Posttranslational mechanisms of peripheral sensitization

Journal of Neurobiology

Volumn 61, Issue 1, 2004, Pages 88-106

  Bhave, Gautam ^a   Gereau IV, Robert W ^b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CaMKII; Capsaicin; ERK; Ion channel; Pain; Phosphorylation; PKA; PKC; TRPV1; TTX4

Indexed keywords

CALCIUM CHANNEL; CAPSAICIN; ION CHANNEL; POTASSIUM CHANNEL; SODIUM CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL;

ANIMAL CELL; CELLULAR DISTRIBUTION; GENETIC TRANSCRIPTION; HYPERSENSITIVITY; NONHUMAN; OXIDATION REDUCTION REACTION; PERIPHERAL NERVE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; SENSITIZATION; SENSORY NERVE; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; ION CHANNELS; NEURONS; PAIN MEASUREMENT; PERIPHERAL NERVES; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 4644320317     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.20083     Document Type: Review

References (153)

1. Ahern GP, Klyachko VA, Jackson MB. 2002. cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends Neurosci 25:510-517.
2. Akopian AN, Sivilotti L, Wood JN. 1996. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379:257-262.
3. Akopian AN, Souslova V, England S, Okuse K, Ogata N, Ure J, Smith A, Kerr BJ, McMahon SB, Boyce S, et al. 1999. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat Neurosci 2:541-548.
4. Aley KO, Martin A, McMahon T, Mok J, Levine JD, Messing RO. 2001. Nociceptor sensitization by extracellular signal-regulated kinases. J Neurosci 21:6933-6939.
5. Aley KO, McCarter G, Levine JD. 1998. Nitric oxide signaling in pain and nociceptor sensitization in the rat. J Neurosci 18:7008-7014.
6. Amaya F, Decosterd I, Samad TA, Plumpton C, Tate S, Mannion RJ, Costigan M, Woolf CJ. 2000. Diversity of expression of the sensory neuron-specific TTX-resistant voltage-gated sodium ion channels SNS and SNS2. Mol Cell Neurosci 15:331-342.
7. Barber LA, Vasko MR. 1996. Activation of protein kinase C augments peptide release from rat sensory neurons. J Neurochem 67:72-80.
8. Bevan S, Yeats J. 1991. Protons activate a cation conductance in a sub-population of rat dorsal root ganglion neurones. J Physiol 433:145-161.
9. Bhave G, Hu HJ, Glauner KS, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW. 2003. Protein kinase C phosphorylation sensitizes but does not activate the capsaicin receptor transient receptor potential vanilloid 1 (TRPV1). Proc Natl Acad Sci USA 100:12480-12485.
10. Bhave G, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW. 2002. cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 35:721-731.
11. Blair NT, Bean BP. 2002. Roles of tetrodotoxin (TTX)-sensitive Na+ current, TTX-resistant Na+ current, and Ca2+ current in the action potentials of nociceptive sensory neurons. J Neurosci 22:10277-10290.
12. Brock JA, McLachlan EM, Belmonte C. 1998. Tetrodotoxin-resistant impulses in single nociceptor nerve terminals in guinea-pig cornea. J Physiol 512 (Pt 1):211-217.
13. Caffrey JM, Eng DL, Black JA, Waxman SG, Kocsis JD. 1992. Three types of sodium channels in adult rat dorsal root ganglion neurons. Brain Res 592:283-297.
14. Cardenas CG, Del Mar LP, Cooper BY, Scroggs R. 1997a. 5HT4 receptors couple positively to tetrodotoxin-insensitive sodium channels in a subpopulation of capsaicin-sensitive rat sensory neurons. J Neurosci 17:7181-7189.
15. Cardenas CG, Del Mar LP, Scroggs RS. 1995. Variation in serotonergic inhibition of calcium channel currents in four types of rat sensory neurons differentiated by membrane properties. J Neurophysiol 74:1870-1879.
