Phosphatidylinositol 3-kinase activates ERK in primary sensory neurons and mediates inflammatory heat hyperalgesia through TRPV1 sensitization

Journal of Neuroscience

Volumn 24, Issue 38, 2004, Pages 8300-8309

  Zhuang, Zhi Ye ^a   Xu, Haoxing ^b   Clapham, David E ^b   Ji, Ru Rong ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Capsaicin; Dorsal root ganglion; ERK; Inflammatory pain; NGF; PI3K

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CAPSAICIN; MITOGEN ACTIVATED PROTEIN KINASE; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B; TRANSIENT RECEPTOR POTENTIAL VANILLOID RECEPTOR 1; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; WORTMANNIN;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; HEAT SENSITIVITY; HYPERALGESIA; INFLAMMATION; MALE; NERVE CELL PLASTICITY; NERVE ENDING; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANDROSTADIENES; ANIMALS; CAPSAICIN; CELLS, CULTURED; CHROMONES; ENZYME ACTIVATION; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GANGLIA, SPINAL; HEAT; HYPERALGESIA; INFLAMMATION; ION CHANNELS; MALE; MORPHOLINES; NERVE GROWTH FACTOR; NEURONS, AFFERENT; PAIN MEASUREMENT; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; SIGNAL TRANSDUCTION; SKIN; TRPV CATION CHANNELS;

EID: 4644250844     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2893-04.2004     Document Type: Article

References (82)

