Isorhamnetin mitigates learning and memory disturbances in streptozotocin-induced diabetic rats

Document Type: Research Paper

Authors

Department of Physiology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran

Abstract

Background and Objective: Diabetes as a metabolic disorder can cause memory and learning impairment. In recent years, the effect of plant extracts on the treatment of diabetes mellitus has been raised. The purpose of this study was to determine the effect of isorhmnetin administration on learning and memory disability in an experimental model of streptozotocin-induced diabetes mellitus in rats.
Materials and Methods: In the present study, for inducing diabetes, streptozotocin was administered at a dose of 60 mg/kg (intraperitoneal) in
male rats. Intraperitoneal injection of isorhmnetin (10 mg/kg) was performed after induction of diabetes (10 mg/kg) for 12 weeks. Control groups also received relevant doses. Y-maze and passive avoidance tests were used for assessing of learning and memory ability. The serum glucose and body weight were determined before and 12 weeks after diabetic development.
Results: Behavior data showed that compared to control rats, alternation percentage in Y-maze task (p Conclusion: This study reveals that isorhmnetin administration to diabetic rats attenuates learning and memory impairment.

Keywords


1.      Tripathi B, Srivastava A. Diabetes mellitus: complications and therapeutics. Medical Science Monitor 2006; 12(7): RA130-47.

2.      Jackson-Guilford J, Leander J, Nisenbaum L. The effect of streptozotocin-induced diabetes on cell proliferation in the rat dentate gyrus. Neuroscience Letter 2000; 293(2): 91-4.

3.      Biessels G, Smale S, Duis S, Kamal A, Gispen W. The effect of gamma-linolenic acidalpha-lipoic acid on functional deficits in the peripheral and central nervous system of streptozotocin-diabetic rats. Journal of the Neurological Sciences 2001;182(2): 99-106.

4.      Parihar M, Chaudhary M, Shetty R, Hemnani T. Susceptibility of hippocampus and cerebral cortex to oxidative damage in streptozotocin treated mice: prevention by extracts of Withania somnifera and Aloe vera. Journal of Clinical Neuroscience 2004;11(4): 397-402.

5.      Reagan L, McEwen B. Diabetes, but not stress, reduces neuronal nitric oxide synthase expression in rat hippocampus: implications for hippocampal synaptic plasticity. Neuroreport 2002;13(14):1801-4.

6.      Baydas G, Nedzvetskii V, Nerush P, Kirichenko S, Yoldas T. Altered expression of NCAM in hippocampus and cortex may underlie memory and learning deficits in rats with streptozotocin-induced diabetes mellitus. Life Science 2003;73(15):1907-16.

7.      Scartezzini P, Speroni E. Review on some plants of Indian traditional medicine with antioxidant activity. Journal of Ethnopharmacology 2000; 71(1-2): 23-43.

8.      Wiczkowski W, Skipor J, Misztal T, Szawara-Nowak D, Topolska J,Piskula MK. Quercetin and isorhamnetin aglycones are the main metabolites of dietary quercetin in cerebrospinal fluid. Molecular Nutrition & Food Research 2015; 59(6):1088–1094.

9.      Boesch-Saadatmandi C, Egert S, Schrader C, Coumoul X, Barouki R, Muller MJ, et al. Effect of quercetin on paraoxonase 1 activity—studies in cultured cells, mice and humans. Journal of Physiology and Pharmacology 2010; 61(1): 99–105.

10.  Park JC, Young HS, Yu YB, Lee JH. Isorhamnetin sulphate from the leaves and stems of Oenanthe javanica in Korea. Planta Medica 1995; 61:377–378.

11.  Sun B, Sun GB, Xiao J, Chen RC, Wang X, Wu Y, et al. Isorhamnetin inhibits H2O2-induced activation of the intrinsic apoptotic pathway in H9c2 cardiomyocytes through scavenging reactive oxygen species and ERK inactivation. Journal of Cellular Biochemistry 2012; 113(2): 473–485.

12.  Li W, Chen Z, Yan M, He P, Chen Z, Dai H.The protective role of isorhamnetin on human brain microvascular endothelial cells from cytotoxicity induced by methylglyoxal and oxygen glucose deprivation. Journal of Neurochemistry 2016; 136(3): 651–659.

