Metabolic reprogramming in skin wound healing

Zitong Wang , Feng Zhao , Chengcheng Xu , Qiqi Zhang , Haiyue Ren , Xing Huang , Cai He , Jiajie Ma , Zhe Wang

Burns & Trauma ›› 2024, Vol. 12 ›› Issue (1) : tkad047

PDF (1386KB)
Burns & Trauma ›› 2024, Vol. 12 ›› Issue (1) :tkad047 DOI: 10.1093/burnst/tkad047
Review
research-article
Metabolic reprogramming in skin wound healing
Author information +
History +
PDF (1386KB)

Abstract

Metabolic reprogramming refers to the ability of a cell to alter its metabolism in response to different stimuli and forms of pressure. It helps cells resist external stress and provides them with new functions. Skin wound healing involves the metabolic reprogramming of nutrients, such as glucose, lipids, and amino acids, which play vital roles in the proliferation, differentiation, and migration of multiple cell types. During the glucose metabolic process in wounds, glucose transporters and key enzymes cause elevated metabolite levels. Glucose-mediated oxidative stress drives the proinflammatory response and promotes wound healing. Reprogramming lipid metabolism increases the number of fibroblasts and decreases the number of macrophages. It enhances local neovascularization and improves fibrin stability to promote extracellular matrix remodelling, accelerates wound healing, and reduces scar formation. Reprogramming amino acid metabolism affects wound re-epithelialization, collagen deposition, and angiogenesis. However, comprehensive reviews on the role of metabolic reprogramming in skin wound healing are lacking. Therefore, we have systematically reviewed the metabolic reprogramming of glucose, lipids, and amino acids during skin wound healing. Notably, we identified their targets with potential therapeutic value and elucidated their mechanisms of action.

Keywords

Metabolic reprogramming / Wound healing / Skin / Molecular mechanism / Therapeutic potential

Cite this article

Download citation ▾
Zitong Wang, Feng Zhao, Chengcheng Xu, Qiqi Zhang, Haiyue Ren, Xing Huang, Cai He, Jiajie Ma, Zhe Wang. Metabolic reprogramming in skin wound healing. Burns & Trauma, 2024, 12 (1) : tkad047 DOI:10.1093/burnst/tkad047

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Schreml S, Szeimies RM, Prantl L, Landthaler M, Babilas P. Wound healing in the 21st century. J Am Acad Dermatol. 2010; 63: 866-81.

[2]

Broughton GN, Janis JE, Attinger CE. Wound healing: an overview. Plast Reconstr Surg. 2006; 117: 1e-S-32e-S.

[3]

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

[4]

Phillipson M, Kubes P. The healing power of neutrophils. Trends Immunol. 2019; 40: 635-47.

[5]

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

[6]

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

[7]

Talbott HE, Mascharak S, Griffin M, Wan DC, Longaker MT. Wound healing, fibroblast heterogeneity, and fibrosis. Cell Stem Cell. 2022; 29: 1161-80.

[8]

Pastar I, Stojadinovic O, Yin NC, Ramirez H, Nusbaum AG, Sawaya A, et al. Epithelialization in wound healing: a comprehensive review. Adv Wound Care (New Rochelle). 2014; 3: 445-64.

[9]

Hinz B.Formation and function of the myofibroblast during tissue repair. J Invest Dermatol. 2007; 127: 526-37.

[10]

Widgerow AD. Cellular/extracellular matrix cross-talk in scar evolution and control. Wound Repair Regen. 2011; 19: 117-33.

[11]

Ehrlich HP, Tarver H, Hunt TK. Inhibitory effects of vitamin E on collagen synthesis and wound repair. Ann Surg. 1972; 175: 235-40.

[12]

Stincone A, Prigione A, Cramer T, Wamelink MM, Campbell K, Cheung E, et al. The return of metabolism: biochemistry and physiology of the pentose phosphate pathway. Biol Rev Camb Philos Soc. 2015; 90: 927-63.

[13]

Phan AT, Goldrath AW, Glass CK. Metabolic and epigenetic coordination of T cell and macrophage immunity. Immunity. 2017; 46: 714-29.

[14]

Balestrieri B, Di Costanzo D, Dwyer DF. Macrophage-mediated immune responses: from fatty acids to Oxylipins. Molecules. 2021; 27: 152-67. https://doi.org/10.3390/molecules27010152.

