PKC activation during training restores mushroom spine synapses and memory in the aged rat

Neurobiology of Disease

Volumn 55, Issue , 2013, Pages 44-62

  Hongpaisan, Jarin ^a   Xu, Changqing ^a   Sen, Abhik ^a   Nelson, Thomas J ^a   Alkon, Daniel L ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

Aging; Dendritic spine; Hippocampus; PKC; Synapse

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRYOSTATIN; MESSENGER RNA; PROTEIN KINASE C ALPHA; PROTEIN KINASE C EPSILON;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; HIPPOCAMPAL CA1 REGION; LEARNING DISORDER; MAZE TEST; MEMORY CONSOLIDATION; NERVE FIBER; NONHUMAN; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; SPATIAL MEMORY; SPINAL CORD NERVE CELL; SYNAPSE; SYNAPTOGENESIS; TREATMENT RESPONSE;

AGING; ANESTHETICS, LOCAL; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; BRYOSTATINS; CAPRYLATES; DENDRITES; ELECTRIC STIMULATION; ENZYME ACTIVATION; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; INHIBITORY POSTSYNAPTIC POTENTIALS; LIDOCAINE; MAZE LEARNING; MEMORY; PATCH-CLAMP TECHNIQUES; PROTEIN KINASE C; PYRAMIDAL CELLS; RATS; SYNAPSES; TIME FACTORS;

EID: 84877075794     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.03.012     Document Type: Article

References (91)

