Excessive hippocampal acetylcholine levels in acetylcholinesterase- deficient mice are moderated by butyrylcholinesterase activity

Journal of Neurochemistry

Volumn 100, Issue 5, 2007, Pages 1421-1429

  Hartmann, Joachim ^a   Kiewert, Cornelia ^a   Duysen, Ellen G ^b   Lockridge, Oksana ^b   Greig, Nigel H ^c   Klein, Jochen ^b,d  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c NATIONAL INSTITUTE ON AGING   (United States)

^d Texas Tech School of Pharmacy   (United States)

Author keywords

Alzheimer's disease; Bambuterol; BW284c51; Central cholinergic system; Dementia with Lewy bodies; Microdialysis

Indexed keywords

1,5 BIS(4 ALLYLDIMETHYLAMMONIUMPHENYL)PENTAN 3 ONE DIBROMIDE; ACETYLCHOLINE; ACETYLCHOLINESTERASE; BAMBUTEROL; BIS NORCYMSERINE; CHOLINESTERASE; CHOLINESTERASE INHIBITOR; TETRODOTOXIN; TOLSERINE; UNCLASSIFIED DRUG;

ACETYLCHOLINE RELEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HIPPOCAMPUS; IN VIVO STUDY; MALE; MICRODIALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

ACETYLCHOLINE; ACETYLCHOLINESTERASE; ANIMALS; BUTYRYLCHOLINESTERASE; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; NEURONS;

ANIMALIA; MUS;

EID: 33846981174     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04347.x     Document Type: Article

References (44)