[15]

Pils V, Terlecki-Zaniewicz L, Schosserer M, Grillari J, Lämmermann I. The role of lipid-based signalling in wound healing and senescence. Mech Ageing Dev. 2021; 198: 111527.

[16]

Vettore L, Westbrook RL, Tennant DA. New aspects of amino acid metabolism in cancer. Br J Cancer. 2020; 122: 150-6.

[17]

Wang S, Liu R, Yu Q, Dong L, Bi Y, Liu G. Metabolic reprogramming of macrophages during infections and cancer. Cancer Lett. 2019; 452: 14-22.

[18]

Yoshida GJ. Metabolic reprogramming: the emerging concept and associated therapeutic strategies. J Exp Clin Cancer Res. 2015; 34: 111.

[19]

Russo S, Kwiatkowski M, Govorukhina N, Bischoff R, Melgert BN. Meta-inflammation and metabolic reprogramming of macrophages in diabetes and obesity: the importance of metabolites. Front Immunol. 2021; 12: 746151.

[20]

Zhu L, Zhao Q, Yang T, Ding W, Zhao Y. Cellular metabolism and macrophage functional polarization. Int Rev Immunol. 2015; 34: 82-100.

[21]

Cibrian D, de la Fuente H, Sánchez-Madrid F. Metabolic pathways that control skin homeostasis and inflammation. Trends Mol Med. 2020; 26: 975-86.

[22]

Li X, Kumar A, Carmeliet P. Metabolic pathways Fueling the endothelial cell drive. Annu Rev Physiol. 2019; 81: 483-503.

[23]

Eming SA, Murray PJ, Pearce EJ. Metabolic orchestration of the wound healing response. Cell Metab. 2021; 33: 1726-43.

[24]

Manchanda M, Torres M, Inuossa F, Bansal R, Kumar R, Hunt M, et al. Metabolic reprogramming and reliance in human skin wound healing. J Invest Dermatol. 2023; 143: 2039-51. https://doi.org/10.1016/j.jid.2023.02.039.

[25]

Wang Y, Beekman J, Hew J, Jackson S, Issler-Fisher AC, Parungao R, et al. Burn injury: challenges and advances in burn wound healing, infection, pain and scarring. Adv Drug Deliv Rev. 2018; 123: 3-17.

[26]

Falanga V. Wound healing and its impairment in the diabetic foot. Lancet. 2005; 366: 1736-43.

[27]

Hart T, Milner R, Cifu A. Management of a Diabetic Foot. JAMA. 2017; 318: 1387-8.

[28]

Singh N, Armstrong DG, Lipsky BA. Preventing foot ulcers in patients with diabetes. JAMA. 2005; 293: 217-28.

[29]

Tohma A, Ohkura N, Yoshiba K, Takeuchi R, Yoshiba N, Edanami N, et al. Glucose transporter 2 and 4 are involved in glucose supply during pulpal wound healing after Pulpotomy with mineral trioxide aggregate in rat molars. J Endod. 2020; 46: 81-8.

[30]

Mathew SA, Chandravanshi B, Bhonde R. Hypoxia primed placental mesenchymal stem cells for wound healing. Life Sci. 2017; 182: 85-92.

[31]

Xie W, Hu W, Huang Z, Li M, Zhang H, Huang X, et al. Betulinic acid accelerates diabetic wound healing by modulating hyperglycemia-induced oxidative stress, inflammation and glucose intolerance. Burns Trauma. 2022; 10: tkac007.

[32]

Freemerman AJ, Johnson AR, Sacks GN, Milner JJ, Kirk EL, Troester MA, et al. Metabolic reprogramming of macrophages: glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a proinflammatory phenotype. J Biol Chem. 2014; 289: 7884-96.

[33]

Vinaik R, Barayan D, Auger C, Abdullahi A, Jeschke MG. Regulation of glycolysis and the Warburg effect in wound healing. JCI Insight. 2020; 5:e138949. https://doi.org/10.1172/jci.insight.138949.

