Effective protective mechanisms of HO-1 in diabetic complications: a narrative review

  • Balooch Hasankhani M, Mirzaei H, Karamoozian A. Global trend analysis of diabetes mellitus incidence, mortality, and mortality-to-incidence ratio from 1990 to 2019. Sci Rep 2023;13:21908.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lovic D, Piperidou A, Zografou I, Grassos H, Pittaras A, Manolis A. The growing epidemic of diabetes mellitus. Curr Vasc Pharmacol 2020;18:104–9.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sun H, Saeedi P, Karuranga S, Pinkepank M, Ogurtsova K, Duncan BB, et al. IDF diabetes atlas: global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diab Res Clin Pr 2022;183:109119.

    Article 

    Google Scholar
     

  • Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the international diabetes federation diabetes atlas, 9th edition. Diab Res Clin Pr 2019;157:107843.

    Article 

    Google Scholar
     

  • Zheng Y, Ley SH, Hu FB. Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat Rev Endocrinol 2018;14:88–98.

    Article 
    PubMed 

    Google Scholar
     

  • Kikuchi G, Yoshida T, Noguchi M. Heme oxygenase and heme degradation. Biophys Biochem Res Commun 2005;338:558–67.

    Article 
    CAS 

    Google Scholar
     

  • Negi G, Nakkina V, Kamble P, Sharma SS. Heme oxygenase-1, a novel target for the treatment of diabetic complications: focus on diabetic peripheral neuropathy. Pharm Res. 2015;102:158–67.

    Article 
    CAS 

    Google Scholar
     

  • Dou Y, Ai G, Huang R, Huang Z, Li Y, Liu Y, et al. In vitro and in vivo hypoglycemia effect of oxyberberine, a novel HO-1 agonist: A renewed evidence linking HO-1 to diabetes mellitus. Phytomedicine 2022;101:154135.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ryter SW. Heme oxygenase-1: an anti-inflammatory effector in cardiovascular, lung, and related metabolic disorders. Antioxidants. 2022;11:555.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu Y, Wang S, Jin G, Gao K, Wang S, Zhang X, et al. Network pharmacology-based study on the mechanism of ShenKang injection in diabetic kidney disease through Keap1/Nrf2/Ho-1 signaling pathway. Phytomedicine 2023;118:154915.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gell DA. Structure and function of haemoglobins. Blood Cell Mol Dis. 2018;70:13–42.

    Article 
    CAS 

    Google Scholar
     

  • Rochette L, Zeller M, Cottin Y, Vergely C. Redox functions of heme oxygenase-1 and biliverdin reductase in diabetes. Trends Endocrinol Met 2018;29:74–85.

    Article 
    CAS 

    Google Scholar
     

  • Takeda T-A, Sasai M, Adachi Y, Ohnishi K, Fujisawa J-i, Izawa S, et al. Potential role of heme metabolism in the inducible expression of heme oxygenase-1. BBA-Gen Subj 2017;1861:1813–24.

    Article 
    CAS 

    Google Scholar
     

  • Sassa S. Why heme needs to be degraded to iron, biliverdin IXα, and carbon monoxide? Antioxid Redox Signal 2004;6:819–24.

    CAS 
    PubMed 

    Google Scholar
     

  • Intagliata S, Salerno L, Ciaffaglione V, Leonardi C, Fallica AN, Carota G, et al. Heme oxygenase-2 (HO-2) as a therapeutic target: activators and inhibitors. Eur J Med Chem. 2019;183:111703.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hayashi S, Omata Y, Sakamoto H, Higashimoto Y, Hara T, Sagara Y, et al. Characterization of rat heme oxygenase-3 gene. Implication of processed pseudogenes derived from heme oxygenase-2 gene. Gene 2004;336:241–50.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Facchinetti MM. Heme-oxygenase-1. Antioxid Redox Signal 2020;32:1239–42.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pittala V, Vanella L, Salerno L, Romeo G, Marrazzo A, Di Giacomo C, et al. Effects of polyphenolic derivatives on heme oxygenase-system in metabolic dysfunctions. Curr Med Chem 2018;25:1577–95.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pogu J, Tzima S, Kollias G, Anegon I, Blancou P, Simon T. Genetic restoration of heme oxygenase-1 expression protects from type 1 diabetes in NOD mice. Int J Mol Sci 2019;20:1676.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Medzhitov R. Origin and physiological roles of inflammation. Nature 2008;454:428–35.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Singh N, Baby D, Rajguru JP, Patil PB, Thakkannavar SS, Pujari VB. Inflammation and cancer. Ann Afr Med 2019;18:121–6.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kawai T, Autieri MV, Scalia R. Adipose tissue inflammation and metabolic dysfunction in obesity. Am J Physiol Cell Physiol 2020;320:C375–C91.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lee SH, Lee TW, Ihm CG, Kim MJ, Woo JT, Chung JH. Genetics of diabetic nephropathy in type 2 DM: candidate gene analysis for the pathogenic role of inflammation. Nephrology 2005;10:S32–S6.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Carrizales-Sepúlveda EF, Ordaz-Farías A, Vera-Pineda R, Flores-Ramírez R. Periodontal disease, systemic inflammation and the risk of cardiovascular disease. Heart Lung Circ 2018;27:1327–34.

    Article 
    PubMed 

    Google Scholar
     

  • Kirpichnikov D, Sowers JR. Diabetes mellitus and diabetes-associated vascular disease. Trends Endocrinol Metab 2001;12:225–30.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kornelius E, Tsou SH, Chang CC, Ho YJ, Lin SC, Chen WL, et al. Liraglutide attenuates glucolipotoxicity-induced RSC96 schwann cells’ inflammation and dysfunction. Biomolecules 2022;21:1338.

    Article 

    Google Scholar
     

  • Wang S, Cao M, Xu S, Shi J, Mao X, Yao X, et al. Luteolin alters macrophage polarization to inhibit inflammation. Inflammation 2020;43:95–108.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Faas M, Ipseiz N, Ackermann J, Culemann S, Grüneboom A, Schröder F, et al. IL-33-induced metabolic reprogramming controls the differentiation of alternatively activated macrophages and the resolution of inflammation. Immunity 2021;54:2531–46.e5.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yunna C, Mengru H, Lei W, Weidong C. Macrophage M1/M2 polarization. Eur J Pharmacol 2020;877:173090.

