Adipose-Derived Stem Cell Exosomes Facilitate Diabetic Wound Healing: Mechanisms and Potential Applications

References

• Li J, Wang X, Mao H, et al. Precision therapy for three Chinese families with maturity-onset diabetes of the young (MODY12). Front Endocrinol. 2022;13:858096. doi:10.3389/fendo.2022.858096
   PubMed Web of Science ®Google Scholar
• Sun H, Saeedi P, Karuranga S, et al. IDF Diabetes Atlas: global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabet Res Clin Pract. 2022;183:109119. doi:10.1016/j.diabres.2021.109119
   PubMed Web of Science ®Google Scholar
• Forbes JM, Cooper ME. Mechanisms of diabetic complications. Physiol Rev. 2013;93(1):137–188. doi:10.1152/physrev.00045.2011
   PubMed Web of Science ®Google Scholar
• Mahyoub MA, Elhoumed M, Maqul AH, et al. Fatty infiltration of the pancreas: a systematic concept analysis. Front Med Lausanne. 2023;10:1227188. doi:10.3389/fmed.2023.1227188
   PubMed Web of Science ®Google Scholar
• Zhao B, Li M, Su Y, et al. Role of transcription factor FOXM1 in diabetes and its complications (Review). Int J Mol Med. 2023;52(5). doi:10.3892/ijmm.2023.5304
   Web of Science ®Google Scholar
• Zhou YF, Liu HW, Yang X, Li CX, Chen JS, Chen ZP. Probucol attenuates high glucose-induced Müller cell damage through enhancing the Nrf2/p62 signaling pathway. Int Ophthalmol. 2023;43(12):4595–4604. doi:10.1007/s10792-023-02859-z
   PubMed Web of Science ®Google Scholar
• Zheng Y, Ma S, Huang Q, et al. Meta-analysis of the efficacy and safety of finerenone in diabetic kidney disease. Kidney Blood Press Res. 2022;47(4):219–228. doi:10.1159/000521908
   PubMed Web of Science ®Google Scholar
• Chang M, Nguyen TT. Strategy for Treatment of Infected Diabetic Foot Ulcers. Acc Chem Res. 2021;54(5):1080–1093. doi:10.1021/acs.accounts.0c00864
   PubMed Web of Science ®Google Scholar
• Beyaz S, Guler UO, Bagir GS. Factors affecting lifespan following below-knee amputation in diabetic patients. Acta Orthop Traumatol Turc. 2017;51(5):393–397. doi:10.1016/j.aott.2017.07.001
   PubMed Web of Science ®Google Scholar
• Perez-Favila A, Martinez-Fierro ML, Rodriguez-Lazalde JG, et al. Current therapeutic strategies in diabetic foot ulcers. Medicina. 2019;55(11). doi:10.3390/medicina55110714
   PubMedGoogle Scholar
• Lewis J, Lipp A. Pressure-relieving interventions for treating diabetic foot ulcers. Cochrane Database Syst Rev. 2013;(1):Cd002302. doi:10.1002/14651858.CD002302.pub2
   PubMed Web of Science ®Google Scholar
• Lei M, Guo X, Yao Y, et al. Trelagliptin relieved cognitive impairment of diabetes mellitus rats: involvement of PI3K/Akt/GSK-3β and inflammation pathway. Exp Gerontol. 2023;182:112307. doi:10.1016/j.exger.2023.112307
   PubMed Web of Science ®Google Scholar
• Bacakova L, Zarubova J, Travnickova M, et al. Stem cells: their source, potency and use in regenerative therapies with focus on adipose-derived stem cells - a review. Biotechnol Adv. 2018;36(4):1111–1126. doi:10.1016/j.biotechadv.2018.03.011
   PubMed Web of Science ®Google Scholar
• Mazini L, Rochette L, Admou B, Amal S, Malka G. Hopes and limits of adipose-derived stem cells (ADSCs) and mesenchymal stem cells (MSCs) in Wound Healing. Int J Mol Sci. 2020;21(4):1.
