Nervous network for lower urinary tract function

International Journal of Urology

Volumn 20, Issue 1, 2013, Pages 4-12

  Birder, Lori A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Afferents; Barrier function; Mucosa; Sensory function; Uroepithelium

Indexed keywords

NITRIC OXIDE;

CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CHOLINERGIC NERVE; GLIA CELL; HUMAN; PRIORITY JOURNAL; REVIEW; SENSORY NERVE; SIGNAL TRANSDUCTION; URETHRA; UROTHELIUM;

AFFERENT PATHWAYS; ANIMALS; CELL COMMUNICATION; HUMANS; URETHRA; URINARY BLADDER; UROTHELIUM;

EID: 84871936063     PISSN: 09198172     EISSN: 14422042     Source Type: Journal    
DOI: 10.1111/j.1442-2042.2012.03210.x     Document Type: Review

References (91)

1. Khanderwal P, Abraham SN, Apodaca G. Cell biology and physiology of the uroepithelium. Am. J. Physiol. 2009; 297: F1477-1501.
2. Apodaca G. The uroepithelium: not just a passive barrier. Traffic 2004; 5: 117-128.
3. Sun TT. Altered phenotype of cultured urothelial and other stratified epithelial cells: implications for wound healing. Am. J. Physiol. 2006; 291: F9-21.
4. Thomas JC, DeMarco RT, Pope JC. Molecular biology of ureteral bud and trigonal development. Curr. Urol. Rep. 2005; 6: 146-151.
5. Hashimoto Y, Ushiki T, Uchida T, Yamada J, Iwanaga T. Scanning electron microscopic observation of apical sites of open-type paraneurons in the stomach, intestine and urethra. Arch. Histol. Cytol. 1999; 62: 181-189.
6. Czaja K, Sienkiewica W, Vittoria A, Costagliola A, Cecio A. Neuroendocrine cells in the female urogenital tract of the pig, and their immunohistochemical characterization. Acta Anat. (Basel) 1996; 157: 11-19.
7. Iwanaga T, Han H, Hoshi O, Kanazawa H, Adachi I, Fujita T. Topographical relation between serotonin-containing paraneurons and peptidergic neurons in the intestine and urethra. Biol. Signals 1994; 3: 259-270.
8. Saban MR, Memet S, Jackson DG etal. Visualization of lymphatic vessels through NF-kappaB activity. Blood 2004; 104: 3228-3230.
9. Aitken KJ, Bagli DJ. The bladder extracellular matrix. Part I: architecture, development and disease. Nat. Rev. Urol. 2009; 6: 596-611.
10. Dixon JS, Gosling JA. Histology and fine structure of the muscularis mucosae of the human urinary bladder. J. Anat. 1983; 136: 265-271.
11. Gevaert T, De Vos R, Everaerts W etal. Characterization of upper lamina propria interstitial cells in bladders from patients with neurogenic detrusor overactivity and bladder pain syndrome. J. Cell. Mol. Med. 2011b; 15: 2586-2593.
12. McCloskey KD. Interstitial cells in the urinary bladder - localization and function. Neurourol. Urodyn. 2010; 29: 82-87.
13. McCloskey KD. Interstitial cells of Cajal in the urinary tract. Handb. Exp. Pharmacol. 2011; 202: 233-254.
14. Sui GP, Wu C, Fry CH. Electrical characteristics of suburothelial cells isolated from the human bladder. J. Urol. 2004; 171: 938-943.
15. Wiseman OJ, Fowler CJ, Landon DN. The role of the human bladder lamina propria myofibroblast. BJU Int. 2003; 91: 89-93.
16. de Groat WC, Yoshimura N. Afferent nerve regulation of bladder function in health and disease. Handb. Exp. Pharmacol. 2009; 194: 91-138.
17. Andersson KE. Detrusor myocyte activity and afferent signaling. Neurourol. Urodyn. 2010; 29: 97-106.
18. Kanai AJ, Andersson KE. Bladder afferent signaling: recent findings. J. Urol. 2010; 183: 1288-1295.
19. Janig W, Morrison JF. Functional properties of spinal visceral afferents supplying abdominal and pelvic organs, with special emphasis on visceral nociception. Prog. Brain Res. 1986; 67: 87-114.
20. de Groat WC. Spinal cord projections and neuropeptides in visceral afferent neurons. Prog. Brain Res. 1986; 67: 167-187.
21. Gabella G, Davis C. Distribution of afferent axons in the bladder of rats. J. Neurocytol. 1998; 27: 141-155.
