Central insulin resistance and synaptic dysfunction in intracerebroventricular-streptozotocin injected rodents

Neurobiology of Aging

Volumn 33, Issue 2, 2012, Pages 430.e5-430.e18

  Shonesy, Brian C ^a   Thiruchelvam, Kariharan ^a   Parameshwaran, Kodeeswaran ^a   Rahman, Engy Abdel ^a   Karuppagounder, Senthilkumar S ^a   Huggins, Kevin W ^b   Pinkert, Carl A ^b   Amin, Rajesh ^a   Dhanasekaran, Muralikrishnan ^a   Suppiramaniam, Vishnu ^a  

^a AUBURN UNIVERSITY   (United States)

^b AUBURN UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; AMPAR; Hippocampus; Ic STZ; Insulin resistance; Long term potentiation (LTP); NMDAR; Synaptic plasticity

Indexed keywords

AMPA RECEPTOR; BETA INTEGRIN; BRAIN DERIVED NEUROTROPHIC FACTOR; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN; INTEGRIN LINKED KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; STARGAZIN PROTEIN; STREPTOZOCIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; ENZYME ACTIVATION; HIPPOCAMPUS; INSULIN RESISTANCE; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PATHOLOGY; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RAT; SIGNAL TRANSDUCTION; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION;

EID: 82755187412     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2010.12.002     Document Type: Article

References (70)

