Repeated variate stress in male rats induces increased voiding frequency, somatic sensitivity, and urinary bladder nerve growth factor expression

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 305, Issue 2, 2013, Pages

  Merrill, Liana ^a   Malley, Susan ^a   Vizzard, Margaret A ^a  

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

Author keywords

ELISA; Micturition; Nerve growth factor; Somatic sensitivity; Stress

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CHEMOKINE RECEPTOR CXCR4; EVANS BLUE; HISTAMINE; MYELOPEROXIDASE; NERVE GROWTH FACTOR; SODIUM CHLORIDE;

ANIMAL TISSUE; ARTICLE; BLADDER; BLADDER FUNCTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; MALE; MICTURITION; MICTURITION REFLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; RAT; STRESS; TARGET ORGAN; WEIGHT GAIN;

ELISA; MICTURITION; NERVE GROWTH FACTOR; SOMATIC SENSITIVITY; STRESS;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; HISTAMINE; MALE; NERVE GROWTH FACTOR; PEROXIDASE; PHYSICAL STIMULATION; RATS; RATS, WISTAR; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL; URINARY BLADDER; URINATION;

EID: 84880144023     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00089.2013     Document Type: Article

References (78)

1. Aloe L, Tuveri MA, Levi-Montalcini R. Studies on carrageenan-induced arthritis in adult rats: presence of nerve growth factor and role of sympathetic innervation. Rheumatol Int 12: 213-216, 1992.
2. Arms L, Girard BM, Vizzard MA. Expression and function of CXCL12/ CXCR4 in rat urinary bladder with cyclophosphamide-induced cystitis. Am J Physiol Renal Physiol 298: F589-F600, 2010.
3. Bazi T, Hajj-Hussein IA, Awwad J, Shams A, Hijaz M, Jurjus A. A modulating effect of epigallocatechin gallate (EGCG), a tea catechin, on the bladder of rats exposed to water avoidance stress. Neurourol Urodyn 32: 287-292, 2012.
4. Bhatnagar S, Vining C, Iyer V, Kinni V. Changes in hypothalamicpituitary-adrenal function, body temperature, body weight and food intake with repeated social stress exposure in rats. J Neuroendocrinol 18: 13-24, 2006.
5. Birder LA, de Groat WC. Mechanisms of disease: involvement of the urothelium in bladder dysfunction. Nat Clin Pract Urol 4: 46-54, 2007.
6. Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai AJ, Wang E, Ruiz G, De Groat WC, Apodaca G, Watkins S, Caterina MJ. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci 5: 856-860, 2002.
7. Black LV, Ness TJ, Robbins MT. Effects of oxytocin and prolactin on stress-induced bladder hypersensitivity in female rats. J Pain 10: 1065-1072, 2009.
8. Bohm-Starke N, Hilliges M, Brodda-Jansen G, Rylander E, Torebjork E. Psychophysical evidence of nociceptor sensitization in vulvar vestibulitis syndrome. Pain 94: 177-183, 2001.
9. Bon K, Lichtensteiger CA, Wilson SG, Mogil J. Characterization of cyclophosphamide cystitis, a model of visceral and referred pain, in the mouse: species and strain differences. J Urol 170: 1008-1012, 2003.
10. Boucher W, Kempuraj D, Michaelian M, Theoharides TC. Corticotropin-releasing hormone-receptor 2 is required for acute stress-induced bladder vascular permeability and release of vascular endothelial growth factor. BJU Int 106: 1394-1399, 2010.
11. Boucher WS, Letourneau R, Huang M, Kempuraj D, Green M, Sant GR, Theoharides TC. Intravesical sodium hyaluronate inhibits the rat urinary mast cell mediator increase triggered by acute immobilization stress. J Urol 167: 380-384, 2002.
12. Bradley PP, Priebat DA, Christensen RD, Rothstein G. Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 78: 206-209, 1982.
13. Calupca MA, Vizzard MA, Parsons RL. Origin of pituitary adenylate cyclase-activating polypeptide (PACAP)-immunoreactive fibers innervating guinea pig parasympathetic cardiac ganglia. J Comp Neurol 423: 26-39, 2000.
14. Cetinel S, Ercan F, Cikler E, Contuk G, Sener G. Protective effect of melatonin on water avoidance stress induced degeneration of the bladder. J Urol 173: 267-270, 2005.
15. Chang A, Butler S, Sliwoski J, Valentino R, Canning D, Zderic S. Social stress in mice induces voiding dysfunction and bladder wall remodeling. Am J Physiol Renal Physiol 297: F1101-F1108, 2009.
16. Cheppudira BP, Girard BM, Malley SE, Dattilio A, Schutz KC, May V, Vizzard MA. Involvement of JAK-STAT signaling/function after cyclophosphamide-induced bladder inflammation in female rats. Am J Physiol Renal Physiol 297: F1038-F1044, 2009.
17. Chien CC, Fu WM, Huang HI, Lai YH, Tsai YF, Guo SL, Wu TJ, Ling QD. Expression of neurotrophic factors in neonatal rats after peripheral inflammation. J Pain 8: 161-167, 2007.
18. 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.
