Cell and Tissue Research

, Volume 257, Issue 2, pp 379–388 | Cite as

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

  • Jean-Marie Peyronnard
  • Louise Charron
  • Jean-Pierre Messier
  • Jeanne Lavoie
  • Christian Leger
  • Feliciana Faraco-Cantin
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.

Key words

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

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References

  1. 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 10:27–46Google Scholar
  2. 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 373:15–21Google Scholar
  3. Barbut D, Polak JM, Wall PD (1981) Substance P in spinal cord dorsal horn decreases following peripheral nerve injury. Brain Res 205:289–298Google Scholar
  4. 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 7–40Google Scholar
  5. Bisby MA, Keen P (1986) Regeneration of primary afferent neurons containing substance P-like immunoreactivity. Brain Res 365:85–95Google Scholar
  6. Blümcke S, Niedorf HR, Rode J (1966) Axoplasmic alterations in the proximal and distal stumps of transected nerves. Acta Neuropathol 7:44–61Google Scholar
  7. Borges LF, Sidman RL (1982) Axonal transport of lectins in the peripheral nervous system. J Neurosci 2:647–653Google Scholar
  8. Csillik B (1984) Nerve growth factor regulates central terminals of primary sensory neurons. Z Mikrosk Anat Forsch 98:11–16Google Scholar
  9. Devor M, Claman D (1980) Mapping and plasticity of acid phosphatase afferents in the rat dorsal horn. Brain Res 190:17–28Google Scholar
  10. Devor M, Wall PD (1981) Plasticity in the spinal cord sensory map following peripheral nerve injury in rats. J Neurosci 1:679–684Google Scholar
  11. Devor M, Wall PD, McMahon SB (1984) Dichotomizing somatic nerve fibers exist in rats but they are rare. Neurosci Lett 49:187–192Google Scholar
  12. 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 3:139–167Google Scholar
  13. 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 5:3278–3294Google Scholar
  14. Dolapchieva S, Ichev K, Ovtscharoff W (1986) Lectin binding sites in axon-myelin-Schwann cell complex. Acta Histochem Cytochem 19:253–261Google Scholar
  15. 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 170:491–505Google Scholar
  16. Estruch R, Damjanov I (1986) Lectin histochemistry applied to human nerves. Arch Pathol Lab Med 110:730–735Google Scholar
  17. Everly JL, Brady RO, Quarles RH (1973) Evidence that the major protein in rat sciatic nerve myelin is a glycoprotein. J Neurochem 21:329–334Google Scholar
  18. 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 37:749–758Google Scholar
  19. Fischer J, Csillik B (1985) Lectin binding: a genuine marker for transganglionic regulation of human primary sensory neurons. Neurosci Lett 54:263–267Google Scholar
  20. 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 332:131–141Google Scholar
  21. Friede RL, Bischhausen R (1980) The fine structure of stumps of transected nerve fibers in subserial sections. J Neurol Sci 44:181–203Google Scholar
  22. 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 34:1487–1493Google Scholar
  23. 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 50:237–242Google Scholar
  24. Harry GJ, Goodrum JF, Toews AR, Morell P (1987) Axonal transport characteristics of gangliosides in sensory axons of rat sciatic nerve. J Neurochem 48:1529–1536Google Scholar
  25. Holtzman E, Novikoff AB (1965) Lysosomes in the rat sciatic nerve following crush. J Cell Biol 27:651–669Google Scholar
  26. 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 111–133Google Scholar
  27. 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 168:247–259Google Scholar
  28. 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] 172:39–51Google Scholar
  29. 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 26:73–87Google Scholar
  30. 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 34:363–371Google Scholar
  31. 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 247:599–604Google Scholar
  32. Langford LA, Coggeshall RE (1981) Branching of sensory axons in the peripheral nerve of the rat. J Comp Neurol 203:745–750Google Scholar
  33. 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 123–132Google Scholar
  34. Lieberman AR (1971) The axonal reaction: a review of the principal features of perikaryal responses to axon injury. Int Rev Neurobiol 14:49–124Google Scholar
  35. 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 211:582–585Google Scholar
  36. Matthieu JM, Everly JL, Brady RO, Quarles RH (1975) [35S]Sulfate incorporation into myelin glycoproteins. II. Peripheral nervous tissue. Biochim Biophys Acta 392:167–174Google Scholar
  37. 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 13:207–216Google Scholar
  38. McMahon SB, Wall PD (1987) Physiological evidence for branching of peripheral unmyelinated sensory afferent fibers in the rat. J Comp Neurol 261:130–136Google Scholar
  39. Miller RG (1981) Simultaneous statistical inference. Springer, Berlin Heidelberg New York, pp 48–67Google Scholar
  40. 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 365:404–408Google Scholar
  41. 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 4:291–303Google Scholar
  42. 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 245:579–589Google Scholar
  43. 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 364:137–150Google Scholar
  44. 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 70:550–560Google Scholar
  45. Pierau FK, Taylor DCM, Abel W, Friedrich B (1982) Dichotomizing peripheral fibres revealed by intracellular recording from rat sensory neurones. Neurosci Lett 31:123–128Google Scholar
  46. 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 83:2248–2252Google Scholar
  47. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212Google Scholar
  48. 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 16:261–268Google Scholar
  49. 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 76:1510–1514Google Scholar
  50. 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 33:1042–1052Google Scholar
  51. 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 377:1–17Google Scholar
  52. Tenser RB (1985) Sequential changes of sensory neuron (fluorideresistant) acid phosphatase in dorsal root ganglion neurons following neurectomy and rhizotomy. Brain Res 332:386–389Google Scholar
  53. 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 332:209–218Google Scholar
  54. 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 209:95–111Google Scholar
  55. Ygge J, Aldskogius H, Grant G (1981) Asymmetries and symmetries in the number of thoracic dorsal root ganglion cells. J Comp Neurol 202:365–372Google Scholar
  56. Zelena J, Lubinska L, Gutmann E (1968) Accumulation of organelles at the ends of interrupted axons. Z Zellforsch 91:200–219Google Scholar

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • Jean-Marie Peyronnard
    • 1
  • Louise Charron
    • 1
  • Jean-Pierre Messier
    • 1
  • Jeanne Lavoie
    • 1
  • Christian Leger
    • 2
  • Feliciana Faraco-Cantin
    • 1
  1. 1.Centre de recherche en sciences neurologiques and Hôpital Hôtel-DieuMontréalCanada
  2. 2.Département d'informatique et de recherche opérationnelleUniversité de MontréalMontréalCanada

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