Up-regulation of calcitonin gene-related peptide and receptor tyrosine kinase TrkB in rat bladder afferent neurons following TNBS colitis

Experimental Neurology

Volumn 204, Issue 2, 2007, Pages 667-679

  Qiao, Li Ya ^a   Grider, John R ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

CGRP; Convergence; Cross sensitization; Neurotrophins; Primary afferent neuron; Visceral inflammation

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CALCITONIN GENE RELATED PEPTIDE; K 252A; NEUROTROPHIN; PROTEIN TYROSINE KINASE; TRINITROBENZENESULFONIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER; COLITIS; COLON DISEASE; CONTROLLED STUDY; CYSTITIS; HYPERSENSITIVITY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; NERVE CELL CULTURE; NEUROGENIC BLADDER; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE; SPINAL GANGLION;

AMIDINES; ANALYSIS OF VARIANCE; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CARBOCYANINES; CELLS, CULTURED; COLITIS; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; MALE; METHACRYLATES; NEURONS, AFFERENT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB; UP-REGULATION; URINARY BLADDER;

EID: 33947646443     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2006.12.024     Document Type: Article

References (64)

1. Alagiri M., Chottiner S., Ratner V., Slade D., and Hanno P.M. Interstitial cystitis: unexplained associations with other chronic disease and pain syndromes. Urology 49 (1997) 52-57
2. Applebaum A.E., Vance W.H., and Coggeshall R.E. Segmental localization of sensory cells that innervate the bladder. J. Comp. Neurol. 192 (1980) 203-209
3. Ben-Ami H., Ginesin Y., Behar D.M., Fischer D., Edoute Y., and Lavy A. Diagnosis and treatment of urinary tract complications in Crohn's disease: an experience over 15 years. Can. J. Gastroenterol. 16 (2002) 225-229
4. Bennett D.L., Dmietrieva N., Priestley J.V., Clary D., and McMahon S.B. TrkA, CGRP and IB4 expression in retrogradely labeled cutaneous and visceral primary sensory neurons in the rat. Neurosci. Lett. 206 (1996) 33-36
5. Berkemeier L.R., Winslow J.W., Kaplan D.R., Nikolics K., Goeddel D.V., and Rosenthal A. Neurotrophin-5: a novel neurotrophic factor that activates trk and trkB. Neuron 7 (1991) 857-866
6. Berthoud H.R., Blackshaw L.A., Brookes S.J., and Grundy D. Neuroanatomy of extrinsic afferents supplying the gastrointestinal tract. Neurogastroenterol. Motil. 16 (2004) 28-33
7. Bielefeldt K., Christianson J.A., and Davis B.M. Basic and clinical aspects of visceral sensation: transmission in the CNS. Neurogastroenterol. Motil. 17 (2005) 488-499
8. Bielefeldt K., Lamb K., and Gebhart G.F. Convergence of sensory pathways in the development of somatic and visceral hypersensitivity. Am. J. Physiol. Gastrointest. Liver Physiol. 291 (2006) G658-G665
9. Campenot R.B., and MacInnis B.L. Retrograde transport of neurotrophins: fact and function. J. Neurobiol. 58 (2004) 217-229
10. Chao M.V. Neurotrophin receptors: a window into neuronal differentiation. Neuron 9 (1992) 583-593
11. Chen M.W., Levin R.M., and Buttyan R. Peptide growth factors in normal and hypertrophied bladder. World J. Urol. 13 (1995) 344-348
12. Cho H.J., Kim J.K., Zhou X.F., and Rush R.A. Increased brain-derived neurotrophic factor immunoreactivity in rat dorsal root ganglia and spinal cord following peripheral inflammation. Brain Res. 764 (1997) 269-272
