In vitro phosphorylation of acetylcholinesterase at non-consensus protein kinase A sites enhances the rate of acetylcholine hydrolysis

Molecular Brain Research

Volumn 51, Issue 1-2, 1997, Pages 179-187

  Grifman, Mirta ^a   Arbel, Ayelet ^a   Ginzberg, Dalia ^a   Glick, David ^a   Elgavish, Sharona ^a   Shaanan, Boaz ^a   Soreq, Hermona ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Acetylcholinesterase; cAMP dependent protein kinase A; Neurotransmission; Non consensus phosphorylation site; Protein phosphorylation

Indexed keywords

ACETYLCHOLINESTERASE; CYCLIC AMP DEPENDENT PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CHOLINERGIC TRANSMISSION; ENZYME ACTIVE SITE; FEEDBACK SYSTEM; HUMAN; ISOELECTRIC POINT; MOUSE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ACETYLCHOLINE; ACETYLCHOLINESTERASE; ACETYLTHIOCHOLINE; ANIMALS; BRAIN; CATTLE; CLONING, MOLECULAR; CONSENSUS SEQUENCE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ERYTHROCYTES; ESCHERICHIA COLI; HUMANS; HYDROLYSIS; KINETICS; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SERINE; THREONINE;

ANIMALIA; MAMMALIA;

EID: 0030778075     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-328X(97)00246-5     Document Type: Article

References (51)

