Abstract
The present study explores the possible involvement of a purinergic mechanism in mechanosensory transduction in the bladder using P2X(3) receptor knock-out (P2X(3)-/-) and wild-type control (P2X(3)+/+) mice. Immunohistochemistry revealed abundant nerve fibers in a suburothelial plexus in the mouse bladder that are immunoreactive to anti-P2X(3). P2X(3)-positive staining was completely absent in the subepithelial plexus of the P2X(3)-/- mice, whereas staining for calcitonin gene-related peptide and vanilloid receptor 1 receptors remained. Using a novel superfused mouse bladder-pelvic nerve preparation, we detected a release of ATP proportional to the extent of bladder distension in both P2X(3)+/+ and P2X(3)-/- mice, although P2X(3)-/- bladder had an increased capacity compared with that of the P2X(3)+/+ bladder. The activity of multifiber pelvic nerve afferents increased progressively during gradual bladder distension (at a rate of 0.1 ml/min). However, the bladder afferents from P2X(3)-/- mice showed an attenuated response to bladder distension. Mouse bladder afferents of P2X(3)+/+, but not P2X(3)-/-, were rapidly activated by intravesical injections of P2X agonists (ATP or alpha,beta-methylene ATP) and subsequently showed an augmented response to bladder distension. By contrast, P2X antagonists [2',3'-O-(2,4,6-trinitrophenyl)-ATP and pyridoxal 5-phosphate 6-azophenyl-2',4'-disulfonic acid] and capsaicin attenuated distension-induced discharges in bladder afferents. These data strongly suggest a major sensory role for urothelially released ATP acting via P2X(3) receptors on a subpopulation of pelvic afferent fibers.
MeSH Terms
Adenosine Triphosphate/analogs & derivatives,metabolism,pharmacology
Animals
Capsaicin/pharmacology
Dilatation
Electrophysiology
Immunohistochemistry
In Vitro Techniques
Male
Mechanoreceptors/metabolism
Mice
Mice, Knockout
Neurons, Afferent/classification,drug effects,physiology
Pelvis/innervation
Peripheral Nerves/drug effects,physiology
Purinergic P2 Receptor Agonists
Purinergic P2 Receptor Antagonists
Pyridoxal Phosphate/analogs & derivatives,pharmacology
Receptors, Purinergic P2/deficiency
Receptors, Purinergic P2X3
Urinary Bladder/drug effects,innervation,metabolism
Urothelium/metabolism
Chemicals
2',3'-O-(2,4,6-trinitrophenyl)adenosine 5'-triphosphate
P2rx3 protein, mouse
Purinergic P2 Receptor Agonists
Purinergic P2 Receptor Antagonists
Receptors, Purinergic P2
Receptors, Purinergic P2X3
pyridoxal phosphate-6-azophenyl-2',4'-disulfonic acid
Pyridoxal Phosphate
Adenosine Triphosphate
alpha,beta-methyleneadenosine 5'-triphosphate
Capsaicin
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Vlaskovska M
Autonomic Neuroscience Institute, Royal Free and University College Medical School, London NW3 2PF, United Kingdom.
Kasakov L
Rong W
Bodin P
Bardini M
Cockayne D A
Ford A P
Burnstock G
References (28)
28 references, click to expand
-
P2X purinoceptor-mediated excitation of trigeminal lingual nerve terminals in an in vitro intra-arterially perfused rat tongue preparation.
J Physiol. 2000 May 1;524 Pt 3:891-902
PMID: 10790166
-
Electrophysiological study of micturition reflexes in rats.
Am J Physiol. 1989 Aug;257(2 Pt 2):R410-21
PMID: 2764162
-
A bladder-to-bladder cooling reflex in the cat.
J Physiol. 1990 Aug;427:281-300
PMID: 2213600
-
Purinergic sensory neurotransmission in the urinary bladder: an in vitro study in the rat.
