Generic placeholder image

Current Molecular Medicine

Editor-in-Chief

ISSN (Print): 1566-5240
ISSN (Online): 1875-5666

Review Article

Role of Innate Immune and Inflammatory Responses in the Development of Secondary Diabetic Complications

Author(s): Trevor J. Plowman, Mujtaba H. Shah, Emely Fernandez, Hannah Christensen, Myia Aiges and Kota V. Ramana*

Volume 23, Issue 9, 2023

Published on: 25 October, 2022

Page: [901 - 920] Pages: 20

DOI: 10.2174/1566524023666220922114701

Price: $65

Abstract

Increased hyperglycemia due to uncontrolled diabetes is the major cause of secondary diabetic complications such as retinopathy, neuropathy, nephropathy, and cardiovascular diseases. Although it is well known that increased oxidative stress, activation of the polyol pathway, protein kinase C and increased generation of advanced glycation end products could contribute to the development of diabetic complications, recent studies implicated the role of innate immunity and its related inflammatory responses in the pathophysiology of secondary diabetic complications. Increased activation of oxidative stress signaling could regulate NLRP3 inflammasome-mediated innate immune responses as well as NF-κB signalosome-mediated pro-inflammatory responses. This review article focused on the pathogenic role of innate immune and inflammatory responses in the progression of hyperglycemia-induced secondary diabetic complications. Specifically, we discussed in depth how deregulated innate immune and inflammatory responses could lead to an aggravated release of cytokines, chemokines, and growth factors resulting in the development of various secondary complications of diabetes.

Keywords: Diabetes, hyperglycemia, innate immunity, inflammation, oxidative stress, glucose.

