Botulinum toxin type A-induced changes in the chemical coding of dorsal root ganglion neurons supplying the porcine urinary bladder

• Autorzy: Bossowska A. , Majewski M.
• Języki publikacji: EN

Abstrakty

EN

Botulinum toxin type A (BTX) is a potent neurotoxin, which in recent years has been effectively applied in experimental treatments of many neurogenic disorders of the urinary bladder. BTX is a selective, presynaptically-acting blocking agent of acetylcholine release from nerve terminals what, in turn, leads to the cessation of somatic motor and/or parasympathetic transmission. However, application of this toxin in urological practice is still in the developmental stages and the full mechanism of its action remain elusive. Thus, the present study was aimed at investigating the neurochemical characterization of dorsal root ganglion (DRG) neurons supplying the porcine urinary bladder after BTX treatment. Retrograde tracer Fast Blue (FB) was injected into the urinary bladder wall in six juvenile female pigs and three weeks later, intramural bladder injections of BTX (100 IU per animal) were carried out in all the animals. After a week, DRG from L1 to Cq1 were harvested from the pigs and neurochemical characterization of FB+ neurons was performed using double-labeling immunofluorescence technique on 10-μm-thick cryostat sections. BTX injections led to a significant decrease in the number of FB+ neurons containing substance P (SP), calcitonin gene-related peptide (CGRP), calbindin (CB), somatostatin (SOM) and neuronal nitric oxide synthase (nNOS) when compared with that found in the healthy animals (19% vs. 45%, 18% vs. 36%, 0.6% vs. 3%, 0.4 vs. 4% and 0.1% vs. 6%, respectively) These data demonstrated that BTX changed the chemical coding of bladder sensory neurons, and therefore this drug should be taken into consideration when it planning experimental therapy of selected neurogenic bladder disorders.

• Wydawca: -
• Czasopismo: Polish Journal of Veterinary Sciences
• Rocznik: 2012
• Tom: 15
• Numer: 2
• Opis fizyczny: p.345-353,fig.,ref.

Twórcy

autor

Bossowska A.

• Department of Human Physiology, Faculty of Medical Sciences, University of Warmia and Mazury in Olsztyn, Poland

autor

Majewski M.

