Nitric oxide pathway and female lower urinary tract. Physiological and pathophysiological role

Progres en Urologie

Volumn 23, Issue 11, 2013, Pages 926-935

  Game X ^a   Rischmann, P ^a   Arnal, J F ^a   Malavaud, B ^a  

^a CHU RANGUEIL   (France)

Author keywords

Bladder; Lower urinary tract; Nitric oxide; Urethra; Women

Indexed keywords

BIOLOGICAL MARKER; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NOS1 PROTEIN, HUMAN; NOS3 PROTEIN, HUMAN; PHOSPHODIESTERASE;

BAS APPAREIL URINAIRE; BIOSYNTHESIS; BLADDER; BLADDER OBSTRUCTION; ENZYMOLOGY; FEMALE; FEMME; HUMAN; INNERVATION; METABOLISM; MONOXYDE D'AZOTE; OVERACTIVE BLADDER; PATHOPHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; URÈTRE; URETHRA; URINARY TRACT; URINARY TRACT FUNCTION; URINARY TRACT INFECTION; URINE INCONTINENCE; VESSIE;

BAS APPAREIL URINAIRE; BLADDER; FEMME; LOWER URINARY TRACT; MONOXYDE D'AZOTE; NITRIC OXIDE; URÈTRE; URETHRA; VESSIE; WOMEN;

BIOLOGICAL MARKERS; FEMALE; HUMANS; METABOLIC NETWORKS AND PATHWAYS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORIC DIESTER HYDROLASES; SIGNAL TRANSDUCTION; URETHRA; URINARY BLADDER; URINARY BLADDER NECK OBSTRUCTION; URINARY BLADDER, OVERACTIVE; URINARY INCONTINENCE; URINARY TRACT; URINARY TRACT INFECTIONS; URINARY TRACT PHYSIOLOGICAL PHENOMENA; BIOMARKERS;

EID: 84883492151     PISSN: 11667087     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.purol.2013.07.005     Document Type: Short Survey

References (101)

