Lipid hydroperoxide-derived insulin resistance and its inhibition by pyridoxamine in skeletal muscle cells

Toxicological Research - Tập 39 - Trang 147-156 - 2022
Seon Hwa Lee1, Mizuki Tsutsui1, Atsushi Matsunaga1, Tomoyuki Oe1
1Department of Bio-Analytical Chemistry, Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai, Japan

Tóm tắt

Oxidative stress is strongly associated with the onset and/or progression of diabetes. Under conditions of oxidative stress, lipid hydroperoxides are decomposed to reactive aldehydes that have been reported to induce insulin resistance by modifying proteins involved in insulin signaling. Pyridoxamine (PM) can inhibit the formation of advanced glycation/lipoxidation end products by scavenging reactive carbonyl species. Thus, PM has emerged as a promising drug candidate for various chronic conditions, including diabetic complications. In this study, L6 skeletal muscle cells were treated with 4-oxo-2(E)-nonenal (ONE), one of the most abundant and reactive lipid-derived aldehydes. Cellular insulin resistance was assessed by measuring insulin-stimulated glucose uptake using 2-deoxyglucose. ONE induced a time- and dose-dependent decrease in glucose uptake. Liquid chromatography/electrospray ionization-mass spectrometry analysis of the reaction between ONE and insulin receptor substrate 1 (IRS1) lysate identified multiple modifications that could disturb the interaction between IRS1 and activated IR, leading to insulin resistance. Pretreatment of the cells with PM restored the ONE-induced decrease in glucose uptake. Concomitantly, the formation of PM-ONE adducts in cell culture medium was increased in a PM-dose dependent manner. PM can therefore prevent lipid hydroperoxide-derived insulin resistance by quenching ONE.

