Earliest sensory nerve fibres are guided to peripheral targets by attractants other than nerve growth factor

Earliest sensory nerve fibres are guided to peripheral targets by attractants other than nerve growth factor

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ABSTRACT Recent studies have shown that developing nerve fibres grow directly to their targets1–4 and are guided by specific cues5,6, but the nature of these cues and the mechanism of guidance remain unknown7,8. The growth of sympathetic axons towards an artificial source of nerve growth factor (NGF) _in vivo_9 and of sensory neurites up a concentration gradient of NGF _in vitro_10,11 has supported the hypothesis that NGF, produced by target tissues, acts as a chemotactic attractant for these nerve fibres during development12. Both these studies and those of the influence of NGF13,14 or target tissues15–19 on neurite growth _in vitro_ were conducted late in development when, following target encounter, the neurones had become dependent on NGF or target for survival. Here we have co-cultured embryonic mouse sensory neurones and their peripheral target tissue at a stage preceding their contact _in vivo_. Neurites grew directly and exclusively towards their own target but not to regionally inappropriate peripheral tissue. Antiserum to isogeneric NGF did not reduce this outgrowth but did reduce undirected neurite outgrowth which occurred in co-cultures of older neurones with denervated target tissue. These results demonstrate that agents other than NGF guide neurites of NGF-responsive neurones in development. Access through your institution Buy or subscribe This is a preview of subscription content, access via your institution ACCESS OPTIONS Access through your institution Subscribe to this journal Receive 51 print issues and online access $199.00 per year only $3.90 per issue Learn more Buy this article * Purchase on SpringerLink * Instant access to full article PDF Buy now Prices may be subject to local taxes which are calculated during checkout ADDITIONAL ACCESS OPTIONS: * Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS MOTOR INNERVATION DIRECTS THE CORRECT DEVELOPMENT OF THE MOUSE SYMPATHETIC NERVOUS SYSTEM Article Open access 16 August 2024 SYMPATHETIC NEURONS SECRETE RETROGRADELY TRANSPORTED TRKA ON EXTRACELLULAR VESICLES Article Open access 04 March 2023 NEURONAL PROCESSES AND GLIAL PRECURSORS FORM A SCAFFOLD FOR WIRING THE DEVELOPING MOUSE COCHLEA Article Open access 17 November 2020 REFERENCES * Holt, C. E. & Harris, W. A. _Nature_ 301, 150–152 (1983). Article  ADS  CAS  Google Scholar  * Honig, M. G. _J. Physiol., Lond._ 330, 175–202 (1982). Article  CAS  Google Scholar  * Scott, S. A. _J. Physiol., Lond._ 330, 203–230 (1982). Article  CAS  Google Scholar  * Lance-Jones, C. & Landmesser, L. _Proc. R. Soc._ B214, 1–18 (1981). ADS  CAS  Google Scholar  * Lance-Jones, C. & Landmesser, L. _J. Physiol., Lond._ 302, 559–580 (1980). Article  CAS  Google Scholar  * Lance-Jones, C. & Landmesser, L. _Proc. R. Soc._ B214, 19–52 (1981). ADS  CAS  Google Scholar  * Purves, D. in _Repair and Regeneration of the Nervous System_ (ed. Nicholls, J. G.), 107–125 (Springer, Berlin, 1982). Book  Google Scholar  * Landmesser, L. in _Studies in Developmental Neurobiology_ (ed. Cowan, W. M.), 53–73 (Oxford University Press, 1981). Google Scholar  * Menesini Chen, M. G., Chen, J. S. & Levi-Montalcini, R. _Arch. Ital. Biol._ 116, 53–84 (1978). CAS  PubMed  Google Scholar  * Letourneau, P. C. _Devl Biol._ 66, 183–196 (1978). Article  CAS  Google Scholar  * Gundersen, R. W. & Barrett, J. N. _Science_ 206, 1079–1080 (1979). Article  ADS  CAS  Google Scholar  * Levi-Montalcini, R. _A. Rev. Neurosci._ 5, 341–362 (1982). Article  CAS  Google Scholar  * Charlwood, K. A., Lamont, D. M. & Banks, B. in _Nerve Growth Factor and its Antiserum_ (eds Zaimis, E. & Knight, J.) 