Glial cell line-derived neurotrophic factor increases calcitonin gene-related peptide immunoreactivity in sensory and motoneurons in vivo

European Journal of Neuroscience

Volumn 18, Issue 10, 2003, Pages 2713-2721

  Ramer, Matt S ^a,c   Bradbury, Elizabeth J ^a   Michael, Gregory J ^b   Lever, Isobel J ^a   McMahon, Stephen B ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Dorsal root ganglion; Endplate; Pain; Rat; Spinal cord

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; IN VIVO STUDY; MALE; MOTONEURON; NERVE CELL PLASTICITY; NERVE FIBER REGENERATION; NOCICEPTION; NONHUMAN; PAIN THRESHOLD; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPINAL CORD NERVE CELL; SPINAL GANGLION; TARGET CELL; VASODILATATION;

ANIMALS; ANTERIOR HORN CELLS; CALCITONIN GENE-RELATED PEPTIDE; CARRIER PROTEINS; CELL COUNT; GENE EXPRESSION REGULATION; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MEMBRANE PROTEINS; NERVE GROWTH FACTOR; NERVE GROWTH FACTORS; PAIN MEASUREMENT; PAIN THRESHOLD; POSTERIOR HORN CELLS; RATS; RATS, WISTAR; REACTION TIME; RECEPTOR, TRKA; SPINAL CORD;

EID: 0348011932     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2003.03012.x     Document Type: Article

References (56)

