Targeting adenosine monophosphate-activated protein kinase (AMPK) in preclinical models reveals a potential mechanism for the treatment of neuropathic pain

Molecular Pain

Volumn 7, Issue , 2011, Pages

  Melemedjian, Ohannes K ^a   Asiedu, Marina N ^a   Tillu, Dipti V ^a   Sanoja, Raul ^a   Yan, Jin ^a   Lark, Arianna ^a   Khoutorsky, Arkady ^b,c   Johnson, Jessica ^a   Peebles, Katherine A ^a   Lepow, Talya ^a   Sonenberg, Nahum ^b,c   Dussor, Gregory ^a   Price, Theodore J ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

6,7 DIHYDRO 4 HYDROXY 3 (2' HYDROXY 1,1' BIPHENYL 4 YL) 6 OXOTHIENO[2,3 B]PYRIDINE 5 CARBONITRILE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INITIATION FACTOR 2ALPHA; INITIATION FACTOR 4E BINDING PROTEIN; INITIATION FACTOR 4F; MAMMALIAN TARGET OF RAPAMYCIN; METFORMIN; SODIUM CHANNEL; AMP ACTIVATED PROTEIN KINASE KINASE; AMP-ACTIVATED PROTEIN KINASE KINASE; ENZYME ACTIVATOR; PROTEIN KINASE;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; DISEASE MODEL; DRUG TARGETING; ENZYME ACTIVATION; INHIBITION KINETICS; MALE; MOUSE; NERVE CELL EXCITABILITY; NERVE INJURY; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; ACTION POTENTIAL; ANIMAL; BIOSYNTHESIS; DRUG EFFECT; ENZYMOLOGY; HYPERALGESIA; INJURY; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; MOLECULARLY TARGETED THERAPY; NEURALGIA; PATHOLOGY; PATHOPHYSIOLOGY; SCIATIC NERVE; SENSORY RECEPTOR; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ACTION POTENTIALS; ANIMALS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ENZYME ACTIVATORS; EUKARYOTIC INITIATION FACTOR-4F; HYPERALGESIA; MALE; MICE; MICE, INBRED ICR; MOLECULAR TARGETED THERAPY; NEURALGIA; PROTEIN BIOSYNTHESIS; PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION;

EID: 80053174960     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-7-70     Document Type: Article

References (60)

1. Baron R. Mechanisms of disease: neuropathic pain--a clinical perspective. Nat Clin Pract Neurol 2006, 2(2):95-106. 10.1038/ncpneuro0113, 16932531.
2. Campbell JN, Meyer RA. Mechanisms of neuropathic pain. Neuron 2006, 52(1):77-92. 10.1016/j.neuron.2006.09.021, 1810425, 17015228.
3. Costa-Mattioli M, Sossin WS, Klann E, Sonenberg N. Translational control of long-lasting synaptic plasticity and memory. Neuron 2009, 61(1):10-26. 10.1016/j.neuron.2008.10.055, 19146809.
4. Geranton SM, Jimenez-Diaz L, Torsney C, Tochiki KK, Stuart SA, Leith JL, Lumb BM, Hunt SP. A rapamycin-sensitive signaling pathway is essential for the full expression of persistent pain states. J Neurosci 2009, 29(47):15017-15027. 10.1523/JNEUROSCI.3451-09.2009, 2830115, 19940197.
5. Huang HL, Cendan CM, Roza C, Okuse K, Cramer R, Timms JF, Wood JN. Proteomic profiling of neuromas reveals alterations in protein composition and local protein synthesis in hyper-excitable nerves. Mol Pain 2008, 4:33. 10.1186/1744-8069-4-33, 2525634, 18700027.
6. Jimenez-Diaz L, Geranton SM, Passmore GM, Leith JL, Fisher AS, Berliocchi L, Sivasubramaniam AK, Sheasby A, Lumb BM, Hunt SP. Local translation in primary afferent fibers regulates nociception. PLoS One 2008, 3(4):e1961. 10.1371/journal.pone.0001961, 2276314, 18398477.
