Permissive role of insulin in the expression of long-term potentiation in the hippocampus of immature rats

NeuroSignals

Volumn 18, Issue 4, 2011, Pages 236-245

  Zhao, Wenchao ^a   Wu, Xiaomei ^a   Xie, Hui ^a   Ke, Ya ^a   Yung, Wing Ho ^a  

^a and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

Author keywords

Insulin; Long term potentiation; Synaptic plasticity

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 3 BROMO 5 TERT BUTYL 4 HYDROXYBENZYLIDENEMALONONITRILE; GLUCOSE; INDINAVIR; INSULIN; INSULIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1;

AGE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; GLUCOSE HOMEOSTASIS; GLUCOSE UTILIZATION; HIPPOCAMPUS; INHIBITION KINETICS; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; RAT;

ANIMALS; HIPPOCAMPUS; INSULIN; LONG-TERM POTENTIATION; NEURONS; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, INSULIN;

EID: 79953657859     PISSN: 1424862X     EISSN: None     Source Type: Journal    
DOI: 10.1159/000324040     Document Type: Article

References (60)

1. Chiu SL, Cline HT: Insulin receptor signaling in the development of neuronal structure and function. Neural Dev 2010; 15: 7.
2. Kodl CT, Seaquist ER: Cognitive dysfunction and diabetes mellitus. Endocr Rev 2008; 29: 494-511. (Pubitemid 351831510)
3. McNay EC: Insulin and ghrelin: Peripheral hormones modulating memory and hippocampal function. Curr Opin Pharmacol 2007; 7: 628-632. (Pubitemid 350185858)
4. Van der Heide LP, Ramakers GM, Smidt MP: Insulin signaling in the central nervous system: Learning to survive. Prog Neurobiol 2006; 79: 205-221. (Pubitemid 44331498)
5. Margolis RU, Altszuler N: Insulin in the cerebrospinal fluid. Nature 1967; 215: 1375-1376.
6. Posner BI, Kelly PA, Shiu RP, Friesen HG: Studies of insulin, growth hormone and prolactin binding: Tissue distribution, species variation and characterization. Endocrinology 1974; 95: 521-531.
7. Havrankova J, Roth J, Brownstein M: Insulin receptors are widely distributed in the central nervous system of the rat. Nature 1978; 272: 827-829. (Pubitemid 8316991)
8. Havrankova J, Schmechel DE, Roth J, Brownstein M: Identification of insulin in the rat brain. Proc Natl Acad Sci USA 1978; 75: 5737-5741.
9. Winocur G, Greenwood CE, Piroli GG, Grillo CA, Reznikov LR, Reagan LP, McEwen BS: Memory impairment in obese Zucker rats: An investigation of cognitive function in an animal model of insulin resistance and obesity. Behav Neurosci 2005; 119: 1389-1395. (Pubitemid 41598751)
10. Hoyer S: The brain insulin signal transduction system and sporadic (type II) Alzheimer disease: An update. J Neural Transm 2002; 109: 341-360. (Pubitemid 34251638)
11. Gasparini L, Xu H: Potential roles of insulin and IGF-1 in Alzheimer's disease. Trends Neurosci 2003; 26: 404-406. (Pubitemid 37288973)
12. de la Monte SM, Wands JR: Alzheimer-associated neuronal thread protein mediated cell death is linked to impaired insulin signaling. J Alzheimers Dis 2004; 6: 231-242. (Pubitemid 38823258)
13. Craft S, Peskind E, Schwartz MW, Schellenberg GD, Raskind M, Porte D Jr: Cerebrospinal fluid and plasma insulin levels in Alzheimer's disease. Neurology 1998; 50: 164-168.
14. Benedict C, Hallschmid M, Schultes B, Born J, Kern W: Intranasal insulin to improve memory function in humans. Neuroendocrinology 2007; 86: 136-142. (Pubitemid 47494214)
15. 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: 270-280. (Pubitemid 34701752)
16. Park CR, Seeley RJ, Craft S, Woods SC: Intracerebroventricular insulin enhances memory in a passive-avoidance task. Physiol Behav 2000; 68: 509-514. (Pubitemid 30129236)
17. Biessels GJ, Kamal A, Urban IJA, 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: 125-135. (Pubitemid 28361929)
