CaMKII-dependent dendrite ramification and spine generation promote spatial training-induced memory improvement in a rat model of sporadic Alzheimer's disease

Neurobiology of Aging

Volumn 36, Issue 2, 2015, Pages 867-876

  Jiang, Xia ^a,b   Chai, Gao Shang ^a,c   Wang, Zhi Hao ^a   Hu, Yu ^a   Li, Xiao Guang ^a   Ma, Zhi Wei ^a   Wang, Qun ^a   Wang, Jian Zhi ^a   Liu, Gong Ping ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b HUBEI UNIVERSITY OF CHINESE MEDICINE   (China)

^c JIANGNAN UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Calcium calmodulin dependent protein kinase II; Dendrite ramification; Spatial memory; Spatial training; Spine generation

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CELL PROTEIN; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; PROTEIN GLUA1; PROTEIN GLUN2A; PROTEIN GLUN2B; PROTEIN PSD93; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BARNES MAZE TEST; CONDITIONING; CONTROLLED STUDY; DENDRITE; DENDRITE RAMIFICATION; DENTATE GYRUS; ENZYME ACTIVATION; ENZYME INHIBITION; FEAR; HYPERHOMOCYSTEINEMIA; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; MENTAL CAPACITY; NERVE CELL CHARACTERISTICS AND FUNCTIONS; NERVE CELL PLASTICITY; NONHUMAN; RAT; RISK ASSESSMENT; RISK FACTOR; SHORT TERM MEMORY; SPATIAL LEARNING; SPATIAL MEMORY; SPINE; ANIMAL; COGNITION; DENDRITIC SPINE; DISEASE MODEL; GENETICS; MEMORY; MOLECULARLY TARGETED THERAPY; NERVE REGENERATION; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; SPATIAL ORIENTATION; SPRAGUE DAWLEY RAT;

ALZHEIMER DISEASE; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; COGNITION; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; LONG-TERM POTENTIATION; MALE; MEMORY; MOLECULAR TARGETED THERAPY; NERVE REGENERATION; NEURONAL PLASTICITY; PHYSICAL CONDITIONING, ANIMAL; RATS, SPRAGUE-DAWLEY; SPATIAL NAVIGATION;

EID: 84922782820     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.10.018     Document Type: Article

References (52)