[34]

Nguyen DT, Keast D. Maximal activities of glutaminase, citrate synthase, hexokinase, 6-phosphofructokinase and lactate dehydrogenase in skin of immune-competent Balb/c and immune-deficient Balb/c (nu/nu) mice during wound healing. Int J BioChemiPhysics. 1991; 23: 589-93.

[35]

Gupta A, Raghubir R. Energy metabolism in the granulation tissue of diabetic rats during cutaneous wound healing. Mol Cell Biochem. 2005; 270: 71-7.

[36]

Zahra K, Dey T, Ashish MSP, Pandey U. Pyruvate kinase M2 and cancer: the role of PKM2 in promoting tumorigenesis. Front Oncologia. 2020; 10: 159.

[37]

Zhang Z, Ito WD, Hopfner U, Böhmert B, Kremer M, Reckhenrich AK, et al. The role of single cell derived vascular resident endothelial progenitor cells in the enhancement of vascularization in scaffold-based skin regeneration. Biomaterials. 2011; 32: 4109-17.

[38]

Ren R, Guo J, Shi J, Tian Y, Li M, Kang H. PKM2 regulates angiogenesis of VR-EPCs through modulating glycolysis, mitochondrial fission, and fusion. J Cell Physiol. 2020; 235: 6204-17.

[39]

Zhang Y, Li L, Liu Y, Liu ZR. PKM2 released by neutrophils at wound site facilitates early wound healing by promoting angiogenesis. Wound Repair Regen. 2016; 24: 328-36.

[40]

Gómez-Escudero J, Clemente C, García-Weber D, Acín-Pérez R, Millán J, Enríquez JA, et al. PKM2 regulates endothelial cell junction dynamics and angiogenesis via ATP production. Sci Rep. 2019; 9: 15022.

[41]

Sych K, Nold SP, Pfeilschifter J, Vutukuri R, Meisterknecht J, Wittig I, et al. Expression of PKM2 in wound keratinocytes is coupled to angiogenesis during skin repair in vivo and in HaCaT keratinocytes in vitro. J Mol Med (Berl). 2023; 101: 151-69.

[42]

Forkasiewicz A, Dorociak M, Stach K, Szelachowski P, Tabola R, Augoff K. The usefulness of lactate dehydrogenase measurements in current oncological practice. Cell Mol Biol Lett. 2020; 25: 35.

[43]

Constant JS, Feng JJ, Zabel DD, Yuan H, Suh DY, Scheuenstuhl H, et al. Lactate elicits vascular endothelial growth factor from macrophages: a possible alternative to hypoxia. Wound Repair Regen. 2000; 8: 353-60.

[44]

Porporato PE, Payen VL, De Saedeleer CJ, Préat V, Thissen JP, Feron O, et al. Lactate stimulates angiogenesis and accelerates the healing of superficial and ischemic wounds in mice. Angiogenesis. 2012; 15: 581-92.

[45]

Jeffery MR, Jane WH, Wijeratne D, William FM, San WH, O’Handley R. Secreted biofilm factors adversely affect cellular wound healing responses in vitro. Sci Rep. 2015; 5: 13296.

[46]

Kim JH, Bae KH, Byun JK, Lee S, Kim JG, Lee IK, et al. Lactate dehydrogenase-a is indispensable for vascular smooth muscle cell proliferation and migration. Biochem Biophys Res Commun. 2017; 492: 41-7.

[47]

Levoux J, Prola A, Lafuste P, Gervais M, Chevallier N, Koumaiha Z, et al. Platelets facilitate the wound-healing capability of mesenchymal stem cells by mitochondrial transfer and metabolic reprogramming. Cell Metab. 2021; 33: 283-299.e9.

[48]

Zhou RH, Yao M, Lee TS, Zhu Y, Martins-Green M, Shyy JY. Vascular endothelial growth factor activation of sterol regulatory element binding protein: a potential role in angiogenesis. Circ Res. 2004; 95: 471-8.

[49]

Horton JD, Shimomura I, Brown MS, Hammer RE, Goldstein JL, Shimano H. Activation of cholesterol synthesis in preference to fatty acid synthesis in liver and adipose tissue of transgenic mice overproducing sterol regulatory element-binding protein-2. J Clin Invest. 1998; 101: 2331-9.

[50]

Pai JT, Guryev O, Brown MS, Goldstein JL. Differential stimulation of cholesterol and unsaturated fatty acid biosynthesis in cells expressing individual nuclear sterol regulatory element-binding proteins. J Biol Chem. 1998; 273: 26138-48.

