Curcumin-induced degradation of PKCδ is associated with enhanced dentate NCAM PSA expression and spatial learning in adult and aged Wistar rats

Biochemical Pharmacology

Volumn 77, Issue 7, 2009, Pages 1254-1265

  Conboy, Lisa ^a   Foley, Andrew G ^a   O'Boyle, Noel M ^a   Lawlor, Marie ^a   Gallagher, Helen C ^a   Murphy, Keith J ^a   Regan, Ciaran M ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Curcumin; NCAM PSA; PKC ; PST; Spatial learning

Indexed keywords

CURCUMIN; NERVE CELL ADHESION MOLECULE; NERVE CELL ADHESION MOLECULE POLY ALPHA2,8 LINKED SIALIC ACID; PROTEIN KINASE C DELTA; SIALIC ACID DERIVATIVE; TYROSINE; UNCLASSIFIED DRUG;

AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COMPUTER PROGRAM; CONTROLLED STUDY; CRYSTAL STRUCTURE; DENTATE GYRUS; DEPTH PERCEPTION; DRUG EFFECT; DRUG PROTEIN BINDING; ENZYME ACTIVITY; ENZYME DEGRADATION; LEARNING; MEMORY CONSOLIDATION; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT; SPATIAL MEMORY;

AGING; ANIMALS; CELL LINE, TUMOR; CURCUMIN; DENTATE GYRUS; GENE EXPRESSION REGULATION; MALE; MAZE LEARNING; NEURAL CELL ADHESION MOLECULE L1; PROTEIN KINASE C-DELTA; RATS; RATS, WISTAR; SIALIC ACIDS; SPATIAL BEHAVIOR;

EID: 61449159627     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2008.12.011     Document Type: Article

References (81)

