Adult-onset hypothyroidism facilitates and enhances LTD: Reversal by chronic nicotine treatment

Neurobiology of Disease

Volumn 26, Issue 1, 2007, Pages 264-272

  Alzoubi, K H ^c   Aleisa, A M ^b   Alkadhi, K A ^a  

^a UNIVERSITY OF HOUSTON   (United States)

^b KING SAUD UNIVERSITY   (Saudi Arabia)

^c JORDAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Jordan)

Author keywords

4 2nAChRs; 7nAChRs; BDNF; NR1; NR2A; NR2B; Paired pulse stimulation; Thyroidectomy

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BUNGAROTOXIN RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NICOTINE; NICOTINIC RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; HYPOTHYROIDISM; LONG TERM DEPRESSION; MALE; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; SPATIAL MEMORY; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION; THYROIDECTOMY; WESTERN BLOTTING; WISTAR RAT;

ANIMALS; BLOTTING, WESTERN; BRAIN-DERIVED NEUROTROPHIC FACTOR; ELECTROPHYSIOLOGY; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HIPPOCAMPUS; HYPOTHYROIDISM; LEARNING; MALE; NEURONAL PLASTICITY; NICOTINE; NICOTINIC AGONISTS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, NICOTINIC; SPACE PERCEPTION; THYROIDECTOMY;

EID: 33947218771     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2007.01.002     Document Type: Article

References (67)