   Web of Science ®Google Scholar
• Hu C, Zhao L, Li L. Current understanding of adipose-derived mesenchymal stem cell-based therapies in liver diseases. Stem Cell Res Ther. 2019;10(1):199. doi:10.1186/s13287-019-1310-1
   PubMedGoogle Scholar
• Sheashaa H, Lotfy A, Elhusseini F, et al. Protective effect of adipose-derived mesenchymal stem cells against acute kidney injury induced by ischemia-reperfusion in Sprague-Dawley rats. Exp Ther Med. 2016;11(5):1573–1580. doi:10.3892/etm.2016.3109
   PubMed Web of Science ®Google Scholar
• Cai Y, Li J, Jia C, He Y, Deng C. Therapeutic applications of adipose cell-free derivatives: a review. Stem Cell Res Ther. 2020;11(1):312. doi:10.1186/s13287-020-01831-3
   PubMed Web of Science ®Google Scholar
• Long C, Wang J, Gan W, Qin X, Yang R, Chen X. Therapeutic potential of exosomes from adipose-derived stem cells in chronic wound healing. Front Surg. 2022;9:1030288. doi:10.3389/fsurg.2022.1030288
   PubMed Web of Science ®Google Scholar
• Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science. 2020;367(6478). doi:10.1126/science.aau6977
   PubMed Web of Science ®Google Scholar
• An Y, Lin S, Tan X, et al. Exosomes from adipose-derived stem cells and application to skin wound healing. Cell Prolif. 2021;54(3):e12993. doi:10.1111/cpr.12993
   PubMed Web of Science ®Google Scholar
• Zhu Z, Lian X, Su X, Wu W, Zeng Y, Chen X. Exosomes derived from adipose-derived stem cells alleviate cigarette smoke-induced lung inflammation and injury by inhibiting alveolar macrophages pyroptosis. Respir Res. 2022;23(1):5. doi:10.1186/s12931-022-01926-w
   PubMed Web of Science ®Google Scholar
• Zhang Q, Piao C, Xu J, et al. ADSCs-exo attenuates hepatic ischemia-reperfusion injury after hepatectomy by inhibiting endoplasmic reticulum stress and inflammation. J Cell Physiol. 2023;238(3):659–669. doi:10.1002/jcp.30968
   PubMed Web of Science ®Google Scholar
• Sheykhhasan M, Amini R, Soleimani Asl S, Saidijam M, Hashemi SM, Najafi R. Neuroprotective effects of coenzyme Q10-loaded exosomes obtained from adipose-derived stem cells in a rat model of Alzheimer’s disease. Biomed Pharmacother. 2022;152:113224. doi:10.1016/j.biopha.2022.113224
   PubMed Web of Science ®Google Scholar
• Hu X, Pan J, Li Y, et al. Extracellular vesicles from adipose-derived stem cells promote microglia M2 polarization and neurological recovery in a mouse model of transient middle cerebral artery occlusion. Stem Cell Res Ther. 2022;13(1):21. doi:10.1186/s13287-021-02668-0
   PubMed Web of Science ®Google Scholar
• Lou G, Chen L, Xia C, et al. MiR-199a-modified exosomes from adipose tissue-derived mesenchymal stem cells improve hepatocellular carcinoma chemosensitivity through mTOR pathway. J Exp Clin Cancer Res. 2020;39(1):4. doi:10.1186/s13046-019-1512-5
   PubMed Web of Science ®Google Scholar
• Liang Z, Liu H, Zhang Y, et al. Cyr61 from adipose-derived stem cells promotes colorectal cancer metastasis and vasculogenic mimicry formation via integrin α(V) β(5). Mol Oncol. 2021;15(12):3447–3467. doi:10.1002/1878-0261.12998
   PubMed Web of Science ®Google Scholar
• Trams EG, Lauter CJ, Heine U, Heine U. Exfoliation of membrane ecto-enzymes in the form of micro-vesicles. Biochim et Bio Acta. 1981;645(1):63–70. doi:10.1016/0005-2736(81)90512-5
   PubMed Web of Science ®Google Scholar
• Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell. 1983;33(3):967–978. doi:10.1016/0092-8674(83)90040-5
   PubMed Web of Science ®Google Scholar
• Théry C, Witwer KW, Aikawa E, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles. 2018;7(1):1535750. doi:10.1080/20013078.2018.1535750
   PubMed Web of Science ®Google Scholar
• Ludwig AK, Giebel B. Exosomes: small vesicles participating in intercellular communication. Int J Biochem Cell Biol. 2012;44(1):11–15. doi:10.1016/j.biocel.2011.10.005
   PubMed Web of Science ®Google Scholar
• He C, Zheng S, Luo Y, Wang B. Exosome theranostics: biology and translational medicine. Theranostics. 2018;8(1):237–255. doi:10.7150/thno.21945
   PubMed Web of Science ®Google Scholar
• Théry C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2(8):569–579. doi:10.1038/nri855
   PubMed Web of Science ®Google Scholar
• Raiborg C, Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature. 2009;458(7237):445–452. doi:10.1038/nature07961
   PubMed Web of Science ®Google Scholar
• Stuffers S, Sem Wegner C, Stenmark H, Brech A. Multivesicular endosome biogenesis in the absence of ESCRTs. Traffic. 2009;10(7):925–937. doi:10.1111/j.1600-0854.2009.00920.x
   PubMed Web of Science ®Google Scholar
• Robbins PD, Morelli AE. Regulation of immune responses by extracellular vesicles. Nat Rev Immunol. 2014;14(3):195–208. doi:10.1038/nri3622