1. Sadoul R., Hirn M., Deagostini-Bazin H., Rougon G., and Goridis C. Adult and embryonic mouse neural cell adhesion molecules have different binding properties. Nature 30 (1983) 347-349
2. Rougon G., Dubois C., Buckley N., Magnani J.L., and Zollinger W. A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J Cell Biol 103 (1986) 429-437
3. Bonfanti L. PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog Neurobiol 80 (2006) 129-164
4. Gascon E., Vutskits L., and Kiss J.Z. Polysialic acid-neural cell adhesion molecule in brain plasticity: from synapses to integration of new neurons. Brain Res Rev 56 (2007) 101-118
5. Rutishauser U. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci 9 (2008) 26-35
6. Hoyk Z.S., Parducz A., and Theodosis D.T. The highly sialylated isoform of the neural cell adhesion molecule is required for estradiol-induced morphological plasticity in the adult arcuate nucleus. Eur J Neurosci 13 (2001) 649-656
7. Stoenica L., Senkov O., Gerardy-Schahn R., Weinhold B., Schachner M., and Dityatev A. In vivo synaptic plasticity in the dentate gyrus of mice deficient in the neural cell adhesion molecule NCAM or its polysialic acid. Eur J Neurosci 23 (2006) 2255-2264
8. O'Malley A., O'Connell C., and Regan C.M. Ultrastructural analysis reveals avoidance conditioning to induce a transient increase in hippocampal dentate spine density in the 6 h post-training period of consolidation. Neuroscience 87 (1998) 607-613
9. O'Malley A., O'Connell C., Murphy K.J., and Regan C.M. Transient spine density increases in the mid-molecular layer of the hippocampal dentate gyrus accompany consolidation of a spatial learning task in the rodent. Neuroscience 99 (2000) 229-232
10. Eyre M.D., Richter-Levin G., Avital A., and Stewart M.G. Morphological changes in the hippocampal dentate gyrus synapses following spatial learning in rats are transient. Eur J Neurosci 17 (2003) 1973-1980
11. Fox G.B., O'Connell A.W., Murphy K.J., and Regan C.M. Memory consolidation induces a transient and time-dependent increase in the frequency of NCAM-polysialylated cells in the adult rat hippocampus. J Neurochem 65 (1995) 2796-2797
12. Murphy K.J., O' Connell A.W., and Regan C.M. Repetitive and transient increases in hippocampal neural cell adhesion molecule polysialylation state following multi-trial spatial training. J Neurochem 67 (1996) 1268-1274
13. Sandi C., Merino J.J., Cordero M.I., Kruyt N., Murphy K.J., and Regan C.M. Modulation of hippocampal NCAM polysialylation by stressful experiences. Biol Psychiatry 15 (2003) 599-607
14. Becker C.G., Artola A., Gerardy-Schahn R., Becker T., Welzl H., and Schachner M. The polysialic acid modification of the neural cell adhesion molecule is involved in spatial learning and hippocampal long-term potentiation. J Neurosci Res 45 (1996) 143-152
15. Muller D., Wang C., Skibo G., Toni N., Cremer H., Calaora V., et al. PSA-NCAM is required for activity-induced synaptic plasticity. Neuron 17 (1996) 413-422
16. Venero C., Herrero A.I., Touyarot K., Cambon K., López-Fernández M.A., Berezin V., et al. Hippocampal up-regulation of NCAM expression and polysialylation plays a key role on spatial memory. Eur J Neurosci 23 (2006) 1585-1595
17. Lópéz-Fernández M.A., Montaron M.-F., Varea E., Rougon G., Venero C., Abrous D.N., et al. Upregulation of polysialylated neural cell adhesion molecule in dorsal hippocampus after contextual fear conditioning is involved in long-term memory formation. J Neurosci 27 (2007) 4552-4561
18. Seymour C.M., Foley A.G., Murphy K.J., and Regan C.M. Intraventricular infusions of anti-NCAM PSA impair the process of consolidation of both avoidance conditioning and spatial learning paradigms in Wistar rats. Neuroscience 157 (2008) 813-820
