Inhibition of acetylcholinesterase in CSF versus brain assessed by 11C-PMP PET in AD patients treated with galantamine

Neurobiology of Aging

Volumn 29, Issue 2, 2008, Pages 168-184

  Darreh Shori, T ^a   Kadir, A ^a   Almkvist, O ^a   Grut, M ^b   Wall, A ^c   Blomquist, G ^c   Eriksson, B ^d   Langstrom B ^c   Nordberg, A ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b DANDERYD HOSPITAL   (Sweden)

^c UPPSALA UNIVERSITY   (Sweden)

^d Janssen Cilag   (Sweden)

Author keywords

Acetylcholinesterase; Alzheimer's disease; Cerebrospinal fluid (CSF); Galantamine; Positron emission tomography (PET); Red blood cells (RBC)

Indexed keywords

ACETYLCHOLINESTERASE; CHOLINESTERASE INHIBITOR; GALANTAMINE; METHYLPIPERIDIN 4 YL PROPIONATE C 11; PIPERIDINE DERIVATIVE; PLACEBO; PROPIONIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; ATTENTION; BRAIN REGION; CEREBROSPINAL FLUID; CLINICAL ARTICLE; CLINICAL TRIAL; COGNITION; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CORRELATION ANALYSIS; DEPTH PERCEPTION; DIARRHEA; DOUBLE BLIND PROCEDURE; DRUG DOSE REDUCTION; ENZYME ACTIVITY; ENZYME INHIBITION; EPISODIC MEMORY; ERYTHROCYTE; FEMALE; HUMAN; IN VIVO STUDY; MALE; MENTAL PERFORMANCE; NAUSEA; NEUROIMAGING; NEUROPSYCHOLOGY; OUTCOME ASSESSMENT; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SYNAPSE; TREATMENT DURATION; TREATMENT OUTCOME; VOMITING;

ACETYLCHOLINESTERASE; AGED; ALZHEIMER DISEASE; BRAIN; BUTYRYLCHOLINESTERASE; CHOLINESTERASE INHIBITORS; DOUBLE-BLIND METHOD; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GALANTAMINE; HUMANS; IMMUNOPRECIPITATION; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; PHENYLCARBAMATES; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS;

EID: 37549048238     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2006.09.020     Document Type: Article

References (75)

