Effects of metformin on inflammation and short-term memory in streptozotocin-induced diabetic mice

Brain Research

Volumn 1644, Issue , 2016, Pages 149-160

  De Oliveira, Wilma Helena ^a,b   De Santana Nunes, Ana Karolina ^a   De França, Maria Eduarda Rocha ^a,b   Dos Santos, Laise Aline ^a   Lós, Deniele Bezerra ^a,b   Rocha, Sura Wanessa Santos ^a   De Sousa Barbosa, Karla Patrícia ^b   Rodrigues, Gabriel Barros ^a,b   Peixoto, Christina Alves ^a  

^a Cidade Universitria   (Brazil)

^b FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

Author keywords

Diabetic brain; Diabetic encephalopathy; Impairment cognitive; Type 1 diabetes

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; FOX 1 PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; I KAPPA B ALPHA; IBA 1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; METFORMIN; NEURON SPECIFIC NUCLEAR PROTEIN; PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; ANTIDIABETIC AGENT; GLUCOSE BLOOD LEVEL; I KAPPA B KINASE ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN-1BETA (163-171); NOS3 PROTEIN, MOUSE; PEPTIDE FRAGMENT; STREPTOZOCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN LEVEL; CELL ACTIVATION; CELL LOSS; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DOSE RESPONSE; DRUG DOSE COMPARISON; ENZYME PHOSPHORYLATION; GLIA CELL; GLIOSIS; HIPPOCAMPUS; IN VIVO STUDY; MALE; MICROGLIA; MOUSE; NERVE CELL NECROSIS; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHORT TERM MEMORY; SIGNAL TRANSDUCTION; SPATIAL MEMORY; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; T-MAZE TEST; TREATMENT OUTCOME; ANIMAL; C57BL MOUSE; COMPLICATION; DRUG EFFECTS; ENCEPHALITIS; EXPERIMENTAL DIABETES MELLITUS; GLUCOSE BLOOD LEVEL; METABOLISM; NERVE CELL; PATHOLOGY; PSYCHOLOGY;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; APOPTOSIS; ASTROCYTES; BLOOD GLUCOSE; DIABETES MELLITUS, EXPERIMENTAL; ENCEPHALITIS; HIPPOCAMPUS; HYPOGLYCEMIC AGENTS; INTERLEUKIN-1BETA; MALE; MEMORY, SHORT-TERM; METFORMIN; MICE; MICE, INBRED C57BL; MICROGLIA; NEURONS; NF-KAPPAB INHIBITOR ALPHA; NITRIC OXIDE SYNTHASE TYPE III; PEPTIDE FRAGMENTS; STREPTOZOCIN;

EID: 84969716580     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2016.05.013     Document Type: Article

References (71)