19. Scheidegger E.P., Sternberg L.R., Roth J., and Lowe J.B. A human STX cDNA confers polysialic acid expression in mammalian cells. J Biol Chem 270 (1995) 22685-22688
20. Yoshida Y., Kojima N., Kurosawa N., Hamamoto T., and Tsuji S. Molecular cloning of Sia alpha 2,3Gal beta 1,4GlcNAc alpha 2,8-sialyltransferase from mouse brain. J Biol Chem 270 (1995) 14628-14633
21. Eckhardt M., Mühlenhoff M., Bethe A., Koopman J., Frosch M., and Gerardy-Schahn R. Molecular characterization of eukaryotic polysialyltransferase-1. Nature 373 (1995) 715-718
22. Nakayama J., Fukuda M.N., Fredette B., Ranscht B., and Fukuda M. Expression cloning of a human polysialyltransferase that forms the polysialylated neural cell adhesion molecule present in embryonic brain. Proc Natl Acad Sci USA 92 (1995) 7031-7035
23. Hildebrandt H., Becker C., Murau M., Gerardy-Schahn R., and Rahmann H. Heterogenous expression of the polysialyltransferases ST8Sia II and ST8Sia IV during postnatal rat brain development. J Neurochem 71 (1998) 2339-2348
24. Ong E., Nakayama J., Angata K., Reyes L., Katsuyama T., Arai Y., and Fukuda M. Developmental regulation of polysialic acid synthesis in mouse directed by two polysialyltransferases, PST and STX. Glycobiology 8 (1998) 415-424
25. Alcaraz G., and Goridis G. Biosynthesis and processing of polysialylated NCAM by AtT20 cells. Eur J Cell Biol 55 (1991) 165-173
26. Gallagher H.C., Odumeru O.A., and Regan C.M. Regulation of neural cell adhesion molecule polysialylation state by cell-cell contact and protein kinase C delta. J Neurosci Res 61 (2000) 636-645
27. Gallagher H.C., Murphy K.J., Foley A.G., and Regan C.M. Protein kinase C delta regulates neural cell adhesion molecule polysialylation state in the rat brain. J Neurochem 77 (2001) 425-434
28. Fox G.B., Kennedy N., and Regan C.M. Polysialylated neural cell adhesion molecule expression by neurons and astroglila processes in the rat dentate gyrus declines dramatically with increasing age. Int J Dev Neurosci 13 (1995) 663-672
29. Gu X., Preuβ U., Gu T., and Yu R.K. Regulation of sialyltransferase activities by phosphorylation and dephosphorylation. J Neurochem 64 (1995) 2295-2302
30. Gao L., Gu X.-B., Yu D.S., Yu R.K., and Zeng G. Association of a 14-3-3 protein with CMP-NeuNAc: GM1 α2,3-sialyltransferase. Biochem Biophys Res Commun 224 (1996) 103-107
31. Ma J., Siminovic M., Qian R., and Colley K.J. Sialyltransferase isoforms are phosphorylated in the cis-medial Golgi on serine and threonine residues in their luminal sequences. J Biol Chem 274 (1999) 8046-8052
32. Breen K.C., and Georgopoulou N. The role of protein phosphorylation in α2,6(N)-sialyltransferase activity. Biochem Biophys Res Commun 309 (2003) 32-35
33. Kishimoto A., Mikawa K., Hashimoto K., Yasuda I., Tanaka S., Tominaga M., et al. Limited proteolysis of protein kinase C subspecies by calcium-dependent neutral protease (calpain). J Biol Chem 264 (1989) 4088-4092
34. Blake R.A., Garcia-Paramio P., Parkera P.J., and Courtneidge S.A. Src promotes PKCδ degradation. Cell Growth Diff 10 (1999) 231-241
35. Gschwendt M., Muller H.J., Kielbassa K., Zang R., Kittstein W., Rincke G., et al. Rottlerin, a novel protein kinase inhibitor. Biochem Biophys Res Commun 199 (1994) 93-98
36. Davies S.P., Reddy H., Caivano M., and Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351 (2000) 95-105
37. Soltoff S.P. Rottlerin: an inappropriate and ineffective inhibitor of PKCδ. Trends Pharmacol Sci 28 (2007) 453-458
38. Lipinski C.A., Lombardo F., Dominy B.W., and Feeney F.P. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 23 (1997) 3-25
39. Godl K., Wissing J., Kurtenbach A., Habenberger P., Blencke S., Gutbrod H., et al. An efficient proteomics method to identify the cellular targets of protein kinase inhibitors. Proc Natl Acad Sci USA 100 (2003) 15434-15439
