N-glycosylation determines ionic permeability and desensitization of the TRPV1 capsaicin receptor

Journal of Biological Chemistry

Volumn 287, Issue 26, 2012, Pages 21765-21772

  Veldhuis, Nicholas A ^a   Lew, Michael J ^b   Abogadie, Fe C ^a   Poole, Daniel P ^b   Jennings, Ernest A ^c   Ivanusic, Jason J ^b   Eilers, Helge ^d   Bunnett, Nigel W ^e   McIntyre, Peter ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c JAMES COOK UNIVERSITY   (Australia)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CATIONIC DYES; CELL-TO-CELL VARIABILITY; CONCENTRATION-DEPENDENT; DEGLYCOSYLATION; FUSION PROTEINS; GLYCOSYLATED; HEK293 CELLS; INDIVIDUAL CELLS; INTRACELLULAR CALCIUM; ION CHANNEL; ION SELECTIVITY; IONIC PERMEABILITY; KEY DETERMINANTS; N-GLYCOSYLATION; PERIPHERAL SENSORY; WESTERN BLOTTING; WILD TYPES;

AMINO ACIDS; CELL MEMBRANES; ESTERIFICATION; GLYCOSYLATION;

CYTOLOGY;

CAPSAICIN; VANILLOID RECEPTOR 1;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; HUMAN; HUMAN CELL; ION PERMEABILITY; MALE; NERVE FIBER; NONHUMAN; PERIPHERAL NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN SYNTHESIS; RAT; SENSORY NERVE; SENSORY NERVE CELL;

ANIMALS; BIOTINYLATION; CELL MEMBRANE; COLORING AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENETIC VECTORS; GLYCOSYLATION; HEK293 CELLS; HUMANS; IONS; MALE; MICE; MICE, TRANSGENIC; NEURONS; PEPTIDE-N4-(N-ACETYL-BETA-GLUCOSAMINYL) ASPARAGINE AMIDASE; PERMEABILITY; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RATS; TRPV CATION CHANNELS;

EID: 84862644876     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.342022     Document Type: Article

References (38)

