A model for dynamic regulation of choline acetyltransferase by phosphorylation

Journal of Neurochemistry

Volumn 95, Issue 2, 2005, Pages 305-313

  Dobransky, Tomas ^a   Rylett, R Jane ^a  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

Acetylcholine; Binding motifs; Choline acetyltransferase; Phosphorylation; Regulation

Indexed keywords

ACETYLCHOLINE; ADENOSINE TRIPHOSPHATASE; AMINO ACID; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; CALCIUM ION; CHOLINE ACETYLTRANSFERASE; MITOGEN ACTIVATED PROTEIN KINASE; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE (CALCIUM,CALMODULIN) II; PROTEIN KINASE C; SERINE; THREONINE;

ACETYLCHOLINE RELEASE; ALZHEIMER DISEASE; BRAIN; CHOLINERGIC NERVE CELL; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HIPPOCAMPUS; HUMAN; MODEL; NERVE ENDING; NEUROLOGIC DISEASE; NEUROTRANSMITTER RELEASE; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REVIEW;

ACETYLCHOLINE; AMINO ACID SEQUENCE; ANIMALS; CHOLINE O-ACETYLTRANSFERASE; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 26844474356     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03367.x     Document Type: Review

References (59)

1. Auld D. S., Kar S. and Quirion R. (1998) Beta-amyloid peptides as direct cholinergic neuromodulators: a missing link? Trends Neurosci. 21, 43-49.
2. Banik U., Wang G. A., Wagner P. D. and Kaufman S. (1997) Interaction of phosphorylated tryptophan hydroxylase with 14-3-3 proteins. J. Biol. Chem. 272, 26 219-26 225.
3. Battaini F. (2001) Protein kinase C isoforms as therapeutic targets in nervous system disease states. Pharmacol. Res. 44, 353-361.
4. Benishin C. G. and Carroll P. T. (1981) Acetylation of choline and homocholine by membrane-bound choline-O-acetyltransferase in mouse forebrain nerve endings. J. Neurochem. 36, 732-740.
5. Bruce G. and Hersh L. B. (1989) The phosphorylation of choline acetyltransferase. Neurochem. Res. 14, 613-620.
6. Cai Y., Cronin C. N., Engel A. G., Ohno K., Hersh L. B. and Rodgers D. W. (2004) Choline acetyltransferase structure reveals distribution of mutations that cause motor disorders. EMBO J. 23, 2047-2058.
7. Carroll P. T. (1987) Veratridine-induced activation of choline-O-acetyltransferase activity in rat hippocampal tissue: relationship to the veratridine-induced release of acetylcholine. Brain Res. 414, 401-404.
8. Carroll P. T., Badamchian M., Craig P. and Lyness W. H. (1986) Veratridine-induced breakdown of cytosolic acetylcholine in rat hippocampal minces: an intraterminal form of acetylcholinesterase or choline O-acetyltransferase? Brain Res. 383, 83-99.
9. Cooke L. J. and Rylett R. J. (1997) Inhibitors of serine/threonine phosphatases increase membrane-bound choline acetyltransferase activity and enhance acetylcholine synthesis. Brain Res. 751, 232-238.
10. Dai R. M. and Li C. C. (2001) Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitin-proteasome degradation. Nat. Cell Biol. 3, 740-744.
11. Dobransky T., Davis W. L., Xiao G. H. and Rylett R. J. (2000) Expression, purification and characterization of recombinant human choline acetyltransferase: phosphorylation of the enzyme regulates catalytic activity. Biochem. J. 349, 141-151.
12. Dobransky T., Davis W. L. and Rylett R. J. (2001) Functional characterization of phosphorylation of 69-kDa human choline acetyltransferase at serine 440 by protein kinase C. J. Biol. Chem. 276, 22 244-22 250.
13. Dobransky T., Brewer D., Lajoie G. and Rylett R. J. (2003) Phosphorylation of 69-kDa choline acetyltransferase at threonine 456 in response to amyloid-beta peptide 1-42. J. Biol. Chem. 278, 5883-5893.
14. Dobransky T., Doherty-Kirby A., Kim A. R., Brewer D., Lajoie G. and Rylett R. J. (2004) Protein kinase-C isoforms differentially phosphorylate human choline acetyltransferase regulating its catalytic activity. J. Biol. Chem. 279, 52 059-52 068.
15. Eder-Colli L., Amato S. and Froment Y. (1986) Amphiphilic and hydrophilic forms of choline-O-acetyltransferase in cholinergic nerve endings of the Torpedo. Neuroscience 19, 275-287.
16. Fiol C. J., Williams J. S., Chou C., Wang Q. M., Roach P. J. and Anderisani O. M. (1994) A secondary phosphorylation of CREB341 at Ser129 is required for the cAMP-mediated control of gene expression. A role for glycogen synthase kinase-3 in the control of gene expression. J. Biol. Chem. 269, 32 187-32 193.
