Autophagy and skin wound healing

Haiyue Ren; Feng Zhao; Qiqi Zhang; Xing Huang; Zhe Wang

doi:10.1093/burnst/tkac003

您当前的位置：

首页 >

文章列表页 >

Autophagy and skin wound healing

更新时间：2022-06-09

- Autophagy and skin wound healing
- Burns & Trauma Vol. 10, Issue 1, (2022)
- 作者机构：
  
  1. Department of Pathology
  2. Shengjing Hospital of China Medical University
  3. Department of Stem Cells and Regenerative Medicine
  4. China Medical University
  5. Department of General Surgery
- 作者简介：
- 基金信息：
- DOI：10.1093/burnst/tkac003
  CLC：
- Published：2022，
  
  Published Online：16 February 2022，
扫描看全文
Haiyue Ren, Feng Zhao, Qiqi Zhang, Xing Huang, Zhe Wang, Autophagy and skin wound healing, Burns & Trauma, Volume 10, 2022, tkac003, https://doi.org/10.1093/burnst/tkac003
DOI：

Haiyue Ren, Feng Zhao, Qiqi Zhang, Xing Huang, Zhe Wang, Autophagy and skin wound healing, Burns & Trauma, Volume 10, 2022, tkac003, https://doi.org/10.1093/burnst/tkac003 DOI：

摘要

Abstract

Autophagy is a lysosome-dependent

self-renewal mechanism that can degrade and recycle cellular components in eukaryotic cells to maintain the stability of the intracellular environment and the cells ability to cope with unfavorable environments. Numerous studies suggest that autophagy participates in regulating various cellular functions and is closely associated with the onset and progression of various diseases. Wound healing is a complex

multistep biological process that involves multiple cell types. Refractory wounds

which include diabetic skin ulcers

can seriously endanger human health. Previous studies have confirmed that autophagy plays an essential role in various phases of wound healing. Specifically

in the inflammatory phase

autophagy has an anti-infection effect and it negatively regulates the inflammatory response

which prevents excessive inflammation from causing tissue damage. In the proliferative phase

local hypoxia in the wound can induce autophagy

which plays a role in anti-apoptosis and anti-oxidative stress and promotes cell survival. Autophagy of vascular endothelial cells promotes wound angiogenesis and that of keratinocytes promotes their differentiation

proliferation and migration

which is conducive to the completion of wound re-epithelialisation. In the remodeling phase

autophagy of fibroblasts affects the formation of hypertrophic scars. Additionally

a refractory diabetic wound may be associated with increased levels of autophagy

and the regulation of mesenchymal stem cell autophagy may improve its application to wound healing. Therefore

understanding the relationship between autophagy and skin wound healing and exploring the molecular mechanism of autophagy regulation may provide novel strategies for the clinical treatment of wound healing.

关键词

Keywords

AutophagyWound healingdiabetesMesenchymal stem cellsmicroRNAskin

references

1.Singer AJ, Clark RA. Cutaneous wound healing. N Engl J Med. 1999;341:738–46.

2.Martin P. Wound healing--aiming for perfect skin regeneration. Science. 1997;276:75–81.

3.Rodrigues M, Kosaric N, Bonham CA, Gurtner GC. Wound healing: a cellular perspective. Physiol Rev. 2019;99:665–706.

4.Reinke JM, Sorg H. Wound repair and regeneration. Eur Surg Res. 2012;49:35–43.

5.Yang R, Liu F, Wang J, Chen X, Xie J, Xiong K. Epidermal stem cells in wound healing and their clinical applications. Stem Cell Res Ther. 2019;10:229. https://doi.org/10.1186/s13287-019-1312-z.

6.Guo S, Dipietro LA. Factors affecting wound healing. J Dent Res. 2010;89:219–29.

7.Han G, Ceilley R. Chronic wound healing: a review of current management and treatments. Adv Ther. 2017;34:599–610.

8.Sorg H, Tilkorn DJ, Hager S, Hauser J, Mirastschijski U. Skin wound healing: An update on the current knowledge and concepts. Eur Surg Res. 2017;58:81–94.

9.Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol. 2009;10:458–67.

10.Galluzzi L, Green DR. Autophagy-independent functions of the autophagy machinery. Cell. 2019;177:1682–99.

11.Galluzzi L, Baehrecke EH, Ballabio A, Boya P, Bravo-San Pedro JM, Cecconi F, et al. Molecular definitions of autophagy and related processes. EMBO J. 2017;36:1811–36.

