Neurotrophin-3 attenuates galanin expression in the chronic constriction injury model of neuropathic pain

Neuroscience

Volumn 141, Issue 4, 2006, Pages 2075-2085

  Wilson Gerwing, T D ^a   Verge, V M K ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

dorsal root ganglion; galanin; neurotrophins; PACAP; pain; trkA

Indexed keywords

GALANIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; MESSENGER RNA; NEUROTROPHIN 3; PROTEIN TYROSINE KINASE A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC DISEASE; CONTROLLED STUDY; DISEASE ASSOCIATION; IN SITU HYBRIDIZATION; INCIDENCE; MALE; NERVE COMPRESSION; NEUROPATHIC PAIN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; CONSTRICTION; DISEASE MODELS, ANIMAL; GALANIN; GENE EXPRESSION REGULATION; IN SITU HYBRIDIZATION; MALE; NEUROTROPHIN 3; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RATS; RATS, WISTAR; RECEPTOR, TRKA; RNA, MESSENGER; SCIATICA;

EID: 33747173007     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.05.056     Document Type: Article

References (70)

1. Amann R., Schuligoi R., Herzeg G., and Donnerer J. Intraplantar injection of nerve growth factor into the rat hind paw. local edema and effects on thermal nociceptive threshold. Pain 64 (1996) 323-329
2. Amaya F., Shimosato G., Nagano M., Ueda M., Hashimoto S., Tanaka Y., Suzuki H., and Tanaka M. NGF and GDNF differentially regulate TRPV1 expression that contributes to development of inflammatory thermal hyperalgesia. Eur J Neurosci 20 (2004) 2303-2310
3. Armstrong B.D., Hu Z., Abad C., Yamamoto M., Rodriguez W.I., Cheng J., Tam J., Gomariz R.P., Patterson P.H., and Waschek J.A. Lymphocyte regulation of neuropeptide gene expression after neuronal injury. J Neurosci Res 74 (2003) 240-247
4. Barker P.A., Lomen-Hoerth C., Gensch E.M., Meakin S.O., Glass D.J., and Shooter E.M. Tissue-specific alternative splicing generates two isoforms of the trkA receptor. J Biol Chem 268 (1993) 15150-15157
5. Bennett G.J., and Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33 (1988) 87-107
6. Blakeman K.H., Holmberg K., Hao J.X., Xu X.J., Kahl U., Lendahl U., Bartfai T., Wiesenfeld-Hallin Z., and Hokfelt T. Mice over-expressing galanin have elevated heat nociceptive threshold. Neuroreport 12 (2001) 423-425
7. Dagerlind A., Friberg K., Bean A.J., and Hokfelt T. Sensitive mRNA detection using unfixed tissue. combined radioactive and non-radioactive in situ hybridization histochemistry. Histochemistry 98 (1992) 39-49
8. Dickinson T., Mitchell R., Robberecht P., and Fleetwood-Walker S.M. The role of VIP/PACAP receptor subtypes in spinal somatosensory processing in rats with an experimental peripheral mononeuropathy. Neuropharmacology 38 (1999) 167-180
9. Eaton M.J., Karmally S., Martinez M.A., Plunkett J.A., Lopez T., and Cejas P.J. Lumbar transplant of neurons genetically modified to secrete galanin reverse pain-like behaviors after partial sciatic nerve injury. J Peripher Nerv Syst 4 (1999) 245-257
10. Grass S., Crawley J.N., Xu X.J., and Wiesenfeld-Hallin Z. Reduced spinal cord sensitization to C-fibre stimulation in mice over-expressing galanin. Eur J Neurosci 17 (2003) 1829-1832
11. Gratto K.A., and Verge V.M. Neurotrophin-3 down-regulates trkA mRNA, NGF high-affinity binding sites, and associated phenotype in adult DRG neurons. Eur J Neurosci 18 (2003) 1535-1548
12. Hao J.X., Shi T.J., Xu I.S., Kaupilla T., Xu X.J., Hokfelt T., Bartfai T., and Wiesenfeld-Hallin Z. Intrathecal galanin alleviates allodynia-like behaviour in rats after partial peripheral nerve injury. Eur J Neurosci 11 (1999) 427-432
13. Herzberg U., Eliav E., Dorsey J.M., Gracely R.H., and Kopin I.J. NGF involvement in pain induced by chronic constriction injury of the rat sciatic nerve. Neuroreport 8 (1997) 1613-1618
14. Hokfelt T., Wiesenfeld-Hallin Z., Villar M., and Melander T. Increase of galanin-like immunoreactivity in rat dorsal root ganglion cells after peripheral axotomy. Neurosci Lett 83 (1987) 217-220
