The aging brain, a key target for the future: The protein kinase C involvement

Pharmacological Research

Volumn 55, Issue 6, 2007, Pages 560-569

  Pascale, Alessia ^a   Amadio, Marialaura ^a   Govoni, Stefano ^a   Battaini, Fiorenzo ^b  

^a UNIVERSITY OF PAVIA   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Aging; Brain; ELAV; Memory and Alzheimer's disease; PKC; RACK; Signal transduction

Indexed keywords

HU ANTIGEN; PROTEIN KINASE C;

AGING; ALZHEIMER DISEASE; BRAIN AGING; CELLULAR DISTRIBUTION; DISEASE ASSOCIATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME STRUCTURE; HUMAN; MEMORY DISORDER; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW;

AGING; ALZHEIMER DISEASE; ANIMALS; BRAIN; ENZYME ACTIVATION; HUMANS; ISOENZYMES; MEMORY; PHOSPHORYLATION; PROTEIN KINASE C; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

EID: 34250771556     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2007.04.013     Document Type: Review

References (94)

1. Flood D.G., and Coleman P.D. Neuron numbers and sizes in aging brain: comparisons of human, monkey, and rodent data. Neurobiol Aging 9 (1988) 453-456
2. Bertoni-Freddari C., Fattoretti P., Paoloni R., Caselli U., Galeazzi L., and Meier-Ruge W. Synaptic structural dynamics and aging. Gerontology 42 3 (1996) 170-180
3. Wickelgren I. For the cortex, neuron loss may be less than thought. Science 273 (1996) 48-50
4. Rapp P.R., and Gallagher M. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc Natl Acad Sci USA 93 (1996) 9926-9930
5. Gallagher M. Aging and hippocampal/cortical circuits in rodents. Alzheimer Dis Assoc Disord 17 (2003) S45-S47
6. Kelly K.M., Nadon N.L., Morrison J.H., Thibault O., Barnes C.A., and Blalock E.M. The neurobiology of aging. Epilepsy Res 68 Suppl 1 (2006) S5-S20
7. Agnati L.F., Zoli M., Grimaldi R., Fuxe K., Toffano G., and Zini I. Cellular and synaptic alterations in the aging brain. Aging 2 (1990) 5-25
8. Fulop Jr. T., and Seres I. Age-related changes in signal transduction. Drugs Aging 5 (1994) 366-390
9. Yamada K., and Nabeshima T. Changes in NMDA receptor/nitric oxide signaling pathway in the brain with aging. Microsc Res Tech 43 (1998) 68-74
10. Yamamoto M., Suhara T., Okubo Y., Ichimiya T., Sudo Y., Inoue M., et al. Age-related decline of serotonin transporters in living human brain of healthy males. Life Sci 71 (2002) 751-757
11. Nishizuka Y. The protein kinase C family and lipid mediators for transmembrane signaling and cell regulation. Alcohol Clin Exp Res 25 5 Suppl ISBRA (2001) 3S-7S
12. Newton A.C. Regulation of the ABC kinases by phosphorylation: PKC as a paradigm. Biochem J 370 (2003) 361-371
13. Balendran A., Hare G.R., Kieloch A., Williams M.R., and Alessi D.R. Further evidence that 3-phosphoinositide-dependent protein kinase-1 (PDK1) is required for the stability and phosphorylation of protein kinase C (PKC) isoforms. FEBS Lett 484 (2000) 217-223
14. Parker P.J. Protein kinase C phosphorylation: an introduction. Methods Mol Biol 233 (2003) 159-162
15. Giorgione J.R., Lin J.H., McCammon J.A., and Newton A.C. Increased membrane affinity of the C1 domain of protein kinase C delta compensates for the lack of involvement of its C2 domain in membrane recruitment. J Biol Chem 28 (2006) 1660-1669
16. Newton A.C., and Johnson J.E. Protein kinase C: a paradigm for regulation of protein function by two membrane-targeting modules. Biochim Biophys Acta 1376 2 (1998) 155-172
