Spinal phosphinositide 3-kinase-Akt-mammalian target of rapamycin signaling cascades in inflammation-induced hyperalgesia

Journal of Neuroscience

Volumn 31, Issue 6, 2011, Pages 2113-2124

  Xu, Qinghao ^a   Fitzsimmons, Bethany ^a   Steinauer, Joanne ^a   O'Neill, Audrey ^a   Newton, Alexandra C ^a   Hua, Xiao Ying ^a   Yaksh, Tony L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FORMALDEHYDE; MAMMALIAN TARGET OF RAPAMYCIN; NEUROKININ 1 RECEPTOR; PHOSPHINOSITIDE 3 KINASE; PROTEIN KINASE; PROTEIN KINASE B; RAPAMYCIN; SUBSTANCE P; UNCLASSIFIED DRUG; WORTMANNIN;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GLIA CELL; HYPERALGESIA; IMMUNOCYTOCHEMISTRY; INFLAMMATION; MALE; NERVE CELL; NONHUMAN; ORGANUM VASCULOSUM OF THE LAMINA TERMINALIS; PAIN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN; WESTERN BLOTTING;

ANDROSTADIENES; ANIMALS; CARRAGEENAN; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENZYME INHIBITORS; FORMALDEHYDE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HYPERALGESIA; INFLAMMATION; MALE; NERVE TISSUE PROTEINS; PAIN MEASUREMENT; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; SIGNAL TRANSDUCTION; SIROLIMUS; SPINAL CORD; STATISTICS, NONPARAMETRIC; SUBSTANCE P; TIME FACTORS; TOR SERINE-THREONINE KINASES;

EID: 79951538149     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2139-10.2011     Document Type: Article

References (56)

