Allosteric regulation of the P2X4 receptor channel pore dilation

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 4, 2015, Pages 713-726

  Zemkova, Hana ^a   Khadra, Anmar ^b   Rokic, Milos B ^a,d   Tvrdonova, Vendula ^a   Sherman, Arthur ^c   Stojilkovic, Stanko S ^d  

^a INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^b MCGILL UNIVERSITY   (Canada)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

ATP; Ivermectin; Markov state model; Pore dilation; Purinergic receptor channels; Sensitization of receptors

Indexed keywords

IVERMECTIN; PROTEIN BINDING; PURINERGIC P2X4 RECEPTOR;

ALLOSTERISM; ANIMAL; CHANNEL GATING; CHEMISTRY; GENETICS; HEK293 CELL LINE; HUMAN; KINETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE; RAT;

ALLOSTERIC REGULATION; ANIMALS; HEK293 CELLS; HUMANS; ION CHANNEL GATING; IVERMECTIN; KINETICS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, PURINERGIC P2X4;

EID: 84939885478     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1546-7     Document Type: Article

References (38)

1. Bobanovic LK, Royle SJ, Murrell-Lagnado RD (2002) P2X receptor trafficking in neurons is subunit specific. J Neurosci 22(12):4814–4824
2. Brandle U, Spielmanns P, Osteroth R, Sim J, Surprenant A, Buell G, Ruppersberg JP, Plinkert PK, Zenner HP, Glowatzki E (1997) Desensitization of the P2X(2) receptor controlled by alternative splicing. FEBS Lett 404(2–3):294–298
3. 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. doi:10.1523/JNEUROSCI.2235-12.2013
4. Coddou C, Yan Z, Obsil T, Huidobro-Toro JP, Stojilkovic SS (2011) Activation and regulation of purinergic P2X receptor channels. Pharmacol Rev 63(3):641–683. doi:10.1124/pr.110.003129
5. Compan V, Ulmann L, Stelmashenko O, Chemin J, Chaumont S, Rassendren F (2012) P2X2 and P2X5 subunits define a new heteromeric receptor with P2X7-like properties. J Neurosci 32(12):4284–4296. doi:10.1523/JNEUROSCI.6332-11.2012
6. Fischer W, Wirkner K, Weber M, Eberts C, Koles L, Reinhardt R, Franke H, Allgaier C, Gillen C, Illes P (2003) Characterization of P2X3, P2Y1 and P2Y4 receptors in cultured HEK293-hP2X3 cells and their inhibition by ethanol and trichloroethanol. J Neurochem 85(3):779–790
7. He ML, Gonzalez-Iglesias AE, Stojilkovic SS (2003) Role of nucleotide P2 receptors in calcium signaling and prolactin release in pituitary lactotrophs. J Biol Chem 278(47):46270–46277. doi:10.1074/jbc.M309005200
8. He ML, Zemkova H, Koshimizu TA, Tomic M, Stojilkovic SS (2003) Intracellular calcium measurements as a method in studies on activity of purinergic P2X receptor channels. Am J Physiol Cell Physiol 285(2):C467–C479. doi:10.1152/ajpcell.00042.2003
9. Jacobson KA, Gao ZG, Goblyos A, Ijzerman AP (2011) Allosteric modulation of purine and pyrimidine receptors. Adv Pharmacol 61:187–220. doi:10.1016/B978-0-12-385526-8.00007-2
10. Jelinkova I, Vavra V, Jindrichova M, Obsil T, Zemkova HW, Zemkova H, Stojilkovic SS (2008) Identification of P2X(4) receptor transmembrane residues contributing to channel gating and interaction with ivermectin. Pflugers Arch 456(5):939–950. doi:10.1007/s00424-008-0450-4
11. Jelinkova I, Yan Z, Liang Z, Moonat S, Teisinger J, Stojilkovic SS, Zemkova H (2006) Identification of P2X4 receptor-specific residues contributing to the ivermectin effects on channel deactivation. Biochem Biophys Res Commun 349(2):619–625. doi:10.1016/j.bbrc.2006.08.084
12. Jindrichova M, Vavra V, Obsil T, Stojilkovic SS, Zemkova H (2009) Functional relevance of aromatic residues in the first transmembrane domain of P2X receptors. J Neurochem 109(3):923–934
13. Khadra A, Tomic M, Yan Z, Zemkova H, Sherman A, Stojilkovic SS (2013) Dual gating mechanism and function of P2X7 receptor channels. Biophys J 104(12):2612–2621. doi:10.1016/j.bpj.2013.05.006
14. Khadra A, Yan Z, Coddou C, Tomic M, Sherman A, Stojilkovic SS (2012) Gating properties of the P2X2a and P2X2b receptor channels: experiments and mathematical modeling. J Gen Physiol 139(5):333–348. doi:10.1085/jgp.201110716