1. Adriani W., Granstrem O., Macri S., Izykenova G., Dambinova S., and Laviola G. Behavioral and neurochemical vulnerability during adolescence in mice: studies with nicotine. Neuropsychopharmacology 29 (2004) 869-878
2. Akaneya Y., Tsumoto T., and Hatanaka H. Brain-derived neurotrophic factor blocks long-term depression in rat visual cortex. J. Neurophysiol. 76 (1996) 4198-4201
3. Akaneya Y., Tsumoto T., Kinoshita S., and Hatanaka H. Brain-derived neurotrophic factor enhances long-term potentiation in rat visual cortex. J. Neurosci. 17 (1997) 6707-6716
4. Aleisa A.M., Alzoubi K.H., and Alkadhi K.A. Nicotine prevents stress-induced enhancement of long-term depression in hippocampal area CA1: electrophysiological and molecular studies. J. Neurosci. Res. 83 (2006) 309-317
5. Alzoubi K.H., and Alkadhi K.A. The critical role of CREB in hypothyroidism induced L-LTP impairment. Exp. Neurol. 203 1 (2007) 63-71
6. Alzoubi K.H., Bedawi A.S., Aleisa A.M., and Alkadhi K.A. Hypothyroidism impairs long-term potentiation in sympathetic ganglia: electrophysiologic and molecular studies. J. Neurosci. Res. 78 (2004) 393-402
7. Alzoubi K.H., Gerges N.Z., and Alkadhi K.A. Levothyroxin restores hypothyroidism-induced impairment of LTP of hippocampal CA1: electrophysiological and molecular studies. Exp. Neurol. 195 (2005) 330-341
8. Alzoubi K.H., Aleisa A.M., and Alkadhi K.A. Impairment of long-term potentiation in the CA1, but not dentate gyrus, of the hippocampus in Obese Zucker rats: role of calcineurin and phosphorylated CaMKII. J. Mol. Neurosci. 27 (2005) 337-346
9. Alzoubi K.H., Aleisa A.M., and Alkadhi K.A. Molecular studies on the protective effect of nicotine in adult-onset hypothyroidism-induced impairment of long-term potentiation. Hippocampus 16 10 (2006) 861-874
10. Alzoubi K.H., Aleisa A.M., Gerges N.Z., and Alkadhi K.A. Nicotine reverses adult-onset hypothyroidism-induced impairment of learning and memory: behavioral and electrophysiological studies. J. Neurosci. Res. 84 5 (2006) 944-953
11. Anwyl R. Induction and expression mechanisms of postsynaptic NMDA receptor-independent homosynaptic long-term depression. Prog. Neurobiol. 78 1 (2006) 17-37
12. Bear M.F., and Abraham W.C. Long-term depression in hippocampus. Annu. Rev. Neurosci. 19 (1996) 437-462
13. Beattie E.C., Carroll R.C., Yu X., Morishita W., Yasuda H., vonZastrow M., and Malenka R.C. Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat. Neurosci. 3 (2000) 1291-1300
14. Breese C.R., Hampson R.E., and Deadwyler S.A. Hippocampal place cells: stereotypy and plasticity. J. Neurosci. 9 (1989) 1097-1111
15. Castro N.G., and Albuquerque E.X. alpha-Bungarotoxin-sensitive hippocampal nicotinic receptor channel has a high calcium permeability. Biophys. J. 68 (1995) 516-524
16. Collingridge G.L., Kehl S.J., and McLennan H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J. Physiol. 334 (1983) 33-46
17. Doyere V., Errington M.L., Laroche S., and Bliss T.V. Low-frequency trains of paired stimuli induce long-term depression in area CA1 but not in dentate gyrus of the intact rat. Hippocampus 6 (1996) 52-57
18. Dudek S.M., and Bear M.F. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-d-aspartate receptor blockade. Proc. Natl. Acad Sci. U. S. A. 89 (1992) 4363-4367
19. Errington M.L., Bliss T.V., Richter-Levin G., Yenk K., Doyere V., and Laroche S. Stimulation at 1-5 Hz does not produce long-term depression or depotentiation in the hippocampus of the adult rat in vivo. J. Neurophysiol. 74 (1995) 1793-1799
20. Ferchmin P.A., Perez D., Eterovic V.A., and de Vellis J. Nicotinic receptors differentially regulate N-methyl-d-aspartate damage in acute hippocampal slices. J. Pharmacol. Exp. Ther. 305 (2003) 1071-1078
21. Figurov A., Pozzo-Miller L.D., Olafsson P., Wang T., and Lu B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381 (1996) 706-709
22. French S.J., Humby T., Horner C.H., Sofroniew M.V., and Rattray M. Hippocampal neurotrophin and trk receptor mRNA levels are altered by local administration of nicotine, carbachol and pilocarpine. Brain Res. Mol. Brain Res. 67 (1999) 124-136
23. Frotscher M., and Leranth C. Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J. Comp. Neurol. 239 (1985) 237-246
24. Fujii S., and Sumikawa K. Nicotine accelerates reversal of long-term potentiation and enhances long-term depression in the rat hippocampal CA1 region. Brain Res. 894 (2001) 340-346
