Epigenetic regulation of macrophage polarization in wound healing

Cheng Chen; Tengfei Liu; Yuanyang Tang; Gaoxing Luo; Guangping Liang; Weifeng He

doi:10.1093/burnst/tkac057

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Epigenetic regulation of macrophage polarization in wound healing

更新时间：2023-05-16

- Epigenetic regulation of macrophage polarization in wound healing
- Epigenetic regulation of macrophage polarization in wound healing
- Burns & Trauma 2023年11卷第1期
- 作者机构：
  
  1. State Key Laboratory of Trauma
  2. Southwest Hospital, Third Military Medical University (Army Medical University)
  3. Chongqing Key Laboratory for Disease Proteomics
  4. No. Hospital of Joint Logistic Support Force of PLA,906
  5. Academy of Biological Engineering
- 作者简介：
- 基金信息：
  
  This work was supported by grants from the National Natural Sciences Foundation of China (No. 81901961 to TFL;No. 81630055 and No. 81920108022 to GXL;No. 31872742 to WFH), the Military Medical Science and Technology Youth Training Program of the Army Military Medical University (Third Military Medical University) (No. 20QNPY024 to WFH) and the Special Project for Enhancing Science and Technology Innovation Ability (frontier exploration) of the Army Military Medical University (Third Military Medical University) (No. 2019XQY12 to WFH).
- DOI：10.1093/burnst/tkac057
  中图分类号：
- 纸质出版日期：2023，
  
  网络出版日期：2023-1-17，
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Cheng Chen, Tengfei Liu, Yuanyang Tang, 等. Epigenetic regulation of macrophage polarization in wound healing[J]. Burns & Trauma, 2023,11(1).

Cheng Chen, Tengfei Liu, Yuanyang Tang, Gaoxing Luo, Guangping Liang, Weifeng He, Epigenetic regulation of macrophage polarization in wound healing, Burns & Trauma, Volume 11, 2023, tkac057, https://doi.org/10.1093/burnst/tkac057
Cheng Chen, Tengfei Liu, Yuanyang Tang, 等. Epigenetic regulation of macrophage polarization in wound healing[J]. Burns & Trauma, 2023,11(1). DOI： 10.1093/burnst/tkac057.

Cheng Chen, Tengfei Liu, Yuanyang Tang, Gaoxing Luo, Guangping Liang, Weifeng He, Epigenetic regulation of macrophage polarization in wound healing, Burns & Trauma, Volume 11, 2023, tkac057, https://doi.org/10.1093/burnst/tkac057 DOI：

摘要

Abstract

The immune microenvironment plays a critical role in regulating skin wound healing. Macrophages

the main component of infiltrating inflammatory cells

play a pivotal role in shaping the immune microenvironment in the process of skin wound healing. Macrophages comprise the classic proinflammatory M1 subtype and anti-inflammatory M2 population. In the early inflammatory phase of skin wound closure

M1-like macrophages initiate and amplify the local inflammatory response to disinfect the injured tissue. In the late tissue-repairing phase

M2 macrophages are predominant in wound tissue and limit local inflammation to promote tissue repair. The biological function of macrophages is tightly linked with epigenomic organization. Transcription factors are essential for macrophage polarization. Epigenetic modification of transcription factors determines the heterogeneity of macrophages. In contrast

transcription factors also regulate the expression of epigenetic enzymes. Both transcription factors and epigenetic enzymes form a complex network that regulates the plasticity of macrophages. Here

we describe the latest knowledge concerning the potential epigenetic mechanisms that precisely regulate the biological function of macrophages and their effects on skin wound healing.

关键词

Keywords

EpigeneticsMacrophage polarizationWound healingImmune microenvironmentSignaling pathways

references

1.He L, Marneros AG. Macrophages are essential for the early wound healing response and the formation of a fibrovascular scar. Am J Pathol. 2013;182:2407–17.

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

3.Kimball A, Schaller M, Joshi A, Davis FM, denDekker A, Boniakowski A, et al. Ly6C(hi) blood monocyte/macrophage drive chronic inflammation and impair wound healing in diabetes mellitus. Arterioscler Thromb Vasc Biol. 2018;38:1102–14.

4.Cavalli G, Heard E. Advances in epigenetics link genetics to the environment and disease. Nature. 2019;571:489–99.

5.Álvarez-Errico D, Vento-Tormo R, Sieweke M, Ballestar E. Epigenetic control of myeloid cell differentiation, identity and function. Nat Rev Immunol. 2015;15:7–17.

6.Lewis CJ, Stevenson A, Fear MW, Wood FM. A review of epigenetic regulation in wound healing: implications for the future of wound care. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society. 2020;28:710–8.

7.Britt EC, John SV, Locasale JW, Fan J. Metabolic regulation of epigenetic remodeling in immune cells. Curr Opin Biotechnol. 2020;63:111–7.

