Acetylcholinesterase — new roles for an old actor (original) (raw)
Dale, H. The action of certain esters and ethers of choline, and their relation to muscarine . J. Pharmacol. Exp. Therap.6, 147– 190 (1914). CAS Google Scholar
Loewi, O. & Navratil, E. Uber humorale Ubertragbarkeit der Herznervenwirkung. X Mitteilung. Pfluger's Arch.214 , 678–688 (1926). ArticleCAS Google Scholar
Wright, C. I., Geula, C. & Mesulam, M. M. Neurological cholinesterases in the normal brain and in Alzheimer's disease: relationship to plaques, tangles, and patterns of selective vulnerability. Ann. Neurol.34, 373–384 (1993). ArticleCASPubMed Google Scholar
Polinsky, R. J., Holmes, K. V., Brown, R. T. & Weise, V. CSF acetylcholinesterase levels are reduced in multiple system atrophy with autonomic failure. Neurology39, 40– 44 (1989). ArticleCASPubMed Google Scholar
Ohno, K. et al. The spectrum of mutations causing end-plate acetylcholinesterase deficiency. Ann. Neurol.47, 162– 170 (2000). ArticleCASPubMed Google Scholar
Silver, A. A histochemical investigation of cholinesterases at neuromuscular junctions in mammalian and avian muscle. J. Physiol. (Lond.)169, 386–393 (1963). ArticleCAS Google Scholar
Augustinsson, K. B. & Nachmansohn, D. Distinction between acetylcholinesterase and other choline ester-splitting enzymes. Science110, 98–99 ( 1949). ArticleCASPubMed Google Scholar
Li, B. et al. Abundant tissue butyrylcholinesterase and its possible function in the acetylcholinesterase knockout mouse. J. Neurochem.75, 1320–1331 (2000). ArticleCASPubMed Google Scholar
Sussman, J. L. et al. Atomic structure of acetylcholinesterase from Torpedo californica : a prototypic acetylcholine-binding protein. Science253, 872–879 (1991). ArticleCASPubMed Google Scholar
Bourne, Y., Taylor, P. & Marchot, P. Acetylcholinesterase inhibition by fasciculin: crystal structure of the complex. Cell83, 503– 512 (1995). ArticleCASPubMed Google Scholar
Harel, M. et al. Three-dimensional structures of Drosophila melanogaster acetylcholinesterase and of its complexes with two potent inhibitors. Protein Sci.9, 1063–1072 (2000). ArticleCASPubMedPubMed Central Google Scholar
Kryger, G. et al. Structures of recombinant native and E202Q mutant human acetylcholinesterase complexed with the snake-venom toxin fasciculin-II. Acta Crystallogr. D Biol. Crystallogr.56, 1385–1394 (2000). ArticleCASPubMed Google Scholar
Shafferman, A. et al. Mutagenesis of human acetylcholinesterase. Identification of residues involved in catalytic activity and in polypeptide folding. J. Biol. Chem.267, 17640–17648 (1992). ArticleCASPubMed Google Scholar
Nair, H. K., Seravalli, J., Arbuckle, T. & Quinn, D. M. Molecular recognition in acetylcholinesterase catalysis: free-energy correlations for substrate turnover and inhibition by trifluoro ketone transition-state analogs. Biochemistry33, 8566– 8576 (1994). ArticleCASPubMed Google Scholar
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. USA90, 5128– 5132 (1993). ArticleCASPubMedPubMed Central Google Scholar
Shafferman, A. et al. Electrostatic attraction by surface charge does not contribute to the catalytic efficiency of acetylcholinesterase. EMBO J.13, 3448–3455 (1994). ArticleCASPubMedPubMed Central Google Scholar
Radic, Z., Kirchhoff, P. D., Quinn, D. M., McCammon, J. A. & Taylor, P. Electrostatic influence on the kinetics of ligand binding to acetylcholinesterase. Distinctions between active center ligands and fasciculin. J. Biol. Chem.272, 23265–23277 (1997). ArticleCASPubMed Google Scholar
Taylor, P., Luo, Z. D. & Camp, S. in Cholinesterases and Cholinesterase Inhibitors (ed. Giacobini, E.) 63–79 (Martin Dunitz, London, 2000). Google Scholar
Botti, S. A., Felder, C. E., Sussman, J. L. & Silman, I. Electrotactins: a class of adhesion proteins with conserved electrostatic and structural motifs. Protein Eng.11, 415–420 (1998). ArticleCASPubMed Google Scholar