1. Aley KO, Levine JD (1999) Role of protein kinase A in the maintenance of inflammatory pain. J Neurosci 19:2181-2186.
2. 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.
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. Atwal JK, Massie B, Miller FD, Kaplan DR (2000) The TrkB-Shc site signals neuronal survival and local axon growth via MEK and PI3-kinase. Neuron 27:265-277.
5. 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.
6. Bhave G, Gereau RW (2003) Growing pains: the cytoskeleton as a critical regulator of pain plasticity. Neuron 39:577-579.
7. 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.
8. Bonnington JK, McNaughton PA (2003) Signalling pathways involved in the sensitisation of mouse nociceptive neurones by nerve growth factor. J Physiol (Lond) 551:433-446.
9. Bron R, Klesse LJ, Shah K, Parada LF, Winter J (2003) Activation of Ras is necessary and sufficient for upregulation of vanilloid receptor type 1 in sensory neurons by neurotrophic factors. Mol Cell Neurosci 22:118-132.
10. 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.
11. 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. Science 288:306-313.
12. Cesare P, Dekker LV, Sardini A, Parker PJ, McNaughton PA (1999) Sepcific involvement of PKC-ε in sensitization of the neuronal response to painful heat. Neuron 23:617-624.
13. Chan TO, Rittenhouse SE, Tsichlis PN (1999) AKT/PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide- dependent phosphorylation. Annu Rev Biochem 68:965-1014.
14. Chandler LJ, Sutton G, Dorairaj NR, Norwood D (2001) N-methyl-D-aspartate receptor-mediated bidirectional control of extracellular signal-regulated kinase activity in cortical neuronal cultures. J Biol Chem 276:2627-2636.
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. Clapham DE (2003) TRP channels as cellular sensors. Nature 426:517-524.
17. 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.
18. 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.
19. Datta SR, Brunet A, Greenberg ME (1999) Cellular survival: a play in there akts. Genes Dev 13:2905-2927.
20. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Ranee K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA (2000) Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405:183-187.
21. Dina OA, McCarter GC, de Coupade C, Levine JD (2003) Role of the sensory neuron cytoskeleton in second messenger signaling for inflammatory pain. Neuron 39:613-624.
22. Duckworth BC, Cantley LC (1997) Conditional inhibition of the mitogen-activated protein kinase cascade by wortmannin. Dependence on signal strength. J Biol Chem 272:27665-27670.
23. English JD, Sweatt JD (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272:19103-19106.
24. Farquhar-Smith WP, Rice AS (2003) A novel neuroimmune mechanism in cannabinoid-mediated attenuation of nerve growth factor-induced hyperalgesia. Anesthesiology 99:1391-1401.
25. 2+-dependent routes to Ras: mechanisms for neuronal survival, differentiation, and plasticity? Neuron 16:233-236.
26. Fitzgerald M, Gibson S (1984) The postnatal physiological and neurochemical development of peripheral sensory C fibres. Neuroscience 13:933-944.
27. Franke TF, Kaplan DR, Cantley LC (1997) PI3K: downstream AKTion blocks apoptosis. Cell 88:435-437.
28. Galoyan SM, Petruska JC, Mendell LM (2003) Mechanisms of sensitization of the response of single dorsal root ganglion cells from adult rat to noxious heat. Eur J Neurosci 18:535-541.
29. Gold MS, Levine JD, Correa AM (1998) Modulation of TTX-R INa by PKC and PKA and their role in PGE2-induced sensitization of rat sensory neurons in vitro. J Neurosci 18:10345-10355.
30. Graness A, Adomeit A, Heinze R, Wetzker R, Liebmann C (1998) A novel mitogenic signaling pathway of bradykinin in the human colon carcinoma cell line SW-480 involves sequential activation of a Gq/11 protein, phosphatidylinositol 3-kinase beta, and protein kinase Cepsilon. J Biol Chem 273:32016-32022.
31. Hargreaves K, Dubner R, Brown F, Flores C, Joris J (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88.
32. Huang YY, Martin KC, Kandel ER (2000) Both protein kinase A and mitogen-activated protein kinase are required in the amygdala for the macromolecular synthesis-dependent late phase of long-term potentiation. J Neurosci 20:6317-6325.
33. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21:869-883.
34. Izzo E, Martin-Pardon R, Koob GF, Weiss F, Sanna PP (2002) Neural plasticity and addiction: PI3-kinase and cocaine behavioral sensitization. Nat Neurosci 5:1263-1264.
35. Ji RR (2003) Activation of MAP kinase in primary sensory neurons. Proceedings of the 10th World Congress on Pain 24:81-87.
36. Ji RR, Zhang Q, Pettersson RF, Hokfelt T (1996) aFGF, bFGF and NGF differentially regulate neuropeptide expression in dorsal root ganglia after axotomy and induce autotomy. Regul Pept 66:179-189.
37. Ji RR, Befort K, Brenner GJ, Woolf CJ (2002a) ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 up-regulation and contributes to persistent inflammatory pain hypersensitivity. J Neurosci 22:478-485.
38. Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ (2002b) p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36:57-68.
39. Joyal JL, Burks DJ, Pons S, Matter WF, Vlahos CJ, White MF, Sacks DB (1997) Calmodulin activates phosphatidylinositol 3-kinase. J Biol Chem 272:28183-28186.
40. Julius D, Basbaum AI (2001) Molecular mechanisms of nociception. Nature 413:203-210.
41. Kaplan DR, Cooper E (2001) PI-3 kinase and IP3: partners in NT-3-induced synaptic transmission. Nat Neurosci 4:5-7.
42. Kelly A, Lynch MA (2000) Long-term potentiation in dentate gyrus of the rat is inhibited by the phosphoinositide 3-kinase inhibitor, wortmannin. Neuropharmacology 39:643-651.
43. 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.
44. 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 epsilon mutant mice. Neuron 24:253-260.
45. Kuruvilla R, Ye H, Ginty DD (2000) Spatially and functionally distinct roles of the PI3-K effector pathway during NGF signaling in sympathetic neurons. Neuron 27:499-512.
46. Lin CH, Yeh SH, Lin CH, Lu KT, Leu TH, Chang WC, Gean PW (2001) A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala. Neuron 31:841-851.
