Journal of Molecular Neuroscience

, Volume 36, Issue 1–3, pp 175–187

Urinary Bladder Function and Somatic Sensitivity in Vasoactive Intestinal Polypeptide (VIP)−/− Mice

  • Simon Studeny
  • Bopaiah P. Cheppudira
  • Susan Meyers
  • Elena M. Balestreire
  • Gerard Apodaca
  • Lori A. Birder
  • Karen M. Braas
  • James A. Waschek
  • Victor May
  • Margaret A. Vizzard
Article

Abstract

Vasoactive intestinal polypeptide (VIP) is an immunomodulatory neuropeptide widely distributed in neural pathways that regulate micturition. VIP is also an endogenous anti-inflammatory agent that has been suggested for the development of therapies for inflammatory disorders. In the present study, we examined urinary bladder function and hindpaw and pelvic sensitivity in VIP−/− and littermate wildtype (WT) controls. We demonstrated increased bladder mass and fewer but larger urine spots on filter paper in VIP−/− mice. Using cystometry in conscious, unrestrained mice, VIP−/− mice exhibited increased void volumes and shorter intercontraction intervals with continuous intravesical infusion of saline. No differences in transepithelial resistance or water permeability were demonstrated between VIP−/− and WT mice; however, an increase in urea permeability was demonstrated in VIP−/− mice. With the induction of bladder inflammation by acute administration of cyclophosphamide, an exaggerated or prolonged bladder hyperreflexia and hindpaw and pelvic sensitivity were demonstrated in VIP−/− mice. The changes in bladder hyperreflexia and somatic sensitivity in VIP−/− mice may reflect increased expression of neurotrophins and/or proinflammatory cytokines in the urinary bladder. Thus, these changes may further regulate the neural control of micturition.

