Abstract
The study determined the distribution and immunohistochemical coding of the sensory neurons innervating the male pig urinary bladder. Retrograde tracer Fast Blue was injected bilaterally into the bladder trigone, base or dome. The presence of neuropeptide Y (NPY), somatostatin (SOM), galanin (GAL), vasoactive intestinal polypeptide (VIP), nitric oxide synthase (NOS), calcitonin gene-related peptide (CGRP) and substance P (SP) were studied with immunofluorescence. Fast Blue-positive neurons were localized bilaterally in dorsal root ganglia from L1 to L6 and from S3 to S4 with specific differences regarding the injection site. The number of Fast Blue-positive neurons was higher in the right ganglia. Immunohistochemistry revealed that sensory neurons innervating the urinary bladder trigone, base and dome displayed immunoreactivities to CGRP, SP, NOS, GAL and SOM. Differences in the neuropeptide content were observed between the Fast Blue-positive neurons in lumbar and sacral ganglia. Taken together, these data indicate that the lumbar and sacral pathways probably play different roles in sensory transmission from the urinary bladder trigone, base and dome.
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References
Andersson KE, Persson K (1995) Nitric oxide synthase and the lower urinary tract: possible implications for physiology and pathophysiology. Scand J Urol Nephrol Suppl 175:43–53
Applebaum AE, Vance WH, Coggeshall RE (1980) Segmental localization of sensory cells that innervate the bladder. J Comp Neurol 192:203–209
Arms L, Vizzard MA (2011) Neuropeptides in lower urinary tract function. Handb Exp Pharmacol 395–423
Bennett DL, Dmietrieva N, Priestley JV, Clary D, McMahon SB (1996) trkA, CGRP and IB4 expression in retrogradely labelled cutaneous and visceral primary sensory neurones in the rat. Neurosci Lett 206:33–36
Birder L, de Groat W, Mills I, Morrison J, Thor K, Drake M (2010) Neural control of the lower urinary tract: peripheral and spinal mechanisms. Neurourol Urodyn 29:128–139
Birder L, Drake M, De Groat WC, Fowler C, Mayer E, Morrison J, Paton J, Griffiths D, Mills IW, Thor K (2009) Neural control. In: Abrams P, Cardozo L, Khoury S, Wein A (eds) Incotinence, 4th edn. Health Publications Ltd, Paris, pp 167–254
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(Suppl 4):77–81
Callsen-Cencic P, Mense S (1997) Expression of neuropeptides and nitric oxide synthase in neurones innervating the inflamed rat urinary bladder. J Auton Nerv Syst 65:33–44
Chapple CR, Milner P, Moss HE, Burnstock G (1992) Loss of sensory neuropeptides in the obstructed human bladder. Br J Urol 70:373–381
Conzen MA, Sollmann H (1982) Reinnervation of the urinary bladder after microsurgical reconstruction of transsected caudal fibres. An experimental study in pigs. Urol Res 10:141–144
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
de Groat WC, Yoshimura N (2009) Afferent nerve regulation of bladder function in health and disease. Handb Exp Pharmacol 91–138
Djouhri L, Lawson SN (2004) Abeta-fiber nociceptive primary afferent neurons: a review of incidence and properties in relation to other afferent A-fiber neurons in mammals. Brain Res Brain Res Rev 46:131–145
Downie JW, Champion JA, Nance DM (1984) A quantitative analysis of the afferent and extrinsinc efferent innervation of specyfic regions of the bladder and urethra in the cat. Brain Res Bull 12:735–740
Jezernik S, Wen JG, Rijkhoff NJ, Djurhuus JC, Sinkjaer T (2000) Analysis of bladder related nerve cuff electrode recordings from preganglionic pelvic nerve and sacral roots in pigs. J Urol 163:1309–1314
Kaleczyc J, Scheuermann DW, Pidsudko Z, Majewski M, Lakomy M, Timmermans JP (2002) Distribution, immunohistochemical characteristics and nerve pathways of primary sensory neurons supplying the porcine vas deferens. Cell Tissue Res 310:9–17
Keast JR, Groat D (1992) Segmental distribution and peptide content of primary afferent neurons innervating the urogenital organs and colon of male rats. J Comp Neurol 319:615–623
Krane RJ, Olsson CA (1973) Phenoxybenzamine in neurogenic bladder dysfunction: I. A theory of micturition. J Urol 110:650–652
Lasanen LT, Tammela TL, Liesi P, Waris T, Polak JM (1992) The effect of acute distension on vasoactive intestinal polypeptide (VIP), neuropeptide Y (NPY) and substance P (SP) immunoreactive nerves in the female rat urinary bladder. Urol Res 20:259–263
