Neurochemical Research

, Volume 21, Issue 8, pp 929–938

Expression of mRNAs for neurotrophic factors (NGF, BDNF, NT-3, and GDNF) and their receptors (p75ngfr, TrkA, TrkB, and TrkC) in the adult human peripheral nervous system and nonneural tissues

  • M. Yamamoto
  • G. Sobue
  • K. Yamamoto
  • T. Mitsuma
Original Articles


The steady-state mRNA levels of the four neurotrophic factors of nerve growth factor (NGF), brain-dervied neurotrophic factor (BDNF), neurotrophin-3 (NT-3) and glial cell line-derived neurotrophic factor (GDNF) and their receptors (p74ngfr, trkA, trkB and trkC) in the adult human peripheral nervous system (PNS) as well as nonneural tissues were examined using quantitative reverse transcription-polymerase chain reaction (RT-PCR). NGF and BDNF mRNA levels were high in the heart and spleen as well as in the dorsal root ganglia (DRG) and spinal cord, showing similar spatial expression patterns, while NT-3 mRNA levels were more pronounced in the liver and spleen. In contrast to these neurotrophins, GDNF mRNA expression occurred at the highest levels in the muscle, and it was also comparatively high in the spinal cord. p75ngfr mRNA was expressed extensively throughout the PNS tissues and in the spleen. The spatial expression patterns differed among trkA, and trkB and trkC mRNAs. trkA mRNA was greatly expressed in the DRG, sympathetic ganglia and spleen, while the trkB and trkC mRNA levels were high in the DRG, spinal cord and brain. The levels of trkB and trkC mRNAs with tyrosine kinase domain, compared to those with extracellular domain, were relatively high in the DRG, whereas they were low in the spinal cord and brain. The spatial patterns of the distributions of neurotrophic factors and their receptors mRNA levels in the adult human PNS and nonneural tissues are largely similar to those reported in other mammals, but these findings provide further, more specific, understanding relevant to the therapeutic approach to human diseases.

Key Words

Neurotrophic factors (NGF, BDNF, NT-3, GDNF) neurotrophin receptors (p75ngfr, trkA, trkB, trkC) adult humans peripheral nervous system reverse transcriptase-polymerase chain reaction 


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  1. 1.
    Funakoshi, H., Frisén, J., Barbany, G., Timmusk, T., Zachrisson, O., Verge, V. M. K., and Persson, H. 1993. Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J. Cell Biol. 123:455–465.PubMedCrossRefGoogle Scholar
  2. 2.
    Heumann, R., Korsching, S., Bandtlow, C., and Thoenen, H. 1987. Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J. Cell Biol. 104:1623–1631.PubMedCrossRefGoogle Scholar
  3. 3.
    Barde, Y.-A. 1994. Neurotrophic factors: an evolutionary perspective. J. Neurobiol. 25:1329–1333.PubMedCrossRefGoogle Scholar
  4. 4.
    Snider, W. D. 1994. Function of the neurotrophins during nervous system development: What the knockouts are teaching us. Cell 77:627–638.PubMedCrossRefGoogle Scholar
  5. 5.
    Maisonpierre, P. C., Belluscio, L., Friedman, B., Alderson, R. F., Wiegand, S. J., Furth, M. E., Lindsay, R. M., and Yancopoulos, G. D. 1990. NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron 5:501–509.PubMedCrossRefGoogle Scholar
  6. 6.
    Lin, L.-F. H., Doherty, D. H., Lile, J. D., Bektesh, S., and Collins, F. 1993. GDNF: A glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260:1130–1132.PubMedCrossRefGoogle Scholar
  7. 7.
    Chao, M. V., Bothwell, M. A., Ross, A. H., Koprowski, H., Lanahan, A. A., Buck, C. R., and Sehgal, A. 1986. Gene transfer and molecular cloning of the human NGF receptor. Science 232:518–521.PubMedCrossRefGoogle Scholar
  8. 8.
    Johnson, D., Lanahan, A., Buck, C. R., Sehgal, A., Morgan, C., Mercer, M., Bothwell, M., and Chao, M. 1986. Expression and structure of the human NGF receptor. Cell 47:545–554.PubMedCrossRefGoogle Scholar
  9. 9.