13. Cho H.J., Kim S.Y., Park M.J., Kim D.S., Kim J.K., and Chu M.Y. Expression of mRNA for brain-derived neurotrophic factor in the dorsal root ganglion following peripheral inflammation. Brain Res. 749 (1997) 358-362
14. Christensen M.D., and Hulsebosch C.E. Spinal cord injury and anti-NGF treatment results in changes in CGRP density and distribution in the dorsal horn in the rat. Exp. Neurol. 147 (1997) 463-475
15. Christianson J.A., Liang R., Davis B.M., Fraser M.O., and Pezzone M.A. Retrograde labeling of urinary bladder and distal colonic afferents: a potential role of dichotomizing afferents in the overlap of chronic pelvic pain disorders. Gastroenterology 126 (2004) A115
16. de Groat W.C., Booth A.M., and Yoshimura N. Neurophysiology of micturition and its modification in animal models of human disease. In: Maggi C.A. (Ed). The Autonomic Nervous System (1993), Harwood Academic Publishers, London 227-290
17. Delafoy L., Raymond F., Doherty A.M., Eschalier A., and Diop L. Role of nerve growth factor in the trinitrobenzene sulfonic acid-induced colonic hypersensitivity. Pain 105 (2003) 489-497
18. Delafoy L., Gelot A., Ardid D., Eschalier A., Bertrand C., Doherty A.M., and Diop L. Interactive involvement of BDNF, NGF and CGRP in colonic hypersensitivity in the rat. Gut 55 (2006) 940-945
19. di Mola F.F., Friess H., Zhu Z.W., Koliopanos A., Bley T., Di Sebastiano P., Innocenti P., Zimmermann A., and Buchler M.W. Nerve growth factor and Trk high affinity receptor (TrkA) gene expression in inflammatory bowel disease. Gut 46 (2000) 670-679
20. Donnerer J., Schuligoi R., and 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
21. Galeazza M.T., Garry M.G., Yost H.J., Strait K.A., Hargreaves K.M., and 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
22. Hanesch U., Pfrommer U., Grubb B.D., and 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. Ichikawa H., Yabuuchi T., Jin H.W., Terayama R., Yamaai T., Deguchi T., Kamioka H., Takano-Yamamoto T., and Sugimoto T. Brain-derived neurotrophic factor-immunoreactive primary sensory neurons in the rat trigeminal ganglion and trigeminal sensory nuclei. Brain Res. 1081 (2006) 113-118
24. Janig W., and Koltzenburg M. On the function of spinal primary afferent fibres supplying colon and urinary bladder. J. Auton. Nerv. Syst. 30 (1990) S89-S96
25. Kaplan D., and Miller F. Signal transduction by the neurotrophin receptors. Curr. Biol. 9 (1997) 213-221
26. Keast J.R., and 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
27. Kim D.S., Lee S.J., and Cho H.J. Differential usage of multiple brain-derived neurotrophic factor promoter in rat dorsal root ganglia following peripheral nerve injuries and inflammation. Brain Res. Mol. Brain Res. 92 (2001) 167-171
28. Krenz N.R., Meakin S.O., Krassioukov A.V., and Weaver L.C. Neutralizing intraspinal nerve growth factor blocks autonomic dysreflexia caused by spinal cord injury. J. Neurosci. 19 (1999) 7405-7414
29. Kruse M.N., and de Groat W.C. Changes in lower urinary tract function following spinal cord injury. J. Restor. Neurol. Neurosci. 5 (1993) 79-80
30. Lamb K., Zhong F., Gebhart G.F., and Bielefeldt K. Experimental colitis in mice and sensitization of converging visceral and somatic afferent pathways. Am. J. Physiol.: Gastrointest. Liver Physiol. 290 (2006) G451-G457
31. Lanigan T., and Russo A. Binding of upstream stimulatory factor and a cell-specific activator to the calcitonin/calcitonin gene-related peptide enhancer. J. Biol. Chem. 272 (1997) 18316-18324
