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Role of exosome-derived miRNAs in diabetic wound angiogenesis

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Abstract

Chronic wounds with high disability are among the most common and serious complications of diabetes. Angiogenesis dysfunction impair wound healing in patients with diabetes. Compared with traditional therapies that can only provide symptomatic treatment, stem cells—owing to their powerful paracrine properties, can alleviate the pathogenesis of chronic diabetic wounds and even cure them. Exosome-derived microRNAs (miRNAs), important components of stem cell paracrine signaling, have been reported for therapeutic use in various disease models, including diabetic wounds. Exosome-derived miRNAs have been widely reported to be involved in regulating vascular function and have promising applications in the repair and regeneration of skin wounds. Therefore, this article aims to review the current status of the pathophysiology of exosome-derived miRNAs in the diabetes-induced impairment of wound healing, along with current knowledge of the underlying mechanisms, emphasizing the regulatory mechanism of angiogenesis, we hope to document the emerging theoretical basis for improving wound repair by restoring angiogenesis in diabetes.

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Data sharing is not applicable to this article as no new data were created or analyzed in this study.

Abbreviations

ADSC:

Adipose-derived stem cell

AGE:

Advanced glycation end product

AGER:

Advanced glycosylation end product-specific receptor

AGO:

Argonaute

CARD10:

Caspase recruitment domain protein-10

circRNAs:

Circular RNAs

CSE:

Cystathionine γ-lyase

DFU:

Diabetic foot ulcer

DM:

Diabetes mellitus

DNMT:

DNA methyltransferase

EC:

Endothelial cell

ECM:

Extracellular matrix

eNOS:

Endothelial including nitric oxide synthase

EPCs:

Endothelial progenitor cells

ER:

Endoplasmic reticulum

GAPDH:

Glyceraldehyde 3-phosphate dehydrogenase

GATA2:

Globin transcription factor-binding protein 2

HbA1c:

Glycated hemoglobin A1c

HG:

High glucose

HUVEC:

Human umbilical vein endothelial cell

HIF:

Hypoxia-induced factor

IL:

Interleukin

lncRNA:

Long ncRNAs

miRNA:

MicroRNA

MSCs:

Mesenchymal stem cells

MMP:

Matrix metalloproteinase

mRNAs:

Messenger RNAs

NADPH:

Nicotinamide adenine dinucleotide phosphate

ncRNA:

Non-coding RNA

NF-κB:

Nuclear factor kappa-B

NO:

Nitric oxide

piRNAs:

Piwi RNAs

pri-miRNA:

Primary miRNA transcript

ROS:

Reactive oxygen species

RAGE:

Receptor for advanced glycation end product

RISC:

RNA-induced silencing complex

ROCK1:

Rho-associated coiled-coil kinase 1

siRNA:

Small interfering RNA

SIRT1:

Silent information regulator 1

SPRED1:

Sprouty-related EVH1 domain-containing protein1

TGF-β:

Transforming growth factor-beta

TNF-α:

Tumor necrosis factor-alpha

UTRs:

Untranslated regions

VEGF:

Vascular endothelial growth factor

VEGFA:

Vascular endothelial growth factor A

VEGFR:

Vascular endothelial growth factor receptor

VCAM-1:

Vascular endothelial adhesion molecule 1

References

  1. Sorg H, Tilkorn DJ, Hager S, Hauser J, Mirastschijski U (2017) Skin wound healing: an update on the current knowledge and concepts. Eur Surg Res 58(1–2):81–94

    Article  PubMed  Google Scholar 

  2. Badr G (2013) Camel whey protein enhances diabetic wound healing in a streptozotocin-induced diabetic mouse model: the critical role of β-defensin-1, -2 and -3. Lipids Health Dis 12:46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bevan D, Gherardi E, Fan TP, Edwards D, Warn R (2004) Diverse and potent activities of HGF/SF in skin wound repair. J Pathol 203(3):831–838

    Article  CAS  PubMed  Google Scholar 

  4. Sun H, Saeedi P, Karuranga S et al (2022) IDF diabetes atlas: global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract 183:109119

    Article  PubMed  Google Scholar 

  5. Rao MR, Shen XH, Zou X (1987) Calcium antagonistic action of saponins from Panax notoginseng (sanqi-ginseng). J Tradit Chin Med 7(2):127–130

    CAS  PubMed  Google Scholar 

  6. Wang Y, Chen X, Cao W et al (2014) Plasticity of mesenchymal stem cells in immunomodulation: pathological and therapeutic implications. Nat Immunol 15(11):1009–1016. https://doi.org/10.1038/ni.3002

    Article  CAS  PubMed  Google Scholar 

  7. Smalheiser NR (2007) Exosomal transfer of proteins and RNAs at synapses in the nervous system. Biol Direct 2:35

    Article  PubMed  PubMed Central  Google Scholar 

  8. Hade MD, Suire CN, Suo Z (2021) Mesenchymal stem cell-derived exosomes: applications in regenerative medicine. Cells 10(8):1959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Ke X, Yang R, Wu F et al (2021) Exosomal miR-218-5p/miR-363-3p from endothelial progenitor cells ameliorate myocardial infarction by targeting the p53/JMY signaling pathway. Oxid Med Cell Longev 2021:5529430

    Article  PubMed  PubMed Central  Google Scholar 

  10. Lou R, Chen J, Zhou F, Wang C, Leung CH, Lin L (2022) Exosome-cargoed microRNAs: potential therapeutic molecules for diabetic wound healing. Drug Discov Today 27:103323. https://doi.org/10.1016/j.drudis.2022.07.008