    Klein, R., Jing, S., Nanduri, V., O'Rourke, E., and Barbacid, M. 1991. The trk proto-oncogene encodes a receptor for nerve growth factor. Cell 65:189–197.PubMedCrossRefGoogle Scholar
  10. 10.
    Klein, R., Nanduri, V., Jing, S., Lamballe, F., Tapley, P., Bryant, S., Cordon-Cardo, C., Jones, K. R., Reichardt, L. F., and Barbacid, M. 1991. The trkB tyrosine protein kinase is a receptor for brainderived neurotrophic factor and neurotrophin-3. Cell 66:395–403.PubMedCrossRefGoogle Scholar
  11. 11.
    Squinto, S. P., Stitt, T. N., Aldrich, T. H., Davis, S., Bianco, S. M., Radziejewski, C., Glass, D. J., Masiakowski, P., Furth, M. E., Valenzuela, D. M., DiStefano, P. S., and Yancopoulos, G. D. 1991. trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell 65:885–893.PubMedCrossRefGoogle Scholar
  12. 12.
    Lamballe, F., Klein, R., and Barbacid, M. 1991. trkC, a new member of the trk family of tyrosine kinase, is a receptor for Neurotrophin-3. Cell 66:967–979.PubMedCrossRefGoogle Scholar
  13. 13.
    Allen, S. J., Dawbarn, D., Eckford, S. D., Wilcock, G. K., Ashcroft, M., Colebrook, S. M., Feeney, R., and MacGowan, S. H. 1994. Cloning of a non-catalytic form of human trkB and distribution of messenger RNA for trkB in human brain. Neuroscience 60:825–834.PubMedCrossRefGoogle Scholar
  14. 14.
    Garner, A. S., and Large, T. H. 1994. Isoforms of the avian trkC receptor: a novel kinase insertion dissociates transformation and process outgrowth from survival. Neuron 13:457–472.PubMedCrossRefGoogle Scholar
  15. 15.
    Klein, R., Conway, D., Parada, L. F., and Barbacid, M. 1990. The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell 61:647–656.PubMedCrossRefGoogle Scholar
  16. 16.
    Shelton, D. L., Sutherland, J., Gripp, J., Camerato, T., Armanini, M. P., Phillips, H. S., Carroll, K., Spencer, S. D., and Levinson, A. D. 1995. Human trks: molecular cloning, tissue distribution. and expression of extracellular domain immunoadhesins. J. Neurosci. 15:477–491.PubMedGoogle Scholar
  17. 17.
    Tsoulfas, P., Soppet, D., Escandon, E., Tessarollo, L., Mendoza-Ramirez, J., Rosenthal, A., Nikolics, K., and Parada, L. F. 1993. The rat trkC locus encodes multiple neurogenic receptors that exhibit differential response to neurotrophin-3 in PC12 cells. Neuron 10:975–990.PubMedCrossRefGoogle Scholar
  18. 18.
    Crowley, C., Spencer, S. D., Nishimura, M. C., Chen, K. S., Pitts-Meek, S., Armanini, M. P., Ling, L. H., MacMahon, S. B., Shelton, D. L., Levinson, A. D., and Phillips, H. S. 1994. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76:1001–1011.PubMedCrossRefGoogle Scholar
  19. 19.
    DiStefano, P. S., Friedman, B., Radziejewski, C., Alexander, C., Boland, P., Schick, C. M., Lindsay, R. M., and Wiegand, S. J. 1992. The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron 8:983–993.PubMedCrossRefGoogle Scholar
  20. 20.
    Ernfors, P., Lee, K. F., and Jaenisch, R. 1994. Mice lacking brainderived neurotrophic factor develop with sensory deficits. Nature 368:147–150.PubMedCrossRefGoogle Scholar
  21. 21.
    Ernfors, P., Lee, K. F., Kucera, J., and Jaenisch, R. 1994. Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 77:503–512.PubMedCrossRefGoogle Scholar
  22. 22.
    Farinas, I., Jones, K. R., Backus, C., Wang, X. Y., and Reichardt, L. F. 1994. Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369:658–661.PubMedCrossRefGoogle Scholar
  23. 23.
    Jones, K. R., Farinas, I., Backus, C., and Reichardt, L. F. 1994. Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76: 989–999.PubMedCrossRefGoogle Scholar
  24. 24.
