Changes in galanin immunoreactivity in rat micturition reflex pathways after cyclophosphamide-induced cystitis

Cell and Tissue Research

Volumn 324, Issue 2, 2006, Pages 213-224

  Zvarova, K ^a   Vizzard, M A ^a  

^a UNIVERSITY OF VERMONT   (United States)

Author keywords

Cystitis; Hyperalgesia; Micturition reflexes; Rat (Wistar, female); Spinal cord

Indexed keywords

CYCLOPHOSPHAMIDE; GALANIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER; BLADDER DISEASE; CONTROLLED STUDY; CYSTITIS; DENSITOMETRY; FEMALE; GRAY MATTER; HYPERALGESIA; IMMUNOREACTIVITY; LUMBAR SPINAL CORD; LUMBOSACRAL SPINE; MICTURITION REFLEX; NONHUMAN; PARASYMPATHETIC NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSORY DYSFUNCTION; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL GANGLION;

AFFERENT PATHWAYS; ANIMALS; CYCLOPHOSPHAMIDE; CYSTITIS; FEMALE; GALANIN; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; RATS; RATS, WISTAR; REFLEX; SPINAL CORD; URINARY BLADDER; URINATION;

ANIMALIA;

EID: 33645813852     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-005-0114-z     Document Type: Article

References (90)