[1]
Koye DN, Magliano DJ, Nelson RG, Pavkov ME. The global epidemiology of diabetes and kidney disease. Adv Chronic Kidney Dis 2018; 25(2): 121-32.
[http://dx.doi.org/10.1053/j.ackd.2017.10.011] [PMID: 29580576]
[2]
Rhodes CJ. Type 2 diabetes-a matter of beta-cell life and death? Science 2005; 307(5708): 380-4.
[http://dx.doi.org/10.1126/science.1104345] [PMID: 15662003]
[3]
Sherry NA, Tsai EB, Herold KC. Natural history of beta-cell function in type 1 diabetes. Diabetes 2005; 54(S2): S32-9.
[http://dx.doi.org/10.2337/diabetes.54.suppl_2.S32] [PMID: 16306337]
[4]
Fowler MJ. Microvascular and macrovascular complications of diabetes. Clin Diabetes 2008; 26(2): 77-82.
[http://dx.doi.org/10.2337/diaclin.26.2.77]
[5]
Nishikawa T, Edelstein D, Du XL, et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000; 404(6779): 787-90.
[http://dx.doi.org/10.1038/35008121] [PMID: 10783895]
[6]
Nishikawa T, Edelstein D, Brownlee M. The missing link: A single unifying mechanism for diabetic complications. Kidney Int 2000; 58: S26-30.
[http://dx.doi.org/10.1046/j.1523-1755.2000.07705.x] [PMID: 10997687]
[7]
Nishikawa T, Araki E. Impact of mitochondrial ROS production in the pathogenesis of diabetes mellitus and its complications. Antioxid Redox Signal 2007; 9(3): 343-53.
[http://dx.doi.org/10.1089/ars.2006.1458] [PMID: 17184177]
[8]
Hammes HP, Du X, Edelstein D, et al. Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nat Med 2003; 9(3): 294-9.
[http://dx.doi.org/10.1038/nm834] [PMID: 12592403]
[9]
Bönhof GJ, Sipola G, Strom A, et al. BOND study: A randomised double-blind, placebo-controlled trial over 12 months to assess the effects of benfotiamine on morphometric, neurophysiological and clinical measures in patients with type 2 diabetes with symptomatic polyneuropathy. BMJ Open 2022; 12(2): e057142.
[http://dx.doi.org/10.1136/bmjopen-2021-057142] [PMID: 35115359]
[10]
Srivastava SK, Ramana KV, Bhatnagar A. Role of aldose reductase and oxidative damage in diabetes and the consequent potential for therapeutic options. Endocr Rev 2005; 26(3): 380-92.
[http://dx.doi.org/10.1210/er.2004-0028] [PMID: 15814847]
[11]
Wu XQ, Zhang DD, Wang YN, Tan YQ, Yu XY, Zhao YY. AGE/RAGE in diabetic kidney disease and ageing kidney. Free Radic Biol Med 2021; 171: 260-71.
[http://dx.doi.org/10.1016/j.freeradbiomed.2021.05.025] [PMID: 34019934]
[12]
Sanajou D, Ghorbani HA, Argani H, Aslani S. AGE-RAGE axis blockade in diabetic nephropathy: Current status and future directions. Eur J Pharmacol 2018; 833: 158-64.
[http://dx.doi.org/10.1016/j.ejphar.2018.06.001] [PMID: 29883668]
[13]
Kolczynska K, Loza-Valdes A, Hawro I, Sumara G. Diacylglycerol-evoked activation of PKC and PKD isoforms in regulation of glucose and lipid metabolism: A review. Lipids Health Dis 2020; 19(1): 113.
[http://dx.doi.org/10.1186/s12944-020-01286-8] [PMID: 32466765]
[14]
Geraldes P, King GL. Activation of protein kinase C isoforms and its impact on diabetic complications. Circ Res 2010; 106(8): 1319-31.
[http://dx.doi.org/10.1161/CIRCRESAHA.110.217117] [PMID: 20431074]
[15]
Kang Q, Yang C. Oxidative stress and diabetic retinopathy: Molecular mechanisms, pathogenetic role and therapeutic implications. Redox Biol 2020; 37: 101799.
[http://dx.doi.org/10.1016/j.redox.2020.101799] [PMID: 33248932]
[16]
Elumalai S, Karunakaran U, Moon JS, Won KC. NADPH oxidase (NOX) targeting in diabetes: A special emphasis on pancreatic β-cell dysfunction. Cells 2021; 10(7): 1573.
[http://dx.doi.org/10.3390/cells10071573] [PMID: 34206537]
[17]
Moscat J, Diaz-Meco MT, Rennert P. NF‐κB activation by protein kinase C isoforms and B‐cell function. EMBO Rep 2003; 4(1): 31-6.
[http://dx.doi.org/10.1038/sj.embor.embor704] [PMID: 12524517]
[18]
Ramana KV, Friedrich B, Srivastava S, Bhatnagar A, Srivastava SK. Activation of nuclear factor-kappaB by hyperglycemia in vascular smooth muscle cells is regulated by aldose reductase. Diabetes 2004; 53(11): 2910-20.
[http://dx.doi.org/10.2337/diabetes.53.11.2910] [PMID: 15504972]
[19]
Du XL, Edelstein D, Dimmeler S, Ju Q, Sui C, Brownlee M. Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J Clin Invest 2001; 108(9): 1341-8.
[http://dx.doi.org/10.1172/JCI11235] [PMID: 11696579]
[20]
Daniels MC, McClain DA, Crook ED. Transcriptional regulation of transforming growth factor β1 by glucose: Investigation into the role of the hexosamine biosynthesis pathway. Am J Med Sci 2020; 359(2): 79-83.
[http://dx.doi.org/10.1016/j.amjms.2019.12.013] [PMID: 32039769]
[21]
Patel S, Santani D. Role of NF-κB in the pathogenesis of diabetes and its associated complications. Pharmacol Rep 2009; 61(4): 595-603.
[http://dx.doi.org/10.1016/S1734-1140(09)70111-2] [PMID: 19815941]
[22]
Bai Y, Mu Q, Bao X, et al. Targeting NLRP3 inflammasome in the treatment of diabetes and diabetic complications: Role of natural compounds from herbal medicine. Aging Dis 2021; 12(7): 1587-604.
