Intrinsic versus extrinsic factors in determining the regeneration of the central processes of rat dorsal root ganglion neurons: The influence of a peripheral nerve graft

Journal of Comparative Neurology

Volumn 370, Issue 1, 1996, Pages 97-104

  Chong, M S ^a,b   Woolf, C J ^a   Turmaine, M ^a   Emson, P C ^a,c   Anderson, P N ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b SELLY OAK HOSPITAL   (United Kingdom)

^c BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

GAP 43; nerve injury; primary sensory neurons; Schwann cells; spinal cord

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DORSAL RHIZOTOMY; DORSAL ROOT; NERVE CELL GROWTH; NERVE CRUSH; NERVE GRAFT; NERVE INJURY; NERVE REGENERATION; NERVE TRANSECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL GANGLION;

ANIMALS; AXONS; GANGLIA, SPINAL; GAP-43 PROTEIN; GROWTH SUBSTANCES; MEMBRANE GLYCOPROTEINS; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEURONS; PERIPHERAL NERVES; RATS; RATS, INBRED F344; RNA, MESSENGER;

EID: 0030003895     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960617)370:1<97::AID-CNE9>3.0.CO;2-G     Document Type: Article

References (56)

1. Aguayo, A.J. (1985) Axonal regeneration from injured neurons in the adult mammalian central nervous system. In C.W. Cotman (ed): Synaptic Plasticity. New York: Guilford Press, pp. 457-484.
2. Aigner, L., and P. Caroni (1995) Absence of persistent spreading, branching, and adhesion in GAP-43-depleted growth cones. J. Cell Biol. 728:647-660.
3. Aldskogius, H., J. Arvidsson, and G. Grant (1992) Axotomy-induced changes in primary sensory neurons. In S.A. Scott (ed): Sensory Neurons. Diversity, Development and Plasticity. Oxford: Oxford University Press, pp. 363-383.
4. Anderson, P.N., J. Mitchell, D. Mayor, and V.V. Stauber (1983) An ultrastructural study of the early stages of axonal regeneration through rat nerve grafts. Neuropathol. Appl. Neurobiol. 9:455-466.
5. Bandtlow, C, R. Heumann, M.E. Schwab, and H. Thoenen (1987) Cellular localization of nerve growth factor synthesis by in situ hybridization. EMBO J. 6:891-899.
6. Bisby, M.A. (1988) Dependence of GAP-43 (B50,F1) transport on axonal regeneration in rat dorsal root ganglion neurons. Brain Res. 458:157-161.
7. Bixby, J.L., J. Lilien, and L.F. Reichardt (1988) Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro. J. Cell Biol. 107:353-361.
8. Campbell, G., P.N. Anderson, M. Turmaine, and A.R. Lieberman (1991) GAP-43 in the axons of mammalian CNS neurons regenerating into peripheral nerve grafts. Exp. Brain Res. 87:67-74.
9. Campbell, G., A.R. Lieberman, P.N. Anderson, and M. Turmaine (1992) Regeneration of adult rat CNS axons into peripheral nerve autografts: Ultrastructural studies of the early stages of axonal sprouting and regenerative axonal growth. J. Neurocytol. 21:755-787.
10. Carlstedt, T. (1985) Regenerating axons form nerve terminals at astrocytes. Brain Res. 347:188-191.
11. Chong, M.S., M. Fitzgerald, J. Winter, M. Hu-Tsai, P.C. Emson, U. Wiese, and C.J. Woolf (1992) Gap-43 mRNA in rat spinal cord dorsal root ganglion neurons: Developmental changes and re-expression following peripheral nerve injury. Eur. J. Neurosci. 4:883-895.
12. Chong, M.S., M.L. Reynolds, N. Irwin, R.E. Coggeshall, P.C.Emson, L.I. Benowitz, and C.J. Woolf (1994a) GAP-43 expression in primary sensory neurons following central axotomy. J. Neurosci. 14:4375-4384.
13. Chong, M.S., C.J. Woolf, P. Andrews, M. Turmaine, D.J. Schreyer, and P.N. Anderson (1994b) The downregulation of GAP-43 is not responsible for the failure of regeneration in freeze-killed nerve grafts in the rat. Exp. Neurol. 129:311-320.
14. Coggeshall, R.E (1992) A consideration of neural counting methods. TINS 15:9-13.
15. Daniloff, J.K., K.L. Crossin, M. Pincon-Raymond, M. Murawsky, F. Rieger, and G.M. Edelman (1989) Expression of cytotactin in the normal and regenerating neuromuscular system. J. Cell Biol. 108:625-635.
