On the permeation of large organic cations through the pore of ATP-gated P2X receptors

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

Volumn 114, Issue 19, 2017, Pages E3786-E3795

  Harkat, Mahboubi ^a,b   Peverini, Laurie ^a,b   Cerdan, Adrien H ^a,b   Dunning, Kate ^a,b   Beudez, Juline ^a,b   Martz, Adeline ^a,b   Calimet, Nicolas ^a,b   Specht, Alexandre ^a,b   Cecchini, Marco ^a,b   Chataigneau, Thierry ^a,b   Grutter, Thomas ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Photoswitches; Pore dilation; Purinergic receptor; Spermidine; Yo pro uptake

Indexed keywords

ADENOSINE TRIPHOSPHATE; MEGLUMINE; PURINERGIC P2X RECEPTOR; SODIUM ION; SPERMIDINE; GAMMA-GLUTAMYLMETHYLAMIDE; GLUTAMIC ACID DERIVATIVE;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; ION CONDUCTANCE; ION PERMEABILITY; MODULATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; BIOLOGICAL MODEL; CELL MEMBRANE PERMEABILITY; HEK293 CELL LINE; METABOLISM;

CELL MEMBRANE PERMEABILITY; GLUTAMATES; HEK293 CELLS; HUMANS; MODELS, BIOLOGICAL; RECEPTORS, PURINERGIC P2X; SPERMIDINE;

EID: 85019068954     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1701379114     Document Type: Article

References (53)