1. Abeliovich A., Paylor R., Chen C., Kim J.J., Wehner J.M., Tonegawa S. PKCγ mutant mice exhibit mild deficits in spatial and contextual learning. Cell 1993, 75:1263-1271.
2. Ahlskog J.E., Geda Y.E., Graff-Radford N.R., Petersen R.C. Physical exercise as a preventive or disease-modifying treatment of dementia and brain aging. Mayo Clin. Proc. 2011, 86:876-884.
3. Akten B., Kye M.J., Hao L.T., Wertz M.H., Singh S., Nie D., Huang J., Merianda T.T., Twiss J.L., Beattie C.E., Steen J.A., Sahin M. Interaction of survival of motor neuron (SMN) and HuD proteins with mRNA cpg15 rescues motor neuron axonal deficits. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:10337-10342.
4. Antic D., Keene J.D. Messenger ribonucleoprotein complexes containing human ELAV proteins: interactions with cytoskeleton and translational apparatus. J. Cell Sci. 1998, 111:183-197.
5. Aranda-Abreu G.E., Behar L., Chung S., Furneaux H., Ginzburg I. Embryonic lethal abnormal vision-like RNA-binding proteins regulate neurite outgrowth and tau expression in PC12 cells. J. Neurosci. 1999, 19:6907-6917.
6. Bank B., Deweer A., Kuzirian A.M., Ramussen H., Alkon D.L. Classical conditioning induces long-term translocation of protein kinase C in rabbit hippocampal CA1 Cells. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:1988-1992.
7. Barnes C.A., McNaughton B.L. Physiological compensation for loss of afferent synapses in rat hippocampal granule cells during senescence. J. Physiol. 1980, 309:473-485.
8. Barnes C.A., Rao G., Foster T.C., McNaughton B.L. Region-specific age effects on AMPA sensitivity: electrophysiological evidence for loss of synaptic contacts in hippocampal field CA1. Hippocampus 1992, 2:457-468.
9. Barnes C.A., Rao G., Shen J. Age-related decrease in the N-methyl-d-aspartateR-mediated excitatory postsynaptic potential in hippocampal region CA1. Neurobiol. Aging 1997, 18:445-452.
10. Barnes C.A., Rao G., Orr G. Age-related decrease in the Schaffer collateral-evoked EPSP in awake, freely behaving rats. Neural Plast. 2000, 7:167-178.
11. Battaini F., Pascale A. Protein kinase C signal transduction regulation in physiological and pathological aging. Ann. N. Y. Acad. Sci. 2005, 1057:177-192.
12. Beltran-Campos V., Prado-Alcala R.A., Leon-Jacinto U., Aguilar-Vazques A., Quirarte G.L., Ramirez-Amaya V., Diaz-Cintra S. Increase of mushroom spine density in CA1 apical dendrites produced by water maze training is prevented by ovariectomy. Brain Res. 2011, 1369:119-130.
13. Bourne J., Harris K.M. Do thin spines learn to be mushroomspines that remember?. Curr. Opin. Neurobiol. 2007, 17:381-386.
14. Brennan A.B., Yuan P., Dickstein D.L., Rocher A.B., Hof P.R., Maniji H., Arnsten F.T. Protein kinase C activity is associated with prefrontal cortical decline in aging. Neurobiol. Aging 2009, 30:782-792.
15. Burke S.N., Barnes C.A. Neural plasticity in the ageing brain. Nat. Rev. Neurosci. 2006, 7:30-40.
16. Calhoun M.E., Kurth D., Phinney A.L., Long J.M., Hengemihle J., Mouton P.R., Ingram D.K., Jucker M. Hippocampal neuron and synaptophysin-positive bouton number in aging C57BL/6 mice. Neurobiol. Aging 1998, 19:599-606.
17. Chapleau C.A., Carlo M.E., Larimore J.L., Pozzo-Miller L. The actions of BDNF on denritic spine density and morphology in organotypic slice cultures depend on the presence of serum in culture media. J. Neurosci. Methods 2008, 169:182-190.
18. Chapman T.R., Barrientos R.M., Ahrendsen J.T., Hoover J.M., Maier S.F., Patterson S.L. Aging and infection reduce expression of specific brain-derived neurotrophic factor mRNAs in hippocampus. Neurobiol. Aging 2012, 33(832):e1-e14.
19. Chisholm N.C., Juraska J. Effects of long-term treatment with estrogen and medroxyprogesterone acetate on synapse number in the medial prefrontal cortex of aged female rats. Menopause 2012, 19(7):804-811.
20. Chung S., Eckrich M., Perrone-Bizzozero N., Kohn D.T., Furneaux H. The ELAV-like proteins bind to a conserved regulatory element in the 3'-untranslated region of GAP-43 mRNA. J. Biol. Chem. 1997, 272:6593-6598.
21. Colombo P.J., Wetsel W.C., Gallagher M. Spatial memory is related to hippocampal subcellular concentrations of calcium-dependent protein kinase C isoforms in young and aged rats. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:14195-14199.
