Reactive oxygen species mediate insulin signal transduction in mouse hypothalamus

Neuroscience Letters

Volumn 619, Issue , 2016, Pages 1-7

  Onoue, Takeshi ^a   Goto, Motomitsu ^a   Tominaga, Takashi ^a   Sugiyama, Mariko ^a   Tsunekawa, Taku ^a   Hagiwara, Daisuke ^a   Banno, Ryoichi ^a   Suga, Hidetaka ^a   Sugimura, Yoshihisa ^a   Arima, Hiroshi ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Hypothalamus; Insulin signal; NADPH oxidase; Reactive oxygen species

Indexed keywords

HYDROGEN PEROXIDE; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR BETA; OXIDOREDUCTASE INHIBITOR; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SCAVENGER; SUCCINATE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HYPOTHALAMIC SLICE; HYPOTHALAMUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; INTRACELLULAR SPACE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; TISSUE CULTURE TECHNIQUE;

ANIMALS; CELLS, CULTURED; ELECTRON TRANSPORT COMPLEX II; HYDROGEN PEROXIDE; HYPOTHALAMUS; INSULIN; INTRACELLULAR SPACE; MICE, INBRED C57BL; NADP; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUES;

EID: 84960927921     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2016.03.011     Document Type: Article

References (41)

1. Houstis N., Rosen E.D., Lander E.S. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 2006, 440:944-948.
2. 2 and plays an integral role in insulin signal transduction. Mol. Cell. Biol. 2004, 24:1844-1854.
3. Goldstein B.J., Mahadev K., Wu X. Redox paradox: insulin action is facilitated by insulin-stimulated reactive oxygen species with multiple potential signaling targets. Diabetes 2005, 54:311-321.
4. Goldstein B.J., Mahadev K., Wu X., Zhu L., Motoshima H. Role of insulin-induced reactive oxygen species in the insulin signaling pathway. Antioxid. Redox Signal. 2005, 7:1021-1031.
5. Kleinridders A., Ferris H.A., Cai W., Kahn C.R. Insulin action in brain regulates systemic metabolism and brain function. Diabetes 2014, 63:2232-2243.
6. Woods S.C., Lotter E.C., McKay L.D., Porte D. Chronic intracerebroventricular infusion of insulin reduces food intake and body weight of baboons. Nature 1979, 282:503-505.
7. Brown L.M., Clegg D.J., Benoit S.C., Woods S.C. Intraventricular insulin and leptin reduce food intake and body weight in C57BL/6J mice. Physiol. Behav. 2006, 89:687-691.
8. Rahmouni K., Morgan D.A., Morgan G.M., Liu X., Sigmund C.D., Mark A.L., Haynes W.G. Hypothalamic PI3 K and MAPK differentially mediate regional sympathetic activation to insulin. J. Clin. Invest. 2004, 114:652-658.
9. Obici S., Zhang B.B., Karkanias G., Rossetti L. Hypothalamic insulin signaling is required for inhibition of glucose production. Nat. Med. 2002, 8:1376-1382.
10. Koch L., Wunderlich F.T., Seibler J., Konner A.C., Hampel B., Irlenbusch S., Brabant G., Kahn C.R., Schwenk F., Bruning J.C. Central insulin action regulates peripheral glucose and fat metabolism in mice. J. Clin. Invest. 2008, 118:2132-2147.
11. 2 as an enable signal for triggering autophosphorylation of insulin receptor in neurons. J. Mol. Signal 2013, 8:11.
12. Benani A., Troy S., Carmona M.C., Fioramonti X., Lorsignol A., Leloup C., Casteilla L., Penicaud L. Role for mitochondrial reactive oxygen species in brain lipid sensing: redox regulation of food intake. Diabetes 2007, 56:152-160.
13. Jaillard T., Roger M., Galinier A., Guillou P., Benani A., Leloup C., Casteilla L., Penicaud L., Lorsignol A. Hypothalamic reactive oxygen species are required for insulin-induced food intake inhibition: an NADPH oxidase-dependent mechanism. Diabetes 2009, 58:1544-1549.
14. Goto M., Arima H., Watanabe M., Hayashi M., Banno R., Sato I., Nagasaki H., Oiso Y. Ghrelin increases neuropeptide Y and agouti-related peptide gene expression in the arcuate nucleus in rat hypothalamic organotypic cultures. Endocrinology 2006, 147:5102-5109.
15. Arima H., House S.B., Gainer H., Aguilera G. Neuronal activity is required for the circadian rhythm of vasopressin gene transcription in the suprachiasmatic nucleus in vitro. Endocrinology 2002, 143:4165-4171.
16. Ito Y., Banno R., Hagimoto S., Ozawa Y., Arima H., Oiso Y. TNFα increases hypothalamic PTP1B activity via the NF(B pathway in rat hypothalamic organotypic cultures. Regul. Pept. 2012, 174:58-64.
17. Yamagishi S.I., Edelstein D., Du X.L., Kaneda Y., Guzmán M., Brownlee M. Leptin induces mitochondrial superoxide production and monocyte chemoattractant protein-1 expression in aortic endothelial cells by increasing fatty acid oxidation via protein kinase A. J. Biol. Chem. 2001, 276:25096-25100.
18. Kreuzer J., Nurnberg B., Krieger-Brauer H.I. Ligand-dependent autophosphorylation of the insulin receptor is positively regulated by Gi-proteins. Biochem. J. 2004, 380:831-836.
19. 2 generation in human adipocyte plasma membranes is mediated by Galphai2. J. Biol. Chem. 1997, 272:10135-10143.
