Direct evidence of primary afferent sprouting in distant segments following spinal cord injury in the rat: Colocalization of GAP-43 and CGRP

Experimental Neurology

Volumn 184, Issue 1, 2003, Pages 373-380

  Ondarza, Adrianne B ^a   Ye, Zaiming ^b   Hulsebosch, Claire E ^b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

C fiber; Dorsal horn; GAP 43; Pain; Plasticity; Primary afferent; Spinal cord injury; Sprouting

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; MONOCLONAL ANTIBODY; NEUROMODULIN; POLYCLONAL ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CERVICAL SPINAL CORD; COMPUTER PROGRAM; CONTROLLED STUDY; DENSITY; FLUORESCENCE; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; LUMBAR SPINAL CORD; MALE; MUSCLE SPINDLE AFFERENT NERVE; NERVE CELL; NERVE FIBER GROWTH; NERVE SPROUTING; NOCICEPTION; NONHUMAN; PAIN; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT; RAT STRAIN; SPINAL CORD HEMISECTION; SPINAL CORD INJURY; THORACIC SPINAL CORD; TISSUE PREPARATION;

EID: 0345257363     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2003.07.002     Document Type: Article

References (57)

1. Aigner L., Arber S., Kapfhammer J.P., Laux T., Schneider C., Botteri F., Brenner H.R., Caroni P. Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell. 83:1995;269-278.
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. Bennett A.D., Chastain K.M., Hulsebosch C.E. Alleviation of mechanical and thermal allodynia by CGRP(8-37) in a rodent model of chronic central pain. Pain. 86:2000;163-175.
4. Bennett A.D., Everhart A.W., Hulsebosch C.E. Intrathecal administration of an NMDA or a non-NMDA receptor antagonist reduces mechanical but not thermal allodynia in a rodent model of chronic central pain after spinal cord injury. Brain Res. 859:2000;72-82.
5. Brook G.A., Plate D., Franzen R., Martin D., Moonen G., Shoenen J., Schmitt A.B., Noth J., Nacimiento W. Spontaneous longitudinally orientated axonal regeneration is associated with the Schwann cell framework within the lesion site following spinal cord compression injury of the rat. J. Neurosci. Res. 53:1998;51-65.
6. Brook G.A., Schmitt A.B., Nacimiento W., Weis J., Schröder J.M., Noth J. Distribution of B-50 (GAP-43) mRNA and protein in the normal adult human spinal cord. Acta Neuropathol. 95:1998;378-386.
7. Brown P.B. A reassessment of evidence for primary afferent sprouting in the dorsal horn. Pubols L.M., Sessle B.J. Effect of Injury on Trigeminal and Spinal Somatosensory Systems. 1987;273-280 Alan R. Liss, New York.
8. Cameron A.A., Leah J.D., Snow P.J. The coexistence of neuropeptides in feline sensory neurons. Neuroscience. 27:1988;969-979.
9. Christensen M.D., Everhart A.W., Pickelman J.T., Hulsebosch C.E. Mechanical allodynia and thermal hyperalgesia in chronic central pain following spinal cord injury. Pain. 68:1996;97-107.
10. Christensen M.D., Hulsebosch C.E. Chronic central pain after spinal cord injury. J. Neurotrauma. 14:1997;517-537.
11. Christensen M.D., Hulsebosch C.E. Spinal cord injury and anti-NGF treatment results in changes in CGRP density and distribution in the dorsal horn in the rat. Exp. Neurol. 147:1997;463-475.
12. Christensen M.D., Supoowit S.C., Dipette D.J., Hulsebosch C.E. Enhanced gene expression of CGRP and GAP-43 in dorsal root ganglia by spinal hemisection. J. Neurotrauma. 13:1996;602.
13. Chung K., Lee W.T., Carlton S.M. The effects of dorsal rhizotomy and spinal cord isolation on calcitonin gene related peptide labeled terminals in the rat lumbar dorsal horn. Neurosci. Lett. 90:1988;27-32.
14. Curtis R., Green D., Lindsay R.M., Wilkin G.P. Up-regulation of GAP-43 and growth of axons in rat spinal cord after compression injury. J. Neurocytol. 22:1993;51-64.
15. Galeazza M.T., Garry M.G., Yost H.J., Strait K.A., Hargreaves K.M., Seybold V.S. Plasticity in the synthesis and storage of substance P and calcitonin gene-related peptide in primary afferent neurons during peripheral inflammation. Neuroscience. 66:1995;443-458.