16. Cardenas CG, Del Mar LP, Scroggs RS. 1997b. Two parallel signaling pathways couple 5HT1A receptors to N- and L-type calcium channels in C-like rat dorsal root ganglion cells. J Neurophysiol 77:3284-3296.
17. Caterina MJ, Julius D. 2001. The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 24:487-517.
18. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D. 2000. Impaired nociception and pain sensation in mice lacking the capsaicin receptor [see comments]. Science 288:306-313.
19. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D. 1999. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398:436-441.
20. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. 1997. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824.
21. Catterall WA. 2000. Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol 16:521-555.
22. 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.
23. Cesare P, McNaughton P. 1996. A novel heat-activated current in nociceptive neurons and its sensitization by bradykinin [see comments]. Proc Natl Acad Sci USA 93:15435-15439.
24. Cho H, Shin J, Shin CY, Lee SY, Oh U. 2002. Mechanosensitive ion channels in cultured sensory neurons of neonatal rats. J Neurosci 22:1238-1247.
25. Cholewinski A, Burgess GM, Bevan S. 1993. The role of calcium in capsaicin-induced desensitization in rat cultured dorsal root ganglion neurons. Neuroscience 55:1015-1023.
26. 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.
27. Clark JD, Tempel BL. 1998. Hyperalgesia in mice lacking the Kv1.1 potassium channel gene. Neurosci Lett 251:121-124.
28. Corey DP. 2003. New TRP channels in hearing and mechanosensation. Neuron 39:585-588.
29. Crandall M, Kwash J, Yu W, White G. 2002. Activation of protein kinase C sensitizes human VR1 to capsaicin and to moderate decreases in pH at physiological temperatures in Xenopus oocytes. Pain 98:109-117.
30. Cummins TR, Dib-Hajj SD, Black JA, Akopian AN, Wood JN, Waxman SG. 1999. A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J Neurosci 19:RC43.
31. Cunha FQ, Teixeira MM, Ferreira SH. 1999. Pharmacological modulation of secondary mediator systems-cyclic AMP and cyclic GMP-on inflammatory hyperalgesia. Br J Pharmacol 127:671-678.
32. Dai Y, Iwata K, Fukuoka T, Kondo E, Tokunaga A, Yamanaka H, Tachibana T, Liu Y, Noguchi K. 2002. Phosphorylation of extracellular signal-regulated kinase in primary afferent neurons by noxious stimuli and its involvement in peripheral sensitization. J Neurosci 22:7737-7745.
33. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, et al. 2000. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405:183-187.
34. De Waard M, Liu H, Walker D, Scott VE, Gurnett CA, Campbell KP. 1997. Direct binding of G-protein beta-gamma complex to voltage-dependent calcium channels. Nature 385:446-450.
35. Dib-Hajj S, Black JA, Cummins TR, Waxman SG. 2002. NaN/Nav1.9: a sodium channel with unique properties. Trends Neurosci 25:253-259.
36. Dib-Hajj SD, Tyrrell L, Black JA, Waxman SG. 1998. NaN, a novel voltage-gated Na channel, is expressed preferentially in peripheral sensory neurons and down-regulated after axotomy. Proc Natl Acad Sci USA 95:8963-8968.
37. Djouhri L, Bleazard L, Lawson SN. 1998. Association of somatic action potential shape with sensory receptive properties in guinea-pig dorsal root ganglion neurones. J Physiol 513(Pt 3):857-872.
38. Djouhri L, Lawson SN. 1999. Changes in somatic action potential shape in guinea-pig nociceptive primary afferent neurones during inflammation in vivo. J Physiol 520(Pt 2):565-576.
39. Docherty RJ, Yeats JC, Bevan S, Boddeke HW. 1996. Inhibition of calcineurin inhibits the desensitization of capsaicin-evoked currents in cultured dorsal root ganglion neurones from adult rats. Pflugers Arch 431:828-837.