15. 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
16. Khakh BS, Lester HA (1999) Dynamic selectivity filters in ion channels. Neuron 23(4):653–658
17. Khakh BS, North RA (2012) Neuromodulation by extracellular ATP and P2X receptors in the CNS. Neuron 76(1):51–69. doi:10.1016/j.neuron.2012.09.024
18. Khakh BS, Proctor WR, Dunwiddie TV, Labarca C, Lester HA (1999) Allosteric control of gating and kinetics at P2X(4) receptor channels. J Neurosci 19(17):7289–7299
19. Klapperstuck M, Buttner C, Schmalzing G, Markwardt F (2001) Functional evidence of distinct ATP activation sites at the human P2X(7) receptor. J Physiol 534(Pt 1):25–35
20. Koshimizu T, Tomic M, Van Goor F, Stojilkovic SS (1998) Functional role of alternative splicing in pituitary P2X2 receptor-channel activation and desensitization. Mol Endocrinol 12(7):901–913
21. Norenberg W, Illes P (2000) Neuronal P2X receptors: localisation and functional properties. Naunyn Schmiedeberg's Arch Pharmacol 362(4–5):324–339
22. North RA (2002) Molecular physiology of P2X receptors. Physiol Rev 82(4):1013–1067
23. Popova M, Trudell J, Li K, Alkana R, Davies D, Asatryan L (2013) Tryptophan 46 is a site for ethanol and ivermectin action in P2X4 receptors. Purinergic Signal 9(4):621–632. doi:10.1007/s11302-013-9373-4
24. Priel A, Silberberg SD (2004) Mechanism of ivermectin facilitation of human P2X4 receptor channels. J Gen Physiol 123(3):281–293
25. Qureshi OS, Paramasivam A, Yu JC, Murrell-Lagnado RD (2007) Regulation of P2X4 receptors by lysosomal targeting, glycan protection and exocytosis. J Cell Sci 120(Pt 21):3838–3849. doi:10.1242/jcs.010348
26. Roger S, Pelegrin P, Surprenant A (2008) Facilitation of P2X7 receptor currents and membrane blebbing via constitutive and dynamic calmodulin binding. J Neurosci 28(25):6393–6401
27. Rokic MB, Stojilkovic SS (2013) Two open states of P2X receptor channels. Front Cell Neurosci 7:215. doi:10.3389/fncel.2013.00215
28. Rokic MB, Stojilkovic SS, Vavra V, Kuzyk P, Tvrdonova V, Zemkova H (2013) Multiple roles of the extracellular vestibule amino acid residues in the function of the rat P2X4 receptor. PLoS One 8(3):e59411. doi:10.1371/journal.pone.0059411
29. Schachter JB, Sromek SM, Nicholas RA, Harden TK (1997) HEK293 human embryonic kidney cells endogenously express the P2Y1 and P2Y2 receptors. Neuropharmacology 36(9):1181–1187
30. 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
31. Stojilkovic SS, Yan Z, Obsil T, Zemkova H (2010) Structural insights into the function of P2X4: an ATP-gated cation channel of neuroendocrine cells. Cell Mol Neurobiol 30(8):1251–1258. doi:10.1007/s10571-010-9568-y
32. Surprenant A, Rassendren F, Kawashima E, North RA, Buell G (1996) The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 272(5262):735–738
33. Toulme E, Soto F, Garret M, Boue-Grabot E (2006) Functional properties of internalization-deficient P2X4 receptors reveal a novel mechanism of ligand-gated channel facilitation by ivermectin. Mol Pharmacol 69(2):576–587
34. Virginio C, MacKenzie A, North RA, Surprenant A (1999) Kinetics of cell lysis, dye uptake and permeability changes in cells expressing the rat P2X7 receptor. J Physiol 519(Pt 2):335–346
35. Virginio C, MacKenzie A, Rassendren FA, North RA, Surprenant A (1999) Pore dilation of neuronal P2X receptor channels. Nat Neurosci 2(4):315–321
36. Yan Z, Khadra A, Li S, Tomic M, Sherman A, Stojilkovic SS (2010) Experimental characterization and mathematical modeling of P2X7 receptor channel gating. J Neurosci 30(42):14213–14224. doi:10.1523/JNEUROSCI.2390-10.2010
37. Yan Z, Li S, Liang Z, Tomic M, Stojilkovic SS (2008) The P2X7 receptor channel pore dilates under physiological ion conditions. J Gen Physiol 132(5):563–573. doi:10.1085/jgp.200810059
38. Zemkova H, Yan Z, Liang Z, Jelinkova I, Tomic M, Stojilkovic SS (2007) Role of aromatic and charged ectodomain residues in the P2X(4) receptor functions. J Neurochem 102(4):1139–1150. doi:10.1111/j.1471-4159.2007.04616.x