Insulin receptor signaling in long-term memory consolidation following spatial learning

Learning and Memory

Volumn 12, Issue 6, 2005, Pages 646-655

  Dou, Jing Tao ^a,d   Chen, Min ^c   Dufour, Franck ^a   Alkon, Daniel L ^a   Zhao, Wei Qin ^a,b  

^a Blanchette Rockefeller Neurosciences Institute   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN RECEPTOR; SOMATOMEDIN RECEPTOR; STREPTOZOCIN;

ARTICLE; COGNITION; CORRELATION ANALYSIS; DIABETES MELLITUS; DOWN REGULATION; GENE EXPRESSION; GLUCOSE BRAIN LEVEL; HIPPOCAMPUS; INSULIN DEFICIENCY; LEARNING; LONG TERM MEMORY; MAZE TEST; MEMORY; MEMORY DISORDER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; HIPPOCAMPUS; INSULIN; MALE; MAZE LEARNING; MEMORY; RATS; RATS, WISTAR; RECEPTOR, INSULIN; RNA; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION;

EID: 28844495644     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.88005     Document Type: Article

References (46)

1. Bailyes, E.M., Navé, B.T., Soos, M.A., Orr, S.R., Hayward, A.C., and Siddle, K. 1997. Insulin receptor/IGF-I receptor hybrids are widely distributed in mammalian tissues: Quantification of individual receptor species by selective immunoprecipitation and immunoblotting. J. Biochem. 327: 209-215.
2. Beattie, E.C., Carroll, R.C., Yu, X., Morishita, W., Yasuda, H., von Zastrow, M., and Malenka, R.C. 2000. Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat. Neurosci. 3: 1291-1300.
3. Benton, D. and Nabb, S. 2003. Carbohydrate, memory, and mood. Nutr. Rev. 61: S61-S67.
4. Bhattacharya, S.K. and Saraswati, M. 1991. Effect of intracerebroventricularly administered insulin on brain monoamines and acetylcholine in euglycaemic and alloxan-induced hyperglycaemic rats. Indian J. Exp. Biol. 29: 1095-1100.
5. Biessels, G.J., Kamal, A., Ramakers, G.M., Urban, I.J., Spruijt, B.M., Erkelens, D.W., and Gispen, W.H. 1996. Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes 45: 1259-1266.
6. Biessels, G.J., Kamal, A., Urban, I.J.A., Spruijt, B.M., Erkelens, D.W., and Gispen, W.H. 1998. Water maze learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: Effects of insulin treatment. Brain Res. 800: 125-135.
7. Craft, S., Newcomer, J., Kanne, S., Dagogo-Jack, S., Cryer, P., Sheline, Y., Luby, J., Dagogo-Jack, A., and Alderson, A. 1996. Memory improvement following induced hyperinsulinemia in Alzheimer's disease. Neurobiol. Aging. 17: 123-130.
8. Dou, J., Cui, C., Dufour, F., Alkon, D.L., and Zhao, W.Q. 2003. Gene expression of α-endosulfine in the rat brain: Correlative changes with aging, learning and stress. J. Neurochem. 87: 1086-1100.
9. Englund, M., Bjurling, M., Edin, F., Hyllienmark, L., and Brismar, T. 2004. Hypoxic excitability changes and sodium currents in hippocampal CA1 neurons. Cell Mol. Neurobiol. 24: 685-694.
10. Figlewicz, D.P. and Szot, P. 1991. Insulin stimulates membrane phospholipid metabolism by enhancing endogenous α 1-adrenergic activity in the rat hippocampus. Brain Res. 550: 101-107.
11. Frank, L.M., Stanley, G.B., and Brown, E.N. 2004. Hippocampal plasticity across multiple days of exposure to novel environment. J. Neurosci. 24: 7681-7689.