    Article 
    PubMed 

    Google Scholar
     

  • Landis CR, Quimby RK, Greenidge RA. M1/M2 macrophages in diabetic nephropathy: Nrf2/HO-1 as therapeutic targets. Curr Pharm Des 2018;24:2241–9.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Josefs T, Barrett TJ, Brown EJ, Quezada A, Wu X, Voisin M, et al. Neutrophil extracellular traps promote macrophage inflammation and impair atherosclerosis resolution in diabetic mice. JCI Insight 2020;5:e134796.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Orozco LD, Kapturczak MH, Barajas B, Wang X, Weinstein MM, Wong J, et al. Heme oxygenase-1 expression in macrophages plays a beneficial role in atherosclerosis. Circ Res 2007;100:1703–11.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tsai CF, Chen GW, Chen YC, Shen CK, Lu DY, Yang LY, et al. Regulatory effects of quercetin on M1/M2 macrophage polarization and oxidative/antioxidative balance. Nutrients 2021;14:67.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wu ML, Ho YC, Lin CY, Yet SF. Heme oxygenase-1 in inflammation and cardiovascular disease. Am J Cardiovasc Dis 2011;1:150–8.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Naito Y, Takagi T, Higashimura Y. Heme oxygenase-1 and anti-inflammatory M2 macrophages. Arch Biochem Biophys 2014;564:83–8.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Neshatian L, Gibbons SJ, Farrugia G. Macrophages in diabetic gastroparesis—the missing link? Neurogastroent Motil 2015;27:7–18.

    Article 
    CAS 

    Google Scholar
     

  • Wang H, Zhao K, Ba Y, Gao T, Shi N, Niu Q, et al. Gastric electrical pacing reduces apoptosis of interstitial cells of Cajal via antioxidative stress effect attributing to phenotypic polarization of M2 macrophages in diabetic rats. Oxid Med Cell Longev. 2021;2021:1298657.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Oh YJ, Jin SE, Shin HK, Ha H. Daeshiho-tang attenuates inflammatory response and oxidative stress in LPS-stimulated macrophages by regulating TLR4/MyD88, NF-κB, MAPK, and Nrf2/HO-1 pathways. Sci Rep 2023;13:18891.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sha W, Zhao B, Wei H, Yang Y, Yin H, Gao J, et al. Astragalus polysaccharide ameliorates vascular endothelial dysfunction by stimulating macrophage M2 polarization via potentiating Nrf2/HO-1 signaling pathway. Phytomedicine 2023;112:154667.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wu B, Pan W, Luo S, Luo X, Zhao Y, Xiu Q, et al. Turmeric-derived nanoparticles functionalized aerogel regulates multicellular networks to promote diabetic wound healing. Adv Sci 2024;11:2307630.

    Article 
    CAS 

    Google Scholar
     

  • Li BZ, Guo B, Zhang HY, Liu J, Tao SS, Pan HF, et al. Therapeutic potential of HO-1 in autoimmune diseases. Inflammation 2014;37:1779–88.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Campbell NK, Williams DG, Fitzgerald HK, Barry PJ, Cunningham CC, Nolan DP, et al. Trypanosoma brucei secreted aromatic ketoacids activate the Nrf2/HO-1 pathway and suppress pro-inflammatory responses in primary murine glia and macrophages. Front Immunol 2019;10:2137.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Franchina DG, Dostert C, Brenner D. Reactive oxygen species: involvement in T cell signaling and metabolism. Trends Immunol 2018;39:489–502.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chauveau C, Rémy S, Royer PJ, Hill M, Tanguy-Royer SV, Hubert FO-X, et al. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 2005;106:1694–702.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • George JF, Braun A, Brusko TM, Joseph R, Bolisetty S, Wasserfall CH, et al. Suppression by CD4+CD25+ regulatory T cells is dependent on expression of heme oxygenase-1 in antigen-presenting cells. Am J Dance Ther 2008;173:154–60.

    CAS 

    Google Scholar
     

  • Campbell NK, Fitzgerald HK, Malara A, Hambly R, Sweeney CM, Kirby B, et al. Naturally derived heme-oxygenase 1 inducers attenuate inflammatory responses in human dendritic cells and T cells: relevance for psoriasis treatment. Sci Rep 2018;8:10287.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Listopad J, Asadullah K, Sievers C, Ritter T, Meisel C, Sabat R, et al. Heme oxygenase-1 inhibits T cell-dependent skin inflammation and differentiation and function of antigen-presenting cells. Exp Derm 2007;16:661–70.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mahmoud FF, Haines D, Dashti AA, El-Shazly S, Al-Najjar F. Correlation between heat shock proteins, adiponectin, and T lymphocyte cytokine expression in type 2 diabetics. Cell Stress Chaperones 2018;23:955–65.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Song F, Chen W, Jia W, Yao P, Nussler AK, Sun X, et al. A natural sweetener, Momordica grosvenori, attenuates the imbalance of cellular immune functions in alloxan-induced diabetic mice. Phytother Res 2006;20:552–60.

    Article 
    PubMed 

    Google Scholar
     

  • Ali MAM, Heeba GH, El-Sheikh AAK. Modulation of heme oxygenase-1 expression and activity affects streptozotocin-induced diabetic nephropathy in rats. Fund Clin Pharmacol 2017;31:546–57.

    Article 
    CAS 

    Google Scholar
     

  • Jansen T, Hortmann M, Oelze M, Opitz B, Steven S, Schell R, et al. Conversion of biliverdin to bilirubin by biliverdin reductase contributes to endothelial cell protection by heme oxygenase-1-evidence for direct and indirect antioxidant actions of bilirubin. J Mol Cell Cardiol 2010;49:186–95.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yao Q, Lan QH, Jiang X, Du CC, Zhai YY, Shen X, et al. Bioinspired biliverdin/silk fibroin hydrogel for antiglioma photothermal therapy and wound healing. Theranostics 2020;10:11719–36.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ahanger, Prawez AA, Kumar S, Prasad D, Amarpal R, Tandan SK, et al. Wound healing activity of carbon monoxide liberated from co-releasing molecule (CO-RM). Naunyn Schmiedeberg Arch Pharmacol 2011;384:93–102.

    Article 
    CAS 

    Google Scholar
     

  • Fan J, Xu G, Jiang T, Qin Y. Pharmacologic Induction of Heme oxygenase-1 plays a protective role in diabetic retinopathy in rats. Investig Ophth Vis Sci 2012;53:6541–56.

    Article 
    CAS 

    Google Scholar
     

  • Kumar D, Jena GR, Ram M, Lingaraju MC, Singh V, Prasad R, et al. Hemin attenuated oxidative stress and inflammation to improve wound healing in diabetic rats. Naunyn Schmiedeberg Arch Pharmacol 2019;392:1435–45.

    Article 
    CAS 

    Google Scholar
     

  • Ndisang JF, Jadhav A. Hemin therapy improves kidney function in male streptozotocin-induced diabetic rats: role of the heme oxygenase/atrial natriuretic peptide/adiponectin axis. Endocrinology 2014;155:215–29.

