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

Neurochemical Research

Volumn 21, Issue 8, 1996, Pages 929-938

  Yamamoto, M ^a,b   Sobue, G ^a   Yamamoto, K ^b   Terao, S ^b   Mitsuma, T ^b  

^a NAGOYA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b AICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

Adult humans; Neurotrophic factors (NGF, BDNF, NT 3, GDNF); Neurotrophin receptors (p75NGFR, trkA, trkB, trkC); Peripheral nervous system; Reverse transcriptase polymerase chain reaction

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR; NEUROTROPHIN 3; NEUROTROPHIN RECEPTOR; PROTEIN TYROSINE KINASE;

ADULT; AGED; ARTICLE; CONTROLLED STUDY; FEMALE; HEART; HUMAN; HUMAN TISSUE; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD; SPINAL GANGLION; SPLEEN; TISSUE DISTRIBUTION;

ADULT; AGED; AGED, 80 AND OVER; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DNA PRIMERS; FEMALE; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; HUMANS; KIDNEY; LIVER; LUNG; MALE; MIDDLE AGED; MUSCLE, SKELETAL; MYOCARDIUM; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEUROTROPHIN 3; ORGAN SPECIFICITY; PERIPHERAL NERVOUS SYSTEM; POLYMERASE CHAIN REACTION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, CILIARY NEUROTROPHIC FACTOR; RECEPTOR, NERVE GROWTH FACTOR; RECEPTOR, TRKA; RECEPTOR, TRKC; RECEPTORS, NERVE GROWTH FACTOR; RNA, MESSENGER; SPLEEN; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 0029854439     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02532343     Document Type: Article

References (80)

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.
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.
3. Barde, Y.-A. 1994. Neurotrophic factors: an evolutionary perspective. J. Neurobiol. 25:1329-1333.
4. Snider, W. D. 1994. Function of the neurotrophins during nervous system development: What the knockouts are teaching us. Cell 77:627-638.
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.
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.
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.
8. Johnson, D., Lanahan, A., Buck, C. R., Sehgal, A., Morgan, C., Mercer, E., Bothwell, M., and Chao, M. 1986. Expression and structure of the human NGF receptor. Cell 47:545-554.
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.
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 brain-derived neurotrophic factor and neurotrophin-3. Cell 66:395-403.
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.
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.
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.
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.
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.
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.
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.
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.
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.
20. Ernfors, P., Lee, K. F., and Jaenisch, R. 1994. Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368:147-150.
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.
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.
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.
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.
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 Ia muscle afferents and results in abnormal movement. Nature 368: 249-251.
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.
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.
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.
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 infusin on NGF. J. Neurosci. 12:4011-4022.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
41. trk) and low-affinity nerve growth factor receptor (LNGFR) in the adult and aged human peripheral nervous system. Neurosci. Lett. 158:39-43.
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.
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.
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.
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.
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.
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 tis-sues. EMBO J. 3:3183-3189.
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.
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.
50. Timmusk, 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.
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.
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.
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.
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.
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.
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.
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.
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.
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 cAMP. Neurosci. Lett. 152:37-40.
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.
61. trkB mRNA in amyotrophic lateral sclerosis. Brain Res. 621:111-115.
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 of trkA receptor. J. Biol. Chem. 20:15150-15157.
63. Martin-Zanca, D., Oskam, R., Mitra, G., Copeland, T., and Barbacid, M. 1989. Molecular and biochemical characterization of the human trk proto-oncogene, Mol. Cell Biol. 9:24-33.
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.
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.
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.
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.
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.
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.
70. Frisén, J., Arvidsson, U., Lindholm, D., Frïed, 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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
80. Haendler, B., Hofer-Warbinek, R., and Hofer, E. 1987. Complementary DNA for human T-cell cyclophilin. EMBO J. 6:947-950.