18. Dou JT, Chen M, Dufour F, Alkon DL, Zhao WQ: Insulin receptor signaling in long-term memory consolidation following spatial learning. Learn Mem 2005; 12: 646-655. (Pubitemid 41770090)
19. Moosavi M, Naghdi N, Maghsoudi N, Zahedi Asl S: Insulin protects against stress-induced impairments in water maze performance. Behav Brain Res 2007; 176: 230-236. (Pubitemid 44880084)
20. 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: 1135-1140.
21. Bondy CA, Bach MA, Lee WH: Mapping of brain insulin and insulin-like growth factor receptor gene expression by in situ hybridization. Neuroprotocols 1992; 1: 240-249.
22. Marks JL, Porte D Jr, Stahl WL, Baskin DG: Localization of insulin receptor mRNA in rat brain by in situ hybridization. Endocrinology 1990; 127: 3234-3236.
23. Hopkins DF, Williams G: Insulin receptors are widely distributed in human brain and bind human and porcine insulin with equal affinity. Diabet Med 1997; 14: 1044-1050. (Pubitemid 28015389)
24. Zhao WQ, Alkon DL: Role of insulin and insulin receptor in learning and memory. Mol Cell Endocrinol 2001; 177: 125-134. (Pubitemid 32506813)
25. Zhao W, Chen H, Xu H, Moore E, Meiri N, Quon MJ, Alkon DL: 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 1999; 274: 34893-34902. (Pubitemid 129509536)
26. 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: 143-157. (Pubitemid 19209704)
27. Doré S, Kar S, Rowe W, Quirion R: Distribution and levels of [ 125 I]IGF-I, [ 125 I]IGF-II and [ 125 I]insulin receptor binding sites in the hippocampus of aged memory-unimpaired and -impaired rats. Neuroscience 1997; 80: 1033-1040. (Pubitemid 27359790)
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: 217-231.
29. Lee CC, Kuo YM, Huang CC, Hsu KS: Insulin rescues amyloidβ-induced impairment of hippocampal long-term potentiation. Neurobiol Aging 2009; 30: 377-387.
30. Biessels GJ, Kamal A, Ramakers GM, Urban IJ, Spruijt BM, Erkelens DW, Gispen WH: Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes 1996; 45: 1259-1266. (Pubitemid 26296329)
31. Bélanger A, Lavoie N, Trudeau F, Massicotte G, Gagnon S: Preserved LTP and water maze learning in hyperglycaemic-hyperinsulinemic ZDF rats. Physiol Behav 2004; 83: 483-494. (Pubitemid 39586671)
32. Park CW, Yoo KY, Hwang IK, Choi JH, Lee CH, Park OK, Cho JH, Lee YL, Shin HC, Won MH: Age-related changes in the insulin receptor beta in the gerbil hippocampus. Neurochem Res 2009; 34: 2154-2162.
33. Shehata G, Eltayeb A: Cognitive function and event-related potentials in children with type 1 diabetes mellitus J Child Neurol 2010; 25: 469-474.
34. Oka H, Shimono K, Ogawa R, Sugihara H, Taketani M: A new planar multielectrode array for extracellular recording: Application to hippocampal acute slice. J Neurosci Methods 1999; 93: 61-67. (Pubitemid 29516627)
35. Shimono K, Baudry M, Ho L, Taketani M, Lynch G: Long-term recording of LTP in cultured hippocampal slices. Neural Plast 2002; 9: 249-254. (Pubitemid 37069440)
36. Parrizas M, Gazit A, Levitzki A, Wertheimer E, LeRoith D: Specific inhibition of insulinlike growth factor-1 and insulin receptor tyrosine kinase activity and biological function by tyrphostins. Endocrinology 1997; 138: 1427-1433. (Pubitemid 27137089)
37. Laron Z: Insulin and the brain. Arch Physiol Biochem 2009; 15: 112-116.
38. Biessels GJ, Bravenboer B, Gispen WH: Glucose, insulin and the brain: Modulation of cognition and synaptic plasticity in health and disease: A preface. Eur J Pharmacol 2004; 490: 1-4. (Pubitemid 38482156)
39. Saltiel AR, Kahn CR: Insulin signalling and the regulation of glucose and lipid metabolism. Nature 2001; 414: 799-806. (Pubitemid 34000783)
40. Van der Heide LP, Kamal A, Artola A, Gispen WH, Ramakers GM: Insulin modulates hippocampal activity-dependent synaptic plasticity in a N-methyl- D -aspartate receptor and phosphatidyl-inositol-3-kinase-dependent manner. J Neurochem 2005; 94: 1158-1166. (Pubitemid 41170602)
