Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Melatonin and Oxidative Stress in the Diabetic State: Clinical Implications and Potential Therapeutic Applications

Author(s): Javier Espino, Ana B. Rodríguez and José A. Pariente*

Volume 26, Issue 22, 2019

Page: [4178 - 4190] Pages: 13

DOI: 10.2174/0929867325666180410094149

Price: $65

Abstract

All living organisms exhibit circadian rhythms, which govern the majority of biological functions, including metabolic processes. Misalignment of these circadian rhythms increases the risk of developing metabolic diseases. Thus, disruption of the circadian system has been proven to affect the onset of type 2 diabetes mellitus (T2DM). In this context, the pineal indoleamine melatonin is a signaling molecule able to entrain circadian rhythms. There is mounting evidence that suggests a link between disturbances in melatonin production and impaired insulin, glucose, lipid metabolism, and antioxidant capacity. Besides, several genetic association studies have causally associated various single nucleotide polymorphysms (SNPs) of the human MT2 receptor with increased risk of developing T2DM. Taken together, these data suggest that endogenous as well as exogenous melatonin may influence diabetes and associated metabolic disturbances not only by regulating insulin secretion but also by providing protection against reactive oxygen species (ROS) since pancreatic β-cells are very susceptible to oxidative stress due to their low antioxidant capacity.

Keywords: Melatonin, melatonin receptor, circadian rhythm, oxidative stress, type 1 and type 2 diabetes, insulin, β- cell.

[1]
International Diabetes Federation. IDF Diabetes Atlas, 7th ed; International Diabetes Federation: Brussels, Belgium, 2015.
[2]
Bass, J.; Takahashi, J.S. Circadian integration of metabolism and energetics. Science, 2010, 330(6009), 1349-1354.
[http://dx.doi.org/10.1126/science.1195027] [PMID: 21127246]
[3]
Shi, S.Q.; Ansari, T.S.; McGuinness, O.P.; Wasserman, D.H.; Johnson, C.H. Circadian disruption leads to insulin resistance and obesity. Curr. Biol., 2013, 23(5), 372-381.
[http://dx.doi.org/10.1016/j.cub.2013.01.048] [PMID: 23434278]
[4]
Scheer, F.A.; Hilton, M.F.; Mantzoros, C.S.; Shea, S.A. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc. Natl. Acad. Sci. USA, 2009, 106(11), 4453-4458.
[http://dx.doi.org/10.1073/pnas.0808180106] [PMID: 19255424]
[5]
Gale, J.E.; Cox, H.I.; Qian, J.; Block, G.D.; Colwell, C.S.; Matveyenko, A.V. Disruption of circadian rhythms accelerates development of diabetes through pancreatic beta-cell loss and dysfunction. J. Biol. Rhythms, 2011, 26(5), 423-433.
[http://dx.doi.org/10.1177/0748730411416341] [PMID: 21921296]
[6]
Kawakami, N.; Takatsuka, N.; Shimizu, H. Sleep disturbance and onset of type 2 diabetes. Diabetes Care, 2004, 27(1), 282-283.
[http://dx.doi.org/10.2337/diacare.27.1.282] [PMID: 14694011]
[7]
Knutson, K.L.; Spiegel, K.; Penev, P.; Van Cauter, E. The metabolic consequences of sleep deprivation. Sleep Med. Rev., 2007, 11(3), 163-178.
[http://dx.doi.org/10.1016/j.smrv.2007.01.002] [PMID: 17442599]
[8]
Lyssenko, V.; Nagorny, C.L.; Erdos, M.R.; Wierup, N.; Jonsson, A.; Spégel, P.; Bugliani, M.; Saxena, R.; Fex, M.; Pulizzi, N.; Isomaa, B.; Tuomi, T.; Nilsson, P.; Kuusisto, J.; Tuomilehto, J.; Boehnke, M.; Altshuler, D.; Sundler, F.; Eriksson, J.G.; Jackson, A.U.; Laakso, M.; Marchetti, P.; Watanabe, R.M.; Mulder, H.; Groop, L. Common variant in MTNR1B associated with increased risk of type 2 diabetes and impaired early insulin secretion. Nat. Genet., 2009, 41(1), 82-88.
[http://dx.doi.org/10.1038/ng.288] [PMID: 19060908]
[9]
Peschke, E.; Bähr, I.; Mühlbauer, E. Experimental and clinical aspects of melatonin and clock genes in diabetes. J. Pineal Res., 2015, 59(1), 1-23.
[http://dx.doi.org/10.1111/jpi.12240] [PMID: 25904189]
[10]
Hardeland, R.; Cardinali, D.P.; Srinivasan, V.; Spence, D.W.; Brown, G.M.; Pandi-Perumal, S.R. Melatonin--a pleiotropic, orchestrating regulator molecule. Prog. Neurobiol., 2011, 93(3), 350-384.
[http://dx.doi.org/10.1016/j.pneurobio.2010.12.004] [PMID: 21193011]
[11]
Bubenik, G.A. Gastrointestinal melatonin: localization, function, and clinical relevance. Dig. Dis. Sci., 2002, 47(10), 2336-2348.
[http://dx.doi.org/10.1023/A:1020107915919] [PMID: 12395907]
[12]
Pandi-Perumal, S.R.; Srinivasan, V.; Maestroni, G.J.M.; Cardinali, D.P.; Poeggeler, B.; Hardeland, R. Melatonin: Nature’s most versatile biological signal? FEBS J., 2006, 273(13), 2813-2838.
[http://dx.doi.org/10.1111/j.1742-4658.2006.05322.x] [PMID: 16817850]
[13]
Axelrod, J.; Weissbach, H. Enzymatic O-methylation of N-acetylserotonin to melatonin. Science, 1960, 131(3409), 1312.
[http://dx.doi.org/10.1126/science.131.3409.1312] [PMID: 13795316]
[14]
Macchi, M.M.; Bruce, J.N. Human pineal physiology and functional significance of melatonin. Front. Neuroendocrinol., 2004, 25(3-4), 177-195.
[http://dx.doi.org/10.1016/j.yfrne.2004.08.001] [PMID: 15589268]
[15]
Aldhous, M.; Franey, C.; Wright, J.; Arendt, J. Plasma concentrations of melatonin in man following oral absorption of different preparations. Br. J. Clin. Pharmacol., 1985, 19(4), 517-521.
[http://dx.doi.org/10.1111/j.1365-2125.1985.tb02679.x] [PMID: 3994899]
[16]
Claustrat, B.; Brun, J.; Chazot, G. The basic physiology and pathophysiology of melatonin. Sleep Med. Rev., 2005, 9(1), 11-24.
