Changes in chemical coding of sympathetic chain ganglia (SChG) neurons supplying porcine urinary bladder after botulinum toxin (BTX) treatment

Springer Science and Business Media LLC - Tập 360 - Trang 263-272 - 2015
E. Lepiarczyk1, A. Bossowska1, M. Majewski1
1Department of Human Physiology, Faculty of Medical Sciences, University of Warmia and Mazury in Olsztyn, Olsztyn, Poland

Tóm tắt

Botulinum toxin (BTX) is a neurotoxin used in medicine as an effective drug in experimental therapy of neurogenic urinary bladder disorders. We have investigated the influence of BTX on the chemical coding of sympathetic chain ganglia (SChG) neurons supplying the porcine urinary bladder. The toxin was injected into the wall of the bladder. SChG neurons were visualized by a retrograde tracing method with fluorescent tracer fast blue (FB) and their chemical coding was investigated by double-labelling immunohistochemistry with antibodies against dopamine β-hydroxylase (DβH; a marker of noradrenergic neurons), neuropeptide Y (NPY), vasoactive intestinal polypeptide (VIP), somatostatin (SOM), galanin (GAL), Leu5-enkephalin (L-ENK) and neuronal nitric oxide synthase (nNOS). In both the control (n = 5) and BTX-treated pigs (n = 5), the vast majority (91 ± 2.3 % and 89.8 ± 2.5 %, respectively) of FB-positive (FB+) nerve cells were DβH+. BTX injections caused a decrease in the number of FB+/DβH+ neurons that were immunopositive to NPY (39.5 ± 4.5 % vs 74.5 ± 11.9 %), VIP (8.9 ± 5.3 % vs 22.3 ± 8.8 %), SOM (5.8 ± 2.3 % vs 17.4 ± 3.7 %) or GAL (0.9 ± 1.2 % vs 5.4 ± 4.4 %) and a distinct increase in the number of FB+/DβH+ neurons that were immunoreactive to L-ENK (3.7 ± 2.9 % vs 1.1 % ± 0.8 %) or nNOS (7.7 ± 3.5 % vs 0.8 ± 0.6 %). Our study provides novel evidence that the therapeutic effects of BTX on the mammalian urinary bladder are partly mediated by SChG neurons.

