Overexpression of GDNF in the uninjured DRG exerts analgesic effects on neuropathic pain following segmental spinal nerve ligation in mice

Journal of Pain

Volumn 12, Issue 11, 2011, Pages 1130-1139

  Takasu, Kumiko ^a   Sakai, Atsushi ^a   Hanawa, Hideki ^a   Shimada, Takashi ^a   Suzuki, Hidenori ^a  

^a NIPPON MEDICAL SCHOOL   (Japan)

Author keywords

DRG; GDNF; lentiviral vector; neuropathic pain; spinal cord

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; LENTIVIRUS VECTOR;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MALE; MOUSE; NERVE LIGATION; NEUROPATHIC PAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; SPINAL GANGLION;

ANIMALS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GANGLIA, SPINAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; IMMUNOHISTOCHEMISTRY; LIGATION; MALE; MICE; MICE, INBRED C57BL; NEURALGIA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPINAL NERVES;

EID: 80255137410     PISSN: 15265900     EISSN: 15288447     Source Type: Journal    
DOI: 10.1016/j.jpain.2011.04.003     Document Type: Article

References (49)

1. M.S. Airaksinen, and M. Saarma The GDNF family: Signalling, biological functions and therapeutic value Nat Rev Neurosci 3 2002 383 394 (Pubitemid 135706635)
2. F. Amaya, G. Shimosato, M. Nagano, M. Ueda, S. Hashimoto, Y. Tanaka, H. Suzuki, and M. Tanaka NGF and GDNF differentially regulate TRPV1 expression that contributes to development of inflammatory thermal hyperalgesia Eur J Neurosci 20 2004 2303 2310 (Pubitemid 39472393)
3. S. Averill, G.J. Michael, P.J. Shortland, R.C. Leavesley, V.R. King, E.J. Bradbury, S.B. McMahon, and J.V. Priestley NGF and GDNF ameliorate the increase in ATF3 expression which occurs in dorsal root ganglion cells in response to peripheral nerve injury Eur J Neurosci 19 2004 1437 1445 (Pubitemid 38437906)
4. A.I. Basbaum, D.M. Bautista, G. Scherrer, and D. Julius Cellular and molecular mechanisms of pain Cell 139 2009 267 284
5. D.L.H. Bennett, T.J. Boucher, M.P. Armanini, K.T. Poulsen, G.J. Michael, J.V. Priestley, H.S. Phillips, S.B. McMahon, and D.L. Shelton The glial cell line-derived neurotrophic factor family receptor components are differentially regulated within sensory neurons after nerve injury J Neurosci 20 2000 427 437 (Pubitemid 30220528)
6. D.L.H. Bennett, G.J. Michael, N. Ramachandran, J.B. Munson, S. Averill, Q. Yan, S.B. McMahon, and J.V. Priestley A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury J Neurosci 18 1998 3059 3072 (Pubitemid 28163236)
7. O. Bogen, E.K. Joseph, X. Chen, and J.D. Levine GDNF hyperalgesia is mediated by PLCγ, MAPK/ERK, PI3K, CDK5 and Src family kinase signaling and dependent on the IB4-binding protein versican Eur J Neurosci 28 2008 12 19
8. T.J. Boucher, K. Okuse, D.L.H. Bennett, J.B. Munson, J.N. Wood, and S.B. McMahon Potent analgesic effects of GDNF in neuropathic pain states Science 290 2000 124 127
9. 3 purinoreceptors in sensory neurons: Effects of axotomy and glial-derived neurotrophic factor Mol Cell Neurosci 12 1998 256 268 (Pubitemid 28536078)
10. A. Buj-Bello, V.L. Buchman, A. Horton, A. Rosenthal, and A.M. Davies GDNF is an age-specific survival factor for sensory and autonomic neurons Neuron 15 1995 821 828
11. D.J. Cavanaugh, H. Lee, L. Lo, S.D. Shields, M.J. Zylka, A.I. Basbaum, and D.J. Anderson Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli Proc Natl Acad Sci U S A 106 2009 9075 9080
12. C. Ciobanu, G. Reid, and A. Babes Acute and chronic effects of neurotrophic factors BDNF and GDNF on responses mediated by thermo-sensitive TRP channels in cultured rat dorsal root ganglion neurons Brain Res 1284 2009 54 67
13. M. Costigan, T.A. Samad, A. Allchorne, C. Lanoue, S. Tate, and C.J. Woolf High basal expression and injury-induced down regulation of two regulator of G-protein signaling transcripts, RGS3 and RGS4 in primary sensory neurons Mol Cell Neurosci 24 2003 106 116 (Pubitemid 37194537)