    Article 
    PubMed 

    Google Scholar
     

  • Kwak HJ, Song JS, No ZS, Song JH, Yang SD, Cheon HG. The inhibitory effects of roflumilast on lipopolysaccharide-induced nitric oxide production in RAW264.7 cells are mediated by heme oxygenase-1 and its product carbon monoxide. Inflamm Res 2005;54:508–13.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Qin S, Du R, Yin S, Liu X, Xu G, Cao W. Nrf2 is essential for the anti-inflammatory effect of carbon monoxide in LPS-induced inflammation. Inflamm Res 2015;64:537–48.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pae HO, Lee CY, Chung HT. Heme oxygenase-1 and carbon monoxide: emerging therapeutic targets in inflammation and allergy. Recent Pat Inflamm 2008;2:159–65.

    CAS 

    Google Scholar
     

  • Mishra S, Fujita T, Lama VN, Nam D, Liao H, Okada M, et al. Carbon monoxide rescues ischemic lungs by interrupting MAPK-driven expression of early growth response 1 gene and its downstream target genes. Proc Natl Acad Sci USA 2006;103:5191–6.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li M, Li Q, Zhao Q, Zhang J, Lin J. Luteolin improves the impaired nerve functions in diabetic neuropathy: behavioral and biochemical evidences. Int J Clin Exp Pathol 2015;8:10112–20.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Khan A, Wang F, Shal B, Khan AU, Zahra SS, Haq IU, et al. Anti-neuropathic pain activity of ajugarin-i via activation of Nrf2 signaling and inhibition of TRPV1/TRPM8 nociceptors in STZ-induced diabetic neuropathy. Pharm Res 2022;183:106392.

    Article 
    CAS 

    Google Scholar
     

  • Zhao P, Wei Y, Sun G, Xu L, Wang T, Tian Y, et al. Fetuin-A alleviates neuroinflammation against traumatic brain injury-induced microglial necroptosis by regulating Nrf-2/HO-1 pathway. J Neuroinflammation Amm 2022;19:269.

    Article 
    CAS 

    Google Scholar
     

  • Kopeina GS, Zhivotovsky B. Programmed cell death: past, present and future. Biochem Biophys Res Commun 2022;633:55–8.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 2007;35:495–516.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jorgensen I, Rayamajhi M, Miao EA. Programmed cell death as a defence against infection. Nat Rev Immunol 2017;17:151–64.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shi J, Gao W, Shao F. Pyroptosis: gasdermin-mediated programmed necrotic cell death. Trends Biochem Sci 2017;42:245–54.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Shi J, Zhao Y, Wang K, Shi X, Wang Y, Huang H, et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 2015;526:660–5.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhang Z, Tang M, Liu W, Song Y, Gao M, Ni P, et al. Dapagliflozin prevents kidney podocytes pyroptosis via miR-155-5p/HO-1/NLRP3 axis modulation. Int Immunopharmacol 2024;131:111785.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zuo Y, Chen L, He X, Ye Z, Li L, Liu Z, et al. Atorvastatin regulates MALAT1/miR-200c/NRF2 activity to protect against podocyte pyroptosis induced by high glucose. Diab Metab Syndr Obes 2021;14:1631–45.

    Article 

    Google Scholar
     

  • Lv C, Cheng T, Zhang B, Sun K, Lu K. Triptolide protects against podocyte injury in diabetic nephropathy by activating the Nrf2/HO-1 pathway and inhibiting the NLRP3 inflammasome pathway. Ren Fail 2023;45:2165103.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li G, Liu C, Yang L, Feng L, Zhang S, An J, et al. Syringaresinol protects against diabetic nephropathy by inhibiting pyroptosis via NRF2-mediated antioxidant pathway. Cell Biol Toxicol. 2023;39:621–39.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wei Z, pinfang K, jing Z, zhuoya Y, Shaohuan Q, Chao S. Curcumin improves diabetic cardiomyopathy by Inhibiting pyroptosis through AKT/Nrf2/ARE pathway. Mediat Inflamm 2023;2023:3906043.

    Article 

    Google Scholar
     

  • Li J, Cao F, Yin H-l, Huang Z-j, Lin Z-t, Mao N, et al. Ferroptosis: past, present and future. Cell Death Dis 2020;11:88.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li Y, Zeng X, Lu D, Yin M, Shan M, Gao Y. Erastin induces ferroptosis via ferroportin-mediated iron accumulation in endometriosis. Hum Reprod 2021;36:951–64.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhu W, Liu D, Lu Y, Sun J, Zhu J, Xing Y, et al. PHKG2 regulates RSL3-induced ferroptosis in Helicobacter pylori related gastric cancer. Arch Biochem Biophys 2023;740:109560.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Feng Q, Yang Y, Qiao Y, Zheng Y, Yu X, Liu F, et al. Quercetin ameliorates diabetic kidney injury by inhibiting ferroptosis via activating Nrf2/HO-1 signaling pathway. Am J Chin Med 2023;51:997–1018.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Feng X, Wang S, Sun Z, Dong H, Yu H, Huang M, et al. Ferroptosis enhanced diabetic renal tubular injury via HIF-1α/HO-1 pathway in db/db mice. Front Endocrinol 2021;12:626390.

    Article 

    Google Scholar
     

  • Xu P, Lin B, Deng X, Huang K, Zhang Y, Wang N. VDR activation attenuates osteoblastic ferroptosis and senescence by stimulating the Nrf2/GPX4 pathway in age-related osteoporosis. Free Radic Bio Med 2022;193:720–35.

    Article 
    CAS 

    Google Scholar
     

  • Hu Z, Zhang H, Yi B, Yang S, Liu J, Hu J, et al. VDR activation attenuate cisplatin induced AKI by inhibiting ferroptosis. Cell Death Dis 2020;11:73.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li L, Li WJ, Zheng XR, Liu QL, Du Q, Lai YJ, et al. Eriodictyol ameliorates cognitive dysfunction in APP/PS1 mice by inhibiting ferroptosis via vitamin D receptor-mediated Nrf2 activation. Mol Med 2022;28:11.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang H, Yu X, Liu D, Qiao Y, Huo J, Pan S, et al. VDR activation attenuates renal tubular epithelial cell ferroptosis by regulating Nrf2/HO-1 signaling pathway in diabetic nephropathy. Adv Sci 2024;11:2305563.

    Article 
    CAS 

    Google Scholar
     

  • Gordon DM, Adeosun SO, Ngwudike SI, Anderson CD, Hall JE, Hinds TD, et al. CRISPR cas9-mediated deletion of biliverdin reductase A (BVRA) in mouse liver cells induces oxidative stress and lipid accumulation. Arch Biochem Biophys. 2019;672:108072.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Almourani R, Chinnakotla B, Patel R, Kurukulasuriya LR, Sowers J. Diabetes and cardiovascular disease: an update. Curr Diab Rep 2019;19:161.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Glovaci D, Fan W, Wong ND. Epidemiology of diabetes mellitus and cardiovascular disease. Curr Cardiol Rep. 2019;21:21.

