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Immunocytochemical evidence for the localization of the GM1 ganglioside in carbonic anhydrase-containing and RT 97-immunoreactive rat primary sensory neurons

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Journal of Neurocytology

Summary

Localization of GM1 ganglioside, the receptor for cholera toxin, and choleragenoid, which is the binding subunit of cholera toxin, was studied in the rat L5 dorsal root ganglion. Sections were incubated with choleragenoid and treated immunocytochemically. Choleragenoid-like immunoreactive cells were then examined for possible co-localization with carbonic anhydrase-like, RT 97 (antibody to neurofilament proteins), substance P-like, somatostatin-like and calcitonin gene-related peptide-like immunoreactivity and fluoride-resistant acid phosphatase (FRAP) activity, using adjacent sections. A subpopulation of dorsal root ganglion neurons exhibited choleragenoid-like immunoreactivity. The majority of these were medium-sized and large neurons. The strongest immunoreactivity was found in the area of the plasma membrane, but strong reactivity was also seen in the cytoplasm. The majority of the choleragenoid-like immunoreactive cells showed carbonic anhydrase-like and RT 97 immunoreactivity. Cells showing co-localization of choleragenoid-like and neuropeptide-like immunoreactivity or activity for FRAP were rarely observed. Our results suggest that the GM1 receptor is localized primarily on carbonic anhydrase-containing and RT 97-immunoreactive primary sensory neurons.

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References

  • Aldskogius, H., Arvidsson, J. &Hansson, P. (1988) Carbonic anhydrase enzyme histochemistry of cranial nerve primary sensory afferent neurons in the rat.Histochemistry 88, 151–4.

    PubMed  Google Scholar 

  • Anderton, B., Coakham, H. B., Garson, J. A., Harper, A. A., Harper, E. I. &Lawson, S. N. (1983) A monoclonal antibody against neurofilament protein specifically labels the large light cell population in rat dorsal root ganglia.journal of Physiology 334, 97–8P.

    Google Scholar 

  • Andres, K. H. (1961) Untersuchungen uber den Feinbau von Spinalganglien.Zeitschrift für Zellforschung und mikroskopische Anatomie 55, 1–48.

    Google Scholar 

  • Arvidsson, J. (1982) Somatotopic organization of vibrissae afferents in the trigeminal sensory nuclei of the rat studied by transganglionic transport of HRP.Journal of Comparative Neurology 211, 84–92.

    PubMed  Google Scholar 

  • Brown, A. G. (1981) Organization in the spinal cord. InThe Anatomy and Physiology of Identified Neurones, Berlin, Heidelberg, New York: Springer-Verlag.

    Google Scholar 

  • Cuatrecasas, P. (1973) Gangliosides and membrane receptors for cholera toxin.Biochemistry 12, 3558–66.

    PubMed  Google Scholar 

  • Dalsgaard, C. J., Ygge, J., Vincent, S. R., Ohrling, M., Dockray, G. J. &Elde, R. (1984) Peripheral projections and neuropeptide coexistence in a subpopulation of fluoride-resistant acid phosphatase reactive spinal primary sensory neurons.Neuroscience Letters 51, 139–44.

    PubMed  Google Scholar 

  • De Baecque, C., Johnson, A. B., Naiki, M., Schwarting, G. &Marcus, D. M. (1976) Ganglioside localization in cerebellar cortex: an immunoperoxidase study with antibody to GM1 ganglioside.Brain Research 114, 117–22.

    PubMed  Google Scholar 

  • Duce, I. R. &Keen, P. (1977) An ultrastructural classification of the neuronal cell bodies of the rat dorsal root ganglion using zinc iodide-osmium impregnation.Cell and Tissue Research 185, 263–77.

    PubMed  Google Scholar 

  • Ganser, A. L. &Kirschner, D. A. (1984) Differential expression of gangliosides on the surfaces of myelinated nerve fibers.Journal of Neuroscience Research 12, 245–55.

    PubMed  Google Scholar 

  • Ganser, A. L., Kirschner, D. A. &Willinger, M. (1983) Ganglioside localization on myelinated nerve fibres by cholera toxin binding.Journal of Neurocytology 12, 921–38.

    PubMed  Google Scholar 

  • Gibson, S. J., Polak, J. M., Bloom, S. R., Sabate, I. M., Mulderry, P. M., Ghatel, M. A., McGregor, G. P., Morrison, J. F. B., Kelly, J. S., Evans, R. M. &Rosenfeld, M. G. (1984) Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species.Journal of Neuroscience 4, 3101–11.

    PubMed  Google Scholar 

  • Harper, A. A. &Lawson, S. N. (1985) Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones.Journal of Physiology 359, 31–46.

    PubMed  Google Scholar 

  • Holmgren, J., Lönnrot, I. &Svennerholm, L. (1973) Tissue receptor for cholera exotoxin: postulated structure from studies with GM1 ganglioside and related glycolipids.Infection and Immunity 8, 208–14.

