AKAP150-mediated TRPV1 sensitization is disrupted by calcium/calmodulin

Molecular Pain

Volumn 7, Issue , 2011, Pages

  Chaudhury, Sraboni ^a   Bal, Manjot ^a   Belugin, Sergei ^a   Shapiro, Mark S ^a   Jeske, Nathaniel A ^a,b  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CALCIUM; CALMODULIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN 150; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; AKAP5 PROTEIN, RAT; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; TRPV1 PROTEIN, RAT; VANILLOID RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CALCIUM CELL LEVEL; CHO CELL; CONTROLLED STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; RECEPTOR UPREGULATION; TRIGEMINAL NERVE; WILD TYPE; ANIMAL; CELL MEMBRANE; CRICETULUS; DRUG ANTAGONISM; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE DELETION; HAMSTER; INTRACELLULAR SPACE; METABOLISM; PROTEIN BINDING; SPRAGUE DAWLEY RAT;

A KINASE ANCHOR PROTEINS; ANIMALS; BINDING SITES; CALCIUM; CALMODULIN; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; FLUORESCENCE RESONANCE ENERGY TRANSFER; INTRACELLULAR SPACE; MALE; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; SEQUENCE DELETION; TRPV CATION CHANNELS;

EID: 79955821040     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-7-34     Document Type: Article

References (43)