    Klein, R., Smeyne, R. J., Wurst, W., Long, L. K., Auerbach, B. A., Joyner, A. L., and Barbacid, M. 1993. Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death. Cell 75:113–122.PubMedGoogle Scholar
  25. 25.
    Klein, R., Silos-Santiago, I., Smeyne, R. J., Lira, S. A., Brambilla, R., Bryant, S., Zhang, L., Snider, W. D., and Barbacid, M. 1994. Disruption of the neurotrophin-3 receptor gene trkC eliminates 1a muscle afferents and results in abnormal movement. Nature 368: 249–251.PubMedCrossRefGoogle Scholar
  26. 26.
    McMahon, S. B., Armanini, M. P., Ling, L. H., and Phillips, H. S. 1994. Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12:1161–1171.PubMedCrossRefGoogle Scholar
  27. 27.
    Merlio, J. P., Ernfors, P., Japer, M., and Persson, H. 1992. Molecular cloning of rat trkC and identification of cell expressing mRNAs for members of the trk family in the rat central nervous system. Neuroscience 51:513–532.PubMedCrossRefGoogle Scholar
  28. 28.
    Smeyne, R. J., Klein, R., Schnapp, A., Long, L. K., Bryant, S., Lewin, A., Lira, S. A., and Barbacid, M. 1994. Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 368:246–249.PubMedCrossRefGoogle Scholar
  29. 29.
    Verge, V. M. K., Merlio, J. P., Grondin, J., Ernfors, P., Riopelle, J., Hökfelt, T., and Richardson, P. M. 1992. Colocalization of NGF binding sites, trk mRNA, and low-affinity NGF receptor mRNA in primary sensory neurons: responses to injury and infusion on NGF. J. Neurosci. 12:4011–4022.PubMedGoogle Scholar
  30. 30.
    Koliatsos, V. E., Clatterbuck, R. E., Winslow, J. W., Cayouette, M. H., and Price, D. L. 1993. Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo. Neuron 10:359–367.PubMedCrossRefGoogle Scholar
  31. 31.
    Henderson, C. E., Phillips, H. S., Pollock, R. A., Davies, A. M., Lemeulle, C., Armanini, M., Simpson, L. C., Moffet, B., Vandlen, R. A., Koliatsos, V. E., and Rosenthal, A. 1994. GDNF: A potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266:1062–1064.PubMedCrossRefGoogle Scholar
  32. 32.
    Oppenheim, R. W., Houenou, L. J., Johnson, J. E., Lin, L.-F. H., Li, L., Lo, A. C., Newsome, A. L., Prevette, D. M., and Wang, S. 1995. Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature 373:344–346.PubMedCrossRefGoogle Scholar
  33. 33.
    Yan, Q., Matheson, C., and Lopez, O. T. 1995. In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons. Nature 373:341–344.PubMedCrossRefGoogle Scholar
  34. 34.
    Ernfors, P., Hallböök, F., Ebendal, T., Shooter, E. M., Radeke, M. J., Misko, T. P., and Persson, H. 1988. Developmental and regional expression of β-nerve growth factor receptor mRNA in the chick and rat. Neuron 1:983–996.PubMedCrossRefGoogle Scholar
  35. 35.
    Klein, R., Martin-Zanca, D., Barbacid, M., and Parada, L. F. 1990. Expression of the tyrosine kinase receptor gene trkB is confined to the murine embryonic and adult nervous system. Development 109:845–850.PubMedGoogle Scholar
  36. 36.
    Lamballe, F., Smeyne, R. J., and Barbacid, M. 1994. Developmental expression of trkC, the neurotrophin-3 receptor, in the mammalian nervous system. J. Neurosci. 14:14–28.PubMedGoogle Scholar
  37. 37.
    Martin-Zanca, D., Barbacid, M., and Parada, L. F. 1990. Expression of the trk proto-oncogene is restricted to the sensory cranial and spinal ganglia of neural crest origin in mouse development. Genes Dev. 4:683–694.PubMedGoogle Scholar
  38. 38.
    Tessarollo, L., Tsoulfas, P., Martin-Zanca, D., Gilbert, D. J., Jenkins, N. A., Copeland, N. G., and Parada, L. F. 1993. trkC, a receptor for neurotrophin-3, is widely expressed in the developing nervous system and non-neuronal tissues. Development 118:463–475.PubMedGoogle Scholar
  39. 39.