Tài liệu tham khảo

Andersson KE, Arner A (2004) Urinary bladder contraction and relaxation: physiology and pathophysiology. Physiol Rev 84:935–986 Apostolidis A, Popat R, Yiangou Y, Cockayne D, Ford AP, Davis JB, Dasgupta P, Fowler CJ, Anand P (2005) Decreased sensory receptor P2X3 and TRPV1 in suburothelial nerve fibers following intradetrusor injections of botulinum toxin for human detrusor overactivity. J Urol 174:977–983 Bitran M, Torres G, Tapia W, Huidobro-Toro JP (1996) Neuropeptide Y inhibits 3[H]noradrenaline release in the rat vas deferens independently of cAMP levels. Neurochem Int 28:309–317 Bossowska A, Majewski M (2012) Botulinum toxin type A-induced changes in the chemical coding of dorsal root ganglion neurons supplying the porcine urinary bladder. Pol J Vet Sci 15:345–353 Bossowska A, Crayton R, Radziszewski P, Kmiec Z, Majewski M (2009) Distribution and neurochemical characterization of sensory dorsal root ganglia neurons supplying porcine urinary bladder. J Physiol Pharmacol 4:77–81 Bråtveit M, Helle KB (1991) Inhibition by VIP and atriopeptin II on the field stimulation evoked release of [3H]noradrenaline in the rat portal vein. Regul Pept 33:331–337 Burnett AL (1995) Nitric oxide control of lower genitourinary tract functions: a review. Urology 45:1071–1083 Calhau C, Martel F, Moura D, Azevedo I (2000) Somatostatin inhibits the release of noradrenaline induced by electrical stimulation of the rat mesenteric artery. Pharmacol Res 41:497–501 Carruthers J, Carruthers A (2004) Botox beyond wrinkles. Clin Dermatol 22:89–93 Chernaeva L, Charakchieva S (1988) Leucine-enkephalin- and neuropeptide Y-modulation of [3H]noradrenaline release in the oviduct of mature and juvenile rabbits. Gen Pharmacol 19:137–142 Chien CH, Li SH, Shen CL (1991) The ovarian innervation in the dog: a preliminary study for the base for electro-acupuncture. J Auton Nerv Syst 35:185–192 Collins VM, Daly DM, Liaskos M, McKay NG, Snellers D, Chapple C, Grundy D (2013) OnabotulinumtoxinA significantly attenuates bladder afferent nerve firing and inhibits ATP release from the urothelium. BJU Int 112:1018–1026 Crayton R, Soller W, Mattiasson A, Bossowska A, Borkowski T, Majewski M, Radziszewski P (2010) Exogenously administered opioids contract the female rat intrinsic urethral sphincter in vivo. Neurourol Urodyn 29:777–782 Cruz F, Herschorn S, Aliotta P, Brin M, Thompson C, Lam W, Daniell G, Heesakkers J, Haag-Molkenteller C (2011) Efficacy and safety of onabotulinumtoxinA in patients with urinary incontinence due to neurogenic detrusor overactivity: a randomised, double-blind, placebo-controlled trial. Eur Urol 60:742–750 Dalmose AL, Hvistendahl JJ, Olsen LH, Eskild-Jensen A, Djurhuus JC, Swindle MM (2000) Surgically induced urologic models in swine. J Invest Surg 13:133–145 Downie JW, Champion JA, Nance DM (1984) A quantitative analysis of the afferent and extrinsic efferent innervation of specific regions of the bladder and urethra in the cat. Brain Res Bull 12:735–740 Ermengem E van (1897) Über einen neuen anaeroben Bacillus and seine Beziehungen zum Botulismus. Z Hyg Infekt 26:1–56 Göthert M (1980) Somatostatin selectively inhibits noradrenaline release from hypothalamic neurones. Nature 288:86–88 Groat de WC, Wickens C (2013) Organization of the neural switching circuitry underlying reflex micturition. Acta Physiol (Oxf) 207:66–84 Haferkamp A, Schurch B, Reitz A, Krengel U, Grosse J, Kramer G, Schumacher S, Bastian PJ, Buttner R, Muller SC, Stohrer M (2004) Lack of ultrastructural detrusor changes following endoscopic injection of botulinum toxin type A in overactive neurogenic bladder. Eur Urol 46:784–791 Hanna-Mitchell AT, Wolf-Johnston AS, Barrick SR, Kanai AJ, Chancellor MB, Groat WC de, Birder LA (2013) Effect of botulinum toxin A on urothelial-release of ATP and expression of SNARE targets within the urothelium. Neurourol Urodyn (in press) Heym C, Webber R, Horn M, Kummer W (1990) Neuronal pathways in the guinea-pig lumbar sympathetic ganglia as revealed by immunohistochemistry. Histochemistry 93:547–557 Hill EL, Elde R (1989) Vasoactive intestinal peptide distribution and colocalization with dopamine-beta-hydroxylase in sympathetic chain ganglia of pig. J Auton Nerv Syst 27:229–239 Houdeau E, Rousseau A, Meusnier C, Prud’Homme MJ, Rousseau JP (1998) Sympathetic innervation of the upper and lower regions of the uterus and cervix in the rat have different origins and routes. J Comp Neurol 399:403–412 Iravani MM, Zar MA (1994) Presence of neuropeptide Y in the rat seminal vesicle and its effects on noradrenaline- and nerve-induced contractions. Br J Pharmacol 113:877–882 Jobling P (2011) Autonomic control of the urogenital tract. Auton Neurosci 165:113–126 Kaleczyc J, Timmermans JP, Majewski M, Łakomy M, Scheuermann DW (1995) Distribution and immunohistochemical characteristics of neurons in the porcine caudal mesenteric ganglion projecting to the vas deferens and seminal vesicle. Cell Tissue Res 282:59–68 Keast JR (1992) Location and peptide content of pelvic neurons supplying the muscle and lamina propria of the rat vas deferens. J Auton Nerv Syst 40:1–11 Kummer W (1987) Galanin- and neuropeptide Y-like immunoreactivities coexist in paravertebral sympathetic neurons of the cat. Neurosci