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Changes in lectin binding of lumbar dorsal root ganglia neurons and peripheral axons after sciatic and spinal nerve injury in the rat

Cell and Tissue Research volume 257, pages 379–388 (1989)Cite this article

Summary

The effects of chronic lesions of rat lumbar spinal or sciatic nerves on the binding of Glycine max (soybean) agglutinin to galacto-conjugates, in small-and medium-size primary sensory neurons of the L4 and L5 dorsal root ganglia, were examined over a 580-day period. Spinal nerve section resulted in a marked decrease in the population of stained neurons within 7 days. However, despite some retrograde morphological changes triggered by axonal injury, the proportion of stained nerve cells was normalized 180 days postoperatively. This temporary decrease in perikaryal lectin reactivity was initially associated with a marked accumulation of stained material in the nerve, proximal and distal to the site of section, with similar accumulations also being noticeable at each level of injury in sciatic nerves subjected to double ligature. This may reflect the presence of glycocompounds linked to the autolysis of nerve fibers during the phase of retrograde dying-back and Wallerian degeneration. At later stages, stained deposits could be seen scattered along central and peripheral axonal processes of the dorsal root ganglion neurons in the vicinity of the cell body. They may indicate a disturbance in the peripheral turnover of glycoproteins in chronically-transected nerves, with piling up of neuronal products. Sciatic nerve injury caused similar but less severe effects which, except for the L4 ganglion cells, were rapidly reversible.

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References

  • Aldskogius H, Arvidsson J, Grant G (1985) The reaction of primary sensory neurons to peripheral nerve injury with particular emphasis on transganglionic changes. Brain Res Rev 10:27–46

    Google Scholar 

  • Arvidsson J, Ygge J, Grant G (1986) Cell loss in lumbar dorsal root ganglia and transganglionic degeneration after sciatic nerve resection in the rat. Brain Res 373:15–21

    Google Scholar 

  • Barbut D, Polak JM, Wall PD (1981) Substance P in spinal cord dorsal horn decreases following peripheral nerve injury. Brain Res 205:289–298

    Google Scholar 

  • Barron KD (1983) Comparative observations on the cytologic reactions of central and peripheral nerve cells to axotomy. In: Kao CC, Bunge RP, Reier PJ (eds) Spinal cord reconstruction. Raven Press, New York, pp 7–40

    Google Scholar 

  • Bisby MA, Keen P (1986) Regeneration of primary afferent neurons containing substance P-like immunoreactivity. Brain Res 365:85–95

    Google Scholar 

  • Blümcke S, Niedorf HR, Rode J (1966) Axoplasmic alterations in the proximal and distal stumps of transected nerves. Acta Neuropathol 7:44–61

    Google Scholar 

  • Borges LF, Sidman RL (1982) Axonal transport of lectins in the peripheral nervous system. J Neurosci 2:647–653

    Google Scholar 

  • Csillik B (1984) Nerve growth factor regulates central terminals of primary sensory neurons. Z Mikrosk Anat Forsch 98:11–16

    Google Scholar 

  • Devor M, Claman D (1980) Mapping and plasticity of acid phosphatase afferents in the rat dorsal horn. Brain Res 190:17–28

    Google Scholar 

  • Devor M, Wall PD (1981) Plasticity in the spinal cord sensory map following peripheral nerve injury in rats. J Neurosci 1:679–684

    Google Scholar 

  • Devor M, Wall PD, McMahon SB (1984) Dichotomizing somatic nerve fibers exist in rats but they are rare. Neurosci Lett 49:187–192

    Google Scholar 

  • Devor M, Govrin-Lippmann R, Frank I, Raber P (1985) Proliferation of primary sensory neurons in adult rat dorsal root ganglion and the kinetics of retrograde cell loss after sciatic nerve section. Somatosens Res 3:139–167

    Google Scholar 

  • Dodd J, Jessell TM (1985) Lactoseries carbohydrates specify subsets of dorsal root ganglion neurons projecting to the superficial dorsal horn of rat spinal cord. J Neurosci 5:3278–3294

    Google Scholar 

  • Dolapchieva S, Ichev K, Ovtscharoff W (1986) Lectin binding sites in axon-myelin-Schwann cell complex. Acta Histochem Cytochem 19:253–261

    Google Scholar 

  • Duce IR, Keen P (1976) A light and electron microscope study of changes occurring at the cut ends following section of the dorsal roots of rat spinal nerves. Cell Tissue Res 170:491–505

    Google Scholar 

  • Estruch R, Damjanov I (1986) Lectin histochemistry applied to human nerves. Arch Pathol Lab Med 110:730–735

    Google Scholar 

  • Everly JL, Brady RO, Quarles RH (1973) Evidence that the major protein in rat sciatic nerve myelin is a glycoprotein. J Neurochem 21:329–334

    Google Scholar 

  • Figlewicz DA, Quarles RH, Johnson D, Barbarash GR, Stern-berger NH (1981) Biochemical demonstration of the myelin-associated glycoprotein in the peripheral nervous system. J Neurochem 37:749–758