17. _, phospholipid-dependent protein kinase associated with plasma membrane. Nature 301 (1983) 621-623
18. Mochly-Rosen D., Smith B.L., Chen C.H., Disatnik M.H., and Ron D. Interaction of protein kinase C with RACK1, a receptor for activated C-kinase: a role in beta protein kinase C mediated signal transduction. Biochem Soc Trans 23 3 (1995) 596-600
19. Stabel S., and Parker P.J. Protein kinase C. Pharmacol Ther 51 (1991) 71-95
20. Tanaka C., and Nishizuka Y. The protein kinase C family for neuronal signaling. Annu Rev Neurosci 17 (1994) 551-567
21. Gao T., and Newton A.C. The turn motif is a phosphorylation switch that regulates the binding of Hsp70 to protein kinase C. J Biol Chem 277 (2002) 31585-31592
22. Hernandez A.I., Blace N., Crary J.F., Serrano P.A., Leitges M., Libien J.M., et al. Protein kinase M zeta synthesis from a brain mRNA encoding an independent protein kinase C zeta catalytic domain. Implications for the molecular mechanism of memory. J Biol Chem 278 (2003) 40305-40316
23. Mochly-Rosen D., Khaner H., and Lopez J. Identification of intracellular receptor proteins for activated protein kinase C. Proc Natl Acad Sci USA 88 (1991) 3997-4000
24. Jaken S. Protein kinase C isozymes and substrates. Curr Opin Cell Biol 8 (1996) 168-173
25. Battaini F., Pascale A., Paoletti R., and Govoni S. The role of anchoring protein RACK1 in PKC activation in the ageing rat brain. Trends Neurosci 20 (1997) 410-415
26. Csukai M., and Mochly-Rosen D. Pharmacologic modulation of protein kinase C isozymes: the role of RACKs and subcellular localisation. Pharmacol Res 39 (1999) 253-259
27. Schechtman D., and Mochly-Rosen D. Adaptor proteins in protein kinase C-mediated signal transduction. Oncogene 20 (2001) 6339-6347
28. McCahill A., Warwicker J., Bolger G.B., Houslay M.D., and Yarwood S.J. The RACK1 scaffold protein: a dynamic cog in cell response mechanisms. Mol Pharmacol 62 (2002) 1261-1273
29. Sklan E.H., Podoly E., and Soreq H. RACK1 has the nerve to act: structure meets function in the nervous system. Prog Neurobiol 78 2 (2006) 117-134
30. Robles-Flores M., and Garcia-Sainz J.A. Activated protein kinase C binds to intracellular receptors in rat hepatocytes. Biochem J 296 Pt 2 (1993) 467-472
31. Smith B.L., and Mochly-Rosen D. Inhibition of protein kinase C function by injection of intracellular receptor for the enzyme. Biochem Biophys Res Commun 188 (1992) 1235-1240
32. Ron D., Luo J., and Mochly-Rosen D. C2 region-derived peptides inhibit translocation and function of beta protein kinase C in vivo. J Biol Chem 270 41 (1995) 24180-24187
33. Ron D., Jiang Z., Yao L., Vagts A., Diamond I., and Gordon A. Coordinated movement of RACK1 with activated betaII PKC. J Biol Chem 274 38 (1999) 27039-27046
34. Pascale A., Alkon D.L., and Grimaldi M. Translocation of protein kinase C-betaII in astrocytes requires organized actin cytoskeleton and is not accompanied by synchronous RACK1 relocation. Glia 46 2 (2004) 169-182
35. Schechtman D., and Mochly-Rosen D. Isozyme-specific inhibitors and activators of protein kinase C. Methods Enzymol 345 (2002) 470-489
36. Choi D.S., Young H., McMahon T., Wang D., and Messing R.O. The mouse RACK1 gene is regulated by nuclear factor-kappa B and contributes to cell survival. Mol Pharmacol 64 (2003) 1541-1548
37. Bar-Am O., Yogev-Falach M., Amit T., Sagi Y., and Youdim M.B. Regulation of protein kinase C by the anti-Parkinson drug, MAO-B inhibitor, rasagiline and its derivatives, in vivo. J Neurochem 89 (2004) 1119-1125
