Activation of fibroblast growth factor receptor by axotomy, through downstream p38 in dorsal root ganglion, contributes to neuropathic pain

Neuroscience

Volumn 150, Issue 1, 2007, Pages 202-211

  Yamanaka, H ^a   Obata, K ^a   Kobayashi, K ^a   Dai, Y ^a   Fukuoka, T ^a   Noguchi, K ^a  

^a HYOGO COLLEGE OF MEDICINE   (Japan)

Author keywords

DRG; MAPK; peripheral nerve injury; rat; trophic factor receptor

Indexed keywords

3 [3 (2 CARBOXYETHYL) 4 METHYLPYRROL 2 METHYLIDENYL] 2 INDOLINONE; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; FIBROBLAST GROWTH FACTOR RECEPTOR 4; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN ANTIBODY; PROTEIN INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG INHIBITION; ENZYME ACTIVATION; IMMUNOHISTOCHEMISTRY; MALE; NERVE FIBER TRANSECTION; NERVE LIGATION; NEUROPATHIC PAIN; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SCIATIC NERVE; SPINAL GANGLION;

ANIMALS; AXOTOMY; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; ENZYME INHIBITORS; FUNCTIONAL LATERALITY; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; MALE; NERVE TISSUE PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PAIN MEASUREMENT; PHOSPHORYLATION; PYRROLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, FIBROBLAST GROWTH FACTOR; SCIATICA; TIME FACTORS;

EID: 36649008327     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.08.024     Document Type: Article

References (43)