7. Melemedjian OK, Asiedu MN, Tillu DV, Peebles KA, Yan J, Ertz N, Dussor GO, Price TJ. IL-6- and NGF-induced rapid control of protein synthesis and nociceptive plasticity via convergent signaling to the eIF4F complex. J Neurosci 2010, 30(45):15113-15123. 10.1523/JNEUROSCI.3947-10.2010, 3056511, 21068317.
8. Price TJ, Geranton SM. Translating nociceptor sensitivity: the role of axonal protein synthesis in nociceptor physiology. Eur J Neurosci 2009, 29(12):2253-2263. 10.1111/j.1460-9568.2009.06786.x, 2914561, 19490023.
9. Price TJ, Rashid MH, Millecamps M, Sanoja R, Entrena JM, Cervero F. Decreased nociceptive sensitization in mice lacking the fragile × mental retardation protein: role of mGluR1/5 and mTOR. J Neurosci 2007, 27(51):13958-13967. 10.1523/JNEUROSCI.4383-07.2007, 2206543, 18094233.
10. Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009, 136(4):731-745. 10.1016/j.cell.2009.01.042, 19239892.
11. Zoncu R, Efeyan A, Sabatini DM. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 2011, 12(1):21-35. 10.1038/nrm3025, 21157483.
12. Costa-Mattioli M, Gobert D, Harding H, Herdy B, Azzi M, Bruno M, Bidinosti M, Ben Mamou C, Marcinkiewicz E, Yoshida M, et al. Translational control of hippocampal synaptic plasticity and memory by the eIF2alpha kinase GCN2. Nature 2005, 436(7054):1166-1173. 10.1038/nature03897, 1464117, 16121183.
13. Banerjee S, Neveu P, Kosik KS. A coordinated local translational control point at the synapse involving relief from silencing and MOV10 degradation. Neuron 2009, 64(6):871-884. 10.1016/j.neuron.2009.11.023, 20064393.
14. Nave BT, Ouwens M, Withers DJ, Alessi DR, Shepherd PR. Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J 1999, 344(Pt 2):427-431. 1220660, 10567225.
15. Dieterich DC, Lee JJ, Link AJ, Graumann J, Tirrell DA, Schuman EM. Labeling, detection and identification of newly synthesized proteomes with bioorthogonal non-canonical amino-acid tagging. Nat Protoc 2007, 2(3):532-540. 10.1038/nprot.2007.52, 17406607.
16. Dieterich DC, Link AJ, Graumann J, Tirrell DA, Schuman EM. Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT). Proc Natl Acad Sci USA 2006, 103(25):9482-9487. 10.1073/pnas.0601637103, 1480433, 16769897.
17. Tzatsos A, Tsichlis PN. Energy depletion inhibits phosphatidylinositol 3-kinase/Akt signaling and induces apoptosis via AMP-activated protein kinase-dependent phosphorylation of IRS-1 at Ser-794. J Biol Chem 2007, 282(25):18069-18082. 10.1074/jbc.M610101200, 17459875.
18. Ouyang J, Parakhia RA, Ochs RS. Metformin activates AMP kinase through inhibition of AMP deaminase. J Biol Chem 2011, 286(1):1-11. 10.1074/jbc.M110.121806, 21059655.
19. Shaw RJ, Lamia KA, Vasquez D, Koo SH, Bardeesy N, Depinho RA, Montminy M, Cantley LC. The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science 2005, 310(5754):1642-1646. 10.1126/science.1120781, 3074427, 16308421.
20. Combs TP, Wagner JA, Berger J, Doebber T, Wang WJ, Zhang BB, Tanen M, Berg AH, O'Rahilly S, Savage DB, et al. Induction of adipocyte complement-related protein of 30 kilodaltons by PPARgamma agonists: a potential mechanism of insulin sensitization. Endocrinology 2002, 143(3):998-1007. 10.1210/en.143.3.998, 11861525.