    Article  CAS  PubMed  Google Scholar 

  11. Meng Z, Zhou D, Gao Y et al (2018) miRNA delivery for skin wound healing. Adv Drug Deliv Rev 129:308–318. https://doi.org/10.1016/j.addr.2017.12.011

    Article  CAS  PubMed  Google Scholar 

  12. Cooke JP (2019) Inflammation and its role in regeneration and repair. Circ Res 124(8):1166–1168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Singer AJ, Clark RA (1999) Cutaneous wound healing[J]. N Engl J Med 341(10):738–746. https://doi.org/10.1056/NEJM199909023411006

    Article  CAS  PubMed  Google Scholar 

  14. Griffin DR, Archang MM, Kuan CH et al (2021) Activating an adaptive immune response from a hydrogel scaffold imparts regenerative wound healing. Nat Mater 20(4):560–569. https://doi.org/10.1038/s41563-020-00844-w

    Article  CAS  PubMed  Google Scholar 

  15. Zhang Y, Sun X, Icli B et al (2017) Emerging roles for microRNAs in diabetic microvascular disease: novel targets for therapy. Endocr Rev 38(2):145–168. https://doi.org/10.1210/er.2016-1122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Shen YI, Cho H, Papa AE et al (2016) Engineered human vascularized constructs accelerate diabetic wound healing. Biomaterials 102:107–119. https://doi.org/10.1016/j.biomaterials.2016.06.009

    Article  CAS  PubMed  Google Scholar 

  17. Woo K, Ayello EA, Sibbald RG (2007) The edge effect: current therapeutic options to advance the wound edge. Adv Skin Wound Care 20(2):99–117

    Article  PubMed  Google Scholar 

  18. Lyttle BD, Vaughn AE, Bardill JR et al (2023) Effects of microRNAs on angiogenesis in diabetic wounds. Front Med 10:1140979. https://doi.org/10.3389/fmed.2023.1140979

    Article  Google Scholar 

  19. Torre-Blanco A, Adachi E, Hojima Y, Wootton JA, Minor RR, Prockop DJ (1992) Temperature-induced post-translational over-modification of type I procollagen. Effects of over-modification of the protein on the rate of cleavage by procollagen N-proteinase and on self-assembly of collagen into fibrils. J Biol Chem 267(4):2650–2655

    Article  CAS  PubMed  Google Scholar 

  20. Yang CL, Rui H, Mosler S, Notbohm H, Sawaryn A, Müller PK (1993) Collagen II from articular cartilage and annulus fibrosus. Structural and functional implication of tissue specific posttranslational modifications of collagen molecules. Eur J Biochem 213(3):1297–1302

    Article  CAS  PubMed  Google Scholar 

  21. Canty EG, Lu Y, Meadows RS, Shaw MK, Holmes DF, Kadler KE (2004) Coalignment of plasma membrane channels and protrusions (fibripositors) specifies the parallelism of tendon. J Cell Biol 165(4):553–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Khalid M, Petroianu G, Adem A (2022) Advanced glycation end products and diabetes mellitus: mechanisms and perspectives. Biomolecules. https://doi.org/10.3390/biom12040542

    Article  PubMed  PubMed Central  Google Scholar 

  23. Peppa M, Stavroulakis P, Raptis SA (2009) Advanced glycoxidation products and impaired diabetic wound healing. Wound Repair Regen 17(4):461–472

    Article  PubMed  Google Scholar 

  24. Hu H, Han CM, Hu XL, Ye WL, Huang WJ, Smit AJ (2012) Elevated skin autofluorescence is strongly associated with foot ulcers in patients with diabetes: a cross-sectional, observational study of Chinese subjects. J Zhejiang Univ Sci B 13(5):372–377

    Article  PubMed  PubMed Central  Google Scholar 

  25. Feng X, Tonnesen MG, Mousa SA, Clark RA (2013) Fibrin and collagen differentially but synergistically regulate sprout angiogenesis of human dermal microvascular endothelial cells in 3-dimensional matrix. Int J Cell Biol 2013:231279

    Article  PubMed  PubMed Central  Google Scholar 

  26. Yamauchi M, Sricholpech M (2012) Lysine post-translational modifications of collagen. Essays Biochem 52:113–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Avery NC, Bailey AJ (2006) The effects of the Maillard reaction on the physical properties and cell interactions of collagen. Pathol Biol (Paris) 54(7):387–395

    Article  CAS  PubMed  Google Scholar 

  28. Verzijl N, DeGroot J, Thorpe SR et al (2000) Effect of collagen turnover on the accumulation of advanced glycation end products. J Biol Chem 275(50):39027–39031

    Article  CAS  PubMed  Google Scholar 

  29. Liao H, Zakhaleva J, Chen W (2009) Cells and tissue interactions with glycated collagen and their relevance to delayed diabetic wound healing. Biomaterials 30(9):1689–1696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Niu Y, Xie T, Ge K, Lin Y, Lu S (2008) Effects of extracellular matrix glycosylation on proliferation and apoptosis of human dermal fibroblasts via the receptor for advanced glycosylated end products. Am J Dermatopathol 30(4):344–351

    Article  PubMed  Google Scholar 

  31. Khalid M, Alkaabi J, Khan M, Adem A (2021) Insulin signal transduction perturbations in insulin resistance. Int J Mol Sci 22(16):8590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Giacco F, Brownlee M (2010) Oxidative stress and diabetic complications. Circ Res 107(9):1058–1070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Peppa M, Raptis SA (2011) Glycoxidation and wound healing in diabetes: an interesting relationship. Curr Diabetes Rev 7(6):416–425

