Physiological evidence that D-aspartate activates a current distinct from ionotropic glutamate receptor currents in Aplysia californica neurons

Journal of Neurophysiology

Volumn 106, Issue 4, 2011, Pages 1629-1636

  Carlson, Stephen L ^a   Fieber, Lynne A ^a  

^a UNIVERSITY OF MIAMI   (United States)

Author keywords

Buccal ganglion; Cation channel; Invertebrate; Nmethyl D aspartate; Reversal potential

Indexed keywords

DEXTRO ASPARTIC ACID; IONOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

APLYSIA; ARTICLE; CELL CULTURE; EVOKED RESPONSE; NERVOUS SYSTEM; NEUROPHYSIOLOGY; NONHUMAN; PHOTORECEPTOR CELL; POTASSIUM CURRENT; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; RNA TRANSLATION; SODIUM CURRENT; VOLTAGE CLAMP; WHOLE CELL;

ACTION POTENTIALS; ANIMALS; APLYSIA; ASPARTIC ACID; CALCIUM; CATIONS; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACIDS; GANGLIA, INVERTEBRATE; GLUTAMIC ACID; ION CHANNEL GATING; ION CHANNELS; MAGNESIUM; MEGLUMINE; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM; RECEPTORS, IONOTROPIC GLUTAMATE; SODIUM; STEREOISOMERISM;

EID: 80054050523     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00403.2011     Document Type: Article

References (49)

