6mms › Citations

Mechanisms for Zinc and Proton Inhibition of the GluN1/GluN2A NMDA Receptor.

Jalali-Yazdi F, Chowdhury S, Yoshioka C, Gouaux E
Cell 175 1520-1532.e15 (2018)
Related entries: 6mm9, 6mma, 6mmb, 6mmg, 6mmh, 6mmi, 6mmj, 6mmk, 6mml, 6mmm, 6mmn, 6mmp, 6mmr, 6mmt, 6mmu, 6mmv, 6mmw, 6mmx

Cited: 47 times
EuropePMC logo PMID: 30500536

Abstract

N-methyl-D-aspartate receptors (NMDARs) play essential roles in memory formation, neuronal plasticity, and brain development, with their dysfunction linked to a range of disorders from ischemia to schizophrenia. Zinc and pH are physiological allosteric modulators of NMDARs, with GluN2A-containing receptors inhibited by nanomolar concentrations of divalent zinc and by excursions to low pH. Despite the widespread importance of zinc and proton modulation of NMDARs, the molecular mechanism by which these ions modulate receptor activity has proven elusive. Here, we use cryoelectron microscopy to elucidate the structure of the GluN1/GluN2A NMDAR in a large ensemble of conformations under a range of physiologically relevant zinc and proton concentrations. We show how zinc binding to the amino terminal domain elicits structural changes that are transduced though the ligand-binding domain and result in constriction of the ion channel gate.

Articles - 6mms mentioned but not cited (3)

  1. Treatment of autosomal dominant hearing loss by in vivo delivery of genome editing agents. Gao X, Tao Y, Lamas V, Huang M, Yeh WH, Pan B, Hu YJ, Hu JH, Thompson DB, Shu Y, Li Y, Wang H, Yang S, Xu Q, Polley DB, Liberman MC, Kong WJ, Holt JR, Chen ZY, Liu DR. Nature 553 217-221 (2018)
  2. Mechanisms for Zinc and Proton Inhibition of the GluN1/GluN2A NMDA Receptor. Jalali-Yazdi F, Chowdhury S, Yoshioka C, Gouaux E. Cell 175 1520-1532.e15 (2018)
  3. Structure of the Arabidopsis Glutamate Receptor-like Channel GLR3.2 Ligand-Binding Domain. Gangwar SP, Green MN, Michard E, Simon AA, Feijó JA, Sobolevsky AI. Structure 29 161-169.e4 (2021)


Reviews citing this publication (10)

  1. Structure, Function, and Pharmacology of Glutamate Receptor Ion Channels. Hansen KB, Wollmuth LP, Bowie D, Furukawa H, Menniti FS, Sobolevsky AI, Swanson GT, Swanger SA, Greger IH, Nakagawa T, McBain CJ, Jayaraman V, Low CM, Dell'Acqua ML, Diamond JS, Camp CR, Perszyk RE, Yuan H, Traynelis SF. Pharmacol Rev 73 298-487 (2021)
  2. Dissecting diverse functions of NMDA receptors by structural biology. Wang JX, Furukawa H. Curr Opin Struct Biol 54 34-42 (2019)
  3. Acetazolamide: Old drug, new evidence? Shukralla AA, Dolan E, Delanty N. Epilepsia Open 7 378-392 (2022)
  4. From bedside-to-bench: What disease-associated variants are teaching us about the NMDA receptor. Amin JB, Moody GR, Wollmuth LP. J Physiol 599 397-416 (2021)
  5. Molecular Mechanisms of Environmental Metal Neurotoxicity: A Focus on the Interactions of Metals with Synapse Structure and Function. Carmona A, Roudeau S, Ortega R. Toxics 9 198 (2021)
  6. Structural insights into NMDA receptor pharmacology. Zhou C, Tajima N. Biochem Soc Trans 51 1713-1731 (2023)
  7. The Extracellular Domains of GluN Subunits Play an Essential Role in Processing NMDA Receptors in the ER. Horak M, Barackova P, Langore E, Netolicky J, Rivas-Ramirez P, Rehakova K. Front Neurosci 15 603715 (2021)
  8. Progresses in GluN2A-containing NMDA Receptors and their Selective Regulators. Niu M, Yang X, Li Y, Sun Y, Wang L, Ha J, Xie Y, Gao Z, Tian C, Wang L, Sun Y. Cell Mol Neurobiol (2022)
  9. Recent progress in allosteric modulators for GluN2A subunit and development of GluN2A-selective nuclear imaging probes. He Y, Mu L, Ametamey SM, Schibli R. J Labelled Comp Radiopharm 62 552-560 (2019)
  10. Structural Dynamics of Glutamate Signaling Systems by smFRET. Durham RJ, Latham DR, Sanabria H, Jayaraman V. Biophys J 119 1929-1936 (2020)

