A transient receptor potential vanilloid 4-dependent mechanism of hyperalgesia is engaged by concerted action of inflammatory mediators

Journal of Neuroscience

Volumn 26, Issue 14, 2006, Pages 3864-3874

  Alessandri Haber, Nicole ^a   Dina, Olayinka A ^a   Joseph, Elizabeth K ^a   Reichling, David ^a   Levine, Jon D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dorsal root ganglion; Inflammatory mediators; Mechanotransduction; Pain; Sensory nerve; Silent nociceptor

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; CARRAGEENAN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; PROTEIN KINASE C EPSILON; UNCLASSIFIED DRUG; VANILLOID RECEPTOR; VANILLOID RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; CONTROLLED STUDY; HYPERALGESIA; INFLAMMATION; MALE; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; MOUSE; MUSCLE SPINDLE AFFERENT NERVE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOSIS; PAIN; PAIN THRESHOLD; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SENSORY NERVE; SPINAL GANGLION; WITHDRAWAL REFLEX;

ANIMALS; CELLS, CULTURED; GANGLIA, SPINAL; HYPERALGESIA; INFLAMMATION MEDIATORS; MALE; MECHANOTRANSDUCTION, CELLULAR; RATS; RATS, SPRAGUE-DAWLEY; TOUCH; TRPV CATION CHANNELS;

EID: 33645557094     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5385-05.2006     Document Type: Article

References (72)