   PubMed Web of Science ®Google Scholar
• van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018;19(4):213–228. doi:10.1038/nrm.2017.125
   PubMed Web of Science ®Google Scholar
• Dai J, Su Y, Zhong S, et al. Exosomes: key players in cancer and potential therapeutic strategy. Signal Transduct Target Ther. 2020;5(1):145. doi:10.1038/s41392-020-00261-0
   PubMed Web of Science ®Google Scholar
• Mathieu M, Martin-Jaular L, Lavieu G, Théry 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. doi:10.1038/s41556-018-0250-9
   PubMed Web of Science ®Google Scholar
• Jeppesen DK, Fenix AM, Franklin JL, et al. Reassessment of Exosome Composition. Cell. 2019;177(2):428–445.e18. doi:10.1016/j.cell.2019.02.029
   PubMed Web of Science ®Google Scholar
• Keerthikumar S, Chisanga D, Ariyaratne D, et al. ExoCarta: a Web-Based Compendium of Exosomal Cargo. J Mol Biol. 2016;428(4):688–692. doi:10.1016/j.jmb.2015.09.019
   PubMed Web of Science ®Google Scholar
• Lai H, Li Y, Zhang H, et al. exoRBase 2.0: an atlas of mRNA, lncRNA and circRNA in extracellular vesicles from human biofluids. Nucleic Acids Res. 2022:50(D1):D118–D128. doi:10.1093/nar/gkab1085
   PubMed Web of Science ®Google Scholar
• Shen K, Wang X, Wang Y, et al. miR-125b-5p in adipose derived stem cells exosome alleviates pulmonary microvascular endothelial cells ferroptosis via Keap1/Nrf2/GPX4 in sepsis lung injury. Redox Biol. 2023;62:102655. doi:10.1016/j.redox.2023.102655
   PubMed Web of Science ®Google Scholar
• Shen K, Jia Y, Wang X, et al. Exosomes from adipose-derived stem cells alleviate the inflammation and oxidative stress via regulating Nrf2/HO-1 axis in macrophages. Free Radic Biol Med. 2021;165:54–66. doi:10.1016/j.freeradbiomed.2021.01.023
   PubMed Web of Science ®Google Scholar
• Liu M, Yang Y, Zhao B, et al. Exosomes derived from adipose-derived mesenchymal stem cells ameliorate radiation-induced brain injury by activating the SIRT1 pathway. Front Cell Dev Biol. 2021;9:693782. doi:10.3389/fcell.2021.693782
   PubMed Web of Science ®Google Scholar
• Zhao S, Liu Y, Wang J, et al. ADSCs increase the autophagy of chondrocytes through decreasing miR-7-5p in Osteoarthritis rats by targeting ATG4A. Int Immunopharmacol. 2023;120:110390. doi:10.1016/j.intimp.2023.110390
   PubMed Web of Science ®Google Scholar
• Gould SJ, Raposo G. As we wait: coping with an imperfect nomenclature for extracellular vesicles. J Extracell Vesicles. 2013;2. doi:10.3402/jev.v2i0.20389
   PubMedGoogle Scholar
• van der Pol E, Böing AN, Harrison P, Sturk A, Nieuwland R. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev. 2012;64(3):676–705. doi:10.1124/pr.112.005983
   PubMed Web of Science ®Google Scholar
• Baranyai T, Herczeg K, Onódi Z, et al. Isolation of exosomes from blood plasma: qualitative and quantitative comparison of ultracentrifugation and size exclusion chromatography methods. PLoS One. 2015;10(12):e0145686. doi:10.1371/journal.pone.0145686
   PubMed Web of Science ®Google Scholar
• Gheinani AH, Vögeli M, Baumgartner U, et al. Improved isolation strategies to increase the yield and purity of human urinary exosomes for biomarker discovery. Sci Rep. 2018;8(1):3945. doi:10.1038/s41598-018-22142-x
   PubMedGoogle Scholar
• Taylor DD, Shah S. Methods of isolating extracellular vesicles impact down-stream analyses of their cargoes. Methods. 2015;87:3–10. doi:10.1016/j.ymeth.2015.02.019
   PubMed Web of Science ®Google Scholar
• Wu B, Feng J, Guo J, et al. ADSCs-derived exosomes ameliorate hepatic fibrosis by suppressing stellate cell activation and remodeling hepatocellular glutamine synthetase-mediated glutamine and ammonia homeostasis. Stem Cell Res Ther. 2022;13(1):494. doi:10.1186/s13287-022-03049-x
   PubMed Web of Science ®Google Scholar
• Mathew A, Bell A, Johnstone RM. Hsp-70 is closely associated with the transferrin receptor in exosomes from maturing reticulocytes. Biochem J. 1995;308(Pt 3):823–830. doi:10.1042/bj3080823
   PubMedGoogle Scholar
• Zhang W, Bai X, Zhao B, et al. Cell-free therapy based on adipose tissue stem cell-derived exosomes promotes wound healing via the PI3K/Akt signaling pathway. Exp Cell Res. 2018;370(2):333–342. doi:10.1016/j.yexcr.2018.06.035
   PubMed Web of Science ®Google Scholar
• Airuddin SS, Halim AS, Wan Sulaiman WA, Kadir R, Nasir NAM. Adipose-derived stem cell: ”treat or trick”. Biomedicines. 2021;9(11). doi:10.3390/biomedicines9111624
   PubMed Web of Science ®Google Scholar
• Deng S, zhou X, Ge Z, et al. Exosomes from adipose-derived mesenchymal stem cells ameliorate cardiac damage after myocardial infarction by activating S1P/SK1/S1PR1 signaling and promoting macrophage M2 polarization. Int J Biochem Cell Biol. 2019;114:105564. doi:10.1016/j.biocel.2019.105564