Luo, Z. D., Camp, S., Mutero, A. & Taylor, P. Splicing of 5′ introns dictates alternative splice selection of acetylcholinesterase pre-mRNA and specific expression during myogenesis. J. Biol. Chem.273, 28486–28495 (1998). ArticleCASPubMed Google Scholar
Atanasova, E., Chiappa, S., Wieben, E. & Brimijoin, S. Novel messenger RNA and alternative promoter for murine acetylcholinesterase. J. Biol. Chem.274, 21078–21084 (1999). ArticleCASPubMed Google Scholar
Li, Y., Camp, S., Rachinsky, T. L., Getman, D. & Taylor, P. Gene structure of mammalian acetylcholinesterase. Alternative exons dictate tissue-specific expression. J. Biol. Chem.266, 23083–23090 ( 1991). ArticleCASPubMed Google Scholar
Bon, S., Coussen, F. & Massoulie, J. Quaternary associations of acetylcholinesterase. II. The polyproline attachment domain of the collagen tail. J. Biol. Chem.272, 3016–3021 ( 1997). ArticleCASPubMed Google Scholar
Donger, C. et al. Mutation in the human acetylcholinesterase-associated collagen gene, COLQ, is responsible for congenital myasthenic syndrome with end-plate acetylcholinesterase deficiency (Type Ic). Am. J. Hum. Genet.63, 967–975 (1998). ArticleCASPubMedPubMed Central Google Scholar
Futerman, A. H., Low, M. G., Ackermann, K. E., Sherman, W. R. & Silman, I. Identification of covalently bound inositol in the hydrophobic membrane-anchoring domain of Torpedo acetylcholinesterase . Biochem. Biophys. Res. Commun.129, 312 –317 (1985). ArticleCASPubMed Google Scholar
Massoulie, J. et al. The polymorphism of acetylcholinesterase: post-translational processing, quaternary associations and localization. Chem. Biol. Interact119–120, 29–42 (1999). ArticlePubMed Google Scholar
Fitzpatrick-McElligott, S. & Stent, G. S. Appearance and localization of acetylcholinesterase in embryos of the leech Helobdella triserialis. J. Neurosci.1, 901– 907 (1981). ArticleCASPubMedPubMed Central Google Scholar
Betz, H., Bourgeois, J. P. & Changeux, J. P. Evolution of cholinergic proteins in developing slow and fast skeletal muscles in chick embryo. J. Physiol.302, 197–218 (1980). ArticleCASPubMedPubMed Central Google Scholar
Layer, P. G. Cholinesterases preceding major tracts in vertebrate neurogenesis. Bioessays12, 415–420 ( 1990). ArticleCASPubMed Google Scholar
Kreutzberg, G. W. Neuronal dynamics and axonal flow. IV. Blockage of intra-axonal enzyme transport by colchicine. Proc. Natl Acad. Sci. USA62, 722–728 (1969). ArticleCASPubMedPubMed Central Google Scholar
Appleyard, M. E. Secreted acetylcholinesterase: non-classical aspects of a classical enzyme . Trends Neurosci.15, 485– 490 (1992). ArticleCASPubMed Google Scholar
Small, D. H. Non-cholinergic actions of acetylcholinesterases: proteases regulating cell growth and development? Trends Biochem. Sci.15, 213–216 (1990). ArticleCASPubMed Google Scholar
Checler, F., Grassi, J. & Vincent, J. P. Cholinesterases display genuine arylacylamidase activity but are totally devoid of intrinsic peptidase activities. J. Neurochem.62, 756–763 ( 1994). ArticleCASPubMed Google Scholar
Layer, P. G., Weikert, T. & Alber, R. Cholinesterases regulate neurite growth of chick nerve cells in vitro by means of a non-enzymatic mechanism. Cell Tissue Res.273, 219–226 (1993). ArticleCASPubMed Google Scholar
Small, D. H., Reed, G., Whitefield, B. & Nurcombe, V. Cholinergic regulation of neurite outgrowth from isolated chick sympathetic neurons in culture. J. Neurosci.15, 144–151 (1995). ArticleCASPubMedPubMed Central Google Scholar
Koenigsberger, C., Chiappa, S. & Brimijoin, S. Neurite differentiation is modulated in neuroblastoma cells engineered for altered acetylcholinesterase expression. J. Neurochem.69, 1389–1397 (1997). ArticleCASPubMed Google Scholar
Grifman, M., Galyam, N., Seidman, S. & Soreq, H. Functional redundancy of acetylcholinesterase and neuroligin in mammalian neuritogenesis. Proc. Natl Acad. Sci. USA95, 13935– 13940 (1998). ArticleCASPubMedPubMed Central Google Scholar
Bigbee, J. W., Sharma, K. V., Chan, E. L. & Bogler, O. Evidence for the direct role of acetylcholinesterase in neurite outgrowth in primary dorsal root ganglion neurons. Brain Res.861, 354–362 (2000). ArticleCASPubMed Google Scholar
