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2 0 0 5 B J U I N T E R N A T I O N A L | 9 6 , 6 7 0 – 6 7 6 | doi:10.1111/j.1464-410X.2005.05703.x
Original Article
CONNEXIN EXPRESSION IN THE BLADDER
NEUHAUS
et al.
Alterations in connexin expression in the bladder of
patients with urge symptoms
JOCHEN NEUHAUS, FRIEDERIKE PFEIFFER*, HARTWIG WOLBURG*, LARS-CHRISTIAN HORN† and WOLFGANG DORSCHNER
Departments of Urology and †Pathology, University of Leipzig, Leipzig, and *Department of Pathology, University of Tubingen, Tubingen, Germany
Accepted for publication 21 March 2005
transurethral tumour resection for bladder
cancer were used as controls. Tissue samples
from patients with severe idiopathic urge
symptoms were taken for exclusion
diagnostics of interstitial cystitis (IC) and
carcinoma in situ. The formation of functional
syncytia between detrusor smooth muscle
cells were examined in dye-coupling
experiments by injecting with Lucifer Yellow.
The morphology and structure of gap
junctions were assessed by transmission
electron microscopy and immunogold
labelling of Cx43 and Cx45. The expression of
connexin subtypes Cx40, Cx43 and Cx45 was
compared by indirect immunofluorescence,
and confocal laser scanning microscopy used
for semiquantitative analysis.
RESULTS
There was dye coupling between smooth
muscle cells of the detrusor in situ. Electron
microscopy and immunogold labelling
showed very small gap junctional plaques.
These findings were confirmed by confocal
immunofluorescence. Semiquantitative
analyses showed significantly higher Cx43
expression in the detrusor muscle, and a
tendency to higher Cx45 expression in the
suburothelial layer associated with urge
symptoms, whereas Cx40 expression was
unaffected.
CONCLUSIONS
Smooth muscle cells of the human detrusor
muscle are coupled by classical gap junctions,
forming limited local functional syncytia.
Both Cx43 and Cx45 are expressed at low
levels in normal detrusor. Up-regulation of
Cx43 in patients with urge incontinence
supports the possibility of functional changes
in the syncytial properties of detrusor smooth
muscle cells in this condition. In addition,
the observed increase of Cx45 in the
myofibroblast cell layer supports the idea that
alterations in sensory signalling are also
involved. Comparison with previous reports
implies that the pathophysiology of urgency
is distinct from that of the unstable bladder
and other forms of incontinence.
KEYWORDS
gap junction, electron microscopy, functional
syncytium, myofibroblast, smooth muscle cell,
urge incontinence
OBJECTIVE
To compare the formation of gap junctions
between detrusor smooth muscle cells in situ
and the distribution of connexin (Cx)40, Cx43
and Cx45 expressions in bladder biopsies from
a control group (with bladder tumour) and
from patients with urge symptoms, as smooth
muscle cells of the human detrusor muscle
communicate via gap junctions and express
several connexin subtypes, alterations of
which may be involved in the causes of lower
urinary tract symptoms.
MATERIALS AND METHODS
Connexin expression is prominent in
myofibroblast-like cells, supposedly involved
in afferent signalling pathways of the bladder.
Their strategic position directly beneath the
urothelium suggests they are a link between
urothelial ATP signalling during bladder filling
and afferent Ad-fibre stimulation for co-
ordination of bladder tonus and initialization
of the micturition reflex. Modification of their
coupling characteristics may have profound
impact on bladder sensation. Bladder tissue
probes of patients undergoing cystectomy or
INTRODUCTION
Coupling between smooth muscle cells of the
detrusor muscle is evident in normal human
urinary bladder [1–4]. Connexin (Cx) 43 and
Cx45 are the predominant connexins
expressed in human urinary bladder, as shown
by RT-PCR [2], immunohistochemistry and
Western blot analysis [3,4]. While connexin
expression in normal bladder is usually low in
detrusor muscle, strong Cx43 expression was
found in a suburothelial cell layer [4]. These
cells stained positively for vimentin and
a-actin and negative for desmin on
immunofluorescence, and had the
ultrastructural characteristics of
myofibroblasts [4]. The suburothelial
myofibroblasts are supposedly a major
component of the afferent signalling system
of the urinary bladder, serving as an amplifier
and a relay between urothelium and Ad
sensory nerve fibres [5]. ATP release on stretch
activation by urothelium can be detected by
the suburothelial myofibroblasts, leading to
higher tonus or contraction [6]. Recently ATP
activation of suburothelial myofibroblasts via
metabotropic P2Y receptors, possibly of the
P2Y2 or P2Y4 subtype, was reported in an
electrophysiological study in guinea pigs [7].
The functional myofibroblast syncytium
might not only serve to amplify the urothelial
signal, but modulating the coupling strength
between the cells would influence the travel
distance of the signal within the syncytium,
and consequently the number of Ad-fibres
stimulated. As the myofibroblasts are
susceptible to various other chemical
activators they are an ideal candidate for
signal integration [5].
The importance of ATP signalling under
pathological conditions has been implicated
in idiopathic detrusor instability [8,9] and in
patients with BOO [10]. Recently, Birder et al.
[11] found down-regulation of P2X1 and P2Y2
purinergic receptors in cats with feline
interstitial cystitis, in which ATP release from
urothelium is increased; Wada et al. [12]
reported an increase in bladder sensitivity to
purinergic stimulation in rats after
experimental BOO. These results suggest