Keywords

Neurotrophins Cytokines Cystometry Pelvic pain Bladder permeability 

References

  1. Abad, C., Martinez, C., Juarranz, M. G., et al. (2003). Therapeutic effects of vasoactive intestinal peptide in the trinitrobenzene sulfonic acid mice model of Crohn’s disease. Gastroenterology, 124, 961–971.PubMedCrossRefGoogle Scholar
  2. Abbadie, C. (2005). Chemokines, chemokine receptors and pain. Trends in Immunology, 26, 529–534.PubMedCrossRefGoogle Scholar
  3. Anderson, L. C., & Rao, R. D. (2001). Interleukin-6 and nerve growth factor levels in peripheral nerve and braistem after trigeminal nerve injury in the rat. Archives of Oral Biology, 46, 633–640.PubMedCrossRefGoogle Scholar
  4. Bielefeldt, K., Lamb, K., & Gebhart, G. F. (2006). Convergence of sensory pathways in the development of somatic and visceral hypersensitivity. American Journal of Physiology. Gastrointestinal and Liver Physiology, 291, G658–G665.PubMedCrossRefGoogle Scholar
  5. Bik, W., Wolinska-Witort, E., Chmielowska, M., Baranowska-Bik, A., Rusiecka-Kuczalek, E., & Baranowska, B. (2004). Vasoactive intestinal peptide can modulate immune and endocrine responses during lipopolysaccharide-induced acute inflammation. Neuroimmunomodulation, 11, 358–364.PubMedCrossRefGoogle Scholar
  6. Birder, L. A., Nakamura, Y., Kiss, S., et al. (2002). Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nature Neuroscience, 5, 856–860.PubMedCrossRefGoogle Scholar
  7. Birder, L. A., Wolf-Johnston, A., Griffiths, D., & Resnick, N. M. (2007). Role of urothelial nerve growth factor in human bladder function. Neurourology and Urodynamics, 26(3), 405–409.PubMedCrossRefGoogle Scholar
  8. Braas, K. M., May, V., Zvara, P., et al. (2006). Role for pituitary adenylate cyclase activating polypeptide in cystitis-induced plasticity of micturition reflexes. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 290, R951–962.PubMedGoogle Scholar
  9. Chaplan, S. R., Bach, F. W., Pogrel, J. W., Chung, J. M., & Yaksh, T. L. (1994). Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods, 53, 55–63.Google Scholar
  10. Chapple, C. R., Milner, P., Moss, H. E., & Burnstock, G. (1992). Loss of sensory neuropeptides in the obstructed human bladder. British Journal of Urology, 70, 373–381.PubMedCrossRefGoogle Scholar
  11. Chorny, A., Gonzalez-Rey, E., Varela, N., Robledo, G., & Delgado, M. (2006). Signaling mechanisms of vasoactive intestinal peptide in inflammatory conditions. Regulatory Peptides, 137, 67–74.PubMedCrossRefGoogle Scholar
  12. Clausen, C., Lewis, S. A., & Diamond, J. M. (1979). Impedance analysis of a tight epithelium using a distributed resistance model. Biophysical Journal, 26, 291–317.PubMedGoogle Scholar
  13. Colwell, C. S., Michel, S., Itri, J., et al. (2003). Disrupted circadian rhythms in VIP- and PHI-deficient mice. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 285, R939–949.PubMedGoogle Scholar
  14. Cominelli, F., & Pizarro, T. T. (1996). Interleukin-1 and interleukin-1 receptor antagonist in inflammatory bowel disease. Alimentary Pharmacology & Therapeutics, 10, 49–53.Google Scholar
  15. Delgado, M., Gomariz, R. P., Martinez, C., Abad, C., & Leceta, J. (2000). Anti-inflammatory properties of the type 1 and type 2 vasoactive intestinal peptide receptors: role in lethal endotoxic shock. European Journal of Immunology, 30, 3236–3246.PubMedCrossRefGoogle Scholar
  16. Delgado, M., Munoz-Elias, E. J., Gomariz, R. P., & Ganea, D. (1999). Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide enhance IL-10 production by murine macrophages: in vitro and in vivo studies. Journal of Immunology, 162, 1707–1716.Google Scholar
  17. Derand, R., Montoni, A., Bulteau-Pignoux, L., et al. (2004). Activation of VPAC1 receptors by VIP and PACAP-27 in human bronchial epithelial cells induces CFTR-dependent chloride secretion. British Journal of Pharmacology, 141, 698–708.PubMedCrossRefGoogle Scholar
  18. Dickinson, T., Mitchell, R., Robberecht, P., & Fleetwood-Walker, S. M. (1999). The role of VIP/PACAP receptor subtypes in spinal somatosensory processing in rats with an experimental peripheral mononeuropathy. Neuropharmacology, 38, 167–180.PubMedCrossRefGoogle Scholar
