Effect of N-acetylaspartylglutamate (NAAG) on non-quantal and spontaneous quantal release of acetylcholine at the neuromuscular synapse of rat

Journal of Neurochemistry

Volumn 94, Issue 1, 2005, Pages 257-267

  Malomouzh, Artem I ^a   Nikolsky, Eugen E ^a,b   Lieberman, Edward M ^c   Sherman, Jessica A ^d   Lubischer, Jane L ^d   Grossfeld, Robert M ^d   Urazaev, Albert Kh ^b,e  

^a KAZAN INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Russian Federation)

^b KAZAN STATE MEDICAL UNIVERSITY   (Russian Federation)

^c EAST CAROLINA UNIVERSITY   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

^e PURDUE UNIVERSITY   (United States)

Author keywords

Glutamate; Muscle endplate; N methyl D aspartate receptor; Nitric oxide

Indexed keywords

2 (PHOSPHONOMETHYL)PENTANEDIOIC ACID; 2 AMINO 5 PHOSPHONOVALERIC ACID; 3 BROMO 7 NITROINDAZOLE; ACETYLCHOLINE; ACETYLCHOLINESTERASE; ARMIN; DIZOCILPINE; GAMMA GLUTAMYL HYDROLASE; GLUTAMIC ACID; GLUTARIC ACID DERIVATIVE; N ACETYLASPARTIC ACID; N ACETYLASPARTYLGLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N(G) NITROARGININE METHYL ESTER; NICOTINIC RECEPTOR; NITRIC OXIDE SYNTHASE; TUBOCURARINE CHLORIDE; UNCLASSIFIED DRUG; VALERIC ACID DERIVATIVE;

ACETYLCHOLINE RELEASE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HYPERPOLARIZATION; MALE; MOTONEURON; NERVE ENDING; NEUROMODULATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; RAT; SCHWANN CELL;

ACETYLCHOLINE; ANIMALS; DIPEPTIDES; EXTRACELLULAR SPACE; HYDROLYSIS; MALE; MOTOR NEURONS; NERVE ENDINGS; NEUROMUSCULAR JUNCTION; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; RATS; RATS, WISTAR; SYNAPSES;

EID: 21344432097     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03194.x     Document Type: Article

References (84)