22. Xu L, Gebhart GA. Characterization of mouse lumbar splanchnic and pelvic nerve urinary bladder mechanosensory afferents. J. Neurophysiol. 2007; 99: 244-253.
23. Habler HJ, Janig W, Koltzenburg M. Activation of unmyelinated afferent fibres by mechanical stimuli and inflammation of the urinary bladder in the cat. J. Physiol. 1990; 425: 545-562.
24. Snellings AE, Yoo PB, Grill WM. Urethral flow-responsive afferents in the cat sacral dorsal root ganglia. Neurosci. Lett. 2012; 516: 34-38.
25. Hanno P, Andersson KE, Birder L, Elneil S, Kanai A, Pontari M. Chronic pelvic pain syndrome/bladder pain syndrome: taking stock, looking ahead: ICI-RS 2011. Neurourol. Urodyn. 2012; 31: 375-383.
26. Nazif O, Teichman JM, Gebhart GF. Neural upregulation in interstitial cystitis. Urology 2007; 69: 24-33.
27. Cruz F, Dinis P. Resiniferatoxin and botulinum toxin type A for treatment of lower urinary tract symptoms. Neurourol. Urodyn. 2007; 26: 920-927.
28. Sanchez-Freire V, Blanchard MG, Burkhard FC, Kessler TM, Kellenberger S, Monastyrskaya K. Acid-sensing channels in human bladder: expression, function and alterations during bladder pain syndrome. J. Urol. 2011; 186: 1509-1516.
29. Ford AP. In pursuit of P2X3 antagonists: novel therapeutics for chronic pain and afferent sensitization. Purinergic Signal. 2012; 8: S3-S26.
30. Ochodnicky P, Cruz CD, Yoshimura N, Michel MC. Nerve growth factor in bladder dysfunction: contributing factor, biomarker, and therapeutic target. Neurourol. Urodyn. 2011; 30: 1227-1241.
31. Lowe EM, Anand P, Terenghi G. Increased nerve growth factor levels in the urinary bladder of women with idiopathic sensory urgency and interstitial cystitis. Br. J. Urol. 1997; 79: 572-577.
32. Schnegelsberg B, Sun TT, Cain G etal. Overexpression of NGF in mouse urothelium leads to neuronal hyperinnervation, pelvic sensitivity, and changes in urinary bladder function. Am. J. Physiol. 2010; 298: R534-547.
33. Mulligan ED, Watkins LR. Pathological and protective roles of glia in chronic pain. Nat. Rev. Neurosci. 2009; 10: 23-36.
34. Ren K, Dubnew R. Neuron-glia crosstalk gets serious: role in pain hypersensitivity. Curr. Opin. Anaesthiol. 2008; 21: 570-579.
35. Birder LA, Wolf-Johnston AS, Chib MK. Beyond neurons: involvement of urothelial and glial cells in bladder function. Neurourol. Urodyn. 2010; 29: 88-96.
36. Bradesi S, Golovatschka V, Ennes HS etal. Role of astrocytes and altered regulation of spinal glutamatergic neurotransmission in stress-induced visceral hyperalgesia in rats. Am. J. Physiol. Gastrointest. Liver 2011; 301: G580-589.
37. Parson CL, Boychuk D, Jones S, Hurst R, Callahan H. Bladder surface glycosaminoglycans: an epithelial permeability barrier. J. Urol. 1990; 143: 139-142.
38. Wang EC, Lee JM, Ruiz WG etal. ATP and purinergic receptor-dependent membrane traffic in bladder umbrella cells. J. Clin. Invest. 2005; 115: 2412-2422.
39. Hicks M. The mammalian urinary bladder: an accomodating organ. Biol. Rev. 1975; 50: 215-246.
40. Balestreire EM, Apodaca G. Apical EGF receptor signaling: regulation of stretch-dependent exocytosis in bladder umbrella cells. Mol. Biol. Cell 2007; 13: 830-843.
41. Romih R, Korosec P, de Mello W, Jezernik K. Differentiation of epithelial cells in the urinary tract. Cell Tissue Res. 2005; 320: 259-268.
42. Martin BF. Cell replacement and differentiation in transitional epithelium: a histological and autoradiographic study of the guinea-pig bladder and ureter. J. Anat. 1972; 112: 433-455.
43. Hicks M, Ketterer B, Warren R. The ultrastructure and chemistry of the luminal plasma membrane of the mammalian urinary bladder: a structure with low permeability to water and ions. Phil. Trans. R. Soc. Lond. 1974; 268: 23-38.
44. Kreft ME, Sterle M, Veranic P, Jezernik K. Urothelial injuries and the early wound healing response: tight junctions and urothelial cytodifferentiation. Histochem. Cell Biol. 2005; 123: 529-539.