  19. Dmitrieva, N., Shelton, D., Rice, A. S., & McMahon, S. B. (1997). The role of nerve growth factor in a model of visceral inflammation. Neuroscience, 78, 449–459.PubMedCrossRefGoogle Scholar
  20. Dorr, W. (1992). Cystometry in mice—influence of bladder filling rate and circadian variations in bladder compliance. Journal of Urology, 148, 183–187.PubMedGoogle Scholar
  21. Dray, A. (1995). Inflammatory mediators of pain. British Journal of Anaesthesia, 75, 125–131.PubMedGoogle Scholar
  22. Driscoll, A., & Teichman, J. M. (2001). How do patients with interstitial cystitis present? Journal of Urology, 166, 2118–2120.PubMedCrossRefGoogle Scholar
  23. Erol, K., Ulak, G., Donmez, T., Cingi, M. I., Alpan, R. S., & Ozdemir, M. (1992). Effects of vasoactive intestinal polypeptide on isolated rat urinary bladder smooth muscle. Urol. Int, 49, 151–153.PubMedCrossRefGoogle Scholar
  24. Girard, B., Malley, S., Braas, K. M., Waschek, J., May, V., Vizzard, M. A. (2008). Exaggerated expression of inflammatory mediators in vasoactive intestinal polypeptde knockout (VIP-/-) mice with cyclophosphamide (CYP)-induced cystitis. Submitted.Google Scholar
  25. Girard, B. A., Lelievre, V., Braas, K. M., et al. (2006). Noncompensation in peptide/receptor gene expression and distinct behavioral phenotypes in VIP- and PACAP-deficient mice. Journal of Neurochemistry, 99, 499–513.PubMedCrossRefGoogle Scholar
  26. Gonzalez-Rey, E., & Delgado, M. (2006). Therapeutic treatment of experimental colitis with regulatory dendritic cells generated with vasoactive intestinal peptide. Gastroenterology, 131, 1799–1811.PubMedCrossRefGoogle Scholar
  27. Guerios, S. D., Wang, Z. Y., & Bjorling, D. E. (2006). Nerve growth factor mediates peripheral mechanical hypersensitivity that accompanies experimental cystitis in mice. Neuroscience Letters, 392, 193–197.PubMedCrossRefGoogle Scholar
  28. Harmar, A. J., Arimura, A., Gozes, I., et al. (1998). International Union of Pharmacology. XVIII. Nomenclature of receptors for vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. Pharmacological Reviews, 50, 265–270.PubMedGoogle Scholar
  29. Hernandez, M., Barahona, M. V., Recio, P., et al. (2006). Neuronal and smooth muscle receptors involved in the PACAP- and VIP-induced relaxations of the pig urinary bladder neck. British Journal of Pharmacology, 149, 100–109.PubMedCrossRefGoogle Scholar
  30. Herrera, G. M., Pozo, M. J., Zvara, P., et al. (2003). Urinary bladder instability induced by selective suppression of the murine small conductance calcium-activated potassium (SK3) channel. Journal of Physiology, 551, 893–903.PubMedCrossRefGoogle Scholar
  31. Hill, J. K., Gunion-Riner, L., Kulhanek, D., et al. (1999). Temporal modulation of cytokine expression following focal cerebral ischemia in mice. Brain Research, 820, 45–54.PubMedCrossRefGoogle Scholar
  32. Hu, V. Y., Malley, S., Dattilio, A., Folsom, J. B., Zvara, P., & Vizzard, M. A. (2003). COX-2 and prostanoid expression in micturition pathways after cyclophosphamide-induced cystitis in the rat. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 284, R574–R585.PubMedGoogle Scholar
  33. Hu, V. Y., Zvara, P., Dattilio, A., et al. (2005). Decrease in bladder overactivity with REN1820 in rats with cyclophosphamide induced cystitis. Journal of Urology, 173, 1016–1021.PubMedCrossRefGoogle Scholar
  34. Igawa, Y., Persson, K., Andersson, K. E., Uvelius, B., & Mattiasson, A. (1993). Facilitatory effect of vasoactive intestinal polypeptide on spinal and peripheral micturition reflex pathways in conscious rats with and without detrusor instability. Journal of Urology, 149, 884–889.PubMedGoogle Scholar
  35. Jennings, L. J., & Vizzard, M. A. (1999). Cyclophosphamide-induced inflammation of the urinary bladder alters electrical properties of small diameter afferent neurons from dorsal root ganglia. FASEB Journal, 13, A57.Google Scholar