25. Fujii S., Saito K., Miyakawa H., Ito K., and Kato H. Reversal of long-term potentiation (depotentiation) induced by tetanus stimulation of the input to CA1 neurons of guinea pig hippocampal slices. Brain Res. 555 (1991) 112-122
26. Fujii S., Ji Z., and Sumikawa K. Inactivation of alpha7 ACh receptors and activation of non-alpha7 ACh receptors both contribute to long term potentiation induction in the hippocampal CA1 region. Neurosci. Lett. 286 (2000) 134-138
27. Gerges N.Z., and Alkadhi K.A. Hypothyroidism impairs late LTP in CA1 region but not in dentate gyrus of the intact rat hippocampus: MAPK involvement. Hippocampus 14 (2004) 40-45
28. Gerges N.Z., Stringer J.L., and Alkadhi K.A. Combination of hypothyroidism and stress abolishes early LTP in the CA1 but not dentate gyrus of hippocampus of adult rats. Brain Res. 922 (2001) 250-260
29. Gerges N.Z., Aleisa A.M., Schwarz L.A., and Alkadhi K.A. Reduced basal CaMKII levels in hippocampal CA1 region: possible cause of stress-induced impairment of LTP in chronically stressed rats. Hippocampus 14 (2004) 402-410
30. Gerges N.Z., Alzoubi K.H., Park C.R., Diamond D.M., and Alkadhi K.A. Adverse effect of the combination of hypothyroidism and chronic psychosocial stress on hippocampus-dependent memory in rats. Behav. Brain Res. 155 (2004) 77-84
31. Gerges N.Z., Alzoubi K.H., and Alkadhi K.A. Role of phosphorylated CaMKII and calcineurin in the differential effect of hypothyroidism on LTP of CA1 and dentate gyrus. Hippocampus 15 (2005) 480-490
32. Gray R., Rajan A.S., Radcliffe K.A., Yakehiro M., and Dani J.A. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383 (1996) 713-716
33. Ho O.H., Delgado J.Y., and O'Dell T.J. Phosphorylation of proteins involved in activity-dependent forms of synaptic plasticity is altered in hippocampal slices maintained in vitro. J. Neurochem. 91 (2004) 1344-1357
34. Kang H., Welcher A.A., Shelton D., and Schuman E.M. Neurotrophins and time: different roles for TrkB signaling in hippocampal long-term potentiation. Neuron 19 (1997) 653-664
35. Kenny PJ., File S.E., and Rattray M. Acute nicotine decreases, and chronic nicotine increases the expression of brain-derived neurotrophic factor mRNA in rat hippocampus. Brain Res. Mol. Brain Res. 85 (2000) 234-238
36. Kiprianova I., Sandkuhler J., Schwab S., Hoyer S., and Spranger M. Brain-derived neurotrophic factor improves long-term potentiation and cognitive functions after transient forebrain ischemia in the rat. Exp. Neurol. 159 (1999) 511-519
37. Kiyama Y., Manabe T., Sakimura K., Kawakami F., Mori H., and Mishina M. Increased thresholds for long-term potentiation and contextual learning in mice lacking the NMDA-type glutamate receptor epsilon1 subunit. J. Neurosci. 18 (1998) 6704-6712
38. Kobayashi K., Tsuji R., Yoshioka T., Kushida M., Yabushita S., Sasaki M., Mino T., and Seki T. Effects of hypothyroidism induced by perinatal exposure to PTU on rat behavior and synaptic gene expression. Toxicology 212 (2005) 135-147
39. Kobayashi K., Tsuji R., Yoshioka T., Mino T., and Seki T. Perinatal exposure to PTU delays switching from NR2B to NR2A subunits of the NMDA receptor in the rat cerebellum. Neurotoxicology 27 (2006) 284-290
40. Kohr G., Jensen V., Koester H.J., Mihaljevic A.L., Utvik J.K., Kvello A., Ottersen O.P., Seeburg P.H., Sprengel R., and Hvalby O. Intracellular domains of NMDA receptor subtypes are determinants for long-term potentiation induction. J. Neurosci. 23 (2003) 10791-10799
41. Korte M., Staiger V., Griesbeck O., Thoenen H., and Bonhoeffer T. The involvement of brain-derived neurotrophic factor in hippocampal long-term potentiation revealed by gene targeting experiments. J. Physiol. (Paris) 90 (1996) 157-164
42. Kutsuwada T., Kashiwabuchi N., Mori H., Sakimura K., Kushiya E., Araki K., Meguro H., Masaki H., Kumanishi T., and Arakawa M. Molecular diversity of the NMDA receptor channel. Nature 358 (1992) 36-41
43. Lee P.R., Brady D., and Koenig J.I. Thyroid hormone regulation of N-methyl-d-aspartic acid receptor subunit mRNA expression in adult brain. J. Neuroendocrinol. 15 (2003) 87-92
44. Levin E.D. Nicotinic receptor subtypes and cognitive function. J. Neurobiol. 53 (2002) 633-640