16. Gibbins I.L., Furness J.B., Costa M., MacIntyre I., Hillyard C.J., Girgis S. Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pigs. Neurosci. Lett. 57:1985;125-130.
17. Gibson S.J., Polak J.M., Bloom S.R., Sabate I.M., Mulderry P.M., Ghatei M.A., McGregor G.P., Morrison J.F., Kelly J.S., Evans R.M. Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J. Neurosci. 4:1984;3011-3101.
18. Goldstein B., Little J.W., Harris R.M. Axonal sprouting following incomplete spinal cord injury an experimental model. J. Spinal Cord Med. 20:1997;200-206.
19. Hökfelt T., Arvidsson U., Ceccatelli S., Cortes R., Cullheim S., Dagerlind A., Johnson H., Orazzo C., Piehl F., Pieribone V., Schalling M., Terenius L., Ulfhake B., Verge V.M., Villar M., Wiesenfeld-Hallin Z., Xu X.J., Zhang X. Calcitonin gene-related peptide in the brain, spinal cord and some peripheral systems. Ann. NY Acad. Sci. 657:1992;119-133.
20. Hulsebosch C.E., Coggeshall R.E. Quantitation of sprouting of dorsal root axons. Science. 213:1981;1020-1021.
21. Hulsebosch C.E., Coggeshall R.E. A comparison of axonal numbers in dorsal roots following spinal cord hemisection in neonate and adult rats. Brain Res. 265:1983;187-197.
22. Ishida-Yamamota A., Tohayama M. Calcitonin gene-related peptide in the nervous tissue. Prog. Neurobiol. 33:1989;335-386.
23. Kapfhammer J.P., Schwab M.E. Inverse patterns of myelination and GAP-43 expression in the adult CNS neurite growth inhibitors as regulators of neuronal plasticity. J. Comp. Neurol. 340:1994;194-206.
24. Kapfhammer J.P., Schwab M.E. Increased expression of the growth-associated protein GAP-43 in the myelin-free rat spinal cord. Eur. J. Neurosci. 6:1994;403-411.
25. Koerber H.R., Mirnics K., Brown P.B., Mendell L.M. Central sprouting and functional plasticity of regenerated primary afferents. J. Neurosci. 14:1994;3655-3671.
26. Krenz N.R., Weaver L.C. Sprouting of primary afferent fibers after spinal cord transection in the rat. Neuroscience. 85:1998;443-458.
27. Leem J.W., Willis W.D., Chung J.M. Cutaneous sensory receptors in the rat foot. J. Neurophysiol. 69:1993;1684-1699.
28. Li J.Y., Kling-Petersen A., Dahlström A. GAP-43-like immunoreactivity in normal adult rat sciatic nerve, spinal cord, and motoneurons axonal transport and effect of spinal cord transection. Neuroscience. 57:1993;759-779.
29. Liu C.N., Chambers W.W. Intraspinal sprouting of dorsal root axons. Arch. Neurol. Psychiatry. 79:1958;46-61.
30. Löfgren O., Yu L.C., Theodorsson E., Hansson P., Lundberg T. Intrathecal CGRP(8-37) results in a bilateral increase in hindpaw withdrawal latency in rats with a unilateral thermal injury. Neuropeptides. 31:1997;601-607.
31. Malcangio M., Bowery N.G. Calcitonin gene-related peptide content, basal outflow and electrically-evoked release from monoarthritic rat spinal cord in vitro. Pain. 66:1996;351-358.
32. McNeill D.L., Carlton S.M., Coggeshall R.E., Hulsebosch C.E. Denervation induced intraspinal synaptogenesis of calcitonin gene-related peptide containing primary afferent terminals. J. Comp. Neurol. 296:1990;263-268.
33. McNeill D.L., Carlton S.M., Hulsebosch C.E. Intraspinal sprouting of calcitonin gene-related peptide containing primary afferents after deafferentation in the rat. Exp. Neurol. 114:1991;321-329.
34. McNeill D.L., Chung K., Carlton S.M., Coggeshall R.E. Calcitonin gene-related peptide immunostained axons provide evidence for fine primary afferent fibers in the dorsal and dorsolateral funiculi of the rat spinal cord. J. Comp. Neurol. 272:1988;303-308.
35. McNeill D.L., Hulsebosch C.E. Intraspinal sptrouting of rat primary afferents after deafferentation. Neurosci. Lett. 81:1987;57-62.
36. Miki K., Fukuoka T., Tokunaga A., Noguchi K. Calcitonin gene-related peptide increase in the rat spinal dorsal horn and dorsal column nucleus following peripheral nerve injury up-regulation in a subpopulation of primary afferent sensory neurons. Neuroscience. 82:1998;1243-1252.
37. Murray M., Goldberger M.E. Restitution of function and collateral sprouting in the cat spinal cord the partially hemisected animal. J. Comp. Neurol. 158:1974;19-36.
