Extracellular vesicle-mimetic nanovesicles transport LncRNA-H19 as competing endogenous RNA for the treatment of diabetic wounds

References

• Abels ER, Breakefield XO. (2016). Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake. Cell Mol Neurobiol 36:301–12.
   PubMed Web of Science ®Google Scholar
• Amin MA, Rabquer BJ, Mansfield PJ, et al. (2010). Interleukin 18 induces angiogenesis in vitro and in vivo via Src and Jnk kinases. Ann Rheum Dis 69:2204–12.
   PubMed Web of Science ®Google Scholar
• Andreu Z, Yanez-Mo M. (2014). Tetraspanins in extracellular vesicle formation and function. Front Immunol 5:442.
   PubMed Web of Science ®Google Scholar
• Bergan JJ, Schmid-Schonbein GW, Smith PD, et al. (2006). Chronic venous disease. N Engl J Med 355:488–98.
   PubMed Web of Science ®Google Scholar
• Blandino A, Macias M, Cantero D. (1999). Formation of calcium alginate gel capsules: influence of sodium alginate and CaCl2 concentration on gelation kinetics. J Biosci Bioeng 88:686–9.
   PubMed Web of Science ®Google Scholar
• Boelens MC, Wu TJ, Nabet BY, et al. (2014). Exosome transfer from stromal to breast cancer cells regulates therapy resistance pathways. Cell 159:499–513.
   PubMed Web of Science ®Google Scholar
• Burgess DJ. (2014). Signalling: vesicle vehicles of genetic information. Nat Rev Genet 15:514.
   Web of Science ®Google Scholar
• Carboni JM, Wittman M, Yang Z, et al. (2009). BMS-754807, a small molecule inhibitor of insulin-like growth factor-1R/IR. Mol Cancer Ther 8:3341–9.
   PubMed Web of Science ®Google Scholar
• Cesana M, Cacchiarelli D, Legnini I, et al. (2011). A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147:358–69.
   PubMed Web of Science ®Google Scholar
• Chaudhuri O, Koshy ST, Branco Da Cunha C, et al. (2014). Extracellular matrix stiffness and composition jointly regulate the induction of malignant phenotypes in mammary epithelium. Nat Mater 13:970–8.
   PubMed Web of Science ®Google Scholar
• Ding GL, Wang FF, Shu J, et al. (2012). Transgenerational glucose intolerance with Igf2/H19 epigenetic alterations in mouse islet induced by intrauterine hyperglycemia. Diabetes 61:1133–42.
   PubMed Web of Science ®Google Scholar
• Dunn LL, Simpson PJ, Prosser HC, et al. (2014). A critical role for thioredoxin-interacting protein in diabetes-related impairment of angiogenesis. Diabetes 63:675–87.
   PubMed Web of Science ®Google Scholar
• El-Andaloussi S, Lee Y, Lakhal-Littleton S, et al. (2012). Exosome-mediated delivery of siRNA in vitro and in vivo. Nat Protoc 7:2112–26.
   PubMed Web of Science ®Google Scholar
• Eming SA, Brachvogel B, Odorisio T, Koch M. (2007). Regulation of angiogenesis: wound healing as a model. Prog Histochem Cytochem 42:115–70.
   PubMedGoogle Scholar
• Eming SA, Martin P, Tomic-Canic M. (2014). Wound repair and regeneration: mechanisms, signaling, and translation. Sci Transl Med 6:265sr6.
   PubMed Web of Science ®Google Scholar
• Eubank TD, Roberts R, Galloway M, et al. (2004). GM-CSF induces expression of soluble VEGF receptor-1 from human monocytes and inhibits angiogenesis in mice. Immunity 21:831–42.
   PubMed Web of Science ®Google Scholar
• Flegg JA, Menon SN, Maini PK, Mcelwain DL. (2015). On the mathematical modeling of wound healing angiogenesis in skin as a reaction-transport process. Front Physiol 6:262.
   PubMed Web of Science ®Google Scholar
• Frank DN, Wysocki A, Specht-Glick DD, et al. (2009). Microbial diversity in chronic open wounds. Wound Repair Regen 17:163–72.