40. Drew LJ, Wood JN, Cesare P. 2002. Distinct mechanosensitive properties of capsaicin-sensitive and -insensitive sensory neurons. J Neurosci 22:RC228.
41. Duarte ID, dos Santos IR, Lorenzetti BB, Ferreira SH. 1992. Analgesia by direct antagonism of nociceptor sensitization involves the arginine-nitric oxide-cGMP pathway. Eur J Pharmacol 217:225-227.
42. Elliott AA, Elliott JR. 1993. Characterization of TTX-sensitive and TTX-resistant sodium currents in small cells from adult rat dorsal root ganglia. J Physiol 463:39-56.
43. England S, Bevan S, Docherty RJ. 1996. 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(Pt 2):429-440.
44. Evans AR, Nicol GD, Vasko MR. 1996. Differential regulation of evoked peptide release by voltage-sensitive calcium channels in rat sensory neurons. Brain Res 712:265-273.
45. Evans AR, Vasko MR, Nicol GD. 1999. The cAMP transduction cascade mediates the PGE2-induced inhibition of potassium currents in rat sensory neurones. J Physiol 516(Pt 1):163-178.
46. Fitzgerald EM, Okuse K, Wood JN, Dolphin AC, Moss SJ. 1999. cAMP-dependent phosphorylation of the tetrodotoxin-resistant voltage-dependent sodium channel SNS. J Physiol 516(Pt 2):433-446.
47. Fjell J, Cummins TR, Dib-Hajj SD, Fried K, Black JA, Waxman SG. 1999. Differential role of GDNF and NGF in the maintenance of two TTX-resistant sodium channels in adult DRG neurons. Brain Res Mol Brain Res 67:267-282.
48. Gillespie PG, Walker RG. 2001. Molecular basis of mechanosensory transduction. Nature 413:194-202.
49. NA by PKC and PKA and their role in PGE2-induced sensitization of rat sensory neurons in vitro. J Neurosci 18:10345-10355.
50. Gold MS, Reichling DB, Shuster MJ, Levine JD. 1996a. Hyperalgesic agents increase a tetrodotoxin-resistant Na+ current in nociceptors. Proc Natl Acad Sci USA 93:1108-1112.
51. Gold MS, Shuster MJ, Levine JD. 1996b. Role of a Ca(2+)-dependent slow afterhyperpolarization in prostaglandin E2-induced sensitization of cultured rat sensory neurons. Neurosci Lett 205:161-164.
52. Gross RA, Macdonald RL. 1989. Cyclic AMP selectively reduces the N-type calcium current component of mouse sensory neurons in culture by enhancing inactivation. J Neurophysiol 61:97-105.
53. Gross RA, Uhler MD, Macdonald RL. 1990. The cyclic AMP-dependent protein kinase catalytic subunit selectively enhances calcium currents in rat nodose neurones. J Physiol 429:483-496.
54. Guenther S, Reeh PW, Kress M. 1999. Rises in [Ca2+]i mediate capsaicin- and proton-induced heat sensitization of rat primary nociceptive neurons. Eur J Neurosci 11:3143-3150.
55. Hamid J, Nelson D, Spaetgens R, Dubel SJ, Snutch TP, Zamponi GW. 1999. Identification of an integration center for cross-talk between protein kinase C and G protein modulation of N-type calcium channels. J Biol Chem 274:6195-6202.
56. Herlitze S, Garcia DE, Mackie K, Hille B, Scheuer T, Catterall WA. 1996. Modulation of Ca2+ channels by G-protein beta gamma subunits. Nature 380:258-262.
57. Hille B. 2001. Ion channels of excitable membranes. Sunderland, MA: Sinauer, p xviii, 814.
58. Hingtgen CM, Waite KJ, Vasko MR. 1995. Prostaglandins facilitate peptide release from rat sensory neurons by activating the adenosine 3′,5′-cyclic monophosphate transduction cascade. J Neurosci 15:5411-5419.
