Near-complete adaptation of the PRiMA knockout to the lack of central acetylcholinesterase

Journal of Neurochemistry

Volumn 122, Issue 5, 2012, Pages 1065-1080

  Farar, Vladimir ^a,b   Mohr, Franziska ^c   Legrand, Marie ^a   Lamotte D'Incamps, Boris ^d   Cendelin, Jan ^b   Leroy, Jacqueline ^a   Abitbol, Marc ^a   Bernard, Veronique ^e   Baud, Frédéric ^a   Fournet, Vincent ^e   Houze, Pascal ^a   Klein, Jochen ^c   Plaud, Benoit ^f   Tuma, Jan ^b   Zimmermann, Martina ^c   Ascher, Philippe ^d   Hrabovska, Anna ^g   Myslivecek, Jaromir ^b,h   Krejci, Eric ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b CHARLES UNIVERSITY   (Czech Republic)

^c GOETHE UNIVERSITY   (Germany)

^d CNRS   (France)

^e INSERM   (France)

^f UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^g Faculty of Natural Sciences   (Slovakia)

^h Institute of Health Studies   (Czech Republic)

Author keywords

acetylcholine; Alzheimer's disease; autonomous nervous system; cholinergic receptors; microdialysis; mouse genetics

Indexed keywords

ACETYLCHOLINE; ACETYLCHOLINESTERASE; CHOLINESTERASE INHIBITOR; MEMBRANE PROTEIN; MUSCARINIC RECEPTOR; PROLINE RICH MEMBRANE ANCHOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BRAIN ELECTROPHYSIOLOGY; BRAIN LEVEL; BRAIN TISSUE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME DEFICIENCY; GAIT; KNOCKOUT MOUSE; LIGAND BINDING; MAZE TEST; MICRODIALYSIS; MOUSE; MUTANT; NONHUMAN; OPEN FIELD TEST; PERIPHERAL NERVOUS SYSTEM; PHENOTYPE; PRIORITY JOURNAL; RECEPTOR DENSITY; ROTAROD TEST; TELEMETRY; WILD TYPE;

ACETYLCHOLINE; ACETYLCHOLINESTERASE; ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, NEWBORN; BICYCLO COMPOUNDS, HETEROCYCLIC; BODY TEMPERATURE; BRAIN; BUNGAROTOXINS; CHOLINE; CHOLINERGIC AGENTS; CHOLINESTERASE INHIBITORS; COLLAGEN; DIHYDRO-BETA-ERYTHROIDINE; DOSE-RESPONSE RELATIONSHIP, DRUG; EXPLORATORY BEHAVIOR; GAIT; GENE EXPRESSION REGULATION; MAZE LEARNING; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICRODIALYSIS; MOTOR ACTIVITY; MUSCARINIC ANTAGONISTS; MUSCLE PROTEINS; NAILS, INGROWN; NEOSTIGMINE; NERVE TISSUE PROTEINS; NEURONS; PIRENZEPINE; PROTEIN BINDING; PYRIDINES; RADIOISOTOPES; RECEPTORS, MUSCARINIC; ROTAROD PERFORMANCE TEST; SCOPOLAMINE HYDROBROMIDE; SPINAL CORD; STATISTICS, NONPARAMETRIC; TRITIUM;

MUS;

EID: 84865324037     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07856.x     Document Type: Article

References (63)

1. Albin R. L., Howland M. M., Higgins D. S., and, Frey K. A., (1994) Autoradiographic quantification of muscarinic cholinergic synaptic markers in bat, shrew, and rat brain. Neurochem. Res. 19, 581-589. (Pubitemid 24139252)
2. Andersson D. R., Björnsson E., Bergquist F., and, Nissbrandt H., (2010) Motor activity-induced dopamine release in the substantia nigra is regulated by muscarinic receptors. Exp. Neurol. 221, 251-259.
3. Araki T., Tanji H., Fujihara K., Kato H., Imai Y., Mizugaki M., and, Itoyama Y., (2000) Sequential changes of cholinergic and dopaminergic receptors in brains after 6-hydroxydopamine lesions of the medial forebrain bundle in rats. J. Neural Transm. 107, 873-884.
4. Ayata C., Ayata G., Hara H., et al. (1997) Mechanisms of reduced striatal NMDA excitotoxicity in type I nitric oxide synthase knock-out mice. J. Neurosci. 17, 6908-6917. (Pubitemid 27427869)
5. Barbour B., (2001) An Evaluation of Synapse Independence. J. Neurosci., 21, 7969-7984. (Pubitemid 32952754)
6. Bennett M. R., Farnell L., Gibson W. G., and, Lavidis N. A., (1997) Synaptic transmission at visualized sympathetic boutons: stochastic interaction between acetylcholine and its receptors. Biophys. J. 72, 1595-1606. (Pubitemid 27133099)
7. 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. (Pubitemid 36687856)
8. Bernard V., Girard E., Hrabovska A., Camp S., Taylor P., Plaud B., and, Krejci E., (2011) Distinct localization of collagen Q and PRiMA forms of acetylcholinesterase at the neuromuscular junction. Mol. Cell. Neurosci. 46, 272-281.
9. Berrard S., Varoqui H., Cervini R., IsraÃl M., Mallet J., and, Diebler M. F., (1995) Coregulation of two embedded gene products, choline acetyltransferase and the vesicular acetylcholine transporter. J. Neurochem. 65, 939-942.
10. Bon S., Coussen F., and, Massoulié J., (1997) Quaternary Associations of Acetylcholinesterase. J. Biol. Chem. 272, 3016-3021.
11. Boudinot E., Emery M. J., Mouisel E., Chatonnet A., Champagnat J., Escourrou P., and, Foutz A. S., (2004) Increased ventilation and CO2 chemosensitivity in acetylcholinesterase knockout mice. Respir Physiol Neurobiol 140, 231-241. (Pubitemid 38746882)
12. Boudinot E., Bernard V., Camp S., Taylor P., Champagnat J., Krejci E., and, Foutz A. S., (2009) Influence of differential expression of acetylcholinesterase in brain and muscle on respiration. Respir Physiol Neurobiol 165, 40-48.
13. Camp S., Zhang L., Marquez M., de la Torre B., Long J. M., Bucht G., and, Taylor P., (2005) Acetylcholinesterase (AChE) gene modification in transgenic animals: functional consequences of selected exon and regulatory region deletion. Chem. Biol. Interact., 157-158, 79-86. (Pubitemid 41757637)
14. Camp S., De Jaco A., Zhang L., Marquez M., De la Torre B., and, Taylor P., (2008) Acetylcholinesterase expression in muscle is specifically controlled by a promoter-selective enhancesome in the first intron. J. Neurosci. 28, 2459-2470. (Pubitemid 351348184)
15. Camp S., Zhang L., Krejci E., Dobbertin A., Bernard V., Girard E., Duysen E. G., Lockridge O., De Jaco A., and, Taylor P., (2010) Contributions of selective knockout studies to understanding cholinesterase disposition and function. Chem. Biol. Interact. 187, 72-77.
16. Chatonnet F., Boudinot É., Chatonnet A., Taysse L., Daulon S., Champagnat J., and, Foutz A. S., (2003) Respiratory survival mechanisms in acetylcholinesterase knockout mouse. Eur. J. Neurosci. 18, 1419-1427. (Pubitemid 37220055)
17. Clement J. G., (1993) Pharmacological nature of soman-induced hypothermia in mice. Pharmacol. Biochem. Behav. 44, 689-702.
18. Dean B., Hussain T., Hayes W., Scarr E., Kitsoulis S., Hill C., Opeskin K., and, Copolov D. L., (1999) Changes in serotonin2A and GABA(A) receptors in schizophrenia: studies on the human dorsolateral prefrontal cortex. J. Neurochem. 72, 1593-1599. (Pubitemid 29140833)
19. Descarries L., (1998) The hypothesis of an ambient level of acetylcholine in the central nervous system. J. Physiol. Paris 92, 215-220. (Pubitemid 29050937)
20. Dobbertin A., Hrabovska A., Dembele K., Camp S., Taylor P., Krejci E., and, Bernard V., (2009) Targeting of acetylcholinesterase in neurons in vivo: a dual processing function for the proline-rich membrane anchor subunit and the attachment domain on the catalytic subunit. J. Neurosci. 29, 4519-4530.