[http://dx.doi.org/10.1016/j.smrv.2004.08.001] [PMID: 15649735]
[17]
Hirata, F.; Hayaishi, O.; Tokuyama, T.; Seno, S. In vitro and in vivo formation of two new metabolites of melatonin. J. Biol. Chem., 1974, 249(4), 1311-1313.
[PMID: 4814344]
[18]
Kelly, R.W.; Amato, F.; Seamark, R.F. N-acetyl-5-methoxy kynurenamine, a brain metabolite of melatonin, is a potent inhibitor of prostaglandin biosynthesis. Biochem. Biophys. Res. Commun., 1984, 121(1), 372-379.
[http://dx.doi.org/10.1016/0006-291X(84)90732-0] [PMID: 6428407]
[19]
Peschke, E.; Frese, T.; Chankiewitz, E.; Peschke, D.; Preiss, U.; Schneyer, U.; Spessert, R.; Mühlbauer, E. Diabetic Goto Kakizaki rats as well as type 2 diabetic patients show a decreased diurnal serum melatonin level and an increased pancreatic melatonin-receptor status. J. Pineal Res., 2006, 40(2), 135-143.
[http://dx.doi.org/10.1111/j.1600-079X.2005.00287.x] [PMID: 16441550]
[20]
Espino, J.; Pariente, J.A.; Rodríguez, A.B. Role of melatonin on diabetes-related metabolic disorders. World J. Diabetes, 2011, 2(6), 82-91.
[http://dx.doi.org/10.4239/wjd.v2.i6.82] [PMID: 21860691]
[21]
Srinivasan, V.; Ohta, Y.; Espino, J.; Pariente, J.A.; Rodriguez, A.B.; Mohamed, M.; Zakaria, R. Metabolic syndrome, its pathophysiology and the role of melatonin. Recent Pat. Endocr. Metab. Immune Drug Discov., 2013, 7(1), 11-25.
[http://dx.doi.org/10.2174/187221413804660953] [PMID: 22946959]
[22]
Reppert, S.M.; Weaver, D.R.; Godson, C. Melatonin receptors step into the light: cloning and classification of subtypes. Trends Pharmacol. Sci., 1996, 17(3), 100-102.
[http://dx.doi.org/10.1016/0165-6147(96)10005-5] [PMID: 8936344]
[23]
Dubocovich, M.L.; Markowska, M. Functional MT1 and MT2 melatonin receptors in mammals. Endocrine, 2005, 27(2), 101-110.
[http://dx.doi.org/10.1385/ENDO:27:2:101] [PMID: 16217123]
[24]
Poirel, V.J.; Cailotto, C.; Streicher, D.; Pévet, P.; Masson-Pévet, M.; Gauer, F. MT1 melatonin receptor mRNA tissular localization by PCR amplification. Neuroendocrinol. Lett., 2003, 24(1-2), 33-38.
[PMID: 12743529]
[25]
Sallinen, P.; Saarela, S.; Ilves, M.; Vakkuri, O.; Leppäluoto, J. The expression of MT1 and MT2 melatonin receptor mRNA in several rat tissues. Life Sci., 2005, 76(10), 1123-1134.
[http://dx.doi.org/10.1016/j.lfs.2004.08.016] [PMID: 15620576]
[26]
Soares, J.M., Jr; Masana, M.I.; Erşahin, C.; Dubocovich, M.L. Functional melatonin receptors in rat ovaries at various stages of the estrous cycle. J. Pharmacol. Exp. Ther., 2003, 306(2), 694-702.
[http://dx.doi.org/10.1124/jpet.103.049916] [PMID: 12721330]
[27]
Meyer, P.; Pache, M.; Loeffler, K.U.; Brydon, L.; Jockers, R.; Flammer, J.; Wirz-Justice, A.; Savaskan, E. Melatonin MT-1-receptor immunoreactivity in the human eye. Br. J. Ophthalmol., 2002, 86(9), 1053-1057.
[http://dx.doi.org/10.1136/bjo.86.9.1053] [PMID: 12185137]
[28]
Pozo, D.; Delgado, M.; Fernandez-Santos, J.M.; Calvo, J.R.; Gomariz, R.P.; Martin-Lacave, I.; Ortiz, G.G.; Guerrero, J.M. Expression of the Mel1a-melatonin receptor mRNA in T and B subsets of lymphocytes from rat thymus and spleen. FASEB J., 1997, 11(6), 466-473.
[http://dx.doi.org/10.1096/fasebj.11.6.9194527] [PMID: 9194527]
[29]
Naji, L.; Carrillo-Vico, A.; Guerrero, J.M.; Calvo, J.R. Expression of membrane and nuclear melatonin receptors in mouse peripheral organs. Life Sci., 2004, 74(18), 2227-2236.
[http://dx.doi.org/10.1016/j.lfs.2003.08.046] [PMID: 14987948]
[30]
Stebelová, K.; Anttila, K.; Mänttäri, S.; Saarela, S.; Zeman, M. Immunohistochemical definition of MT(2) receptors and melatonin in the gastrointestinal tissues of rat. Acta Histochem., 2010, 112(1), 26-33.
[http://dx.doi.org/10.1016/j.acthis.2008.03.004] [PMID: 19004484]
[31]
Carrillo-Vico, A.; García-Pergañeda, A.; Naji, L.; Calvo, J.R.; Romero, M.P.; Guerrero, J.M. Expression of membrane and nuclear melatonin receptor mRNA and protein in the mouse immune system. Cell. Mol. Life Sci., 2003, 60(10), 2272-2278.
[http://dx.doi.org/10.1007/s00018-003-3207-4] [PMID: 14618273]
[32]
Soták, M.; Mrnka, L.; Pácha, J. Heterogeneous expression of melatonin receptor MT1 mRNA in the rat intestine under control and fasting conditions. J. Pineal Res., 2006, 41(2), 183-188.
[http://dx.doi.org/10.1111/j.1600-079X.2006.00355.x] [PMID: 16879325]
[33]
Nagorny, C.L.F.; Sathanoori, R.; Voss, U.; Mulder, H.; Wierup, N. Distribution of melatonin receptors in murine pancreatic islets. J. Pineal Res., 2011, 50(4), 412-417.
[http://dx.doi.org/10.1111/j.1600-079X.2011.00859.x] [PMID: 21355877]
[34]
Ramracheya, R.D.; Muller, D.S.; Squires, P.E.; Brereton, H.; Sugden, D.; Huang, G.C.; Amiel, S.A.; Jones, P.M.; Persaud, S.J. Function and expression of melatonin receptors on human pancreatic islets. J. Pineal Res., 2008, 44(3), 273-279.
