AMPA receptor inhibition by synaptically released zinc

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 51, 2015, Pages 15749-15754

  Kalappa, Bopanna I ^a   Anderson, Charles T ^a   Goldberg, Jacob M ^b   Lippard, Stephen J ^b   Tzounopoulos, Thanos ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

AMPA receptors; Auditory; Synaptic plasticity; Zinc; ZnT3

Indexed keywords

AMPA RECEPTOR; ZINC;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; DORSAL COCHLEAR NUCLEUS; EVOKED RESPONSE; GLUTAMATERGIC SYNAPSE; HIPPOCAMPUS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SOUND; SYNAPTOSOME; ANIMAL; ANTAGONISTS AND INHIBITORS; COCHLEAR NUCLEUS; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; INSTITUTE FOR CANCER RESEARCH MOUSE; MALE; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ANIMALS; COCHLEAR NUCLEUS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; HIPPOCAMPUS; MALE; MICE; MICE, INBRED ICR; NEURONAL PLASTICITY; RECEPTORS, AMPA; SYNAPTIC TRANSMISSION; ZINC;

EID: 84952690927     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1512296112     Document Type: Article

References (51)

1. Traynelis SF, et al. (2010) Glutamate receptor ion channels: Structure, regulation, and function. Pharmacol Rev 62(3):405-496.
2. Lerma J, Marques JM (2013) Kainate receptors in health and disease. Neuron 80(2):292-311.
3. Zhu S, Paoletti P (2015) Allosteric modulators of NMDA receptors: Multiple sites and mechanisms. Curr Opin Pharmacol 20:14-23.
4. Hansen KB, Furukawa H, Traynelis SF (2010) Control of assembly and function of glutamate receptors by the amino-terminal domain. Mol Pharmacol 78(4):535-549.
5. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51(1):7-61.
6. Bowie D, Mayer ML (1995) Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 15(2):453-462.
7. Aizenman CD, Muñoz-Elías G, Cline HT (2002) Visually driven modulation of glutamatergic synaptic transmission is mediated by the regulation of intracellular polyamines. Neuron 34(4):623-634.
8. Karakas E, Furukawa H (2014) Crystal structure of a heterotetrameric NMDA receptor ion channel. Science 344(6187):992-997.
9. Lee CH, et al. (2014) NMDA receptor structures reveal subunit arrangement and pore architecture. Nature 511(7508):191-197.
10. Sobolevsky AI, Rosconi MP, Gouaux E (2009) X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462(7274):745-756.
11. O'Neill MJ, Bleakman D, Zimmerman DM, Nisenbaum ES (2004) AMPA receptor potentiators for the treatment of CNS disorders. Curr Drug Targets CNS Neurol Disord 3(3):181-194.
12. Vogt K, Mellor J, Tong G, Nicoll R (2000) The actions of synaptically released zinc at hippocampal mossy fiber synapses. Neuron 26(1):187-196.
13. Pan E, et al. (2011) Vesicular zinc promotes presynaptic and inhibits postsynaptic longterm potentiation of mossy fiber-CA3 synapse. Neuron 71(6):1116-1126.
14. Vergnano AM, et al. (2014) Zinc dynamics and action at excitatory synapses. Neuron 82(5):1101-1114.
15. Anderson CT, et al. (2015) Modulation of extrasynaptic NMDA receptors by synaptic and tonic zinc. Proc Natl Acad Sci USA 112(20):E2705-E2714.
16. Frederickson CJ, Koh JY, Bush AI (2005) The neurobiology of zinc in health and disease. Nat Rev Neurosci 6(6):449-462.
17. Sindreu CB, Varoqui H, Erickson JD, Pérez-Clausell J (2003) Boutons containing vesicular zinc define a subpopulation of synapses with low AMPAR content in rat hippocampus. Cereb Cortex 13(8):823-829.
18. Mayer ML, Vyklicky L, Jr, Westbrook GL (1989) Modulation of excitatory amino acid receptors by group IIB metal cations in cultured mouse hippocampal neurones. J Physiol 415:329-350.
19. Rassendren FA, Lory P, Pin JP, Nargeot J (1990) Zinc has opposite effects on NMDA and non-NMDA receptors expressed in Xenopus oocytes. Neuron 4(5):733-740.
20. Dreixler JC, Leonard JP (1994) Subunit-specific enhancement of glutamate receptor responses by zinc. Brain Res Mol Brain Res 22(1-4):144-150.
21. Zhang DQ, Ribelayga C, Mangel SC, McMahon DG (2002) Suppression by zinc of AMPA receptor-mediated synaptic transmission in the retina. J Neurophysiol 88(3):1245-1251.
22. Perez-Rosello T, et al. (2013) Synaptic Zn2+ inhibits neurotransmitter release by promoting endocannabinoid synthesis. J Neurosci 33(22):9259-9272.
23. Oertel D, Young ED (2004) What's a cerebellar circuit doing in the auditory system? Trends Neurosci 27(2):104-110.