   PubMed Web of Science ®Google Scholar
• Frantz S, Vincent KA, Feron O, Kelly RA. (2005). Innate immunity and angiogenesis. Circ Res 96:15–26.
   PubMed Web of Science ®Google Scholar
• Gao Y, Wu F, Zhou J, et al. (2014). The H19/let-7 double-negative feedback loop contributes to glucose metabolism in muscle cells. Nucleic Acids Res 42:13799–811.
   PubMed Web of Science ®Google Scholar
• Ghazal S, Mckinnon B, Zhou J, et al. (2015). H19 lncRNA alters stromal cell growth via IGF signaling in the endometrium of women with endometriosis. EMBO Mol Med 7:996–1003.
   PubMed Web of Science ®Google Scholar
• Grotendorst GR, Martin GR, Pencev D, et al. (1985). Stimulation of granulation tissue formation by platelet-derived growth factor in normal and diabetic rats. J Clin Invest 76:2323–9.
   PubMed Web of Science ®Google Scholar
• Guo P, Yang J, Jia D, et al. (2016). ICAM-1-Targeted, Lcn2 siRNA-encapsulating liposomes are potent anti-angiogenic agents for Triple Negative Breast Cancer. Theranostics 6:1–13.
   PubMed Web of Science ®Google Scholar
• Guo SC, Tao SC, Yin WJ, et al. (2017). Exosomes derived from platelet-rich plasma promote the re-epithelization of chronic cutaneous wounds via activation of YAP in a diabetic rat model. Theranostics 7:81–96.
   PubMed Web of Science ®Google Scholar
• Hwang DW, Choi H, Jang SC, et al. (2015). Noninvasive imaging of radiolabeled exosome-mimetic nanovesicle using (99m)Tc-HMPAO. Sci Rep 5:15636.
   PubMed Web of Science ®Google Scholar
• Icli B, Nabzdyk CS, Lujan-Hernandez J, et al. (2016). Regulation of impaired angiogenesis in diabetic dermal wound healing by microRNA-26a. J Mol Cell Cardiol 91:151–9.
   PubMed Web of Science ®Google Scholar
• Iwakura A, Tabata Y, Tamura N, et al. (2001). Gelatin sheet incorporating basic fibroblast growth factor enhances healing of devascularized sternum in diabetic rats. Circulation 104:I325–9.
   PubMed Web of Science ®Google Scholar
• Jang SC, Kim OY, Yoon CM, et al. (2013). Bioinspired exosome-mimetic nanovesicles for targeted delivery of chemotherapeutics to malignant tumors. ACS Nano 7:7698–710.
   PubMed Web of Science ®Google Scholar
• Jeong HJ, Lee SA, Moon PD, et al. (2006). Alginic acid has anti-anaphylactic effects and inhibits inflammatory cytokine expression via suppression of nuclear factor-kappaB activation. Clin Exp Allergy 36:785–94.
   PubMed Web of Science ®Google Scholar
• Jia P, Cai H, Liu X, et al. (2016). Long non-coding RNA H19 regulates glioma angiogenesis and the biological behavior of glioma-associated endothelial cells by inhibiting microRNA-29a. Cancer Lett 381:359–69.
   PubMed Web of Science ®Google Scholar
• Jo W, Kim J, Yoon J, et al. (2014). Large-scale generation of cell-derived nanovesicles. Nanoscale 6:12056–64.
   PubMed Web of Science ®Google Scholar
• Kao HK, Chen B, Murphy GF, et al. (2011). Peripheral blood fibrocytes: enhancement of wound healing by cell proliferation, re-epithelialization, contraction, and angiogenesis. Ann Surg 254:1066–74.
   PubMed Web of Science ®Google Scholar
• Kolb EA, Gorlick R, Lock R, et al. (2011). Initial testing (stage 1) of the IGF-1 receptor inhibitor BMS-754807 by the pediatric preclinical testing program. Pediatr Blood Cancer 56:595–603.
   PubMed Web of Science ®Google Scholar
• Kourembanas S. (2015). Exosomes: vehicles of intercellular signaling, biomarkers, and vectors of cell therapy. Annu Rev Physiol 77:13–27.