38. Nacimiento W., Mautes A., Töpper R., Oestreicher A.B., Gispen W.H., Nacimiento A.C., Noth J., Kreutzberg G.W. B-50 (GAP-43) in the spinal cord caudal to hemisection indication for lack of intraspinal sprouting in dorsal root axons. J. Neurosci. Res. 35:1993;603-617.
39. Nacimiento W., Sappok T., Brook G.A., Tóth L., Oestreicher A.B., Gispen W.H., Noth J., Kreutzberg G.W. B-50 (GAP-43) in the rat spinal cord caudal to hemisection lack of intraspinal sprouting by dorsal root axons. Neurosci. Lett. 194:1995;13-16.
40. Neugebauer V., Rumenapp P., Schaible H.G. Calcitonin gene-related peptide is involved in the spinal processing of mechanosensory input from the rat's knee joint and in the generation and maintenance of hyperexcitability of dorsal horn neurons during development of acute inflammation. Neuroscience. 71:1996;1095-1109.
41. Neve R.L., Finch E.A., Bird E.D., Benowitz L.I. Growth-associated protein Gap-43 is expressed selectively in associateive regions of the adult human brain. Proc. Natl. Acad. Sci. USA. 85:1988;3638-3642.
42. Oestreicher A.B., De Graan P.N., Gispen W.H., Verhaagen J., Schrama L.H. B-50, the growth associated protein-43 modulation of cell morphology and communication in the nervous system. Prog. Neurobiol. 53:1997;627-686.
43. Paxinos G. The Rat Nervous System. 1995;Academic Press, San Diego.
44. Polistina D.C., Murray M., Goldberger M.E. Plasticity of dorsal root descending serotoninergic projections after partial deafferentation of the adult rat spinal cord. J. Comp. Neurol. 299:1990;349-363.
45. Rodin B.E., Kruger L. Absence of intraspinal sprouting in dorsal root axons caudal to a partial spinal hemisection a horseradish peroxidase transport study. Somat. Res. 2:1984;171-192.
46. Rodin C.E., Sampogna S.L., Kruger L. An examination of intraspinal sprouting in dorsal root axons with the tracer horseradish peroxidase. J. Comp. Neurol. 215:1983;187-198.
47. Sarter M. Denervation-induced collateral sprouting no case for tracing methods. Int. J. Neurosci. 29:1986;65-72.
48. Schaible H.-G. On the role of tachykinins and calcitonin gene-related peptide in the spinal mechanisms of nociception and in the induction and maintenance of inflammation-evoked hyperexcitability in spinal cord neurons (with special reference to nociception in joints). Kumazawa T., Kruger L., Misumura K. Progress in Brain Research. Vol. 113:1996;423-441 Elsevier, Amsterdam.
49. Schwab M.E. Structural plasticity of the adult CNS. Negative control by neurite growth inhibitory signals. Int. J. Dev. Neurosci. 14:1995;379-385.
50. Schwab M.E., Brosamle C. Regeneration of lesioned corticospinal tract fibers in the adult rat spinal cord under experimental conditions. Spinal Cord. 35:1997;469-473.
51. Seybold V.S., Galeazza M.T., Garry M.G., Hargreaves K.M. Plasticity of calcitonin gene related peptide neurotransmission in the spinal cord during peripheral inflammation. Can. J. Physiol. Pharmacol. 73:1995;1007-1014.
52. Siddall P.J., Yezierski R.P., Loeser J.D. Taxonomy abd epidemiology of spinal cord injury pain. Yezierski R.P., Burchiel K.J. Spinal Cord Injury Pain Assessment, Mechanisms, Management, Progress in Pain Research and Management. Vol. 23:2002;9-24 IASP Press, Seattle.
53. Skene P. Axonal growth associated proteins. Annu. Rev. Neurosci. 12:1989;127-156.
54. Weaver L.C., Cassam A.K., Krassioukov A.V., Llewellyn-Smith I.J. Changes in immunoreactivity for growth associated protein-43 suggest reorganization of synapses on spinal sympathetic neurons after cord transection. Neuroscience. 81:1997;535-551.
55. Willis W.D., Coggeshall R.E. Sensory Mechanisms of the Spinal Cord. 1991;Plenum Press, New York.
56. Wong S.T., Atkinson B.A., Weaver L.C. Confocal microscopic analysis reveals sprouting of primary afferent fibres in rat dorsal horn after spinal cord injury. Neurosci. Lett. 296:2000;65-68.
57. Yu L.-C., Hansson P., Lundeberg T. The calcitonin gene-related peptide antagonist CGRP(8-37) increases the latency to withdrawal responses in rats. Brain Res. 653:1994;223-230.