12.Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol. 2007;9:1102–9.

13.Li W, He P, Huang Y, Li YF, Lu J, Li M, et al. Selective autophagy of intracellular organelles: recent research advances. Theranostics. 2021;11:222–56.

14.Wirawan E, Vanden Berghe T, Lippens S, Agostinis P, Vandenabeele P. Autophagy: for better or for worse. Cell Res. 2012;22:43–61.

15.Zachari M, Ganley IG. The mammalian ULK1 complex and autophagy initiation. Essays Biochem. 2017;61:585–96.

16.Saha S, Panigrahi DP, Patil S, Bhutia SK. Autophagy in health and disease: a comprehensive review. Biomed Pharmacother. 2018;104:485–95.

17.Matsuzawa-Ishimoto Y, Hwang S, Cadwell K. Autophagy and inflammation. Annu Rev Immunol. 2018;36:73–101.

18.Runwal G, Stamatakou E, Siddiqi FH, Puri C, Zhu Y, Rubinsztein DC. LC3-positive structures are prominent in autophagy-deficient cells. Sci Rep. 2019;9:10147. https://doi.org/10.1038/s41598-019-46657-z.

19.Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13:132–41.

20.Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010;221:3–12.

21.Peng X, Wei C, Li HZ, Li HX, Bai SZ, Wang LN, et al. NPS2390, a selective calcium-sensing receptor antagonist controls the phenotypic modulation of hypoxic human pulmonary arterial smooth muscle cells by regulating autophagy. J Transl Int Med. 2019;7:59–68.

22.Tamargo-Gómez I, Mariño G. AMPK: Regulation of metabolic dynamics in the context of autophagy. Int J Mol Sci 2018; 19. https://doi.org/10.3390/ijms19123812

23.Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011;18:571–80.

24.Zhang J, Ney PA. Role of BNIP3 and NIX in cell death, autophagy, and mitophagy. Cell Death Differ. 2009;16:939–46.

25.Fasano C, Disciglio V, Bertora S, Lepore Signorile M, Simone C. FOXO3a from the nucleus to the mitochondria: a round trip in cellular stress response. Cell. 2019;8. https://doi.org/10.3390/cells8091110.

26.van der Vos KE, Coffer PJ. Glutamine metabolism links growth factor signaling to the regulation of autophagy. Autophagy. 2012;8:1862–4.

27.Zhou J, Liao W, Yang J, Ma K, Li X, Wang Y, et al. FOXO3 induces FOXO1-dependent autophagy by activating the AKT1 signaling pathway. Autophagy. 2012;8:1712–23.

28.Li Y, Chen Y. AMPK and autophagy. Adv Exp Med Biol. 2019;1206:85–108.

29.Zhou YY, Li Y, Jiang WQ, Zhou LF. MAPK/JNK signalling: a potential autophagy regulation pathway. Biosci Rep. 2015;35. https://doi.org/10.1042/bsr20140141.

30.Obergasteiger J, Frapporti G, Pramstaller PP, Hicks AA, Volta M. A new hypothesis for Parkinson's disease pathogenesis: GTPase-p38 MAPK signaling and autophagy as convergence points of etiology and genomics. Mol Neurodegener. 2018;13:40. https://doi.org/10.1186/s13024-018-0273-5.

31.Henson SM, Lanna A, Riddell NE, Franzese O, Macaulay R, Griffiths SJ, et al. p38 signaling inhibits mTORC1-independent autophagy in senescent human CD8+ T cells. J Clin Invest. 2014;124:4004–16.

32.Kim JH, Hong SK, Wu PK, Richards AL, Jackson WT, Park JI. Raf/MEK/ERK can regulate cellular levels of LC3B and SQSTM1/p62 at expression levels. Exp Cell Res. 2014;327:340–52.

33.Kinsey CG, Camolotto SA, Boespflug AM, Guillen KP, Foth M, Truong A, et al. Protective autophagy elicited by RAF→MEK→ERK inhibition suggests a treatment strategy for RAS-driven cancers. Nat Med. 2019;25:620–7.

34.Klionsky DJ, Abdel-Aziz AK, Abdelfatah S, Abdellatif M, Abdoli A, Abel S, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition)(1). Autophagy. 2021;17:1–382.

35.Hill D, Cosgarea I, Reynolds N, Lovat P, Armstrong J. Research techniques made simple: analysis of autophagy in the skin. J Invest Dermatol. 2021;141:5–9.e1. https://doi.org/10.1016/j.jid.2020.10.004.

