Erratum: Overexpression of NGF in mouse urothelium leads to neuronal hyperinnervation, pelvic sensitivity, and changes in urinary bladder function (The American Journal of Physiology - Regulatory, Integrative and Comparative Physiology (2010) 298 (R534-R547) DOI: 10.1152/ajpregu.00367.2009);Overexpression of NGF in mouse urothelium leads to neuronal hyperinnervation, pelvic sensitivity, and changes in urinary bladder function

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 298, Issue 3, 2010, Pages

  Schnegelsberg, Birthe ^a   Sun, Tung Tien ^b   Cain, Gary ^a   Bhattacharya, Anindya ^a   Nunn, Philip A ^a   Ford, Anthony P D W ^a   Vizzard, Margaret A ^c   Cockayne, Debra A ^a  

^a ROCHE BIOSCIENCE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

Author keywords

Afferent innervation; Bladder hypersensitivity; Inflammation; Nerve growth factor; Transgenic mouse; Urothelium

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; MEMBRANE PROTEIN; MESSENGER RNA; NERVE GROWTH FACTOR; NEUROFILAMENT PROTEIN; PROTEIN UROPLAKIN II; SUBSTANCE P; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

AGE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLADDER; BLADDER CAPACITY; BLADDER CONTRACTION; BLADDER DISTENSION; BODY WEIGHT; C FIBER; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; CYSTOMETRY; DETRUSOR MUSCLE; EXPERIMENTAL MODEL; FEMALE; GENE OVEREXPRESSION; HYPERPLASIA; HYPERSENSITIVITY; LONG TERM EXPOSURE; LOWER URINARY TRACT SYMPTOM; MALE; MAST CELL; MOUSE; NERVE CELL; NERVE CELL STIMULATION; NERVE FIBER; NERVE PLEXUS; NONHUMAN; PATHOPHYSIOLOGY; PELVIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SENSORY EVALUATION; SENSORY NERVE; SUBMUCOSA; SUBUROTHELIAL NERVE PLEXUS; SYMPATHETIC NERVE; TISSUE LEVEL; TRANSGENIC MOUSE; UROTHELIUM;

EID: 77749315509     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.zh6-7196-corr.2010     Document Type: Erratum

References (112)

1. Alagiri M, Chottiner S, Ratner V, Slade D, Hanno PM. Interstitial cystitis: unexplained associations with other chronic disease and pain syndromes. Urology 49: 52-57, 1997.
2. Albers KM, Wright DE, Davis BM. Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J Neurosci 14: 1422-1432, 1994.
3. Allen SJ, Dawbarn D. Clinical relevance of the neurotrophins and their receptors. Clin Sci 110: 175-191, 2006.
4. Aloe L. The effect of nerve growth factor and its antibody on mast cells in vivo. J Neuroimmunol 18: 1-12, 1988.
5. Andreev NY, Dimitrieva N, Koltzenburg M, McMahon SB. Peripheral administration of nerve growth factor in the adult rat produces a thermal hyperalgesia that requires the presence of sympathetic postganglionic neurones. Pain 63: 109-115, 1995.
6. Applebaum AE, Vance WH, Coggeshall RE. Segmental localization of sensory cells that innervate the bladder. J Comp Neurol 192: 203-209, 1980.
7. Bielefeldt K, Lamb K, Gebhart GF. Convergence of sensory pathways in the development of somatic and visceral hypersensitivity. Am J Physiol Gastrointest Liver Physiol 291: G658-G665, 2006.
8. Birder LA, Wolf-Johnston A, Griffiths D, Resnick NM. Role of urothelial nerve growth factor in human bladder function. Neurourol Urodyn 26: 405-409, 2007.
9. Bjorling DE, Jacobsen HE, Blum JR, Shih A, Beckman M, Wang ZY, Uehling DT. Intravesical Escherichia coli lipopolysaccharide stimulates an increase in bladder nerve growth factor. BJU Int 87: 697-702, 2001.
10. Braas KM, May V, Zvara P, Nausch B, Kliment J, Dunleavy JD, Nelson MT, Vizzard MA. Role for pituitary adenylate cyclase activating polypeptide in cystitis-induced plasticity of micturition reflexes. Am J Physiol Regul Integr Comp Physiol 290: R951-R962, 2006.
11. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53: 55-63, 1994.
12. Cheng J, Huang H, Zhang ZT, Shapiro E, Pellicer A, Sun TT, Wu XR. Overexpression of epidermal growth factor receptor in urothelium elicits urothelial hyperplasia and promotes bladder tumor growth. Cancer Res 62: 4157-4163, 2002.