45. Kanai AJ, Zeidel M, Lavelle JP etal. Manganese superoxide dismutase gene therapy protects against irradiation-induced cystitis. Am. J. Physiol. 2002; 283: F1304-1312.
46. Kreft ME, Jezernik K, Kreft M, Romih R. Apical plasma membrane traffic in superficial cells of bladder urothelium. Ann. N.Y. Acad. Sci. 2009; 1152: 18-29.
47. Apodaca G, Kiss S, Ruiz W, Meyers S, Zeidel M, Birder L. Disruption of bladder epithelium barrier function after spinal cord injury. Am. J. Physiol. Renal Physiol. 2003; 284: F966-976.
48. Lavelle JP, Meyers SA, Ruiz WG, Buffington CAT, Zeidel M, Apodaca G. Urothelial pathophysiological changes in feline interstitial cystitis: a human model. Am. J. Physiol. Renal Physiol. 2000; 278: F540-553.
49. Kaufman J, Tyagi P, Chancellor MB. Intravesical liposomal (LP09) instillation protects bladder urothelium from chemical irritation. Am. Urol. Assoc. 2009; 182: 1506.
50. Nirmal J, Tyagi P, Dang L etal. Endocytosis uptake of liposomes in urothelium cells detected by transmission electron microscopy. Am. Urol. Assoc. 2012; 187: 1202359.
51. Peters KM, Hasenau DL, Anthony M, Kaufman J, Killinger KA, Chancellor MB. Novel therapy with intravesical liposomes for ulcerative interstitial cystitis/painful bladder syndrome. LUTS 2012; 4: 51-53.
52. Bonfiglio JJ, Inda C, Refojo D, Holsboer F, Arzt E, Silberstein S. The corticotropin-releasing hormone network and the hypothalamic-pituitary-adrenal axis: molecular and cellular mechanisms involved. Neuroendocrinology 2011; 94: 12-20.
53. Larauche M, Mulak A, Tache Y. Stress and visceral pain: from animal models to clinical therapies. Exp. Neurol. 2012; 233: 49-67.
54. Chang L, Sundaresh S, Elliott J etal. Dysregulation of the hypothalamic-pituitary-adrenal (HPA) axis in irritable bowel syndrome. Neurogastroenterol. Motil. 2009; 21: 149-159.
55. Hendrix S. Neuroimmune communication in skin: far from peripheral. J. Invest. Dermatol. 2008; 128: 260-261.
56. Aberg KM, Radek KA, Choi EH etal. Psychological stress downregulates epidermal antimicrobial peptide expression and increases severity of cutaneous infections in mice. J. Clin. Invest. 2007; 117: 3339-3349.
57. Anderson G, Palermo J, Schilling J, Roth R, Heuser J, Hultgren S. Intracellular bacterial biofilm-like pods in urinary tract infections. Science 2003; 301: 105-107.
58. Schilling J, Hultgren S. Recent advances into the pathogenesis of recurrent urinary tract infections: the bladder as a reservoir for uropathogenic Escherichia coli. Int. J. Antimicrob. Agents 2002; 19: 457-560.
59. Feneley RSL, Kunin CM, Stickler DJ. An indwelling urinary catheter for the 21st century. BJU Int. 2011; 109: 1746-1749.
60. Thumbikat P, Berry RE, Zhou G etal. Bacteria-induced uroplakin signaling mediates bladder response to infection. PLoS Pathog. 2009; 5: 1-17.
61. Rudick CN, Billips BK, Pavlov VI, Yaggie RE, Schaeffer AJ, Klumpp DJ. Host-pathogen interactions mediating pain of urinary tract infection. J. Infect. Dis. 2010; 201: 1240-1249.
62. Birder LA, Nakamura Y, Kiss S etal. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat. Neurosci. 2002; 5: 856-860.
63. Jen PY, Dixon JS, Gosling JA. Immunohistochemical localization of neuromarkers and neuropeptides in human fetal and neonatal urinary bladder. Br. J. Urol. 1995; 75: 230-235.
64. Grol S, van Koeveringe GA, de Vente J, van Kerrebroeck PE, Gillespie JI. Regional differences in sensory innervation and suburothelial interstitial cells in the bladder neck and urethra. BJU Int. 2008; 102: 870-877.
65. Birder LA, Ruggieri M, Takeda M etal. How does the urothelium affect bladder function in health and disease? Neurourol. Urodyn. 2012; 31: 293-299.
66. Birder LA, DeGroat WC. Mechanisms of disease: involvement of the urothelium in bladder dysfunction. Nat. Clin. Pract. 2007; 4: 46-54.