12. Frolich, L., Blum-Degen, D., Bernstein, H.G., Engelsberger, S., Humrich, J., Laufer, S., Muschner, D., Thalheimer, A., Turk, A., Hoyer, S., et al. 1998. Brain insulin and insulin receptors in aging and sporadic Alzheimer's disease. J. Neural Transm. 105: 423-438.
13. Gallagher, M., Burwell, R., and Burchinal, M. 1993. Severity of spatial learning impairment in aging: Development of a learning index for performance in the Morris water maze. Behav. Neurosci. 107: 618-626.
14. Gasparini, L. and Xu, H. 2003. Potential roles of insulin and IGF-1 in Alzheimer's disease. Trends Neurosci. 26: 404-406.
15. Heidenreich, K.A. and Brandenburg, D. 1986. Oligosaccharide heterogeneity of insulin receptors. Comparison of N-linked glycosylation of insulin receptors in adipocytes and brain. Endocrinology 118: 1835-1842.
16. 2+ pool and of neuropeptide secretion. Nature 385: 343-346.
17. Kenner, K.A., Kusari, J., and Heidenreich, K.A. 1995. cDNA sequence analysis of the human brain insulin receptor. Biochem. Biophys. Res. Commun. 217: 304-312.
18. Kern, W., Born, J., Schreiber, H., and Fehm, H.L. 1999. Central nervous system effects of intranasally administered insulin during euglycemia in men. Diabetes 48: 557-563.
19. Kern, W., Peters, A., Fruehwald-Schultes, B., Deininger, E., Born, J., and Fehm, H.L. 2001. Improving influence of insulin on cognitive functions in humans. Neuroendocrinology 74: 270-280.
20. Knafo, S., Ariav, G., Barkai, E., and Libersat, F. 2004. Olfactory learning-induced increase in spine density along the apical dendrites of CA1 hippocampal neurons. Hippocampus 4: 819-825.
21. Korol, D.L. and Gold, P.E. 1998. Glucose, memory, and aging. Am. J. Clin. Nutr. 67: 764S-771S.
22. Li, Z.G., Zhang, W., Grunberger, G., and Sima, A.A. 2002. Hippocampal neuronal apoptosis in type 1 diabetes. Brain Res. 946: 221-231.
23. Lin, J.W., Ju, W., Foster, K., Lee, S.H., Ahmadian, G., Wyszynski, M., Wang, Y.T., and Shen, M. 2000. Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat. Neurosci. 3: 1282-1290.
24. Lin, C.H., Yeh, S.H., Lin, C.H., Lu, K.T., Leu, T.H., Chang, W.C., and Gean, P.W. 2001. Role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala. Neuron 31: 841-851.
25. Lukyanetz, E.A., Shkryl, V.M., Kravchuk, O.V., and Kostyuk, P.G. 2003. Action of hypoxia on different types of calcium channels in hippocampal neurons. Biochim. Biophys. Acta. 1618: 33-38.
26. Man, H.Y., Lin, J.W., Ju, W.H., Ahmadian, G., Liu, L., Becker, L.E., Sheng, M., and Wang, Y.T., 2000. Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 25: 649-662.
27. Montagnani, M., Ravichandran, L.V., Chen, H., Esposito, D.L., and Quon, M.J. 2002. Insulin receptor substrate-1 and phosphoinositide-dependent kinase-1 are required for insulin-stimulated production of nitric oxide in endothelial cells. Mol. Endocrinol. 16: 1931-1942.
28. Morozov, A., Muzzio, I.A., Bourtchouladze, R., Van-Strien, N., Lapidus, K., Yin, D., Winder, D.G., Adams, J.P., Sweatt, J.D., Kandel, E.R. 2003. Rap1 couples cAMP signaling to a distinct pool of p42/44MAPK regulating excitability, synaptic plasticity, learning, and memory. Neuron 39: 309-325.
29. Nolan, M.F., Malleret, G., Dudman, J.T., Buhl, D.L., Santoro, B. Gibbs, E., Vronskaya, S., Buzsaki, G., Siegelbaum, S.A., Kandel, E.R., et al. 2004. A behavioral role for dendritic integration: NCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell 119: 719-732.