8.Chen C, Meng Z, Ren H, Zhao N, Shang R, He W, et al. The molecular mechanisms supporting the homeostasis and activation of dendritic epidermal T cell and its role in promoting wound healing. Burns Trauma. 2021;9:tkab009. https://doi.org/10.1093/burnst/tkab009.

9.Ellis S, Lin EJ, Tartar D. Immunology of wound healing. Curr Dermatol Rep. 2018;7:350–8.

10.Martin P, Nunan R. Cellular and molecular mechanisms of repair in acute and chronic wound healing. Br J Dermatol. 2015;173:370–8.

11.Boniakowski AE, Kimball AS, Jacobs BN, Kunkel SL, Gallagher KA. Macrophage-mediated inflammation in normal and diabetic wound healing. J Immunol. 2017;199:17–24.

12.Xu X, Gu S, Huang X, Ren J, Gu Y, Wei C, et al. The role of macrophages in the formation of hypertrophic scars and keloids. Burns Trauma. 2020;8:tkaa006. https://doi.org/10.1093/burnst/tkaa006.

13.Gu XY, Shen SE, Huang CF, Liu YN, Chen YC, Luo L, et al. Effect of activated autologous monocytes/macrophages on wound healing in a rodent model of experimental diabetes. Diabetes Res Clin Pract. 2013;102:53–9.

14.Miki S, Suzuki JI, Takashima M, Ishida M, Kokubo H, Yoshizumi M. S-1-Propenylcysteine promotes IL-10-induced M2c macrophage polarization through prolonged activation of IL-10R/STAT3 signaling. Sci Rep. 2021;11:22469.

15.Ferrante CJ, Leibovich SJ. Regulation of macrophage polarization and wound healing. Adv Wound Care. 2012;1:10–6.

16.Koh TJ, DiPietro LA. Inflammation and wound healing: the role of the macrophage. Expert Rev Mol Med. 2011;13:e23.

17.Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest. 2012;122:787–95.

18.Dorrington MG, Fraser IDC. NF-κB Signaling in macrophages: dynamics, crosstalk, and signal integration. Front Immunol. 2019;10:705. https://doi.org/10.3389/fimmu.2019.00705.

19.Cheng Q, Ohta S, Sheu K, Spreafico R, Adelaja A, Taylor B, et al. NF-κB dynamics determine the stimulus specificity of epigenomic reprogramming in macrophages. Science. 2021;372:1349–53.

20.Platanitis E, Decker T. Regulatory networks involving STATs, IRFs, and NFκB in inflammation. Front Immunol. 2018;9:2542. https://doi.org/10.3389/fimmu.2018.02542.

21.Chistiakov DA, Myasoedova VA, Revin VV, Orekhov AN, Bobryshev YV. The impact of interferon-regulatory factors to macrophage differentiation and polarization into M1 and M2. Immunobiology. 2018;223:101–11.

22.Negishi H, Taniguchi T, Yanai H. The interferon (IFN) class of cytokines and the IFN regulatory factor (IRF) transcription factor family. Cold Spring Harb Perspect Biol. 2018;10:1018-27. https://doi.org/10.1101/cshperspect.a028423.

23.Krausgruber T, Blazek K, Smallie T, Alzabin S, Lockstone H, Sahgal N, et al. IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat Immunol. 2011;12:231–8.

24.Tarassishin L, Suh HS, Lee SC. Interferon regulatory factor 3 plays an anti-inflammatory role in microglia by activating the PI3K/Akt pathway. J Neuroinflammation. 2011;8:187. https://doi.org/10.1186/1742-2094-8-187.

25.Nan Y, Wu C, Zhang YJ. Interplay between Janus kinase/signal transducer and activator of transcription Signaling activated by type I interferons and viral antagonism. Front Immunol. 2017;8:1758. https://doi.org/10.3389/fimmu.2017.01758.

26.Hu X, Chen J, Wang L, Ivashkiv LB. Crosstalk among Jak-STAT, toll-like receptor, and ITAM-dependent pathways in macrophage activation. J Leukoc Biol. 2007;82:237–43.

27.Stetson DB, Medzhitov R. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity. 2006;24:93–103.

28.Dobrian AD, Galkina EV, Ma Q, Hatcher M, Aye SM, Butcher MJ, et al. STAT4 deficiency reduces obesity-induced insulin resistance and adipose tissue inflammation. Diabetes. 2013;62:4109–21.

29.Wang N, Liang H, Zen K. Molecular mechanisms that influence the macrophage m1-m2 polarization balance. Front Immunol. 2014;5:614. https://doi.org/10.3389/fimmu.2014.00614.

30.Porta C, Riboldi E, Ippolito A, Sica A. Molecular and epigenetic basis of macrophage polarized activation. Semin Immunol. 2015;27:237–48.

