Glutamate Receptor Subunit and Calmodulin Kinase II Expression, with and without T Maze Training, in the Rat Hippocampus following Bilateral Vestibular Deafferentation

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Zheng, Yiwen ^a   Wilson, Georgina ^a   Stiles, Lucy ^a   Smith, Paul F ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; GLUTAMATE RECEPTOR 4; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILATERAL VESTIBULAR DEAFFERENTATION; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; DENTATE GYRUS; ENZYME PHOSPHORYLATION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; MALE; MAZE TEST; MEMORY DISORDER; NEUROLOGICAL AND SENSORIAL PROCEDURES; NONHUMAN; PROTEIN EXPRESSION; RAT; RECEPTOR DOWN REGULATION; SPATIAL LEARNING; SPATIAL MEMORY; TRAINING; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CLUSTER ANALYSIS; HIPPOCAMPUS; MALE; MAZE LEARNING; NEURONS, AFFERENT; PROTEOME; RATS; RATS, WISTAR; RECEPTORS, GLUTAMATE;

EID: 84873597795     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054527     Document Type: Article

References (53)

1. Stackman R, Herbert A, (2002) Rats with lesions of the vestibular system require a visual landmark for spatial navigation. Behav Brain Res 128: 27-40.
2. Wallace D, Hines D, Pellis S, Whishaw I, (2002) Vestibular information is required for dead reckoning in the rat. J Neurosci 22: 10009-10017.
3. Russell N, Horii A, Smith PF, Darlington CL, Bilkey DK, (2003) Bilateral peripheral vestibular lesions produce long-term changes in spatial learning in the rat. J Vest Res 13: 9-16.
4. Zheng Y, Darlington C, Smith PF, (2006) Impairment and recovery on a food foraging task following unilateral vestibular deafferentation in rats. Hippocampus 16: 368-378.
5. Zheng Y, Goddard M, Darlington C, Smith PF, (2007) Bilateral vestibular deafferentation impairs performance in a spatial forced alternation task in rats. Hippocampus 17: 253-256.
6. Zheng Y, Goddard M, Darlington C, Smith PF, (2009) Long-term deficits on a foraging task after bilateral vestibular deafferentation in rats. Hippocampus 19: 480-486.
7. Baek J, Zheng Y, Darlington C, Smith PF, (2010) Evidence that spatial memory deficits following bilateral vestibular deafferentation in rats are probably permanent. Neurobiol Learn Mem 94: 402-413.
8. Besnard S, Machado M, Vignaux G, Boulouard M, Coquerel A, et al. (2012) Influence of vestibular input on spatial and nonspatial memory and on hippocampal NMDA receptors. Hippocampus 22: 814-826.
9. Neo P, Carter D, Zheng Y, Smith PF, Darlington CL, et al. (2012) Septal elicitation of hippocampal theta rhythm did not repair the cognitive and emotional deficits resulting from vestibular lesions. Hippocampus 22: 1176-1187.
10. Brandt T, Schautzer F, Hamilton D, Brüning R, Markowitsch H, et al. (2005) Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128: 2732-2741.
11. Stackman R, Clark A, Taube J, (2002) Hippocampal spatial representations require vestibular input. Hippocampus 12: 291-303.
12. Russell N, Horii A, Smith PF, Darlington CL, Bilkey DK, (2003) Long-term effects of permanent vestibular lesions on hippocampal spatial firing. J Neurosci 23: 6490-6498.
13. Russell N, Horii A, Smith PF, Darlington CL, Bilkey DK, (2006) Lesions of the vestibular system disrupt hippocampal theta rhythm in the rat. J Neurophysiol 96: 4-14.
14. Tai SK, Ma J, Ossenkopp KP, Leung LS, (2012) Activation of immobility-related hippocampal theta by cholinergic septohippocampal neurons during vestibular stimulation. Hippocampus 22: 914-925.
15. Zheng Y, Balabhadrapatruni S, Chung P, Gliddon CM, Zhang M, et al. (2012) The effects of bilateral vestibular loss on hippocampal volume, neuronal number and cell proliferation in rats. Frontiers in Neuro-Otology. 3 20: 1-8 doi:10.3389/fneur.2012.00020.