   PubMed Web of Science ®Google Scholar
• Kuo YR, Wang CT, Wang FS, et al. (2009). Extracorporeal shock-wave therapy enhanced wound healing via increasing topical blood perfusion and tissue regeneration in a rat model of STZ-induced diabetes. Wound Repair Regen 17:522–30.
   PubMed Web of Science ®Google Scholar
• Lai HJ, Kuan CH, Wu HC, et al. (2014). Tailored design of electrospun composite nanofibers with staged release of multiple angiogenic growth factors for chronic wound healing. Acta Biomater 10:4156–66.
   PubMed Web of Science ®Google Scholar
• Larger E, Marre M, Corvol P, Gasc JM. (2004). Hyperglycemia-induced defects in angiogenesis in the chicken chorioallantoic membrane model. Diabetes 53:752–61.
   PubMed Web of Science ®Google Scholar
• Lee J, Saw PE, Gujrati V, et al. (2016). Mono-arginine cholesterol-based small lipid nanoparticles as a systemic siRNA delivery platform for effective cancer therapy. Theranostics 6:192–203.
   PubMed Web of Science ®Google Scholar
• Lee KY, Mooney DJ. (2012). Alginate: properties and biomedical applications. Prog Polym Sci 37:106–26.
   PubMed Web of Science ®Google Scholar
• Liu D, Yang F, Xiong F, Gu N. (2016). The smart drug delivery system and its clinical potential. Theranostics 6:1306–23.
   PubMed Web of Science ®Google Scholar
• Liu ZJ, Velazquez OC. (2008). Hyperoxia, endothelial progenitor cell mobilization, and diabetic wound healing. Antioxid Redox Signal 10:1869–82.
   PubMed Web of Science ®Google Scholar
• Lu Y, Liu YH, Fu W, et al. (2016). Long noncoding RNA H19 accelerates tenogenic differentiation and promotes tendon healing through targeting miR-29b-3p and activating TGF-β1 signaling. FASEB 31:954–964. doi: 10.1096/fj.201600722R
   Web of Science ®Google Scholar
• Lunavat TR, Jang SC, Nilsson L, et al. (2016). RNAi delivery by exosome-mimetic nanovesicles – implications for targeting c-Myc in cancer. Biomaterials 102:231–8.
   PubMed Web of Science ®Google Scholar
• Maas SL, Breakefield XO, Weaver AM. (2017). Extracellular vesicles: unique intercellular delivery vehicles. Trends Cell Biol 27:172–88.
   PubMed Web of Science ®Google Scholar
• Marrotte EJ, Chen DD, Hakim JS, Chen AF. (2010). Manganese superoxide dismutase expression in endothelial progenitor cells accelerates wound healing in diabetic mice. J Clin Invest 120:4207–19.
   PubMed Web of Science ®Google Scholar
• Mendez JJ, Ghaedi M, Sivarapatna A, et al. (2015). Mesenchymal stromal cells form vascular tubes when placed in fibrin sealant and accelerate wound healing in vivo. Biomaterials 40:61–71.
   PubMed Web of Science ®Google Scholar
• Morton LM, Phillips TJ. (2016). Wound healing and treating wounds: Differential diagnosis and evaluation of chronic wounds. J Am Acad Dermatol 74:589–605. quiz 605-6.
   PubMed Web of Science ®Google Scholar
• Mulcahy LA, Pink RC, Carter DR. (2014). Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles 3:24641.
   PubMedGoogle Scholar
• Nakamura Y, Ishikawa H, Kawai K, et al. (2013). Enhanced wound healing by topical administration of mesenchymal stem cells transfected with stromal cell-derived factor-1. Biomaterials 34:9393–400.
   PubMed Web of Science ®Google Scholar
• Oh K, Kim SR, Kim DK, et al. (2015). In vivo differentiation of therapeutic insulin-producing cells from bone marrow cells via extracellular vesicle-mimetic Nanovesicles. ACS Nano 9:11718–27.
   PubMed Web of Science ®Google Scholar
• Ohno S, Kuroda M. (2016). Exosome-mediated targeted delivery of miRNAs. Methods Mol Biol 1448:261–70.