[51]

Yao M, Zhou RH, Petreaca M, Zheng L, Shyy J, Martins-Green M. Activation of sterol regulatory element-binding proteins (SREBPs) is critical in IL-8-induced angiogenesis. J Leukoc Biol. 2006; 80: 608-20.

[52]

Oishi Y, Spann NJ, Link VM, Muse ED, Strid T, Edillor C, et al. SREBP1 contributes to resolution of pro-inflammatory TLR4 Signaling by reprogramming fatty acid metabolism. Cell Metab. 2017; 25: 412-27.

[53]

Lee HJ, Jung YH, Choi GE, Ko SH, Lee SJ, Lee SH, et al. BNIP3 induction by hypoxia stimulates FASN-dependent free fatty acid production enhancing therapeutic potential of umbilical cord blood-derived human mesenchymal stem cells. Redox Biol. 2017; 13: 426-43.

[54]

Ip W, Hoshi N, Shouval DS, Snapper S, Medzhitov R. Anti-inflammatory effect of IL-10 mediated by metabolic reprogramming of macrophages. Science. 2017; 356: 513-9.

[55]

Ecker J, Liebisch G, Englmaier M, Grandl M, Robenek H, Schmitz G. Induction of fatty acid synthesis is a key requirement for phagocytic differentiation of human monocytes. Proc Natl Acad Sci U S A. 2010; 107: 7817-22.

[56]

Nakayama Y, Fujiu K, Yuki R, Oishi Y, Morioka MS, Isagawa T, et al. A long noncoding RNA regulates inflammation resolution by mouse macrophages through fatty acid oxidation activation. Proc Natl Acad Sci U S A. 2020; 117: 14365-75.

[57]

Zhang S, Weinberg S, DeBerge M, Gainullina A, Schipma M, Kinchen JM, et al. Efferocytosis fuels requirements of fatty acid oxidation and the electron transport chain to polarize macrophages for tissue repair. Cell Metab. 2019; 29: 443-456.e5.

[58]

Hokynková A, Nováková M, Babula P, Sedláčková M, Paulová H, Hlaváčová M, et al. Fatty acid supplementation affects skin wound healing in a rat model. Nutrients. 2022; 14. https://doi.org/10.3390/nu14112245.

[59]

Cardoso CR, Favoreto SJ, Oliveira LL, Vancim JO, Barban GB, Ferraz DB, et al. Oleic acid modulation of the immune response in wound healing: a new approach for skin repair. Immunobiology. 2011; 216: 409-15.

[60]

Cardoso CR, Souza MA, Ferro EA, Favoreto SJ, Pena JD. Influence of topical administration of n-3 and n-6 essential and n-9 nonessential fatty acids on the healing of cutaneous wounds. Wound Repair Regen. 2004; 12: 235-43.

[61]

Babaei S, Ansarihadipour H, Nakhaei M, Darabi M, Bayat P, Sakhaei M, et al. Effect of Omegaven on mast cell concentration in diabetic wound healing. J Tissue Viability. 2017; 26: 125-30.

[62]

Babaei S, Nakhaei M, Ansarihadipour H, Sakhaei M, Hosseini S, Nikgoftar A. Omegaven improves skin morphometric indices in diabetic rat model wound healing. J Am Coll Clin Wound Spec. 2017; 9: 39-45.

[63]

Bardaa S, Ben HN, Aloui F, Ben MR, Jabeur H, Bouaziz M, et al. Oil from pumpkin (Cucurbita pepo L.) seeds: evaluation of its functional properties on wound healing in rats. Lipids Health Dis. 2016; 15: 73.

[64]

Gál P, Toporcer T, Grendel T, Vidová Z, Smetana KJ, Dvoránková B, et al. Effect of Atropa belladonna L. on skin wound healing: biomechanical and histological study in rats and in vitro study in keratinocytes, 3T3 fibroblasts, and human umbilical vein endothelial cells. Wound Repair Regen. 2009; 17: 378-86.

[65]

Park NY, Valacchi G, Lim Y. Effect of dietary conjugated linoleic acid supplementation on early inflammatory responses during cutaneous wound healing. Mediat Inflamm. 2010; 2010: 342328.