36.Skendros P, Mitroulis I, Ritis K. Autophagy in neutrophils: from Granulopoiesis to neutrophil extracellular traps. Front Cell Dev Biol. 2018;6:109. https://doi.org/10.3389/fcell.2018.00109.

37.Ullah I, Ritchie ND, Evans TJ. The interrelationship between phagocytosis, autophagy and formation of neutrophil extracellular traps following infection of human neutrophils by Streptococcus pneumoniae. Innate Immun. 2017;23:413–23.

38.Bhattacharya A, Wei Q, Shin JN, Abdel Fattah E, Bonilla DL, Xiang Q, et al. Autophagy is required for neutrophil-mediated inflammation. Cell Rep. 2015;12:1731–9.

39.Park SY, Shrestha S, Youn YJ, Kim JK, Kim SY, Kim HJ, et al. Autophagy primes neutrophils for neutrophil extracellular trap formation during sepsis. Am J Respir Crit Care Med. 2017;196:577–89.

40.Li C, Qu L, Farragher C, Vella A, Zhou B. MicroRNA regulated macrophage activation in obesity. J Transl Int Med. 2019;7:46–52.

41.Zhu Y, Li H, Ding S, Wang Y. Autophagy inhibition promotes phagocytosis of macrophage and protects mice from methicillin-resistant staphylococcus aureus pneumonia. J Cell Biochem. 2018;119:4808–14.

42.Liu K, Zhao E, Ilyas G, Lalazar G, Lin Y, Haseeb M, et al. Impaired macrophage autophagy increases the immune response in obese mice by promoting proinflammatory macrophage polarization. Autophagy. 2015;11:271–84.

43.Kawano A, Ariyoshi W, Yoshioka Y, Hikiji H, Nishihara T, Okinaga T. Docosahexaenoic acid enhances M2 macrophage polarization via the p38 signaling pathway and autophagy. J Cell Biochem. 2019;120:12604–17.

44.Das LM, Binko AM, Traylor ZP, Peng H, Lu KQ. Vitamin D improves sunburns by increasing autophagy in M2 macrophages. Autophagy. 2019;15:813–26.

45.Wu MY, Lu JH. Autophagy and macrophage functions: inflammatory response and phagocytosis. Cell. 2019;9. https://doi.org/10.3390/cells9010070.

46.Sharma V, Verma S, Seranova E, Sarkar S, Kumar D. Selective autophagy and Xenophagy in infection and disease. Front Cell Dev Biol. 2018;6:147. https://doi.org/10.3389/fcell.2018.00147.

47.Liu W, Zhuang J, Jiang Y, Sun J, Prinz RA, Sun J, et al. Toll-like receptor signalling cross-activates the autophagic pathway to restrict salmonella Typhimurium growth in macrophages. Cell Microbiol. 2019;21:e13095. https://doi.org/10.1111/cmi.13095.

48.Qiang L, Yang S, Cui YH, He YY. Keratinocyte autophagy enables the activation of keratinocytes and fibroblasts and facilitates wound healing. Autophagy. 2020;1–16.

49.Wang J, Kaplan N, Wang S, Yang W, Wang L, He C, et al. Autophagy plays a positive role in induction of epidermal proliferation. FASEB J. 2020;34:10657–67.

50.Zhang J, Zhang C, Jiang X, Li L, Zhang D, Tang D, et al. Involvement of autophagy in hypoxia-BNIP3 signaling to promote epidermal keratinocyte migration. Cell Death Dis. 2019;10:234. https://doi.org/10.1038/s41419-019-1473-9.

51.Meng Q, Li Y, Ji T, Chao Y, Li J, Fu Y, et al. Estrogen prevent atherosclerosis by attenuating endothelial cell pyroptosis via activation of estrogen receptor α-mediated autophagy. J Adv Res. 2021;28:149–64.

52.Rezabakhsh A, Ahmadi M, Khaksar M, Montaseri A, Malekinejad H, Rahbarghazi R, et al. Rapamycin inhibits oxidative/nitrosative stress and enhances angiogenesis in high glucose-treated human umbilical vein endothelial cells: role of autophagy. Biomed Pharmacother. 2017;93:885–94.

53.Guo H, Ding H, Yan Y, Chen Q, Zhang J, Chen B, et al. Intermittent hypoxia-induced autophagy via AMPK/mTOR signaling pathway attenuates endothelial apoptosis and dysfunction in vitro. Sleep Breath. 2021;25:1859–65.