31.Whyte CS, Bishop ET, Rückerl D, Gaspar-Pereira S, Barker RN, Allen JE, et al. Suppressor of cytokine signaling (SOCS)1 is a key determinant of differential macrophage activation and function. J Leukoc Biol. 2011;90:845–54.

32.Yasukawa H, Ohishi M, Mori H, Murakami M, Chinen T, Aki D, et al. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat Immunol. 2003;4:551–6.

33.Pachva MC, Kisselev AF, Matkarimov BT, Saparbaev M, Groisman R. DNA-histone cross-links: formation and repair. Front Cell Dev Biol. 2020;8:607045. https://doi.org/10.3389/fcell.2020.607045.

34.Hashimoto H, Vertino PM, Cheng X. Molecular coupling of DNA methylation and histone methylation. Epigenomics. 2010;2:657–69.

35.Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature. 2009;462:315–22.

36.He Y, Ecker JR. Non-CG methylation in the human genome. Annu Rev Genomics Hum Genet. 2015;16:55–77.

37.van der Wijst MG, Venkiteswaran M, Chen H, Xu GL, Plösch T, Rots MG. Local chromatin microenvironment determines DNMT activity: from DNA methyltransferase to DNA demethylase or DNA dehydroxymethylase. Epigenetics. 2015;10:671–6.

38.de Groot AE, Pienta KJ. Epigenetic control of macrophage polarization: implications for targeting tumor-associated macrophages. Oncotarget. 2018;9:20908–27.

39.Yang X, Wang X, Liu D, Yu L, Xue B, Shi H. Epigenetic regulation of macrophage polarization by DNA methyltransferase 3b. Molecular endocrinology (Baltimore, Md). 2014;28:565–74.

40.Denis H, Ndlovu MN, Fuks F. Regulation of mammalian DNA methyltransferases: a route to new mechanisms. EMBO Rep. 2011;12:647–56.

41.Cheng C, Huang C, Ma TT, Bian EB, He Y, Zhang L, et al. SOCS1 hypermethylation mediated by DNMT1 is associated with lipopolysaccharide-induced inflammatory cytokines in macrophages. Toxicol Lett. 2014;225:488–97.

42.Zhang Q, Zhao K, Shen Q, Han Y, Gu Y, Li X, et al. Tet2 is required to resolve inflammation by recruiting Hdac2 to specifically repress IL-6. Nature. 2015;525:389–93.

43.Kohli RM, Zhang Y. TET enzymes, TDG and the dynamics of DNA demethylation. Nature. 2013;502:472–9.

44.Zhou K, Gaullier G, Luger K. Nucleosome structure and dynamics are coming of age. Nat Struct Mol Biol. 2019;26:3–13.

45.Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21:381–95.

46.Morgan MAJ, Shilatifard A. Reevaluating the roles of histone-modifying enzymes and their associated chromatin modifications in transcriptional regulation. Nat Genet. 2020;52:1271–81.

47.Greer EL, Shi Y. Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet. 2012;13:343–57.

48.Li Y, Reddy MA, Miao F, Shanmugam N, Yee JK, Hawkins D, et al. Role of the histone H3 lysine 4 methyltransferase, SET7/9, in the regulation of NF-kappaB-dependent inflammatory genes. Relevance to diabetes and inflammation. J Biol Chem. 2008;283:26771–81.

49.Xu G, Liu G, Xiong S, Liu H, Chen X, Zheng B. The histone methyltransferase Smyd2 is a negative regulator of macrophage activation by suppressing interleukin 6 (IL-6) and tumor necrosis factor α (TNF-α) production. J Biol Chem. 2015;290:5414–23.

50.Liu C, Xu D, Han H, Fan Y, Schain F, Xu Z, et al. Transcriptional regulation of 15-lipoxygenase expression by histone h3 lysine 4 methylation/demethylation. PLoS One. 2012;7:e52703. https://doi.org/10.1371/journal.pone.0052703.

51.Tikhanovich I, Zhao J, Olson J, Adams A, Taylor R, Bridges B, et al. Protein arginine methyltransferase 1 modulates innate immune responses through regulation of peroxisome proliferator-activated receptor γ-dependent macrophage differentiation. J Biol Chem. 2017;292:6882–94.

52.Fan Z, Li J, Li P, Ye Q, Xu H, Wu X, et al. Protein arginine methyltransferase 1 (PRMT1) represses MHC II transcription in macrophages by methylating CIITA. Sci Rep. 2017;7:40531. https://doi.org/10.1038/srep40531.

53.De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G, Natoli G. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell. 2007;130:1083–94.

54.Satoh T, Takeuchi O, Vandenbon A, Yasuda K, Tanaka Y, Kumagai Y, et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol. 2010;11:936–44.