13. Cheppudira BP, Girard BM, Malley SE, Schutz KC, May V, Vizzard MA. Upregulation of vascular endothelial growth factor isoform VEGF-164 and receptors (VEGFR-2, Npn-1, and Npn-2) in rats with cyclophosphamide-induced cystitis. Am J Physiol Renal Physiol 295: F826-F836, 2008.
14. Christmas TJ, Rode J, Chapple CR, Milroy EJ, and Turner-Warwick RT. Nerve fibre proliferation in interstitial cystitis. Virchows Arch A Pathol Anat Histopathol 416: 447-451, 1990.
15. Chuang YC, Fraser MO, Yu Y, Chancellor MB, De Groat WC, Yoshimura N. The role of bladder afferent pathways in bladder hyperactivity induced by the intravesical administration of nerve growth factor. J Urol 165: 975-979, 2001.
16. Clemow DB, Steers WD, McCarty R, Tuttle JB. Altered regulation of bladder nerve growth factor and neurally mediated hyperactive voiding. Am J Physiol Regul Integr Comp Physiol 275: R1279-R1286, 1998.
17. Cockayne DA, Bodine DM, Cline A, Nienhuis AW, Dunbar CE. Transgenic mice expressing antisense interleukin-3 RNA develop a B-cell lymphoproliferative syndrome or neurologic dysfunction. Blood 84: 2699-2710, 1994.
18. Dang K, Bielefeldt K, Gebhart GF. Differential responses of bladder lumbosacral and thoracolumbar dorsal root ganglion neurons to purinergic agonists, protons, and capsaicin. J Neurosci 25: 3973-3984, 2005.
19. Dang K, Lamb K, Cohen M, Bielefeldt K, Gebhart GF. Cyclophosphamide-induced bladder inflammation sensitizes and enhances P2X receptor function in rat bladder sensory neurons. J Neurophysiol 99: 49-59, 2008.
20. Davis BM, Albers KM, Seroogy KB, Katz DM. Overexpression of nerve growth factor in transgenic mice induces novel sympathetic projections to primary sensory neurons. J Comp Neurol 349: 464-474, 1994.
21. Delafoy L, Gelot A, Ardid D, Eschalier A, Bertrand C, Doherty AM, Diop L. Interactive involvement of brain derived neurotrophic factor, nerve growth factor, and calcitonin gene related peptide in colonic hypersensitivity in the rat. Gut 55: 940-945, 2006.
22. Dmitrieva N, McMahon SB. Sensitisation of visceral afferents by nerve growth factor in the adult rat. Pain 66: 87-97, 1996.
23. Dmitrieva N, Shelton D, Rice AS, McMahon SB. The role of nerve growth factor in a model of visceral inflammation. Neuroscience 78: 449-459, 1997.
24. Dorr W. Cystometry in mice-influence of bladder filling rate and circadian variations in bladder compliance. J Urol 148: 183-187, 1992.
25. Driscoll A, Teichman JM. How do patients with interstitial cystitis present? J Urol 166: 2118-2120, 2001.
26. Dupont MC, Spitsbergen JM, Kim KB, Tuttle JB, Steers WD. Histological and neurotrophic changes triggered by varying models of bladder inflammation. J Urol 166: 1111-1118, 2001.
27. Edwards RH, Rutter WJ, Hanahan D. Directed expression of NGF to pancreatic beta cells in transgenic mice leads to selective hyperinnervation of the islets. Cell 58: 161-170, 1989.
28. Elliott J, MacLellan A, Saini JK, Chan J, Scott S, Kawaja MD. Transgenic mice expressing nerve growth factor in smooth muscle cells. Neuroreport 20: 223-227, 2009.
29. Fitzgerald MP, Koch D, Senka J. Visceral and cutaneous sensory testing in patients with painful bladder syndrome. Neurourol Urodyn 24: 627-632, 2005.
30. Ford AP, Gever JR, Nunn PA, Zhong Y, Cefalu JS, Dillon MP, Cockayne DA. Purinoceptors as therapeutic targets for lower urinary tract dysfunction. Br J Pharmacol 147 Suppl 2: S132-S143, 2006.
31. Freund-Michel V, Frossard N. The nerve growth factor and its receptors in airway inflammatory diseases. Pharmacol Ther 117: 52-76, 2008.
32. Frossard N, Freund V, Advenier C. Nerve growth factor and its receptors in asthma and inflammation. Eur J Pharmacol 500: 453-465, 2004.