    Wheeler, E. F., and Bothwell, M. 1992. Spatiotemporal patterns of expression of NGF and the low-affinity NGF receptor in rat embryo suggest functional roles in tissue morphogenesis and myogenesis. J. Neurosci. 12:930–945.PubMedGoogle Scholar
  40. 40.
    Sobue, G., Yasuda, T., Mitsuma, T., Ross, A. H., and Pleasure, D. 1988. Expression of nerve growth factor receptor in human peripheral neuropathies. Ann. Neurol. 24:64–72.PubMedCrossRefGoogle Scholar
  41. 41.
    Yamamoto, M., Sobue, G., Mutoh, T., and Mitsuma, T. 1993. Gene expression of high- (pl40trk) and low-affinity nerve growth factor receptor (LNGFR) in the adult and aged human peripheral nervous system. Neurosci. Lett. 158:39–43.PubMedCrossRefGoogle Scholar
  42. 42.
    Yamamoto, M., Sobue, G., Yamamoto, K., Terao, S., and Mitsuma, T. 1996. Expression of glial cell line-derived neurotrophic factor mRNA in the spinal cord and muscle in amyotrophic lateral sclerosis. Neurosci. Lett. 204:117–120.PubMedCrossRefGoogle Scholar
  43. 43.
    Chomczynski, P., and Sacch, N. 1987. Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloform extraction. Anal. Biochem. 162:156–159.PubMedCrossRefGoogle Scholar
  44. 44.
    Maisonpierre, P. C., Belluscio, L., Squinto, S., Ip, N. Y., Furth, M. E., Lindsay, R. M., and Yancopoulos, G. D. 1990. Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. Science 247:1446–1451.PubMedCrossRefGoogle Scholar
  45. 45.
    Maisonpierre, P. C., Le Beau, M. M., Espinosa, III R., Ip, N. Y., Belluscio, L., De La Monte, S. M., Squinto, S., Furth, M. E., and Yancopoulos, G. D. 1991. Human and rat brain-derived neurotrophic factor and neurotrophin-3: gene structures, distributions, and chromosomal localizations. Genomics 10:558–568.PubMedCrossRefGoogle Scholar
  46. 46.
    Valenzuela, D. M., Maisonpierre, P. C., Glass, D. J., Rojas, E., Nunez, L., Kong, Y., Gies, D. R., Stitt, T. N., Ip, N. Y., and Yancopoulos, G. D. 1993. Alternative forms of rat TrkC with different functional capabilities. Neuron 10:963–974.PubMedCrossRefGoogle Scholar
  47. 47.
    Heumann, R., Korsching, S., Scott, J., and Thoenen, H. 1984. Relationship between levels of nerve growth factor (NGF) and its messenger RNA in sympathetic ganglia and peripheral target tissues. EMBO J. 3:3183–3189.PubMedGoogle Scholar
  48. 48.
    Shelton, D. L., and Reichardt, L. F. 1984. Expression of the β-nerve growth factor correlates with the density of sympathetic innervation in effector organs. Proc. Natl. Acad. Sci. USA 8: 7951–7955.CrossRefGoogle Scholar
  49. 49.
    MacGrogan, D., Saint Andre, J. P., and Dicou, E. 1992. Expression of nerve growth factor and nerve growth factor receptor genes in human tissues and in prostatic adenocarcinoma cell lines. J. Neurochem. 59:1381–1391.PubMedCrossRefGoogle Scholar
  50. 50.
    Timmunsk, T., Palm, K., Metsis, M., Reintam, T., Paalme, V., Saarma, M., and Persson, H. 1993. Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron 10:475–489.CrossRefGoogle Scholar
  51. 51.
    Alpers, K. M., Wright, D. E., and Davis B. M. 1994. Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J. Neurosci. 14:1422–1432.Google Scholar
  52. 52.
    Zhou, X. F., and Rush, R. A. 1993. Localization of neurotrophin-3-like immunoreactivity in peripheral tissues of the rat. Brain Res. 621:189–199.PubMedCrossRefGoogle Scholar
  53. 53.
    Ernfors, P., Wetmore, C., Olson, L., and Persson, H. 1990. Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron 5: 511–526PubMedCrossRefGoogle Scholar
  54. 54.