1. Barak D., Ordentlich A., Bromberg A., Kronman C., Marcus D., Lazar A., Ariel N., Velan B., Shafferman A. Allosteric modulation of acetylcholinesterase activity by peripheral ligands involves a conformational transition of the anionic subsite. Biochemistry. 34:1995;15444-15452.
2. Barthalay Y., Hipeau-Jacquotte R., De la Escalera S., Jimenez F., Piovant M. Drosophila neurotactin mediates heterophilic cell adhesion. EMBO J. 9:1990;3603-3609.
3. Ben Aziz-Aloya R., Seidman S., Timberg R., Sternfeld M., Zakut H., Soreq H. Expression of a human acetylcholinesterase promoter-reporter construct in developing neuromuscular junctions of Xenopus embryos. Proc. Natl. Acad. Sci. USA. 90:1993;2471-2475.
4. D.M. Bolag and S.J. Edelstein, Protein Methods, Wiley-Liss, New York, 1991, pp. 161-174.
5. Bourne Y., Taylor P., Marchot P. Acetylcholinesterase inhibition by fasciculin: crystal structure of the complex. Cell. 83:1995;503-512.
6. Changeux J.-P. Responses of acetylcholinesterase from Torpedo marmorata to salts and curarizing drugs. Mol. Pharmacol. 2:1966;369-392.
7. Fischer M., Ittah A., Liefer I., Gorecki M. Expression and reconstitution of biologically active human acetylcholinesterase from Escherichia coli. Cell. Mol. Neurobiol. 13:1993;25-38.
8. Greenfield S. Acetylcholinesterase may have novel functions in the brain. Trends Neurosci. 7:1984;364-368.
9. Gross E., Goldberg D., Levitzki A. Phosphorylation of S. cerevisiae Cdc25 in response to glucose results in its dissociation from Ras. Nature. 360:1992;762-765.
10. Harel M., Kleywegt G.J., Ravelli R.B., Silman I., Sussman J.L. Crystal structure of an acetylcholinesterase-fasciculin complex: interaction of a three-fingered toxin from snake venom with its target. Structure. 3:1995;1355-1366.
11. E. Harlow, D. Lane, Antibodies: A Laboratory Manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1988, pp. 488-495.
12. R. Higuchi, Recombinant PCR, in: M.A. Innis, D.H. Gelfand, J.J. Sninsky, T.J. White (Eds.), PCR Protocols: A Guide to Methods and Applications, Academic Press, San Diego, CA, 1990, pp. 177-183.
13. Hoffman P.W., Ravindran A., Huganir R.L. Role of phosphorylation in desensitization of acetylcholine receptors expressed in Xenopus oocytes. J. Neurosci. 14:1994;4185-4195.
14. Hyde E.G., Carmichael W.W. Anatoxin-a(s), a naturally occurring organophosphate, is an irreversible active site-directed inhibitor of acetylcholinesterase (EC 3.1.1.7). J. Biochem. Toxicol. 6:1991;195-201.
15. Ichtchenko K., Nguyen T., Sudhof T.C. Structures, alternative splicing and neurexin binding of multiple neuroligins. J. Biol. Chem. 271:1996;2676-2682.
16. Inestrosa N.C., Alvarez A., Perez C.A., Moreno R.D., Vicente M., Linker C., Casanueva O.I., Soto C., Garrido J. Acetylcholinesterase accelerates assembly of amyloid-β-peptides into Alzheimer's fibrils: possible role of the peripheral site of the enzyme. Neuron. 16:1996;881-891.
17. Johansson I.M., Nordberg A. Pharmacokinetic studies of cholinesterase inhibitors. Acta Neurol. Scand. Suppl. 149:1993;22-25.
18. Karpel R., Sternfeld M., Ginzberg D., Guhl E., Graessmann A., Soreq H. Overexpression of alternative human acetylcholinesterase forms modulates process extensions in cultured glioma cells. J. Neurochem. 66:1996;114-123.
19. Knapp M.J., Knopman D.S., Solomon P.R., Pendlebury W.W., David C.S., Gracon S.I. A 30-week randomized controlled trial of high-dose tacrine in patients with Alzheimer's disease. J. Am. Med. Assoc. 271:1994;985-991.
20. Kreimer D.I., Szosenfogel R., Goldfarb D., Silman I., Weiner L. Two-state transition between molten globule and unfolded states of acetylcholinesterase as monitored by electron paramagnetic resonance spectroscopy. Proc. Natl. Acad. Sci. USA. 91:1994;12145-12149.
21. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London). 227:1970;680-683.
22. Layer P., Willbold E. Novel functions of cholinesterases in development, physiology and disease. Prog. Hisotchem. Cytochem. 29:1995;1-92.
23. L'Na C., Changeux J.-P. Allosteric modulation of the nicotinic acetylcholine receptor. Trends Neurolog. Sci. 16:1993;181-186.
24. Loewenstein-Lichtenstein Y., Glick D., Gluzman N., Sternfeld M., Zakut H., Soreq H. Overlapping drug interaction sites of human butyrylcholinesterase dissected by site-directed mutagenesis. Mol. Pharmacol. 50:1996;1423-1431.
25. Massoulié J., Pezzementi L., Bon S., Krejci E., Vallette F.M. Molecular and cellular biology of cholinesterases. Prog. Neurobiol. 41:1993;31-91.
26. Meflah K., Bernard S., Massouli' J. Interaction with lectins indicates differences in the carbohydrate composition of the membrane-enzymes acetylcholinesterase and 5′-nucleotidase in different cell types. Biochemie. 66:1984;59-69.
27. Millard C.B., Broomfield C.A. Anticholinesterases: medical applications of neurochemical principles. J. Neurochem. 64:1995;1909-1918.
