Nerve growth factor receptor TrkA is down-regulated during postnatal development by a subset of dorsal root ganglion neurons

Journal of Comparative Neurology

Volumn 381, Issue 4, 1997, Pages 428-438

  Molliver, Derek C ^a   Snider, William D ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

dorsal horn; nerve growth factor; neurotrophins; nociceptors; regulation of phenotype

Indexed keywords

NERVE GROWTH FACTOR; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; EMBRYO; EMBRYO DEVELOPMENT; IMMUNOCYTOCHEMISTRY; MOUSE; NOCICEPTION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RECEPTOR DOWN REGULATION; SPINAL GANGLION;

EID: 0031002106     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19970519)381:4<428::AID-CNE3>3.0.CO;2-4     Document Type: Article

References (57)

1. Apfel, S. (1996) Nerve growth factor regulates the expression of brain-derived neurotrophic factor mRNA in the peripheral nervous system. Mol. Cell Neurosci. 7:134-142.
2. Averill, S., S.B. McMahon, D.O. Clary, L.F. Reichardt, and J.V. Priestley (1995) Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur. J. Neurosci. 7:1484-1494.
3. Basbaum, A.I., and J.D. Levine (1991) The contribution of the nervous system to inflammation and inflammatory disease. Can. J. Physiol. Pharmacol. 69:647-651.
4. Bevan, S., and J. Winter (1995) Nerve growth factor (NGF) differentially regulates the chemosensitivity of adult rat cultured sensory neurons. J. Neurosci. 15:4918-4926.
5. Biffo, S., N. Offenhauser, B.D. Carter, and Y.-A. Barde (1995) Selective binding and internalisation by truncated receptors restrict the availability of BDNF during development. Development 121:2461-2470.
6. Boccini, V., and P.U. Angeletti (1969) The nerve growth factor: Purification as a 30,000-molecular weight protein. Proc. Natl. Acad. Sci. USA 64:787-794.
7. Buchman, V.L., and A.M. Davies (1993) Different neurotrophins are expressed and act in a developmental sequence to promote the survival of embryonic sensory neurons. Development 118:989-1001.
8. Crowley, C., S.D. Spencer, M.C. Nishimura, K.S. Chen, S. Pitts-Meek, M.P. Armanini, L.H. Ling, S.B. McMahon, D.L. Shelton, A.D. Levinson, and H.S. Phillips (1994) Mice lacing nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76:1001-1011.
9. Davies, A.M., C. Bandtlow, R. Heumann, S. Korsching, H. Rohrer, and H. Thoenen (1987) Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 326:353-358.
10. Davies, A.M., S. Wyatt, M. Nishimura, and H. Phillips (1995) NGF receptor expression in sensory neurons develops normally in embryos lacking NGF. Dev. Biol. 171:434-438.
11. Elkabes, S., C.F. Dreyfus, D.G. Schaar, and I.B. Black (1994) Embryonic sensory development: Local expression of neurotrophin-3 and target expression of nerve growth factor. J. Comp. Neurol. 341:204-213.
12. Ernfors, P., J.-P. Merlio, and H. Persson (1992) Cells expressing mRNA for neurotrophins and their receptors during embryonic rat development. Eur. J. Neurosci. 4:1140-1158.
13. Ernfors, P., C.M. Rosario, J.-P. Merlio, G. Grant, H. Aldskogius, and H. Persson (1993) Expression of mRNAs for neurotrophin receptors in the dorsal root ganglion and spinal cord during development and following peripheral or central axotomy. Mol. Brain. Res. 17:217-226.
14. Escandon, E., D. Soppet, A. Rosenthal, J.-L. Mendoza-Ramirez, E. Szonyi, L.E. Burton, C.E. Henderson, L.F. Parada, and K. Nikolics (1994) Regulation of neurotrophin receptor expression during embryonic and postnatal development. J. Neurosci. 14:2054-2068.
15. Fenton, E.L. (1970) Tissue culture assay of nerve growth factor and of the specific antiserum. Exp. Cell. Res. 59:383-392.
16. Gaese, F., R. Kolbeck, and Y.-A. Barde (1994) Sensory ganglia require neurotrophin-3 early in development. Development 120:1613-1619.
