The role of insulin receptor signaling in synaptic plasticity and cognitive function

Chang Gung Medical Journal

Volumn 33, Issue 2, 2010, Pages 115-125

  Huang, Chiung Chun ^a   Lee, Cheng Che ^a   Hsu, Kuei Sen ^a,b  

^a Institute of Clinical Pharmacy and Pharmaceutical Sciences   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Cognitive function; Insulin; Neuron; Synaptic plasticity

Indexed keywords

AMPA RECEPTOR; INSULIN; INSULIN RECEPTOR;

BRAIN CORTEX; BRAIN FUNCTION; COGNITION; ENDOCYTOSIS; EXPERIENCE; HIPPOCAMPUS; HUMAN; INFORMATION PROCESSING; INSULIN RELEASE; LEARNING; LONG TERM DEPRESSION; NERVE CELL PLASTICITY; NERVE DEGENERATION; NONHUMAN; REGULATORY MECHANISM; REVIEW; SYNAPTIC TRANSMISSION;

ANIMALS; COGNITION; HUMANS; INSULIN; NEURONAL PLASTICITY; RECEPTOR, INSULIN; SYNAPTIC TRANSMISSION;

EID: 77951741583     PISSN: 20720939     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (75)

1. Havrankova J, Roth J, Brownstein M. Insulin receptors are widely distributed in the central nervous system of the rat. Nature 1978;272:827-9.
2. Unger J, McNeill TH, Moxley RT 3rd, White M, Moss A, Livingston JN. Distribution of insulin receptor-like immunoreactivity in the rat forebrain. Neuroscience 1989;31:143-57.
3. Park CR. Cognitive effects of insulin in the central nervous system. Neurosci Biobehav Rev 2001;25:311-23.
4. Zhao WQ, Alkon DL. Role of insulin and insulin receptor in learning and memory. Mol Cell Endocrinol 2001;177:125-34.
5. Plum L, Schubert M, Brüning JC. The role of insulin receptor signaling in the brain. Trends Endocrinol Metab 2005;16:59-65.
6. van der Heide LP, Ramakers GM, Smidt MP. Insulin signaling in the central nervous system: learning to survive. Prog Neurobiol 2006;79:205-21.
7. Figlewicz DP, Benoit SC. Insulin, leptin, and food reward: update 2008. Am J Physiol Regul Integr Comp Physiol 2009;296:R9-19.
8. Olefsky JM. The insulin receptor. A multifunctional protein. Diabetes 1990;39:1009-16.
9. Taylor SI, Cama A, Accili D, Barbetti F, Quon MJ, de la Luz Sierra M, Suzuki Y, Koller E, Levy-Toledano R, Wertheimer E, Moncadaj VY, Kadowaki H, Kadowaki T. Mutations in the insulin receptor gene. Endocr Rev 1992;13:566-95.
10. Orban PC, Chapman PF, Brambilla R. Is the Ras-MAPK signalling pathway necessary for long-term memory formation? Trends Neurosci 1999;22:38-44.
11. Baskin DG, Woods SC, West DB, van Houten M, Posner BI, Dorsa DM, Porte D Jr. Immunocytochemical detection of insulin in rat hypothalamus and its possible uptake from cerebrospinal fluid. Endocrinology 1983;113:1818-25.
12. van Houten M, Posner BI, Kopriwa BM, Brawer JR. Insulin-binding sites in the rat brain: in vivo localization to the circumventricular organs by quantitative radioautography. Endocrinology 1979;105:666-73.
13. Hill JM, Lesniak MA, Pert CB, Roth J. Autoradiographic localization of insulin receptors in rat brain: prominence in olfactory and limbic areas. Neuroscience 1986;17:1127-38.
14. Wickelgren I. Tracking insulin to the mind. Science 1998;280:517-9.
15. Stockhorst U, de Fries D, Steingrueber HJ, Scherbaum WA. Insulin and the CNS: effects on food intake, memory, and endocrine parameters and the role of intranasal insulin administration in humans. Physiol Behav 2004;83:47-54.
16. Schwartz MW, Figlewicz DP, Baskin DG, Woods SC, Porte D Jr. Insulin in the brain: a hormonal regulator of energy balance. Endocr Rev 1992;13:387-414.
17. Marks JL, Maddison J, Eastman CJ. Subcellular localization of rat brain insulin binding sites. J Neurochem 1988;50:774-81.
18. Adamo M, Lowe WL Jr, LeRoith D, Roberts CT Jr. Insulin-like growth factor I messenger ribonucleic acids with alternative 5'-untranslated regions are differentially expressed during development of the rat. Endocrinology 1989;124:2737-44.
19. Woods SC, Seeley RJ, Baskin DG, Schwartz MW. Insulin and the blood-brain barrier. Curr Pharm Des 2003;9:795-800.
20. Banks WA. The source of cerebral insulin. Eur J Pharmacol 2004;490:5-12.
21. Schechter R, Whitmire J, Wheet GS, Beju D, Jackson KW, Harlow R, Gavin JR 3rd. Immunohistochemical and in situ hybridization study of an insulin-like substance in fetal neuron cell cultures. Brain Res 1994;636:9-27.