    PubMed  Google Scholar 

  • Hökfelt, T., Elde, R., Johansson, O., Luft, R. &Arimura, A. (1975a) Immunohistochemical evidence for the presence of somatostatin, a powerful inhibitory peptide, in some primary sensory neurons.Neuroscience Letters 1, 231–5.

    Google Scholar 

  • Hökfelt, T., Elde, R., Johansson, O., Luft, R., Nilsson, G. &Arimura, A. (1976) Immunohistochemical evidence for separate populations of somatostatin-containing and substance P-containing primary afferent neurons in the rat.Neuroscience 1, 131–6.

    PubMed  Google Scholar 

  • Hökfelt, T., Kellerth, J. O., Nilsson, G. &Pernow, B. (1975b) Substance P: Localization in the central nervous system and in some primary sensory neurons.Science 190, 889–90.

    PubMed  Google Scholar 

  • Jancso, G. &Kiraly, E. (1980) Distribution of chemosensitive primary sensory afferents in the central nervous system of the rat.Journal of Comparative Neurology 190, 781–92.

    PubMed  Google Scholar 

  • King, C. A. &Van Heyningen, W. E. (1973) Deactivation of cholera toxin by a sialidase-resistant monosialosyl-ganglioside.Journal of Infectious Diseases 127, 639–47.

    PubMed  Google Scholar 

  • Lamotte, C. (1977) Distribution of the tract of Lissauer and the dorsal root fibers in the primate spinal cord.Journal of Comparative Neurology 172, 529–62.

    PubMed  Google Scholar 

  • Larsson, L. I. (1983) Methods for immunocytochemistry of neurohormonal peptides. InMethods in Chemical Neuroanatomy (edited byBjörklund, A. &Hökfelt, T.), pp. 147–209. Amsterdam, New York, Oxford: Elsevier Science Publishers B.V.

    Google Scholar 

  • Lawson, S. N., Harper, A. A., Harper, E. I., Garson, J. A. &Anderton, B. H. (1984) A monoclonal antibody against neurofilament protein specifically labels a sub-population of rat sensory neurones.Journal of Comparative Neurology 228, 263–72.

    PubMed  Google Scholar 

  • Lawson, S. N., McCarthy, P. W., Waddell, P. J. &Jancso, G. (1987) Immunocytochemical and electro-physiological characterisation of rat dorsal root ganglion (DRG) neurones.7th European Winter Conference on Brain Research, p. 43.

  • Ledeen, R. W. (1985) Gangliosides of the neuron.Trends in Neuroscience 8, 169–74.

    Google Scholar 

  • Lee, K. H., Chung, K., Chung, J. M. &Coggeshall, R. E. (1986) Correlation of cell body size, axon size, and signal conduction velocity for individuality labelled dorsal root ganglion cells in the cat.Journal of Comparative Neurology 243, 335–46.

    PubMed  Google Scholar 

  • Lee, Y., Takami, K., Kawai, Y., Girgis, S., Hillyard, C. J., Macintyre, I., Emson, P. C. &Tohyama, M. (1985) Distribution of calcitonin gene-related peptide in the rat peripheral nervous system with reference to its coexistence with substance P.Neuroscience 15, 1227–37.

    PubMed  Google Scholar 

  • Libber-Man, A. R. (1976) Sensory ganglia. InThe Peripheral Nerve (edited byLandon, D. N.), pp. 188–278. London: Chapman & Hall.

    Google Scholar 

  • Light, A. R. &Perl, E. R. (1979) Reexamination of the dorsal root projection to. the spinal dorsal horn including observations on the differential termination of coarse and fine fibers.Journal of Comparative Neurology 186, 117–32.

    PubMed  Google Scholar 

  • Nagy, J. I. &Hunt, S. P. (1982) Fluoride-resistant acid phosphatase-containing neurones in dorsal root ganglia are separate from those containing substance P or somatostatin.Neuroscience 7, 89–97.

    PubMed  Google Scholar 

  • Nagy, J. I. &Hunt, S. P. (1983) The termination of primary afferents within the rat dorsal horn: evidence for rearrangement following capsaicin treatment.Journal of Comparative Neurology 218, 145–58.

    PubMed  Google Scholar 

  • Peyronnard, J. M., Charron, L., Lavoie, J., Messier, J. P. &Dubreuil, M. (1988) Carbonic anhydrase and horseradish peroxidase: double labelling of rat dorsal root ganglion neurons innervating motor and sensory peripheral nerves.Anatomy and Embryology 177, 353–9.

    PubMed  Google Scholar 

  • Price, J. (1985) An immunohistochemical and quantitative examination of dorsal root ganglion neuronal subpopulations.Journal of Neuroscience 5, 2051–9.

    PubMed  Google Scholar 

  • Rambourg, A., Clermont, Y. &Beaudet, A. (1983) Ultrastructural features of six types of neurons in rat dorsal root ganglia.Journal of Neurocytology 12, 47–66.

    PubMed  Google Scholar 

  • Riley, D. A., Ellis, S. &Bain, J. L. W. (1984) Ultrastructural cytochemical localization of carbonic anhydrase activity in rat peripheral sensory and motor nerves, dorsal root ganglia and dorsal column nuclei.Neuroscience 13, 189–206.