16. De la Monte, S.M., H.J. Federoff, S.-C. Ng, E. Grabczyk, and M.C. Fishman (1989) GAP-43 gene expression during development: Persistence in a distinctive set of neurons in the mature central nervous system. Dev. Brain Res. 46:161-168.
17. Fawcett, J.W. (1992) Intrinsic neuronal determinants of regeneration. TINS 15:5-8.
18. Fitzgerald, M., M.L. Reynolds, and L.I. Benowitz (1991) GAP-43 expression in the developing rat lumbar spinal cord. Neuroscience 41:187-199.
19. Gundersen, H.J.G., P. Bagger, T.F. Bendtsen, S.M. Evans, L. Korbo, N. Marcussen, A. Møller, K. Nielsen, J.R. Nyengaard, B Pakkenberg, F.B. Sørensen, A. Vesterby, and M.J. West (1988) The new stereological tools: Disector, fractionator, nucleator and point sampling intercepts and their use in pathological research and diagnosis. Acta Pathol. Microbiol. Immunol. Scand. 96:857-879.
20. Horch, K. (1979) Guidance of regrowing sensory axons after cutaneous nerve lesion in the cat. J. Neurophysiol. 42:1437-1447.
21. Jacobson, R.D., I. Virag, and J.H.P. Skene (1986) A protein associated with axonal growth, GAP-43, is widely distributed and developmentally regulated in rat CNS. J. Neurosci. 6:1843-1855.
22. Kalil, K., and J.H.P. Skene (1986) Elevated synthesis of an axonally transported protein correlates with axonal outgrowth in normal and injured pyramidal tracts. J. Neurosci. 6:2563-2570.
23. Karns, L.R., S.-C. Ng, J.A. Freeman, and M.C. Fishman (1987) Cloning of complementary DNA for GAP-43, a neuronal growth-related protein. Science 236:597-560.
24. Kozlova, E.N., I. Strömberg, M. Bygdeman, and H. Aldskogius (1995) Peripherally grafted human foetal dorsal root ganglion cells extend axons into the spinal cord of adult host rats by circumventing dorsal root entry zone astrocytes. NeuroReport 5:269-272.
25. Lieberman, A.R. (1971) The axon reaction: A review of the principal features of perikaryon responses to axon injury. Int. Rev. Neurobiol. 14:49-124.
26. Liuzzi, F.J., and R.J. Lasek (1987) Astrocytes block axonal regeneration in mammals by activating the physiological stop pathway. Science 237:642-645.
27. Lu, X., and P.M. Richardson (1991) Inflammation near the nerve cell body enhances axonal regeneration. J. Neurosci. 11:972-978.
28. Martini, R. (1994) Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves. J. Neurocytol. 23:1-28.
29. Martini, R., Y. Xin, B. Schmitz, and M. Schachner (1992) The L2/HNK-1 carbohydrate epitope is involved in the preferential outgrowth of motor neurons on ventral roots and motor nerves. Eur. J. Neurosci. 4:628-639.
30. Meyer, M., I. Matsuoka, C. Wetmore, L. Olsen, and H. Theonen (1992) Enhanced synthesis of BDNF in the lesioned peripheral nerve: Different cellular mechanisms are respoonsible for the regulation of BDNF and NGF mRNA. J. Cell Biol. 119:45-54.
31. Morrow, D.R., G. Campbell, A.R. Lieberman, and P.N. Anderson (1993) Differential regenerative growth of CNS axons into tibial and peroneal nerve grafts in the thalamus of adult rats. Exp. Neurol. 120:60-69.
32. Moya, K.L., L.I. Benowitz, S. Jhaveri, and G. Schneider (1988) Changes in rapidly transported proteins in developing hamster retinofugal axons. J. Neurosci. 5:4445-4454.
33. Nadim, W., P.N. Anderson, and M. Turmaine (1990) The role of Schwann cells and basal lamina tubes in the regeneration of axons through long lengths of freeze-killed nerve grafts. Neuropathol. Appl. Neurobiol. 16:411-421.
34. Oblinger, M.M., and R.J. Lasek (1984) A conditioning lesion of the peripheral axons of dorsal root ganglion cells accelerates regeneration of only their peripheral axons. J. Neurosci. 4:1736-1744.
35. Oudega, M., S. Varon and T. Hagg (1994) Regeneration of adult rat sensory axons into intraspinal nerve grafts: Promoting effects of conditioning lesion and graft predegeneration. Exp. Neurol. 129:194-206.