33. Gabella G, Davis C. Distribution of afferent axons in the bladder of rats. J Neurocytol 27: 141-155, 1998.
34. Guerios SD, Wang ZY, Bjorling DE. Nerve growth factor mediates peripheral mechanical hypersensitivity that accompanies experimental cystitis in mice. Neurosci Lett 392: 193-197, 2006.
35. Guerios SD, Wang ZY, Boldon K, Bushman W, Bjorling DE. Blockade of NGF and trk receptors inhibits increased peripheral mechanical sensitivity accompanying cystitis in rats. Am J Physiol Regul Integr Comp Physiol 295: R111-R122, 2008.
36. Guidry G, Landis SC, Davis BM, Albers KM. Overexpression of nerve growth factor in epidermis disrupts the distribution and properties of sympathetic innervation in footpads. J Comp Neurol 393: 231-243, 1998.
37. Hassankhani A, Steinhelper ME, Soonpaa MH, Katz EB, Taylor DA, Andrade-Rozental A, Factor SM, Steinberg JJ, Field LJ, Federoff HJ. Overexpression of NGF within the heart of transgenic mice causes hyperinnervation, cardiac enlargement, and hyperplasia of ectopic cells. Dev Biol 169: 309-321, 1995.
38. Hohenfellner M, Nunes L, Schmidt RA, Lampel A, Thuroff JW, Tanagho EA. Interstitial cystitis: increased sympathetic innervation and related neuropeptide synthesis. J Urol 147: 587-591, 1992.
39. Hoyle GW, Graham RM, Finkelstein JB, Nguyen KP, Gozal D, Friedman M. Hyperinnervation of the airways in transgenic mice overexpressing nerve growth factor. Am J Respir Cell Mol Biol 18: 149-157, 1998.
40. Hu VY, Zvara P, Dattilio A, Redman TL, Allen SJ, Dawbarn D, Stroemer RP, Vizzard MA. Decrease in bladder overactivity with REN1820 in rats with cyclophosphamide induced cystitis. J Urol 173: 1016-1021, 2005.
41. Huang EJ, Reichardt LF. Neutrophins: Roles in neuronal development and function. Ann Rev Neurosci 24: 677-736, 2001.
42. Jaggar SI, Scott HCF, Rice AS. 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, 1999.
43. Janig W, Levine JD, Michaelis M. Interactions of sympathetic and primary afferent neurons following nerve injury and tissue trauma. Prog Brain Res 113: 161-184, 1996.
44. Jiang S, Gitlin J, Deng FM, Liang FX, Lee A, Atala A, Bauer SB, Ehrlich GD, Feather SA, Goldberg JD, Goodship JA, Goodship TH, Hermanns M, Hu FZ, Jones KE, Malcolm S, Mendelsohn C, Preston RA, Retik AB, Schneck FX, Wright V, Ye XY, Woolf AS, Wu XR, Ostrer H, Shapiro E, Yu J, Sun TT. Lack of major involvement of human uroplakin genes in vesicoureteral reflux: implications for disease heterogeneity. Kidney Int 66: 10-19, 2004.
45. Kawaja MD, Crutcher KA. Sympathetic axons invade the brains of mice overexpressing nerve growth factor. J Comp Neurol 383: 60-72, 1997.
46. Kawaja MD, Walsh GS, Petruccelli K, Coome GEA. Sensory nociceptive axons invade the cerebellum of transgenic mice overexpressing nerve growth factor. Brain Res 774: 77-86, 1997.
47. Kerr DE, Liang F, Bondioli KR, Zhao H, Kreibich G, Wall RJ, Sun TT. The bladder as a bioreactor: urothelium production and secretion of growth hormone into urine. Nat Biotechnol 16: 75-79. 1998.
48. Kim JC, Kim DB, Seo SI, Park YH, Hwang TK. Nerve growth factor and vanilloid receptor expression, and detrusor instability, after relieving bladder outlet obstruction in rats. BJU Int 94: 915-918, 2004.
49. Kim JC, Park EY, Hong SH, Seo SI, Park YH, Hwang TK. Changes of urinary nerve growth factor and prostaglandins in male patients with overactive bladder symptom. Int J Urol 12: 875-880, 2005.
50. Kim JC, Park EY, Seo SI, Park YH, Hwang TK. Nerve growth factor and prostaglandins in the urine of female patients with overactive bladder. J Urol 175: 1773-1776, 2006.
