The trafficking and targeting of P2X receptors

Frontiers in Cellular Neuroscience

Volumn 7, Issue NOV, 2013, Pages

  Robinson, Lucy E ^a   Murrell Lagnado, Ruth D ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Lipid rafts; P2X receptor targeting; P2X receptor trafficking; Receptor endocytosis; Receptor regulation

Indexed keywords

ANTIDEPRESSANT AGENT; CAVEOLIN 1; PURINERGIC P2X RECEPTOR; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X5 RECEPTOR; PURINERGIC P2X6 RECEPTOR; PURINERGIC P2X7 RECEPTOR;

ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; ENDOPLASMIC RETICULUM; ENDOSOME; HUMAN; LIPID RAFT; LYSOSOME; MEMBRANE TRANSPORT; NONHUMAN; PROTEIN MOTIF; RECEPTOR TRAFFICKING;

EID: 84888346844     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00233     Document Type: Article

References (53)

1. Allsopp, R. C., Lalo, U., and Evans, R. J. (2010). Lipid raft association and cholesterol sensitivity of P2X1-4 receptors for ATP: chimeras and point mutants identify intracellular amino-terminal residues involved in lipid regulation of P2X1 receptors. J. Biol. Chem. 285, 32770-32777. doi: 10.1074/jbc.m110.148940
2. Baines, A., Parkinson, K., Sim, J. A., Bragg, L., Thompson, C. R., and North, R. A. (2013). Functional properties of five Dictyostelium discoideum P2X receptors. J. Biol. Chem. 288, 20992-21000. doi: 10.1074/jbc.m112.
3. Barrera, N. P., Henderson, R. M., Murrell-Lagnado, R. D., and Edwardson, J. M. (2007). The stoichiometry of P2X2/6 receptor heteromers depends on relative subunit expression levels. Biophys. J. 93, 505-512. doi: 10.1529/biophysj.106. 101048
4. Barrera, N. P., Ormond, S. J., Henderson, R. M., Murrell-Lagnado, R. D., and Edwardson, J. M. (2005). Atomic force microscopy imaging demonstrates that P2X2 receptors are trimers but that P2X6 receptor subunits do not oligomerize. J. Biol. Chem. 280, 10759-10765. doi: 10.1074/jbc.m412265200
5. Barth, K., Weinhold, K., Guenther, A., Linge, A., Gereke, M., and Kasper, M. (2008). Characterization of the molecular interaction between caveolin-1 and the P2X receptors 4 and 7 in E10 mouse lung alveolar epithelial cells. Int. J. Biochem. Cell Biol. Cell Biol. 40, 2230-2239. doi: 10.1016/j.biocel.2008.03.001
6. Barth, K., Weinhold, K., Guenther, A., Young, M. T., Schnittler, H., and Kasper, M. (2007). Caveolin-1 influences P2X7 receptor expression and localization in mouse lung alveolar epithelial cells. FEBS J. 274, 3021-3033. doi: 10.1111/j.17424658.2007.05830.x
7. Bo, X., Jiang, L. H., Wilson, H. L., Kim, M., Burnstock, G., Surprenant, A., et al. (2003). Pharmacological and biophysical properties of the human P2X5 receptor. Mol. Pharmacol. 63, 1407-1416. doi: 10.1124/mol.63.6.1407
8. Bobanovic, L. K., Royle, S. J., and Murrell-Lagnado, R. D. (2002). P2X receptor trafficking in neurons is subunit specific. J. Neurosci. 22, 4814-4824.
9. Boumechache, M., Masin, M., Edwardson, J. M., Gorecki, D. C., and MurrellLagnado, R. (2009). Analysis of assembly and trafficking of native p2x4 and p2x7 receptor complexes in rodent immune cells. J. Biol. Chem. 284, 13446-13454. doi: 10.1074/jbc.m901255200
10. Bradley, H. J., Liu, X., Collins, V., Owide, J., Goli, G. R., Smith, M., et al. (2010). Identification of an intracellular microdomain of the P2X7 receptor that is crucial in basolateral membrane targeting in epithelial cells. FEBS Lett. 584, 4740-4744. doi: 10.1016/j.febslet.2010.11.007