59. Holthusen H, Arndt JO. 1994. Nitric oxide evokes pain in humans on intracutaneous injection. Neurosci Lett 165:71-74.
60. Holthusen H, Arndt JO. 1995. Nitric oxide evokes pain at nociceptors of the paravascular tissue and veins in humans. J Physiol 487(Pt 1):253-258.
61. Hu HJ, Bhave G, Gereau RW. 2002. Prostaglandin and protein kinase A-dependent modulation of vanilloid receptor function by metabotropic glutamate receptor 5: potential mechanism for thermal hyperalgesia. J Neurosci 22:7444-7452.
62. Hu HJ, Gereau RW. 2003. ERK integrates PKA and PKC signaling in superficial dorsal horn neurons. II. Modulation of neuronal excitability. J Neurophysiol 90:1680-1688.
63. Hu HJ, Glauner KS, Gereau RW. 2003. ERK integrates PKA and PKC signaling in superficial dorsal horn neurons. I. Modulation of A-type K+ currents. J Neurophysiol 90:1671-1679.
64. Hwang SW, Cho H, Kwak J, Lee SY, Kang CJ, Jung J, Cho S, Min KH, Suh YG, Kim D, Oh U. 2000. Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc Natl Acad Sci USA 97:6155-6160.
65. Ji R-R, Baba H, Brenner GJ, Woolf CJ. 1999. Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 2:1114-1119.
66. Ji RR, Rupp F. 1997. Phosphorylation of transcription factor CREB in rat spinal cord after formalin-induced hyperalgesia: relationship to c-fos induction. J Neurosci 17:1776-1785.
67. Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ. 2002. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36:57-68.
68. Jiang X, Zhang YH, Clark JD, Tempel BL, Nicol GD. 2003. Prostaglandin E2 inhibits the potassium current in sensory neurons from hyperalgesic Kv1.1 knockout mice. Neuroscience 119:65-72.
69. Johnston D, Wu SM-s. 1995. Foundations of cellular neurophysiology. Cambridge, MA: MIT Press, p xxxi, 676.
70. Jung J, Shin JS, Lee SY, Hwang SW, Koo J, Cho H, Oh U. 2003. Phosphorylation of vanilloid receptor 1 by Ca+2/calmodulin-dependent kinase II regulates its vanilloid binding. J Biol Chem 279:7048-7054.
71. Karim F, Wang C-C, Gereau RW. 2001. Metabotropic glutamate receptor subtypes 1 and 5 are activators of extracellular signal-regulated kinase signaling required for inflammatory pain in mice. J Neurosci 21:3771-3779.
72. Kawabata A, Manabe S, Manabe Y, Takagi H. 1994. Effect of topical administration of L-arginine on formalin-induced nociception in the mouse: a dual role of peripherally formed NO in pain modulation. Br J Pharmacol 112:547-550.
73. Kerr BJ, Souslova V, McMahon SB, Wood JN. 2001. A role for the TTX-resistant sodium channel Nav 1.8 in NGF-induced hyperalgesia, but not neuropathic pain. Neuroreport 12:3077-3080.
74. Khasar SG, Gold MS, Levine JD. 1998. A tetrodotoxin-resistant sodium current mediates inflammatory pain in the rat. Neurosci Lett 256:17-20.
75. Khasar SG, Lin YH, Martin A, Dadgar J, McMahon T, Wang D, Hundle B, Aley KO, Isenberg W, McCarter G, et al. 1999a. A novel nociceptor signaling pathway revealed in protein kinase C epsilon mutant mice. Neuron 24:253-260.
76. Khasar SG, McCarter G, Levine JD. 1999b. Epinephrine produces a beta-adrenergic receptor-mediated mechanical hyperalgesia and in vitro sensitization of rat nociceptors. J Neurophysiol 81:1104-1112.