15. Hurley J.D., Gardiner J.V., Jones P.M., and Bloom S.R. Cloning and molecular characterization of complementary deoxyribonucleic acid corresponding to a novel form of pituitary adenylate cyclase-activating polypeptide messenger ribonucleic acid in the rat testis. Endocrinology 136 (1995) 550-557
16. Hygge-Blakeman K., Brumovsky P., Hao J.X., Xu X.J., Hokfelt T., Crawley J.N., and Wiesenfeld-Hallin Z. Galanin over-expression decreases the development of neuropathic pain-like behaviors in mice after partial sciatic nerve injury. Brain Res 1025 (2004) 152-158
17. Ji R.R., Samad T.A., Jin S.X., Schmoll R., and Woolf C.J. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36 (2002) 57-68
18. Ji R.R., Zhang Q., Bedecs K., Arvidsson J., Zhang X., Xu X.J., Wiesenfeld-Hallin Z., Bartfai T., and Hokfelt T. Galanin antisense oligonucleotides reduce galanin levels in dorsal root ganglia and induce autotomy in rats after axotomy. Proc Natl Acad Sci U S A 91 (1994) 12540-12543
19. Jongsma H., Danielsen N., Sundler F., and Kanje M. Alteration of PACAP distribution and PACAP receptor binding in the rat sensory nervous system following sciatic nerve transection. Brain Res 853 (2000) 186-196
20. Jongsma Wallin H., Pettersson L.M., Verge V.M., and Danielsen N. Effect of anti-nerve growth factor treatment on pituitary adenylate cyclase activating polypeptide expression in adult sensory neurons exposed to adjuvant induced inflammation. Neuroscience 120 (2003) 325-331
21. Jongsma Wallin H., Danielsen N., Johnston J.M., Gratto K.A., Karchewski L.A., and Verge V.M. Exogenous NT-3 and NGF differentially modulate PACAP expression in adult sensory neurons, suggesting distinct roles in injury and inflammation. Eur J Neurosci 14 (2001) 267-282
22. Kajander K.C., and Bennett G.J. Onset of a painful peripheral neuropathy in rat. a partial and differential deafferentation and spontaneous discharge in A beta and A delta primary afferent neurons. J Neurophysiol 68 (1992) 734-744
23. Karchewski L.A., Gratto K.A., Wetmore C., and Verge V.M. Dynamic patterns of BDNF expression in injured sensory neurons. differential modulation by NGF and NT-3. Eur J Neurosci 16 (2002) 1449-1462
24. Karchewski L.A., Kim F.A., Johnston J., McKnight R.M., and Verge V.M. Anatomical evidence supporting the potential for modulation by multiple neurotrophins in the majority of adult lumbar sensory neurons. J Comp Neurol 413 (1999) 327-341
25. Kerr B.J., Gupta Y., Pope R., Thompson S.W., Wynick D., and McMahon S.B. Endogenous galanin potentiates spinal nociceptive processing following inflammation. Pain 93 (2001) 267-277
26. Lee F.S., Rajagopal R., Kim A.H., Chang P.C., and Chao M.V. Activation of Trk neurotrophin receptor signaling by pituitary adenylate cyclase-activating polypeptides. J Biol Chem 277 (2002) 9096-9102
27. Lewin G.R., Ritter A.M., and Mendell L.M. Nerve growth factor-induced hyperalgesia in the neonatal and adult rat. J Neurosci 13 (1993) 2136-2148
28. Li L., Deng Y.S., and Zhou X.F. Downregulation of TrkA expression in primary sensory neurons after unilateral lumbar spinal nerve transection and some rescuing effects of nerve growth factor infusion. Neurosci Res 38 (2000) 183-191
29. Lindsay R.M., and Harmar A.J. Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurons. Nature 337 (1989) 362-364
30. Lioudyno M., Skoglosa Y., Takei N., and Lindholm D. Pituitary adenylate cyclase-activating polypeptide (PACAP) protects dorsal root ganglion neurons from death and induces calcitonin gene-related peptide (CGRP) immunoreactivity in vitro. J Neurosci Res 51 (1998) 243-256
31. Ma W., and Bisby M.A. Differential expression of galanin immunoreactivities in the primary sensory neurons following partial and complete sciatic nerve injuries. Neuroscience 79 (1997) 1183-1195
32. Mabuchi T., Shintani N., Matsumura S., Okuda-Ashitaka E., Hashimoto H., Muratani T., Minami T., Baba A., and Ito S. Pituitary adenylate cyclase-activating polypeptide is required for the development of spinal sensitization and induction of neuropathic pain. J Neurosci 24 (2004) 7283-7291
