Historical landmarks in the histochemistry of the cholinergic synapse: Perspectives for future researches

Biomedical Research

Volumn 31, Issue 1, 2010, Pages 1-12

  Anglade, Philippe ^a   Larabi Godinot, Yamina ^b  

^a Muséum National d'Histoire Naturelle ^*  (France)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ACETYLCHOLINESTERASE; CHOLINE ACETYLTRANSFERASE; NICOTINIC RECEPTOR;

CHOLINERGIC NERVE; CHOLINERGIC SYNAPSE; CHOLINERGIC TRANSMISSION; HISTOCHEMISTRY; HISTORY; HUMAN; MEDICAL RESEARCH; NERVE CONDUCTION; NONHUMAN; REVIEW;

ACETYLCHOLINE; ANIMALS; HISTOCYTOCHEMISTRY; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; NEURONS; SYNAPSES;

VERTEBRATA;

EID: 77749255076     PISSN: 03886107     EISSN: 1880313X     Source Type: Journal    
DOI: 10.2220/biomedres.31.1     Document Type: Review

References (114)

1. Anderson MJ and Cohen MW (1974) Fluorescent staining of acetylcholine receptors in vertebrate skeletal muscle. J Physiol 237, 385-400.
2. Anglade P, Grassi J, Motelica-Heino I, Hashikawa T and Tsuji S (1999) Ultrastructural evidence for dendritic release of acetylcholinesterase in the rat substantia nigra. Folia Histochem Cytobiol 37, 243-247.
3. Anglade P, Michel C, Ozaki T, Tsuji S, Vignon X and Yanaihara N (1988) Simultaneous localization of acetylcholinesterase activity and met-enkephalin, vasoactive intestinal peptide and substance P immunoreactivity in the rat myenteric plexus. Histochem J 20, 464-467.
4. Anglade P and Tsuji S (1997) Hundredth anniversary of the "synapse": I. A short history of the milestones in synapse research. Zool Sci 14, 533-537.
5. Anglade P, Tsuji S, Javoy-Agid F, Agid Y and Hirsch EC (1995) Plasticity of nerve afferents to nigrostriatal neurons in Parkinson's disease. Ann Neurol 37, 265-272.
6. Araque A, Purpura V, Sanzgiri RP and Hydon PG (1999) Tripartite synapse: glia, the unacknowledged partner. Trends Neurosci 22, 208-215.
7. 3H]choline. J Neurosci 1, 691-695.
8. Balasubramanian AS and Bhanumathy CD (1993) Noncholinergic functions of cholinesterases. FASEB J 7, 1354-1358.
9. Bayliss WM (1924) Principles of General Physiology. Longmans and Co, London.
10. Benda P, Tsuji S, Daussant J and Changeux J-P (1970) Localization of acetylcholinesterase by immunofluorescence in eel electroplax. Nature 225, 1149-1150.
11. Berrard S, Brice A, Lottspeich F, Braun A, Barde YA and Mallet J (1987) cDNA cloning and complete sequence of porcine choline acetyltransferase: in vitro translation of the corresponding RNA yields an active protein. Proc Natl Acad Sci USA 84, 9280-9284.
12. Bigbee JW, Sharma KV, Gupta JJ and Dupree JL (1999) Morphogenic role for acetylcholinesterase in axonal outgrowth during neural development. Environ Health Persp (Suppl. 1) 107, 81-87.
13. Bourgeois JP, Tsuji S, Boquet P, Pillot J, Ryter A and Changeux JP (1971) Localization of the cholinergic receptor protein by immunofluorescence in eel electroplax. FEBS Lett 16, 92-94.
14. Brice A, Berrard S, Raynaud B, Ansieau S, Coppola T, Weber MJ and Mallet J (1989) Complete sequence of a cDNA encoding an active rat choline acetyltransferase: a tool to investigate the plasticity of cholinergic phenotype expression. J Neurosci Res 23, 266-273.
15. Brochier G, Israël M and Lesbats B (1993) Immunolabelling of the presynaptic membrane of Torpedo electric organ nerve terminals with an antiserum towards the acetylcholine releasing protein mediatophore. Biol Cell 78, 145-154.
16. Burt AM (1970) A histochemical procedure for the localization of choline acetyltransferase activity. J Histochem Cytochem 18, 408-415.
17. Cartaud J, Sobel A, Rousselet A, Devaux PF and Changeux J-P (1981) Consequence of alkaline-treatment for the ultrastructure of the acetylcholine-receptor-rich-membranes from Torpedo marmorata electric organ. J Cell Biol 90, 418-426.
18. Castro A and Martinez A (2006) Targeting beta-amyloid pathogenesis through acetylcholinesterase inhibitors. Curr Pharma Des 12, 4377-4387.
