Neuropeptides, nitric oxide synthase and GAP-43 in B4-binding and RT97 immunoreactive primary sensory neurons: Normal distribution pattern and changes after peripheral nerve transection and aging

Brain Research

Volumn 832, Issue 1-2, 1999, Pages 63-83

  Bergman, Esbjörn ^a   Carlsson, Kjell ^b   Liljeborg, Anders ^a,b   Manders, Eric ^b   Hökfelt, Tomas ^a   Ulfhake, Brun ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Dept Geodesy Photogramm Roy I ^*  (Sweden)

Author keywords

Confocal microscopy; Dorsal root ganglion; Fluorescence; Immunohistochemistry

Indexed keywords

ANTIBODY; CALCITONIN GENE RELATED PEPTIDE; GALANIN DERIVATIVE; LECTIN; NEUROMODULIN; NEUROPEPTIDE; NITRIC OXIDE SYNTHASE;

ADOLESCENT; AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NERVE TRANSECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SENSORY NERVE CELL; SPINAL GANGLION;

AGING; ANIMALS; AXONS; FEMALE; GAP-43 PROTEIN; IMMUNOHISTOCHEMISTRY; LECTINS; MICROSCOPY, CONFOCAL; NEURONS, AFFERENT; NEUROPEPTIDES; NITRIC OXIDE SYNTHASE; PERIPHERAL NERVES; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; REFERENCE VALUES;

EID: 0033583932     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(99)01469-9     Document Type: Article

References (147)

1. Aimi Y., Fujimara M., Vincent S.R., Kimura H. Localization of NADPH-diaphorase-containing neurons in sensory ganglia of the rat. J. Comp. Neurol. 306:1991;382-392.
2. S. Algeri, G. Calderini, G. Toffano, F. Ponzio, Neurotransmittor alterations in aging rats, in: D. Samuel (Ed.), Aging of the Brain, Raven Press, New York, 1983, pp. 227-243.
3. Ambalavanar R., Morris R. The distribution of binding by isolectin I-B4 from Griffonia simplicifolia in the trigeminal ganglion and brainstem trigeminal nuclei in the rat. Neuroscience. 47:1992;421-429.
4. Arvidsson J., Ygge J., Grant G. Cell loss in lumbar dorsal root ganglia and transganglionic degeneration after sciatic nerve resection in the rat. Brain Res. 373:1986;15-21.
5. Averill S., McMahon S.B., Clary D.O., Reichardt L.F., Priestley J.V. Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur. J. Neurosci. 7:1995;1484-1494.
6. Bennett D.L.H., Michael G.J., Ramachandran N., Munson J.B., Averill S., Yan Q., McMahon S.B., Priestley J.V. 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.
7. Benowitz L.I., Routtenberg A. A membrane phosphoprotein associated with neural development, axonal regeneration, phospholipid metabolism and synaptic plasticity. Trends Neurosci. 10:1987;527-532.
8. Berg B.N., Wolf A., Simms H.S. Degenerative lesions of spinal roots and peripheral nerves in aging rats. Gerontologia (Basel). 6:1962;72-80.
9. Bergman E., Johnson H., Zhang X., Hökfelt T., Ulfhake B. Neuropeptides and neurotrophin receptor mRNAs in primary sensory neurons of aged rats. J. Comp. Neurol. 375:1996;303-320.
10. Bergman E., Ulfhake B. Loss of primary sensory neurons in the very old rat: neuron number estimates using the disector method and confocal optical sectioning. J. Comp. Neurol. 396:1998;211-222.
11. Bisby M.A. Dependence of GAP-43 (B50, F1) transport on axonal regeneration in rat dorsal root ganglion cells. Brain Res. 458:1988;157-161.
12. J.D. Burek, C.F. Hollander, Experimental Gerontology, The Laboratory Rat, Vol. 2, Academic Press, New York, 1980, pp. 149-159.
13. Carlsson K., Ulfhake B. Improved fluorophore separation with IMS confocal microscopy. NeuroReport. 6:1995;1169-1173.
14. Carlsson K., Åslund N., Mossberg K., Philip J. Simultaneous confocal recording of multiple fluorescent labels with improved channel separation. J. Microsc. 176:1994;287-299.