Lett 78:127–131 Kuo HC (2013) Repeated intravesical onabotulinumtoxinA injections are effective in treatment of refractory interstitial cystitis/bladder pain syndrome. Int J Clin Pract 67:427–434 Kuzmuk KN, Schook LB (2011) Pigs as a model for biomedical sciences. In: Rothschild MF, Ruvinsky A (eds) The genetics of the pig, 2nd edn. CAB International, Wallingford, pp 426–444 Łakomy M, Häppölä O, Kaleczyc J, Majewski M (1994) Immunohistochemical localization of neuropeptides in the porcine thoracolumbar paravertebral ganglia. Anat Histol Embryol 23:12–20 Lepiarczyk E, Bossowska A, Kaleczyc J, Majewski M (2011) The influence of botulinum toxin type A (BTX) on the immunohistochemical characteristics of noradrenergic and cholinergic nerve fibers supplying the porcine urinary bladder wall. Pol J Vet Sci 14:181–189 Levin RM, Ruggieri MR, Wein AJ (1986) Functional effects of the purinergic innervation of the rabbit urinary bladder. J Pharmacol Exp Ther 236:452–457 Lowe NJ, Lowe P (2012) Botulinum toxin for facial lines: a concise review. Dermatol Ther (Heidelb) 2:14 Lundberg JM, Stjarne L (1984) Neuropeptide Y (NPY) depresses the secretion of 3H-noradrenaline and the contractile response evoked by field stimulation, in rat vas deferens. Acta Physiol Scand 120:477–479 Majewski M (1999) Synaptogenesis and structure of the autonomic ganglia. Folia Morphol (Warsz) 58:65–99 Matak I, Rossetto O, Lacković Z (2014) Botulinum toxin type A selectivity for certain types of pain is associated with capsaicin-sensitive neurons. Pain 155:1516–1526 Maynard KI, Saville VL, Burnstock G (1991) Somatostatin modulates vascular sympathetic neurotransmission in the rabbit ear artery. Eur J Pharmacol 196:125–131 Morrison J, Birder L, Craggs M, de Groat WC, Downie J, Drake M, Fowler C, Thor K (2005) Neural control. In: Abrams P, Cardozo L, Khoury S, Wein A (eds) Incontinence. Health, Jersey, pp 363–422 Persson K, Alm P, Johansson K, Larsson B, Andersson KE (1993) Nitric oxide synthase in pig lower urinary tract: immunohistochemistry, NADPH diaphorase histochemistry and functional effects. Br J Pharmacol 110:521–530 Pidsudko Z (2014) Immunohistochemical characteristics and distribution of neurons in the paravertebral, prevertebral and pelvic ganglia supplying the urinary bladder in the male pig. J Mol Neurosci 52:56–70 Pinto R, Lopes T, Silva J, Silva C, Dinis P, Cruz F (2013) Persistent therapeutic effect of repeated injections of onabotulinum toxin a in refractory bladder pain syndrome/interstitial cystitis. J Urol 189:548–553 Ragionieri L, Botti M, Gazza F, Sorteni C, Chiocchetti R, Clavenzani P, Minelli LB, Panu R (2013) Localization of peripheral autonomic neurons innervating the boar urinary bladder trigone and neurochemical features of the sympathetic komponent. Eur J Histochem 57:93–105 Rohrsted M, Nordsten CB, Bagi P (2012) Onabotulinum toxin a (botox(R)) in the treatment of neurogenic bladder overactivity. Nephro-Urol Mon 4:437–442 Santos-Silva A, Silva CM da, Cruz F (2013) Botulinum toxin treatment for bladder dysfunction. Int J Urol 20:956–962 Skobowiat C, Całka J, Majewski M (2011) Axotomy induced changes in neuron al plasticity of sympathetic chain ganglia (SChG) neurons supplying descending colon in the pig. Exp Mol Pathol 90:13–18 Smith CP, Franks ME, McNeil BK, Gosh R, Groat WC de, Chancellor MB, Somogyi GT (2003) Effect of botulinum toxin A on the autonomic nervous system of the rat lower urinary tract. J Urol 169:1896–1900 Swindle MM, Makin A, Herron AJ, Clubb FJ Jr, Frazier KS (2012) Swine as models in biomedical research and toxicology testing. Vet Pathol 49:344–356 Terai A, Matsui Y, Ichioka K, Ohara H, Terada N, Yoshimura K (2004) Comparative analysis of lower urinary tract symptoms and bother in both sexes. Urology 63:487–491 Thüroff JW, Bazeed MA, Schmidt RA, Luu DH, Tanagho EA (1982) Regional topography of spinal cord neurons innervating pelvic floor muscles and bladder neck in the dog: a study by combined horseradish peroxidase histochemistry and autoradiography. Urol Int 37:110–120 Tran LV, Somogyi GT, Groat WC de (1994) Inhibitory effect of neuropeptide Y on adrenergic and cholinergic transmission in rat urinary bladder and urethra. Am J Physiol 266:R1411–R1417 Tsuda K, Yokoo H, Goldstein M (1989) Neuropeptide Y and galanin in norepinephrine release in hypothalamic slices. Hypertension 14:81–86 Tsuda K, Tsuda S, Nishio I, Masuyama Y, Goldstein M (1992) Modulation of norepinephrine release by galanin in rat medulla oblongata. Hypertension 20:361–366 Vera PL, Nadelhaft I (1992) Afferent and sympathetic innervation of the dome and the base of the urinary bladder of the female rat. Brain Res Bull 29:651–658 Wakabayashi Y, Makiura Y, Tomoyoshi T, Kitahama K, Geffard M, Maeda T (1994) Adrenergic innervation of the urinary bladder body in the cat with special reference to structure of the detrusor muscle: an immunohistochemical study of noradrenaline and its synthesizing enzymes. Arch Histol Cytol 57:277–289 Wojtkiewicz J, Bossowska A, Zapart A, Skobowiat C, Janiuk I, Borkowski A, Radziszewski P, Majewski M (2008) Botulinum toxin (BTX)—induced changes in the chemical coding of interior mesenteric ganglion (IMG) neurons supplying porcie urinary bladder. Urol Polska 61 (Suppl 1):57–58