de la Escalera, S., Bockamp, E. O., Moya, F., Piovant, M. & Jimenez, F. Characterization and gene cloning of neurotactin, a Drosophila transmembrane protein related to cholinesterases. EMBO J.9, 3593–3601 ( 1990). ArticleCASPubMedPubMed Central Google Scholar
Darboux, I., Barthalay, Y., Piovant, M. & Hipeau Jacquotte, R. The structure–function relationships in Drosophila neurotactin show that cholinesterasic domains may have adhesive properties. EMBO J.15, 4835–4843 ( 1996). ArticleCASPubMedPubMed Central Google Scholar
Sternfeld, M. et al. Acetylcholinesterase enhances neurite growth and synapse development through alternative contributions of its hydrolytic capacity, core protein, and variable C termini. J. Neurosci.18, 1240–1249 (1998). ArticleCASPubMedPubMed Central Google Scholar
Scheiffele, P., Fan, J., Choih, J., Fetter, R. & Serafini, T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell101, 657–669 (2000). ArticleCASPubMed Google Scholar
Song, J. Y., Ichtchenko, K., Sudhof, T. C. & Brose, N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses . Proc. Natl Acad. Sci. USA96, 1100– 1105 (1999). ArticleCASPubMedPubMed Central Google Scholar
Llinas, R. R. & Greenfield, S. A. On-line visualization of dendritic release of acetylcholinesterase from mammalian substantia nigra neurons. Proc. Natl Acad. Sci. USA84, 3047– 3050 (1987). ArticleCASPubMedPubMed Central Google Scholar
Holmes, C., Jones, S. A., Budd, T. C. & Greenfield, S. A. Non-cholinergic, trophic action of recombinant acetylcholinesterase on mid-brain dopaminergic neurons. J. Neurosci. Res.49, 207–218 (1997). ArticleCASPubMed Google Scholar
Inestrosa, N. C. et al. Acetylcholinesterase accelerates assembly of amyloid-β peptides into Alzheimer's fibrils: possible role of the peripheral site of the enzyme. Neuron16, 881– 891 (1996). ArticleCASPubMed Google Scholar
Paoletti, F., Mocali, A. & Vannucchi, A. M. Acetylcholinesterase in murine erythroleukemia (Friend) cells: evidence for megakaryocyte-like expression and potential growth-regulatory role of enzyme activity. Blood79, 2873– 2879 (1992). ArticleCASPubMed Google Scholar
Lev-Lehman, E., Deutsch, V., Eldor, A. & Soreq, H. Immature human megakaryocytes produce nuclear-associated acetylcholinesterase. Blood89, 3644–3653 (1997). ArticleCASPubMed Google Scholar
Kawashima, K. & Fujii, T. Extraneuronal cholinergic system in lymphocytes. Pharmacol. Ther.86, 29– 48 (2000). ArticleCASPubMed Google Scholar
Soreq, H. et al. Antisense oligonucleotide inhibition of acetylcholinesterase gene expression induces progenitor cell expansion and suppresses hematopoietic apoptosis ex vivo. Proc. Natl Acad. Sci. USA91, 7907–7911 (1994). ArticleCASPubMedPubMed Central Google Scholar
Brown, L. M. et al. Pesticide exposure and other agricultural risk factors for leukemia among men in Iowa and Minnesota. Cancer Res.50, 6585–6591 (1990). CASPubMed Google Scholar
Lev-Lehman, E. et al. Synaptogenesis and myopathy under acetylcholinestrase overexpression . J. Mol. Neurosci.14, 93– 105 (2000). ArticleCASPubMed Google Scholar
Lapidot-Lifson, Y. et al. Coamplification of human acetylcholinesterase and butyrylcholinesterase genes in blood cells: correlation with various leukemias and abnormal megakaryocytopoiesis . Proc. Natl Acad. Sci. USA86, 4715– 4719 (1989). ArticleCASPubMedPubMed Central Google Scholar
Stephenson, J., Czepulkowski, B., Hirst, W. & Mufti, G. Deletion of the acetylcholinesterase locus at 7q22 associated with myelodysplastic syndromes (MDS) and acute myeloid leukaemia (AML). Leuk. Res.20, 235–241 (1996). ArticleCASPubMed Google Scholar
Velan, B. et al. N-glycosylation of human acetylcholinesterase: effects on activity, stability and biosynthesis. Biochem. J.296, 649–656 (1993). ArticleCASPubMedPubMed Central Google Scholar