1. Idzko M, Ferrari D, Eltzschig HK (2014) Nucleotide signalling during inflammation. Nature 509:310-317.
2. Khakh BS, North RA (2012) Neuromodulation by extracellular ATP and P2X receptors in the CNS. Neuron 76:51-69.
3. Wirkner K, Sperlagh B, Illes P (2007) P2X3 receptor involvement in pain states. Mol Neurobiol 36:165-183.
4. Yan D, et al. (2013) Mutation of the ATP-gated P2X (2) receptor leads to progressive hearing loss and increased susceptibility to noise. Proc Natl Acad Sci USA 110:2228-2233.
5. Pijacka W, et al. (2016) Purinergic receptors in the carotid body as a new drug target for controlling hypertension. Nat Med 22:1151-1159.
6. North RA, Jarvis MF (2013) P2X receptors as drug targets. Mol Pharmacol 83:759-769.
7. Kawate T, Michel JC, Birdsong WT, Gouaux E (2009) Crystal structure of the ATP-gated P2X (4) ion channel in the closed state. Nature 460:592-598.
8. Hattori M, Gouaux E (2012) Molecular mechanism of ATP binding and ion channel activation in P2X receptors. Nature 485:207-212.
9. Kasuya G, et al. (2016) Structural insights into divalent cation modulations of ATPgated P2X receptor channels. Cell Reports 14:932-944.
10. Mansoor SE, et al. (2016) X-ray structures define human P2X (3) receptor gating cycle and antagonist action. Nature 538:66-71.
11. Karasawa A, Kawate T (2016) Structural basis for subtype-specific inhibition of the P2X7 receptor. eLife 5:5.
12. Browne LE, Jiang LH, North RA (2010) New structure enlivens interest in P2X receptors. Trends Pharmacol Sci 31:229-237.
13. Habermacher C, Dunning K, Chataigneau T, Grutter T (2016) Molecular structure and function of P2X receptors. Neuropharmacology 104:18-30.
14. Ding S, Sachs F (1999) Single channel properties of P2X2 purinoceptors. J Gen Physiol 113:695-720.
15. Evans RJ (1996) Single channel properties of ATP-gated cation channels (P2X receptors) heterologously expressed in Chinese hamster ovary cells. Neurosci Lett 212:212-214.
16. Riedel T, Schmalzing G, Markwardt F (2007) Influence of extracellular monovalent cations on pore and gating properties of P2X7 receptor-operated single-channel currents. Biophys J 93:846-858.
17. Virginio C, MacKenzie A, Rassendren FA, North RA, Surprenant A (1999) Pore dilation of neuronal P2X receptor channels. Nat Neurosci 2:315-321.
18. Khakh BS, Bao XR, Labarca C, Lester HA (1999) Neuronal P2X transmitter-gated cation channels change their ion selectivity in seconds. Nat Neurosci 2:322-330.
19. Rokic MB, Stojilkovic SS (2013) Two open states of P2X receptor channels. Front Cell Neurosci 7:215.
20. Wei L, Caseley E, Li D, Jiang LH (2016) ATP-induced P2X receptor-dependent large pore formation: How much do we know? Front Pharmacol 7:5.
21. Compan V, et al. (2012) P2X2 and P2X5 subunits define a new heteromeric receptor with P2X7-like properties. J Neurosci 32:4284-4296.
22. Jiang LH, et al. (2005) N-methyl-D-glucamine and propidium dyes utilize different permeation pathways at rat P2X (7) receptors. Am J Physiol Cell Physiol 289:C1295-C1302.
23. Pelegrin P, Surprenant A (2006) Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J 25:5071-5082.
24. Eickhorst AN, Berson A, Cockayne D, Lester HA, Khakh BS (2002) Control of P2X (2) channel permeability by the cytosolic domain. J Gen Physiol 120:119-131.
25. Fisher JA, Girdler G, Khakh BS (2004) Time-resolved measurement of state-specific P2X2 ion channel cytosolic gating motions. J Neurosci 24:10475-10487.
26. Khakh BS, Egan TM (2005) Contribution of transmembrane regions to ATP-gated P2X2 channel permeability dynamics. J Biol Chem 280:6118-6129.
27. Chaumont S, Khakh BS (2008) Patch-clamp coordinated spectroscopy shows P2X2 receptor permeability dynamics require cytosolic domain rearrangements but not Panx-1 channels. Proc Natl Acad Sci USA 105:12063-12068.
28. Yan Z, Li S, Liang Z, Tomić M, Stojilkovic SS (2008) The P2X7 receptor channel pore dilates under physiological ion conditions. J Gen Physiol 132:563-573.
29. Shinozaki Y, et al. (2009) Direct observation of ATP-induced conformational changes in single P2X (4) receptors. PLoS Biol 7:e1000103.
30. Khadra A, et al. (2012) Gating properties of the P2X2a and P2X2b receptor channels: Experiments and mathematical modeling. J Gen Physiol 139:333-348.
31. Browne LE, Compan V, Bragg L, North RA (2013) P2X7 receptor channels allow direct permeation of nanometer-sized dyes. J Neurosci 33:3557-3566.
32. Li M, Toombes GE, Silberberg SD, Swartz KJ (2015) Physical basis of apparent pore dilation of ATP-activated P2X receptor channels. Nat Neurosci 18:1577-1583.
33. Ding S, Sachs F (1999) Ion permeation and block of P2X (2) purinoceptors: Single channel recordings. J Membr Biol 172:215-223.
34. Sorge RE, et al. (2012) Genetically determined P2X7 receptor pore formation regulates variability in chronic pain sensitivity. Nat Med 18:595-599.
35. Li M, Chang TH, Silberberg SD, Swartz KJ (2008) Gating the pore of P2X receptor channels. Nat Neurosci 11:883-887.
36. Habermacher C, et al. (2016) Photo-switchable tweezers illuminate pore-opening motions of an ATP-gated P2X ion channel. eLife 5:e11050.
37. Browne LE, et al. (2014) Optical control of trimeric P2X receptors and acid-sensing ion channels. Proc Natl Acad Sci USA 111:521-526.
38. Guerra GP, Rubin MA, Mello CF (2016) Modulation of learning and memory by natural polyamines. Pharmacol Res 112:99-118.
39. Pippel A, et al. (2017) Localization of the gate and selectivity filter of the full-length P2X7 receptor. Proc Natl Acad Sci USA 114:E2156-E2165.
40. Clyne JD, Brown TC, Hume RI (2003) Expression level dependent changes in the properties of P2X2 receptors. Neuropharmacology 44:403-412.
41. Fujiwara Y, Kubo Y (2004) Density-dependent changes of the pore properties of the P2X2 receptor channel. J Physiol 558:31-43.
42. Tochitsky I, et al. (2016) How azobenzene photoswitches restore visual responses to the blind retina. Neuron 92:100-113.
43. Jiang R, et al. (2010) A putative extracellular salt bridge at the subunit interface contributes to the ion channel function of the ATP-gated P2X2 receptor. J Biol Chem 285:15805-15815.
44. Harvey MJ, Giupponi G, Fabritiis GD (2009) ACEMD: Accelerating biomolecular dynamics in the microsecond time scale. J Chem Theory Comput 5:1632-1639.
45. Heymann G, et al. (2013) Inter- and intrasubunit interactions between transmembrane helices in the open state of P2X receptor channels. Proc Natl Acad Sci USA 110:E4045-E4054.
46. Roitberg A, Elber R (1991) Modeling side chains in peptides and proteins: Application of locally enhanced sampling and simulated annealing methods to find minimum energy conformations. J Chem Phys 95:9277-9287.
47. Phillips JC, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26:1781-1802.
48. Best RB, et al. (2012) Optimization of the additive CHARMM all-atom protein force field targeting improved sampling of the backbone φ, Ψ and side-chain χ (1) and χ (2) dihedral angles. J Chem Theory Comput 8:3257-3273.
49. Vanommeslaeghe K, et al. (2010) CHARMM general force field: A force field for druglike molecules compatible with the CHARMM all-atom additive biological force fields. J Comput Chem 31:671-690.
50. Humphrey W, Dalke A, Schulten K (1996) VMD: Visual molecular dynamics. J Mol Graph 14:27-38.
51. Onasch F, et al. (1984) The interactions between nucleic acids and polyamines. III. Microscopic protonation constants of spermidine. Biophys Chem 19:245-253.
52. Roux B (2008) The membrane potential and its representation by a constant electric field in computer simulations. Biophys J 95:4205-4216.
53. Smart OS, Neduvelil JG, Wang X, Wallace BA, Sansom MS (1996) HOLE: A program for the analysis of the pore dimensions of ion channel structuralmodels. J Mol Graph 14:354-360, 376.