Bradykinin-induced functional competence and trafficking of the δ-opioid receptor in trigeminal nociceptors

Journal of Neuroscience

Volumn 25, Issue 39, 2005, Pages 8825-8832

  Patwardhan, Amol M ^a   Berg, Kelly A ^a   Akopain, Armen N ^b   Jeske, Nathaniel A ^b   Gamper, Nikita ^b   Clarke, William P ^a   Hargreaves, Kenneth M ^a,b  

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

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

Author keywords

opioid receptor; Bradykinin; Nociceptor; Pain; Trafficking; Trigeminal

Indexed keywords

BISINDOLYLMALEIMIDE; BRADYKININ; CALCITONIN GENE RELATED PEPTIDE; CYCLIC AMP; DELTA OPIATE RECEPTOR; DELTA OPIATE RECEPTOR AGONIST; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE]; GREEN FLUORESCENT PROTEIN; ICATIBANT; LEUCINE ENKEPHALIN[2 DEXTRO ALANINE]; PHORBOL 13 ACETATE 12 MYRISTATE; PROSTAGLANDIN E2; PROTEIN KINASE C INHIBITOR;

ANALGESIA; ANIMAL CELL; ARTICLE; BIOTINYLATION; CELL MEMBRANE; COMPETENCE; CONTROLLED STUDY; ENZYME INHIBITION; HORMONE RELEASE; HYPOTHESIS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; NERVE CELL CULTURE; NOCICEPTIVE RECEPTOR; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SENSORY NERVE CELL; TRIGEMINAL NERVE; TRIGEMINUS GANGLION;

ANIMALS; BRADYKININ; CELL MEMBRANE; ENZYME ACTIVATION; GREEN FLUORESCENT PROTEINS; INFLAMMATION MEDIATORS; MALE; NEURAL INHIBITION; NEURONS, AFFERENT; NOCICEPTORS; PROTEIN KINASE C; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, BRADYKININ B2; RECEPTORS, OPIOID, DELTA; RECOMBINANT FUSION PROTEINS; TRIGEMINAL GANGLION;

EID: 25644461151     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0160-05.2005     Document Type: Article

References (47)

