Recent progress in understanding the intracellular domain's gating and functional roles in trimeric ligand-gated ion channels.
三聚体配体门控离子通道胞内区域的功能研究进展.
Function
Gating
Intracellular domain
Review
Trimeric ligand-gated ion channels
Journal
Zhejiang da xue xue bao. Yi xue ban = Journal of Zhejiang University. Medical sciences
ISSN: 1008-9292
Titre abrégé: Zhejiang Da Xue Xue Bao Yi Xue Ban
Pays: China
ID NLM: 100927946
Informations de publication
Date de publication:
02 Feb 2024
02 Feb 2024
Historique:
medline:
4
2
2024
pubmed:
4
2
2024
entrez:
3
2
2024
Statut:
aheadofprint
Résumé
Ligand-gated ion channels are a large category of essential ion channels, whose superfamily members may modulate their state by binding to specific ligands, allowing specific ions to pass through the cell membrane. Purinergic ligand- gated ion channel(P2X)and ASIC (acid-sensitive ion channel) are representative members of trimeric ligand-gated ion channels. Recent studies have shown that structural differences in the intracellular domain of P2X receptors (P2XR) may determine the desensitization process. The lateral fenestrations of P2XR potentially serve as a pathway for ion conduction and play a decisive role in ion selectivity. Phosphorylation of numerous amino acid residues in the P2XR is involved in regulating the activity of ion channels. Additionally, the P2XR interacts with other ligand-gated ion channel such as NMDA receptor, GABA receptor, 5-HT 配体门控离子通道是一大类重要的膜蛋白。嘌呤能配体门控离子通道(P2X)受体和酸敏感离子通道(acid-sensing ion channel,ASIC)是三聚体配体门控离子通道的代表成员。P2X受体胞内区域的结构差异可影响脱敏过程,胞内区域的侧窗可作为离子渗透到细胞内的潜在路径并对离子选择性有决定作用,胞内区域众多氨基酸残基的磷酸化参与调节离子通道的活性,此外,胞内区域与N-甲基-D-天冬氨酸受体、γ-氨基丁酸受体、5-羟色胺受体和N型乙酰胆碱受体等其他配体门控离子通道存在相互作用并介导突触可塑性等病理生理过程。ASIC胞内区域的构象变化会暴露胞内信号分子的结合位点并促进代谢信号转导,胞内区域的氨基酸Val16、Ser17、Ile18、Gln19和Ala20可以调节通道上膜表达并参与门控过程,胞内区域的PDZ结构域可与多种细胞内蛋白质如骨架蛋白CIPP和p11相互作用从而参与对受体的调控,胞内区域C端和N端的众多磷酸化位点参与了对受体的调控,此外,胞内区域参与了疼痛、缺血性中风、精神疾病、神经退行性疾病等多种病理生理过程。本文综述了P2X受体和ASIC胞内区域的结构以及在调节离子通道的门控特性和病理生理功能中的作用,以期为三聚体配体门控离子通道的药物研发提供新思路。.
Autres résumés
Type: Publisher
(chi)
配体门控离子通道是一大类重要的膜蛋白。嘌呤能配体门控离子通道(P2X)受体和酸敏感离子通道(acid-sensing ion channel,ASIC)是三聚体配体门控离子通道的代表成员。P2X受体胞内区域的结构差异可影响脱敏过程,胞内区域的侧窗可作为离子渗透到细胞内的潜在路径并对离子选择性有决定作用,胞内区域众多氨基酸残基的磷酸化参与调节离子通道的活性,此外,胞内区域与N-甲基-D-天冬氨酸受体、γ-氨基丁酸受体、5-羟色胺受体和N型乙酰胆碱受体等其他配体门控离子通道存在相互作用并介导突触可塑性等病理生理过程。ASIC胞内区域的构象变化会暴露胞内信号分子的结合位点并促进代谢信号转导,胞内区域的氨基酸Val16、Ser17、Ile18、Gln19和Ala20可以调节通道上膜表达并参与门控过程,胞内区域的PDZ结构域可与多种细胞内蛋白质如骨架蛋白CIPP和p11相互作用从而参与对受体的调控,胞内区域C端和N端的众多磷酸化位点参与了对受体的调控,此外,胞内区域参与了疼痛、缺血性中风、精神疾病、神经退行性疾病等多种病理生理过程。本文综述了P2X受体和ASIC胞内区域的结构以及在调节离子通道的门控特性和病理生理功能中的作用,以期为三聚体配体门控离子通道的药物研发提供新思路。.
