Intranasal insulin improves cerebral blood flow, Nrf-2 expression and BDNF in STZ (ICV)-induced memory impaired rats

Life Sciences

Volumn 173, Issue , 2017, Pages 1-10

  Rajasekar, N ^a,b   Nath, Chandishwar ^a,b   Hanif, Kashif ^a,b   Shukla, Rakesh ^a,b  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

^b ACADEMY OF SCIENTIFIC AND INNOVATIVE RESEARCH ACSIR   (India)

Author keywords

Acetylcholinesterase; Cerebral blood flow; CREB activation; Insulin; Oxidative stress

Indexed keywords

ADENOSINE TRIPHOSPHATE; BRAIN DERIVED NEUROTROPHIC FACTOR; GLUTATHIONE; INDUCIBLE NITRIC OXIDE SYNTHASE; INSULIN; MALONALDEHYDE; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; BUNGAROTOXIN RECEPTOR; NFE2L2 PROTEIN, RAT; STREPTOZOCIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN CORTEX; BRAIN MITOCHONDRION; CONTROLLED STUDY; ENZYME ACTIVITY; EXPERIMENTAL COGNITIVE DEFECT; HIPPOCAMPUS; LASER DOPPLER FLOWMETRY; MALE; MEMORY; MEMORY ASSESSMENT; MORRIS WATER MAZE TEST; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; STREPTOZOTOCIN INDUCED MEMORY IMPAIRMENT; ANIMAL; BIOSYNTHESIS; BLOOD FLOW VELOCITY; BRAIN CIRCULATION; CHEMICALLY INDUCED; DRUG EFFECTS; GENE EXPRESSION REGULATION; INTRANASAL DRUG ADMINISTRATION; MAZE TEST; MEMORY DISORDER; METABOLISM; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT; VASCULARIZATION;

ADMINISTRATION, INTRANASAL; ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; BLOOD FLOW VELOCITY; BRAIN-DERIVED NEUROTROPHIC FACTOR; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; GENE EXPRESSION REGULATION; HIPPOCAMPUS; INSULIN; MALE; MAZE LEARNING; MEMORY DISORDERS; NF-E2-RELATED FACTOR 2; RATS; RATS, SPRAGUE-DAWLEY; STREPTOZOCIN;

EID: 85013187908     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2016.09.020     Document Type: Article

References (60)