1. Avelino A, Cruz C, Cruz F (2002) Nerve growth factor regulates galanin and c-jun expression occurring in dorsal root ganglion cells after intravesical resiniferatoxin application. Brain Res 951:264-269
2. Beitel RE, Dubner (1976) Response of unmyelinated (C) polymodal nociceptors to thermal stimuli applied to monkey's face. J Neurophysiol 39:1160-1175
3. Bauer FE, Christofides ND, Hacker GW, Blank MA, Polak JM, Bloom SR (1986) Distribution of galanin immunoreactivity in the genitourinary tract of man and rat.Peptides 7:5-10
4. Callsen-Cencic P, Mense S (1997) Expression of neuropeptides and nitric oxide synthase in neurones innervating the inflamed rat urinary bladder. J Auton Nerv Syst 65:33-44
5. Calza L, Pozza M, Zanni M, Manzini CU, Manzini E, Hökfelt T (1998) Peptide plasticity in primary sensory neurons and spinal cord during adjuvant-induced arthritis in the rat: an immunocytochemical and in situ hybridization study. Neuroscience 82:575-589
6. Campbell JN, Meyer RA (1986) Primary afferents and hyperalgesia. In: Yaksh T (ed) Spinal afferent processing. Plenum, New York, pp 59-81
7. Chien CT, Yu HJ, Lin TB, Lai MK, Hsu SM (2003) Substance P via NK1 receptor facilitates hyperactive bladder afferent signaling via action of ROS. Am J Physiol 284:F840-F851
8. Chuang YC, Fraser MO, Yu YB, Chancellor MB, Groat WC de, Yoshimura N (2001) The role of bladder afferent pathways in bladder hyperactivity induced by the intravesical administration of nerve growth factor. J Urol 165:975-979
9. Coderre TJ, Katx J, Vaccarino AL, Melzack R (1993) Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence. Pain 52:259-285
10. Colvin LA, Mark MA, Duggan AW (1997) The effect of a peripheral mononeuropathy on immunoreactive (ir)-galanin release in the spinal cord of the rat. Brain Res 766:259-261
11. Cox PJ (1979) Cyclophosphamide cystitis - identification of acrolein as the causative agent. Biochem Pharmacol 28:2045
12. Dattilio A, Vizzard MA (2005) Up-regulation of protease activated receptors in bladder after cyclophosphamide induced cystitis and colocalization with capsaicin receptor (VR1) in bladder nerve fibers. J Urol 173:635-639
13. Dmitrieva N, McMahon SB (1996) Sensitisation of visceral afferents by nerve growth factor in the adult rat. Pain 66:87-97
14. Dmitrieva N, Shelton D, Rice ASC, McMahon SB (1997) The role of nerve growth factor in a model of visceral inflammation. Neuroscience 78:449-459
15. Donaldson LF, Harmar AJ, McQueen DS, Seckl JR (1992) 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 16:143-149
16. Donnerer J, Stein C (1992) Evidence for an increase in the release of CGRP and sensory nerves during inflammation. Ann N Y Acad Sci 657:505-506
17. Donnerer J, Schuligoi R, Stein C (1992) 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 49:693-698
18. Donovan MK, Winternitz SR, Wyss JM (1983) An analysis of the sensory innervation of the urinary system of the rat. Brain Res Bull 11:321-324
19. Dubner R, Ruda MA (1992) Activity dependent neuronal plasticity following tissue injury and inflammation. Trends Neurosci 15:96-103
20. Erickson DR (1999) Interstitial cystitis: update on etiologies and therapeutic options. J Womens Health Gender-Based Med 8:745-758
21. Erickson DR, Davies MF (1998) Interstitial cystitis. Int Urogynecol 19:174-183
22. FitzGerald MP (2003) Chronic pelvic pain. Curr Womens Health Rep 3:327-333
23. Gary MB, Hargreaves KM (1992) Enhanced release of immunoreactive CGRP and substance P from spinal dorsal horn slices occurs during carrageenan inflammation. Brain Res 582:139-142
24. Groat WC de (1993) Anatomy and physiology of the lower urinary tract. Urol Clin North Am 20:383-401
25. Groat WC de, Araki I (1999) Maturation of bladder reflex pathways during postnatal development. Adv Exp Med Biol 462:253-263 (discussion 311-220)
26. Groat WC de, Araki I, Vizzard MA, Yoshiyama M, Yoshimura N, Sugaya K, Tai C, Roppolo JR (1998) Developmental and injury induced plasticity in the micturition reflex pathway. Behav Brain Res 92:127-140
27. Guerios SD, Wang Z-Y, Bjorling DE (2005) Cyclophosphamide-induced peripheral hypersensitivity is mediated by nerve growth factor. Urothelial Cell Physiol Normal Dis States p52