Identifiants
pubmed: 38310082
doi: 10.3724/zdxbyxb-2023-0472
doi:
Types de publication
Journal Article
Langues
eng
chi
Sous-ensembles de citation
IM
Pagination
1-10Références
ZHANG T, LIU Q, LI Z, et al. The role of ion channels in immune-related diseases[J]. Prog Biophys Mol Biol, 2023, 177: 129- 140. /mixed-citation>
doi: 10.1016/j.pbiomolbio.2022.11.003
FOSTER V S, RASH L D, KING G F, et al. Acid-sensing ion channels: expression and function in resident and infiltrating immune cells in the central nervous system[J]. Front Cell Neurosci, 2021, 15: 738043. /mixed-citation>
doi: 10.3389/fncel.2021.738043
ZOU Y, YANG R, LI L, et al. Purinergic signaling: a potential therapeutic target for depression and chronic pain[J]. Purinergic Signal, 2023, 19(1): 163- 172. /mixed-citation>
doi: 10.1007/s11302-021-09801-x
WU P, WANG Y, LIU Y, et al. Emerging roles of the P2X7 receptor in cancer pain[J]. Purinergic Signal, 2023, 19(2): 441- 450. /mixed-citation>
doi: 10.1007/s11302-022-09902-1
YI B, WANG S, LI W, et al. Potential applications of P2X3 receptor antagonists in the treatment of refractory cough[J]. Respir Med, 2023, 217: 107336. /mixed-citation>
doi: 10.1016/j.rmed.2023.107336
HEUSSER S A, PLESS S A. Acid-sensing ion channels as potential therapeutic targets[J]. Trends Pharmacol Sci, 2021, 42(12): 1035- 1050. /mixed-citation>
doi: 10.1016/j.tips.2021.09.008
ORTEGA-RAMÍREZ A, VEGA R, SOTO E. Acid-sensing ion channels as potential therapeutic targets in neurodegeneration and neuroinflammation[J]. Mediators Inflamm, 2017, 2017: 3728096. /mixed-citation>
doi: 10.1155/2017/3728096
SIVCEV S, KUDOVA E, ZEMKOVA H. Neurosteroids as positive and negative allosteric modulators of ligand-gated ion channels: P2X receptor perspective[J]. Neuropharmacology, 2023, 234: 109542. /mixed-citation>
doi: 10.1016/j.neuropharm.2023.109542
MANSOOR S E, LÜ W, OOSTERHEERT W, et al. X-ray structures define human P2X(3) receptor gating cycle and antagonist action[J]. Nature, 2016, 538(7623): 66- 71. /mixed-citation>
doi: 10.1038/nature19367
MCCARTHY A E, YOSHIOKA C, MANSOOR S E. Full-Length P2X7 Structures Reveal How Palmitoylation Prevents Channel Desensitization[J]. Cell, 2019, 179(3): 659- 670.e13. /mixed-citation>
doi: 10.1016/j.cell.2019.09.017
SHEN C, ZHANG Y, CUI W, et al. Structural insights into the allosteric inhibition of P2X4 receptors[J]. Nat Commun, 2023, 14(1): 6437. /mixed-citation>
doi: 10.1038/s41467-023-42164-y
SHENG D, HATTORI M. Recent progress in the structural biology of P2X receptors[J]. Proteins, 2022, 90(10): 1779- 1785. /mixed-citation>
doi: 10.1002/prot.26302
JASTI J, FURUKAWA H, GONZALES E B, et al. Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH[J]. Nature, 2007, 449(7160): 316- 323. /mixed-citation>
doi: 10.1038/nature06163
BACONGUIS I, BOHLEN C J, GOEHRING A, et al. X-ray structure of acid-sensing ion channel 1-snake toxin complex reveals open state of a Na(+)-selective channel[J]. Cell, 2014, 156(4): 717- 729. /mixed-citation>
doi: 10.1016/j.cell.2014.01.011
DAWSON R J, BENZ J, STOHLER P, et al. Structure of the acid-sensing ion channel 1 in complex with the gating modifier Psalmotoxin 1[J]. Nat Commun, 2012, 3: 936. /mixed-citation>
doi: 10.1038/ncomms1917
BACONGUIS I, GOUAUX E. Structural plasticity and dynamic selectivity of acid-sensing ion channel-spider toxin complexes[J]. Nature, 2012, 489(7416): 400- 405. /mixed-citation>
doi: 10.1038/nature11375
LIU Y, MA J, DESJARLAIS R L, et al. Molecular mechanism and structural basis of small-molecule modulation of the gating of acid-sensing ion channel 1[J]. Commun Biol, 2021, 4(1): 174. /mixed-citation>