Articles citing this publication (34)

  1. Structural Basis of Functional Transitions in Mammalian NMDA Receptors. Chou TH, Tajima N, Romero-Hernandez A, Furukawa H. Cell 182 357-371.e13 (2020)
  2. NMDA receptor channel gating control by the pre-M1 helix. McDaniel MJ, Ogden KK, Kell SA, Burger PB, Liotta DC, Traynelis SF. J Gen Physiol 152 e201912362 (2020)
  3. Structural basis of ketamine action on human NMDA receptors. Zhang Y, Ye F, Zhang T, Lv S, Zhou L, Du D, Lin H, Guo F, Luo C, Zhu S. Nature 596 301-305 (2021)
  4. Structure of the Arabidopsis thaliana glutamate receptor-like channel GLR3.4. Green MN, Gangwar SP, Michard E, Simon AA, Portes MT, Barbosa-Caro J, Wudick MM, Lizzio MA, Klykov O, Yelshanskaya MV, Feijó JA, Sobolevsky AI. Mol Cell 81 3216-3226.e8 (2021)
  5. A human stem cell-derived test system for agents modifying neuronal N-methyl-D-aspartate-type glutamate receptor Ca2+-signalling. Klima S, Brüll M, Spreng AS, Suciu I, Falt T, Schwamborn JC, Waldmann T, Karreman C, Leist M. Arch Toxicol 95 1703-1722 (2021)
  6. Architecture and structural dynamics of the heteromeric GluK2/K5 kainate receptor. Khanra N, Brown PM, Perozzo AM, Bowie D, Meyerson JR. Elife 10 e66097 (2021)
  7. Trans-synaptic assemblies link synaptic vesicles and neuroreceptors. Martinez-Sanchez A, Laugks U, Kochovski Z, Papantoniou C, Zinzula L, Baumeister W, Lučić V. Sci Adv 7 eabe6204 (2021)
  8. Cadmium activates AMPA and NMDA receptors with M3 helix cysteine substitutions. Wilding TJ, Huettner JE. J Gen Physiol 152 e201912537 (2020)
  9. Conformational spread and dynamics in allostery of NMDA receptors. Durham RJ, Paudyal N, Carrillo E, Bhatia NK, Maclean DM, Berka V, Dolino DM, Gorfe AA, Jayaraman V. Proc Natl Acad Sci U S A 117 3839-3847 (2020)
  10. Cryo-EM structures of the ionotropic glutamate receptor GluD1 reveal a non-swapped architecture. Burada AP, Vinnakota R, Kumar J. Nat Struct Mol Biol 27 84-91 (2020)
  11. Excitatory and inhibitory D-serine binding to the NMDA receptor. Yovanno RA, Chou TH, Brantley SJ, Furukawa H, Lau AY. Elife 11 e77645 (2022)
  12. HOTSPUR: A Real-time Interactive Preprocessing System for Cryo-EM Data. Elferich J, Posert R, Yoshioka C, Gouaux E. Microsc Microanal 25 1212-1213 (2019)
  13. Leptin modulates pancreatic β-cell membrane potential through Src kinase-mediated phosphorylation of NMDA receptors. Cochrane VA, Wu Y, Yang Z, ElSheikh A, Dunford J, Kievit P, Fortin DA, Shyng SL. J Biol Chem 295 17281-17297 (2020)
  14. N-methyl-D-aspartic acid receptor 2A functionalized stationary phase: A reliable method for pursuing potential ligands against Alzheimer's disease from natural products. Chen YY, Xue Y, Yin JT, Qu LJ, Li HP, Li Q, Zhao XF. CNS Neurosci Ther 29 1290-1299 (2023)
  15. Positive surface charge of GluN1 N-terminus mediates the direct interaction with EphB2 and NMDAR mobility. Washburn HR, Xia NL, Zhou W, Mao YT, Dalva MB. Nat Commun 11 570 (2020)
  16. Allosteric coupling of sub-millisecond clamshell motions in ionotropic glutamate receptor ligand-binding domains. Rajab S, Bismin L, Schwarze S, Pinggera A, Greger IH, Neuweiler H. Commun Biol 4 1056 (2021)
  17. Alzheimer risk factors age and female sex induce cortical Aβ aggregation by raising extracellular zinc. Datki Z, Galik-Olah Z, Janosi-Mozes E, Szegedi V, Kalman J, Hunya ÁG, Fulop L, Tamano H, Takeda A, Adlard PA, Bush AI. Mol Psychiatry 25 2728-2741 (2020)
  18. Binding and Dynamics Demonstrate the Destabilization of Ligand Binding for the S688Y Mutation in the NMDA Receptor GluN1 Subunit. Chen JZ, Church WB, Bastard K, Duff AP, Balle T. Molecules 28 4108 (2023)