[http://dx.doi.org/10.14336/AD.2021.0318] [PMID: 34631209]
[23]
Wang Z, Ni X, Zhang L, et al. Toll-like receptor 4 and inflammatory micro-environment of pancreatic islets in type-2 diabetes mellitus: A therapeutic perspective. Diabetes Metab Syndr Obes 2020; 13: 4261-72.
[http://dx.doi.org/10.2147/DMSO.S279104] [PMID: 33204132]
[24]
Jin X, Zhou R, Huang Y. Role of inflammasomes in HIV-1 infection and treatment. Trends Mol Med 2022; S1471-4914(22): 51.
[http://dx.doi.org/10.1016/j.molmed.2022.02.010]
[25]
Gomes CP, Torloni MR, Gueuvoghlanian-Silva BY, Alexandre SM, Mattar R, Daher S. Cytokine levels in gestational diabetes mellitus: A systematic review of the literature. Am J Reprod Immunol 2013; 69(6): n/a.
[http://dx.doi.org/10.1111/aji.12088] [PMID: 23414425]
[26]
Sabaner MC, Akdogan M, Doğan M, et al. Inflammatory cytokines, oxidative and antioxidative stress levels in patients with diabetic macular edema and hyperreflective spots. Eur J Ophthalmol 2021; 31(5): 2535-45.
[http://dx.doi.org/10.1177/1120672120962054] [PMID: 33008266]
[27]
Khan S, Luck H, Winer S, Winer DA. Emerging concepts in intestinal immune control of obesity-related metabolic disease. Nat Commun 2021; 12(1): 2598.
[http://dx.doi.org/10.1038/s41467-021-22727-7] [PMID: 33972511]
[28]
Zhuang Y, Zhang J, Li Y, et al. B lymphocytes are predictors of insulin resistance in women with gestational diabetes mellitus. Endocr Metab Immune Disord Drug Targets 2019; 19(3): 358-66.
[http://dx.doi.org/10.2174/1871530319666190101130300] [PMID: 30621567]
[29]
Lechner J, O’Leary OE, Stitt AW. The pathology associated with diabetic retinopathy. Vision Res 2017; 139: 7-14.
[http://dx.doi.org/10.1016/j.visres.2017.04.003] [PMID: 28412095]
[30]
Xu HZ, Le YZ. Significance of outer blood-retina barrier breakdown in diabetes and ischemia. Invest Ophthalmol Vis Sci 2011; 52(5): 2160-4.
[http://dx.doi.org/10.1167/iovs.10-6518] [PMID: 21178141]
[31]
Simó R, Stitt AW, Gardner TW. Neurodegeneration in diabetic retinopathy: Does it really matter? Diabetologia 2018; 61(9): 1902-12.
[http://dx.doi.org/10.1007/s00125-018-4692-1] [PMID: 30030554]
[32]
Chen M, Curtis TM, Stitt AW. Advanced glycation end products and diabetic retinopathy. Curr Med Chem 2013; 20(26): 3234-40.
[http://dx.doi.org/10.2174/09298673113209990025] [PMID: 23745547]
[33]
Forrester JV, Xu H. Good news–bad news: the yin and yang of immune privilege in the eye. Front Immunol 2012; 3: 338.
[http://dx.doi.org/10.3389/fimmu.2012.00338] [PMID: 23230433]
[34]
Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet 2010; 376(9735): 124-36.
[http://dx.doi.org/10.1016/S0140-6736(09)62124-3] [PMID: 20580421]
[35]
Anderson DH, Radeke MJ, Gallo NB, et al. The pivotal role of the complement system in aging and age-related macular degeneration: Hypothesis re-visited. Prog Retin Eye Res 2010; 29(2): 95-112.
[http://dx.doi.org/10.1016/j.preteyeres.2009.11.003] [PMID: 19961953]
[36]
Muramatsu D, Wakabayashi Y, Usui Y, Okunuki Y, Kezuka T, Goto H. Correlation of complement fragment C5a with inflammatory cytokines in the vitreous of patients with proliferative diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 2013; 251(1): 15-7.
[http://dx.doi.org/10.1007/s00417-012-2024-6] [PMID: 22527328]
[37]
Cheng L, Bu H, Portillo JAC, et al. Modulation of retinal Müller cells by complement receptor C5aR. Invest Ophthalmol Vis Sci 2013; 54(13): 8191-8.
[http://dx.doi.org/10.1167/iovs.13-12428] [PMID: 24265019]
[38]
Kowluru RA, Chakrabarti S, Chen S. Re-institution of good metabolic control in diabetic rats and activation of caspase-3 and nuclear transcriptional factor (NF-kB) in the retina. Acta Diabetol 2004; 41(4): 194-9.
[http://dx.doi.org/10.1007/s00592-004-0165-8] [PMID: 15660203]
[39]
Chen M, Wang W, Ma J, Ye P, Wang K. High glucose induces mitochondrial dysfunction and apoptosis in human retinal pigment epithelium cells via promoting SOCS1 and Fas/FasL signaling. Cytokine 2016; 78: 94-102.
[http://dx.doi.org/10.1016/j.cyto.2015.09.014] [PMID: 26700587]
[40]
Joussen AM, Murata T, Tsujikawa A, Kirchhof B, Bursell SE, Adamis AP. Leukocyte-mediated endothelial cell injury and death in the diabetic retina. Am J Pathol 2001; 158(1): 147-52.
[http://dx.doi.org/10.1016/S0002-9440(10)63952-1] [PMID: 11141487]
[41]
Yuuki T, Kanda T, Kimura Y, et al. Inflammatory cytokines in vitreous fluid and serum of patients with diabetic vitreoretinopathy. J Diabetes Complications 2001; 15(5): 257-9.
[http://dx.doi.org/10.1016/S1056-8727(01)00155-6] [PMID: 11522500]
[42]
Yoshimura T, Sonoda KH, Sugahara M, et al. Comprehensive analysis of inflammatory immune mediators in vitreoretinal diseases. PLoS One 2009; 4(12): e8158.
[http://dx.doi.org/10.1371/journal.pone.0008158] [PMID: 19997642]
[43]
Chen H, Zhang X, Liao N, Wen F. Assessment of biomarkers using multiplex assays in aqueous humor of patients with diabetic retinopathy. BMC Ophthalmol 2017; 17(1): 176.