19. Ciobanu C, Reid G, Babes A. Acute and chronic effects of neurotrophic factors BDNF and GDNF on responses mediated by thermo-sensitive TRP channels in cultured rat dorsal root ganglion neurons. Brain Res 1284: 54-67, 2009.
20. 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.
21. de Groat WC. The urothelium in overactive bladder: passive bystander or active participant? Urology 64: 7-11, 2004.
22. Desjardins C, Maruniak JA, Bronson FH. Social rank in house mice: differentiation revealed by ultraviolet visualization of urinary marking patterns. Science 182: 939-941, 1973.
23. Dmitrieva N, McMahon SB. Sensitisation of visceral afferents by nerve growth factor in the adult rat. Pain 66: 87-97, 1996.
24. 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.
25. Frias B, Lopes T, Pinto R, Cruz F, Cruz CD. Neurotrophins in the lower urinary tract: becoming of age. Curr Neuropharmacol 9: 553-558, 2011.
26. Friess H, Zhu ZW, di Mola FF, Kulli C, Graber HU, Andren-Sandberg A, Zimmermann A, Korc M, Reinshagen M, Buchler MW. Nerve growth factor and its high-affinity receptor in chronic pancreatitis. Ann Surg 230: 615-624, 1999.
27. Girard BM, Wolf-Johnston A, Braas KM, Birder LA, May V, Vizzard MA. PACAP-mediated ATP release from rat urothelium and regulation of PACAP/VIP and receptor mRNA in micturition pathways after cyclophosphamide (CYP)-induced cystitis. J Mol Neurosci 36: 310-320, 2008.
28. 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.
29. 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.
30. Hammack SE, Cheung J, Rhodes KM, Schutz KC, Falls WA, Braas KM, May V. Chronic stress increases pituitary adenylate cyclase-activating peptide (PACAP) and brain-derived neurotrophic factor (BDNF) mRNA expression in the bed nucleus of the stria terminalis (BNST): roles for PACAP in anxiety-like behavior. Psychoneuroendocrinology 34: 833-843, 2009.
31. Hammack SE, Roman CW, Lezak KR, Kocho-Shellenberg M, Grimmig B, Falls WA, Braas K, May V. Roles for pituitary adenylate cyclase-activating peptide (PACAP) expression and signaling in the bed nucleus of the stria terminalis (BNST) in mediating the behavioral consequences of chronic stress. J Mol Neurosci 42: 327-340, 2010.
32. Herrera GM, Pozo MJ, Zvara P, Petkov GV, Bond CT, Adelman JP, Nelson MT. Urinary bladder instability induced by selective suppression of the murine small conductance calcium-activated potassium (SK3) channel. J Physiol 551: 893-903, 2003.
33. 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.
34. Jaggar SI, Scott HC, 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.
35. Jasmin L, Janni G, Manz HJ, Rabkin SD. Activation of CNS circuits producing a neurogenic cystitis: evidence for centrally induced peripheral inflammation. J Neurosci 18: 10016-10029, 1998.
36. Jorgensen A, Maigaard K, Wortwein G, Hageman I, Henriksen T, Weimann A, Moller P, Loft S, Hau J, Poulsen HE, Jorgensen MB. Chronic restraint stress in rats causes sustained increase in urinary corticosterone excretion without affecting cerebral or systemic oxidatively generated DNA/RNA damage. Prog Neuropsychopharmacol Biol Psychiatry 40C: 30-37, 2012.
37. 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; discussion 1776, 2006.
38. Klausner AP, Steers WD. Corticotropin releasing factor: a mediator of emotional influences on bladder function. J Urol 172: 2570-2573, 2004.
39. 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.
40. 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.
41. Lamb K, Gebhart GF, Bielefeldt K. Increased nerve growth factor expression triggers bladder overactivity. J Pain 5: 150-156, 2004.
42. 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: 700-706, 2009.
43. 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; discussion 108, 2008.
44. 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.
45. May V, Vizzard MA. Bladder dysfunction and altered somatic sensitivity in PACAP-/-mice. J Urol 183: 772-779, 2010.
46. Miczek KA. A new test for aggression in rats without aversive stimulation: differential effects of d-amphetamine and cocaine. Psychopharmacology (Berl) 60: 253-259, 1979.
47. Nazif O, Teichman JM, Gebhart GF. Neural upregulation in interstitial cystitis. Urology 69: 24-33, 2007.
48. Ochodnicky P, Cruz CD, Yoshimura N, Cruz F. Neurotrophins as regulators of urinary bladder function. Nat Rev Urol 9: 628-637, 2012.
49. 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.
50. 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 neurotrophic factor levels in the urine of interstitial cystitis and bladder cancer patients. J Urol 161: 438-441; discussion 441-432, 1999.