102–107 (Athlone, London, 1972). Google Scholar  * Rutishauser, U. & Edelman, G. M. _J. Cell Biol._ 87, 370–378 (1980). Article  CAS  Google Scholar  * Chamley, J. H., Goller, I. & Burnstock, G. _Devl Biol._ 31, 362–379 (1973). Article  Google Scholar  * Chamley, J. H. & Dowel, J. J. _Expl Cell Res._ 90, 1–7 (1975). Article  CAS  Google Scholar  * Ebendal, T. & Jacobson, C. O. _Expl Cell Res._ 105, 379–387 (1977). Article  CAS  Google Scholar  * Ebendal, T. _J. Embryol. exp. Morph._ 61, 289–301 (1981). CAS  PubMed  Google Scholar  * Crain, S. M. & Peterson, E. R. _Devl Brain Res._ 2, 341–362 (1982). Article  Google Scholar  * Davies, A. M. & Lumsden, A. G. S. _J. comp. Neurol._ (in the press). * Ebendal, T. _Expl Cell Res._ 98, 159–169 (1976). Article  CAS  Google Scholar  * Stopak, D. & Harris, A. K. _Devl Biol._ 90, 383–398 (1982). Article  CAS  Google Scholar  * Bray, D. in _Cell Behaviour_ (eds Bellairs, R., Curtis, A. & Dunn, G.) 299–317 (Cambridge University Press, 1982). Google Scholar  * Davies, A. M., Lumsden, A. G. S., Slavkin, H. C. & Burnstock, G. _Devl Neurosci._ 4, 150–156 (1981). Article  CAS  Google Scholar  * Hamburger, V., Brunso-Bechtold, J. K. & Yip, J. _J. Neurosci._ 1, 60–71 (1981). Article  CAS  Google Scholar  * Hendry, I. A. & Campbell, J. _J. Neurocytol._ 5, 351–360 (1976). Article  CAS  Google Scholar  * Johnson, E. M., Gorin, P. D., Brandeis, L. D. & Pearson, J. _Science_ 210, 916–918 (1980). Article  ADS  CAS  Google Scholar  * Levi-Montalcini, R. & Booker, B. _Proc. natn. Acad. Sci. U.S.A._ 46, 384–391 (1960). Article  ADS  CAS  Google Scholar  * Harper, G. P., Pearce, F. L. & Vernon, C. _Devl Biol._ 77, 391–402 (1980). Article  CAS  Google Scholar  * Korsching, S. & Thoenen, H. _Proc. natn. Acad. Sci. U.S.A._ 80, 3513–3516 (1983). Article  ADS  CAS  Google Scholar  * Pearce, F. L., Banthorpe, D. V., Cook, J. M. & Vernon, C. A. _Eur. J. Biochem._ 32, 569–575 (1973). Article  CAS  Google Scholar  * Schubert, D. & Whitlock, C. _Proc. natn. Acad. Sci. U.S.A._ 74, 4055–4058 (1977). Article  ADS  CAS  Google Scholar  * Letourneau, P. C. _Devl Biol._ 44, 92–101 (1975). Article  CAS  Google Scholar  * Barde, Y. A., Edgar, D. & Thoenen, H. _A. Rev. Physiol._ 45, 601–612 (1983). Article  CAS  Google Scholar  * Adler, R., Manthorpe, M., Skaper, S. D. & Varon, S. _Brain Res._ 206, 129–144 (1981). Article  CAS  Google Scholar  * Collins, F. & Dawson, A. _J. Neurosci._ 2, 1005–1010 (1982). Article  CAS  Google Scholar  * Lander, A. D., Fujii, D. K., Gospodarowicz, D. & Reichardt, L. F. _J. Cell Biol._ 94, 574–585 (1982). Article  CAS  Google Scholar  * Collins, F. & Garrett, J. E. _Proc. natn. Acad. Sci. U.S.A._ 77, 6226–6228 (1980). Article  ADS  CAS  Google Scholar  * Adler, R. & Varon, S. _Devl Biol._ 81, 1–11 (1981). Article  CAS  Google Scholar  Download references AUTHOR INFORMATION Author notes * A. M. Davies Present address: Department of Anatomy, St George's Hospital Medical School, London, SW17 0RE, UK AUTHORS AND AFFILIATIONS * Department of Anatomy, Guy's Hospital Medical School, London, SE1 9RT, UK A. G. S. Lumsden & A. M. Davies Authors * A. G. S. Lumsden View author publications You can also search for this author inPubMed Google Scholar * A. M. Davies View author publications You can also search for this author inPubMed Google Scholar RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Lumsden, A., Davies, A. Earliest sensory nerve fibres are guided to peripheral targets by attractants other than nerve growth factor. _Nature_ 306, 786–788 (1983). https://doi.org/10.1038/306786a0 Download citation * Received: 15 April 1983 * Accepted: 17 October 1983 * Issue Date: 22 December 1983 * DOI: https://doi.org/10.1038/306786a0 SHARE THIS ARTICLE Anyone you share the following link with will be able to read this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative

ABSTRACT Recent studies have shown that developing nerve fibres grow directly to their targets1–4 and are guided by specific cues5,6, but the nature of these cues and the mechanism of


guidance remain unknown7,8. The growth of sympathetic axons towards an artificial source of nerve growth factor (NGF) _in vivo_9 and of sensory neurites up a concentration gradient of NGF


_in vitro_10,11 has supported the hypothesis that NGF, produced by target tissues, acts as a chemotactic attractant for these nerve fibres during development12. Both these studies and those


of the influence of NGF13,14 or target tissues15–19 on neurite growth _in vitro_ were conducted late in development when, following target encounter, the neurones had become dependent on NGF


or target for survival. Here we have co-cultured embryonic mouse sensory neurones and their peripheral target tissue at a stage preceding their contact _in vivo_. Neurites grew directly and


exclusively towards their own target but not to regionally inappropriate peripheral tissue. Antiserum to isogeneric NGF did not reduce this outgrowth but did reduce undirected neurite


outgrowth which occurred in co-cultures of older neurones with denervated target tissue. These results demonstrate that agents other than NGF guide neurites of NGF-responsive neurones in


development. Access through your institution Buy or subscribe This is a preview of subscription content, access via your institution ACCESS OPTIONS Access through your institution Subscribe


to this journal Receive 51 print issues and online access $199.00 per year only $3.90 per issue Learn more Buy this article * Purchase on SpringerLink * Instant access to full article PDF


Buy now Prices may be subject to local taxes which are calculated during checkout ADDITIONAL ACCESS OPTIONS: * Log in * Learn about institutional subscriptions * Read our FAQs * Contact


customer support SIMILAR CONTENT BEING VIEWED BY OTHERS MOTOR INNERVATION DIRECTS THE CORRECT DEVELOPMENT OF THE MOUSE SYMPATHETIC NERVOUS SYSTEM Article Open access 16 August 2024


SYMPATHETIC NEURONS SECRETE RETROGRADELY TRANSPORTED TRKA ON EXTRACELLULAR VESICLES Article Open access 04 March 2023 NEURONAL PROCESSES AND GLIAL PRECURSORS FORM A SCAFFOLD FOR WIRING THE


DEVELOPING MOUSE COCHLEA Article Open access 17 November 2020 REFERENCES * Holt, C. E. & Harris, W. A. _Nature_ 301, 150–152 (1983). Article  ADS  CAS  Google Scholar  * Honig, M. G. _J.


Physiol., Lond._ 330, 175–202 (1982). Article  CAS  Google Scholar  * Scott, S. A. _J. Physiol., Lond._ 330, 203–230 (1982). Article  CAS  Google Scholar  * Lance-Jones, C. &


Landmesser, L. _Proc. R. Soc._ B214, 1–18 (1981). ADS  CAS  Google Scholar  * Lance-Jones, C. & Landmesser, L. _J. Physiol., Lond._ 302, 559–580 (1980). Article  CAS  Google Scholar  *


Lance-Jones, C. & Landmesser, L. _Proc. R. Soc._ B214, 19–52 (1981). ADS  CAS  Google Scholar  * Purves, D. in _Repair and Regeneration of the Nervous System_ (ed. Nicholls, J. G.),


107–125 (Springer, Berlin, 1982). Book  Google Scholar  * Landmesser, L. in _Studies in Developmental Neurobiology_ (ed. Cowan, W. M.), 53–73 (Oxford University Press, 1981). Google Scholar


  * Menesini Chen, M. G., Chen, J. S. & Levi-Montalcini, R. _Arch. Ital. Biol._ 116, 53–84 (1978). CAS  PubMed  Google Scholar  * Letourneau, P. C. _Devl Biol._ 66, 183–196 (1978).


Article  CAS  Google Scholar  * Gundersen, R. W. & Barrett, J. N. _Science_ 206, 1079–1080 (1979). Article  ADS  CAS  Google Scholar  * Levi-Montalcini, R. _A. Rev. Neurosci._ 5, 341–362


(1982). Article  CAS  Google Scholar  * Charlwood, K. A., Lamont, D. M. & Banks, B. in _Nerve Growth Factor and its Antiserum_ (eds Zaimis, E. & Knight, J.) 102–107 (Athlone,


London, 1972). Google Scholar  * Rutishauser, U. & Edelman, G. M. _J. Cell Biol._ 87, 370–378 (1980). Article  CAS  Google Scholar  * Chamley, J. H., Goller, I. & Burnstock, G. _Devl


Biol._ 31, 362–379 (1973). Article  Google Scholar  * Chamley, J. H. & Dowel, J. J. _Expl Cell Res._ 90, 1–7 (1975). Article  CAS  Google Scholar  * Ebendal, T. & Jacobson, C. O.


