Co-localization of PRiMA with acetylcholinesterase in cholinergic neurons of rat brain: An immunocytochemical study

Brain Research

Volumn 1344, Issue , 2010, Pages 34-42

  Henderson, Zaineb ^a   Matto, Nazia ^a   John, Danielle ^a   Nalivaeva, Natalia N ^a   Turner, Anthony J ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Acetylcholinesterase; Cranial nerve nuclei; Immunocytochemistry; Medial septum; Nucleus basalis magnocellularis; Pedunculopontine nucleus; PRiMA; Substantia nigra

Indexed keywords

ACETYLCHOLINESTERASE; CELL MEMBRANE PROTEIN; PROLINE RICH MEMBRANE ANCHOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; CRANIAL NERVE; ENZYME ACTIVITY; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SUBSTANTIA NIGRA; TISSUE DISTRIBUTION;

ACETYLCHOLINESTERASE; ANIMALS; BRAIN; CHOLINERGIC AGENTS; MALE; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; NERVE TISSUE PROTEINS; NEURONS; RATS; RATS, WISTAR;

RATTUS;

EID: 77953916706     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.05.022     Document Type: Article

References (50)

1. Appleyard M.E. Secreted acetylcholinesterase-nonclassical aspects of a classical enzyme. TINS 15 (1992) 485-490
2. Appleyard M.E., and Smith A.D. Spontaneous and carbachol-evoked in vivo secretion of acetylcholinesterase from the hippocampus of the rat. Neurochem. Int. 11 (1987) 397-406
3. Behra M., Cousin X., Bertrand C., Vonesch J.L., Biellmann D., Chatonnet A., and Strahle U. Acetylcholinesterase is required for neuronal and muscular development in the zebrafish embryo. Nat. Neurosci. 5 (2002) 111-118
4. Carson K.A., Geula C., and Mesulam M.M. Electron-microscopic localization of cholinesterase activity in Alzheimer brain-tissue. Brain Res. 540 (1991) 204-208
5. Colgin L.L., Kubota D., and Lynch G. Cholinergic plasticity in the hippocampus. Proc. Natl Acad. Sci. USA 100 (2003) 2872-2877
6. Cousin X., Strahle U., and Chatonnet A. Are there non-catalytic functions of acetylcholinesterases? Lessons from mutant animal models. Bioessays 27 (2005) 189-200
7. Davidoff M.S., and Irintchev A.P. Acetylcholinesterase activity and type-C synapses in the hypoglossal, facial and spinal-cord motor nuclei of rats-an electron-microscope study. Histochemistry 84 (1986) 515-524
8. Dobbertin A., Hrabovska A., Dembele K., Camp S., Taylor P., Krejci E., and Bernard V. 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 (2009) 4519-4530
9. Engel A.K., and Kreutzberg G.W. Neuronal surface changes in the dorsal vagal motor nucleus of the guinea-pig in response to axotomy. J. Comp. Neurol. 275 (1988) 181-200
10. Flumerfelt B.A., and Lewis P.R. Cholinesterase activity in hypoglossal nucleus of rat and changes produced by axotomy-a light and electron-microscopic study. J. Anat. 119 (1975) 309-331
11. Freund T.F. GABAergic septohippocampal neurons contain parvalbumin. Brain Res. 478 (1989) 375-381
12. Geula C., and Mesulam M. Special properties of cholinesterases in the cerebral cortex of Alzheimer's disease. Brain Res. 498 (1989) 185-189
13. Greenfield S.A. A noncholinergic action of acetylcholinesterase (AChE) in the brain-from neuronal secretion to the generation of movement. Cell. Mol. Neurobiol. 11 (1991) 55-77
14. Greenfield S.A., Chubb I.W., Grunewald R.A., Henderson Z., May J., Portnoy S., Weston J., and Wright M.C. A non-cholinergic function for acetylcholinesterase in the substantia nigra: behavioural evidence. Exp. Brain Res. 54 (1984) 513-520