doi: 10.1038/s42003-021-01678-1
SOBOLEVSKY A I, ROSCONI M P, GOUAUX E. X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor[J]. Nature, 2009, 462(7274): 745- 756. /mixed-citation>
doi: 10.1038/nature08624
GREGER I H, WATSON J F, CULL-CANDY S G. Structural and Functional Architecture of AMPA-Type Glutamate Receptors and Their Auxiliary Proteins[J]. Neuron, 2017, 94(4): 713- 730. /mixed-citation>
doi: 10.1016/j.neuron.2017.04.009
AITTONIEMI J, JENSEN M Ø, PAN A C, et al. Desensitization dynamics of the AMPA receptor[J]. Structure, 2023, 31(6): 724- 734.e3. /mixed-citation>
doi: 10.1016/j.str.2023.03.013
ZHOU C, TAJIMA N. Structural insights into NMDA receptor pharmacology[J]. Biochem Soc Trans, 2023, 51(4): 1713- 1731. /mixed-citation>
doi: 10.1042/bst20230122
MASTERNAK M, KOCH A, LAULUMAA S, et al. Differences between the GluD1 and GluD2 receptors revealed by GluD1 X-ray crystallography, binding studies and molecular dynamics[J]. FEBS J, 2023, 290(15): 3781- 3801. /mixed-citation>
doi: 10.1111/febs.16631
HASSAINE G, DELUZ C, GRASSO L, et al. X-ray structure of the mouse serotonin 5-HT3 receptor[J]. Nature, 2014, 512(7514): 276- 281. /mixed-citation>
doi: 10.1038/nature13552
ZHU S, NOVIELLO C M, TENG J, et al. Structure of a human synaptic GABA
doi: 10.1038/s41586-018-0255-3
TEREJKO K, KACZOR P T, MICHAŁOWSKI M A, et al. The C loop at the orthosteric binding site is critically involved in GABAA receptor gating[J]. Neuropharmacology, 2020, 166: 107903. /mixed-citation>
doi: 10.1016/j.neuropharm.2019.107903
YU J, ZHU H, LAPE R, et al. Mechanism of gating and partial agonist action in the glycine receptor[J]. Cell, 2021, 184(4): 957- 968.e21. /mixed-citation>
doi: 10.1016/j.cell.2021.01.026
HUANG X, CHEN H, MICHELSEN K, et al. Crystal structure of human glycine receptor-α3 bound to antagonist strychnine[J]. Nature, 2015, 526(7572): 277- 280. /mixed-citation>
doi: 10.1038/nature14972
GONZALES E B, KAWATE T, GOUAUX E. Pore architecture and ion sites in acid-sensing ion channels and P2X receptors[J]. Nature, 2009, 460(7255): 599- 604. /mixed-citation>
doi: 10.1038/nature08218
LIU J P, LIU S C, HU S Q, et al. ATP ion channel P2X purinergic receptors in inflammation response[J]. Biomed Pharmacother, 2023, 158: 114205. /mixed-citation>
doi: 10.1016/j.biopha.2022.114205
KAWATE T, MICHEL J C, BIRDSONG W T, et al. Crystal structure of the ATP-gated P2X(4) ion channel in the closed state[J]. Nature, 2009, 460(7255): 592- 598. /mixed-citation>
doi: 10.1038/nature08198
HATTORI M, GOUAUX E. Molecular mechanism of ATP binding and ion channel activation in P2X receptors[J]. Nature, 2012, 485(7397): 207- 212. /mixed-citation>
doi: 10.1038/nature11010
SATTLER C, BENNDORF K. Enlightening activation gating in P2X receptors[J]. Purinergic Signal, 2022, 18(2): 177- 191. /mixed-citation>
doi: 10.1007/s11302-022-09850-w
WANG J, YU Y. Insights into the channel gating of P2X receptors from structures, dynamics and small molecules[J]. Acta Pharmacol Sin, 2016, 37(1): 44- 55. /mixed-citation>
doi: 10.1038/aps.2015.127
MANSOOR S E. How structural biology has directly impacted our understanding of P2X receptor function and gating[J]. Methods Mol Biol, 2022, 2510: 1- 29. /mixed-citation>
doi: 10.1007/978-1-0716-2384-8_1
SMITH F M, HUMPHREY P P, MURRELL-LAGNADO R D. Identification of amino acids within the P2X2 receptor C-terminus that regulate desensitization[J]. J Physiol, 1999, 520 Pt 1(Pt 1): 91- 99. /mixed-citation>
doi: 10.1111/j.1469-7793.1999.00091.x
