Second messenger-regulated protein kinases in the brain: Their functional role and the action of antidepressant drugs

Journal of Neurochemistry

Volumn 74, Issue 1, 2000, Pages 21-33

  Popoli, Maurizio ^a,b   Brunello, Nicoletta ^c   Perez, Jorge ^a   Racagni, Giorgio ^a,d  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^d IRCCS ISTITUTO CENTRO SAN GIOVANNI DI DIO FATEBENEFRATELLI   (Italy)

Author keywords

Antidepressant; Depression; Neurotransmission; Protein kinase; Signal transduction; Transmitter release

Indexed keywords

ANTIDEPRESSANT AGENT; CALCIUM; CYCLIC AMP; MICROTUBULE ASSOCIATED PROTEIN 2; PROTEIN KINASE; PROTEIN KINASE C; SYNAPTOTAGMIN;

DEPRESSION; LONG TERM CARE; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SECOND MESSENGER; SHORT SURVEY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIDEPRESSIVE AGENTS; BRAIN; CYCLIC AMP; ENZYME ACTIVATION; HUMANS; NEURONS; PHOSPHOPROTEINS; PROTEIN KINASES; SECOND MESSENGER SYSTEMS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 0033957413     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2000.0740021.x     Document Type: Short Survey

References (106)

1. IA antagonists. Trends Neurosci. 19, 378-383.
2. Avissar S., Nechamkin Y., Roitman G., and Schreiber G. (1998) Dynamics of ECT normalization of low G protein function and immunoreactivity in mononuclear leukocytes of patients with major depression. Am. J. Psychiatry 155, 666-671.
3. Barden N., Reul J. M. H. M., and Holsboer F. (1995) Do antidepressants stabilize mood through actions on the hypothalamic-pituitary-adrenocortical system? Trends Neurosci. 18, 6-11.
4. Bel N. and Artigas F. (1993) Chronic treatment with fluvoxamine increases extracellular serotonin in frontal cortex but not in raphe nuclei. Synapse 15, 243-245.
5. Belmaker R. H., Bersudsky Y., Agam G., Levine J., and Kofman O. (1996) How does lithium work on manic depression? Clinical and psychological correlates of the inositol theory. Annu. Rev. Med. 47, 47-56.
6. Bennett M. K., Miller K. G., and Scheller R. H. (1993) Casein kinase II phosphorylates the synaptic vesicle protein p65. J. Neurosci. 13, 1701-1707.
7. Blier P. and Bouchard C. (1994) Modulation of 5-HT release in the guinea pig brain following long-term administration of antidepressant drugs. Br. J. Pharmacol. 113, 485-495.
8. Blier P. and de Montigny C. (1994) Current advances and trends in the treatment of depression. Trends Pharmacol. Sci. 15, 220-225.
9. Bottiglieri T. (1997) Ademetionine (S-adenosylmethionine) neuropharmacology: implications for drug therapies in psychiatric and neurological disorders. Exp. Opin. Invest. Drugs 6, 1-10.
10. Bouron A. and Chatton J.-Y. (1999) Acute application of the tricyclic antidepressant desipramine presynaptically stimulates the exocytosis of glutamate in the hippocampus. Neuroscience 90, 729-736.
11. Braun A. P. and Schulman H. (1995) The multifunctional calcium/ calmodulin-dependent protein kinase: from form to function. Annu. Rev. Physiol. 57, 417-445.
12. Bunney W. E. and Davis J. M. (1965) Norepinephrine in depressive reactions: a review. Arch. Gen. Psychiatry 13, 483-494.
13. Chen J. and Rasenick M. M. (1995) Chronic antidepressant treatment facilitates G protein activation of adenylyl cyclase without altering G protein content. J. Pharmacol. Exp. Ther. 275, 509-517.
14. Dell'Acqua M. L. and Scott J. D. (1997) Protein kinase A anchoring. J. Biol. Chem. 272, 12881-12884.
15. Dubovsky S. L., Christiano J., Daniell L. C., Franks R. D., Murphy J., Adler L., Baker N., and Harris R. A. (1989) Increased platelet intracellular calcium concentration in patients with bipolar affective disorders. Arch. Gen. Psychiatry 46, 632-638.
16. Dubovsky S. L., Murphy J., Thomas M., and Rademacher J. (1992) Abnormal intracellular calcium ion concentration in platelets and lymphocytes of bipolar patients. Am. J. Psychiatry 149, 118-120.