28. Hanesch U, Pfrommer U, Grubb BD, Schaible H-G (1993) 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 5:154-161
29. Hökfelt T, Broberger C, Diez M, Xu ZQ, Shi T, Kopp J, Zhang X, Holmberg K, Landry M, Koistinaho J (1999) Galanin and NPY, two peptides with multiple putative roles in the nervous system. Hormone Metab Res 31:330-334
30. Holmes FE, Bacon A, Pope RJ, Vanderplank PA, Kerr NC, Sukumaran M, Pachnis V, Wynick D (2003) Transgenic overexpression of galanin in the dorsal root ganglia modulates pain-related behavior. Proc Natl Acad Sci USA 100:6180-6185
31. Hu P, McLachlan EM (2001) Long-term changes in the distribution of galanin in dorsal root ganglia after sciatic or spinal nerve transection in rats. Neuroscience 103:1059-1071
32. Hu VY, Malley S, Dattilio A, Folsom JB, Zvara P, Vizzard MA (2003) COX-2 and prostanoid expression in micturition pathways after cyclophosphamide-induced cystitis in the rat. Am J Physiol 284:R574-R585
33. Hua X-Y, Salgado KF, Gu G, Fitzsimmons B, Kondo I, Bartfai T, Yaksh TL (2005) Mechanisms of antinociception of spinal galanin: how does galanin inhibit spinal sensitizations? Neuropeptides 39:211-216
34. Hygge-Blakeman K, Brumovsky P, Hao J-X, Wu X-J, Hökfelt T, Crawley JN, Wiesenfeld-Hallin Z (2004) Galanin over-expression decreases the development of neuropathic pain-like behaviors in mice after partial sciatic nerve injury. Brain Res 1025:152-158
35. Jaggar SI, Scott HC, Rice AS (1999) Inflammation of the rat urinary bladder is associated with a referred thermal hyperalgesia which is nerve growth factor dependent. Br J Anaesth 83:442-448
36. Jennings LJ, Vizzard MA (1999) Cyclophosphamide-induced inflammation of the urinary bladder alters electrical properties of small diameter afferent neurons from dorsal root ganglia. FASEB J 13:A57
37. Ji R-R, Zhang X, Zhang Q, Dagerlind Å, Nilsson S, Wiesenfeld-Hallin Z, Hökfelt T (1995) Central and peripheral expression of galanin in response to inflammation. Neuroscience 68:563-576
38. Keast JR, Groat WC de (1992) Segmental distribution and peptide content of primary afferent neurons innervating the urogenital organs and colon of male rats. J Comp Neurol 19:615-623
39. Landry M, Liu HX, Shi TJ, Brumovsky P, Nagy F, Hökfelt T (2005) Galaninergic mechanisms at the spinal level: focus on histochemical phenotyping. Neuropeptides 39:223-231
40. Landry M, Aman K, Dostrovsky J, Lozano AM, Carlstedt T, Spenger C, Josephson A, Wiesenfeld-Hallin Z, Hökfelt T (2003) Galanin expression in adult human dorsal root ganglion neurons: initial observations. Neuroscience 117:795-809
41. Lantéri-Minet M, Bon K, Pommery J de, Michiels JF, Menétrey D (1995) Cyclophosphamide cystitis as a model of visceral pain in rats: model elaboration and spinal structures involved as revealed by the expression of c-Fos and Krox-24 proteins. Exp Brain Res 105:220-232
42. Lecci A, Giulani S, Santiciolo P, Maggi CA (1994) Involvement of spinal tachykinin NK1 and NK2 receptors in detrusor hyperreflexia during chemical cystitis in anaesthetized rats. Eur J Pharm 259:129-135
43. Liu HX, Hökfelt T (2002) The participation of galanin in pain processing at the spinal level. Trends Pharmacol Sci 23:468-474
44. Lowe EM, Anand P, Terenghi G, Willimans-Chestnut RE, Sinicropi DV (1997) Increased nerve growth factor levels in the urinary bladder of women with idiopathic sensory urgency and interstitial cystitis. Br J Urol 79:572-577
45. Maggi CA, Santicioli P, Patacchini R, Turini D, Barbanti G, Beneforti P, Giuliani S, Meli A (1987) Galanin: a potent modulator of excitatory neurotransmission in the human urinary bladder. Eur J Pharmacol 143:135-137
46. Maggi CA, Lecci A, Santiciolo P, Del Biance E, Giuliani S (1992) Cyclophosphamide cystitis in rats: involvement of capsaicin-sensitive primary afferents. J Auton Nerv Syst 38:201-208
47. Maggi CA, Lecci A, Santicioli P, Del Bianco E, Giuliani S (1993) Cyclophosphamide-induced cystitis in rats: involvement of capsaicin-sensitive primary afferents. Agents Actions 38:C28-C30