15. Greenfield S.A., Zimmermann M., and Bond C.E. Non-hydrolytic functions of acetylcholinesterase-the significance of C-terminal peptides. FEBS J. 275 (2008) 604-611
16. Grisaru D., Sternfeld M., Eldor A., Glick D., and Soreq H. Structural roles of acetylcholinesterase variants in biology and pathology. Eur. J. Biochem. 264 (1999) 672-686
17. Gritti I., Mainville L., and Jones B.E. Codistribution of GABA- with acetylcholine-synthesizing neurons in the basal forebrain of the rat. J. Comp. Neurol. 329 (1993) 438-457
18. Henderson Z. A projection from acetylcholinesterase-containing neurones in the diagonal band to the occipital cortex of the rat. Neuroscience 6 (1981) 1081-1088
19. Henderson Z. Ultrastructure and acetylcholinesterase content of neurones forming connections between the striatum and substantia nigra of rat. J. Comp. Neurol. 197 (1981) 185-196
20. Henderson Z. Acetylcholinesterase on the dendrites of central cholinergic neurons: an electron microscopical study in the ferret. Neuroscience 28 (1989) 95-108
21. Henderson Z. Lamellar bodies are markers of cholinergic neurons in ferret nucleus basalis. J. Neurocytol. 18 (1989) 95-103
22. Henderson Z., and Greenfield S.A. Ultrastructural localization of acetylcholinesterase in substantia nigra: a comparison between rat and guinea pig. J. Comp. Neurol. 230 (1984) 278-286
23. Henderson Z., Morris N.P., Grimwood P., Fiddler G., Yang H.-W., and Appenteng K. Morphology of local axon collaterals of electrophysiologically characterized neurons in the rat medial septal/diagonal band complex. J. Comp. Neurol. 430 (2001) 410-432
24. Henderson Z., Fiddler G., Saha S., Boros A., and Halasy K. A parvalbumin-containing, axosomatic synaptic network in the rat medial septum: relevance to rhythmogenesis. Eur. J. Neurosci. 19 (2004) 2753-2768
25. Henderson Z., Boros A., Janzso G.E., Westwood A.J., Monyer H., and Halasy K. Somato-dendritic nicotinic receptor responses recorded in vitro from the medial septal diagonal band complex of the rodent. J. Physiol. Lond. 562 (2005) 165-182
26. Henderson Z., Lu C.B., Janzsó G., Matto N., McKinley C.E., Yanagawa Y., and Halasy K. Distribution and role of Kv3.1b in neurons in the medial septum diagonal band complex. Neuroscience 166 (2010) 952-969
27. Inestrosa N.C., Alvarez A., Perez C.A., Moreno R.D., Vicente M., Linker C., Casanueva O.I., Soto C., and Garrido J. Acetylcholinesterase accelerates assembly of amyloid-beta-peptides into Alzheimer's fibrils: possible role of the peripheral site of the enzyme. Neuron 16 (1996) 881-891
28. Kar S., Slowikowski S.P.M., Westaway D., and Mount H.T.J. Interactions between beta-amyloid and central cholinergic neurons: implications for Alzheimer's disease. J. Psychiatr. Neurosci. 29 (2004) 427-441
29. Leung K.W., Xie H.Q., Chen V.P., Mok M.K.W., Chu G.K.Y., Choi R.C.Y., and Tsim K.W.K. Restricted localization of proline-rich membrane anchor (PRiMA) of globular form acetylcholinesterase at the neuromuscular junctions-contribution and expression from motor neurons. FEBS J. 276 (2009) 3031-3042
30. Li W., Ochalski P.A.Y., Brimijoin S., Jordan L.M., and Nagy J.I. C-terminals on motoneurons-electron-microscope localization of cholinergic markers in adult-rats and antibody-induced depletion in neonates. Neuroscience 65 (1995) 879-891
31. 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 (2005) 3-14
32. Matsuda W., Furuta T., Nakamura K.C., Hioki H., Fujiyama F., Arai R., and Kaneko T. Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. J. Neurosci. 29 (2009) 444-453