22. Devaskar SU, Giddings SJ, Rajakumar PA, Carnaghi LR, Menon RK, Zahm DS. Insulin gene expression and insulin synthesis in mammalian neuronal cells. J Biol Chem 1994;269:8445-54.
23. Abbott MA, Wells DG, Fallon JR. The insulin receptor tyrosine kinase substrate p58/53 and the insulin receptor are components of CNS synapses. J Neurosci 1999;19:7300-8.
24. Wan Q, Xiong ZG, Man HY, Ackerley CA, Braunton J, Lu WY, Becker LE, MacDonald JF, Wang YT. Recruitment of functional GABAA receptors to postsynaptic domains by insulin. Nature 1997;388:686-90.
25. Man HY, Lin JW, Ju WH, Ahmadian G, Liu L, Becker LE, Sheng M, Wang YT. Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 2000;25:649-62.
26. Wang YT, Linden DJ. Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron 2000;25:635-47.
27. Huang CC, You JL, Lee CC, Hsu KS. Insulin induces a novel form of postsynaptic mossy fiber long-term depression in the hippocampus. Mol Cell Neurosci 2003;24:831-41.
28. Huang CC, Lee CC, Hsu KS. An investigation into signal transduction mechanisms involved in insulin-induced long-term depression in the CA1 region of the hippocampus. J Neurochem 2004;89:217-31.
29. Liu L, Brown JC 3rd, Webster WW, Morrisett RA, Monaghan DT. Insulin potentiates N-methyl-D-aspartate receptor activity in Xenopus oocytes and rat hippocampus. Neurosci Lett 1995;192:5-8.
30. Liao GY, Leonard JP. Insulin modulation of cloned mouse NMDA receptor currents in Xenopus oocytes. J Neurochem 1999;73:1510-9.
31. Siegelbaum SA, Kandel ER. Learning-related synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 1991;1:113-20.
32. Bear MF, Abraham WC. Long-term depression in hippocampus. Annu Rev Neurosci 1996;19:437-62.
33. Manahan-Vaughan D, Braunewell KH. Novelty acquisition is associated with induction of hippocampal longterm depression. Proc Natl Acad Sci USA 1999;96:8739-44.
34. Zhao WQ, Chen GH, Chen H, Pascale A, Ravindranath L, Quon MJ, Alkon DL. Secretion of Annexin II via activation of insulin receptor and insulin-like growth factor receptor. J Biol Chem 2003;278:4205-15.
35. Ziff EB. Enlightening the postsynaptic density. Neuron 1997;19:1163-74.
36. Ehlers MD, Zhang S, Bernhadt JP, Huganir RL. Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 1996;84:745-55.
37. Hering H, Sheng M. Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2001;2:880-8.
38. Kim E, Sheng M. PDZ domain proteins of synapses. Nat Rev Neurosci 2004;5:771-81.
39. El-Husseini AE, Schnell E, Chetkovich DM, Nicoll RA, Bredt DS. PSD-95 involvement in maturation of excitatory synapses. Science 2000;290:1364-8.
40. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, He Y, Ramsay MF, Morris RG, Morrison JH, O'Dell TJ, Grant SG. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 1998;396:433-9.
41. Yao WD, Gainetdinov RR, Arbuckle MI, Sotnikova TD, Cyr M, Beaulieu JM, Torres GE, Grant SG, Caron MG. Identification of PSD-95 as a regulator of dopamine-mediated synaptic and behavioral plasticity. Neuron 2004;41:625-38.
42. Lee CC, Huang CC, Wu MY, Hsu KS. Insulin stimulates postsynaptic density-95 protein translation via the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway. J Biol Chem 2005;280:18543-50.
43. Hering H, Sheng M. Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2001;2:880-8
44. Matus A. Actin-based plasticity in dendritic spines. Science 2000;290:754-8.
45. Yuste R, Majewska A. On the function of dendritic spines. Neuroscientist 2001;7:387-95.
46. Bonhoeffer T, Yuste R. Spine motility. Phenomenology, mechanisms, and function. Neuron 2002;35:1019-27.
47. Tada T, Sheng M. Molecular mechanisms of dendritic spine morphogenesis. Curr Opin Neurobiol 2006;16:95-101.
48. Yuste R, Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 2001;24:1071-89.
49. Alvarez VA, Sabatini BL. Anatomical and physiological plasticity of dendritic spines. Annu Rev Neurosci 2007;30:79-97.
50. Bourne J, Harris KM. Do thin spines learn to be mushroom spines that remember? Curr Opin Neurobiol 2007;17:381-6.
51. Penzes P, Jones KA. Dendritic spine dynamics--a key role for kalirin-7. Trends Neurosci 2008;31:419-27.
52. Chiu SL, Chen CM, Cline HT. Insulin receptor signaling regulates synapse number, dendritic plasticity, and circuit function in vivo. Neuron 2008;58:708-19.