    Article 
    PubMed 

    Google Scholar
     

  • Knapp M, Tu X, Wu R. Vascular endothelial dysfunction, a major mediator in diabetic cardiomyopathy. Acta Pharm Sin 2019;40:1–8.

    Article 
    CAS 

    Google Scholar
     

  • Gu J, Wang S, Guo H, Tan Y, Liang Y, Feng A, et al. Inhibition of p53 prevents diabetic cardiomyopathy by preventing early-stage apoptosis and cell senescence, reduced glycolysis, and impaired angiogenesis. Cell Death Dis 2018;9:82.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jia G, Whaley-Connell A, Sowers JR. Diabetic cardiomyopathy: a hyperglycaemia- and insulin-resistance-induced heart disease. Diabetologia 2018;61:21–8.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jia G, Hill MA, Sowers JR. Diabetic cardiomyopathy. Circ Res 2018;122:624–38.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Khan S, Ahmad SS, Kamal AM. Diabetic cardiomyopathy: from mechanism to management in a nutshell. Endocr Metab Immune 2021;21:268–81.

    CAS 

    Google Scholar
     

  • Maamoun H, Zachariah M, McVey JH, Green FR, Agouni A. Heme oxygenase (HO)-1 induction prevents endoplasmic reticulum stress-mediated endothelial cell death and impaired angiogenic capacity. Biochem Pharmacol 2017;127:46–59.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Maamoun H, Benameur T, Pintus G, Munusamy S, Agouni A. Crosstalk between oxidative stress and endoplasmic reticulum (ER) stress in endothelial dysfunction and aberrant angiogenesis associated with diabetes: a focus on the protective roles of heme oxygenase (HO)-1. Front Physiol 2019;10:70.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu J, Wang L, Tian XY, Liu L, Wong WT, Zhang Y, et al. Unconjugated bilirubin mediates heme oxygenase-1–induced vascular benefits in diabetic mice. Diabetes 2014;64:1564–75.

    Article 
    PubMed 

    Google Scholar
     

  • Zhong ZY, Tang Y. Upregulation of periostin prevents high glucose-induced mitochondrial apoptosis in human umbilical vein endothelial cells via activation of Nrf2/HO-1 signaling. Cell Physiol Biochem 2016;39:71–80.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Luo Y, Lu S, Dong X, Xu L, Sun G, Sun X. Dihydromyricetin protects human umbilical vein endothelial cells from injury through ERK and Akt mediated Nrf2/HO-1 signaling pathway. Apoptosis 2017;22:1013–24.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Collino M, Pini A, Mugelli N, Mastroianni R, Bani D, Fantozzi R, et al. Beneficial effect of prolonged heme oxygenase 1 activation in a rat model of chronic heart failure. Dis Model Mech 2013;6:1012–20.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu X, Wei J, Peng DH, Layne MD, Yet S-F. Absence of heme oxygenase-1 exacerbates myocardial ischemia/reperfusion injury in diabetic mice. Diabetes 2005;54:778–84.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang H, Siren J, Perttunen S, Immonen K, Chen Y-C, Narumanchi S, et al. Deficiency of heme oxygenase 1a causes detrimental effects on cardiac function. J Cell Mol Med 2024;28:e18243.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kovtunovych G, Ghosh MC, Ollivierre W, Weitzel RP, Eckhaus MA, Tisdale JF, et al. Wild-type macrophages reverse disease in heme oxygenase 1-deficient mice. Blood 2014;124:1522–30.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yachie A. Heme oxygenase-1 deficiency and oxidative stress: a review of 9 independent human cases and animal models. Int J Mol Sci 2021;22:1514.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Evans JM, Navarro S, Doki T, Stewart JM, Mitsuhashi N, Kearns-Jonker M. Gene transfer of heme oxygenase-1 using an adeno-associated virus serotype 6 vector prolongs cardiac allograft survival. J Transplant 2012;2012:740653.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu X, Simpson JA, Brunt KR, Ward CA, Hall SRR, Kinobe RT, et al. Preemptive heme oxygenase-1 gene delivery reveals reduced mortality and preservation of left ventricular function 1 yr after acute myocardial infarction. Am J Physiol Heart C 2007;293:H48–H59.

    Article 
    CAS 

    Google Scholar
     

  • Bellner L, Lebovics NB, Rubinstein R, Buchen YD, Sinatra E, Sinatra G, et al. Heme oxygenase-1 upregulation: a novel approach in the treatment of cardiovascular disease. Antioxid Redox Signal 2019;32:1045–60.

    Article 

    Google Scholar
     

  • Ndisang JF, Jadhav A. Heme oxygenase system enhances insulin sensitivity and glucose metabolism in streptozotocin-induced diabetes. Am J Physiol Endocrinol M 2009;296:E829–E41.

    Article 
    CAS 

    Google Scholar
     

  • Xu G, Ma Y, Jin J, Wang X. Activation of AMPK/p38/Nrf2 is involved in resveratrol alleviating myocardial ischemia-reperfusion injury in diabetic rats as an endogenous antioxidant stress feedback. Ann Transl Med 2022;10:890.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhao C, Zhang Y, Liu H, Li P, Zhang H, Cheng G. Fortunellin protects against high fructose-induced diabetic heart injury in mice by suppressing inflammation and oxidative stress via AMPK/Nrf-2 pathway regulation. Biochem Biophys Res Commun 2017;490:552–9.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ge X, Wang L, Fei A, Ye S, Zhang Q. Research progress on the relationship between autophagy and chronic complications of diabetes. Front Physiol 2022;13:956344.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhao Y, Zhang L, Qiao Y, Zhou X, Wu G, Wang L, et al. Heme oxygenase-1 prevents cardiac dysfunction in streptozotocin-diabetic mice by reducing inflammation, oxidative stress, apoptosis and enhancing autophagy. Plos One 2013;8:e75927.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ni J, Li Y, Xu Y, Guo R. Salidroside protects against cardiomyocyte apoptosis and ventricular remodeling by AKT/HO-1 signaling pathways in a diabetic cardiomyopathy mouse model. Phytomedicine 2021;82:153406.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liao HH, Zhu JX, Feng H, Ni J, Zhang N, Chen S, et al. Myricetin possesses potential protective effects on diabetic cardiomyopathy through Inhibiting IκBα/NFκB and enhancing Nrf2/HO-1. Oxid Med Cell Longev 2017;2017:8370593.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wei Z, Shaohuan Q, Pinfang K, Chao S. Curcumin attenuates ferroptosis-induced myocardial injury in diabetic cardiomyopathy through the Nrf2 pathway. Cardiovasc Ther 2022;2022:3159717.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wu X, Zhou X, Lai S, Liu J, Qi J. Curcumin activates Nrf2/HO-1 signaling to relieve diabetic cardiomyopathy injury by reducing ROS in vitro and in vivo. FASEB J 2022;36:e22505.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Monteiro-Soares M, Boyko EJ, Jeffcoate W, Mills JL, Russell D, Morbach S, et al. Diabetic foot ulcer classifications: a critical review. Diabetes Metab Res Rev 2020;36:e3272.