[http://dx.doi.org/10.1186/s12886-017-0572-6] [PMID: 28969616]
[44]
Harada C, Harada T, Mitamura Y, et al. Diverse NF-kappaB expression in epiretinal membranes after human diabetic retinopathy and proliferative vitreoretinopathy. Mol Vis 2004; 10: 31-6.
[PMID: 14737065]
[45]
Sui A, Chen X, Shen J, et al. Inhibiting the NLRP3 inflammasome with MCC950 ameliorates retinal neovascularization and leakage by reversing the IL-1β/IL-18 activation pattern in an oxygen-induced ischemic retinopathy mouse model. Cell Death Dis 2020; 11(10): 901.
[http://dx.doi.org/10.1038/s41419-020-03076-7] [PMID: 33093455]
[46]
Liu Q, Zhang F, Zhang X, et al. Fenofibrate ameliorates diabetic retinopathy by modulating Nrf2 signaling and NLRP3 inflammasome activation. Mol Cell Biochem 2018; 445(1-2): 105-15.
[http://dx.doi.org/10.1007/s11010-017-3256-x] [PMID: 29264825]
[47]
Yin Y, Chen F, Wang W, Wang H, Zhang X. Resolvin D1 inhibits inflammatory response in STZ-induced diabetic retinopathy rats: Possible involvement of NLRP3 inflammasome and NF-κB signaling pathway. Mol Vis 2017; 23: 242-50.
[PMID: 28465656]
[48]
Chen W, Zhao M, Zhao S, et al. Activation of the TXNIP/NLRP3 inflammasome pathway contributes to inflammation in diabetic retinopathy: A novel inhibitory effect of minocycline. Inflamm Res 2017; 66(2): 157-66.
[http://dx.doi.org/10.1007/s00011-016-1002-6] [PMID: 27785530]
[49]
Loukovaara S, Piippo N, Kinnunen K, Hytti M, Kaarniranta K, Kauppinen A. NLRP3 inflammasome activation is associated with proliferative diabetic retinopathy. Acta Ophthalmol 2017; 95(8): 803-8.
[http://dx.doi.org/10.1111/aos.13427] [PMID: 28271611]
[50]
Chen H, Zhang X, Liao N, et al. Enhanced expression of NLRP3 inflammasome-related inflammation in diabetic retinopathy. Invest Ophthalmol Vis Sci 2018; 59(2): 978-85.
[http://dx.doi.org/10.1167/iovs.17-22816] [PMID: 29450537]
[51]
Gross JL, de Azevedo MJ, Silveiro SP, Canani LH, Caramori ML, Zelmanovitz T. Diabetic nephropathy: Diagnosis, prevention, and treatment. Diabetes Care 2005; 28(1): 164-76.
[http://dx.doi.org/10.2337/diacare.28.1.164] [PMID: 15616252]
[52]
Duran-Salgado MB, Rubio-Guerra AF. Diabetic nephropathy and inflammation. World J Diabetes 2014; 5(3): 393-8.
[http://dx.doi.org/10.4239/wjd.v5.i3.393] [PMID: 24936261]
[53]
Chen HY, Zhong X, Huang XR, et al. MicroRNA-29b inhibits diabetic nephropathy in db/db mice. Mol Ther 2014; 22(4): 842-53.
[http://dx.doi.org/10.1038/mt.2013.235] [PMID: 24445937]
[54]
Chien HY, Chen CY, Chiu YH, Lin YC, Li WC. Differential microRNA profiles predict diabetic nephropathy progression in Taiwan. Int J Med Sci 2016; 13(6): 457-65.
[http://dx.doi.org/10.7150/ijms.15548] [PMID: 27279796]
[55]
Huang Y, Liu Y, Li L, et al. Involvement of inflammation-related miR-155 and miR-146a in diabetic nephropathy: Implications for glomerular endothelial injury. BMC Nephrol 2014; 15(1): 142.
[http://dx.doi.org/10.1186/1471-2369-15-142] [PMID: 25182190]
[56]
Sanchez-Alamo B, Shabaka A, Cachofeiro V, Cases-Corona C, Fernandez-Juarez G. Serum interleukin-6 levels predict kidney disease progression in diabetic nephropathy. Clin Nephrol 2022; 97(1): 1-9.
[http://dx.doi.org/10.5414/CN110223] [PMID: 34753557]
[57]
Fujihara CK, Antunes GR, Mattar AL, Malheiros DMAC, Vieira JM Jr, Zatz R. Chronic inhibition of nuclear factor-κB attenuates renal injury in the 5/6 renal ablation model. Am J Physiol Renal Physiol 2007; 292(1): F92-9.
[http://dx.doi.org/10.1152/ajprenal.00184.2006] [PMID: 16896182]
[58]
Foresto-Neto O, Albino AH, Arias SCA, et al. NF-κB system is chronically activated and promotes glomerular injury in experimental type 1 diabetic kidney disease. Front Physiol 2020; 11: 84.
[http://dx.doi.org/10.3389/fphys.2020.00084] [PMID: 32116790]
[59]
Wei M, Li Z, Xiao L, Yang Z. Effects of ROS-relative NF-κB signaling on high glucose-induced TLR4 and MCP-1 expression in podocyte injury. Mol Immunol 2015; 68(2) (2 Pt A): 261-71.
[http://dx.doi.org/10.1016/j.molimm.2015.09.002] [PMID: 26364141]
[60]
Verzola D, Cappuccino L, D’Amato E, et al. Enhanced glomerular Toll-like receptor 4 expression and signaling in patients with type 2 diabetic nephropathy and microalbuminuria. Kidney Int 2014; 86(6): 1229-43.
[http://dx.doi.org/10.1038/ki.2014.116] [PMID: 24786705]
[61]
McCormick BB, Sydor A, Akbari A, Fergusson D, Doucette S, Knoll G. The effect of pentoxifylline on proteinuria in diabetic kidney disease: A meta-analysis. Am J Kidney Dis 2008; 52(3): 454-63.
[http://dx.doi.org/10.1053/j.ajkd.2008.01.025] [PMID: 18433957]
[62]
Tuttle KR, Brosius FC III, Adler SG, et al. JAK1/JAK2 inhibition by baricitinib in diabetic kidney disease: Results from a Phase 2 randomized controlled clinical trial. Nephrol Dial Transplant 2018; 33(11): 1950-9.
[http://dx.doi.org/10.1093/ndt/gfx377] [PMID: 29481660]
[63]