1. Furchgott R.F., Zawadzki J.V. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 1980, 288:373-376.
2. Ignarro L.J., Buga G.M., Wood K.S., Byrns R.E., Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 1987, 84:9265-9269.
3. Giuliano F. Le traitement per os des troubles de l'erection. Prog Urol 1997, 7:108-109.
4. Giuliano F., Uckert S., Maggi M., Birder L., Kissel J., Viktrup L. The mechanism of action of phosphodiesterase type 5inhibitors in the treatment of lower urinary tract symptoms related to benign prostatic hyperplasia. Eur Urol 2013, 63:506-516.
5. Andrew P.J., Mayer B. Enzymatic function of nitric oxide synthases. Cardiovasc Res 1999, 43:521-531.
6. Tomita T., Ogura T., Tsuyama S., Imai Y., Kitagawa T. Effects of GTP on bound nitric oxide of soluble guanylate cyclase probed by resonance Raman spectroscopy. Biochemistry 1997, 36:10155-10160.
7. Lucas K.A., Pitari G.M., Kazerounian S., Ruiz-Stewart I., Park J., Schulz S., et al. Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev 2000, 52:375-414.
8. Wu G., Morris S.M. Arginine metabolism: nitric oxide and beyond. Biochem J 1998, 336(Pt 1):1-17.
9. Komalavilas P., Lincoln T.M. Phosphorylation of the inositol 1,4,5-trisphosphate receptor by cyclic GMP-dependent protein kinase. J Biol Chem 1994, 269:8701-8707.
10. Komori K., Suzuki H. Electrical responses of smooth muscle cells during cholinergic vasodilation in the rabbit saphenous artery. Circ Res 1987, 61:586-593.
11. Woodrum D.A., Brophy C.M. The paradox of smooth muscle physiology. Mol Cell Endocrinol 2001, 177:135-143.
12. Juilfs D.M., Soderling S., Burns F., Beavo J.A. Cyclic GMP as substrate and regulator of cyclic nucleotide phosphodiesterases (PDEs). Rev Physiol Biochem Pharmacol 1999, 135:67-104.
13. Kim S.O., Merchant K., Nudelman R., Beyer W.F., Keng T., DeAngelo J., et al. OxyR: a molecular code for redox-related signaling. Cell 2002, 109:383-396.
14. Davis K.L., Martin E., Turko I.V., Murad F. Novel effects of nitric oxide. Ann Rev Pharmacol Toxicol 2001, 41:203-236.
15. Virag L., Szabo E., Gergely P., Szabo C. Peroxynitrite-induced cytotoxicity: mechanism and opportunities for intervention. Toxicol Lett 2003, 140-141:113-124.
16. Lanone S., Manivet P., Callebert J., Launay J.M., Payen D., Aubier M., et al. Inducible nitric oxide synthase (NOS2) expressed in septic patients is nitrated on selected tyrosine residues: implications for enzymic activity. Biochem J 2002, 366:399-404.
17. Gunther M.R., Hsi L.C., Curtis J.F., Gierse J.K., Marnett L.J., Eling T.E., et al. Nitric oxide trapping of the tyrosyl radical of prostaglandin H synthase-2leads to tyrosine iminoxyl radical and nitrotyrosine formation. J Biol Chem 1997, 272:17086-17090.
18. Goodwin D.C., Gunther M.R., Hsi L.C., Crews B.C., Eling T.E., Mason R.P., et al. Nitric oxide trapping of tyrosyl radicals generated during prostaglandin endoperoxide synthase turnover. Detection of the radical derivative of tyrosine 385. J Biol Chem 1998, 273:8903-8909.
19. Ho K.M., Ny L., McMurray G., Andersson K.E., Brading A.F., Noble J.G. Co-localization of carbon monoxide and nitric oxide synthesizing enzymes in the human urethral sphincter. J Urol 1999, 161:1968-1972.
20. Vizzard M.A., Erdman S.L., Forstermann U., de Groat W.C. Differential distribution of nitric oxide synthase in neural pathways to the urogenital organs (urethra, penis, urinary bladder) of the rat. Brain Res 1994, 646:279-291.
21. Keast J.R., Kawatani M. Extensive distribution of NADPH diaphorase activity in the nerve supply of the cat lower urinary tract. J Auton Nerv Syst 1994, 50:161-169.
22. Persson K., Alm P., Johansson K., Larsson B., Andersson K.E. Nitric oxide synthase in pig lower urinary tract: immunohistochemistry. NADPH diaphorase histochemistry and functional effects. Br J Pharmacol 1993, 110:521-530.
23. Gillespie J.I., Markerink-van Ittersum M., de Vente J. Expression of neuronal nitric oxide synthase (nNOS) and nitric-oxide-induced changes in cGMP in the urothelial layer of the guinea pig bladder. Cell Tissue Res 2005, 321:341-351.