[http://dx.doi.org/10.1111/j.1600-079X.2007.00523.x] [PMID: 18194202]
[35]
Peschke, E.; Fauteck, J.D.; Musshoff, U.; Schmidt, F.; Beckmann, A.; Peschke, D. Evidence for a melatonin receptor within pancreatic islets of neonate rats: functional, autoradiographic, and molecular investigations. J. Pineal Res., 2000, 28(3), 156-164.
[http://dx.doi.org/10.1034/j.1600-079X.2001.280305.x] [PMID: 10739302]
[36]
Mühlbauer, E.; Albrecht, E.; Hofmann, K.; Bazwinsky-Wutschke, I.; Peschke, E. Melatonin inhibits insulin secretion in rat insulinoma β-cells (INS-1) heterologously expressing the human melatonin receptor isoform MT2. J. Pineal Res., 2011, 51(3), 361-372.
[http://dx.doi.org/10.1111/j.1600-079X.2011.00898.x] [PMID: 21585522]
[37]
Tan, D.X.; Hardeland, R.; Manchester, L.C.; Paredes, S.D.; Korkmaz, A.; Sainz, R.M.; Mayo, J.C.; Fuentes-Broto, L.; Reiter, R.J. The changing biological roles of melatonin during evolution: from an antioxidant to signals of darkness, sexual selection and fitness. Biol. Rev. Camb. Philos. Soc., 2010, 85(3), 607-623.
[PMID: 20039865]
[38]
Tan, D.X.; Zheng, X.; Kong, J.; Manchester, L.C.; Hardeland, R.; Kim, S.J.; Xu, X.; Reiter, R.J. Fundamental issues related to the origin of melatonin and melatonin isomers during evolution: relation to their biological functions. Int. J. Mol. Sci., 2014, 15(9), 15858-15890.
[http://dx.doi.org/10.3390/ijms150915858] [PMID: 25207599]
[39]
Manchester, L.C.; Poeggeler, B.; Alvares, F.L.; Ogden, G.B.; Reiter, R.J. Melatonin immunoreactivity in the photosynthetic prokaryote Rhodospirillum rubrum: implications for an ancient antioxidant system. Cell. Mol. Biol. Res., 1995, 41(5), 391-395.
[PMID: 8867786]
[40]
Tan, D.X.; Manchester, L.C.; Esteban-Zubero, E.; Zhou, Z.; Reiter, R.J. Melatonin as a potent and inducible endogenous antioxidant: synthesis and metabolism. Molecules, 2015, 20(10), 18886-18906.
[http://dx.doi.org/10.3390/molecules201018886] [PMID: 26501252]
[41]
Reiter, R.J.; Mayo, J.C.; Tan, D-X.; Sainz, R.M.; Alatorre-Jimenez, M.; Qin, L. Melatonin as an antioxidant: under promises but over delivers. J. Pineal Res., 2016, 61(3), 253-278.
[http://dx.doi.org/10.1111/jpi.12360] [PMID: 27500468]
[42]
Sharafati-Chaleshtori, R.; Shirzad, H.; Rafieian-Kopaei, M.; Soltani, A. Melatonin and human mitochondrial diseases. J. Res. Med. Sci., 2017, 22, 2.
[http://dx.doi.org/10.4103/1735-1995.199092] [PMID: 28400824]
[43]
Brazão, V.; Santello, F.H.; Colato, R.P.; Mazotti, T.T.; Tazinafo, L.F.; Toldo, M.P.A.; do Vale, G.T.; Tirapelli, C.R.; do Prado, J.C. Jr. Melatonin: Antioxidant and modulatory properties in age-related changes during Trypanosoma cruzi infection. J. Pineal Res., 2017, 63(1)e12409
[http://dx.doi.org/10.1111/jpi.12409] [PMID: 28370218]
[44]
Túnez, I.; Muñoz, M.C.; Medina, F.J.; Salcedo, M.; Feijóo, M.; Montilla, P. Comparison of melatonin, vitamin E and L-carnitine in the treatment of neuro- and hepatotoxicity induced by thioacetamide. Cell Biochem. Funct., 2007, 25(2), 119-127.
[http://dx.doi.org/10.1002/cbf.1276] [PMID: 16245358]
[45]
Espino, J.; Pariente, J.A.; Rodríguez, A.B. Oxidative stress and immunosenescence: therapeutic effects of melatonin. Oxid. Med. Cell. Longev., 2012.2012670294
[http://dx.doi.org/10.1155/2012/670294] [PMID: 23346283]
[46]
Ortiz, G.G.; Pacheco-Moisés, F.P.; Gómez-Rodríguez, V.M.; González-Renovato, E.D.; Torres-Sánchez, E.D.; Ramírez-Anguiano, A.C. Fish oil, melatonin and vitamin E attenuates midbrain cyclooxygenase-2 activity and oxidative stress after the administration of 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine. Metab. Brain Dis., 2013, 28(4), 705-709.
[http://dx.doi.org/10.1007/s11011-013-9416-0] [PMID: 23703110]
[47]
Elbe, H.; Vardi, N.; Esrefoglu, M.; Ates, B.; Yologlu, S.; Taskapan, C. Amelioration of streptozotocin-induced diabetic nephropathy by melatonin, quercetin, and resveratrol in rats. Hum. Exp. Toxicol., 2015, 34(1), 100-113.
[http://dx.doi.org/10.1177/0960327114531995] [PMID: 24812155]
[48]
Oxenkrug, G.F.; McIntyre, I.M. Stress-induced synthesis of melatonin: possible involvement of the endogenous monoamine oxidase inhibitor (tribulin). Life Sci., 1985, 37(18), 1743-1746.
[http://dx.doi.org/10.1016/0024-3205(85)90303-0] [PMID: 2414629]
[49]
Stokkan, K.A.; Nonaka, K.O.; Lerchl, A.; Vaughan, M.K.; Reiter, R.J. Low temperature stimulates pineal activity in Syrian hamsters. J. Pineal Res., 1991, 10(1), 43-48.
[http://dx.doi.org/10.1111/j.1600-079X.1991.tb00008.x] [PMID: 2056431]
[50]
Stokkan, K.A.; Reiter, R.J.; Vaughan, M.K.; Nonaka, K.O.; Lerchl, A. Endocrine and metabolic effects of life-long food restriction in rats. Acta Endocrinol. (Copenh.), 1991, 125(1), 93-100.
[http://dx.doi.org/10.1530/acta.0.1250093] [PMID: 1872131]
[51]
Mattison, J.A.; Lane, M.A.; Roth, G.S.; Ingram, D.K. Calorie restriction in rhesus monkeys. Exp. Gerontol., 2003, 38(1-2), 35-46.
