Neuropathic pain- and glial derived neurotrophic factor-associated regulation of cadherins in spinal circuits of the dorsal horn

Pain

Volumn 152, Issue 4, 2011, Pages 924-935

  Patil, Shekhar B ^a   Brock, John H ^a,b   Colman, David R ^a,c   Huntley, George W ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

E cadherin; N cadherin; Nerve regeneration; Rat; Spinal nerve ligation; Synaptic plasticity

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NERVE CELL ADHESION MOLECULE; NEUROMODULIN; PROTEIN RET; UVOMORULIN;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ARTICLE; CONTROLLED STUDY; MALE; NERVE TRANSECTION; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD DORSAL HORN; SPINAL NERVE; SPINE INJURY;

ANIMALS; CADHERINS; DISEASE MODELS, ANIMAL; GAP-43 PROTEIN; GENE EXPRESSION REGULATION; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; HYPERALGESIA; MALE; NEURAL CELL ADHESION MOLECULES; NEURALGIA; PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS C-RET; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SPINAL CORD INJURIES; TIME FACTORS;

EID: 79953033696     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2011.01.017     Document Type: Article

References (99)

1. M.S. Airaksinen, and M. Saarma The GDNF family: signalling, biological functions and therapeutic value Nat Rev 3 2002 383 394 (Pubitemid 135706635)
2. J. Anders, S. Kjar, and C.F. Ibanez Molecular modeling of the extracellular domain of the RET receptor tyrosine kinase reveals multiple cadherin-like domains and a calcium-binding site J Biol Chem 276 2001 35808 35817
3. J. Arikkath, and L.F. Reichardt Cadherins and catenins at synapses: roles in synaptogenesis and synaptic plasticity Trends Neurosci 31 2008 487 494
4. J. Arvidsson, and K. Pfaller Central projections of C4-C8 dorsal root ganglia in the rat studied by anterograde transport of WGA-HRP J Comp Neurol 292 1990 349 362 (Pubitemid 20061570)
5. S. Averill, S.B. McMahon, D.O. Clary, L.F. Reichardt, and J.V. Priestley Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons Eur J Neurosci 19 2004 1437 1445
6. 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)
7. A.W. Barritt, M. Davies, F. Marchand, R. Hartley, J. Grist, P. Yip, S.B. McMahon, and E.J. Bradbury Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury J Neurosci 26 2006 10856 10867
8. I.A. Belyantseva, and G.R. Lewin Stability and plasticity of primary afferent projections following nerve regeneration and central degeneration Eur J Neurosci 11 1999 457 468 (Pubitemid 29050448)
9. D.L. Bennett Neurotrophic factors: important regulators of nociceptive function Neuroscientist 7 2001 13 17 (Pubitemid 32098819)
10. D.L. 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)
11. D.L. 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)
12. L.I. Benowitz, and A. Routtenberg GAP-43: an intrinsic determinant of neuronal development and plasticity Trends Neurosci 20 1997 84 91 (Pubitemid 27050703)
13. D.L. Benson, and H. Tanaka N-cadherin redistribution during synaptogenesis in hippocampal neurons J Neurosci 18 1998 6892 6904 (Pubitemid 28388019)
14. J.L. Bixby, and R. Zhang Purified N-cadherin is a potent substrate for the rapid induction of neurite outgrowth J Cell Biol 110 1990 1253 1260
