The cholinergic gene locus

Journal of Neurochemistry

Volumn 70, Issue 6, 1998, Pages 2227-2240

  Eiden, Lee E ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Acetylcholine; Choline acetyltransferase; Cholinergic gene; Vesicular acetylcholine transporter

Indexed keywords

ACETYLCHOLINE RELEASE; GENE EXPRESSION; GENE LOCUS; HUMAN; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; SYNAPSE VESICLE;

ANIMALIA; MAMMALIA;

EID: 0031745813     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1998.70062227.x     Document Type: Short Survey

References (139)

1. Aigner T. G. and Mishkin M. (1986) The effects of physostigmine and scopolamine on recognition memory in monkeys. Behav. Neural Biol. 45, 81-87.
2. Alfonso A., Grundahl K., Duerr J. S., Han H.-P., and Rand J. B. (1993) The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter. Science 261, 617-619.
3. Alfonso A., Grundahl K., McManus J. R., Asbury J. M., and Rand J. B. (1994) Alternative splicing leads to two cholinergic proteins in C. elegans. J. Mol. Biol. 241, 627-630.
4. Amara S. G. and Kuhar M. J. (1993) Neurotransmitter transporters: recent progress. Annu. Rev. Neurosci. 16, 73-93.
5. 3H-acetylcholine by Torpedo electric organ synaptic vesicles. Biochemistry 21, 3037-3043.
6. Andres C., Beeri R., Friedman A., Lev-Lehman E., Henis S., Timberg R., Shani M., and Soreq H. (1997) Acetylcholinesterase-transgenic mice display embryonic modulations in spinal cord choline acetyltransferase and neurexin Iβ gene expression followed by late-onset neuromotor deterioration. Proc. Natl. Acad. Sci. USA 94, 8173-8178.
7. Armstrong D. M., Saper C. B., Levey A. I., Wainer B. H., and Terry R. D. (1983) Distribution of cholinergic neurons in rat brain demonstrated by the immunocytochemical localization of choline acetyltransferase. J. Comp. Neurol. 216, 53-68.
8. Arvidsson U., Riedl M., Eide R., and Meister B. (1997) Vesicular acetylcholine transporter (VAChT) protein: a novel and unique marker for cholinergic neurons in the central and peripheral nervous systems. J. Comp. Neurol. 378, 454-467.
9. Augustinsson K. B. and Nachmansohn D. (1949) Distinction between acetylcholine-esterase and other choline ester-splitting enzymes. Science 110, 98-99.
10. Bajjalieh S. M., Peterson K., Shinghal R., and Scheller R. H. (1992) SV2, a brain synaptic vesicle protein homologous to bacterial transporters. Science 257, 1271-1273.
11. Barber R. P., Phelps P. E., Houser C. R., Crawford G. D., Salvaterra P. M., and Vaughn J. E. (1984) The morphology and distribution of neurons containing choline acetyltransferase in the adult rat spinal cord: an immunocytochemical study. J. Comp. Neurol. 229, 329-346.
12. 3H] acetylcholine in the presence of vesamicol. J. Neurochem. 69, 2608-2611.
13. Baskin F., Li Y.-P., Hersh L. B., Davis R. M., and Rosenberg R. N. (1997) An AP-2 binding sequence within exon 1 of human and porcine choline acetyltransferase genes enhances transcription in neural cells. Neuroscience 76, 821-827.
14. Beeri R., Andres C., Lev-Lehman E., Timberg R., Huberman T., Shani M., and Soreq H. (1995) Transgenic expression of human acetylcholinesterase induces progressive cognitive deterioration in mice. Curr. Biol. 5, 1063-1071.
15. Bejanin S., Habert E., Berrard S., Edwards J.-B. D. M., Loeffler J.-P., and Mallet J. (1992) Promoter elements of the rat choline acetyltransferase gene allowing nerve growth factor inducibility in transfected primary cultured cells. J. Neurochem. 58, 1580-1583.