    Schaar, D. G., Sieber, B. A., Dreyfus, C. F., and Black, I. B. 1993. Regional and cell-specific expression of GDNF in rat brain. Exp. Neurol. 124:368–371.PubMedCrossRefGoogle Scholar
  55. 55.
    Springer J. E., Mu, X., Bergmann, L. W., and Trojanowski, J. Q. 1994. Expression of GDNF mRNA in rat and human nervous tissue. Exp. Neurol. 127:167–170.PubMedCrossRefGoogle Scholar
  56. 56.
    Springer, J. E., Seeburger, J. L., Gabrea, A., Blankenhorn, E. P., and Bergman, L. W. 1994. cDNA sequence and differential mRNA regulation of two forms of glial cell line-derived neurotrophic factor in Schwann cells and rat skeletal muscle. Exp. Neurol. 131:47–52.CrossRefGoogle Scholar
  57. 57.
    Sobue, G., Yasuda, T., Mitsuma, T., and Pleasure, D., 1989. Nerve growth factor receptor immunoreactivity in the neuronal perikarya of human sensory and sympathetic nerve ganglia. Neurology 39: 937–941.PubMedGoogle Scholar
  58. 58.
    Lee, K. F., Li, E., Huber, L. J., Landis, S. C., Sharpe, A. H., Chao, M. V., and Jaenisch, R. 1992. Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69:737–749.PubMedCrossRefGoogle Scholar
  59. 59.
    Yamamoto, M., Sobue, G., Li, M., Arakawa, Y., Mitsuma, T., and Kimata, K. 1993. Nerve growth factor (NGF), brain-derived neurotrophic factor (BDNF) and low-affinity nerve growth receptor (LNGFR) mRNA levels in cultured rat Schwann cells; differential time- and dose-dependent regulation by cAMF. Neurosci. Lett. 152:37–40.PubMedCrossRefGoogle Scholar
  60. 60.
    Rende, M., Provenzano, C., and Tonali, P. 1993. Modulation of low-affinity nerve growth factor receptor in injured adult rat spinal cord motoneurons. J. Comp. Neurol. 338:560–574.PubMedCrossRefGoogle Scholar
  61. 61.
    Seeburger, J. L., Tarras, S., Natter, H., and Springer, J. E. 1993. Spinal cord motoneurons express p75Fgfr and p145trkB mRNA in amyotrophic lateral sclerosis. Brain Res. 621:111–115.PubMedCrossRefGoogle Scholar
  62. 62.
    Barker, P. A., Lomen-Hoerth, C., Gensch, E. M., Meakin, S. O., Glass, D. J., and Shooter, E. M. 1993. Tissue-specific alternative splicing generates two isoforms oftrkA receptor. J. Biol. Chem. 20:15150–15157.Google Scholar
  63. 63.
    Martin-Zanca, D., Oskam, R., Mitra, G., Copeland, T., and Barbacid, M. 1989. Molecular and biochemical characterization of the humantrk proto-oncogene. Mol. Cell Biol. 9:24–33.PubMedGoogle Scholar
  64. 64.
    Ringstedt, T., Lagercrantx, H. and Persson, H. 1993. Expression of members of the trk family in the developing postnatal rat brain. Dev. Brain Res. 72:119–131.CrossRefGoogle Scholar
  65. 65.
    Zhou, X. F., Parada, L. F., Soppet, D., and Rush, R. A. 1993. Distribution of trkB tyrosine kinase immunoreactivity in the rat central nervous system. Brain Res. 622:63–70.PubMedCrossRefGoogle Scholar
  66. 66.
    Chevalier, S., Praloran, V., Smith, C., MacGrogan, D., Ip, N.Y. Yancopoulos, G. D., Brachet, P., Pouplard, A., and Gascan, H. 1994. Expression and functionality of the trkA proto-oncogene product/NGF receptor in undifferentiated hematopoietic cells. Blood 83:1479–1485.PubMedGoogle Scholar
  67. 67.
    Ehrhard, P. B., Erb, P., Graumann, U., and Otten, U. 1993. Expression of nerve growth factor and nerve growth factor receptor tyrosine kinase Trk in activated CD4-positive T-cell clones. Proc. Natl. Acad. Sci. USA 90:10984–10988.PubMedCrossRefGoogle Scholar
  68. 68.
