Activation of NMDA receptors leads to phosphorylation of TRPV1 S800 by protein kinase C and A-Kinase anchoring protein 150 in rat trigeminal ganglia

Biochemical and Biophysical Research Communications

Volumn 424, Issue 2, 2012, Pages 358-363

  Lee, Jongseok ^a   Chung, Man Kyo ^a   Ro, Jin Y ^a  

^a UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

Author keywords

Nociceptor; Peripheral; Rat; Sensitization

Indexed keywords

A KINASE ANCHORING PROTEIN 150; MEMBRANE PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PROTEIN KINASE C; SERINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANIMAL CELL; ARTICLE; BIOTINYLATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DOSE RESPONSE; DOWN REGULATION; ENZYME ACTIVATION; GANGLION; HYPERALGESIA; MALE; NOCICEPTIVE RECEPTOR; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; RNA SEQUENCE; SENSORY NERVE CELL; TRIGEMINAL NERVE;

A KINASE ANCHOR PROTEINS; ANIMALS; IMMUNOPRECIPITATION; MALE; NOCICEPTORS; PHOSPHORYLATION; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, SMALL INTERFERING; SERINE; TRIGEMINAL GANGLION; TRPV CATION CHANNELS;

RATTUS;

EID: 84864303750     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.07.008     Document Type: Article

References (39)