33. Malcangio M., Garrett N.E., Cruwys S., and Tomlinson D.R. Nerve growth factor- and neurotrophin-3-induced changes in nociceptive threshold and the release of substance P from the rat isolated spinal cord. J Neurosci 17 (1997) 8459-8467
34. Mearow K.M., and Kril Y. Anti-NGF treatment blocks the upregulation of NGF receptor mRNA expression associated with collateral sprouting of rat dorsal root ganglion neurons. Neurosci Lett 184 (1995) 55-58
35. Millan M.J. The induction of pain. an integrative review. Prog Neurobiol 57 (1999) 1-164
36. Mulder H., Jongsma H., Zhang Y., Gebre-Medhin S., Sundler F., and Danielsen N. Pituitary adenylate cyclase-activating polypeptide and islet amyloid polypeptide in primary sensory neurons. functional implications from plasticity in expression on nerve injury and inflammation. Mol Neurobiol 19 (1999) 229-253
37. Murphy P.G., Ramer M.S., Borthwick L., Gauldie J., Richardson P.M., and Bisby M.A. Endogenous interleukin-6 contributes to hypersensitivity to cutaneous stimuli and changes in neuropeptides associated with chronic nerve constriction in mice. Eur J Neurosci 11 (1999) 2243-2253
38. Nahin R.L., Ren K., De Leon M., and Ruda M. Primary sensory neurons exhibit altered gene expression in a rat model of neuropathic pain. Pain 58 (1994) 95-108
39. Narita M., Dun S.L., Dun N.J., and Tseng L.F. Hyperalgesia induced by pituitary adenylate cyclase-activating polypeptide in the mouse spinal cord. Eur J Pharmacol 311 (1996) 121-126
40. Obata K., Yamanaka H., Dai Y., Mizushima T., Fukuoka T., Tokunaga A., and Noguchi K. Differential activation of MAPK in injured and uninjured DRG neurons following chronic constriction injury of the sciatic nerve in rats. Eur J Neurosci 20 (2004) 2881-2895
41. Okamoto K., Martin D.P., Schmelzer J.D., Mitsui Y., and Low P.A. Pro- and anti-inflammatory cytokine gene expression in rat sciatic nerve chronic constriction injury model of neuropathic pain. Exp Neurol 169 (2001) 386-391
42. Petruska J.C., and Mendell L.M. The many functions of nerve growth factor. multiple actions on nociceptors. Neurosci Lett 361 (2004) 168-171
43. Ramer M.S., Ma W., Murphy P.G., Richardson P.M., and Bisby M.A. Galanin expression in neuropathic pain. friend or foe?. Ann N Y Acad Sci 863 (1998) 390-401
44. Richardson P.M., Verge V.M.K., and Riopelle R.J. Quantitative radioautography for NGF receptors. In: Rush R.A. (Ed). Nerve growth factors (1989), John Wiley and Sons, London 315-326
45. Ro L.S., Chen S.T., Tang L.M., and Jacobs J.M. Effect of NGF and anti-NGF on neuropathic pain in rats following chronic constriction injury of the sciatic nerve. Pain 79 (1999) 265-274
46. Schuligoi R., and Amann R. Differential effects of treatment with nerve growth factor on thermal nociception and on calcitonin gene-related peptide content of primary afferent neurons in the rat. Neurosci Lett 252 (1998) 147-149
47. Schwartz J.P., Pearson J., and Johnson E.M. Effect of exposure to anti-NGF on sensory neurons of adult rats and guinea pigs. Brain Res 244 (1982) 378-381
48. Shi T.J., Cui J.G., Meyerson B.A., Linderoth B., and Hokfelt T. Regulation of galanin and neuropeptide Y in dorsal root ganglia and dorsal horn in rat mononeuropathic models. possible relation to tactile hypersensitivity. Neuroscience 93 (1999) 741-757
49. Sterne G.D., Brown R.A., Green C.J., and Terenghi G. NT-3 modulates NPY expression in primary sensory neurons following peripheral nerve injury. J Anat 193 (1998) 273-281
50. Verge V.M.K., and Johnston J.M. Infusion of NGF or NT-3 results in reduced levels of IL-6 and bFGF mRNAs in injured adult primary sensory neurons. Soc Neurosci Abstr 698 (2000) 6
51. Verge V.M., Riopelle R.J., and Richardson P.M. Nerve growth factor receptors on normal and injured sensory neurons. J Neurosci 9 (1989) 914-922
52. Verge V.M.K., Wilson T.D., Karchewski L.A., and Gratto K.A. Changes in DRG neurons after injury. Possible involvement in the development and maintenance of neuropathic pain. In: Malmberge A.B., and Chaplan S. (Eds). Mechanisms and mediators of neuropathic pain (2002), Birkhauser, Berlin 51-65
