Constitutive expression of GAP-43 correlates with rapid, but not slow regrowth of injured dorsal root axons in the adult rat

Experimental Neurology

Volumn 155, Issue 2, 1999, Pages 157-164

  Andersen, Linda B ^a   Schreyer, David J ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Axon; Dorsal root ganglion; GAP 43; Growth; Immunocytochemistry; Regeneration

Indexed keywords

NEUROMODULIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DORSAL ROOT; FEMALE; GENE EXPRESSION; GROWTH CONE; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; LAMINECTOMY; NERVE CRUSH; NERVE DEGENERATION; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; NERVE GRAFT; NERVE GROWTH; NERVE INJURY; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPINAL GANGLION;

EID: 0032977772     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1998.6903     Document Type: Article

References (65)

1. Aigner L., Caroni P. Depletion of 43-kD growth-associated protein in primary sensory neurons leads to diminished formation and spreading of growth cones. J. Cell Biol. 123:1993;417-429.
2. Aigner L., Caroni P. Absence of persistent spreading, branching, and adhesion in GAP-43-depleted growth cones. J. Cell Biol. 128:1995;647-660.
3. Baetge E. E., Hammang J. P. Neurite outgrowth in PC12 cells deficient in GAP-43. Neuron. 6:1991;21-30.
4. Bedi K. S., Winter J., Berry M., Cohen J. Adult rat dorsal root ganglion neurons extend neurites on predegenerated but not normal peripheral nerves in vitro. Eur. J. Neurosci. 4:1992;193-200.
5. Benfey M., Aguayo A. J. Extensive elongation of axons from rat brain into peroneal nerve grafts. Science. 296:1982;150-154.
6. Benowitz L. I., Lewis E. R. Increased transport of 44,000- to 49,000-dalton acidic proteins during regeneration of the goldfish optic nerve: A two-dimensional gel analysis. J. Neurosci. 3:1983;2153-2163.
7. Benowitz L. I., Apostolides P. J., Perrone-Bizzozero N., Finklestein S. P., Zwiers H. Anatomical distribution of the growth-associated protein GAP-43/B-50 in the adult rat brain. J. Neurosci. 8:1988;339-352.
8. Benowitz L. I., Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 20:1997;84-91.
9. Bignami A., Chi N. H., Dahl D. Regenerating dorsal roots and the nerve entry zone: an immunofluorescence study with neurofilament and laminin antisera. Exptl. Neurol. 85:1984;426-436.
10. Bisby M. A. Changes in the composition of labelled protein transported in motor axons during their regeneration. J. Neurobiol. 11:1980;345-360.
11. Bisby M. A., Tetzlaff W., Brown M. C. GAP-43 mRNA in mouse motoneurons undergoing axonal sprouting in response to muscle paralysis of partial denervation. Eur. J. Neurosci. 8:1996;1240-1248.
12. Bolden D. A., Sternini C., Kruger L. GAP-43 mRNA and calcitonin gene-related peptide mRNA expression in sensory neurons are increased following sympathectomy. Brain Res. Bull. 42:1997;39-50.
13. Burry R. W., Perrone-Bizzozero N. I. Nerve growth factor stimulates GAP-43 expression in PC12 cell clones independently of neurite outgrowth. J. Neurosci. Res. 36:1993;241-251.
14. Caroni P., Schwab M. E. Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. J. Cell Biol. 106:1988;1281-1288.
15. Caroni P., Becker M. The downregulation of growth-associated proteins in motoneurons at the onset of synapse elimination is controlled by muscle activity and IGF1. J. Neurosci. 12:1992;3849-3861.
16. Chen S., Bisby M. A. Impaired motor axon regeneration in the C57BL/Ola mouse. J. Comp. Neurol. 333:1993;449-454.
17. Cheng H., Cao Y., Olson L. Spinal cord repair in adult paraplegic rats: Partial restoration of hind limb function. Science. 273:1996;510-513.
18. Chong M. S., Fitzgerald M., Winter J., Hu-Tsai M., Emson P. C., Wiese U., Woolf C. J. GAP-43 mRNA in rat spinal cord and dorsal root ganglia neurons: Developmental changes and reexpression following peripheral nerve injury. Eur. J. Neurosci. 4:1992;883-895.
19. Chong M. S., Reynolds M. L., Irwin N., Coggeshall R. E., Emson P. C., Benowitz L. I., Woolf C. J. GAP-43 expression in primary sensory neurons following central axotomy. J. Neurosci. 14:1994;4375-4386.