32. Lee S.L., Kim J.K., Kim D.S., and Cho H.J. Expression of mRNAs encoding full-length and truncated TrkB receptors in rat dorsal root ganglia and spinal cord following peripheral inflammation. NeuroReport 10 (1999) 2847-2851
33. Lowe E.M., Anand P., Terenghi G., William-Chestnut R.E., and Sinicropi D.V. Increased nerve growth factor levels in the urinary bladder of women with idiopathic sensory urgency and interstitial cystitis. Br. J. Urol. 79 (1997) 572-577
34. Lu Y., and Westlund K.N. Effects of baclofen on colon inflammation-induced Fos, CGRP and SP expression in spinal cord and brainstem. Brain Res. 889 (2001) 118-130
35. Lu C.L., Pasricha P.J., Hsieh J.C., Lu R.H., Lai C.R., Wu L.L., Chang F.Y., and Lee S.D. Changes of the neuropeptides content and gene expression in spinal cord and dorsal root ganglion after noxious colorectal distension. Regul. Pept. 131 (2005) 66-73
36. Luo X.G., Rush R.A., and Zhou X.F. Ultrastructural localization of brain-derived neurotrophic factor in rat primary sensory neurons. Neurosci. Res. 39 (2001) 377-384
37. + currents in bladder sensory neurons. NeuroReport 15 (2004) 2601-2605
38. Mannion R.J., Costigan M., Decosterd I., Amaya F., Ma Q.P., Holstege J.C., Ji R.R., Acheson A., Lindsay R.M., Wilkinson G.A., and Woolf C.J. Neurotrophins: peripherally and centrally acting modulators of tactile stimulus-induced inflammatory pain hypersensitivity. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 9385-9390
39. Michael G.J., Averill S., Shortland P.J., Yan Q., and Priestley J.V. Axotomy results in major changes in BDNF expression by dorsal root ganglion cells: BDNF expression in large trkB and trkC cells, in pericellular baskets, and in projections to deep dorsal horn and dorsal column nuclei. Eur. J. Neurosci. 11 (1999) 3539-3551
40. Morris G.P., Beck P.L., Herridge M.S., Depew W.T., Szewczuk M.R., and Wallace J.L. Hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology 96 (1989) 795-803
41. Nahin R.L., and Byers M.R. Adjuvant-induced inflammation of rat paw is associated with altered calcitonin gene-related peptide immunoreactivity within cell bodies and peripheral endings of primary afferent neurons. J. Comp. Neurol. 349 (1994) 475-485
42. Natura G., von Banchet G.S., and Schaible H.G. Calcitonin gene-related peptide enhances TTX-resistant sodium currents in cultured dorsal root ganglion neurons from adult rats. Pain 116 (2005) 194-204
43. Oddiah D., Anand P., McMahon S.B., and Rattray M. Rapid increase of NGF, BDNF and NT-3 mRNAs in inflamed bladder. NeuroReport 9 (1998) 1455-1458
44. Okragly A.J., Niles A.L., Saban R., Schmidt D., Hoffman R.L., Warner T.F., Moon T.D., Uehling D.T., and Haak-Frendscho M. 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 (1999) 438-442
45. Pezzone M.A., Liang R., and Fraser M.O. A model of neural cross-talk and irritation in the pelvis: implications for the overlap of chronic pelvic pain disorders. Gastroenterology 128 (2005) 1953-1964
46. Plourde V., St-Pierre S., and Quirion R. Calcitonin gene-related peptide in viscerosensitive response to colorectal distension in rats. Am. J. Physiol. 273 (1997) G191-G196
47. Qiao L.Y., and Vizzard M.A. Cystitis-induced upregulation of tyrosine kinase (TrkA, TrkB) receptor expression and phosphorylation in rat micturition pathways. J. Comp. Neurol. 454 (2002) 200-211
48. Qiao L.Y., and Vizzard M.A. 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 (2002) 217-230