17. Gibbs, R.B., and D.W. Pfaff (1994) In situ hybridization detection of trkA mRNA in brain: Distribution, colocalization with p75NGFR and up-regulation by nerve growth factor. J. Comp. Neurol. 341:324-339.
18. Gorin, P.D., and E.M. Johnson, Jr. (1980) Effects of long-term nerve growth factor deprivation on the nervous system of the adult rat: An experimental autoimmune approach. Brain. Res. 198:27-42.
19. Hökfelt, T. (1991) Neuropeptides in perspective: The last ten years. Neuron 7:867-879.
20. Holtzman, D.M., Y. Li, L.F. Parada, S. Kinsman, C.K. Chen, J.S. Valletta, J. Zhou, J.B. Long, and W.C. Mobley (1992) p140trk mRNA marks NGF-responsive forebrain neurons: Evidence that trk gene expression is induced by NGF. Neuron 9:465-478.
21. Hunt, S.P., and J. Rossi (1985) Peptide-and nonpeptide-containing unmyelinated primary afferents: The parallel processing of nociceptive information. Phil. Trans. R. Soc. London B 308:283-289.
22. Hunt, S.P., P.W. Mantyh, and J.V. Priestley (1992) The organization of biochemically characterized sensory neurons. In S.A. Scott (ed): Sensory Neurons: Diversity, Development and Plasticity. New York: Oxford University Press, pp. 60-76.
23. Lawson, S.N. (1992) Morphological and biochemical cell types of sensory neurons. In S.A. Scott (ed): Sensory Neurons: Diversity, Development and Plasticity. New York: Oxford University Press, pp. 27-59.
24. Lawson, S.N., P.W. McCarthy, and E. Prabhakar (1996) Electrophysiological properties of neurons with CGRP-like immunoreactivity in rat dorsal root ganglia. J. Comp. Neurol. 365:355-366.
25. Lewin, G.R., and L.M. Mendell (1993) Nerve growth factor and nociception. Trends Neurosci. 16:353-359.
26. Lewin, G.R., and L.M. Mendell (1994) Regulation of cutaneous C-fiber heat nociceptors by nerve growth factor in the developing rat. J. Neurophysiol. 71:941-949.
27. Lewin, G.R., A.M. Ritter, and L.M. Mendell (1992) On the role of nerve growth factor in the development of myelinated nociceptors. J. Neurosci. 12:1896-1905.
28. Light, A.R. (1992) The Initial Processing of Pain and Its Descending Control: Spinal and Trigeminal Systems. Basel: Karger.
29. Lindsay, R.M., and A.J. Harmar (1989) Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurons. Nature 337:362-364.
30. Lynn, B., and S.E. Carpenter (1982) Primary afferent units from the hairy skin of the rat hind limb. Brain. Res. 238:29-43.
31. McMahon, S.B., M.P. Armanini, L.L. Ling, and H.S. Phillips (1994) Expression and coexpression of trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12:1161-1171.
32. McMahon, S.B., D.L.H. Bennett, J.V. Priestley, and D.L. Shelton (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.
33. Mendell, L.M. (1995) Neurotrophic factors and the specification of neural function. Neuroscientist 1:26-34.
34. Merlio, J.-P., P. Ernfors, M. Jaber, and H. Persson (1992) Molecular cloning of rat trkC and distribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system. Neuroscience 51:513-532.
35. Miller, F.D., A. Speelman, T.C. Mathew, J. Fabian, E. Chang, C. Pozniak, and J.G. Toma (1994) Nerve growth factor derived from terminals selectively increases the ratio of p75 to trkA NGF receptors on mature sympathetic neurons. Dev. Biol. 161:206-217.
36. Molliver, D.C., M.J. Radeke, S.C. Feinstein, and W.D. Snider (1995) Presence or absence of TrkA protein distinguishes subsets of small sensory neurons with unique cytochemical characteristics and dorsal horn projections. J. Comp. Neurol. 361:404-416.
37. Mu, X., I. Silos-Santiago, S.L. Carroll, and W.D. Snider (1993) Neurotrophin receptor genes are expressed in distinct patterns in developing dorsal root ganglia. J. Neurosci. 13:4029-4041.
38. Rich, K.M., H.K. Yip, P.A. Osbourne, R.E. Schmidt, and E.M. Johnson Jr. (1984) Role of nerve growth factor in the adult dorsal root ganglia neuron and its response to injury. J. Comp. Neurol. 230:110-118.