40. Zhang G., Kazanietz M.G., Blumberg P.M., and Hurley J.H. Crystal structure of the cys2 activator-binding domain of protein kinase C delta in complex with phorbol ester. Cell 81 (1995) 917-924
41. Wang Y.J., Pan M.H., Cheng A.L., Lin L.I., Ho Y.S., Hsieh C.Y., et al. Stability of curcumin in buffer solutions and characterization of its degradation products. J Pharm Biomed Anal 15 (1997) 1867-1876
42. Mizuno K., Saido T.C., Ohno S., Tamaoki T., and Suzuki K. Staurosporine-related compounds, K252a and UCN-01, inhibit both cPKC and nPKC. FEBS Lett 330 (1993) 114-116
43. Lu Z., Liu D., Hornia A., Devonish W., Pagano M., and Foster D.A. Activation of protein kinase C triggers its ubiquitination and degradation. Mol Cell Biol 18 (1998) 839-845
44. Steinberg S.F. Distinctive activation mechanisms and functions for protein kinase Cdelta. Biochem J 384 (2004) 449-459
45. Zingg J.M., and Azzi A. Non-antioxidant activities of vitamin E. Curr Med Chem 11 (2004) 1113-1133
46. Zingg J.M., and Azzi A. Non-antioxidant activities of vitamin E. Curr Med Chem 11 (2004) 1113-1133
47. Ferri P., Cecchini T., Ambrogini P., Betti M., Cuppini R., Del Grande P., et al. α-Tocopherol affects neuronal plasticity in adult rat dentate gyrus: the possible role of PKCδ. J Neurobiol 66 (2006) 793-810
48. Goel A., Kunnumakkara A.B., and Aggarwal B.B. Curcumin as "Curecumin": from kitchen to clinic. Biochem Pharmacol 75 (2008) 787-809
49. Ebadi M., Sharma S., Shavali S., and El Reaey H. Neuroprotective actions of selegiline. J Neurosci Res 67 (2002) 285-289
50. Murphy K.J., Foley A.G., O'Connell A.W., and Regan C.M. Chronic exposure of rats to cognition enhancing drugs produces a neuroplastic response identical to that obtained by complex environment rearing. Neuropsychopharmacology 31 (2006) 90-100
51. Duveau V., Arthaud S., Rougier A., and Le Gal le Salle G. Polysialylation of NCAM is upregulated by hyperthermia and participates in heat shock preconditioning-induced neuroprotection. Neurobiol Dis 26 (2007) 385-395
52. Kim S.J., Son T.G., Park H.R., Park M., Kim M.S., Kim H.S., et al. Curcumin stimulates proliferation of embryonic neural progenitor cells and neurogenesis in the adult hippocampus. J Biol Chem 283 (2008) 14497-14505
53. 6 receptor antagonists SB-271046 and SB-399885 potentiate NCAM-PSA immunolabelling of dentate granule cells, but not neurogenesis, in the hippocampal formation of mature Wistar rats. Neuropharmacology 54 (2008) 1166-1174
54. Ge S., Yang C.H., Hsu K.S., Ming G.L., and Song H. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54 (2007) 559-566
55. Kee N., Teixeira C.M., Wang A.H., and Frankland P.W. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10 (2007) 355-362
56. Toni N., Laplagne D.A., Zhao C., Lombardi G., Ribak C.E., Gage F.H., et al. Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci 11 (2008) 901-907
57. Pham K., McEwen B.S., LeDoux J.E., and Nader K. Fear learning transiently impairs hippocampal cell proliferation. Neuroscience 130 (2005) 17-24
58. Sandi C., Cordero M.I., Merino J.J., Kruyt N.D., Regan C.M., and Murphy K.J. Neurobiological correlates of individual differences in spatial learning ability. Learn Mem 11 (2004) 244-252
59. Young D., Lawlor P.A., Leone P., Dragunow M., and During M.J. Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nat Med 5 (1999) 448-453
60. Liu Y., Dargusch R., Maher P., and Schubert D. A broadly protective derivative of curcumin. J Neurochem 105 (2008) 1336-1345
61. Maher P., Akaishi T., Schubert D., Abe K. A pyrazole derivative of curcumin enhances memory. Neurobiol Aging (2008) in press.
62. Silva A.J., Paylor R., Wehner J.M., and Tonegawa S. Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science 257 (1992) 206-211