47. Markus A, Zhong J, Snider WD (2002) Raf and akt mediate distinct aspects of sensory axon growth. Neuron 35:65-76.
48. McCleskey EW, Gold MS (1999) Ion channels of nociception. Annu Rev Physiol 61:835-856.
49. Moriyama T, Iida T, Kobayashi K, Higashi T, Fukuoka T, Tsumura H, Leon C, Suzuki N, Inoue K, Cachet C, Noguchi K, Tominaga M (2003) Possible involvement of P2Y2 metabotropic receptors in ATP-induced transient receptor potential vanilloid receptor 1-mediated thermal hypersensitivity. J Neurosci 23:6058-6062.
50. 2+] at the mouth of a calcium channel. J Neurosci 17:6961-6973.
51. Opazo P, Watabe AM, Grant SG, O'Dell TJ (2003) Phosphatidylinositol 3-kinase regulates the induction of long-term potentiation through extracellular signal-related kinase-independent mechanisms. J Neurosci 23:3679-3688.
52. Parekh D, Ziegler W, Yonezawa K, Kara K, Parker PJ (1999) Mammalian TOR controls one of two kinase pathways acting upon nPKCdelta and nPKCepsilon. J Biol Chem 274:34758-34764.
53. Patapoutian A, Reichardt LF (2001) Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol 11:272-280.
54. 2+-permeable AMPA receptors induce phosphorylation of cAMP response element-binding protein through a phosphatidylinositol 3-kinase-dependent stimulation of the mitogen-activated protein kinase signaling cascade in neurons. J Neurosci 19:5861-5874.
55. Perkinton MS, Ip JK, Wood GL, Crossthwaite AJ, Williams RJ (2002) Phosphatidylinositol 3-kinase is a central mediator of NMDA receptor signalling to MAP kinase (Erk1/2), Akt/PKB and CREB in striatal neurones. J Neurochem 80:239-254.
56. Porreca F, Lai J, Bian D, Wegert S, Ossipov MH, Eglen RM, Kassotakis L, Novakovic S, Rabert DK, Sangameswaran L, Hunter JC (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.
57. Premkumar LS, Ahern GP (2000) Induction of vanilloid receptor channel activity by protein kinase C. Nature 408:985-990.
58. Prescott ED, Julius D (2003) A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300:1284-1288.
59. Rameh LE, Cantley LC (1999) The role of phosphoinositide 3-kinase lipid products in cell function. J Biol Chem 274:8347-8350.
60. Rommel C, Clarke BA, Zimmermann S, Nunez L, Rossman R, Reid K, Moelling K, Yancopoulos GD, Glass DJ (1999) Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science 286:1738-1741.
61. Rueff A, Dawson AJ, Mendell LM (1996) Characteristics of nerve growth factor induced hyperalgesia in adult rats: dependence on enhanced bradykinin-1 receptor activity but not neurokinin-1 receptor activation. Pain 66:359-372.
62. Runnels LW, Yue L, Clapham DE (2002) The TRPM7 channel is inactivated by PIP(2) hydrolysis. Nat Cell Biol 5:329-336.
63. Sanna PP, Cammalleri M, Berton F, Simpson C, Lutjens R, Bloom FE, Francesconi W (2002) Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. J Neurosci 22:3359-3365.
64. Shi SH, Jan LY, Jan YN (2003) Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI3-kinase activity. Cell 112:63-75.
65. Shu X, Mendell LM (1999a) Nerve growth factor acutely sensitizes the response of adult rat sensory neurons to capsaicin. Neurosci Lett 274:159-162.
66. Shu XQ, Mendell LM (1999b) Neurotrophins and hyperalgesia. Proc Natl Acad Sci USA 96:7693-7696.
67. Shu XQ, Mendell LM (2001) Acute sensitization by NGF of the response of small-diameter sensory neurons to capsaicin. J Neurophysiol 86:2931-2938.
68. Simone DA, Nolano M, Johnson T, Wendelschafer-Crabb G, Kennedy WR (1998) Intradermal injection of capsaicin in humans produces degeneration and subsequent reinnervation of epidermal nerve fibers: correlation with sensory function. J Neurosci 18:8947-8959.
69. Snider WD, McMahon SB (1998) Tackling pain at the source: new ideas about nociceptors. Neuron 20:629-632.
70. Tan M, Groszer M, Tan AM, Pandya A, Liu X, Xie CW (2003) Phosphoinositide 3-kinase cascade facilitates μ-opioid desensitization in sensory neurons by altering G-protein-effector interactions. J Neurosci 23:10292-12301.
71. Toker A, Cantley LC (1997) Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 387:673-676.
72. Vlahos CJ, Matter WF, Hui KY, Brown RF, Vlahos CJ, Matter WF, Hui KY, Brown RF (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 269:5241-5248.
73. Watabe AM, Zaki PA, O'Dell TJ (2000) Coactivation of beta-adrenergic and cholinergic receptors enhances the induction of long-term potentiation and synergistically activates mitogen-activated protein kinase in the hippocampal CA1 region. J Neurosci 20:5924-5931.
74. Wennstrom S, Downward J (1999) Role of phosphoinositide 3-kinse in activation of Ras and mitogen-activated protein kinase by epidermal growth factor. Mol Cell Biol 19:4279-4288.
75. Williamson R, Scales T, Clark BR, Gibb G, Reynolds CH, Kellie S, Bird IN, Varndell IM, Sheppard PW, Everall I, Anderton BH (2002) Rapid tyrosine phosphorylation of neuronal proteins including tau and focal adhesion kinase in response to amyloid-β peptide exposure: involvement of Src family protein kinases. J Neurosci 22:10-20.
76. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, Kandel ER (1999) ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron 24:715-726.
77. Woodbury CJ, Zwick M, Wang S, Lawson JJ, Caterina MJ, Koltzenburg M, Albers KM, Koerber HR, Davis BM (2004) Nociceptors lacking TRPV1 and TRPV2 have normal heat responses. J Neurosci 24:6410-6415.
78. Woolf CJ, Salter MW (2000) Neuronal plasticity: increasing the gain in pain. Science 288:1765-1769.
79. Yang F, He X, Feng L, Mizuno K, Liu XW, Russell J, Xiong WC, Lu B (2001) PI-3 kinase and IP3 are both necessary and sufficient to mediate NT3-induced synaptic potentiation. Nat Neurosci 4:19-28.
80. York RD, Molliver DC, Grewal SS, Stenberg PE, McCleskey EW, Stork PJ (2000) Role of phosphoinositide 3-kinase and endocytosis in nerve growth factor-induced extracellular signal-regulated kinase activation via Ras and Rap1. Mol Cell Biol 20:8069-8083.
81. Zhu W, Galoyan SM, Petruska JC, Oxford GS, Mendell LM (2004) A developmental switch in acute sensitization of small dorsal root ganglion (DRG) neurons to capsaicin or noxious heating by NGF. J Neurophysiol Jun 16 [Epub ahead of print].
82. Zimmermann S, Moelling K (1999) Phosphorylation and regulation of Raf by Akt (protein kinase B). Science 286:1741-1744.