19. Couteaux R (1947) Contribution à l'étude de la synapse myoneurale. Rev Canad Biol 6, 563-711.
20. Couteaux R and Nachmansohn D (1940) Changes of cholinesterase at end-plates of voluntary muscles following section of sciatic nerve. Proc Soc Exp Biol 43, 177-181.
21. Couteaux R and Pécot-Dechavassine M (1970) Vésicules synaptiques et poches au niveau des "zones actives" de la jonction neuromusculaire. C R Acad Sci Paris 271 (Série D) 2346-2349.
22. Couteaux R and Pécot-Dechavassine M (1974) Les zones spécialisées des membranes présynaptiques. C R Acad Sci Paris 278 (Série D), 291-293.
23. Couteaux R and Taxi J (1952) Recherches histochimiques sur la distribution des activités cholinestérasiques au niveau de la synapse myoneurale. Arch Anat Micr 41, 352-392.
24. Changeux J-P (1990) The TiPs Lecture. The nicotinic acetylcholine receptor: an allosteric protein prototype of ligandgated ion channels. Trends Pharmacol Sci 11, 485-492.
25. Changeux J-P, Kasai M and Lee CY (1970) Use of snake venom toxin to characterize the cholinergic receptor protein. Proc Natl Acad Sci USA 67, 1241-1247.
26. Changeux J-P, Podleski T and Meunier JC (1969) On some structural analogies between acetylcholinesterase and the macromolecular receptor of acetylcholine. J Gen Physiol 54, 225-244.
27. Chiocchetti R, Poole DP, Kimura H, Aimi Y, Robbins HL, Castelucci P and Furness JB (2003) Evidence that two forms of choline acetyltransferase are differentially expressed in subclasses of enteric neurons. Cell Tissue Res 311, 11-22.
28. Dale HH (1914) The action of certain esters and ethers of choline, and their relation to muscarine. J Pharmacol 6, 147-190.
29. Dale HH, Feldberg W and Vogt M (1936) Release of acetylcholine at voluntary motor nerve endings. J Physiol (London) 86, 353-380.
30. De Castro F (1930) Recherches sur la dégénération et la régénération du système nerveux sympathique. Quelques observations sur la constitution des synapses dans les ganglions. Trab Lab Rech Biol (Madrid) 26, 357-456.
31. De Robertis E and Bennett HS (1955) Some features of the submicroscopic morphology of synapses in frog and earthworm. J Biophys Biochem Cytol 1, 47-58.
32. Del Castillo J and Katz B (1955) La base « quantale » de la transmission neuromusculaire. In Microphysiologie comparée des éléments excitables. Colloque Internat. CNRS 67, Paris Gif Yvette, Paris, pp 245-258.
33. Dixon WE (1907) On the mode of action of drugs. Med Magaz (Lond.) 16, 454-457.
34. Du Bois-Reymond E (1848) Untersuchungen über Thierische Electricität. Reimer, Berlin.
35. Dunant Y (2000) Quantal acetylcholine release : vesicle fusion or intramembrane particles ? Microsc Res Tech 49, 38-46.
36. Dunant Y, Gautron J, Israël M, Lesbats B and Manaranche R (1972) Les compartiments d'acétylcholine de l'organe électrique de la torpille et leurs modifications par la stimulation. J Neurochem 19, 1987-2002.
37. Dvir H, Harel M, Bon S, Liu WQ, Vidal M, Garbay C, Sussman JL, Massoulié J and Silman I (2004) The synaptic acetylcholinesterase tetramer assembles around a polyproline II helix. EMBO J 23, 4394-4405.
38. Eccles JC (1937) Synaptic and neuromuscular transmission. Physiol Rev 17, 538-555.
39. Ehrlich P (1909) Ueber den jetzigen Stand der Chemotherapie. Ber Dtsch Chem Ges 42, 17-47.
40. Elliott TR (1904) On the action of adrenalin. J Physiol (Lond.) 31, 20.
41. Engert F and Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70.
42. Fatt P and Katz B (1952) Spontaneous subthreshold activity at motor nerve endings. J Physiol (London) 117, 109-128.
43. Feng TP and Ting YC (1938) Studies on the neuromuscular junction. XI. A note on the local concentration of the cholinesterase at the motor nerve endings. Chinese J Physiol 13, 141-144.
44. Friedenberg RM and Seligman AM (1972) Acetylcholinesterase at the myoneural junction: cytochemical ultrastructure and some biochemical considerations. J Histochem Cytochem 20, 771-792.