17. Francis P. T., Palmer A. M., Snape M. and Wilcock G. K. (1999) The cholinergic hypothesis of Alzheimer's disease: a review of progress. J. Neurol. Neurosurg. Psych. 66, 137-147.
18. Gates J., Jr, Ferguson S. M., Blakely R. D. and Apparsundaram S. (2004) Regulation of choline transporter surface expression and phosphorylation by protein kinase C and protein phosphatase 1/2A. J. Pharmacol. Exp. Ther. 310, 536-545.
19. Gill S. K., Bhattacharya M., Fesguson S. S. and Rylett R. J. (2003) Identification of a novel nuclear localization signal common to 69- and 82-kDa human choline acetyltransferase. J. Biol. Chem. 278, 20 217-20 224.
20. Habert E., Birman S. and Mallet J. (1992) High-level synthesis and fate of acetylcholine in baculovirus-infected cells: characterization and purification of recombinant rat choline acetyltransferase. J. Neurochem. 58, 1447-1453.
21. Hoshi M., Takashima A., Noguchi K., Marayama M., Sato M., Kondo S., Saitoh Y., Ishiguro K., Hoshino T. and Imahori K. (1996) Regulation of mitochondrial pyruvate dehydrogenase activity by tau protein kinase I/glycogen synthase kinase 3beta in brain. Proc. Natl Acad. Sci. USA 93, 2719-2723.
22. Hoshi M., Takashima A., Murayama M., Yasutake K., Yoshida N., Ishiguro K., Hoshino T. and Imahori K. (1997) Nontoxic amyloid beta peptide 1-42 suppresses acetylcholine synthesis. Possible role in cholinergic dysfunction in Alzheimer's disease. J. Biol. Chem. 272, 2038-2041.
23. Issa A. M., Gauthier S. and Collier B. (1996) Effects of the phosphatase inhibitors calyculin A and okadaic acid on acetylcholine synthesis and content of rat hippocampal formation. J. Neurochem. 66, 1924-1932.
24. Issa A. M., Gauthier S. and Collier B. (1999a) Enzyme activity and protein of multiple forms of choline acetyltransferase: effects of calyculin A and okadaic acid. Neurochem. Res. 24, 987-993.
25. Issa A. M., Gauthier S. and Collier B. (1999b) Effects of calyculin A and okadaic acid on acetylcholine release and subcellular distribution in rat hippocampal formation. J. Neurochem. 72, 166-173.
26. Kar S., Seto D., Gaudreau P. and Quirion R. (1996) Beta-amyloid-related peptides inhibit potassium-evoked acetylcholine release from rat hippocampal slices. J. Neurosci. 16, 1034-1040.
27. Kar S., Issa A. M., Seto D., Auld D. S., Collier B. and Quirion R. (1998) Amyloid beta-peptide inhibits high-affinity choline uptake and acetylcholine release in rat hippocampal slices. J. Neurochem. 70, 2179-2187.
28. Kaytor M. D. and Orr H. T. (2002) The GSK3 beta signaling cascade and neurodegenerative disease. Curr. Opin. Neurobiol. 12, 275-278.
29. Kennelly P. J. and Krebs E. G. (1991) Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J. Biol. Chem. 266, 15 555-15 558.
30. Kumer S. C. and Vrana K. E. D. (1996) Intricate regulation of tyrosine hydroxylase activity and gene expression. J. Neurochem. 67, 443-462.
31. Loureiro-Dos-Santos N. E., Reis R. A., Kubrusly R. C., de Almeida O. M., Gardino P. F., de Mello M. C. and de Mello F. G. (2001) Inhibition of choline acetyltransferase by excitatory amino acids as a possible mechanism for cholinergic dysfunction in the central nervous system. J. Neurochem. 77, 1136-1144.
32. Lu P. J., Zhou X. Z., Shen M. and Lu K. P. (1999) Function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science 283, 1325-1328.
33. McNeill H., Knebel A., Arthur J. S., Cuenda A. and Cohen P. (2004) A novel UBA and UBX domain protein that binds polyubiquitin and VCP and is a substrate for SAPKs. Biochem. J. 384, 391-400.
34. Mykita S. and Collier B. (1989) Acetylcholine synthesis by a sympathetic ganglion in the presence of 2-(4-phenylpiperidino) cyclohexanol (AH5183) and picrylsulfonic acid. J. Neurochem. 52, 1686-1693.
35. Nagahama M., Suzuki M., Hamada Y., Hatsuzawa K., Tani K., Yamamoto A. and Tagaya M. (2003) SVIP is a novel VCP/p97-interacting protein whose expression causes cell vacuolation. Mol. Biol. Cell 14, 262-273.
36. Namchuk M., Lindsay L., Turck C. W., Kanaani J. and Baekkeskov S. (1997) Phosphorylation of serine residues 3, 6, 10, and 13 distinguishes membrane anchored from soluble glutamic acid decarboxylase 65 and is restricted to glutamic acid decarboxylase 65alpha. J. Biol. Chem. 272, 1548-1557.