  19. Chemical shift assignments of calmodulin bound to the GluN1 C0 domain (residues 841-865) of the NMDA receptor. Bej A, Ames JB. Biomol NMR Assign 17 61-65 (2023)
  20. Conformational rearrangement of the NMDA receptor amino-terminal domain during activation and allosteric modulation. Vyklicky V, Stanley C, Habrian C, Isacoff EY. Nat Commun 12 2694 (2021)
  21. Cross-subunit interactions that stabilize open states mediate gating in NMDA receptors. Iacobucci GJ, Wen H, Helou M, Liu B, Zheng W, Popescu GK. Proc Natl Acad Sci U S A 118 (2021)
  22. Development and characterization of functional antibodies targeting NMDA receptors. Tajima N, Simorowski N, Yovanno RA, Regan MC, Michalski K, Gómez R, Lau AY, Furukawa H. Nat Commun 13 923 (2022)
  23. Distinct structure and gating mechanism in diverse NMDA receptors with GluN2C and GluN2D subunits. Zhang J, Zhang M, Wang Q, Wen H, Liu Z, Wang F, Wang Y, Yao F, Song N, Kou Z, Li Y, Guo F, Zhu S. Nat Struct Mol Biol (2023)
  24. GluN2A and GluN2B NMDA receptors use distinct allosteric routes. Tian M, Stroebel D, Piot L, David M, Ye S, Paoletti P. Nat Commun 12 4709 (2021)
  25. Inhibition of NMDA receptors through a membrane-to-channel path. Wilcox MR, Nigam A, Glasgow NG, Narangoda C, Phillips MB, Patel DS, Mesbahi-Vasey S, Turcu AL, Vázquez S, Kurnikova MG, Johnson JW. Nat Commun 13 4114 (2022)
  26. Isomerization of bioactive acylhydrazones triggered by light or thiols. Zhang Z, Le GNT, Ge Y, Tang X, Chen X, Ejim L, Bordeleau E, Wright GD, Burns DC, Tran S, Axerio-Cilies P, Wang YT, Dong M, Woolley GA. Nat Chem 15 1285-1295 (2023)
  27. NMDA Receptors Require Multiple Pre-opening Gating Steps for Efficient Synaptic Activity. Amin JB, Gochman A, He M, Certain N, Wollmuth LP. Neuron 109 488-501.e4 (2021)
  28. NMDA Receptors' Structural Asymmetry. Jalali-Yazdi F, Gouaux E. Microsc Microanal 25 1218-1219 (2019)
  29. Prophylactic Zinc Administration Combined with Swimming Exercise Prevents Cognitive-Emotional Disturbances and Tissue Injury following a Transient Hypoxic-Ischemic Insult in the Rat. Aguilar-Peralta AK, Gonzalez-Vazquez A, Tomas-Sanchez C, Blanco-Alvarez VM, Martinez-Fong D, Gonzalez-Barrios JA, Limon ID, Millán-Perez Peña L, Flores G, Soto-Rodriguez G, Brambila E, Cebada J, Vargas-Castro V, Leon-Chavez BA. Behav Neurol 2022 5388944 (2022)
  30. Review and Hypothesis: A Potential Common Link Between Glial Cells, Calcium Changes, Modulation of Synaptic Transmission, Spreading Depression, Migraine, and Epilepsy-H. Malchow RP, Tchernookova BK, Choi JV, Smith PJS, Kramer RH, Kreitzer MA. Front Cell Neurosci 15 693095 (2021)
  31. Sex bias in social deficits, neural circuits and nutrient demand in Cttnbp2 autism models. Yen TL, Huang TN, Lin MH, Hsu TT, Lu MH, Shih PY, Ellegood J, Lerch J, Hsueh YP. Brain 146 2612-2626 (2023)
  32. Structural insights into assembly and function of GluN1-2C, GluN1-2A-2C, and GluN1-2D NMDARs. Chou TH, Kang H, Simorowski N, Traynelis SF, Furukawa H. Mol Cell 82 4548-4563.e4 (2022)
  33. Structural insights into binding of therapeutic channel blockers in NMDA receptors. Chou TH, Epstein M, Michalski K, Fine E, Biggin PC, Furukawa H. Nat Struct Mol Biol 29 507-518 (2022)
  34. Zinc supplementation affects favorably the frequency of migraine attacks: a double-blind randomized placebo-controlled clinical trial. Ahmadi H, Mazloumi-Kiapey SS, Sadeghi O, Nasiri M, Khorvash F, Mottaghi T, Askari G. Nutr J 19 101 (2020)


Quick links