20. 2-generating system that is activated by insulin via a mechanism bypassing the receptor kinase. J. Clin. Invest. 1992, 89:1006-1013.
21. Mukherjee S.P., Lynn W.S. Reduced nicotinamide adenine dinucleotide phosphate oxidase in adipocyte plasma membrane and its activation by insulin. Possible role in the hormone's effects on adenylate cyclase and the hexose monophosphate shunt. Arch. Biochem. Biophys. 1977, 184:69-76.
22. Yang M., Yang Y., Zhang S., Kahn A.M. Insulin-stimulated hydrogen peroxide increases guanylate cyclase activity in vascular smooth muscle. Hypertension 2003, 42:569-573.
23. Yang M., Foster E., Kahn A.M. Insulin-stimulated NAD(P)H oxidase activity increases migration of cultured vascular smooth muscle cells. Am. J. Hypertens. 2005, 18:1329-1334.
24. Pomytkin I.A., Kolesova O.E. Key role of succinate dehydrogenase in insulin-induced inactivation of protein tyrosine phosphatases. Bull. Exp. Biol. Med. 2002, 133:568-570.
25. Pomytkin I.A., Kolesova O.E. Effect of insulin on the rate of hydrogen peroxide generation in mitochondria. Bull. Exp. Biol. Med. 2003, 135:541-542.
26. Li Y., Trush M.A. Diphenyleneiodonium an NAD(P)H oxidase inhibitor, also potently inhibits mitochondrial reactive oxygen species production. Biochem. Biophys. Res. Commun. 1998, 253:295-299.
27. Aldieri E., Riganti C., Polimeni M., Gazzano E., Lussiana C., Campia I., Ghigo D. Classical inhibitors of NOX NAD(P)H oxidases are not specific. Curr. Drug Metab. 2008, 9:686-696.
28. Iwakami S., Misu H., Takeda T., Sugimori M., Matsugo S., Kaneko S., Takamura T. Concentration-dependent dual effects of hydrogen peroxide on insulin signal transduction in H4IIEC hepatocytes. PLoS One 2011, 6:e27401.
29. Meng T.C., Buckley D.A., Galic S., Tiganis T., Tonks N.K. Regulation of insulin signaling through reversible oxidation of the protein-tyrosine phosphatases TC45 and PTP1B. J. Biol. Chem. 2004, 279:37716-37725.
30. Mahadev K., Zilbering A., Zhu L., Goldstein B.J. Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1b in vivo and enhances the early insulin action cascade. J. Biol. Chem. 2001, 276:21938-21942.
31. Kwon J., Lee S.R., Yang K.S., Ahn Y., Kim Y.J., Stadtman E.R., Rhee S.G. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:16419-16424.
32. Seo J.H., Ahn Y., Lee S.R., Yeol Yeo C., Chung Hur K. The major target of the endogenously generated reactive oxygen species in response to insulin stimulation is phosphatase and tensin homolog and not phosphoinositide-3 kinase (PI-3 kinase) in the PI-3 kinase/Akt pathway. Mol. Biol. Cell 2005, 16:348-357.
33. Loh K., Deng H., Fukushima A., Cai X., Boivin B., Galic S., Bruce C., Shields B.J., Skiba B., Ooms L.M., Stepto N., Wu B., Mitchell C.A., Tonks N.K., Watt M.J., Febbraio M.A., Crack P.J., Andrikopoulos S., Tiganis T. Reactive oxygen species enhance insulin sensitivity. Cell Metab. 2009, 10:260-272.
34. Paolisso G., D'Amore A., Volpe C., Balbi V., Saccomanno F., Galzerano D., Giugliano D., Varricchio M., D'Onofrio F. Evidence for a relationship between oxidative stress and insulin action in non-insulin-dependent (type II) diabetic patients. Metabolism 1994, 43:1426-1429.
35. Vessby J., Basu S., Mohsen R., Berne C., Vessby B. Oxidative stress and antioxidant status in type 1 diabetes mellitus. J. Intern. Med. 2002, 251:69-76.
36. Ohmori K., Ebihara S., Kuriyama S., Ugajin T., Ogata M., Hozawa A., Matsui T., Tsubono Y., Arai H., Sasaki H., Tsuji I. The relationship between body mass index and a plasma lipid peroxidation biomarker in an older, healthy Asian community. Ann. Epidemiol. 2005, 15:80-84.
37. Kaneto H., Xu G., Song K.H., Suzuma K., Bonner-Weir S., Sharma A., Weir G.C. Activation of the hexosamine pathway leads to deterioration of pancreatic beta-cell function through the induction of oxidative stress. J. Biol. Chem. 2001, 276:31099-31104.
38. Sakuraba H., Mizukami H., Yagihashi N., Wada R., Hanyu C., Yagihashi S. Reduced beta-cell mass and expression of oxidative stress-related DNA damage in the islet of Japanese Type II diabetic patients. Diabetologia 2002, 45:85-96.
39. Sakai K., Matsumoto K., Nishikawa T., Suefuji M., Nakamaru K., Hirashima Y., Kawashima J., Shirotani T., Ichinose K., Brownlee M., Araki E. Mitochondrial reactive oxygen species reduce insulin secretion by pancreatic beta-cells. Biochem. Biophys. Res. Commun. 2003, 300:216-222.
40. Liu S., Lee I.M., Song Y., Van Denburgh M., Cook N.R., Manson J.E., Buring J.E. Vitamin E and risk of type 2 diabetes in the women's health study randomized controlled trial. Diabetes 2006, 55:2856-2862.
41. Czernichow S., Couthouis A., Bertrais S., Vergnaud A.C., Dauchet L., Galan P., Hercberg S. Antioxidant supplementation does not affect fasting plasma glucose in the Supplementation with Antioxidant Vitamins and Minerals (SU.VI.MAX) study in France: association with dietary intake and plasma concentrations. Am. J. Clin. Nutr. 2006, 84:395-399.