    Article 
    PubMed 

    Google Scholar
     

  • Dixon D, Edmonds M. Managing diabetic foot ulcers: pharmacotherapy for wound healing. Drugs 2021;81:29–56.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Grochot-Przeczek A, Dulak J, Jozkowicz A. Heme oxygenase-1 in neovascularisation: a diabetic perspective. Thromb Haemost 2010;104:424–31.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Baltzis D, Eleftheriadou I, Veves A. Pathogenesis and treatment of impaired wound healing in diabetes mellitus: new insights. Adv Ther 2014;31:817–36.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen VY, Siegfried LG, Tomic-Canic M, Stone RC, Pastar I. Cutaneous changes in diabetic patients: primed for aberrant healing? Wound Repair Regen 2023;31:700–12.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen QY, Wang GG, Li W, Jiang YX, Lu XH, Zhou PP. Heme oxygenase-1 promotes delayed wound healing in diabetic rats. J Diab Res 2016;2016:9726503.


    Google Scholar
     

  • Fan J, Liu H, Wang J, Zeng J, Tan Y, Wang Y, et al. Procyanidin B2 improves endothelial progenitor cell function and promotes wound healing in diabetic mice via activating Nrf2. J Cell Mol Med 2021;25:652–65.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ram M, Singh V, Kumar D, Kumawat S, Gopalakrishnan A, Lingaraju MC, et al. Antioxidant potential of bilirubin-accelerated wound healing in streptozotocin-induced diabetic rats. Naunyn Schmiedebergs Arch Pharmacol 2014;387:955–61.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Motterlini R, Otterbein LE. The therapeutic potential of carbon monoxide. Nat Rev Drug Discov 2010;9:728–43.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rodella FL, Vanella L, Peterson JS, Drummond G, Rezzani R, Falck RJ, et al. Heme oxygenase-derived carbon monoxide restores vascular function in type 1 diabetes. Drug Metab Lett 2008;2:290–300.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tu C, Lu H, Zhou T, Zhang W, Deng L, Cao W, et al. Promoting the healing of infected diabetic wound by an anti-bacterial and nano-enzyme-containing hydrogel with inflammation-suppressing, ROS-scavenging, oxygen and nitric oxide-generating properties. Biomaterials 2022;286:121597.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Krzyszczyk P, Kang HJ, Kumar S, Meng Y, O’Reggio MD, Patel K, et al. Anti-inflammatory effects of haptoglobin on LPS-stimulated macrophages: role of HMGB1 signaling and implications in chronic wound healing. Wound Repair Regen 2020;28:493–505.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cano Sanchez M, Lancel S, Boulanger E, Neviere R. Targeting oxidative stress and mitochondrial dysfunction in the treatment of impaired wound healing: a systematic review. Antioxidants 2018;7:98.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Leal EC, Carvalho E. Heme oxygenase-1 as therapeutic target for diabetic foot ulcers. Int J Mol Sci 2022;23:12043.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 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.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yan C, Chen J, Wang C, Yuan M, Kang Y, Wu Z, et al. Milk exosomes-mediated miR-31-5p delivery accelerates diabetic wound healing through promoting angiogenesis. Drug Deliv 2022;29:214–28.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Guan Y, Niu H, Liu Z, Dang Y, Shen J, Zayed M, et al. Sustained oxygenation accelerates diabetic wound healing by promoting epithelialization and angiogenesis and decreasing inflammation. Sci Adv 2021;7:eabj0153.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Deshane J, Chen S, Caballero S, Grochot-Przeczek A, Was H, Li Calzi S, et al. Stromal cell–derived factor 1 promotes angiogenesis via a heme oxygenase 1–dependent mechanism. J Exp Med 2007;204:605–18.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Badr, El-Hossary G, Lasheen FM, FE-dM, Negm NZ, Khalaf M, et al. Cold atmospheric plasma induces the curing mechanism of diabetic wounds by regulating the oxidative stress mediators iNOS and NO, the pyroptotic mediators NLRP-3, caspase-1 and IL-1β and the angiogenesis mediators VEGF and Ang-1. Biomed Pharmacother 2023;169:115934.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kuo CS, Chen CY, Huang HL, Tsai HY, Chou RH, Wei JH, et al. Melatonin improves ischemia-induced circulation recovery impairment in mice with streptozotocin-induced diabetes by improving the endothelial progenitor cells functioning. Int J Mol Sci 2022;23:9839.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xu C, Hu L, Zeng J, Wu A, Deng S, Zhao Z, et al. Gynura divaricata (L.) DC. promotes diabetic wound healing by activating Nrf2 signaling in diabetic rats. J Ethnopharmacol 2024;323:117638.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Huang H, Wang L, Qian F, Chen X, Zhu H, Yang M, et al. Liraglutide via activation of AMP-activated protein kinase-hypoxia inducible factor-1α-heme oxygenase-1 signaling promotes wound healing by preventing endothelial dysfunction in diabetic mice. Front Physiol 2021;12:660263.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hasan Maleki M, Siri M, Jafarabadi A, Rajabi M, Amirhossein Mazhari S, Noori Z, et al. Boosting wound healing in diabetic rats: the role of nicotinamide riboside and resveratrol in UPR modulation and pyroptosis inhibition. Int Immunopharmacol 2024;132:112013.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhou D, Liang Q, Ge X, Xu J. Allogeneic platelet-rich plasma inhibits ferroptosis in promoting wound repair of type 2 diabetic ulcers. Free Radic Bio Med 2024;215:37–47.

    Article 
    CAS 

    Google Scholar
     

  • Lu Y, Zhao D, Cao G, Yin S, Liu C, Song R, et al. Research progress on and molecular mechanism of vacuum sealing drainage in the treatment of diabetic foot ulcers. Front Surg 2024;11:1265360.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lee HB, Ha H, Kim SI, Ziyadeh FN. Diabetic kidney disease research: where do we stand at the turn of the century? Kidney Int 2000;58:S1–S2.

    Article 

    Google Scholar
     

  • Pradhan D, Sahu PK, Purohit S, Ranajit SK, Acharya B, Sangam S, et al. Therapeutic interventions for diabetes mellitus-associated complications. Curr Diab Rev 2024;20:1–21.