1. Carlton SM, Coggeshall RE. Peripheral capsaicin receptors increase in the inflamed rat hindpaw: a possible mechanism for peripheral sensitization. Neurosci Lett 2001, 310(1):53-56. 10.1016/S0304-3940(01)02093-6, 11524156.
2. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389(6653):816-824. 10.1038/39807, 9349813.
3. Caterina MJ, Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 2001, 24:487-517. 10.1146/annurev.neuro.24.1.487, 11283319.
4. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 1998, 21(3):531-543. 10.1016/S0896-6273(00)80564-4, 9768840.
5. Price TJ, Patwardhan A, Akopian AN, Hargreaves KM, Flores CM. Modulation of trigeminal sensory neuron activity by the dual cannabinoid-vanilloid agonists anandamide, N-arachidonoyl-dopamine and arachidonyl-2-chloroethylamide. Br J Pharmacol 2004, 141(7):1118-1130. 10.1038/sj.bjp.0705711, 1574881,1574881, 15006899.
6. Ross RA, Gibson TM, Brockie HC, Leslie M, Pashmi G, Craib SJ, Di Marzo V, Pertwee RG. Structure-activity relationship for the endogenous cannabinoid, anandamide, and certain of its analogues at vanilloid receptors in transfected cells and vas deferens. Br J Pharmacol 2001, 132(3):631-640. 10.1038/sj.bjp.0703850, 1572597, 11159715.
7. Patwardhan AM, Akopian AN, Ruparel NB, Diogenes A, Weintraub ST, Uhlson C, Murphy RC, Hargreaves KM. Heat generates oxidized linoleic acid metabolites that activate TRPV1 and produce pain in rodents. J Clin Invest 2010, 120(5):1617-1626. 10.1172/JCI41678, 2860941, 20424317.
8. Bhave G, Hu HJ, Glauner KS, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau R. Protein kinase C phosphorylation sensitizes but does not activate the capsaicin receptor transient receptor potential vanilloid 1 (TRPV1). Proc Natl Acad Sci USA 2003, 100(21):12480-12485. 10.1073/pnas.2032100100, 218783, 14523239.
9. Numazaki M, Tominaga T, Toyooka H, Tominaga M. Direct phosphorylation of capsaicin receptor VR1 by protein kinase Cepsilon and identification of two target serine residues. J Biol Chem 2002, 277(16):13375-13378. 10.1074/jbc.C200104200, 11884385.
10. Premkumar LS, Ahern GP. Induction of vanilloid receptor channel activity by protein kinase C. Nature 2000, 408(6815):985-990. 10.1038/35050121, 11140687.
11. Bhave G, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau R. cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 2002, 35(4):721-731. 10.1016/S0896-6273(02)00802-4, 12194871.
12. De Petrocellis L, Harrison S, Bisogno T, Tognetto M, Brandi I, Smith GD, Creminon C, Davis JB, Geppetti P, Di Marzo V. The vanilloid receptor (VR1)-mediated effects of anandamide are potently enhanced by the cAMP-dependent protein kinase. J Neurochem 2001, 77(6):1660-1663. 10.1046/j.1471-4159.2001.00406.x, 11413249.
13. Rathee PK, Distler C, Obreja O, Neuhuber W, Wang GK, Wang SY, Nau C, Kress M. PKA/AKAP/VR-1 module: A common link of Gs-mediated signaling to thermal hyperalgesia. J Neurosci 2002, 22(11):4740-4745.
14. Goswami C, Dreger M, Jahnel R, Bogen O, Gillen C, Hucho F. Identification and characterization of a Ca2+ -sensitive interaction of the vanilloid receptor TRPV1 with tubulin. J Neurochem 2004, 91(5):1092-1103. 10.1111/j.1471-4159.2004.02795.x, 15569253.
15. Kim AY, Tang Z, Liu Q, Patel KN, Maag D, Geng Y, Dong X. Pirt, a phosphoinositide-binding protein, functions as a regulatory subunit of TRPV1. Cell 2008, 133(3):475-485. 10.1016/j.cell.2008.02.053, 2605970, 18455988.
16. Jeske NA, Diogenes A, Ruparel NB, Fehrenbacher JC, Henry M, Akopian AN, Hargreaves KM. A-kinase anchoring protein mediates TRPV1 thermal hyperalgesia through PKA phosphorylation of TRPV1. Pain 2008, 138(3):604-616. 10.1016/j.pain.2008.02.022, 2593399, 18381233.
17. Jeske NA, Patwardhan AM, Ruparel NB, Akopian AN, Shapiro MS, Henry MA. A-kinase anchoring protein 150 controls protein kinase C-mediated phosphorylation and sensitization of TRPV1. Pain 2009, 146(3):301-307. 10.1016/j.pain.2009.08.002, 2783249, 19767149.
18. Schnizler K, Shutov LP, Van Kanegan MJ, Merrill MA, Nichols B, McKnight GS, Strack S, Hell JW, Usachev YM. Protein kinase A anchoring via AKAP150 is essential for TRPV1 modulation by forskolin and prostaglandin E2 in mouse sensory neurons. J Neurosci 2008, 28(19):4904-4917. 10.1523/JNEUROSCI.0233-08.2008, 2641040, 18463244.
19. Zhang X, Li L, McNaughton PA. Proinflammatory mediators modulate the heat-activated ion channel TRPV1 via the scaffolding protein AKAP79/150. Neuron 2008, 59(3):450-461. 10.1016/j.neuron.2008.05.015, 18701070.