16. Bejanin S., Cervini R., Mallet J., and Berrard S. (1994) A unique gene organization for two cholinergic markers, choline acetyl-transferase and a putative vesicular transporter of acetylcholine. J. Biol. Chem. 269, 21944-21947.
17. Berrard S., Varoqui H., Cervini R., Israël 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.
18. Berse B. and Blusztajn J. K. (1995) Coordinated up-regulation of choline acetyltransferase and vesicular acetylcholine transporter gene expression by the retinoic acid receptor alpha, cAMP, and leukemia inhibitory factor/ciliary neurotrophic factor signaling pathways in a murine septal cell line. J. Biol. Chem. 270, 22101-22104.
19. Bird T. D., Stranahan S., Sumi S. M., and Raskind M. (1983) Alzheimer's disease: choline acetyltransferase activity in brain tissue from clinical and pathological subgroups. Ann. Neurol. 14, 284-293.
20. Brownstein M. J. and Hoffman B. J. (1993) Neurotransmitter transporters. Recent Prog. Horm. Res. 49, 27-42.
21. Brownstein M., Kobayashi R., Palkovits M., and Saavedra J. M. (1975) Choline acetyltransferase levels in diencephalic nuclei of the rat. J. Neurochem. 24, 35-38.
22. Brownstein M. J., Palkovits M., Tappaz M. L., Saavedra J. M. and Kizer J. S. (1976) Effect of surgical isolation of the hypothalamus on its neurotransmitter content. Brain Res. 117, 287-295.
23. Bruce G., Wainer B. H., and Hersh L. B. (1985) Immunoaffinity purification of human choline acetyltransferase: comparison of the brain and placental enzymes. J. Neurochem. 45, 611-620.
24. Butcher L. L., Oh J. D., Woolf N. J., Edwards R. H., and Roghani A. (1992) Organization of central cholinergic neurons revealed by combined in situ hybridization histochemistry and choline-O-acetyltransferase immunocytochemistry. Neurochem. Int. 21, 429-445.
25. Butcher L. L., Oh J. D., and Woolf N. J. (1993) Cholinergic neurons identified by in situ hybridization histochemistry. Prog. Brain Res. 98, 1-8.
26. Carson K. A., Nemeroff C. B., Rone M. S., Youngblood W. W., Prange A. J. J., Hanker J. S., and Kizer J. S. (1977) Biochemical and histochemical evidence for the existence of a tuberoinfundibular cholinergic pathway in the rat. Brain Res. 129, 169-173.
27. Cervini R., Houhou L., Pradat P.-F., Bejanin S., Mallet J., and Berrard S. (1995) Specific vesicular acetylcholine transporter promoters lie within the first intron of the rat choline acetyltransferase gene. J. Biol. Chem. 270, 24654-24657.
28. Chireux M. A., Le Van Thai A., and Weber M. J. (1995) Human choline acetyltransferase gene: localization of alternative first exons. J. Neurosci. Res. 40, 427-438.
29. Chong J. A., Tapia-Ramirez J., Kim S., Toledo-Arai J. J., Zheng Y., Boutros M. C., Altshuller Y. M., Frohman M. A., Kraner S. D., and Mandel G. (1995) REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80, 949-957.
30. Collier B., Tandon A., Prado M. A. M., and Bachoo M. (1993) Storage and release of acetylcholine in a sympathetic ganglion. Prog. Brain Res. 98, 183-189.
31. Coyle J. T., Price D. L., and DeLong M. R. (1983) Alzheimer's disease: a disorder of cortical cholinergic innervation. Science 219, 1184-1190.
32. Darchen F., Scherman D., Desnos C., and Henry J.-P. (1988) Characteristics of the transport of the quaternary ammonium 1-methyl-4-phenylpyridinium by chromaffin granules. Biochem. Pharmacol. 37, 4381-4387.
33. Davies P. and Maloney M. R. (1976) Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 2, 1403.
34. Eckenstein F. and Baughman R. W. (1984) Two types of cholinergic innervation in cortex, one co-localized with vasoactive intestinal polypeptide. Nature 309, 153-155.