15. Carr P.A., Yamamoto T., Nagy J.I. Calcitonin gene-related peptide in primary afferent neurons of the rat: co-existence with fluoride-resistant acid phosphatase and depletion by neonatal capsaicin. Neuroscience. 36:1990;751-760.
16. N. Cauna, The effects of aging on the receptor organs of the human dermis, in: W. Montagna (Ed.), Advances in Biology of the Skin, Vol. 6, Pergamon, New York, 1965, pp. 63-96.
17. Cecchini T., Cuppini R., Ciaroni S., De Matteis R., Del Grande P. Increased number of sciatic sensory neurons in vitamin-E-deficient rats. Somatosens. Motor Res. 11:1994;269-278.
18. Chen C., Zhou X.F., Rush R.A. Neurotrophin-3 and trkC-immunoreactive neurons in rat dorsal root ganglia correlate by distribution and morphology. Neurochem. Res. 21:1996;809-814.
19. Ch'ng J.L.C., Christofides N.D., Anand P., Gibson S.J., Allen Y.S., Su H.C., Tatemoto K., Morrison J.F.B., Polak J.M., Bloom S.R. Distribution of galanin immunoreactivity in the central nervous system and responses of galanin-containing neuronal pathways to injury. Neuroscience. 16:1985;343-354.
20. Choi Y., Raja S.N., Moore L.C., Tobin J.R. Neuropathic pain in rats is associated with altered nitric oxide synthase activity in neural tissue. J. Neurol. Sci. 138:1996;14-20.
21. Christensson-Nylander I., Herrera-Marschitz M., Staines W., T H.K., Terenius L., Ungerstedt U., Cuello A.C., Oertel W.L., Goldstein M. Striato-nigral dynorphin and substance P pathways in the rat: I. Biochemical and immunohistochemical studies. Exp. Brain Res. 64:1986;164-192.
22. Coggeshall R.E. A consideration of neural counting methods. Trends Neurosci. 15:1992;9-13.
23. A.H. Coons, Fluorescent antibody methods, in: J.F. Danielli (Ed.), General Cytochemical Methods, Academic Press, New York, 1958, pp. 399-422.
24. Cotard-Bartley M.P., Secchi J., Glomot R., Cavanagh J.B. Spontaneous degenerative lesions of peripheral nerves in aging rats. Vet. Pathol. 18:1981;110-113.
25. C.J. Dalsgaard, The sensory system, in: A. Björklund, T. Hökfelt, C. Owman (Eds.), Handbook of Chemical Neuroanatomy, Vol. 6, Elsevier, Amsterdam, 1988, pp. 599-636.
26. de Neeling J.N., Beks P.J., Bertelsmann F.W., Heine R.J., Bouter L.M. Sensory thresholds in older adults: reproducibility and reference values. Muscle and Nerve. 17:1994;454-461.
27. Devor M., Govrin-Lippmann R., Frank I., Raber P. Proliferation of primary sensory neurons in adult rat dorsal root ganglion and the kinetics of retrograde cell loss after sciatic nerve section. Somatosens. Res. 3:1985;139-167.
28. Duggan A.W., Hope P.J., Lang C.W. Microinjection of neuropeptide Y into the superficial dorsal horn reduces stimulus-evoked release of immunoreactive substance P in the anaesthetized cat. Neuroscience. 44:1991;733-740.
29. Ferrell W.R., Crighton A., Sturrock R.D. Age-dependent changes in position sense in human proximal interphalangeal joints. NeuroReport. 3:1992;259-261.
30. Fiallos-Estrada C.E., Kummer C.E., Mayer B., Bravo R., Zimmermann M., Herdegen T. Long-lasting increase of nitric oxide synthase immunoreactivity, NADPH-diaphorase reaction and c-JUN co-expression in rat dorsal root ganglion neurons following sciatic nerve transection. Neurosci. Lett. 150:1993;169-173.
31. Fitzgerald M., Wall P.D., Goedert M., Emson P.C. Nerve growth factor counteracts the neurophysiological and neurochemical effects of chronic sciatic nerve section. Brain Res. 332:1985;131-141.