[http://dx.doi.org/10.1016/S0531-5565(02)00146-8] [PMID: 12543259]
[52]
Tan, D.X.; Manchester, L.C.; Sainz, R.M.; Mayo, J.C.; León, J.; Reiter, R. J. Physiological ischemia/reperfusion phenomena and their relation to endogenous melatonin production: a hypothesis. Endocrine, 2005, 27(2), 149-158.
[http://dx.doi.org/10.1385/ENDO:27:2:149] [PMID: 16217128]
[53]
Green, C.B.; Takahashi, J.S.; Bass, J. The meter of metabolism. Cell, 2008, 134(5), 728-742.
[http://dx.doi.org/10.1016/j.cell.2008.08.022] [PMID: 18775307]
[54]
Karlsson, B.; Knutsson, A.; Lindahl, B. Is there an association between shift work and having a metabolic syndrome? Results from a population based study of 27,485 people. Occup. Environ. Med., 2001, 58(11), 747-752.
[http://dx.doi.org/10.1136/oem.58.11.747] [PMID: 11600731]
[55]
Knutson, K.L.; Ryden, A.M.; Mander, B.A.; Van Cauter, E. Role of sleep duration and quality in the risk and severity of type 2 diabetes mellitus. Arch. Intern. Med., 2006, 166(16), 1768-1774.
[http://dx.doi.org/10.1001/archinte.166.16.1768] [PMID: 16983057]
[56]
Scheer, F.A.; Hilton, M.F.; Mantzoros, C.S.; Shea, S.A. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc. Natl. Acad. Sci. USA, 2009, 106(11), 4453-4458.
[http://dx.doi.org/10.1073/pnas.0808180106] [PMID: 19255424]
[57]
Lima, F.B.; Machado, U.F.; Bartol, I.; Seraphim, P.M.; Sumida, D.H.; Moraes, S.M.; Hell, N.S.; Okamoto, M.M.; Saad, M.J.; Carvalho, C.R.; Cipolla-Neto, J. Pinealectomy causes glucose intolerance and decreases adipose cell responsiveness to insulin in rats. Am. J. Physiol., 1998, 275(6), E934-E941.
[PMID: 9843734]
[58]
Bähr, I.; Mühlbauer, E.; Schucht, H.; Peschke, E. Melatonin stimulates glucagon secretion in vitro and in vivo. J. Pineal Res., 2011, 50(3), 336-344.
[http://dx.doi.org/10.1111/j.1600-079X.2010.00848.x] [PMID: 21244480]
[59]
Peschke, E. Melatonin, endocrine pancreas and diabetes. J. Pineal Res., 2008, 44(1), 26-40.
[PMID: 18078445]
[60]
Peschke, E.; Stumpf, I.; Bazwinsky, I.; Litvak, L.; Dralle, H.; Mühlbauer, E. Melatonin and type 2 diabetes - a possible link? J. Pineal Res., 2007, 42(4), 350-358.
[http://dx.doi.org/10.1111/j.1600-079X.2007.00426.x] [PMID: 17439551]
[61]
Rasmussen, D.D.; Boldt, B.M.; Wilkinson, C.W.; Yellon, S.M.; Matsumoto, A.M. Daily melatonin administration at middle age suppresses male rat visceral fat, plasma leptin, and plasma insulin to youthful levels. Endocrinology, 1999, 140(2), 1009-1012.
[http://dx.doi.org/10.1210/endo.140.2.6674] [PMID: 9927336]
[62]
Wolden-Hanson, T.; Mitton, D.R.; McCants, R.L.; Yellon, S.M.; Wilkinson, C.W.; Matsumoto, A.M.; Rasmussen, D.D. Daily melatonin administration to middle-aged male rats suppresses body weight, intraabdominal adiposity, and plasma leptin and insulin independent of food intake and total body fat. Endocrinology, 2000, 141(2), 487-497.
[http://dx.doi.org/10.1210/endo.141.2.7311] [PMID: 10650927]
[63]
Rasmussen, D.D.; Mitton, D.R.; Larsen, S.A.; Yellon, S.M. Aging-dependent changes in the effect of daily melatonin supplementation on rat metabolic and behavioral responses. J. Pineal Res., 2001, 31(1), 89-94.
[http://dx.doi.org/10.1034/j.1600-079X.2001.310113.x] [PMID: 11485011]
[64]
Dhar, M.; Dayal, S.S.; Ramesh Babu, C.S.; Arora, S.R. Effect of melatonin on glucose tolerance and blood glucose circadian rhythm in rabbits. Indian J. Physiol. Pharmacol., 1983, 27(2), 109-117.
[PMID: 6885122]
[65]
Cagnacci, A.; Arangino, S.; Renzi, A.; Paoletti, A.M.; Melis, G.B.; Cagnacci, P.; Volpe, A. Influence of melatonin administration on glucose tolerance and insulin sensitivity of postmenopausal women. Clin. Endocrinol. (Oxf.), 2001, 54(3), 339-346.
[http://dx.doi.org/10.1046/j.1365-2265.2001.01232.x] [PMID: 11298086]
[66]
Champney, T.H.; Steger, R.W.; Christie, D.S.; Reiter, R.J. Alterations in components of the pineal melatonin synthetic pathway by acute insulin stress in the rat and Syrian hamster. Brain Res., 1985, 338(1), 25-32.
[http://dx.doi.org/10.1016/0006-8993(85)90244-6] [PMID: 3896393]
[67]
Champney, T.H.; Brainard, G.C.; Richardson, B.A.; Reiter, R.J. Experimentally-induced diabetes reduces nocturnal pineal melatonin content in the Syrian hamster. Comp. Biochem. Physiol. A Comp. Physiol., 1983, 76(1), 199-201.
[http://dx.doi.org/10.1016/0300-9629(83)90314-6] [PMID: 6138184]
[68]
Boden, G.; Ruiz, J.; Urbain, J.L.; Chen, X. Evidence for a circadian rhythm of insulin secretion. Am. J. Physiol., 1996, 271(2 Pt 1), E246-E252.
[PMID: 8770017]
[69]
Champney, T.H.; Holtorf, A.P.; Craft, C.M.; Reiter, R.J. Hormonal modulation of pineal melatonin synthesis in rats and Syrian hamsters: effects of streptozotocin-induced diabetes and insulin injections. Comp. Biochem. Physiol. A Comp. Physiol., 1986, 83(2), 391-395.
[http://dx.doi.org/10.1016/0300-9629(86)90594-3] [PMID: 2420523]
[70]
Peschke, E.; Mühlbauer, E.; Musshoff, U.; Csernus, V.J.; Chankiewitz, E.; Peschke, D. Receptor (MT(1)) mediated influence of melatonin on cAMP concentration and insulin secretion of rat insulinoma cells INS-1. J. Pineal Res., 2002, 33(2), 63-71.