35. Eckenstein F. and Baughman R. W. (1987) The anatomical organization of the cholinergic system in the cerebral cortex, in The Cerebral Cortex, Vol. 6 (Peters A. and Jones E. G., eds), pp. 129-160. Plenum, New York.
36. Eckenstein F. and Sofroniew M. V. (1983) Identification of central cholinergic neurons containing both choline acetyltransferase and acetylcholinesterase and of central neurons containing only acetylcholinesterase. J. Neurosci. 3, 2286-2291.
37. Eckenstein F. and Thoenen H. (1983) Cholinergic neurons in the rat cerebral cortex demonstrated by immunohistochemical localization of choline acetyltransferase. Neurosci. Lett. 36, 211-215.
38. Emre M., Heckers S., Mash D. C., Geula C., and Mesulam M.-M. (1993) Cholinergic innervation of the amygdaloid complex in the human brain and its alterations in old age and Alzheimer's disease. J. Comp. Neurol. 336, 117-134.
39. Erickson J. D., Eiden L. E., and Hoffman B. (1992) Expression cloning of a reserpine-sensitive vesicular monoamine transporter. Proc. Natl. Acad. Sci. USA 89, 10993-10997.
40. Erickson J. D., Varoqui H., Schäfer M., Diebler M.-F., Weihe E., Modi W., Rand J., Eiden L. E., Bonner T. I., and Usdin T. (1994) Functional characterization of the mammalian vesicular acetylcholine transporter and its expression from a "cholinergic" gene locus. J. Biol. Chem. 269, 21929-21932.
41. Erickson J. D., Weihe E., Schäfer M. K.-H., Neale E., Williamson L., Bonner T. I., Tao-Cheng J.-H., and Eiden L. E. (1996) The VAChT/ChAT "cholinergic gene locus": new aspects of genetic and vesicular regulation of cholinergic function, in Cholinergic Mechanisms: From Molecular Biology to Clinical Significance, Vol. 109 (Klein J. and Löffelholz K., eds), pp. 69-82. Elsevier, Amsterdam.
42. Feany M. B., Lee S., Edwards R. H., and Buckley K. M. (1992) The synaptic vesicle protein SV2 is a novel type of transmembrane transporter. Cell 70, 861-867.
43. Fischer W., Wictorin K., Bjorklund A., Williams L. R., Varon S., and Gage F. H. (1987) Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 329, 65-68.
44. Frisby D., McManus J., Duerr J., and Rand J. (1996) Regulation of cholinergic gene expression in C. elegans. Soc. Neurosci. Abstr. 22, 1032.
45. Furness J. B., Costa M., and Eckenstein F. (1983) Neurons localized with antibodies against choline acetyltransferase in the enteric nervous system. Neurosci. Lett. 40, 105-109.
46. Giacobini E. (1990) The cholinergic system in Alzheimer disease, in Progress in Brain Research, Vol. 84 (Aquilonius S.-M. and Gillberg P.-G., eds), pp. 321-332. Elsevier; Amsterdam.
47. Gilmor M. L., Nash N. R., Roghani A., Edwards R. H., Yi H., Hersch S. M., and Levey A. I. (1996) Expression of the putative vesicular acetylcholine transporter in rat brain and localization in cholinergic synaptic vesicles. J. Neurosci. 16, 2179-2190.
48. Grant M. P., Francis N. J., and Landis S. C. (1995) The role of acetylcholine in regulating secretory responsiveness. Mol. Cell. Neurosci. 6, 32-42.
49. +-dependent creatine transporter in rabbit brain, muscle, heart, and kidney. J. Biol. Chem. 268, 8418-8421.
50. Hahm S. H., Chen L., Patel C., Erickson J., Bonner T. I., Weihe E., Schäfer M. K.-H., and Eiden L. E. (1997) The human cholinergic gene locus: upstream sequencing, in vivo transcription patterns, and role of the NRSE/RE-1 and other control elements in VAChT expression. J. Mol. Neurosci. 9, 223-236.