11. Chaumont, S., Compan, V., Toulme, E., Richler, E., Housley, G. D., Rassendren, F., et al. (2008). Regulation of P2X2 receptors by the neuronal calcium sensor VILIP1. Sci. Signal. 1, ra8. doi: 10.1126/scisignal.1162329
12. Chaumont, S., Jiang, L. H., Penna, A., North, R. A., and Rassendren, F. (2004). Identification of a trafficking motif involved in the stabilization and polarization of P2X receptors. J. Biol. Chem. 279, 29628-29638. doi: 10.1074/jbc.m403940200
13. Compan, V., Ulmann, L., Stelmashenko, O., Chemin, J., Chaumont, S., and Rassendren, F. (2012). P2X2 and P2X5 subunits define a new heteromeric receptor with P2X7-like properties. J. Neurosci. 32, 4284-4296. doi: 10.1523/jneurosci. 6332-11.2012
14. Denlinger, L. C., Fisette, P. L., Sommer, J. A., Watters, J. J., Prabhu, U., Dubyak, G. R., et al. (2001). Cutting edge: the nucleotidereceptor P2X7 contains multiple proteinand lipid-interaction motifs including a potential binding site for bacterial lipopolysaccharide. J. Immunol. 167, 1871-1876.
15. Denlinger, L. C., Sommer, J. A., Parker, K., Gudipaty, L., Fisette, P. L., Watters, J. W., et al. (2003). Mutation of a dibasic amino acid motif within the C terminus of the P2X7 nucleotide receptor results in trafficking defects and impaired function. J. Immunol. 171, 1304-1311.
16. Ennion, S. J., and Evans, R. J. (2001). Agonist-stimulated internalisation of the ligand-gated ion channel P2X(1) in rat vas deferens. FEBS Lett. 489, 154-158. doi: 10.1016/s0014-5793(01)02102-0
17. Fabbretti, E., D'Arco, M., Fabbro, A., Simonetti, M., Nistri, A., and Giniatullin, R. (2006). Delayed upregulation of ATP P2X3 receptors of trigeminal sensory neurons by calcitonin gene-related peptide. J. Neurosci. 26, 6163-6171. doi: 10. 1523/jneurosci.0647-06.2006
18. Fountain, S. J., Parkinson, K., Young, M. T., Cao, L., Thompson, C. R., and North, R. A. (2007). An intracellular P2X receptor required for osmoregulation in Dictyostelium discoideum. Nature 448, 200-203. doi: 10.1038/nature05926
19. Garcia-Marcos, M., Perez-Andres, E., Tandel, S., Fontanils, U., Kumps, A., Kabre, E., et al. (2006a). Coupling of two pools of P2X7 receptors to distinct intracellular signaling pathways in rat submandibular gland. J. Lipid Res. 47, 705-714. doi: 10. 1194/jlr.m500408-jlr200
20. Garcia-Marcos, M., Pochet, S., Tandel, S., Fontanils, U., Astigarraga, E., FernandezGonzalez, J. A., et al. (2006b). Characterization and comparison of raftlike membranes isolated by two different methods from rat submandibular gland cells. Biochim. Biophys. Acta 1758, 796-806. doi: 10.1016/j.bbamem.2006. 05.008
21. Gnanasekaran, A., Sundukova, M., van den Maagdenberg, A. M., Fabbretti, E., and Nistri, A. (2011). Lipid rafts control P2X3 receptor distribution and function in trigeminal sensory neurons of a transgenic migraine mouse model. Mol. Pain 7:77. doi: 10.1186/1744-8069-7-77
22. Gonnord, P., Delarasse, C., Auger, R., Benihoud, K., Prigent, M., Cuif, M. H., et al. (2009). Palmitoylation of the P2X7 receptor, an ATP-gated channel, controls its expression and association with lipid rafts. FASEB J. 23, 795-805. doi: 10.1096/fj. 08-114637
23. Gu, B. J., Zhang, W. Y., Bendall, L. J., Chessell, I. P., Buell, G. N., and Wiley, J. S. (2000). Expression of P2X(7) purinoceptors on human lymphocytes and monocytes: evidence for nonfunctional P2X(7) receptors. Am. J. Physiol. Cell Physiol. 279, C1189-C1197.