54.Zha S, Li Z, Chen S, Liu F, Wang F. MeCP2 inhibits cell functionality through FoxO3a and autophagy in endothelial progenitor cells. Aging (Albany NY). 2019;11:6714–33.

55.Liang P, Jiang B, Li Y, Liu Z, Zhang P, Zhang M, et al. Autophagy promotes angiogenesis via AMPK/Akt/mTOR signaling during the recovery of heat-denatured endothelial cells. Cell Death Dis. 2018;9:1152. https://doi.org/10.1038/s41419-018-1194-5.

56.Sprott D, Poitz DM, Korovina I, Ziogas A, Phieler J, Chatzigeorgiou A, et al. Endothelial-specific deficiency of ATG5 (autophagy protein 5) attenuates ischemia-related angiogenesis. Arterioscler Thromb Vasc Biol. 2019;39:1137–48.

57.Jeong IH, Bae WY, Choi JS, Jeong JW. Ischemia induces autophagy of endothelial cells and stimulates angiogenic effects in a hindlimb ischemia mouse model. Cell Death Dis. 2020;11:624. https://doi.org/10.1038/s41419-020-02849-4.

58.Chandel S, Manikandan A, Mehta N, Nathan AA, Tiwari RK, Mohapatra SB, et al. The protein tyrosine phosphatase PTP-PEST mediates hypoxia-induced endothelial autophagy and angiogenesis via AMPK activation. J Cell Sci. 2021;134. https://doi.org/10.1242/jcs.250274.

59.Zhou L, Liu Z, Chen S, Qiu J, Li Q, Wang S, et al. Transcription factor EB-mediated autophagy promotes dermal fibroblast differentiation and collagen production by regulating endoplasmic reticulum stress and autophagy-dependent secretion. Int J Mol Med. 2021;47:547–60.

60.Yoon JY, Park CG, Park BS, Kim EJ, Byeon GJ, Yoon JU. Effects of remifentanil preconditioning attenuating oxidative stress in human dermal fibroblast. Tissue Eng Regen Med. 2017;14:133–41.

61.Migneault F, Hébert MJ. Autophagy, tissue repair, and fibrosis: a delicate balance. Matrix Biol. 2021;100–101:182–96.

62.Asai E, Yamamoto M, Ueda K, Waguri S. Spatiotemporal alterations of autophagy marker LC3 in rat skin fibroblasts during wound healing process. Fukushima J Med Sci. 2018;64:15–22.

63.Vescarelli E, Pilloni A, Dominici F, Pontecorvi P, Angeloni A, Polimeni A, et al. Autophagy activation is required for myofibroblast differentiation during healing of oral mucosa. J Clin Periodontol. 2017;44:1039–50.

64.Shi J, Xiao H, Li J, Zhang J, Li Y, Zhang J, et al. Wild-type p53-modulated autophagy and autophagic fibroblast apoptosis inhibit hypertrophic scar formation. Lab Investig. 2018;98:1423–37.

65.Cao C, Wang W, Lu L, Wang L, Chen X, Guo R, et al. Inactivation of Beclin-1-dependent autophagy promotes ursolic acid-induced apoptosis in hypertrophic scar fibroblasts. Exp Dermatol. 2018;27:58–63.

66.Dai J, Sun Y, Chen D, Zhang Y, Yan L, Li X, et al. Negative regulation of PI3K/AKT/mTOR axis regulates fibroblast proliferation, apoptosis and autophagy play a vital role in triptolide-induced epidural fibrosis reduction. Eur J Pharmacol. 2019;864:172724. https://doi.org/10.1016/j.ejphar.2019.172724.

67.Shi W, Wu Y, Bian D. p75NTR silencing inhibits proliferation, migration, and extracellular matrix deposition of hypertrophic scar fibroblasts by activating autophagy through inhibiting the PI3K/Akt/mTOR pathway. Can J Physiol Pharmacol. 2021;99:349–59.

68.Hong Y, Li S, Wang J, Li Y. In vitro inhibition of hepatic stellate cell activation by the autophagy-related lipid droplet protein ATG2A. Sci Rep. 2018;8:9232. https://doi.org/10.1038/s41598-018-27686-6.

69.Hazari Y, Bravo-San Pedro JM, Hetz C, Galluzzi L, Kroemer G. Autophagy in hepatic adaptation to stress. J Hepatol. 2020;72:183–96.

70.O'Dwyer DN, Ashley SL, Moore BB. Influences of innate immunity, autophagy, and fibroblast activation in the pathogenesis of lung fibrosis. Am J Physiol Lung Cell Mol Physiol. 2016;311:L590–601.