  36. Jensen, D. G., Studeny, S., May, V., Waschek, J., Vizzard, M. A. (2008). Expression of Phosphorylated cAMP Response Element Binding Protein (p-CREB) in Bladder Afferent Pathways in VIP(-/-) Mice with Cyclophosphamide (CYP)-Induced Cystitis. Journal of Molecular Neuroscience.Google Scholar
  37. Juarranz, Y., Abad, C., Martinez, C., et al. (2005). Protective effect of vasoactive intestinal peptide on bone destruction in the collagen-induced arthritis model of rheumatoid arthritis. Arthritis Research and Therapy, 7, R1034–1045.PubMedCrossRefGoogle Scholar
  38. Kanai, A. J., Zeidel, M. L., Lavelle, J. P., et al. (2002). Manganese superoxide dismutase gene therapy protects against irradiation-induced cystitis. Am J Physiol Renal Physiol, 283, F1304–1312.PubMedGoogle Scholar
  39. Keast, J. R., & de Groat, W. C. (1989). Immunohistochemical characterization of pelvic neurons which project to the bladder, colon or penis in rats. Journal of Comparative Neurology, 288, 387–400.PubMedCrossRefGoogle Scholar
  40. Keast, J. R., & de Groat, W. C. (1992). Segmental distribution and peptide content of primary afferent neurons innervating the urogenital organs and colon of male rats. Journal of Comparative Neurology, 319, 615–623.PubMedCrossRefGoogle Scholar
  41. LaBerge, J., Malley, S. E., Zvarova, K., & Vizzard, M. A. (2006). Expression of corticotropin-releasing factor and CRF receptors in micturition pathways after cyclophosphamide-induced cystitis. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 291, R692–703.PubMedGoogle Scholar
  42. Lagou, M., Gillespie, J. I., Andersson, K. E., Kirkwood, T., & Drake, M. J. (2006). Bladder volume alters cholinergic responses of the isolated whole mouse bladder. Journal of Urology, 175, 771–776.PubMedCrossRefGoogle Scholar
  43. Laird, J. M., Souslova, V., Wood, J. N., & Cervero, F. (2002). Deficits in visceral pain and referred hyperalgesia in Nav1.8 (SNS/PN3)-null mice. Journal of Neuroscience, 22, 8352–8356.PubMedGoogle Scholar
  44. Laird, J. M. A., MartinezCaro, L., GarciaNicas, E., & Cervero, F. (2001). A new model of visceral pain and referred hyperalgesia in the mouse. Pain, 92, 335–342.PubMedCrossRefGoogle Scholar
  45. Laird, J. M. A., Olivar, T., Roza, C., DeFelipe, C., Hunt, S. P., & Cervero, F. (2000). Deficits in visceral pain and hyperalgesia of mice with a disruption of the tachykinin NK1 receptor gene. Neuroscience, 98, 345–352.PubMedCrossRefGoogle Scholar
  46. Lamb, K., Gebhart, G. F., & Bielefeldt, K. (2004). Increased nerve growth factor expression triggers bladder overactivity. Journal of Pain, 5, 150–156.PubMedCrossRefGoogle Scholar
  47. Lasanen, L. T., Tammela, T. L., Liesi, P., Waris, T., & Polak, J. M. (1992). The effect of acute distension on vasoactive intestinal polypeptide (VIP), neuropeptide Y (NPY) and substance P (SP) immunoreactive nerves in the female rat urinary bladder. Urological Research, 20, 259–263.PubMedCrossRefGoogle Scholar
  48. Lavelle, J., Meyers, S., Ramage, R., et al. (2002). Bladder permeability barrier: recovery from selective injury of surface epithelial cells. American Journal of Physiology. Renal Physiology, 283, F242–F253.PubMedGoogle Scholar
  49. Lelievre, V., Favrais, G., Abad, C., et al. (2007). Gastrointestinal dysfunction in mice with a targeted mutation in the gene encoding vasoactive intestinal polypeptide: a model for the study of intestinal ileus and Hirschsprung's disease. Peptides, 28, 1688–1699.PubMedCrossRefGoogle Scholar
  50. Lewis, S. A., & de Moura, J. L. (1984). Apical membrane area of rabbit urinary bladder increases by fusion of intracellular vesicles: an electrophysiological study. Journal of Membrane Biology, 82, 123–136.PubMedCrossRefGoogle Scholar
  51. Lowe, E. M., Anand, P., Terenghi, G., Williams-Chestnut, R. E., Sinicropi, D. V., & Osborne, J. L. (1997). Increased nerve growth factor levels in the urinary bladder of women with idiopathic sensory urgency and interstitial cystitis. British Journal of Urology, 79, 572–577.PubMedGoogle Scholar
