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ORIGINAL RESEARCH

Preparation of Apoptotic Extracellular Vesicles from Adipose Tissue and Their Efficacy in Promoting High-Quality Skin Wound Healing

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Pages 2923-2938 | Received 22 Mar 2023, Accepted 30 May 2023, Published online: 02 Jun 2023

References

  • Rodrigues M, Kosaric N, Bonham C, Gurtner G. Wound healing: a cellular perspective. Physiol Rev. 2019;99(1):665–706. doi:10.1152/physrev.00067.2017
  • Nosrati H, Khodaei M, Alizadeh Z, Banitalebi-Dehkordi M. Cationic, anionic and neutral polysaccharides for skin tissue engineering and wound healing applications. Int J Biol Macromol. 2021;192:298–322. doi:10.1016/j.ijbiomac.2021.10.013
  • Dong J, Wu B, Tian W. How to maximize the therapeutic effect of exosomes on skin wounds in diabetes mellitus: review and discussion. Front Endocrinol. 2023;14:1146991. doi:10.3389/fendo.2023.1146991
  • Zhang Z, Shao M, Hepler C, et al. Dermal adipose tissue has high plasticity and undergoes reversible dedifferentiation in mice. J Clin Invest. 2019;129(12):5327–5342. doi:10.1172/JCI130239
  • Liu S, Jiang L, Li H, et al. Mesenchymal stem cells prevent hypertrophic scar formation via inflammatory regulation when undergoing apoptosis. J Invest Dermatol. 2014;134(10):2648–2657. doi:10.1038/jid.2014.169
  • Galleu A, Riffo-Vasquez Y, Trento C, et al. Apoptosis in mesenchymal stromal cells induces in vivo recipient-mediated immunomodulation. Sci Transl Med. 2017;9(416). doi:10.1126/scitranslmed.aam7828
  • Fu Y, Sui B, Xiang L, et al. Emerging understanding of apoptosis in mediating mesenchymal stem cell therapy. Cell Death Dis. 2021;12(6):596. doi:10.1038/s41419-021-03883-6
  • Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26(4):239–257. doi:10.1038/bjc.1972.33
  • Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007;35(4):495–516. doi:10.1080/01926230701320337
  • Atkin-Smith GK, Tixeira R, Paone S, et al. A novel mechanism of generating extracellular vesicles during apoptosis via a beads-on-a-string membrane structure. Nat Commun. 2015;6:7439. doi:10.1038/ncomms8439
  • Ye Q, Xu H, Liu S, et al. Apoptotic extracellular vesicles alleviate Pg-LPS induced inflammation of macrophages via AMPK/SIRT1/NF-κB pathway and inhibit adjacent osteoclast formation. J Periodontol. 2022;93:1738–1751. doi:10.1002/JPER.21-0657
  • Li M, Xing X, Huang H, et al. BMSC-Derived ApoEVs promote craniofacial bone repair via ROS/JNK signaling. J Dent Res. 2022;101(6):714–723. doi:10.1177/00220345211068338
  • Ou Q, Tan L, Shao Y, et al. Electrostatic charge-mediated apoptotic vesicle biodistribution attenuates sepsis by switching neutrophil NETosis to apoptosis. Small. 2022;18(20):e2200306. doi:10.1002/smll.202200306
  • Zhang X, Tang J, Kou X, et al. Proteomic analysis of MSC‐derived apoptotic vesicles identifies Fas inheritance to ameliorate haemophilia a via activating platelet functions. J Extracelr Ves. 2022;11(7). doi:10.1002/jev2.12240
  • Ma L, Chen C, Liu D, et al. Apoptotic extracellular vesicles are metabolized regulators nurturing the skin and hair. Bio Mat. 2023;19:626–641. doi:10.1016/j.bioactmat.2022.04.022