55.De Santa F, Narang V, Yap ZH, Tusi BK, Burgold T, Austenaa L, et al. Jmjd3 contributes to the control of gene expression in LPS-activated macrophages. EMBO J. 2009;28:3341–52.

56.Ishii M, Wen H, Corsa CA, Liu T, Coelho AL, Allen RM, et al. Epigenetic regulation of the alternatively activated macrophage phenotype. Blood. 2009;114:3244–54.

57.Jin Q, Yu LR, Wang L, Zhang Z, Kasper LH, Lee JE, et al. Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBO J. 2011;30:249–62.

58.Li W, Wang Y, Zhu L, Du S, Mao J, Wang Y, et al. The P300/XBP1s/Herpud1 axis promotes macrophage M2 polarization and the development of choroidal neovascularization. J Cell Mol Med. 2021;25:6709–20.

59.Wang X, Li H, Chen S, He J, Chen W, Ding Y, et al. P300/CBP-associated factor (PCAF) attenuated M1 macrophage inflammatory responses possibly through KLF2 and KLF4. Immunol Cell Biol. 2021;99:724–36.

60.Chen X, Barozzi I, Termanini A, Prosperini E, Recchiuti A, Dalli J, et al. Requirement for the histone deacetylase Hdac3 for the inflammatory gene expression program in macrophages. Proc Natl Acad Sci U S A. 2012;109:E2865–74.

61.Mullican SE, Gaddis CA, Alenghat T, Nair MG, Giacomin PR, Everett LJ, et al. Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation. Genes Dev. 2011;25:2480–8.

62.Cao Q, Rong S, Repa JJ, St Clair R, Parks JS, Mishra N. Histone deacetylase 9 represses cholesterol efflux and alternatively activated macrophages in atherosclerosis development. Arterioscler Thromb Vasc Biol. 2014;34:1871–9.

63.Liu Y, Du M, Lin HY. Histone deacetylase 9 deficiency exaggerates uterine M2 macrophage polarization. J Cell Mol Med. 2021;25:7690–708.

64.Yoshizaki T, Schenk S, Imamura T, Babendure JL, Sonoda N, Bae EJ, et al. SIRT1 inhibits inflammatory pathways in macrophages and modulates insulin sensitivity. Am J Physiol Endocrinol Metab. 2010;298:E419–28.

65.Wang F, Liu H, Blanton WP, Belkina A, Lebrasseur NK, Denis GV. Brd2 disruption in mice causes severe obesity without type 2 diabetes. Biochem J. 2009;425:71–83.

66.Belkina AC, Nikolajczyk BS, Denis GV. BET protein function is required for inflammation: Brd2 genetic disruption and BET inhibitor JQ1 impair mouse macrophage inflammatory responses. J Immunol. 2013;190:3670–8.

67.Samanta S, Zhou Z, Rajasingh S, Panda A, Sampath V, Rajasingh J. DNMT and HDAC inhibitors together abrogate endotoxemia mediated macrophage death by STAT3-JMJD3 signaling. Int J Biochem Cell Biol. 2018;102:117–27.

68.Sherry-Lynes MM, Sengupta S, Kulkarni S, Cochran BH. Regulation of the JMJD3 (KDM6B) histone demethylase in glioblastoma stem cells by STAT3. PLoS One. 2017;12:e0174775. https://doi.org/10.1371/journal.pone.0174775.

69.Mattick JS, Makunin IV. Non-coding RNA. Hum Mol Genet. 2006;15 Spec No 1:R17–29.

70.Ning P, Liu DW. Advances in the research of the role of MicroRNAs in wound healing. Chin J Burns. 2013;29:374–7.

71.Louafi F, Martinez-Nunez RT, Sanchez-Elsner T. MicroRNA-155 targets SMAD2 and modulates the response of macrophages to transforming growth factor-{beta}. J Biol Chem. 2010;285:41328–36.

72.Qin Y, Wang Q, Zhou Y, Duan Y, Gao Q. Inhibition of IFN-γ-induced nitric oxide dependent Antimycobacterial activity by miR-155 and C/EBPβ. Int J Mol Sci. 2016;17:535. https://doi.org/10.3390/ijms17040535.

73.Lin L, Hou J, Ma F, Wang P, Liu X, Li N, et al. Type I IFN inhibits innate IL-10 production in macrophages through histone deacetylase 11 by downregulating microRNA-145. J Immunol. 2013;191:3896–904.

74.Li D, Peng H, Qu L, Sommar P, Wang A, Chu T, et al. miR-19a/b and miR-20a promote wound healing by regulating the inflammatory response of keratinocytes. J Invest Dermatol. 2021;141:659–71.