48. Mahoney SA, Hosking R, Farrant S, Holmes FE, Jacoby AS, Shine J, Iismaa TP, Scott MK, Schmidt R, Wynick D (2003) The second galanin receptor GalR2 plays a key role in neurite outgrowth from adult sensory neurons. J Neurosci 23: 416-421
49. McMahon SB, Abel C (1987) A model for the study of visceral pain states: chronic inflammation of the chronic decerebrate rat urinary bladder by irritant chemicals. Pain 28:109-127
50. Meller ST, Gebhart GF (1993) Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain 52:127-136
51. Morgan C, Nadelhaft I, Groat WC de (1981) 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 201:415-440
52. Morrison JFB (1987) Reflex control of the lower urinary tract. In: Torrens M, Morrison JFB (eds) The physiology of the lower urinary tract. Springer, Berlin Heidelberg New York, pp 53-132
53. Nadelhaft I, Vera PL (1995) Central nervous system neurons infected by pseudorabies virus injected into the rat urinary bladder following unilateral transection of the pelvic nerve. J Comp Neurol 359:443-456
54. Newton BW (1992a) Galanin-like immunoreactivity in autonomic regions of the rat lumbosacral spinal cord is sexually dimorphic and varies with the estrous cycle. Brain Res 589:69-83
55. Newton BW (1992b) A sexually dimorphic population of galanin-like neurons in the rat lumbar spinal cord: functional implications. Neurosci Lett 137:119-122
56. Ohmachi T, Nakamura T, Zhang FZ, Tani I, Takagi H (1996) Morphological analyses of galaninergic inputs to the rat spinal parasympathetic nucleus. Exp Brain Res 109:399-406
57. Okragly AJ, Niles AL, Saban R, Schmidt D, Hoffman RL, Warner TF, Moon TD, Uehling DT, Haak-Frendscho M (1999) Elevated tryptase, nerve growth factor, neurotrophin-3 and glial cell line-derived neurotrophic factor levels in the urine of interstitial cystitis and bladder cancer patients. J Urol 161:438-442
58. Perl ER, Kumuzawa T, Lynn B, Kenins P (1974) Sensitization of high threshold receptors with unmyelinated (C) afferent fibres. In: Iggo A, Ilynsky I (eds) Somatosensory and visceral receptor mechanisms: progress in brain research. Elsevier, Amsterdam, pp 263-278
59. Qiao LY, Vizzard MA (2002a) Up-regulation of tyrosine kinase (Trka, Trkb) receptor expression and phosphorylation in lumbosacral dorsal root ganglia after chronic spinal cord (T8-T10) injury. J Comp Neurol 449:217-230
60. Qiao LY, Vizzard MA (2002b) Cystitis-induced upregulation of tyrosine kinase (TrkA, TrkB) receptor expression and phosphorylation in rat micturition pathways. J Comp Neurol 454:200-211
61. Qiao LY, Vizzard MA (2004) Up-regulation of phosphorylated CREB but not c-Jun in bladder afferent neurons in dorsal root ganglia after cystitis. J Comp Neurol 469:262-274
62. Ruda MA, Iadarola MJ, Cohen LV, Young II WS (1988) In situ hybridization, histochemistry and immunocyctochemistry reveal an increase in spinal dynorphin biosynthesis in a rat model of peripheral inflammation and hyperalgesia. Proc Natl Acad Sci USA 85:622-626
63. Seki S, Erickson KA, Seki M, Nishizawa O, Igawa Y, Ogawa T, Groat WC de, Chancellor MB, Yoshimura N (2005) Elimination of rat spinal neurons expressing neurokinin 1 receptors reduces bladder overactivity and spinal c-fos expression induced by bladder irritation. Am J Physiol Renal 288:F466-F473
64. Smith GD, Harmar AJ, McQueen DS, Seckl JR (1992) Increase in substance P and CGRP, but not somatostatin content of innervating dorsal root ganglia in adjuvant monoarthritis in the rat. Neurosci Lett 137:257-260
65. Steers WD, Groat WC de (1988) Effect of bladder outlet obstruction on micturition reflex pathways in the rat. J Urol 140:864-871
66. Steers WD, Kolbeck S, Creedon D, Turtle JB (1991a) Nerve growth factor in the urinary bladder of the adult regulates neuronal form and function. J Clin Invest 88:1709-1715
67. Steers WD, Ciambotti J, Etzel B, Erdman S, Groat WC de (1991b) Alterations in afferent pathways from the urinary bladder of the rat in response to partial urethral obstruction. J Comp Neurol 310:1-10
68. Steers WD, Creedon DJ, Turtle JB (1996) Immunity to nerve growth factor prevents afferent plasticity following urinary bladder hypertrophy. J Urol 155:379-385