1. Adriaensen H, Gybels J, Handwerker HO, Van Hees J (1984) Nociceptor discharges and sensations due to prolonged noxious mechanical stimulation - a paradox. Hum Neurobiol 3:53-58.
2. Alessandri-Haber N, Yeh JJ, Boyd AE, Parada CA, Chen X, Reichling DB, Levine JD (2003) Hypotonicity induces TRPV4-mediated nociception in rat. Neuron 39:497-511.
3. Alessandri-Haber N, Dina OA, Yeh JJ, Parada CA, Reichling DB, Levine JD (2004) Transient receptor potential vanilloid 4 is essential in chemotherapy-induced neuropathic pain in the rat. J Neurosci 24:4444-4452.
4. Alessandri-Haber N, Joseph E, Dina OA, Liedtke W, Levine JD (2005) TRPV4 mediates pain-related behavior induced by mild hypertonic stimuli in the presence of inflammatory mediator. Pain 118:70-79.
5. Aley KO, Levine JD (1999) Role of protein kinase A in the maintenance of inflammatory pain. J Neurosci 19:2181-2186.
6. Aley KO, Levine JD (2001) Rapid onset pain induced by intravenous streptozotocin in the rat. J Pain 2:146-150.
7. 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.
8. Andrew D, Greenspan JD (1999) Peripheral coding of tonic mechanical cutaneous pain: comparison of nociceptor activity in rat and human psychophysics. J Neurophysiol 82:2641-2648.
9. + channels by protein kinase C and protein kinase A anchored to AKAP-15. Mol Cell Neurosci 21:63-80.
10. 4 receptors couple positively to tetrodotoxin-insensitive sodium channels in a subpopulation of capsaicin-sensitive rat sensory neurons. J Neurosci 17:7181-7189.
11. 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.
12. Chen Y, Button B, Altenberg GA, Reuss L (2004) Potentiation of effect of PKA stimulation of Xenopus CFTR by activation of PKC: role of NBD2. Am J Physiol Cell Physiol 287:C1436-C1444.
13. 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.
14. Daaka Y, Luttrell LM, Lefkowitz RJ (1997) Switching of the coupling of the β2-adrenergic receptor to different G proteins by protein kinase A. Nature 390:88-91.
15. Gao X, Wu L, O'Neil RG (2003) Temperature-modulated diversity of TRPV4 channel gating: activation by physical stresses and phorbol ester derivatives through protein kinase C-dependent and -independent pathways. J Biol Chem 278:27129-27137.
16. Graness A, Adomeit A, Ludwig B, Muller WD, Kaufmann R, Liebmann C (1997) Novel bradykinin signalling events in PC-12 cells: stimulation of the cAMP pathway leads to cAMP-mediated translocation of protein kinase Cε. Biochem J 327:147-154.
17. Grubb BD, Birrell GJ, McQueen DS, Iggo A (1991) The role of PGE2 in the sensitization of mechanoreceptors in normal and inflamed ankle joints of the rat. Exp Brain Res 84:383-392.
18. - channels by protein kinase C and cAMP-dependent protein kinase in the rat. J Physiol (Lond) 506:331-339.
19. Guler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M (2002) Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22:6408-6414.
20. Habler HJ, Janig W, Koltzenburg M (1988) A novel type of unmyelinated chemosensitive nociceptor in the acutely inflamed urinary bladder. Agents Actions 25:219-221.
21. Handwerker HO, Kilo S, Reeh PW (1991) Unresponsive afferent nerve fibres in the sural nerve of the rat. J Physiol (Lond) 435:229-242.
22. Heubach JF, Ravens U, Kaumann AJ (2004) Epinephrine activates both Gs and Gi pathways, but norepinephrine activates only the Gs pathway through human β2-adrenoceptors overexpressed in mouse heart. Mol Pharmacol 65:1313-1322.
23. Houck CS, Khodorova A, Reale AM, Strichartz GR, Davar G (2004) Sensory fibers resistant to the actions of tetrodotoxin mediate nocifensive responses to local administration of endothelin-1 in rats. Pain 110:719-726.
24. + neuron-specific mechanism. J Neurosci 25:6119-6126.
25. Khasar SG, Ho T, Green PG, Levine JD (1994) Comparison of prostaglandin E1- and prostaglandin E2-induced hyperalgesia in the rat. Neuroscience 62:345-350.
26. Khasar SG, Lin YH, Martin A, Dadgar J, McMahon T, Wang D, Hundle B, Aley KO, Isenberg W, McCarter G, Green PG, Hodge CW, Levine JD, Messing RO (1999) A novel nociceptor signaling pathway revealed in protein kinase C εmutant mice. Neuron 24:253-260.
27. Kress M, Koltzenburg M, Reeh PW, Handwerker HO (1992) Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J Neurophysiol 68:581-595.
28. 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.
29. Kress M, Reeh PW, Vyklicky L (1997) An interaction of inflammatory mediators and protons in small diameter dorsal root ganglion neurons of the rat. Neurosci Lett 224:37-40.
30. Lang E, Novak A, Reeh PW, Handwerker HO (1990) Chemosensitivity of fine afferents from rat skin in vitro. J Neurophysiol 63:887-901.
31. Lecar H, Larsson HP, Grabe M (2003) Electrostatic model of S4 motion in voltage-gated ion channels. Biophys J 85:2854-2864.
32. Levine JD, Reichling D (1999) Peripheral mechanisms of inflammatory pain (Wall PD, Melzack R, Bonica JJ, eds). New York: Churchill Livingston.
33. -/- mice. Proc Natl Acad Sci USA 100:13698-13703.
34. Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, Heller S (2000) Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103:525-535.
35. Linhart O, Obreja O, Kress M (2003) The inflammatory mediators serotonin, prostaglandin E2 and bradykinin evoke calcium influx in rat sensory neurons. Neuroscience 118:69-74.
36. Lotz M, Carson DA, Vaughan JH (1987) Substance P activation of rheumatoid synoviocytes: neural pathway in pathogenesis of arthritis. Science 235:893-895.
37. Malmberg AB, Brandon EP, Idzerda RL, Liu H, McKnight GS, Basbaum AI (1997) 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 17:7462-7470.
38. Mannikko R, Elinder F, Larsson HP (2002) Voltage-sensing mechanism is conserved among ion channels gated by opposite voltages. Nature 419:837-841.
