Prostaglandin E2/EP4 signalling facilitates EP4 receptor externalization in primary sensory neurons in vitro and in vivo

Pain

Volumn 154, Issue 2, 2013, Pages 313-323

  St Jacques, Bruno ^a   Ma, Weiya ^a,b  

^a DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Dorsal root ganglion; EP4 receptor; Inflammatory pain; Prostaglandin E2; Receptor trafficking; Sensitization

Indexed keywords

7 [5 (4 BIPHENYLYLMETHOXY) 2 MORPHOLINO 3 OXOCYCLOPENTYL] 4 HEPTENOIC ACID; CYCLIC AMP; FREUND ADJUVANT; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; PROSTAGLANDIN E RECEPTOR 2; PROSTAGLANDIN E RECEPTOR 4; PROSTAGLANDIN E2; PROSTAGLANDIN RECEPTOR STIMULATING AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURFACE; CONTROLLED STUDY; ENDOSOME; EXPLANT; GOLGI COMPLEX; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY PAIN; MALE; MUSCLE SPINDLE AFFERENT NERVE; NERVE CELL CULTURE; NONHUMAN; PAIN RECEPTOR; PAW EDEMA; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN SYNTHESIS INHIBITION; RAT; SENSITIZATION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPINAL GANGLION;

EID: 84872681810     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2012.11.005     Document Type: Article

References (52)

1. K.O. Aley, R.O. Messing, D. Mochly-Rosen, and J.D. Levine Chronic hypersensitivity for inflammatory nociceptor sensitization mediated by the epsilon isozyme of protein kinase C J Neurosci 20 2000 4680 4685
2. L. Arancibia-Cárcamo, B.P. Fairfax, S.J. Moss, and J.T. Kittler Studying the localization, surface stability and endocytosis of neurotransmitter receptors by antibody labeling and biotinylation approaches J.T. Kittler, S.J. Moss, The dynamic synapse: molecular methods in ionotropic receptor biology 2006 CRC Press Boca Raton, FL 91 118
3. P. Clark, S.E. Rowland, D. Denis, M.C. Mathieu, R. Stocco, H. Poirier, J. Burch, Y. Han, L. Audoly, A.G. Therien, and D. Xu MF498 [N-{[4-(5,9-Diethoxy-6- oxo-6,8-dihydro-7H-pyrrolo[3,4-g]quinolin-7-yl)-3-m ethylbenzyl]sulfonyl}-2-(2- methoxyphenyl)acetamide], a selective E prostanoid receptor 4 antagonist, relieves joint inflammation and pain in rodent models of rheumatoid and osteoarthritis J Pharmacol Exp Ther 325 2008 425 434
4. P. Cruz Duarte, B. St-Jacques, and W. Ma Prostaglandin E2 contributes to the synthesis of brain-derived neurotrophic factor in primary sensory neuron in cultures and in a neuropathic pain model Exp Neurol 234 2012 466 481
5. S. England, S. Bevan, and R.J. Docherty PGE2 modulates the tetrodotoxin-resistant sodium current in neonatal rat dorsal root ganglion neurones via the cyclic AMP-protein kinase A cascade J Physiol 495 1996 429 440
6. E. Fabbretti, M. D'Arco, A. Fabbro, M. Simonetti, A. Nistri, and R. Giniatullin Delayed upregulation of ATP P2X3 receptors of trigeminal sensory neurons by calcitonin gene-related peptide J Neurosci 26 2006 6163 6171
7. A. Galan, J.M. Laird, and F. Cervero In vivo recruitment by painful stimuli of AMPA receptor subunits to the plasma membrane of spinal cord neurons PAIN® 112 2004 315 323
8. M.S. Gold, and G.F. Gebhart Nociceptor sensitization in pain pathogenesis Nat Med 16 2010 1248 1257
9. M.S. Gold, D.B. Reichling, M.J. Shuster, and J.D. Levine Hyperalgesic agents increase a tetrodotoxin-resistant na+ current in nociceptors Proc Natl Acad Sci U S A 93 1996 1108 1112
10. M.S. Gold, M.J. Shuster, and J.D. Levine Role of a Ca(2+)-dependent slow afterhyperpolarization in prostaglandin E2-induced sensitization of cultured rat sensory neurons Neurosci Lett 205 1996 161 164
11. C.M. Hingtgen, K.J. Waite, and M.R. Vasko Prostaglandins facilitate peptide release from rat sensory neurons by activating the adenosine 3′,5′-cyclic monophosphate transduction cascade J Neurosci 15 1995 5411 5419
12. G.G. Holz, G. Kang, M. Harbeck, M.W. Roe, and O.G. Chepurny Cell physiology of cAMP sensor Epac J Physiol 577 2006 5 15
13. C.A. Kassuya, J. Ferreira, R.F. Claudino, and J.B. Calixto Intraplantar PGE2 causes nociceptive behaviour and mechanical allodynia: the role of prostanoid E receptors and protein kinases Br J Pharmacol 150 2007 727 737
14. A. Kawabata Prostaglandin E2 and pain-an update Biol Pharm Bull 34 2011 1170 1173
15. S.G. Khasar, A.K. Ouseph, B. Chou, T. Ho, P.G. Green, and J.D. Levine Is there more than one prostaglandin E receptor subtype mediating hyperalgesia in the rat hindpaw? Neuroscience 64 1995 1161 1165
16. C.R. Lin, F. Amaya, L. Barrett, H. Wang, J. Takada, T.A. Samad, and C.J. Woolf Prostaglandin E2 receptor EP4 contributes to inflammatory pain hypersensitivity J Pharmacol Exp Ther 319 2006 1096 1103
17. J.C. Lopshire, and G.D. Nicol The cAMP transduction cascade mediates the prostaglandin E2 enhancement of the capsaicin-elicited current in rat sensory neurons: whole-cell and single-channel studies J Neurosci 18 1998 6081 6092
18. W. Ma Chronic prostaglandin E2 treatment induces the synthesis of the pain-related peptide substance P and calcitonin gene-related peptide in cultured sensory ganglion explants J Neurochem 115 2010 363 372
19. W. Ma, J.G. Chabot, F. Vercauteren, and R. Quirion Injured nerve-derived COX2/PGE2 contributes to the maintenance of neuropathic pain in aged rats Neurobiol Aging 31 2010 1227 1237
20. W. Ma, and J.C. Eisenach Intraplantar injection of the cyclooxygenase inhibitor ketorolac reduces immunoreactivities of substance P, calcitonin gene-related peptide, and dynorphin in the dorsal horn of rats with nerve injury or inflammation Neuroscience 121 2003 681 690
21. W. Ma, and R. Quirion Up-regulation of interleukin 6 induced by prostaglandin E2 from invading macrophages following nerve injury: an in vivo and in vitro study J Neurochem 93 2005 664 673
22. W. Ma, and R. Quirion Increased calcitonin gene-related peptide in neuroma and invading macrophages is involved in the up-regulation of interleukin-6 and nerve injury associated thermal hyperalgesia in a rat model of mononeuropathy J Neurochem 98 2006 180 192
23. W. Ma, and B. St-Jacques Cruz Duarte P. Targeting pain mediators induced by injured nerve-derived COX2 and PGE2 to treat neuropathic pain Expert Opin Ther Targets 16 2012 527 540
24. A.B. Malmberg, E.P. Brandon, R.L. Idzerda, H. Liu, G.S. McKnight, and A.I. Basbaum Diminished inflammation and nociceptive pain with preservation of neuropathic pain in mice with a targeted mutation of the type I regulatory subunit of cAMP-dependent protein kinase J Neurosci 17 1997 7462 7470
25. H. Mebane, M.E. Turnbach, and A. Randich Spinal EP receptors mediating prostaglandin E2-induced mechanical hyperalgesia, thermal hyperalgesia, and touch-evoked allodynia in rats J Pain 4 2003 392 399
26. K. Nakao, A. Murase, H. Ohshiro, T. Okumura, K. Taniguchi, Y. Murata, M. Masuda, T. Kato, Y. Okumura, and J. Takada CJ-023,423, a novel, potent and selective prostaglandin EP4 receptor antagonist with antihyperalgesic properties J Pharmacol Exp Ther 322 2007 686 694
27. G.D. Nicol, D.K. Klingberg, and M.R. Vasko Prostaglandin E2 increases calcium conductance and stimulates release of substance P in avian sensory neurons J Neurosci 12 1992 1917 1927
28. T.A. Nicolson, A.F. Foster, S. Bevan, and C.D. Richards Prostaglandin E2 sensitizes primary sensory neurons to histamine Neuroscience 150 2007 22 30
29. J. Odegard, M. Aasrum, I.H. Tveteraas, S.P. Bharath, D. Sandnes, and T. Christoffersen Role of ErbB2 in the prostaglandin E(2)-induced enhancement of the mitogenic response to epidermal growth factor in cultured hepatocytes Biochem Biophys Res Commun 421 2012 255 260
30. H. Oida, T. Namba, Y. Sugimoto, F. Ushikubi, H. Ohishi, A. Ichikawa, and S. Narumiya In situ hybridization studies of prostacyclin receptor mRNA expression in various mouse organs Br J Pharmacol 116 1995 2828 2837
31. E.T. Olesen, M.R. Rutzler, H.B. Moeller, H.A. Praetorius, and R.A. Fenton Vasopressin-independent targeting of aquaporin-2 by selective E-prostanoid receptor agonists alleviates nephrogenic diabetes insipidus Proc Natl Acad Sci U S A 108 2011 12949 12954
32. S. Pitchford, and J.D. Levine Prostaglandins sensitize nociceptors in cell culture Neurosci Lett 132 1991 105 108
33. D.B. Reichling, and J.D. Levine Critical role of nociceptor plasticity in chronic pain Trends Neurosci 32 2009 611 618
34. R. Rukwied, B.A. Chizh, U. Lorenz, O. Obreja, S. Margarit, M. Schley, and M. Schmelz Potentiation of nociceptive responses to low pH injections in humans by prostaglandin E2 J Pain 8 2007 443 451
35. A.M. Rush, and S.G. Waxman PGE2 increases the tetrodotoxin-resistant Nav1.9 sodium current in mouse DRG neurons via G-proteins Brain Res 1023 2004 264 271
36. M. Schmidt, A.E. Dubin, M.J. Petrus, T.J. Earley, and A. Patapoutian Nociceptive signals induce trafficking of TRPA1 to the plasma membrane Neuron 64 2009 498 509
37. R.S. Scroggs Up-regulation of low-threshold tetrodotoxin-resistant Na+ current via activation of a cyclic AMP/protein kinase A pathway in nociceptor-like rat dorsal root ganglion cells Neuroscience 186 2011 13 20
38. T. Singh, and S.K. Katiyar Green tea catechins reduce invasive potential of human melanoma cells by targeting COX-2, PGE2 receptors and epithelial-to-mesenchymal transition PLoS One 6 2011 e25224
39. J.A. Smith, C.L. Davis, and G.M. Burgess Prostaglandin E2-induced sensitization of bradykinin-evoked responses in rat dorsal root ganglion neurons is mediated by cAMP-dependent protein kinase A Eur J Neurosci 12 2000 3250 3258
40. A.L. Souza, F.A. Moreira, K.R. Almeida, C.M. Bertollo, K.A. Costa, and M.M. Coelho In vivo evidence for a role of protein kinase C in peripheral nociceptive processing Br J Pharmacol 135 2002 239 247
41. B. St-Jacques, P. Cruz Duarte, and W. Ma Agonist or inflammation increases prostaglandin E2 EP4 receptor externalization in primary sensory neurons Soc Neurosci Abstr 381.23 2011
42. B. St-Jacques, and W. Ma Role of prostaglandin E2 in the synthesis of the pro-inflammatory cytokine interleukin-6 in primary sensory neurons: an in vivo and in vitro study J Neurochem 118 2011 841 854
43. C.L. Stucky, S.A. Thayer, and V.S. Seybold Prostaglandin E2 increases the proportion of neonatal rat dorsal root ganglion neurons that respond to bradykinin Neuroscience 74 1996 1111 1123
44. Y.O. Taiwo, and J.D. Levine Prostaglandin effects after elimination of indirect hyperalgesic mechanisms in the skin of the rat Brain Res 492 1989 397 399
45. J.H. Tao-Cheng, V.T. Crocker, C.A. Winters, R. Azzam, J. Chludzinski, and T.S. Reese Trafficking of AMPA receptors at plasma membranes of hippocampal neurons J Neurosci 31 2011 4834 4843
46. A. Tappe-Theodor, N. Agarwal, I. Katona, T. Rubino, L. Martini, J. Swiercz, K. Mackie, H. Monyer, D. Parolaro, J. Whistler, T. Kuner, and R. Kuner A molecular basis of analgesic tolerance to cannabinoids J Neurosci 27 2007 4165 4177
47. P.K. Tripathi, C.G. Cardenas, C.A. Cardenas, and R.S. Scroggs Up-regulation of tetrodotoxin-sensitive sodium currents by prostaglandin E(2) in type-4 rat dorsal root ganglion cells Neuroscience 185 2011 14 26
48. H. Vanegas, and H.G. Schaible Prostaglandins and cycloxygenases in the spinal cord Prog Neurobiol 64 2001 327 363
49. M.R. Vasko Prostaglandin-induced neuropeptide release from spinal cord Prog Brain Res 104 1995 367 380
50. C. Wang, Y. Gu, G.W. Li, and L.Y. Huang A critical role of the cAMP sensor Epac in switching protein kinase signalling in prostaglandin E2-induced potentiation of P2X3 receptor currents in inflamed rats J Physiol 584 2007 191 203
51. C. Wang, G.W. Li, and L.Y. Huang Prostaglandin E2 potentiation of P2X3 receptor mediated currents in dorsal root ganglion neurons Mol Pain 3 2007 22
52. X. Zhang, J. Huang, and P.A. McNaughton NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels EMBO J 24 2005 4211 4223