[http://dx.doi.org/10.1034/j.1600-079X.2002.02919.x] [PMID: 12153439]
[71]
Kemp, D.M.; Ubeda, M.; Habener, J.F. Identification and functional characterization of melatonin Mel 1a receptors in pancreatic beta cells: potential role in incretin-mediated cell function by sensitization of cAMP signaling. Mol. Cell. Endocrinol., 2002, 191(2), 157-166.
[http://dx.doi.org/10.1016/S0303-7207(02)00064-3] [PMID: 12062899]
[72]
Picinato, M.C.; Haber, E.P.; Cipolla-Neto, J.; Curi, R.; de Oliveira Carvalho, C.R.; Carpinelli, A.R. Melatonin inhibits insulin secretion and decreases PKA levels without interfering with glucose metabolism in rat pancreatic islets. J. Pineal Res., 2002, 33(3), 156-160.
[http://dx.doi.org/10.1034/j.1600-079X.2002.02903.x] [PMID: 12220330]
[73]
Scheer, F.A.; Hilton, M.F.; Mantzoros, C.S.; Shea, S.A. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc. Natl. Acad. Sci. USA, 2009, 106(11), 4453-4458.
[http://dx.doi.org/10.1073/pnas.0808180106] [PMID: 19255424]
[74]
O’Brien, I.A.; Lewin, I.G.; O’Hare, J.P.; Arendt, J.; Corrall, R.J. Abnormal circadian rhythm of melatonin in diabetic autonomic neuropathy. Clin. Endocrinol. (Oxf.), 1986, 24(4), 359-364.
[http://dx.doi.org/10.1111/j.1365-2265.1986.tb01639.x] [PMID: 3742831]
[75]
Frese, T.; Bach, A.G.; Mühlbauer, E.; Pönicke, K.; Brömme, H.J.; Welp, A.; Peschke, E. Pineal melatonin synthesis is decreased in type 2 diabetic Goto-Kakizaki rats. Life Sci., 2009, 85(13-14), 526-533.
[http://dx.doi.org/10.1016/j.lfs.2009.08.004] [PMID: 19695268]
[76]
Peschke, E.; Wolgast, S.; Bazwinsky, I.; Pönicke, K.; Muhlbauer, E. Increased melatonin synthesis in pineal glands of rats in streptozotocin induced type 1 diabetes. J. Pineal Res., 2008, 45(4), 439-448.
[http://dx.doi.org/10.1111/j.1600-079X.2008.00612.x] [PMID: 18624957]
[77]
Pang, S.F.; Tang, F.; Tang, P.L. Alloxan-induced diabetes and the pineal gland: differential effects on the levels of pineal N-acetylserotonin, pineal melatonin, and serum melatonin. J. Pineal Res., 1985, 2(1), 79-85.
[http://dx.doi.org/10.1111/j.1600-079X.1985.tb00629.x] [PMID: 3831302]
[78]
Ha, E.; Yim, S.V.; Chung, J.H.; Yoon, K.S.; Kang, I.; Cho, Y.H.; Baik, H.H. Melatonin stimulates glucose transport via insulin receptor substrate-1/phosphatidylinositol 3-kinase pathway in C2C12 murine skeletal muscle cells. J. Pineal Res., 2006, 41(1), 67-72.
[http://dx.doi.org/10.1111/j.1600-079X.2006.00334.x] [PMID: 16842543]
[79]
Nishida, S. Metabolic effects of melatonin on oxidative stress and diabetes mellitus. Endocrine, 2005, 27(2), 131-136.
[http://dx.doi.org/10.1385/ENDO:27:2:131] [PMID: 16217126]
[80]
Peschke, E.; Hofmann, K.; Pönicke, K.; Wedekind, D.; Mühlbauer, E. Catecholamines are the key for explaining the biological relevance of insulin-melatonin antagonisms in type 1 and type 2 diabetes. J. Pineal Res., 2012, 52(4), 389-396.
[http://dx.doi.org/10.1111/j.1600-079X.2011.00951.x] [PMID: 21929683]
[81]
Reiter, R.J.; Paredes, S.D.; Manchester, L.C.; Tan, D.X. Reducing oxidative/nitrosative stress: a newly-discovered genre for melatonin. Crit. Rev. Biochem. Mol. Biol., 2009, 44(4), 175-200.
[http://dx.doi.org/10.1080/10409230903044914] [PMID: 19635037]
[82]
Grapengiesser, E.; Salehi, A.; Qader, S.S.; Hellman, B. Glucose induces glucagon release pulses antisynchronous with insulin and sensitive to purinoceptor inhibition. Endocrinology, 2006, 147(7), 3472-3477.
[http://dx.doi.org/10.1210/en.2005-1431] [PMID: 16614082]
[83]
Meier, J.J.; Kjems, L.L.; Veldhuis, J.D.; Lefèbvre, P.; Butler, P.C. Postprandial suppression of glucagon secretion depends on intact pulsatile insulin secretion: further evidence for the intraislet insulin hypothesis. Diabetes, 2006, 55(4), 1051-1056.
[http://dx.doi.org/10.2337/diabetes.55.04.06.db05-1449] [PMID: 16567528]
[84]
Ruiter, M.; La Fleur, S.E.; van Heijningen, C.; van der Vliet, J.; Kalsbeek, A.; Buijs, R.M. The daily rhythm in plasma glucagon concentrations in the rat is modulated by the biological clock and by feeding behavior. Diabetes, 2003, 52(7), 1709-1715.
[http://dx.doi.org/10.2337/diabetes.52.7.1709] [PMID: 12829637]
[85]
Bähr, I.; Mühlbauer, E.; Albrecht, E.; Peschke, E. Evidence of the receptor-mediated influence of melatonin on pancreatic glucagon secretion via the Gαq protein-coupled and PI3K signaling pathways. J. Pineal Res., 2012, 53(4), 390-398.
[http://dx.doi.org/10.1111/j.1600-079X.2012.01009.x] [PMID: 22672634]
[86]
Peschke, E.; Schucht, H.; Mühlbauer, E. Long-term enteral administration of melatonin reduces plasma insulin and increases expression of pineal insulin receptors in both Wistar and type 2-diabetic Goto-Kakizaki rats. J. Pineal Res., 2010, 49(4), 373-381.
[http://dx.doi.org/10.1111/j.1600-079X.2010.00804.x] [PMID: 20840603]
[87]
Mühlbauer, E.; Gross, E.; Labucay, K.; Wolgast, S.; Peschke, E. Loss of melatonin signalling and its impact on circadian rhythms in mouse organs regulating blood glucose. Eur. J. Pharmacol., 2009, 606(1-3), 61-71.
