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Nerve Growth Factor and the Reinnervation of Skin After Peripheral Nerve Lesions

  • J. Diamond
Conference paper

Abstract

The reinnervation of any tissue following an injury of its nerves can be achieved only by (1) regenerating fibres originating from the damaged nerves (or other cut nerves appropriately redirected to the deprived region), and/or (2) the collateral sprouting of intact axons that were spared when the original lesion occurred. The two growth behaviours have a lot in common; they are both initiated as a consequence of axonal damage (though of different sets of nerves), they are both able to restore lost physiological functions, and both will readily occur along degenerating pathways (see below). It seems unlikely that they would utilize different cellular mechanisms of axonal extension. What then can explain the obvious differences that often are observed between regeneration and collateral sprouting? For example, the large diameter, low threshold, mechanosensory nerves supplying the skin of adult mammals will readily regenerate after they are crushed, but when intact they do not sprout into adjacent, denervated, territory (reviewed in Diamond 1987). In the adult rat this applies even within the confines of a single, but dually innervated, touch dome: after elimination of one of the axons supplying such a dome, the other fails to sprout functionally into the deprived region, even as little as 50–100 μm; nevertheless if this remaining axon is crushed, it regenerates to occupy much or all of the dome (Yasargil et al. 1988). In very young animals, however, these same low threshold axons show a variety of sprouting behaviours. For example, axons of the dorsal cutaneous nerves of rats can sprout collaterally during an early “window” of time which ends at about 20 days of age (Jackson and Diamond 1984); with a different rat population we now find that in some animals of a litter no sprouting occurs at all (Mills, Macintyre, Holmes and Diamond in preparation).

