Targeting Oxidative Stress and Mitochondrial Dysfunction in the Treatment of Impaired Wound Healing: A Systematic Review
Tóm tắt
Wound healing is a well-tuned biological process, which is achieved via consecutive and overlapping phases including hemostasis, inflammatory-related events, cell proliferation and tissue remodeling. Several factors can impair wound healing such as oxygenation defects, aging, and stress as well as deleterious health conditions such as infection, diabetes, alcohol overuse, smoking and impaired nutritional status. Growing evidence suggests that reactive oxygen species (ROS) are crucial regulators of several phases of healing processes. ROS are centrally involved in all wound healing processes as low concentrations of ROS generation are required for the fight against invading microorganisms and cell survival signaling. Excessive production of ROS or impaired ROS detoxification causes oxidative damage, which is the main cause of non-healing chronic wounds. In this context, experimental and clinical studies have revealed that antioxidant and anti-inflammatory strategies have proven beneficial in the non-healing state. Among available antioxidant strategies, treatments using mitochondrial-targeted antioxidants are of particular interest. Specifically, mitochondrial-targeted peptides such as elamipretide have the potential to mitigate mitochondrial dysfunction and aberrant inflammatory response through activation of nucleotide-binding oligomerization domain (NOD)-like family receptors, such as the pyrin domain containing 3 (NLRP3) inflammasome, nuclear factor-kappa B (NF-κB) signaling pathway inhibition, and nuclear factor (erythroid-derived 2)-like 2 (Nrf2).
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Tài liệu tham khảo
Janis, 2016, Wound healing: Part I. Basic science, Plast. Reconstr. Surg., 138, 9S, 10.1097/PRS.0000000000002773
Sen, 2008, Redox signals in wound healing, Biochim. Biophys. Acta, 1780, 1348, 10.1016/j.bbagen.2008.01.006
Schafer, 2008, Oxidative stress in normal and impaired wound repair, Pharmacol. Res., 58, 165, 10.1016/j.phrs.2008.06.004
Dunnill, 2017, Reactive oxygen species (ROS) and wound healing: The functional role of ROS and emerging ROS-modulating technologies for augmentation of the healing process, Int. Wound J., 14, 89, 10.1111/iwj.12557
Sen, 2009, Wound healing essentials: Let there be oxygen, Wound Repair Regen., 17, 1, 10.1111/j.1524-475X.2008.00436.x
Bryan, 2012, Reactive oxygen species (ROS)—A family of fate deciding molecules pivotal in constructive inflammation and wound healing, Eur. Cells Mater., 24, 249, 10.22203/eCM.v024a18
Fitzmaurice, 2011, Antioxidant therapies for wound healing: A clinical guide to currently commercially available products, Skin Pharmacol. Physiol., 24, 113, 10.1159/000322643
Kunkemoeller, 2017, Redox signaling in diabetic wound healing regulates extracellular matrix deposition, Antioxid. Redox Signal., 27, 823, 10.1089/ars.2017.7263
Golebiewska, 2015, Platelet secretion: From haemostasis to wound healing and beyond, Blood Rev., 29, 153, 10.1016/j.blre.2014.10.003
Redondo, 2013, Molecular interplay between platelets and the vascular wall in thrombosis and hemostasis, Curr. Vasc. Pharmacol., 11, 409, 10.2174/1570161111311040006
Kaltalioglu, 2015, A bioactive molecule in a complex wound healing process: Platelet-derived growth factor, Int. J. Dermatol., 54, 972, 10.1111/ijd.12731
Hamblin, 2012, Acute and impaired wound healing: Pathophysiology and current methods for drug delivery, part 2: Role of growth factors in normal and pathological wound healing: Therapeutic potential and methods of delivery, Adv. Skin Wound Care, 25, 349, 10.1097/01.ASW.0000418541.31366.a3