20. Chong M. S., Woolf C. J., Turmaine M., Emson P. C., Anderson P. N. 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. J. Comp. Neurol. 370:1996;97-104.
21. Dani J. W., Armstrong D. M., Benowitz L. I. Mapping the development of the rat brain by GAP-43 immunocytochemistry. Neuroscience. 40:1991;277-287.
22. David S., Aguayo A. J. Axonal elongation into peripheral nervous system bridges after central nervous system injury. Science. 214:1981;931-933.
23. Diamond J., Coughlin M., Macintyre L., Holmes M., Visheau B. Evidence that endogenous NGF is responsible for the collateral sprouting, but not the regeneration, of nociceptive axons in adult rats. Proc. Natl. Acad. Sci. USA. 84:1987;6596-6600.
24. Diamond J., Holmes M., Coughlin M. Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat. J. Neurosci. 12:1992;1454-1466.
25. Diamond J., Foerster A., Holmes M., Coughlin M. Sensory nerves in adult rats regenerate and restore sensory function to the skin independently of endogenous NGF. J. Neurosci. 12:1992;1467-1476.
26. Doster S. K., Lozano A. M., Aguayo A. J., Willard M. B. Expression of the growth-associated protein GAP-43 in adult rat retinal ganglion cells following axon injury. Neuron. 6:1991;635-647.
27. Erzurumlu R., Jhaveri S., Takahashi H., Mckay R. D. G. Target-derived influences on axon growth modes in cultures of trigeminal neurons. Proc. Natl. Acad. Sci. USA. 90:1993;7235-7239.
28. Goslin K., Schreyer D. J., Skene J. H. P., Banker G. Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones. Nature. 336:1988;672-674.
29. Goslin K., Schreyer D. J., Skene J. H. P., Banker G. Changes in the distribution of GAP-43 during the development of neuronal polarity. J. Neurosci. 10:1990;588-602.
30. Greenberg S. G., Lasek R. J. Neurofilament protein synthesis in DRG neurons decreases more after peripheral axotomy than after central axotomy. J. Neurosci. 8:1988;1739-1746.
31. Henken D. B., Battisti W. P., Chesselet M. F., Murray M., Tessler A. Expression of β-preprotachykinin mRNA and tachykinins in rat dorsal root ganglion cells following peripheral or central axotomy. Neuroscience. 39:1990;733-742.
32. Hirschberg D. L., Yoles E., Belkin M., Schwartz M. Inflammation after axonal injury has conflicting consequences for recovery of function: Rescue of spared axons is impaired but regeneration is supported. J. Neuroimmunol. 50:1994;9-16.
33. Hoffman P. N. Expression of GAP-43, a rapidly transported growth-associated protein, and class II beta tubulin, a slowly transported cytoskeletal protein, are coordinated in regenerating neurons. J. Neurosci. 9:1989;893-897.
34. Hu-Tsai M., Winter J., Emson P. C., Woolf C. J. Neurite outgrowth and GAP-43 mRNA expression in cultured adult rat dorsal root ganglion neurons: Effects of NGF or prior axotomy. J. Neurosci. Res. 39:1994;634-645.
35. Jacobsen R. D., Virág I., Skene J. H. P. A protein associated with axon growth, GAP-43, is widely distributed and developmentally regulated in rat CNS. J. Neurosci. 6:1986;1843-1855.
36. Jhaveri S., Edwards M. A., Schneider G. E. Initial stages of retinofugal axon development in the hamster: evidence for two distinct modes of growth. Exp. Brain Res. 87:1991;371-382.
37. Lieberman A. R. Some factors affecting retrograde neuronal responses to axonal lesions. Essays on the Nervous System. 1974;Clarendon, Oxford. p. 71-105.
38. Lin L.-H., Block S., Carpenter K., Rose M., Norden J. J. Synthesis and transport of GAP-43 in entorhinal cortex neurons and perforant pathway during lesion-induced sprouting and reactive synaptogenesis. Mol. Brain Res. 14:1992;147-153.
39. McKerracher L., David S., Jackson D. L., Kottis V., Dunn R. J., Braun P. E. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron. 13:1994;805-811.
40. McQuarrie I. G. Axon outgrowth enhanced by a previous nerve injury. Arch. Neurol. 29:1973;53-55.
41. Mearow K. M., Kril Y., Gloster A., Diamond J. Expression of NGF receptor and GAP-43 mRNA in DRG neurons during collateral sprouting and regeneration of dorsal cutaneous nerves. J. Neurobiol. 25:1994;127-142.