BJU Int. 1999 Nov;84(7):854-60
PMID: 10532986
-
Urothelial function.
BJU Int. 1999 Aug;84(3):235-42
PMID: 10468713
-
ATP is released from rabbit urinary bladder epithelial cells by hydrostatic pressure changes--a possible sensory mechanism?
J Physiol. 1997 Dec 1;505 ( Pt 2):503-11
PMID: 9423189
-
Distinct ATP receptors on pain-sensing and stretch-sensing neurons.
Nature. 1997 May 29;387(6632):505-8
PMID: 9168113
-
P2X receptor-mediated excitation of nociceptive afferents in the normal and arthritic rat knee joint.
Br J Pharmacol. 1998 Sep;125(2):341-6
PMID: 9786507
-
Distribution of afferent axons in the bladder of rats.
J Neurocytol. 1998 Mar;27(3):141-55
PMID: 10640174
-
NERVOUS CONTROL OF MICTURITION.
Physiol Rev. 1965 Jul;45:425-94
PMID: 14340716
-
Receptors for purines and pyrimidines.
Pharmacol Rev. 1998 Sep;50(3):413-92
PMID: 9755289
-
Distribution of P2X receptors in the urinary bladder and the ureter of the rat.
J Urol. 2000 Jun;163(6):2002-7
PMID: 10799247
-
Functional properties of spinal visceral afferents supplying abdominal and pelvic organs, with special emphasis on visceral nociception.
Prog Brain Res. 1986;67:87-114
PMID: 3823484
-
The expression of P2X3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor.
Mol Cell Neurosci. 1998 Nov;12(4-5):256-68
PMID: 9828090
-
Mechanosensitive properties of pelvic nerve afferent fibers innervating the urinary bladder of the rat.
J Neurophysiol. 1994 Nov;72(5):2420-30
PMID: 7884468
-
Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X3-deficient mice.
Nature. 2000 Oct 26;407(6807):1011-5
PMID: 11069181
-
Acute nociception mediated by hindpaw P2X receptor activation in the rat.
Br J Pharmacol. 1997 Sep;122(2):365-71
PMID: 9313948
-
Activation of unmyelinated afferent fibres by mechanical stimuli and inflammation of the urinary bladder in the cat.
J Physiol. 1990 Jun;425:545-62
PMID: 2213588
-
ATP in human skin elicits a dose-related pain response which is potentiated under conditions of hyperalgesia.
Brain. 2000 Jun;123 ( Pt 6):1238-46
PMID: 10825361
-
A P2X purinoceptor expressed by a subset of sensory neurons.
Nature. 1995 Oct 5;377(6548):428-31
PMID: 7566119
-
Intravesical capsaicin and resiniferatoxin therapy: spicing up the ways to treat the overactive bladder.
J Urol. 1999 Jul;162(1):3-11
PMID: 10379728
-
A novel in vitro bladder pelvic nerve afferent model in the rat.
Br J Urol. 1998 Dec;82(6):902-5
PMID: 9883232
-
Release of vasoactive substances from endothelial cells by shear stress and purinergic mechanosensory transduction.
J Anat. 1999 Apr;194 ( Pt 3):335-42
PMID: 10386771
-
Functional characteristics of lumbar visceral afferent fibres from the urinary bladder and the urethra in the cat.
Pflugers Arch. 1986 Nov;407(5):510-8
PMID: 3786110
-
Systemic capsaicin treatment impairs the micturition reflex in the rat.
Br J Pharmacol. 1984 Dec;83(4):935-41
PMID: 6518344
-
The innervation and function of the lower urinary tract.
J Neurosurg. 1986 Sep;65(3):278-85
PMID: 3488376
-
ATP-stimulated release of ATP by human endothelial cells.
J Cardiovasc Pharmacol. 1996 Jun;27(6):872-5
PMID: 8761855
-
Cloning OF P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channels.
J Neurosci. 1996 Apr 15;16(8):2495-507
PMID: 8786426