Nurden, 2018, The biology of the platelet with special reference to inflammation, wound healing and immunity, Front. Biosci. (Landmark Ed.), 23, 726, 10.2741/4613
Portou, 2015, The innate immune system, toll-like receptors and dermal wound healing: A review, Vasc. Pharmacol., 71, 31, 10.1016/j.vph.2015.02.007
Kasuya, 2014, Attempts to accelerate wound healing, J. Dermatol. Sci., 76, 169, 10.1016/j.jdermsci.2014.11.001
Landen, 2016, Transition from inflammation to proliferation: A critical step during wound healing, Cell. Mol. Life Sci., 73, 3861, 10.1007/s00018-016-2268-0
Tracy, 2016, Extracellular matrix and dermal fibroblast function in the healing wound, Adv. Wound Care (New Rochelle), 5, 119, 10.1089/wound.2014.0561
Bainbridge, 2013, Wound healing and the role of fibroblasts, J. Wound Care, 22, 407, 10.12968/jowc.2013.22.8.407
Zhu, 2017, Hydrogen peroxide: A potential wound therapeutic target?, Med. Princ. Pract., 26, 301, 10.1159/000475501
Andre-Levigne, D., Modarressi, A., Pepper, M.S., and Pittet-Cuenod, B. (2017). Reactive oxygen species and nox enzymes are emerging as key players in cutaneous wound repair. Int. J. Mol. Sci., 18.
Hoffmann, M.H., and Griffiths, H.R. (2018). The dual role of ROS in autoimmune and inflammatory diseases: Evidence from preclinical models. Free Radic. Biol. Med.
Jiang, 2011, Nadph oxidase-mediated redox signaling: Roles in cellular stress response, stress tolerance, and tissue repair, Pharmacol. Rev., 63, 218, 10.1124/pr.110.002980
Levigne, 2016, Nadph oxidase 4 deficiency leads to impaired wound repair and reduced dityrosine-crosslinking, but does not affect myofibroblast formation, Free Radic. Biol. Med., 96, 374, 10.1016/j.freeradbiomed.2016.04.194
Hesketh, M., Sahin, K.B., West, Z.E., and Murray, R.Z. (2017). Macrophage phenotypes regulate scar formation and chronic wound healing. Int. J. Mol. Sci., 18.
Patel, 2016, Biomarkers for wound healing and their evaluation, J. Wound Care, 25, 46, 10.12968/jowc.2016.25.1.46
Smith, 2017, Redox signaling during hypoxia in mammalian cells, Redox Biol., 13, 228, 10.1016/j.redox.2017.05.020
Waypa, 2016, O2 sensing, mitochondria and ROS signaling: The fog is lifting, Mol. Asp. Med., 47–48, 76, 10.1016/j.mam.2016.01.002
Fuhrmann, 2017, Mitochondrial composition and function under the control of hypoxia, Redox Biol., 12, 208, 10.1016/j.redox.2017.02.012
Wautier, 2017, Activation of the receptor for advanced glycation end products and consequences on health, Diabetes Metab. Syndr., 11, 305, 10.1016/j.dsx.2016.09.009
Shah, 2016, Molecular and cellular mechanisms of cardiovascular disorders in diabetes, Circ. Res., 118, 1808, 10.1161/CIRCRESAHA.116.306923
Schramm, 2012, Targeting nadph oxidases in vascular pharmacology, Vasc. Pharmacol., 56, 216, 10.1016/j.vph.2012.02.012
Kurosaka, 2009, Reduced angiogenesis and delay in wound healing in angiotensin ii type 1a receptor-deficient mice, Biomed. Pharmacother., 63, 627, 10.1016/j.biopha.2009.01.001
Fernandez, 2018, Xanthine oxidoreductase: A novel therapeutic target for the treatment of chronic wounds?, Adv. Wound Care (New Rochelle), 7, 95, 10.1089/wound.2016.0724
Forrester, 2018, Reactive oxygen species in metabolic and inflammatory signaling, Circ. Res., 122, 877, 10.1161/CIRCRESAHA.117.311401
Zinkevich, 2011, Ros-induced ROS release in vascular biology: Redox-redox signaling, Am. J. Physiol. Heart Circ. Physiol., 301, H647, 10.1152/ajpheart.01271.2010
Zorov, 2014, Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release, Physiol. Rev., 94, 909, 10.1152/physrev.00026.2013