    Article 

    Google Scholar
     

  • Kuang Y, Yang J, Sun M, Rui T, Yang Z, Shi M. Depression of LncRNA DANCR alleviates tubular injury in diabetic nephropathy by regulating KLF5 through sponge miR-214-5p. BMC Nephrol 2024;25:130.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Matoba K, Takeda Y, Nagai Y, Sekiguchi K, Yokota T, Utsunomiya K, et al. The physiology, pathology, and therapeutic interventions for ROCK isoforms in diabetic kidney disease. Front Pharmacol 2020;11:585633.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ptilovanciv EON, Fernandes GS, Teixeira LC, Reis LA, Pessoa EA, Convento MB, et al. Heme oxygenase 1 improves glucoses metabolism and kidney histological alterations in diabetic rats. Diabetol Metab Synd 2013;5:3.

    Article 
    CAS 

    Google Scholar
     

  • Darenskaya MA, Kolesnikova LI, Kolesnikov SI. Oxidative Stress: Pathogenetic role in diabetes mellitus and its complications and therapeutic approaches to correction. Bull Exp Biol Med 2021;171:179–89.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Halim M, Halim A. The effects of inflammation, aging and oxidative stress on the pathogenesis of diabetes mellitus (type 2 diabetes). Diab Metab Synd 2019;13:1165–72.

    Article 

    Google Scholar
     

  • Ma L, Wu F, Shao Q, Chen G, Xu L, Lu FA-O. Baicalin alleviates oxidative stress and inflammation in diabetic nephropathy via Nrf2 and MAPK signaling pathway. Drug Des Dev Ther 2021;15:3207–21.

    Article 

    Google Scholar
     

  • Zhang B, Zhang X, Zhang C, Shen Q, Sun G, Sun X. Notoginsenoside R1 protects db/db mice against diabetic nephropathy via upregulation of Nrf2-Mediated HO-1 expression. Molecules 2019;24:247.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pham TK, Nguyen THT, Yun HR, Vasileva EA, Mishchenko NP, Fedoreyev SA, et al. Echinochrome A prevents diabetic nephropathy by inhibiting the PKC-iota pathway and enhancing renal mitochondrial function in db/db mice. Mar Drugs 2023;21:222.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen ZQ, Sun XH, Li XJ, Xu ZC, Yang Y, Lin ZY, et al. Polydatin attenuates renal fibrosis in diabetic mice through regulating the Cx32-Nox4 signaling pathway. Acta Pharm Sin 2020;41:1587–96.

    Article 
    CAS 

    Google Scholar
     

  • Chen Q, Tao J, Xie X. Astaxanthin promotes Nrf2/ARE signaling to inhibit HG-induced renal fibrosis in GMCs. Mar Drugs 2018;16:117.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen Q, Tao J, Li G, Zheng D, Tan Y, Li R, et al. Astaxanthin ameliorates experimental diabetes-induced renal oxidative stress and fibronectin by upregulating connexin43 in glomerular mesangial cells and diabetic mice. Eur J Pharmacol 2018;840:33–43.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yu WC, Huang RY, Chou TC. Oligo-Fucoidan improves diabetes-induced renal fibrosis via activation of Sirt-1, GLP-1R, and Nrf2/HO-1: an in vitro and in vivo study. Nutrients 2020;12:3068.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wei X, Ma Y, Li Y, Zhang W, Zhong Y, Yu Y, et al. Anti-apoptosis of podocytes and pro-apoptosis of mesangial cells for telmisartan in alleviating diabetic kidney injury. Front Pharmacol 2022;13:876469.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Antar SA, Abdo W, Taha RS, Farage AE, El-Moselhy LE, Amer ME, et al. Telmisartan attenuates diabetic nephropathy by mitigating oxidative stress and inflammation, and upregulating Nrf2/HO-1 signaling in diabetic rats. Life Sci 2022;291:120260.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Alaofi AL. Sinapic acid ameliorates the progression of streptozotocin (STZ)-induced diabetic nephropathy in rats via NRF2/HO-1 mediated pathways. Front Pharmacol 2020;11:1119.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang Y, Bi R, Quan F, Cao Q, Lin Y, Yue C, et al. Ferroptosis involves in renal tubular cell death in diabetic nephropathy. Eur J Pharmacol 2020;888:173574.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jin T, Chen C. Umbelliferone delays the progression of diabetic nephropathy by inhibiting ferroptosis through activation of the Nrf-2/HO-1 pathway. Food Chem Toxicol 2022;163:112892.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wu Y, Zhao Y, Yang H-z, Wang Y-j, Chen Y. HMGB1 regulates ferroptosis through Nrf2 pathway in mesangial cells in response to high glucose. Biosci Rep. 2021;41:BSR20202924.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kour V, Swain J, Singh J, Singh H, Kour H. A review on diabetic retinopathy. Curr Diab Rev 2024;20:74–88.

    Article 

    Google Scholar
     

  • Cano-Cano F, Alcalde-Estévez E, Gómez-Jaramillo L, Iturregui M, Sánchez-Fernández EM, García Fernández JM, et al. Anti-inflammatory (M2) response is induced by a sp2-iminosugar glycolipid sulfoxide in diabetic retinopathy. Front Immunol 2021;12:632132.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sun Z, Wang Y, Xu R, Zhang S, Yang H, Song J, et al. Hydroxysafflor yellow a improved retinopathy via Nrf2/HO-1 pathway in rats. Open Life Sci 2022;17:284–92.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li S, Lu S, Wang L, Liu S, Zhang L, Du J, et al. Effects of amygdalin on ferroptosis and oxidative stress in diabetic retinopathy progression via the NRF2/ARE signaling pathway. Exp Eye Res 2023;234:109569.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ke B, Zhang T, An T, Lu R. Soy isoflavones ameliorate the cognitive dysfunction of Goto-Kakizaki rats by activating the Nrf2-HO-1 signalling pathway. Aging 2020;12:21344–54.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang F, Shang Y, Zhang R, Gao X, Zeng Q. A SIRT1 agonist reduces cognitive decline in type 2 diabetic rats through antioxidative and anti‑inflammatory mechanisms. Mol Med Rep 2019;19:1040–8.

    CAS 
    PubMed 

    Google Scholar
     

  • Liang E, Ma M, Wang L, Liu X, Xu J, Zhang M, et al. The BET/BRD inhibitor JQ1 attenuates diabetes-induced cognitive impairment in rats by targeting Nox4-Nrf2 redox imbalance. Biochem Biophys Res Commun 2018;495:204–11.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Deng C, Meng Z, Chen H, Meng S. Tetramethylpyrazine ameliorates systemic streptozotocin-induced Alzheimer-like pathology. J Chem Neuroanat 2023;127:102207.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Xiaojun M, Min S, Yushan Y, Gaofei R, Jingwen H, Guijun Q. et al. Albiflorin alleviates cognitive dysfunction in STZ-induced rats. Aging. 2021;13:18287–97.