30. Olson, E.E. and McKeon, R.J. 2004. Characterization of cellular and neurological damage following unilateral hypoxia/ischemia. J. Neurol. Sci. 227: 7-19.
31. Park, C.R., Seeley, R.J., Craft, S., and Woods, S.C. 2000. Intracerebroventricular insulin enhances memory in a passive-avoidance task. Physiol. Behav. 68: 509-514.
32. Paxinos, G. and Watson, C. 1998. The rat brain: In stereotaxic coordinates, 4th ed. Academic Press, San Diego.
33. Robles, Y., Vivas-Mejia, P.E., Ortiz-Zuazaga, H.G., Felix, J., Ramos, X., and Pena de Ortiz, S. 2003. Hippocampal gene expression profiling in spatial discrimination learning. Neurobiol. Learn. Mem. 80: 80-95.
34. Russell, J.W., Sullivan, K.A., Windebank, A.J., Herrmann, D.N., and Feldman, E.L. 1999. Neurons undergo apoptosis in animal and cell culture models of diabetes. Neurobiol. Dis. 6: 347-363.
35. Schubert, M., Gautam, D., Surjo, D., Ueki, K., Baudler, S., Schubert, D., Kondo, T., Alber, J., Galldiks, N., Kustermann, E., et al. 2004. Role for neuronal insulin resistance in neurodegenerative diseases. Proc. Natl. Acad. Sci. 101: 3100-3105.
36. Selcher, J.C., Atkins, C.M., Trzaskos, J.M., Paylor, R., and Sweatt, J.D. 1999. A necessity for MAP kinase activation in mammalian spatial learning. Learn. Mem. 6: 478-490.
37. Selcher, J.C., Weeber, E.J., Christian, J., Nekrasova, T., Landreth, G.E., and Sweatt, J.D. 2003. A role for ERK MAP kinase in physiologic temporal integration in hippocampal area CA1. Learn. Mem. 10: 26-39.
38. Simon, J. and Leroith, D. 1986. Insulin receptors of chicken liver and brain: Characterization of α and β subunit properties. Eur. J. Biochem. 158: 125-132.
39. Skeberdis, V.A., Lan, J., Zheng, X., Zukin, R.S., and Bennett, M.V. 2001. Insulin promotes rapid delivery of N-methyl-D-aspartate receptors to the cell surface by exocytosis. Proc. Natl. Acad. Sci. 98: 3561-3566.
40. Sweatt, J.D. 2001. The neuronal MAP kinase cascade: A biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem. 76: 1-10.
41. Tomizawa, K., Iga, N., Lu, Y.F., Moriwaki, A., Matsushita, M., Li, S.T., Miyamoto, O., Itano, T., and Matsui, H. 2003. Oxytocin improves long-lasting spatial memory during motherhood through MAP kinase cascade. Nat. Neurosci. 6: 384-390.
42. Vincent, A.M., Brownlee, M., and Russell, J.W. 2002. Oxidative stress and programmed cell death in diabetic neuropathy. Ann. NY Acad. Sci. 959: 368-383.
43. Wan, Q., Xiong, Z.G., Man, H.Y., Ackerley, C.A., Braunton, J., Lu, W.Y., Becker, L.E., MacDonald, J.F., and Wang, Y.T. 1997. Recruitment of functional GABA(A) receptors to postsynaptic domains by insulin. Nature 388: 686-690.
44. Watson, G.S. and Craft, S. 2003. The role of insulin resistance in the pathogenesis of Alzheimer's disease: Implications for treatment CNS. Drugs 17: 27-45.
45. Zhao, W., Chen, H., Xu, H., Moore, E., Meiri, N., Quon, M.J., and Alkon, D.L. 1999. Brain insulin receptors and spatial memory. Correlated changes in gene expression, tyrosine phosphorylation, and signaling molecules in the hippocampus of water maze trained rats. J. Biol. Chem. 274: 34893-34902.
46. Zhou, Q., Xiao, M.Y., and Nicoll, R.A. 2001. Contribution of cytoskeleton to the internalization of AMPA receptors. Proc. Natl. Acad. Sci. 98: 1261-1266.