124–31.

Liu F, Lou YL, Wu J, Ruan QF, Xie A, Guo F, Cui SP, Deng ZF, Wang Y. Upregulation of MicroRNA-210 regulates renal angiogenesis mediated by activation of VEGF signaling pathway under ischemia/perfusion injury in vivo and in vitro. Kidney Blood Pressure Res. 2012;35:182–91.

Zeng LL, He XS, Liu JR, Zheng CB, Wang YT, Yang GY. Lentivirus-mediated overexpression of MicroRNA-210 improves long-term outcomes after focal cerebral ischemia in mice. CNS Neurosci Ther. 2016;22:961–9.

Zeng L, He X, Wang Y, Tang Y, Zheng C, Cai H, Liu J, Wang Y, Fu Y, Yang GY. MicroRNA-210 overexpression induces angiogenesis and neurogenesis in the normal adult mouse brain. Gene Ther. 2014;21:37–43.

Cook DJ, Teves L, Tymianski M. Treatment of stroke with a PSD-95 inhibitor in the gyrencephalic primate brain. Nature. 2012;483:213–7.

Thompson BJ, Ronaldson PT. Drug delivery to the ischemic brain. Adv Pharmacol. 2014;71:165–202.

Rufino-Ramos D, Albuquerque PR, Carmona V, Perfeito R, Nobre RJ, Pereira de Almeida L. Extracellular vesicles: novel promising delivery systems for therapy of brain diseases. J Control Release. 2017;262:247–58.

Wang W, Luo J, Wang S. Recent progress in isolation and detection of extracellular vesicles for cancer diagnostics. Adv Healthcare Mater. 2018;7:e1800484.

Ahmed M, Carrascosa LG, Wuethrich A, Mainwaring P, Trau M. An exosomal- and interfacial-biosensing based strategy for remote monitoring of aberrantly phosphorylated proteins in lung cancer cells. Biomater Sci. 2018;6:2336–41.

Bunggulawa EJ, Wang W, Yin T, Wang N, Durkan C, Wang Y, Wang G. Recent advancements in the use of exosomes as drug delivery systems. J Nanobiotechnol. 2018;16:81.

Alyautdin R, Khalin I, Nafeeza MI, Haron MH, Kuznetsov D. Nanoscale drug delivery systems and the blood-brain barrier. Int J Nanomed. 2014;9:795–811.

Quek C, Hill AF. The role of extracellular vesicles in neurodegenerative diseases. Biochem Biophys Res Commun. 2017;483:1178–86.

Yong X, Yang X, Emory SR, Wang J, Dai J, Yu X, Mei L, Xie J, Ruan G. A potent, minimally invasive and simple strategy of enhancing intracellular targeted delivery of Tat peptide-conjugated quantum dots: organic solvent-based permeation enhancer. Biomater Sci. 2018;6:3085–95.

Tian T, Zhang HX, He CP, Fan S, Zhu YL, Qi C, Huang NP, Xiao ZD, Lu ZH, Tannous BA, Gao J. Surface functionalized exosomes as targeted drug delivery vehicles for cerebral ischemia therapy. Biomaterials. 2018;150:137–49.

Alvarez-Erviti L, Seow YQ, Yin HF, Betts C, Lakhal S, Wood MJA. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol. 2011;29:341-U179.

Haney MJ, Klyachko NL, Zhaoa YL, Gupta R, Plotnikova EG, He ZJ, Patel T, Piroyan A, Sokolsky M, Kabanov AV, Batrakova EV. Exosomes as drug delivery vehicles for Parkinson’s disease therapy. J Control Release. 2015;207:18–30.

O’Loughlin AJ, Mager I, de Jong OG, Varela MA, Schiffelers RM, El Andaloussi S, Wood MJA, Vader P. Functional delivery of lipid-conjugated siRNA by extracellular vesicles. Mol Ther. 2017;25:1580–7.

Zhu DY, Deng Q, Yao HH, Wang DC, Deng Y, Liu GQ. Inducible nitric oxide synthase expression in the ischemic core and penumbra after transient focal cerebral ischemia in mice. Life Sci. 2002;71:1985–96.

Zaccagnini G, Maimone B, Fuschi P, Maselli D, Spinetti G, Gaetano C, Martelli F. Overexpression of miR-210 and its significance in ischemic tissue damage. Sci Rep. 2017;7:9563.

Zaccagnini G, Maimone B, Di Stefano V, Fasanaro P, Greco S, Perfetti A, Capogrossi MC, Gaetano C, Martelli F. Hypoxia-induced miR-210 modulates tissue response to acute peripheral ischemia. Antioxid Redox Signal. 2014;21:1177–88.