ZEMKOVA H, HE M L, KOSHIMIZU T A, et al. Identification of ectodomain regions contributing to gating, deactivation, and resensitization of purinergic P2X receptors[J]. J Neurosci, 2004, 24(31): 6968- 6978. /mixed-citation>
doi: 10.1523/jneurosci.1471-04.2004
TAM S W, HUFFER K, LI M, et al. Ion permeation pathway within the internal pore of P2X receptor channels[J/OL]. Elife, 2023, 12: e84796. /mixed-citation>
doi: 10.7554/elife.84796
YAFFE M B. Phosphotyrosine-binding domains in signal transduction[J]. Nat Rev Mol Cell Biol, 2002, 3(3): 177- 186. /mixed-citation>
doi: 10.1038/nrm759
RODRIGUEZ L, YI C, CHU C, et al. Cross-talk between P2X and NMDA receptors[J]. Int J Mol Sci, 2020, 21(19): 7187. /mixed-citation>
doi: 10.3390/ijms21197187
POUGNET J T, COMPANS B, MARTINEZ A, et al. P2X-mediated AMPA receptor internalization and synaptic depression is controlled by two CaMKⅡ phosphorylation sites on GluA1 in hippocampal neurons[J]. Sci Rep, 2016, 6: 31836. /mixed-citation>
doi: 10.1038/srep31836
TOULMÉ E, BLAIS D, LÉGER C, et al. An intra-cellular motif of P2X(3) receptors is required for functional cross-talk with GABA(A) receptors in noci-ceptive DRG neurons[J]. J Neurochem, 2007, 102(4): 1357- 1368. /mixed-citation>
doi: 10.1111/j.1471-4159.2007.04640.x
EMERIT M B, BARANOWSKI C, DIAZ J, et al. A new mechanism of receptor targeting by interaction between two classes of ligand-gated ion channels[J]. J Neurosci, 2016, 36(5): 1456- 1470. /mixed-citation>
doi: 10.1523/jneurosci.2390-15.2016
DECKER D A, GALLIGAN J J. Molecular mechanisms of cross-inhibition between nicotinic acetylcholine receptors and P2X receptors in myenteric neurons and HEK-293 cells[J]. Neurogastroenterol Motil, 2010, 22(8): 901- 908, e 235. /mixed-citation>
doi: 10.1111/j.1365-2982.2010.01505.x
SIVILS A, YANG F, WANG J Q, et al. Acid-sensing ion channel 2: function and modulation[J]. Membranes (Basel), 2022, 12(2): 113. /mixed-citation>
doi: 10.3390/membranes12020113
VAN BEMMELEN M X, HUSER D, GAUTSCHI I, et al. The human acid-sensing ion channel ASIC1a: evidence for a homotetrameric assembly state at the cell surface[J/OL]. PLoS One, 2015, 10(8): e0135191. /mixed-citation>
doi: 10.1371/journal.pone.0135191
GWIAZDA K, BONIFACIO G, VULLO S, et al. Extra-cellular Subunit interactions control transitions between functional states of acid-sensing ion channel 1a[J]. J Biol Chem, 2015, 290(29): 17956- 17966. /mixed-citation>
doi: 10.1074/jbc.m115.641688
ROOK M L, MUSGAARD M, MACLEAN D M. Coupling structure with function in acid-sensing ion channels: challenges in pursuit of proton sensors[J]. J Physiol, 2021, 599(2): 417- 430. /mixed-citation>
doi: 10.1113/jp278707
YODER N, YOSHIOKA C, GOUAUX E. Gating mecha-nisms of acid-sensing ion channels[J]. Nature, 2018, 555(7696): 397 - 401. /mixed-citation>
doi: 10.1038/nature25782
COUCH T, BERGER K D, KNEISLEY D L, et al. Topography and motion of acid-sensing ion channel intracellular domains[J/OL]. Elife, 2021, 10: e68955. /mixed-citation>
doi: 10.7554/elife.68955
LI W, WANG X, MENG X, et al. The intracellular N-terminal domain of the acid-sensing ion channel 1a participates in channel opening and membrane expression[J]. Mol Pharmacol, 2021, 100(2): 113- 118. /mixed-citation>
doi: 10.1124/molpharm.120.000153
HRUSKA-HAGEMAN A M, BENSON C J, LEONARD A S, et al. PSD-95 and Lin-7b interact with acid-sensing ion channel-3 and have opposite effects on H
doi: 10.1074/jbc.m405874200
DEVAL E, FRIEND V, THIRANT C, et al. Regulation of sensory neuron-specific acid-sensing ion channel 3 by the adaptor protein Na
doi: 10.1074/jbc.m509669200