49. Qiao L.Y., and Vizzard M.A. Upregulation of phosphorylated CREB but not c-Jun in bladder afferent neurons in dorsal root ganglia after cystitis. J. Comp. Neurol. 469 (2004) 262-274
50. Qiao L.Y., Keummerle J.F., Gulick M.A., Bowers J., and Grider J.R. Differential changes in brain-derived neurotrophic factor (BDNF) mRNA and protein in lumbosacral DRG and spinal cord following trinitrobenzene sulfonic acid (TNBS) colitis. AGA/BSG Joint Symposium, Visceral Hypersensitivity, 7-8th September 2006, Cambridge (2006)
51. Qin C., and Foreman R.D. Viscerovisceral convergence of urinary bladder and colorectal inputs to lumbosacral spinal neurons in rats. NeuroReport 15 (2004) 467-471
52. Qin C., Talihina A.P., Akbarali H.I., and Foreman R.D. Cross-organ sensitization of lumbosacral spinal neurons receiving urinary bladder input in rats with inflamed colon. Gastroenterology 129 (2005) 1967-1978
53. Sevcik M.A., Ghilardi J.R., Peters C.M., Lindsay T.H., Halvorson K.G., Jonas B.M., Kubota K., Kuskowski M.A., Boustany L., Shelton D.L., and Mantyh P.W. Anti-NGF therapy profoundly reduces bone cancer pain and the accompanying increase in markers of peripheral and central sensitization. Pain 115 (2005) 128-141
54. Shadiack A.M., Sun Y., and Zigmond R.E. Nerve growth factor antiserum induces axotomy-like changes in neuropeptide expression in intact sympathetic and sensory neurons. J. Neurosci. 21 (2001) 363-371
55. Sharkey K.A., and Kroese A.B. Consequences of intestinal inflammation on the enteric nervous system: neuronal activation induced by inflammatory mediators. Anat. Rec. 262 (2001) 79-90
56. Smith G.D., Harmar A.J., McQueen D.S., and Seckl J.R. Increase in substance P and CGRP, but not somatostatin content of innervating dorsal root ganglia in adjuvant monoarthritis in the rat. Neurosci. Lett. 137 (1992) 257-260
57. Tonra J.R. Classical and novel directions in neurotrophin transport and research: anterograde transport of brain-derived neurotrophic factor by sensory neurons. Microsc. Res. Tech. 45 (1999) 225-232
58. Traub R.J., Hutchcroft K., and Gebhart G.F. The peptide content of colonic afferents decreases following colonic inflammation. Peptides 20 (1999) 267-273
59. Ustinova E.E., Fraser M.O., and Pezzone M.A. Colonic irritation in the rat sensitizes urinary bladder afferents to mechanical and chemical stimuli: an afferent origin of pelvic organ cross-sensitization. Am. J. Physiol.: Renal Physiol. 290 (2006) F1478-F1487
60. Ustinova E.E., Gutkin D.W., and Pezzone M.A. Sensitization of pelvic nerve afferents and mast cell infiltration in the urinary bladder following chronic colonic irritation is mediated by neuropeptides. Am. J. Physiol.: Renal Physiol. 292 (2007) F123-F130
61. Vizzard M.A. Alterations in neuropeptide expression in lumbosacral bladder pathways following chronic cystitis. J. Chem. Neuroanat. 21 (2001) 125-138
62. Winston J.H., Toma H., Shenoy M., He Z.J., Zou L., Xiao S.Y., Micci M.A., and Pasricha P.J. Acute pancreatitis results in referred mechanical hypersensitivity and neuropeptide up-regulation that can be suppressed by the protein kinase inhibitor k252a. J. Pain 4 (2003) 329-337
63. Yoshimura N., and de Groat W.C. Increased excitability of afferent neurons innervating rat urinary bladder after chronic bladder inflammation. J. Neurosci. 19 (1999) 4644-4653
64. Zhang L., Hoff A.O., Wimalawansa S.J., Cote G.J., Gagel R.F., and Westlund K.N. Arthritic calcitonin/alpha calcitonin gene-related peptide knockout mice have reduced nociceptive hypersensitivity. Pain 89 (2001) 265-273