75.Gallant-Behm CL, Piper J, Dickinson BA, Dalby CM, Pestano LA, Jackson AL. A synthetic microRNA-92a inhibitor (MRG-110) accelerates angiogenesis and wound healing in diabetic and nondiabetic wounds. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society. 2018;26:311–23.

76.Wang P, Yin B, Su YJ, Jia CY. Research advances in healing mechanism of chronic refractory wounds mediated by long non-coding RNA. Chin J Burns. 2020;36:758–61.

77.Ye Y, Xu Y, Lai Y, He W, Li Y, Wang R, et al. Long non-coding RNA cox-2 prevents immune evasion and metastasis of hepatocellular carcinoma by altering M1/M2 macrophage polarization. J Cell Biochem. 2018;119:2951–63.

78.Du M, Yuan L, Tan X, Huang D, Wang X, Zheng Z, et al. The LPS-inducible lncRNA Mirt2 is a negative regulator of inflammation. Nat Commun. 2017;8:2049. https://doi.org/10.1038/s41467-017-02229-1.

79.Xue YL, Zhang SX, Zheng CF, Li YF, Zhang LH, Su QY, et al. Long non-coding RNA MEG3 inhibits M2 macrophage polarization by activating TRAF6 via microRNA-223 down-regulation in viral myocarditis. J Cell Mol Med. 2020;24:12341–54.

80.Liu D, Wei Y, Liu Y, Wu T, Hu J, Lu H. The long non-coding RNA NEAT1/miR-224-5p/IL-33 Axis modulates macrophage M2a polarization and A1 astrocyte activation. Mol Neurobiol. 2021;58:4506–19.

81.Pi L, Fang B, Meng X, Qian L. LncRNA XIST accelerates burn wound healing by promoting M2 macrophage polarization through targeting IL-33 via miR-19b. Cell Death Dis. 2022;8:220. https://doi.org/10.1038/s41420-022-00990-x.

82.Song H, Yang Y, Sun Y, Wei G, Zheng H, Chen Y, et al. Circular RNA Cdyl promotes abdominal aortic aneurysm formation by inducing M1 macrophage polarization and M1-type inflammation. Mol Ther. 2022;30:915–31.

83.Zhang C, Han X, Yang L, Fu J, Sun C, Huang S, et al. Circular RNA circPPM1F modulates M1 macrophage activation and pancreatic islet inflammation in type 1 diabetes mellitus. Theranostics. 2020;10:10908–24.

84.Zhang J, Cheng F, Rong G, Tang Z, Gui B. Circular RNA hsa_circ_0005567 overexpression promotes M2 type macrophage polarization through miR-492/SOCS2 axis to inhibit osteoarthritis progression. Bioengineered. 2021;12:8920–30.

85.Lian C, Sun J, Guan W, Zhang L, Zhang X, Yang L, et al. Circular RNA circHIPK3 activates macrophage NLRP3 Inflammasome and TLR4 pathway in gouty arthritis via sponging miR-561 and miR-192. Inflammation. 2021;44:2065–77.

86.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. https://doi.org/10.1016/j.biopha.2022.113463.

87.Kapellos T, Iqbal A. Epigenetic control of macrophage polarisation and soluble mediator gene expression during inflammation. Mediat Inflamm. 2016;2016:1–15.

88.Aung H, Schroder K, Himes S, Brion K, van Zuylen W, Trieu A, et al. LPS regulates proinflammatory gene expression in macrophages by altering histone deacetylase expression. FASEB J 2006;20:1315–27.

89.Kittan N, Allen R, Dhaliwal A, Cavassani K, Schaller M, Gallagher K, et al. Cytokine induced phenotypic and epigenetic signatures are key to establishing specific macrophage phenotypes. PLoS One. 2013;8:e78045. https://doi.org/10.1371/journal.pone.0078045.

90.denDekker AD, Davis FM, Joshi AD, Wolf SJ, Allen R, Lipinski J, et al. TNF-α regulates diabetic macrophage function through the histone acetyltransferase MOF. JCI Insight. 2020;5:e132306. https://doi.org/10.1172/jci.insight.132306.

91.Gordon S, Martinez F. Alternative activation of macrophages: mechanism and functions. Immunity. 2010;32:593–604.

92.Murray P, Allen J, Biswas S, Fisher E, Gilroy D, Goerdt S, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 2014;41:14–20.

93.Frykberg RG, Banks J. Challenges in the treatment of chronic wounds. Adv Wound Care (New Rochelle). 2015;4:560–82.

94.Tottoli EM, Dorati R, Genta I, Chiesa E, Pisani S, Conti B. Skin wound healing process and new emerging Technologies for Skin Wound Care and Regeneration. Pharmaceutics. 2020;12:735. https://doi.org/10.3390/pharmaceutics12080735.