15. F.G. Bottone Jr., Y. Moon, J.S. Kim, B. Alston-Mills, M. Ishibashi, and T.E. Eling The anti-invasive activity of cyclooxygenase inhibitors is regulated by the transcription factor ATF3 (activating transcription factor 3) Mol Can Ther 4 2005 693 703 (Pubitemid 40767113)
16. T.J. Boucher, K. Okuse, D.L. 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
17. O. Bozdagi, W. Shan, H. Tanaka, D.L. Benson, and G.W. Huntley Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation Neuron 28 2000 245 259
18. O. Bozdagi, M. Valcin, K. Poskanzer, H. Tanaka, and D.L. Benson Temporally distinct demands for classic cadherins in synapse formation and maturation Mol Cel Neurosci 27 2004 509 521 (Pubitemid 39540004)
19. J.H. Brock, A. Elste, and G.W. Huntley Distribution and injury-induced plasticity of cadherins in relationship to identified synaptic circuitry in adult rat spinal cord J Neurosci 24 2004 8806 8817 (Pubitemid 39362975)
20. J.M. Castro-Lopes, A. Coimbra, G. Grant, and J. Arvidsson Ultrastructural changes of the central scalloped (C1) primary afferent endings of synaptic glomeruli in the substantia gelatinosa Rolandi of the rat after peripheral neurotomy J Neurocytol 19 1990 329 337 (Pubitemid 20222708)
21. S.R. Chaplan, F.W. Bach, J.W. Pogrel, J.M. Chung, and T.L. Yaksh Quantitative assessment of tactile allodynia in the rat paw J Neurosci Methods 53 1994 55 63 (Pubitemid 24238751)
22. M.S. Chong, M.L. Reynolds, N. Irwin, R.E. Coggeshall, P.C. Emson, L.I. Benowitz, and C.J. Woolf GAP-43 expression in primary sensory neurons following central axotomy J Neurosci 14 1994 4375 4384 (Pubitemid 24200559)
23. R.E. Coggeshall, M.L. Reynolds, and C.J. Woolf Distribution of the growth associated protein GAP-43 in the central processes of axotomized primary afferents in the adult rat spinal cord; presence of growth cone-like structures Neurosci Lett 131 1991 37 41
24. F. Coussen, E. Normand, C. Marchal, P. Costet, D. Choquet, M. Lambert, R.M. Mege, and C. Mulle Recruitment of the kainate receptor subunit glutamate receptor 6 by cadherin/catenin complexes J Neurosci 22 2002 6426 6436 (Pubitemid 35386399)
25. B. Csillik, and E. Knyihar Degenerative atrophy and regenerative proliferation in the rat spinal cord Z Mikrosk Anat Forsch 89 1975 1099 1103
26. W.J. Dixon Efficient analysis of experimental observations Annu Rev Pharmacol Toxicol 20 1980 441 462
27. P. Doherty, L.H. Rowett, S.E. Moore, D.A. Mann, and F.S. Walsh Neurite outgrowth in response to transfected N-CAM and N-cadherin reveals fundamental differences in neuronal responsiveness to CAMs Neuron 6 1991 247 258
28. T.P. Doubell, and C.J. Woolf Growth-associated protein 43 immunoreactivity in the superficial dorsal horn of the rat spinal cord is localized in atrophic C-fiber, and not in sprouted A-fiber, central terminals after peripheral nerve injury J Comp Neurol 386 1997 111 118 (Pubitemid 27392145)
29. P. Durbec, C.V. Marcos-Gutierrez, C. Kilkenny, M. Grigoriou, K. Wartiowaara, P. Suvanto, D. Smith, B. Ponder, F. Costantini, M. Saarma, H. Sariola, and V. Pachnis GDNF signalling through the Ret receptor tyrosine kinase Nature 381 1996 789 793 (Pubitemid 26243119)
30. H. Enomoto, T. Araki, A. Jackman, R.O. Heuckeroth, W.D. Snider, E.M. Johnson Jr., and J. Milbrandt GFR alpha1-deficient mice have deficits in the enteric nervous system and kidneys Neuron 21 1998 317 324 (Pubitemid 28399692)
31. E.M. Garry, and S.M. Fleetwood-Walker A new view on how AMPA receptors and their interacting proteins mediate neuropathic pain Pain 109 2004 210 213 (Pubitemid 38638696)