45. Geffard M, McRae-Degueurce A and Souan ML (1985) Immunocytochemical detection of acetylcholine in the rat central nervous system. Science 229, 77-79.
46. Golgi C (1885) Sulla fina anatomia degli organi centrali del sistema nervoso, « Revista sperimentale di Freniatria ». Reprint. in Golgi C., Opera omnia (1903), Hoepli, Milano.
47. Golgi C (1891) Le réseau nerveux diffus des centres du système nerveux. Ses attributs physiologiques. Méthodes suivies dans les recherches histologiques. Arch Ital Biol 15, 434-463.
48. Hanker JS, Thornburg LP, Yates PE and Moore HG (1973) The demonstration of cholinesterases by the formation of osmium blacks at the site of Hatchett's brown. Histochemistry 37, 223-242.
49. Hirai K, Katayama Y, Peltre G and Tsuji S (2008) Ultrastructural visualization of the transmembranous and cytomatrix-related part of nicotinic acetylcholine receptor of frog motor endplate by means of an immunochemical avidity of IgG for d- tubocurarine. Folia Histochem Cytobiol 46, 111-116.
50. Hoover DB, Ganote CE, Ferguson SM, Blakely RD and Parsons RL (2004) Localization of cholinergic innervation in guinea pig heart by immunocytochemistry for high-affinity choline transporter. Cardiovasc Res 62, 112-121.
51. Houser CR (1990) cholinergic synapses in the central nervous system: studies of the immunocytochemical localization of choline acetyltransferase. J Electron Microsc Tech 15, 2-19.
52. Hunt R and Taveau M (1906) On the physiological action of certain cholin derivatives and new method for detecting cholin. Brit Med J 2, 1788-1789.
53. Hütter G and Luppa H (1976) The histochemical demonstration of choline acetyltransferase by semipermeable membrane technique. Histochemistry 49, 303-307.
54. Ishii K, Hayashida T, Hashikawa T and Tsuji S (2004) Dendritic spinules in rat nigral neurons revealed by acetylcholinesterase immunocytochemistry and serial sections of the dendritic spine heads. Folia Histochem Cytobiol 42, 77-81.
55. Israël M and Dunant Y (1996) A unifying hypothesis for acetylcholine release. Neurochem Int 28, 1-9.
56. Israël M and Dunant Y (1999) Mediatophore, a protein supporting quantal acetylcholine release. Can J Physiol Pharmacol 77, 689-698.
57. Israël M, Dunant Y and Manaranche R. (1979) The present status of the vesicular hypothesis. Prog Neurobiol 13, 237-275.
58. Karnovsky MJ and Roots L (1964) A "direct-coloring" thiocholine method for cholinesterases. J Histochem Cytochem 12, 219-221.
59. Kasa P, Mann SP and Hebb C (1970) Localization of choline acetyltransferase: histochemistry at the light microscope level. Nature 226, 812-814.
60. Kasai M and Changeux J-P (1970) Démonstration de l'excitation par des agonistes cholinergiques à partir des fractions de membranes purifiées, in vitro. C R Acad Sci Paris 270, 1400-1403.
61. Koelle GB and Friedenwald JS (1949) A histochemical method for localizing cholinesterase activity. Proc Soc Exp Biol Med 70, 617-622.
62. Kordeli E (2000) Introduction to organization of the neuromuscular junction: from structure to function. Microsc Res Tech 49, 1-2.
63. Kriebel ME, Llados F and Matteson DR (1976) Spontaneous subminiature end-plate potentials in mouse diaphragm muscle evidence for synchronous release. J Physiol (Lond.) 262, 553-581.
64. Kuhar MJ (1979) Sodium-dependent high affinity choline uptake. In: The Cholinergic Synapse (Tucek S, ed.), Progress in Brain Research vol. 49, Elsevier, Amsterdam.
65. Kumari S, Borroni V, Chaudhry A, Chanda B, Massol R, Mayor S and Barrantes FJ (2008) Nicotinic acetylcholine receptor is internalized via a Rac-dependent, dynaminindependent endocytic pathway. J Cell Biol 181, 1179-1193.
66. Lane RM, Kivipelto M and Greig NH (2004) Acetylcholinesterase and its inhibition in Alzheimer disease. Clin Neuro Pharmacol 27, 141-149.
67. Lehrer GM and Ornstein L (1959) A diazo coupling method for the electron microscopic localization of cholinesterase. J Bioph Biochem Cytol 6, 399-406.
