Sensory neuron cAMP signaling in chronic pain

Cyclic Nucleotide Signaling

Volumn , Issue , 2015, Pages 113-134

  Eijkelkamp, Niels ^a   Singhmar, Pooja ^b   Heijnen, Cobi J ^b   Kavelaars, Annemieke ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84962564072     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/b18477     Document Type: Chapter

References (96)

1. Basbaum, A.I., Bautista, D.M., Scherrer, G., and Julius, D. Cellular and molecular mechanisms of pain. Cell 2009 (139), 267-284.
2. Woolf, C.J., and Ma, Q. Nociceptors-Noxious stimulus detectors. Neuron 2007 (55), 353-364.
3. von Hehn, C.A., Baron, R., and Woolf, C.J. Deconstructing the neuropathic pain phenotype to reveal neural mechanisms. Neuron 2012 (73), 638-652.
4. Reichling, D.B., and Levine, J.D. Critical role of nociceptor plasticity in chronic pain. Trends Neurosci 2009 (32), 611-618.
5. Bielefeldt, K., Davis, B., and Binion, D.G. Pain and inflammatory bowel disease. Inflamm Bowel Dis 2009 (15), 778-788.
6. Wood, J.N., and Eijkelkamp, N. Noxious mechanosensation-Molecules and circuits. Curr Opin Pharmacol 2012 (12), 4-8.
7. McMahon, S.B., and Bevan, S. Inflammatory mediators and modulators of pain. In Wall and Melzack’s Textbook of Pain Edition. Edited by S. McMahon and M. Koltzenburg, Churchill Livingstone (Elsevier Health Sciences), Amsterdam, 2005, pp. 49-72.
8. Tarpley, J.W., Kohler, M.G., and Martin, W.J. The behavioral and neuroanatomical effects of IB4-saporin treatment in rat models of nociceptive and neuropathic pain. Brain Res 2004 (1029), 65-76.
9. Joseph, E.K., Chen, X., Bogen, O., and Levine, J.D. Oxaliplatin acts on IB4-positive nociceptors to induce an oxidative stress-dependent acute painful peripheral neuropathy. J Pain 2008 (9), 463-472.
10. Joseph, E.K., and Levine, J.D. Hyperalgesic priming is restricted to isolectin B4-positive nociceptors. Neuroscience 2010 (169), 431-435.
11. Ferrari, L.F., Bogen, O., and Levine, J.D. Nociceptor subpopulations involved in hyperalgesic priming. Neuroscience 2010 (165), 896-901.
12. Abrahamsen, B., Zhao, J., Asante, C.O. et al. The cell and molecular basis of mechanical, cold, and inflammatory pain. Science 2008 (321), 702-705.
13. Collier, H.O., and Schneider, C. Nociceptive response to prostaglandins and analgesic actions of aspirin and morphine. Nat New Biol 1972 (236), 141-143.
14. Ferreira, S.H., Nakamura, M., and de Abreu Castro, M.S. The hyperalgesic effects of prostacyclin and prostaglandin E2. Prostaglandins 1978 (16), 31-37.
15. Cunha, F.Q., Poole, S., Lorenzetti, B.B., and Ferreira, S.H. The pivotal role of tumour necrosis factor alpha in the development of inflammatory hyperalgesia. Br J Pharmacol 1992 (107), 660-664.
16. Wise, H. Lack of interaction between prostaglandin E2 receptor subtypes in regulating adenylyl cyclase activity in cultured rat dorsal root ganglion cells. Eur J Pharmacol 2006 (535), 69-77.
17. Taiwo, Y.O., and Levine, J.D. Prostaglandin effects after elimination of indirect hyperalgesic mechanisms in the skin of the rat. Brain Res 1989 (492), 397-399.
18. Eijkelkamp, N., Wang, H., Garza-Carbajal, A. et al. Low nociceptor GRK2 prolongs prostaglandin E2 hyperalgesia via biased cAMP signaling to Epac/Rap1, protein kinase Cepsilon, and MEK/ERK. J Neurosci 2010 (30), 12806-12815.
19. Lin, C.R., Amaya, F., Barrett, L. et al. Prostaglandin E2 receptor EP4 contributes to inflammatory pain hypersensitivity. J Pharmacol Exp Ther 2006 (319), 1096-1103.