   PubMed Web of Science ®Google Scholar
• Tian J, Cui X, Sun J, Zhang J. Exosomal microRNA-16-5p from adipose mesenchymal stem cells promotes TLR4-mediated M2 macrophage polarization in septic lung injury. Int Immunopharmacol. 2021;98:107835. doi:10.1016/j.intimp.2021.107835
   PubMed Web of Science ®Google Scholar
• Liu Z, Xu Y, Wan Y, Gao J, Chu Y, Li J. Exosomes from adipose-derived mesenchymal stem cells prevent cardiomyocyte apoptosis induced by oxidative stress. Cell Death Discov. 2019;5:79. doi:10.1038/s41420-019-0159-5
   PubMed Web of Science ®Google Scholar
• Zhang W, Zhang J, Huang H. Exosomes from adipose-derived stem cells inhibit inflammation and oxidative stress in LPS-acute kidney injury. Exp Cell Res. 2022;420(1):113332. doi:10.1016/j.yexcr.2022.113332
   PubMed Web of Science ®Google Scholar
• Li X, Xie X, Lian W, et al. Exosomes from adipose-derived stem cells overexpressing Nrf2 accelerate cutaneous wound healing by promoting vascularization in a diabetic foot ulcer rat model. Exp Mol Med. 2018;50(4):1–14. doi:10.1038/s12276-018-0058-5
   Web of Science ®Google Scholar
• Zhang X, Zhang X, Chen L, et al. Adipose mesenchymal stem cell-derived exosomes enhanced glycolysis through the SIX1/HBO1 pathway against oxygen and glucose deprivation injury in human umbilical vein endothelial cells. Curr Stem Cell Res Ther. 2023. doi:10.2174/011574888x265623230921045240
   Web of Science ®Google Scholar
• Ji Z, Cai Z, Gu S, et al. Exosomes derived from human adipose-derived stem cells inhibit lipogenesis involving hedgehog signaling pathway. Front Bioeng Biotechnol. 2021;9:734810. doi:10.3389/fbioe.2021.734810
   PubMed Web of Science ®Google Scholar
• Shin KO, Ha DH, Kim JO, et al. Exosomes from human adipose tissue-derived mesenchymal stem cells promote epidermal barrier repair by inducing de novo synthesis of ceramides in atopic dermatitis. Cells. 2020;9(3):680. doi:10.3390/cells9030680
   PubMed Web of Science ®Google Scholar
• Choi EW, Seo MK, Woo EY, Kim SH, Park EJ, Kim S. Exosomes from human adipose-derived stem cells promote proliferation and migration of skin fibroblasts. Exp Dermatol. 2018;27(10):1170–1172. doi:10.1111/exd.13451
   PubMed Web of Science ®Google Scholar
• Wang L, Hu L, Zhou X, et al. Exosomes secreted by human adipose mesenchymal stem cells promote scarless cutaneous repair by regulating extracellular matrix remodelling. Sci Rep. 2017;7(1):13321. doi:10.1038/s41598-017-12919-x
   PubMed Web of Science ®Google Scholar
• Zhu S, Li J, Zhao X. Comparative risk of new-onset hyperkalemia for antihypertensive drugs in patients with diabetic nephropathy: a Bayesian network meta-analysis. Int J Clin Pract. 2021;75(8):e13940. doi:10.1111/ijcp.13940
   PubMed Web of Science ®Google Scholar
• Velnar T, Bailey T, Smrkolj V. The wound healing process: an overview of the cellular and molecular mechanisms. J Int Med Res Sep-Oct. 2009;37(5):1528–1542. doi:10.1177/147323000903700531
   PubMed Web of Science ®Google Scholar
• Gantwerker EA, Hom DB. Skin: histology and Physiology of Wound Healing. Facial Plastic Surg Clin North Am. 2011;19(3):441–453. doi:10.1016/j.fsc.2011.06.009
   PubMed Web of Science ®Google Scholar
• Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev. 2003;83(3):835–870. doi:10.1152/physrev.2003.83.3.835
   PubMed Web of Science ®Google Scholar
• Aitcheson SM, Frentiu FD, Hurn SE, Edwards K, Murray RZ. Skin wound healing: normal macrophage function and macrophage dysfunction in diabetic wounds. Molecules. 2021;26(16):4917. doi:10.3390/molecules26164917
   PubMed Web of Science ®Google Scholar
• Hesketh M, Sahin KB, West ZE, Murray RZ. Macrophage phenotypes regulate scar formation and chronic wound healing. Int J Mol Sci. 2017;18(7):1545. doi:10.3390/ijms18071545
   PubMed Web of Science ®Google Scholar
• Louiselle AE, Niemiec SM, Zgheib C, Liechty KW. Macrophage polarization and diabetic wound healing. Transl Res. 2021;236:109–116. doi:10.1016/j.trsl.2021.05.006
   PubMed Web of Science ®Google Scholar
• Rodrigues M, Kosaric N, Bonham CA, Gurtner GC. Wound Healing: a Cellular Perspective. Physiol Rev. 2019;99(1):665–706. doi:10.1152/physrev.00067.2017
   PubMed Web of Science ®Google Scholar
• Zhou B, Gao Z, Liu W, Wu X, Wang W. Important role of mechanical microenvironment on macrophage dysfunction during keloid pathogenesis. Exp Dermatol. 2022;31(3):375–380. doi:10.1111/exd.14473
   PubMed Web of Science ®Google Scholar
• Burgess JL, Wyant WA, Abdo Abujamra B, Kirsner RS, Jozic I. Diabetic wound-healing science. Medicina. 2021;57:1.