20. Mohapatra DP, Nau C. Regulation of Ca2+-dependent desensitization in the vanilloid receptor TRPV1 by calcineurin and cAMP-dependent protein kinase. J Biol Chem 2005, 280(14):13424-13432. 10.1074/jbc.M410917200, 15691846.
21. Jeske NA, Patwardhan AM, Gamper N, Price TJ, Akopian AN, Hargreaves KM. Cannabinoid WIN 55,212-2 Regulates TRPV1 Phosphorylation in Sensory Neurons. J Biol Chem 2006, 281(43):32879-32890. 10.1074/jbc.M603220200, 2910918, 16954222.
22. Docherty RJ, Yeats JC, Bevan S, Boddeke HW. Inhibition of calcineurin inhibits the desensitization of capsaicin-evoked currents in cultured dorsal root ganglion neurones from adult rats. Pflugers Arch 1996, 431(6):828-837. 10.1007/s004240050074, 8927498.
23. Lishko PV, Procko E, Jin X, Phelps CB, Gaudet R. The ankyrin repeats of TRPV1 bind multiple ligands and modulate channel sensitivity. Neuron 2007, 54(6):905-918. 10.1016/j.neuron.2007.05.027, 17582331.
24. Numazaki M, Tominaga T, Takeuchi K, Murayama N, Toyooka H, Tominaga M. Structural determinant of TRPV1 desensitization interacts with calmodulin. Proc Natl Acad Sci USA 2003, 100(13):8002-8006. 10.1073/pnas.1337252100, 164702, 12808128.
25. Rosenbaum T, Gordon-Shaag A, Munari M, Gordon SE. Ca2+/calmodulin modulates TRPV1 activation by capsaicin. J Gen Physiol 2004, 123(1):53-62. 2217413, 14699077.
26. Welch EJ, Jones BW, Scott JD. Networking with AKAPs: context-dependent regulation of anchored enzymes. Mol Interv 2010, 10(2):86-97. 10.1124/mi.10.2.6, 2895371, 20368369.
27. Bonnington JK, McNaughton PA. Signalling pathways involved in the sensitisation of mouse nociceptive neurones by nerve growth factor. J Physiol 2003, 551(Pt 2):433-446. 2343223, 12815188.
28. Price TJ, Jeske NA, Flores CM, Hargreaves KM. Pharmacological interactions between calcium/calmodulin-dependent kinase II alpha and TRPV1 receptors in rat trigeminal sensory neurons. Neurosci Lett 2005, 389(2):94-98. 10.1016/j.neulet.2005.07.029, 1892278, 16095822.
29. Gamper N, Li Y, Shapiro MS. Structural requirements for differential sensitivity of KCNQ K+ channels to modulation by Ca2+/calmodulin. Mol Biol Cell 2005, 16(8):3538-3551. 10.1091/mbc.E04-09-0849, 1182296, 15901836.
30. Gamper N, Shapiro MS. Calmodulin mediates Ca2+-dependent modulation of M-type K+ channels. J Gen Physiol 2003, 122(1):17-31. 10.1085/jgp.200208783, 2234471, 12810850.
31. Geiser JR, van Tuinen D, Brockerhoff SE, Neff MM, Davis TN. Can calmodulin function without binding calcium?. Cell 1991, 65(6):949-959. 10.1016/0092-8674(91)90547-C, 2044154.
32. Yamniuk AP, Vogel HJ. Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides. Mol Biotechnol 2004, 27(1):33-57. 10.1385/MB:27:1:33, 15122046.
33. Faux MC, Scott JD. Regulation of the AKAP79-protein kinase C interaction by Ca2+/Calmodulin. J Biol Chem 1997, 272(27):17038-17044. 10.1074/jbc.272.27.17038, 9202019.
34. Wu ZZ, Chen SR, Pan HL. Transient receptor potential vanilloid type 1 activation down-regulates voltage-gated calcium channels through calcium-dependent calcineurin in sensory neurons. J Biol Chem 2005, 280(18):18142-18151.
35. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.
36. Axelrod D. Total internal reflection fluorescence microscopy in cell biology. Methods Enzymol 2003, 361:1-33.
37. Centonze VE, Sun M, Masuda A, Gerritsen H, Herman B. Fluorescence resonance energy transfer imaging microscopy. Methods Enzymol 2003, 360:542-560.
38. Erickson MG, Alseikhan BA, Peterson BZ, Yue DT. Preassociation of calmodulin with voltage-gated Ca(2+) channels revealed by FRET in single living cells. Neuron 2001, 31(6):973-985. 10.1016/S0896-6273(01)00438-X, 11580897.
39. Oliveria SF, Gomez LL, Dell'Acqua ML. Imaging kinase--AKAP79--phosphatase scaffold complexes at the plasma membrane in living cells using FRET microscopy. J Cell Biol 2003, 160(1):101-112. 10.1083/jcb.200209127, 2172743, 12507994.
40. Sorkin A, McClure M, Huang F, Carter R. Interaction of EGF receptor and grb2 in living cells visualized by fluorescence resonance energy transfer (FRET) microscopy. Curr Biol 2000, 10(21):1395-1398. 10.1016/S0960-9822(00)00785-5, 11084343.
41. Zheng J, Zagotta WN. Stoichiometry and assembly of olfactory cyclic nucleotide-gated channels. Neuron 2004, 42(3):411-421. 10.1016/S0896-6273(04)00253-3, 15134638.
42. Gordon GW, Berry G, Liang XH, Levine B, Herman B. Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy. Biophys J 1998, 74(5):2702-2713. 10.1016/S0006-3495(98)77976-7, 1299610, 9591694.
43. Patterson G, Day RN, Piston D. Fluorescent protein spectra. J Cell Sci 2001, 114(Pt 5):837-838.