Deficits in LTP and recognition memory in the genetically hypertensive rat are associated with decreased expression of neurotrophic factors and their receptors in the dentate gyrus

Behavioural Brain Research

Volumn 197, Issue 2, 2009, Pages 371-377

  Hennigan, Amy ^a   Callaghan, Charlotte K ^a   Kealy, John ^a   Rouine, Jennifer ^a   Kelly, Áine M ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

BDNF; Dentate gyrus; LTP; NGF; Recognition memory; Trk

Indexed keywords

ABELSON KINASE; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; LIGAND; NERVE GROWTH FACTOR; NEUROTROPHIC FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; NEUROTROPHIN 4; NEUROTROPHIN RECEPTOR; PROTEIN TYROSINE KINASE A; TYROSINE KINASE RECEPTOR;

AMNESIA; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE; COMPARATIVE STUDY; CONTROLLED STUDY; DENTATE GYRUS; GENETIC ASSOCIATION; HYPERTENSION; LEARNING DISORDER; LONG TERM MEMORY; LONG TERM POTENTIATION; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RAT STRAIN; RECOGNITION; WISTAR RAT;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DENTATE GYRUS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HYPERTENSION; LONG-TERM POTENTIATION; MALE; MEMORY; NERVE GROWTH FACTORS; NEUROTROPHIN 3; RATS; RATS, WISTAR; RECEPTOR, TRKA; RECEPTOR, TRKB; RECEPTOR, TRKC;

EID: 58149357248     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2008.09.037     Document Type: Article

References (43)