[66]

Chang CS, Sun HL, Lii CK, Chen HW, Chen PY, Liu KL. Gamma-linolenic acid inhibits inflammatory responses by regulating NF-kappaB and AP-1 activation in lipopolysaccharide-induced RAW 264.7 macrophages. Inflammation. 2010; 33: 46-57.

[67]

Rossen NS, Hansen AJ, Selhuber-Unkel C, Oddershede LB. Arachidonic acid randomizes endothelial cell motion and regulates adhesion and migration. PLoS One. 2011; 6: e25196.

[68]

Sivamani RK. Eicosanoids and keratinocytes in wound healing. Adv Wound Care (New Rochelle). 2014; 3: 476-81.

[69]

Grubauer G, Feingold KR, Harris RM, Elias PM.Lipid content and lipid type as determinants of the epidermal permeability barrier. J Lipid Res. 1989; 30: 89-96.

[70]

Lampe MA, Burlingame AL, Whitney J, Williams ML, Brown BE, Roitman E, et al. Human stratum corneum lipids: characterization and regional variations. J Lipid Res. 1983; 24: 120-30.

[71]

Schiefelbein D, Goren I, Fisslthaler B, Schmidt H, Geisslinger G, Pfeilschifter J, et al. Biphasic regulation of HMG-CoA reductase expression and activity during wound healing and its functional role in the control of keratinocyte angiogenic and proliferative responses. J Biol Chem. 2008; 283: 15479-90.

[72]

Tan A, Levrey H, Dahm C, Polunovsky VA, Rubins J, Bitterman PB. Lovastatin induces fibroblast apoptosis in vitro and in vivo. A possible therapy for fibroproliferative disorders. Am J Respir Crit Care Med. 1999; 159: 220-7.

[73]

Indolfi C, Cioppa A, Stabile E, Di Lorenzo E, Esposito G, Pisani A, et al. Effects of hydroxymethylglutaryl coenzyme a reductase inhibitor simvastatin on smooth muscle cell proliferation in vitro and neointimal formation in vivo after vascular injury. J Am Coll Cardiol. 2000; 35: 214-21.

[74]

Ko JH, Kim PS, Zhao Y, Hong SJ, Mustoe TA. HMG-CoA reductase inhibitors (statins) reduce hypertrophic scar formation in a rabbit ear wounding model. Plast Reconstr Surg. 2012; 129: 252e-61.

[75]

Vincent L, Chen W, Hong L, Mirshahi F, Mishal Z, Mirshahi-Khorassani T, et al. Inhibition of endothelial cell migration by cerivastatin, an HMG-CoA reductase inhibitor: contribution to its anti-angiogenic effect. FEBS Lett. 2001; 495: 159-66.

[76]

Vincent L, Soria C, Mirshahi F, Opolon P, Mishal Z, Vannier JP, et al. Cerivastatin, an inhibitor of 3-hydroxy-3-methylglutaryl coenzyme a reductase, inhibits endothelial cell proliferation induced by angiogenic factors in vitro and angiogenesis in in vivo models. Arterioscler Thromb Vasc Biol. 2002; 22: 623-9.

[77]

Aarons CB, Cohen PA, Gower A, Reed KL, Leeman SE, Stucchi AF, et al. Statins (HMG-CoA reductase inhibitors) decrease postoperative adhesions by increasing peritoneal fibrinolytic activity. Ann Surg. 2007; 245: 176-84.

[78]

Ansell BJ, Watson KE, Fogelman AM, Navab M, Fonarow GC. High-density lipoprotein function recent advances. J Am Coll Cardiol. 2005; 46: 1792-8.

[79]

Kimura T, Tomura H, Mogi C, Kuwabara A, Damirin A, Ishizuka T, et al. Role of scavenger receptor class B type I and sphingosine 1-phosphate receptors in high density lipoprotein-induced inhibition of adhesion molecule expression in endothelial cells. J Biol Chem. 2006; 281: 37457-67.

[80]

Murphy AJ, Woollard KJ. High-density lipoprotein: a potent inhibitor of inflammation. Clin Exp Pharmacol Physiol. 2010; 37: 710-8.