   Google Scholar
• Zhang P, Lu J, Jing Y, Tang S, Zhu D, Bi Y. Global epidemiology of diabetic foot ulceration: a systematic review and meta-analysis. Anna Med. 2017;49(2):106–116. doi:10.1080/07853890.2016.1231932
   PubMed Web of Science ®Google Scholar
• Schreml S, Berneburg M. The global burden of diabetic wounds. Br J Dermatol. 2017;176(4):845–846. doi:10.1111/bjd.15254
   PubMed Web of Science ®Google Scholar
• Seidel D, Storck M, Lawall H, et al. Negative pressure wound therapy compared with standard moist wound care on diabetic foot ulcers in real-life clinical practice: results of the German DiaFu-RCT. BMJ Open. 2020;10(3):e026345. doi:10.1136/bmjopen-2018-026345
   PubMed Web of Science ®Google Scholar
• Liu Z, Dumville JC, Hinchliffe RJ, et al. Negative pressure wound therapy for treating foot wounds in people with diabetes mellitus. Cochrane Database Syst Rev. 2018;10(10):Cd010318. doi:10.1002/14651858.CD010318.pub3
   PubMedGoogle Scholar
• Boniakowski AE, Kimball AS, Jacobs BN, Kunkel SL, Gallagher KA. Macrophage-Mediated Inflammation in Normal and Diabetic Wound Healing. J Immunol. 2017;199(1):17–24. doi:10.4049/jimmunol.1700223
   PubMed Web of Science ®Google Scholar
• Li S, Ding X, Zhang H, Ding Y, Tan Q. IL-25 improves diabetic wound healing through stimulating M2 macrophage polarization and fibroblast activation. Int Immunopharmacol. 2022;106:108605. doi:10.1016/j.intimp.2022.108605
   PubMed Web of Science ®Google Scholar
• Al Sadoun H. Macrophage phenotypes in normal and diabetic wound healing and therapeutic interventions. Cells. 2022;11(15):2430. doi:10.3390/cells11152430
   PubMed Web of Science ®Google Scholar
• Di G, Du X, Qi X, et al. Mesenchymal stem cells promote diabetic corneal epithelial wound healing through TSG-6-dependent stem cell activation and macrophage switch. Invest Ophthalmol Vis Sci. 2017;58(10):4344–4354. doi:10.1167/iovs.17-21506
   PubMed Web of Science ®Google Scholar
• Sharifiaghdam M, Shaabani E, Faridi-Majidi R, De Smedt SC, Braeckmans K, Fraire JC. Macrophages as a therapeutic target to promote diabetic wound healing. Mol Ther. 2022;30(9):2891–2908. doi:10.1016/j.ymthe.2022.07.016
   PubMed Web of Science ®Google Scholar
• Schaper NC, van Netten JJ, Apelqvist J, Bus SA, Hinchliffe RJ, Lipsky BA. Practical Guidelines on the prevention and management of diabetic foot disease (IWGDF 2019 update). Diabetes Metab Res Rev. 2020;36(1):e3266. doi:10.1002/dmrr.3266
   PubMedGoogle Scholar
• Rayman G, Vas P, Dhatariya K, et al. Guidelines on use of interventions to enhance healing of chronic foot ulcers in diabetes (IWGDF 2019 update). Diabetes Metab Res Rev. 2020;36(1):e3283. doi:10.1002/dmrr.3283
   PubMedGoogle Scholar
• Raghupathy S, Arikrishnan A. A PROSPECTIVE RANDOMIZED TRIAL OF VACUUM-ASSISTED CLOSURE VERSUS STANDARD THERAPY OF CHRONIC NON-HEALING WOUNDS. J Evolution of Med Dent Sci. 2016;5. doi:10.14260/jemds/2016/733
   Google Scholar
• Normandin S, Safran T, Winocour S, et al. Negative pressure wound therapy: mechanism of action and clinical applications. Semin Plast Surg. 2021;35(3):164–170. doi:10.1055/s-0041-1731792
   PubMedGoogle Scholar
• McCallon SK, Knight CA, Valiulus JP, Cunningham MW, McCulloch JM, Farinas LP. Vacuum-assisted closure versus saline-moistened gauze in the healing of postoperative diabetic foot wounds. Ostomy Wound Man. 2000;46(8):28–32, 34.
   PubMedGoogle Scholar
• Ubbink DT, van der Oord BM, Sobotka MR, Jacobs MJ. Effects of vacuum compression therapy on skin microcirculation in patients suffering from lower limb ischaemia. Vasa. 2000;29(1):53–57. doi:10.1024/0301-1526.29.1.53
   PubMedGoogle Scholar
• Bai Q, Han K, Dong K, et al. Potential applications of nanomaterials and technology for diabetic wound healing. Int J Nanomed. 2020;15:9717–9743. doi:10.2147/ijn.S276001
   PubMed Web of Science ®Google Scholar
• Feng J, Yao Y, Wang Q, et al. Exosomes: potential key players towards novel therapeutic options in diabetic wounds. Biomed Pharmacother. 2023;166:115297. doi:10.1016/j.biopha.2023.115297
   PubMed Web of Science ®Google Scholar
• Yuan T, Meijia L, Xinyao C, Xinyue C, Lijun H. Exosome derived from human adipose-derived stem cell improve wound healing quality: a systematic review and meta-analysis of preclinical animal studies. Int Wound J. 2023;20(6):2424–2439. doi:10.1111/iwj.14081
   PubMed Web of Science ®Google Scholar
• Ren S, Chen J, Guo J, et al. Exosomes from adipose stem cells promote diabetic wound healing through the eHSP90/LRP1/AKT axis. Cells. 2022;11(20):3229. doi:10.3390/cells11203229
   PubMed Web of Science ®Google Scholar
• Zhang Y, Bai X, Shen K, et al. Exosomes derived from adipose mesenchymal stem cells promote diabetic chronic wound healing through SIRT3/SOD2. Cells. 2022;11(16):1.