1. Amara, S.G., Arriza, J.L., Leff, S.E., Swanson, L.W., Evans, R.M. & Rosenfeld. M.G. (1985) Expression in brain of a messenger RNA encoding a novel neuropeptide homologous to calcitonin gene-related peptide. Science, 229, 1094-1097.
2. Arvidsson, U., Johnson, H., Piehl, F., Cullheim, S., Hokfelt, T., Risling, M., Terenius, L. & Ulfhake, B. (1990) Peripheral nerve section induces increased levels of calcitonin gene-related peptide (CGRP)-like immunoreactivity in axotomized motoneurons. Exp. Brain Res., 79, 212-216.
3. Bennett, D.L., Michael, G.J., Ramachandran, N., Munson, J.B., Averill, S., Yan, Q., McMahon, S.B. & Priestley, J.V. (1998) A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J. Neurosci., 18, 3059-3072.
4. Blanco, C.E., Popper, P. & Micevych, P. (1997) Alpha-CGRP mRNA levels in motoneurons innervating specific rat muscles. Brain Res. Mol. Brain Res., 44, 253-261.
5. Blesch, A. & Tuszynski, M.H. (2001) GDNF gene delivery to injured adult CNS motor neurons promotes axonal growth, expression of the trophic neuropeptide CGRP, and cellular protection. J. Comp. Neurol., 436, 399-410.
6. Boucher, T.J., Okuse, K., Bennett, D.L., Munson, J.B., Wood, J.N. & McMahon, S.B. (2000) Potent analgesic effects of GDNF in neuropathic pain states. Science, 290, 124-127.
7. Bradbury, E.J., Burnstock, G. & McMahon, S.B. (1998) The expression of P2X3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mol. Cell Neurosci., 12, 256-268.
8. Brain, S.D., Williams, T.J., Tippins, J.R., Morris, H.R. & MacIntyre, I. (1985) Calcitonin gene-related peptide is a potent vasodilator. Nature, 313, 54-56.
9. Brushart, T.M., Hoffman, P.N., Royall, R.M., Murinson, B.B., Witzel, C. & Gordon, T. (2002) Electrical stimulation promotes motoneuron regeneration without increasing its speed or conditioning the neuron. J. Neurosci., 22, 6631-6638.
10. Fang, M., Wang, Y., He, Q.H., Sun, Y.X., Deng, L.B., Wang, X.M. & Han, J.S. (2003) Glial cell line-derived neurotrophic factor contributes to delayed inflammatory hyperalgesia in adjuvant rat pain model. Neuroscience, 117, 503-512.
11. Fontaine, B., Klarsfeld, A., Hokfelt, T. & Changeux, J.P. (1986) Calcitonin gene-related peptide, a peptide present in spinal cord motoneurons, increases the number of acetylcholine receptors in primary cultures of chick embryo myotubes. Neurosci. Lett., 71, 59-65.
12. Fontaine, B., Klarsfeld, A. & Changeux, J.P. (1987) Calcitonin gene-related peptide and muscle activity regulate acetylcholine receptor alpha-subunit mRNA levels by distinct intracellular pathways. J. Cell Biol., 105, 1337-1342.
13. Fukuoka, T., Tokunaga, A., Kondo, E., Miki, K., Tachibana, T. & Noguchi, K. (1999) Differential regulation of alpha-and beta-CGRP mRNAs within oculomotor, trochlear, abducens, and trigeminal motoneurons in response to axotomy. Brain Res. Mol. Brain Res., 63, 304-315.
14. Gharakhanlou, R., Chadan, S. & Gardiner, P. (1999) Increased activity in the form of endurance training increases calcitonin gene-related peptide content in lumbar motoneuron cell bodies and in sciatic nerve in the rat. Neuroscience, 89, 1229-1239.
15. Gibson, S.J., Polak, J.M., Bloom, S.R., Sabate, I.M., Mulderry, P.M., Ghatei, M.A., McGregor, G.P., Morrison, J.F., Kelly, J.S. & Evans, R.M. (1984) Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J. Neurosci., 4, 3101-3111.
16. Gonzalez-Forero, D., De La Cruz, R.R., Delgado-Garcia, J.M., Alvarez, F.J. & Pastor, A.M. (2002) Correlation between CGRP immunoreactivity and firing activity in cat abducens motoneurons. J. Comp. Neurol., 451, 201-212.
17. Hassan, S.M., Jennekens, F.G., Wieneke, G. & Veldman, H. (1994) Calcitonin gene-related peptide-like immunoreactivity, in botulinum toxin-paralysed rat muscles. Neuromuscul. Disord., 4, 489-496.
18. Henderson, C.E., Phillips, U.S., Pollock, R.A., Davies, A.M., Lemeulle, C., Armanini, M., Simmons, L., Moffet, B., Vandlen, R.A. & Simpson, L.C. (1994) GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science, 266, 1062-1064.
