Agrin downregulation induced by nerve injury contributes to neuropathic pain

Journal of Neuroscience

Volumn 30, Issue 45, 2010, Pages 15286-15297

  Cui, Jian Guo ^a   Bazan, Nicolas G ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; AGRIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; PARACETAMOL DERIVATIVE; SERINE DERIVATIVE; SMALL INTERFERING RNA;

ADENO ASSOCIATED VIRUS; ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE SILENCING; HYPERALGESIA; INTERNEURON; NEUROPATHIC PAIN; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SPINAL CORD DORSAL HORN; TOUCH; UPREGULATION;

AGRIN; ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; DOWN-REGULATION; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; MALE; NEURALGIA; NEURONS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SCIATIC NERVE;

EID: 78149484426     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4418-10.2010     Document Type: Article

References (48)

1. Bennett GJ, Xie YK (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33:87-107.
2. Bowe MA, Fallon JR (1995) The role of agrin in synapse formation. Annu Rev Neurosci 18:443-462.
3. Bowe MA, Deyst KA, Leszyk JD, Fallon JR (1994) Identification and purification of an agrin receptor from Torpedo postsynaptic membranes: a heteromeric complex related to the dystroglycans. Neuron 12:1173-1180.
4. Campanelli JT, Roberds SL, Campbell KP, Scheller RH (1994) A role for dystrophin-associated glycoproteins and utrophin in agrin-induced AChR clustering. Cell 77:663-674. (Pubitemid 24175603)
5. Chergui K, Svenningsson P, Greengard P (2005) Physiological role for casein kinase 1 in glutamatergic synaptic transmission. J Neurosci 25:6601-6609.
6. Cui J-G, Linderoth B, Meyerson BA (1997) Incidence of mononeuropathy in rats is influenced by pre-emptive alteration of spinal excitability. Eur J Pain 1:53-59.
7. Cui J-G, O'Connor WT, Ungerstedt U, Linderoth B, Meyerson BA (1997) Spinal cord stimulation attenuates augmented dorsal horn release of excitatory amino acids in mononeuropathy via a GABAergic mechanism. Pain 73:87-95.
8. Cui J-G, Zhang X, Zhao YH, Chen C, Bazan N (2006) Allodynia and hyperalgesia suppression by a novel analgesic in experimental neuropathic pain. Biochem Biophys Res Commun 350:358-363.
9. Dunah AW, Yasuda RP, Luo J, Wang Y, Prybylowski KL, Wolfe BB (1999) Biochemical studies of the structure and function of the N-methyl-D-aspartate subtype of glutamate receptors. Mol Neurobiol 19:151-179.
10. Erichsen HK, Hao JX, Xu XJ, Blackburn-Munro G (2003) A comparison of the antinociceptive effects of voltage-activated Na+ channel blockers in two rat models of neuropathic pain. Eur J Pharmacol 458:275-282.
11. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-811.
12. Furukawa H, Singh SK, Mancusso R, Gouaux E (2005) Subunit arrangement and function in NMDA receptors. Nature 438:185-192.
13. Gao X, Kim HK, Chung JM, Chung K (2007) Reactive oxygen species (ROS) are involved in enhancement of NMDA-receptor phosphorylation in animal models of pain. Pain 131:262-271.
14. Gautam M, Noakes PG, Mudd J, Nichol M, Chu GC, Sanes JR, Merlie JP (1995) Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377:232-236.
15. Gazelius B, Cui J-G, Svensson M, Meyerson B, Linderoth B (1996) Photo-chemically induced ischaemic lesion of the rat sciatic nerve. A novel method providing high incidence of mononeuropathy. Neuroreport 7:2619-2623.
16. Glass DJ, Bowen DC, Stitt TN, Radziejewski C, Bruno J, Ryan TE, Gies DR, Shah S, Mattsson K, Burden SJ, DiStefano PS, Valenzuela DM, DeChiara TM, Yancopoulos GD (1996) Agrin acts via a MuSK receptor complex. Cell 85:513-523.
17. Gorgels TG, Van Lookeren Campagne M, Oestreicher AB, Gribnau AA, Gispen WH (1989) B-50/GAP43 is localized at the cytoplasmic side of the plasma membrane in developing and adult rat pyramidal tract. J Neurosci 9:3861-3869.
18. Guo W, Zou S, Guan Y, Ikeda T, Tal M, Dubner R, Ren K (2002) Tyrosine phosphorylation of the NR2B subunit of the NMDA receptor in the spinal cord during the development and maintenance of inflammatory hyperalgesia. J Neurosci 22:6208-6217.
19. Hildebrand JG, Christensen TA, Harrow ID, Homberg U, Matsumoto SG, Waldrop BR (1992) The roles of local interneurons in the processing of olfactory information in the antennal lobes of the moth Manduca sexta. Acta Biol Hung 43:167-174.
20. Hilgenberg LG, Smith MA (2004) Agrin signaling in cortical neurons is mediated by a tyrosine kinase-dependent increase in intracellular Ca2+ that engages both CaMKII and MAPK signal pathways. J Neurobiol 61:289-300.