14. M.L.L. Donnelly, G. Luke, A. Mehrotra, X. Li, L.E. Hughes, D. Gani, and M.D. Ryan Analysis of the aphthovirus 2A/2B polyprotein 'cleavage' mechanism indicates not a proteolytic reaction, but a novel translational effect: A putative ribosomal 'skip' J Gen Virol 82 2001 1013 1025 (Pubitemid 32454602)
15. E. Dowd, C. Monville, E.M. Torres, L.F. Wong, M. Azzouz, N.D. Mazarakis, and S.B. Dunnett Lentivector-mediated delivery of GDNF protects complex motor functions relevant to human Parkinsonism in a rat lesion model Eur J Neurosci 22 2005 2587 2595 (Pubitemid 41759001)
16. M. Fang, Y. Wang, Q.H. He, Y.X. Sun, L.B. Deng, X.M. Wang, and J.S. Han Glial cell line-derived neurotrophic factor contributes to delayed inflammatory hyperalgesia in adjuvant rat pain model Neuroscience 117 2003 503 512 (Pubitemid 36263146)
17. S. Furler, J.C. Paterna, M. Weibel, and H. Büeler Recombinant AAV vectors containing the foot and mouth disease virus 2A sequence confer efficient bicistronic gene expression in cultured cells and rat substantia nigra neurons Gene Ther 8 2001 864 873 (Pubitemid 32577191)
18. J.P. Golden, M. Hoshi, M.A. Nassar, H. Enomoto, J.N. Wood, J. Milbrandt, R.W. Gereau, E.M. Johnson Jr., and S. Jain RET signaling is required for survival and normal function of nonpeptidergic nociceptors J Neurosci 30 2010 3983 3994
19. H. Hanawa, D.A. Persons, and A.W. Nienhuis Mobilization and mechanism of transcription of integrated self-inactivating lentiviral vectors J Virol 79 2005 8410 8421 (Pubitemid 40853543)
20. S. Hao, M. Mata, D. Wolfe, S. Huang, J.C. Glorioso, and D.J. Fink HSV-mediated gene transfer of the glial cell-derived neurotrophic factor provides an antiallodynic effect on neuropathic pain Mol Ther 8 2003 367 375 (Pubitemid 37161458)
21. J. Hu, M. Mata, S. Hao, G. Zhang, and D.J. Fink Central sprouting of uninjured small fiber afferents in the adult rat spinal cord following spinal nerve ligation Eur J Neurosci 20 2004 1705 1712 (Pubitemid 39471563)
22. J.H. Jang, B.H. Lee, T.S. Nam, J.W. Kim, D.W. Kim, and J.W. Leem Peripheral contributions to the mechanical hyperalgesia following a lumbar 5 spinal nerve lesion in rats Neuroscience 165 2010 221 232
23. S.H. Kim, and J.M. Chung An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat Pain 50 1992 355 363
24. Y.J. Lee, O. Zachrisson, D.A. Tonge, and P.A. McNaughton Upregulation of bradykinin B2 receptor expression by neurotrophic factors and nerve injury in mouse sensory neurons Mol Cell Neurosci 19 2002 186 200 (Pubitemid 34211899)
25. Y. Li, M.J. Dorsi, R.A. Meyer, and A.J. Belzberg Mechanical hyperalgesia after an L5 spinal nerve lesion in the rat is not dependent on input from injured nerve fibers Pain 85 2000 493 502 (Pubitemid 30214178)
26. Y.S. Lyu, S.K. Park, K. Chung, and J.M. Chung Low dose of tetrodotoxin reduces neuropathic pain behaviors in an animal model Brain Res 871 2000 98 103 (Pubitemid 30406873)
27. M. Malcangio, S.J. Getting, J. Grist, J.R. Cunningham, E.J. Bradbury, P. Charbel Issa, I.J. Lever, S. Pezet, and M. Perretti A novel control mechanism based on GDNF modulation of somatostatin release from sensory neurones FASEB J 16 2002 730 732
28. S.A. Malin, D.C. Molliver, H.R. Koerber, P. Cornuet, R. Frye, K.M. Albers, and B.M. Davis Glial cell line-derived neurotrophic factor family members sensitize nociceptors in vitro and produce thermal hyperalgesia in vivo J Neurosci 26 2006 8588 8599 (Pubitemid 44316188)
29. J.L. McBride, S. Ramaswamy, M. Gasmi, R.T. Bartus, C.D. Herzog, E.P. Brandon, L. Zhou, M.R. Pitzer, E.M. Berry-Kravis, and J.H. Kordower Viral delivery of glial cell line-derived neurotrophic factor improves behavior and protects striatal neurons in a mouse model of Huntington's disease Proc Natl Acad Sci U S A 103 2006 9345 9350 (Pubitemid 43902579)
30. J. Nielsen, K. Gotfryd, S. Li, N. Kulahin, V. Soroka, K.K. Rasmussen, E. Bock, and V. Berezin Role of glial cell line-derived neurotrophic factor (GDNF)-neural cell adhesion molecule (NCAM) interactions in induction of neurite outgrowth and identification of a binding site for NCAM in the heel region of GDNF J Neurosci 29 2009 11360 11376