1. Al-Khater KM, Kerr R, Todd AJ (2008) A quantitative study of spinothalamic neurons in laminae I, III, and IV in lumbar and cervical segments of the rat spinal cord. J Comp Neurol 511:1-18.
2. Asante CO, Wallace VC, Dickenson AH (2009) Formalin-induced behavioural hypersensitivity and neuronal hyperexcitability are mediated by rapid protein synthesis at the spinal level. Mol Pain 5:27.
3. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P (2007) The selectivity of protein kinase inhibitors: a further update. Biochem J 408:297-315.
4. Bird GC, Han JS, Fu Y, Adwanikar H, Willis WD, Neugebauer V (2006) Pain-related synaptic plasticity in spinal dorsal horn neurons: role of CGRP. Mol Pain 2:31.
5. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63. (Pubitemid 24238751)
6. Choi JI, Svensson CI, Koehrn FJ, Bhuskute A, Sorkin LS (2010) Peripheral inflammation induces tumor necrosis factor dependent AMPA receptor trafficking and Akt phosphorylation in spinal cord in addition to pain behavior. Pain 149:243-253.
7. Codeluppi S, Svensson CI, Hefferan MP, Valencia F, Silldorff MD, Oshiro M, Marsala M, Pasquale EB (2009) The Rheb-mTOR pathway is upregulated in reactive astrocytes of the injured spinal cord. J Neurosci 29:1093-1104.
8. Dirig DM, Salami A, Rathbun ML, Ozaki GT, Yaksh TL (1997) Characterization of variables defining hindpaw withdrawal latency evoked by radiant thermal stimuli. J Neurosci Methods 76:183-191. (Pubitemid 27428253)
9. Dümmler BA, Hauge C, Silber J, Yntema HG, Kruse LS, Kofoed B, Hemmings BA, Alessi DR, Frödin M (2005) Functional characterization of human RSK4, a new 90-kDa ribosomal S6 kinase, reveals constitutive activation in most cell types. J Biol Chem 280:13304-13314.
10. Eberwine J, Belt B, Kacharmina JE, Miyashiro K (2002) Analysis of subcellularly localized mRNAs using in situ hybridization, mRNA amplification, and expression profiling. Neurochem Res 27:1065-1077. (Pubitemid 35316103)
11. Frödin M, Jensen CJ, Merienne K, Gammeltoft S (2000) A phosphoserine-regulated docking site in the protein kinase RSK2 that recruits and activates PDK1. EMBO J 19:2924-2934. (Pubitemid 30386764)
12. Géranton SM, Jiménez-Díaz L, Torsney C, Tochiki KK, Stuart SA, Leith JL, Lumb BM, Hunt SP (2009) A rapamycin-sensitive signaling pathway is essential for the full expression of persistent pain states. J Neurosci 29:15017-15027.
13. Haley JE, Sullivan AF, Dickenson AH (1990) Evidence for spinal N-methyl-D-aspartate receptor involvement in prolonged chemical nociception in the rat. Brain Res 518:218-226.
14. Hoeffer CA, Klann E (2010) mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci 33:67-75.
15. Hou L, Klann E (2004) Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J Neurosci 24:6352-6361. (Pubitemid 38944226)
16. Huang J, Manning BD (2009) A complex interplay between Akt, TSC2 and the two mTOR complexes. Biochem Soc Trans 37:217-222.
17. Huber KM, Kayser MS, Bear MF (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288:1254-1257.
18. Jaworski J, Sheng M (2006) The growing role of mTOR in neuronal development and plasticity. Mol Neurobiol 34:205-219.
19. Jiménez-Díaz L, Géranton SM, Passmore GM, Leith JL, Fisher AS, Berliocchi L, Sivasubramaniam AK, Sheasby A, Lumb BM, Hunt SP (2008) Local translation in primary afferent fibers regulates nociception. PLoS One 3:e1961.
20. Khasabov SG, Rogers SD, Ghilardi JR, Peters CM, Mantyh PW, Simone DA (2002) Spinal neurons that possess the substance P receptor are required for the development of central sensitization. J Neurosci 22:9086-9098. (Pubitemid 35379079)
21. Kondo I, Marvizon JC, Song B, Salgado F, Codeluppi S, Hua XY, Yaksh TL (2005) Inhibition by spinal mu-and delta-opioid agonists of afferent-evoked substance P release. J Neurosci 25:3651-3660.
22. Latremoliere A, Woolf CJ (2009) Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 10:895-926.
23. Ma W, Chabot JG, Quirion R (2006) A role for adrenomedullin as a pain-related peptide in the rat. Proc Natl Acad Sci U S A 103:16027-16032. (Pubitemid 44657586)
24. Ma XM, Blenis J (2009) Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10:307-318.
25. Malkmus SA, Yaksh TL (2004) Intrathecal catheterization and drug delivery in the rat. Methods Mol Med 99:109-121..
26. Malmberg AB, Yaksh TL (1992) Hyperalgesia mediated by spinal glutamate or substance P receptor blocked by spinal cyclooxygenase inhibition. Science 257:1276-1279.
27. Mantyh PW, Allen CJ, Ghilardi JR, Rogers SD, Mantyh CR, Liu H, Basbaum AI, Vigna SR, Maggio JE (1995a) Rapid endocytosis of a G protein-coupled receptor: substance P evoked internalization of its receptor in the rat striatum in vivo. Proc Natl Acad Sci U S A 92:2622-2626.
28. Mantyh PW, DeMaster E, Malhotra A, Ghilardi JR, Rogers SD, Mantyh CR, Liu H, Basbaum AI, Vigna SR, Maggio JE (1995b) Receptor endocytosis and dendrite reshaping in spinal neurons after somatosensory stimulation. Science 268:1629-1632.
29. Neugebauer V, Schaible HG (1990) Evidence for a central component in the sensitization of spinal neurons with joint input during development of acute arthritis in cat's knee. J Neurophysiol 64:299-311. (Pubitemid 20206375)