71.Li L, Zhang J, Zhang Q, Zhang D, Xiang F, Jia J, et al. High glucose suppresses keratinocyte migration through the inhibition of p38 MAPK/autophagy pathway. Front Physiol. 2019;10:24. https://doi.org/10.3389/fphys.2019.00024.

72.Shaikh-Kader A, Houreld NN, Rajendran NK, Abrahamse H. The link between advanced glycation end products and apoptosis in delayed wound healing. Cell Biochem Funct. 2019;37:432–42.

73.Guo Y, Lin C, Xu P, Wu S, Fu X, Xia W, et al. AGEs induced autophagy impairs cutaneous wound healing via stimulating macrophage polarization to M1 in diabetes. Sci Rep. 2016;6:36416. https://doi.org/10.1038/srep36416.

74.Jin H, Zhang Z, Wang C, Tang Q, Wang J, Bai X, et al. Melatonin protects endothelial progenitor cells against AGE-induced apoptosis via autophagy flux stimulation and promotes wound healing in diabetic mice. Exp Mol Med. 2018;50:1–15.

75.Aragonès G, Dasuri K, Olukorede O, Francisco SG, Renneburg C, Kumsta C, et al. Autophagic receptor p62 protects against glycation-derived toxicity and enhances viability. Aging Cell. 2020;19:e13257. https://doi.org/10.1111/acel.13257.

76.Laughlin T, Tan Y, Jarrold B, Chen J, Li L, Fang B, et al. Autophagy activators stimulate the removal of advanced glycation end products in human keratinocytes. J Eur Acad Dermatol Venereol. 2020;34 Suppl 3:12–8.

77.An Y, Liu WJ, Xue P, Ma Y, Zhang LQ, Zhu B, et al. Autophagy promotes MSC-mediated vascularization in cutaneous wound healing via regulation of VEGF secretion. Cell Death Dis. 2018;9:58. https://doi.org/10.1038/s41419-017-0082-8.

78.Liu J, Qiu X, Lv Y, Zheng C, Dong Y, Dou G, et al. Apoptotic bodies derived from mesenchymal stem cells promote cutaneous wound healing via regulating the functions of macrophages. Stem Cell Res Ther. 2020;11:507. https://doi.org/10.1186/s13287-020-02014-w.

79.Luo G, Cheng W, He W, Wang X, Tan J, Fitzgerald M, et al. Promotion of cutaneous wound healing by local application of mesenchymal stem cells derived from human umbilical cord blood. Wound Repair Regen. 2010;18:506–13.

80.Sylakowski K, Bradshaw A, Wells A. Mesenchymal stem cell/multipotent stromal cell augmentation of wound healing: lessons from the physiology of matrix and hypoxia support. Am J Pathol. 2020;190:1370–81.

81.Jakovljevic J, Harrell CR, Fellabaum C, Arsenijevic A, Jovicic N, Volarevic V. Modulation of autophagy as new approach in mesenchymal stem cell-based therapy. Biomed Pharmacother. 2018;104:404–10.

82.Hu C, Zhao L, Wu D, Li L. Modulating autophagy in mesenchymal stem cells effectively protects against hypoxia- or ischemia-induced injury. Stem Cell Res Ther. 2019;10:120. https://doi.org/10.1186/s13287-019-1225-x.

83.Ceccariglia S, Cargnoni A, Silini AR, Parolini O. Autophagy: a potential key contributor to the therapeutic action of mesenchymal stem cells. Autophagy. 2020;16:28–37.

84.Liu Y, Wang N, Zhang S, Liang Q. Autophagy protects bone marrow mesenchymal stem cells from palmitate-induced apoptosis through the ROS-JNK/p38 MAPK signaling pathways. Mol Med Rep. 2018;18:1485–94.

85.Lv B, Hua T, Li F, Han J, Fang J, Xu L, et al. Hypoxia-inducible factor 1 α protects mesenchymal stem cells against oxygen-glucose deprivation-induced injury via autophagy induction and PI3K/AKT/mTOR signaling pathway. Am J Transl Res. 2017;9:2492–9.

86.Yin Y, Chen F, Li J, Yang J, Li Q, Jin P. AURKA enhances autophagy of adipose derived stem cells to promote diabetic wound repair via targeting FOXO3a. J Invest Dermatol. 2020;140:1639–49.e4. https://doi.org/10.1016/j.jid.2019.12.032.

