Vesicular acetylcholine transporter (VAChT) protein: A novel and unique marker for cholinergic neurons in the central and peripheral nervous systems

Journal of Comparative Neurology

Volumn 378, Issue 4, 1997, Pages 454-467

  Arvidsson, Ulf ^a   Riedl, Maureen ^b   Elde, Robert ^b   Meister, Björn ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

antibody; autonomic nervous system; ChAT; synaptic vesicle; uptake

Indexed keywords

ACETYL COENZYME A; ACETYLCHOLINE; CARRIER PROTEIN; CHOLINE ACETYLTRANSFERASE; COMPLEMENTARY DNA; POLYCLONAL ANTIBODY;

ACETYLCHOLINE RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM; BRAIN CORTEX; CENTRAL NERVOUS SYSTEM; CHOLINERGIC NERVE CELL; CHOLINERGIC SYNAPSE; CONTROLLED STUDY; CORPUS STRIATUM; FOREBRAIN; HIPPOCAMPUS; MALE; NERVE ENDING; NONHUMAN; OLFACTORY BULB; PERIKARYON; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE;

ANIMALS; BIOLOGICAL MARKERS; CARRIER PROTEINS; CATS; CENTRAL NERVOUS SYSTEM; GOATS; GUINEA PIGS; IMMUNE SERA; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE TRANSPORT PROTEINS; MICE; NEURONS; PARASYMPATHETIC NERVOUS SYSTEM; PC12 CELLS; PERIPHERAL NERVES; RABBITS; RATS; RATS, SPRAGUE-DAWLEY; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 0031049911     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19970224)378:4<454::AID-CNE2>3.0.CO;2-1     Document Type: Article

References (77)

