Abstract
Data on the presence of NGF receptors in the satellite cells of spinal ganglia are scanty and contradictory. In the present study we used immunocytochemistry to examine the distribution of these receptors in spinal ganglia of the adult rat by light and electron microscopy. We found that (1) all satellite cells were immmunoreactive to p75 and the mean density of gold particles (mean number per μm2) was significantly greater in the satellite cell sheath than in the nerve cell body; (2) numerous satellite cells were immunoreactive for trkA with a mean density of gold particles slightly greater in the satellite cell sheath than in the nerve cell body, although the difference was not statistically significant; (3) both p75 and trkA immunoreactivity were confined to the cytoplasm. We suggest that the p75 receptor may be involved in the NGF-induced outgrowth of slender projections from the nerve cell body surface. With regard to the trkA receptor, satellite cells might be supported trophically by NGF released from the neuron with which they are associated; alternatively, satellite cells might internalize NGF to constitute a reservoir for later release to the neuron.
Similar content being viewed by others
References
Althaus, H. H. & Richter-Landsberg, C. (2000) Glial cells as targets and producers of neurotrophins. International Review of Cytology 197, 203–277.
Barbacid, M. (1993) Nerve growth factor: A tale of two receptors. Oncogene 8, 2033–2042.
Barde, Y.-A. (1999) Biological roles of neurotrophins. In Neurotrophic Factors (edited by Hefti, F.) pp. 1–31. Berlin, Heidelberg & New York: Springer-Verlag.
Bennett, D. L., Dmietrieva, N, Priestley, J. V., Clary, D. & McMahon, S B. (1996) trkA,CGRPand IB4 expression in retrogradely labelled cutaneous and visceral primary sensory neurones in the rat. Neuroscience Letters 206, 33–36.
Ben-Ze'ev, A., Farmer, S. R. & Penman, S. (1980) Protein synthesis requires cell-surface contact while nuclear events respond to cell shape in anchoragedependent fibroblasts. Cell 21, 365–372.
Carbonetto, S. & Stach, R. W. (1982) Localization of nerve growth factor bound to neurons growing nerve fibers in culture. Developmental Brain Research 3, 463–473.
Carroll, S. L., Silos-Santiago, I., Frese, S. E., Ruit K. G., Milbrandt, J. & Snider, W. D. (1992) Dorsal root ganglion neurons expressing trk are selectively sensitive to NGF deprivation in utero. Neuron 9, 779–788.
Connolly, J. L., Green, S. A. & Greene, L. A. (1981) Pit formation and rapid changes in surface morphology of sympathetic neurons in response to nerve growth factor. Journal of Cell Biology 90, 176–180.
Davies, A. M. (1994) The role of neurotrophins in the developing nervous system. Journal of Neurobiology 25, 1334–1348.
Deng, L. L. Y.-S. & Zhou, X.-F. (2000) Downregulation of TrkA expression in primary sensory neurons after unilateral lumbar spinal nerve transection and some rescuing effects of nerve growth factor infusion. Neuroscience Research 38, 183–191.
Distefano, P. S. & Johnson, E. M. Jr. (1988) Nerve growth factor receptors on cultured rat Schwann cells. Journal of Neuroscience 8, 231–241.
Ernfors, P., Rosario, C. M., Merlio, J.-P., Grant, G., Aldskogius, H. & Persson, H. (1993) Expression of mRNAs for neurotrophin receptors in the dorsal root ganglion and spinal cord during development and following peripheral or central axotomy. Molecular Brain Research 17, 217–226.
Gallo, G. (1998) Personal communication.
Gallo, G., Lefcort, F. B. & Letourneau, P. C. (1997) The trkA receptor mediates growth cone turning toward a localized source of nerve growth factor. Journal of Neuroscience 17, 5445–5454.
Gibney, J. & Zheng, J. Q. (2003) Cytoskeletal dynamics underlying collateral membrane protrusions induced by neurotrophins in cultured Xenopus embryonic neurons. Journal of Neurobiology 54, 393–405.