51. Klinger MB, Girard B, Vizzard MA. p75NTR expression in rat urinary bladder sensory neurons and spinal cord with cyclophosphamide-induced cystitis. J Comp Neurol 507: 1379-1392, 2008.
52. Klinger MB, Vizzard MA. Role of p75NTR in female rat urinary bladder with cyclophosphamide-induced cystitis. Am J Physiol Renal Physiol 295: F1778-F1789, 2008.
53. Laird JMA, Martinez-Caro L, Garcia-Nicas E, Cervero F. A new model of visceral pain and referred hyperalgesia in the mouse. Pain 92: 335-342, 2001.
54. Laird JMA, Souslova V, Wood JN, Cervero F. Deficits in visceral pain and referred hyperalgesia in Nav1.8 (SNS/PN3)- null mice. J Neurosci 22: 8352-8356, 2002.
55. Lamb K, Gebhart GF, Bielefeldt K. Increased nerve growth factor expression triggers bladder overactivity. J Pain 5: 150-156, 2004.
56. Levi-Montalcini R, Skaper SD, Dal Toso R, Petrelli L, Leon A. Nerve growth factor: from neurotrophin to neurokine. Trends Neurosci 19: 514-520, 1996.
57. Liang FX, Bosland MC, Huang H, Romih R, Baptiste S, Deng FM, Wu XR, Shapiro E, Sun TT. Cellular basis of urothelial squamous metaplasia: roles of lineage heterogeneity and cell replacement. J Cell Biol 171: 835-844, 2005.
58. Lin JH, Zhao H, Sun TT. A tissue-specific promoter that can drive a foreign gene to express in the suprabasal urothelial cells of transgenic mice. Proc Nat Acad Sci USA 92: 679-683, 1995.
59. Liu HT, Chancellor MB, Kuo HC. Urinary nerve growth factor level could be a biomarker in the differential diagnosis of mixed urinary incontinence in women. BJU Int 102: 1440-1444, 2008.
60. Liu HT, Chancellor MB, Kuo HC. Urinary nerve growth factor levels are elevated in patients with detrusor overactivity and decreased in responders to detrusor botulinum toxin-A injection. Eur Urol 56: 700-707, 2009.
61. Liu HT, Kuo HC. Intravesical botulinum toxin A injections plus hydrodistension can reduce nerve growth factor production and control bladder pain in interstitial cystitis. Urology 70: 463-468, 2007.
62. Liu HT, Kuo HC. Urinary nerve growth factor level could be a potential biomarker for diagnosis of overactive bladder. J Urol 179: 2270-2274, 2008.
63. Liu HT, Kuo HC. Urinary nerve growth factor levels are increased in patients with bladder outlet obstruction with overactive bladder symptoms and reduced after successful medical treatment. Urology 72: 104-108, 2008.
64. Liu HT, Kuo HC. Urinary nerve growth factor levels are elevated in patients with overactive bladder and do not significantly increase with bladder distention. Neurourol Urodyn 28: 78-81, 2009.
65. Lowe EM, Anand P, Terenghi G, Williams-Chestnut RE, Sinicropi DV, Osborne JL. Increased nerve growth factor levels in the urinary bladder of women with idiopathic sensory urgency and interstitial cystitis. Br J Urol 79: 572-577, 1997.
66. Lundeberg T, Liedberg H, Nordling L, Theodorsson E, Owzarski A, Ekman P. Interstitial cystitis: correlation with nerve fibres, mast cells and histamine. Br J Urol 71: 427-429, 1993.
67. Lynes WL, Flynn SD, Shortliffe LD, Lemmers M, Zipser R, Roberts LJ, Stamey TA. Mast cell involvement in interstitial cystitis. J Urol 138: 746-752, 1987.
68. Maggi CA, Santicioli P, Meli A. The nonstop transvesical cystometrogram in urethane-anesthetized rats: a simple procedure for quantitative studies on the various phases of urinary bladder voiding cycle. J Pharmacol Methods 15: 157-167, 1986.
69. Martin RS, Luong LA, Welsh NJ, Eglen RM, Martin GR, MacLennan SJ. Effects of cannabinoid receptor agonists on neuronally-evoked contractions of urinary bladder tissues isolated from rat, mouse, pig, dog, monkey and human. Br J Pharmacol 129: 1707-1715, 2000.
70. McMahon SB, Dmitrieva N, Koltzenburg M. Visceral pain. Br J Anaesth 75: 132-144, 1995.
71. Meen M, Coudore-Civiale MA, Eschalier A, Boucher M. Involvement of hypogastric and pelvic nerves for conveying cystitis induced nociception in conscious rats. J Urol 166: 318-322, 2001.