Banerjee, 2014, Reactive metabolites and antioxidant gene polymorphisms in type 2 diabetes mellitus, Redox Biol., 2, 170, 10.1016/j.redox.2013.12.001
David, 2017, The Nrf2/Keap1/ARE pathway and oxidative stress as a therapeutic target in type ii diabetes mellitus, J. Diabetes Res., 2017, 4826724, 10.1155/2017/4826724
Bitar, 2011, A defect in Nrf2 signaling constitutes a mechanism for cellular stress hypersensitivity in a genetic rat model of type 2 diabetes, Am. J. Physiol. Endocrinol. Metab., 301, E1119, 10.1152/ajpendo.00047.2011
Soares, 2016, Restoration of Nrf2 signaling normalizes the regenerative niche, Diabetes, 65, 633, 10.2337/db15-0453
Ambrozova, 2017, Models for the study of skin wound healing. The role of Nrf2 and NF-kappaB, Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub., 161, 1, 10.5507/bp.2016.063
Wang, T., He, R., Zhao, J., Mei, J.C., Shao, M.Z., Pan, Y., Zhang, J., Wu, H.S., Yu, M., and Yan, W.C. (2017). Negative pressure wound therapy inhibits inflammation and upregulates activating transcription factor-3 and downregulates nuclear factor-kappab in diabetic patients with foot ulcerations. Diabetes Metab. Res. Rev., 33.
Vistoli, 2013, Advanced glycoxidation and lipoxidation end products (ages and ales): An overview of their mechanisms of formation, Free Radic. Res., 47, 3, 10.3109/10715762.2013.815348
Frimat, 2017, Kidney, heart and brain: Three organs targeted by ageing and glycation, Clin. Sci. (Lond.), 131, 1069, 10.1042/CS20160823
Neviere, 2016, Implication of advanced glycation end products (AGES) and their receptor (RAGE) on myocardial contractile and mitochondrial functions, Glycoconj. J., 33, 607, 10.1007/s10719-016-9679-x
Van Putte, L., De Schrijver, S., and Moortgat, P. (2016). The effects of advanced glycation end products (ages) on dermal wound healing and scar formation: A systematic review. Scars Burn Heal., 2.
Huijberts, 2008, Advanced glycation end products and diabetic foot disease, Diabetes Metab. Res. Rev., 24, S19, 10.1002/dmrr.861
Yamagishi, 2017, Glycation and cardiovascular disease in diabetes: A perspective on the concept of metabolic memory, J. Diabetes, 9, 141, 10.1111/1753-0407.12475
Peppa, 2009, Advanced glycoxidation products and impaired diabetic wound healing, Wound Repair Regen., 17, 461, 10.1111/j.1524-475X.2009.00518.x
Koulis, 2015, Linking rage and nox in diabetic micro- and macrovascular complications, Diabetes Metab., 41, 272, 10.1016/j.diabet.2015.01.006
Niu, 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, 344, 10.1097/DAD.0b013e31816a8c5b
Peppa, 2003, Adverse effects of dietary glycotoxins on wound healing in genetically diabetic mice, Diabetes, 52, 2805, 10.2337/diabetes.52.11.2805
Goova, 2001, Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice, Am. J. Pathol., 159, 513, 10.1016/S0002-9440(10)61723-3
Lee, 2004, Use of topical srage in diabetic wounds increases neovascularization and granulation tissue formation, Ann. Plast. Surg., 52, 519, 10.1097/01.sap.0000122857.49274.8c
Bigot, 2012, Nf-kappab accumulation associated with col1a1 transactivators defects during chronological aging represses type I collagen expression through a -112/-61-bp region of the col1a1 promoter in human skin fibroblasts, J. Investig. Dermatol., 132, 2360, 10.1038/jid.2012.164
Ito, 2018, Activation of NLRP3 signalling accelerates skin wound healing, Exp. Dermatol., 27, 80, 10.1111/exd.13441
Weinheimer-Haus, E.M., Mirza, R.E., and Koh, T.J. (2015). Nod-like receptor protein-3 inflammasome plays an important role during early stages of wound healing. PLoS ONE, 10.
