Inter- and intrasubunit interactions between transmembrane helices in the open state of P2X receptor channels

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

Volumn 110, Issue 42, 2013, Pages

  Heymann, Gabriel ^a   Dai, Jian ^b,c   Li, Mufeng ^a   Silberberg, Shai D ^a   Zhou, Huan Xiang ^b,c   Swartz, Kenton J ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

^c Florida State University   (United States)

Author keywords

Pore opening mechanism; Transmembrane intersubunit crevices

Indexed keywords

ADENOSINE TRIPHOSPHATE; PURINERGIC P2X RECEPTOR;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; INTERSUBUNIT INTERACTION; INTRASUBUNIT INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; TRANSMEMBRANE HELIX; ZEBRA FISH;

PORE-OPENING MECHANISM; TRANSMEMBRANE INTERSUBUNIT CREVICES;

ADENOSINE TRIPHOSPHATE; ANIMALS; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, PURINERGIC P2X4; ZEBRAFISH;

EID: 84885767038     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1311071110     Document Type: Article

References (38)

1. Khakh BS, North RA (2012) Neuromodulation by extracellular ATP and P2X receptors in the CNS. Neuron 76(1): 51-69.
2. Jiang R, Taly A, Grutter T (2013) Moving through the gate in ATP-activated P2X receptors. Trends Biochem Sci 38(1): 20-29.
3. Surprenant A, North RA (2009) Signaling at purinergic P2X receptors. Annu Rev Physiol 71: 333-359.
4. 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(7255): 592-598.
5. Hattori M, Gouaux E (2012) Molecular mechanism of ATP binding and ion channel activation in P2X receptors. Nature 485(7397): 207-212.
6. Li M, Chang TH, Silberberg SD, Swartz KJ (2008) Gating the pore of P2X receptor channels. Nat Neurosci 11(8): 883-887.
7. Li M, Kawate T, Silberberg SD, Swartz KJ (2010) Pore-opening mechanism in trimeric P2X receptor channels. Nat Commun 1: 44.
8. Kracun S, Chaptal V, Abramson J, Khakh BS (2010) Gated access to the pore of a P2X receptor: Structural implications for closed-open transitions. J Biol Chem 285(13): 10110-10121.
9. Kawate T, Robertson JL, Li M, Silberberg SD, Swartz KJ (2011) Ion access pathway to the transmembrane pore in P2X receptor channels. J Gen Physiol 137(6): 579-590.
10. Samways DS, Khakh BS, Dutertre S, Egan TM (2011) Preferential use of unobstructed lateral portals as the access route to the pore of human ATP-gated ion channels (P2X receptors). Proc Natl Acad Sci USA 108(33): 13800-13805.
11. Jiang R, et al. (2011) Agonist trapped in ATP-binding sites of the P2X2 receptor. Proc Natl Acad Sci USA 108(22): 9066-9071.
12. Du J, Dong H, Zhou HX (2012) Gating mechanism of a P2X4 receptor developed from normal mode analysis and molecular dynamics simulations. Proc Natl Acad Sci USA 109(11): 4140-4145.
13. Lörinczi E, et al. (2012) Involvement of the cysteine-rich head domain in activation and desensitization of the P2X1 receptor. Proc Natl Acad Sci USA 109(28): 11396-11401.
14. Jiang R, et al. (2012) Tightening of the ATP-binding sites induces the opening of P2X receptor channels. EMBO J 31(9): 2134-2143.
15. Zhou HX, Cross TA (2013) Influences of membrane mimetic environments on membrane protein structures. Annu Rev Biophys 42: 361-392.
16. Liang X, et al. (2013) Functional Identification of Close Proximity Amino Acid Side Chains within the Transmembrane-Spanning Helixes of the P2X2 Receptor. PLoS ONE 8(8):e70629.
17. Arnold FH, Haymore BL (1991) Engineered metal-binding proteins: Purification to protein folding. Science 252(5014): 1796-1797.
