Inhibition of inflammation by astaxanthin alleviates cognition deficits in diabetic mice

Physiology and Behavior

Volumn 151, Issue , 2015, Pages 412-420

  Zhou, Xiaoyan ^a   Zhang, Fang ^a   Hu, Xiaotong ^a   Chen, Jing ^a   Wen, Xiangru ^a   Sun, Ying ^a   Liu, Yonghai ^a   Tang, Renxian ^a   Zheng, Kuiyang ^a   Song, Yuanjian ^a  

^a XUZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Astaxanthin; Cognition deficits; Diabetic encephalopathy; Inflammation; Nuclear factor B; Tumor necrosis factor

Indexed keywords

ASTAXANTHIN; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; STREPTOZOCIN; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR ALPHA; GLUCOSE BLOOD LEVEL; XANTHOPHYLL;

ADULT; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL SURVIVAL; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DIABETES MELLITUS; DOWN REGULATION; DRUG EFFECT; FRONTAL CORTEX; GLUCOSE BLOOD LEVEL; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; IMMUNOBLOTTING; INFLAMMATION; INSULIN RESISTANCE; LATENT PERIOD; MALE; MORRIS WATER MAZE TEST; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SPATIAL MEMORY; ANALYSIS OF VARIANCE; ANIMAL; COGNITION DISORDERS; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; FRONTAL LOBE; INSTITUTE FOR CANCER RESEARCH MOUSE; LOCOMOTION; MAZE TEST; METABOLISM; PATHOLOGY; REACTION TIME;

ANALYSIS OF VARIANCE; ANIMALS; BLOOD GLUCOSE; COGNITION DISORDERS; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; FRONTAL LOBE; HIPPOCAMPUS; INFLAMMATION; LOCOMOTION; MALE; MAZE LEARNING; MICE; MICE, INBRED ICR; NF-KAPPA B; REACTION TIME; TUMOR NECROSIS FACTOR-ALPHA; XANTHOPHYLLS;

EID: 84939806378     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2015.08.015     Document Type: Article

References (45)