[http://dx.doi.org/10.1016/j.ejphar.2009.01.029] [PMID: 19374844]
[88]
Rodríguez, V.; Mellado, C.; Álvarez, E.; De Diego, J.G.; Blázquez, E. Effect of pinealectomy on liver insulin and glucagon receptor concentrations in the rat. J. Pineal Res., 1989, 6(1), 77-88.
[http://dx.doi.org/10.1111/j.1600-079X.1989.tb00405.x] [PMID: 2537898]
[89]
McCarthy, M.I. Genomics, type 2 diabetes, and obesity. N. Engl. J. Med., 2010, 363(24), 2339-2350.
[http://dx.doi.org/10.1056/NEJMra0906948] [PMID: 21142536]
[90]
Liao, S.; Liu, Y.; Tan, Y.; Gan, L.; Mei, J.; Song, W.; Chi, S.; Dong, X.; Chen, X.; Deng, S. Association of genetic variants of melatonin receptor 1B with gestational plasma glucose level and risk of glucose intolerance in pregnant Chinese women. PLoS One, 2012, 7(7)e40113
[http://dx.doi.org/10.1371/journal.pone.0040113] [PMID: 22768333]
[91]
Andersson, E.A.; Holst, B.; Sparsø, T.; Grarup, N.; Banasik, K.; Holmkvist, J.; Jørgensen, T.; Borch-Johnsen, K.; Egerod, K.L.; Lauritzen, T.; Sørensen, T.I.; Bonnefond, A.; Meyre, D.; Froguel, P.; Schwartz, T.W.; Pedersen, O.; Hansen, T. MTNR1B G24E variant associates With BMI and fasting plasma glucose in the general population in studies of 22,142 Europeans. Diabetes, 2010, 59(6), 1539-1548.
[http://dx.doi.org/10.2337/db09-1757] [PMID: 20200315]
[92]
Prokopenko, I.; Langenberg, C.; Florez, J.C.; Saxena, R.; Soranzo, N.; Thorleifsson, G.; Loos, R.J.; Manning, A.K.; Jackson, A.U.; Aulchenko, Y.; Potter, S.C.; Erdos, M.R.; Sanna, S.; Hottenga, J.J.; Wheeler, E.; Kaakinen, M.; Lyssenko, V.; Chen, W.M.; Ahmadi, K.; Beckmann, J.S.; Bergman, R.N.; Bochud, M.; Bonnycastle, L.L.; Buchanan, T.A.; Cao, A.; Cervino, A.; Coin, L.; Collins, F.S.; Crisponi, L.; de Geus, E.J.; Dehghan, A.; Deloukas, P.; Doney, A.S.; Elliott, P.; Freimer, N.; Gateva, V.; Herder, C.; Hofman, A.; Hughes, T.E.; Hunt, S.; Illig, T.; Inouye, M.; Isomaa, B.; Johnson, T.; Kong, A.; Krestyaninova, M.; Kuusisto, J.; Laakso, M.; Lim, N.; Lindblad, U.; Lindgren, C.M.; McCann, O.T.; Mohlke, K.L.; Morris, A.D.; Naitza, S.; Orrù, M.; Palmer, C.N.; Pouta, A.; Randall, J.; Rathmann, W.; Saramies, J.; Scheet, P.; Scott, L.J.; Scuteri, A.; Sharp, S.; Sijbrands, E.; Smit, J.H.; Song, K.; Steinthorsdottir, V.; Stringham, H.M.; Tuomi, T.; Tuomilehto, J.; Uitterlinden, A.G.; Voight, B.F.; Waterworth, D.; Wichmann, H.E.; Willemsen, G.; Witteman, J.C.; Yuan, X.; Zhao, J.H.; Zeggini, E.; Schlessinger, D.; Sandhu, M.; Boomsma, D.I.; Uda, M.; Spector, T.D.; Penninx, B.W.; Altshuler, D.; Vollenweider, P.; Jarvelin, M.R.; Lakatta, E.; Waeber, G.; Fox, C.S.; Peltonen, L.; Groop, L.C.; Mooser, V.; Cupples, L.A.; Thorsteinsdottir, U.; Boehnke, M.; Barroso, I.; Van Duijn, C.; Dupuis, J.; Watanabe, R.M.; Stefansson, K.; McCarthy, M.I.; Wareham, N.J.; Meigs, J.B.; Abecasis, G.R. Variants in MTNR1B influence fasting glucose levels. Nat. Genet., 2009, 41(1), 77-81.
[http://dx.doi.org/10.1038/ng.290] [PMID: 19060907]
[93]
Bouatia-Naji, N.; Bonnefond, A.; Cavalcanti-Proença, C.; Sparsø, T.; Holmkvist, J.; Marchand, M.; Delplanque, J.; Lobbens, S.; Rocheleau, G.; Durand, E.; De Graeve, F.; Chèvre, J.C.; Borch-Johnsen, K.; Hartikainen, A.L.; Ruokonen, A.; Tichet, J.; Marre, M.; Weill, J.; Heude, B.; Tauber, M.; Lemaire, K.; Schuit, F.; Elliott, P.; Jørgensen, T.; Charpentier, G.; Hadjadj, S.; Cauchi, S.; Vaxillaire, M.; Sladek, R.; Visvikis-Siest, S.; Balkau, B.; Lévy-Marchal, C.; Pattou, F.; Meyre, D.; Blakemore, A.I.; Jarvelin, M.R.; Walley, A.J.; Hansen, T.; Dina, C.; Pedersen, O.; Froguel, P. A variant near MTNR1B is associated with increased fasting plasma glucose levels and type 2 diabetes risk. Nat. Genet., 2009, 41(1), 89-94.
[http://dx.doi.org/10.1038/ng.277] [PMID: 19060909]
[94]
Chambers, J.C.; Zhang, W.; Zabaneh, D.; Sehmi, J.; Jain, P.; McCarthy, M.I.; Froguel, P.; Ruokonen, A.; Balding, D.; Jarvelin, M.R.; Scott, J.; Elliott, P.; Kooner, J.S. Common genetic variation near melatonin receptor MTNR1B contributes to raised plasma glucose and increased risk of type 2 diabetes among Indian Asians and European Caucasians. Diabetes, 2009, 58(11), 2703-2708.