51. Hahn M., Hahn S. L., Stone D. M., and Joh T. H. (1992) Cloning of the rat gene encoding choline acetyltransferase, a cholinergic neuron-specific marker. Proc. Natl. Acad. Sci. USA 89, 4387-4391.
52. Haigh J. R., Noremberg K., and Parsons S. M. (1994) Acetylcholine active transport by rat brain synaptic vesicles. Neuroreport 5, 773-776.
53. Henke H. and Lang W. (1983) Cholinergic enzymes in neocortex, hippocampus and basal forebrain of non-neurological and senile dementia of Alzheimer-type patients. Brain Res. 267, 281-291.
54. Hersh L. B., Kong C. F., Sampson C., Mues G., Li Y.-P., Fisher A., Hilt D., and Baetge E. E. (1993) Comparison of the promoter region of the human and porcine choline acetyltransferase genes: localization of an important enhancer region. J. Neurochem. 61, 306-314.
55. Holler T., Berse B., Cermak J. M., Diebler M.-F., and Blusztajn J. K. (1996) Differences in the developmental expression of the vesicular acetylcholine transporter and choline acetyltransferase in the rat brain. Neurosci. Lett. 212, 107-110.
56. Houser C. R., Crawford G. D., Barber R. P., Salvaterra P. M., and Vaughn J. E. (1983) Organization and morphological characteristics of cholinergic neurons: an immunocytochemical study with a monoclonal antibody to choline acetyltransferase. Brain Res. 266, 97-119.
57. Ibanez C. F. and Persson H. (1991) Localization of sequences determining cell type specificity and NGF responsiveness in the promoter region of the rat choline acetyltransferase gene. Eur. J. Neurosci. 3, 1309-1315.
58. Ibanez C., Pelto F., Huikko M., Soder O., Ritzen E. M., and Hersh L. B. (1991a) Expression of choline acetyltransferase mRNA in spermatogenic cells results in an accumulation of the enzyme in the postacrosomal region of mature spermatozoa. Proc. Natl. Acad. Sci. USA 88, 3676-3680.
59. Ibanez C. F., Ernfors P., and Persson H. (1991b) Developmental and regional expression of choline acetyltransferase mRNA in the rat central nervous system. J. Neurosci. Res. 29, 163-171.
60. Ichikawa T., Ajiki K., Matsuura J., and Misawa H. (1997) Localization of two cholinergic markers, choline acetyltransferase and vesicular acetylcholine transporter in the central nervous system of the rat: in situ hybridization histochemistry and immunohistochemistry. J. Chem. Neuroanat. 13, 23-39.
61. Israël M. and Dunant Y. (1993) Acetylcholine release, from molecules to function, in Progress in Brain Research, Vol. 98 (Cuello A. C., ed), pp. 219-233. Elsevier, Amsterdam.
62. Israël M., Lesbats B., Syngublakis M., and Joliot A. (1994) Acetylcholine accumulation and release by hybrid NG108-15, glioma, and neuroblastoma cells-role of a 16 kDa membrane protein in release. Neurochem. Int. 25, 103-109.
63. Jacob F. and Monod J. (1961) Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 3, 318-356.
64. Johnson R. G. Jr. (1988) Accumulation of biological amines into chromaffin granules: a model for hormone and neurotransmitter transport. Physiol. Rev. 68, 232-307.
65. Kaback H. R. (1997) A molecular mechanism for energy coupling in a membrane transport protein, the lactose permease of Escherichia coli. Proc. Natl. Acad. Sci. USA 94, 5539-5543.
66. Kitamoto T. and Salvaterra P. M. (1995) A POU homeo domain protein related to dPOU-19/pdm-1 binds to the regulatory DNA necessary for vital expression of the Drosophila choline acetyltransferase gene. J. Neurosci. 15, 3509-3518.
67. Kitamoto T., Ikeda K., and Salvaterra P. M. (1995) Regulation of choline acetyltransferase/lacZ fusion gene expression in putative cholinergic neurons of Drosophila melanogaster. J. Neurobiol. 28, 70-81.
68. Kitamoto T., Wang W., and Salvaterra P. M. (1998) Structure and organization of the Drosophila cholinergic locus. J. Biol. Chem. 273, 2706-2713.