Maggi CA, Giuliani S (1991) The neurotransmitter role of calcitonin gene-related peptide in the rat and guinea-pig ureter: effect of a calcitonin gene-related peptide antagonist and species-related differences in the action of omega conotoxin on calcitonin gene-related peptide release from primary afferents. Neuroscience 43:261–268
Maggi CA, Santicioli P, Patacchini R, Turini D, Barbanti G, Beneforti P, Giuliani S, Meli A (1987) Galanin: a potent modulator of excitatory neurotransmission in the human urinary bladder. Eur J Pharmacol 143:135–137
Nadelhaft I, Booth AM (1984) The location and morphology of preganglionic neurons and the distribution of visceral afferents from the rat pelvic nerve: a horseradish peroxidase study. J Comp Neurol 226:238–245
Nandigama R, Bonitz M, Papadakis T, Schwantes U, Bschleipfer T, Kummer W (2010) Muscarinic acetylcholine receptor subtypes expressed by mouse bladder afferent neurons. Neuroscience 168:842–850
Pidsudko Z, Kaleczyc J, Majewski M, Lakomy M, Scheuermann DW, Timmermans JP (2001) Differences in the distribution and chemical coding between neurons in the inferior mesenteric ganglion supplying the colon and rectum in the pig. Cell Tissue Res 303:147–158
Radziszewski P, Crayton R, Zaborski J, Czlonkowska A, Borkowski A, Bossowska A, Majewski M (2009) Multiple sclerosis produces significant changes in urinary bladder innervation which are partially reflected in the lower urinary tract functional status—sensory nerve fibers role in detrusor overactivity. Mult Scler 15:860–868
Russo D, Clavenzani P, Sorteni C, Bo ML, Botti M, Gazza F, Panu R, Ragionieri L, Chiocchetti R (2013) Neurochemical features of boar lumbosacral dorsal root ganglion neurons and characterization of sensory neurons innervating the urinary bladder trigone. J Comp Neurol 521:342–366
Smet PJ, Moore KH, Jonavicius J (1997) Distribution and colocalization of calcitonin gene-related peptide, tachykinins, and vasoactive intestinal peptide in normal and idiopathic unstable human urinary bladder. Lab Invest 77:37–49
Swindle MM, Moody DC, Phillips LD (1992) Swine as a models in biomedical research. Iowa State Univ Press, Ames
Tsaknakis A (1971) Morphological studies of the pelvic plexus of the pig. Zentralbl Veterinarmed A 18:310–324
Vizzard MA (1997) Increased expression of neuronal nitric oxide synthase in bladder afferent and spinal neurons following spinal cord injury. Dev Neurosci 19:232–246
Vizzard MA (2000) Up-regulation of pituitary adenylate cyclase-activating polypeptide in urinary bladder pathways after chronic cystitis. J Comp Neurol 420:335–348
Vizzard MA (2001) Alterations in neuropeptide expression in lumbosacral bladder pathways following chronic cystitis. J Chem Neuroanat 21:125–138
Wasowicz K, Majewski M, Lakomy M (1998) Distribution of neurons innervating the uterus of the pig. J Auton Nerv Syst 74:13–22
Wyndaele JJ (2010) Investigating afferent nerve activity from the lower urinary tract: highlighting some basic research techniques and clinical evaluation methods. Neurourol Urodyn 29:56–62
Yau WM, Dorsett JA, Youther ML (1986) Evidence for galanin as an inhibitory neuropeptide on myenteric cholinergic neurons in the guinea-pig small intestine. Neurosci Lett 72:305–308
Yoshimura N, White G, Weight FF, De Groat WC (1996) Different types of Na+ and A-type K+ currents in dorsal root ganglion neurones innervating the rat urinary bladder. J Physiol Lond 494:1–16
Zhou Y, Ling EA (1997) Increased NADPH-diaphorase reactivity in bladder afferent pathways following urethral obstruction in guinea pigs. J Peripher Nerv Syst 2:333–342
Zvarova K, Vizzard MA (2006) Changes in galanin immunoreactivity in rat micturition reflex pathways after cyclophosphamide-induced cystitis. Cell Tissue Res 324:213–224
Acknowledgments
The author thanks M. Marczak and A. Penkowski for their excellent technical assistance. This study was supported by a grant NN 308 2334 38 from the National Committee for Scientific Research Poland.
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Pidsudko, Z. Immunohistochemical Characteristics and Distribution of Sensory Dorsal Root Ganglia Neurons Supplying the Urinary Bladder in the Male Pig. J Mol Neurosci 52, 71–81 (2014). https://doi.org/10.1007/s12031-013-0117-2
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DOI: https://doi.org/10.1007/s12031-013-0117-2