1. Ahrén, B., S. Karlsson, and S. Lindskog (1990) Cholinergic regulation of the endocrine pancreas. Progr. Brain Res. 84:209-225.
2. Alfonso, A., K. Grundahl, J.S. Duerr, H.-P. Han, and J.B. Rand (1993) The Caenorhabtidis elegans unc-17 gene: A putative vesicular acetylcholine transporter. Science 261:617-619.
3. Armstrong, D.M., C.B. Saper, A.I. Levey, B.H. Wainer, and R.D. Terry (1983) Distribution of cholinergic neurons in rat brain: Demonstrated by the immunocytochemical localization of choline acetyltransferase. J. Comp. Neurol. 229:329-346.
4. Barber, R.P., P.E. Phelps, C.R. Houser, G.D. Crawford, P.M. Salvaterra, and J.E. Vaughn (1984) The morphology and distribution of neurons containing choline acetyltransferase in the adult spinal cord: An immunocytochemical study. J. Comp. Neurol. 229:329-346.
5. Bejanin, S., R. Cervini, J. Mallet, and S. Berrard (1994) A unique gene organization for two cholinergic markers, choline acetyltransferase and a putative vesicular transporter of acetylcholine. J. Biol. Chem. 269:21944-21947.
6. Berrard, S., H. Varoqui, R. Cervini, M. Israel, J. Mallet, and M.-F. Diebler (1995) Coregulation of two embedded gene products, choline acetyltransferase and vesicular acetylcholine transporter. J. Neurochem. 65:939-942.
7. Berse, B., and J.K. Blusztajn (1995) Coordinated up-regulation of choline acetyltransferase and vesicular acetylcholine transporter gene expression by the retinoic acid receptor a, cAMP, and leukemia inhibitory factor/ciliary neurotrophic factor signaling pathways in a murine septal cell line. J. Biol. Chem. 270:22101-22104.
8. Bodian, D. (1964) An electron microscopic study of the monkey spinal cord. Bull. Johns Hopkins Hosp. 114:13-119.
9. Brelje, T.C., M.W. Wessendorf, and R.L. Sorenson (1993) Multicolor laser scanning confocal immunofluorescence microscopy: Practical application and limitations. Methods Cell Biol. 38:97-181.
10. Butcher, L.L., J.D. Oh, N.J. Woolf, R.H. Edwards, and A. Roghani (1992) Organization of central cholinergic neurons revealed by combined in situ hybridization histochemistry and choline-O-acetyltransferase immunocytochemistry. Neurochem. Int. 21:429-445.
11. Cervini, R., L. Houhou, P.F. Pradat, S. Bejanin, J. Mallet, and S. Berrard (1995) Specific vesicular acetylcholine transporter promoters lie within the first intron of the rat choline acetyltransferase gene. J. Biol. Chem. 270:24654-24657.
12. Cherami, A., V. Leviel, and J. Glowinski (1981) Dendritic release of dopamine in the substantia nigra. Nature 366:537-542.
13. Connaughton, M., J.V. Priestly, M.V. Sofroniew, F. Eckenstein, and A.C. Cuello (1986) Inputs to motoneurones in the hypoglossal nucleus of the rat: Light and electron microscopic immunocytochemistry for choline acetyltransferase, substance P and enkephalins using monoclonal antibodies. Neuroscience 17:205-224.
14. Conradi, S. (1969) Ultrastructure and distribution of neuronal and glial elements on the motoneuron surface in the lumbosacral spinal cord of the adult cat. Acta Physiol. Scand. 332:5-48.
15. Cozzari, C., and B.K. Hartmann (1980) Preparation of antibodies specific to choline acetyltransferase from bovine caudate nucleus and immunohistochemical localization of the enzyme. Proc. Natl. Acad. Sci. USA 77:7453-7457.
16. Dodd, J., and L.W. Role (1991) The autonomic nervous system. In E.R. Kandel, J.H. Schwartz, and T.M. Jessell (eds): Principles of Neural Science, 3rd Ed. Amsterdam: Elsevier, pp. 761-775.
17. Eckenstein, F., and H. Thoenen (1982) Production of specific antisera and monoclonal antibodies to choline acetyltransferase: Characterization and use for identification of cholinergic neurons. EMBO J. 1:363-368.
18. Ehinger, B., and J.E. Dowling (1987) Retinal neurocircuitry and transmission. In A. Björklund, T. Hökfelt, and L.W. Swanson (eds): Handbook of Chemical Neuroanatomy, Vol. 5, Integrated Systems of the CNS, Hypothalamus, Hippocampus, Amygdala, Retina. Amsterdam: Elsevier, pp. 389-446.