    Article 

    Google Scholar
     

  • Sun H, Lu S, Qu G, Li J, Song B. Mesenchymal stem cells-derived exosomes ameliorate high glucose and lipopolysaccharide-induced HPMECs injury through the Nrf2/HO-1 pathway. Autoimmunity 2023;56:2290357.

    Article 
    PubMed 

    Google Scholar
     

  • Song JX, An JR, Chen Q, Yang XY, Jia CL, Xu S, et al. Liraglutide attenuates hepatic iron levels and ferroptosis in db/db mice. Bioengineered 2022;13:8334–48.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cheng X, Huang J, Li H, Zhao D, Liu Z, Zhu L, et al. Quercetin: a promising therapy for diabetic encephalopathy through inhibition of hippocampal ferroptosis. Phytomedicine 2024;126:154887.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yao Q, Sun R, Bao S, Chen R, Kou L. Bilirubin protects transplanted islets by targeting ferroptosis. Front Pharmacol 2020;11:907.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gao Z, Zhang Z, Gu D, Li Y, Zhang K, Dong X, et al. Hemin mitigates contrast-induced nephropathy by inhibiting ferroptosis via HO-1/Nrf2/GPX4 pathway. Clin Exp Pharm P 2022;49:858–70.

    Article 
    CAS 

    Google Scholar
     

  • Stancic A, Velickovic K, Markelic M, Grigorov I, Saksida T, Savic N, et al. Involvement of ferroptosis in diabetes-induced liver pathology. Int J Mol Sci 2022;23:9309.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wu J, Zhao Y, Fan Z, Chen Q, Chen J, Sun Y, et al. Soluble epoxide hydrolase inhibitor protects against blood-brain barrier dysfunction in a mouse model of type 2 diabetes via the AMPK/HO-1 pathway. Biochem Biophys Res Commun 2020;524:354–9.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wu S, Zhu J, Wu G, Hu Z, Ying P, Bao Z, et al. 6-Gingerol alleviates ferroptosis and Inflammation of diabetic cardiomyopathy via the Nrf2/HO-1 pathway. Oxi Med Cell Longev 2022;2022:3027514.


    Google Scholar
     

  • Puhari SSM, Yuvaraj S, Vasudevan V, Ramprasath T, Arunkumar K, Amutha C, et al. Fucoidan from sargassum wightii reduces oxidative stress through upregulating Nrf2/HO-1 signaling pathway in alloxan-induced diabetic cardiomyopathy rats. Mol Biol Rep 2023;50:8855–66.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Uddandrao VVS, Parim B, Singaravel S, Ponnusamy P, Ponnusamy C, Sasikumar V, et al. Polyherbal formulation ameliorates diabetic cardiomyopathy through attenuation of cardiac inflammation and oxidative stress via NF-κB/Nrf-2/HO-1 pathway in diabetic rats. J Cardiovasc Pharm 2022;79:e75–e86.

    Article 
    CAS 

    Google Scholar
     

  • Li H, Shi Y, Wang X, Li P, Zhang S, Wu T, et al. Piceatannol alleviates inflammation and oxidative stress via modulation of the Nrf2/HO-1 and NF-κB pathways in diabetic cardiomyopathy. Chem Biol Interact 2019;310:108754.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Umar U, Ahmed S, Iftikhar A, Iftikhar M, Majeed W, Liaqat A, et al. Phenolics extracted from Jasminum sambac mitigates diabetic cardiomyopathy by modulating oxidative stress, apoptotic mediators and the Nfr-2/HO-1 pathway in alloxan-induced diabetic rats. Molecules 2023;28:5453.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li X, Wu D, Tian Y. Fibroblast growth factor 19 protects the heart from oxidative stress-induced diabetic cardiomyopathy via activation of AMPK/Nrf2/HO-1 pathway. Biochem Biophys Res Commun 2018;502:62–68.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wei Z, Jing Z, Pinfang K, Chao S, Shaohuan Q. Quercetin inhibits pyroptosis in diabetic cardiomyopathy through the Nrf2 pathway. J Diabetes Res 2022;2022:9723632.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen J, Guo P, Han M, Chen K, Qin J, Yang F. Cognitive protection of sinomenine in type 2 diabetes mellitus through regulating the EGF/Nrf2/HO-1 signaling, the microbiota-gut-brain axis, and hippocampal neuron ferroptosis. Phytother Res 2023;37:3323–41.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang B, Zhu S, Guo M, Ma R-D, Tang Y-L, Nie Y-X, et al. Artemisinin ameliorates cognitive decline by inhibiting hippocampal neuronal ferroptosis via Nrf2 activation in T2DM mice. Mol Med 2024;30:35.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zou W, Yuan J, Tang ZJ, Wei HJ, Zhu WW, Zhang P, et al. Hydrogen sulfide ameliorates cognitive dysfunction in streptozotocin-induced diabetic rats: involving suppression in hippocampal endoplasmic reticulum stress. Oncotarget 2017;8:64203–16.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xianchu L, Kang L, Beiwan D, Huan P, Ming L. Apocynin ameliorates cognitive deficits in streptozotocin-induced diabetic rats. Bratisl Lek Listy 2021;122:78–84.