21. Cool B, Zinker B, Chiou W, Kifle L, Cao N, Perham M, Dickinson R, Adler A, Gagne G, Iyengar R, et al. Identification and characterization of a small molecule AMPK activator that treats key components of type 2 diabetes and the metabolic syndrome. Cell Metab 2006, 3(6):403-416. 10.1016/j.cmet.2006.05.005, 16753576.
22. Wild KD, Bian D, Zhu D, Davis J, Bannon AW, Zhang TJ, Louis JC. Antibodies to nerve growth factor reverse established tactile allodynia in rodent models of neuropathic pain without tolerance. J Pharmacol Exp Ther 2007, 322(1):282-287. 10.1124/jpet.106.116236, 17431136.
23. Anand P. Neurotrophic factors and their receptors in human sensory neuropathies. Prog Brain Res 2004, 146:477-492.
24. Kinkade CW, Castillo-Martin M, Puzio-Kuter A, Yan J, Foster TH, Gao H, Sun Y, Ouyang X, Gerald WL, Cordon-Cardo C, et al. Targeting AKT/mTOR and ERK MAPK signaling inhibits hormone-refractory prostate cancer in a preclinical mouse model. The Journal of Clinical Investigation 2008, 118(9):3051-3064. 2518074, 18725989.
25. Martin KC. Local protein synthesis during axon guidance and synaptic plasticity. Curr Opin Neurobiol 2004, 14(3):305-310. 10.1016/j.conb.2004.05.009, 15194110.
26. Willis D, Li KW, Zheng JQ, Chang JH, Smit A, Kelly T, Merianda TT, Sylvester J, van Minnen J, Twiss JL. Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J Neurosci 2005, 25(4):778-791. 10.1523/JNEUROSCI.4235-04.2005, 15673657.
27. Zheng JQ, Kelly TK, Chang B, Ryazantsev S, Rajasekaran AK, Martin KC, Twiss JL. A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J Neurosci 2001, 21(23):9291-9303.
28. Gumy LF, Yeo GS, Tung YC, Zivraj KH, Willis D, Coppola G, Lam BY, Twiss JL, Holt CE, Fawcett JW. Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization. RNA 2011, 17(1):85-98. 10.1261/rna.2386111, 21098654.
29. Wang W, van Niekerk E, Willis DE, Twiss JL. RNA transport and localized protein synthesis in neurological disorders and neural repair. Dev Neurobiol 2007, 67(9):1166-1182. 10.1002/dneu.20511, 17514714.
30. Willis DE, van Niekerk EA, Sasaki Y, Mesngon M, Merianda TT, Williams GG, Kendall M, Smith DS, Bassell GJ, Twiss JL. Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. J Cell Biol 2007, 178(6):965-980. 10.1083/jcb.200703209, 2064621, 17785519.
31. Tremblay F, Brule S, Hee Um S, Li Y, Masuda K, Roden M, Sun XJ, Krebs M, Polakiewicz RD, Thomas G, et al. Identification of IRS-1 Ser-1101 as a target of S6K1 in nutrient- and obesity-induced insulin resistance. Proc Natl Acad Sci USA 2007, 104(35):14056-14061. 10.1073/pnas.0706517104, 1950339, 17709744.
32. Ji RR, Gereau R, Malcangio M, Strichartz GR. MAP kinase and pain. Brain Res Rev 2009, 60(1):135-148. 10.1016/j.brainresrev.2008.12.011, 2666786, 19150373.
33. Dib-Hajj SD, Cummins TR, Black JA, Waxman SG. Sodium channels in normal and pathological pain. Annu Rev Neurosci 2010, 33:325-347. 10.1146/annurev-neuro-060909-153234, 20367448.
34. Black JA, Nikolajsen L, Kroner K, Jensen TS, Waxman SG. Multiple sodium channel isoforms and mitogen-activated protein kinases are present in painful human neuromas. Ann Neurol 2008, 64(6):644-653. 10.1002/ana.21527, 19107992.
35. Beneng K, Renton T, Yilmaz Z, Yiangou Y, Anand P. Sodium channel Na v 1.7 immunoreactivity in painful human dental pulp and burning mouth syndrome. BMC Neurosci 2010, 11:71. 10.1186/1471-2202-11-71, 2890014, 20529324.