1. Caterina M.J., Schmacher M., Tominaga T.A., Rosen J.D. Levine, The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389:816-824.
2. Caterina M.J., Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu. Rev. Neurosci. 2001, 24:487-517.
3. Clapham D.E. TRP channels as cellular sensors. Nature 2003, 426:517-524.
4. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., Raumann B.E., Basbaum A.I., Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 1998, 21:531-543.
5. Chung M.K., Jung S.J., Oh S.B. Role of TRP channels in pain sensation. Adv. Exp. Med. Biol. 2011, 704:615-636.
6. Schumacher M.A. Transient receptor potential channels in pain and inflammation: therapeutic opportunities. Pain Pract. 2010, 10:185-200.
7. Hu H.J., Bhave G., Gereau R.W. Prostaglandin and protein kinase A-dependent modulation of vanilloid receptor function by metabotropic glutamate receptor 5: potential mechanism for thermal hyperalgesia. J. Neurosci. 2002, 22:7444-7452.
8. Amadesi S., Cottrell G.S., Divino L., Chapman K., Grady E.F., Bautista F., Karanjia R., Barajas-Lopez C., Vanner S., Vergnolle N., Bunnett N.W. Protease-activated receptor 2 sensitized TRPV1 by protein kinase-Cepsilon- and A-dependent mechanisms in rats and mice. J. Physiol. 2006, 575:555-571.
9. Zhang H., Cang C.L., Kawasaki Y., Liang L.L., Zhang Y.Q., Ji R.R., Zhao Z.Q. Neurokinin-1 receptor enhances TRPV1 activity in primary sensory neurons via PKCepsilon: a novel pathway for heat hyperalgesia. J. Neurosci. 2007, 31:12067-12077.
10. J. Lee, J.L. Saloman, G. Weiland, M.K. Chung, J.Y. Ro, Functional interactions between NMDA receptors and TRPV1 in trigeminal sensory neurons mediate mechanical hyperalgesia in the rat masseter muscle, Pain (2012) In press.
11. Bauman A.L., Soughayer J., Nguyen B.T., Willoughby D., Carnegie G.K., Wong W., Hoshi N., Langeberg L.K., Cooper D.M., Dessauer C.W., Scott J.D. Dynamic regulation of cAMP synthesis through anchored PKA-adenylyl cyclase V/VI complexes. Mol. Cell 2006, 23:925-931.
12. Ku C.Y., Sanborn B.M. Progesterone prevents the pregnancy-related decline in protein kinase A association with rat myometrial plasma membrane and A-kinase anchoring protein. Biol. Reprod. 2002, 67:605-609.
13. Xie G., Raufman J.P. Association of protein kinase A with AKAP150 facilitates pepsinogen secretion from gastric chief cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 281:G1051-1058.
14. Faux M.C., Rollins E.N., Edwards A.S., Langeberg L.K., Newton A.C., Scott J.D. Mechanism of A-kinase-anchoring protein 79 (AKAP79) and protein kinase C interaction. Biochem. J. 1999, 343:443-452.
15. Zhang J., Bal M., Bierbower S., Zaika O., Shapiro M.S. AKAP79/150 complexs in G-protein modulation of neuronal ion channels. J. Neurosci. 2011, 31:7199-7211.
16. Oliveria S.F., Dell'Acqua M.L., Sather W.A. AKAP79/150 anchoring of calcineurin controls neuronal L-type Ca2+ channel activity and nuclear signaling. Neuron 2007, 55:261-275.
17. Chai S., Li M., Lan J., Xiong Z.G., Saugstad J.A., Simon R.P. A Kinase-anchoring protein 150 and calcineurin are involved in regulation of acid-sensing ion channels ASIC1 and ASIC2a. J. Biol. Chem. 2007, 282:22668-22677.
18. Brandao K.E., Dell'Acqua M.L., Levinson S.R. A-kinase anchoring protein 150 expression in a specific subset of TRPV1-and CaV 1.2-positive nociceptive rat dorsal root ganglion neurons. J. Comp. Neurol. 2012, 520:81-99.
19. Zhang X., Li L., McNaughton P.A. Proinflammatory mediators modulate the heat-activated channel TRPV1 via the scaffolding protein AKAP79/150. Neuron 2008, 59:450-461.
20. Jeske N.A., Diogenes A., Ruparel N.B., Fehrenbacher J.C., Henry M., Akopian A.N., Hargreaves K.M. A-kinase anchoring protein mediates TRPV1 thermal hyperalgesia through PKA phosphorylation of TRPV1. Pain 2008, 138:604-616.
21. Akopian A.N., Ruparel N.B., Jeske N.A., Hargreaves K.M. Transient receptor potential TRPA1 channel desensitization in sensory neurons is agonist dependent and regulated by TRPV1-directed internalization. J. Physiol. 2007, 583:175-193.
22. Haapasalo A., Sipola I., Larsson K., Akerman K.E., Stoilov P., Stamm S., Wong G., Castren E. Regulation of TRKB surface expression by brain-derived neurotropic factor and truncated TRKB isoforms. J. Biol. Chem. 2002, 277:43160-43167.
23. Mandadi S., Tominaga T., Numazaki M., Murayama N., Saito N., Armati P.J., Roufogalis B.D., Tominaga M. Increased sensitivity of desensitized TRPV1 by PMA occurs through PKCepsilon-mediated phosphorylation at S800. Pain 2006, 123:106-116.
24. Popescu G., Auerbach A. The NMDA receptor gating machine: lessons from single channels. Neuroscientist 2004, 3:192-198.
25. Beutler L.R., Wanat M.J., Quintana A., Sanz E., Bamford N.S., Zweifel L.S., Palmiter R.D. Balanced NMDA receptor acitivity in dopamine D1 receptor (D1R) and D2R-expressing medium spiny neurons in required for amphetamine sensitization. Proc. Nat. Acad. Sci. USA 2011, 108:4206-4211.
26. Herin G.A., Aizenman E. Amino terminal domain regulation of NMDA receptor function. Eur. J. Pharmacol. 2004, 500:101-111.
27. Chung M.K., Lee J., Duraes G., Ro J.Y. Lipopolysaccharide-induced pulpitis up-regulates TRPV1 in trigeminal ganglia. J. Dent. Res. 2011, 90:1103-1107.
28. Jeske N.A., Patwardhan A.M., Ruparel N.B., Akopain A.N., Shapiro M.S., Henry M.A. A-kinase anchoring protein 150 controls protein kinase C-mediated phosphorylation and sensitization of TRPV1. Pain 2009, 146:301-307.
29. Du J., Zhou S., Coggeshall R.J., Carlton S.M. N-methyl-d-aspartate-induced excitation and sensitization of normal and inflamed nociceptors. Neuroscience 2003, 118(2):547-562.
30. Bhave G., Zhu W., Wang H., Brasier D.J., Oxford G.S., Gereau R.W. cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 2002, 35:721-731.
31. 2+/calmodulin-dependent kinase II regulates its vanilloid binding. J. Biol. Chem. 2004, 279:7048-7054.
32. Woo D.H., Jung S.J., Zhu M.H., Park C.K., Kim Y.H., Oh S.B., Lee C.J. Direct activation of transient receptor potential vanilloid 1(TRPV1) by diacylglycerol (DAG). Mol. Pain 2008, 4:42.
33. Numazaki M., Tominaga T., Toyooka H., Tominaga M. Direct of phosphorylation of capsaicin receptor VR1 by protein kinase C epsilon and identification of two target serine residues. J. Biol. Chem. 2002, 277:13375-13378.
34. Rathee P.K., Distler C., Obreja O., Neuhuber W., Wang G.K., Wang S.Y., Nau C., Kress M. PKA/AKAP/VR-1 module: a common link of Gs-mediated signaling to thermal hyperalgesia. J. Neurosci. 2002, 22:4740-4745.
35. Tang H.B., Li Y.S., Miyano K., Nakata Y. Phosphorylation of TRPV1 by neurokinin-1 receptor agonist exaggerates the capsaicin-mediated substance P release from cultured rat dorsal root ganglion neurons. Neuropharmacology 2008, 55:1405-1411.
36. Schnizler K., Shutov L.P., Van Kanegan M.J., Merrill M.A., Nichols B., McKnight G.S., Strack S., Hell J.W., Usachev Y.M. Protein Kinase A anchoring via AKAP150 is essential for TRPV1 modulation by forskolin and prostaglandin E2 in mouse sensory neurons. J. Neurosci. 2008, 28:4904-4917.
37. Bhattacharyya S., Biou V., Xu W., Schluter O., Malenka R.C. A critical role for PSD-95/AKAP interactions in endocytosis of synaptic AMAP receptors. Nat. Neurosci. 2009, 12:172-181.
38. Lu M., Zhang I.A., Lim D.D., Hall M., Allen Y., Medvedeva G.S., McKnight Y.M., Usachev J.W. Hell, AKAP150-anchored PKA activity is important for LTD during its induction phase. J. Physiol. 2008, 586:4155-4164.
39. Colledge M., Dean R.A., Scott G.K., Langeberg L.K., Huganir R.L., Scott J.D. Targeting of PKA to glutamate receptors through a MAGUK-AKAP complex. Neuron 2000, 27:107-119.