24. Gudipaty, L., Humphreys, B. D., Buell, G., and Dubyak, G. R. (2001). Regulation of P2X(7) nucleotide receptor function in human monocytes by extracellular ions and receptor density. Am. J. Physiol. Cell Physiol. 280, C943-C953.
25. Hickman, S. E., el Khoury, J., Greenberg, S., Schieren, I., and Silverstein, S. C. (1994). P2Z adenosine triphosphate receptor activity in cultured human monocyte-derived macrophages. Blood 84, 2452-2456.
26. Kotnis, S., Bingham, B., Vasilyev, D. V., Miller, S. W., Bai, Y., Yeola, S., et al. (2010). Genetic and functional analysis of human P2X5 reveals a distinct pattern of exon 10 polymorphism with predominant expression of the nonfunctional receptor isoform. Mol. Pharmacol. 77, 953-960. doi: 10.1124/mol.110.063636
27. Kundra, R., and Kornfeld, S. (1999). Asparagine-linked oligosaccharides protect Lamp-1 and Lamp-2 from intracellular proteolysis. J. Biol. Chem. 274, 31039-31046. doi: 10.1074/jbc.274.43.31039
28. Lalo, U., Allsopp, R. C., Mahaut-Smith, M. P., and Evans, R. J. (2010). P2X1 receptor mobility and trafficking; regulation by receptor insertion and activation. J. Neurochem. 113, 1177-1187. doi: 10.1111/j.1471-4159.2010.06730.x
29. Lalo, U., Jones, S., Roberts, J. A., Mahaut-Smith, M. P., and Evans, R. J. (2012). Heat shock protein 90 inhibitors reduce trafficking of ATP-gated P2X1 receptors and human platelet responsiveness. J. Biol. Chem. 287, 32747-32754. doi: 10. 1074/jbc.m112.376566
30. Lalo, U., Roberts, J. A., and Evans, R. J. (2011). Identification of human P2X1 receptor-interacting proteins reveals a role of the cytoskeleton in receptor regulation. J. Biol. Chem. 286, 30591-30599. doi: 10.1074/jbc.m111. 253153
31. Li, J., and Fountain, S. J. (2012). Fluvastatin suppresses native and recombinant human P2X4 receptor function. Purinergic Signal. 8, 311-316. doi: 10. 1007/s11302-011-9289-9
32. Lister, M. F., Sharkey, J., Sawatzky, D. A., Hodgkiss, J. P., Davidson, D. J., Rossi, A. G., et al. (2007). The role of the purinergic P2X7 receptor in inflammation. J. Inflamm. (Lond.) 4:5. doi: 10.1186/1476-9255-4-5
33. Ludlow, M. J., Durai, L., and Ennion, S. J. (2009). Functional characterization of intracellular Dictyostelium discoideum P2X receptors. J. Biol. Chem. 284, 35227-35239. doi: 10.1074/jbc.M109.045674
34. Masin, M., Kerschensteiner, D., Dumke, K., Rubio, M. E., and Soto, F. (2006). Fe65 interacts with P2X2 subunits at excitatory synapses and modulates receptor function. J. Biol. Chem. 281, 4100-4108. doi: 10.1074/jbc.m507735200
35. Miklavc, P., Mair, N., Wittekindt, O. H., Haller, T., Dietl, P., Felder, E., et al. (2011). Fusion-activated Ca2+ entry via vesicular P2X4 receptors promotes fusion pore opening and exocytotic content release in pneumocytes. Proc. Natl. Acad. Sci. USA108,14503-14508. doi:10.1073/pnas.1101039108
36. Ormond, S. J., Barrera, N. P., Qureshi, O. S., Henderson, R. M., Edwardson, J. M., and Murrell-Lagnado, R. D. (2006). An uncharged region within the N terminus of the P2X6 receptor inhibits its assembly and exit from the endoplasmic reticulum. Mol. Pharmacol. 69, 1692-1700. doi: 10.1124/mol.105. 020404
37. Pike, L. J. (2004). Lipid rafts: heterogeneity on the high seas. Biochem. J. 378(Pt 2), 281-292. doi: 10.1042/bj20031672
38. Pike, L. J., Han, X., Chung, K. N., and Gross, R. W. (2002). Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis. Biochemistry 41, 2075-2088. doi: 10.1021/ bi0156557