77. King AP, Hall KE, Macdonald RL. 1999. kappa- and mu-Opioid inhibition of N-type calcium currents is attenuated by 4beta-phorbol 12-myristate 13-acetate and protein kinase C in rat dorsal root ganglion neurons. J Pharmacol Exp Ther 289:312-320.
78. Koplas PA, Rosenberg RL, Oxford GS. 1997. The role of calcium in the desensitization of capsaicin responses in rat dorsal root ganglion neurons. J Neurosci 17:3525-3537.
79. Kress M, Fetzer S, Reeh PW, Vyklicky L. 1996. Low pH facilitates capsaicin responses in isolated sensory neurons of the rat. Neurosci Lett 211:5-8.
80. Kress M, Rodl J, Reeh PW. 1996. Stable analogues of cyclic AMP but not cyclic GMP sensitize unmyelinated primary afferents in rat skin to heat stimulation but not to inflammatory mediators, in vitro. Neuroscience 74:609-617.
81. Krishtal O. 2003. The ASICs: signaling molecules? Modulators? Trends Neurosci 26:477-483.
82. Lang E, Novak A, Reeh PW, Handwerker HO. 1990. Chemosensitivity of fine afferents from rat skin in vitro. J Neurophysiol 63:887-901.
83. Lawand NB, Willis WD, Westlund KN. 1997. Blockade of joint inflammation and secondary hyperalgesia by L-NAME, a nitric oxide synthase inhibitor. Neuroreport 8:895-899.
84. Leng S, Mizumura K, Koda H, Kumazawa T. 1996. Excitation and sensitization of the heat response induced by a phorbol ester in canine visceral polymodal receptors studied in vitro. Neurosci Lett 206:13-16.
85. Levine JD, Reichling DB. 1999. Peripheral mechanisms of inflammatory pain. In: Melzack R, editor. Textbook of pain. Edinburgh: Churchill Livingstone, p 59-84.
86. Levine JD, Taiwo YO. 1989. Involvement of the mu-opiate receptor in peripheral analgesia. Neuroscience 32:571-575.
87. Li M, West JW, Numann R, Murphy BJ, Scheuer T, Catterall WA. 1993. Convergent regulation of sodium channels by protein kinase C and cAMP-dependent protein kinase. Science 261:1439-1442.
88. Liang YF, Haake B, Reeh PW. 2001. Sustained sensitization and recruitment of rat cutaneous nociceptors by bradykinin and a novel theory of its excitatory action. J Physiol 532:229-239.
89. Liu L, Simon SA. 1996. Capsaicin-induced currents with distinct desensitization and Ca2+ dependence in rat trigeminal ganglion cells. J Neurophysiol 75:1503-1514.
90. Lopshire JC, Nicol GD. 1998. 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 18:6081-6092.
91. Luttrell LM, Daaka Y, Lefkowitz RJ. 1999. Regulation of tyrosine kinase cascades by G-protein-coupled receptors. Curr Opin Cell Biol 11:177-183.
92. Lynn B, O'Shea NR. 1998. Inhibition of forskolin-induced sensitisation of frog skin nociceptors by the cyclic AMP-dependent protein kinase A antagonist H-89. Brain Res 780:360-362.
93. McCarter GC, Reichling DB, Levine JD. 1999. Mechanical transduction by rat dorsal root ganglion neurons in vitro. Neurosci Lett 273:179-182.
94. McCleskey EW, Gold MS. 1999. Ion channels of nociception. Annu Rev Physiol 61:835-856.
95. McKemy DD, Neuhausser WM, Julius D. 2002. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52-58.
96. Mohapatra DP, Nau C. 2003. Desensitization of capsaicin-activated currents in the vanilloid receptor TRPV1 is decreased by the cyclic AMP-dependent protein kinase pathway. J Biol Chem 278:50080-50090.
97. Moises HC, Rusin KI, Macdonald RL. 1994. Mu- and kappa-opioid receptors selectively reduce the same transient components of high-threshold calcium current in rat dorsal root ganglion sensory neurons. J Neurosci 14:5903-5916.
