1,053
Views
59
CrossRef citations to date
0
Altmetric
ORIGINAL ARTICLE

The novel NADPH oxidase 4 inhibitor GLX351322 counteracts glucose intolerance in high-fat diet-treated C57BL/6 mice

, , &
Pages 1308-1318 | Received 03 Mar 2015, Accepted 26 Jun 2015, Published online: 30 Jul 2015

References

  • Weir GC, Bonner-Weir S. Islet β cell mass in diabetes and how it relates to function, birth, and death. Ann N Y Acad Sci 2013;1281:92–105.
  • Meneghini LF. Intensifying insulin therapy: what options are available to patients with type 2 diabetes? Am J Med 2013;126:S28–37.
  • Robertson RP. Oxidative stress and impaired insulin secretion in type 2 diabetes. Curr Opin Pharmacol 2006;6:615–619.
  • Newsholme P, Haber EP, Hirabara SM, Rebelato EL, Procopio J, Morgan D, et al. Diabetes associated cell stress and dysfunction: role of mitochondrial and non-mitochondrial ROS production and activity. J Physiol 2007;583:9–24.
  • Sakai K, Matsumoto K, Nishikawa T, Suefuji M, Nakamaru K, Hirashima Y, et al. Mitochondrial reactive oxygen species reduce insulin secretion by pancreatic beta-cells. Biochem Biophys Res Commun 2003;300:216–222.
  • Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction? Diabetes 2003;52:1–8.
  • Wei Y, Sowers JR, Nistala R, Gong H, Uptergrove GM, Clark SE, et al. Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J Biol Chem 2006;281:35137–35146.
  • Wu X, Williams KJ. NOX4 pathway as a source of selective insulin resistance and responsiveness. Arterioscler Thromb Vasc Biol 2012;32:1236–1245.
  • Styskal J, Van Remmen H, Richardson A, Salmon AB. Oxidative stress and diabetes: what can we learn about insulin resistance from antioxidant mutant mouse models? Free Radic Biol Med 2012;52:46–58.
  • Sedeek M, Callera G, Montezano A, Gutsol A, Heitz F, Szyndralewiez C, et al. Critical role of NOX4-based NADPH oxidase in glucose-induced oxidative stress in the kidney: implications in type 2 diabetic nephropathy. Am J Physiol Renal Physiol 2010;299:F1348–1358.
  • Matsuzawa-Nagata N, Takamura T, Ando H, Nakamura S, Kurita S, Misu H, et al. Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism 2008;57:1071–1077.
  • Guichard C, Moreau R, Pessayre D, Epperson TK, Krause KH. NOX family NADPH oxidases in liver and in pancreatic islets: a role in the metabolic syndrome and diabetes? Biochem Soc Trans 2008;36:920–929.
  • Oliveira HR, Verlengia R, Carvalho CR, Britto LR, Curi R, Carpinelli AR. Pancreatic beta-cells express phagocyte-like NAD(P)H oxidase. Diabetes 2003;52:1457–1463.
  • Uchizono Y, Takeya R, Iwase M, Sasaki N, Oku M, Imoto H, et al. Expression of isoforms of NADPH oxidase components in rat pancreatic islets. Life Sci 2006;80:133–139.
  • Rebelato E, Mares-Guia TR, Graciano MF, Labriola L, Britto LR, Garay-Malpartida HM, et al. Expression of NADPH oxidase in human pancreatic islets. Life Sci 2012;91:244–249.
  • Morgan D, Rebelato E, Abdulkader F, Graciano MF, Oliveira-Emilio HR, Hirata AE, et al. Association of NAD(P)H oxidase with glucose-induced insulin secretion by pancreatic beta-cells. Endocrinology 2009;150:2197–2201.
  • Imoto H, Sasaki N, Iwase M, Nakamura U, Oku M, Sonoki K, et al. Impaired insulin secretion by diphenyleneiodium associated with perturbation of cytosolic Ca2 + dynamics in pancreatic beta-cells. Endocrinology 2008;149:5391–5400.
  • Syed I, Kyathanahalli CN, Kowluru A. Phagocyte-like NADPH oxidase generates ROS in INS 832/13 cells and rat islets: role of protein prenylation. Am J Physiol Regul Integr Comp Physiol 2011;300:R756–762.