32. Fleetwood-Walker S.M., Mitchell R., Hope P.J., El-Yassir N., Molony V., Bladon C.M. The involvement of neurokinin receptor subtypes in somatosensory processing in the superficial dorsal horn of the cat. Brain Res. 519:1990;169-182.
33. Fundin B.T., Bergman E., Ulfhake B. Alterations in mystacial pad innervation in the aged rat. Exp. Brain Res. 117:1997;324-340.
34. Gescheider G.A., Bolanowski S.J., Hall K.L., Hoffman K.E., Verrillo R.T. The effects of aging on information-processing channels in the sense of touch: I. Absolute sensitivity. Somatosens. Motor Res. 11:1994;345-357.
35. Gibson S.J., Polk J.M., Bloom S.R., Sabate I.M., Mulderry P.M., Ghatei M.A., Morrison J.F.B., Kelly J.S., Rosenfeld M.G. Calcitonin gene-related peptide (CGRP)-immunoreactivity in the spinal cord of man and of eight species. J. Neurosci. 4:1984;3101-3111.
36. Gilmore S.A. Spinal nerve root degeneration in aging laboratory rats: a light microscopic study. Anat. Rec. 174:1972;251-257.
37. Goedert M., Stoeckel K., Otten U. Biological importance of the retrograde axonal transport of nerve growth factor in sensory neurons. Proc. Natl. Acad. Sci. USA. 78:1981;5895-5898.
38. Goldstein M.E., Cooper H.S., Bruce J., Carden M.J., Lee V.M.Y., Schlaepfer W.W. Phosphorylation of neurofilament proteins and chromatolysis following transection of rat sciatic nerve. J. Neurosci. 7:1987;1586-1594.
39. 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.
40. B. Gutman, V. Hanzlikova, Age Changes in the Neuromuscular System, Scientechnica, Bristol, 1972.
41. Haegerstrand A., Dalsgaard C.J., Jonson B., Larsson O., Nilsson J. Calcitonin gene-related peptide stimulates proliferation of human endothelial cells. Proc. Natl. Acad. Sci. USA. 87:1990;3299-3303.
42. Haley J.E., Dickenson A.H., Schachter M. Electrophysiological evidence for a role of nitric oxide in prolonged chemical nociception in the rat. Neuropharmacology. 31:1992;251-258.
43. Hamers F.P., Plantinga L.C., Verhaagen J., Neijt J.P., Gispen W.H. Upregulation of B50/GAP-43 protein mRNA in rat dorsal root ganglia during cisplatin intoxication. J. Neurosci. Res. 44:1996;142-148.
44. Hartman B.K., Zide D., Udenfriend S. The use of dopamine á-hydroxylase as a marker for the central noradrenergic nervous system in rat brain. Proc. Natl. Acad. Sci. USA. 69:1972;2722-2726.
45. Henry J.L. Effects of substance P on functionally identified units in cat spinal cord. Brain Res. 114:1976;439-451.
46. Herbison A.E., Simonian S.X., Norris P.J., Emson P.C. Relationship of neuronal nitric oxide synthase immunoreactivity to GnRH neurons in the ovariectomized and intact female rat. J. Neuroendocrinol. 8:1996;73-82.
47. 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.
48. Holzer P. Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience. 24:1988;739-768.
49. Hua X.Y., Boublik J., Spicer M.A., Rivier J.E., Brown M.R., Yaksh T.L. The antinociceptive effects of spinally administered neuropeptide Y in the rat: systematic studies on structure-activity relationship. J. Pharmacol. Exp. Ther. 258:1991;243-248.
50. Hunt S.P., Rossi J. Peptide- and non-peptide-containing unmyelinated primary afferents: the parallel processing of nociceptive information. Philos. Trans. R. Soc. London, Ser. B. 308:1985;283-289.
51. Hökfelt T., Wiesenfeld-Hallin Z., Villar M.J., Melander T. Increase of galanin-like immunoreactivity in rat dorsal root ganglion cells after peripheral axotomy. Neurosci. Lett. 83:1987;217-220.