69. Knapp M. J., Knopman D. S., Solomon P. R., Pendlebury W. W., Davis C. S., and Gracon S. I. (1994) A 30-week randomized controlled trial of high-dose tacrine in patients with Alzheimer's disease. JAMA 271, 985-991.
70. Krantz D. E., Peter D., Liu Y., and Edwards R. H. (1997) Phosphorylation of a vesicular monoamine transporter by casein kinase II. J. Biol. Chem. 272, 6752-6759.
71. Landis S. C. (1990) Target regulation of neurotransmitter phenotype. Trends Neurosci. 13, 344-350.
72. Levey A. I. (1996) Muscarinic acetylcholine receptor expression in memory circuits: implications for treatment of Alzheimer disease. Proc. Natl. Acad. Sci. USA 93, 13541-13546.
73. Li Y.-P., Baskin F., Davis R., and Hersh L. B. (1993) Cholinergic neuron-specific expression of the human choline acetyltransferase gene is controlled by silencer elements. J. Neurochem. 61, 748-751.
74. Li Y.-P., Baskin F., Davis R., Wu D., and Hersh L. B. (1995) A cell type-specific silencer in the human choline acetyltransferase gene requiring two distinct and interactive E boxes. Mol. Brain Res. 30, 106-114.
75. Loewi O. (1921) Uber humorale Ubertragbarkeit der Hirzenwickung. Pflugers Arch. 189, 239-242.
76. Lönnerberg P., Lendahl U., Funakoshi H., Arhlund-Richter L., Persson H., and Ibanez C. F. (1995) Regulatory region in choline acetyltransferase gene directs developmental and tissue-specific expression in transgenic mice. Proc. Natl. Acad. Sci. USA 92, 4046-4050.
77. Lönnerberg P., Schoenherr C. J., Anderson D. J., and Ibanez C. F. (1996) Cell type-specific regulation of choline acetyltransferase gene expression. Role of the neuron-restrictive silencer element and cholinergic-specific enhancer sequences. J. Biol. Chem. 271, 33358-33365.
78. Maas W. K., Maas R., Wiame J. M., and Glansdorff N. (1964) Studies on the mechanism of repression of arginine biosynthesis in Escherichia coli. I. Dominance of repressibility in zygotes. J. Mol. Biol. 8, 359-364.
79. Merickel A., Kaback H. R., and Edwards R. H. (1997) Charged residues in transmembrane domains II and XI of a vesicular monoamine transporter form a charge pair that promotes high affinity substrate recognition. J. Biol. Chem. 272, 5403-5408.
80. Mesulam M.-M. (1990) Human brain cholinergic pathways in Progress in Brain Research, Vol. 84 (Aquilonius S.-M. and Gillberg P.-G., eds), pp. 231-241. Elsevier, Amsterdam.
81. Mesulam M.-M., Mufson E. J., Levey A. I., and Wainer B. H. (1984) Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience 12, 669-686.
82. Michaelson D. M. and Angel I. (1981) Saturable acetylcholine transport into purified cholinergic synaptic vesicles. Proc. Natl. Acad. Sci. USA 78, 2048-2052.
83. Misawa H., Takahashi R., and Deguchi T. (1994) Calcium-independent release of acetylcholine from stable cell lines expressing mouse choline acetyltransferase cDNA. J. Neurochem. 62, 465-470.
84. Misawa H., Takahashi R., and Deguchi T. (1995) Coordinate expression of vesicular acetylcholine transporter and choline acetyltransferase in sympathetic superior cervical neurones. Neuroreport 6, 965-968.
85. Misawa H., Matsuura J., Oda Y., Takahashi R., and Deguchi T. (1997) Human choline acetyltransferase mRNAs with different 5′-region produce a 69-kDa major translation product. Mol. Brain Res. 44, 323-333.