18. Suh SS, Haymore BL, Arnold FH (1991) Characterization of His-X3-His sites in alphahelices of synthetic metal-binding bovine somatotropin. Protein Eng 4(3): 301-305.
19. Taraska JW, Puljung MC, Olivier NB, Flynn GE, Zagotta WN (2009) Mapping the structure and conformational movements of proteins with transition metal ion FRET. Nat Methods 6(7): 532-537.
20. Holmgren M, Shin KS, Yellen G (1998) The activation gate of a voltage-gated K+ channel can be trapped in the open state by an intersubunit metal bridge. Neuron 21(3): 617-621.
21. Browne LE, Compan V, Bragg L, North RA (2013) P2X7 receptor channels allow direct permeation of nanometer-sized dyes. J Neurosci 33(8): 3557-3566.
22. Virginio C, MacKenzie A, Rassendren FA, North RA, Surprenant A (1999) Pore dilation of neuronal P2X receptor channels. Nat Neurosci 2(4): 315-321.
23. Khakh BS, Bao XR, Labarca C, Lester HA (1999) Neuronal P2X transmitter-gated cation channels change their ion selectivity in seconds. Nat Neurosci 2(4): 322-330.
24. Villarroel A, Burnashev N, Sakmann B (1995) Dimensions of the narrow portion of a recombinant NMDA receptor channel. Biophys J 68(3): 866-875.
25. Zhou Y, Morais-Cabral JH, Kaufman A, MacKinnon R (2001) Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 A resolution. Nature 414(6859): 43-48.
26. Payandeh J, Gamal El-Din TM, Scheuer T, Zheng N, Catterall WA (2012) Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 486(7401): 135-139.
27. Silberberg SD, Li M, Swartz KJ (2007) Ivermectin Interaction with transmembrane helices reveals widespread rearrangements during opening of P2X receptor channels. Neuron 54(2): 263-274.
28. Silberberg SD, Chang TH, Swartz KJ (2005) Secondary structure and gating rearrangements of transmembrane segments in rat P2X4 receptor channels. J Gen Physiol 125(4): 347-359.
29. Cao L, Broomhead HE, Young MT, North RA (2009) Polar residues in the second transmembrane domain of the rat P2X2 receptor that affect spontaneous gating, unitary conductance, and rectification. J Neurosci 29(45): 14257-14264.
30. Jo S, Kim T, Iyer VG, ImW (2008) CHARMM-GUI: A web-based graphical user interface for CHARMM. J Comput Chem 29(11): 1859-1865.
31. Humphrey W, Dalke A. Schulten K. (1996) VMD: Visual molecular dynamics. J Mol Graph 14(1): 33-38.
32. Phillips JC, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26(16): 1781-1802.
33. Mackerell AD, Jr., Feig M, Brooks CL, 3rd (2004) Extending the treatment of backbone energetics in protein force fields: Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comput Chem 25(11): 1400-1415.
34. Klauda JB, et al. (2010) Update of the CHARMM all-atom additive force field for lipids: Validation on six lipid types. J Phys Chem B 114(23): 7830-7843.
35. Pavelites JJ, Gao J, Bash PA, Mackerell AD (1997) A molecular mechanics force field for NAD+, NADH, and the pyrophosphate groups of nucleotides. J Comput Chem 18(2): 221-239.
36. Smart OS, Neduvelil JG, Wang X, Wallace BA, Sansom MS (1996) HOLE: A program for the analysis of the pore dimensions of ion channel structural models. J Mol Graph 14(6): 354-360, 376.
37. Stoop R, et al. (1999) Contribution of individual subunits to the multimeric P2X(2) receptor: Estimates based on methanethiosulfonate block at T336C. Mol Pharmacol 56(5): 973-981.
38. Nagaya N, Tittle RK, Saar N, Dellal SS, Hume RI (2005) An intersubunit zinc binding site in rat P2X2 receptors. J Biol Chem 280(28): 25982-25993.