32. C.G. Hahn, and J. Covault Neural regulation of N-cadherin gene expression in developing and adult skeletal muscle J Neurosci 12 1992 4677 4687
33. D.L. Hammond, L. Ackerman, R. Holdsworth, and B. Elzey Effects of spinal nerve ligation on immunohistochemically identified neurons in the L4 and L5 dorsal root ganglia of the rat J Comp Neurol 475 2004 575 589 (Pubitemid 38859367)
34. P. Honore, S.D. Rogers, M.J. Schwei, J.L. Salak-Johnson, N.M. Luger, M.C. Sabino, D.R. Clohisy, and P.W. Mantyh Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons Neuroscience 98 2000 585 598 (Pubitemid 30408178)
35. 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)
36. S.P. Hunt, and P.W. Mantyh The molecular dynamics of pain control Nat Rev 2 2001 83 91 (Pubitemid 33673362)
37. G.W. Huntley Dynamic aspects of cadherin-mediated adhesion in synapse development and plasticity Biol Cell 94 2002 335 344 (Pubitemid 35407395)
38. G.W. Huntley, D.L. Benson, and D.R. Colman Structural remodeling of the synapse in response to physiological activity Cell 108 2002 1 4 (Pubitemid 34137005)
39. G.W. Huntley, A.M. Elste, S.B. Patil, O. Bozdagi, D.L. Benson, and O. Steward Synaptic loss and retention of different classic cadherins with LTP-associated synaptic structural remodeling in vivo Hippocampus 2010 10.1002/hipo.2085 [Epub ahead of print]
40. H. Husi, M.A. Ward, J.S. Choudhary, W.P. Blackstock, and S.G. Grant Proteomic analysis of NMDA receptor-adhesion protein signaling complexes Nat Neurosci 3 2000 661 669 (Pubitemid 30437200)
41. K. Itoh, M. Ozaki, B. Stevens, and R.D. Fields Activity-dependent regulation of N-cadherin in DRG neurons: differential regulation of N-cadherin, NCAM, and L1 by distinct patterns of action potentials J Neurobiol 33 1997 735 748 (Pubitemid 27465581)
42. J.D. Jontes, M.R. Emond, and S.J. Smith In vivo trafficking and targeting of N-cadherin to nascent presynaptic terminals J Neurosci 24 2004 9027 9034 (Pubitemid 39372247)
43. K. Jungling, V. Eulenburg, R. Moore, R. Kemler, V. Lessmann, and K. Gottmann N-cadherin transsynaptically regulates short-term plasticity at glutamatergic synapses in embryonic stem cell-derived neurons J Neurosci 26 2006 6968 6978 (Pubitemid 44309864)
44. A. Kalous, P.B. Osborne, and J.R. Keast Acute and chronic changes in dorsal horn innervation by primary afferents and descending supraspinal pathways after spinal cord injury J Comp Neurol 504 2007 238 253 (Pubitemid 350012211)
45. S.E. Kapadia, and C.C. LaMotte Deafferentation-induced alterations in the rat dorsal horn: I. Comparison of peripheral nerve injury vs. rhizotomy effects on presynaptic, postsynaptic, and glial processes J Comp Neurol 266 1987 183 197 (Pubitemid 18021934)
46. 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
47. W.S. Kingery, and J.A. Vallin The development of chronic mechanical hyperalgesia, autotomy and collateral sprouting following sciatic nerve section in rat Pain 38 1989 321 332 (Pubitemid 19251255)
48. P.D. Kitchener, M.D. Lapiz, P. Wilson, and P.J. Snow Transganglionic labelling of primary sensory afferents in the rat lumbar spinal cord: comparison between wheatgerm agglutinin and the I-B4 isolectin from Bandeiraea simplicifolia J Neurocytol 23 1994 745 757