1. Albuquerque E. X., Schuh F. T. and Kaufman F. C. (1971) Early membrane depolarization of the fast mammalian muscle after denervation. Pflügers Arch. 328, 36-50.
2. Bacich D. J., Ramada E., O'Keefe D. S. et al. (2002) Deletion of the glutamate carboxypeptidase II gene in mice reveals a second enzyme activity that hydrolyzes N-acetylaspartylglutamate. J. Neurochem. 83, 20-29.
3. Berger U. V., Carter R. E. and Coyle J. T. (1995a) The immunocytochemical localization of N-acetylaspartyl glutamate, its hydrolysing enzyme NAALADase, and the NMDAR-1 receptor at a vertebrate neuromuscular junction. Neuroscience 64, 847-850.
4. Berger U. V., Carter R. E., McKee M. et al. (1995b) N-Acetylated alpha-linked acidic peptidase is expressed by non-myelinating Schwann cells in the peripheral nervous system. J. Neurocytol. 24, 99-109.
5. Blakely R. D., Robinson M. B., Thompson R. C. et al. (1988) Hydrolysis of the brain dipeptide N-acetyl-L-aspartyl-L-glutamate: subcellular and regional distribution, ontogeny, and the effect of lesions on N-acetylated-alpha-linked acidic dipeptidase activity. J. Neurochem. 50, 1200-1209.
6. Bray J. J., Forrest J. W. and Hubbard J. I. (1982) Evidence for the role of non-quantal acetylcholine in the maintenance of the membrane potential of rat skeletal muscle. J. Physiol. 326, 285-296.
7. Brenman J. E., Chao D. S., Xia H. et al. (1995) Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 82, 743-752.
8. Bzdega T., Crowe S. L., Ramada E. et al. (2004) The cloning and characterization of a second brain enzyme with NAAG peptidase activity. J. Neurochem. 89, 627-635.
9. Cassidy M. and Neale J. H. (1993) N-Acetylaspartylglutamate catabolism is achieved by an enzyme on the cell surface of neurons and glia. Neuropeptides 24, 271-278.
10. Chang W. J., Iannaccone S. T., Lau K. S. et al. (1996) Neuronal nitric oxide synthase and dystropin-deficient muscular dystrophy. Proc. Natl Acad. Sci. USA 93, 9142-9147.
11. Forloni G., Grzanna R., Blakely R. D. et al. (1987) Co-localization of N-acetyl-aspartyl-glutamate in central cholinergic, noradrenergic, and serotonergic neurons. Synapse 1, 455-460.
12. Frandsen U., Lopez-Figueroa M. and Hellsten Y. (1996) Localization of nitric oxide synthase in human skeletal muscle. Biochem. Biophys. Res. Commun. 227, 88-93.
13. Fuhrman S., Palkovits M., Cassidy M. et al. (1994) The regional distribution of N-acetylaspartylglutamate (NAAG) and peptidase activity against NAAG in the rat nervous system. J. Neurochem. 62, 275-281.
14. Giniatullin R. A., Khazipov R. N., Oranska T. I. et al. (1993) The effect of non-quantal acetylcholine release on quantal miniature currents at mouse diaphragm. J. Physiol. 466, 105-114.
15. Gossrau R., Christova T., Grozdanovic Z. et al. (1996) Adhalin (alpha-sarcoglycan) is not required for anchoring of nitric oxide synthase I (NOS I) to the sarcolemma in non-mammalian skeletal (striated) muscle fibers. Acta Histochem. 98, 345-355.
16. Grozdanovic Z. and Gossrau R. (1998) Co-localization of nitric oxide synthase I (NOS I) and NMDA receptor subunit 1 (NMDAR-1) at the neuromuscular junction in rat and mouse skeletal muscle. Cell Tissue Res. 291, 57-63.
17. Grozdanovic Z., Nakos G., Christova T. et al. (1995a) Demonstration of nitric oxide synthase (NOS) in marmosets by NADPH diaphorase (NADPH-d) histochemistry and NOS immunoreactivity. Acta Histochem. 97, 321-331.
18. Grozdanovic Z., Nakos G., Dahrmann G. et al. (1995b) Species-independent expression of nitric oxide synthase in the sarcolemma region of visceral and somatic striated muscle fibers. Cell Tissue Res. 281, 493-499.
19. Grozdanovic Z., Gosztonyi G. and Gossrau R. (1996) Nitric oxide synthase I (NOS-I) is deficient in the sarcolemma of striated muscle fibers in patients with Duchenne muscular dystrophy, suggesting an association with dystrophin. Acta Histochem. 98, 61-69.
20. Hess S. D., Pasieczny R., Rao S. P. et al. (1999) Activity of N-acetyl-aspartylglutamate at human recombinant glutamate receptors. Soc. Neurosci. Abstr. 25, 975.