Gray, E. G. (1969) Electron microscopy of the glio-vascular organization of the brain of Octopus. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 255, 13–32.
Johnson, D., Lanahan, A., Buck, C. R., Sehgal, A., Morgan, C., Mercer, E., Bothwell, M. & Chao, M. (1986) Expression and structure of thehuman NGF receptor. Cell 47, 545–554.
Johnson, E. M. Jr, Rich, K. M. & Yip, H. K. (1986) The role of NGF in sensory neurons in vivo. Trends in Neurosciences 9, 33–37.
Josephson, A., Widenfalk, J., Trifunovski, A., Widmer, H. R., Olson, L. & Spenger, C. (2001) GDNFandNGFfamilymembersand receptors inhuman fetalandadult spinal cordanddorsal root ganglia. Journal of Comparative Neurology 440, 204–217.
Kaplan, D. R., Hempstead, B. L., Martin-Zanca, D., Chao, M. V. & Parada, L. F. (1991) The trk proto-oncogene product: A signal transducing receptor for nerve growth factor. Science 252, 554–558.
Karchewski, L. A., Kim, F. A., Johnston, J., Mcknight, R. M. & Verge, V. M. K. (1999) Anatomical evidence supporting the potential for modulation by multiple neurotrophins in the majority of adult lumbar sensory neurons. Journal of Comparative Neurology 413, 327–341.
Kashiba, H., Noguchi, K., Ueda, Y. & Senba, E. (1995) Coexpression of trk family members and low-affinity neurotrophin receptors in rat dorsal root ganglion neurons. Molecular Brain Research 30, 158–164.
Kashiba, H., Uchida, Y. & Senba, E. (2003) Distribution and colocalization of NGF and GDNF family ligand receptor mRNAs in dorsal root and nodose ganglion neurons of adult rats. Molecular Brain Research 110, 52–62.
Khorooshi, M. H., Hansen, B. F., Keeling, J. W., Nolting, D. S. & Kjaer, I. M. (2001) p75NGFR immunoreactivity in normal prenatal human dorsal root ganglia. Pediatric Neurology 25, 401–404.
Klein, R., Jing, S., Nanduri, V., O'Rourke, E. & Barbacid, M. (1991) The trk proto-oncogene encodes a receptor for nerve growth factor. Cell 65, 189–197.
Korsching, S. (1986) The role of nerve growth factor in the CNS. Trends in Neurosciences 9, 570–573.
Lanlua, P., Decorti, F., Gangula, P. R. R., Chung, K., Taglialatela, G. & Yallampalli, C. (2001) Female steroid hormones modulate receptors for nerve growth factor in rat dorsal root ganglia. Biology of Reproduction 64, 331–338.
Lee, S. E., Shen, H., Taglialatela, G., Chung, J. M. & Chung, K. (1998) Expression of nerve growth factor in the dorsal root ganglion after peripheral nerve injury. Brain Research 796, 99–106.
Lemke, G. & Chao, M. (1988) Axons regulate Schwann cell expression of the major myelin and NGF receptor genes. Development 102, 499–504.
Lindsay, R. M. (1996) Role of neurotrophins and trk receptors in the development and maintenance of sensory neurons: An overview. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 351, 365–373.
Lindsay, R. M., Shooter, E. M., Radeke, M. J., Misko, T. P., Dechant, G., Thoenen, H. & Lindholm, D. (1990) Nerve growth factor regulates expression of the nerve growth factor receptor gene in adult sensory neurons. European Journal of Neuroscience 2, 389–396.
Martin-Zanca, D., Barbacid, M. & 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 & Development 4, 683–694.
McMahon, S. B., Armanini, M. P., Ling, L. H. & 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.
Ming, G.-L., Lohof, A. M. & Zheng, J. Q. (1997) Acute morphogenic and chemotropic effects of neurotrophins on cultured embryonic Xenopus spinal neurons. Journal of Neuroscience 17, 7860–7871.
Mu, X., Silos-Santiago, I., Carroll, S. L. & Snider, W. D. (1993) Neurotrophin receptor genes are expressed in distinct patterns in developing dorsal root ganglia. Journal of Neuroscience 13, 4029–4041.