[81]

Bursill CA, Castro ML, Beattie DT, Nakhla S, van der Vorst E, Heather AK, et al. High-density lipoproteins suppress chemokines and chemokine receptors in vitro and in vivo. Arterioscler Thromb Vasc Biol. 2010; 30: 1773-8.

[82]

Guccione E, Richard S. The regulation, functions and clinical relevance of arginine methylation. Nat Rev Mol Cell Biol. 2019; 20: 642-57.

[83]

Kämpfer H, Pfeilschifter J, Frank S. Expression and activity of arginase isoenzymes during normal and diabetes-impaired skin repair. J Invest Dermatol. 2003; 121: 1544-51.

[84]

Goumas G, Tentolouris C, Tousoulis D, Stefanadis C, Toutouzas P. Therapeutic modification of the L-arginine-eNOS pathway in cardiovascular diseases. Atherosclerosis. 2001; 154: 255-67.

[85]

Nguyen MC, Park JT, Jeon YG, Jeon BH, Hoe KL, Kim YM, et al. Arginase inhibition restores Peroxynitrite-induced endothelial dysfunction via L-arginine-dependent endothelial nitric oxide synthase phosphorylation. Yonsei Med J. 2016; 57: 1329-38.

[86]

Surks HK. cGMP-dependent protein kinase I and smooth muscle relaxation: a tale of two isoforms. Circ Res. 2007; 101: 1078-80.

[87]

Lehners M, Dobrowinski H, Feil S, Feil R. cGMP Signaling and vascular smooth muscle cell plasticity. J Cardiovasc Dev Dis. 2018; 5: 20.

[88]

Grandvuillemin I, Buffat C, Boubred F, Lamy E, Fromonot J, Charpiot P, et al. Arginase upregulation and eNOS uncoupling contribute to impaired endothelium-dependent vasodilation in a rat model of intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol. 2018; 315: R509-20.

[89]

Kim JH, Bugaj LJ, Oh YJ, Bivalacqua TJ, Ryoo S, Soucy KG, et al. Arginase inhibition restores NOS coupling and reverses endothelial dysfunction and vascular stiffness in old rats. J Appl Physiol (1985). 2009; 107: 1249-57.

[90]

Swierczynski J, Hebanowska A, Sledzinski T. Role of abnormal lipid metabolism in development, progression, diagnosis and therapy of pancreatic cancer. World J Gastroenterol. 2014; 20: 2279-303.

[91]

Campos AC, Groth AK, Branco AB. Assessment and nutritional aspects of wound healing. Curr Opin Clin Nutr Metab Care. 2008; 11: 281-8.

[92]

Arnold M, Barbul A. Nutrition and wound healing. Plast Reconstr Surg. 2006; 117: 42S-58.

[93]

Murphy C, Newsholme P. Importance of glutamine metabolism in murine macrophages and human monocytes to L-arginine biosynthesis and rates of nitrite or urea production. Clin Sci (Lond). 1998; 95: 397-407.

[94]

Blass SC, Goost H, Tolba RH, Stoffel-Wagner B, Kabir K, Burger C, et al. Time to wound closure in trauma patients with disorders in wound healing is shortened by supplements containing antioxidant micronutrients and glutamine: a PRCT. Clin Nutr. 2012; 31: 469-75.

[95]

Sproston NR, Ashworth JJ. Role of C-reactive protein at sites of inflammation and infection. Front Immunol. 2018; 9: 754.

[96]

Johnson BZ, Stevenson AW, Prêle CM, Fear MW, Wood FM. The role of IL-6 in skin fibrosis and cutaneous wound healing. Biomedicine. 2020; 8: 101.

[97]

van der Vos KE, Eliasson P, Proikas-Cezanne T, Vervoort SJ, van Boxtel R, Putker M, et al. Modulation of glutamine metabolism by the PI(3)K-PKB-FOXO network regulates autophagy. Nat Cell Biol. 2012; 14: 829-37.

[98]

Qiang L, Yang S, Cui YH, He YY. Keratinocyte autophagy enables the activation of keratinocytes and fibroblasts and facilitates wound healing. Autophagy. 2021; 17: 2128-43.

[99]

Chen X, Tong G, Fan J, Shen Y, Wang N, Gong W, et al. FGF21 promotes migration and differentiation of epidermal cells during wound healing via SIRT1-dependent autophagy. Br J Pharmacol. 2022; 179: 1102-21.