    Article  CAS  PubMed  Google Scholar 

  34. Vlassara H, Striker GE (2011) AGE restriction in diabetes mellitus: a paradigm shift. Nat Rev Endocrinol 7(9):526–539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Fukui M, Tanaka M, Senmaru T et al (2013) LOX-1 is a novel marker for peripheral artery disease in patients with type 2 diabetes. Metabolism 62(7):935–938

    Article  CAS  PubMed  Google Scholar 

  36. Leguina-Ruzzi A, Pereira J, Pereira-Flores K et al (2015) Increased RhoA/Rho-Kinase activity and markers of endothelial dysfunction in young adult subjects with metabolic syndrome. Metab Syndr Relat Disord 13(9):373–380

    Article  CAS  PubMed  Google Scholar 

  37. Zhang L, Dong L, Liu X et al (2014) α-Melanocyte-stimulating hormone protects retinal vascular endothelial cells from oxidative stress and apoptosis in a rat model of diabetes. PLoS ONE 9(4):e93433

    Article  PubMed  PubMed Central  Google Scholar 

  38. Wang G, Li W, Chen Q, Jiang Y, Lu X, Zhao X (2015) Hydrogen sulfide accelerates wound healing in diabetic rats. Int J Clin Exp Pathol 8(5):5097–5104

    PubMed  PubMed Central  Google Scholar 

  39. Pavkov ME, Weil EJ, Fufaa GD et al (2016) Tumor necrosis factor receptors 1 and 2 are associated with early glomerular lesions in type 2 diabetes. Kidney Int 89(1):226–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Portillo JA, Greene JA, Okenka G et al (2014) CD40 promotes the development of early diabetic retinopathy in mice. Diabetologia 57(10):2222–2231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Portillo JA, Schwartz I, Zarini S et al (2014) Proinflammatory responses induced by CD40 in retinal endothelial and Müller cells are inhibited by blocking CD40-Traf 2,3 or CD40-Traf6 signaling. Invest Ophthalmol Vis Sci 55(12):8590–8597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Abu El-Asrar AM, De Hertogh G, Nawaz MI et al (2015) The tumor necrosis factor superfamily members TWEAK, TNFSF15 and fibroblast growth factor-inducible protein 14 are upregulated in proliferative diabetic retinopathy. Ophthalmic Res 53(3):122–130

    Article  CAS  PubMed  Google Scholar 

  43. Du X, Matsumura T, Edelstein D et al (2003) Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells. J Clin Invest 112(7):1049–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Apte RS, Chen DS, Ferrara N (2019) VEGF in signaling and disease: beyond discovery and development. Cell 176(6):1248–1264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Arrigo A, Aragona E, Bandello F (2022) VEGF-targeting drugs for the treatment of retinal neovascularization in diabetic retinopathy. Ann Med 54(1):1089–1111. https://doi.org/10.1080/07853890.2022.2064541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Rodrigues M, Xin X, Jee K et al (2013) VEGF secreted by hypoxic Müller cells induces MMP-2 expression and activity in endothelial cells to promote retinal neovascularization in proliferative diabetic retinopathy. Diabetes 62(11):3863–3873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Jiang F, Chen Q, Huang L et al (2016) TNFSF15 inhibits blood retinal barrier breakdown induced by diabetes. Int J Mol Sci 17(5):615

    Article  PubMed  PubMed Central  Google Scholar 

  48. Costa R, Negrão R, Valente I et al (2013) Xanthohumol modulates inflammation, oxidative stress, and angiogenesis in type 1 diabetic rat skin wound healing. J Nat Prod 76(11):2047–2053

    Article  CAS  PubMed  Google Scholar 

  49. Li X, Gan K, Song G, Wang C (2015) VEGF gene transfected umbilical cord mesenchymal stem cells transplantation improve the lower limb vascular lesions of diabetic rats. J Diabetes Complications 29(7):872–881

    Article  PubMed  Google Scholar 

  50. Semenza GL (2003) Angiogenesis in ischemic and neoplastic disorders. Annu Rev Med 54:17–28

    Article  CAS  PubMed  Google Scholar 

  51. Zhong X, Liao Y, Chen L et al (2015) The MicroRNAs in the Pathogenesis of Metabolic Memory. Endocrinology 156(9):3157–3168. https://doi.org/10.1210/en.2015-1063

    Article  CAS  PubMed  Google Scholar 

  52. Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414(6865):813–820

    Article  CAS  PubMed  Google Scholar 

  53. Dubey R, Prabhakar PK, Gupta J (2022) Epigenetics: key to improve delayed wound healing in type 2 diabetes. Mol Cell Biochem 477:371–383. https://doi.org/10.1007/s11010-021-04285-0

    Article  CAS  PubMed  Google Scholar 

  54. Reddy MA, Zhang E, Natarajan R (2015) Epigenetic mechanisms in diabetic complications and metabolic memory. Diabetologia 58(3):443–455. https://doi.org/10.1007/s00125-014-3462-y

    Article  CAS  PubMed  Google Scholar 

  55. Gonçalves S, Yin K, Ito Y et al (2021) COX2 regulates senescence secretome composition and senescence surveillance through PGE2. Cell Rep 34(11):108860. https://doi.org/10.1016/j.celrep.2021.108860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Li D, Zhang L, He Y et al (2022) Novel histone post-translational modifications in diabetes and complications of diabetes: the underlying mechanisms and implications. Biomed Pharmacother 156:113984. https://doi.org/10.1016/j.biopha.2022.113984