Murray, S. S. & Cheema, S. S. (2003) Constitutive expression of the low-affinity neurotrophin receptor and changes during axotomy-induced death of sensory neurones in the neonatal rat dorsal root ganglion. Journal of Anatomy 202, 227–238.
Pannese, E. (1981) The satellite cells of the sensory ganglia. Advances in Anatomy Embryology and Cell Biology 65, 1–111. Berlin, Heidelberg & New York: Springer-Verlag.
Pannese, E. (1994) Neurocytology. Fine Structure of Neurons, Nerve Processes, and Neuroglial Cells. Stuttgart: Georg Thieme Verlag.
Pannese, E. (2002) Perikaryal surface specializations of neurons in sensory ganglia. International Review of Cytology 220, 1–34.
Pannese, E., Bianchi, R., Gioia, M. & Ventura, R. (1985) A quantitative electron microscope study of the perikaryal projections of sensory ganglion neurons. II. Gecko and lizard. Journal of Comparative Neurology 240, 212–218.
Pannese, E., Gioia, M., Carandente, O. & Ventura, R. (1983) A quantitative electron microscope study of the perikaryal projections of sensory ganglion neurons. I. Cat and rabbit. Journal of Comparative Neurology 214, 239–250.
Qiao, L. & Vizzard, M. A. (2002) Up-regulation of tyrosine kinase (Trka, Trkb) receptor expression and phosphorylation in lumbosacral dorsal root ganglia after chronic spinal cord (T8–T10) injury. Journal of Comparative Neurology 449, 217–230.
Richardson, P. M., Verge Issa, V. M. K. & Riopelle, R. J. (1986) Distribution of neuronal receptors for nerve growth factor in the rat. Journal of Neuroscience 6, 2312–2321.
Rifkin, J. T., Todd, V. J., Anderson, L. W. & Lefcort, F. (2000) Dynamic expression of neurotrophin receptors during sensory neuron genesis and differentiation. Developmental Biology 227, 465–480.
Rohrer, H. (1985) Nonneuronal cells from chick sympathetic and dorsal root sensory ganglia express catecholamine uptake and receptors for nerve growth factor during development. Developmental Biology 111, 95–107.
Scala, C., Cenacchi, G., Ferrari, C., Pasquinelli, G., Preda, P. & Manara, G. C. (1992) A new acrylic resin formulation: A useful tool for histological, ultrastructural, and immunocytochemical investigations. Journal of Histochemistry and Cytochemistry 40, 1799–1804.
Scala, C., Preda, P., Cenacchi, G., Badiali de Giorgi, L., Martini, D., Borsetti, G. & pasquinelli, G. (1995) Modificazione della resina acrilica Bioacryl per la formulazione di nuovi polimeri applicabili in metodi di inclusione a basse temperature e di sezionamento mediante abrasione controllata. Societ'a italiana di microscopia elettronica, Atti del XX Congresso, Rimini 1995, 63–64.
Sebert, M. E. & Shooter, E. M. (1993) Expression of mRNA for neurotrophic factors and their receptors in the rat dorsal root ganglion and sciatic nerve following nerve injury. Journal of Neuroscience Research 36, 357–367.
Shelton, D. L. & Reichardt, L. F. (1984) Expression of the β-nerve growth factor gene correlates with the density of sympathetic innervation in effector organs. Proceedings of the National Academy of Sciences of the USA 81, 7951–7955.
Shen, H., Chung, J. M., Coggeshall, R. E. & Chung, K. (1999) Changes in trkA expression in the dorsal root ganglion after peripheral nerve injury. Experimental Brain Research 127, 141–146.
Sobue, G., Yasuda, T., Mitsuma, T. & Pleasure, D. (1989) Nerve growth factor receptor immunoreactivity in the neuronal perikarya of human sensory and sympathetic nerve ganglia. Neurology 39, 937–941.
