Peptide plasticity in primary sensory neurons and spinal cord during adjuvant-induced arthritis in the rat: An immunocytochemical and in situ hybridization study

Neuroscience

Volumn 82, Issue 2, 1997, Pages 575-589

  Calza L ^a,b   Pozza, M ^b   Zanni, M ^c   Manzini, C U ^c   Manzini, E ^c   Hokfelt T ^d  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b HESPERIA HOSPITAL   (Italy)

^c UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Galanin; Inflammation; Nerve injury; Pain; Plasticity; Substance P

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CHOLECYSTOKININ; DYNORPHIN; ENKEPHALIN; FREUND ADJUVANT; GALANIN; MESSENGER RNA; NEUROPEPTIDE Y; PEPTIDE; SUBSTANCE P;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NERVE CELL PLASTICITY; NERVE INJURY; NEUROPATHY; NONHUMAN; PAIN; PRIORITY JOURNAL; RAT; RHEUMATOID ARTHRITIS; SENSORY NERVE CELL; SPINAL CORD; SPINAL GANGLION;

EID: 0342327377     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00272-8     Document Type: Article

References (73)

1. Ahmed M., Bjurholm A., Srinivasan G. R., Lundberg T., Theodorsson E., Schultzberg M., Kreicbergs A. Capsaicin effects on substance P and CGRP in rat adjuvant arthritis. Regul. Pept. 55:1995;85-102.
2. Ahmed M., Srinivasan G. R., Theodorsson E., Schultzberg M., Kreicbergs A. Effect of surgical denervation on substance P and calcitonin gene-related peptide in adjuvant arthritis. Peptides. 16:1995;569-579.
3. Ahmed M., Bjurholm A., Theodorsson E., Schultzberg M., Kreicbergs A. Neuropeptide Y- and vasoactive intestinal peptide-like immunoreactivity in adjuvant arthritis: effects of capsaicin treatment. Neuropeptides. 29:1995;33-43.
4. Amara S. G., Arriza J. L., Leff S. E., Swanson L. W., Evans R. M., Rosenfeld M. G. Neuropeptide homologous to calcitonin gene-related peptide. Science. 229:1985;1094-1097.
5. Arnér L. D., Meyerson B. A. Lack of analgesic effect of opioids on neuropathic and idiopathic forms of pain. Pain. 33:1988;11-23.
6. Arnér S., Meyerson B. A. Opioids in neuropathic pain. Pain Digest. 3:1993;15-22.
7. Attal N., Jazat F., Kayser V., Guilbaud G. Further evidence for "pain-related" behaviors in a model of unilateral peripheral mononeuropathy. Pain. 41:1990;235-251.
8. Bennett G. J., Xie Y. K. A peripheral mononeuropathy in rat that produces abnormal pain sensation like those seen in man. Pain. 33:1988;87-107.
9. Chapman V., Besson J.-M. Physiological contribution of neurokinin 1 receptor activation, and interactions with NMDA receptors, to inflammatory-evoked spinal c-Fos expression. J. Neurophysiol. 76:1996;1817-1827.
10. 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.
11. Civelli O., Douglass J., Goldstein A., Herbert E. Sequence and expression of the rat prodynorphin gene. Proc. natn. Acad. Sci. U.S.A. 82:1985;4291-4295.
12. Cortes R., Aman K., Arvidsson U., Terenius L., Frey P., Rehfeld J. F., Walsh J. H., Hökfelt T. Immunocytochemical study of cholecystokinin peptide in rat spinal motoneurons. Synapse. 9:1991;103-110.
13. Crawley J. N., Corwin R. L. Biological actions of cholecystokinin. Peptides. 15:1994;731-755.
14. Cruwys S. C., Garrett N. E., Kidd B. L. Sensory denervation with capsaicin attenuates inflammation and nociception in arthritic rats. Neurosci. Lett. 193:1995;205-207.
15. Dagerlind Å., Friberg K., Bean A., Hökfelt T. Sensitive mRNA detection using unfixed tissue: combined radioactive and non-radioactive in situ hybridization histochemistry. Histochemistry. 98:1992;39-49.
16. Dalsgaard C.-J. (1988) The sensory system. In Handbook of Chemical Neuroanatomy (eds Bjorklund A., Hokfelt T. and Owman C.), Vol. 6, pp. 599-636. Elsevier Science, Amsterdam.
17. Deschenes R. J., Lorenz L. J., Haun R. S., Roos B. A., Collier K. J., Dixon J. E. Cloning and sequence analysis of cDNA encoding rat PPT. Proc. natn. Acad. Sci. U.S.A. 81:1984;726-730.
18. Donnerer J., Schuligoi R., Stein C. Increased content and transport of substance P and calcitonin gene-related peptide in sensory nerves innervating inflamed tissue: evidence for a regulatory function of nerve growth factor in vivo. Neuroscience. 49:1992;693-698.
19. Dray A., Urban L., Dickenson A. Pharmacology of chronic pain. Trends pharmac. Sci. 15:1994;190-197.
20. Dubner R., Ruda M. A. Activity-dependent neuronal plasticity following tissue injury and inflammation. Trends Neurosci. 15:1992;96-103.
21. Esser R. E., Hildebrand A. R., Angelo R. A., Watts L. M., Murphey M. D., Baugh L. E. Measurement of radiographic changes in adjuvant-induced arthritis in rats by quantitative image analysis. Arth. Rheum. 38:1995;129-138.
22. 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.
23. Garrett N. E., Kidd B. L., Cruwys S. C., Tomlinson D. R. Changes in preprotachykinin mRNA expression and substance P levels in dorsal root ganglia of monoarthritic rats: comparison with changes in synovial substance P levels. Brain Res. 675:1995;203-207.
24. Garry M. G., Hargreaves K. M. Enhanced release of immunoreactive CGRP and substance P from spinal dorsal horn slices occurs during carrageenan inflammation. Brain Res. 582:1992;139-142.
25. Glick E. N. Asymmetrical rheumatoid arthritis after poliomyelitis. Br. med. J. 3:1967;26-29.
26. Hanesch U., Pfrommer U., Grubb B. D., Schaible H.-G. Acute and chronic phases of unilateral inflammatin in rat's ankle increase the proportion of calcitonin gene-related peptide-immunoreactive dorsal root ganglion cells. Eur. J. Neurosci. 5:1993;154-161.
27. Heppelmann B., Hanesch U. and Schmidt R. F. (1994) Neuropeptides in primary afferents from normal and inflamed joints. In Neuropeptides, Nociception and Pain (eds Hökfelt T., Schaible H.-G. and Schmidt R. F.), pp. 33-42. Chapman & Hall, London.
28. 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.
29. 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.
30. Hökfelt T., Zhang X., Xu X.-Q., Ji R.-R., Shi T., Corness J., Kerekes N., Landry M., Rydh-Rinder M., Broberger C., Wiesenfeld-Hallin Z., Bartfai T., Elde R. and Ju G. (1997) Transition of pain from acute to chronic cellular and synaptic mechanisms. In Proc. 8th World Congress on Pain, Vancouver, 17-22 August (eds Jensen T. S. et al.), IASP, Seattle, in press.
31. Hope P. J., Jarrott J. B., Schaible H.-G., Clarke R. W., Duggan A. W. Release and spread of immunoreactive neurokinin A in the cat spinal cord in a model of acute arthritis. Brain Res. 533:1990;292-299.
32. Hope P. J., Lang C. W., Grubb B. D., Duggan A. W. Release of immunoreactive galanin in the spinal cord of rats with ankle inflammation: studies with antibody microprobes. Neuroscience. 60:1994;801-807.
33. Howells R. D., Kilpatrick D. L., Bhatt R., Monham J. J., Poonian M., Underfriend S. Molecular cloning and sequence determination of rat preproenkephalin cDNA: sensitive probe for studying transcriptional changes in rat tissue. Proc. natn. Acad. Sci. U.S.A. 81:1984;7651-7655.
34. Iadarola M. J., Brady L. S., Draisci G., Dubner R. Enhancement of dynorphin gene expression in spinal cord following experimental inflammation: stimulus specificity, behavioural parameters and opioid receptor binding. Pain. 35:1988;313-326.
35. Iversen L. L. The possible role of neuropeptides in the pathophysiology of rheumatoid arthritis. J. Rheumatol. 12:1985;399-400.
36. Jessell T., Tsunoo A., Kanazawa I., Otsuka M. Depletion in the dorsal horn of the rat spinal cord after section of peripheral processess of primary sensory neurons. Brain Res. 168:1978;247-259.
37. Ji R.-R., Zhang X., Zhang Q., Dagerlind A., Nilssosn S., Wiesenfeld-Hallin Z., Hökfelt T. Central and peripheral expression of galanin in response to inflammation. Neuroscience. 68:1995;563-576.
38. Johnson H., Mossberg K., Arvidsson K., 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.
39. Kar S., Gibson S. J., Rees R. G., Jura W. G., Brewerton D. A., Polak J. M. Increased calcitonin gene-related peptide (CGRP), substance P, and enkephalin immunoreactivities in dorsal spinal cord and loss of CGRP-immunoreactive motoneurons in arthritic rats depend on intact peripheral nerve supply. J. molec. Neurosci. 3:1991;7-18.
40. Kidd B. L., Mapp P. I., Blake D. R., Gibson S. J., Polak J. M. Neurogenic influences in arthritis. Ann. Rheum. Dis. 49:1990;649-652.
41. Kidd B. L., Morris V. H., Urban L. Pathophysiology of joint pain. Ann. Rheum. Dis. 55:1996;276-283.
42. Krause J. E., Chirgwin J. M., Carter M. S., Xu Z. S., Hershey D. Three rat PPT mRAs encode the neuropeptide SP and NKA. Proc. natn. Acad. Sci. U.S.A. 84:1987;881-885.
43. Kupers R. C., Konings H., Adriensen H., Gybels J. M. Morphine differentially affects the sensory and affective pain ratings in neurogenic and idiopathic forms of pain. Pain. 47:1991;5-12.
44. Kuraishi Y., Nanayama T., Ohno H., Fuji N., Otaka A., Yajima H., Satoh M. Calcitonin gene-related peptide increases in the dorsal root ganglia in adjuvant arthritic rat. Peptides. 10:1989;447-452.
45. Larhammar D., Ericsson A., Persson H. Structure and expression of the rat neuropeptide Y gene. Proc. natn. Acad. Sci. U.S.A. 84:1987;2068-2072.
46. Levine J. D., Clark R., Doever M., Helms C., Moskowitz M. A., Basbaum A. I. Intraneuronal substance P contributes to the severity of experimental arthritis. Science. 226:1984;547.
47. Levine J. D., Moskowitz M. A., Basbaum A. I. The contribution of neurogenic inflammation in experimental arthritis. J. Immun. 135:1985;843s-847s.
48. Levine J. D., Collier D. H., Basbaum A. I., Moskowitz M. A., Helms C. A. Hypothesis: the nervous system may contribute to the pathophysiology of rheumatoid arthritis. J. Rheumatol. 12:1985;406-411.
49. Luis S. M., Johnstone D., Russell A., Jamieson A., Dockray G. J. Antibodies to calcitonin gene-related peptide reduce inflammation induced by topical mustard oil but not to carrageenin in the rat. Neurosci. Lett. 102:1989;257-260.
50. Marlier L., Poulat P., Rajaofetra N., Privat A. Modifications of serotonin, substance P- and calcitonin gene-related peptide-like immunoreactivities in the dorsal horn of the spinal cord of arthritic rats: a quantitative immunocytochemical study. Expl Brain Res. 85:1991;482-490.
51. Merchenthaler I., Lopez F. J., Negro-Vilar A. Anatomy and physiology of central galanin-containing pathways. Prog. Neurobiol. 40:1993;711-769.
52. Millan M. J., Millan M. H., Czlonkowski A., Hollt V., Pilcher C. W. T., Herz A., Colpaert F. C. A model of chronic pain in the rat: response of multiple opioid systems to adjuvant-induced arthritis. J. Neurosci. 6:1986;899-906.
53. Minami Y., Kuraishi Y., Kawamura M., Yamaguchi T., Masu Y., Nakanishi S., Satoh M. Enhancement of preprotachykinin A gene expression by adjuvant-induced inflammation in the rat spinal cord: possible involvement of substance P-containing spinal neurons in nociception. Neurosci. Lett. 98:1989;105-110.
54. Noguchi K., Ruda M. A. Gene regulation in an ascending nociceptive pathway: inflammation-induced increase in preprotachykinin mRNA in rat lamina I spinal neurons. J. Neurosci. 12:1992;2563-2572.
55. Pernow B. Role of tachykinins in neurogenic inflammation. J. Immun. 135:1985;812S-815S.
56. Piehl F., Ji R.-R., Cullheim S., Hökfelt T., Lindholm D., Hughes R. A. Fibroblast growth factors regulate calcitonin gene-related peptide mRNA expression in rat motoneurons after lesion and in culture. Eur. J. Neurosci. 7:1995;1739-1750.
57. Ruda M. A., Iadarola M. J., Cohen L. V., Young W. S. I. In situ hybridization histochemistry and immunocytochemistry reveal an increase in spinal dynorphin biosynthesis in rat model of peripheral inflammation and hyperalgesia. Proc. natn. Acad. Sci. U.S.A. 85:1988;622-626.
58. Safieh-Garabedian B., Poole S., Allchorne A., Winter J., Woolf C. J. Contribution of interleukin-1 beta to the inflammation-induced increase in nerve growth factor levels and inflammatory hyperalgesia. Br. J. Pharmac. 115:1995;1265-1275.
59. Schaible H.-G., Jarrott B., Hope P. J., Duggan A. W. Release of immunoreactive substance P in the spinal cord during development of acute arthritis in the knee joint of the cat: a study with antibody microprobes. Brain Res. 529:1990;214-223.
60. Senba E., Yanaihara C., Yanaihara N., Tohyama M. Co-localization of substance P and Met-enkephalin-Arg-Gly-Leu in the intraspinal neurons of the rats, with special reference to the neurons in the substantia gelatinosa. Brain Res. 453:1988;110-116.
61. Skofitsch G., Jacobowitz D. M. Galanin-like immunoreactivity in capsaicin sensitive sensory neurons and ganglia. Brain Res. Bull. 15:1985;191-195.
62. Taquet H., Plachot J. J., Pohl M., Collin E., Benoliel J. J., Bourgoin S., Mauborgna A., Meunier J. C., Cesselin F., Hamon M. Increased calcitonin gene-related peptide and cholecystokinin-like immunoreactivities in spinal motoneurones after dorsal rhizotomy. J. neural Transm. (Gen Sect.). 88:1992;127-141.
63. Thoenen H., Hughes R. A., Sendtner M. Trophic support of motoneurons: physiological, pathophysiological and therapeutic implications. Expl Neurol. 124:1993;47-55.
64. Thomson M., Bywaters E. G. Unilateral rheumatoid arthritis following hemiplegia. Ann. Rheum. Dis. 21:1962;370-377.
65. Uhl G. R., Nishimori T. Neuropeptide gene expression regulation and neural activity: assessing a working hypothesis in nucleus caudalis and dorsal horn neurons expressing preproenkephalin and preprodynorphin. Cell. molec. Neurobiol. 10:1990;73-98.
66. 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.
67. Vrontakis M. E., Peden L. M., Duckworth M. L., Friesen H. G. Isolation and characterization of a complementary DNA (galanin) clone from estrogene-induced pituitary tumor messenger RNA. J. biol. Chem. 262:1987;16755-16758.
68. Wakisaka S., Kajander K. C., Bennett G. J. Increased neuropeptide (NPY)-like immunoreactivity in rat sensory neurons following peripheral axotomy. Neurosci. Lett. 124:1991;200-203.
69. Weihe E., Nohr D., Millan M. J., Stein C., Gramsch C., Höllt V., Herz A. Experimental mono- and polyarthritis differentially intensify immunostaining of multiple proenkephalin- and prodynorphin-opioid peptides in rat lumbosacral neurons. Adv. Biosci. 75:1988;359-362.
70. Weihe E., Millan M. J., Hollt V., Nohr D., Herz A. Induction of the gene encoding pro-dynorphin by experimentally induced arthritis enhances staining for dynorphin in the spinal cord of rats. Neuroscience. 31:1989;77-95.
71. Weihe E., Schäfer M. K.-H., Nohr D. and Persson S. (1994) Expression of neuropeptides, neuropeptide receptors and neuropeptide processing enzymes in spinal neurons and peripheral non-neural cells and plasticity in models of inflammatory pain. In Neuropeptides, Nociception and Pain (eds Hökfelt T., Schaible H.-G. and Schmidt R. F.), pp. 43-69. Chapman & Hall, London.
72. Wiesenfeld-Hallin Z., Bartfai T., Hökfelt T. Galanin in sensory neurons in spinal cord. Front. Neuroendocr. 13:1992;319-343.
73. Zhang X., Nicholas A. P., Hökfelt T. Ultrastructural studies on peptides in the dorsal horn of the rat spinal cord - II. Co-existence of galanin with other peptides in local neurons. Neuroscience. 64:1995;875-891.