39. Qureshi, O. S., Paramasivam, A., Yu, J. C., and Murrell-Lagnado, R. D. (2007). Regulation of P2X4 receptors by lysosomal targeting, glycan protection and exocytosis. J. Cell Sci. 120(Pt 21), 3838-3349. doi: 10.1242/jcs. 010348
40. Richler, E., Shigetomi, E., and Khakh, B. S. (2011). Neuronal P2X2 receptors are mobile ATP sensors that explore the plasma membrane when activated. J. Neurosci. 31, 16716-16730. doi: 10.1523/jneurosci.3362-11.2011
41. Royle, S. J., Bobanovic, L. K., and Murrell-Lagnado, R. D. (2002). Identification of a non-canonical tyrosine-based endocytic motif in an ionotropic receptor. J. Biol. Chem. 277, 35378-35385. doi: 10.1074/jbc.m204844200
42. Royle, S. J., Qureshi, O. S., Bobanovic, L. K., Evans, P. R., Owen, D. J., and MurrellLagnado, R. D. (2005). Non-canonical YXXGPhi endocytic motifs: recognition by AP2 and preferential utilization in P2X4 receptors. J. Cell Sci. 118(Pt 14), 3073-3080. doi: 10.1242/jcs.02451
43. Shrivastava, A. N., Triller, A., Sieghart, W., and Sarto-Jackson, I. (2011). Regulation of GABA(A) receptor dynamics by interaction with purinergic P2X(2) receptors. J. Biol. Chem. 286, 14455-14468. doi: 10.1074/jbc.m110.165282
44. Sivaramakrishnan, V., and Fountain, S. J. (2012a). A mechanism of intracellular P2X receptor activation. J. Biol. Chem. 287, 28315-28326. doi: 10.1074/jbc. m112.372565
45. Sivaramakrishnan, V., and Fountain, S. J. (2012b). Intracellular P2X receptors as novel calcium release channels and modulators of osmoregulation in Dictyostelium: a comparison of two common laboratory strains. Channels (Austin) 7, 43-46. doi: 10.4161/chan.22737
46. Smart, M. L., Gu, B., Panchal, R. G., Wiley, J., Cromer, B., Williams, D. A., et al. (2003). P2X7 receptor cell surface expression and cytolytic pore formation are Trafficking and targeting of P2X receptors regulated by a distal C-terminal region. J. Biol. Chem. 278, 8853-8860. doi: 10. 1074/jbc.m211094200
47. Toulme, E., Garcia, A., Samways, D., Egan, T. M., Carson, M. J., and Khakh, B. S. (2010). P2X4 receptors in activated C8-B4 cells of cerebellar microglial origin. J. Gen. Physiol. 135, 333-353. doi: 10.1085/jgp.200910336
48. Toulme, E., and Khakh, B. S. (2012). Imaging P2X4 receptor lateral mobility in microglia: regulation by calcium and p38 MAPK. J. Biol. Chem. 287, 14734-14748. doi: 10.1074/jbc.m111.329334
49. Vacca, F., Giustizieri, M., Ciotti, M. T., Mercuri, N. B., and Volonte, C. (2009). Rapid constitutive and ligand-activated endocytic trafficking of P2X receptor. J. Neurochem. 109, 1031-1041. doi: 10.1111/j.1471-4159.2009.06029.x
50. Vial, C., and Evans, R. J. (2005). Disruption of lipid rafts inhibits P2X1 receptormediated currents and arterial vasoconstriction. J. Biol. Chem. 280, 30705-30711. doi: 10.1074/jbc.m504256200
51. Vial, C., Fung, C. Y., Goodall, A. H., Mahaut-Smith, M. P., and Evans, R. J. (2006). Differential sensitivity of human platelet P2X1 and P2Y1 receptors to disruption of lipid rafts. Biochem. Biophys. Res. Commun. 343, 415-419. doi: 10.1016/j.bbrc. 2006.02.174
52. Weinhold, K., Krause-Buchholz, U., Rodel, G., Kasper, M., and Barth, K. (2010). Interaction and interrelation of P2X7 and P2X4 receptor complexes in mouse lung epithelial cells. Cell. Mol. Life Sci. 67, 2631-2642. doi: 10.1007/s00018-010-0355-1
53. Wiley, J. S., Dao-Ung, L. P., Li, C., Shemon, A. N., Gu, B. J., Smart, M. L., et al. (2003). An Ile-568 to Asn polymorphism prevents normal trafficking and function of the human P2X7 receptor. J. Biol. Chem. 278, 17108-17113. doi: 10. 1074/jbc.m212759200