  52. Maggi, C. A., Santicioli, P., & Meli, A. (1986). The nonstop transvesical cystometrogram in urethane-anesthetized rats: a simple procedure for quantitative studies on the various phases of urinary bladder voiding cycle. Journal of Pharmacological Methods, 15, 157–167.PubMedCrossRefGoogle Scholar
  53. Malley, S. E., & Vizzard, M. A. (2002). Changes in urinary bladder cytokine mRNA and protein after cyclophosphamide-induced cystitis. Physiological Genomics, 9, 5–13.PubMedGoogle Scholar
  54. Martinez, C., Juarranz, Y., Abad, C., et al. (2005). Analysis of the role of the PAC1 receptor in neutrophil recruitment, acute-phase response, and nitric oxide production in septic shock. Journal of Leukocyte Biology, 77, 729–738.PubMedCrossRefGoogle Scholar
  55. Martinez, V., & Melgar, S. (2008) Lack of colonic inflammation-induced acute visceral hypersensitivity to colorectal distension in Na(v)1.9 knockout mice. European Journal of Pain.Google Scholar
  56. Maruno, K., Absood, A., & Said, S. I. (1995). VIP inhibits basal and histamine-stimulated proliferation of human airway smooth muscle cells. American Journal of Physiology, 268, L1047–L1051.PubMedGoogle Scholar
  57. Mason, J. L., Suzuki, K., Chaplin, D. D., & Matsushima, G. K. (2001). Interleukin-1 beta promotes repair of the CNS. Journal of Neuroscience, 21, 7046–7052.PubMedGoogle Scholar
  58. Morgan, C. W., Ohara, P. T., & Scott, D. E. (1999). Vasoactive intestinal polypeptide in sacral primary sensory pathways in the cat. Journal of Comparative Neurology, 407, 381–394.PubMedCrossRefGoogle Scholar
  59. Newman, R., Cuan, N., Hampartzoumian, T., Connor, S. J., Lloyd, A. R., & Grimm, M. C. (2005). Vasoactive intestinal peptide impairs leucocyte migration but fails to modify experimental murine colitis. Clinical and Experimental Immunology, 139, 411–420.PubMedCrossRefGoogle Scholar
  60. Okragly, A. J., Niles, A. L., Saban, R., et al. (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. Journal of Urology, 161, 438–441 discussion 441–432.PubMedCrossRefGoogle Scholar
  61. Parsons, C. L. (2007). The role of the urinary epithelium in the pathogenesis of interstitial cystitis/prostatitis/urethritis. Urology, 69, 9–16.PubMedCrossRefGoogle Scholar
  62. Qiao, L. Y., & Vizzard, M. A. (2002a). Cystitis-induced upregulation of tyrosine kinase (TrkA, TrkB) receptor expression and phosphorylation in rat micturition pathways. Journal of Comparative Neurology, 454, 200–211.PubMedCrossRefGoogle Scholar
  63. Qiao, L. Y., & Vizzard, M. A. (2002b). Up-regulation of tyrosine kinase (TrkA, TrkB) receptor expression and phosphorylation in lumbosacral dorsal root ganglia after chronic spinal cord (T8-T10) injury. Journal of Comparative Neurology, 449, 217–230.PubMedCrossRefGoogle Scholar
  64. Qiao, L. Y., & Vizzard, M. A. (2004). Up-regulation of phosphorylated CREB but not c-Jun in bladder afferent neurons in dorsal root ganglia after cystitis. Journal of Comparative Neurology, 469, 262–274.PubMedCrossRefGoogle Scholar
  65. Rudick, C. N., Chen, M. C., Mongiu, A. K., & Klumpp, D. J. (2007). Organ cross talk modulates pelvic pain. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 293, R1191–1198.PubMedGoogle Scholar
  66. Said, S. I. (1991). Vasoactive intestinal polypeptide (VIP) in asthma. Annals of the New York Academy of Sciences, 629, 305–318.PubMedCrossRefGoogle Scholar
  67. Samad, T. A., Moore, K. A., Sapirstein, A., et al. (2001). Interleukin-1 beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature, 410, 471–475.PubMedCrossRefGoogle Scholar
  68. Sant, G. R., & Hanno, P. M. (2001). Interstitial cystitis: current issues and controversies in diagnosis. Urology, 57, 82–88.PubMedCrossRefGoogle Scholar
  69. Shin, J. W., Hwang, K. S., Kim, Y. K., Leem, J. G., & Lee, C. (2006). Nonsteroidal antiinflammatory drugs suppress pain-related behaviors, but not referred hyperalgesia of visceral pain in mice. Anesthesia and Analgesia, 102, 195–200.PubMedCrossRefGoogle Scholar