   PubMedGoogle Scholar
• Pachnis V, Belayew A, Tilghman SM. (1984). Locus unlinked to alpha-fetoprotein under the control of the murine raf and Rif genes. Proc Natl Acad Sci USA 81:5523–7.
   PubMed Web of Science ®Google Scholar
• Peer D, Karp JM, Hong S, et al. (2007). Nanocarriers as an emerging platform for cancer therapy. Nat Nanotech 2:751–60.
   PubMed Web of Science ®Google Scholar
• Perez-Gonzalez R, Gauthier SA, Kumar A, Levy E. (2012). The exosome-secretory pathway transports amyloid precursor protein carboxyl terminal fragments from the cell into the brain extracellular space. J Biol Chem 287:43108–15.
   PubMed Web of Science ®Google Scholar
• Qu L, Ding J, Chen C, et al. (2016). Exosome-transmitted lncARSR promotes sunitinib resistance in renal cancer by acting as a competing endogenous RNA. Cancer Cell 29:653–68.
   PubMed Web of Science ®Google Scholar
• Robbins PD, Morelli AE. (2014). Regulation of immune responses by extracellular vesicles. Nat Rev Immunol 14:195–208.
   PubMed Web of Science ®Google Scholar
• Roche ED, Renick PJ, Tetens SP, et al. (2012). Increasing the presence of biofilm and healing delay in a porcine model of MRSA-infected wounds. Wound Repair Regen 20:537–43.
   PubMed Web of Science ®Google Scholar
• Ruttermann M, Maier-Hasselmann A, Nink-Grebe B, Burckhardt M. (2013). Local treatment of chronic wounds: in patients with peripheral vascular disease, chronic venous insufficiency, and diabetes. Dtsch Arztebl Int 110:25–31.
   PubMed Web of Science ®Google Scholar
• Salmena L, Poliseno L, Tay Y, et al. (2011). A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146:353–8.
   PubMed Web of Science ®Google Scholar
• Schoneberg J, Lee IH, Iwasa JH, Hurley JH. (2017). Reverse-topology membrane scission by the ESCRT proteins. Nat Rev Mol Cell Biol 18:5–17.
   PubMed Web of Science ®Google Scholar
• Shiojima I, Walsh K. (2002). Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res 90:1243–50.
   PubMed Web of Science ®Google Scholar
• Su R, Wang C, Feng H, et al. (2016). Alteration in expression and methylation of IGF2/H19 in Placenta and umbilical cord blood are associated with Macrosomia exposed to intrauterine Hyperglycemia. PLoS One 11:e0148399.
   PubMed Web of Science ®Google Scholar
• Sun JY, Zhao X, Illeperuma WR, et al. (2012). Highly stretchable and tough hydrogels. Nature 489:133–6.
   PubMed Web of Science ®Google Scholar
• Tao SC, Guo SC, Li M, et al. (2017a). Chitosan wound dressings incorporating exosomes derived from MicroRNA-126-overexpressing synovium mesenchymal stem cells provide sustained release of exosomes and heal full-thickness skin defects in a diabetic rat model. Stem Cells Transl Med 6:736–47.
   PubMed Web of Science ®Google Scholar
• Tao SC, Guo SC, Zhang CQ. (2017b). Platelet-derived extracellular vesicles: an emerging therapeutic approach. Int J Biol Sci 13:828–34.
   PubMed Web of Science ®Google Scholar
• Tao SC, Yuan T, Rui BY, et al. (2017c). Exosomes derived from human platelet-rich plasma prevent apoptosis induced by glucocorticoid-associated endoplasmic reticulum stress in rat osteonecrosis of the femoral head via the Akt/Bad/Bcl-2 signal pathway. Theranostics 7:733–50.
   PubMed Web of Science ®Google Scholar
• Tao SC, Yuan T, Zhang YL, et al. (2017d). Exosomes derived from miR-140-5p-overexpressing human synovial mesenchymal stem cells enhance cartilage tissue regeneration and prevent osteoarthritis of the knee in a rat model. Theranostics 7:180–95.
   PubMed Web of Science ®Google Scholar
• Tarnuzzer RW, Schultz GS. (1996). Biochemical analysis of acute and chronic wound environments. Wound Repair Regen 4:321–5.