21. Israel M., Lesbats B. and Bruner J. (1993) Glutamate and acetylcholine release from cholinergic nerve terminals, a calcium control of the specificity of the release mechanism. Neurochem. Int. 22, 53-58.
22. Kaminski H. J. and Andrade F. H. (2001) Nitric oxide: biologic effects on muscle and role in muscle diseases. Neuromuscul. Disord. 11, 517-524.
23. Katz B. and Miledi R. (1977) Transmitter leakage from motor nerve endings. Proc. R. Soc. Lond. B. Biol. Sci. 196, 59-72.
24. Khairova R. A., Malomuzh A. I., Naumenko N. V. et al. (2002) Effect of glutamate on membrane potential and volume of the skeletal muscle fibers in rats following NO-synthase inhibition in vivo. Ross. Fiziol. Zh. Im. I. M. Sechenova 88, 1458-1466.
25. Khairova R. A., Malomuzh A. I., Naumenko N. V. et al. (2003) Effect of oxotremorine on resting membrane potential and cell volume in skeletal muscle fibers in rats after in vivo blockade of NO-synthase. Bull. Exp. Biol. Med. 135, 120-122.
26. Kobzik L., Reid M. B., Bredt D. S. et al. (1994) Nitric oxide in skeletal muscle. Nature 372, 546-548.
27. 2+ in vitro. Neuroreport 5, 1063-1068.
28. Kraus T., Neuhuber W. L. and Raab M. (2004) Vesicular glutamate transporter 1 immunoreactivity in motor endplates of striated esophageal but not skeletal muscles in the mouse. Neurosci. Lett. 360, 53-56.
29. Kusner L. L. and Kaminski H. J. (1996) Nitric oxide synthase is concentrated at the skeletal muscle endplate. Brain Res. 730, 238-242.
30. Landry M., Bouali-Benazzouz R., El Mestikawi S. et al. (2004) Expression of vesicular glutamate transporters in rat lumbar spinal cord with a note on dorsal root ganglia. J. Comp. Neurol. 468, 380-394.
31. Li W. C., Soffe S. R. and Roberts A. (2004) Glutamate and acetylcholine corelease at developing synapses. Proc. Natl Acad. Sci. USA 101, 15 488-15 493.
32. Losi G., Vicini S. and Neale J. (2004) NAAG fails to antagonize synaptic and extrasynaptic NMDA receptors in cerebellar granule neurons. Neuropharmacology 46, 490-496.
33. Lu B. and Fu W. M. (1995) Regulation of postsynaptic responses by calcitonin gene related peptide and ATP at developing neuromuscular junctions. Can. J. Physiol. Pharmacol. 73, 1050-1056.
34. Lück G., Hoch W., Hopf C. et al. (2000) Nitric oxide synthase (NOS-I) coclustered with agrin-induced AchR-specializations on cultured skeletal myotubes. Mol. Cell. Neurosci. 16, 269-281.
35. Lupa M. T., Tabti N., Thesleff S. et al. (1986) The nature and origin of calcium-insensitive miniature end-plate potentials at rodent neuromuscular junctions. J. Physiol. 381, 607-618.
36. Malomouzh A. I., Mukhtarov M. R., Nikolsky E. E. et al. (2003) Glutamate regulation of non-quantal release of acetylcholine in the rat neuromuscular junction. J. Neurochem. 85, 206-213.
37. Meister B., Arvidsson U., Zhang X. et al. (1993) Glutamate transporter mRNA and glutamate-like immunoreactivity in spinal motoneurones. Neuroreport 5, 337-340.
38. Miyake M., Kakimoto Y. and Sorimachi M. (1981) A gas chromatographic method for the determination of N-acetyl-L-aspartic acid. N-acetyl- aspartylglutamic acid, and β-citryl-L-glutamic acid and their distribution in the brain and other organs of various animals. J. Neurochem. 36, 804-810.
39. Moffett J. R., Williamson L., Palkovits M. et al. (1990) N-Acetyl-aspartylglutamate: a transmitter candidate for the retinohypothalamic tract. Proc. Natl Acad. Sci. USA 87, 8065-8069.
40. Molinar-Rode R. and Pasik P. (1992) Amino acids and N-acetyl-aspartyl- glutamate as neurotransmitter candidates in the monkey retinogeniculate pathways. Exp. Brain Res. 89, 40-48.
41. Mori-Okamoto J., Okamoto K. and Sekiguchi M. (1987) Electrophysiological and pharmacological actions of N-acetylaspartylglutamate intracellularly studied in cultured chick cerebellar neurons. Brain Res. 401, 60-67.