63. Williams E.J., Mittal B., Walsh F.S., and Doherty P. A Ca2+/calmodulin kinase inhibitor, KN-62, inhibits neurite outgrowth stimulated by CAMs and FGF. Mol Cell Neurosci 6 (1995) 69-79
64. Jagatha B., Mythri R.B., Vali S., and Bharath M.M.S. Curcumin treatment alleviates the effects of glutathione depletion in vitro and in vivo: therapeutic implications for Parkinson's disease explained via in silico studies. Free Radic Biol Med 44 (2008) 907-917
65. Shukla P.K., Khanna V.K., Ali M.M., Khan M.Y., and Srimal R.C. Anti-ischemic effect of curcumin in rat brain. Neurochem Res 33 (2008) 1036-1043
66. Ryu E.K., Choe Y.S., Lee K.H., Choi Y., and Kim B.T. Curcumin and dihydrozingerone derivatives: synthesis, radiolabelling, and evaluation for beta-amyloid plaque imaging. J Med Chem 49 (2006) 6111-6119
67. Shankar T.N., Shanta N.V., Ramesh H.P., Murthy I.A., and Murthy V.S. Toxicity studies on turmeric (Curcuma longa): acute toxicity studies in rats, guineapigs and monkeys. Indian J Exp Biol 18 (1980) 73-75
68. Lao C.D., Ruffin M.T., Normolle D., Heath D.D., Murray S.I., Bailey J.M., et al. Dose escalation of a curcuminoid formulation. BMC Complement Altern Med 6 (2006) 10
69. Abrous D.N., Montaron M.F., Petry K.G., Rougon G., Darnaudery M., Le Moal M., et al. Decrease in highly polysialylated neuronal cell adhesion molecules and in spatial learning during ageing are not correlated. Brain Res 744 (1997) 285-292
70. Stanton M.E. Multiple memory systems, development and conditioning. Behav Brain Res 110 (2000) 25-37
71. Romano A., Freudenthal R., Merlo E., and Routtenberg A. Evolutionarily-conserved role of the NF-kappaB transcription factor in neural plasticity and memory. Eur J Neurosci 24 (2006) 1507-1516
72. Wang Y., Chan S.L., Miele L., Yao P.J., Mackes J., Ingram D.K., et al. Involvement of Notch signalling in hippocampal plasticity. Proc Natl Acad Sci USA 101 (2004) 9458-9462
73. Chen Y., Shu W., Chen W., Wu Q., Liu H., and Cui G. Curcumin, both histone deacetylase and p300/CBP-specific inhibitor, represses the activity of nuclear factor kappa B and Notch 1 in Raji cells. Basic Clin Pharmacol Toxicol 101 (2007) 427-433
74. Conboy L., Seymour C.M., Monopoli M.P., O'Sullivan N.C., Murphy K.J., and Regan C.M. Notch signalling becomes transiently attenuated during long-term memory consolidation in adult Wistar rats. Neurobiol Learn Mem 88 (2007) 342-351
75. Shishodia S., Singh T., and Chaturvedi M.M. Modulation of transcription factors by curcumin. Adv Exp Med Biol 595 (2007) 127-148
76. Mikkonen M., Soininen H., Tapiola T., Alafuzoff I., and Miettinen R. Hippocampal plasticity in Alzheimer's disease: changes in highly polysialylated NCAM immunoreactivity in the hippocampal formation. Eur J Neurosci 11 (1999) 1754-1764
77. Wu A., Ying Z., and Gomez-Pinilla F. Dietary curcumin counteracts the outcome of traumatic brain injury on oxidative stress, synaptic plasticity, and cognition. Exp Neurol 197 (2006) 309-317
78. Xu Y., Ku B., Tie L., Yao H., Jiang W., Ma X., et al. Curcumin reverses the effects of chronic stress on behaviour, the HPA axis, BDNF expression and phosphorylation of CREB. Brain Res 1122 (2006) 56-64
79. Begum A.N., Jones M.R., Lim G.P., Morihara T., Kim P., Heath D.D., et al. Curcumin structure-function, bioavailability, and efficacy in models of neuroinflammation and Alzheimer's disease. J Pharmacol Exp Ther 326 (2008) 196-208
80. Ganguli M., Chandra V., Kamboh M.I., Johnston J.M., Dodge H.H., Thelma B.H., et al. Apolipoprotein E polymorphism and Alzheimer disease. Arch Neurol 57 (2000) 824-830
81. Ng T.P., Chiam P.C., Lee T., Chua H.C., Lim L., and Kua E.H. Curry consumption and cognitive function in the elderly. Am J Epidemiol 164 (2006) 898-906