1. 2+ currents in rat sensory neurons. J Neurosci 19:8337-8348.
2. Allen MR, Zhang BR, Hettinger AM, Goad DW, Malayer JR, Geisert RD (2002) Detection of bradykinin and bradykinin-beta(2) receptors in the porcine endometrium during the estrous cycle and early pregnancy. Biol Reprod 66:574-579.
3. Amadesi S, Nie J, Vergnolle N, Cottrell GS, Grady EF, Trevisani M, Manni C, Geppetti P, McRoberts JA, Ennes H, Davis JB, Mayer EA, Bunnett NW (2004) Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J Neurosci 24:4300-4312.
4. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:849-857.
5. Bao L, Jin SX, Zhang C, Wang LH, Xu ZZ, Zhang FX, Wang LC, Ning FS, Cai HJ, Guan JS, Xiao HS, Xu ZQ, He C, Hokfelt T, Zhou Z, Zhang X (2003) Activation of delta opioid receptors induces receptor insertion and neuropeptide secretion. Neuron 37:121-133.
6. Barber LA, Vasko MR (1996) Activation of protein kinase C augments peptide release from rat sensory neurons. J Neurochem 67:72-80.
7. Berg KA, Clarke WP, Sailstad C, Saltzman A, Maayani S (1994) Signal transduction differences between 5-hydroxytryptamine type 2A and type 2C receptor systems. Mol Pharmacol 46:477-484.
8. Berg KA, Maayani S, Goldfarb J, Clarke WP (1998) Pleiotropic behavior of 5-HT2A and 5-HT2C receptor agonists. Ann NY Acad Sci 861:104-110.
9. Berg KA, Evans KL, Cropper JD, Clarke WP (2003) Temporal regulation of agonist efficacy at 5-hydroxytryptamine (5-HT)1A and 5-HT 1B receptors. J Pharmacol Exp Ther 304:200-205.
10. Browning KN, Kalyuzhny AE, Travagli RA (2004) μ-Opioid receptor trafficking on inhibitory synapses in the rat brainstem. J Neurosci 24:9344-9352.
11. Cahill CM, Morinville A, Lee MC, Vincent JP, Collier B, Beaudet A (2001a) Prolonged morphine treatment targets δ opioid receptors to neuronal plasma membranes and enhances δ-mediated antinociception. J Neurosci 21:7598-7607.
12. Cahill CM, McClellan KA, Morinville A, Hoffert C, Hubatsch D, O'Donnell D, Beaudet A (2001b) Immunohistochemical distribution of delta opioid receptors in the rat central nervous system: evidence for somatodendritic labeling and antigen-specific cellular compartmentalization. J Comp Neurol 440:65-84.
13. Cahill CM, Morinville A, Hoffert C, O'Donnell D, Beaudet A (2003) Up-regulation and trafficking of delta opioid receptor in a model of chronic inflammation: implications for pain control. Pain 101:199-208.
14. Cesare P, Dekker LV, Sardini A, Parker PJ, McNaughton PA (1999) Specific involvement of PKC-epsilon in sensitization of the neuronal response to painful heat. Neuron 23:617-624.
15. Chuang HH, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, Chao MV, Julius D (2001) Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411:957-962.
16. Grain SM, Shen KF (1998) GM1 ganglioside-induced modulation of opioid receptor-mediated functions. Ann NY Acad Sci 845:106-125.
17. Dai Y, Moriyama T, Higashi T, Togashi K, Kobayashi K, Yamanaka H, Tominaga M, Noguchi K (2004) Proteinase-activated receptor 2-mediated potentiation of transient receptor potential vanilloid subfamily 1 activity reveals a mechanism for proteinase-induced inflammatory pain. J Neurosci 24:4293-4299.
18. Evans CJ (2004) Secrets of the opium poppy revealed. Neuropharmacology 47 [Suppl 1]:293-299.
19. Carry MG, Richardson JD, Hargreaves KM (1994) Sodium nitroprusside evokes the release of immunoreactive calcitonin gene-related peptide and substance P from dorsal horn slices via nitric oxide-dependent and nitric oxide-independent mechanisms. J Neurosci 14:4329-4337.
20. Hassan AH, Ableitner A, Stein C, Herz A (1993) Inflammation of the rat paw enhances axonal transport of opioid receptors in the sciatic nerve and increases their density in the inflamed tissue. Neuroscience 55:185-195.
21. Hayashi C, Ueda H, Fukushima N, Katayama T, Misu Y (1995) Protein kinase C inhibitor potentiates the agonist-induced GTPase activity in COS cell membranes expressing delta-opioid receptor. Brain Res Mol Brain Res 33:347-350.
22. Hur EM, Kim KT (2002) G protein-coupled receptor signalling and cross-talk: achieving rapidity and specificity. Cell Signal 14:397-405.
23. Ji RR, Zhang Q, Law PY, Low HH, Eide R, Hokfelt T (1995) Expression of μ-, δ-, and κ-opioid receptor-like immunoreactivities in rat dorsal root ganglia after carrageenan-induced inflammation. J Neurosci 15:8156-8166.