  • Syed I, Kyathanahalli CN, Jayaram B, Govind S, Rhodes CJ, Kowluru RA, Kowluru A. Increased phagocyte-like NADPH oxidase and ROS generation in type 2 diabetic ZDF rat and human islets: role of Rac1-JNK1/2 signaling pathway in mitochondrial dysregulation in the diabetic islet. Diabetes 2011;60:2843–2852.
  • Syed I, Jayaram B, Subasinghe W, Kowlsuru A. Tiam1/Rac1 signaling pathway mediates palmitate-induced, ceramide-sensitive generation of superoxides and lipid peroxides and the loss of mitochondrial membrane potential in pancreatic beta-cells. Biochem Pharmacol 2010;80:874–883.
  • Zhou YP, Grill VE. Long-term exposure of rat pancreatic islets to fatty acids inhibits glucose-induced insulin secretion and biosynthesis through a glucose fatty acid cycle. J Clin Invest 1994;93:870–876.
  • Graciano MF, Valle MM, Curi R, Carpinelli AR. Evidence for the involvement of GPR40 and NADPH oxidase in palmitic acid-induced superoxide production and insulin secretion. Islets 2013;5:139–148.
  • Patel H, Chen J, Das KC, Kavdia M. Hyperglycemia induces differential change in oxidative stress at gene expression and functional levels in HUVEC and HMVEC. Cardiovasc Diabetol 2013;12:142.
  • Hecker L, Logsdon NJ, Kurundkar D, Kurundkar A, Bernard K, Hock T, et al. Reversal of persistent fibrosis in aging by targeting NOX4-Nrf2 redox imbalance. Sci Transl Med 2014;6:231ra47.
  • Lau J, Carlsson PO. Low revascularization of human islets when experimentally transplanted into the liver. Transplantation 2009;287:322–325.
  • Weaver JR, Holman TR, Imai Y, Jadhav A, Kenyon V, Maloney DJ, et al. Integration of pro-inflammatory cytokines, 12-lipoxygenase and NOX-1 in pancreatic islet beta cell dysfunction. Mol Cell Endocrinol 2012;358:88–95.
  • Altenhöfer S, Radermacher KA, Kleikers PW, Wingler K, Schmidt HH. Evolution of NADPH Oxidase Inhibitors: Selectivity and Mechanisms for Target Engagement. Antioxid Redox Signal 2014;doi:10.1089/ars.2013.5814.
  • Sedeek M, Callera G, Montezano A, Gutsol A, Heitz F, Szyndralewiez C, et al. Critical role of NOX4-based NADPH oxidase in glucose-induced oxidative stress in the kidney: implications in type 2 diabetic nephropathy. Am J Physiol Renal Physiol 2010;299:F1348–1358.
  • Xiong Q, Kadota S, Tani T, Namba T. Antioxidative effects of phenylethanoids from Cistanche deserticola. Biol Pharm Bull 1996;19:1580–1585.
  • Wilcke M, Walum E, Wikström, P. Thiophene-based compounds exhibiting nox4 inhibitory activity and use thereof in therapy. 2013 Patent application number PCT/EP2013/055218.
  • Kreher CR, Dittrich MT, Guerkov R, Boehm BO, Tary-Lehmann M. CD4 + and CD8 + cells in cryopreserved human PBMC maintain full functionality in cytokine ELISPOT assays. J Immunol Methods 2003;278:79–93.
  • Hubatsch I, Ragnarsson EGE, Artursson P. Determination of drug permeability and prediction of drug absorption in Caco-2 monolayers. Nature Protocols 2007;2:2111–2119.
  • Kristinsson H, Smith DM, Bergsten P, Sargsyan E. FFAR1 is involved in both the acute and chronic effects of palmitate on insulin secretion. Endocrinology 2013;154:4078–4088.
  • Prentki M, Vischer S, Glennon MC, Regazzi R, Deeney JT, Corkey BE. Malonyl-CoA and long chain acyl-CoA esters as metabolic coupling factors in nutrient-induced insulin secretion. J Biol Chem 1992;267:5802–5810.
  • Brown RJ, Rother KI. Effects of beta-cell rest on beta-cell function: a review of clinical and preclinical data. Pediatr Diabetes 2008;9:14–22.
  • Ikemura M, Nishikawa M, Hyoudou K, Kobayashi Y, Yamashita F, Hashida M. Improvement of insulin resistance by removal of systemic hydrogen peroxide by PEGylated catalase in obese mice. Mol Pharm 2010;7:2069–2076.