Moon JY, Jeong KH, Lee TW, Ihm CG, Lim SJ, Lee SH. Aberrant recruitment and activation of T cells in diabetic nephropathy. Am J Nephrol 2012; 35(2): 164-74.
[http://dx.doi.org/10.1159/000334928] [PMID: 22286547]
[64]
Moriwaki Y, Yamamoto T, Shibutani Y, et al. Elevated levels of interleukin-18 and tumor necrosis factor-α in serum of patients with type 2 diabetes mellitus: Relationship with diabetic nephropathy. Metabolism 2003; 52(5): 605-8.
[http://dx.doi.org/10.1053/meta.2003.50096] [PMID: 12759891]
[65]
Wu J, Raman A, Coffey NJ, et al. The key role of NLRP3 and STING in APOL1-associated podocytopathy. J Clin Invest 2021; 131(20): e136329.
[http://dx.doi.org/10.1172/JCI136329] [PMID: 34651582]
[66]
Xu X, Huang X, Zhang L, Huang X, Qin Z, Hua F. Adiponectin protects obesity-related glomerulopathy by inhibiting ROS/NF-κB/NLRP3 inflammation pathway. BMC Nephrol 2021; 22(1): 218.
[http://dx.doi.org/10.1186/s12882-021-02391-1] [PMID: 34107901]
[67]
Chen K, Feng L, Hu W, et al. Optineurin inhibits NLRP3 inflammasome activation by enhancing mitophagy of renal tubular cells in diabetic nephropathy. FASEB J 2019; 33(3): 4571-85.
[http://dx.doi.org/10.1096/fj.201801749RRR] [PMID: 30571313]
[68]
Ying C, Zhou Z, Dai J, et al. Activation of the NLRP3 inflammasome by RAC1 mediates a new mechanism in diabetic nephropathy. Inflamm Res 2022; 71(2): 191-204.
[http://dx.doi.org/10.1007/s00011-021-01532-4] [PMID: 35028708]
[69]
Lu M, Yin N, Liu W, Cui X, Chen S, Wang E. Curcumin ameliorates diabetic nephropathy by suppressing NLRP3 inflammasome signaling. BioMed Res Int 2017; 2017: 1-10.
[http://dx.doi.org/10.1155/2017/1516985] [PMID: 28194406]
[70]
Dong W, Jia C, Li J, et al. Fisetin attenuates diabetic nephropathy-induced podocyte injury by inhibiting NLRP3 inflammasome. Front Pharmacol 2022; 13: 783706.
[http://dx.doi.org/10.3389/fphar.2022.783706] [PMID: 35126159]
[71]
Said G. Diabetic neuropathy—a review. Nat Clin Pract Neurol 2007; 3(6): 331-40.
[http://dx.doi.org/10.1038/ncpneuro0504] [PMID: 17549059]
[72]
Russell JW, Zilliox LA. Diabetic neuropathies. Continuum 2014; 20(5): 1226-40.
[http://dx.doi.org/10.1212/01.CON.0000455884.29545.d2]
[73]
Lipnick JA, Lee TH. Diabetic neuropathy. Am Fam Physician 1996; 54(8): 2478-2484, 2487-2488.
[PMID: 8961847]
[74]
Feldman EL, Callaghan BC, Pop-Busui R, et al. Diabetic neuropathy. Nat Rev Dis Primers 2019; 5(1): 41.
[http://dx.doi.org/10.1038/s41572-019-0092-1] [PMID: 31197153]
[75]
Albers JW, Pop-Busui R. Diabetic neuropathy: Mechanisms, emerging treatments, and subtypes. Curr Neurol Neurosci Rep 2014; 14(8): 473.
[http://dx.doi.org/10.1007/s11910-014-0473-5] [PMID: 24954624]
[76]
Zhou J, Zhou S. Inflammation: Therapeutic targets for diabetic neuropathy. Mol Neurobiol 2014; 49(1): 536-46.
[http://dx.doi.org/10.1007/s12035-013-8537-0] [PMID: 23990376]
[77]
Edwards JL, Vincent AM, Cheng HT, Feldman EL. Diabetic neuropathy: Mechanisms to management. Pharmacol Ther 2008; 120(1): 1-34.
[http://dx.doi.org/10.1016/j.pharmthera.2008.05.005] [PMID: 18616962]
[78]
Qiang X, Satoh J, Sagara M, et al. Gliclazide inhibits diabetic neuropathy irrespective of blood glucose levels in streptozotocin-induced diabetic rats. Metabolism 1998; 47(8): 977-81.
[http://dx.doi.org/10.1016/S0026-0495(98)90354-7] [PMID: 9711995]
[79]
Santos DFS, Donahue RR, Laird DE, Oliveira MCG, Taylor BK. The PPARγ agonist pioglitazone produces a female-predominant inhibition of hyperalgesia associated with surgical incision, peripheral nerve injury, and painful diabetic neuropathy. Neuropharmacology 2022; 205: 108907.
[http://dx.doi.org/10.1016/j.neuropharm.2021.108907] [PMID: 34856203]
[80]
Shi X, Chen Y, Nadeem L, Xu G. Beneficial effect of TNF-α inhibition on diabetic peripheral neuropathy. J Neuroinflammation 2013; 10(1): 836.
[http://dx.doi.org/10.1186/1742-2094-10-69] [PMID: 23735240]
[81]
Chanda D, Ray S, Chakraborti D, Sen S, Mitra A. Interleukin-6 levels in patients with diabetic polyneuropathy. Cureus 2022; 14(2): e21952.
[http://dx.doi.org/10.7759/cureus.21952] [PMID: 35155045]
[82]
Doupis J, Lyons TE, Wu S, Gnardellis C, Dinh T, Veves A. Microvascular reactivity and inflammatory cytokines in painful and painless peripheral diabetic neuropathy. J Clin Endocrinol Metab 2009; 94(6): 2157-63.
[http://dx.doi.org/10.1210/jc.2008-2385] [PMID: 19276232]
[83]
Magrinelli F, Briani C, Romano M, Ruggero S, Toffanin E, Triolo G, et al. The association between serum cytokines and damage to large and small nerve fibers in diabetic peripheral neuropathy. J Diabetes Res 2015; 2015: 547834.
[http://dx.doi.org/10.1155/2015/547834]
[84]
Zheng H, Sun W, Zhang Q, et al. Proinflammatory cytokines predict the incidence of diabetic peripheral neuropathy over 5 years in Chinese type 2 diabetes patients: A prospective cohort study. EClinic Med 2021; 31: 100649.
[http://dx.doi.org/10.1016/j.eclinm.2020.100649] [PMID: 33385123]
[85]