37. Nishikawa K., Toker A., Johannes F.-J., Songyang Z. and Cantley L. C. (1997) Determination of the specific substrate sequence motifs of protein kinase C isozymes. J. Biol. Chem. 272, 952-960.
38. Ohno K., Tsujino A., Brengman J. M., Harper C. M., Bajzer Z., Udd B., Beyring R., Robb S., Kirkham F. J. and Engel A. G. (2001) Choline acetyltransferase mutations cause myasthenic syndrome associated with episodic apnea in humans. Proc. Natl Acad. Sci. USA 98, 2017-2022.
39. Patel S. and Latterich M. (1998) The AAA team: related ATPases with diverse functions. Trends Cell. Biol. 8, 65-71.
40. Pedersen W. A., Kloczewiak M. A. and Blusztajn J. K. (1996) Amyloid beta-protein reduces acetylcholine synthesis in a cell line derived from cholinergic neurons of the basal forebrain. Proc. Natl Acad. Sci. USA 93, 8068-8071.
41. Polo S., Sigismund S., Feretta M., Guidi M., Capua M. R., Bossi G., Chen H., De Camilli P. and Di Fiore P. P. (2002) A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416, 451-455.
42. Pongrac J. L. and Rylett R. J. (1996) Differential effects of nerve growth factor on expression of choline acetyltransferase and sodium-coupled choline transport in basal forebrain cholinergic neurons in culture. J. Neurochem. 66, 804-810.
43. Prado M. A., Reis R. A., Prado V. F., de Mello M. C., Gomez M. V. and de Mello F. G. (2002) Regulation of acetylcholine synthesis and storage. Neurochem. Int. 41, 291-299.
44. Resendes M. C., Dobransky T., Ferguson S. S. and Rylett R. J. (1999) Nuclear localization of the 82-kDa form of human choline acetyltransferase. J. Biol. Chem. 274, 19 417-19 421.
45. Salem N., Medilanski J., Pellegrinelli N. and Eder-Colli L. (1994) Hydrophilic and amphiphilic forms of Drosophila choline acetyltransferase are encoded by a single mRNA. Eur. J. Neurosci. 6, 737-745.
46. Salvaterra P. M. and McCaman R. E. (1985) Choline acetyltransferase and acetylcholine levels in Drosophila melanogaster: a study using two temperature-sensitive mutants. J. Neurosci. 5, 903-910.
47. Schmidt B. M. and Rylett R. J. (1993a) Phosphorylation of rat brain choline acetyltransferase and its relationship to enzyme activity. J. Neurochem. 61, 1774-1781.
48. Schmidt B. M. and Rylett R. J. (1993b) Basal synthesis of acetylcholine in hippocampal synaptosomes is not dependent upon membrane-bound choline acetyltransferase activity. Neuroscience 54, 649-656.
49. Sha D., Jin H., Kopke R. D. and Wu J. Y. (2004) Choline acetyltransferase: regulation and coupling with protein kinase and vesicular acetylcholine transporter on synaptic vesicles. Neurochem. Res. 29, 199-207.
50. Soghomonian J. J. and Martin D. L. (1998) Two isoforms of glutamate decarboxylase: why? Trends Pharmacol. Sci. 19, 500-505.
51. Song E. J., Yim S. H., Kim E., Kim N. S. and Lee K. J. (2005) Human Fas-associated factor 1, interacting with ubiquitinated proteins and valosin-containing protein, is involved in the ubiquitin-proteasome pathway. Mol. Cell. Biol. 25, 2511-2524.
52. Tandon A., Bachoo M., Weldon P., Polosa C. and Collier B. (1996) Effects of colchicine application to preganglionic axons on choline acetyltransferase activity and acetylcholine content and release in the superior cervical ganglion. J. Neurochem. 66, 1033-1041.
53. Tran M. H., Yamada K. and Nabeshima T. (2002) Amyloid beta-peptide induces cholinergic dysfunction and cognitive deficits: a mini review. Peptides 23, 1271-1283.
54. Tzivion G. and Avruch J. (2002) 14-3-3 proteins: Active cofactors in cellular regulation by serine/threonine phosphorylation. J. Biol. Chem. 277, 3061-3064.
55. Wei J., Davis K. M., Wu H. and Wu J. Y. (2004) Protein phosphorylation of human brain glutamic acid decarboxylase (GAD) 65 and GAD67 and its physiological implications. Biochemistry 43, 6182-6189.
56. Wu D. and Hersh L. B. (1994) Choline acetyltransferase: celebrating its fiftieth year. J. Neurochem. 62, 1653-1663.
57. Yaffe M. B. and Elia A. E. (2001) Phosphoserine/threonine-binding domains. Curr. Opin. Cell Biol. 13, 131-138.
58. Yaffe M. B. and Smerdon S. J. (2001) PhosphoSerine/Threonine binding domains: you can't pSERious? Structure 9, R33-R38.
59. Zhang H., Wang Q., Kajino K. and Greene M. I. (2000) VCP, a weak ATPase involved in multiple cellular events, interacts physically with BRCA1 in the nucleus of living cells. DNA Cell Biol. 19, 253-263.