20. Taiwo, Y.O., Heller, P.H., and Levine, J.D. Mediation of serotonin hyperalgesia by the cAMP second messenger system. Neuroscience 1992 (48), 479-483.
21. Dina, O.A., Hucho, T., Yeh, J., Malik-Hall, M., Reichling, D.B., and Levine, J.D. Primary afferent second messenger cascades interact with specific integrin subunits in producing inflammatory hyperalgesia. Pain 2005 (115), 191-203.
22. Wang, H., Heijnen, C.J., Eijkelkamp, N. et al. GRK2 in sensory neurons regulates epinephrine-induced signalling and duration of mechanical hyperalgesia. Pain 2011 (152), 1649-1658.
23. Gold, M.S., Reichling, D.B., Shuster, M.J., and Levine, J.D. Hyperalgesic agents increase a tetrodotoxin-resistant Na+ current in nociceptors. Proc Natl Acad Sci U S A 1996 (93), 1108-1112.
24. Taiwo, Y.O., and Levine, J.D. Further confirmation of the role of adenyl cyclase and of cAMP-dependent protein kinase in primary afferent hyperalgesia. Neuroscience 1991 (44), 131-135.
25. Dostmann, W.R. (RP)-cAMPS inhibits the cAMP-dependent protein kinase by blocking the cAMP-induced conformational transition. FEBS Lett 1995 (375), 231-234.
26. Cunha, F.Q., Teixeira, M.M., and Ferreira, S.H. Pharmacological modulation of secondary mediator systems-Cyclic AMP and cyclic GMP-On inflammatory hyperalgesia. Br J Pharmacol 1999 (127), 671-678.
27. Ferreira, S.H., Lorenzetti, B.B., and De Campos, D.I. Induction, blockade and restoration of a persistent hypersensitive state. Pain 1990 (42), 365-371.
28. Aley, K.O., and Levine, J.D. Role of protein kinase A in the maintenance of inflammatory pain. J Neurosci 1999 (19), 2181-2186.
29. Ma, W., and Quirion, R. Does COX2-dependent PGE2 play a role in neuropathic pain? Neurosci Lett 2008 (437), 165-169.
30. St-Jacques, B., and Ma, W. 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 2011 (118), 841-854.
31. Ingram, S.L., and Williams, J.T. Opioid inhibition of Ih via adenylyl cyclase. Neuron 1994 (13), 179-186.
32. Ferreira, S.H., and Nakamura, M. III-Prostaglandin hyperalgesia: Relevance of the peripheral effect for the analgesic action of opioid-antagonists. Prostaglandins 1979 (18), 201-208.
33. Schnorr, S., Eberhardt, M., Kistner, K. et al. HCN2 channels account for mechanical (but not heat) hyperalgesia during long-standing inflammation. Pain 2014 (155), 1079-1090.
34. Emery, E.C., Young, G.T., Berrocoso, E.M., Chen, L., and McNaughton, P.A. HCN2 ion channels play a central role in inflammatory and neuropathic pain. Science 2011 (333), 1462-1466.
35. Kawasaki, H., Springett, G.M., Mochizuki, N. et al. A family of cAMP-binding proteins that directly activate Rap1. Science 1998 (282), 2275-2279.
36. de Rooij, J., Zwartkruis, F.J., Verheijen, M.H. et al. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 1998 (396), 474-477.
37. Grandoch, M., Roscioni, S.S., and Schmidt, M. The role of Epac proteins, novel cAMP mediators, in the regulation of immune, lung and neuronal function. Br J Pharmacol 2010 (159), 265-284.
38. Holz, G.G., Kang, G., Harbeck, M., Roe, M.W., and Chepurny, O.G. Cell physiology of cAMP sensor Epac. J Physiol 2006 (577), 5-15.
39. Suzuki, S., Yokoyama, U., Abe, T. et al. Differential roles of Epac in regulating cell death in neuronal and myocardial cells. J Biol Chem 2010 (285), 24248-24259.
40. Wang, H., Heijnen, C.J., van Velthoven, C.T. et al. Balancing GRK2 and EPAC1 levels prevents and relieves chronic pain. J Clin Invest 2013 (123), 5023-5034.