Herder C, Kannenberg JM, Huth C, et al. Myeloperoxidase, superoxide dismutase-3, cardiometabolic risk factors, and distal sensorimotor polyneuropathy: The KORA F4/FF4 study. Diabetes Metab Res Rev 2018; 34(5): e3000.
[http://dx.doi.org/10.1002/dmrr.3000] [PMID: 29577557]
[86]
Jia M, Wu C, Gao F, et al. Activation of NLRP3 inflammasome in peripheral nerve contributes to paclitaxel-induced neuropathic pain. Mol Pain 2017; 13.
[http://dx.doi.org/10.1177/1744806917719804] [PMID: 28714351]
[87]
Kang L, Yayi H, Fang Z, Bo Z, Zhongyuan X. Dexmedetomidine attenuates P2X4 and NLRP3 expression in the spine of rats with diabetic neuropathic pain. Acta Cir Bras 2019; 34(11): e201901105.
[http://dx.doi.org/10.1590/s0102-865020190110000005] [PMID: 31859818]
[88]
Sun Q, Wang C, Yan B, et al. Jinmaitong ameliorates diabetic peripheral neuropathy through suppressing TXNIP/NLRP3 inflammasome activation in the streptozotocin-induced diabetic rat model. Diabetes Metab Syndr Obes 2019; 12: 2145-55.
[http://dx.doi.org/10.2147/DMSO.S223842] [PMID: 31802922]
[89]
Zheng T, Wang Q, Bian F, et al. Salidroside alleviates diabetic neuropathic pain through regulation of the AMPK-NLRP3 inflammasome axis. Toxicol Appl Pharmacol 2021; 416: 115468.
[http://dx.doi.org/10.1016/j.taap.2021.115468] [PMID: 33639149]
[90]
Li DX, Wang CN, Wang Y, et al. NLRP3 inflammasome-dependent pyroptosis and apoptosis in hippocampus neurons mediates depressive-like behavior in diabetic mice. Behav Brain Res 2020; 391: 112684.
[http://dx.doi.org/10.1016/j.bbr.2020.112684] [PMID: 32454054]
[91]
Cheng YC, Chu LW, Chen JY, et al. Loganin attenuates high glucose-induced schwann cells pyroptosis by inhibiting ROS generation and NLRP3 inflammasome activation. Cells 2020; 9(9): 1948.
[http://dx.doi.org/10.3390/cells9091948] [PMID: 32842536]
[92]
Patel S, Srivastava S, Singh MR, Singh D. Mechanistic insight into diabetic wounds: Pathogenesis, molecular targets and treatment strategies to pace wound healing. Biomed Pharmacother 2019; 112: 108615.
[http://dx.doi.org/10.1016/j.biopha.2019.108615] [PMID: 30784919]
[93]
Bevan D, Gherardi E, Fan TP, Edwards D, Warn R. Diverse and potent activities of HGF/SF in skin wound repair. J Pathol 2004; 203(3): 831-8.
[http://dx.doi.org/10.1002/path.1578] [PMID: 15221943]
[94]
Barrientos S, Brem H, Stojadinovic O, Tomic-Canic M. Clinical application of growth factors and cytokines in wound healing. Wound Repair Regen 2014; 22(5): 569-78.
[http://dx.doi.org/10.1111/wrr.12205] [PMID: 24942811]
[95]
Kaur P, Choudhury D. Insulin promotes wound healing by inactivating NFkβP50/P65 and activating protein and lipid biosynthesis and alternating Pro/Anti-inflammatory cytokines dynamics. Biomol Concepts 2019; 10(1): 11-24.
[http://dx.doi.org/10.1515/bmc-2019-0002] [PMID: 30827953]
[96]
Fei J, Ling YM, Zeng MJ, Zhang KW. Shixiang plaster, a traditional chinese medicine, promotes healing in a rat model of diabetic ulcer through the receptor for advanced glycation end products (RAGE)/Nuclear Factor kappa B (NF-κB) and Vascular Endothelial Growth Factor (VEGF)/Vascular Cell Adhesion Molecule-1 (VCAM-1)/Endothelial Nitric Oxide Synthase (eNOS) signaling pathways. Med Sci Monit 2019; 25: 9446-57.
[http://dx.doi.org/10.12659/MSM.918268] [PMID: 31825949]
[97]
Cam ME, Ertas B, Alenezi H, et al. Accelerated diabetic wound healing by topical application of combination oral antidiabetic agents-loaded nanofibrous scaffolds: An in vitro and in vivo evaluation study. Mater Sci Eng C 2021; 119: 111586.
[http://dx.doi.org/10.1016/j.msec.2020.111586] [PMID: 33321632]
[98]
Yuan YF, Das SK, Li MQ, Vitamin D. Vitamin D ameliorates impaired wound healing in streptozotocin-induced diabetic mice by suppressing endoplasmic reticulum stress. J Diabetes Res 2018; 2018: 1-10.
[http://dx.doi.org/10.1155/2018/1757925] [PMID: 29707582]
[99]
Mabood Khalil MA, Al-Ghamdi SMG, Dawood US, et al. Mammalian target of rapamycin inhibitors and wound healing complications in kidney transplantation: Old myths and new realities. J Transplant 2022; 2022: 1-28.
[http://dx.doi.org/10.1155/2022/6255339] [PMID: 35265364]
[100]
Huang X, Sun J, Chen G, et al. Resveratrol promotes diabetic wound healing via SIRT1-FOXO1-c-Myc signaling pathway-mediated angiogenesis. Front Pharmacol 2019; 10: 421.
[http://dx.doi.org/10.3389/fphar.2019.00421] [PMID: 31068817]
[101]
Wang X, Li W, Lu S, Ma Z. Modulation of the wound healing through noncoding RNA interplay and GSK-3β/NF-κB signaling interaction. Int J Genomics 2021; 2021: 1-11.
[http://dx.doi.org/10.1155/2021/9709290] [PMID: 34485505]
[102]
Mirza RE, Fang MM, Weinheimer-Haus EM, Ennis WJ, Koh TJ. Sustained inflammasome activity in macrophages impairs wound healing in type 2 diabetic humans and mice. Diabetes 2014; 63(3): 1103-14.
[http://dx.doi.org/10.2337/db13-0927] [PMID: 24194505]
[103]