53. Verge V.M., Richardson P.M., Wiesenfeld-Hallin Z., and Hokfelt T. Differential influence of nerve growth factor on neuropeptide expression in vivo. a novel role in peptide suppression in adult sensory neurons. J Neurosci 15 (1995) 2081-2096
54. Verge V.M., Xu Z., Xu X.J., Wiesenfeld-Hallin Z., and Hokfelt T. Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy. in situ hybridization and functional studies. Proc Natl Acad Sci U S A 89 (1992) 11617-11621
55. Verge V.M., Xu X.J., Langel U., Hokfelt T., Wiesenfeld-Hallin Z., and Bartfai T. Evidence for endogenous inhibition of autotomy by galanin in the rat after sciatic nerve section. demonstrated by chronic intrathecal infusion of a high affinity galanin receptor antagonist. Neurosci Lett 149 (1993) 193-197
56. Villar M.J., Wiesenfeld-Hallin Z., Xu X.J., Theodorsson E., Emson P.C., and Hokfelt T. Further studies on galanin-, substance P-, and CGRP-like immunoreactivities in primary sensory neurons and spinal cord. effects of dorsal rhizotomies and sciatic nerve lesions. Exp Neurol 112 (1991) 29-39
57. Villar M.J., Cortes R., Theodorsson E., Wiesenfeld-Hallin Z., Schalling M., Fahrenkrug J., Emson P.C., and Hokfelt T. Neuropeptide expression in rat dorsal root ganglion cells and spinal cord after peripheral nerve injury with special reference to galanin. Neuroscience 33 (1989) 587-604
58. Vrontakis M.E., Peden L.M., Duckworth M.L., and Friesen H.G. Isolation and characterization of a complementary DNA (galanin) clone from estrogen-induced pituitary tumor messenger RNA. J Biol Chem 262 (1987) 16755-16758
59. Wiesenfeld-Hallin Z., and Xu X.J. Galanin in somatosensory function. Ann N Y Acad Sci 863 (1998) 383-389
60. Wilson T.D., and Verge V.M.K. NT-3 alters phenotypic changes associated with chronic constriction injury (CCI) in adult DRG neurons. Soc Neurosci Abstr 698 (2000) 8
61. Wilson-Gerwing T.D., Dmyterko M.V., Zochodne D.W., Johnston J.M., and Verge V.M. Neurotrophin-3 suppresses thermal hyperalgesia associated with neuropathic pain and attenuates transient receptor potential vanilloid receptor-1 expression in adult sensory neurons. J Neurosci 25 (2005) 758-767
62. Woolf C.J. Phenotypic modification of primary sensory neurons. the role of nerve growth factor in the production of persistent pain. Philos Trans R Soc Lond B Biol Sci 351 (1996) 441-448
63. Woolf C.J., Safieh-Garabedian B., Ma Q.P., Crilly P., and Winter J. Nerve growth factor contributes to the generation of inflammatory sensory hypersensitivity. Neuroscience 62 (1994) 327-331
64. Wu W.P., Hao J.X., Lundstrom L., Wiesenfeld-Hallin Z., Langel U., Bartfai T., and Xu X.J. Systemic galnon, a low-molecular weight galanin receptor agonist, reduces heat hyperalgesia in rats with nerve injury. Eur J Pharmacol 482 (2003) 133-137
65. Xu X.J., Hokfelt T., Bartfai T., and Wiesenfeld-Hallin Z. Galanin and spinal nociceptive mechanisms. recent advances and therapeutic implications. Neuropeptides 34 (2000) 137-147
66. Yamamoto T., and Tatsuno I. Antinociceptive effect of intrathecally administered pituitary adenylate cyclase activating polypeptide (PACAP) on the rat formalin test. Neurosci Lett 184 (1995) 32-35
67. Zhang Q., Shi T.J., Ji R.R., Zhang Y.Z., Sundler F., Hannibal J., Fahrenkrug J., and Hokfelt T. Expression of pituitary adenylate cyclase-activating polypeptide in dorsal root ganglia following axotomy. time course and coexistence. Brain Res 705 (1995) 149-158
68. Zhang Y., Malmberg A.B., Sjolund B., and Yaksh T.L. The effect of pituitary adenylate cyclase activating peptide (PACAP) on the nociceptive formalin test. Neurosci Lett 207 (1996) 187-190
69. Zhang Y.Z., Hannibal J., Zhao Q., Moller K., Danielsen N., Fahrenkrug J., and Sundler F. Pituitary adenylate cyclase activating peptide expression in the rat dorsal root ganglia. up-regulation after peripheral nerve injury. Neuroscience 74 (1996) 1099-1110
70. Zhang Y., Danielsen N., Sundler F., and Mulder H. Pituitary adenylate cyclase-activating peptide is upregulated in sensory neurons by inflammation. Neuroreport 9 (1998) 2833-2836