NT-3 modulates NPY expression in primary sensory neurons following peripheral nerve injury

Journal of Anatomy

Volumn 193, Issue 2, 1998, Pages 273-281

  Sterne, G D ^a   Brown, R A ^b   Green, C J ^a   Terenghi, G ^a  

^a QUEEN VICTORIA HOSPITAL   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Dorsal root ganglia; Fibronectin; Nerve regeneration; Neuropeptides; Trophic factors

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; FIBRONECTIN; NEUROPEPTIDE Y; NEUROTROPHIN 3; SUBSTANCE P; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SIZE; CONTROLLED STUDY; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; MALE; NERVE GRAFT; NONHUMAN; OPTICAL DENSITY; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCIATIC NERVE; SENSORY NERVE CELL; SPINAL GANGLION;

ANALYSIS OF VARIANCE; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; FIBRONECTINS; GANGLIA, SPINAL; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MALE; NERVE GROWTH FACTORS; NERVE REGENERATION; NEURONS, AFFERENT; NEUROPEPTIDE Y; NEUROTROPHIN 3; PERIPHERAL NERVES; RATS; RATS, INBRED LEW; SUBSTANCE P; TIME FACTORS; VASOACTIVE INTESTINAL PEPTIDE;

ANIMALIA;

EID: 0031724434     PISSN: 00218782     EISSN: None     Source Type: Journal    
DOI: 10.1017/S002187829800394X     Document Type: Article

References (56)