21. 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. (Pubitemid 34786635)
22. Duysen E. G., Li B., Darvesh S., and, Lockridge O., (2007) Sensitivity of butyrylcholinesterase knockout mice to ( - )-huperzine A and donepezil suggests humans with butyrylcholinesterase deficiency may not tolerate these Alzheimer's disease drugs and indicates butyrylcholinesterase function in neurotransmission. Toxicology 233, 60-69. (Pubitemid 46509686)
23. Eccles J. C., (1944) The nature of synaptic transmission in a sympathetic ganglion. J. Physiol. 103, 27-54.
24. Fayuk D., and, Yakel J. L., (2004) Regulation of Nicotinic Acetylcholine Receptor Channel Function by Acetylcholinesterase Inhibitors in Rat Hippocampal CA1 Interneurons. Mol. Pharmacol. 66, 658-666. (Pubitemid 39329265)
25. Feng G., Krejci E., Molgo J., Cunningham J. M., Massoulié J., and, Sanes J. R., (1999) Genetic analysis of collagen Q: roles in acetylcholinesterase and butyrylcholinesterase assembly and in synaptic structure and function. J. Cell Biol. 144, 1349-1360. (Pubitemid 29157310)
26. Fernagut P.-O., Chalon S., Diguet E., Guilloteau D., Tison F., and, Jaber M., (2003) Motor behaviour deficits and their histopathological and functional correlates in the nigrostriatal system of dopamine transporter knockout mice. Neuroscience 116, 1123-1130. (Pubitemid 36262970)
27. Fonnum F., (1969) Radiochemical micro assays for the determination of choline acetyltransferase and acetylcholinesterase activities. Biochem. J. 115, 465-472.
28. Hamers F. P. T., Koopmans G. C., and, Joosten E. A. J., (2006) CatWalk-assisted gait analysis in the assessment of spinal cord injury. J. Neurotrauma 23, 537-548. (Pubitemid 43726327)
29. Hartmann J., Kiewert C., Duysen E. G., Lockridge O., Greig N. H., and, Klein J., (2007) Excessive hippocampal acetylcholine levels in acetylcholinesterase-deficient mice are moderated by butyrylcholinesterase activity. J. Neurochem. 100, 1421-1429.
30. Hartmann J., Kiewert C., Duysen E. G., Lockridge O., and, Klein J., (2008) Choline availability and acetylcholine synthesis in the hippocampus of acetylcholinesterase-deficient mice. Neurochem. Int. 52, 972-978. (Pubitemid 351418054)
31. Hrabovska A., Farar V., Bernard V., Duysen E. G., Brabec J., Lockridge O., and, Myslivecek J., (2010) Drastic decrease in dopamine receptor levels in the striatum of acetylcholinesterase knock-out mouse. Chem. Biol. Interact. 183, 194-201.
32. Jones I. W., and, Wonnacott S., (2004) Precise Localization of α7 Nicotinic Acetylcholine Receptors on Glutamatergic Axon Terminals in the Rat Ventral Tegmental Area. J. Neurosci. 24, 11244-11252. (Pubitemid 39658259)
33. Koelle G. B., Massoulié J., Eugène D., Melone M. A., and, Boulla G., (1987) Distributions of molecular forms of acetylcholinesterase and butyrylcholinesterase in nervous tissue of the cat. Proc. Natl. Acad. Sci. USA 84, 7749-7752.
34. Krejci E., Thomine S., Boschetti N., Legay C., Sketelj J., and, Massoulié J., (1997) The mammalian gene of acetylcholinesterase- associated collagen. J. Biol. Chem. 272, 22840-22847. (Pubitemid 27386105)
35. Kristofiková Z., Rícnà J., Kozmiková I., Rípová D., Zach P., and, Klaschka J., (2006) Sex-dependent actions of amyloid beta peptides on hippocampal choline carriers of postnatal rats. Neurochem. Res. 31, 351-360. (Pubitemid 43829324)
36. Lamotte d'Incamps B., and, Ascher P., (2008) Four Excitatory Postsynaptic Ionotropic Receptors Coactivated at the Motoneuron-Renshaw Cell Synapse. J. Neurosci. 28, 14121-14131.
37. Lamotte d'Incamps B., Krejci E., and, Ascher P., (2012) Mechanisms shaping the slow nicotinic synaptic current at the motoneuron-Renshaw cell synapse. J. Neurosci. 32, 8413-8423.
38. Lendvai B.,. (2008) Cholinergic Transmission, in Handbook of Neurochemistry and Molecular Neurobiology (, Lajtha A., and, Vizi E. S., eds), pp. 113-127. Springer US, Boston, MA.
39. 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. (Pubitemid 36351661)
40. Machová E., Jakubík J., Michal P., Oksman M., Iivonen H., Tanila H., and, Dolezal V., (2008) Impairment of muscarinic transmission in transgenic APPswe/PS1dE9 mice. Neurobiol. Aging 29, 368-378. (Pubitemid 351215591)