72. Mitsui T, Kakizaki H, Matsuura S, Ameda K, Yoshioka M, Koyanagi T. Afferent fibers of the hypogastric nerves are involved in the facilitating effects of chemical bladder irritation in rats. J Neurophysiol 86: 2276-2284, 2001.
73. Mo L, Cheng J, Lee EYH, Sun TT, Wu XR. Gene deletion in urothelium by specific expression of Cre recombinase. Am J Physiol Renal Physiol 289: F562-F568, 2005.
74. Moss NG, Harrington WW, Tucker MS. Pressure, volume, and chemosensitivity in afferent innervation of urinary bladder in rats. Am J Physiol Regul Integr Comp Physiol 272: R695-R703, 1997.
75. Murray E, Malley SE, Qiao LY, Hu VY, Vizzard MA. Cyclophosphamide induced cystitis alters neurotrophin and receptor tyrosine kinase expression in pelvic ganglia and bladder. J Urol 172: 2434-2439, 2004.
76. Ness TJ. Pelvic pain in women and men: recent findings. Curr Opin Anaesthesiol 18: 555-562, 2005.
77. Ness TJ, Powell-Boone T, Cannon R, Lloyd LK, Fillingim RB. Psychophysical evidence of hypersensitivity in subjects with interstitial cystitis. J Urol 173: 1983-1987, 2005.
78. Oddiah D, Anand P, McMahon SB, Rattray M. Rapid increase of NGF, BDNF, and NT-3 mRNAs in inflamed bladder. Neuroreport 9: 1455-1458, 1998.
79. Okragly AJ, Niles AL, Saban R, Schmidt D, Hoffman RL, Warner TF, Moon TD, Uehling DT, Haak-Frendscho M. Elevated tryptase, nerve growth factor, neurotrophin-3 and glial cell line-derived neurotro phic factor levels in the urine of interstitial cystitis and bladder cancer patients. J Urol 161: 438-441, 1999.
80. Pang X, Boucher W, Triadafilopoulos G, Sant GR, Theoharides TC. Mast cell and substance P-positive nerve involvement in a patient with both irritable bowel syndrome and interstitial cystitis. Urology 47: 436-438, 1996.
81. Pang X, Marchand J, Sant GR, Kream RM, Theoharides TC. Increased number of substance P-positive nerve fibres in interstitial cystitis. Br J Urol 75: 744-750, 1995.
82. Peeker R, Aldenborg F, Dahlstrom A, Johansson SL, Li JY, Fall M. Increased tyrosine hydroxylase immunoreactivity in bladder tissue from patients with classic and nonulcer interstitial cystitis. J Urol 163: 1112-1115, 2000.
83. Peeker R, Enerback L, Fall M, Aldenborg F. Recruitment, distribution and phenotypes of mast cells in interstitial cystitis. J Urol 163: 1009-1015, 2000.
84. Pezet S, McMahon SB. Neurotrophins: Mediators and modulators of pain. Ann Rev Neurosci 29: 507-538, 2006.
85. Pezet S, Onteniente B, Jullien J, Junier MP, Grannec G, Rudkin BB, Calvino B. Differential regulation of NGF receptors in primary sensory neurons by adjuvant-induced arthritis in the rat. Pain 90: 113-125, 2001.
86. Ramer MS, Bisby MA. Adrenergic innervation of rat sensory ganglia following proximal or distal painful sciatic neuropathy: distinct mechanisms revealed by anti-NGF treatment. Eur J Neurosci 11: 837-846, 1999.
87. Ramer MS, Kawaja MD, Henderson JT, Roder JC, Bisby MA. Glial overexpression of NGF enhances neuropathic pain and adrenergic sprouting into DRG following chronic sciatic constriction in mice. Neurosci Lett 251: 53-56, 1998.
88. Ramer MS, Thompson SW, McMahon SB. Causes and consequences of sympathetic basket formation in dorsal root ganglia. Pain Suppl 6: S111-S120, 1999.
89. Robinson DR, Gebhart GF. Inside information: The unique features of visceral sensation. Mol Interv 8: 242-253, 2008.
90. Rudick CN, Chen MC, Mongiu AK, Klumpp DJ. Organ cross talk modulates pelvic pain. Am J Physiol Regul Integr Comp Physiol 293: R1191-R1198, 2007.