Zhang, 2017, Nlrp3 inflammasome expression and signaling in human diabetic wounds and in high glucose induced macrophages, J. Diabetes Res., 2017, 5281358, 10.1155/2017/5281358
Meyer, 2018, Mitochondria: An organelle of bacterial origin controlling inflammation, Front. Immunol., 9, 536, 10.3389/fimmu.2018.00536
Demyanenko, 2017, Mitochondria-targeted antioxidant SkQ1 improves dermal wound healing in genetically diabetic mice, Oxid. Med. Cell. Longev., 2017, 6408278, 10.1155/2017/6408278
Dashdorj, A., Jyothi, K.R., Lim, S., Jo, A., Nguyen, M.N., Ha, J., Yoon, K.S., Kim, H.J., Park, J.H., and Murphy, M.P. (2013). Mitochondria-targeted antioxidant mitoq ameliorates experimental mouse colitis by suppressing nlrp3 inflammasome-mediated inflammatory cytokines. BMC Med., 11.
Jabaut, 2013, Mitochondria-targeted drugs enhance Nlrp3 inflammasome-dependent IL-1beta secretion in association with alterations in cellular redox and energy status, Free Radic. Biol. Med., 60, 233, 10.1016/j.freeradbiomed.2013.01.025
Zielins, 2015, Emerging drugs for the treatment of wound healing, Expert Opin. Emerg. Drugs, 20, 235, 10.1517/14728214.2015.1018176
Iuchi, 2010, Spontaneous skin damage and delayed wound healing in sod1-deficient mice, Mol. Cell. Biochem., 341, 181, 10.1007/s11010-010-0449-y
Deshane, 2007, Stromal cell-derived factor 1 promotes angiogenesis via a heme oxygenase 1-dependent mechanism, J. Exp. Med., 204, 605, 10.1084/jem.20061609
Weinstein, 2015, Normalizing dysfunctional purine metabolism accelerates diabetic wound healing, Wound Repair Regen., 23, 14, 10.1111/wrr.12249
Fadini, 2010, The redox enzyme p66Shc contributes to diabetes and ischemia-induced delay in cutaneous wound healing, Diabetes, 59, 2306, 10.2337/db09-1727
Luo, 2004, Gene therapy of endothelial nitric oxide synthase and manganese superoxide dismutase restores delayed wound healing in type 1 diabetic mice, Circulation, 110, 2484, 10.1161/01.CIR.0000137969.87365.05
Tao, 2013, The Nrf2-inducers tanshinone I and dihydrotanshinone protect human skin cells and reconstructed human skin against solar simulated Uv, Redox Biol., 1, 532, 10.1016/j.redox.2013.10.004
Kim, 2017, Mitochondria-targeted antioxidants for the treatment of cardiovascular disorders, Adv. Exp. Med. Biol., 982, 621, 10.1007/978-3-319-55330-6_32
Reddy, 2017, Mitochondria-targeted molecules as potential drugs to treat patients with alzheimer’s disease, Prog. Mol. Biol. Transl. Sci., 146, 173, 10.1016/bs.pmbts.2016.12.010
Karaa, 2018, Randomized dose-escalation trial of elamipretide in adults with primary mitochondrial myopathy, Neurology, 90, e1212, 10.1212/WNL.0000000000005255