22. Foster T.C., Barnes C.A., Rao G., McNaughton B.L. Increase in perforant path quantal size in aged F-344 rats. Neurobiol. Aging 1991, 12:441-448.
23. Gallagher M., Bizon J.L., Hoyt E.C., Helm K.A., Lund P.K. Effects of aging on the hippocampal formation in a naturally occurring animal model of mild cognitive impairment. Exp. Gerontol. 2003, 38:71-77.
24. Geinisman Y., deToledo-Morrell L., Morrell F., Persina I.S., Rossi M. Age-related loss of axospinous synapses formed by two afferent systems in the rat dentate gyrus as revealed by the unbiased stereological dissector technique. Hippocampus 1992, 2:437-444.
25. Geinisman Y., Disterhoft J.F., Gundersen H.J., McEchron M.D., Persina I.S., Power J.M., van der Zee E.A., West M.J. Remodeling of hippocampal synapses after hippocampus-dependent associative learning. J. Comp. Neurol. 2000, 417:49-59.
26. Geinisman Y., Ganeshina O., Yoshida R., Berry R.W., Disterhoft J.F., Gallagher M. Aging, spatial learning, and total synapse number in the rat CA1 stratum radiatum. Neurobiol. Aging 2004, 25:407-416.
27. Govoni S., Amadio M., Battaini F., Pascale A. Senescence of the brain: focus on cognitive kinases. Curr. Pharm. Des. 2010, 16:660-671.
28. Grabauskas G., Chapman H., Wheal H.V. Role of protein kinase C in modulation of excitability of CA1 pyramidal neurons in the rat. Neuroscience 2006, 139:1301-1313.
29. Hama H., Hara C., Yamaguchi K., Miyawaki A. PKC signaling mediates global enhancement of excitatory synaptogenesis in neurons triggered by local contact with astrocytes. Neuron 2004, 41:405-415.
30. Hara Y., Park C.S., Janssen W.G.M., Roberts M.T., Morrison J.H., Rapp P.R. Synaptic correlates of momory and menopause in the hippocampal dentate gyrus in rhesus monkeys. Neurobiol. Aging 2012, 33(421):e17-e28.
31. Harris K.M., Jensen F.E., Tsao B. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J. Neurosci. 1992, 12:2685-2705.
32. Hof P.R., Morrison J.H. The aging brain: morphomolecular senescence of cortical circuits. Trends Neurosci. 2004, 27:607-613.
33. Hongpaisan J., Alkon D.L. A structural basis for enhancement of long-term associative memory in single dendritic spines regulated by PKC. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19571-19576.
34. Hongpaisan J., Sun M.K., Alkon D.L. PKC epsilon activation prevents synaptic loss, Abeta elevation, and cognitive deficits in Alzheimer's disease transgenic mice. J. Neurosci. 2011, 31:630-643.
35. Hu X., Ballo L., Pietila L., Viesselmann C., Ballweg J., Lumbard D., Stevenson M., Merriam E., Dent E.W. BDNF-induced increase of PSD-95 in dendritic spines requires dynamic microtubule invasions. J. Neurosci. 2011, 31:15597-15603.
36. Hussain R.J., Carpenter D.O. The effects of protein kinase C activity on synaptic transmission in two areas of rat hippocampus. Brain Res. 2003, 990:28-37.
37. Jelks K.B., Wylie R., Floyd C.L., AcAlilister K., Wise P. Estradiol targets synaptic proteins to induce glutamatergic synapse formation in cultured hippocampal neurons: critical role of estrogen receptor-α. J. Neurosci. 2007, 27:6903-6913.
38. Kalus P., Slotboom J., Gallinat J., Mahlberg R., Cattapan-Ludewig K., Wiest R., Nyffeler T., Buri C., Federspiel A., Kunz D., Schroth G., Kiefer C. Examining the gateway to the limbic system with diffusion tensor imaging: the perforant pathway in dementia. NeuroImage 2006, 30:713-720.
39. Kasai H., Fukuda M., Watanabe S., Hayashi-Takagi A., Noguchi J. Structural dynamics of dendritic spines in memory and cognition. Cell 2010, 33:121-129.
40. Kirov S.A., Petrak L.J., Fiala J.C., Harris K.M. Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus. Neuroscience 2004, 127:69-80.
41. Kleim J.A., Hogg T.M., VanderBerg P.M., Cooper N.R., Bruneau R., Remple M. Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J. Neurosci. 2004, 24:628-633.
42. Kraft E. Cognitive function, physical activity, and aging: possible biological links and implication for multimodal interventions. Neuropsychol. Dev. Cogn. Aging Neuropsychol. Cogn. 2012, 19:248-263.
43. Li C., Brake W.G., Romeo R.D., Dunlop J.C., Gordon M., Buzescu R., Magarinos A., Allen P., Greengard P., Luine V., McEwen B.S. Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory tasks in female mice. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2185-2190.