41. Martres M. P., Sales N., Bouthenet M. L., and, Schwartz J. C., (1985) Localisation and pharmacological characterisation of D-2 dopamine receptors in rat cerebral neocortex and cerebellum using [125I]iodosulpride. Eur. J. Pharmacol. 118, 211-219. (Pubitemid 16179845)
42. Mihaylova V., Müller J. S., Vilchez J. J., et al. (2008) Clinical and molecular genetic findings in COLQ-mutant congenital myasthenic syndromes. Brain 131, 747-759. (Pubitemid 351294715)
43. Morris R., (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47-60. (Pubitemid 14088970)
44. Naik R. S., Hartmann J., Kiewert C., Duysen E. G., Lockridge O., and, Klein J., (2009) Effects of rivastigmine and donepezil on brain acetylcholine levels in acetylcholinesterase-deficient mice. J. Pharm. Pharm. Sci. 12, 79-85.
45. Paxinos G., and, Watson C.,. (2007) The Rat Brain in Stereotaxic Coordinates: hard Cover Edition, Academic Press, Sydney, Australia.
46. Pepeu G., and, Giovannini M. G., (2010) Cholinesterase inhibitors and memory. Chem. Biol. Interact. 187, 403-408.
47. Perrier A. L., Massoulié J., and, Krejci E., (2002) PRiMA: the membrane anchor of acetylcholinesterase in the brain. Neuron 33, 275-285. (Pubitemid 34127759)
48. Perry D. C., and, Kellar K. J., (1995) [3H]epibatidine labels nicotinic receptors in rat brain: an autoradiographic study. J. Pharmacol. Exp. Ther. 275, 1030-1034.
49. Rang H. P., (1981) The characteristics of synaptic currents and responses to acetylcholine of rat submandibular ganglion cells. J. Physiol. 311, 23-55. (Pubitemid 11166907)
50. Schumacher M., Camp S., Maulet Y., Newton M., MacPhee-Quigley K., Taylor S. S., Friedmann T., and, Taylor P., (1986) Primary structure of Torpedo californica acetylcholinesterase deduced from its cDNA sequence. Nature 319, 407-409.
51. Sipos M. L., Burchnell V., and, Galbicka G., (1999) Dose-response curves and time-course effects of selected anticholinergics on locomotor activity in rats. Psychopharmacology (Berl) 147, 250-256. (Pubitemid 30010544)
52. Skau K. A., and, Brimijoin S., (1980) Multiple molecular forms of acetylcholinesterase in rat vagus nerve, smooth muscle, and heart. J. Neurochem. 35, 1151-1154. (Pubitemid 11198288)
53. Spurden D. P., Court J. A., Lloyd S., Oakley A., Perry R., Pearson C., Pullen R. G. L., and, Perry E. K., (1997) Nicotinic receptor distribution in the human thalamus: autoradiographical localization of [3H]nicotine and [125I][alpha]-bungarotoxin binding. J. Chem. Neuroanat. 13, 105-113. (Pubitemid 27397131)
54. Sun M., Lee C. J., and, Shin H.-S., (2007) Reduced nicotinic receptor function in sympathetic ganglia is responsible for the hypothermia in the acetylcholinesterase knockout mouse. J. Physiol. (Lond.) 578, 751-764. (Pubitemid 46165507)
55. Taylor P., (1996) Anticholinesterase agents. The pharmacol. basis of ther. 9, 161-176.
56. Volpicelli-Daley L. A., Duysen E. G., Lockridge O., and, Levey A. I., (2003a) Altered hippocampal muscarinic receptors in acetylcholinesterase- deficient mice. Ann. Neurol. 53, 788-796. (Pubitemid 36622517)
57. Volpicelli-Daley L. A., Hrabovska A., Duysen E. G., Ferguson S. M., Blakely R. D., Lockridge O., and, Levey A. I., (2003b) Altered striatal function and muscarinic cholinergic receptors in acetylcholinesterase knockout mice. Mol. Pharmacol. 64, 1309-1316. (Pubitemid 37532220)
58. Wagner S., Kufleitner J., Zensi A., Dadparvar M., Wien S., Bungert J., Vogel T., Worek F., Kreuter J., and, von Briesen H., (2010) Nanoparticulate Transport of Oximes over an In Vitro Blood-Brain Barrier Model. PLoS One 5, e14213.
59. Wathey J. C., Nass M. M., and, Lester H. A., (1979) Numerical reconstruction of the quantal event at nicotinic synapses. Biophys. J. 27, 145-164. (Pubitemid 9213751)
60. Wolff S. C., Hruska Z., Nguyen L., and, Dohanich G. P., (2008) Asymmetrical distributions of muscarinic receptor binding in the hippocampus of female rats. Eur. J. Pharmacol. 588, 248-250.
61. 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. (Pubitemid 30417856)
62. Yamamura H. I., and, Snyder S. H., (1974) Muscarinic Cholinergic Binding in Rat Brain. Proc. Natl. Acad. Sci. USA 71, 1725-1729.
63. Zhang Z., Coggan J. S., and, Berg D. K., (1996) Synaptic Currents Generated by Neuronal Acetylcholine Receptors Sensitive to α-Bungarotoxin. Neuron 17, 1231-1240. (Pubitemid 27021107)