19. Hiruma, H., Saito, A., Ichikawa, T., Kiriyama, Y., Hoka, S., Kusakabe, T., Kobayashi, H. & Kawakami, T. (2000) Effects of substance P and calcitonin gene-related peptide on axonal transport in isolated and cultured adult mouse dorsal root ganglion neurons. Brain Res., 883, 184-191.
20. Iwakawa, M., Mizoi, K., Tessler, A. & Itoh, Y. (2001) Intraspinal implants of fibrin glue containing glial cell line-derived neurotrophic factor promote dorsal root regeneration into spinal cord. Neurorehabil. Neural Repair, 15, 173-182.
21. Jing, S., Wen, D., Yu, Y., Holst, P.L., Luo, Y., Fang, M., Tamir, R., Antonio, L., Hu, Z., Cupples, R., Louis, J.C., Hu, S., Altrock, B.W. & Fox, G.M. (1996) GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF. Cell, 85, 1113-1124.
22. Keller-Peck, C.R., Feng, G., Sanes, J.R., Yan, Q., Lichtman, J.W. & Shider, W.D. (2001) Glial cell line derived neurotrophic factor administration in postnatal life results in motor unit enlargement and continuous synaptic remodeling at the neuromuscular junction. J. Neurosci., 21, 6136-6146.
23. Lever, I.J., Bradbury, E.J., Cunningham, J.R., Adelson, D.W., Jones, M.G., McMahon, S.B., Marvizon, J.C. & Malcangio, M. (2001) Brain-derived neurotrophic factor is released in the dorsal horn by distinctive patterns of afferent fiber stimulation. J. Neurosci., 21, 4469-4477.
24. Ma, W. & Bisby, M.A. (1998) Increase of calcitonin gene-related peptide immunoreactivity in the axonal fibers of the gracile nuclei of adult and aged rats after complete and partial sciatic nerve injuries. Exp. Neurol., 152, 137-149.
25. Malcangio, M., Ramer, M.S., Boucher, T.J. & McMahon, S.B. (2000) Intrathecally injected neurotrophins and the release of substance P from the rat isolated spinal cord. Eur. J. Neurosci., 12, 139-144.
26. Mason, R.T., Peterfreund, R.A., Sawchenko, P.E., Corrigan, A.Z., Rivier, J.E. & Vale, W.W. (1984) Release of the predicted calcitonin gene-related peptide from cultured rat trigeminal ganglion cells. Nature, 308, 653-655.
27. McMahon, S.B., Bennett, D.L., Priestley, J.V. & Shelton, D.L. (1995) The biological effects of endogenous nerve growth factor on adult sensory neurons revealed by a trkA-IgG fusion molecule. Nature Med., 1, 774-780.
28. Michael, G.J. & Priestley, J.V. (1996a) Combined immunocytochemistry and in situ hybridization. In Hendderson, Z. (Ed.), In situ Hybridization Techniques for the Brain. Wiley, Chichester, pp. 111-118.
29. Michael, G.J. & Priestley, J.V. (1996b) Expression of trkA and p75 nerve growth factor receptors in the adrenal gland. Neuroreport, 7, 1617-1622.
30. Michael, G.J., Averill, S., Nitkunan, A., Rattray, M., Bennett, D.L., Yan, Q. & Priestley, J.V. (1997a) Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J. Neurosci., 17, 8476-8490.
31. Michael, G.J., Kaya, E., Averill, S., Rattray, M., Clary, D.O. & Priestley, J.V. (1997b) TrkA immunoreactive neurones in the rat spinal cord. J. Comp. Neurol., 385, 441-455.
32. Miki, K., Fukuoka, T., Tokunaga, A. & Noguchi, K. (1998) Calcitonin gene-related peptide increase in the rat spinal dorsal horn and dorsal column nucleus following peripheral nerve injury: up-regulation in a subpopulation of primary afferent sensory neurons. Neuroscience, 82, 1243-1252.
33. Molliver, D.C., Wright, D.E., Leitner, M.L., Parsadanian, A.S., Doster, K., Wen, D., Yan, Q. & Snider, W.D. (1997) IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron, 19, 849-861.
34. Munson, J.B. & McMahon, S.B. (1997) Effects of GDNF on axotomized sensory and motor neurons in adult rats. Eur. J. Neurosci., 9, 1126-1129.
35. Nguyen, Q.T., Parsadanian, A.S., Snider, W.D. & Lichtman, J.W. (1998) Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. Science, 279, 1725-1729.
36. Noguchi, K., Senba, E., Morita, Y., Sato, M. & Tohyama, M. (1990) Alpha-CGRP and beta-CGRP mRNAs are differentially regulated in the rat spinal cord and dorsal root ganglion. Brain Res. Mol. Brain Res., 7, 299-304.
37. Nyberg, F., Le Greves, P. & Terenius, L. (1988) Modulation of endopeptidase activity by calcitonin gene related peptide: a mechanism affecting substance P action? Biochimie, 70, 65-68.