24. Lyons A.D., Gardiner T.A., McCloskey K.D. Kit-positive interstitial cells in the rabbit urethra: structural relationships with nerves and smooth muscle. BJU Int 2007, 99:687-694.
25. Ho K.M., Borja M.C., Persson K., Brading A.F., Andersson K.E. Expression of nitric oxide synthase immunoreactivity in the human female intramural striated urethral sphincter. J Urol 2003, 169:2407-2411.
26. Gonzalez-Soriano J., Martin-Palacios S., Rodriguez-Veiga E., Triguero D., Costa G., Garcia-Pascual A. Nitric oxide synthase in the external urethral sphincter of the sheep: immunohistochemical and functional study. J Urol 2003, 169:1901-1906.
27. Burnett A.L., Calvin D.C., Chamness S.L., Liu J.X., Nelson R.J., Klein S.L., et al. Urinary bladder-urethral sphincter dysfunction in mice with targeted disruption of neuronal nitric oxide synthase models idiopathic voiding disorders in humans. Nat Med 1997, 3:571-574.
28. Kim S.O., Song S.H., Hwang E.C., Park K.S., Kwon D.D., Ahn K.Y., et al. The expression of AQP1and eNOS in menopausal rat urinary bladder. Int Neurourol J 2010, 14:78-85.
29. Pace G., Palumbo P., Miconi G., Silvestri V., Cifone M.G., Vicentini C. PDE-5and NOS II mRNA expression in menopausal women: a molecular biology study. World J Urol 2011, 29:243-248.
30. Gamé X., Allard J., Escourrou G., Gourdy P., Tack I., Rischmann P., et al. Estradiol increases urethral tone through the local inhibition of neuronal nitric oxide synthase expression. Am J Physiol Regul Integr Comp Physiol 2008, 294:R851-R857.
31. Sandes E.O., Faletti A.G., Riveros M.D., Vidal Mdel C., Gimenez L., Casabe A.R., et al. Expression of inducible nitric oxide synthase in tumoral and non-tumoral epithelia from bladder cancer patients. Nitric Oxide 2005, 12:39-45.
32. Johansson R., Pandita R.K., Poljakovic M., Garcia-Pascual A., De Vente J., Persson K. Activity and expression of nitric oxide synthase in the hypertrophied rat bladder and the effect of nitric oxide on bladder smooth muscle growth. J Urol 2002, 168:2689-2694.
33. Kim S.O., Oh B.S., Chang I.Y., Song S.H., Ahn K., Hwang E.C., et al. Distribution of interstitial cells of Cajal and expression of nitric oxide synthase after experimental bladder outlet obstruction in a rat model of bladder overactivity. Neurourol Urodyn 2011, 30:1639-1645.
34. Johansson R.K., Poljakovic M., Andersson K.E., Persson K. Expression of nitric oxide synthase in bladder smooth muscle cells: regulation by cytokines and L-arginine. J Urol 2002, 168:2280-2285.
35. Olsson L.E., Wheeler M.A., Sessa W.C., Weiss R.M. Bladder instillation and intraperitoneal injection of Escherichia coli lipopolysaccharide up-regulate cytokines and iNOS in rat urinary bladder. J Pharmacol Exp Ther 1998, 284:1203-1208.
36. Kang W.S., Tamarkin F.J., Wheeler M.A., Weiss R.M. Rapid up-regulation of endothelial nitric-oxide synthase in a mouse model of Escherichia coli lipopolysaccharide-induced bladder inflammation. J Pharmacol Exp Ther 2004, 310:452-458.
37. Koskela L.R., Thiel T., Ehren I., De Verdier P.J., Wiklund N.P. Localization and expression of inducible nitric oxide synthase in biopsies from patients with interstitial cystitis. J Urol 2008, 180:737-741.
38. Lundberg J.O., Ehren I., Jansson O., Adolfsson J., Lundberg J.M., Weitzberg E., et al. Elevated nitric oxide in the urinary bladder in infectious and noninfectious cystitis. Urology 1996, 48:700-702.
39. Ehren I., Hosseini A., Lundberg J.O., Wiklund N.P. Nitric oxide: a useful gas in the detection of lower urinary tract inflammation. J Urol 1999, 162:327-329.
40. Minardi D., Ghiselli R., Lucarini G., Mocchegiani F., Filosa A., Zizzi A., et al. Activity and expression of nitric oxide synthase in rat bladder after sacral neuromodulation. Int J Immunopathol Pharmacol 2008, 21:129-135.
41. Truss M.C., Uckert S., Stief C.G., Forssmann W.G., Jonas U. Cyclic nucleotide phosphodiesterase (PDE) isoenzymes in the human detrusor smooth muscle II. Effect of various PDE inhibitors on smooth muscle tone and cyclic nucleotide levels in vitro. Urol Res 1996, 24:129-134.