1. Aarsland D., Mosimann U. P. and McKeith I. G. (2004) Role of cholinesterase inhibitors in Parkinson's disease and dementia with Lewy bodies. J. Geriatr. Psychiatry Neurol. 17, 164-171.
2. Adler M., Manley H. A., Purcell A. L., Deshpande S. S., Hamilton T. A., Kan R. K., Oyler G., Lockridge O., Duysen E. G. and Sheridan R. E. (2004) Reduced acetylcholine receptor density, morphological remodeling, and butyryl-cholinesterase activity can sustain muscle function in acetylcholinesterase knockout mice. Muscle Nerve 30, 317-327.
3. Arendt T., Bruckner M. K., Lange M. and Bigl V. (1992) Changes in acetylcholinesterase and butyrylcholinesterase in Alzheimer's disease resemble embryonic development - a study of molecular forms. Neurochem. Int. 21, 381-396.
4. Ballard C. G., Greig N. H., Guillozet-Bongaarts A. L., Enz A. and Darvesh S. (2005) Cholinesterases: roles in the brain during health and disease. Curr. Alzheimer Res. 2, 307-318.
5. Behra M., Cousin X., Bertrand C., Vonesch J. L., Biellmann D., Chatonnet A. and Strahle U. (2002) Acetylcholinesterase is required for neuronal and muscular development in the zebrafish embryo. Nat. Neurosci. 5, 111-118.
6. Bernard V., Brana C., Liste I., Lockridge O. and Bloch B. (2003) Dramatic depletion of cell surface m2 muscarinic receptor due to limited delivery from intracytoplasmic stores in neurons of acetylcholinesterase-deficient mice. Mol. Cell. Neurosci. 23, 121-133.
7. Chatonnet A. and Lockridge O. (1989) Comparison of butyrylcholinesterase and acetyl-cholinesterase. Biochem. J. 260, 625-634.
8. Collerton D. (1986) Cholinergic function and intellectual decline in Alzheimer's disease. Neuroscience 19, 1-28.
9. Darvesh S. and Hopkins D. A. (2003) Differential distribution of butyrylcholinesterase and acetylcholinesterase in the human thalamus. J. Comp. Neurol. 463, 25-43.
10. Darvesh S., Hopkins D. A. and Geula C. (2003) Neurobiology of butyrylcholinesterase. Nat. Rev. Neurosci. 4, 131-138.
11. Dutar P., Bassant M.-H., Senut M.-C. and Lamour Y. (1995) The septohippocampal pathway: structure and function of a central cholinergic system. Physiol. Rev. 75, 393-427.
12. Duysen E. G., Stribley J. A., Fry D. L., Hinrichs S. H. and Lockridge O. (2002) Rescue of the acetylcholinesterase knockout mouse by feeding a liquid diet; phenotype of the adult acetylcholinesterase deficient mouse. Brain Res. Dev. Brain Res. 137, 43-54.
13. Everitt B. J. and Robbins T. W. (1997) Central cholinergic systems and cognition. Annu. Rev. Psychol. 48, 649-684.
14. 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. Psychiatry 66, 137-147.
15. Gauthier S. (2002) Advances in the pharmacotherapy of Alzheimer's disease. CMAJ 166, 616-623.
16. Gauthier S., Emre M., Farlow M. R., Bullock R., Grossberg G. T. and Potkin S. G. (2003) Strategies for continued successful treatment of Alzheimer's disease: switching cholinesterase inhibitors. Curr. Med. Res. Opin. 19, 707-714.
17. Giacobini E. (2003) Cholinesterases: new roles in brain function and in Alzheimer's disease. Neurochem. Res. 28, 515-522.
18. Giacobini E. (2004) Cholinesterase inhibitors: new roles and therapeutic alternatives. Pharmacol. Res. 50, 433-440.
19. Gold P. E. (2003) Acetylcholine: cognitive and brain functions. Neurobiol. Learn. Mem. 80, 194-210.
20. Greenspan R. J., Finn J. A. Jr and Hall J. C. (1980) Acetylcholinesterase mutants in Drosophila and their effects on the structure and function of the central nervous system. J. Comp. Neurol. 189, 741-774.
21. Greig N. H., Utsuki T., Ingram D. K., et al. (2005) Selective butyrylcholinesterase inhibition elevates brain acetylcholine, augments learning and lowers Alzheimer beta-amyloid peptide in rodent. Proc. Natl Acad. Sci. USA 102, 17 213-17 218.
22. Hartmann J., Erb C., Ebert U., Baumann K. H., Popp A., König G. and Klein J. (2004) Central cholinergic functions in human amyloid precursor protein knock-in/presenilin-1 transgenic mice. Neuroscience 125, 1009-1017.
23. Haubrich D. R. and Chippendale T. J. (1977) Regulation of acetylcholine synthesis in nervous tissue. Life Sci. 20, 1465-1478.
24. Hoistad M., Chen K. C., Nicholson C., Fuxe K. and Kehr J. (2002) Quantitative dual-probe microdialysis: evaluation of [3H]mannitol diffusion in agar and rat striatum. J. Neurochem. 81, 80-93.
25. Jones S. R., Gainetdinov R. R., Jaber M., Giros B., Wightman R. M. and Caron M. G. (1998) Profound neuronal plasticity in response to inactivation of the dopamine transporter. Proc. Natl Acad. Sci. USA 95, 4029-4034.
26. Karczmar A. G. (1993) Brief presentation of the story and present status of studies of the vertebrate cholinergic system. Neuropsychopharmacology 9, 181-199.
27. Karczmar A. G. (1998) Anticholinesterases: dramatic aspects of their use and misuse. Neurochem. Int. 32, 401-411.
28. Kiewert C., Buchholzer M. L., Hartmann J., Chatterjee S. S. and Klein J. (2004) Stimulation of hippocampal acetylcholine release by hyperforin, a constituent of St John's Wort. Neurosci. Lett. 364, 195-198.
29. Kovarik Z., Radic Z., Grgas B., Skrinjaric-Spoljar M., Reiner E. and Simeon-Rudolf V. (1999) Amino acid residues involved in the interaction of acetylcholinesterase and butyrylcholinesterase with the carbamates Ro 02-0683 and bambuterol, and with terbutaline. Biochim. Biophys. Acta 1433, 261-271.
30. Li B., Stribley J. A., Ticu A., Xie W., Schopfer L. M., Hammond P., Brimijoin S., Hinrichs S. H. and Lockridge O. (2000) Abundant tissue butyrylcholinesterase and its possible function in the acetylcholinesterase knockout mouse. J. Neurochem. 75, 1320-1331.
31. Li B., Duysen E. G., Volpicelli-Daley L. A., Levey A. I. and Lockridge O. (2003) Regulation of muscarinic acetylcholine receptor function in acetylcholinesterase knockout mice. Pharmacol. Biochem. Behav. 74, 977-986.
32. McKeith I. G., Mintzer J., Aarsland A., et al. (2004) International Psychogeriatric Association Expert Meeting on DLB. Dementia with Lewy bodies. Lancet Neurol. 3, 19-28.
33. Mesulam M. M., Guillozet A., Shaw P., Levey A., Duysen E. G. and Lockridge O. (2002) Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyze acetylcholine. Neuroscience 110, 627-639.
34. Perry E. K., Perry R. H., Blessed G. and Tomlinson B. E. (1978) Changes in brain cholinesterases in senile dementia of Alzheimer type. Neuropathol. Appl. Neurobiol. 4, 273-277.
35. Samuel W., Alford M., Hofstetter C. R. and Hansen L. (1997) Dementia with Lewy bodies versus pure Alzheimer disease: differences in cognition, neuropathology, cholinergic dysfunction, and synapse density. J. Neuropathol. Exp. Neurol. 56, 499-508.
36. Silman I. and Sussman J. L. (2005) Acetylcholinesterase: "classical" and "non-classical" functions and pharmacology. Curr. Opin. Pharmacol. 5, 293-302.
37. Soreq H. and Seidman S. (2001) Acetylcholinesterase - new roles for an old actor. Nat. Rev. Neurosci. 2, 294-302.
38. Tasker A., Perry E. K. and Ballard C. G. (2005) Butyrylcholinesterase: impact on symptoms and progression of cognitive impairment. Expert Rev. Neurother. 5, 101-106.
39. Tiraboschi P., Hansen L., Alford M., Merdes A., Masliah E., Thal L. J. and Corey-Bloom J. (2002) Early and widespread cholinergic losses differentiate dementia with Lewy bodies from Alzheimer disease. Arch. Gen. Psychiatry 59, 946-951.
40. Volpicelli-Daley L. A., Duysen E. G., Lockridge O. and Levey A. I. (2003) Altered hippocampal muscarinic receptors in acetylcholinesterase-deficient mice. Ann. Neurol. 53, 788-796.
41. Westerink B. H. and DeVries J. B. (2001) A method to evaluate the diffusion rate of drugs from a microdialysis probe through brain tissue. J. Neurosci. Methods 109, 53-58.
42. Xie W., Stribley J. A., Chatonnet A., Wilder P. J., Rizzino A., McComb R. D., Taylor P., Hinrichs S. H. and Lockridge O. (2000) Postnatal developmental delay and supersensitivity to organophosphate in gene-targeted mice lacking acetylcholinesterase. J. Pharmacol. Exp. Ther. 293, 896-902.
43. Yu Q.-S., Holloway H. W., Utsuki T., Brossi A. and Greig N. H. (1999) Synthesis of novel phenserine-based-selective inhibitors of butyrylcholinesterase for Alzheimer's disease. J. Med. Chem. 42, 1855-1861.
44. Zhang W., Basile A. S., Gomeza J., Volpicelli L. A., Levey A. I. and Wess J. (2002) Characterization of central inhibitory muscarinic autoreceptors by the use of muscarinic acetylcholine receptor knock-out mice. J. Neurosci. 22, 1709-1717.