1. Soares E., Prediger R.D., Nunes S., Castro A.A., Viana S.D., Lemos C., et al. Spatial memory impairments in a prediabetic rat model. Neuroscience 2013, 250(10):565-577.
2. Meng X., Wang X., Tian X., Yang Z., Li M., Zhang C. Protection of neurons from high glucose-induced injury by deletion of MAD2B. J. Cell. Mol. Med. 2014, 18(5):844-851.
3. Sima A.A. Encephalopathies: the emerging diabetic complications. Acta Diabetol. 2010, 47(4):279-293.
4. Abbondante S., Baglietto-Vargas D., Rodriguez-Ortiz C.J., Estrada-Hernandez T., Medeiros R., Laferla F.M. Genetic ablation of tau mitigates cognitive impairment induced by type 1 diabetes. Am. J. Pathol. 2014, 184(3):819-826.
5. Marder T.J., Flores V.L., Bolo N.R., Hoogenboom W.S., Simonson D.C., Jacobson A.M., et al. Task-induced brain activity patterns in type2 diabetes: a potential biomarker for cognitive decline. Diabetes 2014, 63(9):3112-3119.
6. Sandi C., Woodson J.C., Haynes V.F., Park C.R., Touyarot K., Lopez-Fernandez M.A., et al. Acute stress-induced impairment of spatial memory is associated with decreased expression of neural cell adhesion molecule in the hippocampus and frontal cortex. Biol. Psychiatry 2005, 57(8):856-864.
7. Reagan L.P. Diabetes as a chronic metabolic stressor: causes, consequences and clinical complications. Exp. Neurol. 2012, 233(1):68-78.
8. Nijboer C.H., Heijnen C.J., Groenendaal F., Van Bel F., Kavelaars A. Alternate pathways preserve tumor necrosis factor-alpha production after nuclear factor-kappaB inhibition in neonatal cerebral hypoxia-ischemia. Stroke 2009, 40(10):3362-3368.
9. Zhao Z., Huang G., Wang B., Zhong Y. Inhibition of NF-kappaB activation by pyrrolidine dithiocarbamate partially attenuates hippocampal MMP-9 activation and improves cognitive deficits in streptozotocin-induced diabetic rats. Behav. Brain Res. 2013, 238(2):44-47.
10. Shen H., Hu X., Liu C., Wang S., Zhang W., Gao H., et al. Ethyl pyruvate protects against hypoxic-ischemic brain injury via anti-cell death and anti-inflammatory mechanisms. Neurobiol. Dis. 2010, 37(3):711-722.
11. Francis G.J., Martinez J.A., Liu W.Q., Xu K., Ayer A., Fine J., et al. Intranasal insulin prevents cognitive decline, cerebral atrophy and white matter changes in murine type I diabetic encephalopathy. Brain 2008, 131(Pt 12):3311-3314.
12. Ganz M.L., Wintfeld N.S., Li Q., Lee Y.C., Gatt E., Huang J.C. Severe hypoglycemia rates and associated costs among type 2 diabetics starting basal insulin therapy in the United States. Curr. Med. Res. Opin. 2014, 30(10):1991-2000.
13. Ola M.S., Aleisa A.M., Al-Rejaie S.S., Abuohashish H.M., Parmar M.Y., Alhomida A.S., et al. Flavonoid, morin inhibits oxidative stress, inflammation and enhances neurotrophic support in the brain of streptozotocin-induced diabetic rats. Neurol. Sci. 2014, 35(7):1003-1008.
14. Liu L.P., Yan T.H., Jiang L.Y., Hu W., Hu M., Wang C., et al. Pioglitazone ameliorates memory deficits in streptozotocin-induced diabetic mice by reducing brain β-amyloid through PPARγ activation. Acta Pharmacol. Sin. 2013, 34(4):455-463.
15. Kamboj S.S., Sandhir R. Protective effect of N-acetylcysteine supplementation on mitochondrial oxidative stress and mitochondrial enzymes in cerebral cortex of streptozotocin treated diabetic rats. Mitochondrion 2011, 11(1):214-222.
16. Bhutada P., Mundhada Y., Bansod K., Bhutada C., Tawari S., Dixit P., et al. Ameliorative effect of quercetin on memory dysfunction in streptozotocin-induced diabetic rats. Neurobiol. Learn. Mem. 2010, 94(3):293-302.
17. Ambati R.R., Phang S.M., Ravi S., Aswathanarayana R.G. Astaxanthin: sources, extraction, stability, biological activities and its commercial applications a review. Mar. Drugs 2014, 12(1):128-152.
18. Dong L.Y., Jin J., Lu G., Kang X.L. Astaxanthin attenuates the apoptosis of retinal ganglion cells in db/db mice by inhibition of oxidative stress. Mar. Drugs 2013, 11(3):960-974.
19. Speranza L., Pesce M., Patruno A., Franceschelli S., de Lutiis M.A., Grilli A., et al. Astaxanthin treatment reduced oxidative induced pro-inflammatory cytokines secretion in U937: SHP-1 as a novel biological target. Mar. Drugs 2012, 10(4):890-899.
20. Lu Y.P., Liu S.Y., Sun H., Wu X.M., Li J.J., Zhu L. Neuroprotective effect of astaxanthin on H(2)O-(2)-induced neurotoxicity in vitro and on focal cerebral ischemia in vivo. Brain Res. 2010, 1360(11):40-48.
21. Kavitha K., Kowshik J., Kishore T.K., Baba A.B., Nagini S. Astaxanthin inhibits NF-κB and Wnt/β-catenin signaling pathways via inactivation of Erk/MAPK and PI3K/Akt to induce intrinsic apoptosis in a hamster model of oral cancer. Biochim. Biophys. Acta 2013, 1830(10):4433-4444.