    Article  CAS  PubMed  Google Scholar 

  57. Toma C, Wagner WR, Bowry S, Schwartz A, Villanueva F (2009) Fate of culture-expanded mesenchymal stem cells in the microvasculature: in vivo observations of cell kinetics. Circ Res 104(3):398–402

    Article  CAS  PubMed  Google Scholar 

  58. Ratajczak MZ, Kucia M, Jadczyk T et al (2012) Pivotal role of paracrine effects in stem cell therapies in regenerative medicine: can we translate stem cell-secreted paracrine factors and microvesicles into better therapeutic strategies. Leukemia 26(6):1166–1173

    Article  CAS  PubMed  Google Scholar 

  59. Denzer K, Kleijmeer MJ, Heijnen HF, Stoorvogel W, Geuze HJ (2000) Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 113(Pt 19):3365–3374

    Article  CAS  PubMed  Google Scholar 

  60. Keller S, Ridinger J, Rupp AK, Janssen JW, Altevogt P (2011) Body fluid derived exosomes as a novel template for clinical diagnostics. J Transl Med 9:86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Ghafouri-Fard S, Shoorei H, Mohaqiq M et al (2020) Non-coding RNAs regulate angiogenic processes. Vascul Pharmacol 133–134:106778. https://doi.org/10.1016/j.vph.2020.106778

    Article  CAS  PubMed  Google Scholar 

  62. Mattick JS, Makunin IV (2006) Non-coding RNA. Hum Mol Genet 15:R17-29

    Article  CAS  PubMed  Google Scholar 

  63. Sousa-Franco A, Rebelo K, da Rocha ST (2019) LncRNAs regulating stemness in aging. Aging Cell 18(1):e12870

    Article  PubMed  Google Scholar 

  64. Matsui M, Corey DR (2017) Non-coding RNAs as drug targets. Nat Rev Drug Discov 16(3):167–179

    Article  CAS  PubMed  Google Scholar 

  65. Sampath D, Liu C, Vasan K et al (2012) Histone deacetylases mediate the silencing of miR-15a, miR-16, and miR-29b in chronic lymphocytic leukemia. Blood 119(5):1162–1172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19(1):92–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Li XH, Gong QM, Ling Y et al (2014) Inherent lipid metabolic dysfunction in glycogen storage disease IIIa. Biochem Biophys Res Commun 455(1–2):90–97

    Article  CAS  PubMed  Google Scholar 

  68. Moutinho C, Esteller M (2017) MicroRNAs and Epigenetics[J]. Adv Cancer Res 135:189–220. https://doi.org/10.1016/bs.acr.2017.06.003

    Article  CAS  PubMed  Google Scholar 

  69. Lee Y, Kim M, Han J et al (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23(20):4051–4060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ (2004) Processing of primary microRNAs by the Microprocessor complex. Nature 432:231–235. https://doi.org/10.1038/nature03049

    Article  CAS  PubMed  Google Scholar 

  71. Bohnsack MT, Czaplinski K, Gorlich D (2004) Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 10(2):185–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6(5):376–385

    Article  CAS  PubMed  Google Scholar 

  73. Borchert GM, Lanier W, Davidson BL (2006) RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 13(12):1097–1101

    Article  CAS  PubMed  Google Scholar 

  74. Iqbal MA, Arora S, Prakasam G, Calin GA, Syed MA (2019) MicroRNA in lung cancer: role, mechanisms, pathways and therapeutic relevance. Mol Aspects Med 70:3–20

    Article  CAS  PubMed  Google Scholar 

  75. Maeyama M, Matuoka H, Tuchida Y, Hashimoto Y (1970) Metabolism of neutral steroids in the human fetus. II. Metabolism of progesterone and pregnenolone in anencephalic monsters after delivery. Steroids 15(1):167–80

    Article  CAS  PubMed  Google Scholar 

  76. Lino MM, Simões S, Vilaça A et al (2018) Modulation of angiogenic activity by light-activatable miRNA-loaded nanocarriers. ACS Nano 12(6):5207–5220. https://doi.org/10.1021/acsnano.7b07538

    Article  CAS  PubMed  Google Scholar 

  77. Sun Z, Shi K, Yang S et al (2018) Effect of exosomal miRNA on cancer biology and clinical applications. Mol Cancer 17(1):147. https://doi.org/10.1186/s12943-018-0897-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Kir D, Schnettler E, Modi S et al (2018) Regulation of angiogenesis by microRNAs in cardiovascular diseases. Angiogenesis 21(4):699–710. https://doi.org/10.1007/s10456-018-9632-7

    Article  CAS  PubMed  Google Scholar 

  79. Zampetaki A, Kiechl S, Drozdov I et al (2010) Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res 107:810–817. https://doi.org/10.1161/CIRCRESAHA.110.226357

    Article  CAS  PubMed  Google Scholar 

  80. Dangwal S, Stratmann B, Bang C et al (2015) Impairment of wound healing in patients With Type 2 diabetes mellitus influences circulating microRNA patterns via inflammatory cytokines. Arterioscler Thromb Vasc Biol 35(6):1480–1488

