Neonatal capsaicin treatment prevents the normal postnatal withdrawal of A fibres from lamina II without affecting Fos responses to innocuous peripheral stimulation

Developmental Brain Research

Volumn 121, Issue 1, 2000, Pages 55-65

  Torsney, Carole ^a   Meredith Middleton, Jacqueta ^a   Fitzgerald, Maria ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

C fibre; Development; Dorsal root ganglion; Primary afferent; Spinal cord; Substantia gelatinosa

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CAPSAICIN; HORSERADISH PEROXIDASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; IMMUNOREACTIVITY; NERVE CELL; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; RAT; SENSORY SYSTEM; SKIN STIMULATION; SPINAL CORD; SPINAL GANGLION; SUBSTANTIA GELATINOSA;

ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL MARKERS; CALCITONIN GENE-RELATED PEPTIDE; CAPSAICIN; FLUORESCENT ANTIBODY TECHNIQUE; GANGLIA, SPINAL; NERVE FIBERS, MYELINATED; NEURONS, AFFERENT; PHYSICAL STIMULATION; PROTO-ONCOGENE PROTEINS C-FOS; RATS; SUBSTANTIA GELATINOSA;

ANIMALIA; ARMORACIA RUSTICANA; LAMIINAE;

EID: 0034636582     PISSN: 01653806     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-3806(00)00024-9     Document Type: Article

References (51)