86. Morales M. A., Holmberg K., Xu Z. Q., Cozzari C., Hartman B. K., Emson P., Goldstein M., Elfvin L.-G., and Hökfelt T. (1995) Localization of choline acetyltransferase in rat peripheral sympathetic neurons and its coexistence with nitric oxide synthase and neuropeptides. Proc. Natl. Acad. Sci. USA 92, 11819-11823.
87. Nachmansohn D. and Machado A. L. (1943) The formation of acetylcholine. A new enzyme choline acetylase. J. Neurophysiol. 6, 397-403.
88. Naciff J. M., Misawa H., and Dedman J. R. (1997) Molecular characterization of the mouse vesicular acetylcholine transporter gene. Neuroreport 8, 3467-3473.
89. Nguyen M. L. and Parsons S. M. (1996) Interactions of protons with the acetylcholine transporter of synaptic vesicles. Prog. Brain Res. 109, 97-103.
90. Nirenberg M. J., Liu Y., Peter D., Edwards R. H., and Pickel V. M. (1995) The vesicular monoamine transporter 2 is present in small synaptic vesicles and preferentially localizes to large dense core vesicles in rat solitary tract nuclei. Proc. Natl. Acad. Sci. USA 92, 8773-8777.
91. Njus D., Kelley P. M., and Harnadek G. J. (1986) Bioenergetics of secretory vesicles. Biochim. Biophys. Acta 853, 237-265.
92. Oda Y., Nakanishi I., and Deguchi T. (1992) A complementary DNA for human choline acetyltransferase induces two forms of enzyme with different molecular weights in cultured cells. Mol. Brain Res. 16, 287-294.
93. Oda Y., Murioshi Y., and Nakanishi I. (1996) Translation initiation sites and relative activity of large and small forms of human choline acetyltransferase. Mol. Brain Res. 38, 135-138.
94. Parsons S. M., Prior C., and Marshall I. G. (1993) Acetylcholine transport, storage, and release. Int. Rev. Neurobiol. 35, 279-390.
95. Paxinos G. and Butcher L. L. (1985) Organizational principles of the brain as revealed by choline acetyltransferase and acetylcholinesterase distribution and projections, in The Rat Nervous System, Vol. 1 (Paxinos G., ed), pp. 487-521. Academic Press, New York.
96. Perry E. K., Perry R. H., Blessed G., and Tomlinson B. E. (1977) Necropsy evidence of central cholinergic deficits in senile dementia. Lancet 1, 189.
97. Perry E. K., Tomlinson B. E., Blessed G., Bergman K., Gibson P. H., and Perry R. H. (1978) Correlation of cholinergic abnormalities with senile plaques and mental test-scores in senile dementia. Br. Med. J. 2, 1457-1459.
98. Porter A. J., Wattchow D. A., Brookes S. J., Schemann M., and Costa M. (1996) Choline acetyltransferase immunoreactivity in the human small and large intestine. Gastroenterology 111, 401-408.
99. Rand J. B. (1989) Fine-structure genetic analysis of the cha-1-unc-17 gene complex in Caenorhabditis. Genetics 122, 73-80.
100. Rand J. B. and Russell R. L. (1984) Choline acetyltransferase-deficient mutants of the nematode Caenorhabditis elegans. Genetics 106, 227-248.
101. Regnier-Vigouroux A. and Huttner W. B. (1993) Biogenesis of small synaptic vesicles and synaptic-like microvesicles. Neurochem. Res. 18, 59-64.
102. Roghani A., Feldman J., Kohan S. A., Shirzadi A., Gundersen C. B., Brecha N., and Edwards R. H. (1994) Molecular cloning of a putative vesicular transporter for acetylcholine. Proc. Natl. Acad. Sci. USA 91, 10620-10624.
103. Roghani A., Shirzadi A., Butcher L. L., and Edwards R. H. (1998) Distribution of the vesicular transporter for acetylcholine in the rat central nervous system. Neuroscience 82, 1195-1212.
104. 3H]vesamicol binding in the temporal cortex of patients with Alzheimer's disease, Parkinson's disease, and rats with basal forebrain lesions. Neuroscience 35, 327-333.
105. Schäfer M. K.-H., Weihe E., Varoqui H., Eiden L. E., and Erickson J. D. (1994) Distribution of the vesicular acetylcholine transporter (VAChT) in the central and peripheral nervous systems of the rat. J. Mol. Neurosci. 5, 1-18.
106. Schäfer M. K.-H., Weihe E., Erickson J. D., and Eiden L. E. (1995) Human and monkey cholinergic neurons visualized in paraffin-embedded tissues by immunoreactivity for VAChT, the vesicular acetylcholine transporter. J. Mol. Neurosci. 6, 225-235.
107. Schäfer M. K.-H., Schütz B., Weihe E., and Eiden L. E. (1997) Target-independent cholinergic differentiation in the rat sympathetic nervous system. Proc. Natl. Acad. Sci. USA 94, 4149-4154.
108. Schäfer M. K.-H., Eiden L. E., and Weihe E. (1998a) Cholinergic neurons and terminal fields revealed by immunohistochemistry for VAChT. the vesicular acetylcholine transporter. I. Central nervous system. Neuroscience 84, 331-359.
109. Schäfer M. K.-H., Eiden L. E., and Weihe E. (1998b) Cholinergic neurons and terminal fields revealed by immunohistochemistry for VAChT, the vesicular acetylcholine transporter. II. Peripheral nervous system. Neuroscience 84, 360-376.
110. Schemann M., Schaaf C., and Mäder M. (1995) Neurochemical coding of enteric neurons in the guinea pig stomach. J. Comp. Neurol. 353, 161-178.
111. Schloss P., Mayser W., and Betz H. (1994) The putative rat choline transporter CHOT1 transports creatine and is highly expressed in neural and muscle-rich tissues. Biochem. Biophys. Res. Commun. 198, 637-645.
112. Schoenherr C. J. and Anderson D. J. (1995) The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267, 1360-1363.
113. Schuldiner S. (1994) A molecular glimpse of vesicular monoamine transporters. J. Neurochem. 62, 2067-2078.
114. Schuldiner S., Liu Y., and Edwards R. H. (1993) Reserpine binding to a vesicular amine transporter expressed in Chinese hamster ovary fibroblasts. J. Biol. Chem. 268, 29-34.
115. Schuldiner S., Shirvan A., and Linial M. (1995) Vesicular neurotransmitter transporters: from bacteria to humans. Physiol. Rev. 75, 369-392.
116. Schütz B., Schäfer M. K.-H., Eiden L. E., and Weihe E. (1998a) Ontogeny of vesicular amine transporter expression in the rat: new perspectives on aminergic neuronal and neuroendocrine differentiation. Adv. Pharmacol. 42, 903-908.
117. Schütz B., Schäfer M. K.-H., Eiden L. E., and Weihe E. (1998b) Vesicular amine transporter expression and isoform selection in developing brain, peripheral nervous system and gut. Dev. Brain Res. 106, 181-204.
118. Selden N., Geula C., Hersh L., and Mesulam M.-M. (1994) Human striatum: chemoarchitecture of the caudate nucleus, putamen and ventral striatum in health and Alzheimer's disease. Neuroscience 60, 621-636.
119. Semba K. (1992) Development of central cholinergic neurons, in Handbook of Chemical Neuroanatomy, Vol. 10 (Bjorklund A., Hokfelt T., and Tohyama M., eds). pp. 33-62. Elsevier Science Publishers, New York.
120. Sims N. R., Bowen D. M., Allen S. J., Smith C. C., Neary D., Thomas D. J., and Davison A. M. (1983) Presynaptic cholinergic dysfunction in patients with dementia. J. Neurochem. 40, 503-509.
121. Sofroniew M. V., Campbell P. E., Cuello A. C., and Eckenstein F. (1985) Central cholinergic neurons visualized by immunohistochemical detection of choline acetyltransferase, in The Rat Nervous System, Vol. 1 (Paxinos G., ed), pp. 471-485. Academic Press, New York.
122. Song H., Ming G., Fon E., Bellocchio E., Edwards R. H., and Poo M. (1997) Expression of a putative vesicular acetylcholine transporter facilitates quantal transmitter packaging. Neuron 18, 815-826.