16. Zheng Y, Mason-Parker S, Logan B, Darlington C, Smith PF, et al. (2010) Hippocampal synaptic transmission and LTP in vivo are intact following bilateral vestibular deafferentation in the rat. Hippocampus 20: 461-468.
17. Liu P, Zheng Y, King J, Darlington C, Smith PF, (2003) Long-term change in hippocampal N-methyl-D-asparate receptor subunits following unilateral vestibular damage in rat. Neurosci 117: 965-970.
18. Petralia R, Yokotani N, Wenthold R, (1994) Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J Neurosci 14: 667-696.
19. Kutsuwada T, Kashiwabuchi N, Mori H, Sakimura K, Kushiya E, et al. (1992) Molecular diversity of the NMDA receptor channel. Nature 358: 36-41.
20. Ishii T, Moriyoshi K, Sugihara H, Sakurada K, Kadotani H, et al. (1993) Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J Biol Chem 268: 2836-2843.
21. Krupp J, Vissel B, Heinemann S, Westbrook G, (1998) N-terminal domains in the NR2 subunit control desensitization of NMDA receptors. Neuron 20: 317-327.
22. Williams K, Zappia A, Pritchett D, Shen Y, Molinoff P, (1994) Sensitivity of the N-methyl-D-aspartate receptor to polyamines is controlled by NR2 subunits. Mol Pharmacol 45: 803-809.
23. Craig A, Blackstone C, Huganir R, Banker G, (1993) The distribution of glutamate receptors in cultured rat hippocampal neurons: postsynaptic clustering of AMPA selective subunits. Neuron 10: 1055-1068.
24. Geiger J, Melcher T, Koh D, Sakmann B, Seeburg P, et al. (1995) Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15: 193-204.
25. Wenthold R, Petralia R, Blahos J, Niedzielski A, (1996) Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 16: 1982-1989.
26. Leonard A, Lim I, Hemsworth D, Horne M, Hell J, (1999) Calcium/calmodulin-dependent protein kinase II is associated with the N-methyl-D-aspartate receptor. PNAS USA 96: 3239-3244.
27. Barria A, Derkach V, Griffith L, Muller D, Soderling T, (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaMKII during long-term potentiation. Science 276: 2042-2045.
28. Giese K, Fedorov N, Filipkowski R, Silva A, (1998) Autophosphorylation at Thr286 of the calcium-calmodulin kinase II in LTP and learning. Science 279: 870-873.
29. Smith PF, Curthoys IS, (1989) Mechanisms of recovery following unilateral labyrinthectomy: a review. Brain Res Revs 14: 155-180.
30. Zheng Y, Horii A, Appleton I, Darlington C, Smith PF, (2001) Damage to the vestibular inner ear causes long-term changes in neuronal nitric oxide synthase expression in the rat hippocampus. Neurosci 105: 1-5.
31. Wang HY, Stucky A, Liu J, Shen C, Trocme-Thibierge C, et al. (2009) Dissociating beta-amyloid from alpha 7 nicotinic acetylcholine receptor by a novel therapeutic agent, S 24795, normalizes alpha 7 nicotinic acetylcholine and NMDA receptor function in Alzheimer's disease brain. J Neurosci 29(35): 10961-10973.
32. Wang HY, Crupi D, Liu J, Stucky A, Cruciata G, et al. (2011) Repetitive transcranial magnetic stimulation enhances BDNF-TrkB signaling in both brain and lymphocyte. J Neurosci 31(30): 11044-11054.
33. Han X, Tomitori H, Mizuno S, Higashi K, Füll C, et al. (2008) Binding of spermine and ifenprodil to a purified, soluble regulatory domain of the N-methyl-D-aspartate receptor. J Neurochem 107(6): 1566-1577.
34. Yun-Hong Y, Chih-Fan C, Chia-Wei C, Yen-Chung C, (2011) A study of the spatial protein organization of the postsynaptic density isolated from porcine cerebral cortex and cerebellum. Mol Cell Proteomics 10(10): M110.007138.
35. Kennard JT, Barmanray R, Sampurno S, Ozturk E, Reid CA, et al. (2011) Stargazin and AMPA receptor membrane expression is increased in the somatosensory cortex of Genetic Absence Epilepsy Rats from Strasbourg. Neurobiol Dis 42(1): 48-54.