[http://dx.doi.org/10.2337/db08-1805] [PMID: 19651812]
[95]
Staiger, H.; Machicao, F.; Schäfer, S.A.; Kirchhoff, K.; Kantartzis, K.; Guthoff, M.; Silbernagel, G.; Stefan, N.; Häring, H.U.; Fritsche, A. Polymorphisms within the novel type 2 diabetes risk locus MTNR1B determine beta-cell function. PLoS One, 2008, 3(12)e3962
[http://dx.doi.org/10.1371/journal.pone.0003962] [PMID: 19088850]
[96]
Sparsø, T.; Bonnefond, A.; Andersson, E.; Bouatia-Naji, N.; Holmkvist, J.; Wegner, L.; Grarup, N.; Gjesing, A.P.; Banasik, K.; Cavalcanti-Proença, C.; Marchand, M.; Vaxillaire, M.; Charpentier, G.; Jarvelin, M.R.; Tichet, J.; Balkau, B.; Marre, M.; Lévy-Marchal, C.; Faerch, K.; Borch-Johnsen, K.; Jørgensen, T.; Madsbad, S.; Poulsen, P.; Vaag, A.; Dina, C.; Hansen, T.; Pedersen, O.; Froguel, P. G-allele of intronic rs10830963 in MTNR1B confers increased risk of impaired fasting glycemia and type 2 diabetes through an impaired glucose-stimulated insulin release: studies involving 19,605 Europeans. Diabetes, 2009, 58(6), 1450-1456.
[http://dx.doi.org/10.2337/db08-1660] [PMID: 19324940]
[97]
Rasmussen-Torvik, L.J.; Guo, X.; Bowden, D.W.; Bertoni, A.G.; Sale, M.M.; Yao, J.; Bluemke, D.A.; Goodarzi, M.O.; Chen, Y.I.; Vaidya, D.; Raffel, L.J.; Papanicolaou, G.J.; Meigs, J.B.; Pankow, J.S. Fasting glucose GWAS candidate region analysis across ethnic groups in the multiethnic study of atherosclerosis (MESA). Genet. Epidemiol., 2012, 36(4), 384-391.
[http://dx.doi.org/10.1002/gepi.21632] [PMID: 22508271]
[98]
Langenberg, C.; Pascoe, L.; Mari, A.; Tura, A.; Laakso, M.; Frayling, T.M.; Barroso, I.; Loos, R.J.; Wareham, N.J.; Walker, M. RISC Consortium. Common genetic variation in the melatonin receptor 1B gene (MTNR1B) is associated with decreased early-phase insulin response. Diabetologia, 2009, 52(8), 1537-1542.
[http://dx.doi.org/10.1007/s00125-009-1392-x] [PMID: 19455304]
[99]
Renström, F.; Koivula, R.W.; Varga, T.V.; Hallmans, G.; Mulder, H.; Florez, J.C.; Hu, F.B.; Franks, P.W. Season-dependent associations of circadian rhythm-regulating loci (CRY1, CRY2 and MTNR1B) and glucose homeostasis: the GLACIER study. Diabetologia, 2015, 58(5), 997-1005.
[http://dx.doi.org/10.1007/s00125-015-3533-8] [PMID: 25707907]
[100]
Tuomi, T.; Nagorny, C.L.F.; Singh, P.; Bennet, H.; Yu, Q.; Alenkvist, I.; Isomaa, B.; Östman, B.; Söderström, J.; Pesonen, A.K.; Martikainen, S.; Räikkönen, K.; Forsén, T.; Hakaste, L.; Almgren, P.; Storm, P.; Asplund, O.; Shcherbina, L.; Fex, M.; Fadista, J.; Tengholm, A.; Wierup, N.; Groop, L.; Mulder, H. Increased melatonin signaling is a risk factor for type 2 diabetes. Cell Metab., 2016, 23(6), 1067-1077.
[http://dx.doi.org/10.1016/j.cmet.2016.04.009] [PMID: 27185156]
[101]
Bonnefond, A.; Clément, N.; Fawcett, K.; Yengo, L.; Vaillant, E.; Guillaume, J.L.; Dechaume, A.; Payne, F.; Roussel, R.; Czernichow, S.; Hercberg, S.; Hadjadj, S.; Balkau, B.; Marre, M.; Lantieri, O.; Langenberg, C.; Bouatia-Naji, N.; Charpentier, G.; Vaxillaire, M.; Rocheleau, G.; Wareham, N.J.; Sladek, R.; McCarthy, M.I.; Dina, C.; Barroso, I.; Jockers, R.; Froguel, P. Meta-Analysis of Glucose and Insulin-Related Traits Consortium (MAGIC). Rare MTNR1B variants impairing melatonin receptor 1B function contribute to type 2 diabetes. Nat. Genet., 2012, 44(3), 297-301.
[http://dx.doi.org/10.1038/ng.1053] [PMID: 22286214]
[102]
Kawahito, S.; Kitahata, H.; Oshita, S. Problems associated with glucose toxicity: role of hyperglycemia-induced oxidative stress. World J. Gastroenterol., 2009, 15(33), 4137-4142.
[http://dx.doi.org/10.3748/wjg.15.4137] [PMID: 19725147]
[103]
Evans, J.L.; Goldfine, I.D.; Maddux, B.A.; Grodsky, G.M. Are oxidative stress-activated signaling pathways mediators of insulin resistance and β-cell dysfunction? Diabetes, 2003, 52(1), 1-8.
[http://dx.doi.org/10.2337/diabetes.52.1.1] [PMID: 12502486]
[104]
Tiedge, M.; Lortz, S.; Drinkgern, J.; Lenzen, S. Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes, 1997, 46(11), 1733-1742.
[http://dx.doi.org/10.2337/diab.46.11.1733] [PMID: 9356019]
[105]
Bojunga, J.; Dresar-Mayert, B.; Usadel, K.H.; Kusterer, K.; Zeuzem, S. Antioxidative treatment reverses imbalances of nitric oxide synthase isoform expression and attenuates tissue-cGMP activation in diabetic rats. Biochem. Biophys. Res. Commun., 2004, 316(3), 771-780.
[http://dx.doi.org/10.1016/j.bbrc.2004.02.110] [PMID: 15033467]
[106]
Reiter, R.J. Melatonin: lowering the high price of free radicals. News Physiol. Sci., 2000, 15, 246-250.
[http://dx.doi.org/10.1152/physiologyonline.2000.15.5.246] [PMID: 11390919]
[107]
Anwar, M.M.; Meki, A.R.M. Oxidative stress in streptozotocin-induced diabetic rats: effects of garlic oil and melatonin. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 2003, 135(4), 539-547.
[http://dx.doi.org/10.1016/S1095-6433(03)00114-4] [PMID: 12890544]
[108]
Derlacz, R.A.; Poplawski, P.; Napierala, M.; Jagielski, A.K.; Bryla, J. Melatonin-induced modulation of glucose metabolism in primary cultures of rabbit kidney-cortex tubules. J. Pineal Res., 2005, 38(3), 164-169.