Chan, R. Y., Adatia, F. A., Krupa, A. M. & Jasmin, B. J. Increased expression of acetylcholinesterase T and R transcripts during hematopoietic differentiation is accompanied by parallel elevations in the levels of their respective molecular forms. J. Biol. Chem.273, 9727–9733 (1998). ArticleCASPubMed Google Scholar
Camp, S. & Taylor, P. in Structure and Function of Cholinesterases and Related Proteins (eds Doctor, B. P., Taylor, P., Quinn, D. M., Rotundo, R. L. & Gentry, M. K.) 51–55 (Plenum, New York, 1998). Book Google Scholar
Grisaru, D. et al. ARP, a peptide derived from the stress-associated acetylcholinesterase variant has hematopoietic growth promoting activities. Mol. Med. (in the press).
Li, Y., Camp, S., Rachinsky, T. L., Bongiorno, C. & Taylor, P. Promoter elements and transcriptional control of the mouse acetylcholinesterase gene. J. Biol. Chem.268, 3563–3572 ( 1993). ArticleCASPubMed Google Scholar
Shapira, M. et al. A transcription-activating polymorphism in the ACHE promoter associated with acute sensitivity to anti-acetylcholinesterases. Hum. Mol. Genet.9, 1273–1281 (2000). ArticleCASPubMed Google Scholar
Chan, R. Y., Boudreau-Lariviere, C., Angus, L. M., Mankal, F. A. & Jasmin, B. J. An intronic enhancer containing an N-Box motif is required for synapse- and tissue-specific expression of the acetylcholinesterase gene in skeletal muscle fibers. Proc. Natl Acad. Sci. USA96, 4627–4632 (1999). ArticleCASPubMedPubMed Central Google Scholar
Rotundo, R. L. Nucleus-specific translation and assembly of acetylcholinesterase in multinucleated muscle cells. J. Cell Biol.110, 715– 719 (1990). ArticleCASPubMed Google Scholar
Galyam, N. et al. Complex host cell responses to antisense suppression of ACHE gene expression. Antisense Nucl. Acid Drug Dev.11, 51–57 (2001). ArticleCAS Google Scholar
Kaufer, D., Friedman, A., Seidman, S. & Soreq, H. Acute stress facilitates long-lasting changes in cholinergic gene expression . Nature393, 373–377 (1998). ArticleCASPubMed Google Scholar
Nordberg, A., Hellstrom-Lindahl, E., Almkvist, O. & Meurling, L. Activity of acetylcholinesterase in CSF increases in Alzheimer's patients after treatment with tacrine. Alzheimer's Reports2 , 347–352 (1999). Google Scholar
Grisaru, D. et al. Human osteogenesis involves differentiation-dependent increases in the morphogenically active 3′ alternative splicing variant of acetylcholinesterase . Mol. Cell. Biol.19, 788– 795 (1999). ArticleCASPubMedPubMed Central Google Scholar
Schober, A. et al. Reduced acetylcholinesterase (AChE) activity in adrenal medulla and loss of sympathetic preganglionic neurons in TrkA-deficient, but not TrkB-deficient, mice. J. Neurosci.17, 891– 903 (1997). ArticleCASPubMedPubMed Central Google Scholar
Robertson, R. T. et al. Do subplate neurons comprise a transient population of cells in developing neocortex of rats? J. Comp. Neurol.426 , 632–650 (2000). ArticleCASPubMed Google Scholar
Shohami, E. et al. Antisense prevention of neuronal damages following head injury in mice. J. Mol. Med.78, 228– 236 (2000). ArticleCASPubMed Google Scholar
Gray, R., Rajan, A. S., Radcliffe, K. A., Yakehiro, M. & Dani, J. A. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature383, 713–716 (1996). ArticleCASPubMed Google Scholar
Ashani, Y. et al. Butyrylcholinesterase and acetylcholinesterase prophylaxis against soman poisoning in mice. Biochem. Pharmacol.41, 37–41 (1991). ArticleCASPubMed Google Scholar
Evans, W. E. & Relling, M. V. Pharmacogenomics: translating functional genomics into rational therapeutics. Science286, 487–491 (1999). ArticleCASPubMed Google Scholar
Luo, Z. D. et al. Calcineurin enhances acetylcholinesterase mRNA stability during C2-C12 muscle cell differentiation. Mol. Pharmacol.56, 886–894 (1999). ArticleCASPubMed Google Scholar
Giacobini, E. in Cholinesterases and Cholinesterase Inhibitors (ed. Giacobini, E.) 181–226 (Martin Dunitz, London, 2000 ). Google Scholar
Erb, C. et al. Compensatory mechanisms facilitate hippocampal acetylcholine release in transgenic mice expressing human acetylcholinesterase. J. Neurochem. (in the press).