36. Luo S, Perry GM, Levinson SR, Henry MA. Nav1.7 expression is increased in painful human dental pulp. Mol Pain 2008, 4:16. 10.1186/1744-8069-4-16, 2377237, 18426592.
37. Estacion M, Waxman SG, Dib-Hajj SD. Effects of ranolazine on wild-type and mutant hNav1.7 channels and on DRG neuron excitability. Mol Pain 2010, 6:35. 10.1186/1744-8069-6-35, 2898769, 20529343.
38. Schmalhofer WA, Calhoun J, Burrows R, Bailey T, Kohler MG, Weinglass AB, Kaczorowski GJ, Garcia ML, Koltzenburg M, Priest BT. ProTx-II, a selective inhibitor of NaV1.7 sodium channels, blocks action potential propagation in nociceptors. Mol Pharmacol 2008, 74(5):1476-1484. 10.1124/mol.108.047670, 18728100.
39. Nassar MA, Stirling LC, Forlani G, Baker MD, Matthews EA, Dickenson AH, Wood JN. Nociceptor-specific gene deletion reveals a major role for Nav1.7 (PN1) in acute and inflammatory pain. Proc Natl Acad Sci USA 2004, 101(34):12706-12711. 10.1073/pnas.0404915101, 515119, 15314237.
40. Hoyt SB, London C, Gorin D, Wyvratt MJ, Fisher MH, Abbadie C, Felix JP, Garcia ML, Li X, Lyons KA, et al. Discovery of a novel class of benzazepinone Na(v)1.7 blockers: potential treatments for neuropathic pain. Bioorg Med Chem Lett 2007, 17(16):4630-4634. 10.1016/j.bmcl.2007.05.076, 17588748.
41. Hoyt SB, London C, Ok H, Gonzalez E, Duffy JL, Abbadie C, Dean B, Felix JP, Garcia ML, Jochnowitz N, et al. Benzazepinone Nav1.7 blockers: potential treatments for neuropathic pain. Bioorg Med Chem Lett 2007, 17(22):6172-6177. 10.1016/j.bmcl.2007.09.032, 17889534.
42. London C, Hoyt SB, Parsons WH, Williams BS, Warren VA, Tschirret-Guth R, Smith MM, Priest BT, McGowan E, Martin WJ, et al. Imidazopyridines: a novel class of hNav1.7 channel blockers. Bioorg Med Chem Lett 2008, 18(5):1696-1701. 10.1016/j.bmcl.2008.01.047, 18243692.
43. Tyagarajan S, Chakravarty PK, Zhou B, Taylor B, Fisher MH, Wyvratt MJ, Lyons K, Klatt T, Li X, Kumar S, et al. Substituted biaryl pyrazoles as sodium channel blockers. Bioorg Med Chem Lett 2010, 20(18):5480-5483. 10.1016/j.bmcl.2010.07.080, 20709545.
44. Stamboulian S, Choi JS, Ahn HS, Chang YW, Tyrrell L, Black JA, Waxman SG, Dib-Hajj SD. ERK1/2 mitogen-activated protein kinase phosphorylates sodium channel Na(v)1.7 and alters its gating properties. J Neurosci 2010, 30(5):1637-1647. 10.1523/JNEUROSCI.4872-09.2010, 20130174.
45. Asante CO, Wallace VC, Dickenson AH. Formalin-induced behavioural hypersensitivity and neuronal hyperexcitability are mediated by rapid protein synthesis at the spinal level. Mol Pain 2009, 5:27. 10.1186/1744-8069-5-27, 2699332, 19500426.
46. Asante CO, Wallace VC, Dickenson AH. Mammalian target of rapamycin signaling in the spinal cord is required for neuronal plasticity and behavioral hypersensitivity associated with neuropathy in the rat. J Pain 2010, 11(12):1356-1367. 10.1016/j.jpain.2010.03.013, 3000494, 20452291.