    Horigome, K., Pryor, J. C., Bullock, E. D., and Johnson, E. M. 1993. Mediator release from mast cells by nerve growth factor. J. Biol. Chem. 268:14881–14887.PubMedGoogle Scholar
  69. 69.
    Laurenzi, M. A., Barbany, G., Timmusk, T., Lindgren, J. A. and Persson, H., 1994. Expression of mRNA encoding neurotrophins and neurotrophin receptors in rat thymus, spleen tissue and immunocompetent cells. Regulation of neurotrophin-4 mRNA expression, by mitogens and leukotriene B4. Eur. J. Biochem. 223: 733–741.PubMedCrossRefGoogle Scholar
  70. 70.
    Frisén, J., Arvidsson, U., Lindholm, D., Fried, K., Verge, V. M. K., Cullheim, S., Hökfelt, T., and Risling, M. 1993. trkC expression in the injured rat spinal cord. Neuroreport 5:349–352.PubMedCrossRefGoogle Scholar
  71. 71.
    Middlemas, D. S., Lindberg, R. A., and Hunter, T. 1991. trkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors. Mol. Cell Biol. 11:143–153.PubMedGoogle Scholar
  72. 72.
    Ernfors, P., Rosario, C. M., Merlio, J.-P., Grant, G., Aldskogius, H., and Persson, H. 1993. Expression of mRNAs for neurotrophin receptors in the dorsal root ganglion and spinal cord during and following peripheral or central axotomy. Mol. Brain Res. 17:217–226.PubMedCrossRefGoogle Scholar
  73. 73.
    Frisén, J., Verge, V. M. K., Fried, K., Risling, M., Persson, H., Trotter, J., Hökfelt, T., and Lindholm, D. 1993. Characterization of glial trkB receptors: Differential response to injury in the central and peripheral nervous system. Proc. Natl. Acad. Sci. USA 90:4971–4975.PubMedCrossRefGoogle Scholar
  74. 74.
    Acheson, A., Conover, J. C., Fandl, J. P., Dechiara, T. M., Russell, M., Thadani, A., Squinto, S. P., Yancopoulos, G. D., and Lindsay, R. M. 1995. A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature 374:450–453.PubMedCrossRefGoogle Scholar
  75. 75.
    Dixon, J. E., and McKinnon, D. 1994. Expression of the trk gene family of neurotrophin receptors in prevertebral sympathetic ganglia. Dev. Brain Res. 77:177–182.CrossRefGoogle Scholar
  76. 76.
    Ehrhard, P. B., and Otten, U. 1994. Postnatal ontogeny of the neurotrophin receptor trk and trkB mRNA in rat sensory and sympathetic ganglia, Neurosci. Lett. 166:207–210.PubMedCrossRefGoogle Scholar
  77. 77.
    Itoh, T., Sobue G., Yasuda, T., Kimata, K., Mitsuma, T., and Takahashi, A. 1993. Geometric response to nerve growth factor is preserved in aged rat sensory neurons: a single-neuron culture study. Neurobiol. Aging 14:167–176.PubMedCrossRefGoogle Scholar
  78. 78.
    Ullrich, A., Gray, A., Berman, C., and Dull, T. J. 1983. Human beta-nerve growth factor gene sequence highly homologous to that of mouse. Nature 303:821–825.PubMedCrossRefGoogle Scholar
  79. 79.
    McGregor, L. M., Baylin, S. B., Griffin, C. A., Hawkins, A. L., and Nelkin, B. D. 1994. Molecular cloning of the cDNA for human TrkC (NTRK3), chromosomal assignment, and evidence for a splice variant. Genomics 22:267–272.PubMedCrossRefGoogle Scholar
  80. 80.
    Haendler, B., Hofer-Warbinek, R., and Hofer, E. 1987. Complementary DNA for human T-cell cyclophilin. EMBO J. 6:947–950.PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1996

Authors and Affiliations

  • M. Yamamoto
    • 2
    • 1
  • G. Sobue
    • 2
  • K. Yamamoto
    • 1
  • T. Mitsuma
    • 1
  1. 1.Division of Neurology Fourth Department of Internal MedicineAichi Medical UniversityNagakute, AichiJapan
  2. 2.Department of NeurologyNagoya University School of MedicineNagoyaJapan

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