17. Duman R. S. (1998) Novel therapeutic approaches beyond the serotonin receptor. Biol. Psychiatry 44, 324-335.
18. Edelman A. M., Blumenthal D. K., and Krebs E. G. (1987) Protein serine-threonine kinases. Annu. Rev. Biochem. 56, 567-613.
19. Erlichman J., Sarkar D., Fleischer N., and Rubin C. S. (1980) Identification of two subclasses of type II cAMP-dependent protein kinases: neural specific and non-neural protein kinases. J. Biol. Chem. 255, 8179-8184.
20. Faux M. C. and Scott J. D. (1996) More on target with protein phosphorylation: conferring specificity by location. Trends Biochem. Sci. 21, 312-315.
21. 2+ sensor for transmitter release at a central synapse. Cell 79, 717-727.
22. 2+/calmodulin-dependent protein kinase II in intact nerve terminals. J. Biol. Chem. 263, 17209-17212.
23. Greengard P., Valtorta F., Czernik A. J., and Benfenati F. (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259, 780-785.
24. Hanks S. K., Quinn A. M., and Hunter T. (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42-52.
25. Hausdorff W. P., Caron M. G., and Lefkowitz R. J. (1990) Turning off the signal: desensitization of beta-adrenergic receptor function. FASEB J. 4, 2881-2889.
26. Haydon P. G., Man-Son-Hing H., Doyle R. T., and Zoran M. (1991) FMRFamide modulation of secretory machinery underlying presynaptic inhibition of synaptic transmission requires a pertussis toxin-sensitive G-protein. J. Neurosci. 11, 3851-3860.
27. 2+/calmodulin-dependent protein kinases within the nucleus. Cell Calcium 23, 103-114.
28. Hirling H. and Scheller R. H. (1996) Phosphorylation of synaptic vesicle proteins: modulation of the aSNAP interaction with the core complex. Proc. Natl. Acad. Sci. USA 93, 11945-11949.
29. Hoyer D., Clarke D. E., Fozard J. R., Hartig P. R., Martin G. R., Mylecharane E. J., Saxena P. R., and Humphrey P. P. A. (1994) International union of pharmacology classification of receptors for 5-hydroxytryptamine (serotonin). Pharmacol. Rev. 46, 157-203.
30. Huganir R. L. and Greengard P. (1990) Regulation of neurotransmitter receptor desensitization by protein phosphorylation. Neuron 5, 555-567.
31. Hyman S. E. and Nestler E. J. (1996) Initiation and adaptation: a paradigm for understanding psychotropic drug action. Am. J. Psychiatry 153, 151-162.
32. Kennedy M. B. (1997) The postsynaptic density at glutamatergic synapses. Trends Neurosci. 20, 264-268.
33. Kreiss D. S. and Lucki I. (1995) Effects of acute and repeated administration of antidepressant drugs on extracellular levels of 5-hydroxytryptamine measured in vivo. J. Pharmacol. Exp. Ther. 274, 866-876.
34. Laduron P. M. (1998) Presynaptic receptors: more hetero than auto. Trends Pharmacol. Sci. 19, 127-128.
35. Lavoie P. A., Beauchamp G., and Elie R. (1997) Atypical antidepressants inhibit depolarization-induced calcium uptake in rat hippocampus synaptosomes. Can. J. Physiol. Pharmacol. 75, 983-987.
36. Lawrence J. C. (1992) Signal transduction and protein phosphorylation in the regulation of cellular metabolism by insulin. Annu. Rev. Physiol. 54, 177-193.
37. Lenox R. H., McNamara R. K., Watterson J. M., and Watson D. G. (1996) Myristoylated alanine-rich C kinase substrate (MARCKS): a molecular target for the therapeutic action of mood stabilizers in the brain? J. Clin. Psychiatry 57 (Suppl. 13), 23-31.
38. Lenox R. H., McNamara R. K., Papke R. L., and Manji H. K. (1998) Neurobiology of lithium: an update. J. Clin. Psychiatry 59 (Suppl. 6), 37-47.
39. Levitan I. B. (1994) Modulation of ion channels by protein phosphorylation and dephosphorylation. Annu. Rev. Physiol. 56, 193-212.
40. 2+-calmodulin-dependent protein kinase II of the transmitter release in squid giant synapse. J. Physiol. (Lond.) 436, 257-282.
41. 3H]cAMP binding sites are unaltered in depressed suicides, but decreased by antidepressants. Brain Res. 758, 223-228.
42. Manji H. K. (1992) G proteins: implications for psychiatry. Am. J. Psychiatry 149, 746-760.