    PubMed  Google Scholar 

  • Robertson, B. &Arvidsson, J. (1985) Transganglionic transport of wheat germ agglutinin-HRP and choleragenoid-HRP in rat trigeminal primary sensory neurons.Brain Research 348, 44–51.

    PubMed  Google Scholar 

  • Robertson, B. &Grant, G. (1985) A comparison between wheat germ agglutinin- and choleragenoid-horseradish peroxidase as anterogradely transported markers in central branches of primary sensory neurones in the rat with some observations in the cat.Neuroscience 14, 895–905.

    PubMed  Google Scholar 

  • Skofitsch, G. &Jacobowitz, D. M. (1985) Calcitonin gene-related peptide coexists with substance P in capsaicin sensitive neurons and sensory ganglia of the rat.Peptides 6, 747–54.

    PubMed  Google Scholar 

  • Sommer, E. W., Kazimierczak, J. &Droz, B. (1985) Neuronal subpopulations in the dorsal root ganglion of the mouse as characterized by combination of ultrastructural and cytochemical features.Brain Research 346, 310–26.

    PubMed  Google Scholar 

  • Sugiura, Y., Lee, C. L. &Perl, E. R. (1986) Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin.Science 234, 358–61.

    PubMed  Google Scholar 

  • Szönyi, G., Knyihar, E. &Csillik, B. (1979) Extralysosomal, fluoride-resistant acid phosphatase-active neuronal system subserving nociception in the rat cornea.Zeitschrift für Mikroskopisch-Anatomische Forschung, Leipzig 93, 974–81.

    Google Scholar 

  • Trojanowski, J. Q., Gonatas, J. O. &Gonatas, N. K. (1981) Conjugates of horseradish peroxidase (HRP) with cholera toxin and wheat germ agglutinin are superior to free HRP as orthogradely transported markers.Brain Research 223, 381–5.

    PubMed  Google Scholar 

  • Trojanowski, J. Q., Gonatas, J. O. &Gonatas, N. K. (1982) Horseradish peroxidase (HRP) conjugates of cholera toxin and lectins are more sensitive retrogradely transported markers than free HRP.Brain Research 231, 33–50.

    PubMed  Google Scholar 

  • Wan, X. C. S., Trojanowski, J. Q. &Gonatas, J. O. (1982) Cholera toxin and wheat germ agglutinin conjugates as neuroanatomical probes: their uptake and clearance, transganglionic and retrograde transport and sensitivity.Brain Research 243, 215–24.

    PubMed  Google Scholar 

  • Wiesenfeld-Hallin, Z., Hökfelt, T., Lundberg, J. M., Forssmann, W. G., Reinecke, M., Tschopp, F. A. &Fischer, J. A. (1984) Immunoreactive calcitonin generelated peptide and substance P coexist in sensory neurons to the spinal cord and interact in spinal behavioral responses of the rat.Neuroscience Letters 52, 199–204.

    PubMed  Google Scholar 

  • Willinger, M. &Schachner, M. (1980) GM1 ganglioside as a marker for neuronal differentiation in mouse cerebellum.Developmental Biology 74, 101–17.

    PubMed  Google Scholar 

  • Wong, V., Barrett, C. P., Donati, E. J., Eng, L. F. &Guth, L. (1983) Carbonic anhydrase activity in first-order sensory neurons of the rat.Journal of Histochemistry and Cytochemistry 31, 293–300.

    PubMed  Google Scholar 

  • Wong, V., Barrett, C. P., Donati, E. J. &Guth, L. (1987) Distribution of carbonic anhydrase activity in neurons of the rat.journal of Comparative Neurology 257, 122–9.

    PubMed  Google Scholar 

  • Wood, J. N. &Anderton, B. H. (1981) Monoclonal antibodies to mammalian neurofilaments.Bioscience Reports 1, 263–8.

    PubMed  Google Scholar 

  • Yamadori, T. (1970) A light and electron microscopic study on the postnatal development of spinal ganglia in rats.Acta Anatomica Nipponica 45, 191–205.

    PubMed  Google Scholar 

  • Yoshida, S. &Matsuda, Y. (1979) Studies on sensory neurons of the mouse with intracellular-recording and horseradish peroxidase-injection techniques.Journal of Neurophysiology 42, 1134–45.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, Karolinska Institutet, Box 60400, S-10401, Stockholm, Sweden

    Brita Robertson & Gunnar Grant

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  1. Brita Robertson
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  2. Gunnar Grant
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The main part of this study was carried out in the laboratory of Dr Lana R. Skirboll, Clinical Neuroscience Branch, NIMH, National Institutes of Health, Bethesda, MD 20892, USA.

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Robertson, B., Grant, G. Immunocytochemical evidence for the localization of the GM1 ganglioside in carbonic anhydrase-containing and RT 97-immunoreactive rat primary sensory neurons. J Neurocytol 18, 77–86 (1989). https://doi.org/10.1007/BF01188426

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  • DOI: https://doi.org/10.1007/BF01188426

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