   Web of Science ®Google Scholar
• Wang J, Yi Y, Zhu Y, et al. Effects of adipose-derived stem cell released exosomes on wound healing in diabetic mice. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi. 2020;34(1):124–131. doi:10.7507/1002-1892.201903058
   PubMedGoogle Scholar
• Shi R, Jin Y, Zhao S, Yuan H, Shi J, Zhao H. Hypoxic ADSC-derived exosomes enhance wound healing in diabetic mice via delivery of circ-Snhg11 and induction of M2-like macrophage polarization. Biomed Pharmacother. 2022;153:113463. doi:10.1016/j.biopha.2022.113463
   PubMed Web of Science ®Google Scholar
• Hu N, Cai Z, Jiang X, et al. Hypoxia-pretreated ADSC-derived exosome-embedded hydrogels promote angiogenesis and accelerate diabetic wound healing. Acta Biomater. 2023;157:175–186. doi:10.1016/j.actbio.2022.11.057
   PubMed Web of Science ®Google Scholar
• Wang Z, Feng C, Liu H, et al. Exosomes from circ-Astn1-modified adipose-derived mesenchymal stem cells enhance wound healing through miR-138-5p/SIRT1/FOXO1 axis regulation. World J Stem Cells. 2023;15(5):476–489. doi:10.4252/wjsc.v15.i5.476
   PubMed Web of Science ®Google Scholar
• Shi R, Jin Y, Hu W, et al. Exosomes derived from mmu_circ_0000250-modified adipose-derived mesenchymal stem cells promote wound healing in diabetic mice by inducing miR-128-3p/SIRT1-mediated autophagy. Am J Physiol Cell Physiol. 2020;318(5):C848–C856. doi:10.1152/ajpcell.00041.2020
   PubMed Web of Science ®Google Scholar
• Cao T, Xiao D, Ji P, et al. Effects of exosomes from hepatocyte growth factor-modified human adipose mesenchymal stem cells on full-thickness skin defect in diabetic mice. Zhonghua Shao Shang Za Zhi. 2022;38(11):1004–1013. doi:10.3760/cma.j.cn501225-20220731-00330
   Google Scholar
• Jiang T, Liu S, Wu Z, et al. ADSC-exo@MMP-PEG smart hydrogel promotes diabetic wound healing by optimizing cellular functions and relieving oxidative stress. Mater Today Bio. 2022;16:100365. doi:10.1016/j.mtbio.2022.100365
   PubMedGoogle Scholar
• Khalatbary AR, Omraninava M, Nasiry D, et al. Exosomes derived from human adipose mesenchymal stem cells loaded bioengineered three-dimensional amniotic membrane-scaffold-accelerated diabetic wound healing. Arch Dermatol Res. 2023;315:2853–2870. doi:10.1007/s00403-023-02709-z
   PubMed Web of Science ®Google Scholar
• Shiekh PA, Singh A, Kumar A. Exosome laden oxygen releasing antioxidant and antibacterial cryogel wound dressing OxOBand alleviate diabetic and infectious wound healing. Biomaterials. 2020;249:120020. doi:10.1016/j.biomaterials.2020.120020
   PubMed Web of Science ®Google Scholar
• Huang H, Zhu W, Huang Z, Zhao D, Cao L, Gao X. Adipose-derived stem cell exosome NFIC improves diabetic foot ulcers by regulating miR-204-3p/HIPK2. J Orthop Surg Res. 2023;18(1):687. doi:10.1186/s13018-023-04165-x
   PubMed Web of Science ®Google Scholar
• Che D, Xiang X, Xie J, Chen Z, Bao Q, Cao D. Exosomes Derived from Adipose Stem Cells Enhance Angiogenesis in Diabetic Wound Via miR-146a-5p/JAZF1 Axis. Stem Cell Rev Rep. 2024;20(4):1026–1039. doi:10.1007/s12015-024-10685-8
   PubMed Web of Science ®Google Scholar
• Liang ZH, Pan NF, Lin SS, et al. Exosomes from mmu_circ_0001052-modified adipose-derived stem cells promote angiogenesis of DFU via miR-106a-5p and FGF4/p38MAPK pathway. Stem Cell Res Ther. 2022;13(1):336. doi:10.1186/s13287-022-03015-7
   PubMed Web of Science ®Google Scholar
• Qiu J, Shu C, Li X, Ye C, Zhang WC. Exosomes from linc00511-overexpressing ADSCs accelerates angiogenesis in diabetic foot ulcers healing by suppressing PAQR3-induced Twist1 degradation. Diabet Res Clin Pract. 2021;180:109032. doi:10.1016/j.diabres.2021.109032
   PubMed Web of Science ®Google Scholar
• Jin J, Shi Y, Gong J, et al. Exosome secreted from adipose-derived stem cells attenuates diabetic nephropathy by promoting autophagy flux and inhibiting apoptosis in podocyte. Stem Cell Res Ther. 2019;10(1):95. doi:10.1186/s13287-019-1177-1
   PubMed Web of Science ®Google Scholar
• Qu Y, Zhang Q, Cai X, et al. Exosomes derived from miR-181-5p-modified adipose-derived mesenchymal stem cells prevent liver fibrosis via autophagy activation. J Cell Mol Med. 2017;21(10):2491–2502. doi:10.1111/jcmm.13170
   PubMed Web of Science ®Google Scholar
• Hu J, Jiang Y, Wu X, et al. Exosomal miR-17-5p from adipose-derived mesenchymal stem cells inhibits abdominal aortic aneurysm by suppressing TXNIP-NLRP3 inflammasome. Stem Cell Res Ther. 2022;13(1):349. doi:10.1186/s13287-022-03037-1
   PubMed Web of Science ®Google Scholar
• Yang H, Tu Z, Yang D, et al. Exosomes from hypoxic pre-treated ADSCs attenuate acute ischemic stroke-induced brain injury via delivery of circ-Rps5 and promote M2 microglia/macrophage polarization. Neurosci Lett. 2022;769:136389. doi:10.1016/j.neulet.2021.136389
   PubMed Web of Science ®Google Scholar
• Hong P, Yang H, Wu Y, Li K, Tang Z. The functions and clinical application potential of exosomes derived from adipose mesenchymal stem cells: a comprehensive review. Stem Cell Res Ther. 2019;10(1):242. doi:10.1186/s13287-019-1358-y