Didiot MC, Hall LM, Coles AH, Haraszti RA, Godinho BM, Chase K, Sapp E, Ly S, Alterman JF, Hassler MR, et al. Exosome-mediated delivery of hydrophobically modified siRNA for huntingtin mRNA silencing. Mol Ther. 2016;24:1836–47.

Lai CP, Kim EY, Badr CE, Weissleder R, Mempel TR, Tannous BA, Breakefield XO. Visualization and tracking of tumour extracellular vesicle delivery and RNA translation using multiplexed reporters. Nat Commun. 2015;6:7029.

Tian YH, Li SP, Song J, Ji TJ, Zhu MT, Anderson GJ, Wei JY, Nie GJ. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials. 2014;35:2383–90.

Ley K, Rivera-Nieves J, Sandborn WJ, Shattil S. Integrin-based therapeutics: biological basis, clinical use and new drugs. Nat Rev Drug Discov. 2016;15:173–83.

Li L, Welser JV, Milner R. Absence of the alpha v beta 3 integrin dictates the time-course of angiogenesis in the hypoxic central nervous system: accelerated endothelial proliferation correlates with compensatory increases in alpha 5 beta 1 integrin expression. J Cereb Blood Flow Metab. 2010;30:1031–43.

Rosenstein JM, Mani N, Silverman WF, Krum JM. Patterns of brain angiogenesis after vascular endothelial growth factor administration in vitro and in vivo. Proc Natl Acad Sci USA. 1998;95:7086–91.

Agrawal R, Pandey P, Jha P, Dwivedi V, Sarkar C, Kulshreshtha R. Hypoxic signature of microRNAs in glioblastoma: insights from small RNA deep sequencing. BMC Genomics. 2014;15:686.

Qiu J, Zhou XY, Zhou XG, Cheng R, Liu HY, Li Y. Neuroprotective effects of microRNA-210 on hypoxic-ischemic encephalopathy. Biomed Res Int. 2013;2013:350419.

Liu LL, Li D, He YL, Zhou YZ, Gong SH, Wu LY, Zhao YQ, Huang X, Zhao T, Xu L, et al. miR-210 protects renal cell against hypoxia-induced apoptosis by targeting HIF-1 alpha. Mol Med. 2017;23:258.

Kim JH, Park SG, Song SY, Kim JK, Sung JH. Reactive oxygen species-responsive miR-210 regulates proliferation and migration of adipose-derived stem cells via PTPN2. Cell Death Dis. 2013;4:e588.

Ruan L, Wang B, ZhuGe Q, Jin K. Coupling of neurogenesis and angiogenesis after ischemic stroke. Brain Res. 2015;1623:166–73.

Kwon EJ, Skalak M, Lo BuR, Bhatia SN. Neuron-targeted nanoparticle for siRNA delivery to traumatic brain injuries. ACS Nano. 2016;10:7926–33.

Sun L, Xu R, Sun X, Duan Y, Han Y, Zhao Y, Qian H, Zhu W, Xu W. Safety evaluation of exosomes derived from human umbilical cord mesenchymal stromal cell. Cytotherapy. 2016;18:413–22.

Zhang ZG, Chopp M. Exosomes in stroke pathogenesis and therapy. J Clin Invest. 2016;126:1190–7.

Kooijmans SAA, Stremersch S, Braeckmans K, de Smedt SC, Hendrix A, Wood MJA, Schiffelers RM, Raemdonck K, Vader P. Electroporation-induced siRNA precipitation obscures the efficiency of siRNA loading into extracellular vesicles. J Control Release. 2013;172:229–38.

Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol. 2009;19:43–51.

Todorova D, Simoncini S, Lacroix R, Sabatier F, Dignat-George F. Extracellular vesicles in angiogenesis. Circ Res. 2017;120:1658–73.

Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke. 1989;20:84–91.

Ashwal S, Tone B, Tian HR, Cole DJ, Pearce WJ. Core and penumbral nitric oxide synthase activity during cerebral ischemia and reperfusion. Stroke. 1998;29:1037–46 (discussion 47).

Shimamura N, Matchett G, Tsubokawa T, Ohkuma H, Zhang J. Comparison of silicon-coated nylon suture to plain nylon suture in the rat middle cerebral artery occlusion model. J Neurosci Methods. 2006;156:161–5.

Bederson JB, Pitts LH, Germano SM, Nishimura MC, Davis RL, Bartkowski HM. Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats. Stroke. 1986;17:1304–8.

Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006;3:3–22.