    Article  CAS  PubMed  Google Scholar 

  81. Sun X, Lin J, Zhang Y et al (2016) MicroRNA-181b improves glucose homeostasis and insulin sensitivity by regulating endothelial function in white adipose tissue. Circ Res 118:810–821. https://doi.org/10.1161/CIRCRESAHA.115.308166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Xiong Y, Chen L, Yu T et al (2020) Inhibition of circulating exosomal microRNA-15a-3p accelerates diabetic wound repair. Aging 12(10):8968–8986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Xiao S, Zhang D, Liu Z et al (2020) Diabetes-induced glucolipotoxicity impairs wound healing ability of adipose-derived stem cells-through the miR-1248/CITED2/HIF-1α pathway. Aging 12(8):6947–6965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Baldeón RL, Weigelt K, de Wit H et al (2014) Decreased serum level of miR-146a as sign of chronic inflammation in type 2 diabetic patients. PLoS ONE 9:e115209. https://doi.org/10.1371/journal.pone.0115209

    Article  CAS  Google Scholar 

  85. Feng B, Chen S, McArthur K et al (2011) miR-146a-Mediated extracellular matrix protein production in chronic diabetes complications. Diabetes 60:2975–2984. https://doi.org/10.2337/db11-0478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Liu J, Wang J, Fu W et al (2021) MiR-195–5p and miR-205–5p in extracellular vesicles isolated from diabetic foot ulcer wound fluid decrease angiogenesis by inhibiting VEGFA expression. Aging 13:19805–19821. https://doi.org/10.18632/aging.203393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Tang W, Guo J, Gu R et al (2020) MicroRNA-29b-3p inhibits cell proliferation and angiogenesis by targeting VEGFA and PDGFB in retinal microvascular endothelial cells. Mol Vis 26:64–75

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Wang H, Wang X, Liu X et al (2022) miR-199a-5p plays a pivotal role on wound healing via suppressing VEGFA and ROCK1 in diabetic ulcer foot. Oxid Med Cell Longev 2022:4791059. https://doi.org/10.1155/2022/4791059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Lin CJ, Lan YM, Ou MQ, Ji LQ, Lin SD (2019) Expression of miR-217 and HIF-1α/VEGF pathway in patients with diabetic foot ulcer and its effect on angiogenesis of diabetic foot ulcer rats. J Endocrinol Invest 42:1307–1317. https://doi.org/10.1007/s40618-019-01053-2

    Article  CAS  PubMed  Google Scholar 

  90. Kujawa M, O’Meara M, Li H et al (2022) MicroRNA-466 and microRNA-200 increase endothelial permeability in hyperglycemia by targeting Claudin-5. Mol Ther Nucleic Acids 29:259–271. https://doi.org/10.1016/j.omtn.2022.07.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Chan YC, Roy S, Khanna S, Sen CK (2012) Downregulation of endothelial microRNA-200b supports cutaneous wound angiogenesis by desilencing GATA binding protein 2 and vascular endothelial growth factor receptor 2. Arterioscler Thromb Vasc Biol 32:1372–1382. https://doi.org/10.1161/ATVBAHA.112.248583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Xiao X, Xu M, Yu H et al (2021) Mesenchymal stem cell-derived small extracellular vesicles mitigate oxidative stress-induced senescence in endothelial cells via regulation of miR-146a/Src. Signal Transduct Target Ther 6:354. https://doi.org/10.1038/s41392-021-00765-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Mortuza R, Feng B, Chakrabarti S (2014) miR-195 regulates SIRT1-mediated changes in diabetic retinopathy. Diabetologia 57:1037–1046. https://doi.org/10.1007/s00125-014-3197-9

    Article  CAS  PubMed  Google Scholar 

  94. Zheng D, Ma J, Yu Y et al (2015) Silencing of miR-195 reduces diabetic cardiomyopathy in C57BL/6 mice. Diabetologia 58:1949–1958. https://doi.org/10.1007/s00125-015-3622-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Menghini R, Casagrande V, Cardellini M et al (2009) MicroRNA 217 modulates endothelial cell senescence via silent information regulator 1. Circulation 120:1524–1532. https://doi.org/10.1161/CIRCULATIONAHA.109.864629

    Article  CAS  PubMed  Google Scholar 

  96. Mocharla P, Briand S, Giannotti G et al (2013) AngiomiR-126 expression and secretion from circulating CD34(+) and CD14(+) PBMCs: role for proangiogenic effects and alterations in type 2 diabetics. Blood 121:226–236. https://doi.org/10.1182/blood-2012-01-407106

    Article  CAS  PubMed  Google Scholar 

  97. Witkowski M, Weithauser A, Tabaraie T et al (2016) Micro-RNA-126 reduces the blood thrombogenicity in diabetes mellitus via targeting of tissue factor. Arterioscler Thromb Vasc Biol 36:1263–1271. https://doi.org/10.1161/ATVBAHA.115.306094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Zhang D, Li Z, Wang Z, Zeng F, Xiao W, Yu A (2019) MicroRNA-126: a promising biomarker for angiogenesis of diabetic wounds treated with negative pressure wound therapy. Diabetes Metab Syndr Obes 12:1685–1696. https://doi.org/10.2147/DMSO.S199705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Harris TA, Yamakuchi M, Ferlito M, Mendell JT, Lowenstein CJ (2008) MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci U S A 105:1516–1521. https://doi.org/10.1073/pnas.0707493105

    Article  PubMed  PubMed Central  Google Scholar 

  100. Xue WL, Chen RQ, Zhang QQ et al (2020) Hydrogen sulfide rescues high glucose-induced migration dysfunction in HUVECs by upregulating miR-126–3p. Am J Physiol Cell Physiol 318:C857-857C869. https://doi.org/10.1152/ajpcell.00406.2019