52. Hökfelt T., Zhang X., Wiesenfeld-Hallin Z. Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci. 17:1994;22-30.
53. Hökfelt T., Åman K., Arvidsson U., Bedecs K., Ceccatelli S., Hulting A.L., Langel U., Meister B., Pieribone V., Bartfai T. Galanin message-associated peptide (GMAP)- and galanin-like immunoreactivities: overlapping and differential distributions in the rat. Neurosci. Lett. 142:1992;139-142.
54. Inoue T., Mashimo T., Shibata M., Shibuta S., Yoshiya I. Rapid development of nitric oxide-induced hyperalgesia depends on an alternate to the cGMP-mediated pathway in the rat neuropathic pain model. Brain Res. 792:1998;263-270.
55. Johnson G.D., Nogueira Araujo G.M.deC. A simple method of reducing the fading of immunofluorescence during microscopy. J. Immunol. Methods. 43:1981;349-350.
56. Johnson H., Mossberg K., Arvidsson U., Piehl F., Hökfelt T., Ulfhake B. Increase in alpha-CGRP and GAP-43 in aged motoneurons: a study of peptides, growth factors, and ChaT mRNA in the lumbar spinal cord of senescent rats with symptoms of hindlimb incapacities. J. Comp. Neurol. 359:1995;69-89.
57. Ju G., Hökfelt T., Brodin E., Fahrenkrug J., Fischer J.A., Frey P., Elde R.P., Brown J.C. Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptide- and cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res. 247:1987;417-431.
58. Kashiba H., Noguchi K., Ueda Y., Senba E. Coexpression of trk family members and low-affinity neurotrophin receptors in rat dorsal root ganglion neurons. Mol. Brain Res. 30:1995;158-164.
59. Kashiba H., Noguchi K., Ueda Y., Senba E. Neuropeptide Y and galanin are coexpressed in rat large type A sensory neurons after peripheral transection. Peptides. 15:1994;411-416.
60. Khalil Z., Helme R. Sensory peptides as neuromodulators of wound healing in aged rats. J. Gerontol., Ser. A. 51:1996;B354-B361.
61. Khalil Z., Helme R.D. Sequence of events in substance P plasma extravasation in rat skin. Brain Res. 500:1989;256-262.
62. Kitchener P.D., Wilson P., Snow P.J. Selective labelling of primary sensory afferent terminals in lamina II of the dorsal horn by injection of Bendiraea simplicifolia isolectin B4 into peripheral nerves. Neuroscience. 54:1993;545-551.
63. Knox C.A., Kokmen E., Dyck P.J. Morphometric alteration of rat myelinated fibers with aging. J. Neuropathol. Exp. Neurol. 48:1989;119-139.
64. S.L. Lawson, Morphological and biochemical cell types of sensory neurons, in: S.E. Scott (Ed.), Sensory Neurons: Diversity, Development, Plasticity, Oxford Univ. Press, New York, 1992, pp. 27-59.
65. Lawson S.N. Neuropeptides in morphologically and functionally identified primary afferent neurons in dorsal root ganglia: substance P, CGRP and somatostatin. Prog. Brain Res. 104:1995;161-173.
66. Lawson S.N., Harper A.A., Harper E.I., Garson J.A., Anderton B.H. A monoclonal antibody against neurofilament protein specifically labels a subpopulation of rat sensory neurons. J. Comp. Neurol. 228:1984;263-272.
67. Lawson S.N., Perry M.J., Prabhakar E., McCarthy P.W. Primary sensory neurones: neurofilament, neuropeptides, and conduction velocity. Brain Res. Bull. 30:1993;239-243.
68. Lawson S.N., Waddell P.J. Soma neurofilament immunoreactivity is related to cell size and fibre conduction velocity in rat primary sensory neurons. J. Physiol. 435:1991;41-63.
69. Levy D., Zochodne D.W. Local nitric oxide synthase activity in a model of neuropathic pain. Eur. J. Neurosci. 10:1998;1846-1855.
70. Ma W., Bisby M.A. Increase of calcitonin gene-related peptide immunoreactivity in the axonal fibers of the gracile nuclei of adult and aged rats after complete and partial sciatic nerve injuries. Exp. Neurol. 152:1998;137-149.
71. Macintosh S.R., Sinclair D.C. Age-related changes in the innervation of the rat snout. J. Anat. 125:1978;149-154.
72. Masoro E.J. Mortality and characteristics of rat strains commonly used in aging research. Exp. Aging Res. 6:1980;219-233.
73. Meller S.T., Pechman P.S., Gebhart G.F., Maves T.J. Nitric oxide mediates the thermal hyperalgesia produced in a model of neuropathic pain in the rat. Neuroscience. 50:1992;7-10.
74. 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.
75. Mitsumori K., Maita K., Shirasu Y. An ultrastructural study on spinal nerve roots and dorsal root ganglia in aging rats with spontaneous radiculoneuropathy. Vet. Pathol. 18:1981;714-726.
76. Molander C., Wang H.F., Rivero-Melián C., Grant G. Early decline and late restoration of spinal cord binding and transganglionic transport of isolectin B4 from Griffonia simplicifolia I after peripheral nerve transection or crush. Restor. Neurol. Neurosci. 10:1996;123-133.
77. Morris R., Southam E., Braid D.J., Garthwaite J. Nitric oxide may act as a messenger between dorsal root ganglion neurones and their satellite cells. Neurosci. Lett. 137:1992;29-32.
78. Nielsch V., Bisby M.A., Keen P. Effect of cutting or crushing the rat sciatic nerve on synthesis of substance P by isolated L5 dorsal root ganglia. Neuropeptides. 10:1987;137-145.
79. Nilsson J., von Euler A.M., Dalsgaard C.J. Stimulation of connective tissue cell growth by substance P and substance K. Nature. 315:1985;61-63.
80. Noguchi K., Dubner R., De Leon M., Senba E., Ruda M.A. Axotomy induces preprotachykinin gene expression in a subpopulation of dorsal root ganglion neurons. J. Neurosci. Res. 37:1994;596-603.
81. Noguchi K., Senba E., Morita Y., Sato M., Tohyama M. a-CGRP and b-CGRP mRNAs are differentially regulated in the rat spinal cord and dorsal root ganglion. Mol. Brain Res. 7:1990;299-304.
82. Ohara S., Tantuwaya V., Distefano P.S., Schmidt R. Exogenous NT-3 mitigates the transganglionic neuropeptide Y response to sciatic nerve injury. Brain Res. 699:1995;143-148.
83. Orazzo C., Pieribone V.A., Ceccatelli S., Terenius L., Hökfelt T. CGRP-like immunoreactivity in A11 dopamine neurons projecting to the spinal cord and a note on CGRP-CCK cross reactivity. Brain Res. 600:1992;39-48.
84. Parhad I.M., Scott J.N., Cellars L.A., Bains J.S., Krekoski C.A., Clark A.W. Axonal atrophy in aging is associated with a decline in neurofilament gene expression. J. Neurosci. Res. 41:1995;355-366.
85. Patwardhan A., Manders E.M.M. Three-colour confocal microscopy with improved colocalization capability and cross-talk suppression. BioImaging. 4:1996;17-24.
86. Pease P.C. Buffered formaldehyde as a killing agent and primary fixative for electron microscopy. Anat. Rec. 142:1962;342.
87. Perry M.J., Lawson S.N. Differences in expression of oligosaccharides, neuropeptides, carbonic anhydrase and neurofilament in rat primary afferent neurons retrogradely labelled via skin, muscle or visceral nerves. Neuroscience. 85:1998;293-310.
88. Platt J.L., Michael A.F. Retardation of fading and enhancement of intensity of immunofluorescence by p-phenylenediamine. J. Histochem. Cytochem. 31:1983;840-842.
89. Quoniam C., Hay L., Roll J.P., Harlay F. Age effects on reflex and postural responses to propriomuscular inputs generated by tendon vibration. J. Gerontol., Ser. A. 50:1995;B155-B165.
90. Raivich G., Hellweg R., Kreutzberg G.W. NGF receptor-mediated reduction in axonal NGF uptake and retrograde transport following sciatic nerve injury during regeneration. Neuron. 7:1991;151-164.
91. Robbins S., Waked E., McClaran J. Proprioception and stability: foot position awareness as a function of age and footwear. Age Ageing. 24:1995;67-72.
92. Rökaeus Å., Brownstein M.J. Construction of a porcine adrenal medullary cDNA library and nucleotide sequence analysis of two clones encoding a galanin precursor. Proc. Natl. Acad. Sci. USA. 83:1986;6287-6291.
93. Schmidt R.F., Wahren L.K., Hagbarth K.E. Multiunit neural responses to strong finger pulp vibration: I. Relationship to age. Acta Physiol. Scand. 140:1990;1-10.
94. Schreyer D.J., Skene J.H. 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.
95. Schreyer D.J., Skene J.H. Injury-associated induction of GAP-43 expression displays axon branch specificity in rat dorsal root ganglion neurons. J. Neurobiol. 24:1993;959-970.
96. Sharma A.K., Bajada S., Thomas P.K. Age changes in the tibial and plantar nerves of the rat. J. Anat. 130:1980;417-428.
97. Shehab S.A., Atkinson M.E. Vasoactive intestinal polypeptide (VIP) increases in the spinal cord after peripheral axotomy of the sciatic nerve originate from primary afferent neurons. Brain Res. 372:1986;37-44.
98. Shi T.J., Holmberg K., Xu Z.Q., Steinbusch H., de Vente J., Hökfelt T. Effect of peripheral nerve injury on cGMP and nitric oxide synthase levels in rat dorsal root ganglia: time course and coexistence. Pain. 78:1998;171-180.
99. Silverman J.D., Kruger L. Lectin and neuropeptide labeling of separate populations of dorsal root ganglion neurons and associated 'nociceptor' thin axons in rat testis and cornea whole-mount preparations. Somatosens. Res. 5:1988;259-267.
100. Silverman J.D., Kruger L. Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: relation of lectin reactivity to peptide and enzyme markers. J. Neurocytol. 19:1990;789-801.
101. Skene J.H.P. Axonal growth-associated proteins. Annu. Rev. Neurosci. 12:1989;127-156.
102. Skene J.H.P., Willard M. Axonally transported proteins associated with growth in rabbit central and peripheral nervous system. J. Cell Biol. 89:1981;96-103.
103. Skofitsch G., Jacobowitz D.M. Calcitonin gene-related peptide coexists with substance P in capsaicin sensitive neurons and sensory ganglia of the rat. Peptides. 6:1985;747-754.
104. Skofitsch G., Jacobowitz D.M. Galanin-like immunoreactivity in capsaicin sensitive sensory neurons and ganglia. Brain Res. Bull. 15:1985;191-195.
105. Sommervaille T., Reynolds M.L., Woolf C.J. Time-dependent differences in the increase in GAP-43 expression in dorsal root ganglion cells after peripheral axotomy. Neuroscience. 45:1991;213-220.
106. Staines W.A., Meister B., Melander T., Nagy J.I., Hökfelt T. Three-color immunofluorescence histochemistry allowing triple labeling within a single section. J. Histochem. Cytochem. 36:1988;145-151.
107. Streit W.J., Schulte B.A., Balentine D.J., Spicer S.S. Histochemical localization of galactose-containing glycoconjugates in sensory neurons and their processes in the central and peripheral nervous system of the rat. J. Histochem. Cytochem. 33:1985;1042-1052.
108. Streit W.J., Schulte B.A., Balentine J.D., Spicer S.S. Evidence for glycoconjugate in nociceptive primary sensory neurons and its origin from the Golgi complex. Brain Res. 377:1986;1-17.
109. Swett J.E., Torigoe Y., Elie V.R., Bourassa C.M., Miller P.G. Sensory neurons of the rat sciatic nerve. Exp. Neurol. 114:1991;82-103.
110. Tajti J., Fischer J., Knyihar-Csillik E., Csillik B. Transganglionic regulation and fine structural localization of lectin-reactive carbohydrate epitopes in primary sensory neurons of the rat. Histochemistry. 88:1988;213-218.
111. Tandrup T. A method for unbiased and efficient estimation of number and mean volume of specified neuron subtypes in rat dorsal root ganglion. J. Comp. Neurol. 329:1993;269-276.
112. Thippeswamy T., Morris R. Cyclic guanosine 3′,5′-monophosphate-mediated neuroprotection by nitric oxide in dissociated cultures of rat dorsal root ganglion neurones. Brain Res. 774:1997;116-122.
113. Thomas P.K., King R.H., Sharma A.K. Changes with age in the peripheral nerves of the rat. An ultrastructural study. Acta Neuropathol. (Berlin). 52:1980;1-6.
114. Wakisaka S., Kajander K.C., Bennett G.J. Increased neuropeptide Y (NPY)-like immunoreactivity in rat sensory neurons following peripheral axotomy. Neurosci. Lett. 124:1991;200-203.
115. van der Zee C.E., Nielander H.B., Vos J.P., Lopes da Silva S., Verhaagen J., Oestreicher A.B., Schrama L.H., Schotman P., Gispen W.H. Expression of growth-associated protein B-50 (GAP43) in dorsal root ganglia and sciatic nerve during regenerative sprouting. J. Neurosci. 9:1989;3505-3512.
116. Wang F.H., Robertson B., Grant G. Anterograde transport of horseradish-peroxidase conjugated isolectin B4 from Griffonia simplicifolia I in spinal primary sensory neurons of the rat. Brain Res. 811:1998;34-39.
117. Wang H., Rivero-Melian C., Robertson B., Grant G. Transganglionic transport and binding of the isolectin B4 from Griffonia simplicifolia I in rat primary sensory neurons. Neuroscience. 62:1994;539-551.
118. Verge V.M., Richardson P.M., Wiesenfeld-Hallin Z., Hökfelt T. Differential influence of nerve growth factor on neuropeptide expression in vivo: a novel role in peptide suppression in adult sensory neurons. J. Neurosci. 15:1995;2081-2096.
119. 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.
120. Verge V.M.K., Zhang X., Xu X.J., Wiesenfeld-Hallin Z., Hökfelt T. Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy: in situ hybridization and functional studies. Proc. Natl. Acad. Sci. USA. 89:1992;11617-11621.
121. Vestergaard S., Tandrup T., Jakobsen J. Effect of permanent axotomy on number and volume of dorsal root ganglion cell bodies. J. Comp. Neurol. 388:1997;307-312.
122. Wiese U.H., Ruth J.L., Emson P.C. Differential expression of growth-associated protein (GAP-43) mRNA in rat primary sensory neurons after peripheral nerve lesion: a non-radioactive in situ hybridisation study. Brain Res. 592:1992;141-156.
123. Wiesenfeld-Hallin Z. Neuropeptides and spinal cord reflexes. Prog. Brain Res. 104:1995;271-282.
124. Wiesenfeld-Hallin Z., Bartfai T., Hökfelt T. Galanin in sensory neurons in the spinal cord. Front. Neuroendocrinol. 13:1992;319-343.
125. Wiesenfeld-Hallin Z., Hao J.X., Xu X.J., Hökfelt T. Nitric oxide mediates ongoing discharges in dorsal root ganglion cells after peripheral nerve injury. J. Neurophysiol. 70:1993;2350-2353.
126. Wiesenfeld-Hallin Z., Hökfelt T., Lundberg J.M., Forsmann W.G., Reinecke M., Tschopp F.A., Fischer J.A. Immunoreactive calcitonin gene-related peptide and substance P coexist in sensory neurons to the spinal cord and interact in spinal behavioral responses of the rat. Neurosci. Lett. 52:1984;199-204.
127. Villar M.J., Cortes R., Theodorsson E., Wiesenfeld-Hallin Z., Schalling M., Fahrenkrug J., Emson P.C., Hökfelt T. Neuropeptide expression in rat dorsal root ganglion cells and spinal cord after peripheral nerve injury with special reference to galanin. Neuroscience. 33:1989;587-604.
128. W.D. Willis, R.E. Coggeshall, Sensory Mechanisms of the Spinal Cord, Plenum, 1991.
129. Vizzard M.A., Erdman S.L., de Groat W.C. Increased expression of neuronal nitric oxide synthase in dorsal root ganglion neurons after systemic capsaicin administration. Neuroscience. 67:1995;1-5.
130. Wong J., Oblinger M.M. Differential regulation of peripherin and neurofilament gene expression in regenerating rat DRG neurons. J. Neurosci. Res. 27:1990;332-341.
131. Wong J., Oblinger M.M. NGF rescues substance P expression but not neurofilament or tubulin gene expression in axotomized sensory neurons. J. Neurosci. 11:1991;543-552.
132. Wood J.W., Anderton B.H. Monoclonal antibodies to mammalian neurofilaments. Biosci. Rep. 1:1981;263-298.
133. Woolf C.J., Reynolds M.L., Molander C., O'Brien C., Lindsay R.M., Benowitz L.I. The growth-associated protein GAP-43 appears in dorsal root ganglion cells and in the dorsal horn of the rat spinal cord following peripheral nerve injury. Neuroscience. 34:1990;465-478.
134. Woolf C.J., Wiesenfeld-Hallin Z. Substance P and calcitonin gene-related peptide synergistically modulate the gain of the nociceptive flexor withdrawal reflex in the rat. Neurosci. Lett. 66:1986;226-230.
135. Wu W., Li L. Inhibition of nitric oxide synthase reduces motoneuron death due to spinal root avulsion. Neurosci. Lett. 153:1993;121-124.
136. Xu I.S., Luo L., Ji R.R., Hökfelt T., Xu X.J., Wiesenfeld-Hallin Z. The effect of intrathecal neuropeptide Y on the flexor reflex in rats after carrageenan-induced inflammation. Neuropeptides. 32:1998;447-452.
137. Xu X.J., Andell S., Zhang X., Wiesenfeld-Hallin Z., Langel Ü., Bedecs K., Hökfelt T., Bartfai T. Peripheral axotomy increases the expression of galanin message-associated peptide (GMAP) in dorsal root ganglion cells and alters the effects of intrathecal GMAP on the flexor reflex in the rat. Neuropeptides. 28:1995;299-307.
138. Xu X.J., Hao J.X., Hökfelt T., Wiesenfeld-Hallin Z. The effects of intrathecal neuropeptide Y on the spinal nociceptive flexor reflex in rats with intact sciatic nerve and after peripheral axotomy. Neuroscience. 63:1994;817-826.
139. Xu X.J., Wiesenfeld-Hallin Z., Villar M.J., Fahrenkrug J., Hökfelt T. On the role of galanin, substance P and other neuropeptides in primary sensory neurons of the rat: studies on spinal reflex excitability and peripheral anatomy. Eur. J. Neurosci. 2:1990;733-743.
140. Ygge J., Aldskogius H. Intercostal nerve transection and its effect on the dorsal root ganglion. A quantitative study on thoracic ganglion cell numbers and sizes in the rat. Exp. Brain Res. 55:1984;402-408.
141. Zamboni I., De Martino C. Buffered picric acid-formaldehyde: a new, rapid fixative for electron microscopy. J. Cell Biol. 35:1967;148A.
142. Zhang X., Meister B., Elde R., Verge V.M.K., Hökfelt T. Large calibre primary afferent neurons projecting to the gracile nucleus express neuropeptide Y after sciatic nerve lesions: an immunohistochemical and in situ hybridization study in rats. Eur. J. Neurosci. 5:1993;1510-1519.
143. Zhang X., Verge V.M.K., Wiesenfeld-Hallin Z., Ju G., Bredt D., Snyder S.H., Hökfelt T. Nitric oxide synthase-like immunoreactivity in lumbar dorsal root ganglia and spinal cord of rat and monkey and effect of peripheral axotomy. J. Comp. Neurol. 335:1993;563-575.
144. Zhang X., Wiesenfeld-Hallin Z., Hökfelt T. Effect of peripheral axotomy on expression of neuropeptide Y receptor mRNA in rat lumbar dorsal root ganglia. Eur. J. Neurosci. 6:1994;43-57.
145. E. Bergman, B.T. Fundin, B. Ulfhake, Effects of aging and axotomy on the expression of neurotrophin receptors in primary sensory neurons, J. Comp. Neurol. (1999) In Press.
146. E. Bergman, S. Kullberg, Y. Ming, B. Ulfhake, Upregulation of GFRα-1 and c-ret in primary sensory neurons and spinal motoneurons of aged rats, J. Neurosci. Res. (1999) In Press.
147. Y. Ming, E. Bergman, E. Edström, B. Ulfhake, Evidence for increased GDNF signaling in aged sensory and motor neurons, NeuroReport (1999) In Press.