Reduced calcium/calmodulin-dependent protein kinase II activity in the hippocampus is associated with impaired cognitive function in MPTP-treated mice

Journal of Neurochemistry

Volumn 120, Issue 4, 2012, Pages 541-551

  Moriguchi, Shigeki ^a   Yabuki, Yasushi ^a   Fukunaga, Kohji ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

calcium calmodulin dependent protein kinase II; cognitive deficits; long term potentiation; MPTP; Parkinson's disease

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; GLUTAMATE RECEPTOR 1; MITOGEN ACTIVATED PROTEIN KINASE; SERINE; THREONINE; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHOSPHORYLATION; BEAM WALKING TEST; COGNITIVE DEFECT; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXPERIMENTAL TEST; HIPPOCAMPAL CA1 REGION; IMMUNOBLOTTING; LEARNING DISORDER; LOCOMOTION; LONG TERM POTENTIATION; MALE; MAZE TEST; MEMORY CONSOLIDATION; MOTOR COORDINATION; MOUSE; NONHUMAN; PARKINSON DISEASE; PASSIVE AVOIDANCE; PRIORITY JOURNAL; ROTAROD TEST; TASK PERFORMANCE;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; COGNITION DISORDERS; ENZYME ACTIVATION; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; ROTAROD PERFORMANCE TEST;

MUS;

EID: 84855967284     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07608.x     Document Type: Article

References (66)