1. Antzoulatos EG, Byrne JH. Learning insights transmitted by glutamate. Trends Neurosci 27: 555-560, 2004.
2. Ascher P, Nowak L. The role of divalent cations in the N-methyl-D-aspartate responses of mouse central neurons in culture. J Physiol 399: 247-266, 1988.
3. Brown ER, Piscopo S, Chun JT, Francone M, Mirabile I, D'Aniello A. Modulation of an AMPA-like glutamate receptor (SqGluR) gating by L- and D-aspartic acids. Amino Acids 32: 53-57, 2007.
4. Carlson SL, Fieber LA. Unique ionotropic receptors for D-aspartate are a target for serotonin-induced synaptic plasticity in Aplysia californica. Comp Biochem Physiol C Toxicol Pharmacol. In press.
5. Curtis DR, Watkins JC. Amino acids with strong excitatory actions on mammalian neurons. J Physiol 166: 1-14, 1963.
6. Dale N, Kandel ER. L-Glutamate may be the fast excitatory transmitter of Aplysia sensory neurons. Proc Natl Acad Sci USA 90: 7163-7167, 1993.
7. D'Aniello A. D-aspartic acid: an endogenous amino acid with an important neuroendocrine role. Brain Res 53: 215-234, 2007.
8. D'Aniello A, Lee JM, Petrucelli L, Di Fiore MM. Regional decrease of free D-Aspartate levels in Alzheimer's disease. Neurosci Lett 250: 131-134, 1998.
9. D'Aniello A, Nardi G, Vetere A, Ferguson GP. Occurrence of free D-aspartic acid in the circumoesophaeal ganglia of Aplysia fasciata. Life Sci 52: 733-736. 1993.
10. Davies LP, Johnston GA. Uptake and release of D- and L-aspartate by rat brain slices. J Neurochem 26: 1007-1014, 1976.
11. Dingledine R, Borges K, Bowie D, Traynelis SF. The glutamate receptor ion channels. Pharmacol Rev 51: 7-61, 1999.
12. Errico F, Nisticò R, Napolitano F, Mazzola C, Astone D, Pisapia T, Giustizieri M, D'Aniello A, Mercuir NB, Ussielo A. Increased D-aspartate brain content rescues hippocampal age-related synaptic plasticity deterioration of mice. Neurobiol Aging. In press.
13. Errico F, Nistico R, Palma G, Federici M, Affuso A, Brilli E, Topo E, Centonze D, Bernardi G, Bozzi Y, D'Aniello A, Di Lauro R, Mercuri NB, Usiello A. Increased levels of D-aspartate in the hippocampus enhance LTP but do not facilitate cognitive flexibility. Mol Cell Neurosci 37: 236-246, 2008a.
14. Errico F, Rossi S, Napolitano F, Catuogno V, Topo E, Fisone G, D'Aniello A, Centonze D, Usiello A. D-Aspartate prevents corticostriatal long-term depression and attenuates schizophrenia-like symptoms induced by amphetamine and MK-801. J Neurosci 28: 10404-10414, 2008b.
15. Fieber LA. The development of excitatory capability in Aplysia californica bag cells observed in cohorts. Dev Brain Res 122: 47-58, 2000.
16. Fieber LA, Carlson SL, Capo TR, Schmale MC. Changes in D-aspartate ion currents in the Aplysia nervous system with aging. Brain Res 1343: 28-36, 2010.
17. Fuchs SA, Berger R, Klomp LWJ, De Koning TJ. D-Amino acids in the central nervous system in health and disease. Mol Genet Metab 85: 168-180, 2005.
18. Furuchi F, Homma H. Free D-aspartate in mammals. Biol Pharm Bull 28: 1566-1570, 2005.
19. Gong XQ, Frandsen A, Lu WY, Wan Y, Zabek RL, Pickering DS, Bai D. D-Aspartate and NMDA, but not L-aspartate, block AMPA receptors in rat hippocampal neurons. Br J Pharmacol 145: 449-459, 2005.
20. Ha TJ, Kohn AB, Bobkova YV, Moroz LL. Molecular characterization of NMDA-like receptors in Aplysia and Lymnaea: relevance to memory mechanisms. Biol Bull 210: 255-270, 2006.
21. Heckmann M, Dudel J. Desensitization and resensitization kinetics of glutamate receptor channels from Drosophila larval muscle. Biophys J 72: 2160-2169, 1997.
22. Homma H. Biochemistry of D-aspartate in mammalian cells. Amino Acids 32: 3-11, 2007.
23. Huang YH, Sinha SR, Fedoryak OD, Ellis-Davies GCR, Bergles DE. Synthesis and characterization of 4-methoxy-7-nitroindolinyl-D-aspartate, a caged compound for selective activation of glutamate transporters and N-methyl-D-aspartate receptors in brain tissue. Biochemistry 44: 3316-3326, 2005.
24. Jahan-Parwar B, Fredman SM. Cerebral ganglion of Aplysia: cellular organization and origin of nerves. Comp Biochem Physiol 54A: 347-357, 1976.
25. Kim PM, Duan X, Huang AS, Liu CY, Ming GL, Snyder SH. Aspartate racemase, generating neuronal D-aspartate, regulates adult neurogenesis. Proc Natl Acad Sci USA 107: 3175-3179, 2010.
26. - conductance gated by GABA and L-glutamate in single neurons of Aplysia. J Neurophysiol 61: 892-899, 1989.
27. Kiskin NI, Krishtal OA, Tsyndrenko AY. Cross-desensitization reveals pharmacological specificity of excitatory amino acid receptors in isolated hippocampal neurons. Eur J Neurosci 2: 461-470, 1990.
28. Li Q, Roberts AC, Glanzman DL. Synaptic facilitation and behavioral dishabituation in Aplysia: dependence on release of Ca from postsynaptic intracellular stores, postsynaptic exocytosis, and modulation of postsynaptic AMPA receptor efficacy. J Neurosci 25: 5623-5637, 2005.
29. Liu YM, Schneider M, Sticha CM, Toyooka T, Sweedler JV. Separation of amino acid and peptide stereoisomers by nonionic micelle-mediated capillary electrophoresis after chiral derivatization. J Chromatogr A 800: 345-354, 1998.
30. Mayer ML, Westbrook GL. Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurons. J Physiol 394: 501-527, 1987.
31. Miao H, Rubakhin SS, Sweedler JV. Subcellular analysis of D-Aspartate. Anal Chem 77: 7190-7194, 2005.
32. Miao H, Rubakhin SS, Scanlan CR, Wang L, Sweedler JV. D-Aspartate as a putative cell-cell signaling molecule in the Aplysia californica central nervous system. J Neurochem 97: 595-606, 2006.
33. 3H]D-2-amino-5-phosphonopentanoic acid binding in rat brain membranes. Neuroscience 26: 17-31, 1988.
34. Paoletti P. Molecular basis of NMDA receptor functional diversity. Eur J Neurosci 33: 1351-1365, 2011.
35. Patneau DK, Mayer ML. Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors. J Neurosci 10: 2385-2399, 1990.
36. Robert A, Howe JR. How AMPA receptor desensitization depends on receptor occupancy. J Neurosci 23: 847-858, 2003.
37. 3H]-D-aspartate release from hippocampal slices. Neurochem Int 38: 255-267, 2001.
38. Scanlan C, Shi T, Hatcher NG, Rubakhin SS, Sweedler JV. Synthesis, accumulation, and release of D-aspartate in the Aplysia californica CNS. J Neurochem 115: 1234-1244, 2010.
39. Spinelli P, Brown E, Ferrandino G, Branno M, Montarolo PG, D'Aniello E, Rastogi RK, D'Aniello B, Chieffi G, Fisher GH, D'Aniello A. D-As-partic acid in the nervous system of Aplysia limacina: possible role in neurotransmission. J Cell Physiol 206: 672-681, 2006.
40. Trussel LO, Fischbach GD. Glutamate receptor desensitization and its role in synaptic transmission. Neuron 3: 209-218, 1989.
41. Verdoorn TA, Dingledine R. Excitatory amino acid receptors expressed in Xenopus oocytes: agonist pharmacology. Mol Pharmacol 34: 298-307, 1988.
42. Vicini S, Wang JF, Li JH, Zhu WJ, Wang YH, Luo JH, Wolfe BB, Grayson DR. Functional and pharmacological differences between recombinant N-methyl-Daspartate receptors. J Neurophysiol 79: 555-566, 1998.
43. 3H]D-aspartate in astrocytes and glutamatergic neurons. Neurochem Res 26: 661-666, 2001.
44. Wang L, Ota N, Romanova EV, Sweedler JV. A novel pyridoxal 5'-phosphate-dependent amino acid racemase in the Aplysia californica central nervous system. J Biol Chem 286: 13765-13774, 2011.
45. Wilding TJ, Huettner JE. Activation and desensitization of hippocampal kainate receptors. J Neurosci 17: 2713-2721, 1997.
46. Wolosker H, D'Aniello A, Snyder SH. D-Aspartate disposition in neuronal and endocrine tissues: ontogeny, biosynthesis and release. Neuroscience 100: 183-189, 2000.
47. Yamada R, Kera Y, Takahashi S. Occurrence and functions of free D-aspartate and its metabolizing enzymes. Chem Rec 6: 259-266, 2006.
48. Yarowsky PJ, Carpenter DO. Aspartate: distinct receptors on Aplysia neurons. Science 192: 807-809, 1976.
49. Zhang W, Robert A, Vogensen SB, Howe JR. The relationship between agonist potency and AMPA receptor kinetics. Biophys J 91: 1336-1346, 2006.