42. Mukhtarov M. R., Urazaev A. Kh, Nikolsky E. E. et al. (2000) Effect of nitric oxide and NO synthase inhibition on nonquantal acetylcholine release in the rat diaphragm. Eur. J. Neurosci. 12, 980-986.
43. Neale J. H., Bzdega T. and Wroblewska B. (2000) N-Acetylaspartyl- glutamate: the most abundant peptide neurotransmitter in the mammalian central nervous system. J. Neurochem. 75, 443-452.
44. Nikolsky E. E., Voronin V. A., Oranska T. I. et al. (1991) The dependence of non-quantal acetylcholine release on the choline-uptake system in the mouse diaphragm. Pflügers Arch. 418, 74-78.
45. Nikolsky E. E., Zemkova H., Voronin V. A. et al. (1994) Role of non-quantal acetylcholine release in surplus polarization of mouse diaphragm fibres at the endplate zone. J. Physiol. 477, 497-502.
46. Nikolsky E. E., Oranska T. I. and Vyskočil F. (1996) Non-quantal acetylcholine release in the mouse diaphragm after phrenic nerve crush and during recovery. Exp. Physiol. 81, 341-348.
47. Oliver L., Goureau O., Courtois Y. et al. (1996) Accumulation of NO synthase (type-I) at the neuromuscular junctions in adult mice. Neuroreport 7, 924-926.
48. Ory-Lavollée L., Blakely R. D. and Coyle J. T. (1987) Neurochemical and immunocytochemical studies on the distribution of N-acetyl-aspartylglutamate and N-acetyl-aspartate in rat spinal cord and some peripheral nervous tissues. J. Neurochem. 48, 895-899.
49. Pinard A., Levesque S., Vallee J. et al. (2003) Glutamatergic modulation of synaptic plasticity at a PNS vertebrate cholinergic synapse. Eur. J. Neurosci. 18, 3241-3250.
50. Reid M. B. (1998) Role of nitric oxide in skeletal muscle: synthesis, distribution and functional importance. Acta Physiol. Scand. 162, 401-409.
51. Ribeiro J. A., Cunha R. A., Correia-de-Sa P. et al. (1996) Purinergic regulation of acetylcholine release. Prog. Brain Res. 109, 231-241.
52. Robinson M. B., Blakely R. D., Couto R. and Coyle J. T. (1987) Hydrolysis of the brain dipeptide N-acetyl-L-aspartyl-L-glutamate. Identification and characterization of a novel N-acetylated alpha-linked acidic dipeptidase activity from rat brain. J. Biol. Chem. 262, 14 498-14 506.
53. Sanabria E. R., Wozniak K. M., Slusher B. S. and Keller A. (2004) GCP II (NAALADase) inhibition suppresses mossy fiber-CA3 synaptic neurotransmission by a presynaptic mechanism. J. Neurophysiol. 91, 182-193.
54. Sanes J. R. and Lichtman J. W. (1999) Development of the vertebrate neuromuscular junction. Annu. Rev. Neurosci. 22, 389-442.
55. Sekiguchi M., Wada K. and Wenthold R. J. (1992) N-Acetylaspartylglutamate acts as an agonist upon homomeric NMDA receptor (NMDAR1) expressed in Xenopus oocytes. FEBS Lett. 311, 285-289.
56. Serval V., Barbeito L., Pittaluga A. et al. (1990) Competitive inhibition of N-acetylated-a-linked acidic dipeptidase activity by N-acetyl-L-aspartyl- β-linked L-glutamate. J. Neurochem. 55, 39-46.
57. Stamler J. S. and Meissner G. (2001) Physiology of nitric oxide in skeletal muscle. Physiol. Rev. 81, 209-237.
58. Stanley E. F. and Drachman D. B. (1986) The effects of nerve section on the non-quantal release of acetylcholine from the motor nerve terminal. Brain Res. 365, 289-292.
59. Stauch B. L., Robinson M. B., Forloni G. et al. (1989) The effects of N-acetylated alpha-linked acidic dipeptidase (NAALADase) inhibitors on [3H]NAAG catabolism in vivo. Neurosci. Lett. 100, 295-300.
60. Sun Y.-a. and Poo M.-M. (1985) Non-quantal release of acetylcholine at a developing neuromuscular synapse in culture. J. Neurosci. 5, 634-642.
61. Thesleff S. (1990) Functional aspects of quantal and non-quantal release of acetylcholine at the neuromuscular junction. Prog. Brain Res. 84, 93-99.
62. Thomas A. G., Olkowski J. L., Vornov J. J. et al. (1999) Toxicity induced by a polyglutamated folate analog is attenuated by NAALADase inhibition. Brain Res. 843, 48-52.
63. Tiffany C. W., Cai N. S., Rojas C. et al. (2001) Binding of the glutamate carboxypeptidase II (NAALADase) inhibitor 2-PMPA to rat brain membranes. Eur. J. Pharmacol. 427, 91-96.