36. Bakshi K, Gennaro S, Chan CY, Kosciuk M, Liu J, et al. (2009) Prenatal cocaine reduces AMPA receptor synaptic expression through hyperphosphorylation of the synaptic anchoring protein GRIP. J Neurosci 29(19): 6308-6319.
37. Dhar SS, Liang HL, Wong-Riley MT, (2009) Nuclear respiratory factor 1 co-regulates AMPA glutamate receptor subunit 2 and cytochrome c oxidase: tight coupling of glutamatergic transmission and energy metabolism in neurons. J Neurochem 108(6): 1595-1606.
38. Little GH, Saw A, Bai Y, Dow J, Marjoram P, et al. (2009) Critical role of nuclear calcium/calmodulin-dependent protein kinase IIdeltaB in cardiomyocyte survival in cardiomyopathy. J Biol Chem 284(37): 24857-24868.
39. Kojundzic SL, Puljak L, Hogan Q, Sapunar D, (2010) Depression of Ca(2+)/calmodulin-dependent protein kinase II in dorsal root ganglion neurons after spinal nerve ligation. J Comp Neurol 518(1): 64-74.
40. Roscioli E, Di Francesco L, Bolognesi A, Giubettini M, Orlando S, et al. (2012) Importin-β negatively regulates multiple aspects of mitosis including RANGAP1 recruitment to kinetochores. J Cell Biol 196(4): 435-450.
41. Manly BFJ (2005) Multivariate Statistical Methods: A Primer (3rd Edition). London: Chapman & Hall/CRC.
42. Marcoulides GA, Hershberger SL (1997) Multivariate Statistical Methods. A First Course. Lawrence Erlbaum Assoc., Mahwah, New Jersey.
43. Tabachnick BG, Fidell LS (2007) Using Multivariate Statistics. 5th Edition. Pearson Education Inc. Boston.
44. Goddard M, Zheng Y, Darlington C, Smith PF, (2008) Locomotor and exploratory behavior in the rat following bilateral vestibular deafferentation. Behav Neurosci 122: 448-459.
45. Vignaux G, Chabbert C, Gaboyard-Niay S, Travo C, Machado ML, et al. (2012) Evaluation of the chemical model of vestibular lesions induced by arsanilate in rats. Toxicol Appl Pharmacol 258(1): 61-71.
46. Hitier M, Besnard S, Vignaux G, Denise P, Moreau S, (2010) The ventrolateral surgical approach to labyrinthectomy in rats: anatomical description and clinical consequences. Surg Radiol Anat 32(9): 835-842.
47. Poisnel G, Quentin T, Barré L, Coquerel A, Debruyne D, (2006) Competitive displacement binding assay on rat brain sections and using a beta-imager: application to mu-opioid ligands. J Neurosci Methods 154(1-2): 60-67.
48. Langlois X, te Riele P, Wintmolders C, Leysen JE, Jurzak M, (2001) Use of the beta-imager for rapid ex vivo autoradiography exemplified with central nervous system penetrating neurokinin 3 antagonists. J Pharmacol Exp Ther 299(2): 712-717.
49. Zheng Y, Kerr D, Darlington C, Smith PF, (2003) Unilateral inner ear damage results in lasting changes in hippocampal CA1 field potentials in vitro. Hippocampus 13: 873-878.
50. Ghafari M, Falsafi SK, Hoeger H, Lubec G, (2012) Hippocampal levels of GluR1 and GluR2 complexes are modulated by training in the multiple T-Maze in C57BL/6J mice. Brain Struct Funct 217(2): 353-62.
51. Heo S, Jung G, Beuk T, Höger H, Lubec G, (2012) Hippocampal glutamate transporter 1 (GLT-1) complex levels are paralleling memory training in the Multiple T-maze in C57BL/6J mice. Brain Struct Funct 217(2): 363-378.
52. Bannerman DM, Deacon RM, Seeburg PH, Rawlins JN, (2003) GluR-A-deficient mice display normal acquisition of a hippocampus-dependent spatial reference memory task but are impaired during spatial reversal. Behav Neurosci 117: 866-870.
53. McHugh SB, Niewoehner B, Rawlins JN, Bannerman DM, (2008) Dorsal hippocampal N-methyl-D-aspartate receptors underlie spatial working memory performance during non-matching to place testing on the T-maze. Behav Brain Res 186: 41-47.