   PubMedGoogle Scholar
• Vader P, Mol EA, Pasterkamp G, Schiffelers RM. (2016). Extracellular vesicles for drug delivery. Adv Drug Deliv Rev 106:148–156. doi: 10.1016/j.addr.2016.02.006
   Web of Science ®Google Scholar
• Villasante A, Marturano-Kruik A, Ambati SR, et al. (2016). Recapitulating the size and cargo of tumor exosomes in a tissue-engineered model. Theranostics 6:1119–30.
   PubMed Web of Science ®Google Scholar
• Vind BF, Birk JB, Vienberg SG, et al. (2012). Hyperglycaemia normalises insulin action on glucose metabolism but not the impaired activation of AKT and glycogen synthase in the skeletal muscle of patients with type 2 diabetes. Diabetologia 55:1435–45.
   PubMed Web of Science ®Google Scholar
• Wang G, Dinkins M, He Q, et al. (2012). Astrocytes secrete exosomes enriched with proapoptotic ceramide and prostate apoptosis response 4 (PAR-4): potential mechanism of apoptosis induction in Alzheimer disease (AD). J Biol Chem 287:21384–95.
   PubMed Web of Science ®Google Scholar
• Werdin F, Tenenhaus M, Rennekampff HO. (2008). Chronic wound care. Lancet 372:1860–2.
   PubMed Web of Science ®Google Scholar
• Wittman MD, Carboni JM, Yang Z, et al. (2009). Discovery of a 2,4-disubstituted pyrrolo[1,2-f][1,2,4]triazine inhibitor (BMS-754807) of insulin-like growth factor receptor (IGF-1R) kinase in clinical development. J Med Chem 52:7360–3.
   PubMed Web of Science ®Google Scholar
• Xing H, Hwang K, Lu Y. (2016). Recent developments of liposomes as nanocarriers for theranostic applications. Theranostics 6:1336–52.
   PubMed Web of Science ®Google Scholar
• Xu J, Zgheib C, Hu J, et al. (2014). The role of microRNA-15b in the impaired angiogenesis in diabetic wounds. Wound Repair Regen 22:671–7.
   PubMed Web of Science ®Google Scholar
• Yang T, Zhao P, Rong Z, et al. (2016). Anti-tumor efficiency of lipid-coated cisplatin nanoparticles co-loaded with MicroRNA-375. Theranostics 6:142–54.
   PubMed Web of Science ®Google Scholar
• Yoon CH, Choi YE, Koh SJ, et al. (2014). High glucose-induced jagged 1 in endothelial cells disturbs notch signaling for angiogenesis: a novel mechanism of diabetic vasculopathy. J Mol Cell Cardiol 69:52–66.
   PubMed Web of Science ®Google Scholar
• Yu H, Guo C, Feng B, et al. (2016). Triple-Layered pH-Responsive Micelleplexes loaded with siRNA and Cisplatin Prodrug for NF-Kappa B targeted treatment of metastatic breast cancer. Theranostics 6:14–27.
   PubMed Web of Science ®Google Scholar
• Zhang J, Li S, Li L, et al. (2015). Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics 13:17–24.
   PubMed Web of Science ®Google Scholar
• Zhang J, Liu X, Li H, et al. (2016a). Exosomes/tricalcium phosphate combination scaffolds can enhance bone regeneration by activating the PI3K/Akt signaling pathway. Stem Cell Res Ther 7:136.
   PubMed Web of Science ®Google Scholar
• Zhang L, Sun Z, Ren P, et al. (2017). Localized delivery of shRNA against PHD2 protects the heart from acute myocardial infarction through ultrasound-targeted cationic microbubble destruction. Theranostics 7:51–66.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Xu Y, Feng L, et al. (2016b). Comprehensive characterization of lncRNA-mRNA related ceRNA network across 12 major cancers. Oncotarget 7:64148–67.
   PubMed Web of Science ®Google Scholar
• Zhao S, Li L, Wang H, et al. (2015). Wound dressings composed of copper-doped borate bioactive glass microfibers stimulate angiogenesis and heal full-thickness skin defects in a rodent model. Biomaterials 53:379–91.
   PubMed Web of Science ®Google Scholar