1. Atwal J.K., Massiem B., Millerm F.D., and Kaplan D.R. The TrkB-Shc site signals neuronal survival and local axon growth via MEK and P13-kinase. Neuron 27 (2000) 265-277
2. Binder D.K. Neurotrophins in the dentate gyrus. Prog Brain Res 163 (2007) 371-397
3. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72 (1976) 248-254
4. Bramham C.R., Southard T., Sarvey J.M., Herkenham M., and Brady L.S. Unilateral LTP triggers bilateral increases in hippocampal neurotrophin and trk receptor mRNA expression in behaving rats: evidence for interhemispheric communication. J Comp Neurol 368 (1996) 371-382
5. Casey M., Maguire C., Kelly A., Gooney M.A., and Lynch M.A. Analysis of the presynaptic signaling mechanisms underlying the inhibition of LTP in rat dentate gyrus by the tyrosine kinase inhibitor, genistein. Hippocampus 12 (2002) 377-385
6. Castren E., Pitkanen M., Sirvio J., Parsadanian A., Lindholm D., Thoenen H., et al. The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus. Neuroreport 4 (1993) 895-898
7. Chen K.S., Nishimura M.C., Armanini M.P., Crowley C., Spencer S.D., and Phillips H.S. Disruption of a single allele of the nerve growth factor gene results in atrophy of basal forebrain cholinergic neurons and memory deficits. J Neurosci 17 (1997) 7288-7296
8. Chen X., Garelick M.G., Wang H., Lil V., Athos J., and Storm D.R. PI3 kinase signaling is required for retrieval and extinction of contextual memory. Nat Neurosci 8 (2005) 925-931
9. Christie B.R., and Cameron H.A. Neurogenesis in the adult hippocampus. Hippocampus 16 (2006) 199-207
10. Clark R.E., West A.N., Zola S.M., and Squire L.R. Rats with lesions of the hippocampus are impaired on the delayed nonmatching-to-sample task. Hippocampus 11 (2001) 176-186
11. Clements K.M., and Wainwright P.E. Spontaneously hypertensive, Wistar-Kyoto and Sprague-Dawley rats differ in performance on a win-shift task in the water radial arm maze. Behav Brain Res 167 (2006) 295-304
12. Conover J.C., and Yancopoulos G.D. Neurotrophin regulation of the developing nervous system: analyses of knockout mice. Rev Neurosci 8 (1997) 13-27
13. Diana G., Domenici M.R., Loizzo A., Scotti de Carolis A., and Sagratella S. Age and strain differences in rat place learning and hippocampal dentate gyrus frequency-potentiation. Neurosci Lett 171 (1994) 113-116
14. Egan M.F., Kojima M., Callicott J.H., Goldberg T.E., Kolachana B.S., Bertolino A., et al. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112 (2003) 257-269
15. Fischer W., Bjorklund A., Chen K., and Gage F.H. NGF improves spatial memory in aged rodents as a function of age. J Neurosci 11 (1991) 1889-1906
16. Gentry J.J., Barker P.A., and Carter B.D. The p75 neurotrophin receptor: multiple interactors and numerous functions. Prog Brain Res 146 (2004) 25-39
17. Gooney M., Shaw K., Kelly A., O'Mara S.M., and Lynch M.A. Long-term potentiation and spatial learning are associated with increased phosphorylation of TrkB and extracellular signal-regulated kinase (ERK) in the dentate gyrus: evidence for a role for brain-derived neurotrophic factor. Behav Neurosci 116 (2002) 455-463
18. Heldt S.A., Stanek L., Chhatwal J.P., and Ressler K.J. Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol Psychiatry 12 (2007) 656-670
19. Hennigan A., Trotter C., and Kelly A.M. Lipopolysaccharide impairs long-term potentiation and recognition memory and increases p75NTR expression in the rat dentate gyrus. Brain Res 1130 (2007) 158-166
20. Hernandez C.M., Høifødt H., and Terry A.V. Spontaneously hypertensive rats: further evaluation of age-related memory performance and cholinergic marker expression. J Psychiatry Neurosci 28 (2003) 197-209
21. Kelly A., Conroy S., and Lynch M.A. Evidence that nerve growth factor plays a role in long-term potentiation in the rat dentate gyrus. Neuropharmacology 37 (1998) 561-570
22. Kelly A., and Lynch M.A. LTP occludes the interaction between arachidonic acid and ACPD and NGF and ACPD. Neuroreport 9 (1998) 4087-4091
23. Kelly A., Maguire C., and Lynch M.A. Deficits in nerve growth factor release and tyrosine receptor kinase phosphorylation are associated with age-related impairment in long-term potentiation in the dentate gyrus. Neurosci 95 (1999) 359-365
24. Kelly A., and Lynch M.A. Long-term potentiation in dentate gyrus of the rat is inhibited by the phosphoinositide 3-kinase inhibitor, wortmannin. Neuropharmacol 39 (2000) 643-651
25. Kelly A., Laroche S., and Davis S. Activation of the MAP kinase pathway is necessary for the consolidation and reconsolidation of long-term recognition memory. J Neurosci 23 (2003) 5354-5360
26. Koponen E., Võikar V., Riekki R., Saarelainen T., Rauramaa T., Rauvala H., et al. Transgenic mice overexpressing the full-length neurotrophin receptor trkB exhibit increased activation of the trkB-PLCgamma pathway, reduced anxiety, and facilitated learning. Mol Cell Neurosci 26 (2004) 166-181
27. Korte M., Carroll P., Wolf E., Brem G., Thoenen H., and Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci USA 92 (1995) 8856-8860
28. Messina A., and Bell C. Are genetically hypertensive rats deficient in nerve growth factor?. Neuroreport 2 (1991) 45-48
29. Minichiello L., Korte M., Wolfer D., Kühn R., Unsicker K., Cestari V., et al. Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24 (1999) 401-414
30. McGahon B., and Lynch M.A. Analysis of the interaction between arachidonic acid and metabotropic glutamate receptor activation reveals that phospholipase C acts as a coincidence detector in the expression of long-term potentiation in the rat dentate gyrus. Hippocampus 8 (1998) 48-56
31. Muller D., Molinari I., Soldati L., and Bianchi G. A genetic deficiency in calpastatin and isovalerylcarnitine treatment is associated with enhanced hippocampal long-term potentiation. Synapse 19 (1995) 37-45
32. O'Callaghan R.M., Ohle R., and Kelly A.M. The effects of forced exercise on hippocampal plasticity in the rat: a comparison of LTP, spatial- and non-spatial learning. Behav Brain Res 176 (2007) 362-366
33. Patterson S.L., Abel T., Deuel T.A., Martin K.C., Rose J.C., and Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16 (1996) 1137-1145
34. Reichardt L.F. Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 361 1473 (2006) 1545-1564
35. Robertson B.A., Clements K.M., and Wainwright P.E. The working memory capabilities of the spontaneously hypertensive rat. Physiol Behav 94 (2008) 481-486
36. Shimazu K., Zhao M., Sakata K., Akbarian S., Bates B., Jaenisch R., et al. NT-3 facilitates hippocampal plasticity and learning and memory by regulating neurogenesis. Learn Mem 13 (2006) 307-315
37. Terry Jr. A.V., Hernandez C.M., Buccafusco J.J., and Gattu M. Deficits in spatial learning and nicotinic-acetylcholine receptors in older, spontaneously hypertensive rats. Neuroscience (2000) 101357-101368
38. Thomas S.M., DeMarco M., D'Arcangelo G., Halegoua S., and Brugge J.S. Ras is essential for nerve growth factor- and phorbol ester-induced tyrosine phosphorylation of MAP kinases. Cell 68 (1992) 1031-1040
39. Vetter M.L., Martin-Zanca D., Parada L.F., Bishop J.M., and Kaplan D.R. Nerve growth factor rapidly stimulates tyrosine phosphorylation of phospholipase C-gamma 1 by a kinase activity associated with the product of the trk protooncogene. Proc Natl Acad Sci USA 88 (1991) 5650-5654
40. Vuberti F., Capsoni S., Comparini A., Di Daniel E., Franzot J., Gonfloni S., et al. Phenotypic knockout of nerve growth factor in adult transgenic mice reveals severe deficits in basal forebrain cholinergic neurons, cell death in the spleen, and skeletal muscle dystrophy. J Neurosci. 20 7 (2000 Apr 1) 2589-2601
41. Vyssotski A.L., Dell'Omo G., Poletaeva I.I., Vyssotsk D.L., Minichiello L., Klein R., et al. Long-term monitoring of hippocampus-dependent behavior in naturalistic settings: mutant mice lacking neurotrophin receptor TrkB in the forebrain show spatial learning but impaired behavioral flexibility. Hippocampus 12 (2002) 27-38
42. Woolf N.J., Milov A.M., Schweitzer E.S., and Roghani A. Elevation of nerve growth factor and antisense knockdown of TrkA receptor during contextual memory consolidation. J Neurosci 21 (2001) 1047-1055
43. Xie C.W., Sayah D., Chen Q.S., Wei W.Z., Smith D., and Liu X. Deficient long-term memory and long-lasting long-term potentiation in mice with a targeted deletion of neurotrophin-4 gene. Proc Natl Acad Sci USA 97 (2000) 8116-8121