1. K.V. Allen, B.M. Frier, and M.W.J. Strachan The relationship between type 2 diabetes and cognitive dysfunction: Longitudinal studies and their methodological limitations Eur. J. Pharmacol. 490 2004 169 175 10.1016/j.ejphar.2004.02.054
2. E.O. Alvarez, J. Beauquis, Y. Revsin, and et al. Cognitive dysfunction and hippocampal changes in experimental type 1 diabetes Behav. Brain Res. 198 2009 224 230 10.1016/j.bbr.2008.11.001
3. S. Amato, and H. Man Bioenergy sensing in the brain: the role of AMP-activated protein kinase in neuronal metabolism, development and neurological diseases Cell Cycle 10 2011 3452 3460 10.4161/cc.10.20.17953
4. S.E. Arnold, I. Lucki, B.R. Brookshire, and et al. High fat diet produces brain insulin resistance, synaptodendritic abnormalities and altered behavior in mice Neurobiol. Dis. 67 2014 79 87 10.1016/j.nbd.2014.03.011
5. J. Beauquis, F. Saravia, J. Coulaud, and et al. Prominently decreased hippocampal neurogenesis in a spontaneous model of type 1 diabetes, the nonobese diabetic mouse Exp. Neurol. 210 2008 359 367 10.1016/j.expneurol.2007.11.009
6. J. Beauquis, P. Roig, A.F. De Nicola, and F. Saravia Short-term environmental enrichment enhances adult neurogenesis, vascular network and dendritic complexity in the hippocampus of type 1 diabetic mice PLoS One 5 2010 e13993 10.1371/journal.pone.0013993
7. P. Bhutada, Y. Mundhada, K. Bansod, S. Tawari, S. Patil, P. Dixit, S. Umathe, and D. Mundhada Protection of cholinergic and antioxidant system contributes to the effect of berberine ameliorating memory dysfunction in rat model of streptozotocin-induced diabetes Behav. Brain Res. 220 2011 30 41 10.1016/j.bbr.2011.01.022
8. M. Brownlee Biochemistry and molecular cell biology of diabetic complications Nature 414 2001 813 820 10.1038/414813a
9. N.C. Chilelli, S. Burlina, and A. Lapolla AGEs, rather than hyperglycemia, are responsible for microvascular complications in diabetes: A "glycoxidation-centric" point of view Nutr. Metab. Cardiovasc. Dis. 23 2013 913 919 10.1016/j.numecd.2013.04.004
10. B.H. Chung, J.D. Kim, C.K. Kim, and et al. Icariin stimulates angiogenesis by activating the MEK/ERK- and PI3K/Akt/eNOS-dependent signal pathways in human endothelial cells Biochem. Biophys. Res. Commun. 376 2008 404 408 10.1016/j.bbrc.2008.09.001
11. B.-H. Chung, J.J. Lee, J.-D. Kim, and et al. Angiogenic activity of sesamin through the activation of multiple signal pathways Biochem. Biophys. Res. Commun. 391 2010 254 260 10.1016/j.bbrc.2009.11.045
12. A.M. Colangelo, L. Alberghina, and M. Papa Astrogliosis as a therapeutic target for neurodegenerative diseases Neurosci. Lett. 2014 1 6 10.1016/j.neulet.2014.01.014
13. Correia, S.; Carvalho, C.; Santos, M.S.; Seiça, R.; Oliveira, C.R.; Moreira, P.I.; 2008. Mechanisms of Action of Metformin in Type 2 Diabetes and Associated Complications: An Overview. Mini-Reviews Med. Chem. 8, 1343-1354, http://dx.doi.org/1389-5575/08 $55.00+.00
14. B.J. Davis, Z. Xie, B. Viollet, and M. Zou Drug metformin stimulates nitric oxide synthesis in vivo and endothelial nitric oxide synthase Diabetes 55 2006 496 505
15. M.A.R. Dent, E. Segura-Anaya, J. Alva-Medina, and A. Aranda-Anzaldo NeuN/Fox-3 is an intrinsic component of the neuronal nuclear matrix FEBS Lett. 584 2010 2767 2771 10.1016/j.febslet.2010.04.073
16. S.T. Dheen, C. Kaur, and E.-A. Ling Microglial activation and its implications in the brain diseases Curr. Med Chem. 14 2007 1189 1197
17. S. Dimmeler, E. Dernbach, and A.M. Zeiher Phosphorylation of the endothelial nitric oxide synthase at Ser-1177 is required for VEGF-induced endothelial cell migration FEBS Lett. 477 2000 258 262 10.1016/S0014-5793(00)01657-4
18. J.M.N. Duarte, P.M. Agostinho, R.A. Carvalho, and R.A. Cunha Caffeine consumption prevents diabetes-induced memory impairment and synaptotoxicity in the hippocampus of NONcZNO10/LTJ mice PLoS One 7 2012 e21899 10.1371/journal.pone.0021899