49. S. Kjaer, and C.F. Ibanez Identification of a surface for binding to the GDNF-GFR alpha 1 complex in the first cadherin-like domain of RET J Biol Chem 278 2003 47898 47904 (Pubitemid 37523238)
50. E. Knyihar, and B. Csillik Effect of peripheral anatomy on the fine structure and histochemistry of the Rolando substance: degenerative atrophy of central processes of pseudounipolar cells Exp Br Res Exp Hirnf 26 1976 73 87
51. E. Knyihar-Csillik, B. Csillik, and A.B. Oestreicher Light and electron microscopic localization of B-50 (GAP43) in the rat spinal cord during transganglionic degenerative atrophy and regeneration J Neurosci Res 32 1992 93 109
52. A. Latremoliere, and C.J. Woolf Central sensitization: a generator of pain hypersensitivity by central neural plasticity J Pain 10 2009 895 926
53. F. Ledda, G. Paratcha, T. Sandoval-Guzman, and C.F. Ibanez GDNF and GFRalpha1 promote formation of neuronal synapses by ligand-induced cell adhesion Nat Neurosci 10 2007 293 300
54. H.A. Lekan, K. Chung, Y.W. Yoon, J.M. Chung, and R.E. Coggeshall Loss of dorsal root ganglion cells concomitant with dorsal root axon sprouting following segmental nerve lesions Neurosci 81 1997 527 534 (Pubitemid 27382005)
55. 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)
56. C.N. Liu, P.D. Wall, E. Ben-Dor, M. Michaelis, R. Amir, and M. Devor Tactile allodynia in the absence of C-fiber activation: altered firing properties of DRG neurons following spinal nerve injury Pain 85 2000 503 521 (Pubitemid 30214179)
57. X. Liu, S. Eschenfelder, K.H. Blenk, W. Janig, and H. Habler Spontaneous activity of axotomized afferent neurons after L5 spinal nerve injury in rats Pain 84 2000 309 318 (Pubitemid 30074233)
58. A.B. Malmberg, C. Chen, S. Tonegawa, and A.I. Basbaum Preserved acute pain and reduced neuropathic pain in mice lacking PKCgamma Science 278 1997 279 283 (Pubitemid 27450873)
59. J. Mao, D.D. Price, L.L. Phillips, J. Lu, and D.J. Mayer Increases in protein kinase C gamma immunoreactivity in the spinal cord dorsal horn of rats with painful mononeuropathy Neurosci Lett 198 1995 75 78
60. W.J. Martin, H. Liu, H. Wang, A.B. Malmberg, and A.I. Basbaum Inflammation-induced up-regulation of protein kinase C gamma immunoreactivity in rat spinal cord correlates with enhanced nociceptive processing Neuroscience 88 1999 1267 1274 (Pubitemid 28547003)
61. H. Marzban, R.V. Sillitoe, M. Hoy, S.H. Chung, V.F. Rafuse, and R. Hawkes Abnormal HNK-1 expression in the cerebellum of an N-CAM null mouse J Neurocytol 33 2004 117 130 (Pubitemid 38860223)
62. E. Mazzoni, A. Adam, E. Bal de Kier Joffe, and J.A. Aguirre-Ghiso Immortalized mammary epithelial cells overexpressing protein kinase C gamma acquire a malignant phenotype and become tumorigenic in vivo Mol Can Res 1 2003 776 787 (Pubitemid 37025596)
63. C. Molander, H.F. Wang, C. Rivero-Melian, and G. Grant Early decline and late restoration of spinal cord binding and transganglionic transport of isolectin B4 from Griffonia simplicifolia I after peripheral nerve transection and crush Restor Neurol Neuro 10 1996 123 133 (Pubitemid 26423616)
64. J.B. Munson, and S.B. McMahon Effects of GDNF on axotomized sensory and motor neurons in adult rats Eur J Neurosci 9 1997 1126 1129 (Pubitemid 27260739)
65. S.P. Mysore, C.Y. Tai, and E.M. Schuman Effects of N-cadherin disruption on spine morphological dynamics Front Cell Neurosci 1 2007 1 14