42. Qiu Y., Kraft P., Craig E.C., Liu X., Haynes-Johnson D. Identification and functional study of phosphodiesterases in rat urinary bladder. Urol Res 2001, 29:388-392.
43. Werkstrom V., Svensson A., Andersson K.E., Hedlund P. Phosphodiesterase 5in the female pig and human urethra: morphological and functional aspects. BJU Int 2006, 98:414-423.
44. Theobald R.J. The effect of NG-monomethyl-L-arginine on bladder function. Eur J Pharmacol 1996, 311:73-78.
45. Yanai Y., Hashitani H., Hayase M., Sasaki S., Suzuki H., Kohri K. Role of nitric oxide/cyclic GMP pathway in regulating spontaneous excitations in detrusor smooth muscle of the guinea-pig bladder. Neurourol Urodyn 2008, 27:446-453.
46. Sutherland R.S., Kogan B.A., Piechota H.J., Bredt D.S. Vesicourethral function in mice with genetic disruption of neuronal nitric oxide synthase. J Urol 1997, 157:1109-1116.
47. Andersson K.E., Persson K. Nitric oxide synthase and the lower urinary tract: possible implications for physiology and pathophysiology. Scand J Urol Nephrol Suppl 1995, 175:43-53.
48. Moon A. Influence of nitric oxide signalling pathways on pre-contracted human detrusor smooth muscle in vitro. BJU Int 2002, 89:942-949.
49. Birder L.A., Nealen M.L., Kiss S., de Groat W.C., Caterina M.J., Wang E., et al. Beta-adrenoceptor agonists stimulate endothelial nitric oxide synthase in rat urinary bladder urothelial cells. J Neurosci 2002, 22:8063-8070.
50. Birder L.A., Apodaca G., De Groat W.C., Kanai A.J. Adrenergic- and capsaicin-evoked nitric oxide release from urothelium and afferent nerves in urinary bladder. Am J Physiol 1998, 275:F226-F229.
51. Birder L.A., Kanai A.J., de Groat W.C. DMSO: effect on bladder afferent neurons and nitric oxide release. J Urol 1997, 158:1989-1995.
52. Munoz A., Gangitano D.A., Smith C.P., Boone T.B., Somogyi G.T. Removal of urothelium affects bladder contractility and release of ATP but not release of NO in rat urinary bladder. BMC Urol 2010, 10:10.
53. Gillespie J.I., Markerink-van Ittersum M., De Vente J. Endogenous nitric oxide/cGMP signalling in the guinea pig bladder: evidence for distinct populations of sub-urothelial interstitial cells. Cell Tissue Res 2006, 325:325-332.
54. Lagou M., Drake M.J., Markerink V., Dev J., Gillespie J.I. Interstitial cells and phasic activity in the isolated mouse bladder. BJU Int 2006, 98:643-650.
55. Caremel R., Oger-Roussel S., Behr-Roussel D., Grise P., Giuliano F.A. Nitric oxide/cyclic guanosine monophosphate signalling mediates an inhibitory action on sensory pathways of the micturition reflex in the rat. Eur Urol 2010, 58:616-625.
56. Masuda H., Kim J.H., Kihara K., Chancellor M.B., de Groat W.C., Yoshimura N. Inhibitory roles of peripheral nitrergic mechanisms in capsaicin-induced detrusor overactivity in the rat. BJU Int 2007, 100:912-918.
57. Aizawa N., Igawa Y., Nishizawa O., Wyndaele J.J. Effects of nitric oxide on the primary bladder afferent activities of the rat with and without intravesical acrolein treatment. Eur Urol 2011, 59:264-271.
58. Pontari M.A., Ruggieri M.R. Sex differences and role of nitric oxide in blood flow of canine urinary bladder. Am J Physiol 1999, 276:R407-R413.
59. Lieb J., Kogan B., Das A.K., Leggett R.E., Schroder A., Levin R.M. The effect of urine volume and nitric oxide on basal bladder blood flow: response to catheterization and drainage. Neurourol Urodyn 2001, 20:115-124.
60. Oter S., Korkmaz A., Oztas E., Yildirim I., Topal T., Bilgic H. Inducible nitric oxide synthase inhibition in cyclophosphamide induced hemorrhagic cystitis in rats. Urol Res 2004, 32:185-189.
61. Tyagi P., Tyagi V., Yoshimura N., Witteemer E., Barclay D., Loughran P.A., et al. Gender-based reciprocal expression of transforming growth factor-beta1and the inducible nitric oxide synthase in a rat model of cyclophosphamide-induced cystitis. J Inflamm (Lond) 2009, 6:23.
62. Johansson R., Persson K. Phenotypic modulation of cultured bladder smooth muscle cells and the expression of inducible nitric oxide synthase. Am J Physiol Regul Integr Comp Physiol 2004, 286:R642-R648.