   PubMed Web of Science ®Google Scholar
• Bunggulawa EJ, Wang W, Yin T, et al. Recent advancements in the use of exosomes as drug delivery systems. J Nanobiotechnology. 2018;16(1):81. doi:10.1186/s12951-018-0403-9
   PubMed Web of Science ®Google Scholar
• Zhou Y, Zhao B, Zhang XL, et al. Combined topical and systemic administration with human adipose-derived mesenchymal stem cells (hADSC) and hADSC-derived exosomes markedly promoted cutaneous wound healing and regeneration. Stem Cell Res Ther. 2021;12(1):257. doi:10.1186/s13287-021-02287-9
   PubMed Web of Science ®Google Scholar
• Chen F, Zhang H, Wang Z, et al. Adipose-derived stem cell-derived exosomes ameliorate erectile dysfunction in a rat model of type 2 diabetes. J Sex Med. 2017;14(9):1084–1094. doi:10.1016/j.jsxm.2017.07.005
   PubMed Web of Science ®Google Scholar
• Lenzini S, Bargi R, Chung G, Shin JW. Matrix mechanics and water permeation regulate extracellular vesicle transport. Nat Nanotechnol. 2020;15(3):217–223. doi:10.1038/s41565-020-0636-2
   PubMed Web of Science ®Google Scholar
• Zhou Y, Zhang XL, Lu ST, et al. Human adipose-derived mesenchymal stem cells-derived exosomes encapsulated in pluronic F127 hydrogel promote wound healing and regeneration. Stem Cell Res Ther. 2022;13(1):407. doi:10.1186/s13287-022-02980-3
   PubMed Web of Science ®Google Scholar
• Wang C, Wang M, Xu T, et al. Engineering bioactive self-healing antibacterial exosomes hydrogel for promoting chronic diabetic wound healing and complete skin regeneration. Theranostics. 2019;9(1):65–76. doi:10.7150/thno.29766
   PubMed Web of Science ®Google Scholar
• Zhang Y, Li M, Wang Y, et al. Exosome/metformin-loaded self-healing conductive hydrogel rescues microvascular dysfunction and promotes chronic diabetic wound healing by inhibiting mitochondrial fission. Bioact Mater. 2023;26:323–336. doi:10.1016/j.bioactmat.2023.01.020
   PubMed Web of Science ®Google Scholar
• Safari B, Aghazadeh M, Davaran S, Roshangar L. Exosome-loaded hydrogels: a new cell-free therapeutic approach for skin regeneration. Eur J Pharm Biopharm. 2022;171:50–59. doi:10.1016/j.ejpb.2021.11.002
   PubMed Web of Science ®Google Scholar
• Long J, Etxeberria AE, Nand AV, Bunt CR, Ray S, Seyfoddin A. A 3D printed chitosan-pectin hydrogel wound dressing for lidocaine hydrochloride delivery. Mater Sci Eng C Mater Biol Appl. 2019;104:109873. doi:10.1016/j.msec.2019.109873
   PubMed Web of Science ®Google Scholar
• Zhong Y, Ma H, Lu Y, et al. Investigation on repairing diabetic foot ulcer based on 3D bio-printing Gel/dECM/Qcs composite scaffolds. Tissue Cell. 2023;85:102213. doi:10.1016/j.tice.2023.102213
   PubMed Web of Science ®Google Scholar
• Nuutila K, Samandari M, Endo Y, et al. In vivo printing of growth factor-eluting adhesive scaffolds improves wound healing. Bioact Mater. 2022;8:296–308. doi:10.1016/j.bioactmat.2021.06.030
   PubMed Web of Science ®Google Scholar
• Kronstadt SM, Patel DB, Born LJ, et al. Mesenchymal stem cell culture within perfusion bioreactors incorporating 3d-printed scaffolds enables improved extracellular vesicle yield with preserved bioactivity. Adv Healthc Mater. 2023;12(20):e2300584. doi:10.1002/adhm.202300584
   PubMed Web of Science ®Google Scholar
• Chen P, Zheng L, Wang Y, et al. Desktop-stereolithography 3D printing of a radially oriented extracellular matrix/mesenchymal stem cell exosome bioink for osteochondral defect regeneration. Theranostics. 2019;9(9):2439–2459. doi:10.7150/thno.31017
   PubMed Web of Science ®Google Scholar
• Liu X, Zhang J, Cheng X, et al. Integrated printed BDNF-stimulated HUCMSCs-derived exosomes/collagen/chitosan biological scaffolds with 3D printing technology promoted the remodelling of neural networks after traumatic brain injury. Regen Biomater. 2023:10:rbac085. doi:10.1093/rb/rbac085
   PubMed Web of Science ®Google Scholar
• Tenchov R, Sasso JM, Wang X, Liaw W-S, Chen C-A, Zhou QA. Exosomes─nature’s lipid nanoparticles, a rising star in drug delivery and diagnostics. ACS Nano. 2022;16(11):17802–17846. doi:10.1021/acsnano.2c08774
   PubMed Web of Science ®Google Scholar
• Sun D, Zhuang X, Xiang X, et al. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol Ther. 2010;18(9):1606–1614. doi:10.1038/mt.2010.105
   PubMed Web of Science ®Google Scholar
• Tian Y, Li S, Song J, et al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials. 2014;35(7):2383–2390. doi:10.1016/j.biomaterials.2013.11.083
   PubMed Web of Science ®Google Scholar
• Yang T, Martin P, Fogarty B, et al. Exosome delivered anticancer drugs across the blood-brain barrier for brain cancer therapy in Danio rerio. Pharm Res. 2015;32(6):2003–2014. doi:10.1007/s11095-014-1593-y
   PubMed Web of Science ®Google Scholar
• Batrakova EV, Kim MS. Using exosomes, naturally-equipped nanocarriers, for drug delivery. J Control Release. 2015;219:396–405. doi:10.1016/j.jconrel.2015.07.030