42. Mehta A., Reynolds M. L., Woolf C. J. Partial denervation of the medial gastrocnemius muscle results in growth-associated protein-43 immunoreactivity in sprouting axons and Schwann cells. Neuroscience. 57:1993;433-442.
43. Meiri K. F., Pfenninger K. H., Willard M. B. Growth-associated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp46, a major polypeptide of a subcellular fraction enriched in growth cones. Proc. Natl. Acad. Sci. USA. 83:1986;3537-3541.
44. Mukhopadhyay G., Doherty P., Walsh F. S., Crocker P. R., Filbin M. T. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron. 13:1994;757-767.
45. O'Leary D. D. M., Terashima T. Cortical axons branch to multiple subcortical targets by interstitial axon budding: Implications for target recognition and "waiting periods." Neuron. 1:1988;901-910.
46. Perry G. W., Krayaneck S. R., Wilson D. L. Protein synthesis and rapid axonal transport during regrowth of dorsal root axons. J. Neurochem. 40:1983;1590-1598.
47. Reynolds M. L., Fitzgerald M., Benowitz L. I. GAP-43 expression in developing cutaneous and muscle nerves in the rat hindlimb. Neuroscience. 41:1991;201-211.
48. Richardson P. M., Mcguiness U. M., Aguayo A. J. Axons from CNS neurones regenerate into PNS grafts. Nature. 284:1980;264-265.
49. Richardson P. M., Issa V. M. K. Peripheral injury enhances central regeneration in primary sensory neurones. Nature. 308:1984;791-793.
50. Richardson P. M., Verge V. M. K. The induction of a regenerative propensity in sensory neurons following peripheral axonal injury. J. Neurocytol. 15:1986;585-594.
51. Richardson P. M., Verge V. M. K. Axonal regeneration in dorsal spinal roots is accelerated by peripheral axonal transection. Brain Res. 411:1987;406-408.
52. Schnell L., Schwab M. E. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature. 343:1990;269-272.
53. Schreyer D. J., Jones E. G. Growth and target finding by axons of the corticospinal tract in prenatal and postnatal rats. Neuroscience. 7:1982;1837-1853.
54. Schreyer D. J., Skene J. H. P. Fate of GAP-43 in ascending spinal axons of DRG neurons after peripheral nerve injury: Delayed accumulation and correlation with regenerative potential. J. Neurosci. 11:1991;3738-3751.
55. Schreyer D. J., Skene J. H. P. Injury-induced GAP-43 expression displays axon branch specificity in adult rat dorsal root ganglion neurons. J. Neurobiol. 24:1993;959-970.
56. Skene J. H. P., Willard M. Changes in axonally transported proteins during axon regeneration in toad retinal ganglion cells. J. Cell Biol. 89:1981;86-95.
57. Skene J. H. P., Willard M. Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems. J. Cell Biol. 89:1981;96-103.
58. Skene J. H. P., Jacobsen R. D., Snipes G. J., Mcguire C. B., Norden J. J., Freeman J. A. A protein induced during nerve growth (GAP-43) is a major component of growth-cone membranes. Science. 233:1986;783-786.
59. Smith D. S., Skene J. H. P. A transcription-dependent switch controls competence of adult neurons for distinct modes of axon growth. J. Neurosci. 17:1997;646-658.
60. Stewart H. J. S., Cowen T., Curtis R., Wilkin G. P., Mirsky R., Jessen K. R. GAP-43 immunoreactivity is widespread in the autonomic neurons and sensory neurons of the rat. Neuroscience. 47:1992;673-684.
61. Strittmatter S. M., Fankhauser C., Huang P. L., Mashimo H., Fishman M. C. Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell. 80:1995;445-452.
62. Tetzlaff W., Zwiers H., Lederis K., Cassar L., Bisby M. A. Axonal transport and localization of B-50/GAP-43-like immunoreactivity in regenerating sciatic and facial nerves of the rat. J. Neurosci. 9:1989;1303-1313.
63. Tetzlaff W., Alexander S. W., Miller F. D., Bisby M. A. Response of facial and rubrospinal neurons to axotomy: Changes in mRNA expression for cytoskeletal proteins and GAP-43. J. Neurosci. 11:1991;2528-2544.
64. Verge V. M. K., Tetzlaff W., Richardson P. M., Bisby M. A. Correlation between GAP43 and nerve growth factor receptors in rat sensory neurons. J. Neurosci. 10:1990;926-934.
65. Wujek J. R., Lasek R. Correlation of axonal regeneration and slow component B in two branches of a single axon. J. Neurosci. 3:1983;243-251.