The Preventive Effect of IL-1beta Antagonist on Diabetic Peripheral Neuropathy

Author(s): Zheng Hangping, Han Ling, Ji Lijin, Zhao Wenting, Liu Xiaoxia, Zhang Qi, Zhu Xiaoming, Li Qingchun, Li Yiming, Xiong Qian, Hu Ji, Lu Bin*, Zhang Shuo*

Journal Name: Endocrine, Metabolic & Immune Disorders - Drug Targets
Formerly Current Drug Targets - Immune, Endocrine & Metabolic Disorders

Volume 20 , Issue 5 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Objective: To investigate the relationship between Interleukin-1beta (IL-1beta) and diabetic peripheral neuropathy (DPN) using animal models.

Methods: The rat model of diabetic neuropathy was induced by intraperitoneal injection of a single dose of streptozotocin (STZ) at 65mg/kg. Diabetic rats were randomly divided into two groups (10 each), one treated with 0.9% saline (DMS group) and the other with interleukin-1 receptor antagonist (IL-1RA) at 50mg/kg (DMI group) twice a day for 5 weeks. Ten normal rats matched for weight, age and sex served as normal controls (Con group) and were treated with saline. Morphologic studies of sciatic nerves were achieved using light and transmission electron microscopy.

Results: Transmission electron microscopy of the sciatic nerve showed the ultrastructure of myelin and the axon in the IL-1RA group was highly protected compared to diabetic controls.

Conclusion: High levels of circulating IL-1beta may be associated with the risk of DPN and anti-IL-1 treatment may provide a potential strategy for the prevention of diabetic neuropathy.

Keywords: Diabetic peripheral neuropathy, IL-1beta, IL-1RA, inflammation, prevention, rats.