  • Wang J, Cao Z, Wang P, et al. Apoptotic extracellular vesicles ameliorate multiple myeloma by restoring fas-mediated apoptosis. ACS nano. 2021;15(9):14360–14372. doi:10.1021/acsnano.1c03517
  • Zheng C, Sui B, Zhang X, et al. Apoptotic vesicles restore liver macrophage homeostasis to counteract type 2 diabetes. J Extracel Ves. 2021;10(7):e12109. doi:10.1002/jev2.12109
  • Qu Y, He Y, Meng B, et al. Apoptotic vesicles inherit SOX2 from pluripotent stem cells to accelerate wound healing by energizing mesenchymal stem cells. Acta Biomater. 2022;149:258–272. doi:10.1016/j.actbio.2022.07.009
  • Li Z, Wu M, Liu S, et al. Apoptotic vesicles activate autophagy in recipient cells to induce angiogenesis and dental pulp regeneration. Mol Ther. 2022;30:3193–3208. doi:10.1016/j.ymthe.2022.05.006
  • Rahimipour S, Salahinejad E, Sharifi E, Nosrati H, Tayebi L. Structure, wettability, corrosion and biocompatibility of nitinol treated by alkaline hydrothermal and hydrophobic functionalization for cardiovascular applications. Appl Surf Sci. 2020;506:144657. doi:10.1016/j.apsusc.2019.144657
  • Merrick D, Seale P. Skinny fat cells stimulate wound healing. Cell Stem Cell. 2020;26(6):801–803. doi:10.1016/j.stem.2020.04.021
  • Guerrero-Juarez C, Plikus M. Emerging nonmetabolic functions of skin fat. Nat Rev Endocrinol. 2018;14(3):163–173. doi:10.1038/nrendo.2017.162
  • Fredman R, Katz AJ, Hultman CS. Fat grafting for burn, traumatic, and surgical scars. Clin Plast Surg. 2017;44(4):781–791. doi:10.1016/j.cps.2017.05.009
  • Jan SN, Bashir MM, Khan FA, et al. Unfiltered nanofat injections rejuvenate postburn scars of face. Ann Plast Surg. 2019;82(1):28–33. doi:10.1097/SAP.0000000000001631
  • Giudice G, Filoni A, Maggio G, et al. Use of the stromal vascular fraction in intermediate-deep acute burns: a case with its own control. J Burn Care Res. 2018;39(5):846–849. doi:10.1093/jbcr/irx017
  • Karakol P, Bozkurt M, Gelbal C, Tuglu MI. Efficacy of stromal vascular fraction and enzyme-free mechanical isolation therapy in experimental full thickness burn wounds. J Plast Surg Hand Surg. 2021;2021:1–17.
  • Muhammad G, Xu J, Bulte JWM, Jablonska A, Walczak P, Janowski M. Transplanted adipose-derived stem cells can be short-lived yet accelerate healing of acid-burn skin wounds: a multimodal imaging study. Sci Rep. 2017;7(1):4644. doi:10.1038/s41598-017-04484-0
  • Dong J, Wu B, Tian W. Adipose tissue-derived small extracellular vesicles modulate macrophages to improve the homing of adipocyte precursors and endothelial cells in adipose tissue regeneration. Front Cell Dev Biol. 2022;10:1075233. doi:10.3389/fcell.2022.1075233
  • Li Y, Zhang J, Shi J, et al. Exosomes derived from human adipose mesenchymal stem cells attenuate hypertrophic scar fibrosis by miR-192-5p/IL-17RA/Smad axis. Stem Cell Res Ther. 2021;12(1):221. doi:10.1186/s13287-021-02290-0
  • 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
  • Qian L, Pi L, Fang B, Meng X. Adipose mesenchymal stem cell-derived exosomes accelerate skin wound healing via the lncRNA H19/miR-19b/SOX9 axis. Lab Invest. 2021;101(9):1254–1266.