[100]

Ren H, Zhao F, Zhang Q, Huang X, Wang Z. Autophagy and skin wound healing. Burns Trauma. 2022; 10: tkac003.

[101]

Gao Y, Luo C, Rui T, Fan Y, Yao Y, Shen H, et al. Autophagy inhibition facilitates wound closure partially dependent on the YAP/IL-33 signaling in a mouse model of skin wound healing. FASEB J. 2021; 35: e21920.

[102]

Sylakowski K, Wells A. ECM-regulation of autophagy: the yin and the yang of autophagy during wound healing. Matrix Biol. 2021; 100-101: 197-206.

[103]

Lee LY, Oldham WM, He H, Wang R, Mulhern R, Handy DE, et al. Interferon-γ impairs human coronary artery endothelial glucose metabolism by tryptophan catabolism and activates fatty acid oxidation. Circulation. 2021; 144: 1612-28.

[104]

Morino-Koga S, Uchi H, Mitoma C, Wu Z, Kiyomatsu M, Fuyuno Y, et al. 6-Formylindolo[3,2-b]Carbazole accelerates skin wound healing via activation of ERK, but not aryl hydrocarbon receptor. J Invest Dermatol. 2017; 137: 2217-26.

[105]

Ito H, Ando T, Ogiso H, Arioka Y, Saito K, Seishima M. Inhibition of indoleamine 2,3-dioxygenase activity accelerates skin wound healing. Biomaterials. 2015; 53: 221-8.

[106]

Apolinário PP, Zanchetta FC, Breder J, Adams G, Consonni SR, Gillis R, et al. Anti-inflammatory, procollagen, and wound repair properties of topical insulin gel. Braz J Med Biol Res. 2023; 56: e12640.

[107]

Yang P, Wang X, Wang D, Shi Y, Zhang M, Yu T, et al. Topical insulin application accelerates diabetic wound healing by promoting anti-inflammatory macrophage polarization. J Cell Sci. 2020; 133:jcs235838.

[108]

Liang Y, Li M, Yang Y, Qiao L, Xu H, Guo B. pH/glucose dual responsive metformin release hydrogel dressings with adhesion and self-healing via dual-dynamic bonding for athletic diabetic foot wound healing. ACS Nano. 2022; 16: 3194-207.

[109]

Yang J, Zeng W, Xu P, Fu X, Yu X, Chen L, et al. Glucose-responsive multifunctional metal-organic drug-loaded hydrogel for diabetic wound healing. Acta Biomater. 2022; 140: 206-18.

[110]

Hytönen J, Leppänen O, Braesen JH, Schunck WH, Mueller D, Jung F, et al. Activation of peroxisome proliferator-activated receptor-δ as novel therapeutic strategy to prevent in-stent restenosis and stent thrombosis. Arterioscler Thromb Vasc Biol. 2016; 36: 1534-48.

[111]

Danhier F, Ansorena E, Silva JM, Coco R, Le Breton A, Préat V. PLGA-based nanoparticles: an overview of biomedical applications. J Control Release. 2012; 161: 505-22.

[112]

Zheng Z, Liu Y, Huang W, Mo Y, Lan Y, Guo R, et al. Neurotensin-loaded PLGA/CNC composite nanofiber membranes accelerate diabetic wound healing. Artif Cells Nanomed Biotechnol. 2018; 46: 493-501.

[113]

Chereddy KK, Coco R, Memvanga PB, Ucakar B, Des Rieux A, Vandermeulen G, et al. Combined effect of PLGA and curcumin on wound healing activity. J Control Release. 2013; 171: 208-15.

[114]

Chereddy KK, Her CH, Comune M, Moia C, Lopes A, Porporato PE, et al. PLGA nanoparticles loaded with host defense peptide LL37 promote wound healing. J Control Release. 2014; 194: 138-47.

[115]

Gourishetti K, Keni R, Nayak PG, Jitta SR, Bhaskaran NA, Kumar L, et al. Sesamol-loaded PLGA Nanosuspension for accelerating wound healing in diabetic foot ulcer in rats. Int J Nanomedicine. 2020; 15: 9265-82.