1. Almkvist O., Darreh-Shori T., Stefanova E., Spiegel R., and Nordberg A. Preserved cognitive function after 12 months of treatment with rivastigmine in mild Alzheimer's disease in comparison with untreated AD and MCI patients. Eur. J. Neurol. 11 4 (2004) 253-261
2. Backman L., and Forsell Y. Episodic memory functioning in a community-based sample of old adults with major depression: utilization of cognitive support. J. Abnorm. Psychol. 103 2 (1994) 361-370
3. Birikh K.R., Sklan E.H., Shoham S., and Soreq H. Interaction of "readthrough" acetylcholinesterase with RACK1 and PKCbeta II correlates with intensified fear-induced conflict behavior. Proc. Natl. Acad. Sci. U.S.A. 100 1 (2003) 283-288
4. Birks J. Cholinesterase inhibitors for Alzheimer's disease. Cochrane Database Syst. Rev. 1 (2006) 10.1002/14651858.CD005593
5. Blalock E.M., Geddes J.W., Chen K.C., Porter N.M., Markesbery W.R., and Landfield P.W. Incipient Alzheimer's disease: microarray correlation analyses reveal major transcriptional and tumor suppressor responses. Proc. Natl. Acad. Sci. U.S.A. 101 7 (2004) 2173-2178
6. Bohnen N.I., Kaufer D.I., Hendrickson R., Ivanco L.S., Lopresti B.J., Koeppe R.A., Meltzer C.C., Constantine G., Davis J.G., Mathis C.A., Dekosky S.T., and Moore R.Y. Degree of inhibition of cortical acetylcholinesterase activity and cognitive effects by donepezil treatment in Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 76 3 (2005) 315-319
7. Botti S.A., Felder C.E., Sussman J.L., and Silman I. Electrotactins: a class of adhesion proteins with conserved electrostatic and structural motifs. Protein Eng. 11 6 (1998) 415-420
8. Brimijoin S., and Hammond P. Butyrylcholinesterase in human brain and acetylcholinesterase in human plasma: trace enzymes measured by two-site immunoassay. J. Neurochem. 51 4 (1988) 1227-1231
9. Cabeza R., Anderson N.D., Houle S., Mangels J.A., and Nyberg L. Age-related differences in neural activity during item and temporal-order memory retrieval: a positron emission tomography study. J. Cogn. Neurosci. 12 1 (2000) 197-206
10. Cahn-Weiner D.A., Sullivan E.V., Shear P.K., Fama R., Lim K.O., Yesavage J.A., Tinklenberg J.R., and Pfefferbaum A. Brain structural and cognitive correlates of clock drawing performance in Alzheimer's disease. J. Int. Neuropsychol. Soc. 5 6 (1999) 502-509
11. Chubb I.W., Goodman S., and Smith A.D. Is acetylcholinesterase secreted from central neurons into the cerebral fluid?. Neuroscience 1 1 (1976) 57-62
12. Cohen O., Reichenberg A., Perry C., Ginzberg D., Pollmacher T., Soreq H., and Yirmiya R. Endotoxin-induced changes in human working and declarative memory associate with cleavage of plasma "readthrough" acetylcholinesterase. J. Mol. Neurosci. 21 3 (2003) 199-212
13. Cummings J.L. Frontal-subcortical circuits and human behavior. Arch. Neurol. 50 8 (1993) 873-880
14. Darreh-Shori, T., Molecular changes of acetylcholinesterase and butyrylcholinesterase in alzheimer patients during the natural course of the disease and treatment with cholinesterase inhibitors-insight into neurochemical mechanisms affecting the progression of the disease. Thesis for doctoral degree (Ph.D.). Stockholm, 2006, p. 120.
15. Darreh-Shori T., Almkvist O., Guan Z.Z., Garlind A., Strandberg B., Svensson A.L., Soreq H., Hellstrom-Lindahl E., and Nordberg A. Sustained cholinesterase inhibition in AD patients receiving rivastigmine for 12 months. Neurology 59 4 (2002) 563-572
16. Darreh-Shori T., Hellstrom-Lindahl E., Flores-Flores C., Guan Z.Z., Soreq H., and Nordberg A. Long-lasting acetylcholinesterase splice variations in anticholinesterase-treated Alzheimer's disease patients. J. Neurochem. 88 5 (2004) 1102-1113
17. Darreh-Shori T., Meurling L., Pettersson T., Hugosson K., Hellstrom-Lindahl E., Andreasen N., Minthon L., and Nordberg A. Changes in the activity and protein levels of CSF acetylcholinesterases in relation to cognitive function of patients with mild Alzheimer's disease following chronic donepezil treatment. J. Neural. Transm. 113 11 (2006) 1791-1801