41. Eijkelkamp, N., Linley, J.E., Torres, J.M. et al. A role for Piezo2 in EPAC1-dependent mechanical allodynia. Nat Commun 2013 (4), 1682.
42. Shibasaki, T., Takahashi, H., Miki, T. et al. Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci U S A 2007 (104), 19333-19338.
43. Christensen, A.E., Selheim, F., de Rooji, J. et al. cAMP analog mapping of Epac1 and cAMP kinase. Discriminating analogs demonstrate that Epac and cAMP kinase act synergistically to promote PC-12 cell neurite extension. J Biol Chem 2003 (278), 35394-35402.
44. Almahariq, M., Tsalkova, T., Mei, F.C. et al. A novel EPAC-specific inhibitor suppresses pancreatic cancer cell migration and invasion. Mol Pharmacol 2013 (83), 122-128.
45. Taiwo, Y.O., and Levine, J.D. Direct cutaneous hyperalgesia induced by adenosine. Neuroscience 1990 (38), 757-762.
46. Janig, W., Levine, J.D., and Michaelis, M. Interactions of sympathetic and primary afferent neurons following nerve injury and tissue trauma. Prog Brain Res 1996 (113), 161-184.
47. Chen, X., and Levine, J.D. Epinephrine-induced excitation and sensitization of rat C-fiber nociceptors. J Pain 2005 (6), 439-446.
48. Chen, H.S., Lei, J., He, X. et al. Peripheral involvement of PKA and PKC in subcutaneous bee venom-induced persistent nociception, mechanical hyperalgesia, and inflammation in rats. Pain 2008 (135), 31-36.
49. Zhang, J.M., Li, H., Liu, B., and Brull, S.J. Acute topical application of tumor necrosis factor alpha evokes protein kinase A-dependent responses in rat sensory neurons. J Neurophysiol 2002 (88), 1387-1392.
50. Eijkelkamp, N., Heijnen, C.J., Carbajal, A.G. et al. G protein-coupled receptor kinase 6 acts as a critical regulator of cytokine-induced hyperalgesia by promoting phosphatidylinositol 3-kinase and inhibiting p38 signaling. Mol Med 2012 (18), 556-564.
51. Kim, M.J., Lee, S.Y., Yang, K.Y. et al. Differential regulation of peripheral IL-1beta-induced mechanical allodynia and thermal hyperalgesia in rats. Pain 2014 (155), 723-732.
52. Kim, K.S., Kim, J., Back, S.K., Im, J.Y., Na, H.S., and Han, P.L. Markedly attenuated acute and chronic pain responses in mice lacking adenylyl cyclase-5. Genes Brain Behav 2007 (6), 120-127.
53. Song, X.J., Wang, Z.B., Gan, Q., and Walters, E.T. cAMP and cGMP contribute to sensory neuron hyperexcitability and hyperalgesia in rats with dorsal root ganglia compression. J Neurophysiol 2006 (95), 479-492.
54. Liou, J.T., Liu, F.C., Hsin, S.T., Yang, C.Y., and Lui, P.W. Inhibition of the cyclic adenosine monophosphate pathway attenuates neuropathic pain and reduces phosphorylation of cyclic adenosine monophosphate response element-binding in the spinal cord after partial sciatic nerve ligation in rats. Anesth Analg 2007 (105), 1830-1837 (table).
55. Malmberg, A.B., Brandon, E.P., Idzerda, R.L., Liu, H., McKnight, G.S., and Basbaum, A.I. 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 1997 (17), 7462-7470.
56. Isensee, J., Diskar, M., Waldherr, S. et al. Pain modulators regulate the dynamics of PKA-RII phosphorylation in subgroups of sensory neurons. J Cell Sci 2014 (127), 216-229.
57. Yajima, Y., Narita, M., Shimamura, M., Narita, M., Kubota, C., and Suzuki, T. Differential involvement of spinal protein kinase C and protein kinase A in neuropathic and inflammatory pain in mice. Brain Res 2003 (992), 288-293.
58. Molliver, D.C., Wright, D.E., Leitner, M.L. et al. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 1997 (19), 849-861.