38. Jaken S., and Parker P.J. Protein kinase C binding partners. Bioessays 22 (2000) 245-254
39. Osborne H.B. An insight into the post-transcriptional control of gene expression in cell function. Biol Cell 95 (2003) 125-127
40. Kracht M., and Saklatvala J. Transcriptional and post-transcriptional control of gene expression in inflammation. Cytokine 20 (2002) 91-106
41. Shim J., and Karin M. The control of mRNA stability in response to extracellular stimuli. Mol Cells 14 (2002) 323-331
42. Sachs A.B. Messenger RNA degradation in eukaryotes. Cell 74 (1993) 413-421
43. Keene J.D. Why is Hu where? Shuttling of early-response-gene messenger RNA subsets. Proc Natl Acad Sci USA 96 (1999) 5-7
44. Brennan C.M., and Steitz J.A. HuR and mRNA stability. Cell Mol Life Sci 58 (2001) 266-277
45. Amadio M., Battaini F., and Pascale A. The different facets of protein kinase C: old and new players in neuronal signal transduction pathways. Pharmacol Res 54 (2006) 317-325
46. Mobarak C.D., Anderson K.D., Morin M., Beckel-Mitchener A., Rogers S.L., Furneau H., et al. The RNA-binding protein HuD is required for GAP-43 mRNA stability, GAP-43 gene expression, and PKC-dependent neurite outgrowth in PC12 cells. Mol Biol Cell 11 (2000) 3191-3203
47. Quattrone A., Pascale A., Noguès X., Zhao W., Gusev P., Pacini A., et al. Posttranscriptional regulation of gene expression in learning by the neuronal ELAV-like mRNA-stabilizing proteins. Proc Natl Acad Sci USA 98 (2001) 11668-11673
48. Pascale A., Gusev P.A., Amadio M., Dottorini T., Govoni S., Alkon D.L., et al. Increase of the RNA-binding protein HuD and posttranscriptional up-regulation of the GAP-43 gene during spatial memory. Proc Natl Acad Sci USA 101 (2004) 1217-1222
49. Pascale A., Amadio M., Scapagnini G., Lanni C., Racchi M., Provenzani A., et al. Neuronal ELAV proteins enhance mRNA stability by a PKC alpha-dependent pathway. Proc Natl Acad Sci USA 102 34 (2005) 12065-12070
50. Battaini F. Protein kinase C isoforms as therapeutic targets in nervous system disease states. Pharmacol Res 44 (2001) 353-361
51. Durkin J.P., Tremblay R., Chakravarthy B., Mealing G., Morley P., Small D., et al. Evidence that the early loss of membrane protein kinase C is a necessary step in the excitatory amino acid-induced death of primary cortical neurons. J Neurochem 68 (1997) 1400-1412
52. Maher P. How protein kinase C activation protects nerve cells from oxidative stress-induced cell death. J Neurosci 21 (2001) 2929-2938
53. Bright R., Raval A.P., Dembner J.M., Perez-Pinzon M.A., Steinberg G.K., Yenari M., et al. Protein kinase C delta mediates cerebral reperfusion injury in vivo. J Neurosci 4 24 (2004) 6880-6888
54. Wang J., Bright R., Mochly-Rosen D., and Giffard R.G. Cell-specific role for epsilon- and betaI-protein kinase C isozymes in protecting cortical neurons and astrocytes from ischemia-like injury. Neuropharmacology 47 (2004) 136-145
55. Han Y.S., Zheng W.H., Bastianetto S., Chabot J.G., and Quirion R. Neuroprotective effects of resveratrol against beta-amyloid-induced neurotoxicity in rat hippocampal neurons: involvement of protein kinase C. Br J Pharmacol 141 (2004) 997-1005
56. Mandel S., Weinreb O., Amit T., and Youdim M.B. Mechanism of neuroprotective action of the anti-Parkinson drug rasagiline and its derivatives. Brain Res Brain Res Rev 48 (2005) 379-387
57. Szabo C. Roles of poly(ADP-ribose) polymerase activation in the pathogenesis of diabetes mellitus and its complications. Pharmacol Res 52 (2005) 60-71