    Article  CAS  PubMed  Google Scholar 

  101. Wang HJ, Huang YL, Shih YY, Wu HY, Peng CT, Lo WY (2014) MicroRNA-146a decreases high glucose/thrombin-induced endothelial inflammation by inhibiting NAPDH oxidase 4 expression. Mediators Inflamm 2014:379537. https://doi.org/10.1155/2014/379537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Fulzele S, El-Sherbini A, Ahmad S et al (2015) MicroRNA-146b-3p regulates retinal inflammation by suppressing adenosine deaminase-2 in diabetes. Biomed Res Int 2015:846501. https://doi.org/10.1155/2015/846501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Cowan C, Muraleedharan CK, O’Donnell JJ 3rd et al (2014) MicroRNA-146 inhibits thrombin-induced NF-κB activation and subsequent inflammatory responses in human retinal endothelial cells[J]. Invest Ophthalmol Vis Sci 55(8):4944–4951. https://doi.org/10.1167/iovs.13-13631

    Article  CAS  PubMed  Google Scholar 

  104. Poe AJ, Shah R, Khare D et al (2022) Regulatory role of miR-146a in corneal epithelial wound healing via its inflammatory targets in human diabetic cornea. Ocul Surf 25:92–100. https://doi.org/10.1016/j.jtos.2022.06.001

    Article  PubMed  PubMed Central  Google Scholar 

  105. Yu HY, Meng LF, Lu XH, Liu LH, Ci X, Zhuo Z (2020) Protective effect of miR-146 against kidney injury in diabetic nephropathy rats through mediating the NF-κB signaling pathway. Eur Rev Med Pharmacol Sci 24:3215–3222. https://doi.org/10.26355/eurrev_202003_20688

    Article  PubMed  Google Scholar 

  106. Li B, Zhou Y, Chen J et al (2021) Long noncoding RNA H19 acts as a miR-29b sponge to promote wound healing in diabetic foot ulcer. FASEB J 35(1):e20526

    Article  CAS  PubMed  Google Scholar 

  107. Xue W, Zhang Q, Chen Y, Zhu Y (2022) Hydrogen sulfide improves angiogenesis by regulating the transcription of pri-miR-126 in diabetic endothelial cells. Cells. https://doi.org/10.3390/cells11172651

    Article  PubMed  PubMed Central  Google Scholar 

  108. Tao SC, Guo SC, Li M et al (2017) 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(3):736–747

    Article  CAS  PubMed  Google Scholar 

  109. Dewberry LC, Niemiec SM, Hilton SA et al (2022) Cerium oxide nanoparticle conjugation to microRNA-146a mechanism of correction for impaired diabetic wound healing. Nanomedicine 40:102483. https://doi.org/10.1016/j.nano.2021.102483

    Article  CAS  PubMed  Google Scholar 

  110. Sener G, Hilton SA, Osmond MJ et al (2020) Injectable, self-healable zwitterionic cryogels with sustained microRNA - cerium oxide nanoparticle release promote accelerated wound healing. Acta Biomater 101:262–272. https://doi.org/10.1016/j.actbio.2019.11.014

    Article  CAS  PubMed  Google Scholar 

  111. Yang M, Li R, Wang X, Liu X, Zhang B, Wang Y (2021) Preparation, characterization and wound healing effect of alginate/chitosan microcapsules loaded with polysaccharides from nostoc commune vaucher. Biomed Mater 16:025015. https://doi.org/10.1088/1748-605X/abd051

    Article  CAS  PubMed  Google Scholar 

  112. Li Q, Zhao H, Chen W, Huang P, Bi J (2019) Human keratinocyte-derived microvesicle miRNA-21 promotes skin wound healing in diabetic rats through facilitating fibroblast function and angiogenesis. Int J Biochem Cell Biol 114:105570. https://doi.org/10.1016/j.biocel.2019.105570

    Article  CAS  PubMed  Google Scholar 

  113. Wu D, Kang L, Tian J et al (2020) Exosomes derived from bone mesenchymal stem cells with the stimulation of Fe(3)O(4) nanoparticles and static magnetic field enhance wound healing through upregulated miR-21-5p. Int J Nanomedicine 15:7979–7993. https://doi.org/10.2147/IJN.S275650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Wei P, Zhong C, Yang X et al (2020) Exosomes derived from human amniotic epithelial cells accelerate diabetic wound healing via PI3K-AKT-mTOR-mediated promotion in angiogenesis and fibroblast function. Burns Trauma 8:tkaa020. https://doi.org/10.1093/burnst/tkaa020

    Article  PubMed  PubMed Central  Google Scholar 

  115. Huang C, Luo W, Wang Q et al (2021) Human mesenchymal stem cells promote ischemic repairment and angiogenesis of diabetic foot through exosome miRNA-21-5p. Stem Cell Res 52:102235

    Article  CAS  PubMed  Google Scholar 

  116. Fernandes H, Zonnari A, Abreu R et al (2022) Extracellular vesicles enriched with an endothelial cell pro-survival microRNA affects skin tissue regeneration. Mol Ther Nucleic Acids 28:307–327. https://doi.org/10.1016/j.omtn.2022.03.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Yu M, Liu W, Li J et al (2020) Exosomes derived from atorvastatin-pretreated MSC accelerate diabetic wound repair by enhancing angiogenesis via AKT/eNOS pathway. Stem Cell Res Ther 11(1):350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Zhong H, Qian J, Xiao Z et al (2021) MicroRNA-133b inhibition restores EGFR expression and accelerates diabetes-impaired wound healing. Oxid Med Cell Longev 2021:9306760. https://doi.org/10.1155/2021/9306760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Wang JM, Tao J, Chen DD et al (2014) MicroRNA miR-27b rescues bone marrow-derived angiogenic cell function and accelerates wound healing in type 2 diabetes mellitus. Arterioscler Thromb Vasc Biol 34:99–109. https://doi.org/10.1161/ATVBAHA.113.302104