1. ANAND P, GIBSON SJ, MCGREGOR GP, BLANK MA, GHATEI MA, BACARESE-HAMILTON AJ et al (1983) A VIP-containing system concentrated in the lumbo-sacral region of the human spinal cord. Nature 305, 143-145.
2. BARBACID M (1994) The Trk family of neurotrophin receptors. Journal of Neurobiology 25, 1386-1403.
3. BARRON KD (1983) Comparative observations on the cytological reactions of central and peripheral nerve cells to axotomy. In Spinal Cord Reconstruction (ed. Kao CC, Bunge RP, Reier PJ), pp. 7-40, New York: Raven Press.
4. BISBY MA, KEEN P (1986) Regeneration of primary afferent neurons containing substance P-like immunoreactivity. Brain Research 365, 85-95.
5. COGGESHALL RE, POVER CM, FITZGERALD M (1994) Dorsal root ganglion cell death and surviving cell numbers in relation to the development of sensory innervation in the rat hindlimb. Development Brain Research 82, 193-212.
6. DISTEFANO PS, FRIEDMAN B, RADZIEJEWSKI C, ALEXANDER C, BOLAND P, SCHICK CM et al. (1992) The neurotrophins BDNF, NT-3 and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron 8, 983-993.
7. DUGGAN AW, HOPE PJ, LANG CW (1991) Microinjection of neuropeptide Y into the superficial dorsal horn reduces stimulus evoked release of immunoreactive substance P in the anaesthetised cat. Neuroscience 44, 733-740.
8. DUMOULIN FL, RAIVICH G, HAAS CA, LAZAR P, REDDINGTON M, STREIT WJ et al. (1992) Calcitonin gene-related peptide and peripheral nerve regeneration. Annals of the New York Academy of Science 657, 351-360.
9. ERIKSSON NP, LINDSAY RM, ALDSKOGIUS H (1994) BDNF and NT-3 rescue sensory but not motoneurons following axotomy in the neonate. Neuroreport 5, 1445-1448.
10. ERNFORS P, LEE KF, KUCERA J, JAENISCH R (1994) Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 77, 503-512.
11. FITZGERALD M, WALL PD, GOEDERT M, EMSON PC (1985) Nerve growth factor counteracts the neurophysiological and neurochemical effects of chronic sciatic nerve section. Brain Research 332, 131-141.
12. FRANCO-CERECEDA A, RYDH M, DALSGAARD CJ (1992) Nicotine-and capsaicin-, but not potassium-, evoked CGRP release from cultured guinea-pig spinal ganglia is inhibited by Ruthenium red. Neuroscience Letters 137, 72-74.
13. HÖKFELT T, ZHANG X, VERGE V, VILLAR M, ELDE R, BARTFAI T et al. (1993) Coexistence and interaction of neuropeptides with substance P in primary sensory neurons, with special reference to galanin. Regulatory Peptides 46, 76-80.
14. HUA XY, BOUBLIK JH, SPICER MH, RIVIER JE, BROWN MR, YAKSH TL (1991) The antinociceptive effects of spinally administered neuropeptide Y in the rat: systematic studies on structure-activity relationship. Journal of Pharmacology and Experimental Therapeutics 258, 243-248.
15. 125I] neuropeptide Y receptor binding sites in rat spinal cord and the effects of neonatal capsaicin, dorsal rhizotomy and periphery axotomy. Brain Research 574, 333-337.
16. KASHIBA H, SENBA E, KAWAI Y, UEDA Y, TOHYAMA M (1992) Axonal blockade induces the expression of vasoactive intestinal peptide and galanin in rat dorsal root ganglion neurons. Brain Research 577, 19-28.
17. KASHIBA H, NOGUCHI K, UEDA Y, SENBA E (1995) Coexpression of trk family members and low affinity neurotrophin receptors in rat dorsal root ganglion neurons. Molecular Brain Research 30, 158-164.
18. KASHIBA H, UEDA Y, SENBA E (1996) Coexpression of preprotachykinin-A, calcitonin gene-related peptide, somatostatin, and neurotrophin receptor family messenger RNAs in rat dorsal root ganglion neurons. Neuroscience 70, 179-189.
19. KLEIN R, SILOS-SANTIAGO I, SMEYNE RJ, LIRA SA, BRAMBILLA R, BRYANT S et al. (1994) Disruption of the neurotrophin-3 receptor gene trkC eliminates Ia muscle afferents and results in abnormal movements. Nature 368, 249-251.
20. KNYIHAR-CSILLIK E, KREUTZBERG GW, RAIVICH G, CSILLIK B (1991) Vasoactive intestinal polypeptide in dorsal root terminals of the rat spinal cord is regulated by axoplasmic transport in the peripheral nerve. Neuroscience Letters 131, 83-87.
21. LEFCORT F, CLARY DO, RUSOFF AC, REICHARDT LF (1996) Inhibition of the NT-3 receptor TrkC, early in chick embryogenesis, results in severe reductions in multiple neuronal subpopulations in the dorsal root ganglia. Journal of Neuroscience 16, 3704-3713.
22. LEWIN GR (1996) Neurotrophins and the specification of neuronal phenotype. Philosophical Transactions of the Royal Society of London [Biology] 351, 405-411.
23. LINDSAY RM (1996) Role of neurotrophins and trk receptors in the development and maintenance of sensory neurons: an overview. Philosophical Transactions of the Royal Society of London [Biology] 351, 365-373.
24. LINDSAY RM, HARMAR AJ (1989) Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurons. Nature 337, 362-364.
25. MAISONPIERRE PC, BELLUSCIO L, SQUINTO S, IP NY, FURTH ME, LINDSAY RM et al. (1990) Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. Science 247, 1446-1451.
26. MANESS LM, KASTIN AJ, WEBER JT, BANKS WA, BECKMAN BS, ZADINA JE (1994) The neurotrophins and their receptors: structure, function and neuropathology. Neuroscience Biobehaviour Review 18, 143-159.
27. MCMAHON SB, SYKOVA E, WALL PD, WOOLF CJ, GIBSON SJ (1984) Neurogenic extravasation and substance P levels are low in muscle as compared to skin in the rat hindlimb. Neuroscience Letters 52, 235-240.
28. MCMAHON SB, LEWIN GR, ANAND P, GHATEI M, BLOOM SR (1989) Quantitative analysis of peptide levels and neurogenic extravasation following regeneration of afferents to appropriate and inappropriate targets. Neuroscience 33. 67-73.
29. MCMAHON SB, ARMANINI MP, LING LH, PHILLIPS HS (1994) Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12, 1161-1171.
30. MICHAEL GJ, AVERILL S, NITKUNAN A, RATTRAY M, BENNETT DLH, YAN Q et al. (1997) Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in trkA-expressing dorsal root ganglion cells and in their central termination within the spinal cord. Journal of Neuroscience 17, 8476-8490.
31. MULDERRY PK (1994) Neuropeptide expression by newborn and adult rat sensory neurons in culture: effects of nerve growth factor and other neurotrophic factors. Neuroscience 59, 673-688.
32. NIELSCH U, KEEN P (1989) Reciprocal regulation of tachykinin and vasoactive intestinal peptide-gene expression in rat sensory neurons following cut and crush injury. Brain Research 481, 25-30.
33. NOGUCHI K, DE LEON M, NAHIN RL, SENBA E, RUDA MA (1993) Quantification of axotomy-induced alteration of neuropeptide mRNAs in dorsal root ganglion neurons with special reference to neuropeptide Y mRNA and the effects of neonatal capsaicin treatment. Journal of Neuroscience Research 35, 54-66.
34. O'BRIEN C, WOOLF CJ, FITZGERALD M, LINDSAY RM, MOLANDER C (1989) Differences in the chemical expression of rat primary afferent neurons which innervate skin, muscle or joint. Journal of Neuroscience 32, 493-502.
35. O'HARA S, ROTH KA, BEAUDET LN, SCHMIDT RE (1994) Transganglionic neuropeptide Y response to sciatic nerve injury in young and aged rats. Journal of Neuropathology and Experimental Neurology 53, 646-662.
36. O'HARA S, TANTUWAYA V, DISTEFANO PS, SCHMIDT RE (1995) Exogenous NT-3 mitigates the transganglionic neuropeptide Y response to sciatic nerve injury. Brain Research 699, 143-148.
37. PERSSON JKE, LINDH B, ELDE R, ROBERTSON B, RIVERO-MELIAN C, ERIKSON NP et al. (1995) The expression of different cytochemical markers in normal and axotomised dorsal root ganglion cells projecting to the nucleus gracilis in the adult rat. Experimental Brain Research 105, 331-344.
38. RAIVICH G, HELLWEG R, KREUTZBERG GW (1991) NGF receptor-mediated reduction in axonal NGF uptake and retrograde transport following sciatic nerve injury and during regeneration. Neuron 7, 151-164.
39. LNGFR, trkA and trkB mediated by a single functional epitope distinct from that recognised by trkC. Journal of Cell Chemistry 271, 5623-5627.
40. SHU S, JU G, FAN L (1988) The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neuroscience Letters 85, 169-171.
41. STERNE GD, BROWN RA, GREEN CJ, TERENGHI G (1997a) Neurotrophin-3 delivered locally via fibronectin mats enhances peripheral nerve regeneration. European Journal of Neuroscience 9, 1388-1396.
42. STERNE GD, COULTON GR, BROWN RA, GREEN CJ, TERENGHI G (1997b) An immunohistochemical study of myosin heavy chains in gastrocnemius muscle following NT-3 enhanced nerve regeneration. Journal of Cell Biology 139, 1-7.
43. TERENGHI G, CHEN S, CARRINGTON AL, POLAK JM, TOMLINSON DR (1994) Changes in sensory neuropeptides in dorsal root ganglion and spinal cord of spontaneously diabetic BB rats. A quantitative immunohistochemical study. Acta Diabetologica 31, 198-204.
44. TESSAROLLO L, VOGEL KS, PALKO ME, REID SW, PARADA LF (1994) Targeted mutation in the neurotrophin-3 gene results in loss of muscle sensory neurons. Proceedings of the National Academy of Science of the USA 91, 11844-11848.
45. TESSLER A, HIMES BT, KRIEGER NR, MURRAY M, GOLDBERGER ME (1985) Sciatic nerve transection produces death of dorsal root ganglion cells and reversible loss of substance P in spinal cord. Brain Research 332, 209-218.
46. TOJO H, KAISHO Y, NAKATA M, MATSUOKA K, KITAGAWA M, ABE T et al. (1995) Targeted disruption of the neurotrophin-3 gene with lacZ induces loss of trkC-positive neurons in sensory ganglia but not in spinal cords. Brain Research 669, 163-175.
47. VERGE VMK, RICHARDSON PM, BENOIT R, RIOPELLE RJ (1989) Histochemical characterisation of sensory neurons with high affinity receptors for nerve growth factor. Journal of Neurocytology 18, 583-591.
48. VERGE VMK, RICHARDSON PM, WIESENFELD-HALLIN Z, HÖKFELT T (1995) Differential influence of nerve growth factor on neuropeptide expression in vivo: a novel role in peptide suppression in adult sensory neurons. Journal of Neuroscience 15, 2081-2096.
49. VERGE VMK, GRATTO KA, KARCHEWSKI LA, RICHARDSON PM (1996) Neurotrophins and nerve injury in the adult. Philosophical Transactions of the Royal Society of London (Biology) 351, 423-430.
50. WAKISAKA S, KAJANDER KC, BENNETT GJ (1991) Increased neuropeptide Y (NPY)-like immunoreactivity in rat sensory neurons following peripheral axotomy. Neuroscience Letters 124, 200-203.
51. WAKISAKA S, TAKIKITA S, SASAKI Y, KATO J, TABATA MJ, KURISU K (1993) Cell size-specific appearance of neuropeptide Y in the trigeminal ganglion following peripheral axotomy of different branches of the mandibular nerve of the rat. Brain Research 620, 347-350.
52. 2+ currents in rat sensory neurons. Journal of Neuroscience 8, 2438-2446.
53. WONO J, OBLINGER MM (1991) NGF rescues substance P expression but not neurofilament or tubulin gene expression in axotomised sensory neurones. Journal of Neuroscience 11, 543-552.
54. ZHANG X, MEISTER B, ELDE R, VERGE VMK, HÖKFELT T (1993) Large calibre primary afferent neurons projecting to the gracile nucleus express neuropeptide Y after sciatic nerve lesions: an immunohistochemical and in situ hybridisation study in rats. European Journal of Neuroscience 5, 1510-1519.
55. ZHANG X, WIESENFELD-HALLIN Z, HÖKFELT T (1994) Effect of peripheral axotomy on expression of neuropeptide Y receptor mRNA in rat lumbar dorsal root ganglia. European Journal of Neuroscience 6, 43-57.
56. ZHANG Q, JI RR, LINDSAY R, HÖKFELT T (1995) Effect of growth factors on substance P mRNA expression in axotomised dorsal root ganglia. Neuroreport 6, 1309-1312.