18. Darreh-Shori T., Brimijoin S., Kadir A., Almkvist O., and Nordberg A. Differential CSF butyrylcholinesterase levels in Alzheimer's disease patients with the ApoE ε4 allele, in relation to cognitive function and cerebral glucose metabolism. Neurobiol. Dis. 24 2 (2006) 326-333
19. Davidsson P., Blennow K., Andreasen N., Eriksson B., Minthon L., and Hesse C. Differential increase in cerebrospinal fluid-acetylcholinesterase after treatment with acetylcholinesterase inhibitors in patients with Alzheimer's disease. Neurosci. Lett. 300 3 (2001) 157-160
20. Davies P., and Maloney A.J. Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 2 8000 (1976) 1403
21. Day T., and Greenfield S.A. Bioactivity of a peptide derived from acetylcholinesterase in hippocampal organotypic cultures. Exp. Brain Res. 155 4 (2004) 500-508
22. Deutsch V., Pick M., Perry C., Grisaru D., Hemo Y., Golan-Hadari D., Grant A., Eldor A., and Soreq H. The stress-associated acetylcholinesterase variant AChE-R is expressed in human CD34(+) hematopoietic progenitors and its C-terminal peptide ARP promotes their proliferation. Exp. Hematol. 30 10 (2002) 1153
23. Doody R.S., Geldmacher D.S., Gordon B., Perdomo C.A., and Pratt R.D. Open-label, multicenter, phase 3 extension study of the safety and efficacy of donepezil in patients with Alzheimer disease. Arch. Neurol. 58 3 (2001) 427-433
24. Dori A., Cohen J., Silverman W.F., Pollack Y., and Soreq H. Functional manipulations of acetylcholinesterase splice variants highlight alternative splicing contributions to murine neocortical development. Cereb. Cortex 15 4 (2005) 419-430
25. Dori A., and Soreq H. ARP, the cleavable C-terminal peptide of "readthrough" acetylcholinesterase, promotes neuronal development and plasticity. J. Mol. Neurosci. 28 3 (2006) 247-255
26. Ellman G.L., Courtney K.D., Andres Jr. V., and Featherstone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7 (1961) 88-95
27. Fambrough D.M., Engel A.G., and Rosenberry T.L. Acetylcholinesterase of human erythrocytes and neuromuscular junctions: homologies revealed by monoclonal antibodies. Proc. Natl. Acad. Sci. U.S.A. 79 4 (1982) 1078-1082
28. Farlow M., Anand R., Messina Jr. J., Hartman R., and Veach J. A 52-week Study of the Efficacy of Rivastigmine in Patients with Mild to Moderately Severe Alzheimer's Disease. Eur. Neurol. 44 4 (2000) 236-241
29. Folstein M.F., Folstein S.E., and McHugh P.R. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J. Psychiat. Res. 12 3 (1975) 189-198
30. Fukuyama R., Izumoto T., and Fushiki S. The cerebrospinal fluid level of glial fibrillary acidic protein is increased in cerebrospinal fluid from Alzheimer's disease patients and correlates with severity of dementia. Eur. Neurol. 46 1 (2001) 35-38
31. Giacobini E. Cholinesterases: new roles in brain function and in Alzheimer's disease. Neurochem. Res. 28 3-4 (2003) 515-522
32. Giacobini E. From molecular structure to Alzheimer therapy. Jpn. J. Pharmacol. 74 3 (1997) 225-241
33. Giacobini E., Spiegel R., Enz A., Veroff A.E., and Cutler N.R. Inhibition of acetyl- and butyryl-cholinesterase in the cerebrospinal fluid of patients with Alzheimer's disease by rivastigmine: correlation with cognitive benefit. J. Neural. Transm. 109 7-8 (2002) 1053-1065
34. Giacobini E., Zhu X.D., Williams E., and Sherman K.A. The effect of the selective reversible acetylcholinesterase inhibitor E2020 on extracellular acetylcholine and biogenic amine levels in rat cortex. Neuropharmacology 35 2 (1996) 205-211
35. Greenfield S. A peptide derived from acetylcholinesterase is a pivotal signalling molecule in neurodegeneration. Chem. Biol. Interact. 157-158 (2005) 211-218
36. Greenfield S.A., Day T., Mann E.O., and Bermudez I. A novel peptide modulates alpha7 nicotinic receptor responses: implications for a possible trophic-toxic mechanism within the brain. J. Neurochem. 90 2 (2004) 325-331