13.  Dou W, Zhang J, Li H, Kortagere S, Sun K, Di-ng L, et al. Plant flavonol isorhamnetin attenuates chemically induced inflammatory bowel disease via a PXR-depen­dent pathway. Journal of Nutritional Biochemistry 2014; 25(9): 923-933.

14.  Chirumbolo S. Anti-inflammatory action of isorhamnetin. Inflammation 2014; 37(4): 1200-1201.

15.  Seo K, Yang JH, Kim SC, Ku SK, Ki SH, Shin SM. The antioxidant effects of isorhamnetin contribute to inhibit COX-2 expression in re­sponse to inflammation: a potential role of HO-1. Inflammation 2014; 37: 712-722.

16.  Sun B, Sun GB, Xiao J, Chen RC, Wang X, Wu Y, et al. Isorhamnetin inhibits H2O2-induced activation of the intrinsic apop­totic pathway in H9c2 cardiomyocytes through scavenging reactive oxygen species and ERK inactivation. Journal of Cellular Biochemistry 2012; 113: 473-485.

17.  Lupien SB, Bluhm EJ, Ishii DN. Systemic insulin-like growth factor-I administration prevents cognitive impairment in diabetic rats, and brain IGF regulates learning/memory in normal adult rats. Journal of Neuroscience Research 2003; 74: 512-523.

18.  Biessels GJ, ter Laak MP, Kamal A, Gispen WH Effects of the Ca2+ antagonist nimodipine on functional deficits in the peripheral and central nervous system of streptozotocin-diabetic rats. Brain Research 2005; 1035:86-93

19.  Nitta A, Murai R, Suzuki N, Ito H, Nomoto H, Katoh G, Furukawa Y, et al. Diabetic neuropathies in brain are induced by deficiency of BDNF. Neurotoxicology Teratology 2002; 24: 695-701.

20.  Mayer G, Nitsch R, Hoyer S. Effects of changes in peripheral and cerebral glucose metabolism on locomotor activity, learning and memory in adult male rats. Brain Research 1990; 532:95-100.

21.  Artola A, Kamal A, Ramakers GM, Biessels GJ, Gispen WH. Diabetes mellitus concomitantly facilitates the induction of long-term depression and inhibits that of long-term potentiation in hippocampus. European Journal of Neuroscience 2005; 22: 169-178.

22.  Sima AA, Li ZG. The effect of C-peptide on cognitive dysfunction and hippocampal apoptosis in type 1 diabetic rats. Diabetes 2005; 54:1497-1505.

23.  Rodrigo R, Ferna´ndez-Gajardo R, Gutie´rrez R, Matamala JM, Carrasco R, Miranda-Merchak A, et al. Oxidative stress and pathophysiology of ischemic stroke: novel therapeutic opportunities. CNS Neurology Disorder Drug Targets 2013; 12: 698–714

24.  Yang JH, Shin BY, Han JY, Kim MG, Wi JE, Kim YW, et al. Isorhamnetin protects against oxidative stress by activating Nrf2 and inducing the expression of its target genes. Toxicology and Applied Pharmacology 2014; 274(2): 293–301.

25.  Pe´rez-Asensio FJ, Hurtado O, Burguete MC, Moro MA, Salom JB, Lizasoain I, et al. Inhibition of iNOS activity by 1400 W decreases glutamate release and ameliorates stroke outcome after experimental ischemia. Neurobiology Disease 2005; 18(2): 375–384.

26.  Reiter RJ, Tan DX, Manchester LC, Qi W. Biochemical reactivity of melatonin with reactive oxygen and nitrogen species: a review of the evidence. Cell Biochemistry and Biophysics 2001; 34(2): 237–256.

27.  Simats A, Garc─▒´a-Berrocoso T, Montaner J. Neuroinflammatory biomarkers: from stroke diagnosis and prognosis to therapy. Biochimica et Biophysica Acta 2016; 1862(3): 411–424.

28.  Iadecola C, Anrather J. The immunology of stroke: from mechanisms to translation. Nature Medicine 2011; 17(7): 796–808.