1. [1] Agrawal, R., Mishra, B., Tyagi, E., Nath, C., Shukla, R., Effect of curcumin on brain insulin receptors and memory functions in STZ (ICV) induced dementia model of rat. Pharmacol. Res. 61 (2010), 247–252.
2. [2] Agrawal, R., Tyagi, E., Shukla, R., Nath, C., A study of brain insulin receptors, AChE activity and oxidative stress in rat model of ICV STZ induced dementia. Neuropharmacology 56 (2009), 779–787.
3. [3] Agrawal, R., Tyagi, E., Shukla, R., Nath, C., Insulin receptor signaling in rat hippocampus: a study in STZ (ICV) induced memory deficit model. Eur. Neuropsychopharmacol. 21 (2011), 261–273.
4. [4] Ajmani, R.S., Metter, E.J., Jaykumar, R., Ingram, D.K., Spangler, E.L., Abugo, O.O., et al. Hemodynamic changes during aging associated with cerebral blood flow and impaired cognitive function. Neurobiol. Aging 21 (2000), 257–269.
5. [5] Ashok, A., Rai, N.K., Tripathi, S., Bandyopadhyay, S., Exposure to As-, Cd-, and Pb-mixture induces Abeta, amyloidogenic APP processing and cognitive impairments via oxidative stress-dependent neuroinflammation in young rats. Toxicol. Sci. 143 (2015), 64–80.
6. [6] Awasthi, H., Tota, S., Hanif, K., Nath, C., Shukla, R., Protective effect of curcumin against intracerebral streptozotocin induced impairment in memory and cerebral blood flow. Life Sci. 86 (2010), 87–94.
7. [7] Barilar, J.O., Knezovic, A., Grunblatt, E., Riederer, P., Salkovic-Petrisic, M., Nine-month follow-up of the insulin receptor signalling cascade in the brain of streptozotocin rat model of sporadic Alzheimer's disease. J. Neural. Transm. (Vienna) 122 (2015), 565–576.
8. [8] Bhattacharya, S.K., Saraswati, M., Effect of intracerebroventricularly administered insulin on brain monoamines and acetylcholine in euglycaemic and alloxan-induced hyperglycaemic rats. Indian J. Exp. Biol. 29 (1991), 1095–1100.
9. [9] Benedict, C., Hallschmid, M., Schmitz, K., Schultes, B., Ratter, F., Fehm, H.L., et al. Intranasal insulin improves memory in humans: superiority of insulin aspart. Neuropsychopharmacology 32 (2007), 239–243.
10. [10] Bomfim, T.R., Forny-Germano, L., Sathler, L.B., Brito-Moreira, J., Houzel, J.C., Decker, H., et al. An anti-diabetes agent protects the mouse brain from defective insulin signaling caused by Alzheimer's disease-associated Abeta oligomers. J. Clin. Invest. 122 (2012), 1339–1353.
11. [11] Chen, Y., Zhao, Y., Dai, C.L., Liang, Z., Run, X., Iqbal, K., et al. Intranasal insulin restores insulin signaling, increases synaptic proteins, and reduces Abeta level and microglia activation in the brains of 3xTg-AD mice. Exp. Neurol. 261 (2014), 610–619.
12. [12] Cole, G.M., Frautschy, S.A., The role of insulin and neurotrophic factor signaling in brain aging and Alzheimer's disease. Exp. Gerontol. 42 (2007), 10–21.
13. [13] Connor, B., Young, D., Yan, Q., Faull, R.L., Synek, B., Dragunow, M., Brain-derived neurotrophic factor is reduced in Alzheimer's disease. Brain Res. Mol. Brain Res. 49 (1997), 71–81.
14. [14] Craft, S., Insulin resistance syndrome and Alzheimer disease: pathophysiologic mechanisms and therapeutic implications. Alzheimer Dis. Assoc. Disord. 20 (2006), 298–301.
15. [15] Craft, S., Baker, L.D., Montine, T.J., Minoshima, S., Watson, G.S., Claxton, A., et al. Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial. Arch. Neurol. 69 (2012), 29–38.
16. [16] Crawford, J.G., Alzheimer's disease risk factors as related to cerebral blood flow. Med. Hypotheses 46 (1996), 367–377.
17. [17] Cusi, K., Maezono, K., Osman, A., Pendergrass, M., Patti, M.E., Pratipanawatr, T., et al. Insulin resistance differentially affects the PI 3-kinase- and MAP kinase-mediated signaling in human muscle. J. Clin. Invest. 105 (2000), 311–320.
18. [18] De Felice, F.G., Lourenco, M.V., Ferreira, S.T., How does brain insulin resistance develop in Alzheimer's disease?. Alzheimers Dement. 10 (2014), S26–S32.
19. [19] De Felice, F.G., Vieira, M.N., Bomfim, T.R., Decker, H., Velasco, P.T., Lambert, M.P., et al. Protection of synapses against Alzheimer's-linked toxins: insulin signaling prevents the pathogenic binding of Abeta oligomers. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 1971–1976.
20. [20] de la Monte, S.M., Brain insulin resistance and deficiency as therapeutic targets in Alzheimer's disease. Curr. Alzheimer Res. 9 (2012), 35–66.