58. Amadio M., Govoni S., Alkon D.L., and Pascale A. Emerging targets for the pharmacology of learning and memory. Pharmacol Res 50 (2004) 111-122
59. Alkon D.L., and Rasmussen H. A spatial-temporal model of cell activation. Science 239 (1988) 998-1005
60. Olds J.L., Anderson M.L., McPhie D.L., Staten L.D., and Alkon D.L. Imaging of memory-specific changes in the distribution of protein kinase C in the hippocampus. Science 245 (1989) 866-869
61. Wehner J.M., Sleight S., and Upchurch M. Hippocampal protein kinase C activity is reduced in poor spatial learners. Brain Res 523 2 (1990) 181-187
62. Lucchi L., Pascale A., Battaini F., Govoni S., and Trabucchi M. Cognition stimulating drugs modulate protein kinase C activity in cerebral cortex and hippocampus of adult rats. Life Sci 53 (1993) 1821-1832
63. Pascale A., Milano S., Corsico N., Lucchi L., Battaini F., Martelli E.A., et al. Protein kinase C activation and anti-amnesic effect of acetyl-L-carnitine: in vitro and in vivo studies. Eur J Pharmacol 265 (1994) 1-7
64. Noguès X., Micheau J., and Jaffard R. Protein kinase C activity in the hippocampus following spatial learning tasks in mice. Hippocampus 4 1 (1994) 71-77
65. Van der Zee E.A., Compaan J.C., de Boer M., and Luiten P.G. Changes in PKC gamma immunoreactivity in mouse hippocampus induced by spatial discrimination learning. J Neurosci 12 (1992) 4808-4815
66. Angenstein F., Riedel G., Reymann K.G., and Staak S. Hippocampal long-term potentiation in vivo induces translocation of protein kinase Cγ. NeuroReport 5 (1994) 381-384
67. Sacktor T.C., Osten P., Valsamis H., Jiang X., Naik M.U., and Sublette E. Persistent activation of the zeta isoform of protein kinase C in the maintenance of long-term potentiation. Proc Natl Acad Sci USA 90 (1993) 8342-8346
68. Noguès X., Pascale A., Micheau J., Battaini F., and Protein Kinase C. In: Riedel G., and Platt B. (Eds). Memories are made of these: from messengers to molecules (2003), Landes Bioscience, Georgetown, TX 383-410
69. Battaini F., Elkabes S., Bergamaschi S., Ladisa V., Lucchi L., De Graan P.N., et al. Protein kinase C activity, translocation and conventional isoforms in aging rat brain. Neurobiol Aging 16 (1995) 137-148
70. Battaini F., and Pascale A. Protein kinase C signal transduction regulation in physiological and pathological aging. Ann NY Acad Sci 1057 (2005) 177-192
71. Pascale A., Fortino I., Govoni S., Trabucchi M., Wetsel W.C., and Battaini F. Functional impairment in protein kinase C by RACK1 (receptor for activated C kinase 1) deficiency in aged rat brain cortex. J Neurochem 67 (1996) 2471-2477
72. Colombo P.J., and Gallager M. Individual differences in spatial memory among aged rats are related to hippocampal PKC gamma immunoreactivity. Hippocampus 12 (2002) 285-289
73. 2+-dependent PKC isoforms in rabbit hippocampus. Hippocampus 14 (2004) 849-860
74. Sanguino E., Roglans N., Alegret M., Sanchez R.M., Vazquez-Carrera M., and Laguna J.C. Prevention of age-related changes in rat cortex transcription factor activator protein-1 by hypolipidemic drugs. Biochem Pharmacol 68 (2004) 1411-1421
75. Mattson M.P., and Magnus T. Ageing and neuronal vulnerability. Nat Rev Neurosci 7 (2006) 278-294
76. Braak H., and Braak E. Evolution of neuronal changes in the course of Alzheimer's disease. J Neural Transm Suppl 53 (1998) 127-140
77. Whitehouse P.J., Price D.L., Struble R.G., Clark A.W., Coyle J.T., and Delon M.R. Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 215 (1982) 1237-1239