98. Nicol GD, Klingberg DK, Vasko MR. 1992. Prostaglandin E2 increases calcium conductance and stimulates release of substance P in avian sensory neurons. J Neurosci 12:1917-1927.
99. Nicol GD, Vasko MR, Evans AR. 1997. Prostaglandins suppress an outward potassium current in embryonic rat sensory neurons. J Neurophysiol 77:167-176.
100. Numazaki M, Tominaga T, Toyooka H, Tominaga M. 2002. Direct phosphorylation of capsaicin receptor VR1 by protein kinase Cepsilon and identification of two target serine residues. J Biol Chem 277:13375-13378.
101. Ogasawara M, Kurihara T, Hu Q, Tanabe T. 2001. Characterization of acute somatosensory pain transmission in P/Q-type Ca(2+) channel mutant mice, leaner. FEBS Lett. 508:181-186.
102. Olah Z, Karai L, Iadarola MJ. 2002. Protein kinase C(alpha) is required for vanilloid receptor 1 activation. Evidence for multiple signaling pathways. J Biol Chem 277:35752-35759.
103. Patapoutian A, Peier AM, Story GM, Viswanath V. 2003. ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat Rev Neurosci 4:529-539.
104. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A. 2002a. A TRP channel that senses cold stimuli and menthol. Cell 108:705-715.
105. Peier AM, Reeve AJ, Andersson DA, Moqrich A, Barley TJ. Hergarden AC, Story GM, Colley S, Hogenesch JB, McIntyre P, et al. 2002b. A heat-sensitive TRP channel expressed in keratinocytes. Science 296:2046-2049.
106. Piper AS, Yeats JC, Bevan S, Docherty RJ. 1999. A study of the voltage dependence of capsaicin-activated membrane currents in rat sensory neurones before and after acute desensitization. J Physiol 518:721-733.
107. Porreca F, Lai J, Bian D, Wegert S, Ossipov MH, Eglen RM, Kassotakis L, Novakovic S, Rabert DK, Sangameswaran L, et al. 1999. A comparison of the potential role of the tetrodotoxin-insensitive sodium channels, PN3/SNS and NaN/SNS2, in rat models of chronic pain. Proc Natl Acad Sci USA 96:7640-7644.
108. Premkumar LS, Ahern GP. 2000. Induction of vanilloid receptor channel activity by protein kinase C. Nature 408:985-990.
109. Qian Y, Chao DS, Santillano DR, Cornwell TL, Nairn AC, Greengard P, Lincoln TM, Bredt DS. 1996. cGMP-dependent protein kinase in dorsal root ganglion: relationship with nitric oxide synthase and nociceptive neurons. J Neurosci 16:3130-3138.
110. Qiao LY, Vizzard MA. 2004. Up-regulation of phosphorylated CREB but not c-Jun in bladder afferent neurons in dorsal root ganglia after cystitis. J Comp Neurol 469:262-274.
111. Raja SN, Meyer RA, Ringkamp M, Campbell JN. 1999. Peripheral neural mechanisms of nociception. In: Melzack R, editor. Textbook of pain. Edinburgh: Churchill Livingstone, p 11-57.
112. Rasband MN, Park EW, Vanderah TW, Lai J, Porreca F, Trimmer JS. 2001. Distinct potassium channels on pain-sensing neurons. Proc Natl Acad Sci USA 98:13373-13378.
113. Rathee PK, Distler C, Obreja O, Neuhuber W, Wang GK, Wang SY, Nau C, Kress M. 2002. PKA/AKAP/VR-1 Module: A common link of Gs-mediated signaling to thermal hyperalgesia. J Neurosci 22:4740-4745.
114. Renganathan M, Cummins TR, Waxman SG. 2001. Contribution of Na(v)1.8 sodium channels to action potential electrogenesis in DRG neurons. J Neurophysiol 86:629-640.