30. Nichols ML, Allen BJ, Rogers SD, Ghilardi JR, Honore P, Luger NM, Finke MP, Li J, Lappi DA, Simone DA, Mantyh PW (1999) Transmission of chronic nociception by spinal neurons expressing the substance P receptor. Science 286:1558-1561.
31. Norsted Gregory E, Codeluppi S, Gregory JA, Steinauer J, Svensson CI (2010) Mammalian target of rapamycin in spinal cord neurons mediates hypersensitivity induced by peripheral inflammation. Neuroscience 169:1392-1402.
32. Pearce LR, Komander D, Alessi DR (2010) The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 11:9-22.
33. Pende M, Um SH, Mieulet V, Sticker M, Goss VL, Mestan J, Mueller M, Fumagalli S, Kozma SC, Thomas G (2004) S6K1-/-/S6K2-/- mice exhibit perinatal lethality and rapamycin-sensitive 5′-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol Cell Biol 24:3112-3124. (Pubitemid 38452057)
34. Pezet S, Spyropoulos A, Williams RJ, McMahon SB (2005) Activity-dependent phosphorylation of Akt/PKB in adult DRG neurons. Eur J Neurosci 21:1785-1797. (Pubitemid 40685859)
35. Pezet S, Marchand F, D'Mello R, Grist J, Clark AK, Malcangio M, Dickenson AH, Williams RJ, McMahon SB (2008) Phosphatidylinositol 3-kinase is a key mediator of central sensitization in painful inflammatory conditions. J Neurosci 28:4261-4270.
36. Piercey MF, Schroeder LA, Folkers K, Xu JC, Horig J (1981) Sensory and motor functions of spinal cord substance P. Science 214:1361-1363. (Pubitemid 12135124)
37. Price TJ, Rashid MH, Millecamps M, Sanoja R, Entrena JM, Cervero F (2007) Decreased nociceptive sensitization in mice lacking the fragile X mental retardation protein: role of mGluR1/5 and mTOR. J Neurosci 27:13958-13967. (Pubitemid 351377872)
38. Puig S, Sorkin LS (1996) Formalin-evoked activity in identified primary afferent fibers: systemic lidocaine suppresses phase-2 activity. Pain 64:345-355. (Pubitemid 26132446)
39. Richter JD, Sonenberg N (2005) Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433:477-480. (Pubitemid 40204297)
40. Shi TJ, Huang P, Mulder J, Ceccatelli S, Hokfelt T (2009) Expression of p-Akt in sensory neurons and spinal cord after peripheral nerve injury. Neurosignals 17:203-212.
41. Skup M (2008) Dendrites as separate compartment: local protein synthesis. Acta Neurobiol Exp (Wars) 68:305-321.
42. Sun RQ, Tu YJ, Yan JY, Willis WD (2006) Activation of protein kinase B/Akt signaling pathway contributes to mechanical hypersensitivity induced by capsaicin. Pain 120:86-96.
43. Sun R, Yan J, Willis WD (2007) Activation of protein kinase B/Akt in the periphery contributes to pain behavior induced by capsaicin in rats. Neuroscience 144:286-294. (Pubitemid 44839032)
44. Suzuki R, Rahman W, Rygh LJ, Webber M, Hunt SP, Dickenson AH (2005) Spinal-supraspinal serotonergic circuits regulating neuropathic pain and its treatment with gabapentin. Pain 117:292-303. (Pubitemid 41383525)
45. Suzuki R, Morcuende S, Webber M, Hunt SP, Dickenson AH (2002) Superficial NK1-expressing neurons control spinal excitability through activation of descending pathways. Nat Neurosci 5:1319-1326. (Pubitemid 35417767)
46. Swett JE, Woolf CJ (1985) The somatotopic organization of primary afferent terminals in the superficial laminae of the dorsal horn of the rat spinal cord. J Comp Neurol 231:66-77. (Pubitemid 15199486)
47. Todd AJ, Puskar Z, Spike RC, Hughes C, Watt C, Forrest L (2002) Projection neurons in lamina I of rat spinal cord with the neurokinin 1 receptor are selectively innervated by substance p-containing afferents and respond to noxious stimulation. J Neurosci 22:4103-4113. (Pubitemid 37465718)
48. Vierck CJ Jr, Kline RH, Wiley RG (2003) Intrathecal substance p-saporin attenuates operant escape from nociceptive thermal stimuli. Neuroscience 119:223-232.
49. Waung MW, Pfeiffer BE, Nosyreva ED, Ronesi JA, Huber KM (2008) (Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate. Neuron 59:84-97.
50. Xu JT, Tu HY, Xin WJ, Liu XG, Zhang GH, Zhai CH (2007 Activation of phosphatidylinositol 3-kinase and protein kinase B/Akt in dorsal root ganglia and spinal cord contributes to the neuropathic pain induced by spinal nerve ligation in rats. Exp Neurol 206:269-279.
51. Xu JT, Zhao X, Yaster M, Tao YX (2010) Expression and distribution of mTOR, p70S6K, 4E-BP1, and their phosphorylated counterparts in rat dorsal root ganglion and spinal cord dorsal horn. Brain Res 1336:46-57.
52. Yaksh TL, Rudy TA (1976) Chronic catheterization of the spinal subarachnoid space. Physiol Behav 17:1031-1036. (Pubitemid 8063691)
53. Yaksh TL, Ozaki G, McCumber D, Rathbun M, Svensson C, Malkmus S, Yaksh MC (2001) An automated flinch detecting system for use in the formalin nociceptive bioassay. J Appl Physiol 90:2386-2402. (Pubitemid 32467435)
54. Yang Q, Guan KL (2007) ExpandingmTORsignaling. Cell Res 17:666-681.
55. Yashpal K, Henry JL (1983) Endorphins mediate overshoot of substance P-induced facilitation of a spinal nociceptive reflex. Can J Physiol Pharmacol 61:303-307. (Pubitemid 13102969)
56. Zhuang ZY, Xu H, Clapham DE, Ji RR (2004) Phosphatidylinositol 3-kinase activates ERK in primary sensory neurons and mediates inflammatory heat hyperalgesia through TRPV1 sensitization. J Neurosci 24:8300-8309. (Pubitemid 39280809)