68. Leuzinger W, Baker AL and Cauvin E (1968) Acetylcholinesterase, II. Crystallization, absorption spectra, isoionic point. Proc Natl Acad Sci USA 59, 620-623.
69. Lipman F, Novelli GD, Tuttle LC and Guirard BM (1947) Coenzyme for acetylation, a pantothenic acid derivative. J Biol Chem 167, 869-870.
70. Loewi O (1921) Ueber humorale Uebertrakbarkeit der Herznervenwirkung (II. Mitteillung). Pflüg Arch Ges Physiol 193, 201-213.
71. Loewi O and Navratil E (1926) Über humorale Übertragbarkeit der Herznervenwirkung. XI. Über den Mechanismus der Vaguswirkung von Physostigmin und Ergotamin. Pflüg Arch Ges Physiol 214, 689-696.
72. MacDonald F (1950) An investigation of the histochemical technique for the localization of acid phosphomonoesterase. Quart J Microsc Sci 91, 315-330.
73. MacMahan UJ, Sanes JR and Marshall LM (1978) Cholinesterase is associated with the basal lamina at the neuromuscular junction. Nature 271, 172-174.
74. Marnay A and Nachmansohn D (1937) Sur la récupération de la cholinestérase dans le muscle couturier de la grenouille. C R Soc Biol 125, 41-43.
75. Massoulié J (2002) The origin of the molecular diversity and functional anchoring of cholinesterases. Neurosignals 11, 130-143.
76. Massoulié J, Pezzementi L, Bon S, Krejci E and Vallette FM (1993) Molecular and cellular biology of cholinesterases. Prog Neurobiol 41, 31-91.
77. Massoulié J, Rieger F and Bon S (1971) Espèces acétylcholinestérasiques globulaires et alongées des organiques électriques de Poisson. Eur J Biochem 21, 542-551.
78. Matsuo A, Bellier J-P, Hisano T, Aimi Y, Yasuhara O, Tooyama I, Saito N and Kimura H (2005) Rat choline acetyltransferase of the peripheral type differs from that of the common type in intracellular translocation. Neurochem Int 46, 423-433.
79. Menten ML, Junge J and Green MH (1944) A coupling histochemical azo-dye test for alkaline phosphatase in the kidney. J Biol Chem 153, 471-477.
80. Motelica-Heino I and Wernig A (1978) Further investigation on the quantal subunit at the frog neuromuscular junction. J Physiol (Lond.) 284, 142.
81. Nachmansohn D and Machado AL (1943) The formation of acetylcholine. A new enzyme "choline acetylase". J Neurophysiol 6, 397-403.
82. Noda M, Shimizu S, Tanabe T, Takai T, Kayono T, Ikeda T, Takahashi H, Nakayama H, Kanaoka Y, Minamino N, Kangawa K, Matsuo H, Raftery MA, Hirose T, Inayama S, Hayashida H, Miyata T and Numa S (1984) Primary structure of Electrophorus electricus sodium channel deduced from cDNA sequence. Nature 312, 121-127.
83. Oda Y (1999) Choline acetyltransferase: the structure, distribution and pathologic changes in the central nervous system. Pathol Int 49, 921-937.
84. Ohoka T and Tsuji S (1988) Specificity of ionic fixation with silicotungstic acid for cytochemical localization and identification of acetylcholine in synaptic vesicles. Biomed Res 9, 335-341.
85. Palade GE and Palay SL (1954) Electron microscope observations of interneuronal and neuromuscular synapses. Anat Rec 118, 335-336.
86. Parnavelas JG, Kelly W and Burnstock G (1985) Ultrastructural localization of choline acetyltransferase in vascular endothelial cells in rat brain. Nature 316, 724-725.
87. Ramon y Cajal (1890) Réponse à Mr. Golgi à propos des fibrilles collatérales de la moëlle épinière, et de la structure générale de la substance grise. Anat Anz 5, 579- 587.
88. Rees TM and Brimijoin S (2003) The role of acetylcholinesterase in the pathogenesis of Alzheimer's disease. Drugs Today 39, 75-83.
89. Robertson JD (1956) The ultrastructure of a reptilian myoneuronal junction. J Biophys Biochem Cytol 2, 381-394.
90. Shepherd GM and Erulkar SD (1997) Centenary of the synapse: from Sherrington to the molecular biology of the synapse and beyond. Trends Neurosci 20, 385-392.
91. Sherrington CS (1897) The central nervous system. In: A Text Book of Physiology, 7th ed, Part III, p.929, M. Foster, London.