33. Mesulam M.M., Geula C., and Moran M.A. Anatomy of cholinesterase inhibition in Alzheimer's disease: effect of physostigmine and tetrahydroaminoacridine on plaques and tangles. Ann. Neurol. 22 (1987) 683-691
34. Nalivaeva N.N., and Turner A.J. Does acetylcholinesterase secretion involve an ADAMs-like metallosecretase?. Lett. Pept. Sci. 6 (1999) 343-348
35. Navaratnam D.S., Fernando F.S., Priddle J.D., Giles K., Clegg S.M., Pappin D.J., Craig I., and Smith A.D. Hydrophobic protein that copurifies with human brain acetylcholinesterase: amino acid sequence, genomic organization, and chromosomal localization. J. Neurochem. 74 (2000) 2146-2153
36. Pereira E.F., Hilmas C., Santos M.D., Alkondon M., Maelicke A., and Albuquerque E.X. Unconventional ligands and modulators of nicotinic receptors. J. Neurobiol. 53 (2002) 479-500
37. Perrier A.L., Massoulie J., and Krejci E. PRiMA: the membrane anchor of acetylcholinesterase in the brain. Neuron 33 (2002) 275-285
38. Perrier N.A., Kherif S., Perrier A.L., Dumas S., Mallet J., and Massoulie J. Expression of PRiMA in the mouse brain: membrane anchoring and accumulation of 'tailed' acetylcholinesterase. Eur. J. Neurosci. 18 (2003) 1837-1847
39. Quirion R. Cholinergic markers in Alzheimer's disease and the autoregulation of acetylcholine release. J. Psychiatr. Neurosci. 18 (1993) 226-234
40. Rakonczay Z., and Brimijoin S. Monoclonal-antibodies to rat-brain acetylcholinesterase-comparative affinity for soluble and membrane-associated enzyme and for enzyme from different vertebrate species. J. Neurochem. 46 (1986) 280-287
41. Schliebs R., and Arendt T. The significance of the cholinergic system in the brain during aging and in Alzheimer's disease. J. Neural Trans. 113 (2006) 1625-1644
42. Schweitzer E.S. Regulated and constitutive secretion of distinct molecular forms of acetylcholinesterase from PC12 cells. J. Cell Sci. 106 (1993) 731-740
43. Shute C.C.D., and Lewis P.R. Cholinesterase-containing systems of brain of rat. Nature 199 (1963) 1160-1164
44. Shute C.C.D., and Lewis P.R. The ascending cholinergic reticular system: neocortical, olfactory and subcortical projections. Brain 90 (1967) 497-520
45. Wonnacott S., Soliakov L., Wilkie G., Redfern P., and Marshall D. Presynaptic nicotinic acetylcholine receptors in the brain. Drug Dev. Res. 38 (1996) 149-159
46. Woolf N.J. Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 37 (1991) 475-524
47. Xie H.Q., Choi R.C.Y., Leung K.W., Siow N.L., Kong L.W., Lau F.T.C., Peng H.B., and Tsim K.W.K. Regulation of a transcript encoding the proline-rich membrane anchor of globular muscle acetylcholinesterase-the suppressive roles of myogenesis and innervating nerves. J. Biol. Chem. 282 (2007) 11765-11775
48. Xie H.Q., Choi R.C.Y., Leung K.W., Chen V.P., Chu G.K.Y., and Tsim K.W.K. Transcriptional regulation of proline-rich membrane anchor (PRiMA) of globular form acetylcholinesterase in neuron: an inductive effect of neuron differentiation. Brain Res. 1265 (2009) 13-23
49. Zhang W.L., Basile A.S., Gomeza J., Volpicelli L.A., Levey A.I., and Wess J. Characterization of central inhibitory muscarinic autoreceptors by the use of muscarinic acetylcholine receptor knock-out mice. J. Neurosci. 22 (2002) 1709-1717
50. Zimmerman G., and Soreq H. Termination and beyond: acetylcholinesterase as a modulator of synaptic transmission. Cell Tissue Res. 326 (2006) 655-669