39. Martin HA, Basbaum AI, Kwiat GC, Goetzl EJ, Levine JD (1987) Leukotriene and prostaglandin sensitization of cutaneous high-threshold C- and A-δ mechanonociceptors in the hairy skin of rat hindlimbs. Neuroscience 22:651-659.
40. McMahon SB, Koltzenburg M (1990) Novel classes of nociceptors: beyond Sherrington. Trends Neurosci 13:199-201.
41. Millan MJ (1999) The induction of pain: an integrative review. Prog Neurobiol 57:1-164.
42. Mizumura K, Sato J, Kumazawa T (1987) Effects of prostaglandins and other putative chemical intermediaries on the activity of canine testicular polymodal receptors studied in vitro. Pflügers Arch 408:565-572.
43. Nilius B, Prenen J, Wissenbach U, Bodding M, Droogmans G (2001) Differential activation of the volume-sensitive cation channel TRP12 (OTRPC4) and volume-regulated anion currents in HEK-293 cells. Pflügers Arch 443:227-233.
44. Nilius B, Vriens J, Prenen J, Droogmans G, Voets T (2004) TRPV4 calcium entry channel: a paradigm for gating diversity. Am J Physiol Cell Physiol 286:C195-C205.
45. Orstavik K, Weidner C, Schmidt R, Schmelz M, Hilliges M, Jorum E, Handwerker H, Torebjork E (2003) Pathological C-fibres in patients with a chronic painful condition. Brain 126:567-578.
46. Papazian DM, Timpe LC, Jan YN, Jan LY (1991) Alteration of voltage-dependence of Shaker potassium channel by mutations in the S4 sequence. Nature 349:305-310.
47. Ping P, Zhang J, Zheng YT, Li RC, Dawn B, Tang XL, Takano H, Balafanova Z, Bolli R (1999) Demonstration of selective protein kinase C-dependent activation of Src and Lck tyrosine kinases during ischemic preconditioning in conscious rabbits. Circ Res 85:542-550.
48. Ping P, Song C, Zhang J, Guo Y, Cao X, Li RC, Wu W, Vondriska TM, Pass JM, Tang XL, Pierce WM, Bolli R (2002) Formation of protein kinase Cε-Lck signaling modules confers cardioprotection. J Clin Invest 109:499-507.
49. Purcell AL, Carew TJ (2001) Modulation of excitability in Aplysia tail sensory neurons by tyrosine kinases. J Neurophysiol 85:2398-2411.
50. Schaible HG, Schmidt RF (1985) Effects of an experimental arthritis on the sensory properties of fine articular afferent units. J Neurophysiol 54:1109-1122.
51. Schaible HG, Schmidt RF (1988a) Time course of mechanosensitivity changes in articular afferents during a developing experimental arthritis. J Neurophysiol 60:2180-2195.
52. Schaible HG, Schmidt RF (1988b) Excitation and sensitization of fine articular afferents from cat's knee joint by prostaglandin E2. J Physiol (Lond) 403:91-104.
53. Schmelz M, Schmidt R, Ringkamp M, Handwerker HO, Torebjork HE (1994) Sensitization of insensitive branches of C nociceptors in human skin. J Physiol 480:389-394.
54. Schmidt R, Schmelz M, Forster C, Ringkamp M, Torebjork E, Handwerker H (1995) Novel classes of responsive and unresponsive C nociceptors in human skin. J Neurosci 15:333-341.
55. Schmidt R, Schmelz M, Torebjork HE, Handwerker HO (2000) Mechano-insensitive nociceptors encode pain evoked by tonic pressure to human skin. Neuroscience 98:793-800.
56. Steen KH, Steen AE, Kreysel HW, Reeh PW (1996) Inflammatory mediators potentiate pain induced by experimental tissue acidosis. Pain 66:163-170.
57. Stork PJ, Schmitt JM (2002) Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol 12:258-266.
58. Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD (2000) OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2:695-702.
59. Sugita S, Baxter DA, Byrne JH (1997) Modulation of a cAMP/protein kinase A cascade by protein kinase C in sensory neurons of Aplysia. J Neurosci 17:7237-7244.
60. Suzuki M, Mizuno A, Kodaira K, Imai M (2003a) Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278:22664-22668.
61. Suzuki M, Watanabe Y, Oyama Y, Mizuno A, Kusano E, Hirao A, Ookawara S (2003b) Localization of mechanosensitive channel TRPV4 in mouse skin. Neurosci Lett 353:189-192.
62. Taiwo YO, Levine JD (1988) Characterization of the arachidonic acid metabolites mediating bradykinin and noradrenaline hyperalgesia. Brain Res 458:402-406.
63. 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.
64. Taiwo YO, Heller PH, Levine JD (1992) Mediation of serotonin hyperalgesia by the cAMP second messenger system. Neuroscience 48:479-483.
65. Todaka H, Taniguchi J, Satoh JI, Mizuno A, Suzuki M (2004) Warm temperature-sensitive transient receptor potential vanilloid 4 (TRPV4) plays an essential role in thermal hyperalgesia. J Biol Chem 279:35133-35138.
66. Voets T, Prenen J, Vriens J, Watanabe H, Janssens A, Wissenbach U, Bodding M, Droogmans G, Nilius B (2002) Molecular determinants of permeation through the cation channel TRPV4. J Biol Chem 277:33704-33710.
67. Vyklicky L, Knotkova-Urbancova H, Vitaskova Z, Vlachova V, Kress M, Reeh PW (1998) Inflammatory mediators at acidic pH activate capsaicin receptors in cultured sensory neurons from newborn rats. J Neurophysiol 79:670-676.
68. Xiao RP, Ji X, Lakatta EG (1995) Functional coupling of the β2-adrenoceptor to a pertussis toxin-sensitive G protein in cardiac myocytes. Mol Pharmacol 47:322-329.
69. 2+ entry in HEK 293 cells transiently expressing human TRPV4. Br J Pharmacol 140:413-421.
70. Xu GY, Huang LY, Zhao ZQ (2000) Activation of silent mechanoreceptive cat C and Aδ sensory neurons and their substance P expression following peripheral inflammation. J Physiol (Lond) 528:339-348.
71. Zhang XY, Bai ZT, Chai ZF, Zhang JW, Liu Y, Ji YH (2003) Suppressive effects of BmKIT2 on nociceptive behavior and c-Fos expression in spinal cord induced by formalin. J Neurosci Res 74:167-173.
72. Zheng JH, Chen J (2001) Differential roles of spinal neurokinin 1/2 receptors in development of persistent spontaneous nociception and hyperalgesia induced by subcutaneous bee venom injection in the conscious rat. Neuropeptides 35:32-44.