66. S. Neumann, J.M. Braz, K. Skinner, I.J. Llewellyn-Smith, and A.I. Basbaum Innocuous, not noxious, input activates PKCgamma interneurons of the spinal dorsal horn via myelinated afferent fibers J Neurosci 28 2008 7936 7944
67. M. Nuriya, and R.L. Huganir Regulation of AMPA receptor trafficking by N-cadherin J Neurochem 97 2006 652 661
68. T. Okuda, L.M. Yu, L.A. Cingolani, R. Kemler, and Y. Goda Beta-catenin regulates excitatory postsynaptic strength at hippocampal synapses Proc Natl Acad Sci USA 104 2007 13479 13484 (Pubitemid 47293970)
69. G. Paratcha, F. Ledda, and C.F. Ibanez The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands Cell 113 2003 867 879 (Pubitemid 36792031)
70. G.R. Phillips, L. Florens, H. Tanaka, Z.Z. Khaing, L. Fidler, J.R. Yates 3rd, and D.R. Colman Proteomic comparison of two fractions derived from the transsynaptic scaffold J Neurosci Res 81 2005 762 775 (Pubitemid 41532142)
71. E. Polgar, J.H. Fowler, M.M. McGill, and A.J. Todd The types of neuron which contain protein kinase C gamma in rat spinal cord Brain Res 833 1999 71 80 (Pubitemid 29336146)
72. E. Polgar, and A.J. Todd Tactile allodynia can occur in the spared nerve injury model in the rat without selective loss of GABA or GABA(A) receptors from synapses in laminae I-II of the ipsilateral spinal dorsal horn Neuroscience 156 2008 193 202
73. O. Raineteau, and M.E. Schwab Plasticity of motor systems after incomplete spinal cord injury Nature Rev 2 2001 263 273 (Pubitemid 33673067)
74. A. Ribeiro-da-Silva, and A. Coimbra Two types of synaptic glomeruli and their distribution in laminae I-III of the rat spinal cord J Comp Neurol 209 1982 176 186 (Pubitemid 12069045)
75. L. Saglietti, C. Dequidt, K. Kamieniarz, M.C. Rousset, P. Valnegri, O. Thoumine, F. Beretta, L. Fagni, D. Choquet, C. Sala, M. Sheng, and M. Passafaro Extracellular interactions between GluR2 and N-cadherin in spine regulation Neuron 54 2007 461 477 (Pubitemid 46659810)
76. 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)
77. D. Schoffnegger, R. Ruscheweyh, and J. Sandkuhler Spread of excitation across modality borders in spinal dorsal horn of neuropathic rats Pain 135 2008 300 310
78. A. Seto, M. Hasegawa, N. Uchiyama, T. Yamashima, and J. Yamashita Alteration of E-cadherin and alpha N-catenin immunoreactivity in the mouse spinal cord following peripheral axotomy J Neuropathol Exp Neurol 56 1997 1182 1190 (Pubitemid 27492774)
79. W. Shan, M. Yoshida, X.R. Wu, G.W. Huntley, and D.R. Colman Neural (N-) cadherin, a synaptic adhesion molecule, is induced in hippocampal mossy fiber axonal sprouts by seizure J Neurosci Res 69 2002 292 304 (Pubitemid 34809479)
80. S.A. Shehab, K. Al-Marashda, A. Al-Zahmi, A. Abdul-Kareem, and M.A. Al-Sultan Unmyelinated primary afferents from adjacent spinal nerves intermingle in the spinal dorsal horn: a possible mechanism contributing to neuropathic pain Brain Res 1208 2008 111 119
81. K. Shimamura, T. Takahashi, and M. Takeichi E-cadherin expression in a particular subset of sensory neurons Dev Biol 152 1992 242 254
82. J.B. Silverman, S. Restituito, W. Lu, L. Lee-Edwards, L. Khatri, and E.B. Ziff Synaptic anchorage of AMPA receptors by cadherins through neural plakophilin-related arm protein AMPA receptor-binding protein complexes J Neurosci 27 2007 8505 8516 (Pubitemid 47254250)