64. Tsai G., Stauch B. L., Vornov J. J. et al. (1990) Selective release of N-acetylaspartylglutamate from rat optic nerve terminals in vivo. Brain Res. 518, 313-316.
65. Urazaev A. Kh, Chikin A. V., Volkov E. M. et al. (1987a) Effect of acetylcholine and carbamylcholine on the resting membrane potential of denervated muscle in the rat. Fiziol. Zh. SSSR Im. I. M. Sechenova 73, 360-365.
66. Urazaev A. Kh, Surovtsev V. A., Chikin A. V. et al. (1987b) Neurotrophic control of transmembrane chloride transport in the muscle fibers of mammals. Neurophysiology 19, 766-771.
67. Urazaev A. K., Magsumov S. T., Poletayev G. I. et al. (1995) Muscle NMDA receptors regulate the resting membrane potential through NO-synthase. Physiol. Res. 44, 205-208.
68. Urazaev A. Kh, Naumenko N. V., Poletayev G. I. et al. (1996) Nitro-prusside decreases the early post-denervation depolarization of diaphragm muscle fibres of the rat. Eur. J. Pharmacol. 316, 219-222.
69. Urazaev A. Kh, Naumenko N. V., Poletaev G. I. et al. (1997) Acetylcholine and carbachol prevent muscle depolarization in denervated rat diaphragm. Neuroreport 8, 403-406.
70. Urazaev A. Kh, Naumenko N. V., Poletayev G. I. et al. (1998) The effect of glutamate and inhibitors of NMDA receptors on postdenervation decrease of membrane potential in rat diaphragm. Mol. Chem. Neuropathol. 33, 163-174.
71. Urazaev A. K., Naumenko N. V., Nikolsky E. E. et al. (1999) The glutamate and carbachol effects on the early post-denervation depolarization in rat diaphragm are directed towards furosemide-sensitive chloride transport. Neurosci. Res. 33, 81-86.
72. Urazaev A., Naumenko N., Malomough A. et al. (2000) Carbachol and acetylcholine delay the early postdenervation depolarization of muscle fibres through M1-cholinergic receptors. Neurosci. Res. 37, 255-263.
73. Valivullah H. M., Lancaster J., Sweetnam P. M. et al. (1994) Interactions between N-acetylaspartylglutamate and AMPA, kainate, and NMDA binding sites. J. Neurochem. 63, 1714-1719.
74. Vyas S. and Bradford H. F. (1987) Co-release of acetylcholine, glutamate and taurine from synaptosomes of Torpedo electric organ. Neurosci. Lett. 82, 58-64.
75. + ATP-ase. Pflügers Arch. 370, 295-297.
76. Vyskočil F. and Illes P. (1978) Electrophysiological examination of transmitter release in non-quantal form in the mouse diaphragm and the activity of membrane ATPase. Physiol. Bohemoslov. 27, 449-455.
77. Vyskočil F. and Vrbová G. (1993) Non-quantal release of acetylcholine affects polyneuronal innervation on developing rat muscle fibres. Eur. J. Neurosci. 5, 1677-1683.
78. Vyskočil F., Nikolsky E. and Edwards C. (1983) An analysis of the mechanisms underlying the non-quantal release of acetylcholine at the mouse neuromuscular junction. Neuroscience 9, 429-435.
79. Waerhaug O. and Ottersen O. P. (1993) Demonstration of glutamate-like immunoreactivity at rat neuromuscular junctions by quantitative electron microscopic immunocytochemistry. Anal. Embryol. (Berlin) 188, 501-513.
80. Westbrook G. L., Mayer M. L., Namboodiri M. A. et al. (1986) High concentrations of N-acetylaspartylglutamate (NAAG) selectively activate NMDA receptors on mouse spinal cord neurons in cell culture. J. Neurosci. 6, 3385-3392.
81. Wood S. J. and Slater C. R. (2001) Safety factor at the neuromuscular junction. Prog. Neurobiol. 64, 393-429.
82. Wroblewska B., Wroblewski J. T., Pshenichkin S. et al. (1997) N-Acetylaspartylglutamate selectively activates mGluR3 receptors in transfected cells. J. Neurochem. 69, 174-181.
83. Wroblewska B., Santi M. R. and Neale J. H. (1998) N- Acetylaspartylglutamate activates cyclic AMP-coupled metabotropic glutamate receptors in cerebellar astrocytes. Glia 24, 172-179.
84. Zhao J., Ramadan E., Cappiello M., Wroblewska B., Bodega T. and Neale J. H. (2001) NAAG inhibits KCl-induced [(3)H]-GABA release via mGLUR3. cAMP, PKA and 1-type calcium conductance. Eur. J. Neurosci. 13, 340-346.