69. Tuchscherer MM, Seybold VS (1989) A quantitative study of the coexistence of peptides in varicosities within the superficial laminae of the dorsal horn of the rat spinal cord. J Neurosci 9:195-205
70. Tuttle JB, Steers WD, Albo M, Nataluk E (1994) Neural input regulates tissue NGF and growth of the adult rat urinary bladder. J Auton Nerv Syst 49:147-158
71. Villar MJ, Cortes R, Theodorsson E, Wiesenfeld-Hallin Z, Schalling M, Fahrenkrug J, Emson PC, Hökfelt T (1989) Neuropeptide expression in rat dorsal root ganglion cells and spinal cord after peripheral nerve injury with special reference to galanin. Neuroscience 33:587-604
72. Vizzard MA (1997) Increased expression of neuronal nitric oxide synthase in bladder afferent and spinal neurons following spinal cord injury. Dev Neurosci 19:232-246
73. Vizzard MA (1999) Alterations in growth-associated protein (GAP-43) expression in lower urinary tract pathways following chronic spinal cord injury. Somatosens Motor Res 16:369-381
74. Vizzard MA (2000a) Increased expression of spinal Fos protein in lower urinary tract pathways induced by bladder distension following chronic cystitis. Am J Physiol 279:R295-R305
75. Vizzard MA (2000b) Changes in urinary bladder neurotrophic factor mRNA and NGF protein following urinary bladder dysfunction. Exp Neurol 161:273-284
76. Vizzard MA (2000c) Up-regulation of pituitary adenylate cyclase-activating polypeptide in urinary bladder pathways after chronic cystitis. J Comp Neurol 420:335-348
77. Vizzard MA (2001) Alterations in neuropeptide expression in lumbosacral bladder pathways following chronic cystitis. J Chem Neuroanat 21:125-138
78. Vizzard MA, Qiao L, Zvara P (2003) Neurotrophic mechanisms in bladder overactivity after spinal cord injury. Auton Neurosci 106:14
79. Wesselmann U (2001) Neurogenic inflammation and chronic pelvic pain. World J Urol 19:180-185
80. Wiesenfeld-Hallin Z, Xu XJ, Villar MJ, Hökfelt T (1989) The effect of intrathecal galanin on the flexor reflex in rat: increased depression after sciatic nerve section. Neurosci Lett 105:149-154
81. Wisenfeld-Hallin Z, Xu X-J, Crawley JN, Hökfelt T (2005) Galanin and spinal nociceptive mechanisms: recent results from transgenic and knock-out models. Neuropeptides 39:207-210
82. Woolf CJ, Allchorne A, Safieh-Garabedian B, Poole S (1997) Cytokines, nerve growth factor and inflammatory hyperalgesia: the contribution of tumour necrosis factor. Br J Pharm 121:417-424
83. Xu XJ, Hökfelt T, Bartfai T, WiesenfeldHallin Z (2000) Galanin and spinal nociceptive mechanisms: recent advances and therapeutic implications. Neuropeptides 34:137-147
84. Xu ZQ, Zheng K, Hökfelt T (2005) Electrophysiological studies on galanin effects in brain - progress during the last six years. Neuropeptides 39:269-275
85. Yoshimura N (1999) Bladder afferent pathways and spinal cord injury: possible mechanisms inducing hyperreflexia of the urinary bladder. Prog Neurobiol 57:583-606
86. Yoshimura N, Groat WC de (1999) Increased excitability of afferent neurons innervating rat urinary bladder following chronic bladder inflammation. J Neurosci 19:4644-4653
87. Zhang X, Bean AJ, Wiesenfeld-Hallin Z, Hökfelt T (1995) Ultrastructural studies on peptides in the dorsal horn of the rat spinal cord-IV. Effects of peripheral axotomy with special reference to neuropeptide Y and vasoactive intestinal polypeptide/peptide histidine isoleucine. Neuroscience 64:917-941
88. Zhang X, Xu ZO, Shi TJ, Landry M, Holmberg K, Ju G, Tong YG, Bao L, Cheng XP, Wiesenfeld-Hallin Z, Lozano A, Dostrovsky J, Hökfelt T (1998) Regulation of expression of galanin and galanin receptors in dorsal root ganglia and spinal cord after axotomy and inflammation. Ann N Y Acad Sci 863:402-413
89. Zvara P, Kliment J, DeRoss AL, Irwin BH, Malley SE, Plante MK, Vizzard MA (2002) Differential expression of bladder neurotrophic factor mRNA in male and female rats after bladder outflow obstruction. J Urol 168:2682-2688
90. Zvarova K, Murray E, Vizzard MA (2004) Changes in galanin immunoreactivity in rat lumbosacral spinal cord and dorsal root ganglia after spinal cord injury. J Comp Neurol 475:590-603