43. Manji H. K., Chen G., Hsiao J. K., Risby E. D., Masana M. I., and Potter W. Z. (1996) Regulation of signal transduction pathways by mood-stabilizing agents: implications for the delayed onset of the therapeutic efficacy. J. Clin. Psychiatry 57 (Suppl. 13), 34-46.
44. Mann C. D., Bich Vu T., and Hrdina P. D. (1995) Protein kinase C in rat brain cortex and hippocampus: effect of repeated administration of fluoxetine and desipramine. Br. J. Pharmacol. 115, 595-600.
45. McGlade-McCulloh E., Yamamoto H., Tan S.-E., Brickey D. A., and Soderling T. R. (1993) Phosphorylation and regulation of glutamate receptors by calcium/calmodulin-dependent protein kinase II. Nature 362, 640-642.
46. Miyamoto S., Asakura M., Sasuga Y., Osada K., Bodaiji N., Imafuku J., and Aoba A. (1997) Effects of long-term treatment with desipramine on microtubule proteins in rat cerebral cortex. Eur. J. Pharmacol. 333, 279-287.
47. Mochly-Rosen D. (1995) Localization of protein kinases by anchoring proteins: a theme in signal transduction. Science 268, 247-251.
48. Mongeau R., Blier P., and de Montigny C. (1997) The serotonergic and noradrenergic systems of the hippocampus: their interactions and the effects of the antidepressant treatments. Brain Res. Rev. 23, 145-195.
49. Mori S., Garbini S., Caivano M., Perez J., and Racagni G. (1998a) Time-course changes in rat cerebral cortex subcellular distribution of the cyclic-AMP binding after treatment with selective serotonin reuptake inhibitors. Int. J. Neuropsychopharmacol. 1, 3-10.
50. Mori S., Zanardi R., Popoli M., Garbini S., Smeraldi E., Racagni G., and Perez J. (1998b) cAMP-dependent phosphorylation system after short and long-term administration of moclobemide. J. Psychiatr. Res. 32, 111-115.
51. Mover J. A., Sigg E. B., and Silver P. J. (1986) Antidepressants and protein kinases: desipramine treatment affects pineal gland cAMP-dependent protein kinase activity. Eur. J. Pharmacol 121, 57-64.
52. Mudd S. H. and Cantoni G. L. (1964) Biological transmethylation methyl group neogenesis and other 'one carbon metabolic reactions dependent upon tetrahydrofolic acid', in Comprehensive Biochemistry, Vol. 15 (Florkin M. and Stolz E. H., eds), pp. 1-47. Elsevier, New York.
53. Nairn A. C., Hemmings H. C., and Greengard P. (1985) Protein kinases in the brain. Annu. Rev. Biochem. 54, 931-976.
54. Nestler E. J., Terwilliger R. Z., and Duman R. S. (1989) Chronic antidepressant administration alters the subcellular distribution of cyclic AMP-dependent protein kinase in rat frontal cortex. J. Neurochem. 53, 1644-1647.
55. Nibuya M., Morinobu S., and Duman R. S. (1995) Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J. Neurosci. 15, 7539-7547.
56. Nibuya M., Nestler E. J., and Duman R. S. (1996) Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J. Neurosci. 16, 2365-2372.
57. Nichols R. A., Haycock J. W., Wang J. K. T., and Greengard P. (1987) Phorbol ester enhancement of neurotransmitter release from rat brain synaptosomes. J. Neurochem. 48, 615-621.
58. Nichols R. A., Sihra T. S., Czernik A. J., Nairn A. C., and Greengard P. (1990) Calcium/calmodulin-dependent protein kinase II increases glutamate and noradrenaline release from synaptosomes. Nature 343, 647-651.
59. Nishizuka Y. (1995) Protein kinase C and lipid signaling for sustained cellular responses. FASEB J. 9, 484-496.
60. Nunoki K., Florio V., and Catterall W. A. (1989) Activation of purified calcium channels by stoichiometric protein phosphorylation. Proc. Natl. Acad. Sci. USA 86, 6816-6820.
61. Obar R. A., Dingus J., Bayley H., and Valee R. B. (1989) The RII subunit of cAMP-dependent protein kinase binds to a common amino-terminal domain in microtubule-associated proteins 2A, 2B and 2C. Neuron 3, 639-645.
62. Page M. E. and Abercrombie E. D. (1997) An analysis of the effects of acute and chronic fluoxetine on extracellular norepinephrine in the rat hippocampus during stress. Neuropsychopharmacology 16, 419-425.