  • Dong J, Wu Y, Zhang Y, Yu M, Tian W. Comparison of the therapeutic effect of allogeneic and xenogeneic small extracellular vesicles in soft tissue repair. Int J Nanomedicine. 2020;15:6975–6991. doi:10.2147/IJN.S269069
  • Liu D, Kou X, Chen C, et al. Circulating apoptotic bodies maintain mesenchymal stem cell homeostasis and ameliorate osteopenia via transferring multiple cellular factors. Cell Res. 2018;28(9):918–933. doi:10.1038/s41422-018-0070-2
  • Liu H, Liu S, Qiu X, et al. Donor MSCs release apoptotic bodies to improve myocardial infarction via autophagy regulation in recipient cells. Autophagy. 2020;16(12):2140–2155.
  • Liu J, Qiu X, Lv Y, et al. Apoptotic bodies derived from mesenchymal stem cells promote cutaneous wound healing via regulating the functions of macrophages. Stem Cell Res Ther. 2020;11(1):507. doi:10.1186/s13287-020-02014-w
  • Omura S, Iwai Y, Hirano A, et al. A new alkaloid AM-2282 OF Streptomyces origin. Taxonomy, fermentation, isolation and preliminary characterization. J Antibiot. 1977;30(4):275–282. doi:10.7164/antibiotics.30.275
  • Brock CK, Wallin ST, Ruiz OE, et al. Stem cell proliferation is induced by apoptotic bodies from dying cells during epithelial tissue maintenance. Nat Commun. 2019;10(1):1044. doi:10.1038/s41467-019-09010-6
  • Xin L, Wei C, Tong X, et al. In situ delivery of apoptotic bodies derived from mesenchymal stem cells via a hyaluronic acid hydrogel: a therapy for intrauterine adhesions. Bio Mat. 2022;12:107–119. doi:10.1016/j.bioactmat.2021.10.025
  • Le TM, Morimoto N, Ly NT, et al. Ex vivo induction of apoptotic mesenchymal stem cell by high hydrostatic pressure. Stem Cell Rev Rep. 2021;17(2):662–672. doi:10.1007/s12015-020-10071-0
  • 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.
  • 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. Materials Today Bio. 2022;16:100365. doi:10.1016/j.mtbio.2022.100365
  • Wang C, Liang C, Wang R, et al. The fabrication of a highly efficient self-healing hydrogel from natural biopolymers loaded with exosomes for the synergistic promotion of severe wound healing. Biomaterials sci. 2019;8(1):313–324. doi:10.1039/C9BM01207A
  • Geng X, Qi Y, Liu X, Shi Y, Li H, Zhao L. A multifunctional antibacterial and self-healing hydrogel laden with bone marrow mesenchymal stem cell-derived exosomes for accelerating diabetic wound healing. Bio Adv. 2022;133:112613. doi:10.1016/j.msec.2021.112613
  • Driskell R, Lichtenberger B, Hoste E, et al. Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature. 2013;504(7479):277–281. doi:10.1038/nature12783
  • Plikus M, Guerrero-Juarez C, Ito M, et al. Regeneration of fat cells from myofibroblasts during wound healing. Science. 2017;355(6326):748–752. doi:10.1126/science.aai8792
  • Wojciechowicz K, Markiewicz E, Jahoda C. C/EBPalpha identifies differentiating preadipocytes around hair follicles in foetal and neonatal rat and mouse skin. Exp Dermatol. 2008;17(8):675–680. doi:10.1111/j.1600-0625.2007.00689.x
  • Wang F, Mullican S, DiSpirito J, Peed L, Lazar M. Lipoatrophy and severe metabolic disturbance in mice with fat-specific deletion of PPARγ. Proc Natl Acad Sci U S A. 2013;110(46):18656–18661. doi:10.1073/pnas.1314863110
  • Dalirfardouei R, Jamialahmadi K, Jafarian AH, Mahdipour E. Promising effects of exosomes isolated from menstrual blood-derived mesenchymal stem cell on wound-healing process in diabetic mouse model. J Tissue Eng Regen Med. 2019;13(4):555–568. doi:10.1002/term.2799
  • Nosrati H, Aramideh Khouy R, Nosrati A, et al. Nanocomposite scaffolds for accelerating chronic wound healing by enhancing angiogenesis. J Nanobiotechnology. 2021;19(1):1. doi:10.1186/s12951-020-00755-7