91. Sant GR, Hanno PM. Interstitial cystitis: current issues and controversies in diagnosis. Urology 57: 82-88, 2001.
92. Sant GR, Kempuraj D, Marchand JE, Theoharides TC. The mast cell in interstitial cystitis: role in pathophysiology and pathogenesis. Urology 69: S34-S40, 2007.
93. Stanzel RDP, Lourenssen S, Blennerhassett MG. Inflammation causes expression of NGF in epithelial cells of the rat colon. Exp Neurol 211: 203-213, 2008.
94. Steers WD, Ciambotti J, Etzel B, Erdman S, De Groat WC. Alterations in afferent pathways from the urinary bladder of the rat in response to partial urethral obstruction. J Comp Neurol 310: 401-410, 1991.
95. Steers WD, Kolbeck S, Creedon D, Tuttle JB. Nerve growth factor in the urinary bladder of the adult regulates neuronal form and function. J Clin Invest 88: 1709-1715, 1991.
96. Streng T, Hedlund P, Talo A, Andersson KE, Gillespie JI. Phasic non-micturition contractions in the bladder of the anaesthetized and awake rat. BJU Int 97: 1094-1101, 2006.
97. Szallasi A, Cortright DN, Blum CA, Eid SR. The vanilloid receptor TRPV1: 10 years from channel cloning to antagonist proof-of-concept. Nat Rev Drug Discov 6: 357-372, 2007.
98. Uemura E, Fletcher TF, Bradley WE. Distribution of lumbar and sacral afferent axons in submucosa of cat urinary bladder. Anat Rec 183: 579-587, 1975.
99. van Rossum J. Cumulative dose-response curves. II Technique for the making of dose-response curves in isolated organs and the evaluation of drug parameters. Arch Int Pharmacodyn Ther 143: 299-330, 1963.
100. Vizzard MA. Changes in urinary bladder neurotrophic factor mRNA and NGF protein following urinary bladder dysfunction. Exp Neurol 161: 273-284, 2000.
101. Vizzard MA. Increased expression of spinal cord Fos protein induced by bladder stimulation after spinal cord injury. Am J Physiol Regul Integr Comp Physiol 279: R295-R305, 2000.
102. Vizzard MA. Alterations in neuropeptide expression in lumbosacral bladder pathways following chronic cystitis. J Chem Neuroanat 21: 125-138, 2001.
103. Vizzard MA, Boyle MM. Increased expression of growth-associated protein (GAP-43) in lower urinary tract pathways following cyclophosphamide (CYP)-induced cystitis. Brain Res 844: 174-187, 1999.
104. Walsh GS, Kawaja MD. Sympathetic axons surround nerve growth factor-immunoreactive trigeminal neurons: observations in mice overexpressing nerve growth factor. J Neurobiol 34: 347-360, 1998.
105. Wu XR, Kong XP, Pellicer A, Kreibich G, Sun TT. Uroplakins in urothelial biology, function, and disease. Kidney Int 75: 1153-1165, 2009.
106. Yokoyama T, Kumon H, Nagai A. Correlation of urinary nerve growth factor level with pathogenesis of overactive bladder. Neurourol Urodyn 27: 417-420, 2008.
107. Yoshimura N, Bennett NE, Hayashi Y, Ogawa T, Nishizawa O, Chancellor MB, De Groat WC, Seki S. Bladder overactivity and hyperexcitability of bladder afferent neurons after intrathecal delivery of nerve growth factor in rats. J Neurosci 26: 10847-10855, 2006.
108. Yoshimura N, De Groat WC. Increased excitability of afferent neurons innervating rat urinary bladder after chronic bladder inflammation. J Neurosci 19: 4644-4653, 1999.
109. Yoshimura N, Seki S, Chancellor MB, De Groat WC, Ueda T. Targeting afferent hyperexcitability for therapy of the painful bladder syndrome. Urology 59: 61-67, 2002.
110. Zvara P, Kliment J, Jr, DeRoss AL, Irwin BH, Malley SE, Plante MK and Vizzard MA. Differential expression of bladder neurotrophic factor mRNA in male and female rats after bladder outflow obstruction. J Urol 168: 2682-2688, 2002.
111. Zvara P, Vizzard MA. Exogenous overexpression of nerve growth factor in the urinary bladder produces bladder overactivity and altered micturition circuitry in the lumbosacral spinal cord. BMC Physiol 7: 9, 2007.
112. Zvarova K, Vizzard MA. Changes in galanin immunoreactivity in rat micturition reflex pathways after cyclophosphamide-induced cystitis. Cell Tissue Res 324: 213-224, 2006.