37. Grisaru D., Deutsch V., Shapira M., Pick M., Sternfeld M., Melamed-Book N., Kaufer D., Galyam N., Gait M.J., Owen D., Lessing J.B., Eldor A., and Soreq H. ARP, a peptide derived from the stress-associated acetylcholinesterase variant, has hematopoietic growth promoting activities. Mol. Med. 7 2 (2001) 93-105
38. Grisaru D., Pick M., Perry C., Sklan E.H., Almog R., Goldberg I., Naparstek E., Lessing J.B., Soreq H., and Deutsch V. Hydrolytic and nonenzymatic functions of acetylcholinesterase comodulate hemopoietic stress responses. J. Immunol. 176 1 (2006) 27-35
39. Hashimoto M., Kazui H., Matsumoto K., Nakano Y., Yasuda M., and Mori E. Does donepezil treatment slow the progression of hippocampal atrophy in patients with Alzheimer's disease?. Am. J. Psychiatry 162 4 (2005) 676-682
40. Kadir, A., Darreh-Shori, T., Almkvist, O., Wall, A., Grut, M., Strandberg, B., Ringheim, A., Eriksson, B., Blomquist, G., Långström, B., Nordberg, A., 2007. PET imaging of the in vivo brain acetylcholinesterase activity and nicotine binding in galantamine-treated patients with AD, Neurobiol Aging, doi:10.1016/j.neurobiolaging.2007.02.020.
41. Kaufer D., Friedman A., Seidman S., and Soreq H. Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature 393 6683 (1998) 373-377
42. Kaufer D., Friedman A., Seidman S., and Soreq H. Anticholinesterases induce multigenic transcriptional feedback response suppressing cholinergic neurotransmission. Chem. Biol. Interact. 119-120 (1999) 349-360
43. Koeppe R.A., Frey K.A., Snyder S.E., Meyer P., Kilbourn M.R., and Kuhl D.E. Kinetic modeling of N-[11C]methylpiperidin-4-yl propionate: alternatives for analysis of an irreversible positron emission tomography trace for measurement of acetylcholinesterase activity in human brain. J. Cereb. Blood Flow Metab. 19 10 (1999) 1150-1163
44. Kuhl D.E., Minoshima S., Frey K.A., Foster N.L., Kilbourn M.R., and Koeppe R.A. Limited donepezil inhibition of acetylcholinesterase measured with positron emission tomography in living Alzheimer cerebral cortex. Ann. Neurol. 48 3 (2000) 391-395
45. Lezak M. Neuropsychological Assessment. third ed. (1995), Oxford University Press, New York
46. Liao J., Norgaard-Pedersen B., and Brodbeck U. Subunit association and glycosylation of acetylcholinesterase from monkey brain. J. Neurochem. 61 3 (1993) 1127-1134
47. Lockridge O., and La Du B.N. Comparison of atypical and usual human serum cholinesterase. Purification, number of active sites, substrate affinity, and turnover number. J. Biol. Chem. 253 2 (1978) 361-366
48. Luria A.R. Higher Cortical Functions in Man (1966), Basic Books, New York
49. Maelicke A. Allosteric modulation of nicotinic receptors as a treatment strategy for Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 11 Suppl. 1 (2000) 11-18
50. Massoulie J., Anselmet A., Bon S., Krejci E., Legay C., Morel N., and Simon S. The polymorphism of acetylcholinesterase: post-translational processing, quaternary associations and localization. Chem. Biol. Interact. 119-120 (1999) 29-42
51. Massoulie J., Bon S., Perrier N., and Falasca C. The C-terminal peptides of acetylcholinesterase: cellular trafficking, oligomerization and functional anchoring. Chem. Biol. Interact. 157-158 (2005) 3-14
52. McKhann G., Drachman D., Folstein M., Katzman R., Price D., and Stadlan E.M. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34 7 (1984) 939-944
53. Meshorer E., and Soreq H. Virtues and woes of AChE alternative splicing in stress-related neuropathologies. Trends Neurosci. 29 4 (2006) 216-224
54. Mesulam M.M., Geula C., Cosgrove R., Mash D., and Brimijoin S. Immunocytochemical demonstration of axonal and perikaryal acetylcholinesterase in human cerebral cortex. Brain Res. 539 2 (1991) 233-238
55. Metz C.N., and Tracey K.J. It takes nerve to dampen inflammation. Nat. Immunol. 6 8 (2005) 756-757
56. Mori E., Hashimoto M., Krishnan K.R., and Doraiswamy P.M. What constitutes clinical evidence for neuroprotection in Alzheimer disease: support for the cholinesterase inhibitors?. Alzheimer Dis. Assoc. Disord. 20 2 Suppl. 1 (2006) S19-S26