1. Anderson W.W., Collingridge G.L. Capabilities of the WinLTP data acquisition program extending beyond basic LTP experimental functions. J. Neurosci. Methods 2007, 162:346-356.
2. Bats C., Groc L., Choquet D. The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 2007, 53:719-734.
3. Bi H., Sze C.I. N-methyl-d-aspartate receptor subunit NR2A and NR2B messenger RNA levels are altered in the hippocampus and entorhinal cortex in Alzheimer's disease. J. Neurol. Sci 2002, 200:11-18.
4. Biessels G.J., Kamal A., Ramakers G.M., Urban I.J., Spruijt B.M., Erkelens D.W., Gispen W.H. Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes 1996, 45:1259-1266.
5. Billings L.M., Oddo S., Green K.N., McGaugh J.L., LaFerla F.M. Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 2005, 45:675-688.
6. Blattner S.M., Kretzler M. Integrin-linked kinase in renal disease: connecting cell-matrix interaction to the cytoskeleton. Curr. Opin. Nephrol. Hypertens 2005, 14:404-410.
7. Boyd F.T., Clarke D.W., Muther T.F., Raizada M.K. Insulin receptors and insulin modulation of norepinephrine uptake in neuronal cultures from rat brain. J. Biol. Chem 1985, 260:15880-15884.
8. Caldeira M.V., Melo C.V., Pereira D.B., Carvalho R., Correia S.S., Backos D.S., Carvalho A.L., Esteban J.A., Duarte C.B. Brain-derived neurotrophic factor regulates the expression and synaptic delivery of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor subunits in hippocampal neurons. J. Biol. Chem 2007, 282:12619-12628.
9. Chan C.S., Weeber E.J., Zong L., Fuchs E., Sweatt J.D., Davis R.L. Beta 1-integrins are required for hippocampal AMPA receptor-dependent synaptic transmission, synaptic plasticity, and working memory. J. Neurosci 2006, 26:223-232.
10. Chan O., Inouye K., Vranic M., Matthews S.G. Hyperactivation of the hypothalamo-pituitary-adrenocortical axis in streptozotocin-diabetes is associated with reduced stress responsiveness and decreased pituitary and adrenal sensitivity. Endocrinology 2002, 143:1761-1768.
11. Chapman P.F., White G.L., Jones M.W., Cooper-Blacketer D., Marshall V.J., Irizarry M., Younkin L., Good M.A., Bliss T.V., Hyman B.T., Younkin S.G., Hsiao K.K. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat. Neurosci 1999, 2:271-276.
12. Chen Q., Zhu X., Zhang Y., Wetsel W.C., Lee T.H., Zhang X. Integrin-linked kinase is involved in cocaine sensitization by regulating PSD-95 and synapsin I expression and GluR1 Ser845 phosphorylation. J. Mol. Neurosci 2010, 40:284-294.
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 1997, 49:71-81.
14. Coronado R., Latorre R. Phospholipid bilayers made from monolayers on patch-clamp pipettes. Biophys. J 1983, 43:231-236.
15. Cross D.A., Alessi D.R., Cohen P., Andjelkovich M., Hemmings B.A. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995, 378:785-789.
16. Derkach V., Barria A., Soderling T.R. Ca2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc. Natl. Acad. Sci. U S A 1999, 96:3269-3274.
17. Di Luca M., Ruts L., Gardoni F., Cattabeni F., Biessels G.J., Gispen W.H. NMDA receptor subunits are modified transcriptionally and post-translationally in the brain of streptozotocin-diabetic rats. Diabetologia 1999, 42:693-701.
18. Fitzjohn S.M., Morton R.A., Kuenzi F., Rosahl T.W., Shearman M., Lewis H., Smith D., Reynolds D.S., Davies C.H., Collingridge G.L., Seabrook G.R. Age-related impairment of synaptic transmission but normal long-term potentiation in transgenic mice that overexpress the human APP695SWE mutant form of amyloid precursor protein. J. Neurosci 2001, 21:4691-4698.
19. Gagne J., Milot M., Gelinas S., Lahsaini A., Trudeau F., Martinoli M.G., Massicotte G. Binding properties of glutamate receptors in streptozotocin-induced diabetes in rats. Diabetes 1997, 46:841-846.
20. Gardoni F., Kamal A., Bellone C., Biessels G.J., Ramakers G.M., Cattabeni F., Gispent W.H., Di Luca M. Effects of streptozotocin-diabetes on the hippocampal NMDA receptor complex in rats. J. Neurochem 2002, 80:438-447.
21. Gerozissis K. Brain insulin: regulation, mechanisms of action and functions. Cell. Mol. Neurobiol 2003, 23:1-25.
22. Grunblatt E., Salkovic-Petrisic M., Osmanovic J., Riederer P., Hoyer S. Brain insulin system dysfunction in streptozotocin intracerebroventricularly treated rats generates hyperphosphorylated tau protein. J. Neurochem 2007, 101:757-770.
23. Guo L., Yu W., Li X., Zhao G., Liang J., He P., Wang K., Zhou P., Jiang Y., Zhao M. Targeting of integrin-linked kinase with a small interfering RNA suppresses progression of experimental proliferative vitreoretinopathy. Exp. Eye Res 2008, 87:551-560.