29.  Yenari MA, Kunis D, Sun GH, Onley D, Watson L, Turner S, et al. Hu23F2G, an antibody recognizing the leukocyte CD11/CD18 integrin, reduces injury in a rabbit model of transient focal cerebral ischemia. Experimental Neurology 1998; 153(2): 223–233.

30.  Jickling GC, Liu D, Ander BP, Stamova B, Zhan X, Sharp FR. Targeting neutrophils in ischemic stroke: translational insights from experimental studies. Journal of Cerebral Blood Flow and Metabolism 2015; 35(6): 888–901. 

1.      Tripathi B, Srivastava A. Diabetes mellitus: complications and therapeutics. Medical Science Monitor 2006; 12(7): RA130-47.

2.      Jackson-Guilford J, Leander J, Nisenbaum L. The effect of streptozotocin-induced diabetes on cell proliferation in the rat dentate gyrus. Neuroscience Letter 2000; 293(2): 91-4.

3.      Biessels G, Smale S, Duis S, Kamal A, Gispen W. The effect of gamma-linolenic acidalpha-lipoic acid on functional deficits in the peripheral and central nervous system of streptozotocin-diabetic rats. Journal of the Neurological Sciences 2001;182(2): 99-106.

4.      Parihar M, Chaudhary M, Shetty R, Hemnani T. Susceptibility of hippocampus and cerebral cortex to oxidative damage in streptozotocin treated mice: prevention by extracts of Withania somnifera and Aloe vera. Journal of Clinical Neuroscience 2004;11(4): 397-402.

5.      Reagan L, McEwen B. Diabetes, but not stress, reduces neuronal nitric oxide synthase expression in rat hippocampus: implications for hippocampal synaptic plasticity. Neuroreport 2002;13(14):1801-4.

6.      Baydas G, Nedzvetskii V, Nerush P, Kirichenko S, Yoldas T. Altered expression of NCAM in hippocampus and cortex may underlie memory and learning deficits in rats with streptozotocin-induced diabetes mellitus. Life Science 2003;73(15):1907-16.

7.      Scartezzini P, Speroni E. Review on some plants of Indian traditional medicine with antioxidant activity. Journal of Ethnopharmacology 2000; 71(1-2): 23-43.

8.      Wiczkowski W, Skipor J, Misztal T, Szawara-Nowak D, Topolska J,Piskula MK. Quercetin and isorhamnetin aglycones are the main metabolites of dietary quercetin in cerebrospinal fluid. Molecular Nutrition & Food Research 2015; 59(6):1088–1094.

9.      Boesch-Saadatmandi C, Egert S, Schrader C, Coumoul X, Barouki R, Muller MJ, et al. Effect of quercetin on paraoxonase 1 activity—studies in cultured cells, mice and humans. Journal of Physiology and Pharmacology 2010; 61(1): 99–105.

10.  Park JC, Young HS, Yu YB, Lee JH. Isorhamnetin sulphate from the leaves and stems of Oenanthe javanica in Korea. Planta Medica 1995; 61:377–378.

11.  Sun B, Sun GB, Xiao J, Chen RC, Wang X, Wu Y, et al. Isorhamnetin inhibits H2O2-induced activation of the intrinsic apoptotic pathway in H9c2 cardiomyocytes through scavenging reactive oxygen species and ERK inactivation. Journal of Cellular Biochemistry 2012; 113(2): 473–485.

12.  Li W, Chen Z, Yan M, He P, Chen Z, Dai H.The protective role of isorhamnetin on human brain microvascular endothelial cells from cytotoxicity induced by methylglyoxal and oxygen glucose deprivation. Journal of Neurochemistry 2016; 136(3): 651–659.

13.  Dou W, Zhang J, Li H, Kortagere S, Sun K, Di-ng L, et al. Plant flavonol isorhamnetin attenuates chemically induced inflammatory bowel disease via a PXR-depen­dent pathway. Journal of Nutritional Biochemistry 2014; 25(9): 923-933.