19. C. Ersoy, S. Kiyici, F. Budak, and et al. The effect of metformin treatment on VEGF and PAI-1 levels in obese type 2 diabetic patients Diabetes Res. Clin. Pract. 81 2008 56 60 10.1016/j.diabres.2008.02.006
20. J.L. Evans, I.D. Goldfine, B.A. Maddux, and G.M. Grodsky Are Oxidative Stress Activated Signaling Pathways Mediators of Insulin Resistance and B-Cell Dysfunction? Diabetes 52 2003 1 8
21. S. Fischer, M. Wobben, H.H. Marti, and et al. Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in the expression of zonula occludens-1 Microvasc. Res. 63 2002 70 80 10.1006/mvre.2001.2367
22. G.J. Francis, J.a Martinez, W.Q. Liu, K. Xu, A. Ayer, J. Fine, U.I. Tuor, G. Glazner, L.R. Hanson, W.H. Frey, and C. Toth Intranasal insulin prevents cognitive decline, cerebral atrophy and white matter changes in murine type I diabetic encephalopathy Brain 131 2008 3311-34 10.1093/brain/awn288
23. S. Ge, L. Song, and J.S. Pachter Where is the blood-brain barrier? really? J. Neurosci. Res. 79 2005 421 427 10.1002/jnr.20313
24. Goldin, A.; Beckman, J. a, Schmidt, A.M.; Creager, M.A.; 2006. Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation 114, 597-605, http://dx.doi.org/10.1161/CIRCULATIONAHA.106.621854
25. M.O. Goodarzi Comment on Moore et al. Increased risk of cognitive impairment in patients with diabetes is associated with metformin. Diabetes care 2013;36:2981-2987 Diabetes Care 37 2014 e150 10.2337/dc13-2473
26. Y. Han, C. Jiang, J. Tang, and et al. Resveratrol reduces morphine tolerance by inhibiting microglial activation via AMPK signalling Eur. J. Pain. 18 2014 1458 1470 10.1002/ejp.511
27. Haslbeck, K.-M.; Bierhaus, A.; Erwin, S.; Kirchner, A.; Nawroth, P.; Schlötzer, U.; Neundörfer, B.; Heuss, D.; 2004. Receptor for advanced glycation endproduct (RAGE)-mediated nuclear factor-kappaB activation in vasculitic neuropathy. Muscle Nerve 29, 853-60, http://dx.doi.org/10.1002/mus.20039
28. M.S. Hayden, and S. Ghosh Shared principles in NF-kappaB signaling Cell 132 2008 344 362 10.1016/j.cell.2008.01.020
29. J.P. Hernández-Fonseca, J. Rincón, A. Pedreañez, and et al. Structural and ultrastructural analysis of cerebral cortex, cerebellum, and hypothalamus from diabetic rats Exp. Diabetes Res. 2009 2009 329632 10.1155/2009/329632
30. International Diabetes Federation (IDF).; 2015. IDF Diabetes Atlas 7th edition. idf.org.; http://dx.doi.org/10.1289/image.ehp.v119.i03
31. F. Islam, M. Ejaz Ahmed, M.M. Khan, and et al. Amelioration of cognitive impairment and neurodegeneration by catechin hydrate in rat model of streptozotocin-induced experimental dementia of Alzheimer's type Neurochem Int. 62 2013 492 501 10.1016/j.neuint.2013.02.006
32. Y.-H. Jing, K.-H. Chen, P.-C. Kuo, and et al. Neurodegeneration in streptozotocin-induced diabetic rats is attenuated by treatment with resveratrol Neuroendocrinology 98 2013 116 127 10.1159/000350435
33. C.G. Jolivalt, C.A. Lee, K.K. Beiswenger, and et al. Defective insulin signaling pathway and increased glycogen synthase kinase-3 activity in the brain of diabetic mice: parallels with Alzheimer's disease and correction by insulin J. Neurosci. Res. 86 2008 3265 3274 10.1002/jnr.21787
34. C.G. Jolivalt, R. Hurford, C.A. Lee, and et al. Type 1 diabetes exaggerates features of Alzheimer's disease in APP transgenic mice Exp. Neurol. 223 2010 422 431 10.1016/j.expneurol.2009.11.005
35. A. Kamboj, S. Kumar, and V. Kumar Evaluation of Antidiabetic Activity of Hydroalcoholic Extract of Cestrum nocturnum Leaves in Streptozotocin-Induced Diabetic Rats Adv. Pharmacol. Sci. 2013 2013 150401 10.1155/2013/150401
36. K.K. Kim, R.S. Adelstein, and S. Kawamoto Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors J. Biol. Chem. 284 2009 31052 31061 10.1074/jbc.M109.052969