44. Lister J.P., Barnes C.A. Neurobiological changes in the hippocampus during normative aging. Arch. Neurol. 2009, 66:829-833.
45. Luebke J.I., Chang Y.M., Moore T.L., Rosene D.L. Normal aging results in decreased synaptic excitation and increased synaptic inhibition of layer 2/3 pyramidal cells in the monkey prefrontal cortex. Neuroscience 2004, 125:277-288.
46. Matsuo N., Reijmers L., Mayford M. Spine-type-specific recruitment of newly synthesized AMPA receptors with learning. Science 2008, 319:1104-1107.
47. Mattews S.A., Pettit G.R., Rozengurt E. Bryostatin-1 induces biphasic activation of protein kinase D in intact cells. J. Biol. Chem. 1997, 272:20245-20250.
48. Miranda R., Blanco E., Begega A., Santin L.J., Arias J.L. Reversible changes in hippocampal CA1 synapses associated with water maze training in rats. Synapse 2006, 59:177-181.
49. Moser M.B., Trommald M., Andersen P. An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:12673-12675.
50. Mutter R., Wills M. Chemistry and clinical biology of the bryostatins. Bioorg. Med. Chem. 2000, 8:1841-1860.
51. Nelson T.J., Cui C., Luo Y., Alkon D.L. Reduction of beta-amyloid levels by novel protein kinase Cε activators. J. Biol. Chem. 2009, 284:34514-34521.
52. Nicholson D.A., Yoshida R., Berry R.W., Gallagher M., Geinisman Y. Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and age-related spatial learning impairments. J. Neurosci. 2004, 24:7648-7653.
53. Nicholson D.A., Trana R., Katz Y., Kath W.L., Spruston N., Geinisman Y. Distance-dependent differences in synapse number and AMPA receptor expression in hippocampal CA1 pyramidal neurons. Neuron 2006, 50:431-442.
54. Nilsson L.G. Memory function in normal aging. Acta Neurol. Scand. Suppl. 2003, 179:7-13.
55. Olds J.L., Anderson M.L., McPhie D.L., Staten L.D., Alkon D.L. Imaging of memory-specific changes in the distribution of protein kinase c in the hippocampus. Science 1989, 245:866-869.
56. Pascale A., Gusev P.A., Amadio M., Dottorini T., Govoni S., Alkon D.L., Quattrone A. Increase of the RNA-binding protein HuD and posttranscriptional up-regulation of the GAP-43 gene during spatial memory. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:1217-1222.
57. Pascale A., Amadio M., Scapagnini G., Lanni C., Racchi M., Provenzani A., Govoni S., Alkon D.L., Quattrone A. Neuronal ELAV proteins enhance mRNA stability by a PKCalpha-dependent pathway. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12065-12070.
58. Perrone-Bizzozero N., Bolognani F. Role of HuD and other RNA-binding proteins in neural development and plasticity. J. Neurosci. Res. 2002, 68:121-126.
59. Peters A., Sethares C., Luebke J.I. Synapses are lost during aging in the primate prefrontal cortex. Neuroscience 2008, 152:970-981.
60. Phinney A.L., Calhoun M.E., Wolfer D.P., Lipp H.P., Zheng H., Jucker M. No hippocampal neuron or synaptic bouton loss in learning-impaired aged beta-amyloid precursor protein-null mice. Neuroscience 1999, 90:1207-1216.
61. Prekeris R., Mayhew M.W., Cooper J.B., Terrian D.M. Identification and localization of an actin-binding motif that is unique to the epsilon isoform of protein kinase C and participates in the regulation of synaptic function. J. Cell Biol. 1996, 132:77-90.
62. Quattrone A., Pascale A., Nogues X., Zhao W., Gusev P., Pacini A., Alkon D.L. Posttranscriptional regulation of gene expression in learning by the neuronal ELAV-like mRNA-stabilizing proteins. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:11668-11673.
63. Rapp P.R., Gallagher M. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:9926-9930.
64. Rodriguez A., Ehlenberger D.B., Dickstein D.L., Hof P.R., Wearne S.L. Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images. PLoS One 2008, 3:e1997.
65. Rodriguez-Moreno A., Lopez-Garcia J.C., Lerma J. Two populations of kainate receptors with separate signaling mechanisms in hippocampal interneurons. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:1293-1298.
66. Rosenzweig E.S., Rao G., McNaughton B.L., Barnes C.A. Role of temporal summation in age-related long-term potentiation-induction deficits. Hippocampus 1997, 7:549-558.