  70. Smet, P. J., Moore, K. H., & Jonavicius, J. (1997). Distribution and colocalization of calcitonin gene-related peptide, tachykinins, and vasoactive intestinal peptide in normal and idiopathic unstable human urinary bladder. Laboratory Investigation, 77, 37–49.PubMedGoogle Scholar
  71. Steers, W. D., Creedon, D. J., & Tuttle, J. B. (1996). Immunity to nerve growth factor prevents afferent plasticity following urinary bladder hypertrophy. Journal of Urology, 155, 379–385.PubMedCrossRefGoogle Scholar
  72. Steers, W. D., & de Groat, W. C. (1988). Effect of bladder outlet obstruction on micturition reflex pathways in the rat. Journal of Urology, 140, 864–871.PubMedGoogle Scholar
  73. Steers, W. D., Kolbeck, S., Creedon, D., & Tuttle, J. B. (1991). Nerve growth factor in the urinary bladder of the adult regulates neuronal form and function. Journal of Clinical Investigation, 88, 1709–1715.PubMedCrossRefGoogle Scholar
  74. Streng, T., Hedlund, P., Talo, A., Andersson, K. E., & Gillespie, J. I. (2006). Phasic non-micturition contractions in the bladder of the anaesthetized and awake rat. British Journal of Urology International, 97, 1094–1101.Google Scholar
  75. Szema, A. M., Hamidi, S. A., Lyubsky, S., et al. (2006). Mice lacking the VIP gene show airway hyperresponsiveness and airway inflammation, partially reversible by VIP. American Journal of Physiology. Lung Cellular and Molecular Physiology, 291, L880–886.PubMedCrossRefGoogle Scholar
  76. Thor, K. B., Blais, D. P., & de Groat, W. C. (1989). Behavioral analysis of the postnatal development of micturition in kittens. Developmental Brain Research, 46, 137–144.PubMedCrossRefGoogle Scholar
  77. Truschel, S. T., Ruiz, W. G., Shulman, T., et al. (1999). Primary uroepithelial cultures. A model system to analyze umbrella cell barrier function. Journal of Biological Chemistry, 274, 15020–15029.PubMedCrossRefGoogle Scholar
  78. Truschel, S. T., Wang, E., Ruiz, W. G., et al. (2002). Stretch-regulated exocytosis/endocytosis in bladder umbrella cells. Molecular Biology of the Cell, 13, 830–846.PubMedCrossRefGoogle Scholar
  79. Tuttle, J. B., Steers, W. D., Albo, M., & Nataluk, E. (1994). Neural input regulates tissue NGF and growth of the adult rat urinary bladder. Journal of the Autonomic Nervous System, 49, 147–158.PubMedCrossRefGoogle Scholar
  80. Uckert, S., Stief, C. G., Lietz, B., Burmester, M., Jonas, U., & Machtens, S. A. (2002). Possible role of bioactive peptides in the regulation of human detrusor smooth muscle—functional effects in vitro and immunohistochemical presence. World Journal of Urology, 20, 244–249.PubMedGoogle Scholar
  81. Vera, P. L., & Meyer-Siegler, K. L. (2004). Inflammation of the rat prostate evokes release of macrophage migration inhibitory factor in the bladder: evidence for a viscerovisceral reflex. Journal of Urology, 172, 2440–2445.PubMedCrossRefGoogle Scholar
  82. Vizzard, M. A. (2000a). Changes in urinary bladder neurotrophic factor mRNA and NGF protein following urinary bladder dysfunction. Experimental Neurology, 161, 273–284.PubMedCrossRefGoogle Scholar
  83. Vizzard, M. A. (2000b). Up-regulation of pituitary adenylate cyclase-activating polypeptide in urinary bladder pathways after chronic cystitis. Journal of Comparative Neurology, 420, 335–348.PubMedCrossRefGoogle Scholar
  84. Vizzard, M. A. (2000c). Alterations in spinal cord Fos protein expression induced by bladder stimulation following cystitis. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 278, R1027–1039.PubMedGoogle Scholar
  85. Vizzard, M. A. (2000d). Alterations in spinal Fos protein expression induced by bladder stimulation following cystitis. American Journal of Physiology, 278, R1027–R1039.PubMedGoogle Scholar
  86. Vizzard, M. A. (2001). Alterations in neuropeptide expression in lumbosacral bladder pathways following chronic cystitis. Journal of Chemical Neuroanatomy, 21, 125–138.PubMedCrossRefGoogle Scholar
  87. Vizzard, M. A., & Boyle, M. M. (1999). Increased expression of growth-associated protein (GAP-43) in lower urinary tract pathways following cyclophosphamide (CYP)-induced cystitis. Brain Research, 844, 174–187.PubMedCrossRefGoogle Scholar