115. Ritter AM, Mendell LM. 1992. Somal membrane properties of physiologically identified sensory neurons in the rat: effects of nerve growth factor. J Neurophysiol 68:2033-2041.
116. Roy ML, Narahashi T. 1992. Differential properties of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels in rat dorsal root ganglion neurons. J Neurosci 12:2104-2111.
117. Rusin KI, Moises HC. 1995. mu-Opioid receptor activation reduces multiple components of high-threshold calcium current in rat sensory neurons. J Neurosci 15:4315-4327.
118. Saegusa H, Kurihara T, Zong S, Minowa O, Kazuno A, Han W, Matsuda Y, Yamanaka H, Osanai M, Noda T, et al. 2000. Altered pain responses in mice lacking alpha IE subunit of the voltage-dependent Ca2+ channel. Proc Natl Acad Sci USA 97:6132-6137.
119. Saegusa H, Matsuda Y, Tanabe T. 2002. Effects of ablation of N- and R-type Ca(2+) channels on pain transmission. Neurosci Res 43:1-7.
120. Sangameswaran L, Delgado SG, Fish LM, Koch BD, Jakeman LB, Stewart GR, Sze P, Hunter JC, Eglen RM, Herman RC. 1996. Structure and function of a novel voltage-gated, tetrodotoxin-resistant sodium channel specific to sensory neurons. J Biol Chem 271:5953-5956.
121. Schepelmann K, Messlinger K, Schmidt RF. 1993. The effects of phorbol ester on slowly conducting afferents of the cat's knee joint. Exp Brain Res 92:391-398.
122. Sculptoreanu A, de Groat WC. 2003. Protein kinase C is involved in neurokinin receptor modulation of N- and L-type Ca2+ channels in DRG neurons of the adult rat. J Neurophysiol 90:21-31.
123. Shin J, Cho H, Hwang SW, Jung J, Shin CY, Lee SY, Kim SH, Lee MG, Choi YH, Kim J, et al. 2002. Bradykinin-12-lipoxygenase-VR1 signaling pathway for inflammatory hyperalgesia. Proc Natl Acad Sci USA 99:10150-10155.
124. Steen KH, Reeh PW, Anton F, Handwerker HO. 1992. Protons selectively induce lasting excitation and sensitization to mechanical stimulation of nociceptors in rat skin, in vitro. J Neurosci 12:86-95.
125. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, et al. 2003. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819-829.
126. Su X, Wachtel RE, Gebhart GF. 2000. Mechanosensitive potassium channels in rat colon sensory neurons. J Neurophysiol 84:836-843.
127. Sugiura T, Tominaga M, Katsuya H, Mizumura K. 2002. Bradykinin lowers the threshold temperature for heat activation of vanilloid receptor 1. J Neurophysiol 88:544-548.
128. Swartz KJ. 1993. Modulation of Ca2+ channels by protein kinase C in rat central and peripheral neurons: disruption of G protein-mediated inhibition. Neuron 11:305-320.
129. Sweatt JD. 2001. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76:1-10.
130. Szallasi A, Blumberg PM. 1999. Vanilloid (Capsaicin) receptors and mechanisms. Pharmacol Rev 51:159-212.
131. Taiwo YO, Bjerknes LK, Goetzl EJ, Levine JD. 1989. Mediation of primary afferent peripheral hyperalgesia by the cAMP second messenger system. Neuroscience 32:577-580.
132. Taiwo YO, Levine JD. 1991. Further confirmation of the role of adenyl cyclase and of cAMP-dependent protein kinase in primary afferent hyperalgesia. Neuroscience 44:131-135.
133. Tate S, Benn S, Hick C, Trezise D, John V, Mannion RJ, Costigan M, Plumpton C, Grose D, Gladwell Z, et al. 1998. Two sodium channels contribute to the TTX-R sodium current in primary sensory neurons. Nat Neurosci 1:653-655.