1. Adolfsson R., Gottfries C. G., Roos B. E., and, Winblad B. J., (1979) Post-mortem distribution of dopamine and homovanillic acid in human brain, variations related to age, and a review of the literature. J. Neural Transm. 45, 81-105. (Pubitemid 9173404)
2. Ba M., Kong M., Yang H., Ma G., Lu G., Chen S., and, Liu Z., (2006) Changes in subcellular distribution and phosphorylation of GluR1 in lesioned striatum of 6-hydroxydopamine-lesined and L-dopa-treated rats. Neurochem. Res. 31, 1337-1347. (Pubitemid 44800585)
3. Barria A., Muller D., Derkach V., Griffith L. C., and, Sodring T. R., (1997) Regulatory phosphorylation of AMPA-type glutamate receptor by CaM-KII during long-term potentiation. Science 276, 2042-2045. (Pubitemid 27443609)
4. Bliss T. V., and, Collingridge G. L., (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39 (review). (Pubitemid 23020772)
5. Collingridge G. L., Isaac J. T., and, Wang Y. T., (2004) Receptor trafficking and synaptic plasticity. Nat. Rev. Neurosci. 5, 952-962 (review). (Pubitemid 39593358)
6. Cummings J. L., (1992) Depression and Parkinson's disease: a review. Am. J. Psychiatry 149, 443-454.
7. Da Cunha C., Gevaerd M. S., Vital M. A., Miyoshi E., Andreatini R., Silveira R., Takahashi R. N., and, Canteras N. S., (2001) Memory disruption in rats with nigral lesions induced by MPTP: a model for early Parkinson's disease amnesia. Behav. Brain Res. 124, 9-18. (Pubitemid 32567554)
8. Danysz W., Zajaczkowski W., and, Parsons C. G., (1995) Modulation of learning processes by ionotropic glutamate receptor ligands. Behav. Pharmacol. 6, 455-474.
9. 2 +/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc. Natl Acad. Sci. USA 96, 3269-3274. (Pubitemid 29148880)
10. Fernagut P. O., Diguet E., Labattu B., and, Tison F., (2002) A simple method to measure stride length as an index of nigro-striatal dysfunction in mice. J. Neurosci. Methods 113, 123-130. (Pubitemid 34076535)
11. Ferro M. M., Angelucci M. E., Anselmo-Franci J. A., Canteras N. S., and, Da Cunha C., (2007) Neuroprotective effect of ketamine/xylazine on two rat models of Parkinson's disease. Braz. J. Med. Biol. Res. 40, 89-96. (Pubitemid 46117723)
12. Frankland P. W., O'Brien C., Ohno M., Kirkwood A., and, Silva A. J., (2001) α-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature 411, 309-313. (Pubitemid 32467036)
13. 2 +/calmodulin-dependent protein kinase II in rat brain and various tissues. J. Neurochem. 51, 1070-1078.
14. 2 +/calmodulin-dependent protein kinase II and protein kinase C by glutamate in cultured rat hippocampal neurons. J. Biol. Chem. 267, 22527-22533.
15. 2+/ calmodulin-dependent protein kinase II. J. Biol. Chem. 268, 7863-7867. (Pubitemid 23120362)
16. Gasbarri A., Verney C., Innocenzi R., Campana E., and, Pacitti C., (1994) Mesolimbic dopaminergic neurons innervating the hippocampal formation in the rat: a combined retrograde tracing and immnohistochemical study. Brain Res. 668, 71-79.
17. Gevaerd M. S., Miyoshi E., Silveira R., Canteras N. S., Takahashi R. N., and, Da Cunha C., (2001) L-Dopa restores striatal dopamine level but fails to reverse MPTP-induced memory deficits in rats. Int. J. Neuropsychopharmacol. 4, 361-370. (Pubitemid 33151679)
18. Giese K. P., Fedorov N. B., Filipkowski R. K., and, Silva A. J., (1998) Autophosphorylation at Thr286 of the alpha calcium/calmodulin kinase II in LTP and learning. Science 279, 870-873. (Pubitemid 28106282)
19. Hanson J. E., Orr A. L., and, Madison D. V., (2010) Altered hippocampal synaptic physiology in aged parkin-deficient mice. Neuromol. Med. 12, 270-276.
20. Harris E. W., Ganong A. H., and, Cotman C. W., (1984) Long-term potentiation in the hippocampus involves activation of N-methyl-D-aspartate receptors. Brain Res. 323, 132-137. (Pubitemid 15216780)
21. Heikkila R. E., and, Sonsalla P. K., (1987) The use of the MPTP-treated mouse as an animal model of parkinsonism. Can. J. Neurol. Sci. 14, 436-440. (Pubitemid 17147628)
22. Heikkila R. E., Manzino L., Cabatt F. S., and, Duvoisin R. S., (1984a) Protection against the dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine by monoamine oxidase inhibitors. Nature 311, 467-469. (Pubitemid 14035453)
23. Heikkila R. E., Hess A., and, Duvoisin R. C., (1984b) Dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in mice. Science 224, 1451-1453.