    Article  CAS  PubMed  Google Scholar 

  120. Sakshi S, Jayasuriya R, Sathish Kumar RC et al (2023) MicroRNA-27b impairs Nrf2-mediated angiogenesis in the progression of diabetic foot ulcer. J Clin Med. https://doi.org/10.3390/jcm12134551

    Article  PubMed  PubMed Central  Google Scholar 

  121. Lu Y, Wen H, Huang J et al (2020) Extracellular vesicle-enclosed miR-486-5p mediates wound healing with adipose-derived stem cells by promoting angiogenesis. J Cell Mol Med 24:9590–9604. https://doi.org/10.1111/jcmm.15387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Cai HA, Huang L, Zheng LJ et al (2019) Ginsenoside (Rg-1) promoted the wound closure of diabetic foot ulcer through iNOS elevation via miR-23a/IRF-1 axis. Life Sci 233:116525. https://doi.org/10.1016/j.lfs.2019.05.081

    Article  CAS  PubMed  Google Scholar 

  123. Zhang J, Cai W, Fan Z et al (2019) MicroRNA-24 inhibits the oxidative stress induced by vascular injury by activating the Nrf2/Ho-1 signaling pathway. Atherosclerosis 290:9–18. https://doi.org/10.1016/j.atherosclerosis.2019.08.023

    Article  CAS  PubMed  Google Scholar 

  124. Cai W, Zhang J, Yang J et al (2019) MicroRNA-24 attenuates vascular remodeling in diabetic rats through PI3K/Akt signaling pathway. Nutr Metab Cardiovasc Dis 29:621–632. https://doi.org/10.1016/j.numecd.2019.03.002

    Article  CAS  PubMed  Google Scholar 

  125. Yan C, Chen J, Wang C et al (2022) Milk exosomes-mediated miR-31-5p delivery accelerates diabetic wound healing through promoting angiogenesis. Drug Deliv 29:214–228. https://doi.org/10.1080/10717544.2021.2023699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Cheng HS, Pérez-Cremades D, Zhuang R et al (2023) Impaired angiogenesis in diabetic critical limb ischemia is mediated by a miR-130b/INHBA signaling axis. JCI Insight. https://doi.org/10.1172/jci.insight.163041

    Article  PubMed  PubMed Central  Google Scholar 

  127. Ge L, Wang K, Lin H et al (2023) Engineered exosomes derived from miR-132-overexpresssing adipose stem cells promoted diabetic wound healing and skin reconstruction. Front Bioeng Biotechnol 11:1129538. https://doi.org/10.3389/fbioe.2023.1129538

    Article  PubMed  PubMed Central  Google Scholar 

  128. McCoy MG, Jamaiyar A, Sausen G et al (2023) MicroRNA-375 repression of Kruppel-like factor 5 improves angiogenesis in diabetic critical limb ischemia. Angiogenesis 26:107–127. https://doi.org/10.1007/s10456-022-09856-3

    Article  CAS  PubMed  Google Scholar 

  129. Shi R, Jin Y, Zhao S, Yuan H, Shi J, Zhao H (2022) Hypoxic ADSC-derived exosomes enhance wound healing in diabetic mice via delivery of circ-Snhg11 and induction of M2-like macrophage polarization. Biomed Pharmacother 153:113463. https://doi.org/10.1016/j.biopha.2022.113463

    Article  CAS  PubMed  Google Scholar 

  130. Yu M, Huang J, Zhu T et al (2020) Liraglutide-loaded PLGA/gelatin electrospun nanofibrous mats promote angiogenesis to accelerate diabetic wound healing via the modulation of miR-29b-3p. Biomater Sci 8:4225–4238. https://doi.org/10.1039/d0bm00442a

    Article  CAS  PubMed  Google Scholar 

  131. Xu Y, Yu T, He L et al (2020) Inhibition of miRNA-152–3p enhances diabetic wound repair via upregulation of PTEN. Aging 12:14978–14989. https://doi.org/10.18632/aging.103557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Han ZF, Cao JH, Liu ZY, Yang Z, Qi RX, Xu HL (2022) Exosomal lncRNA KLF3-AS1 derived from bone marrow mesenchymal stem cells stimulates angiogenesis to promote diabetic cutaneous wound healing. Diabetes Res Clin Pract 183:109126. https://doi.org/10.1016/j.diabres.2021.109126

    Article  CAS  PubMed  Google Scholar 

  133. Pizzino G, Irrera N, Galfo F et al (2018) Effects of the antagomiRs 15b and 200b on the altered healing pattern of diabetic mice. Br J Pharmacol 175:644–655. https://doi.org/10.1111/bph.14113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Qi L, Lu Y, Wang Z, Zhang G (2021) microRNA-106b derived from endothelial cell-secreted extracellular vesicles prevents skin wound healing by inhibiting JMJD3 and RIPK3. J Cell Mol Med 25:4551–4561. https://doi.org/10.1111/jcmm.16037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Liang ZH, Pan NF, Lin SS et al (2022) 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 13:336. https://doi.org/10.1186/s13287-022-03015-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Chen X, Yang R, Wang J et al (2020) Porcine acellular dermal matrix accelerates wound healing through miR-124-3p.1 and miR-139-5p. Cytotherapy 22:494–502. https://doi.org/10.1016/j.jcyt.2020.04.042