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

96.Larouche J, Sheoran S, Maruyama K, Martino MM. Immune regulation of skin wound healing: mechanisms and novel therapeutic targets. Adv Wound Care (New Rochelle). 2018;7:209–31.

97.Huang Y-Z, Gou M, Da L-C, Zhang W-Q, Xie H-Q. Mesenchymal stem cells for chronic wound healing: current status of preclinical and clinical studies. Tissue Eng Part B Rev. 2020;26:555–70.

98.Geng K, Ma X, Jiang Z, Huang W, Gao C, Pu Y, et al. Innate immunity in diabetic wound healing: focus on the mastermind hidden in chronic inflammatory. Front Pharmacol. 2021;12:653940. https://doi.org/10.3389/fphar.2021.653940.

99.Wang Z, Shi C. Cellular senescence is a promising target for chronic wounds: a comprehensive review. Burns Trauma. 2020;8:tkaa021. https://doi.org/10.3389/fphar.2021.653940.

100.Krzyszczyk P, Schloss R, Palmer A, Berthiaume F. The role of macrophages in acute and chronic wound healing and interventions to promote pro-wound healing phenotypes. Front Physiol. 2018;9:419. https://doi.org/10.3389/fphys.2018.00419.

101.El-Osta A, Brasacchio D, Yao D, Pocai A, Jones P, Roeder R, et al. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med. 2008;205:2409–17.

102.Brasacchio D, Okabe J, Tikellis C, Balcerczyk A, George P, Baker E, et al. Hyperglycemia induces a dynamic cooperativity of histone methylase and demethylase enzymes associated with gene-activating epigenetic marks that coexist on the lysine tail. Diabetes. 2009;58:1229–36.

103.Li M-F, Zhang R, Li T-T, Chen M-Y, Li L-X, Lu J-X, et al. High glucose increases the expression of inflammatory cytokine genes in macrophages through H3K9 Methyltransferase mechanism. J Interf Cytokine Res. 2015;36:48–61.

104.Balasubramanyam M, Aravind S, Gokulakrishnan K, Prabu P, Sathishkumar C, Ranjani H, et al. Impaired miR-146a expression links subclinical inflammation and insulin resistance in type 2 diabetes. Mol Cell Biochem. 2011;351:197–205.

105.Xu J, Wu W, Zhang L, Dorset-Martin W, Morris M, Mitchell M, et al. The role of microRNA-146a in the pathogenesis of the diabetic wound-healing impairment: correction with mesenchymal stem cell treatment. Diabetes. 2012;61:2906–12.

106.Kimball AS, Davis FM, denDekker A, Joshi AD, Schaller MA, Bermick J, et al. The histone Methyltransferase Setdb2 modulates macrophage phenotype and uric acid production in diabetic wound repair. Immunity. 2019;51:258–71.e5.

107.Davis FM, Tsoi LC, Wasikowski R, denDekker A, Joshi A, Wilke C, et al. Epigenetic regulation of the PGE2 pathway modulates macrophage phenotype in normal and pathologic wound repair. JCI Insight. 2020;5:e138443. https://doi.org/10.1172/jci.insight.138443.

108.Ke Q, Costa M. Hypoxia-inducible Factor-1 (HIF-1). Mol Pharmacol. 2006;70:1469–80.

109.Tausendschön M, Dehne N, Brüne B. Hypoxia causes epigenetic gene regulation in macrophages by attenuating Jumonji histone demethylase activity. Cytokine. 2011;53:256–62.

110.Raziyeva K, Kim Y, Zharkinbekov Z, Kassymbek K, Jimi S, Saparov A. Immunology of acute and chronic wound healing. Biomol Ther. 2021;11:700. https://doi.org/10.3390/biom11050700.

111.Alam W, Hasson J, Reed M. Clinical approach to chronic wound management in older adults. J Am Geriatr Soc. 2021;69:2327–34.

112.Ashrafi M, Sebastian A, Shih B, Greaves N, Alonso-Rasgado T, Baguneid M, et al. Whole genome microarray data of chronic wound debridement prior to application of dermal skin substitutes. Wound Repair Regen. 2016;24:870–5.

113.Diamantopoulos PT, Symeonidis A, Pappa V, Kotsianidis I, Galanopoulos A, Pontikoglou C, et al. The effect of 5-azacytidine treatment delays and dose reductions on the prognosis of patients with myelodysplastic syndrome: how to optimize treatment results and outcomes. Br J Haematol. 2021;192:978–87.

114.Kaminskas E, Farrell A, Abraham S, Baird A, Hsieh L-S, Lee S-L, et al. Approval summary: Azacitidine for treatment of myelodysplastic syndrome subtypes. Clin Cancer Res. 2005;11:3604–8.