1. 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
2. Basilico C., and Moscatelli D. The FGF family of growth factors and oncogenes. Review. Adv Cancer Res 59 (1992) 115-165
3. Cassina P., Pehar M., Vargas M.R., Castellanos R., Barbeito A.G., Estevez A.G., Thompson J.A., Beckman J.S., and Barbeito L. Astrocyte activation by fibroblast growth factor-1 and motor neuron apoptosis: implications for amyotrophic lateral sclerosis. J Neurochem 93 (2005) 38-46
4. Claus P., Werner S., Timmer M., and Grothe C. Expression of the fibroblast growth factor-2 isoforms and the FGF receptor 1-4 transcripts in the rat model system of Parkinson's disease. Neurosci Lett 360 (2004) 117-120
5. Costigan M., Befort K., Karchewski L., Griffin R.S., D'Urso D., Allchorne A., Sitarski J., Mannion J.W., Pratt R.E., and Woolf C.J. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci (2002). http://www.biomedcentral.com/1471-2202/3/16 Oct 25;3:16. Epub 2002 Oct 25. URL: http://www.biomedcentral.com/1471-2202/3/16.
6. Fukuoka T., Kondo E., Dai Y., Hashimoto N., and Noguchi. Brain-derived neurotrophic factor increases in the uninjured dorsal root ganglion neurons in selective spinal nerve ligation model. J Neurosci 21 (2001) 4891-4900
7. Gonzalez-Martinez D., Kim S.H., Hu Y., Guimond S., Schofield J., Winyard P., Vannelli G.B., Turnbull J., and Bouloux P.M. Anosmin-1 modulates fibroblast growth factor receptor 1 signaling in human gonadotropin-releasing hormone olfactory neuroblasts through a heparan sulfate-dependent mechanism. J Neurosci 24 (2004) 10384-10392
8. Grothe C., Meisinger C., and Claus P. In vivo expression and localization of the fibroblast growth factor system in the intact and lesioned rat peripheral nerve and spinal ganglia. J Comp Neurol 434 (2001) 342-357
9. Grothe C., Meisinger C., Hertenstein A., Kurz H., and Wewetzer K. Expression of fibroblast growth factor-2 and fibroblast growth factor receptor 1 messenger RNAs in spinal ganglia and sciatic nerve: regulation after peripheral nerve lesion. Neuroscience 76 (1997) 123-135
10. Heffron D.S., and Mandell J.W. Opposing roles of ERK and p38 MAP kinases in FGF2-induced astroglial process extension. Mol Cell Neurosci 28 (2005) 779-790
11. Itoh N., Yazaki N., Tagashira S., Miyake A., Ozaki K., Minami M., Satoh M., Ohta M., and Kawasaki T. Rat FGF receptor-4 mRNA in the brain is expressed preferentially in the medial habenular nucleus. Brain Res Mol Brain Res 21 (1994) 344-348
12. Ji R.R., Zhang Q., Zhang X., Piehl F., Reilly T., Pettersson R.F., and Hokfelt T. Prominent expression of bFGF in dorsal root ganglia after axotomy. Eur J Neurosci 7 (1995) 2458-2468
13. 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
14. Jiao J., Greendorfer J.S., Zhang P., Zinn K.R., Diglio C.A., and Thompson J.A. Alternatively spliced FGFR-1 isoform signaling differentially modulates endothelial cell responses to peroxynitrite. Arch Biochem Biophys 410 (2003) 187-200
15. Jin S.X., Zhuang Z.Y., Woolf C.J., and Ji R.R. p38 Mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain. J Neurosci 23 (2003) 4017-4022
16. Johnson D.E., and Williams L.T. Structural and functional diversity in the FGF receptor multigene family. Review. Adv Cancer Res 60 (1993) 1-41
17. Kalmar B., Greensmith L., Malcangio M., McMahon S.B., Csermely P., and Burnstock G. The effect of treatment with BRX-220, a co-inducer of heat shock proteins, on sensory fibers of the rat following peripheral nerve injury. Exp Neurol 184 (2003) 636-647
18. Klimaschewski L., Meisinger C., and Grothe C. Localization and regulation of basic fibroblast growth factor (FGF-2) and FGF receptor-1 in rat superior cervical ganglion after axotomy. J Neurobiol 38 (1999) 499-506
19. Lever I., Cunningham J., Grist J., Yip P.K., and Malcangio M. Release of BDNF and GABA in the dorsal horn of neuropathic rats. Eur J Neurosci 18 (2003) 1169-1174
20. Liu X., Mashour G.A., Webster H.F., and Kurtz A. Basic FGF and FGF receptor 1 are expressed in microglia during experimental autoimmune encephalomyelitis: temporally distinct expression of midkine and pleiotrophin. Glia 24 (1998) 390-397
21. Luo Z.D., Chaplan S.R., Higuera E.S., Sorkin L.S., Stauderman K.A., Williams M.E., and Yaksh T.L. Upregulation of dorsal root ganglion (alpha)2(delta) calcium channel subunit and its correlation with allodynia in spinal nerve-injured rats. J Neurosci 21 (2001) 1868-1875
22. Ma W., and Quirion R. Increased phosphorylation of cyclic AMP response element-binding protein (CREB) in the superficial dorsal horn neurons following partial sciatic nerve ligation. Pain 93 (2001) 295-301