78. Racchi M., and Govoni S. Rationalizing a pharmacological intervention on the amyloid precursor protein metabolism. Trends Pharmacol Sci 20 (1999) 418-423
79. Gandy S. The role of cerebral amyloid beta accumulation in common forms of Alzheimer disease. J Clin Invest 115 (2005) 1121-1129
80. Gillespie S.L., Golde T.E., and Younkin S.G. Secretory processing of the Alzheimer amyloid beta/A4 protein precursor is increased by protein phosphorylation. Biochem Biophys Res Commun 187 3 (1992) 1285-1290
81. Buxbaum J.D., Koo E.H., and Greengard P. Protein phosphorylation inhibits production of Alzheimer amyloid beta/A4 peptide. Proc Natl Acad Sci USA 90 19 (1993) 9195-9198
82. Wang H.Y., Pisano M.R., and Friedman E. Attenuated PKC activity and translocation in Alzheimer's disease brain. Neurobiol Aging 15 (1994) 293-298
83. Battaini F., Pascale A., Lucchi L., Pasinetti G.M., and Govoni S. Protein kinase C anchoring deficit in postmortem brains of Alzheimer's disease patients. Exp Neurol 159 (1999) 559-564
84. Crary J.F., Shao C.Y., Mirra S.S., Hernandez A.I., and Sacktor T.C. Atypical protein kinase C in neurodegenerative disease I: PKMzeta aggregates with limbic neurofibrillary tangles and AMPA receptors in Alzheimer disease. J Neuropathol Exp Neurol 65 (2006) 319-326
85. Liu S.J., Zhang A.H., Li H.L., Wang Q., Deng H.M., Netzer W.J., et al. Overactivation of glycogen synthase kinase-3 by inhibition of phosphoinositol-3 kinase and protein kinase C leads to hyperphosphorylation of tau and impairment of spatial memory. J Neurochem 87 (2003) 1333-1344
86. Gianotti C., Porta A., De Graan P.N., Oestreicher A.B., and Nunzi M.G. B-50/GAP43 phosphorylation in hippocampal slices from aged rats: effects of phosphatidylserine administration. Neurobiol Aging 14 (1993) 401-406
87. Eckles K.E., Dudek E.M., Bickford P.C., and Browning M.D. Amelioration of age-related deficits in the stimulation of synapsin phosphorylation. Neurobiol Aging 18 (1997) 213-217
88. Racchi M., Govoni S., Solerte S.B., Galli C.L., and Corsini E. Dehydroepiandrosterone and the relationship with aging and memory: a possible link with protein kinase C functional machinery. Brain Res Brain Res Rev 37 (2001) 287-293
89. Joseph J.A., Denisova N.A., Arendash G., Gordon M., Diamond D., Shukitt-Hale B., et al. Blueberry supplementation enhances signaling and prevents behavioral deficits in an Alzheimer disease model. Nutr Neurosci 6 (2003) 153-162
90. Etcheberrigaray R., Tan M., Dewachter I., Kuiperi C., Van der Auwera I., Wera S., et al. Therapeutic effects of PKC activators in Alzheimer's disease transgenic mice. Proc Natl Acad Sci USA 101 (2004) 11141-11146
91. Choi D.S., Wang D., Yu G.Q., Zhu G., Kharazia V.N., Paredes J.P., et al. PKCepsilon increases endothelin converting enzyme activity and reduces amyloid plaque pathology in transgenic mice. Proc Natl Acad Sci USA 103 (2006) 8215-8220
92. Klauck T.M., Faux M.C., Labudda K., Langeberg L.K., Jaken S., and Scott J.D. Coordination of three signaling enzymes by AKAP79, a mammalian scaffold protein. Science 271 5255 (1996) 1589-1592
93. Faux M.C., Rollins E.N., Edwards A.S., Langeberg L.K., Newton A.C., and Scott J.D. Mechanism of A-kinase-anchoring protein 79 (AKAP79) and protein kinase C interaction. Biochem J 343 October (Pt. 2) (1999) 443-452
94. Stebbins E.G., and Mochly-Rosen D. Binding specificity for RACK1 resides in the V5 region of beta II protein kinase C. J Biol Chem 276 32 (2001) 29644-29650