[http://dx.doi.org/10.1111/j.1600-079X.2004.00188.x] [PMID: 15725337]
[109]
Brömme, H.J.; Ebelt, H.; Peschke, D.; Peschke, E. Alloxan acts as a prooxidant only under reducing conditions: influence of melatonin. Cell. Mol. Life Sci., 1999, 55(3), 487-493.
[http://dx.doi.org/10.1007/s000180050305] [PMID: 10228562]
[110]
Stetinová, V.; Smetanová, L.; Grossmann, V.; Anzenbacher, P. In vitro and in vivo assessment of the antioxidant activity of melatonin and related indole derivatives. Gen. Physiol. Biophys., 2002, 21(2), 153-162.
[PMID: 12236544]
[111]
Winiarska, K.; Fraczyk, T.; Malinska, D.; Drozak, J.; Bryla, J. Melatonin attenuates diabetes-induced oxidative stress in rabbits. J. Pineal Res., 2006, 40(2), 168-176.
[http://dx.doi.org/10.1111/j.1600-079X.2005.00295.x] [PMID: 16441554]
[112]
Peschke, E.; Ebelt, H.; Brömme, H.J.; Peschke, D. ‘Classical’ and ‘new’ diabetogens--comparison of their effects on isolated rat pancreatic islets in vitro. Cell. Mol. Life Sci., 2000, 57(1), 158-164.
[http://dx.doi.org/10.1007/s000180050505] [PMID: 10949587]
[113]
Ebelt, H.; Peschke, D.; Brömme, H.J.; Mörke, W.; Blume, R.; Peschke, E. Influence of melatonin on free radical-induced changes in rat pancreatic beta-cells in vitro. J. Pineal Res., 2000, 28(2), 65-72.
[http://dx.doi.org/10.1034/j.1600-079X.2001.280201.x] [PMID: 10709967]
[114]
Brömme, H.J.; Mörke, W.; Peschke, D.; Ebelt, H.; Peschke, D. Scavenging effect of melatonin on hydroxyl radicals generated by alloxan. J. Pineal Res., 2000, 29(4), 201-208.
[http://dx.doi.org/10.1034/j.1600-0633.2002.290402.x] [PMID: 11068942]
[115]
Sailaja Devi, M.M.; Suresh, Y.; Das, U.N. Preservation of the antioxidant status in chemically-induced diabetes mellitus by melatonin. J. Pineal Res., 2000, 29(2), 108-115.
[http://dx.doi.org/10.1034/j.1600-079X.2000.290207.x] [PMID: 10981824]
[116]
Murata, M.; Takahashi, A.; Saito, I.; Kawanishi, S. Site-specific DNA methylation and apoptosis: induction by diabetogenic streptozotocin. Biochem. Pharmacol., 1999, 57(8), 881-887.
[http://dx.doi.org/10.1016/S0006-2952(98)00370-0] [PMID: 10086321]
[117]
Takasu, N.; Komiya, I.; Asawa, T.; Nagasawa, Y.; Yamada, T. Streptozocin- and alloxan-induced H2O2 generation and DNA fragmentation in pancreatic islets. H2O2 as mediator for DNA fragmentation. Diabetes, 1991, 40(9), 1141-1145.
[http://dx.doi.org/10.2337/diab.40.9.1141] [PMID: 1834504]
[118]
Rao, V.S.; Santos, F.A.; Silva, R.M.; Teixiera, M.G. Effects of nitric oxide synthase inhibitors and melatonin on the hyperglycemic response to streptozotocin in rats. Vascul. Pharmacol., 2002, 38(3), 127-130.
[http://dx.doi.org/10.1016/S1537-1891(02)00212-4] [PMID: 12402510]
[119]
Aksoy, N.; Vural, H.; Sabuncu, T.; Aksoy, S. Effects of melatonin on oxidative-antioxidative status of tissues in streptozotocin-induced diabetic rats. Cell Biochem. Funct., 2003, 21(2), 121-125.
[http://dx.doi.org/10.1002/cbf.1006] [PMID: 12736900]
[120]
Montilla, P.L.; Vargas, J.F.; Túnez, I.F.; Muñoz de Agueda, M.C.; Valdelvira, M.E.; Cabrera, E.S. Oxidative stress in diabetic rats induced by streptozotocin: protective effects of melatonin. J. Pineal Res., 1998, 25(2), 94-100.
[http://dx.doi.org/10.1111/j.1600-079X.1998.tb00545.x] [PMID: 9755030]
[121]
Armagan, A.; Uz, E.; Yilmaz, H.R.; Soyupek, S.; Oksay, T.; Ozcelik, N. Effects of melatonin on lipid peroxidation and antioxidant enzymes in streptozotocin-induced diabetic rat testis. Asian J. Androl., 2006, 8(5), 595-600.
[http://dx.doi.org/10.1111/j.1745-7262.2006.00177.x] [PMID: 16752005]
[122]
Baydas, G.; Canatan, H.; Turkoglu, A. Comparative analysis of the protective effects of melatonin and vitamin E on streptozocin-induced diabetes mellitus. J. Pineal Res., 2002, 32(4), 225-230.
[http://dx.doi.org/10.1034/j.1600-079X.2002.01856.x] [PMID: 11982791]
[123]
Abdel-Wahab, M.H.; Abd-Allah, A.R. Possible protective effect of melatonin and/or desferrioxamine against streptozotocin-induced hyperglycaemia in mice. Pharmacol. Res., 2000, 41(5), 533-537.
[http://dx.doi.org/10.1006/phrs.1999.0614] [PMID: 10753552]
[124]
Sudnikovich, E.J.; Maksimchik, Y.Z.; Zabrodskaya, S.V.; Kubyshin, V.L.; Lapshina, E.A.; Bryszewska, M.; Reiter, R.J.; Zavodnik, I.B. Melatonin attenuates metabolic disorders due to streptozotocin-induced diabetes in rats. Eur. J. Pharmacol., 2007, 569(3), 180-187.
[http://dx.doi.org/10.1016/j.ejphar.2007.05.018] [PMID: 17597602]
[125]
Blanco, S.; Hernández, R.; Franchelli, G.; Ramos-Álvarez, M.M.; Peinado, M.A. Melatonin influences NO/NOS pathway and reduces oxidative and nitrosative stress in a model of hypoxic-ischemic brain damage. Nitric Oxide, 2017, 62, 32-43.
[http://dx.doi.org/10.1016/j.niox.2016.12.001] [PMID: 27940344]
[126]
Andersson, A.K.; Sandler, S. Melatonin protects against streptozotocin, but not interleukin-1beta-induced damage of rodent pancreatic beta-cells. J. Pineal Res., 2001, 30(3), 157-165.
[http://dx.doi.org/10.1034/j.1600-079X.2001.300304.x] [PMID: 11316326]

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