Pollet, C. et al. Medical evaluation of Persian Gulf veterans with fatigue and/or chemical sensitivity. J. Med.29, 101– 113 (1998). CASPubMed Google Scholar
Okumura, T. et al. Report on 640 victims of the Tokyo subway sarin attack. Ann. Emerg. Med.28, 129–135 (1996). ArticleCASPubMed Google Scholar
Ohno, K., Brengman, J., Tsujino, A. & Engel, A. G. Human endplate acetylcholinesterase deficiency caused by mutations in the collagen-like tail subunit (ColQ) of the asymmetric enzyme. Proc. Natl Acad. Sci. USA95, 9654–9659 (1998). ArticleCASPubMedPubMed Central Google Scholar
Fournier, D. et al. Drosophila melanogaster acetylcholinesterase gene. Structure, evolution and mutations. J. Mol. Biol.210 , 15–22 (1989). ArticleCASPubMed Google Scholar
Prody, C. A., Dreyfus, P., Zamir, R., Zakut, H. & Soreq, H. De novo amplification within a 'silent' human cholinesterase gene in a family subjected to prolonged exposure to organophosphorous insecticides . Proc. Natl Acad. Sci. USA86, 690– 694 (1989). ArticleCASPubMedPubMed Central Google Scholar
Bartels, C. F., Zelinski, T. & Lockridge, O. Mutation at codon 322 in the human acetylcholinesterase (ACHE) gene accounts for YT blood group polymorphism. Am. J. Hum. Genet.52, 928–936 ( 1993). CASPubMedPubMed Central Google Scholar
Ehrlich, G. et al. Population diversity and distinct haplotype frequencies associated with ACHE and BCHE genes of Israeli Jews from trans-Caucasian Georgia and from Europe. Genomics22, 288– 295 (1994). ArticleCASPubMed Google Scholar
La Du, B. N. et al. Phenotypic and molecular biological analysis of human butyrylcholinesterase variants. Clin. Biochem.23, 423– 431 (1990). ArticleCASPubMed Google Scholar
Beeri, R. et al. Transgenic expression of human acetylcholinesterase induces progressive cognitive deterioration in mice. Curr. Biol.5, 1063–1071 (1995). ArticleCASPubMed Google Scholar
Xie, W. et al. Postnatal developmental delay and supersensitivity to organophosphate in gene-targeted mice lacking acetylcholinesterase. J. Pharmacol. Exp. Ther.293, 896–902 (2000). CASPubMed Google Scholar
von der Kammer, H. et al. Muscarinic acetylcholine receptors activate expression of the EGR gene family of transcription factors. J. Biol. Chem.273, 14538–14544 (1998). ArticleCASPubMed Google Scholar
Xie, J. & McCobb, D. P. Control of alternative splicing of potassium channels by stress hormones. Science280 , 443–446 (1998). ArticleCASPubMed Google Scholar
Daoud, R., Da Penha Berzaghi, M., Siedler, F., Hubener, M. & Stamm, S. Activity-dependent regulation of alternative splicing patterns in the rat brain. Eur. J. Neurosci.11, 788–802 (1999). ArticleCASPubMed Google Scholar
Combes, D., Fedon, Y., Grauso, M., Toutant, J. P. & Arpagaus, M. Four genes encode acetylcholinesterases in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. cDNA sequences, genomic structures, mutations and in vivo expression. J. Mol. Biol.300, 727–742 (2000). ArticleCASPubMed Google Scholar
Anglister, L., Stiles, J. R. & Salpeter, M. M. Acetylcholinesterase density and turnover number at frog neuromuscular junctions, with modeling of their role in synaptic function . Neuron12, 783–794 (1994). ArticleCASPubMed Google Scholar
Peng, H. B., Xie, H., Rossi, S. G. & Rotundo, R. L. Acetylcholinesterase clustering at the neuromuscular junction involves perlecan and dystroglycan . J. Cell Biol.145, 911– 921 (1999). ArticleCASPubMedPubMed Central Google Scholar