1. Alvares D., Fitzgerald M. Building blocks of pain: the regulation of key molecules in spinal sensory neurons during development and following peripheral axotomy. Pain. 71:(Suppl.):1999;71-85.
2. S.A. Beggs, A. Aynsley-Green, J.N. Wood, M. Fitzgerald, Withdrawal of AB fibres from substantia gelatinosa during normal postnatal development is an activity-dependent process, Soc. Neurosci. Abstr. (1999) in press.
3. Bennett D.L.H., French J., Priestley J.V.P., McMahon S.B. NGF but not NT-3 or BDNF prevents the A fibre sprouting into lamina II of the spinal cord that occurs following axotomy. Mol. Cell. Neurosci. 8:1996;211-220.
4. Bennett D.L.H., Michael G.J., Ramachandran N., Munson J.B., Averill S., Yan Q., McMahon S.B., Priestley J.P. A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J. Neurosci. 18:1998;3059-3072.
5. Bicknell H.R.J., Beal J.A. Axonal and dendritic development of substantia gelatinosa neurons in the lumbosacral spinal cord of the rat. J. Comp. Neurol. 226:1984;508-522.
6. Caterina M.J., Shumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat activated ion channel in the pain pathway. Nature. 389:1997;816-824.
7. Cervero F., Plenderleith M.B. Spinal cord sensory systems after neonatal capsaicin. Acta Physiol. Hung. 69:1987;393-401.
8. Coggeshall R.E., Jennings E.A., Fitzgerald M. Evidence that large myelinated primary afferent fibres make synaptic contacts in lamina II of neonatal rats. Dev. Brain Res. 92:1996;81-90.
9. Coimbra A., Ribeiro-da-silva A., Pignatelli D. Rexed's laminae and the acid phosphatase (FRAP) band in the superficial dorsal horn of the neonatal rat spinal cord. Neurosci. Lett. 71:1986;131-136.
10. Doucet J.P., Squinto S.P., Bazan N.G. Fos-Jun and the primary genomic response in the nervous system. Bazan N.G. Molecular Neurobiology. 1990;27-55 Humana Press, New York.
11. Fitzgerald M. Capsaicin and sensory neurones - A review. Pain. 15:1983;109-130.
12. Fitzgerald M. Prenatal growth of fine diameter primary afferents into the rat spinal cord: A transganglionic tracer study. J. Comp. Neurol. 261:1987;98-104.
13. Fitzgerald M. The developmental neurobiology of pain. Bond M.R., Charlton J.E., Woolf C.J. Proceedings of the VIth World Congress on Pain :1991;253-261 Elsevier, Amsterdam.
14. Fitzgerald M. The developmental neurobiology of pain. Wall P.D., Melzack R. The Textbook of Pain. 4th Edition :1999;Churchill Livingstone, Edinburgh. in press.
15. Fitzgerald M., Butcher T., Shortland P. Developmental changes in the laminar termination of A fibre cutaneous sensory afferents in the rat spinal cord dorsal horn. J. Comp. Neurol. 348:1994;225-233.
16. Fitzgerald M., King A.E., Thompson S.W., Woolf C.J. The postnatal development of the ventral root reflex in the rat; a comparative in vivo and in vitro study. Neurosci. Lett. 78:1987;41-45.
17. Fitzgerald M., Reynolds M.L., Benowitz L.I. GAP-43 expression in the developing rat lumbar spinal cord. Neuroscience. 41:1991;187-199.
18. Fitzgerald M., Swett J.E. The termination pattern of sciatic nerve afferents in the substantia gelatinosa of neonatal rats. Neurosci. Lett. 43:1983;149-154.
19. Herschman H.R. Extracellular signals, transcriptional responses and cellular specificity. Trends. Biochem. Sci. 14:1989;435-438.
20. Hori Y., Watanabe S. Morphine-sensitive late components of the flexion reflex in the neonatal rat. Neurosci. Lett. 78:1987;91-96.
21. Hunt S.P., Pini A., Evan G. Induction of c-fos-like protein in spinal cord neurones following sensory stimulation. Nature. 328:1987;632-634.
22. A. Jackman, M. Fitzgerald, The development of peripheral hindlimb and central spinal cord innervation by subpopulations of dorsal root ganglion cells in the embryonic rat, J. Comp. Neurol. (1999) in press.
23. Jennings E., Fitzgerald M. C-fos can be induced in the neonatal rat spinal cord by both noxious and innocuous peripheral stimulation. Pain. 68:1996;301-306.
24. Jennings E., Fitzgerald M. Postnatal changes in responses of rat dorsal horn cells to afferent stimulation: a fibre-induced sensitization. J. Physiol. (Lond.). 509:(3):1998;859-868.
25. Kudo N., Yamada T. Morphological and physiological studies of development of the monosynaptic reflex pathway in the rat lumbar spinal cord. J. Physiol. 389:1987;441-459.
26. LaMotte C.C., Kapadia S.E., Shapiro C.M. Central projections of the sciatic, saphenous, median and ulnar nerves of the rat demonstrated by transganglionic transport of choleragenoid-HRP (B-HRP) and wheat-germ agglutinin-HRP (WGA-HRP). J. Comp. Neurol. 311:1991;546-562.
27. Lawson S.N. Morphological and biochemical cell types of sensory neurons. Scott S.A. Sensory Neurons, Diversity, Development and Plasticity. 1992;27-59.
28. Ma Q.P., Woolf C.J. Basal and touch-evoked fos-like immunoreactivity during experimental inflammation in the rat. Pain. 67:1996;307-316.
29. Mannion R.J., Doubell T.P., Coggeshall R.E., Woolf C.J. Collateral sprouting of uninjured primary afferent A-fibers into the superficial dorsal horn of the adult rat spinal cord after topical capsaicin treatment to the sciatic nerve. J. Neurosci. 16:1996;5189-5195.
30. Marti E., Gibson S.J., Polak J.M., Facer P., Speingall D.R., van Aswegen G., Aitchison M., Koltzenburg P. Ontogeny of peptide- and amine-containing neurones in motor, sensory and autonomic regions of rat and human spinal cord, dorsal root ganglia and skin. J. Comp. Neurol. 226:1987;332-359.
31. McCarthy P.W., Lawson S.N. Cell type and conduction velocity of rat primary sensory neurons with calcitonin gene-related peptide like immunoreactivity. Neuroscience. 34:1990;623-632.
32. Michael G.J., Priestley J.V. Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. J. Neurosci. 19:1999;1844-1854.
33. Mirnics K., Koerber H.R. Prenatal development of rat primary afferent fibers: II. Central projections. J. Comp. Neurol. 355:1995;601-614.
34. Molander C., Xu Q., Grant G. The cytoarchitectonic organisation of the spinal cord in the rat: I. The lower thoracic and lumbosacral cord. J. Comp. Neurol. 230:1984;133-141.
35. Morgan J.I., Curran T. Stimulus-transcription coupling in neurons: role of cellular immediate-early genes. Trends Neurosci. 12:1989;459-462.
36. Nornes H.O., Das G.D. Temporal pattern of neurogenesis in the spinal cord of the rat. I. An autoradiographical study. Time and sites of origin and migration and settling patterns of neuroblasts. Brain Res. 73:1974;121-138.
37. Pignatelli D., Ribeiro-da-Silva A., Coimbra A. Postnatal maturation of primary afferent terminals in the substantia gelatinosa of the rat spinal cord. An electron microscope study. Brain Res. 491:1989;33-44.
38. Rethelyi M., Salim M.Z., Jancso G. Altered distribution of dorsal root fibres in the rat following neonatal capsaicin treatment. Neuroscience. 18:1986;749-761.
39. Rivero-Melian C., Grant G. Distribution of lumbar dorsal root fibres in the lower thoracic and lumbosacral spinal cord of the rat studied with choleragenoid horseradish peroxidase conjugate. J. Comp. Neurol. 299:1990;470-481.
40. Robertson B., Grant G. A comparison between wheatgerm agglutinin and choleragenoid HRP as anterogradely transported markers in central branches of primary sensory neurones in the rat with some observations in the cat. Neuroscience. 14:1985;895-905.
41. Sassone-Corsi P., Ransone L.J., Lamph W.W., Verma I.M. Direct interaction between fos and jun nuclear oncoproteins: role of the 'leucine zipper' domain. Nature. 336:1988;692-695.
42. Sheng M., McFadden G., Greenberg M.E. Membrane depolarisation and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron. 4:1990;571-582.
43. Shortland P., Molander C., Woolf C.J., Fitzgerald M. Neonatal capsaicin treatment induces invasion of the substantia gelatinosa by the terminal arborisations of hair follicle afferents in the rat dorsal horn. J. Comp. Neurol. 296:1990;23-31.
44. Silverman J.D., Kruger L. Selective glycoconjugate expression in sensory and autonomic ganglia: relation of lectin reactivity to peptide and enzyme markers. J. Neurocytol. 19:1990;789-801.
45. Smith C.L. The development and postnatal organisation of primary afferent projections to the rat thoracic spinal cord. J. Comp. Neurol. 220:1983;29-43.
46. Todd A.J., Spike R.C., Polgar E. A quantitative study of neurons which express neurokinin-1 or somatostatin sst2a receptor in rat spinal dorsal horn. Neuroscience. 85:1998;459-473.
47. Tong Y.-G., Wang H.F., Ju G., Grant G., Hökfelt T., Zhang X. Increased uptake and transport of cholera toxin B-subunit in dorsal root ganglion neurons after peripheral axotomy: possible implications for sensory sprouting. J. Comp. Neurol. 404:1999;143-158.
48. Williams S., Evans G., Hunt S.P. Changing patterns of c-fos induction in spinal neurons following thermal cutaneous stimulation in the rat. Neuroscience. 36:1990;73-81.
49. Woolf C.J. Evidence for a central component of post-injury pain hypersensitivity. Nature. 306:1983;686-688.
50. Woolf C.J., Shortland P., Coggeshall R.E. Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature. 355:1992;75-78.
51. Zhang L., Morgan E., Bagust J., Williams R.G. c-fos expression in isolated rat spinal cord. J. Neurosci. Methods. 79:1998;105-113.