47. Asiedu MN, Tillu DV, Melemedjian OK, Shy A, Sanoja R, Bodell B, Ghosh S, Porreca F, Price TJ. Spinal protein kinase M zeta underlies the maintenance mechanism of persistent nociceptive sensitization. J Neurosci 2011, 31(18):6646-6653. 10.1523/JNEUROSCI.6286-10.2011, 21543593.
48. Xu Q, Fitzsimmons B, Steinauer J, O'Neill A, Newton AC, Hua XY, Yaksh TL. Spinal phosphinositide 3-kinase-Akt-mammalian target of rapamycin signaling cascades in inflammation-induced hyperalgesia. J Neurosci 2011, 31(6):2113-2124. 10.1523/JNEUROSCI.2139-10.2011, 3097059, 21307248.
49. Norsted Gregory E, Codeluppi S, Gregory JA, Steinauer J, Svensson CI. Mammalian target of rapamycin in spinal cord neurons mediates hypersensitivity induced by peripheral inflammation. Neuroscience 2010, 169(3):1392-1402. 10.1016/j.neuroscience.2010.05.067, 2914192, 20538043.
50. Ropelle ER, Pauli JR, Fernandes MF, Rocco SA, Marin RM, Morari J, Souza KK, Dias MM, Gomes-Marcondes MC, Gontijo JA, et al. A central role for neuronal AMP-activated protein kinase (AMPK) and mammalian target of rapamycin (mTOR) in high-protein diet-induced weight loss. Diabetes 2008, 57(3):594-605. 10.2337/db07-0573, 18057094.
51. Potter WB, O'Riordan KJ, Barnett D, Osting SM, Wagoner M, Burger C, Roopra A. Metabolic regulation of neuronal plasticity by the energy sensor AMPK. PLoS One 2010, 5(2):e8996.. 2813866, 20126541.
52. Labuzek K, Suchy D, Gabryel B, Bielecka A, Liber S, Okopien B. Quantification of metformin by the HPLC method in brain regions, cerebrospinal fluid and plasma of rats treated with lipopolysaccharide. Pharmacol Rep 2010, 62(5):956-965.
53. Kelleher RJ, Govindarajan A, Tonegawa S. Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 2004, 44(1):59-73. 10.1016/j.neuron.2004.09.013, 15450160.
54. Corton JM, Gillespie JG, Hawley SA, Hardie DG. 5-aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells?. Eur J Biochem 1995, 229(2):558-565. 10.1111/j.1432-1033.1995.tb20498.x, 7744080.
55. Scott JW, van Denderen BJ, Jorgensen SB, Honeyman JE, Steinberg GR, Oakhill JS, Iseli TJ, Koay A, Gooley PR, Stapleton D, et al. Thienopyridone drugs are selective activators of AMP-activated protein kinase beta1-containing complexes. Chem Biol 2008, 15(11):1220-1230. 10.1016/j.chembiol.2008.10.005, 19022182.
56. Goransson O, McBride A, Hawley SA, Ross FA, Shpiro N, Foretz M, Viollet B, Hardie DG, Sakamoto K. Mechanism of action of A-769662, a valuable tool for activation of AMP-activated protein kinase. J Biol Chem 2007, 282(45):32549-32560. 10.1074/jbc.M706536200, 2156105, 17855357.
57. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53(1):55-63. 10.1016/0165-0270(94)90144-9, 7990513.
58. Bourquin AF, Suveges M, Pertin M, Gilliard N, Sardy S, Davison AC, Spahn DR, Decosterd I. Assessment and analysis of mechanical allodynia-like behavior induced by spared nerve injury (SNI) in the mouse. Pain 2006, 122(1-2):14 e11-14.
59. Kim SH, Chung JM. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992, 50(3):355-363. 10.1016/0304-3959(92)90041-9, 1333581.
60. Cummins TR, Howe JR, Waxman SG. Slow closed-state inactivation: a novel mechanism underlying ramp currents in cells expressing the hNE/PN1 sodium channel. J Neurosci 1998, 18(23):9607-9619.