    Google Scholar 

  • Fischer J, Csillik B (1985) Lectin binding: a genuine marker for transganglionic regulation of human primary sensory neurons. Neurosci Lett 54:263–267

    Google Scholar 

  • Fitzgerald M, Wall PD, Goedert M, Emson PC (1985) Nerve growth factor counteracts the neurophysiological and neurochemical effects of chronic sciatic nerve section. Brain Res 332:131–141

    Google Scholar 

  • Friede RL, Bischhausen R (1980) The fine structure of stumps of transected nerve fibers in subserial sections. J Neurol Sci 44:181–203

    Google Scholar 

  • Gulati AK, Zalewski AA, Sharma KB, Ogrowsky D, Sohal GS (1986) A comparison of lectin binding in rat and human peripheral nerve. J Histochem Cytochem 34:1487–1493

    Google Scholar 

  • Guzman-Harty M, Warner JK, Mancini ME, Pearl DK, Yates AJ (1988) Effect of crush lesion on radiolabelling of ganglioside in rat peripheral nerve. J Neurochem 50:237–242

    Google Scholar 

  • Harry GJ, Goodrum JF, Toews AR, Morell P (1987) Axonal transport characteristics of gangliosides in sensory axons of rat sciatic nerve. J Neurochem 48:1529–1536

    Google Scholar 

  • Holtzman E, Novikoff AB (1965) Lysosomes in the rat sciatic nerve following crush. J Cell Biol 27:651–669

    Google Scholar 

  • Jessell TM, Dodd J (1986) Neurotransmitters and differentiation antigens in subsets of sensory neurons projecting to the spinal dorsal horn. In: Martin JB, Barchas JD (eds) Neuropeptides in neurologic and psychiatric disease. Raven Press, New York, pp 111–133

    Google Scholar 

  • Jessell T, Tsunoo A, Kanazawa I, Otsuka M (1979) Substance P: depletion in the dorsal horn of rat spinal cord after section of the peripheral processes of primary sensory neurons. Brain Res 168:247–259

    Google Scholar 

  • Kapeller K, Mayor D (1969) An electron microscopic study of the early changes proximal to a constriction in sympathetic nerves. Proc R Soc Lond [Biol] 172:39–51

    Google Scholar 

  • Knyihar E, Csillik B (1976) Effect of peripheral axotomy on the fine structure and histochemistry of the Rolando substance: degenerative atrophy of central processes of pseudounipolar cells. Exp Brain Res 26:73–87

    Google Scholar 

  • Knyihar-Csillik E, Bezzegh A, Böti S, Csillik B (1986) Thiamine monophosphatase: a genuine marker for transganglionic regulation of primary sensory neurons. J Histochem Cytochem 34:363–371

    Google Scholar 

  • Knyihar-Csillik E, Rakic P, Csillik B (1987) Transganglionic degenerative atrophy in the substantia gelatinosa of the spinal cord after peripheral nerve transection in rhesus monkeys. Cell Tissue Res 247:599–604

    Google Scholar 

  • Langford LA, Coggeshall RE (1981) Branching of sensory axons in the peripheral nerve of the rat. J Comp Neurol 203:745–750

    Google Scholar 

  • Lehmann EL (1975) Nonparametrics: statistical methods based on ranks. In: Lehmann EL (ed) Holden-Day series in probability and statistics, McGraw-Hill, New York, pp 123–132

    Google Scholar 

  • Lieberman AR (1971) The axonal reaction: a review of the principal features of perikaryal responses to axon injury. Int Rev Neurobiol 14:49–124

    Google Scholar 

  • Lis H, Sela B, Sachs L, Sharon N (1970) Specific inhibition by N-acetyl-D-galactosamine of the interaction between soybean agglutinin and animal cell surfaces. Biochim Biophys Acta 211:582–585

    Google Scholar 

  • Matthieu JM, Everly JL, Brady RO, Quarles RH (1975) [35S]Sulfate incorporation into myelin glycoproteins. II. Peripheral nervous tissue. Biochim Biophys Acta 392:167–174

    Google Scholar 

  • McGregor GP, Gibson SJ, Sabate IM, Blank MA, Christofides ND, Wall PD, Polak JM, Bloom SR (1984) Effect of peripheral nerve section and nerve crush on spinal cord neuropeptides in the rat; increased VIP and PHI in the dorsal horn. Neuroscience 13:207–216

    Google Scholar 

  • McMahon SB, Wall PD (1987) Physiological evidence for branching of peripheral unmyelinated sensory afferent fibers in the rat. J Comp Neurol 261:130–136

    Google Scholar 

  • Miller RG (1981) Simultaneous statistical inference. Springer, Berlin Heidelberg New York, pp 48–67

    Google Scholar 

  • Mori K (1986) Lectin Ulex europaeus agglutinin I specifically labels a subset of primary afferent fibers which project selectively to the superficial dorsal horn of the spinal cord. Brain Res 365:404–408