39. Robertson, C.P., and A.K. Hall (1995) Sensory neurons regulate calcitonin gene-related peptide expression with development in vivo and in vitro. Soc. Neurosci. Abstr. 21:569.
40. Ruit, K.G., J.L. Elliott, P.A. Osborne, Q. Yan, and W.D. Snider (1992) Selective dependence of mammalian dorsal root ganglion neurons on nerve growth factor during embryonic development. Neuron 8:573-587.
41. Schecterson, L.C., and M. Bothwell (1992) Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron 9:449-463.
42. Silos-Santiago, I., D.C. Molliver, S. Ozaki, R.J. Smeyne, A.M. Fagan, M. Barbacid, and W.D. Snider (1995) Non-TrkA-expressing small DRG neurons are lost in trkA-deficient mice. J. Neurosci. 15:5929-5942.
43. Silverman, J.D., and L. Kruger (1988) Lectin and neuropeptide labeling of separate populations of dorsal root ganglion neurons and associated "nociceptor" thin axons in rat testis and cornea whole-mount preparations. Somatosens. Res. 5:259-267.
44. Smeyne, R.J., R. Klein, A. Schnapp, L.K. Long, S. Bryant, A. Lewin, S.A. Lira, and M. Barbacid (1994) Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 368:246-249.
45. Tecott, L.H., J.H. Eberwine, V.D. Barchas, and K.L. Valentino (1987) Methodological considerations in the utilization of in situ hybridization. In K.L. Valentino, J.H. Eberwine, and J.D. Barchas (eds): In Situ Hybridization. Applications to Neurobiology. New York: Oxford University Press, pp. 3-24.
46. Thoenen, H., and Y.A. Barde (1980) Physiology of nerve growth factor. Physiol. Rev. 60:1284-1335.
47. Verge, V.M.K., P.M. Richardson, R. Benoit, and R.J. Riopelle (1989) Histochemical characterization of sensory neurons with high-affinity receptors for nerve growth factor. J. Neurocytol. 18:583-591.
48. Verge, V.M., W. Tetzlaff, M.A. Bisby, and P.M. Richardson (1990) Influence of nerve growth factor on neurofilament gene expression in mature primary sensory neurons. J. Neurosci. 10:2018-2025.
49. Verge, V.K., J.-P. Merlio, J. Grondin, P. Ernfors, H. Persson, R.J. Riopelle, T. Hokfelt, and P.M. Richardson (1992) Colocalization of NGF binding sites, trk mRNA, and low-affinity NGF receptor mRNA in primary sensory neurons: Responses to injury and infusion of NGF. J. Neurosci. 12:4011-4022.
50. Verge, V.M., P.M. Richardson, Z. Wiesenfeld-Halin, and T. Hökfelt (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.
51. Wheeler, E.F., and M. Bothwell (1992) Spatiotemporal patterns of expression of NGF and the low-affinity NGF receptor in rat embryos suggest functional roles in tissue morphogenesis and myogenesis. J. Neurosci. 12:930-945.
52. White, F.A., I. Silos-Santiago, D.C. Molliver, M. Harding, H. Phillips, M. Barbacid, and W.D. Snider (1996) Synchronous onset of NGF and TrkA survival dependence in developing dorsal root ganglia. J. Neurosci. 16:4662-4672.
53. Williams, R., and T. Ebendal (1995) Neurotrophin receptor expression during development of the chick spinal sensory ganglion. Neuroreport 6:2277-2282.
54. Woolf, C.J., B. Safieh-Garabedian, Q.-P. Ma, P. Crilly, and J. Winters (1994) Nerve growth factor contributes to the generation of inflammatory sensory hypersensitivity. Neuroscience 62:327-331.
55. Wright, D.E., and W.D. Snider (1995) Neurotrophin receptor mRNA expression defines distinct populations of neurons in rat dorsal root ganglia. J. Comp. Neurol. 351:329-338.
56. Wyatt, S., and A.M. Davies (1993) Regulation of expression of mRNAs encoding the nerve growth factor receptors p75 and trkA in developing sensory neurons. Development 119:635-648.
57. Yan, Q., J.L. Elliott, C. Matheson, J. Sun, L. Zhang, X. Mu, K.L. Rex, and W.D. Snider (1993) Influences of neurotrophins on mammalian motoneurons in vivo. J. Neurobiol. 24:1555-1577.