Weinheimer-Haus EM, Mirza RE, Koh TJ. Nod-like receptor protein-3 inflammasome plays an important role during early stages of wound healing. PLoS One 2015; 10(3): e0119106.
[http://dx.doi.org/10.1371/journal.pone.0119106] [PMID: 25793779]
[104]
Dai J, Jiang C, Chen H, Chai Y. Rapamycin attenuates high glucose-induced inflammation through modulation of mTOR/NF-κB pathways in macrophages. Front Pharmacol 2019; 10: 1292.
[http://dx.doi.org/10.3389/fphar.2019.01292] [PMID: 31736762]
[105]
Zhao Y, Wang Q, Yan S, et al. Bletilla striata polysaccharide promotes diabetic wound healing through inhibition of the NLRP3 inflammasome. Front Pharmacol 2021; 12: 659215.
[http://dx.doi.org/10.3389/fphar.2021.659215] [PMID: 33981238]
[106]
Li X, Wang T, Tao Y, Wang X, Li L, Liu J. MF-094, a potent and selective USP30 inhibitor, accelerates diabetic wound healing by inhibiting the NLRP3 inflammasome. Exp Cell Res 2022; 410(2): 112967.
[http://dx.doi.org/10.1016/j.yexcr.2021.112967] [PMID: 34883112]
[107]
Dal Canto E, Ceriello A, Rydén L, et al. Diabetes as a cardiovascular risk factor: An overview of global trends of macro and micro vascular complications. Eur J Prev Cardiol 2019; 26(2_suppl): 25-32.
[http://dx.doi.org/10.1177/2047487319878371] [PMID: 31722562]
[108]
Zhou Y, Little PJ, Downey L, et al. The role of toll-like receptors in atherothrombotic cardiovascular disease. ACS Pharmacol Transl Sci 2020; 3(3): 457-71.
[http://dx.doi.org/10.1021/acsptsci.9b00100] [PMID: 32566912]
[109]
Yehualashet AS. Toll-like receptors as a potential drug target for diabetes Mellitus and diabetes-associated complications. Diabetes Metab Syndr Obes 2020; 13: 4763-77.
[http://dx.doi.org/10.2147/DMSO.S274844] [PMID: 33311992]
[110]
Schilling J, Lai L, Sambandam N, Dey CE, Leone TC, Kelly DP. Toll-like receptor-mediated inflammatory signaling reprograms cardiac energy metabolism by repressing peroxisome proliferator-activated receptor γ coactivator-1 signaling. Circ Heart Fail 2011; 4(4): 474-82.
[http://dx.doi.org/10.1161/CIRCHEARTFAILURE.110.959833] [PMID: 21558447]
[111]
Dong B, Qi D, Yang L, et al. TLR4 regulates cardiac lipid accumulation and diabetic heart disease in the nonobese diabetic mouse model of type 1 diabetes. Am J Physiol Heart Circ Physiol 2012; 303(6): H732-42.
[http://dx.doi.org/10.1152/ajpheart.00948.2011] [PMID: 22842069]
[112]
Jha JC, Ho F, Dan C, Jandeleit-Dahm K. A causal link between oxidative stress and inflammation in cardiovascular and renal complications of diabetes. Clinical Science 2018; 132(16): 1811-36.
[http://dx.doi.org/10.1042/CS20171459]
[113]
Senatus L, López-Díez R, Egaña-Gorroño L, et al. RAGE impairs murine diabetic atherosclerosis regression and implicates IRF7 in macrophage inflammation and cholesterol metabolism. JCI Insight 2020; 5(13): e137289.
[http://dx.doi.org/10.1172/jci.insight.137289] [PMID: 32641587]
[114]
Tiong YL, Ng KY, Koh RY, Ponnudurai G, Chye SM. Melatonin inhibits high glucose-induced ox-LDL/LDL expression and apoptosis in human umbilical endothelial cells. Horm Mol Biol Clin Investig 2020; 41(4): 20200009.
[http://dx.doi.org/10.1515/hmbci-2020-0009] [PMID: 32598308]
[115]
Wamique M, Himanshu D, Ali W. Expression levels and genetic polymorphism of scavenger receptor class B Type 1 as a biomarker of type 2 diabetes mellitus. Sultan Qaboos Univ Med J 2022; 22(1): 117-22.
[http://dx.doi.org/10.18295/squmj.4.2021.042] [PMID: 35299814]
[116]
Ishigaki Y, Katagiri H, Gao J, et al. Impact of plasma oxidized low-density lipoprotein removal on atherosclerosis. Circulation 2008; 118(1): 75-83.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.107.745174] [PMID: 18559699]
[117]
Kremastiotis G, Handa I, Jackson C, George S, Johnson J. Disparate effects of MMP and TIMP modulation on coronary atherosclerosis and associated myocardial fibrosis. Sci Rep 2021; 11(1): 23081.
[http://dx.doi.org/10.1038/s41598-021-02508-4] [PMID: 34848763]
[118]
Dublin S, Glazer NL, Smith NL, et al. Diabetes mellitus, glycemic control, and risk of atrial fibrillation. J Gen Intern Med 2010; 25(8): 853-8.
[http://dx.doi.org/10.1007/s11606-010-1340-y] [PMID: 20405332]
[119]
Fangel MV, Nielsen PB, Kristensen JK, et al. Glycemic status and thromboembolic risk in patients with atrial fibrillation and type 2 diabetes mellitus. Circ Arrhythm Electrophysiol 2019; 12(5): e007030.
[http://dx.doi.org/10.1161/CIRCEP.118.007030] [PMID: 30995869]
[120]
Frati G, Schirone L, Chimenti I, et al. An overview of the inflammatory signalling mechanisms in the myocardium underlying the development of diabetic cardiomyopathy. Cardiovasc Res 2017; 113(4): 378-88.
[http://dx.doi.org/10.1093/cvr/cvx011] [PMID: 28395009]
[121]
Jubaidi FF, Zainalabidin S, Taib IS, Hamid ZA, Budin SB. the potential role of flavonoids in ameliorating diabetic cardiomyopathy via alleviation of cardiac oxidative stress, inflammation and apoptosis. Int J Mol Sci 2021; 22(10): 5094.
[http://dx.doi.org/10.3390/ijms22105094] [PMID: 34065781]