  88. Vizzard, M. A., Braas, K. M., Studeny, S., et al. (2007). Vasoactive intestinal polypeptide knockout (VIP-/-) mice exhibit altered bladder function and somatic sensitivity with cyclophosphamide (CYP)-induced cystitis. Journal of Molecular Neuroscience, 33, 311.Google Scholar
  89. Vizzard, M. A., & de Groat, W. C. (1996). Increased expression of neuronal nitric oxide synthase (NOS) in bladder afferent pathways following chronic bladder irritation. Journal of Comparative Neurology, 370, 191–202.PubMedCrossRefGoogle Scholar
  90. Voice, J. K., Dorsam, G., Chan, R. C., Grinninger, C., Kong, Y., & Goetzl, E. J. (2002). Immunoeffector and immunoregulatory activities of vasoactive intestinal peptide. Regulatory Peptides, 109, 199–208.PubMedCrossRefGoogle Scholar
  91. Wang, E., Truschel, S., & Apodaca, G. (2003). Analysis of hydrostatic pressure-induced changes in umbrella cell surface area. Methods, 30, 207–217.PubMedCrossRefGoogle Scholar
  92. Wanigasekara, Y., Kepper, M. E., & Keast, J. R. (2003). Immunohistochemical characterisation of pelvic autonomic ganglia in male mice. Cell and Tissue Research, 311, 175–185.PubMedGoogle Scholar
  93. Winkelstein, B. A., Rutkowski, M. D., Sweitzer, S. M., Pahl, J. L., & DeLeo, J. A. (2001). Nerve injury proximal or distal to the DRG induces similar spinal glial activation and selective cytokine expression but differential behavioral responses to pharmacologic treatment. Journal of Comparative Neurology, 439, 127–139.PubMedCrossRefGoogle Scholar
  94. Wong, M.-L., Rettori, V., McCann, S. M., & Licinio, J. (1997). Interleukin (IL) 1-beta, IL-1 receptor antagonist, IL-10 and IL-13 gene expression in the central nervous system and anterior pituitary during systemic inflammation: pathophysiological implications. Proceedings of the National Academy of Sciences of the United States of America, 94, 227–232.PubMedCrossRefGoogle Scholar
  95. Yoshimura, N., Bennett, N. E., Hayashi, Y., et al. (2006). Bladder overactivity and hyperexcitability of bladder afferent neurons after intrathecal delivery of nerve growth factor in rats. Journal of Neuroscience, 26, 10847–10855.PubMedCrossRefGoogle Scholar
  96. Yoshimura, N., & de Groat, W. C. (1999). Increased excitability of afferent neurons innervating rat urinary bladder following chronic bladder inflammation. Journal of Neuroscience, 19, 4644–4653.PubMedGoogle Scholar
  97. Zvara, P., Kliment, J., DeRoss, A. L., et al. (2002). Differential expression of bladder neurotrophic factor mRNA in male and female rats after bladder outflow obstruction. Journal of Urology, 168, 2682–2688.PubMedCrossRefGoogle Scholar
  98. Zvara, P., & Vizzard, M. A. (2007). Exogenous overexpression of nerve growth factor in the urinary bladder produces bladder overactivity and altered micturition circuitry in the lumbosacral spinal cord. BMC Physiology, 7, 9.PubMedCrossRefGoogle Scholar
  99. Zvarova, K., & Vizzard, M. A. (2006). Changes in galanin immunoreactivity in rat micturition reflex pathways after cyclophosphamide-induced cystitis. Cell and Tissue Research, 324, 213–224.PubMedCrossRefGoogle Scholar

Copyright information

© Humana Press 2008

Authors and Affiliations

  • Simon Studeny
    • 1
  • Bopaiah P. Cheppudira
    • 1
  • Susan Meyers
    • 4
  • Elena M. Balestreire
    • 4
    • 5
  • Gerard Apodaca
    • 4
    • 5
  • Lori A. Birder
    • 4
  • Karen M. Braas
    • 2
  • James A. Waschek
    • 3
  • Victor May
    • 2
  • Margaret A. Vizzard
    • 1
    • 2
  1. 1.Department of NeurologyUniversity of Vermont College of MedicineBurlingtonUSA
  2. 2.Anatomy and NeurobiologyUniversity of Vermont College of MedicineBurlingtonUSA
  3. 3.Mental Retardation Research Center, Semel Institute for Neuroscience, The David Geffen School of MedicineUniversity of California at Los AngelesLos AngelesUSA
  4. 4.Renal-Electrolyte Division, Laboratory of Epithelial Cell BiologyUniversity of PittsburghPittsburghUSA
  5. 5.Department of Cell Biology and PhysiologyUniversity of PittsburghPittsburghUSA

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