Spoerri, P. E., Petrelli, L., Guidolin, D. & Skaper, S. D. (1993) Colocalization of low-and highaffinity NGF receptors on PC12 cells, C6 glioma cells and dorsal root ganglion neurons. European Journal of Cell Biology 61, 256–263.
Suburo, A. M., Gu, X.-H., Moscoso, G., Ross, A., Terenghi, G. & Polak, J. M. (1992) Developmental pattern and distribution of nerve growth factor low-affinity receptor immunoreactivity in human spinal cord and dorsal root ganglia: Comparison with synaptophysin, neurofilament and neuropeptide immunoreactivities. Neuroscience 50, 467–482.
Taniuchi, M., Clark, H. B. & Johnson, E. M. Jr. (1986) Induction of nerve growth factor receptor in Schwann cells after axotomy. Proceedings of the National Academy of Sciences of the USA 83, 4094–4098.
Taniuchi, M., Clark, H. B., Schweitzer, J. B. & Johnson, E. M. Jr. (1988) Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: Ultrastructural location, suppression by axonal contact, and binding properties. Journal of Neuroscience 8, 664–681.
Thoenen, H. & Barde, Y.-A. (1980) Physiology of nerve growth factor. Physiological Reviews 60, 1284–1335.
Vega, J. A., Vazquez, E., Naves, F. J., del Valle, M. E., calzada, B. & Represa, J. J. (1994) Immunohistochemical localization of the high-affinity NGF receptor (gp140-trkA) in the adult human dorsal root and sympathetic ganglia and in the nerves and sensory corpuscles supplying digital skin. Anatomical Record 240, 579–588.
Verge, V. M. K., Merlio, J.-P., Grondin, J., Ernfors, P., Persson, H., Riopelle, R. J., HÖkfelt, T. & Richardson, P. M. (1992) Colocalization of NGF binding sites, trk mRNA, and lowaffinity NGF receptor mRNA in primary sensory neurons: Responses to injury and infusion of NGF. Journal of Neuroscience 12, 4011–4022.
Verge, V. M., Richardson, P. M., Benoit, R. & Riopelle, R. J. (1989) Histochemical characterization of sensory neurons with high-affinity receptors for nerve growth factor. Journal of Neurocytology 18, 583–591.
Wetmore, C. & Olson, L. (1995) Neuronal and nonneuronal expression of neurotrophins and their receptors in sensory and sympathetic ganglia suggest new intercellular trophic interactions. Journal of Comparative Neurology 353, 143–159.
Wright, D. E. & Snider, W. D. (1995) Neurotrophin receptor mRNA expression defines distinct populations of neurons in rat dorsal root ganglia. Journal of Comparative Neurology 351, 329–338.
Yamamoto, M., Sobue, G., Li, M., Arakawa, Y., Mitsuma, T. & Kimata, K. (1993) Nerve growth factor (NGF), brain-derived neurotrophic factor (BDNF) and low-affinity nerve growth factor receptor (LNGFR) mRNA levels in cultured rat Schwann cells; differential time-and dose-dependent regulation by cAMP. Neuroscience Letters 152, 37–40.
Yasuda, T., Sobue, G., Mokuno, K., Kreider, B. & Pleasure, D. (1987) Cultured rat Schwann cells express low affinity receptors for nerve growth factor. Brain Research 436, 113–119.
Zhou, X.-F., Rush, R. A. & McLachlan, E. M. (1996) Differential expression of the p75 nerve growth factor receptor in glia and neurons of the rat dorsal root ganglia after peripheral nerve transection. Journal of Neuroscience 16, 2901–2911.
Zimmermann, A. & Sutter, A. (1983) β-nerve growth factor (βNGF)receptors on glial cells. Cell-cell interaction between neurones and Schwann cells in cultures of chick sensory ganglia. EMBO Journal 2, 879–885.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Pannese, E., Procacci, P. Ultrastructural localization of NGF receptors in satellite cells of the rat spinal ganglia. J Neurocytol 31, 755–763 (2002). https://doi.org/10.1023/A:1025708132119
Issue Date:
DOI: https://doi.org/10.1023/A:1025708132119