19. Erickson, J.D., H. Varoqui, M.K. Schäfer, W. Modi, M. Diebler, E. Weihe, J. Rand, L.-E. Eiden, T.I. Bonner, and T.B. Usdin (1994) Functional identification of a vesicular acetylcholine transporter and its expression from a *cholinergic* gene locus. J. Biol. Chem. 269:21929-21932.
20. Feng-Chen, K.C., and J.R. Wolpaw (1996) Operant conditioning of H-reflex changes synaptic terminals on primate motoneurons. Proc. Natl. Acad. Sci. USA 93:9206-9211.
21. Furness, J.B., I.J. Llewellyn-Smit, J.C. Bornstein, and M. Costa (1988) Chemical neuroanatomy and the analysis of neuronal circuitry in the enteric nervous system. In A. Björklund, T. Hökfelt, and C. Owman (eds): Handbook of Chemical Neuroanatomy, Vol. 6: The Peripheral Nervous System. Amsterdam: Elsevier, pp. 161-218.
22. German, D.C., G. Bruce, and L.B. Hersh (1985) Immunohistochemical staining of cholinergic neurons in the human brain using a polyclonal antibody to choline acetyltransferase. Neurosci. Lett. 61:1-5.
23. Gilmor, M.L., N.R. Nash, A. Roghani, R.H. Edwards, H. Yi, S.M. Hersch, and A.I. Levey (1996) Expression of the putative vesicular acetylcholine transporter in rat brain and localization in cholinergic synaptic vesicles. J. Neurosci. 16:2179-2190.
24. Gray, E.G. (1963) Electron microscopy of presynaptic organelles of the spinal cord. J. Anat. 97:101-106.
25. Greengard, P. (1987) Neuronal phosphoproteins. Mediators of signal transduction. Mol. Neurobiol. 1:81-119.
26. Houser, C.R., G.D. Crawford, R.P. Barber, P.M. Salvaterra, and J.E. Vaughn (1985) Organization and morphological characteristics of cholinergic neurons: An immunohistochemical study with antibody to choline acetyltransferase. Brain Res. 266:97-119.
27. Ibanez, C.F., M. Pelto-Huikko, O. Söder, M. Ritzén, L.B. Hersh, T. Hökfelt, and H. Persson (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.
28. Ibanez, C.F., P. Ernfors, and H. Persson (1991b) Developmental and regional expression of choline acetyltransferase mRNA in the rat central nervous system. J. Neurosci. Res. 29:163-171.
29. Ishii, K., Y. Oda, T. Ichikawa, and T. Deguchi (1990) Complementary DNAs for choline acetyltransferase from spinal cords of rat and mouse: Nucleotide sequence, expression in mammalian cells, and in situ hybridization. Mol. Brain Res. 7:151-159.
30. Jacobsson, G., A.J. Bean, R.H. Scheller, L. Juntti-Berggren, J.T. Deeney, P.-O. Berggren, and B. Meister (1994) Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine cells. Proc. Natl. Acad. Sci. USA 91:12487-12491.
31. Kato, M., S. Ohkuma, K. Kataoka, K. Kashima, and K. Kuriyama (1992) Characterization of muscarinic receptor subtypes on rat pancreatic acini: Pharmacological identification by secretory responses and binding studies. Digestion 52:194-203.
32. Kimura, H., P.L. McGeer, and J.H. Peng (1984) Choline acetyltransferase-containing neurons in the rat brain. In A. Björklund, T. Hökfelt, and M.J. Kuhar (eds): Handbook of Chemical Neuroanatomy, Vol. 3, Classical Transmitters and Transmitter Receptors in the CNS. Amsterdam: Elsevier, pp. 51-67.
33. 3H]vesamicol binding in human brain cholinergic deficiency disorders. Neurosci. Lett. 117:347-352.
34. Lauterborn, J.C., P.J. Isackson, R. Montalvo, and C.M. Gall (1993) In situ hybridization localization of choline acetyltransferase mRNA in adult rat brain and spinal cord. Mol. Brain Res. 17:59-69.
35. Levey, A.I., D.M. Armstrong, S.F. Atweh, R.D. Terry, and B.H. Wainer (1983a) Monoclonal antibodies to choline acetyltransferase: Production, specificity, and immunohistochemistry. J. Neurosci. 3:1-9.
36. Levey, A.I., B.H., E.J. Mufson, and M.-M. Mesulam (1983b) Colocalization of acetylcholinesterase and choline acetyltransferase in the rat cerebrum. Neuroscience 9:9-22.
37. Levey, A.I., B.H. Wainer, D.B. Rye, E.J. Mufson, and M.-M. Mesulam (1984) Choline acetyltransferase-immunoreactive neurons intrinsic to rodent cortex and distinction from acetylcholinesterase-positive neurons. Neuroscience 13:341-353.
38. Li, W., P.A.Y. Ochalski, S. Brimjoin, L.M. Jordan, and J.I. Nagy (1995) C-terminals on motoneurons: Electron microscope localization of cholinergic markers in adult rats and antibody-induced depletion in neonates. Neuroscience 65:879-891.
39. Lundberg, J.M., C.-R. Martling, and T. Hökfelt (1988) Airways, oral cavity and salivary glands: Classical transmitters and peptides in sensory and autonomic motor neurons. In A. Björklund, T. Hökfelt, and C. Owman (eds): Handbook of Chemical Neuroanatomy, Vol. 6: The Peripheral Nervous System. Amsterdam: Elsevier, pp. 391-444.
40. Meister, B., and T. Hökfelt (1988) Peptide- and transmitter-containing neurons in the mediobasal hypothalamus and their relation to GABAergic systems: Possible roles in control of prolactin and growth hormone secretion. Synapse 2:585-605.
41. Mesce, K.A., A. Klukas, and T.C. Brelje (1993) Improvements for the anatomical characterization of insect neurons in whole mount: The use of cyanine-derived fluorophores and laser scanning confocal microscopy. Cell Tissue Res. 271:381-397.
42. Müller, E.E., M. Rolla, E. Ghigo, D. Belliti, E. Arvat, A. Andreoni, A. Torsello, V. Locatelli, and F. Camanni (1995) Involvement of brain catecholamines and acetylcholine in growth hormone hypersecretion states. Pathophysiological, diagnostic and therapeutic implications. Drugs 50:805-837.
43. Nagy, J.I., T. Yamamoto, and L.M. Jordan (1993) Evidence for the cholinergic nature of C-terminals associated with subsurface cisterns in alpha-motoneurons of rat. Synapse 15:17-32.
44. Neal, M.J. (1983) Cholinergic mechanisms in the vertebrate retina. Progr. Retinal Res. 2:191-212.
45. Oh, J.D., N.J. Woolf, A. Roghani, R.H. Edwards, and L.L. Butcher (1992) Cholinergic neurons in the rat central nervous system demonstrated by in situ hybridization of choline acetyltransferase mRNA. Neuroscience 47:807-822.
46. Okuda, H., S. Shioda, Y. Nakai, H. Nakayama, M. Okamoto, and T. Nakashima (1993a) Immunocytochemical localization of nicotinic acetylcholine receptor in rat hypothalamus. Brain Res. 625:145-151.
47. Okuda, H., S. Shioda, Y. Nakai, H. Nakayama, M. Okamoto, and T. Nakashima (1993b) The presence of corticotropin-releasing factor-like immunoreactive synaptic vesicle terminals in axon terminals with nicotinic acetylcholine receptor-like immunoreactivity in the median eminence of the rat. Neurosci. Lett. 161:183-186.
48. Phelps, P.E., and J.E. Vaughn (1986) Immunocytochemical localization of choline acetyltransferase in rat ventral striatum: A light and electron microscopic study. J. Neurocytol. 15:595-617.
49. Phelps, P.E., C.R. Houser, and J.E. Vaughn (1985) Immunocytochemical localization of choline acetyltransferase within the rat neostriatum: A correlated light and electron microscopic study of cholinergic neurons and synapses. J. Comp. Neurol. 238:286-307.
50. Piehl, F., J. Ru-Rong, S. Cullheim, T. Hökfelt, D. Lindholm, and R.A. Hughes (1995) Fibroblast growth factors regulate calcitonin gene-related peptide mRNA expression in rat motoneurons after lesion and in culture. Eur. J. Neurosci. 7:1739-1750.
51. Pieribone, V.A., O. Shupliakov, L. Brodin, S. Hilfiker-Rothenfluh, A.J. Czernik, and P. Greengard (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375:493-497.
52. Pullen, A.H., and T.A. Sears (1983) Trophism between C-type axon terminals and thoracic motoneurones in the cat. J. Physiol. 337:373-388.
53. Rodriguez, S.J., and R.J. Morley (1985) Evidence that cell bodies in the arcuate nucleus of the hypothalamus are not cholinergic. Neuroendocrinology 41:427-431.
54. Roghani, A., J. Feldman, S. Kohan, A. Shirzadi, C. Gunderson, N. Brecha, and R. Edwards (1994) Molecular cloning of a putative vesicular transporter for acetylcholine. Proc. Natl. Acad. Sci. USA 91:10620-10624.
55. Rosenbluth, J. (1962) Subsurface cisterns and their relationship to the neuronal plasma membrane. J. Cell Biol. 13:405-421.
56. 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.
57. Ruggiero, D.A., R. Giuliano, M. Anwar, R. Stornetta, and D.J. Reis (1990) Anatomical substrates of cholinergic-autonomic regulation in the rat. J. Comp. Neurol. 292:1-53.
58. Satoh, K., D.M. Armstrong, and H.C. Fibiger (1983) A comparison of central cholinergic neurons as demonstrated by acetylcholinesterase pharmacohistochemistry and choline acetyltransferase immunohistochemistry. Brain Res. Bull. 11:693-720.
59. Schäfer, M.K.-H., E. Weihe, H. Varoqui, L.E. Eiden, and J.D. Erickson (1994) Distribution of the vesicular acetylcholine transporter (VAChT) in the central and peripheral nervous system. J. Mol. Neurosci. 5:1-26.
60. Schemann, M., H. Sann, C. Schaaf, and M. Mader (1993) Identification of cholinergic neurons in enteric nervous system by antibodies against choline acetyltransferase. Am. J. Physiol. 265:G1005-G1009.
61. Steele, P.A., S.J. Brooke, and M. Costa (1991) Immunohistochemical identification of cholinergic neurons in the myenteric plexus of guinea-pig small intestine. Neuroscience 45:227-239.
62. Tago, H., P.L. McGeer, G. Bruce, and L.B. Hersh (1987) Distribution of choline acetyltransferase-containing neurons if the hypothalamus. Brain Res. 415:49-62.
63. Tago, H., PL. McGeer, E.G. McGeer, H. Akiyama, and L.B. Hersh (1989) Distribution of choline acetyltransferase immunopositive structures in the rat brainstem. Brain Res. 495:271-297.
64. Tinner, B., K. Fuxe, C. Köhler, L. Hersh, K. Andersson, A. Jansson, M. Goldstein, and L.F. Agnati (1989) Evidence for the existence of a population of arcuate neurons costoring choline acetyltransferase and tyrosine hydroxylase immunoreactivities in the male rat. Neurosci. Lett. 99:44-49.
65. Torri Tarelli, F., F. Valtorta, A. Villa, and J. Meldolesi (1990) Functional morphology of the nerve terminal at the frog neuromuscular junction: Recent insights using immunocytochemistry. Progr. Brain Res. 84:83-92.
66. Usdin, T.B., L.E. Eiden, T.I. Bonner, and J.D. Erickson (1995) Molecular biology of the vesicular ACh transporter. Trends Neurosci. 18:218-224.
67. Van der Zee, E.A., B. Buwalda, J.H. Strubbe, A.D. Strosberg, and P.G. Luiten (1992) Immunocytochemical localization of muscarinic acetylcholine receptors in the rat endocrine pancreas. Cell Tissue Res. 269:99-106.
68. Varoqui, H., M.-F. Diebler, F.-M. Meunier, J.B. Rand, T.B. Usdin, T.I. Bonner, L.E. Eiden, and J.D. Erickson (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.
69. Vizi, E.S., K. Gyires, G.T. Somogyi, and G. Ungvári (1983) Evidence that transmitter can be released from regions of the nerve cell other than presynaptic axon terminal: Axonal release of acetylcholine without modulation. Neuroscience 10:967-972.
70. Weihe, E., J.-H. Tao-Cheng, M.K.-H. Schäfer, J.D. Erickson, and L.E. Eiden ( 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.
71. Wessendorf, M.W., and T.C. Brelje (1993) Multicolor fluorescence microscopy using the laser-scanning confocal microscope. Neuroprutocols 2:121-140.
72. Wolpaw, J.R., and J.S. Carp (1990) Memory traces in spinal cord. Trends Neurosci. 13:137-142.
73. Woolf, N. J. and L.L. Butcher (1986) Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res. Bull. 16:603-637.
74. Woolf, N.J., and L.L. Butcher (1989) Cholinergic systems in the rat brain: IV. Descending projections of the pontomesencephalic tegmentum. Brain Res. Bull. 23:519-540.
75. Woolf, N.J., F. Eckenstein, and L.L. Butcher (1983) Cholinergic projection from the basal forebrain to the frontal cortex: A combined fluorescent tracer and immunohistochemical analysis. Neurosci. Lett. 40:93-98.
76. Woolf, N. J., F. Eckenstein, and L.L. Butcher ( 1984) Cholinergic systems in the rat brain: I. Projections to the limbic telencephalon. Brain Res. Bull. 143:751-784.
77. Wu, D., and L.B. Hersh (1994) Choline acetyltransferase: Celebrating its fiftieth year. J. Neurochem. 62:1653-1663.