59. Hucho, T.B., Dina, O.A., and Levine, J.D. Epac mediates a cAMP-to-PKC signaling in inflammatory pain: An isolectin B4(+) neuron-specific mechanism. J Neurosci 2005 (25), 6119-6126.
60. Rathee, P.K., Distler, C., Obreja, O. et al. PKA/AKAP/VR-1 module: A common link of Gs-mediated signaling to thermal hyperalgesia. J Neurosci 2002 (22), 4740-4745.
61. Caterina, M.J., Schumacher, M.A., Tominaga, M., Rosen, T.A., Levine, J.D., and Julius, D. The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature 1997 (389), 816-824.
62. Julius, D. TRP channels and pain. Annu Rev Cell Dev Biol 2013 (29), 355-384.
63. Cho, H., Yang, Y.D., Lee, J. et al. The calcium-activated chloride channel anoctamin 1 acts as a heat sensor in nociceptive neurons. Nat Neurosci 2012 (15), 1015-1021.
64. Bhave, G., Zhu, W., Wang, H., Brasier, D.J., Oxford, G.S., and Gereau, R.W. cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 2002 (35), 721-731.
65. Efendiev, R., Bavencoffe, A., Hu, H., Zhu, M.X., and Dessauer, C.W. Scaffolding by A-kinase anchoring protein enhances functional coupling between adenylyl cyclase and TRPV1 channel. J Biol Chem 2013 (288), 3929-3937.
66. Bolcskei, K., Helyes, Z., Szabo, A. et al. Investigation of the role of TRPV1 receptors in acute and chronic nociceptive processes using gene-deficient mice. Pain 2005 (117), 368-376.
67. Moriyama, T., Higashi, T., Togashi, K. et al. Sensitization of TRPV1 by EP1 and IP reveals peripheral nociceptive mechanism of prostaglandins. Mol Pain 2005 (1), 3.
68. McCarter, G.C., and Levine, J.D. Ionic basis of a mechanotransduction current in adult rat dorsal root ganglion neurons. Mol Pain 2006 (2), 28.
69. Coste, B., Mathur, J., Schmidt, M. et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 2010 (330), 55-60.
70. Woo, S.H., Ranade, S., Weyer, A.D. et al. Piezo2 is required for Merkel-cell mechanotransduction. Nature 2014 (509), 622-626.
71. Dubin, A.E., Schmidt, M., Mathur, J. et al. Inflammatory signals enhance piezo2-mediated mechanosensitive currents. Cell Rep 2012 (2), 511-517.
72. Eijkelkamp, N., Quick, K., and Wood, J.N. Transient receptor potential channels and mechanosensation. Annu Rev Neurosci 2013 (36), 519-546.
73. Dall’acqua, M.C., Bonet, I.J., Zampronio, A.R., Tambeli, C.H., Parada, C.A., and Fischer, L. The contribution of transient receptor potential ankyrin 1 (TRPA1) to the in vivo nociceptive effects of prostaglandin E. Life Sci 2014 (105), 7-13.
74. Eijkelkamp, N., Linley, J.E., Baker, M.D. et al. Neurological perspectives on voltage-gated sodium channels. Brain 2012 (135), 2585-2612.
75. Bevan, S., and Storey, N. Modulation of sodium channels in primary afferent neurons. Novartis Found Symp 2002 (241), 144-153.
76. England, S., Bevan, S., and Docherty, R.J. PGE2 modulates the tetrodotoxin-resistant sodium current in neonatal rat dorsal root ganglion neurones via the cyclic AMP-protein kinase A cascade. J Physiol 1996 (495, Pt 2), 429-440.
77. Fitzgerald, E.M., Okuse, K., Wood, J.N., Dolphin, A.C., and Moss, S.J. cAMP-dependent phosphorylation of the tetrodotoxin-resistant voltage-dependent sodium channel SNS. J Physiol 1999 (516, Pt 2), 433-446.
78. Vijayaragavan, K., Boutjdir, M., and Chahine, M. Modulation of Nav1.7 and Nav1.8 peripheral nerve sodium channels by protein kinase A and protein kinase C. J Neurophysiol 2004 (91), 1556-1569.