24. Hong Z., Wang G., Gu J., Pan J., Bai L., Zhang S., and, Chen S. D., (2007) Tripchlorolide protects against MPTP-induced neurotoxicity in C57BL/6 mice. Eur. J. Neurosci. 26, 1500-1508. (Pubitemid 47416517)
25. Hornykiewicz O., (1963) The tropical localization and content of noradrenalin and dopamine (3-hydroxytryramine) in the substantia nigra of normal persons and patients with Parkinson's disease. Wien. Klin. Wochenschr. 75, 309-312.
26. Hornykiewicz O., and, Kish S. J., (1987) Biochemical pathophysiology of Parkinson's disease. Adv. Neurol. 45, 19-34.
27. Hudman A., and, Schulman H., (2002) Neuronal Ca2+/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function. Ann. Rev. Biochem. 71, 473-510 (review). (Pubitemid 34800228)
28. Jackson-Lewis V., Jackowec M., Burke R. E., and, Przedborski S., (1995) Time-course and morphology of dopaminergic neuronal death caused by the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neurodegeneration 4, 257-269.
29. Jellinger K., (1987) Overview of morphological changes in Parkinson's disease. Ann. Neurol. 45, 1-18.
30. Kish S. J., Shannak K., and, Hornykicwicz O., (1988) Uncvcn pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysilogic and clinical implications. N. Engl. J. Med. 318, 876-880. (Pubitemid 18090271)
31. Kitada T., Pisani A., Karouani M., Haburcak M., Martella G., Tscheeter A., Platania P., Wu B., Pothos E. N., and, Shen J., (2009) Impaired dopamine relase and synaptic plasticity in the striatum of Parkin-/- mice. J. Neurochem. 110, 613-621.
32. Laemmli U. K., (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
33. Lisman J., Schulman H., and, Cline H., (2002) The molecular basis of CaMKII function in synaptic and behavioral memory. Nat. Rev. Neurosci. 3, 175-190. (Pubitemid 135706588)
34. Liu S. M., Fa M., Ninan I., Trinchese F., Dauer W., and, Arancio O., (2007) Alpha-synuclein involvement in hippocampal synaptic plasticity: role of NO, cGMP, cGK and CaMKII. Eur. J. Neurosci. 25, 3583-3596. (Pubitemid 47020438)
35. Lledo P. M., Hjelmstad G. O., Mukhherji S., Sodering T. R., Malenka R. C., and, Nicoll R. A., (1995) Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc. Natl Acad. Sci. USA 92, 11175-11179.
36. Malenka R. C., (1994) Synaptic plasticity in the hippocampus: LTP and LTD. Cell 78, 535-538 (review). (Pubitemid 24268575)
37. McGlade-McCulloh E., Yamamoto H., Tan S. E., Brickey D. A., and, Sodering T. R., (1993) Phosphorylation and regulation of glutamate receptors by calcium/calmodulin-dependent protein kinase II. Nature 362, 640-642. (Pubitemid 23109274)
38. Miyoshi E., Wietzikoski S., Camplessei M., Silveira R., Takahasi R. N., and, Da Cunha C., (2002) Imapired learning in a apatial working memory version and in a cued version of the water maze in rats with MPTP-induced mesencephalic dopaminergic lesions. Brain Res. Bull. 58, 41-47. (Pubitemid 34732994)
39. Moriguchi S., Shioda N., Han F., Narahashi T., and, Fukunaga K., (2008) CaM kinase II and protein kinase C activations mediate enhancement of long-term potentiation by nefiracetam in the rat hippocampal CA1 region. J. Neurochem. 106, 1092-1103.
40. Mulkey R. M., and, Malenka R. C., (1992) Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9, 967-975.
41. Nicotra A., and, Parvez S. H., (2000) Cell death induced by MPTP, a substrate for monoamine oxidase B. Toxicology 153, 157-166.
42. Ogawa N., Hirose Y., Ohara S., Ono T., and, Watabe Y., (1985) A simple quantitative bradykinesia test in MPTP-treated mice. Res. Commun. Chem. Pathol. Pharmacol. 50, 435-441. (Pubitemid 16185305)
43. O'Reilly R. C., and, McClelland J. L., (1994) Hippocampal conjunctive encoding, strage, and recall: avoiding a trade-off. Hippocampus 4, 661-682.
44. Perry J. C., Da Cunha C., Anselmo-Franci J., Andreatini R., Miyoshi E., Tufik S., and, Vital M. A., (2004) Behavioral and neurochemical effects of phosphatidylserine in MPTP lesion of the substantia nigra of rats. Eur. J. Pharmacol. 484, 225-233. (Pubitemid 38117214)
45. Pillon B., Dubois B., Cusimano G., Bonnet A. M., Lhermitte F., and, Agid Y., (1989) Does cognitive impairment in Parkinson's disease result from non-dopaminergic lesions? J. Neurol. Neurosurg. Psychiatry 52, 201-206. (Pubitemid 19054194)