123. Steiner-Mordoch S., Shirvan A., and Schuldiner S. (1996) Modification of the pH profile and tetrabenazine sensitivity of rat VMAT1 by replacement of aspartate 404 with glutamate. J. Biol. Chem. 271, 13048-13054.
124. Strada O., Vyas S., Hirsch E. C., Ruberg M., Brice A., Agid Y., and Javoy-Agid F. (1992) Decreased choline acetyltransferase mRNA expression in the nucleus basalis of Meynert in Alzheimer disease: an in situ hybridization study. Proc. Natl. Acad. Sci. USA 89, 9549-9553.
125. Sugihara H., Andrisani V., and Salvaterra P. M. (1991) Genomic organization of Drosophila choline acetyltransferase. J. Neurochem. 57, 1636-1642.
126. Tanaka H., Zhao Y., Wu D., and Hersh L. B. (1998) The use of DNase I hypersensitivity site mapping to identify regulatory regions of the human cholinergic gene locus. J. Neurochem. 70, 1799-1808.
127. Tao-Cheng S. and Eiden L. E. (1998) The vesicular monoamine transporter VMAT2 is targeted to large dense-core vesicles, and the vesicular acetylcholine transporter VAChT to small synaptic vesicles in PC12 cells. Adv. Pharmacol. 42, 250-253.
128. Tian X., Sun X., and Suszkiw J. B. (1996) Developmental age-dependent upregulation of choline acetyltransferase and vesicular acetylcholine transporter mRNA expression in neonatal rat septum by nerve growth factor. Neurosci. Lett. 209, 134-136.
129. Toll L. and Howard B. D. (1980) Evidence that an ATPase and a protonmotive force function in the transport of acetylcholine into storage vesicles. J. Biol. Chem. 255, 1787-1789.
130. Unsworth C. D. and Johnson J. R. G. (1990) Acetylcholine and ATP are coreleased from the electromotor nerve terminals of Narcine brasiliensis by an exocytotic mechanism. Proc. Natl. Acad. Sci. USA 87, 553-557.
131. Usdin T., Eiden L. E., Bonner T. I., and Erickson J. D. (1995) Molecular biology of vesicular acetylcholine transporters (VAChTs). Trends Neurosci. 18, 218-224.
132. Varoqui H. and Erickson J. D. (1996) Active transport of acetylcholine by the human vesicular acetylcholine transporter. J. Biol. Chem. 271, 27229-27232.
133. Varoqui H. and Erickson J. D. (1997) Vesicular transporter chimeras identify domains important for acetylcholine transport and targeting to synaptic vesicles. Soc. Neurosci. Abstr. 23, 694.
134. Varoqui H., Diebler M.-F., Meunier F.-M., Rand J. B., Usdin T. B., Bonner T. I., Eiden L. E., and Erickson J. D. (1994) Cloning and expression of the vesamicol binding protein from the marine ray Torpedo. Homology with the putative vesicular acetylcholine transporter UNC-17 from Caenorhabditis elegans. FEBS Lett. 342, 97-102.
135. Weihe E., Tao-Cheng J.-H., Schäfer M. K.-H., Erickson J. D., and Eiden L. E. (1996) Visualization of the vesicular acetylcholine transporter in cholinergic nerve terminals and its targeting to a specific population of small synaptic vesicles. Proc. Natl. Acad. Sci. USA 93, 3547-3552.
136. Wenk G. L. and Mobley S. L. (1996) Choline acetyltransferase activity and vesamicol binding in Rett syndrome and in rats with nucleus basalis lesions. Neuroscience 73, 79-84.
137. West A. E., Provoda C., Neve R. L., and Buckley K. M. (1998) Protein targeting in neurons and endocrine cells. Adv. Pharmacol. 42, 247-249.
138. Wu D. and Hersh L. B. (1994) Choline acetyltransferase: celebrating its fiftieth year. J. Neurochem. 62, 1653-1663.
139. + antiporter of Escherichia coli. Biochemistry 32, 5698-5704.