[116]

Abu EHA, Klein D, Bekeny JC, Severin JH, Zolper EG, Tefera E, et al. The impact of statins on wound healing: an ally in treating the highly comorbid patient. J Wound Care. 2022; 31: S36-41.

[117]

Ala S, Alvandipour M, Saeedi M, Hamidian M, Shiva A, Rahmani N, et al. Effects of topical atorvastatin (2%) on Posthemorrhoidectomy pain and wound healing: a randomized double-blind placebo-controlled clinical trial. World J Surg. 2017; 41: 596-602.

[118]

Wang CC, Yang PW, Yang SF, Hsieh KP, Tseng SP, Lin YC. Topical simvastatin promotes healing of Staphylococcus aureus-contaminated cutaneous wounds. Int Wound J. 2016; 13: 1150-7.

[119]

Xie P, Dolivo DM, Jia S, Cheng X, Salcido J, Galiano RD, et al. Liposome-encapsulated statins reduce hypertrophic scarring through topical application. Wound Repair Regen. 2020; 28: 460-9.

[120]

Sawaya AP, Pastar I, Stojadinovic O, Lazovic S, Davis SC, Gil J, et al. Topical mevastatin promotes wound healing by inhibiting the transcription factor c-Myc via the glucocorticoid receptor and the long non-coding RNA Gas5. J Biol Chem. 2018; 293: 1439-49.

[121]

Yoon J, Yoon D, Lee H, Lee J, Jo S, Kym D, et al. Wound healing ability of acellular fish skin and bovine collagen grafts for split-thickness donor sites in burn patients: characterization of acellular grafts and clinical application. Int J Biol Macromol. 2022; 205: 452-61.

[122]

Zhang Z, Wang S, Diao Y, Zhang J, Lv D. Fatty acid extracts from Lucilia sericata larvae promote murine cutaneous wound healing by angiogenic activity. Lipids Health Dis. 2010; 9: 24.

[123]

Ishak W, Katas H, Yuen NP, Abdullah MA, Zulfakar MH. Topical application of omega-3-, omega-6-, and omega-9-rich oil emulsions for cutaneous wound healing in rats. Drug Deliv Transl Res. 2019; 9: 418-33.

[124]

Pereira LM, Hatanaka E, Martins EF, Oliveira F, Liberti EA, Farsky SH, et al. Effect of oleic and linoleic acids on the inflammatory phase of wound healing in rats. Cell Biochem Funct. 2008; 26: 197-204.

[125]

Rodrigues HG, Vinolo MA, Magdalon J, Vitzel K, Nachbar RT, Pessoa AF, et al. Oral administration of oleic or linoleic acid accelerates the inflammatory phase of wound healing. J Invest Dermatol. 2012; 132: 208-15.

[126]

Jia YC, Qiu S, Xu J, Kang QL, Chai YM. Docosahexaenoic acid improves diabetic wound healing in a rat model by restoring impaired plasticity of macrophage progenitor cells. Plast Reconstr Surg. 2020; 145: 942e-50.

[127]

Kavalukas SL, Uzgare AR, Bivalacqua TJ, Barbul A. Arginase inhibition promotes wound healing in mice. Surgery. 2012; 151: 287-95.

[128]

Reesi F, Minaiyan M, Taheri A. A novel lignin-based nanofibrous dressing containing arginine for wound-healing applications. Drug Deliv Transl Res. 2018; 8: 111-22.

[129]

Hussein Y, El-Fakharany EM, Kamoun EA, Loutfy SA, Amin R, Taha TH, et al. Electrospun PVA/hyaluronic acid/L-arginine nanofibers for wound healing applications: nanofibers optimization and in vitro bioevaluation. Int J Biol Macromol. 2020; 164: 667-76.

[130]

Goswami S, Kandhare A, Zanwar AA, Hegde MV, Bodhankar SL, Shinde S, et al. Oral L-glutamine administration attenuated cutaneous wound healing in Wistar rats. Int Wound J. 2016; 13: 116-24.

[131]

Guo X, Liu Y, Bera H, Zhang H, Chen Y, Cun D, et al. α-Lactalbumin-based nanofiber dressings improve burn wound healing and reduce scarring. ACS Appl Mater Interfaces. 2020; 12: 45702-13.

PDF (1386KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/

〈 〉