    Google Scholar 

  • Mori K (1987) Specific carbohydrate expression by small-diameter subclasses of rabbit trigeminal, glossopharyngeal, and vagal afferent fibers studied with the lectin Ulex europaeus agglutinin I. Neurosci Res 4:291–303

    Google Scholar 

  • Nakagawa F, Schulte BA, Spicer SS (1986) Lectin cytochemical evaluation of somatosensory neurons and their peripheral and central processes in rat and man. Cell Tissue Res 245:579–589

    Google Scholar 

  • Peyronnard JM, Charron L, Lavoie J, Messier JP (1986) Differences in horseradish peroxidase labeling of sensory, motor and sympathetic neurons following chronic axotomy of the rat sural nerve. Brain Res 364:137–150

    Google Scholar 

  • Peyronnard JM, Charron L, Messier JP, Lavoie J (1988) Effects of distal and proximal nerve lesion on carbonic anhydrase activity in rat primary sensory neurons, ventral and dorsal root axons. Exp Brain Res 70:550–560

    Google Scholar 

  • Pierau FK, Taylor DCM, Abel W, Friedrich B (1982) Dichotomizing peripheral fibres revealed by intracellular recording from rat sensory neurones. Neurosci Lett 31:123–128

    Google Scholar 

  • Regan LJ, Dodd J, Barondes SH, Jessell TM (1986) Selective expression of endogenous lactose-binding lectins and lactoseries glycoconjugates in subsets of rat sensory neurons. Proc Natl Acad Sci USA 83:2248–2252

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Google Scholar 

  • Rich KM, Luszczynski JR, Osborne PA, Johnson EM (1987) Nerve growth factor protects adult sensory neurons from cell death and atrophy caused by nerve injury. J Neurocytol 16:261–268

    Google Scholar 

  • Sternberger NH, Quarles RH, Itoyama Y, Webster HdeF (1979) Myelin-associated glycoprotein demonstrated immunocytochemically in myelin and myelin-forming cells of developing rat. Proc Natl Acad Sci USA 76:1510–1514

    Google Scholar 

  • Streit WJ, Schulte BA, Balentine JD, Spicer SS (1985) Histochemical localization of galactose-containing glycoconjugates in sensory neurons and their processes in the central and peripheral nervous system of the rat. J Histochem Cytochem 33:1042–1052

    Google Scholar 

  • Streit WJ, Schulte BA, Balentine JD, Spicer SS (1986) Evidence for glycoconjugate in nociceptive primary sensory neurons and its origin from the Golgi complex. Brain Res 377:1–17

    Google Scholar 

  • Tenser RB (1985) Sequential changes of sensory neuron (fluorideresistant) acid phosphatase in dorsal root ganglion neurons following neurectomy and rhizotomy. Brain Res 332:386–389

    Google Scholar 

  • Tessler A, Himes BT, Krieger NR, Murray M, Goldberger ME (1985) Sciatic nerve transection produces death of dorsal root ganglion cells and reversible loss of substance P in spinal cord. Brain Res 332:209–218

    Google Scholar 

  • Wall PD, Devor M (1981) The effect of peripheral nerve injury on dorsal root potentials and on transmission of afferent signals into the spinal cord. Brain Res 209:95–111

    Google Scholar 

  • Ygge J, Aldskogius H, Grant G (1981) Asymmetries and symmetries in the number of thoracic dorsal root ganglion cells. J Comp Neurol 202:365–372

    Google Scholar 

  • Zelena J, Lubinska L, Gutmann E (1968) Accumulation of organelles at the ends of interrupted axons. Z Zellforsch 91:200–219

    Google Scholar 

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Affiliations

  1. Centre de recherche en sciences neurologiques and Hôpital Hôtel-Dieu, Succursale A, Case postale 6208, H3C 3T8, Montréal, Québec, Canada

    Jean-Marie Peyronnard, Louise Charron, Jean-Pierre Messier, Jeanne Lavoie & Feliciana Faraco-Cantin

  2. Département d'informatique et de recherche opérationnelle, Université de Montréal, Montréal, Canada

    Christian Leger

Authors
  1. Jean-Marie Peyronnard
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  2. Louise Charron
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  3. Jean-Pierre Messier
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  4. Jeanne Lavoie
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  5. Christian Leger
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  6. Feliciana Faraco-Cantin
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Peyronnard, JM., Charron, L., Messier, JP. et al. Changes in lectin binding of lumbar dorsal root ganglia neurons and peripheral axons after sciatic and spinal nerve injury in the rat. Cell Tissue Res. 257, 379–388 (1989). https://doi.org/10.1007/BF00261840

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  • DOI: https://doi.org/10.1007/BF00261840

Key words

  • Lectins
  • Cytochemistry
  • Dorsal root ganglia
  • Axotomy
  • Rat (Sprague-Dawley)