51. 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.
52. Ratliff TL, Klutke CG, McDougall EM. The etiology of interstitial cystitis. Urol Clin North Am 21: 21-30, 1994.
53. Ro LS, Chen ST, Tang LM, Jacobs JM. Effect of NGF and anti-NGF on neuropathic pain in rats following chronic constriction injury of the sciatic nerve. Pain 79: 265-274, 1999.
54. Robbins MT, DeBerry J, Ness TJ. Chronic psychological stress enhances nociceptive processing in the urinary bladder in high-anxiety rats. Physiol Behav 91: 544-550, 2007.
55. Robbins MT, Ness TJ. Footshock-induced urinary bladder hypersensitivity: role of spinal corticotropin-releasing factor receptors. J Pain 9: 991-998, 2008.
56. Roman CW, Lezak KR, Kocho-Schellenberg M, Garret MA, Braas K, May V, Hammack SE. Excitotoxic lesions of the bed nucleus of the stria terminalis (BNST) attenuate the effects of repeated stress on weight gain: evidence for the recruitment of BNST activity by repeated, but not acute, stress. Behav Brain Res 227: 300-304, 2012.
57. Rostamkhani F, Zardooz H, Zahediasl S, Farrokhi B. Comparison of the effects of acute and chronic psychological stress on metabolic features in rats. J Zhejiang Univ Sci B 13: 904-912, 2012.
58. Rothrock NE, Lutgendorf SK, Kreder KJ, Ratliff T, Zimmerman B. Stress and symptoms in patients with interstitial cystitis: a life stress model. Urology 57: 422-427, 2001.
59. 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.
60. Saitoh C, Yokoyama H, Chancellor MB, de Groat WC, Yoshimura N. Comparison of voiding function and nociceptive behavior in two rat models of cystitis induced by cyclophosphamide or acetone. Neurourol Urodyn 29: 501-505, 2010.
61. Schnegelsberg B, Sun TT, Cain G, Bhattacharya A, Nunn PA, Ford AP, Vizzard MA, Cockayne DA. Overexpression of NGF in mouse urothelium leads to neuronal hyperinnervation, pelvic sensitivity, and changes in urinary bladder function. Am J Physiol Regul Integr Comp Physiol 298: R534-R547, 2010.
62. Smith AL, Leung J, Kun S, Zhang R, Karagiannides I, Raz S, Lee U, Glovatscka V, Pothoulakis C, Bradesi S, Mayer EA, Rodriguez LV. The effects of acute and chronic psychological stress on bladder function in a rodent model. Urology 78: 967 e961-e967, 2011.
63. Solomon MB, Jones K, Packard BA, Herman JP. The medial amygdala modulates body weight but not neuroendocrine responses to chronic stress. J Neuroendocrinol 22: 13-23, 2010.
64. 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.
65. Streng T, Santti R, Andersson KE, Talo A. The role of the rhabdosphincter in female rat voiding. BJU Int 94: 138-142, 2004.
66. Streng T, Santti R, Talo A. Similarities and differences in female and male rat voiding. Neurourol Urodyn 21: 136-141, 2002.
67. Studeny S, Cheppudira BP, Meyers S, Balestreire EM, Apodaca G, Birder LA, Braas KM, Waschek JA, May V, Vizzard MA. Urinary bladder function and somatic sensitivity in vasoactive intestinal polypeptide (VIP)-/-mice. J Mol Neurosci 36: 175-187, 2008.
68. Uvin P, Everaerts W, Pinto S, Alpizar YA, Boudes M, Gevaert T, Voets T, Nilius B, Talavera K, De Ridder D. The use of cystometry in small rodents: a study of bladder chemosensation. J Vis Exp 66: e3869. doi:10.3791/3869, 2012.
69. Verne GN, Robinson ME, Price DD. Hypersensitivity to visceral and cutaneous pain in the irritable bowel syndrome. Pain 93: 7-14, 2001.
70. Vizzard MA. Alterations in neuropeptide expression in lumbosacral bladder pathways following chronic cystitis. J Chem Neuroanat 21: 125-138, 2001.
71. Vizzard MA. Changes in urinary bladder neurotrophic factor mRNA and NGF protein following urinary bladder dysfunction. Exp Neurol 161: 273-284, 2000.
72. Westropp JL, Buffington CA. In vivo models of interstitial cystitis. J Urol 167: 694-702, 2002.
73. Wilson SG, Mogil JS. Measuring pain in the (knockout) mouse: big challenges in a small mammal. Behav Brain Res 125: 65-73, 2001.
74. Wood SK, Baez MA, Bhatnagar S, Valentino RJ. Social stress-induced bladder dysfunction: potential role of corticotropin-releasing factor. Am J Physiol Regul Integr Comp Physiol 296: R1671-R1678, 2009.
75. Xu GY, Winston JH, Shenoy M, Yin H, Pendyala S, Pasricha PJ. Transient receptor potential vanilloid 1 mediates hyperalgesia and is up-regulated in rats with chronic pancreatitis. Gastroenterology 133: 1282-1292, 2007.
76. 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.
77. 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.
78. Zwick M, Molliver DC, Lindsay J, Fairbanks CA, Sengoku T, Albers KM, Davis BM. Transgenic mice possessing increased numbers of nociceptors do not exhibit increased behavioral sensitivity in models of inflammatory and neuropathic pain. Pain 106: 491-500, 2003.