63. Ozawa H., Chancellor M.B., Jung S.Y., Yokoyama T., Fraser M.O., Yu Y., et al. Effect of intravesical nitric oxide therapy on cyclophosphamide-induced cystitis. J Urol 1999, 162:2211-2216.
64. Hosseini A., Ehren I., Wiklund N.P. Nitric oxide as an objective marker for evaluation of treatment response in patients with classic interstitial cystitis. J Urol 2004, 172:2261-2265.
65. Li K., Yao J., Shi L., Sawada N., Chi Y., Yan Q., et al. Reciprocal regulation between proinflammatory cytokine-induced inducible NO synthase (iNOS) and connexin43in bladder smooth muscle cells. J Biol Chem 2011, 286:41552-41562.
66. Wang Z., Humphrey C., Frilot N., Wang G., Nie Z., Moniri N.H., et al. Dynamin2- and endothelial nitric oxide synthase-regulated invasion of bladder epithelial cells by uropathogenic Escherichia coli. J Cell Biol 2011, 192:101-110.
67. Sasatomi K., Hiragata S., Miyazato M., Chancellor M.B., Morris S.M., Yoshimura N. Nitric oxide-mediated suppression of detrusor overactivity by arginase inhibitor in rats with chronic spinal cord injury. Urology 2008, 72:696-700.
68. Smith C.P., Gangitano D.A., Munoz A., Salas N.A., Boone T.B., Aoki K.R., et al. Botulinum toxin type A normalizes alterations in urothelial ATP and NO release induced by chronic spinal cord injury. Neurochem Int 2008, 52:1068-1075.
69. Behr-Roussel D., Oger S., Caisey S., Sandner P., Bernabe J., Alexandre L., et al. Vardenafil decreases bladder afferent nerve activity in unanesthetized, decerebrate, spinal cord-injured rats. Eur Urol 2011, 59:272-279.
70. Lemack G.E., Zimmern P.E., Vazquez D., Connell J.D., Lin V.K. Altered response to partial bladder outlet obstruction in mice lacking inducible nitric oxide synthase. J Urol 2000, 163:1981-1987.
71. Shabsigh A., Hayek O.R., Weiner D., Saidi J., Kaplan S.A., Kiss A., et al. Acute increase in blood flow to the rat bladder subsequent to partial bladder outlet obstruction. Neurourol Urodyn 2000, 19:195-206. [discussion 206-8].
72. Dokita S., Morgan W.R., Wheeler M.A., Yoshida M., Latifpour J., Weiss R.M. NG-nitro-L-arginine inhibits non-adrenergic, non-cholinergic relaxation in rabbit urethral smooth muscle. Life Sci 1991, 48:2429-2436.
73. Bustamante S., Orensanz L.M., Recio P., Carballido J., Garcia-Sacristan A., Prieto D., et al. Functional evidence of nitrergic neurotransmission in the human urinary bladder neck. Neurosci Lett 2010, 477:91-94.
74. Takeda M., Lepor H. Nitric oxide synthase in dog urethra: a histochemical and pharmacological analysis. Br J Pharmacol 1995, 116:2517-2523.
75. Werkstrom V., Persson K., Ny L., Bridgewater M., Brading A.F., Andersson K.E. Factors involved in the relaxation of female pig urethra evoked by electrical field stimulation. Br J Pharmacol 1995, 116:1599-1604.
76. Garcia-Pascual A., Sancho M., Costa G., Triguero D. Interstitial cells of Cajal in the urethra are cGMP-mediated targets of nitrergic neurotransmission. Am J Physiol Renal Physiol 2008, 295:F971-F983.
77. Wai C.Y., Liehr P., Tibbals H.F., Sager M., Schaffer J.I., Word R.A. Effect of periurethral denervation on function of the female urethra. Am J Obstet Gynecol 2003, 189:1637-1645.
78. Kontani H., Shiraoya C. Sex differences in urethral pressure response to electrical stimulation of the hypogastric nerves in rats. J Urol 2000, 163:1364-1368.
79. Yoshida M., Akaike T., Inadome A., Takahashi W., Seshita H., Yono M., et al. The possible effect of nitric oxide on relaxation and noradrenaline release in the isolated rabbit urethra. Eur J Pharmacol 1998, 357:213-219.
80. Seshita H., Yoshida M., Takahashi W., Inadome A., Yono M., Miyamoto Y., et al. Prejunctional alpha-adrenoceptors regulate nitrergic neurotransmission in the rabbit urethra. Eur J Pharmacol 2000, 400:271-278.
81. Garcia-Pascual A., Costa G., Labadia A., Jimenez E., Triguero D., Rodriguez-Veiga E., et al. Partial nicotinic receptor blockade unmasks a modulatory role of nitric oxide on urethral striated neuromuscular transmission. Nitric Oxide 2005, 13:98-110.