38. Ogun-Muyiwa, P., Helliwell, R., McIntyre, P. & Winter, J. (1999) Glial cell line derived neurotrophic factor (GDNF) regulates VR1 and substance P in cultured sensory neurons. Neuroreport, 10, 2107-2111.
39. Oppenheim, R.W., Houenou, L.J., Johnson, J.E., Lin, L.F., Li, L., Lo, A.C., Newsome. A.L., Prevette, D.M. & Wang, S. (1995) Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature, 373, 344-346.
40. Piehl, F., Arvidsson, U., Hokfelt, T. & Cullheim, S. (1993) Calcitonin gene-related peptide-like immunoreactivity in motoneuron pools innervating different hind limb muscles in the rat. Exp. Brain Res., 96, 291-303.
41. Ramer, M.S., Priestley, J.V. & McMahon, S.B. (2000) Functional regeneration of sensory axons into the adult spinal cord. Nature, 403, 312-316.
42. Ramer, M.S., Bradbury, E.J. & McMahon, S.B. (2001) Nerve growth factor induces P2X(3) expression in sensory neurons. J. Neurochem., 77, 864-875.
43. Rose, R.D. & Rohrlich, D. (1988) Counting sectioned cells via mathematical reconstruction. J. Comp. Neurol., 272, 365-386.
44. Rosenfeld, M.G., Mermod, J.J., Amara, S.G., Swanson, L.W., Sawchenko, P.E., Rivier, J., Vale, W.W. & Evans, R.M. (1983) Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Nature, 304, 129-135.
45. Sala, C., Andreose, J.S., Fumagalli, G. & Lomo, T. (1995) Calcitonin gene-related peptide: possible role in formation and maintenance of neuromuscular junctions. J. Neurosci., 15, 520-528.
46. Stucky, C.L. & Lewin, G.R. (1999) Isolectin B(4)-positive and -negative nociceptors are functionally distinct. J. Neurosci., 19, 6497-6505.
47. Takami, K., Hashimoto, K., Uchida, S., Tohyama, M. & Yoshida, H. (1986) Effect of calcitonin gene-related peptide on the cyclic AMP level of isolated mouse diaphragm. Jpn J. Pharmacol., 42, 345-350.
48. Tarabal, O., Caldero, J., Ribera, J., Sorribas, A., Lopez, R., Molgo, J. & Esquerda, J.E. (1996a) Regulation of motoneuronal calcitonin gene-related peptide (CGRP) during axonal growth and neuromuscular synaptic plasticity induced by botulinum toxin in rats. Eur. J. Neurosci., 8, 829-836.
49. Tarabal, O., Caldero, J. & Esquerda, J.E. (1996b) Intramuscular nerve sprouting induced by CNTF is associated with increases in CGRP content in mouse motor nerve terminals. Neurosci. Lett., 219, 60-64.
50. Trupp, M., Arenas, E., Fainzilber, M., Nilsson, A.S., Sieber, B.A., Grigoriou, M., Kilkenny, C., Salazar-Grueso, E., Pachnis, V. & Arumae, U. (1996) Functional receptor for GDNF encoded by the c-ret proto-oncogene. Nature, 381, 785-789.
51. Trupp, M., Belluardo, N., Funakoshi, H. & Ibanez, C.F. (1997) Complementary and overlapping expression of glial cell line-derived neurotrophic factor (GDNF), c-ret proto-oncogene, and GDNF receptor-alpha indicates multiple mechanisms of trophic actions in the adult rat CNS. J. Neurosci., 17, 3554-3567.
52. Verge, V.M., Richardson, P.M., Wiesenfeld-Hallin, Z. & Hokfelt, T. (1995) Differential influence of nerve growth factor on neuropeptide expression in vivo: a novel role in peptide suppression in adult sensory neurons. J. Neurosci., 15, 2081-2096.
53. Verge, V.M., Riopelle, R.J. & Richardson, P.M. (1989) Nerve growth factor receptors on normal and injured sensory neurons. J. Neurosci., 9, 914-922.
54. Vulchanova, L., Riedl, M.S., Shuster, S.J., Stone, L.S., Hargreaves, K.M., Buell, G., Surprenant, A., North, R.A. & Elde, R. (1998) P2X3 is expressed by DRG neurons that terminate in inner lamina II. Eur. J. Neurosci., 10, 3470-3478.
55. Wiesenfeld-Hallin, Z., Hokfelt, T., Lundberg, J.M., Forssmann, W.G., Reinecke, M., Tschopp, F.A. & Fischer, J.A. (1984) Immunoreactive calcitonin gene-related peptide and substance P coexist in sensory neurons to the spinal cord and interact in spinal behavioral responses of the rat. Neurosci. Lett., 52, 199-204.
56. Woolf, C. & Wiesenfeld-Hallin, Z. (1986) Substance P and calcitonin gene-related peptide synergistically modulate the gain of the nociceptive flexor withdrawal reflex in the rat. Neurosci. Lett., 66, 226-230.