1. Tyrrell, L., Renganathan, M., Dib-Hajj, S. D., and Waxman, S. G. (2001) Glycosylation alters steady-state inactivation of sodium channel Nav1.9/NaN in dorsal root ganglion neurons and is developmentally regulated. J. Neurosci. 21, 9629-9637
2. Freeze, H. H. (2006) Genetic defects in the human glycome. Nat. Rev. Genet. 7, 537-551
3. Kedei, N., Szabo, T., Lile, J. D., Treanor, J. J., Olah, Z., Iadarola, M. J., and Blumberg, P. M. (2001) Analysis of the native quaternary structure of vanilloid receptor 1. J. Biol. Chem. 276, 28613-28619
4. Jahnel, R., Dreger, M., Gillen, C., Bender, O., Kurreck, J., and Hucho, F. (2001) Biochemical characterization of the vanilloid receptor 1 expressed in a dorsal root ganglia derived cell line. Eur J Biochem. 268, 5489-5496
5. Welch, J. M., Simon, S. A., and Reinhart, P. H. (2000) The activation mechanism of rat vanilloid receptor 1 by capsaicin involves the pore domain and differs from the activation by either acid or heat. Proc. Natl. Acad. Sci. U.S.A. 97, 13889-13894
6. Wirkner, K., Hognestad, H., Jahnel, R., Hucho, F., and Illes, P. (2005) Characterization of rat transient receptor potential vanilloid 1 receptors lacking the N-glycosylation site N604. Neuroreport 16, 997-1001
7. 2+ channels TRPV5 and TRPV6. Nephrol. Dial Transplant 23, 3397-3402
8. Chang, Q., Hoefs, S., van der Kemp, A. W., Topala, C. N., Bindels, R. J., and Hoenderop, J. G. (2005) The β-glucuronidase klotho hydrolyzes and activates the TRPV5 channel. Science 310, 490-493
9. Xu, H., Fu, Y., Tian, W., and Cohen, D. M. (2006) Glycosylation of the osmoresponsive transient receptor potential channel TRPV4 on Asn-651 influences membrane trafficking. Am. J. Physiol. Renal Physiol 290, F1103-F1109
10. Koplas, P. A., Rosenberg, R. L., and Oxford, G. S. (1997) The role of calcium in the desensitization of capsaicin responses in rat dorsal root ganglion neurons. J. Neurosci. 17, 3525-3537
11. Studer, M., and McNaughton, P. A. (2010) Modulation of single-channel properties of TRPV1 by phosphorylation. J. Physiol. 588, 3743-3756
12. Binshtok, A. M., Bean, B. P., and Woolf, C. J. (2007) Inhibition of nociceptors by TRPV1-mediated entry of impermeant sodium channel blockers. Nature 449, 607-610
13. Chung, M. K., Güler, A. D., and Caterina, M. J. (2008) TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nat Neurosci 11, 555-564
14. Chen, J., Kim, D., Bianchi, B. R., Cavanaugh, E. J., Faltynek, C. R., Kym, P. R., and Reilly, R. M. (2009) Pore dilation occurs in TRPA1 but not in TRPM8 channels. Mol. Pain 5, 3
15. Banke, T. G., Chaplan, S. R., and Wickenden, A. D. (2010) Dynamic changes in the TRPA1 selectivity filter lead to progressive but reversible pore dilation. Am. J. Physiol. Cell Physiol. 298, C1457-C1468
16. Binshtok, A. M., Gerner, P., Oh, S. B., Puopolo, M., Suzuki, S., Roberson, D. P., Herbert, T., Wang, C. F., Kim, D., Chung, G., Mitani, A. A., Wang, G. K., Bean, B. P., and Woolf, C. J. (2009) Coapplication of lidocaine and the permanently charged sodium channel blocker QX-314 produces a long-lasting nociceptive blockade in rodents. Anesthesiology 111, 127-137
17. McIntyre, P., McLatchie, L. M., Chambers, A., Phillips, E., Clarke, M., Savidge, J., Toms, C., Peacock, M., Shah, K., Winter, J., Weerasakera, N., Webb, M., Rang, H. P., Bevan, S., and James, I. F. (2001) Pharmacological differences between the human and rat vanilloid receptor 1 (VR1). Br J. Pharmacol. 132, 1084-1094
18. Sándor, Z., Varga, A., Horváth, P., Nagy, B., and Szolcsányi, J. (2005) Construction of a stable cell line uniformly expressing the rat TRPV1 receptor. Cell Mol. Biol. Lett. 10, 499-514
19. Dragoni, I., Guida, E., and McIntyre, P. (2006) The cold and menthol receptor TRPM8 contains a functionally important double cysteine motif. J. Biol. Chem. 281, 37353-37360
20. Abramoff, M. D., Magelhaes, P. J., and Ram, S. J. (2004) Image Processing with ImageJ. Biophotonics International 11, 36-42
21. Novakova-Tousova, K., Vyklicky, L., Susankova, K., Benedikt, J., Samad, A., Teisinger, J., and Vlachova, V. (2007) Functional changes in the vanilloid receptor subtype 1 channel during and after acute desensitization. Neuroscience 149, 144-154
22. Cohen, D. M. (2006) Regulation of TRP channels by N-linked glycosylation. Semin Cell Dev. Biol. 17, 630-637
23. Dietrich, A., Mederos y Schnitzler, M., Emmel, J., Kalwa, H., Hofmann, T., and Gudermann, T. (2003) N-linked protein glycosylation is a major determinant for basal TRPC3 and TRPC6 channel activity. J. Biol. Chem. 278, 47842-47852
24. Mandadi, S., Tominaga, T., Numazaki, M., Murayama, N., Saito, N., Armati, P. J., Roufogalis, B. D., and Tominaga, M. (2006) Increased sensitivity of desensitized TRPV1 by PMA occurs through PKCε-mediated phosphorylation at S800. Pain 123, 106-116
25. Cholewinski, A., Burgess, G. M., and Bevan, S. (1993) The role of calcium in capsaicin-induced desensitization in rat cultured dorsal root ganglion neurons. Neuroscience 55, 1015-1023
26. Vyklický, L., Nováková-Tousova, K., Benedikt, J., Samad, A., Touska, F., and Vlachová, V. (2008) Calcium-dependent desensitization of vanilloid receptor TRPV1: a mechanism possibly involved in analgesia induced by topical application of capsaicin. Physiol. Res. 57, S59-S68
27. 2+- dependent desensitization in the vanilloid receptor TRPV1 by calcineurin and cAMP-dependent protein kinase. J. Biol. Chem. 280, 13424-13432
28. Numazaki, M., Tominaga, T., Toyooka, H., and Tominaga, M. (2002) Direct phosphorylation of capsaicin receptor VR1 by protein kinase Cepsilon and identification of two target serine residues. J. Biol. Chem. 277, 13375-13378
29. 2+/ calmodulin-dependent kinase II regulates its vanilloid binding. J. Biol. Chem. 279, 7048-7054
30. Tóth, A., Wang, Y., Kedei, N., Tran, R., Pearce, L. V., Kang, S. U., Jin, M. K., Choi, H. K., Lee, J., and Blumberg, P. M. (2005) Different vanilloid agonists cause different patterns of calcium response in CHO cells heterologously expressing rat TRPV1. Life Sci 76, 2921-2932
31. Lam, P. M., McDonald, J., and Lambert, D. G. (2005) Characterization and comparison of recombinant human and rat TRPV1 receptors: effects of exo- and endocannabinoids. Br J Anaesth 94, 649-656
32. Ursu, D., Knopp, K., Beattie, R. E., Liu, B., and Sher, E. (2010) Pungency of TRPV1 agonists is directly correlated with kinetics of receptor activation and lipophilicity. Eur J Pharmacol 641, 114-122
33. Laínez, S., Valente, P., Ontoria-Oviedo, I., Estévez- Herrera, J., Camprubí-Robles, M., Ferrer-Montiel, A., and Planells-Cases, R. (2010) GABAA receptor-associated protein (GABARAP) modulates TRPV1 expression and channel function and desensitization. FASEB J. 24, 1958-1970
34. Jancso-Gabor, A., Szolcsanyi, J., and Jansco, N. (1967)Asimple method for measuring the amount of azovan blue exuded into the skin in response to an inflammatory stimulus. J Pharm. Pharmacol. 19, 486-487
35. Jancsó, N., Jancsó-Gábor, A., and Szolcsányi, J. (1967) Direct evidence for neurogenic inflammation and its prevention by denervation and by pretreatment with capsaicin. Br. J. Pharmacol. Chemother. 31, 138-151
36. 2+ release in sensory neurons. J. Biol. Chem. 279, 16377-16387
37. Olah, Z., Szabo, T., Karai, L., Hough, C., Fields, R. D., Caudle, R. M., Blumberg, P. M., and Iadarola, M. J. (2001) Ligand-induced dynamic membrane changes and cell deletion conferred by vanilloid receptor 1. J. Biol. Chem. 276, 11021-11030
38. Grant, E. R., Dubin, A. E., Zhang, S. P., Zivin, R. A., and Zhong, Z. (2002) Simultaneous intracellular calcium and sodium flux imaging in human vanilloid receptor 1 (VR1)-transfected human embryonic kidney cells: a method to resolve ionic dependence of VR1-mediated cell death. J. Pharmacol. Exp. Ther. 300, 9-17