22. Park J.S., Mathison B.D., Hayek M.G., Massimino S., Reinhart G.A., Chew B.P. Astaxanthin stimulates cell-mediated and humoral immune responses in cats. Vet. Immunol. Immunopathol. 2011, 144(3-4):455-461.
23. Kim Y.J., Kim Y.A., Yokozawa T. Protection against oxidative stress, inflammation, and apoptosis of high-glucose-exposed proximal tubular epithelial cells by astaxanthin. J. Aqric. Food Chem. 2009, 57(19):8793-8797.
24. Marin D.P., Bolin A.P., Macedo Rde C., Sampaio S.C., Otton R. ROS production in neutrophils from alloxan-induced diabetic rats treated in vivo with astaxanthin. Int. Immunopharmacol. 2011, 11(1):103-109.
25. Kidd P. Astaxanthin, cell membrane nutrient with diverse clinical benefits and anti-aging potential. Altern. Med. Rev. 2011, 16(4):355-364.
26. Mattei R., Polotow T.G., Vardaris C.V., Guerra B.A., Leite J.R., Otton R., et al. Astaxanthin limits fish oil-related oxidative insult in the anterior forebrain of Wistar rats: putative anxiolytic effects?. Pharmacol. Biochem. Behav. 2011, 99(3):349-355.
27. Enhamre-Brolin E., Carlsson A., Hallberg M., Nyberg F. Growth hormone reverses streptozotocin-induced cognitive impairments in male mice. Behav. Brain Res. 2013, 238(2):273-278.
28. Tripathi D.N., Jena G.B. Astaxanthin inhibits cytotoxic and genotoxic effects of cyclophosphamide in mice germ cells. Toxicology 2008, 248(2-3):96-103.
29. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297(5868):681-683.
30. Zamzow D.R., Elias V., Legette L.L., Choi J., Stevens J.F., Magnusson K.R. Xanthohumol improved cognitive flexibility in young mice. Behav. Brain Res. 2014, 275(12):1-10.
31. Sheikhzadeh N., Tayefi-Nasrabadi H., Oushani A.K., Enferadi M.H. Effects of Haematococcus pluvialis supplementation on antioxidant system and metabolism in rainbow trout (Oncorhynchus mykiss). Fish Physiol. Biochem. 2012, 38(2):413-419.
32. Bhuvaneswari S., Yogalakshmi B., Sreeja S., Anuradha C.V. Astaxanthin reduces hepatic endoplasmic reticulum stress and nuclear factor-κB-mediated inflammation in high fructose and high fat diet-fed mice. Cell Stress Chaperones 2014, 19(2):183-191.
33. Ishiki M., Nishida Y., Ishibashi H., Wada T., Fujisaka S., Takikawa A., et al. Impact of divergent effects of astaxanthin on insulin signaling in L6 cells. Endocrinology 2013, 154(8):2600-2612.
34. Idan-Feldman A., Schirer Y., Polyzoidou E., Touloumi O., Lagoudaki R., Grigoria-dis N.C., et al. Davunetide (NAP) as a preventative treatment for central nervous system complications in a diabetes rat model. Neurobiol. Dis. 2011, 44(3):327-339.
35. Van der Kooij M.A., Nijboer C.H., Ohl F., Groenendaal F., Heijnen C.J., Van Bel F., et al. NF-kappaB inhibition after neonatal cerebral hypoxia-ischemia improves long-term motor and cognitive outcome in rats. Neurobiol. Dis. 2010, 38(2):266-272.
36. Tiwari V., Chopra K. Protective effect of curcumin against chronic alcohol-induced cognitive deficits and neuroinflammation in the adult rat brain. Neuroscience 2013, 244(6):147-158.
37. Yu X., Wang L.N., Du Q.M., Ma L., Chen L., You R., et al. Akebia saponin D attenuates amyloid β-induced cognitive deficits and inflammatory response in rats: involvement of Akt/NF-κB pathway. Behav. Brain Res. 2012, 235(2):200-209.
38. Preuss H.G., Echard B., Yamashita E., Perricone N.V. High dose astaxanthin lowers blood pressure and increases insulin sensitivity in rats: are these effects interdependent?. Int. J. Med. Sci. 2011, 8(2):126-138.
39. Duarte J.M., Nogueira C., Mackie K., Oliveira C.R., Cunha R.A., Köfalvi A. Increase of cannabinoid CB1 receptor density in the hippocampus of streptozotocin otocin induced diabetic rats. Exp. Neurol. 2007, 204(1):479-484.
40. Watanabe K., Funahashi S. Neural mechanisms of dual-task interference and cognitive capacity limitation in the prefrontal cortex. Nat. Neurosci. 2014, 17(4):601-611.
41. Ho N., Sommers M.S., Lucki I. Effects of diabetes on hippocampal neurogenesis: links to cognition and depression. Neurosci. Biobehav. Rev. 2013, 37(8):1346-1362.
42. Deng W., Lu H., Teng J. Carvacrol attenuates diabetes-associated cognitive deficits in rats. J. Mol. Neurosci. 2013, 51(3):813-819.
43. Kuhad A., Bishnoi M., Tiwari V., Chopra K. Suppression of NF-kappabeta signaling pathway by tocotrienol can prevent diabetes associated cognitive deficits. Pharmacol. Biochem. Behav. 2009, 92(2):251-259.
44. Lu J., Wu D.M., Zheng Y.L., Hu B., Cheng W., Zhang Z.F., et al. Ursolic acid improves high fat diet-induced cognitive impairments by blocking endoplasmic reticulum stress and IκB kinase β/nuclear factor-κB-mediated inflammatory pathways in mice. Brain Behav. Immun. 2011, 25(8):1658-1667.
45. Sima A.A., Zhang W., Kreipke C.W., Rafols J.A., Hoffman W.H. Inflammation in diabetic encephalopathy is prevented by C-peptide. Rev. Diabet. Stud. 2009, 6(1):37-42.