Tài liệu tham khảo

Galicia-Garcia U, Benito-Vicente A, Jebari S, Larrea-Sebal A, Siddiqi H, Uribe KB, Ostolaza H, Martín C (2020) Pathophysiology of type 2 diabetes mellitus. Int J Mol Sci 21:1–34. https://doi.org/10.3390/ijms21176275 The Expert Committee on the Diagnosis and Classification of Diabetes Mellitus (2003) Report of the expert committee on the description of diabetes categories of glucose. Diabetes 26:s5–s20. https://doi.org/10.2337/diacare.26.2007.S5 Czech MP (2017) Insulin action and resistance in obesity and type 2 diabetes. Nat Med 23:804–814. https://doi.org/10.1038/nm.4350 Bashan N, Kovsan J, Kachko I, Ovadia H, Rudich A (2009) Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species. Physiol Rev 89:27–71. https://doi.org/10.1152/physrev.00014.2008 Ceriello A, Motz E (2004) Is Oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb Vasc Biol 24:816–823. https://doi.org/10.1161/01.ATV.0000122852.22604.78 Demozay D, Mas JC, Rocchi S, Van Obberghen E (2008) FALDH reverses the deleterious action of oxidative stress induced by lipid peroxidation product 4-hydroxynonenal on insulin signaling in 3T3-L1 adipocytes. Diabetes 57:1216–1226. https://doi.org/10.2337/db07-0389 Shearn CT, Fritz KS, Reigan P, Petersen DR (2011) Modification of Akt2 by 4-hydroxynonenal inhibits insulin-dependent Akt signaling in HepG2 cells. Biochemistry 50:3984–3996. https://doi.org/10.1021/bi200029w Aoi W, Naito Y, Tokuda H, Tanimura Y, Oya-Ito T, Yoshikawa T (2012) Exercise-induced muscle damage impairs insulin signaling pathway associated with IRS-1 oxidative modification. Physiol Res 61:81–88. https://doi.org/10.33549/physiolres.932239 Stadtman ER (2001) Protein oxidation in aging and age-related diseases. Ann N Y Acad Sci 928:22–38. https://doi.org/10.1111/j.1749-6632.2001.tb05632.x Finkel T (2011) Signal transduction by reactive oxygen species. J Cell Biol 194:7–15. https://doi.org/10.1083/jcb.201102095 Lee SH, Oe T, Blair IA (2001) Vitamin C-induced decomposition of lipid hydroperoxides to endogenous genotoxins. Science 292:2083–2086. https://doi.org/10.1126/science.1059501 Sayre LM, Lin D, Yuan Q, Zhu X, Tang X (2006) Protein adducts generated from products of lipid oxidation: focus on HNE and ONE. Drug Metab Rev 38:651–675. https://doi.org/10.1080/03602530600959508 Lee SH, Goto T, Oe T (2008) A novel 4-oxo-2(E)-nonenal-derived modification to angiotensin II: oxidative decarboxylation of N-terminal aspartic acid. Chem Res Toxicol 21:2237–2244. https://doi.org/10.1021/tx800316v Oe T, Lee SH, Elipe MVS, Arison BH, Blair IA (2003) A novel lipid hydroperoxide-derived modification to arginine. Chem Res Toxicol 16:1598–1605. https://doi.org/10.1021/tx034178l Zhu X, Sayre LM (2007) Long-lived 4-oxo-2-enal-derived apparent Lysine Michael adducts are actually the isomeric 4-ketoamides. Chem Res Toxicol 20:165–170. https://doi.org/10.1021/tx600295j Sasson S (2017) Nutrient overload, lipid peroxidation and pancreatic beta cell function. Free Radic Biol Med 111:102–109. https://doi.org/10.1016/j.freeradbiomed.2016.09.003 Toyokuni S, Yamada S, Kashima M, Ihara Y, Yamada Y, Tanaka T, Hiai H, Seino Y, Uchida K (2000) Serum 4-hydroxy-2-nonenal-modified albumin is elevated in patients with type 2 diabetes mellitus. Antioxid Redox Signal 2:681–685. https://doi.org/10.1089/ars.2000.2.4-681 Ihara Y, Toyokuni S, Uchida K, Odaka H, Tanaka T, Ikeda H, Hiai H, Seino Y, Yamada Y (1999) Hyperglycemia causes oxidative stress in pancreatic beta-cells of GK rats, a model of type 2 diabetes. Diabetes 48:927–932. https://doi.org/10.2337/diabetes.48.4.927 Lou B, Boger M, Bennewitz K, Sticht C, Kopf S, Morgenstern J, Fleming T, Hell R, Yuan Z, Nawroth PP, Kroll J (2020) Elevated 4-hydroxynonenal induces hyperglycaemia via Aldh3a1 loss in zebrafish and associates with diabetes progression in humans. Redox Biol 37:101723. https://doi.org/10.1016/j.redox.2020.101723 Liu G, Ji W, Huang J, Liu L, Wang Y (2016) 4-HNE expression in diabetic rat kidneys and the protective effects of probucol. J Endocrinol Invest 39:865–873. https://doi.org/10.1007/s40618-015-0428-y Akude E, Zherebitskaya E, Roy Chowdhury SK, Girling K, Fernyhough P (2010) 4-Hydroxy-2-nonenal induces mitochondrial dysfunction and aberrant axonal outgrowth in adult sensory neurons that mimics features of diabetic neuropathy. Neurotox Res 17:28–38. https://doi.org/10.1007/s12640-009-9074-5 Lin D, Lee HG, Liu Q, Perry G, Smith MA, Sayre LM (2005) 4-Oxo-2-nonenal is both more neurotoxic and more protein reactive than 4-hydroxy-2-nonenal. Chem Res Toxicol 18:1219–1231. https://doi.org/10.1021/tx050080q Voziyan PA, Hudson BG (2005) Pyridoxamine as a multifunctional pharmaceutical: Targeting pathogenic glycation and oxidative damage. Cell Mol Life Sci 62:1671–1681. https://doi.org/10.1007/s00018-005-5082-7 Parra M, Stahl S, Hellmann H (2018) Vitamin B6 and its role in cell metabolism and physiology. Cells 7:84. https://doi.org/10.3390/cells7070084 Abdullah KM, Abul Qais F, Hasan H, Naseem I (2019) Anti-diabetic study of vitamin B6 on hyperglycaemia induced protein carbonylation, DNA damage and ROS production in alloxan induced diabetic rats. Toxicol Res (Camb) 8:568–579. https://doi.org/10.1039/c9tx00089e Nagaraj RH, Sarkar P, Mally A, Biemel KM, Lederer MO, Padayatti PS (2002) Effect of pyridoxamine on chemical modification of proteins by carbonyls in diabetic rats: characterization of a major product from the reaction of pyridoxamine and methylglyoxal. Arch Biochem Biophys 402:110–119. https://doi.org/10.1016/S0003-9861(02)00067-X Voziyan PA, Metz TO, Baynes JW, Hudson BG (2002) A post-Amadori inhibitor pyridoxamine also inhibits chemical modification of proteins by scavenging carbonyl intermediates of carbohydrate and lipid degradation. J Biol Chem 277:3397–3403. https://doi.org/10.1074/jbc.M109935200 Kang Z, Li H, Li G, Yin D (2006) Reaction of pyridoxamine with malondialdehyde: mechanism of inhibition of formation of advanced lipoxidation end-products. Amino Acids 30:55–61. https://doi.org/10.1007/s00726-005-0209-6 Amarnath V, Amarnath K, Amarnath K, Davies S, Roberts LJ (2004) Pyridoxamine: an extremely potent scavenger of 1,4-dicarbonyls. Chem Res Toxicol 17:410–415. https://doi.org/10.1021/tx0300535 Davies SS, Brantley EJ, Voziyan PA, Amarnath V, Zagol-Ikapitte I, Boutaud O, Hudson BG, Oates JA, Roberts LJ (2006) Pyridoxamine analogues scavenge lipid-derived γ-ketoaldehydes and protect against H2O2-mediated cytotoxicity. Biochemistry 45:15756–15767. https://doi.org/10.1021/bi061860g Amarnath V, Amarnath K (2015) Scavenging 4-oxo-2-nonenal. Chem Res Toxicol 28:1888–1890. https://doi.org/10.1021/acs.chemrestox.5b00301 Lee SH, Matsunaga A, Oe T (2018) Inhibition effect of pyridoxamine on lipid hydroperoxide-derived modifications to human serum albumin. PLoS ONE 13:1–23. https://doi.org/10.1371/journal.pone.0196050 Copps KD, White MF (2012) Regulation of insulin sensitivity by serine/threonine phosphorylation of insulin receptor substrate proteins IRS1 and IRS2. Diabetologia 55:2565–2582. https://doi.org/10.1007/s00125-012-2644-8 Eck MJ, Dhe-Paganon S, Trüb T, Nolle RT, Shoelson SE (1996) Structure of the IRS-1 PTB domain bound to the juxtamembrane region of the insulin receptor. Cell 85:695–705. https://doi.org/10.1016/S0092-8674(00)81236-2