134. Todorovic SM, Jevtovic-Todorovic V, Meyenburg A, Mennerick S, Perez-Reyes E, Romano C, Olney JW, Zorumski CF. 2001. Redox modulation of T-type calcium channels in rat peripheral nociceptors. Neuron 31:75-85.
135. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D. 1998. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21:531-543.
136. Tominaga M, Wada M, Masu M. 2001. Potentiation of capsaicin receptor activity by metabotropic ATP receptors as a possible mechanism for ATP-evoked pain and hyperalgesia. Proc Natl Acad Sci USA 98:6951-6956.
137. Tsien RW, Lipscombe D, Madison DV, Bley KR, Fox AP. 1988. Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci 11:431-438.
138. Vanegas H, Schaible H. 2000. Effects of antagonists to high-threshold calcium channels upon spinal mechanisms of pain, hyperalgesia and allodynia. Pain 85:9-18.
139. Vellani V, Mapplebeck S, Moriondo A, Davis JB, McNaughton PA. 2001. Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide. J Physiol 534:813-825.
140. Vijayaragavan K, Boutjdir M, Chahine M. 2003. Modulation of Nav1.7 and Nav1.8 peripheral nerve sodium channels by protein kinase A and protein kinase C. J Neurophysiol 91:1556-1569.
141. Villiere V, McLachlan EM. 1996. Electrophysiological properties of neurons in intact rat dorsal root ganglia classified by conduction velocity and action potential duration. J Neurophysiol 76:1924-1941.
142. Vivancos GG, Parada CA, Ferreira SH. 2003. Opposite nociceptive effects of the arginine/NO/cGMP pathway stimulation in dermal and subcutaneous tissues. Br J Pharmacol 138:1351-1357.
143. Vyklicky L, Lyfenko A, Susankova K, Teisinger J, Vlachova V. 2002. Reducing agent dithiothreitol facilitates activity of the capsaicin receptor VR-1. Neuroscience 111:435-441.
144. Wang JF, Khasar SG, Ahlgren SC, Levine JD. 1996. Sensitization of C-fibres by prostaglandin E2 in the rat is inhibited by guanosine 5′-O-(2-thiodiphosphate), 2′,5′-dideoxyadenosine and Walsh inhibitor peptide. Neuroscience 71:259-263.
145. Weinreich D, Wonderlin WF. 1987. Inhibition of calcium-dependent spike after-hyperpolarization increases excitability of rabbit visceral sensory neurones. J Physiol 394:415-427.
146. Wilding TJ, Womack MD, McCleskey EW. 1995. Fast, local signal transduction between the mu opioid receptor and Ca2+ channels. J Neurosci 15:4124-4132.
147. Woolf CJ, Salter MW. 2000. Neuronal plasticity: increasing the gain in pain. Science 288:1765-1769.
148. Xu H, Ramsey IS, Kotecha SA, Moran MM, Chong JA, Lawson D, Ge P, Lilly J, Silos-Santiago I, Xie Y, et al. 2002. TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418:181-186.
149. Yang D, Gereau RW. 2002. Peripheral group II metabotropic glutamate receptors (mGluR2/3) regulate prostaglandin E2-mediated sensitization of capsaicin responses and thermal nociception. J Neurosci 22:6388-63893.
150. Zamponi GW, Bourinet E, Nelson D, Nargeot J, Snutch TP. 1997. Crosstalk between G proteins and protein kinase C mediated by the calcium channel alpha1 subunit. Nature 385:442-446.
151. Zhang YH, Kenyon JL, Nicol GD. 2001. Phorbol ester-induced inhibition of potassium currents in rat sensory neurons requires voltage-dependent entry of calcium. J Neurophysiol 85:362-373.
152. Zhou Y, Zhou Z, Zhao Z. 2001. PKC regulates capsaicin-induced currents of dorsal root ganglion neurons in rats. Neuropharmacology 41:601-608.
153. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, Hogestatt ED. 1999. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400:452-457.