63. + channels by antidepressant drugs. J. Pharmacol. Exp. Ther. 284, 208-214.
64. Pasinelli P., Ramakers G. M., Urban I. J., Hens J. J., Oestreicher A. B., de Graan P. N., and Gispen W. H. (1995) Long-term potentiation and synaptic protein phosphorylation. Behav. Brain Res. 66, 53-59.
65. Perez J., Tinelli D., Bianchi E., Brunello N., and Racagni G. (1991) cAMP binding proteins in the rat cerebral cortex after administration of selective 5-HT and NE reuptake blockers with antidepressant activity. Neuropsychopharmacology 4, 57-64.
66. Perez J., Tinelli D., Cagnoli C., Pecin P., Brunello N., and Racagni G. (1993) Evidence for the existence of cAMP-dependent protein kinase phosphorylation system associated with specific phosphoproteins in stable microtubules from rat cerebral cortex. Brain Res. 602, 77-83.
67. Popoli M. (1993a) p65-synaptotagmin: a docking-fusion protein in synaptic vesicle exocytosis? Neuroscience 54, 323-328.
68. 2+/calmodulin protein kinase II in synaptic vesicles. FEBS Lett. 317, 85-88.
69. 2+/calmodulin-dependent protein kinase II: autophosphorylation and activity increase in the hippocampus after long-term blockade of serotonin reuptake. Mol. Pharmacol. 48, 623-629.
70. Popoli M., Venegoni A., Vocaturo C., Buffa L., Perez J., Smeraldi E., and Racagni G. (1997a) Long-term blockade of serotonin reuptake affects synaptotagmin phosphorylation in the hippocampus. Mol. Pharmacol. 51, 19-26.
71. Popoli M., Zanotti S., Rudaelli R., Gaggianesi C., Verona M., Brunello N., and Racagni G. (1997b) The neurotransmitter release machinery as a site of action for psychotropic drugs: effect of typical and atypical antidepressants. Soc. Neurosci. Abstr. 23, 25.
72. Popoli M., Verona M., Zanotti S., Gaggianesi C., Schafer T., and Racagni G. (1998) Regulation by calcium of synaptotagmin interaction with SNARE proteins. Soc. Neurosci. Abstr. 24, 1568.
73. Racagni G., Brunello N., Tinelli D., and Perez J. (1992) New biochemical hypotheses on the mechanism of action of antidepressant drugs: cAMP-dependent phosphorylation system. Pharmacopsychiatry 25, 51-55.
74. Racagni G., Popoli M., Mori S., Brunello N., and Perez J. (1996) Targeting the action of antidepressant drugs on second messenger systems, in Implications of Psychopharmacology to Psychiatry (Ackeneil M., Bondy B., Ermann M., and Nedopil N., eds), pp. 34-40. Springer, New York.
75. Rahimian R. and Hrdina P. D. (1995) Possible role of protein kinase C in regulation of 5-hydroxytryptamine 2A receptors in rat brain. Can. J. Physiol. Pharmacol. 73, 1686-1691.
76. 3H]cyclic AMP binding in postmortem brain from subjects with bipolar affective disorder. J. Neurochem. 68, 297-304.
77. Ramamoorthy S., Giovanetti E., Qian Y., and Blakely R. D. (1998) Phosphorylation and regulation of antidepressant-sensitive serotonin transporters. J. Biol. Chem. 273, 2458-2466.
78. Rosin D. L., Melia K., Knorr A. M., Nestler E. J., Roth R. H., and Duman R. S. (1995) Chronic imipramine administration alters the activity and phosphorylation state of tyrosine hydroxylase in dopaminergic regions of rat brain. Neuropsychopharmacology 12, 113-121.
79. 2+/calmodulin-stimulated protein kinase II in brain. J. Neurochem. 59, 1191-1202.
80. Rotenberg A., Mayford M., Hawkins R. D., Kandel E. R., and Muller R. U. (1996) Mice expressing activated CaMKII lack low frequency LTP and do not form stable place cells in the CA1 region of the hippocampus. Cell 87, 1351-1361.
81. Rubino H. M., Dammerman M., Shafit-Zagardo B., and Erlichman J. (1989) Localization and characterization of the binding site for the regulatory subunit of type II cAMP-dependent protein kinase on MAP2. Neuron 3, 631-638.
82. Sanders-Bush E., Conn J., and Sulser F. (1985) The serotonin/norepinephrine-linked beta-adrenoceptor system and the mode of action of antidepressants. Psychopharmacol. Bull. 21, 373-378.