87.Zhang F, Gao F, Wang K, Liu X, Zhang Z. MiR-34a inhibitor protects mesenchymal stem cells from hyperglycaemic injury through the activation of the SIRT1/FoxO3a autophagy pathway. Stem Cell Res Ther. 2021;12:115. https://doi.org/10.1186/s13287-021-02183-2.

88.Ozdemir D, Feinberg MW. MicroRNAs in diabetic wound healing: pathophysiology and therapeutic opportunities. Trends Cardiovasc Med. 2019;29:131–7.

89.Fahs F, Bi X, Yu FS, Zhou L, Mi QS. New insights into microRNAs in skin wound healing. IUBMB Life. 2015;67:889–96.

90.Akkoc Y, Gozuacik D. MicroRNAs as major regulators of the autophagy pathway. Biochim Biophys Acta Mol Cell Res. 2020;1867:118662. https://doi.org/10.1016/j.bbamcr.2020.118662.

91.Wu P, Cao Y, Zhao R, Wang Y. miR-96-5p regulates wound healing by targeting BNIP3/FAK pathway. J Cell Biochem. 2019;120:12904–11.

92.Zeng T, Wang X, Wang W, Feng Q, Lao G, Liang Y, et al. Endothelial cell-derived small extracellular vesicles suppress cutaneous wound healing through regulating fibroblasts autophagy. Clin Sci (Lond). 2019;133. https://doi.org/10.1042/cs20190008.

93.Wang S, Kobeissi A, Dong Y, Kaplan N, Yang W, He C, et al. MicroRNAs-103/107 regulate autophagy in the epidermis. J Invest Dermatol. 2018;138:1481–90.

94.Silwal P, Kim YS, Basu J, Jo EK. The roles of microRNAs in regulation of autophagy during bacterial infection. Semin Cell Dev Biol. 2020;101:51–8.

95.Wang F, Zhang C, Dai L, Zhang Y, Wang Y, Hao Y, et al. Bafilomycin A1 accelerates chronic refractory wound healing in db/db mice. Biomed Res Int. 2020;2020:6265701. https://doi.org/10.1155/2020/6265701.

96.Lawrence J, Nho R. The role of the mammalian target of rapamycin (mTOR) in pulmonary fibrosis. Int J Mol Sci. 2018;19. https://doi.org/10.3390/ijms19030778.

97.Shi M, Zong X, Chen L, Guo X, Ding X. MiR-506-3p regulates autophagy and proliferation in post-burn skin fibroblasts through post-transcriptionally suppressing Beclin-1 expression. In Vitro Cell Dev Biol Anim. 2020;56:522–32.

98.Wang C, Mao C, Lou Y, Xu J, Wang Q, Zhang Z, et al. Monotropein promotes angiogenesis and inhibits oxidative stress-induced autophagy in endothelial progenitor cells to accelerate wound healing. J Cell Mol Med. 2018;22:1583–600.

99.Zhao K, Hao H, Liu J, Tong C, Cheng Y, Xie Z, et al. Bone marrow-derived mesenchymal stem cells ameliorate chronic high glucose-induced β-cell injury through modulation of autophagy. Cell Death Dis. 2015;6:e1885. https://doi.org/10.1038/cddis.2015.230.

100.Shi R, Jin Y, Hu W, Lian W, Cao C, Han S, 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:C848–c56. https://doi.org/10.1152/ajpcell.00041.2020.

查看原文

Views

下载量

CSCD

Alert me when the article has been cited

提交

Tools

Publicity Resources

Amphibian-derived peptide homodimer OA-GL17d promotes skin wound regeneration through the miR-663a/TGF-β1/Smad axis

Metabolic reprogramming in skin wound healing

Adipose mesenchymal stem cell-derived exosomes promote skin wound healing in diabetic mice by regulating epidermal autophagy

PC4 serves as a negative regulator of skin wound healing in mice

Metal chelation reduces skin epithelial inflammation and rescues epithelial cells from toxicity due to thermal injury in a rat model

Related Author

Yue Zhang

Ying Wang

Lin Zeng

Yixiang Liu

Huiling Sun

Shanshan Li

Siyu Wang

Longjun Shu

Related Institution

Department of Anatomy and Histology & Embryology

Kunming Medical University

Key Laboratory of Chemistry in Ethnic Medicinal Resources & Key Laboratory of Natural Products Synthetic Biology of Ethnic Medicinal Endophytes

Yunnan MinZu University

Institutional Center for Shared Technologies and Facilities of Kunming Institute of Zoology, Chinese Academy of Sciences

⁰