83. J.D. Silverman, and L. Kruger Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: relation of lectin reactivity to peptide and enzyme markers J Neurocytol 19 1990 789 801 (Pubitemid 20378878)
84. W.D. Snider, and S.B. McMahon Tackling pain at the source: new ideas about nociceptors Neuron 20 1998 629 632 (Pubitemid 28199043)
85. L.S. Stewart, and W.J. Martin Influence of postoperative analgesics on the development of neuropathic pain in rats Comp Med 53 2003 29 36 (Pubitemid 36323511)
86. S.C. Suzuki, H. Furue, K. Koga, N. Jiang, M. Nohmi, Y. Shimazaki, Y. Katoh-Fukui, M. Yokoyama, M. Yoshimura, and M. Takeichi Cadherin-8 is required for the first relay synapses to receive functional inputs from primary sensory afferents for cold sensation J Neurosci 27 2007 3466 3476 (Pubitemid 46515127)
87. C.Y. Tai, S.P. Mysore, C. Chiu, and E.M. Schuman Activity-regulated N-cadherin endocytosis Neuron 54 2007 771 785 (Pubitemid 46843522)
88. A.M. Tan, S. Stamboulian, Y.W. Chang, P. Zhao, A.B. Hains, S.G. Waxman, and B.C. Hains Neuropathic pain memory is maintained by Rac1-regulated dendritic spine remodeling after spinal cord injury J Neurosci 28 2008 13173 13183
89. H. Tanaka, W. Shan, G.R. Phillips, K. Arndt, O. Bozdagi, L. Shapiro, G.W. Huntley, D.L. Benson, and D.R. Colman Molecular modification of N-cadherin in response to synaptic activity Neuron 25 2000 93 107 (Pubitemid 30316513)
90. J.W. Tarpley, M.G. Kohler, and W.J. Martin The behavioral and neuroanatomical effects of IB4-saporin treatment in rat models of nociceptive and neuropathic pain Brain Res 1029 2004 65 76 (Pubitemid 39463308)
91. H. Togashi, K. Abe, A. Mizoguchi, K. Takaoka, O. Chisaka, and M. Takeichi Cadherin regulates dendritic spine morphogenesis Neuron 35 2002 77 89 (Pubitemid 34804324)
92. M. Trupp, E. Arenas, M. Fainzilber, A.S. Nilsson, B.A. Sieber, M. Grigoriou, C. Kilkenny, E. Salazar-Grueso, V. Pachnis, and U. Arumae Functional receptor for GDNF encoded by the c-ret proto-oncogene Nature 381 1996 785 789 (Pubitemid 26243118)
93. M. Tsuda, K. Inoue, and M.W. Salter Neuropathic pain and spinal microglia: a big problem from molecules in "small" glia Trends Neurosci 28 2005 101 107 (Pubitemid 40178927)
94. H. Tsujino, E. Kondo, T. Fukuoka, Y. Dai, A. Tokunaga, K. Miki, K. Yonenobu, T. Ochi, and K. Noguchi Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury Mol Cel Neurosci 15 2000 170 182 (Pubitemid 30109120)
95. L. Vulchanova, T.H. Olson, L.S. Stone, M.S. Riedl, R. Elde, and C.N. Honda Cytotoxic targeting of isolectin IB4-binding sensory neurons Neuroscience 108 2001 143 155 (Pubitemid 33152988)
96. 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)
97. S. Wang, G. Lim, Q. Zeng, B. Sung, Y. Ai, G. Guo, L. Yang, and J. Mao Expression of central glucocorticoid receptors after peripheral nerve injury contributes to neuropathic pain behaviors in rats J Neurosci 24 2004 8595 8605 (Pubitemid 39313782)
98. W. Wang, Y. Wang, J. Huang, S. Wu, and Y.Q. Li Temporal changes of astrocyte activation and glutamate transporter-1 expression in the spinal cord after spinal nerve ligation-induced neuropathic pain Anat Rec 291 2008 513 518 (Pubitemid 351644525)
99. C.J. Woolf, M.L. Reynolds, C. Molander, C. O'Brien, R.M. Lindsay, and L.I. Benowitz The growth-associated protein GAP-43 appears in dorsal root ganglion cells and in the dorsal horn of the rat spinal cord after peripheral nerve injury Neuroscience 34 1990 465 478 (Pubitemid 20110151)