[122]
Ren X, Zuo G, Wu W, et al. Atorvastatin alleviates experimental diabetic cardiomyopathy by regulating the GSK-3β-PP2Ac-NF-κB signaling axis. PLoS One 2016; 11(11): e0166740.
[http://dx.doi.org/10.1371/journal.pone.0166740] [PMID: 27851811]
[123]
González-Moro A, Valencia I, Shamoon L, Sánchez-Ferrer CF, Peiró C, de la Cuesta F. NLRP3 inflammasome in vascular disease: A recurrent villain to combat pharmacologically. Antioxidants 2022; 11(2): 269.
[http://dx.doi.org/10.3390/antiox11020269] [PMID: 35204152]
[124]
Luo B, Li B, Wang W, et al. NLRP3 gene silencing ameliorates diabetic cardiomyopathy in a type 2 diabetes rat model. PLoS One 2014; 9(8): e104771.
[http://dx.doi.org/10.1371/journal.pone.0104771] [PMID: 25136835]
[125]
Monnerat G, Alarcón ML, Vasconcellos LR, et al. Macrophage-dependent IL-1β production induces cardiac arrhythmias in diabetic mice. Nat Commun 2016; 7(1): 13344.
[http://dx.doi.org/10.1038/ncomms13344] [PMID: 27882934]
[126]
Wang X, Pan J, Liu H, et al. AIM2 gene silencing attenuates diabetic cardiomyopathy in type 2 diabetic rat model. Life Sci 2019; 221: 249-58.
[http://dx.doi.org/10.1016/j.lfs.2019.02.035] [PMID: 30790610]
[127]
Pfeiler S, Winkels H, Kelm M, Gerdes N. IL-1 family cytokines in cardiovascular disease. Cytokine 2019; 122: 154215.
[http://dx.doi.org/10.1016/j.cyto.2017.11.009] [PMID: 29198612]
[128]
Esser N, Paquot N, Scheen AJ. Anti-inflammatory agents to treat or prevent type 2 diabetes, metabolic syndrome and cardiovascular disease. Expert Opin Investig Drugs 2015; 24(3): 283-307.
[http://dx.doi.org/10.1517/13543784.2015.974804] [PMID: 25345753]
[129]
Everett BM, Cornel JH, Lainscak M, et al. Anti-inflammatory therapy with canakinumab for the prevention of hospitalization for heart failure. Circulation 2019; 139(10): 1289-99.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.118.038010] [PMID: 30586730]
[130]
Pickup JC. Inflammation and activated innate immunity in the pathogenesis of type 2 diabetes. Diabetes Care 2004; 27(3): 813-23.
[http://dx.doi.org/10.2337/diacare.27.3.813] [PMID: 14988310]
[131]
de Lourdes Ochoa-González F, González-Curiel IE, Cervantes-Villagrana AR, Fernández-Ruiz JC, Castañeda-Delgado JE. Innate immunity alterations in type 2 diabetes mellitus: understanding infection susceptibility. Curr Mol Med 2021; 21(4): 318-31.
[http://dx.doi.org/10.2174/1566524020999200831124534] [PMID: 32867637]
[132]
Wohlford GF, Van Tassell BW, Billingsley HE, et al. Phase 1B, randomized, double-blinded, dose escalation, single-center, repeat dose safety and pharmacodynamics study of the oral nlrp3 inhibitor dapansutrile in subjects with NYHA II–III systolic heart failure. J Cardiovasc Pharmacol 2021; 77(1): 49-60.
[http://dx.doi.org/10.1097/FJC.0000000000000931] [PMID: 33235030]
[133]
Pollack RM, Donath MY, LeRoith D, Leibowitz G. Anti-inflammatory agents in the treatment of diabetes and its vascular complications. Diabetes Care 2016; 39(S2) (Suppl. 2): S244-52.
[http://dx.doi.org/10.2337/dcS15-3015] [PMID: 27440839]
[134]
Deans KA, Sattar N. “Anti-inflammatory” drugs and their effects on type 2 diabetes. Diabetes Technol Ther 2006; 8(1): 18-27.
[http://dx.doi.org/10.1089/dia.2006.8.18] [PMID: 16472047]
[135]
Yaribeygi H, Butler AE, Barreto GE, Sahebkar A. Antioxidative potential of antidiabetic agents: A possible protective mechanism against vascular complications in diabetic patients. J Cell Physiol 2019; 234(3): 2436-46.
[http://dx.doi.org/10.1002/jcp.27278] [PMID: 30191997]
[136]
Bellucci PN, González Bagnes MF, Di Girolamo G, González CD. Potential effects of nonsteroidal anti-inflammatory drugs in the prevention and treatment of type 2 diabetes mellitus. J Pharm Pract 2017; 30(5): 549-56.
[http://dx.doi.org/10.1177/0897190016649551] [PMID: 27194069]
[137]
van Asseldonk EJP, Stienstra R, Koenen TB, Joosten LAB, Netea MG, Tack CJ. Treatment with Anakinra improves disposition index but not insulin sensitivity in nondiabetic subjects with the metabolic syndrome: A randomized, double-blind, placebo-controlled study. J Clin Endocrinol Metab 2011; 96(7): 2119-26.
[http://dx.doi.org/10.1210/jc.2010-2992] [PMID: 21508140]
[138]
van Poppel PCM, van Asseldonk EJP, Holst JJ, Vilsbøll T, Netea MG, Tack CJ. The interleukin-1 receptor antagonist anakinra improves first-phase insulin secretion and insulinogenic index in subjects with impaired glucose tolerance. Diabetes Obes Metab 2014; 16(12): 1269-73.
[http://dx.doi.org/10.1111/dom.12357] [PMID: 25039318]
[139]
Hensen J, Howard CP, Walter V, Thuren T. Impact of interleukin-1β antibody (canakinumab) on glycaemic indicators in patients with type 2 diabetes mellitus: Results of secondary endpoints from a randomized, placebo-controlled trial. Diabetes Metab 2013; 39(6): 524-31.
[http://dx.doi.org/10.1016/j.diabet.2013.07.003] [PMID: 24075453]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy