Increased expression of growth-associated protein (GAP-43) in lower urinary tract pathways following cyclophosphamide (CYP)-induced cystitis

Brain Research

Volumn 844, Issue 1-2, 1999, Pages 174-187

  Vizzard, Margaret A ^a   Boyle, Melissa M ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Dorsal root ganglia; Lateral collateral pathway; Neurotrophic factor; Sacral parasympathetic nucleus; Spinal cord; Urinary bladder inflammation

Indexed keywords

CYCLOPHOSPHAMIDE; NEUROMODULIN; NEUROTROPHIC FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER DISEASE; CONTROLLED STUDY; CYSTITIS; DENSITOMETRY; ELECTROPHYSIOLOGY; FEMALE; IMMUNOHISTOCHEMISTRY; LUMBAR SPINAL CORD; MICTURITION REFLEX; NERVE PROJECTION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT; SPINAL GANGLION; URETHRA;

ANIMALS; CYCLOPHOSPHAMIDE; CYSTITIS; DENSITOMETRY; FEMALE; GANGLIA, PARASYMPATHETIC; GANGLIA, SPINAL; GAP-43 PROTEIN; IMMUNOSUPPRESSIVE AGENTS; LUMBOSACRAL REGION; RATS; RATS, WISTAR; SPINAL CORD; URINARY BLADDER;

EID: 0032834944     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(99)01936-8     Document Type: Article

References (77)

1. Alvarez F.J., Rodrigo J., Jessel T.M., Dodd J., Priestley J.V. Morphology and distribution of primary afferent fibres expressing alpha-galactose extended oligosaccharides in the spinal cord and brainstem of the rat. J. Neurocytol. 18:1989;611-629.
2. Beitel R.E., Dubner R. Response of unmyelinated (C) polymodal nociceptors to thermal stimuli applied to monkey's face. J. Neurophysiol. 39:1976;1160-1175.
3. 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.
4. Benowitz L.I., Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 20:1997;84-91.
5. Birder L.A., de Groat W.C. Induction of c-fos expression in spinal neurons by nociceptive and nonnociceptive of the LUT. Am. J. Physiol. 265:1993;R326-R333.
6. J.N. Campbell, R.A. Meyer, Primary afferents and hyperalgesia, in: T.L. Yaksh (Ed.), Spinal Afferent Processing, Plenum, New York, 1986, pp. 59-81.
7. Chong M.S., Reynolds M.L., Irwin N., Coggeshall R.E., Emson P.C., Benowitz L.I., Woolf C.J. GAP-43 expression in primary sensory neurons following central axotomy. J. Neurosci. 14:1994;4375-4384.
8. Chung K., Langford L.A., Applebaum A.E., Coggeshall R.E. Primary afferent fibres in the Tract of Lissauer in the rat. J. Comp. Neurol. 184:1979;587-598.
9. Coderre T.J., Katx J., Vaccarino A.L., Melzack R. Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence. Pain. 52:1993;259-285.
10. Cox P.J. Cyclophosphamide cystitis - identification of acrolein as the causative agent. Biochem. Pharmacol. 28:1979;2045.
11. Curtis R., Averill S., Priestley J.V., Wilkin G.P. The distribution of GAP-43 in normal rat spinal cord. J. Neurocytol. 22:1993;39-50.
12. W.C. de Groat, A.M. Booth, N. Yoshimura, Neurophysiology of micturition and its modification in animal models of human disease, in: C.A. Maggi (Ed.), The Autonomic Nervous System, Harwood Academic Publishers, London, 1993, pp. 227-290.
13. Dmitrieva N., McMahon S.B. Sensitisation of visceral afferents by nerve growth factor in the adult rat. Pain. 66:1996;87-97.
14. Dmitrieva N., Shelton D., Rice A.S.C., McMahon S.B. The role of nerve growth factor in a model of visceral inflammation. Neuroscience. 78:1997;449-459.
15. Donaldson L.F., Harmar A.J., McQueen D.S., Seckl J.R. Increased expression of preprotachykinin, calcitonin gene-related peptide, but not vasoactive intestinal peptide messenger RNA in dorsal root ganglia during the development of adjuvant monoarthritis in the rat. Mol. Brain Res. 16:1992;143-149.
16. Donovan M.K., Winternitz S.R., Wyss J.M. An analysis of the sensory innervation of the urinary system of the rat. Brain Res. Bull. 11:1983;321-324.
17. Doone G.V., Vizzard M.A. Redistribution and increased numbers of Fos-immunoreactive (IR) cells in the lumbosacral (L6-S1) spinal cord induced by urinary bladder distension following chronic cyclophosphamide (CYP)-induced urinary bladder inflammation in the rat: effects of capsaicin. Soc. Neurosci. Abstr. 24:1998;1617.
18. Doubell T.P., Woolf C.J. Growth-associated protein 43 immunoreactivity in the superficial dorsal horn of the rat spinal cord is localized in atrophic C-fiber, and not in sprouted A-fiber, central terminals after peripheral nerve injury. J. Comp. Neurol. 386:1997;111-118.
19. Dubner R., Ruda M.A. Activity dependent neuronal plasticity following tissue injury and inflammation. Trends Neurosci. 15:1992;96-103.
20. Eide F.F., Lowenstein D.H., Reichardt L.F. Neurotrophins and their receptors - current concepts and implications for neurologic disease. Exp. Neurol. 121:1993;200-214.
21. Habler H.J., Jänig W., Koltzenburg M. Activation of unmyelinated afferent fibers by mechanical stimuli and identification of the urinary bladder in the cat. J. Physiol. 425:1990;545-562.
22. Hanesch U., Pfrommer U., Grubb B.D., Schaible H.-G. Acute and chronic phases of unilateral inflammation in rat's ankle are associated with an increase in the proportion of calcitonin gene-related peptide-immunoreactive dorsal root ganglion cells. Eur. J. Neurosci. 5:1993;154-161.
23. Hefti F. Pharmacology of neurotrophic factors. Annu. Rev. Pharmacol. Toxicol. 37:1997;239-267.
24. N. Ho, J.A. Koziol, C.L. Parsons, Epidemiology of interstitial cystitis, In: G.R. Sant (Ed.), Interstitial Cystitis, Lippincott-Raven Publishers, Philadelphia, 1997, pp. 9-16.
25. Jacobson R.D., Virag I., Skene J.H.P. A protein associated with axon growth, GAP-43, is widely distributed and developmentally regulated in rat CNS. J. Neurosci. 6:1986;1843-1855.
26. Jennings L.J., Vizzard M.A. Cyclophosphamide-induced inflammation of the urinary bladder alters electrical properties of small diameter afferent neurons from dorsal root ganglia. FASEB J. 13:1999;A57.
27. S.L. Johansson, K. Ogawa, M. Fall, The pathology of interstitial cystitis, in: G.R. Sant (Ed.), Interstitial Cystitis, Lippincott-Raven Publishers, Philadelphia, 1997, pp. 143-152.
28. Keast J.R., de Groat W.C. Segmental distribution and peptide content of primary afferent neurons innervating the urogenital organs and colon of male rats. J. Comp. Neurol. 319:1992;615-623.
29. Knyihar-Csillik E., Csillik B., Oestreicher A.B. Light and electron microscopic localization of B-50 (GAP-43) in rat spinal cord during transganglionic degenerative atrophy and regeneration. J. Neurosci. Res. 32:1992;93-109.
30. Korsching S. The neurotrophic factor concept: a reexamination. J. Neurosci. 13:1993;2739-2748.
31. Kruse M.N., Noto H., Roppolo J.R., de Groat W.C. Pontine control of the urinary bladder and external urethral sphincter in the rat. Brain Res. 532:1990;182-190.
32. Kuru M. Nervous control of micturition. Physiol. Rev. 45:1965;425-494.
33. Lantéri-Minet M., Bon K., de Pommery J., Michiels J.F., Menétrey D. Cyclophosphamide cystitis as a model of visceral pain in rats: model elaboration and spinal structures involves as revealed by the expression of c-Fos and Krox-24 proteins. Exp. Brain Res. 105:1995;220-232.
34. Lecci, Giulani S., Santiciolo P., Maggi C.A. Involvement of spinal tachykinin NK1 and NK2 receptors in detrusor hyperreflexia during chemical cystitis in anaesthetized rats. Eur. J. Pharmacol. 259:1994;129-135.
35. Leslie T.A., Emson P.C., Dowd P.M., Woolf C.J. Nerve growth factor contributes to the up-regulation of growth-associated protein 43 and preprotachykinin A messenger RNAs in primary sensory neurons following peripheral inflammation. Neuroscience. 67:1995;753-761.
36. Levine L.A., Richie J.P. Urological complications of cyclophosphamide. J. Urol. 141:1989;1063-1069.
37. Loewy A.D., Saper C.B., Baker R.P. Descending projections from the pontine micturition center. Brain Res. 172:1979;533-538.
38. Maggi C.A., Lecci A., Santiciolo P., Del Biance E., Giuliani S. Cyclophosphamide cystitis in rats: involvement of capsaicin-sensitive primary afferents. J. Auton. Nerv. Syst. 38:1992;201-208.
39. McMahon S.B., Armanini M.P., Ling L.H., Phillips H.S. Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron. 12:1994;1161-1171.
40. McMahon S.B. NGF as a mediator of inflammatory pain. Philos. Trans. R. Soc. London. 351:1996;431-440.
41. McNeill D.L., Papka R.E., Hamilton M.O., O'Donoghue D.L., Mayer B. Relationship of nitric oxide synthase (NOS) to L6/S1 spinal neurons that project to the pontine micturition center (PMC) in the rat. Soc. Neurosci. Abstr. 19:1993;509.
42. Meller S.T., Gebhart G.F. Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain. 52:1993;127-136.
43. Morgan, Nadelhaft I., de Groat W.C. The distribution of visceral primary afferents from the pelvic nerve within Lissauer's tract and the spinal gray matter and its relationship to the sacral parasympathetic nucleus. J. Comp. Neurol. 201:1981;415-440.
44. Noto H., Roppolo J.R., Steers W.D., de Groat W.C. Electrophysiological analysis of the ascending and descending components of the micturition reflex pathway in the rat. Brain Res. 549:1989;95-105.
45. Noto H., Roppolo J.R., Steers W.D., de Groat W.C. Excitatory and inhibitory influences on bladder activity elicited by electrical stimulation in the pontine micturition center in rat. Brain Res. 492:1991;99-115.
46. N. Pelissier, G. Doone, M.M. Boyle, M.A. Vizzard, Changes in growth associated protein (GAP-43), calcitonin gene-related peptide (CGRP) and pituitary adenylate cyclase-activating polypeptide (PACAP-38) in L6-S1 spinal cord and dorsal root ganglia (DRG) following cyclophosphamide (CYP)-induced cystitis, Soc. Neurosci. Abstr. (1999) submitted.
47. E.R. Perl, T. Kumuzawa, B. Lynn, P. Kenins, Sensitization of high threshold receptors with unmyelinated (C) afferent fibres, in: A. Iggo, I. Ilynsky (Eds.), Somatosensory and Visceral Receptor Mechanisms, Progress in Brain Research, Elsevier, Amsterdam, 1974, pp. 263-278.
48. Petrone R.L., Agha A.H., Roy J.B., Hurst R.E. Urodynamic findings in patients with interstitial cystitis. J. Urol. 153:1995;290A.
49. L.F. Reichardt, I. Farinas, Neurotrophic factors and their receptors; roles in neuronal development and function, in: W.M. Cowan, T.M. Jessel, S.L. Zipursky (Eds.), Molecular and Cellular Approaches to Neural Development, Oxford Univ. Press, New York, 1997, pp. 220-263.
50. Rinaman L., Card J.P., Enquist L.W. Spatiotemporal responses of astrocytes, ramified microglia, and brain macrophages to central neuronal infection with pseudorabies virus. J. Neurosci. 13:1993;685-702.
51. Ruda M.A., Iadarola M.J., Cohen L.V., Young II W.S. In situ hybridization, histochemistry and immunocytochemistry reveal an increase in spinal dynorphin biosynthesis in a rat model of peripheral inflammation and hyperalgesia. Proc. Natl. Acad. Sci. 85:1988;622-626.
52. Satoh K., Shimizu N., Tohyama M., Maeda T. Localization of the micturition reflex center at dorsolateral pontine tegmentum of the rat. Neurosci. Lett. 8:1978;27-33.
53. Satoh K., Tohyama M., Sakumoto T., Yamamoto K., Shimizu N. Descending projection of the nucleus tegmentalis laterodorsalis to the spinal cord: studied by the horseradish peroxidase method following 6-hydroxydopa administration. Neurosci. Lett. 8:1978;9-15.
54. Schreyer D.J., Skene J.H.P. 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.
55. Sengupta J.N., Gebhart G.F. Mechanosensitive properties of pelvic nerve afferent fibres innervating the urinary bladder of the rat. J. Neurophysiol. 72:1994;2420-2430.
56. Skene J.H.P., Jacobson R.D., Snipes G.J., McGuire C.B., Norden J.J., Freeman J.A. A protein induced during nerve growth (GAP-43) is a major component of growth-cone membranes. Science. 233:1986;783-786.
57. Smith G.D., Harmar A.J., McQueen D.S., Seckl J.R. Increase in substance P and CGRP, but not somatostatin content of innervating dorsal root ganglia in adjuvant monarthritis in the rat. Neurosci. Lett. 137:1992;257-260.
58. Steers W.D., de Groat W.C. Effect of bladder outlet obstruction on micturition reflex pathways in the rat. J. Urol. 140:1988;864-871.
59. Steers W.D., Ciambotti J., Etzel B., Erdman S., de Groat W.C. Alterations in afferent pathways from the urinary bladder of the rat in response to partial urethral obstruction. J. Comp. Neurol. 310:1991;1-10.
60. Steers W.D., Creedon D.J., Tuttle J.B. Immunity to nerve growth factor prevents afferent plasticity following urinary bladder hypertrophy. J. Urol. 155:1996;379-385.
61. Stewart H.J.S., Cowen T., Curtis R., Wilkin G.P., Mirsky R., Jessen K.R. GAP-43 immunoreactivity is widespread in the autonomic neurons and sensory neurons of the rat. Neuroscience. 47:1992;673-684.
62. Stillwell T.J., Benson R.C. Cyclophosphamide-induced cystitis. A review of 100 patients. Cancer. 61:1988;451-457.
63. Strittmatter S.M., Fankhauser C., Huang P.L., Mashimo H., Fishman M.C. Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell. 80:1995;445-452.
64. Su H.C., Polak J.M., Mulderry P.K., Ghatei M.A., Gibson S.J., Terenghi G., Morrison J.F.B., Ballesta J., Bloom S.R. Calcitonin gene-related peptide immunoreactivity in afferent neurons supplying the urinary tract: combined retrograde tracing and immunohistochemistry. Neuroscience. 18:1986;727-747.
65. Sugaya K., Matsuyama K., Takakusaki K., Mori S. Electrical and chemical stimulations of the pontine micturition center. Neurosci. Lett. 80:1987;197-201.
66. Tuttle J.B., Steers W.D., Albo M., Nataluk E. Neural input regulates tissue NGF and growth of the adult rat urinary bladder. J. Auton. Nerv. Syst. 49:1994;147-158.
67. Van Lookeren Campagne M., Oestreicher A.B., Van Bergen en Henegouwen P.M.P., Gispen W.H. Ultrastructural immunocytochemical localisation of B-50/GAP-43, a protein kinase C substrate, in isolated presynaptic nerve terminals and neuronal growth cones. J. Neurocytol. 18:1989;479-489.
68. Vantini G., Skaper S.D. Neurotrophic factors: from physiology to pharmacology. Pharmacol. Res. 26:1992;1-15.
69. Verge V.M., Tetzlaff W., Richardson P.M., Bisby M.A. Correlation between GAP-43 and nerve growth factor receptors in rat sensory neurons. J. Neurosci. 10:1990;926-934.
70. Verkade P., Schrama L.H., Verkleij A.J., Gispen W.H., Oestreicher A.B. Ultrastructural co-localization of calmodulin and B-50/growth-associated protein-43 at the plasma membrane of proximal unmyelinated axon shafts studied in the model of the regenerating rat sciatic nerve. Neuroscience. 79:1997;1207-1218.
71. Vizzard M.A., Erdman S.L., de Groat W.C. Localization of NADPH-diaphorase in bladder afferent and postganglionic efferent neurons of the rat. J. Auton. Nerv. Syst. 44:1993;85-90.
72. Vizzard M.A., de Groat W.C. Increased expression of neuronal nitric oxide synthase (NOS) in bladder afferent pathways following chronic bladder irritation. J. Comp. Neurol. 370:1996;191-202.
73. Vizzard M.A. Neurotrophin mRNA expression is increased in urinary bladder following cyclophosphamide (CYP)-induced inflammation or spinal cord injury. FASEB J. 13:1999;A57.
74. M.A. Vizzard, Changes in neurotrophic factor mRNA and NGF protein following urinary bladder dysfunction (1999) submitted.
75. Watson N.A., Notley R.G. Urological complications of cyclophosphamide. Br. J. Urol. 45:1973;606.
76. 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.
77. Yoshimura N., de Groat W.C. Increased excitability of afferent neurons innervating rat urinary bladder following chronic bladder inflammation. J. Neurosci. 19:1999;4644-4653.