79. Chatelier, A., Dahllund, L., Eriksson, A., Krupp, J., and Chahine, M. Biophysical properties of human Na v1.7 splice variants and their regulation by protein kinase A. J Neurophysiol 2008 (99), 2241-2250.
80. Villarreal, C.F., Sachs, D., Funez, M.I., Parada, C.A., de Queiroz, C.F., and Ferreira, S.H. The peripheral pro-nociceptive state induced by repetitive inflammatory stimuli involves continuous activation of protein kinase A and protein kinase C epsilon and its Na(V)1.8 sodium channel functional regulation in the primary sensory neuron. Biochem Pharmacol 2009 (77), 867-877.
81. Liu, C., Li, Q., Su, Y., and Bao, L. Prostaglandin E2 promotes Na1.8 trafficking via its intracellular RRR motif through the protein kinase A pathway. Traffic 2010 (11), 405-417.
82. Evans, A.R., Vasko, M.R., and Nicol, G.D. The cAMP transduction cascade mediates the PGE2-induced inhibition of potassium currents in rat sensory neurones. J Physiol 1999 (516, Pt 1), 163-178.
83. Ster, J., De Bock, F., Guerineau, N.C. et al. Exchange protein activated by cAMP (Epac) mediates cAMP activation of p38 MAPK and modulation of Ca2+-dependent K+ channels in cerebellar neurons. Proc Natl Acad Sci U S A 2007 (104), 2519-2524.
84. Aley, K.O., Messing, R.O., Mochly-Rosen, D., and Levine, J.D. Chronic hypersensitivity for inflammatory nociceptor sensitization mediated by the epsilon isozyme of protein kinase C. J Neurosci 2000 (20), 4680-4685.
85. Tillu, D.V., Melemedjian, O.K., Asiedu, M.N. et al. Resveratrol engages AMPK to attenuate ERK and mTOR signaling in sensory neurons and inhibits incision-induced acute and chronic pain. Mol Pain 2012 (8), 5.
86. Asiedu, M.N., Tillu, D.V., Melemedjian, O.K. et al. Spinal protein kinase M zeta underlies the maintenance mechanism of persistent nociceptive sensitization. J Neurosci 2011 (31), 6646-6653.
87. Dina, O.A., McCarter, G.C., de Coupade, C., and Levine, J.D. Role of the sensory neuron cytoskeleton in second messenger signaling for inflammatory pain. Neuron 2003 (39), 613-624.
88. Dina, O.A., Khasar, S.G., Gear, R.W., and Levine, J.D. Activation of Gi induces mechanical hyperalgesia poststress or inflammation. Neuroscience 2009 (160), 501-507.
89. Joseph, E.K., Bogen, O., Essandri-Haber, N., and Levine, J.D. PLC-beta 3 signals upstream of PKC epsilon in acute and chronic inflammatory hyperalgesia. Pain 2007 (132), 67-73.
90. Hucho, T., and Levine, J.D. Signaling pathways in sensitization: Toward a nociceptor cell biology. Neuron 2007 (55), 365-376.
91. Pitcher, J.A., Freedman, N.J., and Lefkowitz, R.J. G protein-coupled receptor kinases. Annu Rev Biochem 1998 (67), 653-692.
92. Evron, T., Daigle, T.L., and Caron, M.G. GRK2: Multiple roles beyond G protein-coupled receptor desensitization. Trends Pharmacol Sci 2012 (33), 154-164.
93. Kleibeuker, W., Jurado-Pueyo, M., Murga, C. et al. Physiological changes in GRK2 regulate CCL2-induced signaling to ERK1/2 and Akt but not to MEK1/2 and calcium. J Neurochem 2008 (104), 979-992.
94. Peregrin, S., Jurado-Pueyo, M., Campos, P.M. et al. Phosphorylation of p38 by GRK2 at the docking groove unveils a novel mechanism for inactivating p38MAPK. Curr Biol 2006 (16), 2042-2047.
95. Jimenez-Sainz, M.C., Murga, C., Kavelaars, A. et al. G protein-coupled receptor kinase 2 negatively regulates chemokine signaling at a level downstream from G protein subunits. Mol Biol Cell 2006 (17), 25-31.
96. Wang, C., Gu, Y., Li, G.W., and Huang, L.Y. 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 2007 (584), 191-203.