21. [21] de la Monte, S.M., Type 3 diabetes is sporadic Alzheimer's disease: mini-review. Eur. Neuropsychopharmacol. 24 (2014), 1954–1960.
22. [22] de la Torre, J.C., Aliev, G., Inhibition of vascular nitric oxide after rat chronic brain hypoperfusion: spatial memory and immunocytochemical changes. J. Cereb. Blood Flow Metab. 25 (2005), 663–672.
23. [23] Dineley, K.T., Kayed, R., Neugebauer, V., Fu, Y., Zhang, W., Reese, L.C., et al. Amyloid-beta oligomers impair fear conditioned memory in a calcineurin-dependent fashion in mice. J. Neurosci. Res. 88 (2010), 2923–2932.
24. [24] Duarte, A.I., Santos, M.S., Oliveira, C.R., Rego, A.C., Insulin neuroprotection against oxidative stress in cortical neurons-involvement of uric acid and glutathione antioxidant defenses. Free Radic. Biol. Med. 39 (2005), 876–889.
25. [25] Dwivedi, S., Rajasekar, N., Hanif, K., Nath, C., Shukla, R., Sulforaphane ameliorates okadaic acid-induced memory impairment in rats by activating the Nrf2/HO-1 antioxidant pathway. Mol. Neurobiol., 2015.
26. [26] Formoso, G., Chen, H., Kim, J.A., Montagnani, M., Consoli, A., Quon, M.J., Dehydroepiandrosterone mimics acute actions of insulin to stimulate production of both nitric oxide and endothelin 1 via distinct phosphatidylinositol 3-kinase- and mitogen-activated protein kinase-dependent pathways in vascular endothelium. Mol. Endocrinol. 20 (2006), 1153–1163.
27. [27] Glowinski, J., Iversen, L.L., Regional studies of catecholamines in the rat brain. I. The disposition of [3H]norepinephrine, [3H]dopamine and [3H]dopa in various regions of the brain. J. Neurochem. 13 (1966), 655–669.
28. [28] Goel, R., Bhat, S.A., Hanif, K., Nath, C., Shukla, R., Perindopril attenuates lipopolysaccharide-induced amyloidogenesis and memory impairment by suppression of oxidative stress and RAGE activation. ACS Chem. Neurosci. 7 (2016), 206–217.
29. [29] Hernandez, C.M., Kayed, R., Zheng, H., Sweatt, J.D., Dineley, K.T., Loss of alpha7 nicotinic receptors enhances beta-amyloid oligomer accumulation, exacerbating early-stage cognitive decline and septohippocampal pathology in a mouse model of Alzheimer's disease. J. Neurosci. 30 (2010), 2442–2453.
30. [30] Jiang, Z.Y., Lin, Y.W., Clemont, A., Feener, E.P., Hein, K.D., Igarashi, M., et al. Characterization of selective resistance to insulin signaling in the vasculature of obese Zucker (fa/fa) rats. J. Clin. Invest. 104 (1999), 447–457.
31. [31] Kahn, A.M., Husid, A., Allen, J.C., Seidel, C.L., Song, T., Insulin acutely inhibits cultured vascular smooth muscle cell contraction by a nitric oxide synthase-dependent pathway. Hypertension 30 (1997), 928–933.
32. [32] Kanninen, K., Heikkinen, R., Malm, T., Rolova, T., Kuhmonen, S., Leinonen, H., et al. Intrahippocampal injection of a lentiviral vector expressing Nrf2 improves spatial learning in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 16505–16510.
33. [33] Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J., Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951), 265–275.
34. [34] McGovern, S., Maguire, M.E., Gurd, R.S., Mahler, H.R., Moore, W.J., Separation of adrenergic and cholinergic synaptosomes from immature rat brain. FEBS Lett. 31 (1973), 193–198.
35. [35] Mufson, E.J., Counts, S.E., Perez, S.E., Ginsberg, S.D., Cholinergic system during the progression of Alzheimer's disease: therapeutic implications. Expert. Rev. Neurother. 8 (2008), 1703–1718.
36. [36] O'Brien, J.T., Eagger, S., Syed, G.M., Sahakian, B.J., Levy, R., A study of regional cerebral blood flow and cognitive performance in Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 55 (1992), 1182–1187.
37. [37] Pachauri, S.D., Verma, P.R., Dwivedi, A.K., Tota, S., Khandelwal, K., Saxena, J.K., et al. Ameliorative effect of Noni fruit extract on streptozotocin-induced memory impairment in mice. Behav. Pharmacol. 24 (2013), 307–319.
38. [38] Plaschke, K., Hoyer, S., Action of the diabetogenic drug streptozotocin on glycolytic and glycogenolytic metabolism in adult rat brain cortex and hippocampus. Int. J. Dev. Neurosci. 11 (1993), 477–483.
39. [39] Potenza, M.A., Marasciulo, F.L., Chieppa, D.M., Brigiani, G.S., Formoso, G., Quon, M.J., et al. Insulin resistance in spontaneously hypertensive rats is associated with endothelial dysfunction characterized by imbalance between NO and ET-1 production. Am. J. Physiol. Heart Circ. Physiol. 289 (2005), H813–H822.