ANZAI N, DEVAL E, SCHAEFER L, et al. The multivalent PDZ domain-containing protein CIPP is a partner of acid-sensing ion channel 3 in sensory neurons[J]. J Biol Chem, 2002, 277(19): 16655- 16661. /mixed-citation>
doi: 10.1074/jbc.m201087200
CULLINAN M M, KLIPP R C, BANKSTON J R. Regulation of acid-sensing ion channels by protein binding partners[J]. Channels (Austin), 2021, 15(1): 635- 647. /mixed-citation>
doi: 10.1080/19336950.2021.1976946
DEV K K. PDZ domain protein-protein interactions: a case study with PICK1[J]. Curr Top Med Chem, 2007, 7(1): 3- 20. /mixed-citation>
doi: 10.2174/156802607779318343
ZHA X M. Acid-sensing ion channels: trafficking and synaptic function[J]. Mol Brain, 2013, 6: 1. /mixed-citation>
doi: 10.1186/1756-6606-6-1
LEONARD A S, YERMOLAIEVA O, HRUSKA-HAGEMAN A, et al. cAMP-dependent protein kinase phosphorylation of the acid-sensing ion channel-1 regulates its binding to the protein interacting with C-kinase-1[J]. Proc Natl Acad Sci U S A, 2003, 100(4): 2029- 2034. /mixed-citation>
doi: 10.1073/pnas.252782799
BARON A, DEVAL E, SALINAS M, et al. Protein kinase C stimulates the acid-sensing ion channel ASIC2a via the PDZ domain-containing protein PICK1[J]. J Biol Chem, 2002, 277(52): 50463- 50468. /mixed-citation>
doi: 10.1074/jbc.m208848200
LÓPEZ-RAMÍREZ O, GONZÁLEZ-GARRIDO A. The role of acid sensing ion channels in the cardiovascular function[J]. Front Physiol, 2023, 14: 1194948. /mixed-citation>
doi: 10.3389/fphys.2023.1194948
KLIPP R C, CULLINAN M M, BANKSTON J R. Insights into the molecular mechanisms underlying the inhibition of acid-sensing ion channel 3 gating by stomatin[J/OL]. J Gen Physiol, 2020, 152(3): e201912471. /mixed-citation>
doi: 10.1085/jgp.201912471
VERKEST C, DIOCHOT S, LINGUEGLIA E, et al. C-Jun N-terminal kinase post-translational regulation of pain-related acid-sensing ion channels 1b and 3[J]. J Neurosci, 2021, 41(42): 8673- 8685. /mixed-citation>
doi: 10.1523/jneurosci.0570-21.2021
WANG J J, LIU F, YANG F, et al. Disruption of auto-inhibition underlies conformational signaling of ASIC1a to induce neuronal necroptosis[J]. Nat Commun, 2020, 11(1): 475. /mixed-citation>
doi: 10.1038/s41467-019-13873-0
WANG Y Z, WANG J J, HUANG Y, et al. Tissue acidosis induces neuronal necroptosis via ASIC1a channel independent of its ionic conduction[J/OL]. Elife, 2015, 4: e05682. /mixed-citation>
doi: 10.7554/elife.05682.020
FOCANT M C, HERMANS E. Protein interacting with C kinase and neurological disorders[J]. Synapse, 2013, 67(8): 532- 540. /mixed-citation>
doi: 10.1002/syn.21657
RADU B M, BANCIU A, BANCIU D D, et al. Acid-sensing ion channels as potential pharmacological targets in peripheral and central nervous system diseases[J]. Adv Protein Chem Struct Biol, 2016, 103: 137- 167. /mixed-citation>
doi: 10.1016/bs.apcsb.2015.10.002
GAO J, DUAN B, WANG D G, et al. Coupling between NMDA receptor and acid-sensing ion channel contri-butes to ischemic neuronal death[J]. Neuron, 2005, 48(4): 635- 646. /mixed-citation>
doi: 10.1016/j.neuron.2005.10.011
EVLANENKOV K K, ZHIGULIN A S, TIKHONOV D B. Possible compensatory role of ASICs in glutamatergic synapses[J]. Int J Mol Sci, 2023, 24(16): 12974. /mixed-citation>
doi: 10.3390/ijms241612974
VONDERWALDE I, KOVACS-LITMAN A. Acid-sensing ion channel 1a induces AMPA receptor plasticity: a link between acidotoxicity and excitotoxicity in hippocampal CA1 neurons[J]. J Physiol, 2016, 594(4): 803- 805. /mixed-citation>
doi: 10.1113/jp271814
BOWIE D. Neurotransmitter-gated ion channels, still front and centre stage[J]. J Physiol, 2021, 599(2): 389- 395. /mixed-citation>
doi: 10.1113/jp280800