57. Nitsch R.M., Rossner S., Albrecht C., Mayhaus M., Enderich J., Schliebs R., Wegner M., Arendt T., and von der Kammer H. Muscarinic acetylcholine receptors activate the acetylcholinesterase gene promoter. J. Physiol. Paris 92 3-4 (1998) 257-264
58. Nordberg A., Hellström-Lindahl E., Almkvist O., and Meurling L. Activity of acetylcholinesterase in CSF increases in Alzheimer's patients after treatment with tacrine. Alzheimer's Rep. 2 6 (1999) 347-352
59. O'Brien K.K., Saxby B.K., Ballard C.G., Grace J., Harrington F., Ford G.A., O'Brien J.T., Swan A.G., Fairbairn A.F., Wesnes K., del Ser T., Edwardson J.A., Morris C.M., and McKeith I.G. Regulation of attention and response to therapy in dementia by butyrylcholinesterase. Pharmacogenetics 13 4 (2003) 231-239
60. Pavlov V.A., Ochani M., Gallowitsch-Puerta M., Ochani K., Huston J.M., Czura C.J., Al-Abed Y., and Tracey K.J. Central muscarinic cholinergic regulation of the systemic inflammatory response during endotoxemia. Proc. Natl. Acad. Sci. U.S.A. 103 13 (2006) 5219-5223
61. Perrier A.L., Massoulie J., and Krejci E. PRiMA: the membrane anchor of acetylcholinesterase in the brain. Neuron 33 2 (2002) 275-285
62. Perrier N.A., Salani M., Falasca C., Bon S., Augusti-Tocco G., and Massoulie J. The readthrough variant of acetylcholinesterase remains very minor after heat shock, organophosphate inhibition and stress, in cell culture and in vivo. J. Neurochem. 94 3 (2005) 629-638
63. Pick M., Perry C., Lapidot T., Guimaraes-Sternberg C., Naparstek E., Deutsch V., and Soreq H. Stress-induced cholinergic signaling promotes inflammation-associated thrombopoiesis. Blood 107 8 (2006) 3397-3406
64. Rakonczay Z., and Brimijoin S. Monoclonal antibodies to human brain acetylcholinesterase: properties and applications. Cell Mol. Neurobiol. 8 1 (1988) 85-93
65. Raskind M.A., Peskind E.R., Wessel T., and Yuan W. Galantamine in AD: a 6-month randomized, placebo-controlled trial with a 6-month extension. The Galantamine USA-1 Study Group. Neurology 54 12 (2000) 2261-2268
66. Rosen W.G., Mohs R.C., and Davis K.L. A new rating scale for Alzheimer's disease. Am. J. Psychiatry 141 11 (1984) 1356-1364
67. Rossor M.N. Focal changes in Alzheimer's disease and cholinergic hypothesis. Lancet 2 8347 (1983) 465
68. Saas P., Boucraut J., Quiquerez A.L., Schnuriger V., Perrin G., Desplat-Jego S., Bernard D., Walker P.R., and Dietrich P.Y. CD95 (Fas/Apo-1) as a receptor governing astrocyte apoptotic or inflammatory responses: a key role in brain inflammation?. J. Immunol. 162 4 (1999) 2326-2333 (frame.html)
69. Saeed R.W., Varma S., Peng-Nemeroff T., Sherry B., Balakhaneh D., Huston J., Tracey K.J., Al-Abed Y., and Metz C.N. Cholinergic stimulation blocks endothelial cell activation and leukocyte recruitment during inflammation. J. Exp. Med. 201 7 (2005) 1113-1123
70. Shapira M., Tur-Kaspa I., Bosgraaf L., Livni N., Grant A.D., Grisaru D., Korner M., Ebstein R.P., and Soreq H. A transcription-activating polymorphism in the ACHE promoter associated with acute sensitivity to anti-acetylcholinesterases. Hum. Mol. Genet. 9 9 (2000) 1273-1281
71. Sternfeld M., Shoham S., Klein O., Flores-Flores C., Evron T., Idelson G.H., Kitsberg D., Patrick J.W., and Soreq H. Excess "read-through" acetylcholinesterase attenuates but the "synaptic" variant intensifies neurodeterioration correlates. Proc. Natl. Acad. Sci. U.S.A. 97 15 (2000) 8647-8652
72. Wang H., Yu M., Ochani M., Amella C.A., Tanovic M., Susarla S., Li J.H., Yang H., Ulloa L., Al-Abed Y., Czura C.J., and Tracey K.J. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421 6921 (2003) 384-388
73. Wechsler D. Wechsler Adult Intelligence Scale-Revised. Manual (1981), Psychological Corporation
74. Woodruff-Pak D.S., Lander C., and Geerts H. Nicotinic cholinergic modulation: galantamine as a prototype. CNS Drug Rev. 8 4 (2002) 405-426
75. Zahler R., Sun W., Ardito T., Zhang Z.T., Kocsis J.D., and Kashgarian M. The alpha3 isoform protein of the Na+, K(+)-ATPase is associated with the sites of cardiac and neuromuscular impulse transmission. Circ. Res. 78 5 (1996) 870-879