[1]
Farmer, K.L.; Li, C.; Dobrowsky, R.T. Diabetic peripheral neuropathy: should a chaperone accompany our therapeutic approach? Pharmacol. Rev., 2012, 64(4), 880-900.
[http://dx.doi.org/10.1124/pr.111.005314] [PMID: 22885705]
[2]
Katulanda, P.; Ranasinghe, P.; Jayawardena, R.; Constantine, G.R.; Sheriff, M.H.; Matthews, D.R. The prevalence, patterns and predictors of diabetic peripheral neuropathy in a developing country. Diabetol. Metab. Syndr., 2012, 4(1), 21.
[http://dx.doi.org/10.1186/1758-5996-4-21] [PMID: 22642973]
[3]
Lu, B.; Hu, J.; Wen, J.; Zhang, Z.; Zhou, L.; Li, Y.; Hu, R. Determination of peripheral neuropathy prevalence and associated factors in Chinese subjects with diabetes and pre-diabetes - ShangHai Diabetic neuRopathy Epidemiology and Molecular Genetics Study (SH-DREAMS). PLoS One, 2013, 8(4) e61053
[http://dx.doi.org/10.1371/journal.pone.0061053] [PMID: 23613782]
[4]
Tesfaye, S.; Selvarajah, D. Advances in the epidemiology, pathogenesis and management of diabetic peripheral neuropathy. Diabetes Metab. Res. Rev., 2012, 28(S1)(Suppl. 1), 8-14.
[http://dx.doi.org/10.1002/dmrr.2239] [PMID: 22271716]
[5]
Tesfaye, S.; Boulton, A.J.M.; Dyck, P.J.; Freeman, R.; Horowitz, M.; Kempler, P.; Lauria, G.; Malik, R.A.; Spallone, V.; Vinik, A.; Bernardi, L.; Valensi, P. Toronto diabetic neuropathy expert group.Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care, 2010, 33(10), 2285-2293.
[http://dx.doi.org/10.2337/dc10-1303] [PMID: 20876709]
[6]
Albers, J.W.; Herman, W.H.; Pop-Busui, R.; Feldman, E.L.; Martin, C.L.; Cleary, P.A.; Waberski, B.H.; Lachin, J.M. Diabetes Control and Complications Trial /Epidemiology of Diabetes Interventions and Complications Research Group.Effect of prior intensive insulin treatment during the Diabetes Control and Complications Trial (DCCT) on peripheral neuropathy in type 1 diabetes during the Epidemiology of Diabetes Interventions and Complications (EDIC) Study. Diabetes Care, 2010, 33(5), 1090-1096.
[http://dx.doi.org/10.2337/dc09-1941] [PMID: 20150297]
[7]
Pop-Busui, R.; Ang, L.; Holmes, C.; Gallagher, K.; Feldman, E.L. Inflammation as a therapeutic target for diabetic neuropathies. Curr. Diab. Rep., 2016, 16(3), 29.
[http://dx.doi.org/10.1007/s11892-016-0727-5] [PMID: 26897744]
[8]
Agrawal, N.K.; Kant, S. Targeting inflammation in diabetes: Newer therapeutic options. World J. Diabetes, 2014, 5(5), 697-710.
[http://dx.doi.org/10.4239/wjd.v5.i5.697] [PMID: 25317247]
[9]
Al-Rejaie, S.S.; Abuohashish, H.M.; Ahmed, M.M.; Arrejaie, A.S.; Aleisa, A.M.; AlSharari, S.D. Telmisartan inhibits hyperalgesia and inflammatory progression in a diabetic neuropathic pain model of Wistar rats. Neurosciences (Riyadh), 2015, 20(2), 115-123.
[http://dx.doi.org/10.17712/nsj.2015.2.20140511] [PMID: 25864063]
[10]
Ismail, C.A.N.; Aziz, C.B.A.; Suppian, R.; Long, I. Imbalanced oxidative stress and pro-inflammatory markers differentiate the development of diabetic neuropathy variants in streptozotocin-induced diabetic rats. J. Diabetes Metab. Disord., 2018, 17(2), 129-136.
[http://dx.doi.org/10.1007/s40200-018-0350-x] [PMID: 30918846]
[11]
Miranda, H.F.; Poblete, P.; Sierralta, F.; Noriega, V.; Prieto, J.C.; Zepeda, R.J. Interleukin-1beta in synergism gabapentin with tramadol in murine model of diabetic neuropathy. Inflammopharmacology, 2019, 27(1), 151-155.
[http://dx.doi.org/10.1007/s10787-018-0532-7] [PMID: 30317449]
[12]
Evangelista, A.F.; Vannier-Santos, M.A.; de Assis Silva, G.S.; Silva, D.N.; Juiz, P.J.L.; Nonaka, C.K.V.; Dos Santos, R.R.; Soares, M.B.P.; Villarreal, C.F. Bone marrow-derived mesenchymal stem/stromal cells reverse the sensorial diabetic neuropathy via modulation of spinal neuroinflammatory cascades. J. Neuroinflammation, 2018, 15(1), 189.
[http://dx.doi.org/10.1186/s12974-018-1224-3] [PMID: 29933760]
[13]
Ehses, J.A.; Lacraz, G.; Giroix, M-H.; Schmidlin, F.; Coulaud, J.; Kassis, N.; Irminger, J.C.; Kergoat, M.; Portha, B.; Homo-Delarche, F.; Donath, M.Y. IL-1 antagonism reduces hyperglycemia and tissue inflammation in the type 2 diabetic GK rat. Proc. Natl. Acad. Sci. USA, 2009, 106(33), 13998-14003.
[http://dx.doi.org/10.1073/pnas.0810087106] [PMID: 19666548]
[14]
Weis, J.; Dimpfel, W.; Schröder, J.M. Nerve conduction changes and fine structural alterations of extra- and intrafusal muscle and nerve fibers in streptozotocin diabetic rats. Muscle Nerve, 1995, 18(2), 175-184.
[http://dx.doi.org/10.1002/mus.880180205] [PMID: 7823975]
[15]