37. Kowluru, R.A.; Kennedy, A.; 2001. Therapeutic potential of anti-oxidants and diabetic retinopathy. Expert Opin. Investig. Drugs 10, 1665-1676, http://dx.doi.org/10.1517/13543784.10.9.1665
38. Kunisaki, M.; Bursell, S.E.; Clermont, A.C.; Ishii, H.; Ballas, L.M.; Jirousek, M.R.; Umeda, F.; Nawata, H.; King, G.L.; 1995. Vitamin E prevents diabetes-induced abnormal retinal blood flow via the diacylglycerol-protein kinase C pathway. Am. J. Physiol. 269, E239-E246
39. K. Łabuzek, S. Liber, B. Gabryel, and B. Okopień Metformin has adenosine-monophosphate activated protein kinase (AMPK)-independent effects on LPS-stimulated rat primary microglial cultures Pharmacol. Rep. 62 2010 827 848
40. Majithiya, J.B.; Balaraman, R.; 2006. Metformin reduces blood pressure and restores endothelial function in aorta of streptozotocin-induced diabetic rats. Life Sci. 78, 2615-24, http://dx.doi.org/10.1016/j.lfs.2005.10.020
41. A.D. McNeilly, R. Williamson, D.J.K. Balfour, and et al. A high-fat-diet-induced cognitive deficit in rats that is not prevented by improving insulin sensitivity with metformin Diabetologia 55 2012 3061 3070 10.1007/s00125-012-2686-y
42. Mello, S.; 2012. Correlação entre Hiperglicemia e Células do SNC, com Enfoque na Atividade Glial. Rev Neurocienc 20, 294-301
43. E.M. Moore, A.G. Mander, D. Ames, and et al. Increased risk of cognitive impairment in patients with diabetes is associated with metformin Diabetes Care 36 2013 2981 2987 10.2337/dc13-0229
44. Myint, K.-M.; Yamamoto, Y.; Doi, T.; Kato, I.; Harashima, A.; Yonekura, H.; Watanabe, T.; Shinohara, H.; Takeuchi, M.; Tsuneyama, K.; Hashimoto, N.; Asano, M.; Takasawa, S.; Okamoto, H.; Yamamoto, H.; 2006. RAGE control of diabetic nephropathy in a mouse model: effects of RAGE gene disruption and administration of low-molecular weight heparin. Diabetes 55, 2510-22, http://dx.doi.org/10.2337/db06-0221
45. Nagayach, A.; Patro, N.; Patro, I.; 2014. Astrocytic and microglial response in experimentally induced diabetic rat brain. Metab. Brain Dis.; http://dx.doi.org/10.1007/s11011-014-9562-z
46. Nardin, P.; Tramontina, F.; Leite, M.C.; Tramontina, A.C.; Quincozes-Santos, A.; de Almeida, L.M.V.; Battastini, A.M.; Gottfried, C.; Gonçalves, C.-A.; 2007. S100B content and secretion decrease in astrocytes cultured in high-glucose medium. Neurochem. Int. 50, 774-82, http://dx.doi.org/10.1016/j.neuint.2007.01.013
47. N. Nath, M. Khan, M.K. Paintlia, and et al. Metformin attenuated the autoimmune disease of the central nervous system in animal models of multiple sclerosis J. Immunol. 182 2009 8005 8014 10.4049/jimmunol.0803563
48. Niiya, Y.; Abumiya, T.; Shichinohe, H.; Kuroda, S.; Kikuchi, S.; Ieko, M.; Yamagishi, S.; Takeuchi, M.; Sato, T.; Iwasaki, Y.; 2006. Susceptibility of brain microvascular endothelial cells to advanced glycation end products-induced tissue factor upregulation is associated with intracellular reactive oxygen species. Brain Res. 1108, 179-87, http://dx.doi.org/10.1016/j.brainres.2006.06.038
49. Niiya, Y.; Abumiya, T.; Yamagishi, S.; Takino, J.; Takeuchi, M.; 2012. Advanced glycation end products increase permeability of brain microvascular endothelial cells through reactive oxygen species-induced vascular endothelial growth factor expression. J. Stroke Cerebrovasc. Dis. 21, 293-298, http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2010.09.002
50. T. Nishikawa, D. Edelstein, X.L. Du, and et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage Nature 404 2000 787 790 10.1038/35008121
51. A.R. Pathan, B. Viswanad, S.K. Sonkusare, and P. Ramarao Chronic administration of pioglitazone attenuates intracerebroventricular streptozotocin induced-memory impairment in rats Life Sci. 79 2006 2209 2216 10.1016/j.lfs.2006.07.018
52. C. Patrone, O. Eriksson, and D. Lindholm Diabetes drugs and neurological disorders: new views and therapeutic possibilities Lancet Diabetes Endocrinol. 2 2014 256 262 10.1016/S2213-8587(13)70125-6