Seidman, S. et al. Synaptic and epidermal accumulations of human acetylcholinesterase are encoded by alternative 3′-terminal exons. Mol. Cell. Biol.15, 2993–3002 ( 1995). ArticleCASPubMedPubMed Central Google Scholar
Harlow, M. L., Ress, D., Stoschek, A., Marshall, R. M. & McMahan, U. J. The architecture of active zone material at the frog's neuromuscular junction. Nature409, 479– 484 (2001). ArticleCASPubMed Google Scholar
Feng, G. et al. Genetic analysis of collagen Q: roles in acetylcholinesterase and butyrylcholinesterase assembly and in synaptic structure and function . J. Cell Biol.144, 1349– 1360 (1999). ArticleCASPubMedPubMed Central Google Scholar
Karpel, R. et al. Overexpression of alternative human acetylcholinesterase forms modulates process extensions in cultured glioma cells. J. Neurochem.66, 114–123 ( 1996). ArticleCASPubMed Google Scholar
Sternfeld, M. et al. Excess 'readthrough' acetylcholinesterase attenuates but the 'synaptic' variant intensifies neurodeterioration correlates. Proc. Natl Acad. Sci. USA97, 8647– 8652 (2000). ArticleCASPubMedPubMed Central Google Scholar
Chien, C. T., Bartel, P. L., Sternglanz, R. & Fields, S. The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl Acad. Sci. USA88, 9578–9582 ( 1991). ArticleCASPubMedPubMed Central Google Scholar
Mezey, E., Chandross, K. J., Harta, G., Maki, R. A. & McKercher, S. R. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science290, 1779–1782 ( 2000). ArticleCASPubMed Google Scholar
Kuhl, D. E. et al. In vivo mapping of cerebral acetylcholinesterase activity in aging and Alzheimer's disease. Neurology52, 691–699 (1999). ArticleCASPubMed Google Scholar
Shinotoh, H. et al. Positron emission tomographic measurement of acetylcholinesterase activity reveals differential loss of ascending cholinergic systems in Parkinson's disease and progressive supranuclear palsy. Ann. Neurol.46, 62–69 (1999). ArticleCASPubMed Google Scholar
Vereker, E., O'Donnell, E. & Lynch, M. A. The inhibitory effect of interleukin-1β on long-term potentiation is coupled with increased activity of stress-activated protein kinases. J. Neurosci.20, 6811– 6819 (2000). ArticleCASPubMedPubMed Central Google Scholar
Xu, L., Anwyl, R. & Rowan, M. J. Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature387, 497–500 (1997). ArticleCASPubMed Google Scholar
Hamilton, S. E. et al. Disruption of the m1 receptor gene ablates muscarinic receptor-dependent M current regulation and seizure activity in mice. Proc. Natl Acad. Sci. USA94, 13311–13316 (1997). ArticleCASPubMedPubMed Central Google Scholar
Gennari, K., Brunner, J. & Brodbeck, U. Tetrameric detergent-soluble acetylcholinesterase from human caudate nucleus: subunit composition and number of active sites. J. Neurochem.49, 12–18 (1987). ArticleCASPubMed Google Scholar
Franklin, R. B. J. & Paxinos, G. The Mouse Brain in Stereotaxic Coordinates (Academic, San Diego, 1997 ). Google Scholar
Holmstedt, B. in Cholinesterases and Cholinesterase Inhibitors: Basic, Preclinical and Clinical Aspects (ed. Giacobini, E.) 1–8 (Martin Dunitz, London, 2000). Google Scholar
Abramson, S. N., Radic, Z., Manker, D., Faulkner, D. J. & Taylor, P. Onchidal: a naturally occurring irreversible inhibitor of acetylcholinesterase with a novel mechanism of action. Mol. Pharmacol.36, 349–354 ( 1989). CASPubMed Google Scholar