24. Frederickson CJ, Howell GA, Haigh MD, Danscher G (1988) Zinc-containing fiber systems in the cochlear nuclei of the rat and mouse. Hear Res 36(2-3):203-211.
25. Faber DS, Korn H (1991) Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys J 60(5):1288-1294.
26. Tsien RW, Malinow R (1991) Changes in presynaptic function during long-term potentiation. Ann N Y Acad Sci 635:208-220.
27. Paoletti P, Vergnano AM, Barbour B, Casado M (2009) Zinc at glutamatergic synapses. Neuroscience 158(1):126-136.
28. Cole TB, Wenzel HJ, Kafer KE, Schwartzkroin PA, Palmiter RD (1999) Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene. Proc Natl Acad Sci USA 96(4):1716-1721.
29. Perez-Rosello T, Anderson CT, Ling C, Lippard SJ, Tzounopoulos T (2015) Tonic zinc inhibits spontaneous firing in dorsal cochlear nucleus principal neurons by enhancing glycinergic neurotransmission. Neurobiol Dis 81:14-19, 1.
30. Hansen KB, Ogden KK, Yuan H, Traynelis SF (2014) Distinct functional and pharmacological properties of Triheteromeric GluN1/GluN2AGluN2B NMDA receptors. Neuron 81(5):1084-1096.
31. Miller PS, Da Silva HM, Smart TG (2005) Molecular basis for zinc potentiation at strychnine-sensitive glycine receptors. J Biol Chem 280(45):37877-37884.
32. Rubio ME, Juiz JM (1998) Chemical anatomy of excitatory endings in the dorsal cochlear nucleus of the rat: Differential synaptic distribution of aspartate aminotransferase, glutamate, and vesicular zinc. J Comp Neurol 399(3):341-358.
33. Petralia RS, Rubio ME, Wang YX, Wenthold RJ (2000) Differential distribution of glutamate receptors in the cochlear nuclei. Hear Res 147(1-2):59-69.
34. Zastrow ML, et al. (2015) Reaction-based probes for imaging mobile zinc in live cells and tissues [published online ahead of print September 23, 2015]. ACS Sensors, 10.1021/acssensors.5b00022.
35. Wenthold RJ, Petralia RS, Blahos J II, Niedzielski AS (1996) Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 16(6):1982-1989.
36. Nakashima AS, Dyck RH (2009) Zinc and cortical plasticity. Brain Res Brain Res Rev 59(2):347-373.
37. Kujawa SG, Liberman MC (2009) Adding insult to injury: Cochlear nerve degeneration after "temporary" noise-induced hearing loss. J Neurosci 29(45):14077-14085.
38. Li S, Kalappa BI, Tzounopoulos T (2015) Noise-induced plasticity of KCNQ2/3 and HCN channels underlies vulnerability and resilience to tinnitus. eLife 4, 10.7554/eLife.07242.
39. Salazar G, et al. (2004) The zinc transporter ZnT3 interacts with AP-3 and it is preferentially targeted to a distinct synaptic vesicle subpopulation. Mol Biol Cell 15(2):575-587.
40. Lavoie N, et al. (2011) Vesicular zinc regulates the Ca2+ sensitivity of a subpopulation of presynaptic vesicles at hippocampal mossy fiber terminals. J Neurosci 31(50):18251-18265.
41. Jia Y, Jeng JM, Sensi SL, Weiss JH (2002) Zn2+ currents are mediated by calciumpermeable AMPA/kainate channels in cultured murine hippocampal neurones. J Physiol 543(Pt 1):35-48.
42. Armstrong N, Gouaux E (2000) Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor: Crystal structures of the GluR2 ligand binding core. Neuron 28(1):165-181.
43. Apostolides PF, Trussell LO (2013) Regulation of interneuron excitability by gap junction coupling with principal cells. Nat Neurosci 16(12):1764-1772.
44. Apostolides PF, Trussell LO (2014) Superficial stellate cells of the dorsal cochlear nucleus. Front Neural Circuits 8:63.
45. Zhao Y, Rubio M, Tzounopoulos T (2011) Mechanisms underlying input-specific expression of endocannabinoid-mediated synaptic plasticity in the dorsal cochlear nucleus. Hear Res 279(1-2):67-73.
46. Ryugo DK, Haenggeli CA, Doucet JR (2003) Multimodal inputs to the granule cell domain of the cochlear nucleus. Exp Brain Res 153(4):477-485.
47. Malenka RC, Bear MF (2004) LTP and LTD: An embarrassment of riches. Neuron 44(1):5-21.
48. Tzounopoulos T, Kim Y, Oertel D, Trussell LO (2004) Cell-specific, spike timingdependent plasticities in the dorsal cochlear nucleus. Nat Neurosci 7(7):719-725.
49. Balakrishnan V, Trussell LO (2008) Synaptic inputs to granule cells of the dorsal cochlear nucleus. J Neurophysiol 99(1):208-219.
50. Fujino K, Oertel D (2003) Bidirectional synaptic plasticity in the cerebellum-like mammalian dorsal cochlear nucleus. Proc Natl Acad Sci USA 100(1):265-270.
51. Woodroofe CC, Masalha R, Barnes KR, Frederickson CJ, Lippard SJ (2004) Membranepermeable and -impermeable sensors of the Zinpyr family and their application to imaging of hippocampal zinc in vivo. Chem Biol 11(12):1659-1666.