83. Sandler M. (1998) Forty years in the conceptual wilderness. Science 280, 1709-1710.
84. Scheller R. H. (1995) Membrane trafficking in the presynaptic terminal. Neuron 14, 893-897.
85. Schildkraut J. J. (1965) The catecholamine hypothesis of affective disorders: a review of supportive evidence. Am. J. Psychiatry 122, 509-522.
86. Schulz K. P. and Miller R. J. (1992) Inhibition of quantal transmitter release in the absence of calcium influx by a G protein-linked adenosine receptor at hippocampal synapses. Neuron 8, 1139-1150.
87. Schwartz J. P. and Costa E. (1980) Protein kinase translocation following β-adrenergic receptor activation in C6 glioma cells. J. Biol. Chem. 255, 2943-2948.
88. Selbie L. A. and Hill S. J. (1998) G protein-coupled-receptor cross-talk. The fine tuning of multiple receptor-signalling pathways. Trends Pharmacol. Sci. 19, 87-93.
89. Shelton R. C., Mainer D. H., and Sulser F. (1996) cAMP-dependent protein kinase activity in major depression. Am. J. Psychiatry 153, 1037-1042.
90. Shimazaki Y., Nishiki T., Omori A., Sekiguchi M., Kamata Y., Kozaki S., and Takahashi M. (1996) Phosphorylation of 25-kDa synaptosome-associated protein. J. Biol. Chem. 271, 14548-14553.
91. 2+ of rat cortical neurons. Eur. J. Pharmacol. 268, 65-71.
92. 2+-regulated myosin phosphorylation by fluoxetine and iprindole. Eur. J. Pharmacol. 121, 65-71.
93. Sollner T., Bennet M. K., Whiteheart S. W., Scheller R. H., and Rothman J. E. (1993) A protein assembly-disassembly pathway in vitro thai may correspond to sequential steps of synaptic vesicle docking, activation and fusion. Cell 75, 409-418.
94. Stahl S. M. (1997) Psychopharmacology of Antidepressants. Martin Dunitz, London.
95. Stevens C. F. and Sullivan J. M. (1998) Regulation of the readily releasable vesicle pool by protein kinase C. Neuron 21, 885-893.
96. Tanaka C. and Nishizuka Y. (1994) The protein kinase C family for neuronal signaling. Annu. Rev. Neurosci. 17, 551-567.
97. Taylor S. S., Buechler J. A., and Yonemoto W. (1990) cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu. Rev. Biochem. 59, 971-1005.
98. Taylor S. S., Knighton D. R., Zheng J., Ten Eyck L. F., and Sowadski J. M. (1992) Structural framework for the protein kinase family. Annu. Rev. Cell Biol. 8, 429-462.
99. Travagli R. A., Gillis R. A., and Kellar K. J. (1994) 5-Adenosyl-l-methionine modulates firing rate of dorsal motor nucleus of the vagus neurones in vitro. Eur. J. Pharmacol. 264, 385-390.
100. 2+/calmodulin-dependent protein kinase II with secretion and tyrosine hydroxylase activation in cultured bovine adrenal medullary cells. Mol. Pharmacol. 46, 1041-1047.
101. Verona M., Zanotti S., Gaggianesi C., Schafer T., Racagni G., and Popoli M. (1998) Modulation of protein-protein interaction in presynaptic terminals: a possible site of action for psychotropic drugs. Int. J. Neuropsychopharmacol. 1 (Suppl.), S64.
102. Williams J. T., Colmers W. F., and Pan Z. Z. (1988) Voltage- and ligand-activated inwardly rectifying currents in dorsal raphe neurons in vitro. J. Neurosci. 8, 3499-3506.
103. Wright S. C., Schellenberger U., Ji L., Wang H., and Larrick J. W. (1997) Calmodulin-dependent protein kinase II mediates signal transduction in apoptosis. FASEB J. 11, 843-849.
104. Yamaji T., Kaguya A., Uchitomi Y., Yokota N., and Yamawaki S. (1997) Chronic treatment with antidepressants, verapamil, or lithium inhibits the serotonin-induced intracellular calcium response in individual C6 rat glioma cells. Life Sci. 60, 817-823.
105. Yokoyama C. T., Sheng Z.-H., and Catterall W. A. (1997) Phosphorylation of the synaptic protein interaction site on N-type calcium channels inhibits interactions with SNARE proteins. J. Neurosci. 17, 6929-6938.
106. Zanotti S., Mori S., Radaelli R., Perez J., Racagni G., and Popoli M. (1998) Modifications in brain cAMP- and calcium/calmodulin-dependent protein kinases induced by treatment with S-adenosyl-methionine. Neuropharmacology 37, 1081-1089.