45. Levin E.D., Lee C., Rose J.E., Reyes A., Ellison G., Jarvik M., and Gritz E. Chronic nicotine and withdrawal effects on radial-arm maze performance in rats. Behav. Neural Biol. 53 (1990) 269-276
46. Levin E.D., Conners C.K., Silva D., Hinton S.C., Meck W.H., March J., and Rose J.E. Transdermal nicotine effects on attention. Psychopharmacology (Berlin) 140 (1998) 135-141
47. Liu L., Wong T.P., Pozza M.F., Lingenhoehl K., Wang Y., Sheng M., Auberson Y.P., and Wang Y.T. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304 (2004) 1021-1024
48. Lynch M.A. Long-term potentiation and memory. Physiol. Rev. 84 (2004) 87-136
49. Ma Y.L., Wang H.L., Wu H.C., Wei C.L., and Lee E.H. Brain-derived neurotrophic factor antisense oligonucleotide impairs memory retention and inhibits long-term potentiation in rats. Neuroscience 82 (1998) 957-967
50. Mallon A.P., Auberson Y.P., and Stone T.W. Selective subunit antagonists suggest an inhibitory relationship between NR2B and NR2A-subunit containing N-methyl-d-aspartate receptors in hippocampal slices. Exp. Brain Res. 162 3 (2005) 374-383
51. Manahan-Vaughan D., and Braunewell K.H. Novelty acquisition is associated with induction of hippocampal long-term depression. Proc. Natl. Acad Sci. U. S. A. 96 (1999) 8739-8744
52. Mansuy I.M., Winder D.G., Moallem T.M., Osman M., Mayford M., Hawkins R.D., and Kandel E.R. Inducible and reversible gene expression with the rtTA system for the study of memory. Neuron 21 (1998) 257-265
53. Massey P.V., Johnson B.E., Moult P.R., Auberson Y.P., Brown M.W., Molnar E., Collingridge G.L., and Bashir Z.I. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J. Neurosci. 24 (2004) 7821-7828
54. Miller K.J., Parsons T.D., Whybrow P.C., van Herle K., Rasgon N., vanHerle A., Martinez D., Silverman D.H., and Bauer M. Memory improvement with treatment of hypothyroidism. Int. J. Neurosci. 116 (2006) 895-906
55. Mulkey R.M., Endo S., Shenolikar S., and Malenka R.C. Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369 (1994) 486-488
56. Paterson D., and Nordberg A. Neuronal nicotinic receptors in the human brain. Prog. Neurobiol. 61 (2000) 75-111
57. Prendergast M.A., Harris B.R., Mayer S., Holley R.C., Hauser K.F., and Littleton J.M. Chronic nicotine exposure reduces N-methyl-d-aspartate receptor-mediated damage in the hippocampus without altering calcium accumulation or extrusion: evidence of calbindin-D28K overexpression. Neuroscience 102 (2001) 75-85
58. Sans N., Petralia R.S., Wang Y.X., Blahos J., Hell J.W., and Wenthold R.J. A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J. Neurosci. 20 (2000) 1260-1271
59. Sui L., Wang F., and Li B.M. Adult-onset hypothyroidism impairs paired-pulse facilitation and long-term potentiation of the rat dorsal hippocampo-medial prefrontal cortex pathway in vivo. Brain Res. 1096 (2006) 53-60
60. Thiels E., Xie X., Yeckel M.F., Barrionuevo G., and Berger T.W. NMDA receptor-dependent LTD in different subfields of hippocampus in vivo and in vitro. Hippocampus 6 (1996) 43-51
61. Thiels E., Kanterewicz B.I., Knapp L.T., Barrionuevo G., and Klann E. Protein phosphatase-mediated regulation of protein kinase C during long-term depression in the adult hippocampus in vivo. J. Neurosci. 20 (2000) 7199-7207
62. Tsien J.Z., Huerta P.T., and Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87 (1996) 1327-1338
63. Vara H., MunozCuevas J., and Colino A. Age-dependent alterations of long-term synaptic plasticity in thyroid-deficient rats. Hippocampus 13 (2003) 816-825
64. Wada E., Wada K., Boulter J., Deneris E., Heinemann S., Patrick J., and Swanson L.W. Distribution of alpha 2, alpha 3, alpha 4, and beta 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat. J. Comp. Neurol. 284 (1989) 314-335
65. Wall A., Gong Z.H., Johnson A.E., Meyerson B., and Zhang X. Cross-tolerance in drug response and differential changes in central nicotinic and N-methyl-d-aspartate receptor binding following chronic treatment with either (+)- or (-)-nicotine. Psychopharmacology (Berlin) 148 (2000) 186-195
66. Wang J.H., and Kelly P.T. Postsynaptic calcineurin activity downregulates synaptic transmission by weakening intracellular Ca2+ signaling mechanisms in hippocampal CA1 neurons. J. Neurosci. 17 (1997) 4600-4611
67. Winder D.G., Mansuy I.M., Osman M., Moallem T.M., and Kandel E.R. Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin. Cell 92 (1998) 25-37