36. Perkins, C.S., T. Carlstedt, K. Mizuno, and A.J. Aguayo (1980) Failure of regenerating dorsal root axons to regrow into the spinal cord. Can. J. Neurol. Sci. 7:323.
37. Richardon, P.M., and V.M.K. Issa (1984) Peripheral nerve injury enhances central regeneration of primary sensory neurones. Nature 309:791-793.
38. Richardson, P.M., and V.M.K. Verge (1987) Axonal regeneration in dorsal spinal roots is accelerated by peripheral axonal transection. Brain Res. 411:406-408.
39. Schreyer, D.J., and J.H.P. Skene (1991) Fate of GAP-43 in ascending spinal axons of DRG neurons after peripheral nerve injury: Delayed accumulation and correlation with regenerative potential. J. Neurosci. 11:3738-3751.
40. Schreyer, D.J., and J.H.P. Skene (1993) Injury induced GAP-43 expression displays axon branch specificity in adult dorsal root ganglion neurons. J. Neurobiol. 24:959-970.
41. Siegal, J.D., M. Kliot, G.M. Smith, and J. Silver (1990) A comparison of the regenerating potential of dorsal root fibers into grey or white matter of the adult rat spinal cord. Exp. Neurol. 109:90-97.
42. Skene, J.H.P. (1989) Axonal growth-associated proteins. Annu. Rev. Neurosci. 12:127-156.
43. Skene, J.H.P., and M. Willard (1981a) Changes in axonally transported protein during axon regeneration in toad retinal ganglion cells. J. Cell Biol. 89:86-95.
44. Skene, J.H.P., and M. Willard (1981b) Axonally transported proteins associated with axon growth in rabbit cental and peripheral nervous system. J. Cell Biol. 89:96-103.
45. Skene, J.H.P., and M. Willard (1981c) Characteristics of growth associated polypeptides in regenerating toad retinal ganglion cell axons. J. Neurosci. 1:419-426.
46. Stensaas, L.J., L.M. Partlow, P.R. Burgess, and K.W. Horch (1987) Inhibition of regeneration: The ultrastructure of reactive astrocytes and abortive axon terminals in the transitional zone of the dorsal root. Prog. Brain Res. 71:457-467.
47. Sterio, D.C. (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J. Microsc. 134:127-136.
48. Strittmatter, S.M., C. Fankhauser, P.L. Huang, H. Mashimo, and M.C. Fishman (1995) Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell 80:445-452.
49. Thoenen, H., C. Bandtlow, and R. Heumann (1987) The physiological function of nerve growth factor in the central nervous system: Comparison with the periphery. Rev. Physiol. Biochem. Pharmacol. 109:146-178.
50. Van der Zee, C.E.E.M., H.B. Nielander, J.P. Vos, S.L. da Silva, J. Verhaagen, A.B. Oestreicher, L.H. Schrama, P. Schotman, and W.H. Gispen (1989) Expression of growth-associated protein B-50 (GAP43) in dorsal root ganglia and sciatic nerve during regenerative sprouting. J. Neurosci. 9:3505-3512.
51. Vaudano, E, G. Campbell, P.N. Anderson, A.P. Davies, C. Woolhead, D.J. Schreyer, and A.R. Lieberman (1995) The effects of a lesion or a peripjheral nerve graft on GAP-43 upregulation in adult rat brain: An in situ hybridization and immunocytochemical study. J. Neurosci. 15:3594-3611.
52. Vidal-Sanz, M., G.M. Bray, M.P. Villegas-Perez, S. Thanos, and A.J. Aguayo (1987) Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat. J. Neurosci. 7:2894-2907.
53. Villegas-Perez, M.P., M. Vidal-Sanz, G.M. Bray, and A.J. Aguayo (1988) Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. J. Neurosci. 8:265-280.
54. Wiese, U.H., and P.C. Emson (1991) Intraspinal cellular responses after spinal cord transection in rats: Neuronal expression of growth-associated protein (GAP-93). Res Neurol. Neurosci. 2:199-204.
55. Woolf, C.J., M. Reynolds, C. Molander, C. O'Brien, R.M. Lindsay, and L.I. Benowitz (1990) GAP-43 appears in the rat dorsal horn following peripheral nerve injury. Neuroscience 34:465-478.
56. Zelena, J., and I. Jirmanova (1988) Grafts of pacinian corpuscles reinervated by dorsal root axons. Brain Res. 438: 165-174.