28. Miller S., Janin J., Lisk A.M., Chothia C. Interior and surface of monomeric proteins. J. Mol. Biol. 196:1987;641-656.
29. Muller W., Petrozzino J.J., Griffith L.C., Danho W., Connor J.A. Specific involvement of Ca(2+)-calmodulin kinase II in cholinergic modulation of neuronal responsiveness. J. Neurophysiol. 68:1992;2264-2269.
30. Navaratnam D.S., Priddle J.D., McDonald B., Esiri M.M., Robinson J.R., Smith A.D. Anomalous molecular form of acetylcholinesterase in cerebrospinal fluid in histologically diagnosed Alzheimer's disease. Lancet. 337:1991;447-450.
31. Neville L.F., Gnatt A., Loewenstein Y., Seidman S., Ehrlich G., Soreq H. Intramolecular relationships in cholinesterases revealed by oocyte expression of site-directed and natural variants of human BCHE. EMBO J. 11:1992;1641-1649.
32. Patriotis C., Makris A., Chernoff J., Tsichlis P.N. Tpl-2 acts in concert with Ras and Raf-1 to activate mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA. 91:1994;9755-9759.
33. Perry E.K., Tomlinson B.E., Blessed G., Bergman K., Gibson P.H., Perry R.H. Cholinergic correlates of cognitive impairment in Parkinson's disease: comparison with Alzheimer's disease. J. Neurol. Neurosurg. Psychiat. 48:1985;413-422.
34. Pieribone V.A., Shupliakov O., Brodin L., Hifiker-Rothenfluh S., Czernik A.J., Greengard P. Distinct pools of synaptic vesicles in neurotransmitter release. Nature (London). 375:1995;493-497.
35. Ripoll D.R., Faerman C.H., Axelsen P.H., Silman I., Sussman J.L. An electrostatic mechanism for substrate guidance down the aromatic gorge of acetylcholinesterase. Proc. Natl. Acad. Sci. USA. 90:1993;5128-5132.
36. Schmidt B.M., Rylett R.J. Phosphorylation of rat brain choline acetyltransferase and its relationship to enzyme activity. J. Neurochem. 61:1993;1774-1781.
37. Schwarz M., Glick D., Loewenstein Y., Soreq H. Engineering of human cholinesterases explains and predicts diverse consequences of administration of various drugs and poisons. Pharmacol. Ther. 67:1995;283-322.
38. Seibert F.S., Tabcharani J.A., Chang X.-B., Dulhanty A.M., Mathews C., Hanrahan J.W., Riordan J.R. cAMP-dependent protein kinase-mediated phosphorylation of cystic fibrosis transmembrane conductance regulator residue Ser-753 and its role in channel activation. J. Biol. Chem. 270:1995;2158-2162.
39. Seidman S., Sternfeld M., Ben Aziz-Aloya R., Timberg R., Kaufer D., Soreq H. Synaptic versus epidermal accumulation of human acetylcholinesterase is encoded by alternative 3′-terminal exons. Mol. Cell. Biol. 14:1995;459-473.
40. Shaltiel S., Schwartz I., Korc-Grodzicki B., Kreizman T. Evidence for an extra-cellular function for protein kinase A. Mol. Cell Biochem. 127:1993;283-291.
41. Small D.H., Reed G., Whitefield B., Nurcombe V. Cholinergic regulation of neurite outgrowth from isolated chick sympathetic neurons in culture. J. Neurosci. 15:1995;144-151.
42. Smith A.D., Jobst K.A., Navaratnam D.S., Shen Z.X., Priddle J.D., McDonalds B., King E., Esiri M.M. Anomalous acetylcholinesterase in lumbar CSF in Alzheimer's disease. Lancet. 338:1991;1538.
43. Soreq H., Miskin R., Zutra A., Littauer U.Z. Modulation in the levels and localization of plasminogen activator in differentiating neuroblastoma cells. Dev. Brain. Res. 7:1983;257-259.
44. H. Soreq, H. Zakut, Human Cholinesterases and Anticholinesterases, Academic Press, San Diego, CA, 1993, 300 pp.
45. Sussman J.L., Harel M., Frolow F., Oefner C., Goldman A., Toker L., Silman I. Atomic structure of acetylcholinesterase from Torpedo californica: a prototypic acetylcholine-binding protein. Science. 253:1991;872-879.
46. P. Taylor, Cholinergic agonists, anticholinesterase agents, in: A.G. Gilman, T.W. Rall, A.S. Nies, P. Taylor (Eds.), Pharmacological Basis of Therapeutics, Pergamon, New York, NY, 1990, pp. 122-130, 131-149.
47. Trojanowski J.Q., Lee V.M. Phosphorylation of paired helical tau filaments in Alzheimer's disease neurofibrillary lesions: focusing on phosphatases. FASEB J. 9:1995;1570-1576.
48. Velan B., Kronman C., Grosfeld H., Leitner M., Gozes Y., Flashner Y., Sery T., Cohen S., Ben-Aziz R., Seidman S., Shafferman A., Soreq H. Recombinant human acetylcholinesterase is secreted from transiently transfected 293 cells as a soluble globular enzyme. Cell. Mol. Neurobiol. 11:1991;143-156.
49. Velan B., Kronman C., Ordentlich A., Flashner Y., Leitner M., Cohen S., Shafferman A. N-Glycosylation of human acetylcholinesterase: effects on activity, stability and biosynthesis. Biochem. J. 296:1993;649-656.
50. Volonte C., Merlo D., Ciotti M.T., Calissano P. Identification of an ecto-kinase activity in cerebellar granule primary neuronal cultures. J. Neurochem. 63:1994;2028-2037.
51. Walsh D.A., Van Patten S.M. Multiple pathway signal transduction by the cAMP-dependent protein kinase. FASEB J. 8:1994;1227-1236.