40. [40] Prohovnik, I., Mayeux, R., Sackeim, H.A., Smith, G., Stern, Y., Alderson, P.O., Cerebral perfusion as a diagnostic marker of early Alzheimer's disease. Neurology 38 (1988), 931–937.
41. [41] Pugazhenthi, S., Wang, M., Pham, S., Sze, C.I., Eckman, C.B., Downregulation of CREB expression in Alzheimer's brain and in Abeta-treated rat hippocampal neurons. Mol. Neurodegener., 6, 2011, 60.
42. [42] Rai, S., Kamat, P.K., Nath, C., Shukla, R., Glial activation and post-synaptic neurotoxicity: the key events in streptozotocin (ICV) induced memory impairment in rats. Pharmacol. Biochem. Behav. 117 (2014), 104–117.
43. [43] Rajasekar, N., Dwivedi, S., Nath, C., Hanif, K., Shukla, R., Protection of streptozotocin induced insulin receptor dysfunction, neuroinflammation and amyloidogenesis in astrocytes by insulin. Neuropharmacology 86 (2014), 337–352.
44. [44] Rajasekar, N., Dwivedi, S., Tota, S.K., Kamat, P.K., Hanif, K., Nath, C., et al. Neuroprotective effect of curcumin on okadaic acid induced memory impairment in mice. Eur. J. Pharmacol. 715 (2013), 381–394.
45. [45] Ramsey, C.P., Glass, C.A., Montgomery, M.B., Lindl, K.A., Ritson, G.P., Chia, L.A., et al. Expression of Nrf2 in neurodegenerative diseases. J. Neuropathol. Exp. Neurol. 66 (2007), 75–85.
46. [46] Reger, M.A., Watson, G.S., Green, P.S., Wilkinson, C.W., Baker, L.D., Cholerton, B., et al. Intranasal insulin improves cognition and modulates beta-amyloid in early AD. Neurology 70 (2008), 440–448.
47. [47] Shen, H., Kihara, T., Hongo, H., Wu, X., Kem, W.R., Shimohama, S., et al. Neuroprotection by donepezil against glutamate excitotoxicity involves stimulation of alpha7 nicotinic receptors and internalization of NMDA receptors. Br. J. Pharmacol. 161 (2010), 127–139.
48. [48] Shieh, P.B., Ghosh, A., Molecular mechanisms underlying activity-dependent regulation of BDNF expression. J. Neurobiol. 41 (1999), 127–134.
49. [49] Shigenaga, M.K., Hagen, T.M., Ames, B.N., Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 10771–10778.
50. [50] Shih, A.Y., Johnson, D.A., Wong, G., Kraft, A.D., Jiang, L., Erb, H., et al. Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress. J. Neurosci. 23 (2003), 3394–3406.
51. [51] Tong, L., Prieto, G.A., Kramar, E.A., Smith, E.D., Cribbs, D.H., Lynch, G., et al. Brain-derived neurotrophic factor-dependent synaptic plasticity is suppressed by interleukin-1beta via p38 mitogen-activated protein kinase. J. Neurosci. 32 (2012), 17714–17724.
52. [52] Tota, S., Goel, R., Pachauri, S.D., Rajasekar, N., Najmi, A.K., Hanif, K., et al. Effect of angiotensin II on spatial memory, cerebral blood flow, cholinergic neurotransmission, and brain derived neurotrophic factor in rats. Psychopharmacology 226 (2013), 357–369.
53. [53] Tota, S., Kamat, P.K., Saxena, G., Hanif, K., Najmi, A.K., Nath, C., Central angiotensin converting enzyme facilitates memory impairment in intracerebroventricular streptozotocin treated rats. Behav. Brain Res. 226 (2012), 317–330.
54. [54] Tota, S., Kamat, P.K., Shukla, R., Nath, C., Improvement of brain energy metabolism and cholinergic functions contributes to the beneficial effects of silibinin against streptozotocin induced memory impairment. Behav. Brain Res. 221 (2011), 207–215.
55. [55] Tully, T., Bourtchouladze, R., Scott, R., Tallman, J., Targeting the CREB pathway for memory enhancers. Nat. Rev. Drug Discov. 2 (2003), 267–277.
56. [56] Wang, C., Smith, R.L., Lowry determination of protein in the presence of Triton X-100. Anal. Biochem. 63 (1975), 414–417.
57. [57] Wang, X., Wu, H., Chen, H., Liu, R., Liu, J., Zhang, T., et al. Does insulin bolster antioxidant defenses via the extracellular signal-regulated kinases-protein kinase B-nuclear factor erythroid 2 p45-related factor 2 pathway?. Antioxid. Redox Signal. 16 (2012), 1061–1070.
58. [58] Yang, Y., Ma, D., Wang, Y., Jiang, T., Hu, S., Zhang, M., et al. Intranasal insulin ameliorates tau hyperphosphorylation in a rat model of type 2 diabetes. J. Alzheimers Dis. 33 (2013), 329–338.
59. [59] Yang, Z., Ming, X.F., Recent advances in understanding endothelial dysfunction in atherosclerosis. Clin. Med. Res. 4 (2006), 53–65.
60. [60] Yu, M., Li, H., Liu, Q., Liu, F., Tang, L., Li, C., et al. Nuclear factor p65 interacts with Keap1 to repress the Nrf2-ARE pathway. Cell. Signal. 23 (2011), 883–892.