Bibliografia

• Apostolidis A, Popat R, Yiangou Y, Cockayne D, Ford AP, Davis JB, Dasgupta P, Fowler CJ, Anand P (2005) Decreased sensory receptors P2X3 and TRPV1 in suburothelial nerve fibers following intradetrusor injections of botulinum toxin for human detrusor overactivity. J Urol 174: 977-982.
• Averill S, McMahon SB, Clary DO, Reichardt LF, Priestley JV (1995) Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur J Neurosci 7: 1484-1494.
• Baimbridge KG, Celio MR, Rogers JH (1992) Calcium-binding proteins in the nervous system. Trends Neurosci 15: 303-308.
• Biella G, Panara C, Pecile A, Sotgiu ML (1991) Facilitatory role of calcitonin gene-related peptide (CGRP) on excitation induced by substance P (SP) and noxious stimuli in rat spinal dorsal horn neurons. An iontophoretic study in vivo. Brain Res 559: 352-356.
• Birder LA, Kanai AJ, de Groat WC, Kiss S, Nealen ML, Burke NE, Dineley KE, Watkins S, Reynolds IJ, Caterina MJ (2001) Vanilloid receptor expression suggests a sensory role for urinary bladder epithelial cells. Proc Natl Acad Sci USA 98: 13396-13401.
• 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 60: 77-81.
• Callsen-Cencic P, Mense S (1997) Expression of neuropeptides and nitric oxide synthase in neurons innervating the inflamed rat urinary bladder. J Auton Nerv Syst 65: 33-44.
• Chancellor MB, Fowler CJ, Apostolidis A, de Groat WC, Smith CP, Somogyi GT, Aoki KR (2008) Drug Insight: biological effects of botulinum toxin A in the lower urinary tract. Nat Clin Pract Urol 5: 319-328.
• Charbel Issa P, Lever IJ, Michael GJ, Bradbury EJ, Malcangio M (2001) Intrathecally delivered glial cell line-derived neurotrophic factor produces electrically evoked release of somatostatin in the dorsal horn of the spinal cord. J Neurochem 78: 221-229.
• Chen CY, Liao CH, Kuo HC (2011) Therapeutic effects of detrusor botulinum toxin A injection on neurogenic detrusor overactivity in patients with different levels of spinal cord injury and types of detrusor sphincter dyssynergia. Spinal Cord 49: 659-664.
• Chuang YC, Yoshimura N, Huang CC, Chiang PH, Chancellor MB (2004) Intravesical botulinum toxin a administration produces analgesia against acetic acid induced bladder pain responses in rats. J Urol 172: 1529-1532.
• Coggeshall RE, Carlton SM (1998) Ultrastructural analysis of NMDA, AMPA, and kainiate receptors on unmyelinated and myelinated axons in the periphery. J Comp Neurol 391: 78-86. Cui M, Khanijou S, Rubino J, Aoki KR (2004) Subcutaneous administration of botulinum toxin A reduces formalin-induced pain. Pain 107: 125-133.
• Duggan AW, Riley RC, Mark MA, MacMillan SJ, Schaible HG (1995) Afferent volley patterns and the spinal release of immunoreactive substance P in the dorsal horn of the anaesthetized spinal cat. Neuroscience 65: 849-858.
• Durham PL, Cady R, Cady R (2004) Regulation of calcitonin gene-related peptide secretion from trigeminal nerve cells by botulinum toxin type A: implications for migraine therapy. Headache 44: 35-42.
• Filippi GM, Errico P, Santarelli R, Bagolini B, Manni E (1993) Botulinum A toxin effects on rat jaw muscle spindles. Acta Otolaryngol 113: 400-404.
• Giannantoni A, Di Stasi SM, Nardicchi V, Zucchi A, Macchioni L, Bini V, Goracci G, Porena M (2006) Botulinum-A toxin injections into the detrusor muscle decrease nerve growth factor bladder tissue levels in patients with neurogenic detrusor overactivity. J Urol 175: 2341-2344.
• Girard BM, Wolf-Johnston A, Braas KM, Birder LA, May V, Vizzard MA (2008) 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.
• Gottsch HP, Miller JL, Yang CC, Berger RE (2011) A pilot study of botulinum toxin for interstitial cystitis/painful bladder syndrome. Neurourol Urodyn 30: 93-96.
• Honda CN (1995) Differential distribution of calbindin-D28k and parvalbumin in somatic and visceral sensory neurons. Neuroscience 68: 883-892.
• Jabbari B, Maher N, Difazio MP (2003) Botulinum toxin a improved burning pain and allodynia in two patients with spinal cord pathology. Pain Med 4: 206-210.
• Jankovic J (2004) Botulinum toxin in clinical practice. J Neurol Neurosurg Psychiatry 75: 951-957.
• Jimenez-Andrade JM, Zhou S, Du J, Yamani A, Grady JJ, Castaneda-Hernandez G, Carlton SM (2004) Pronociceptive role of peripheral galanin in inflammatory pain. Pain 110: 10-21. Kakizaki H, de Groat WC (1996) Role of spinal nitric oxide in the facilitation of the micturition reflex by bladder irritation. J Urol 155: 355-360.
• Kanagarajah P, Ayyathurai R, Caruso DJ, Gomez C, Gousse AE (2012) Role of botulinum toxin-A in refractory idiopathic overactive bladder patients without detrusor overactivity. Int Urol Nephrol 44: 91-97.
• Kim WK, Kan Y, Ganea D, Hart RP, Gozes I, Jonakait GM (2000) Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit tumor necrosis factor-alpha production in injured spinal cord and in activated microglia via a cAMP-dependent pathway. J Neurosci 20: 3622-3630.
• Le Greves P, Nyberg F, Terenius L, Hokfelt T (1985) Calcitonin gene-related peptide is a potent inhibitor of substance P degradation. Eur J Pharmacol 115: 309-311.
• Li YN, Sakamoto H, Kawate T, Cheng CX, Li YC, Shimada O, Atsumi S (2005) An immunocytochemical study of calbindin-D28K in laminae I and II of the dorsal horn and spinal ganglia in the chicken with special reference to the relation to substance P-containing primary afferent neurons. Arch Histol Cytol 68: 57-70.
• Maggi CA (1990) The dual function of capsaicin-sensitive sensory nerves in the bladder and urethra. Ciba Found Symp 151: 77-83.
• Maggi CA (1997) Tachykinins as peripheral modulators of primary afferent nerves and visceral sensitivity. Pharmacol Res 36: 153-169.
• Meller ST, Gebhart GF (1993) Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain 52: 127-136.
• Mersdorf A, Schmidt RA, Kaula N, Tanagho EA (1992) Intrathecal administration of substance P in the rat: the effect on bladder and urethral sphincteric activity. Urology 40: 87-96.
• Morton CR, Hutchison WD, Hendry IA (1988) Release of immunoreactive somatostatin in the spinal dorsal horn of the cat. Neuropeptides 12: 189-197.
• Neugart F, Groh R, Gotz T, Horsch R (2006) Injections of botulinum toxin a into the detrusor vesicae for treatment of refractory detrusor hyperactivity in non-neurological patients. Aktuelle Urol 37: 212-217.
• Noguchi K, Senba E, Morita Y, Sato M, Tohyama M (1989) Prepro-VIP and preprotachykinin mRNAs in the rat dorsal root ganglion cells following peripheral axotomy. Brain Res Mol Brain Res 6: 327-330.
• Raivich G, Hellweg R, Kreutzberg GW (1991) NGF receptor-mediated reduction in axonal NGF uptake and retrograde transport following sciatic nerve injury and during regeneration. Neuron 7: 151-164.
• Rapp DE, Turk KW, Bales GT, Cook SP (2006) Botulinum toxin type a inhibits calcitonin gene-related peptide release from isolated rat bladder. J Urol 175: 1138-1142.
• Reitz A, Stohrer M, Kramer G, Del PG, Chartier-Kastler E, Pannek J, Burgdorfer H, Gocking K, Madersbacher H, Schumacher S, Richter R, von Tobel J, Schurch B (2004) European experience of 200 cases treated with botulinum-A toxin injections into the detrusor muscle for urinary incontinence due to neurogenic detrusor overactivity. Eur Urol 45: 510-515.
• Sandkuhler J, Fu QG, Helmchen C (1990) Spinal somatostatin superfusion in vivo affects activity of cat nociceptive dorsal horn neurons: comparison with spinal morphine. Neuroscience 34: 565-576.
• Smith CP, Franks ME, McNeil BK, Ghosh R, de Groat WC, 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.
• Smith CP, Radziszewski P, Borkowski A, Somogyi GT, Boone TB, Chancellor MB (2004) Botulinum toxin a has antinociceptive effects in treating interstitial cystitis. Urology 64: 871-875.
• Vaughan CW, Satchell PM (1995) Urine storage mechanisms. Prog Neurobiol 46: 215-237.
• Vizzard MA (2001) Alterations in neuropeptide expression in lumbosacral bladder pathways following chronic cystitis. J Chem Neuroanat 21: 125-138.
• Welch MJ, Purkiss JR, Foster KA (2000) Sensitivity of embryonic rat dorsal root ganglia neurons to Clostridium botulinum neurotoxins. Toxicon 38: 245-258

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