67. Apodaca G, Balestreire E, Birder LA. The uroepithelial-associated sensory web. Kidney Int. 2007; 72: 1057-1064.
68. Ikeda Y, Fry C, Hayashi F, Stolz D, Griffiths D, Kanai A. Role of gap junctions in spontaneous activity of the rat bladder. Am. J. Physiol. 2007; 293: F1018-1025.
69. Ikeda Y, Kanai A. Urotheliogenic modulation of intrinsic activity in spinal cord-transected rat bladders: role of mucosal muscarinic receptors. Am. J. Physiol. 2008; 295: F454-461.
70. Fry CH, Young JS, Jabr RI, McCarthy C, Ikeda Y, Kanai AJ. Modulation of spontaneous activity in the overactive bladder: the role of P2Y agonists. Am. J. Physiol. 2012; 302: F1447-1454.
71. Arrighi N, Bodei S, Peroni A etal. Detection of muscarinic receptor subtypes in human urinary bladder mucosa: age and gender-dependent modifications. Neurourol. Urodyn. 2008; 27: 421-428.
72. Bschleipfer T, Schukowski K, Weidner W etal. Expression and distribution of cholinergic receptors in the human urothelium. Life Sci. 2007; 80: 2303-2307.
73. Grol S, Essers PB, van Koeveringe GA, Martinez-Martinez P, de Vente J, Gillespie JI. M3 muscarinic receptor expression on suburothelial interstitial cells. BJU Int. 2009; 104: 398-405.
74. Mansfield KJ, Liu L, Mitchelson FJ, Moore KH, Millard RJ, Burcher E. Muscarinic receptor subtypes in human bladder detrusor and mucosa, studied by radioligand binding and quantitative competitive RT-PCR: changes in aging. Br. J. Pharmacol. 2005; 144: 1089-1099.
75. Mukerji G, Yiangou Y, Grogono J etal. Localization of M2 and M3 muscarinic receptors in human bladder disorders and their clinical correlations. J. Urol. 2006; 176: 367-373.
76. Hawthorn MH, Chapple CR, Cock M, Chess-Williams R. Urothelium-derived inhibitory factor(s) influences on detrusor muscle contractility in vitro. Br. J. Pharmacol. 2000; 129: 416-419.
77. Chess-Williams R. Muscarinic receptors of the urinary bladder: detrusor, urothelial and prejunctional. Auton. Autacoid Pharmacol. 2002; 22: 133-145.
78. Andersson KE, Persson K. Nitric oxide synthase and the lower urinary tract: possible implications for physiology and pathophysiology. Scand. J. Urol. Nephrol. 1995; 175: 43-53.
79. Birder LA, Nealen ML, Kiss S etal. Beta-adrenoceptor agonists stimulate endothelial nitric oxide synthase in rat urinary bladder urothelial cells. J. Neurosci. 2002; 22: 8063-8070.
80. Pandita RK, Mizusawa H, Andersson KE. Intravesical oxyhemoglobin initiates bladder overactivity in conscious, normal rats. J. Urol. 2000; 164: 545-550.
81. Ford AP, Cockayne DA. ATP and P2X purinoceptors in urinary tract disorders. Handb. Exp. Pharmacol. 2011; 202: 485-526.
82. Burnstock G. Targeting the visceral purinergic system for pain control. Curr. Opin. Pharmacol. 2012; 12: 80-86.
83. Burnstock G. Purinergic signalling: past, present and future. Braz. J. Med. Biol. Res. 2009; 42: 3-8.
84. Burnstock G. Purine-mediated signalling in pain and visceral perception. Trends Pharmacol. Sci. 2001; 22: 182-188.
85. Folkerts G, Nijkamp FP. Airway epithelium: more than just a barrier. Trends Pharmacol. Sci. 1998; 19: 334-241.
86. Kummer W, Wiegand S, Akinci S etal. Role of acetylcholine and muscarinic receptors in serotonin-induced bronchoconstriction in the mouse. J. Mol. Neurosci. 2006; 30: 67-68.
87. Lumpkin EA, Caterina MJ. Mechanisms of sensory transduction in the skin. Nature 2007; 445: 858-865.
88. Brunet LJ, Gold GH, Ngai J. General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 1996; 17: 681-683.
89. Bosse Y, Pare PD, Seow CY. Airway wall remodeling in asthma: from the epithelial layer to the adventitia. Curr. Allergy Asthma Rep. 2008; 8: 357-366.
90. van de Merwe JP. Interstitial cystitis and systemic autoimmune diseases. Nat. Clin. Pract. Urol. 2007; 4: 484-491.
91. Buffington CA. Comorbidity of interstitial cystitis with other unexplained clinical conditions. J. Urol. 2004; 172: 1242-1248.