82. Wibberley A., Chen Z., Hu E., Hieble J.P., Westfall T.D. Expression and functional role of Rho-kinase in rat urinary bladder smooth muscle. Br J Pharmacol 2003, 138:757-766.
83. Muntener M., Schurch B., Wefer B., Reitz A. Systemic nitric oxide augmentation leads to a rapid decrease of the bladder outlet resistance in healthy men. Eur Urol 2006, 50:112-118.
84. Gamé X., Bouali O., Allard J., Gourdy P., Escourrou G., Tack I., et al. Influence of sildenafil on micturition and urethral tone in ovariectomized and non-ovariectomized mice. J Sex Med 2012, 9:466-471.
85. Masuda H., Tsujii T., Okuno T., Kihara K., Goto M., Azuma H. Involvement of accumulated endogenous NOS inhibitors and decreased NOS activity in the impaired neurogenic relaxation of the rabbit proximal urethra with ischaemia. Br J Pharmacol 2001, 133:97-106.
86. Yang Z., Dolber P.C., Fraser M.O. Diabetic urethropathy compounds the effects of diabetic cystopathy. J Urol 2007, 178:2213-2219.
87. Bossowska A., Crayton R., Radziszewski P., Kmiec Z., Majewski M. Distribution and neurochemical characterization of sensory dorsal root ganglia neurons supplying porcine urinary bladder. J Physiol Pharmacol 2009, 60(Suppl 4):77-81.
88. Yoshimura N., Seki S., de Groat W.C. Nitric oxide modulates Ca(2+) channels in dorsal root ganglion neurons innervating rat urinary bladder. J Neurophysiol 2001, 86:304-311.
89. Zhou Y., Ling E.A. Neuronal nitric oxide synthase in the neural pathways of the urinary bladder. J Anat 1999, 194(Pt 4):481-496.
90. Morrison J.F., Sato A., Sato Y., Suzuki A. The nitric oxide synthase inhibitor L-NAME reduces inhibitory components of somato-vesical parasympathetic reflexes in the rat. Neurosci Res 1996, 24:195-199.
91. Bennett B.C., Kruse M.N., Roppolo J.R., Flood H.D., Fraser M., de Groat W.C. Neural control of urethral outlet activity in vivo: role of nitric oxide. J Urol 1995, 153:2004-2009.
92. Jung S.Y., Fraser M.O., Ozawa H., Yokoyama O., Yoshiyama M., De Groat W.C., et al. Urethral afferent nerve activity affects the micturition reflex; implication for the relationship between stress incontinence and detrusor instability. J Urol 1999, 162:204-212.
93. Zhang F., Liao L., Ju Y., Song A., Liu Y. Neurochemical plasticity of nitric oxide synthase isoforms in neurogenic detrusor overactivity after spinal cord injury. Neurochem Res 2011, 36:1903-1909.
94. Kakizaki H., de Groat W.C. Reorganization of somato-urethral reflexes following spinal cord injury in the rat. J Urol 1997, 158:1562-1567.
95. Zvara P., Folsom J.B., Kliment J., Dattilio A.L., Moravcikova A., Plante M.K., et al. Increased expression of neuronal nitric oxide synthase in bladder afferent cells in the lumbosacral dorsal root ganglia after chronic bladder outflow obstruction. Brain Res 2004, 1002:35-42.
96. Kodama K., Yokoyama O., Komatsu K., Yotsuyanagi S., Niikura S., Namiki M. Contribution of cerebral nitric oxide to bladder overactivity after cerebral infarction in rats. J Urol 2002, 167:391-396.
97. Bossowska A., Majewski M. Botulinum toxin type A-induced changes in the chemical coding of dorsal root ganglion neurons supplying the porcine urinary bladder. Pol J Vet Sci 2012, 15:345-353.
98. Bossowska A., Majewski M. Conantokin G-induced changes in the chemical coding of dorsal root ganglion neurons supplying the porcine urinary bladder. Pol J Vet Sci 2012, 15:101-109.
99. Bossowska A., Majewski M. The influence of resiniferatoxin on the chemical coding of neurons in dorsal root ganglia supplying the urinary bladder in the female pig. Pol J Vet Sci 2012, 15:135-142.
100. Burlinski P.J., Gonkowski S., Calka J. Tetrodotoxin- and resiniferatoxin-induced changes in paracervical ganglion ChAT- and nNOS-IR neurons supplying the urinary bladder in female pigs. Acta Vet Hung 2011, 59:455-463.
101. Bossowska A., Majewski M. Tetrodotoxin induced changes in the chemical coding of dorsal root ganglion neurons supplying the porcine urinary bladder. Pol J Vet Sci 2012, 15:355-363.