92. Silman I and Sussman JL (2005) Acetylcholinesterase: " classical" and "non-classical" functions and pharmacology. Curr Opin Pharmacol 5, 293-302.
93. Silver A (1974) The Biology of Cholinesterases. North Holland, Amsterdam.
94. Sobel A, Weber M and Changeux J-P (1977) Large-scale purification of the acetylcholine-receptor protein in its membrane-bound detergent-extracted forms from Torpedo marmorata electric organ. Eur J Biochem 80, 215-224.
95. Tago H, Kimura H and Maeda T (1986) Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure. J Histochem Cytochem 34, 1431-1438.
96. Taxi J (1965) Contribution à ĺtude des connexions des neurones moteurs du système nerveux autonome. Ann Sci Nat Zool 7, 413-674.
97. Trifonov S, Houtani T, Hamada S, Kase M, Maruyama M and Sugimoto T (2009) In situ hybridization study of the distribution of choline acetyltransferase mRNA and its splice variants in the mouse brain and spinal cord. Neuroscience 159, 344-357.
98. Tsuji S (1974) On the chemical basis of thiocholine methods for demonstration of acetylcholinesterase activities. Histochemistry 42, 99-110.
99. Tsuji S (1985) Ultracytochemical localization of acetylcholine-like cations in excited motor end-plates by means of ionic fixation. Histochemistry 83, 213-219.
100. Tsuji S (1998) Electron microscopic localization of acetylcholinesterase activity in the central nervous system: chemical basis of a catalytic activity of Hatchett's brown (cupric ferrocyanide) precipitate revealed by 3,3′-diaminobenzidine. Folia Histochem Cytobiol 36, 67-70.
101. Tsuji S (2006) René Couteaux (1909-1999) and the morphological identification of synapes. Bio Cell 98, 503-509.
102. Tsuji S, Alameddine HS, Nakanishi S and Ohoka T (1983) Molybdic and Tungstic heteropolyanions for "ionic fixation" of acetylcholine in cholinergic nerve terminals. Histochemistry 77, 51-56.
103. Tsuji S and Anglade P (1997) Hundredth anniversary of the « synapse »: II. Study of the cholinergic synapse. Zool Sci 14, 539-548.
104. Tsuji S and Larabi Y (1983) A modification of thiocholine-ferricyanide method of Karnovsky and Roots for localization of acetylcholinesterase activity without interference by Koelle's copper thiocholine iodide precipitate. Histochemistry 78, 317-323.
105. Tsuji S and Motelica-Heino I (1993) Further studies on electron microscopic localization of acetylcholine-like cations in frog neuromuscular junctions. Acta Histochem Cytochem 26, 577-582.
106. 3H] choline by fibrocytes of frog motor endplate region. Proc Japan Acad 73, 158-160.
107. 3H] choline after retrograde axonal transport. Proc Japan Acad 68, 145-149.
108. Tsuji S, Nakatomi R, Tsuchiya H, Hirai K, Katayama Y, Motelica-Heino I and Hashikawa T (2002) Perineuronal surface acetylcholinesterase activity of a fine neural network stained histochemically and observed with backscattered electron imaging and X-ray mapping methods. Brain Res Protocols 9, 16-22.
109. Tsuji S and Tobin-Gros C (1980) A simple silver nitrate impregnation of nerve fibers with preservation of acetylcholinesterase activity at the motor end-plate. Experientia 36, 1317-1319.
110. Tsuji S, Tooyama I, Kato T, Peltre G and Kimura H (2003) Binding avidity of immunoglobulin G for acetylcholine. Biomed Res 24, 217-221.
111. Unwin N (2000) The Croonian lecture 2000. Nicotinic acetylcholine receptor and the structural basis of fast synaptic transmission. Phil Trans R Soc Lond B Biol Sci 335, 1813-1829.
112. Unwin N (2005) Refined structure of the nicotinic acetylcholine receptor at 4 Å resolution. J Mol Biol 346, 967-989.
113. Yasuhara O, Matsuo A, Bellier J-P and Aimi Y (2007) Demonstration of choline acetyltransferase of a peripheral type in the rat heart. J Histochem Cytochem 55, 287-299.
114. Zhang XJ, Yang L, Zhao Q, Caen JP, He HY, Jin QH, Guo LH, Alemany M, Zhang LY and Shi YF (2002) Induction of acetylcholinesterase expression during apoptosis in various cell types. Cell Death Diff 9, 790-800.