46. 2 +/calmodulin-dependent protein kinase II. J. Neurosci. 22, 4406-4411. (Pubitemid 37465657)
47. Prickaerts J., Van Staveren W. C. G., Sik A., Markerink-Van Ittersum M., Niewohner U., Van der Staay F. J., Blokland A., and, De Vente J., (2002) Effects of two selective phosphodiesterase type 5 inhibitors, sildenafil and vardenafil, on object recognition memory and hippocampal cyclic GMP levels in the rat. Neuroscience 113, 349-359.
48. Quinn L. P., Perren M. J., Brackenborough K. T., Woodhams P. L., Vidgeon-Hart M., Chapman H., Pangalos M. N., Upton N., and, Virley D. J., (2007) A beam walking apparatus to assess behavioral impairments in MPTP-treaed mice: Pharmacological validation with R-(-)-deprenyl. J. Neurosci. Res. 164, 43-49. (Pubitemid 46938674)
49. Reksidler A. B., Lima M. M., Zanata S. M., Machado H. B., Da Cunha C., Andreatini R., Tufik S., and, Vital M. A., (2007) The COX-2 inhibitor parecoxib produces neuroprotective effects in MPTP-lesioned rats. Eur. J. Pharmacol. 560, 163-175. (Pubitemid 46341312)
50. Reksidler A. B., Lima M. M., Dombrowski P., Andersen M. L., Zanata S. M., Andreatini R., Tufik S., and, Vital M. A., (2008) Repeated intranigral MPTP administration: a new protocol of prolonged locomotor impairment mimicking Parkinson's disease. J. Neurosci. Methods 167, 268-277. (Pubitemid 350235638)
51. Ricaurte G. A., Irwin I., Forno L. S., Delanny L. E., Langston E., and, Langston J. W., (1987) Aging and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine- induced degeneration of dopaminergic neurons in the substantia nigra. Brain Res. 403, 43-51. (Pubitemid 17009738)
52. Rozas G., Lopez-Martin E., Guerra M. J., and, Labandeira-Garcia J. L., (1998) The overall rod performance test in the MPTP-trated mouse model of Parkinsonism. J. Neurosci. Methods 83, 165-175. (Pubitemid 28442608)
53. Schneider J. S., Tinker I. P., Van Velson M., and, Giardiniere M., (2000) Effects of the partial glycine agonist D-cycloserine on cognitive functioning in chronic low dose MPTP-treated monkeys. Brain Res. 860, 190-194. (Pubitemid 30155856)
54. Shi S. H., Hayashi Y., Petralia R. S., Zaman S. H., Wenthold R. J., Svoboda K., and, Malinow R., (1999) Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 1811-1826.
55. Smeyne R. J., and, Jackson-Lewis V., (2005) The MPTP model of Parkinson's disease. Brain Res. Mol. Brain Res. 134, 57-66. (Pubitemid 40409495)
56. Song I., and, Huganir R. L., (2002) Regulation of AMPA receptor during synaptic plasticity. Trends Neurosci. 25, 578-588 (review). (Pubitemid 35254182)
57. Sonsalla P. K., and, Heikkila R. E., (1986) The influence of dose and dosing interval on MPTP-induced dopaminergic neurotoxicity in mice. Eur. J. Pharmacol. 129, 339-345. (Pubitemid 16008029)
58. Tanila H., Bjorklund M., and, Riekkinen P., Jr, (1998) Cognitive changes in mice following moderate MPTP exposure. Brain Res. Bull. 45, 577-582. (Pubitemid 28262597)
59. Tingley W. G., Rocke K. W., Thompson A. K., and, Huganir R. L., (1993) Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain. Nature 364, 70-73. (Pubitemid 23233458)
60. Walsh K., and, Bennett G., (2001) Parkinson's disease and anxiety. Postgrad. Med. J. 77, 89-93. (Pubitemid 32120976)
61. 2 +/CaM induces synaptic potentiation requiring CaMKII and PKC activity. Neuron 15, 443-452.
62. Wang Y., Chandran J. S., Cai H. B., and, Mattson M. P., (2008) DJ-1 is essential for long-term depression at hippocampal CA1 synapses. Neuromol. Med. 10, 40-45.
63. Williams S., Mmbaga N., and, Chirwa S., (2006) Dopaminergic D1 receptor agonist SKF38393 induces GAP-43 expression and long-term potentiation in hippocampus in vivo. Neurosci. Lett. 402, 46-50. (Pubitemid 43766432)
64. Xia Z., and, Storm D. R., (2005) The role of calmodulin as a signal integrator for synaptic plasticity. Nat. Rev. Neurosci. 6, 267-276. (Pubitemid 40469981)
65. Yamagata Y., (2003) New aspects of neurotransmitter release and exocytosis: dynamic and differential regulation of synapsin I phosphorylation by acute neuronal excitation in vivo. J. Pharmacol. Sci. 93, 22-29. (Pubitemid 37254262)
66. Zhu G., Chen Y., Huang Y. Y., Li Q. L., and, Behnisch T., (2011) MPTP-mediated hippocampal dopamine deprivation modulates synaptic transmission and active-dependent synaptic plasticity. Toxicol. Appl. Pharmacol. 254, 332-341.