    Article  CAS  PubMed  Google Scholar 

  137. Liang F, Luo YF, Guo Z, Qian Q, Meng XB, Mo ZH (2023) MicroRNA-139-5p mediates BMSCs impairment in diabetes by targeting HOXA9/c-Fos. FASEB J 37:e22697. https://doi.org/10.1096/fj.202201059R

    Article  CAS  PubMed  Google Scholar 

  138. Shi R, Jin Y, Hu W et al (2020) 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 318:C848-848C856. https://doi.org/10.1152/ajpcell.00041.20204

    Article  CAS  PubMed  Google Scholar 

  139. Huang L, Cai HA, Zhang MS, Liao RY, Huang X, Hu FD (2021) Ginsenoside Rg1 promoted the wound healing in diabetic foot ulcers via miR-489-3p/Sirt1 axis. J Pharmacol Sci 147:271–283. https://doi.org/10.1016/j.jphs.2021.07.008

    Article  CAS  PubMed  Google Scholar 

  140. Lucas T, Schäfer F, Müller P, Eming SA, Heckel A, Dimmeler S (2017) Light-inducible antimiR-92a as a therapeutic strategy to promote skin repair in healing-impaired diabetic mice. Nat Commun 8:15162. https://doi.org/10.1038/ncomms15162

    Article  PubMed  PubMed Central  Google Scholar 

  141. Li H, Chang L, Du WW et al (2014) Anti-microRNA-378a enhances wound healing process by upregulating integrin beta-3 and vimentin. Mol Ther 22:1839–1850. https://doi.org/10.1038/mt.2014.115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Wang JM, Qiu Y, Yang ZQ, Li L, Zhang K (2017) Inositol-requiring enzyme 1 facilitates diabetic wound healing through modulating MicroRNAs. Diabetes 66:177–192. https://doi.org/10.2337/db16-0052

    Article  CAS  PubMed  Google Scholar 

  143. Icli B, Wu W, Ozdemir D et al (2019) MicroRNA-135a-3p regulates angiogenesis and tissue repair by targeting p38 signaling in endothelial cells. FASEB J 33:5599–5614. https://doi.org/10.1096/fj.201802063RR

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. 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 91:151–159. https://doi.org/10.1016/j.yjmcc.2016.01.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Asadi-Yousefabad SL, Nammian P, Tabei S et al (2022) Angiogenesis in diabetic mouse model with critical limb ischemia; cell and gene therapy. Microvasc Res 141:104339

    Article  CAS  PubMed  Google Scholar 

  146. Niemiec SM, Louiselle AE, Hilton SA et al (2020) Nanosilk increases the strength of diabetic skin and delivers CNP-miR146a to improve wound healing. Front Immunol 11:590285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Stager MA, Bardill J, Raichart A et al (2022) Photopolymerized zwitterionic hydrogels with a sustained delivery of cerium oxide nanoparticle-miR146a conjugate accelerate diabetic wound healing. ACS Appl Bio Mater 5(3):1092–1103

    Article  CAS  PubMed  Google Scholar 

  148. Wu D, Chang X, Tian J et al (2021) Bone mesenchymal stem cells stimulation by magnetic nanoparticles and a static magnetic field: release of exosomal miR-1260a improves osteogenesis and angiogenesis. J Nanobiotechnology 19(1):209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Wang J, Wu H, Peng Y et al (2021) Hypoxia adipose stem cell-derived exosomes promote high-quality healing of diabetic wound involves activation of PI3K/Akt pathways. J Nanobiotechnology 19(1):202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Galiano RD, Michaels J, Dobryansky M et al (2004) Quantitative and reproducible murine model of excisional wound healing. Wound Repair Regen 12(4):485–92

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors are grateful for financial supports from the National Natural Science Foundation of China, the Ministry of the Science and Technology, the Guizhou Provincial Department of Science and Technology, and the Guizhou Provincial Department of Education, P.R.China.

Funding

National Natural Science Foundation of China (Nos. 81460156, 31960191), the Science and Technology Innovation Leading Academics of National High-level Personnel of Special Support Program (No. GKFZ-2018-29), the High-Level Innovative Talent Support Program of Guizhou Province (No. QKHPT-RC-GCC[2022]001-1), the Natural Science Foundation of Guizhou Province (No. QKHJC-ZK-2021-ZD-026), and the Special Funds from the Central Government to Support the Development of Local Colleges and Universities - the Construction Project of Key Laboratory in Guizhou Province (No. QJJ[2023]020), P.R.China.

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  1. Institute of Medicinal Biotechnology, Affiliated Hospital of Zunyi Medical University, 149 Dalian Road, Huichuan District, Zunyi, 563003, China

    Wen-Ting Chen, Yi Luo, Xue-Mei Chen & Jian-Hui Xiao

  2. Guizhou Provincial Universities Key Laboratory of Medicinal Biotechnology & Research Center for Translational Medicine, Affiliated Hospital of Zunyi Medical University, 149 Dalian Road, Huichuan District, Zunyi, 563003, China

    Yi Luo & Jian-Hui Xiao

  3. Department of Pediatrics, Affiliated Hospital of Zunyi Medical University, 149 Dalian Road, Huichuan District, Zunyi, 563003, China

    Xue-Mei Chen & Jian-Hui Xiao

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JHX contributed to the study conception and design, supervision, and critical revision. Material preparation, data collection and analysis, and writing of original draft were performed by WTC. YL and XMC revised the manuscript. All authors read and approved the final manuscript.

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Chen, WT., Luo, Y., Chen, XM. et al. Role of exosome-derived miRNAs in diabetic wound angiogenesis. Mol Cell Biochem (2023). https://doi.org/10.1007/s11010-023-04874-1

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