24. Guo W., Jiang H., Gray V., Dedhar S., Rao Y. Role of the integrin-linked kinase (ILK) in determining neuronal polarity. Dev. Biol 2007, 306:457-468.
25. Hannigan G.E., Leung-Hagesteijn C., Fitz-Gibbon L., Coppolino M.G., Radeva G., Filmus J., Bell J.C., Dedhar S. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 1996, 379:91-96.
26. Hooper C., Markevich V., Plattner F., Killick R., Schofield E., Engel T., Hernandez F., Anderton B., Rosenblum K., Bliss T., Cooke S.F., Avila J., Lucas J.J., Giese K.P., Stephenson J., Lovestone S. Glycogen synthase kinase-3 inhibition is integral to long-term potentiation. Eur. J. Neurosci 2007, 25:81-86.
27. Hoyer S., Lee S.K., Loffler T., Schliebs R. Inhibition of the neuronal insulin receptor. An in vivo model for sporadic Alzheimer disease?. Ann. N Y Acad. Sci 2000, 920:256-258.
28. Hoyer S. Glucose metabolism and insulin receptor signal transduction in Alzheimer disease. Eur. J. Pharmacol 2004, 490:115-125.
29. Hsia A.Y., Masliah E., McConlogue L., Yu G.Q., Tatsuno G., Hu K., Kholodenko D., Malenka R.C., Nicoll R.A., Mucke L. Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc. Natl. Acad. Sci. U S A 1999, 96:3228-3233.
30. Johnson M.W., Chotiner J.K., Watson J.B. Isolation and characterization of synaptoneurosomes from single rat hippocampal slices. J. Neurosci. Methods 1997, 77:151-156.
31. Johnson-Farley N.N., Patel K., Kim D., Cowen D.S. Interaction of FGF-2 with IGF-1 and BDNF in stimulating Akt, ERK, and neuronal survival in hippocampal cultures. Brain Res 2007, 1154:40-49.
32. Johnston A.M., Pirola L., Van Obberghen E. Molecular mechanisms of insulin receptor substrate protein-mediated modulation of insulin signalling. FEBS Lett 2003, 546:32-36.
33. Kamal A., Biessels G.J., Ramakers G.M., Hendrik-Gispen W. The effect of short duration streptozotocin-induced diabetes mellitus on the late phase and threshold of long-term potentiation induction in the rat. Brain Res 2005, 1053:126-130.
34. Kamal A., Biessels G.J., Gispen W.H., Ramakers G.M. Synaptic transmission changes in the pyramidal cells of the hippocampus in streptozotocin-induced diabetes mellitus in rats. Brain Res 2006, 1073-1074. 276-280.
35. Katz B., Miledi R. The binding of acetylcholine to receptors and its removal from the synaptic cleft. J. Physiol 1973, 231:549-574.
36. Kim C.H., Lisman J.E. A role of actin filament in synaptic transmission and long-term potentiation. J. Neurosci 1999, 19:4314-4324.
37. Krucker T., Siggins G.R., Halpain S. Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc. Natl. Acad. Sci. U S A 2000, 97:6856-6861.
38. Lannert H., Hoyer S. Intracerebroventricular administration of streptozotocin causes long-term diminutions in learning and memory abilities and in cerebral energy metabolism in adult rats. Behav. Neurosci 1998, 112:1199-1208.
39. Lester-Coll N., Rivera E.J., Soscia S.J., Doiron K., Wands J.R., de la Monte S.M. Intracerebral streptozotocin model of type 3 diabetes: relevance to sporadic Alzheimer's disease. J. Alzheimers Dis 2006, 9:13-33.
40. Magleby K.L., Stevens C.F. The effect of voltage on the time course of end plate currents. J. Physiol 1972, 223:151-171.
41. Mayer G., Nitsch R., Hoyer S. Effects of changes in peripheral and cerebral glucose metabolism on locomotor activity, learning and memory in adult male rats. Brain Res 1990, 532:95-100.
42. Moechars D., Dewachter I., Lorent K., Reverse D., Baekelandt V., Naidu A., Tesseur I., Spittaels K., Haute C.V., Checler F., Godaux E., Cordell B., Van Leuven F. Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J. Biol. Chem 1999, 274:6483-6492.
43. Naska S., Park K.J., Hannigan G.E., Dedhar S., Miller F.D., Kaplan D.R. An essential role for the integrin-linked kinase-glycogen synthase kinase-3 beta pathway during dendrite initiation and growth. J. Neurosci 2006, 26:13344-13356.
44. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., LaFerla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 2003, 39:409-421.
45. Nitsch R., Hoyer S. Local action of the diabetogenic drug, streptozotocin, on glucose and energy metabolism in rat brain cortex. Neurosci. Lett 1991, 128:199-202.
46. Olds J.L., Golski S., McPhie D.L., Olton D., Mishkin M., Alkon D.L. Discrimination learning alters the distribution of protein kinase C in the hippocampus of rats. J. Neurosci 1990, 10:3707-3713.
47. Peineau S., Taghibiglou C., Bradley C., Wong T.P., Liu L., Lu J., Lo E., Wu D., Saule E., Bouschet T., Matthews P., Isaac J.T., Bortolotto Z.A., Wang Y.T., Collingridge G.L. LTP inhibits LTD in the hippocampus via regulation of GSK3beta. Neuron 2007, 53:703-717.
48. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
49. Plitzko D., Rumpel S., Gottmann K. Insulin promotes functional induction of silent synapses in differentiating rat neocortical neurons. Eur. J. Neurosci 2001, 14:1412-1415.
50. Pietropaolo S., Feldon J., Yee B.K. Age-dependent phenotypic characteristics of a triple transgenic mouse model of Alzheimer disease. Behav Neurosci 2008, 122:733-747.
51. Priller C., Dewachter I., Vassallo N., Paluch S., Pace C., Kretzschmar H.A., Van Leuven F., Herms J. Mutant presenilin 1 alters synaptic transmission in cultured hippocampal neurons. J. Biol. Chem 2007, 282:1119-1127.
52. Salkovic-Petrisic M., Tribl F., Schmidt M., Hoyer S., Riederer P. Alzheimer-like changes in protein kinase B and glycogen synthase kinase-3 in rat frontal cortex and hippocampus after damage to the insulin signalling pathway. J. Neurochem 2006, 96:1005-1015.
53. Salkovic-Petrisic M., Hoyer S. Central insulin resistance as a trigger for sporadic Alzheimer-like pathology: an experimental approach. J. Neural Transm. Suppl 2007, 217-233.
54. Shalaby T.H., Yousef M.K., Dupre R.K. Thermoregulatory responses of diabetic rats. Comp. Biochem. Physiol. A Comp. Physiol 1989, 94:153-157.
55. Skeberdis V.A., Lan J., Zheng X., Zukin R.S., Bennett M.V. Insulin promotes rapid delivery of N-methyl-D-aspartate receptors to the cell surface by exocytosis. Proc. Natl. Acad. Sci. U S A 2001, 98:3561-3566.
56. Soderling T.R. Modulation of glutamate receptors by calcium/calmodulin-dependent protein kinase II. Neurochem. Int 1996, 28:359-361.
57. Steen E., Terry B.M., Rivera E.J., Cannon J.L., Neely T.R., Tavares R., Xu X.J., Wands J.R., de la Monte S.M. Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease-is this type 3 diabetes?. J. Alzheimers Dis 2005, 7:63-80.
58. Sui L., Wang J., Li B.M. Role of the phosphoinositide 3-kinase-Akt-mammalian target of the rapamycin signaling pathway in long-term potentiation and trace fear conditioning memory in rat medial prefrontal cortex. Learn. Mem 2008, 15:762-776.
59. Ting J.T., Kelley B.G., Lambert T.J., Cook D.G., Sullivan J.M. Amyloid precursor protein overexpression depresses excitatory transmission through both presynaptic and postsynaptic mechanisms. Proc. Natl. Acad. Sci. U S A 2007, 104:353-358.
60. Tjalve H. Streptozotocin-Distribution, Metabolism and Mechanisms of Action. Ups. J. Med. Sci 1983, 145-157.
61. Vaithianathan T., Bedi D., Kanju P.M., Wang Z., Bahr B.A., Dityatev A., Judd R.L., Suppiramaniam V.D. Evidence of AMPA-Glutamate Receptor Dysfunction in Brain of Streptozotocin-Diabetic Rats 2003, 18. Society of Neuroscience.
62. Vaithianathan T., Manivannan K., Kleene R., Bahr B.A., Dey M.P., Dityatev A., Suppiramaniam V. Single channel recordings from synaptosomal AMPA receptors. Cell Biochem. Biophys 2005, 42:75-85.
63. Valastro B., Cossette J., Lavoie N., Gagnon S., Trudeau F., Massicotte G. Up-regulation of glutamate receptors is associated with LTP defects in the early stages of diabetes mellitus. Diabetologia 2002, 45:642-650.
64. Wang J.Y., Gualco E., Peruzzi F., Sawaya B.E., Passiatore G., Marcinkiewicz C., Staniszewska I., Ferrante P., Amini S., Khalili K., Reiss K. Interaction between serine phosphorylated IRS-1 and beta1-integrin affects the stability of neuronal processes. J. Neurosci. Res 2007, 85:2360-2373.
65. Werther G.A., Hogg A., Oldfield B.J., McKinley M.J., Figdor R., Allen A.M., Mendelsohn F.A. Localization and characterization of insulin receptors in rat brain and pituitary gland using in vitro autoradiography and computerized densitometry. Endocrinology 1987, 121:1562-1570.
66. Wu L.G., Saggau P. Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus. J. Neurosci 1994, 14:645-654.
67. Zhao W., Chen H., Xu H., Moore E., Meiri N., Quon M.J., Alkon D.L. 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.
68. Zhou Q., Xiao M., Nicoll R.A. Contribution of cytoskeleton to the internalization of AMPA receptors. Proc. Natl. Acad. Sci. U S A 2001, 98:1261-1266.
69. Zhu L.Q., Wang S.H., Liu D., Yin Y.Y., Tian Q., Wang X.C., Wang Q., Chen J.G., Wang J.Z. Activation of glycogen synthase kinase-3 inhibits long-term potentiation with synapse-associated impairments. J. Neurosci 2007, 27:12211-12220.
70. Zhu S.Q., Kum W., Ho S.K., Young J.D., Cockram C.S. Structure-function relationships of insulin receptor interactions in cultured mouse astrocytes. Brain Res 1990, 529:329-332.