53. Gispen WH, Biessels GJ. Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci 2000;23:542-9.
54. Ott A, Stolk RP, van Harskamp F, Pols HA, Hofman A, Breteler MM. Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology 1999;53:1937-42.
55. Biessels GJ, Staekenborg S, Brunner E, Brayne C, Scheltens P. Risk of dementia in diabetes mellitus: a systematic review. Lancet Neurol 2006;5:64-74.
56. Craft S, Newcomer J, Kanne S, Dagogo-Jack S, Cryer P, Sheline Y, Luby J, Dagogo-Jack A, Alderson A. Memory improvement following induced hyperinsulinemia in Alzheimer's disease. Neurobiol Aging 1996;17:123-30.
57. Craft S, Asthana S, Cook DG, Baker LD, Cherrier M, Purganan K, Wait C, Petrova A, Latendresse S, Watson GS, Newcomer JW, Schellenberg GD, Krohn AJ. Insulin dose-response effects on memory and plasma amyloid precursor protein in Alzheimer's disease: interactions with apolipoprotein E genotype. Psychoneuroendocrinology 2003;28:809-22.
58. Kern W, Peters A, Fruehwald-Schultes B, Deininger E, Born J, Fehm HL. Improving influence of insulin on cognitive functions in humans. Neuroendocrinology 2001;74:270-80.
59. Park CR, Seeley RJ, Craft S, Woods SC. Intracerebroventricular insulin enhances memory in a passiveavoidance task. Physiol Behav 2000;68:509-14.
60. Biessels GJ, Kamal A, Urban IJ, Spruijt BM, Erkelens DW, Gispen WH. Water maze learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: effects of insulin treatment. Brain Res 1998;800:125-35.
61. Kamal A, Biessels GJ, Duis SE, Gispen WH. Learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: interaction of diabetes and ageing. Diabetologia 2000;43:500-6.
62. LaFerla FM, Oddo S. Alzheimer's disease: Abeta, tau and synaptic dysfunction. Trends Mol Med 2005;11:170-6.
63. Grundke-Iqbal I, Iqbal K, Quinlan M, Tung YC, Zaidi MS, Wisniewski HM. Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J Biol Chem 1986;261:6084-9.
64. Glenner GG, Wong CW. Alzheimer's disease and Down's syndrome: sharing of a unique cerebrovascular amyloid fibril protein. Biochem Biophys Res Commun 1984;122:1131-5.
65. Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci USA 1985;82:4245-9.
66. Craft S, Peskind E, Schwartz MW, Schellenberg GD, Raskind M, Porte D Jr. Cerebrospinal fluid and plasma insulin levels in Alzheimer's disease: relationship to severity of dementia and apolipoprotein E genotype. Neurology 1998;50:164-8.
67. Craft S, Asthana S, Newcomer JW, Wilkinson CW, Matos IT, Baker LD, Cherrier M, Lofgreen C, Latendresse S, Petrova A, Plymate S, Raskind M, Grimwood K, Veith RC. Enhancement of memory in Alzheimer disease with insulin and somatostatin, but not glucose. Arch Gen Psychiatry 1999;56:1135-40.
68. Reger MA, Watson GS, Green PS, Wilkinson CW, Baker LD, Cholerton B, Fishel MA, Plymate SR, Breitner JC, DeGroodt W, Mehta P, Craft S. Intranasal insulin improves cognition and modulates beta-amyloid in early AD. Neurology 2008;70:440-8.
69. 22-35-amyloid peptide (β22-35) on the hippocampal neuron and its prevention. Neurosci Lett 1993;161:41-4.
70. De Felice FG, Vieira MN, Bomfim TR, Decker H, Velasco PT, Lambert MP, Viola KL, Zhao WQ, Ferreira ST, Klein WL. Protection of synapses against Alzheimer's-linked toxins: insulin signaling prevents the pathogenic binding of Aβ oligomers. Proc Natl Acad Sci USA 2009;106:1971-6.
71. Rensink AA, Otte-Holler I, de Boer R, Bosch RR, ten Donkelaar HJ, de Waal RM, Verbeek MM, Kremer B. Insulin inhibits amyloid β-induced cell death in cultured human brain pericytes. Neurobiol Aging 2004;25:93-103.
72. Xie L, Helmerhorst E, Taddei K, Plewright B, Van Bronswijk W, Martins R. Alzheimer's β-amyloid peptides compete for insulin binding to the insulin receptor. J Neurosci 2002;22:RC221.
73. Kurochkin IV. Amyloidogenic determinant as a substrate recognition motif of insulin-degrading enzyme. FEBS Lett 1998;427:153-6.
74. Gasparini L, Gouras GK, Wang R, Gross RS, Beal MF, Greengard P, Xu H. Stimulation of β-amyloid precursor protein trafficking by insulin reduces intraneuronal β-amyloid and requires mitogen-activated protein kinase signaling. J Neurosci 2001;21:2561-70.
75. Lee CC, Kuo YM, Huang CC, Hsu KS. Insulin rescues amyloid beta-induced impairment of hippocampal longterm potentiation. Neurobiol Aging 2009;30:377-87.