31. C. Nolte, M. Moos, and M. Schachner Immunolocalization of the neural cell adhesion molecule L1 in epithelia of rodents Cell Tissue Res 298 1999 261 273 (Pubitemid 29512078)
32. K. Obata, H. Yamanaka, T. Fukuoka, D. Yi, A. Tokunaga, N. Hashimoto, H. Yoshikawa, and K. Noguchi Contribution of injured and uninjured dorsal root ganglion neurons to pain behavior and the changes in gene expression following chronic constriction injury of the sciatic nerve in rats Pain 101 2003 65 77 (Pubitemid 36050112)
33. K. Ohta, T. Inokuchi, E. Gen, and J. Chang Ultrastructural study of anterograde transport of glial cell line-derived neurotrophic factor from dorsal root ganglion neurons of rats towards the nerve terminal Cells Tissues Organs 169 2001 410 421 (Pubitemid 32722262)
34. G. Paratcha, and F. Ledda GDNF and GFRα: A versatile molecular complex for developing neurons Trends Neurosci 31 2008 384 391
35. G. Paratcha, F. Ledda, and C.F. Ibáñez The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands Cell 113 2003 867 879 (Pubitemid 36792031)
36. S. Pezet, A. Krzyzanowska, L.F. Wong, J. Grist, N.D. Mazarakis, B. Georgievska, and S.B. McMahon Reversal of neurochemical changes and pain-related behavior in a model of neuropathic pain using modified lentiviral vectors expressing GDNF Mol Ther 13 2006 1101 1109 (Pubitemid 44207843)
37. D.S. Richardson, A.Z. Lai, and L.M. Mulligan RET ligand-induced internalization and its consequences for downstream signaling Oncogene 25 2006 3206 3211 (Pubitemid 43881561)
38. H.B. Rind, and C.S. von Bartheld Anterograde axonal transport of internalized GDNF in sensory and motor neurons Neuroreport 13 2002 659 664 (Pubitemid 34293487)
39. A. Sakai, M. Asada, N. Seno, and H. Suzuki Involvement of neural cell adhesion molecule signaling in glial cell line-derived neurotrophic factor-induced analgesia in a rat model of neuropathic pain Pain 137 2008 378 388 (Pubitemid 351853300)
40. G. Scherrer, N. Imamachi, Y.Q. Cao, C. Contet, F. Mennicken, D. O'Donnell, B.L. Kieffer, and A.I. Basbaum Dissociation of the opioid receptor mechanisms that control mechanical and heat pain Cell 137 2009 1148 1159
41. I. Sukhotinsky, E. Ben-Dor, P. Raber, and M. Devor Key role of the dorsal root ganglion in neuropathic tactile hypersensibility Eur J Pain 8 2004 135 143 (Pubitemid 38325883)
42. T. Sun, H.S. Xiao, P.B. Zhou, Y.J. Lu, L. Bao, and X. Zhang Differential expression of synaptoporin and synaptophysin in primary sensory neurons and up-regulation of synaptoporin after peripheral nerve injury Neuroscience 141 2006 1233 1245 (Pubitemid 44128686)
43. 4-saporin treatment in rat models of nociceptive and neuropathic pain Brain Res 1029 2004 65 76 (Pubitemid 39463308)
44. A.J. Todd Neuronal circuitry for pain processing in the dorsal horn Nat Rev Neurosci 11 2010 823 836
45. V. Vellani, O. Zachrisson, and P.A. McNaughton Functional bradykinin B1 receptors are expressed in nociceptive neurones and are upregulated by the neurotrophin GDNF J Physiol 560 2004 391 401 (Pubitemid 39440102)
46. R. Wang, W. Guo, M.H. Ossipov, T.W. Vanderah, F. Porreca, and J. Lai Glial cell line-derived neurotrophic factor normalizes neurochemical changes in injured dorsal root ganglion neurons and prevents the expression of experimental neuropathic pain Neuroscience 121 2003 815 824 (Pubitemid 38367518)
47. Wu G, Ringkamp M, Hartke TV, Murinson BB, Campbell JN, Griffin JW, Meyer RA: Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J Neurosci 21:140RC-2001
48. M. Zimmermann Ethical guidelines for investigations of experimental pain in conscious animals Pain 16 1983 109 110 (Pubitemid 13058546)
49. M. Zwick, B.M. Davis, C.J. Woodbury, J.N. Burkett, H.R. Koerber, J.F. Simpson, and K.M. Albers Glial cell line-derived neurotrophic factor is a survival factor for isolectin B4-positive, but not vanilloid receptor 1-positive, neurons in the mouse J Neurosci 22 2002 4057 4065 (Pubitemid 37465714)