53. P. Piccioli, and A. Rubartelli The secretion of IL-1β and options for release Semin Immunol. 25 2013 425 429 10.1016/j.smim.2013.10.007
54. H. Pintana, N. Apaijai, W. Pratchayasakul, and et al. Effects of metformin on learning and memory behaviors and brain mitochondrial functions in high fat diet induced insulin resistant rats Life Sci. 91 2012 409 414 10.1016/j.lfs.2012.08.017
55. K. Plaschke, and J. Kopitz In vitro streptozotocin model for modeling Alzheimer-like changes: effect on amyloid precursor protein secretases and glycogen synthase kinase-3 J. Neural Transm. 2014 551 557 10.1007/s00702-014-1319-7
56. W.B. Potter, K.J. O'Riordan, D. Barnett, and et al. Metabolic regulation of neuronal plasticity by the energy sensor AMPK PLoS One 2010 10.1371/journal.pone.0008996
57. M.B. Potts, and D.A. Lim An old drug for new ideas: metformin promotes adult neurogenesis and spatial memory formation Cell Stem Cell 11 2012 5 6 10.1016/j.stem.2012.06.003
58. Y. Revsin, F. Saravia, P. Roig, and et al. Neuronal and astroglial alterations in the hippocampus of a mouse model for type 1 diabetes Brain Res. 1038 2005 22 31 10.1016/j.brainres.2004.12.032
59. A. Salminen, K. Kaarniranta, A. Haapasalo, and et al. AMP-activated protein kinase: a potential player in Alzheimer's disease J. Neurochem 118 2011 460 474 10.1111/j.1471-4159.2011.07331.x
60. Augusto Cézar Santomauro Junior, Michelle Remião Ugolini, Ana Tereza Santomauro, and Ricardo Peres do Souto Metformina e AMPK: um antigo fármaco e uma nova enzima no contexto da síndrome metabólica Arq. Bras. Endocrinol. 52 2008 120 125
61. S. Sharma, S. Rakoczy, and H. Brown-Borg Assessment of spatial memory in mice Life Sci. 87 2010 521 536 10.1016/j.lfs.2010.09.004
62. A.A.F. Sima, and Z. Li The effect of C-peptide on cognitive dysfunction and hippocampal apoptosis in type 1 diabetic rats Diabetes 54 2005 1497 1505
63. A.A.F. Sima, W. Zhang, C.W. Kreipke, and et al. Inflammation in diabetic encephalopathy is prevented by C-peptide Rev. Diabet. Stud. 6 2009 37 42 10.1900/RDS.2009.6.37
64. S. Skovsø Modeling type 2 diabetes in rats using high fat diet and streptozotocin J. Diabetes Invest. 5 2014 349 358 10.1111/jdi.12235
65. M.V. Sofroniew, C.L. Howe, and W.C. Mobley Nerve growth factor signaling, neuroprotection, and neural repair Annu Rev. Neurosci. 24 2001 1217 1281 10.1146/annurev.neuro.24.1.1217
66. Shoji, T.; Koyama, H.; Morioka, T.; Tanaka, S.; Kizu, A.; Motoyama, K.; Mori, K.; Fukumoto, S.; Shioi, A.; Shimogaito, N.; Takeuchi, M.; Yamamoto, Y.; Yonekura, H.; Yamamoto, H.; Nishizawa, Y.; 2006. Receptor for advanced glycation end products is involved in impaired angiogenic response in diabetes. Diabetes 55, 2245-2255, http://dx.doi.org/10.2337/db05-1375
67. Terpstra, A.H.M.; 2001. Issues and Opinions Differences between Humans and Mice in Efficacy of the Body Fat Lowering Effect of Conjugated Linoleic Acid: Role of Metabolic Rate 2067-2068, http://dx.doi.org/0022-3166/01
68. Toth, C.; Schmidt, A.M.; Tuor, U.I.; Francis, G.; Foniok, T.; Brussee, V.; Kaur, J.; Yan, S.F.; Martinez, J.A.; Barber, P.A.; Buchan, A.; Zochodne, D.W.; 2006. Diabetes, leukoencephalopathy and rage. Neurobiol. Dis. 23, 445-461, http://dx.doi.org/10.1016/j.nbd.2006.03.015
69. J. Wang, D. Gallagher, L.M. Devito, and et al. Metformin activates an atypical PKC-CBP pathway to promote neurogenesis and enhance spatial memory formation Cell Stem Cell 11 2012 23 35 10.1016/j.stem.2012.03.016
70. World Health organization.; 2006. Prevetion of blindness from diabetes mellitus: report of WHO consulation in Geneva, Switzerland
71. L. Ye, F. Wang, and R.-H. Yang Diabetes impairs learning performance and affects the mitochondrial function of hippocampal pyramidal neurons Brain Res. 1411 2011 57 64 10.1016/j.brainres.2011.07.011