1. Abe K., Chisaka O., Van Roy F., Takeichi M. Stability of dendritic spines and synaptic contacts is controlled by N-catenin. Nat. Neurosci. 2004, 7:357-363.
2. Amaral D.G., Witter M.P. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 1989, 31:571-591.
3. Arendt T. Synaptic degeneration in Alzheimer's disease. Acta Neuropathol. 2009, 118:167-179.
4. Ball K., Berch D.B., Helmers K.F., Jobe J.B., Leveck M.D., Marsiske M., Morris J.N., Rebok G.W., Smith D.M., Tennstedt S.L., Unverzagt F.W., Willis S.L. Effects of cognitive training interventions with older adults: a randomized controlled trial. JAMA 2002, 288:2271-2281. Advanced Cognitive Training for Independent and Vital Elderly Study Group.
5. Barnes C.A. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J.Comp. Physiol. Psychol. 1979, 93:74-104.
6. Bayer K.U., De Koninck P., Leonard A.S., Hell J.W., Schulman H. Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 2001, 411:801-805.
7. Billings L.M., Green K.N., McGaugh J.L., LaFerla F.M. Learning decreases Abeta *56 and tau pathology and ameliorates behavioral decline in 3xTg-AD mice. J.Neurosci. 2007, 27:751-761.
8. Bourne J., Harris K.M. Do thin spines learn to be mushroom spines that remember?. Curr. Opin. Neurobiol. 2007, 17:381-386.
9. Caiati M.D., Safiulina V.F., Fattorini G., Sivakumaran S., Legname G., Cherubini E. PrPC controls via protein kinase A the direction of synaptic plasticity in the immature hippocampus. J.Neurosci. 2013, 33:2973-2983.
10. Chai G.S., Jiang X., Ni Z.F., Ma Z.W., Xie A.J., Cheng X.S., Wang Q., Wang J.Z., Liu G.P. Betaine attenuates Alzheimer-like pathological changes and memory deficits induced by homocysteine. J.Neurochem. 2013, 124:388-396.
11. Crews L., Masliah E. Molecular mechanisms of neurodegeneration in Alzheimer's disease. Hum. Mol. Genet. 2010, 19(R1):R12-R20.
12. de Ruiter J.P., Uylings H.B. Morphometric and dendritic analysis of fascia dentata granule cells in human aging and senile dementia. Brain Res. 1987, 402:217-229.
13. Engert F., Bonhoeffer T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 1999, 399:66-70.
14. Fiala J.C., Spacek J., Harris K.M. Dendritic spine pathology: cause or consequence of neurological disorders?. Brain Res. Brain Res. Rev. 2002, 39:29-54.
15. Flood D.G., Coleman P.D. Hippocampal plasticity in normal aging and decreased plasticity in Alzheimer's disease. Prog. Brain Res. 1990, 83:435-443.
16. Horner C.H., Arbuthnott E. Methods of estimation of spine density: are spines evenly distributed throughout the dendritic field?. J.Anat. 1991, 177:179-184.
17. Hudmon A., Schulman H. Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem. J. 2002, 364:593-611.
18. Jankowsky J.L., Melnikova T., Fadale D.J., Xu G.M., Slunt H.H., Gonzales V., Younkin L.H., Younkin S.G., Borchelt D.R., Savonenko A.V. Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer's disease. J.Neurosci. 2005, 25:5217-5224.
19. Kim J.J., Rison R.A., Fanselow M.S. Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behav. Neurosci. 1993, 107:1093-1098.
20. Kitamura T., Saitoh Y., Takashima N., Murayama A., Niibori Y., Ageta H., Sekiguchi M., Sugiyama H., Inokuchi K. Adult neurogenesis modulates the hippocampus-dependent period of associative fear memory. Cell 2009, 139:814-827.
21. Laurin D., Verreault R., Lindsay J., MacPherson K., Rockwood K. Physical activity and risk of cognitive impairment and dementia in elderly persons. Arch. Neurol. 2001, 58:498-504.
22. Li C., Brake W.G., Romeo R.D., Dunlop J.C., Gordon M., Buzescu R., Magarinos A.M., Allen P.B., Greengard P., Luine V., McEwen B.S. Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2185-2190.
23. Lisman J., Schulman H., Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci. 2002, 3:175-190.
24. Matsuo N., Reijmers L., Mayford M. Spine type-specific recruitment of newly synthesized AMPA receptors with training. Science 2008, 319:1104-1107.
25. McAllister A.K., Katz L.C., Lo D.C. Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron 1997, 18:767-778.
26. Morris R.G., Garrud P., Rawlins J.N., Okeefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
27. Ota K.T., Monsey M.S., Wu M.S., Schafe G.E. Synaptic plasticity and NO-cGMP-PKG signaling regulate pre- and postsynaptic alterations at rat lateral amygdale synapses following fear conditioning. PLoS One 2010, 5:e11236.
28. Park C.S., Elgersma Y., Grant S.G., Morrison J.H. alpha-Isoform of calcium-calmodulin-dependent protein kinase II and postsynaptic density protein 95 differentially regulate synaptic expression of NR2A- and NR2B-containing N-methyl-d-aspartate receptors in hippocampus. Neuroscience 2008, 151:43-55.