115.Ma J, Ge Z. Comparison between Decitabine and Azacitidine for patients with acute myeloid Leukemia and higher-risk myelodysplastic syndrome: a systematic review and network meta-analysis. Front Pharmacol. 2021;12:701690. https://doi.org/10.3389/fphar.2021.701690.

116.Jeong H, Kang W, Hong M, Jeong H, Shin M, Jeong M, et al. 5-Azacytidine modulates interferon regulatory factor 1 in macrophages to exert a cardioprotective effect. Sci Rep. 2015;5:15768. https://doi.org/10.1038/srep15768.

117.Kim Y, Kang W, Kwon J, Hong M, Jeong H, Jeong H, et al. Protective role of 5-azacytidine on myocardial infarction is associated with modulation of macrophage phenotype and inhibition of fibrosis. J Cell Mol Med. 2014;18:1018–27.

118.Kim H, Kang H, Rimbach G, Park Y. Heat shock and 5-azacytidine inhibit nitric oxide synthesis and tumor necrosis factor-alpha secretion in activated macrophages. Antioxid Redox Signal. 1999;1:297–304.

119.Wang G, Badylak SF, Heber-Katz E, Braunhut SJ, Gudas LJ. The effects of DNA methyltransferase inhibitors and histone deacetylase inhibitors on digit regeneration in mice. Regen Med. 2010;5:201–20.

120.Gomes FS, de Souza GF, Nascimento LF, Arantes EL, Pedro RM, Vitorino DC, et al. Topical 5-azacytidine accelerates skin wound healing in rats. Wound Repair Regen. 2014;22:640–6.

121.Cao Q, Wang X, Jia L, Mondal A, Diallo A, Hawkins G, et al. Inhibiting DNA methylation by 5-Aza-2′-deoxycytidine ameliorates atherosclerosis through suppressing macrophage inflammation. Endocrinology. 2014;155:4925–38.

122.Thangavel J, Samanta S, Rajasingh S, Barani B, Xuan Y, Dawn B, et al. Epigenetic modifiers reduce inflammation and modulate macrophage phenotype during endotoxemia-induced acute lung injury. J Cell Sci. 2015;128:3094–105.

123.Hams E, Saunders SP, Cummins EP, O'Connor A, Tambuwala MT, Gallagher WM, et al. The hydroxylase inhibitor dimethyloxallyl glycine attenuates endotoxic shock via alternative activation of macrophages and IL-10 production by B1 cells. Shock. 2011;36:295–302.

124.Jeong SY, Lee JH, Kim HS, Hong SH, Cheong CH, Kim IK. 3-deazaadenosine analogues inhibit the production of tumour necrosis factor-α in RAW264.7 cells stimulated with lipopolysaccharide. Immunology. 1996;89:558–62.

125.Van den Bossche J, Neele A, Hoeksema M, de Heij F, Boshuizen M, van der Velden S, et al. Inhibiting epigenetic enzymes to improve atherogenic macrophage functions. Biochem Biophys Res Commun. 2014;455:396–402.

126.Keyel P, Romero M, Wu W, Kwak D, Zhu Q, Liu X, et al. Methylthioadenosine reprograms macrophage activation through adenosine receptor stimulation. PLoS One. 2014;9:e104210. https://doi.org/10.1371/journal.pone.0104210.

127.Ara A, Xia M, Ramani K, Mato J, Lu S. S-adenosylmethionine inhibits lipopolysaccharide-induced gene expression via modulation of histone methylation. Hepatology (Baltimore, MD). 2008;47:1655–66.

128.Stammler D, Eigenbrod T, Menz S, Frick JS, Sweet MJ, Shakespear MR, et al. Inhibition of histone deacetylases permits lipopolysaccharide-mediated secretion of bioactive IL-1β via a Caspase-1-independent mechanism. J Immunol. 2015;195:5421–31.

129.Du J, Wei N, Guan T, Xu H, An J, Pritchard K, et al. Inhibition of CDKS by roscovitine suppressed LPS-induced *NO production through inhibiting NFkappaB activation and BH4 biosynthesis in macrophages. Am J Physiol Cell Physiol. 2009;297:C742–9.

130.Guimarães MR, Leite FRM, Spolidorio LC, Kirkwood KL, Rossa C, Jr. Curcumin abrogates LPS-induced pro-inflammatory cytokines in RAW 264.7 macrophages. Evidence for novel mechanisms involving SOCS-1, −3 and p38 MAPK. Arch Oral Biol. 2013;58:1309–17.

131.Zhong Y, Liu T, Lai W, Tan Y, Tian D, Guo Z. Heme oxygenase-1-mediated reactive oxygen species reduction is involved in the inhibitory effect of curcumin on lipopolysaccharide-induced monocyte chemoattractant protein-1 production in RAW264.7 macrophages. Mol Med Rep. 2013;7:242–6.