24. Jordan BA, Trapaidze N, Gomes I, Nivarthi R, Devi LA (2001) Oligomerization of opioid receptors with beta 2-adrenergic receptors: a role in trafficking and mitogen-activated protein kinase activation. Proc Natl Acad Sci USA 98:343-348.
25. Jordan BA, Gomes I, Rios C, Filipovska J, Devi LA (2003) Functional interactions between mu opioid and alpha 2A-adrenergic receptors. Mol Pharmacol 64:1317-1324.
26. Joris JL, Dubner R, Hargreaves KM (1987) Opioid analgesia at peripheral sites: a target for opioids released during stress and inflammation? Anesth Analg 66:1277-1281.
27. Kessler F, Habelt C, Averbeck B, Reeh PW, Kress M (1999) Heat-induced release of CGRP from isolated rat skin and effects of bradykinin and the protein kinase C activator PMA. Pain 83:289-295.
28. Lorenz K, Lohse MJ, Quitterer U (2003) Protein kinase C switches the Raf kinase inhibitor from Raf-1 to GRK-2. Nature 426:574-579.
29. 2 metabotropic receptors in ATP-induced transient receptor potential vanilloid receptor 1-mediated thermal hypersensitivity. J Neurosci 23:6058-6062.
30. Mukhin YV, Garnovsky EA, Ullian ME, Garnovskaya MN (2003) Bradykinin B2 receptor activates extracellular signal-regulated protein kinase in mIMCD-3 cells via epidermal growth factor receptor transactivation. J Pharmacol Exp Ther 304:968-977.
31. Ostrom RS, Insel PA (2004) The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: implications for molecular pharmacology. Br J Pharmacol 143:235-245.
32. Petho G, Derow A, Reeh PW (2001) Bradykinin-induced nociceptor sensitization to heat is mediated by cyclooxygenase products in isolated rat skin. Eur J Neurosci 14:210-218.
33. Premkumar LS, Ahern GP (2000) Induction of vanilloid receptor channel activity by protein kinase C. Nature 408:985-990.
34. Price TJ, Helesic G, Parghi D, Hargreaves KM, Flores CM (2003) The neuronal distribution of cannabinoid receptor type 1 in the trigeminal ganglion of the rat. Neuroscience 120:155-162.
35. Satoh M, Minami M (1995) Molecular pharmacology of the opioid receptors. Pharmacol Ther 68:343-364.
36. 2+ currents, but spares a sustained current. Neuron 6:13-20.
37. Shin J, Cho H, Hwang SW, Jung J, Shin CY, Lee SY, Kim SH, Lee MG, Choi YH, Kim J, Haber NA, Reichling DB, Khasar S, Levine JD, Oh U (2002) Bradykinin-12-lipoxygenase-VR1 signaling pathway for inflammatory hyperalgesia. Proc Natl Acad Sci USA 99:10150-10155.
38. Shuster SJ, Riedl M, Li X, Vulchanova L, Eide R (1999) Stimulus-dependent translocation of κ opioid receptors to the plasma membrane. J Neurosci 19:2658-2664.
39. Stein C, Millan MJ, Shippenberg TS, Peter K, Herz A (1989) Peripheral opioid receptors mediating antinociception in inflammation. Evidence for involvement of mu, delta and kappa receptors. J Pharmacol Exp Ther 248:1269-1275.
40. Stein C, Schafer M, Machelska H (2003) Attacking pain at its source: new perspectives on opioids. Nat Med 9:1003-1008.
41. Sugiuar T, Bielefeldt K, Gebhart GF (2004) TRPV1 function in mouse colon sensory neurons is enhanced by metabotropic 5-hydroxytryptamine receptor activation. J Neurosci 24:9521-9530.
42. Ueda H, Miyamae T, Hayashi C, Watanabe S, Fukushima N, Sasaki Y, Iwamura T, Misu Y (1995) Protein kinase C involvement in homologous desensitization of δ-opioid receptor coupled to Gi1-phospholipase C activation in Xenopus oocytes. J Neurosci 15:7485-7499.
43. Ulrich-Lai YM, Flores CM, Harding-Rose CA, Goodis HE, Hargreaves KM (2001) Capsaicin-evoked release of immunoreactive calcitonin gene-related peptide from rat trigeminal ganglion: evidence for intraganglionic neurotransmission. Pain 91:219-226.
44. Vellani V, Zachrisson O, McNaughton PA (2004) Functional bradykinin B1 receptors are expressed in nociceptive neurones and are upregulated by the neurotrophin GDNF. J Physiol (Lond) 560:391-401.
45. Xiang B, Yu GH, Guo J, Chen L, Hu W, Pei G, Ma L (2001) Heterologous activation of protein kinase C stimulates phosphorylation of delta-opioid receptor at serine 344, resulting in beta-arrestin- and clathrin-mediated receptor internalization. J Biol Chem 276:4709-4716.
46. Zhang N, Rogers TJ, Caterina M, Oppenheim JJ (2004) Proinflammatory chemokines, such as C-C chemokine ligand 3, desensitize mu-opioid receptors on dorsal root ganglia neurons. J Immunol 173:594-599.
47. Zhang Z, Xin SM, Wu GX, Zhang WB, Ma L, Pei G (1999) Endogenous delta-opioid and ORL1 receptors couple to phosphorylation and activation of p38 MAPK in NG108-15 cells and this is regulated by protein kinase A and protein kinase C. J Neurochem 73:1502-1509.