Keywords

Nerve Growth Factor Axonal Regeneration Nerve Growth Factor Level Peripheral Nerve Lesion Nociceptive Nerve 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Aguilar CE, Bisby MA, Cooper E, Diamond J (1973) Evidence that axoplasmic transport of trophic factors is involved in the regulation of peripheral nerve fields in salamanders. J Physiol (Lond) 234: 449–464Google Scholar
  2. Angeletti PU, Levi-Montalcini R, Caramia F (1971) Analysis of the effects of the antiserum to the nerve growth factor in adult mice. Brain Res 27: 343–355PubMedCrossRefGoogle Scholar
  3. Assouline JG, Bosch P, Lim R, Kim IS, Jensen R, Pantazis NJ (1987) Rat astrocytes and Schwann cells in culture synthesize nerve growth factor-like neurite-promoting factors. Dev Brain Res 31: 103–118CrossRefGoogle Scholar
  4. Bjerre B, Bjorklund A, Edwards DC (1974) Axonal regeneration of peripheral adrenergic neurons: effects of antiserum of antiserum to nerve growth factor in mouse. Cell Tissue Res 148: 441–476PubMedCrossRefGoogle Scholar
  5. Brenan A (1982) Plasma extravasation following antidromic stimulation of cutaneous nerves in the rat. J Physiol (Lond) 327: 7Google Scholar
  6. Campenot RB (1982) Development of sympathetic neurons in compartmentalized culture. I. Local control of neurite growth by nerve growth factor. Dev Biol 93: 1–12PubMedCrossRefGoogle Scholar
  7. Cauna N (1969) The fine morphology of the sensory receptor organs in the auricle of the rat. J Comp Neurol 136: 81–98PubMedCrossRefGoogle Scholar
  8. Devor M, Schonfeld D, Seltzer Z, Wall PD (1979) Two modes of cutaneous reinnervation following peripheral nerve injury. J Comp Neurol 185: 211–220PubMedCrossRefGoogle Scholar
  9. Diamond J (1982) Modelling and competition in the nervous system: clues from the sensory innervation of skin. In: Moscona AA, Monroy A (eds) Current topics in developmental biology, vol 17. Academic Press, London, pp 147–205Google Scholar
  10. Diamond J (1987) Plasticity and stability in the sensory innervation of skin. In: Pubols LM, Sessle BJ (eds) Neurology and neurobiology, vol 30. Alan R Liss, New York, pp 43–48Google Scholar
  11. Diamond J, Coughlin M, Macintyre L, Holmes M, Visheau B (1987) Evidence that endogenous β-nerve growth factor is responsible for the collateral sprouting but not the regeneration of nociceptive axons in adult rats. Proc Natl Acad Sci USA 84: 6956–6600Google Scholar
  12. Doucette R, Diamond J (1987) Normal and precocious sprouting of heat nociceptors in the skin of adult rats. J Comp Neurol 261: 592–603PubMedCrossRefGoogle Scholar
  13. Doucette R, Theriault E, Diamond J (1987) Regionally selective elimination of cutaneous thermal nociception in rats by neonatal capsaicin. J Comp Neurol 261: 583–591PubMedCrossRefGoogle Scholar
  14. Ebendal T, Olson L, Seiger A (1983) The level of nerve growth factor (NGF) as a function of innervation: a correlative radio-immunoassay and bioassay study of the rat iris. Exp Cell Res 148: 311–317PubMedCrossRefGoogle Scholar
  15. Finn PJ, Ferguson I A, Renton FJ, Rush RA (1986) Nerve growth factor immunohistochemistry and biological activity in the rat iris. J Neurocytol 15: 169–176PubMedCrossRefGoogle Scholar
  16. Greene LA, Shooter EM (1980) The nerve growth factor: biochemistry, synthesis, and mechanism of action. Annu Rev Neurosci 3: 353–402PubMedCrossRefGoogle Scholar
  17. Hefti F, Hortikka J, Eckenstein F, Gnahn H, Heumann R, Schwab M (1985) Nerve growth factor increases choline acetyltransferase but not survival or fiber outgrowth of cultured fetal septal cholinergic neurons. Neuroscience 14: 55–68PubMedCrossRefGoogle Scholar
  18. Heumann R, Korsching S, Scott J, Thoenen J (1984) Relationship between levels of nerve growth factor ( NGF) and its messenger RNA in sympathetic ganglia and peripheral targt tissues. EMBO J 3: 3183–3189PubMedGoogle Scholar
  19. Honegger P, Lenoir D (1982) Nerve growth factor (NGF) stimulation of cholinergic telencephalic neurons in aggregating cell cultures. Dev Brain Res 3: 229–238CrossRefGoogle Scholar
  20. Horch KW (1979) Guidance of regrowing sensory axons after cutaneous lesions in the cat. J Neurophysiol 42: 1437–1449PubMedGoogle Scholar
  21. Jackson P, Diamond J (1984) Temporal and spatial constraints on the collateral sprouting of low-threshold mechanosensory nerves in the skin of rats. J Comp Neurol 226: 336–345PubMedCrossRefGoogle Scholar
