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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

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Abstract

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.

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References

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  3. Barde, Y.-A. 1994. Neurotrophic factors: an evolutionary perspective. J. Neurobiol. 25:1329–1333.

    Article  PubMed  CAS  Google Scholar 

  4. Snider, W. D. 1994. Function of the neurotrophins during nervous system development: What the knockouts are teaching us. Cell 77:627–638.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  20. Ernfors, P., Lee, K. F., and Jaenisch, R. 1994. Mice lacking brainderived neurotrophic factor develop with sensory deficits. Nature 368:147–150.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  Google Scholar 

  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. 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.

    Article  PubMed  CAS  Google Scholar 

  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: 511–526

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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. 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.

    PubMed  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  80. Haendler, B., Hofer-Warbinek, R., and Hofer, E. 1987. Complementary DNA for human T-cell cyclophilin. EMBO J. 6:947–950.

    PubMed  CAS  Google Scholar 

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Yamamoto, M., Sobue, G., Yamamoto, K. et al. 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. Neurochem Res 21, 929–938 (1996). https://doi.org/10.1007/BF02532343

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