Nursal, A.F.; Inanir, A.; Rustemoglu, A.; Uzun, S.; Sahin, K.; Yigit, S. IL-1β and IL-1Ra variant profiles in turkish patients with diabetic peripheral neuropathy. Endocr. Metab. Immune Disord. Drug Targets, 2019, 19(2), 150-158.
[http://dx.doi.org/10.2174/1871530318666181022165048] [PMID: 30360750]
[16]
Dinarello, C.A. Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol., 2009, 27, 519-550.
[http://dx.doi.org/10.1146/annurev.immunol.021908.132612] [PMID: 19302047]
[17]
Jager, J.; Grémeaux, T.; Cormont, M.; Le Marchand-Brustel, Y.; Tanti, J.F. Interleukin-1β-induced insulin resistance in adipocytes through down-regulation of insulin receptor substrate-1 expression. Endocrinology, 2007, 148(1), 241-251.
[http://dx.doi.org/10.1210/en.2006-0692] [PMID: 17038556]
[18]
Nov, O.; Kohl, A.; Lewis, E.C.; Bashan, N.; Dvir, I.; Ben-Shlomo, S.; Fishman, S.; Wueest, S.; Konrad, D.; Rudich, A. Interleukin-1β may mediate insulin resistance in liver-derived cells in response to adipocyte inflammation. Endocrinology, 2010, 151(9), 4247-4256.
[http://dx.doi.org/10.1210/en.2010-0340] [PMID: 20660063]
[19]
Liou, J.T.; Liu, F.C.; Mao, C.C.; Lai, Y.S.; Day, Y.J. Inflammation confers dual effects on nociceptive processing in chronic neuropathic pain model. Anesthesiology, 2011, 114(3), 660-672.
[http://dx.doi.org/10.1097/ALN.0b013e31820b8b1e] [PMID: 21307767]
[20]
Liu, S.; Liu, X.; Xiong, H.; Wang, W.; Liu, Y.; Yin, L.; Tu, C.; Wang, H.; Xiang, X.; Xu, J.; Duan, B.; Tao, A.; Zhao, Z.; Mei, Z. CXCL13/CXCR5 signaling contributes to diabetes-induced tactile allodynia via activating pERK, pSTAT3, pAKT pathways and pro-inflammatory cytokines production in the spinal cord of male mice. Brain Behav. Immun., 2019, 80, 711-724.
[http://dx.doi.org/10.1016/j.bbi.2019.05.020] [PMID: 31100371]
[21]
Zelenka, M.; Schäfers, M.; Sommer, C. Intraneural injection of interleukin-1β and tumor necrosis factor-alpha into rat sciatic nerve at physiological doses induces signs of neuropathic pain. Pain, 2005, 116(3), 257-263.
[http://dx.doi.org/10.1016/j.pain.2005.04.018] [PMID: 15964142]
[22]
Wolf, G.; Gabay, E.; Tal, M.; Yirmiya, R.; Shavit, Y. Genetic impairment of interleukin-1 signaling attenuates neuropathic pain, autotomy, and spontaneous ectopic neuronal activity, following nerve injury in mice. Pain, 2006, 120(3), 315-324.
[http://dx.doi.org/10.1016/j.pain.2005.11.011] [PMID: 16426759]
[23]
Schuh, C.D.; Pierre, S.; Weigert, A.; Weichand, B.; Altenrath, K.; Schreiber, Y.; Ferreiros, N.; Zhang, D.D.; Suo, J.; Treutlein, E.M.; Henke, M.; Kunkel, H.; Grez, M.; Nüsing, R.; Brüne, B.; Geisslinger, G.; Scholich, K. Prostacyclin mediates neuropathic pain through interleukin 1β-expressing resident macrophages. Pain, 2014, 155(3), 545-555.
[http://dx.doi.org/10.1016/j.pain.2013.12.006] [PMID: 24333781]
[24]
Herder, C.; Kannenberg, J.M.; Huth, C.; Carstensen-Kirberg, M.; Rathmann, W.; Koenig, W.; Heier, M.; Püttgen, S.; Thorand, B.; Peters, A.; Roden, M.; Meisinger, C.; Ziegler, D. Proinflammatory Cytokines Predict the Incidence and Progression of Distal Sensorimotor Polyneuropathy: KORA F4/FF4 Study. Diabetes Care, 2017, 40(4), 569-576.
[http://dx.doi.org/10.2337/dc16-2259] [PMID: 28174259]
[25]
Mattingly, G.E.; Fischer, V.W. Peripheral nerve axonal dwindling with concomitant myelin sheath hypertrophy in experimentally induced diabetes. Acta Neuropathol., 1985, 68(2), 149-154.
[http://dx.doi.org/10.1007/BF00688637] [PMID: 2933920]
[26]
Zhong, JM.; Lu, YC.; Zhang, J. Dexmedetomidine reduces diabetic neuropathy pain in rats through the Wnt 10a/β-catenin signaling pathway. Biomed Res. Int., 2018, Nov 27 2018 9043628
[27]
Lu, Y.; Lin, B.; Zhong, J. The therapeutic effect of dexmedetomidine on rat diabetic neuropathy pain and the mechanism. Biol. Pharm. Bull., 2017, 40(9), 1432-1438.
[http://dx.doi.org/10.1248/bpb.b17-00224] [PMID: 28626198]
[28]
Hajhashemi, V.; Minaiyan, M.; Banafshe, H.R.; Mesdaghinia, A.; Abed, A. The anti-inflammatory effects of venlafaxine in the rat model of carrageenan-induced paw edema. Iran. J. Basic Med. Sci., 2015, 18(7), 654-658.
[PMID: 26351555]
[29]
Ridker, P.M.; Thuren, T.; Zalewski, A.; Libby, P. Interleukin-1β inhibition and the prevention of recurrent cardiovascular events: rationale and design of the Canakinumab Anti-inflammatory Thrombosis Outcomes Study (CANTOS). Am. Heart J., 2011, 162(4), 597-605.
[http://dx.doi.org/10.1016/j.ahj.2011.06.012] [PMID: 21982649]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 20
ISSUE: 5
Year: 2020
Published on: 01 June, 2020
Page: [753 - 759]
Pages: 7
DOI: 10.2174/1871530319666191022114139
Price: $65

Article Metrics

PDF: 22
HTML: 1