   PubMed Web of Science ®Google Scholar
• Xi XM, Xia SJ, Lu R. Drug loading techniques for exosome-based drug delivery systems. Pharmazie. 2021;76(2):61–67. doi:10.1691/ph.2021.0128
   PubMed Web of Science ®Google Scholar
• Wang F, Zhang W, Li H, Chen X, Feng S, Mei Z. How effective are nano-based dressings in diabetic wound healing? A comprehensive review of literature. Int J Nanomed. 2022;17:2097–2119. doi:10.2147/ijn.S361282
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zhang P, Gao X, Chang L, Chen Z, Mei X. Preparation of exosomes encapsulated nanohydrogel for accelerating wound healing of diabetic rats by promoting angiogenesis. Mater Sci Eng C. 2021;120:111671. doi:10.1016/j.msec.2020.111671
   PubMed Web of Science ®Google Scholar
• Xiong Y, Chen L, Liu P, et al. All-in-one: multifunctional hydrogel accelerates oxidative diabetic wound healing through timed-release of exosome and fibroblast growth factor. Small. 2022;18(1):e2104229. doi:10.1002/smll.202104229
   PubMed Web of Science ®Google Scholar
• Chen J, Zhao Q, Peng J, Yang X, Yu D, Zhao W. Antibacterial and mechanical properties of reduced graphene-silver nanoparticle nanocomposite modified glass ionomer cements. J Dent. 2020;96:103332. doi:10.1016/j.jdent.2020.103332
   PubMed Web of Science ®Google Scholar
• Kong L, Zhao H, Fan J, et al. Predictors of frailty among Chinese community-dwelling older adults with type 2 diabetes: a cross-sectional survey. BMJ Open. 2021;11(3):e041578. doi:10.1136/bmjopen-2020-041578
   PubMed Web of Science ®Google Scholar
• Olsson M, Järbrink K, Divakar U, et al. The humanistic and economic burden of chronic wounds: a systematic review. Wound Repair Regen. 2019;27(1):114–125. doi:10.1111/wrr.12683
   PubMed Web of Science ®Google Scholar
• Chen Z, Jin M, He H, et al. Mesenchymal stem cells and macrophages and their interactions in tendon-bone healing. J Orthop Transl. 2023;39:63–73. doi:10.1016/j.jot.2022.12.005
   PubMed Web of Science ®Google Scholar
• He Y, Li Q, Feng F, et al. Extracellular vesicles produced by human-induced pluripotent stem cell-derived endothelial cells can prevent arterial stenosis in mice via autophagy regulation. Front Cardiovasc Med. 2022;9:922790. doi:10.3389/fcvm.2022.922790
   PubMed Web of Science ®Google Scholar
• Xiong M, Zhang Q, Hu W, et al. Exosomes from adipose-derived stem cells: the emerging roles and applications in tissue regeneration of plastic and cosmetic surgery. Front Cell Dev Biol. 2020;8:574223. doi:10.3389/fcell.2020.574223
   PubMed Web of Science ®Google Scholar
• Ha DH, Kim HK, Lee J, et al. Mesenchymal Stem/Stromal Cell-Derived Exosomes for Immunomodulatory Therapeutics and Skin Regeneration. Cells. 2020;9(5):1.
   Web of Science ®Google Scholar
• Lopez-Verrilli MA, Caviedes A, Cabrera A, Sandoval S, Wyneken U, Khoury M. Mesenchymal stem cell-derived exosomes from different sources selectively promote neuritic outgrowth. Neuroscience. 2016;320:129–139. doi:10.1016/j.neuroscience.2016.01.061
   PubMed Web of Science ®Google Scholar
• Wang ZG, He ZY, Liang S, Yang Q, Cheng P, Chen AM. Comprehensive proteomic analysis of exosomes derived from human bone marrow, adipose tissue, and umbilical cord mesenchymal stem cells. Stem Cell Res Ther. 2020;11(1):511. doi:10.1186/s13287-020-02032-8
   PubMed Web of Science ®Google Scholar
• Dash M, Palaniyandi K, Ramalingam S, Sahabudeen S, Raja NS. Exosomes isolated from two different cell lines using three different isolation techniques show variation in physical and molecular characteristics. Biochim Biophys Acta Biomembr. 2021;1863(2):183490. doi:10.1016/j.bbamem.2020.183490
   PubMed Web of Science ®Google Scholar
• Huang LH, Rau CS, Wu SC, et al. Identification and characterization of hADSC-derived exosome proteins from different isolation methods. J Cell Mol Med. 2021;25(15):7436–7450. doi:10.1111/jcmm.16775
   PubMed Web of Science ®Google Scholar
• Smith ZJ, Lee C, Rojalin T, et al. Single exosome study reveals subpopulations distributed among cell lines with variability related to membrane content. J Extracell Vesicles. 2015;4:28533. doi:10.3402/jev.v4.28533
   PubMed Web of Science ®Google Scholar
• Tschuschke M, Kocherova I, Bryja A, et al. Inclusion biogenesis, methods of isolation and clinical application of human cellular exosomes. J Clin Med. 2020;9(2). doi:10.3390/jcm9020436
   PubMed Web of Science ®Google Scholar
• Zhao R, Chen X, Song H, Bie Q, Zhang B. Dual role of MSC-derived exosomes in tumor development. Stem Cells Int. 2020;2020:8844730. doi:10.1155/2020/8844730
   PubMed Web of Science ®Google Scholar
• Schara K, Štukelj R, Krek JL, et al. A study of extracellular vesicle concentration in active diabetic Charcot neuroarthropathy. Eur J Pharm Sci. 2017;98:58–63. doi:10.1016/j.ejps.2016.09.009
   PubMed Web of Science ®Google Scholar
• Dardari D. An overview of Charcot’s neuroarthropathy. J Clin Transll Endocrinol. 2020;22:100239. doi:10.1016/j.jcte.2020.100239
   PubMedGoogle Scholar