  22. Jancso G, Jancso-Gabor A (1980) Effects of capsaicin on morphine analgesia: possible involvement of hypothalamic structures. Naunyn Schmiedebergs Arch Pharmacol 211: 285–288CrossRefGoogle Scholar
  23. Johnson EM, Yip HK (1985) Central nervous system and peripheral nerve growth factor provide trophic support critical to mature sensory neuronal survival. Nature 314: 751–752PubMedCrossRefGoogle Scholar
  24. Kessler JA (1985) Parasympathetic, sympathetic, and sensory interactions in the iris: nerve growth factor regulates cholinergic ciliary ganglion innervation in vivo. J Neurosci 5: 2719–2725PubMedGoogle Scholar
  25. Levi-Montalcini R, Angeletti PU (1968) Nerve growth factor. Physiol Rev 48: 534–569PubMedGoogle Scholar
  26. Longo RM, Hayman EG, Davis GE, Ruoslahti E, Engvall E, Manthorpe M, Varon S (1984) Neurite-promoting factors and extracellular matrix components accumulating in vivo within nerve regeneration chambers. Brain Res 309: 105–117PubMedCrossRefGoogle Scholar
  27. Mills L (1987) Interactions between Merkel cells and nerve endings in the rat. Ph D Thesis, McMaster University, HamiltonGoogle Scholar
  28. Nixon BJ, Doucette R, Jackson PC, Diamond J (1984) Impulse activity evokes precocious sprouting of nociceptive nerves into denervated skin. Somatosens Res 2: 97–126PubMedGoogle Scholar
  29. Rich KM, Yip HK, Osborne PA, Schmidt RE, Johnson EM (1984) Role of nerve growth factor in the adult dorsal root ganglia neuron and its response to injury. J Comp Neurol 230: 110–118PubMedCrossRefGoogle Scholar
  30. Richardson PM, Ebendal T (1982) Nerve growth activities in the rat peripheral nerve. Brain Res 246: 57–64PubMedCrossRefGoogle Scholar
  31. Richardson PM, Riopelle RJ (1984) Uptake of nerve growth factor along peripheral and spinal axons of primary sensory neurons. J Neurosci 4: 1683–1689PubMedGoogle Scholar
  32. Schwartz JP, Pearson J, Johnson EM (1982) Effect of exposure to anti-NGF on sensory neurons of adult rats and guinea pigs. Brain Res 244: 378–381PubMedCrossRefGoogle Scholar
  33. Seiler M, Schwab ME (1984) Specific retrograde transport of nerve growth factor (NGF) from neocortex to nucleus basalis in the rat. Brain Res 300: 33–39PubMedCrossRefGoogle Scholar
  34. Shelton D, Reichardt L (1984) Expression of the β-nerve growth factor gene correlates with the density of sympathetic innervation in effector organs. Proc Natl Acad Sci USA 81: 7951–7955PubMedCrossRefGoogle Scholar
  35. Shelton DL, Reichardt LF (1986) Studies on the regulation of beta-nerve growth factor gene expression in the rat iris: the level of mRNA-encoding nerve growth factor is increased in irises placed in explant cultures in vitro, but not in irises deprived of sensory or sympathetic innervation in vivo. J Cell Biol 102: 1940–1948PubMedCrossRefGoogle Scholar
  36. Simpson SA, Young JZ (1945) Regeneration of fibre diameter after cross-unions of visceral and somatic nerves. J Anat 79: 48–65PubMedGoogle Scholar
  37. So KF, Aguayo AJ (1985) Lengthy regrowth of cut axons from ganglion cells after peripheral nerve transplantation into the retina of adult rats. Brain Res 328: 349–354PubMedCrossRefGoogle Scholar
  38. Sparrow JR, Kiernan J A (1981) Endoneurial vascular permeability in degenerating and regenerating peripheral nerves. Acta Neuropathol 53: 181–188PubMedCrossRefGoogle Scholar
  39. Taniuchi M, Clark HB, Johnson EM (1986) Induction of nerve growth factor receptor in Schwann cells after axotomy. Proc Natl Acad Sci USA 83: 4094–4098PubMedCrossRefGoogle Scholar
  40. Tsukahara N (1981) Synaptic plasticity in the mammalian central nervous system. Annu Rev Neurosci 4: 351–379PubMedCrossRefGoogle Scholar
  41. Vidal-Sanz M, Bray GM, Villegas-Perez MP, Thanos S, Aguayo AJ (1987) Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat. J Neurosci 7: 2894–2909PubMedGoogle Scholar
  42. Windebank AJ, Poduslo JF (1986) Neuronal growth factors produced by adult peripheral nerve after injury. Brain Res 385: 197–200PubMedCrossRefGoogle Scholar
  43. Yasargil GM, Macintyre L, Doucette R, Visheau B, Holmes M, Diamond J (1988) Axonal domains within shared touch domes in the rat: a comparison of their fate during conditions favoring collateral sprouting and following axonal regeneration. J Comp Neurol 270: 301–312PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1988

Authors and Affiliations

  • J. Diamond
    • 1
  1. 1.Department of NeurosciencesMcmaster UniversityOntarioCanada

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