14.  Chirumbolo S. Anti-inflammatory action of isorhamnetin. Inflammation 2014; 37(4): 1200-1201.

15.  Seo K, Yang JH, Kim SC, Ku SK, Ki SH, Shin SM. The antioxidant effects of isorhamnetin contribute to inhibit COX-2 expression in re­sponse to inflammation: a potential role of HO-1. Inflammation 2014; 37: 712-722.

16.  Sun B, Sun GB, Xiao J, Chen RC, Wang X, Wu Y, et al. Isorhamnetin inhibits H2O2-induced activation of the intrinsic apop­totic pathway in H9c2 cardiomyocytes through scavenging reactive oxygen species and ERK inactivation. Journal of Cellular Biochemistry 2012; 113: 473-485.

17.  Lupien SB, Bluhm EJ, Ishii DN. Systemic insulin-like growth factor-I administration prevents cognitive impairment in diabetic rats, and brain IGF regulates learning/memory in normal adult rats. Journal of Neuroscience Research 2003; 74: 512-523.

18.  Biessels GJ, ter Laak MP, Kamal A, Gispen WH Effects of the Ca2+ antagonist nimodipine on functional deficits in the peripheral and central nervous system of streptozotocin-diabetic rats. Brain Research 2005; 1035:86-93

19.  Nitta A, Murai R, Suzuki N, Ito H, Nomoto H, Katoh G, Furukawa Y, et al. Diabetic neuropathies in brain are induced by deficiency of BDNF. Neurotoxicology Teratology 2002; 24: 695-701.

20.  Mayer G, Nitsch R, Hoyer S. Effects of changes in peripheral and cerebral glucose metabolism on locomotor activity, learning and memory in adult male rats. Brain Research 1990; 532:95-100.

21.  Artola A, Kamal A, Ramakers GM, Biessels GJ, Gispen WH. Diabetes mellitus concomitantly facilitates the induction of long-term depression and inhibits that of long-term potentiation in hippocampus. European Journal of Neuroscience 2005; 22: 169-178.

22.  Sima AA, Li ZG. The effect of C-peptide on cognitive dysfunction and hippocampal apoptosis in type 1 diabetic rats. Diabetes 2005; 54:1497-1505.

23.  Rodrigo R, Ferna´ndez-Gajardo R, Gutie´rrez R, Matamala JM, Carrasco R, Miranda-Merchak A, et al. Oxidative stress and pathophysiology of ischemic stroke: novel therapeutic opportunities. CNS Neurology Disorder Drug Targets 2013; 12: 698–714

24.  Yang JH, Shin BY, Han JY, Kim MG, Wi JE, Kim YW, et al. Isorhamnetin protects against oxidative stress by activating Nrf2 and inducing the expression of its target genes. Toxicology and Applied Pharmacology 2014; 274(2): 293–301.

25.  Pe´rez-Asensio FJ, Hurtado O, Burguete MC, Moro MA, Salom JB, Lizasoain I, et al. Inhibition of iNOS activity by 1400 W decreases glutamate release and ameliorates stroke outcome after experimental ischemia. Neurobiology Disease 2005; 18(2): 375–384.

26.  Reiter RJ, Tan DX, Manchester LC, Qi W. Biochemical reactivity of melatonin with reactive oxygen and nitrogen species: a review of the evidence. Cell Biochemistry and Biophysics 2001; 34(2): 237–256.

27.  Simats A, Garc─▒´a-Berrocoso T, Montaner J. Neuroinflammatory biomarkers: from stroke diagnosis and prognosis to therapy. Biochimica et Biophysica Acta 2016; 1862(3): 411–424.

28.  Iadecola C, Anrather J. The immunology of stroke: from mechanisms to translation. Nature Medicine 2011; 17(7): 796–808.

29.  Yenari MA, Kunis D, Sun GH, Onley D, Watson L, Turner S, et al. Hu23F2G, an antibody recognizing the leukocyte CD11/CD18 integrin, reduces injury in a rabbit model of transient focal cerebral ischemia. Experimental Neurology 1998; 153(2): 223–233.

30.  Jickling GC, Liu D, Ander BP, Stamova B, Zhan X, Sharp FR. Targeting neutrophils in ischemic stroke: translational insights from experimental studies. Journal of Cerebral Blood Flow and Metabolism 2015; 35(6): 888–901.