23. Madiai F., Hussain S.R., Goettl V.M., Burry R.W., Stephens Jr. R.L., and Hackshaw K.V. Upregulation of FGF-2 in reactive spinal cord astrocytes following unilateral lumbar spinal nerve ligation. Exp Brain Res 148 (2003) 366-376
24. Madiai F., Goettl V.M., Hussain S.R., Clairmont A.R., Stephens Jr. R.L., and Hackshaw K.V. Anti-fibroblast growth factor-2 antibodies attenuate mechanical allodynia in a rat model of neuropathic pain. J Mol Neurosci 27 (2005) 315-324
25. Maher P.A. Nuclear translocation of fibroblast growth factor (FGF) receptors in response to FGF-2. J Cell Biol 134 (1996) 529-536
26. Meisinger C., and Grothe C. Differential regulation of fibroblast growth factor (FGF)-2 and FGF receptor 1 mRNAs and FGF-2 isoforms in spinal ganglia and sciatic nerve after peripheral nerve lesion. J Neurochem 68 (1997) 1150-1158
27. Messersmith D.J., Murtie J.C., Le T.Q., Frost E.E., and Armstrong R.C. Fibroblast growth factor 2 (FGF2) and FGF receptor expression in an experimental demyelinating disease with extensive remyelination. J Neurosci Res 62 (2000) 241-256
28. Mohammadi M., Dikic I., Sorokin A., Burgess W.H., Jaye M., and Schlessinger J. Identification of six novel autophosphorylation sites on fibroblast growth factor receptor 1 and elucidation of their importance in receptor activation and signal transduction. Mol Cell Biol 16 (1996) 977-989
29. Nindl W., Kavakebi P., Claus P., Grothe C., Pfaller K., and Klimaschewski L. Expression of basic fibroblast growth factor isoforms in postmitotic sympathetic neurons: synthesis, intracellular localization and involvement in karyokinesis. Neuroscience 124 (2004) 561-572
30. 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
31. Oellig C., Pirvola U., Taylor L., Elde R., Hokfelt T., and Pettersson R.F. Acidic FGF and FGF receptors are specifically expressed in neurons of developing and adult rat dorsal root ganglia. Eur J Neurosci 7 (1995) 863-874
32. Otto D., Unsicker K., and Grothe C. Pharmacological effects of nerve growth factor and fibroblast growth factor applied to the transectioned sciatic nerve on neuron death in adult rat dorsal root ganglia. Neurosci Lett 83 (1987) 156-160
33. Pezet S., and McMahon S.B. Neurotrophins: mediators and modulators of pain. Review. Annu Rev Neurosci 29 (2006) 507-538
34. Salvarezza S.B., Lopez H.S., and Masco D.H. The same cellular signaling pathways mediate survival in sensory neurons that switch their trophic requirements during development. J Neurochem 85 (2003) 1347-1358
35. Seltzer Z., Dubner R., and Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43 (1990) 205-218
36. Tsujino H., Kondo E., Fukuoka T., Dai Y., Tokunaga A., Miki K., Yonenobu K., Ochi T., and Noguchi K. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: A novel neuronal marker of nerve injury. Mol Cell Neurosci 15 (2000) 170-182
37. Weise B., Unsicker K., and Grothe C. Localization of basic fibroblast growth factor in a subpopulation of rat sensory neurons. Cell Tissue Res 267 (1992) 125-130
38. Xiao H.S., Huang Q.H., Zhang F.X., Bao L., Lu Y.J., Guo C., Yang L., Huang W.J., Fu G., Xu S.H., Cheng X.P., Yan Q., Zhu Z.D., Zhang X., Chen Z., Han Z.G., and Zhang X. Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Proc Natl Acad Sci U S A 99 (2002) 8360-8365
39. Yamanaka H., Obata K., Fukuoka T., Dai Y., Kobayashi K., Tokunaga A., and Noguchi K. Tissue plasminogen activator in primary afferents induces dorsal horn excitability and pain response after peripheral nerve injury. Eur J Neurosci 19 (2004) 93-102
40. Zhou X.F., Chie E.T., Deng Y.S., Zhong J.H., Xue Q., Rush R.A., and Xian C.J. Injured primary sensory neurons switch phenotype for brain-derived neurotrophic factor in the rat. Neuroscience 92 (1999) 841-853
41. Zhuang Z.Y., Gerner P., Woolf C.J., and Ji R.R. ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 114 (2005) 149-159
42. Zhuang Z.Y., Xu H., Clapham D.E., and Ji R.R. Phosphatidylinositol 3-kinase activates ERK in primary sensory neurons and mediates inflammatory heat hyperalgesia through TRPV1 sensitization. J Neurosci 24 (2004) 8300-8309
43. Zhuang Z.Y., Wen Y.R., Zhang D.R., Borsello T., Bonny C., Strichartz G.R., Decosterd I., and Ji R.R. A peptide c-Jun N-terminal kinase (JNK) inhibitor blocks mechanical allodynia after spinal nerve ligation: respective roles of JNK activation in primary sensory neurons and spinal astrocytes for neuropathic pain development and maintenance. J Neurosci 26 (2006) 3551-3560