29. Pasternak J.F., Woolsey T.A. On the selectivity of the Golgi-Cox method. J.Comp. Neurol. 1975, 160:307-312.
30. Polleux F., Morrow T., Ghosh A. Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 2000, 404:567-573.
31. Purves D. Body and Brain: A Trophic Theory of Neural Connections 1990, Harvard University Press, Cambridge.
32. Sejnowski T.J. The year of the dendrite. Science 1997, 275:178-179.
33. Seshadri S., Beiser A., Selhub J., Jacques P.F., Rosenberg I.H., D'Agostino R.B., Wilson P.W., Wolf P.A. Plasma homocysteine as a risk factor for dementia and Alzheimer's disease. N.Engl. J. Med. 2002, 346:476-483.
34. Silingardi D., Angelucci A., De Pasquale R., Borsotti M., Squitieri G., Brambilla R., Putignano E., Pizzorusso T., Berardi N. ERK pathway activation bidirectionally affects visual recognition memory and synaptic plasticity in the perirhinal cortex. Front. Behav. Neurosci. 2011, 5:84.
35. Sholl D.A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J.Anat. 1953, 87:387-406.
36. Spacek J., Harris K.M. Three dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J.Neurosci. 1997, 17:190-203.
37. Spector A., Thorgrimsen L., Woods B., Royan L., Davies S., Butterworth M., Orrell M. Efficacy of an evidence-based cognitive stimulation therapy programme for people with dementia: randomized controlled trial. Br. J. Psychiatry 2003, 183:248-254.
38. Tronel S., Fabre A., Charrier V., Oliet S.H., Gage F.H., Abrous D.N. Spatial learning sculpts the dendritic arbor of adult-born hippocampal neurons. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7963-7968.
39. Vaillant A.R., Zanassi P., Walsh G.S., Aumont A., Alonso A., Miller F.D. Signaling mechanisms underlying reversible, activity-dependent dendrite formation. Neuron 2002, 34:985-998.
40. Vaynman S., Ying Z., Gomez-Pinilla F. Interplay between brain-derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience 2003, 122:647-657.
41. Vaynman S., Ying Z., Gomez-Pinilla F. The select action of hippocampal calcium calmodulin protein kinase II in mediating exercise-enhanced cognitive function. Neuroscience 2007, 144:825-833.
42. Verghese J., LeValley A., Derby C., Kuslansky G., Katz M., Hall C., Buschke H., Lipton R.B. Leisure activities and the risk of amnestic mild cognitive impairment in the elderly. Neurology 2006, 66:821-827.
43. Verghese J., Lipton R.B., Katz M.J., Hall C.B., Derby C.A., Kuslansky G., Ambrose A.F., Sliwinski M., Buschke H. Leisure activities and the risk of dementia in the elderly. N.Engl. J. Med. 2003, 348:2508-2516.
44. Wei W., Liu Y.H., Zhang C.E., Wang Q., Wei Z., Mousseau D.D., Wang J.Z., Tian Q., Liu G.P. Folate/vitamin-B12 prevents chronic hyperhomocysteinemia-induced tau hyperphosphorylation and memory deficits in aged rats. J.Alzheimers Dis. 2011, 27:639-650.
45. Whitford K.L., Dijkhuizen P., Polleux F., Ghosh A. Molecular control of cortical dendrite development. Annu. Rev. Neurosci. 2002, 25:127-149.
46. Whitford K.L., Marillat V., Stein E., Goodman C.S., Tessier-Lavigne M., Chédotal A., Ghosh A. Regulation of cortical dendrite development by Slit-Robo interactions. Neuron 2002, 33:47-61.
47. Wilson R.S., Bennett D.A., Bienias J.L., Aggarwal N.T., Mendes De Leon C.F., Morris M.C., Schneider J.A., Evans D.A. Cognitive activity and incident AD in a population-based sample of older persons. Neurology 2002, 59:1910-1914.
48. Wilson R.S., Mendes De Leon C.F., Barnes L.L., Schneider J.A., Bienias J.L., Evans D.A., Bennett D.A. Participation in cognitively stimulating activities and risk of incident Alzheimer disease. JAMA 2002, 287:742-748.
49. Yao Z., Guo Z., Yang C., Tian Q., Gong C.X., Liu G., Wang J.Z. Phenylbutyric acid prevents rats from electroconvulsion-induced memory deficit with alterations of memory-related proteins and tau hyperphosphorylation. Neuroscience 2010, 168(2):405-415.
50. Yesavage J.A. Nonpharmacological treatments for memory losses with normal aging. Am. J. Psychiatry 1985, 142:600-605.
51. Zhang C.E., Tian Q., Wei W., Peng J.H., Liu G.P., Zhou X.W., Wang Q., Wang D.W., Wang J.Z. Homocysteine induces tau phosphorylation by inactivating protein phosphatase 2A in rat hippocampus. Neurobiol. Aging 2008, 29:1654-1665.
52. Zhang C.E., Wei W., Liu Y.H., Peng J.H., Tian Q., Liu G.P., Zhang Y., Wang J.Z. Hyperhomocysteinemia increases beta-amyloid by enhancing expression of gamma-secretase and phosphorylation of amyloid precursor protein in rat brain. Am. J. Pathol. 2009, 174:1481-1491.