132.Zhou Y, Zhang T, Wang X, Wei X, Chen Y, Guo L, et al. Curcumin modulates macrophage polarization through the inhibition of the toll-like receptor 4 expression and its Signaling pathways. Cell Physiol Biochem. 2015;36:631–41.

133.Xu Y, Liu L. Curcumin alleviates macrophage activation and lung inflammation induced by influenza virus infection through inhibiting the NF-κB signaling pathway. Influenza Other Respir Viruses. 2017;11:457–63.

134.Chen F-Y, Zhou J, Guo N, Ma W-G, Huang X, Wang H, et al. Curcumin retunes cholesterol transport homeostasis and inflammation response in M1 macrophage to prevent atherosclerosis. Biochem Biophys Res Commun. 2015;467:872–8.

135.Gao S, Zhou J, Liu N, Wang L, Gao Q, Wu Y, et al. Curcumin induces M2 macrophage polarization by secretion IL-4 and/or IL-13. J Mol Cell Cardiol. 2015;85:131–9.

136.Manca M, Castangia I, Zaru M, Nácher A, Valenti D, Fernàndez-Busquets X, et al. Development of curcumin loaded sodium hyaluronate immobilized vesicles (hyalurosomes) and their potential on skin inflammation and wound restoring. Biomaterials. 2015;71:100–9.

137.Zakerikhoob M, Abbasi S, Yousefi G, Mokhtari M, Noorbakhsh M. Curcumin-incorporated crosslinked sodium alginate-g-poly (N-isopropyl acrylamide) thermo-responsive hydrogel as an in-situ forming injectable dressing for wound healing: in vitro characterization and in vivo evaluation. Carbohydr Polym. 2021;271:118434. https://doi.org/10.1016/j.carbpol.2021.118434.

138.Xia S, Weng T, Jin R, Yang M, Yu M, Zhang W, et al. Curcumin-incorporated 3D bioprinting gelatin methacryloyl hydrogel reduces reactive oxygen species-induced adipose-ederived stem cell apoptosis and improves implanting survival in diabetic wounds. Burns Trauma. 2022;10:tkac001. https://doi.org/10.1093/burnst/tkac001.

139.Cabanel M, da Costa TP, El-Cheikh MC, Carneiro K. The epigenome as a putative target for skin repair: the HDAC inhibitor Trichostatin a modulates myeloid progenitor plasticity and behavior and improves wound healing. J Transl Med. 2019;17:247. https://doi.org/10.1186/s12967-019-1998-9.

140.Leus N, van den Bosch T, van der Wouden P, Krist K, Ourailidou M, Eleftheriadis N, et al. HDAC1-3 inhibitor MS-275 enhances IL10 expression in RAW264.7 macrophages and reduces cigarette smoke-induced airway inflammation in mice. Sci Rep. 2017;7:45047. https://doi.org/10.1038/srep45047.

141.Lohman R, Iyer A, Fairlie T, Cotterell A, Gupta P, Reid R, et al. Differential anti-inflammatory activity of HDAC inhibitors in human macrophages and rat arthritis. J Pharmacol Exp Ther. 2016;356:387–96.

142.Roger T, Lugrin J, Le Roy D, Goy G, Mombelli M, Koessler T, et al. Histone deacetylase inhibitors impair innate immune responses to toll-like receptor agonists and to infection. Blood. 2011;117:1205–17.

143.Jambalganiin U, Tsolmongyn B, Koide N, Odkhuu E, Naiki Y, Komatsu T, et al. A novel mechanism for inhibition of lipopolysaccharide-induced proinflammatory cytokine production by valproic acid. Int Immunopharmacol. 2014;20:181–7.

144.Ji J, Shu D, Zheng M, Wang J, Luo C, Wang Y, et al. Microbial metabolite butyrate facilitates M2 macrophage polarization and function. Sci Rep. 2016;6:24838. https://doi.org/10.1038/srep24838.

145.Aguilar E, Leonel A, Teixeira L, Silva A, Silva J, Pelaez J, et al. Butyrate impairs atherogenesis by reducing plaque inflammation and vulnerability and decreasing NFκB activation. Nutr Metab Cardiovasc Dis. 2014;24:606–13.

146.Chang P, Hao L, Offermanns S, Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci U S A. 2014;111:2247–52.

147.Halili MA, Andrews MR, Labzin LI, Schroder K, Matthias G, Cao C, et al. Differential effects of selective HDAC inhibitors on macrophage inflammatory responses to the toll-like receptor 4 agonist LPS. J Leukoc Biol. 2010;87:1103–14.

148.Ohira H, Fujioka Y, Katagiri C, Mamoto R, Aoyama-Ishikawa M, Amako K, et al. Butyrate attenuates inflammation and lipolysis generated by the interaction of adipocytes and macrophages. J Atheroscler Thromb. 2013;20:425–42.

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