67. Rusakov D.A., Davies H.A., Harrison E., Diana G., Richter-Levin G., Bliss T.V., Stewart M.G. Ultrastructural synaptic correlates of spatial learning in rat hippocampus. Neuroscience 1997, 80:69-77.
68. Sametsky E.A., Disterhoft J.F., Geinisman Y., Nicholson D.A. Synaptic strength and postsynaptically silent synapses through advanced aging in rat hippocampal CA1 pyramidal neurons. Neurobiol. Aging 2010, 31:813-825.
69. Scheff S.W., Price D.A., Schmitt F.A., Mufson E.J. Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment. Neurobiol. Aging 2006, 27:1372-1384.
70. Shirai Y., Adachi N., Saito N. Protein kinase C epsilon: function in neurons. FEBS J. 2008, 275:3988-3994.
71. Shrager Y., Bayley P.J., Bontempi B., Hopkins R.O., Squire L.R. Spatial memory and the human hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:2961-2966.
72. Smith M.L., Milner B. The role of the right hippocampus in the recall of spatial location. Neuropsychologia 1981, 19:781-793.
73. Smith T.D., Adams M.M., Gallagher M., Morrison J.H., Rapp P.R. Circuit-specific alterations in hippocampal synaptophysin immunoreactivity predict spatial learning impairment in aged rats. J. Neurosci. 2000, 20:6587-6593.
74. Sorra K.E., Harris K.M. Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus 2000, 10:501-511.
75. Sun M.K., Hongpaisan J., Nelson T.J., Alkon D.L. Poststroke neuronal rescue and synaptogenesis mediated in vivo by protein kinase C in adult brains. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13620-13625.
76. Sun M.K., Hongpaisan J., Alkon D.L. Postischemic PKC activation rescues retrograde and anterograde long-term memory. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14676-14680.
77. Tao-Cheng J.H., Gallant P.E., Brightman M.W., Dosemeci A., Reese T.S. Structural changes at synapses after delayed perfusion fixation in different regions of the mouse brain. J. Comp. Neurol. 2007, 501:731-740.
78. Uttl B., Graf P. Episodic spatial memory in adulthood. Psychol. Aging 1993, 8:257-273.
79. Van der Zee E.A., Kronforst-Collins M.A., Maizels E.T., Hunzicker-Dunn M., Disterhoft J.F. Gamma isoform-selective changes in PKC immunoreactivity after trace eyeblink conditioning in the rabbit hippocampus. Hippocampus 1997, 7:271-285.
80. 2+-dependent PKC isoforms in rabbit hippocampus. Hippocampus 2004, 14:849-860.
81. von Bohlen und Halbach O. Involvement of BDNF in age-dependent alterations in the hippocampus. Front. Aging Neurosci. 2010, 36:1-11.
82. Vorhees C.V., Williams M.T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat. Protoc. 2006, 1:848-858.
83. Walker M.P., LaFerla F.M., Oddo S.S., Brewer G.J., in press. Reversible epigenetic histone modifications and BDNF expression in neurons with aging and from a mouse model of Alzheimer's disease. Age (Dordr).
84. Wang M., Gamo N.J., Yang Y., Jin L.E., Wang X.J., Laubach M., Mazer J.A., Lee D., Arnsten A.F. Neuronal basis of age-related working memory decline. Nature 2011, 476:210-213.
85. Weeber E.J., Atkins C.M., Selcher J.C., Varga A.W., Mirnikjoo B., Paylor R., Leitges M., Sweatt J.D. J. Neurosci. 2000, 20:5906-5914.
86. Wilkniss S.M., Jones M.G., Korol D.L., Gold P.E., Manning C.A. Age-related differences in an ecologically based study of route learning. Psychol. Aging 1997, 12:372-375.
87. Wilson I.A., Gallagher M., Eichenbaum H., Tanila H. Neurocognitive aging: prior memories hinder new hippocampal encoding. Trends Neurosci. 2006, 29:662-670.
88. Wu M., Zhang Z., Leranth C., Xu C., van den Pol A.N., Alreja M. Hypocretin increases impulse flow in the septohippocampal GABAergic pathway: implications for arousal via a mechanism of hippocampal disinhibition. J. Neurosci. 2002, 22:7754-7765.
89. Xu C., Cui C., Alkon D.L. Age-dependent enhancement of inhibitory synaptic transmission in CA1 pyramidal neurons via GluR5 kainate receptors. Hippocampus 2009, 19:706-717.
90. Yankova M., Hart S.A., Wooley C.S. Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: a serial electron-microscopy study. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:3525-3530.
91. Zhang X., Zhang R., Zhoa H., Cai H., Gush K.A., Kerr R.G., Pettit G.R., Kraft A.S. Preclinical pharmacology of the natural product anticancer agent bryostatin 1, an activator of protein kinase C. Cancer Res. 1996, 56:802-808.