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Neurotrophin-3 and TrkC-immunoreactive neurons in rat dorsal root ganglia correlate by distribution and morphology

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Abstract

Previous studies have shown that a subpopulation of large dorsal root ganglion neurons contains neurotrophin-3 (NT3)-like immunoreactivity. It is not known, however, whether these NT3 immunoreactive neurons also express the high affinity receptor for NT3, trkC. In the present study, the distribution and morphology of trkC immunoreactive neurons have been correlated with those of NT3 immunoreactive neurons in the dorsal root ganglia. Size and segmental distributions of both antigens indicate that they are present in the same group of large sensory neurons. Almost twice the number of these neurons are present in the cervical and lumbar spinal ganglia than in the thoracic. Co-localization study indicates that 94% of NT3 immunoreactive neurons express trkC. Our findings support the proposal that NT3 in these neurons is derived from their peripheral targets rather than synthesized in situ.

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References

  1. Levi-Montalcini, R. 1987. The nerve growth factor: 35 years later. Science 237:1154–1162.

    Article  PubMed  CAS  Google Scholar 

  2. Hohn, A., Leibrock, J., Bailey, K., and Barde, Y.-A. 1990. Identification and characterization of a novel member of the nerve growth factor/brain derived neurotrophic factor family. Nature 344:339–341.

    Article  PubMed  CAS  Google Scholar 

  3. Maisonpierre, P. C., Beluscio, 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 

  4. 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 

  5. Farinas, J., Jones, K. R., Bachus, 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 

  6. Gaese, F., Kolbeck, F., and Barde, Y.-A. 1994. Sensory ganglia require neurotrophin-3 early in development. Development 120:1613–1619.

    PubMed  CAS  Google Scholar 

  7. Lamballe, F., Klein, R., and Barbacid, M. 1991. TrkC, a New member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 66:967–979.

    Article  PubMed  CAS  Google Scholar 

  8. 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 in non-neuronal tissues. Development 118:463–475.

    PubMed  CAS  Google Scholar 

  9. Zhang, D., Yao, L., and Bernd, P. 1994. Expression of trk and neurotrophin mRNA in dorsal root and sympathetic ganglia of the quail during development. J. Neurobiol. 25:1517–1532.

    Article  PubMed  CAS  Google Scholar 

  10. Schecterson, L. C., and Bothwell, M. 1992. Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron 9:449–463.

    Article  PubMed  CAS  Google Scholar 

  11. 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 

  12. 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 

  13. Henderson, C. E., Camu, W., Mettling, C., Gouin, A., Poulsen, K., Karihaloo, M., Rullamas, J., Evans, T., McMahon, S. B., Armanini, M. P., Berkemeier, L., Phillips, H. S., and Resenthal, A. 1993. Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363:266–270.

    Article  PubMed  CAS  Google Scholar 

  14. Arumäe, U., Pirvola, U., Palgi, J., Kiema, T.-R., Palm, K., Moshnyakov, M., Ylikoski, J., and Saarma, M. 1993. Neurotrophins and their receptors in rat peripheral trigeminal system during maxillary nerve growth. J. Cell Biol. 122:1053–1065.

    Article  PubMed  Google Scholar 

  15. Copray, J. C. V. M., and Brouwer, N. 1994. Selective expression of neurotrophin-3 messenger RNA in muscle spindles of the rat. Neurosci. 63:1125–1135.

    Article  CAS  Google Scholar 

  16. 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 

  17. 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 movements. Nature 368:249–251.

    Article  PubMed  CAS  Google Scholar 

  18. Williams, R., Vickers, J. C., Zhou, X.-F., Costa, M., and Rush, R. A. 1993. A subpopulation of chicken primary sensory neurons defined by complete co-localization of Peripherin- and ovalbumin-immunoreactivities. Brain Res. 627:354–356.

    Article  PubMed  CAS  Google Scholar 

  19. Mu, X., Silos-Santiago, I., Carroll, S. L., and Snider, W. D. 1993. Neurotrophin receptor genes are expressed in distinct patterns in developing dorsal root ganglia. J. Neurosci. 13:4029–4041.

    PubMed  CAS  Google Scholar 

  20. 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 

  21. Williams, R., Backstrom, A., Ebendal, T., and Hallbook, F. 1993. Molecular cloning and cellular localization of trkC in the chicken embryo. Dev. Brain Res. 75:235–252.

    Article  CAS  Google Scholar 

  22. Barde, Y.-A., Edgar, D., and Thoenen, H. 1982. Purification of a new neurotrophic factor from mammalian brain. EMBO J. 1:549–553.

    PubMed  CAS  Google Scholar 

  23. Hallbook, F., Ibanez, C. F., and Persson, H. 1991. Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron 6:845–858.

    Article  PubMed  CAS  Google Scholar 

  24. Oakley, R. A., Garner, S. A., Large, T. H., and Frank, E. 1993. Differential distribution of trkC-positive neurons in spinal ganglia. Society of Neuroscience Abstract Vol. 19, 538.32.

    Google Scholar 

  25. Verge, V. M. K., Merlio, J.-P., Grondin, J., Ernfors, P., Persson, H., Riopelle, R. J., Hökfelt, T., and Richardson, P. M. 1992. Collocalization 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.

    PubMed  CAS  Google Scholar 

  26. Zhou, X.-F., Gai, W. P., and Rush, R. A. 1993. CGRP immunoreactive neurons in rat dorsal root ganglia do not all contain low-affinity NGF receptor immunoreactivity. Brain Res. 612:322–325.

    Article  PubMed  CAS  Google Scholar 

  27. Zhou, X.-F., and Rush, R. A. 1995. Peripheral projections of rat primary sensory neurons immunoreactive for neurotrophin 3. J. Comp. Neurol 363:69–77.

    Article  PubMed  CAS  Google Scholar 

  28. Zhou, X.-F., and Rush, R. A. 1995. Sympathetic neurons in neonatal rats require endogenous neurotrophin-3 for survival. J. Neurosci. 15:6521–6530.

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Human Physiology and Centre for Neuroscience, Flinders University of South Australia, G.P.O. Box 2100, 5001, Adelaide, Australia

    Colin Chen,  Xin-Fu Zhou & Robert A. Rush

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  1. Colin Chen
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  2. Xin-Fu Zhou
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  3. Robert A. Rush
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Correspondence to Xin-Fu Zhou.

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Special issue dedicated to Dr. Hans Thoenen.

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Chen, C., Zhou, XF. & Rush, R.A. Neurotrophin-3 and TrkC-immunoreactive neurons in rat dorsal root ganglia correlate by distribution and morphology. Neurochem Res 21, 809–814 (1996). https://doi.org/10.1007/BF02532304

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  • DOI: https://doi.org/10.1007/BF02532304

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