41. Harris KM, Teyler TJ: Developmental onset of long-term potentiation in area CA1 of the rat hippocampus. J Physiol 1984; 346: 27-48. (Pubitemid 14058462)
42. Jackson PS, Suppes T, Harris KM: Stereotypical changes in the pattern and duration of long-term potentiation expressed at postnatal days 11 and 15 in the rat hippocampus. J Neurophysiol 1993; 70: 1412-1419. (Pubitemid 23326378)
43. 2+ /calmodulin-dependent phosphatase inhibitor, inhibits the induction of long-term potentiation in the rat hippocampus. Neurosci Lett 1996; 205: 103-106.
44. Gaudieri PA, Chen R, Greer TF, Holmes CS: Cognitive function in children with type 1 diabetes: A meta-analysis. Diabetes Care 2008; 31: 1892-1897.
45. Naguib JM, Kulinskaya E, Lomax CL, Garralda ME: Neuro-cognitive performance in children with type 1 diabetes - a metaanalysis. J Pediatr Psychol 2009; 34: 271-282.
46. Lund-Andersen H: Transport of glucose from blood to brain. Physiol Rev 1979; 59: 305-352. (Pubitemid 9165968)
47. Benomar Y, Naour N, Aubourg A, Bailleux V, Gertler A, Djiane J, Guerre-Millo M, Taouis M: Insulin and leptin induce Glut4 plasma membrane translocation and glucose uptake in a human neuronal cell line by a phosphatidylinositol 3-kinase-dependent mechanism. Endocrinology 2006; 147: 2550-2556.
48. Messari El S, Ait-Iklef A, Ambroise DH, Penicaud L, Arluison M: Expression of insulin- responsive glucose transporter Glut4 mRNA in the rat brain and spinal cord: An in situ hybridization study. J Chem Neuroanat 2002; 24: 225-242. (Pubitemid 35287439)
49. Piroli GG, Grillo CA, Reznikov LR, Adams S, McEwen BS, Charron MJ, Reagan LP: Corticosterone impairs insulin-stimulated translocation of GLUT4 in the rat hippocampus. Neuroendocrinology 2007; 85: 71-80. (Pubitemid 46725693)
50. Grillo CA, Piroli GG, Hendry RM, Reagan LP: Insulin-stimulated translocation of GLUT4 to the plasma membrane in rat hippocampus is PI3-kinase dependent. Brain Res 2009; 1296: 35-45.
51. McEwen BS, Reagan LP: Glucose transporter expression in the central nervous system: Relationship to synaptic function. Eur J Pharmacol 2004; 490: 13-24. (Pubitemid 38482158)
52. Murata H, Hruz PW, Mueckler M: The mechanism of insulin resistance caused by HIV protease inhibitor therapy. J Biol Chem 2000; 275: 20251-20254. (Pubitemid 30457596)
53. Murata H, Hruz PW, Mueckler M: Indinavir inhibits the glucose transporter isoform Glut4 at physiologic concentrations. AIDS 2002; 16: 859-863. (Pubitemid 34409009)
54. Skeberdis VA, Lan J, Zheng X, Zukin RS, Bennett MV: Insulin promotes rapid delivery of N-methyl- D -aspartate receptors to the cell surface by exocytosis. Proc Natl Acad Sci USA 2001; 98: 3561-3566. (Pubitemid 32220884)
55. Passafaro M, Piëch V, Sheng M: Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 2001; 4: 917-926. (Pubitemid 32801595)
56. Liu L, Brown III JC, Webster, WW, Morrisett RA; Monaghan DT: Insulin potentiates Nmethyl- D -aspartate receptor activity in Xenopus oocytes and rat hippocampus. Neurosci Lett 1995; 192: 5-8.
57. Zadran S, Qin Q, Bi X, Zadran H, Kim Y, Foy MR, Thompson R, Baudry M: 17-Beta-estradiol increases neuronal excitability through MAP kinase-induced calpain activation. Proc Natl Acad Sci USA 2009; 106: 21936-21941.
58. Irving AJ, Wallace L, Durakoglugil D, Harvey J: Leptin enhances NR2B-mediated Nmethyl- D -aspartate responses via a mitogenactivated protein kinase-dependent process in cerebellar granule cells. Neuroscience 2006; 138: 1137-1148. (Pubitemid 43363532)
59. 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: 18543-18550.
60. Hori K, Yasuda H, Konno D, Maruoka H, Tsumoto T, Sobue K: NMDA receptor-dependent synaptic translocation of insulin receptor substrate p53 via protein kinase C signaling. Neurosci 2005; 25: 2670-2681. (Pubitemid 40365178)