21. Hilgenberg LG, Su H, Gu H, O'Dowd DK, Smith MA (2006) Alpha3Na+/ K+-ATPase is a neuronal receptor for agrin. Cell 125:359-369.
22. Hoch W, Ferns M, Campanelli JT, Hall ZW, Scheller RH (1993) Developmental regulation of highly active alternatively spliced forms of agrin. Neuron 11:479-490.
23. Hoover CL, Hilgenberg LG, Smith MA (2003) The COOH-terminal domain of agrin signals via a synaptic receptor in central nervous system neurons. J Cell Biol 161:923-932.
24. Ji RR, Böse CM, Lesuisse C, Qiu D, Huang JC, Zhang Q, Rupp F (1998) Specific agrin isoforms induce cAMP response element binding protein phosphorylation in hippocampal neurons. J Neurosci 18:9695-9702.
25. Kennedy S, Wang D, Ruvkun G (2004) A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 427:645-649.
26. Kim N, Burden SJ (2008) MuSK controls where motor axons grow and form synapses. Nat Neurosci 11:19-27.
27. Kim N, Stiegler AL, Cameron TO, Hallock PT, Gomez AM, Huang JH, Hubbard SR, Dustin ML, Burden SJ (2008) Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell 135:334-342.
28. Liu H, Wang H, Sheng M, Jan LY, Jan YN, Basbaum AI (1994) Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn. Proc Natl Acad Sci U S A 91:8383-8387.
29. Magill C, Reist NE, Fallon JR, Nitkin RM, Wallace BG, McMahan UJ (1987) Agrin. Prog Brain Res 71:391-396.
30. Mantych KB, Ferreira A (2001) Agrin differentially regulates the rates of axonal and dendritic elongation in cultured hippocampal neurons. J Neurosci 21:6802-6809.
31. Mayer ML, Westbrook GL, Guthrie PB (1984) Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature 309:261-263.
32. McBain CJ, Fisahn A (2001) Interneurons unbound. Nat Rev Neurosci 2:11-23.
33. McMahon SB, Lewin GR, Wall PD (1993) Central hyperexcitability triggered by noxious inputs. Curr Opin Neurobiol 3:602-610.
34. McManus MT, Sharp PA (2002) Gene silencing in mammals by small interfering RNAs. Nat Rev Genet 3:737-747.
35. O'Connor AB, Dworkin RH (2009) Treatment of neuropathic pain: an overview of recent guidelines. Am J Med 122:S22-S32.
36. Roh DH, Kim HW, Yoon SY, Seo HS, Kwon YB, Han HJ, Beitz AJ, Lee JH (2008) Intrathecal clonidine suppresses phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit in spinal dorsal horn neurons of rats with neuropathic pain. Anesth Analg 107:693-700.
37. Rostas JA, Brent VA, Voss K, Errington ML, Bliss TV, Gurd JW (1996) Enhanced tyrosine phosphorylation of the 2B subunit of the N-methyl-Daspartate receptor in long-term potentiation. Proc Natl Acad Sci U S A 93:10452-10456.
38. Ruegg MA, Tsim KW, Horton SE, Kröger S, Escher G, Gensch EM, McMahan UJ (1992) The agrin gene codes for a family of basal lamina proteins that differ in function and distribution. Neuron 8:691-699.
39. Rupp F, Hoch W, Campanelli JT, Kreiner T, Scheller RH (1992) Agrin and the organization of the neuromuscular junction. Curr Opin Neurobiol 2:88-93.
40. Salter MW, Kalia LV (2004) Src kinases: a hub for NMDA receptor regulation. Nat Rev Neurosci 5:317-328.
41. Santiago-Figueroa J, Kuffler DP (2009) Reducing and eliminating neuropathic pain. P R Health Sci J 28:289-300.
42. Schipke CG, Ohlemeyer C, Matyash M, Nolte C, Kettenmann H, Kirchhoff F (2001) Astrocytes of the mouse neocortex express functional N-methyl- D-aspartate receptors. FASEB J 15:1270-1272.
43. Schrattenholz A, Soskic V (2006) NMDA receptors are not alone: dynamic regulation of NMDA receptor structure and function by neuregulins and transient cholesterol-rich membrane domains leads to disease-specific nuances of glutamate-signalling. Curr Top Med Chem 6:663-686.
44. Skene JH, Jacobson RD, Snipes GJ, McGuire CB, Norden JJ, Freeman JA (1986) Aprotein induced during nerve growth (GAP-43) is a major component of growth-cone membranes. Science 233:783-786.
45. Smith MA, Hilgenberg LG (2002) Agrin in the CNS: a protein in search of a function? Neuroreport 13:1485-1495.
46. Ultenius C, Linderoth B, Meyerson BA, Wallin J (2006) Spinal NMDA receptor phosphorylation correlates with the presence of neuropathic signs following peripheral nerve injury in the rat. Neurosci Lett 399:85-90.
47. Vaccarino AL, Paul D, Mukherjee PK, Rodríguez de Turco EB, Marcheselli VL, Xu L, Trudell ML, Minguez JM, Matía MP, Sunkel C, Alvarez-Builla J, Bazan NG (2007) Synthesis and in vivo evaluation of non-hepatotoxic acetaminophen analogs. Bioorg Med Chem 15:2206-2215.
48. Xi D, Keeler B, Zhang W, Houle JD, Gao WJ (2009) NMDA receptor sub-unit expression in GABAergic interneurons in the prefrontal cortex: application of laser microdissection technique. J Neurosci Methods 176: 172-181.