  • Raddatz K, Turner N, Frangioudakis G, Liao BM, Pedersen DJ, Cantley J, et al. Time-dependent effects of Prkce deletion on glucose homeostasis and hepatic lipid metabolism on dietary lipid oversupply in mice. Diabetologia 2011;54:1447–1456.
  • Hagiwara S, Gohda T, Tanimoto M, Ito T, Murakoshi M, Ohara I, et al. Effects of pyridoxamine (K-163) on glucose intolerance and obesity in high-fat diet C57BL/6 J mice. Metabolism 2009;58:934–945.
  • Zhang ZF, Lu J, Zheng YL, Wu DM, Hu B, Shan Q, et al. Purple sweet potato color attenuates hepatic insulin resistance via blocking oxidative stress and endoplasmic reticulum stress in high-fat-diet-treated mice. J Nutr Biochem 2013;24:1008–1018.
  • Kendig EL, Schneider SN, Clegg DJ, Genter MB, Shertzer HG. Over-the-counter analgesics normalize blood glucose and body composition in mice fed a high fat diet. Biochem Pharmacol 2008;2076:216–224.
  • Espinosa A, Campos C, Díaz-Vegas A, Galgani JE, Juretic N, Osorio-Fuentealba C, et al. Insulin-dependent H2O2 production is higher in muscle fibers of mice fed with a high-fat diet. Int J Mol Sci 2013;14:15740–15754.
  • Li Y, Mouche S, Sajic T, Veyrat-Durebex C, Supale R, Pierroz D, et al. Deficiency in the NADPH oxidase 4 predisposes towards diet-induced obesity. Int J Obes (Lond) 2013; 36:1503–1513.
  • Fu Y, Zhang Y, Wang Z, Wang L, Wei X, Zhang B, et al. Regulation of NADPH oxidase activity is associated with miRNA-25-mediated NOX4 expression in experimental diabetic nephropathy. Am J Nephrol 2010;32:581–589.
  • Takac I, Schröder K, Brandes RP. The NOX family of NADPH oxidases: friend or foe of the vascular system? Curr Hypertens Rep 2012;14:70–78.
  • Parr EL, Bowen KM, Lafferty KJ. Cellular changes in cultured mouse thyroid glands and islets of Langerhans. Transplantation 1980;30:135–141.
  • Lacraz G, Giroix MH, Kassis N, Coulaud J, Galinier A, Noll C, et al. Homo-Delarche F. Islet endothelial activation and oxidative stress gene expression is reduced by IL-1Ra treatment in the type 2 diabetic GK rat. PLoS One 2009; 24:e6963.
  • Takac I, Schröder K, Zhang L, Lardy B, Anilkumar N, Lambeth JD, et al. The E-loop is involved in hydrogen peroxide formation by the NADPH oxidase NOX4. J Biol Chem 2011;286:13304–13313.
  • Vasa-Nicotera M, Chen H, Tucci P, Yang AL, Saintigny G, Menghini R, et al. miR-146a is modulated in human endothelial cell with aging. Atherosclerosis 2011;217:326–330.
  • Li N, Li B, Brun T, Deffert-Delbouille C, Mahiout Z, Daali Y, et al. NADPH oxidase NOX2 defines a new antagonistic role for reactive oxygen species and cAMP/PKA in the regulation of insulin secretion. Diabetes 2012;61: 2842–2850.
  • Mailloux RJ, Fu A, Robson-Doucette C, Allister EM, Wheeler MB, Screaton R, Harper ME. Glutathionylation state of uncoupling protein-2 and the control of glucose-stimulated insulin secretion. J Biol Chem 2012;287:39673–39685
  • Robertson R, Zhou H, Zhang T, Harmon JS. Chronic oxidative stress as a mechanism for glucose toxicity of the beta cell in type 2 diabetes. Cell Biochem Biophys 2007;48:139–146.
  • Corkey BE. Diabetes: have we got it all wrong? Insulin hypersecretion and food additives: cause of obesity and diabetes? Diabetes Care 2012;35:2432–2437.
  • Fred RG, Kappe C, Ameur A, Cen J, Bergsten P, Ravassard P, et al. Role of the AMP kinase in cytokine-induced human EndoC-βH1 cell death. Mol Cell Endo conditionally accepted for publication.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.