Wilson, I. B. Molecular complementarity and antidotes for alkylphosphate poisoning. Fed. Proc.18, 752–758 ( 1959). CASPubMed Google Scholar
Keeler, J. R., Hurst, C. G. & Dunn, M. A. Pyridostigmine used as a nerve agent pretreatment under wartime conditions. J. Am. Med. Assoc.266, 693–695 (1991). ArticleCAS Google Scholar
Haley, R. W., Kurt, T. L. & Hom, J. Is there a Gulf War Syndrome? Searching for syndromes by factor analysis of symptoms. J. Am. Med. Assoc.277, 215–222 (1997). ArticleCAS Google Scholar
Sapolsky, R. M. The stress of Gulf War syndrome. Nature Med.393, 308–309 (1998). CAS Google Scholar
Friedman, A. et al. Pyridostigmine brain penetration under stress enhances neuronal excitability and induces early immediate transcriptional response. Nature Med.2, 1382–1385 (1996). ArticleCASPubMed Google Scholar
Grauer, E., Alkalai, D., Kapon, J., Cohen, G. & Raveh, L. Stress does not enable pyridostigmine to inhibit brain cholinesterase after parenteral administration. Toxicol. Appl. Pharmacol.164, 301–304 (2000). ArticleCASPubMed Google Scholar
Lallement, G. et al. Heat stress, even extreme, does not induce penetration of pyridostigmine into the brain of guinea pigs. Neurotoxicology19, 759–766 (1998). CASPubMed Google Scholar
Esposito, P. et al. Acute stress increases permeability of the blood–brain-barrier through activation of brain mast cells. Brain Res.888, 117–127 (2001). ArticleCASPubMed Google Scholar
Grauer, E. et al. Viral neuroinvasion as a marker for BBB integrity following exposure to cholinesterase inhibitors. Life Sci.68 , 985–990 (2001). ArticleCASPubMed Google Scholar
Relyea, R. A. & Mills, N. Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proc. Natl Acad. Sci. USA98, 2491–2496 (2001). ArticleCASPubMedPubMed Central Google Scholar
Coyle, J. T., Price, D. L. & DeLong, M. R. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science219, 1184– 1190 (1983). ArticleCASPubMed Google Scholar
Patrick, J. & Lindstrom, J. Autoimmune response to acetylcholine receptor. Science180, 871– 872 (1973). ArticleCASPubMed Google Scholar
Keesey, J. C. Contemporary opinions about Mary Walker: a shy pioneer of therapeutic neurology . Neurology51, 1433–1439 (1998). ArticleCASPubMed Google Scholar
Beeri, R. et al. Enhanced hemicholinium binding and attenuated dendrite branching in cognitively impaired acetylcholinesterase-transgenic mice. J. Neurochem.69, 2441–2451 (1997). ArticleCASPubMed Google Scholar
Alvarez, A. et al. Stable complexes involving acetylcholinesterase and amyloid-β peptide change the biochemical properties of the enzyme and increase the neurotoxicity of Alzheimer's fibrils. J. Neurosci.18, 3213–3223 (1998). ArticleCASPubMedPubMed Central Google Scholar
Sberna, G. et al. Acetylcholinesterase is increased in the brains of transgenic mice expressing the C-terminal fragment (CT100) of the β-amyloid protein precursor of Alzheimer's disease. J. Neurochem.71, 723–731 (1998). ArticleCASPubMed Google Scholar
Wilson, B. W. & Viola, G. A. Multiple forms of acetylcholinesterase in nutritional and inherited muscular dystrophy of the chicken. J. Neurol. Sci.16, 183– 192 (1972). ArticleCASPubMed Google Scholar
Silman, I., di Giamberardino, L., Lyles, L., Couraud, J. Y. & Barnard, E. A. Parallel regulation of acetylcholinesterase and pseudocholinesterase in normal, denervated and dystrophic chicken skeletal muscle. Nature280, 160– 162 (1979). ArticleCASPubMed Google Scholar