    CAS 
    PubMed 

    Google Scholar
     

  • Ma C, Long H. Protective effect of betulin on cognitive decline in streptozotocin (STZ)-induced diabetic rats. NeuroToxicology 2016;57:104–11.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yuan S, Liang X, He W, Liang M, Jin J, He QA-O. ATF4-dependent heme-oxygenase-1 attenuates diabetic nephropathy by inducing autophagy and inhibiting apoptosis in podocyte. Ren Fail 2021;43:968–79.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jiang N, Zhao H, Han Y, Li L, Xiong S, Zeng L, et al. HIF-1α ameliorates tubular injury in diabetic nephropathy via HO–1–mediated control of mitochondrial dynamics. Cell Prolif 2020;53:e12909.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Raish M, Ahmad A, Bin Jardan YA, Shahid M, Alkharfy KM, Ahad A, et al. Sinapic acid ameliorates cardiac dysfunction and cardiomyopathy by modulating NF-κB and Nrf2/HO-1 signaling pathways in streptozocin induced diabetic rats. Biomed Pharmacother 2022;145:112412.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yan Y, Yuan N, Chen Y, Ma Y, Chen A, Wang F, et al. SKP alleviates the ferroptosis in diabetic kidney disease through suppression of HIF-1α/HO-1 pathway based on network pharmacology analysis and experimental validation. Chin Med 2024;19:31.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang G, Zhang X, Lu X, Liu J, Zhang Z, Wei Z, et al. Fish oil supplementation attenuates cognitive impairment by inhibiting neuroinflammation in STZ-induced diabetic rats. Aging 2020;12:15281–9.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ma H, Wang X, Zhang W, Li H, Zhao W, Sun J, et al. Melatonin suppresses ferroptosis induced by high glucose via activation of the Nrf2/HO-1 signaling pathway in type 2 diabetic osteoporosis. Oxid Med Cell Longev 2020;2020:9067610.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li Y, Liu J, Ma X, Bai X. Maresin-1 inhibits high glucose induced ferroptosis in ARPE-19 cells by activating the Nrf2/HO-1/GPX4 pathway. BMC Ophthalmol 2023;23:368.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Huang YC, Chen BC, Chang KF, Hsieh MC, Sheu GT, Hsiao CY, et al. The alleviation effects of n-butylidenephthalide on apoptosis, senescence, and tight junction impairment of retinal pigment epithelium by activating Nrf-2/HO-1 signaling pathway in early diabetic retinopathy. Life Sci 2023;327:121815.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Xu Z, Li S, Li K, Wang X, Li X, An M, et al. Urolithin a ameliorates diabetic retinopathy via activation of the Nrf2/HO-1 pathway. Endocr J 2022;69:971–82.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhang XX, Ji YL, Zhu LP, Wang ZH, Fang CQ, Jiang CH, et al. Arjunolic acid from cyclocarya paliurus ameliorates diabetic retinopathy through AMPK/mTOR/HO-1 regulated autophagy pathway. J Ethnopharmacol 2022;284:114772.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Song Y, Lv P, Yu J. Platycodin d inhibits diabetic retinopathy via suppressing TLR4/MyD88/NF-κB signaling pathway and activating Nrf2/HO-1 signaling pathway. Chem Biol Drug Des 2024;103:e14419.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fang J, Bai W, Yang L. Astaxanthin inhibits oxidative stress and apoptosis in diabetic retinopathy. Acta Histochem 2023;125:152069.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yang X, Li D. Tricin attenuates diabetic retinopathy by inhibiting oxidative stress and angiogenesis through regulating Sestrin2/Nrf2 signaling. Hum Exp Toxicol 2023;42:09603271231171642.

    Article 
    CAS 

    Google Scholar
     

  • D’Agata V, D’Amico AG, Maugeri G, Bucolo C, Rossi S, Giunta S. Carnosol attenuates high glucose damage in human retinal endothelial cells through regulation of ERK/Nrf2/HO-1 pathway. J Asian Nat Prod Res 2023;25:783–95.

    Article 
    PubMed 

    Google Scholar
     

  • Shi Q, Cheng Y, Dong X, Zhang M, Pei C, Zhang M. Effects of rhaponticin on retinal oxidative stress and inflammation in diabetes through NRF2/HO-1/NF-κB signalling. J Biochem Mol Toxic 2020;34:e22568.

    Article 
    CAS 

    Google Scholar
     

  • Pu Q, Guo XX, Hu JJ, Li AL, Li GG, Li XY. Nicotinamide mononucleotide increases cell viability and restores tight junctions in high-glucose-treated human corneal epithelial cells via the SIRT1/Nrf2/HO-1 pathway. Biomed Pharmacother 2022;147:112659.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang P, Fan S, Hu X, Luo L, Ying J, Li J. MG132, attenuates the retinal vascular injury through the upregulation of Nrf2 expression. J Ocul Pharm Ther 2023;39:661–71.

    Article 
    CAS 

    Google Scholar
     

  • Yang J, Hua Z, Zheng Z, Ma X, Zhu L, Li Y. Acteoside inhibits high glucose-induced oxidative stress injury in RPE cells and the outer retina through the Keap1/Nrf2/ARE pathway. Exp Eye Res 2023;232:109496.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lin HD, Lee YC, Chiang CY, Lin YJ, Shih CY, Tsai RK, et al. Protective effects of Scoparia dulcis L. extract on high glucose-induced injury in human retinal pigment epithelial cells. Front Nutr 2023;10:1085248.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hao Y, Gao X. Diosgenin protects retinal pigment epithelial cells from inflammatory damage and oxidative stress induced by high glucose by activating AMPK/Nrf2/HO-1 pathway. Immun Inflamm Dis 2022;10:e698.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhu J, Sun H, Kang X, Zhu H, Yan X. Acidic polysaccharides from Buddleja officinalis inhibit angiogenesis via the Nrf2/ARE pathway to attenuate diabetic retinopathy. Food Funct 2022;13:9021–31.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Xu Z, Liu Y, Ma R, Chen J, Qiu J, Du S, et al. Thermosensitive hydrogel incorporating Prussian blue nanoparticles promotes diabetic wound healing via ROS scavenging and mitochondrial function restoration. ACS Appl Mater Interfaces 2022;14:14059–71.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Vendidandala NR, Yin TP, Nelli G, Pasupuleti VR, Nyamathulla S, Mokhtar SI. Gallocatechin‑silver nanoparticle impregnated cotton gauze patches enhance wound healing in diabetic rats by suppressing oxidative stress and inflammation via modulating the Nrf2/HO-1 and TLR4/NF-κB pathways. Life Sci 2021;286:120019.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhang Z, Zheng Y, Chen N, Xu C, Deng J, Feng X, et al. San Huang Xiao Yan recipe modulates the HMGB1-mediated abnormal inflammatory microenvironment and ameliorates diabetic foot by activating the AMPK/Nrf2 signalling pathway. Phytomedicine 2023;118:154931.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang S, Shi M, Zhou J, Wang W, Zhang Y, Li Y Circulating exosomal mir-181b-5p promoted cell senescence and inhibited angiogenesis to impair diabetic foot ulcer via the nuclear factor erythroid 2-related factor 2/Heme oxygenase-1 pathway. Front Cardiovasc Med. 2022;9844047.

  • Lin S, Zhang Q, Li S, Zhang T, Wang L, Qin X, et al. Antioxidative and angiogenesis-promoting effects of tetrahedral framework nucleic acids in diabetic wound healing with activation of the Akt/Nrf2/HO-1 Pathway. ACS Appl Mater Interfaces 2020;12:11397–408.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yin X, Fan X, Zhou Z, Li Q. Encapsulation of berberine decorated ZnO nano-colloids into injectable hydrogel using for diabetic wound healing. Front Chem 2022;10:964662.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pan-Yue Q, Ya-Jing X, Xiang-Duo Z, Jun-Hua D, Bin Q, Xue-Fang L, et al. Effect and mechanisms of Polygonatum kingianum (polygonati rhizome) on wound healing in diabetic rats. J Ethnopharmacol 2022;298:115612.

    Article 
    PubMed 

    Google Scholar
     

  • Wang G, Li W, Chen Q, Jiang Y, Lu X, Zhao X. Hydrogen sulfide accelerates wound healing in diabetic rats. Int J Clin Exp Pathol 2015;8:5097–104.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li M, Yu H, Pan H, Zhou X, Ruan Q, Kong D, et al. Nrf2 suppression delays diabetic wound healing through sustained oxidative stress and inflammation. Front Pharmacol 2019;10:1099.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

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