_Expl Cell Res._ 105, 379–387 (1977). Article  CAS  Google Scholar  * Ebendal, T. _J. Embryol. exp. Morph._ 61, 289–301 (1981). CAS  PubMed  Google Scholar  * Crain, S. M. & Peterson, E.


R. _Devl Brain Res._ 2, 341–362 (1982). Article  Google Scholar  * Davies, A. M. & Lumsden, A. G. S. _J. comp. Neurol._ (in the press). * Ebendal, T. _Expl Cell Res._ 98, 159–169


(1976). Article  CAS  Google Scholar  * Stopak, D. & Harris, A. K. _Devl Biol._ 90, 383–398 (1982). Article  CAS  Google Scholar  * Bray, D. in _Cell Behaviour_ (eds Bellairs, R.,


Curtis, A. & Dunn, G.) 299–317 (Cambridge University Press, 1982). Google Scholar  * Davies, A. M., Lumsden, A. G. S., Slavkin, H. C. & Burnstock, G. _Devl Neurosci._ 4, 150–156


(1981). Article  CAS  Google Scholar  * Hamburger, V., Brunso-Bechtold, J. K. & Yip, J. _J. Neurosci._ 1, 60–71 (1981). Article  CAS  Google Scholar  * Hendry, I. A. & Campbell, J.


_J. Neurocytol._ 5, 351–360 (1976). Article  CAS  Google Scholar  * Johnson, E. M., Gorin, P. D., Brandeis, L. D. & Pearson, J. _Science_ 210, 916–918 (1980). Article  ADS  CAS  Google


Scholar  * Levi-Montalcini, R. & Booker, B. _Proc. natn. Acad. Sci. U.S.A._ 46, 384–391 (1960). Article  ADS  CAS  Google Scholar  * Harper, G. P., Pearce, F. L. & Vernon, C. _Devl


Biol._ 77, 391–402 (1980). Article  CAS  Google Scholar  * Korsching, S. & Thoenen, H. _Proc. natn. Acad. Sci. U.S.A._ 80, 3513–3516 (1983). Article  ADS  CAS  Google Scholar  * Pearce,


F. L., Banthorpe, D. V., Cook, J. M. & Vernon, C. A. _Eur. J. Biochem._ 32, 569–575 (1973). Article  CAS  Google Scholar  * Schubert, D. & Whitlock, C. _Proc. natn. Acad. Sci.


U.S.A._ 74, 4055–4058 (1977). Article  ADS  CAS  Google Scholar  * Letourneau, P. C. _Devl Biol._ 44, 92–101 (1975). Article  CAS  Google Scholar  * Barde, Y. A., Edgar, D. & Thoenen, H.


_A. Rev. Physiol._ 45, 601–612 (1983). Article  CAS  Google Scholar  * Adler, R., Manthorpe, M., Skaper, S. D. & Varon, S. _Brain Res._ 206, 129–144 (1981). Article  CAS  Google Scholar


  * Collins, F. & Dawson, A. _J. Neurosci._ 2, 1005–1010 (1982). Article  CAS  Google Scholar  * Lander, A. D., Fujii, D. K., Gospodarowicz, D. & Reichardt, L. F. _J. Cell Biol._ 94,


574–585 (1982). Article  CAS  Google Scholar  * Collins, F. & Garrett, J. E. _Proc. natn. Acad. Sci. U.S.A._ 77, 6226–6228 (1980). Article  ADS  CAS  Google Scholar  * Adler, R. &


Varon, S. _Devl Biol._ 81, 1–11 (1981). Article  CAS  Google Scholar  Download references AUTHOR INFORMATION Author notes * A. M. Davies Present address: Department of Anatomy, St


George's Hospital Medical School, London, SW17 0RE, UK AUTHORS AND AFFILIATIONS * Department of Anatomy, Guy's Hospital Medical School, London, SE1 9RT, UK A. G. S. Lumsden & 


A. M. Davies Authors * A. G. S. Lumsden View author publications You can also search for this author inPubMed Google Scholar * A. M. Davies View author publications You can also search for


this author inPubMed Google Scholar RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Lumsden, A., Davies, A. Earliest sensory nerve fibres are guided to


peripheral targets by attractants other than nerve growth factor. _Nature_ 306, 786–788 (1983). https://doi.org/10.1038/306786a0 Download citation * Received: 15 April 1983 * Accepted: 17


October 1983 * Issue Date: 22 December 1983 * DOI: https://doi.org/10.1038/306786a0 SHARE THIS ARTICLE Anyone you share the following link with will be able to read this content: Get


shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative