Evidence that prostaglandin is responsible for the ‘rebound contraction’ following stimulation of non-adrenergic, non-cholinergic (‘purinergic’) inhibitory nerves

Burnstock, Geoffrey; Cocks, T. M.; Paddle, Brian M.; Staszewska-Barczak, Janina

doi:10.1016/0014-2999(75)90060-6

Cited by 140 publications

(57 citation statements)

References 8 publications

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“…The present data show this to be because ATP elicits excitatory prostaglandin production, which in turn causes direct stimulation of the muscle. Prostaglandin generation following exposure to endogenous or exogenous purines has been demonstrated in a variety of intestinal and nonintestinal tissues (1,2,8,20,23), and its occurrence in the muscularis mucosae/mucosa of the rabbit distal colon adds to the list of sites where this pathway operates. Paradoxically, ATP exerts its largest motor effects on the muscularis mucosae in the rabbit proximal colon, where prostaglandins elicit minimal contractions (31,33).…”

Section: Discussionmentioning

confidence: 99%

“…The pharmacological agents used to test this hypothesis were selected on the basis of their respective abilities to 1) directly stimulate either the muscularis mucosae (30) or the mucosa (1,14), 2) initiate prostaglandin production (1,2,8,20,23,25), 3) reproduce the actions of endogenous eicosanoid mediators, 4) stimulate ganglionic nicotinic receptors on submucosal neurons, and 5) block the synthesis or the effects of agents with actions on the muscle or the mucosa and/or their respective innervation.…”

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confidence: 99%

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Muscularis mucosae contraction evokes colonic secretion via prostaglandin synthesis and nerve stimulation

Percy

Fromm

Wangsness

2003

American Journal of Physiology-Gastrointestinal and Liver Physi

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Muscularis mucosae contraction evokes colonic secretion via prostaglandin synthesis and nerve stimulation. Am J Physiol Gastrointest Liver Physiol 284: G213-G220, 2003. First published October 16, 2002 10.1152/ajpgi.00179.2002-This in vitro study tested the hypothesis that muscularis mucosae contractile activity contributes to rabbit colonic mucosal function by mechanisms other than simple mechanical deformation of the epithelium. Experiments were performed by using a technique that allows simultaneous recording of muscle activity and transmucosal potential difference, a measure of epithelial ion transport. ATP, bradykinin, histamine, PGE2, PGF1␣, and PGF2␣ elicited muscularis mucosae contractions that were resistant to atropine and TTX. Only ATP-induced contractions were indomethacin sensitive, and only those to dimethylphenylpiperazinium iodide (DMPP) were reduced by atropine. All agonist-evoked increases in transmucosal potential difference were atropine resistant, and, with the exception of those to PGE2, PGF2␣, and VIP, they were also TTX sensitive. Mucosal responses to ATP, bradykinin, and histamine were indomethacin sensitive, whereas those to DMPP, the prostaglandins, and VIP were not. When cyclooxygenase activity or the mucosal innervation was compromised, even maximal muscularis mucosae contractions did not produce large secretory responses. It is concluded that contraction-related prostaglandin synthesis and noncholinergic secretomotor neuron stimulation represent the physiological transduction mechanism through which muscularis mucosae motor activity is translated into mucosal secretion. motility; mucosa; submucosal plexus; transduction pathway; integrated function; rabbit THE RELATIONSHIP BETWEEN INTESTINAL motility and mucosal absorption and secretion has been given only scant attention over the last three decades, and almost without exception the focus has been on the effects of muscularis propria motor activity on mucosal function (15)(16)(17)(18)(19)37). More recently, attention has shifted to the influence of muscularis mucosae contractions on mucosal activity. This was based on the observations that this muscle layer is physically attached to the mucosa, both are innervated via the submucosal plexus (30), and the muscularis mucosae can respond to specific changes in the luminal environment via a neurally mediated afferent-efferent link (27, 30). In the rabbit colon, the latter pathway appears to be associated with mucosal protection, as evidenced by the potentially harmful stimuli required to elicit this type of response (30).In an early Ussing chamber study, morphological analysis of rat colonic mucosa immediately following stimulation with bradykinin revealed significant changes in mucosal architecture associated with anion secretion (3). The authors felt that this was unrelated to muscularis mucosae contraction because bradykinin caused relaxation of the colonic muscularis propria (13); therefore, they assumed it would have the same effect on the third muscle layer. Subsequent work on the m...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Muscularis mucosae contraction evokes colonic secretion via prostaglandin synthesis and nerve stimulation

Percy

Fromm

Wangsness

2003

American Journal of Physiology-Gastrointestinal and Liver Physi

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“…The possibility should be considered that ATP and APPCP act indirectly by inducing prostaglandin synthesis (Needleman et al, 1974;Burnstock et al, 1975). Prostaglandins have been implicated in the contractile response to non-cholinergic nerve stimulation in the bladder of the rat (Choo & Mitchelson, 1977), and rabbit and monkey (Johns & Paton, 1977).…”

Section: Discussionmentioning

confidence: 99%

“…ATP is a potent stimulant of prostaglandin synthesis in a wide range of tissues (Needleman, Minkes & Douglas, 1974;Burnstock, Cocks, Paddle & Staszewska-Barczak, 1975) and prostaglandins have been shown to potentiate the contractile response to intramural nerve stimulation in the bladder of the guinea-pig and rat (Choo & Mitchelson, 1977). Therefore to test whether the potentiating effect of ATP on carbachol-induced contractions was due to stimulation of prostaglandin synthesis, the experiments were repeated in the presence of the prostaglandin synthesis inhibitor, indomethacin.…”

Section: Responses To Atpmentioning

confidence: 99%

EFFECTS OF ADENOSINE 5′‐TRIPHOSPHATE (ATP) AND Β‐γ‐METHYLENE ATP ON THE RAT URINARY BLADDER

Brown

Burnstock

Cocks

1979

British J Pharmacology

104

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High concentrations of adenosine 5′‐triphosphate (ATP, 100 to 1000 μm) were required to cause contraction of the rat urinary bladder, while adenosine and adenosine 5′‐monophosphate (AMP, 1 to 50/im) produced relaxation. One hundred fold lower concentrations of β‐γ‐methylene ATP, which is resistant to degradation to AMP and adenosine, caused dose‐dependent, phasic contractions which mimicked atropine‐resistant responses to nerve stimulation. Adenosine and AMP caused dose‐dependent inhibition of carbachol‐induced contractions; theophylline competitively antagonized this inhibition but not the contractile responses to β‐γ‐methylene ATP, ATP or atropine‐resistant nerve stimulation. These results suggest that the insensitivity of the rat bladder to ATP is due to its rapid degradation to AMP and adenosine and support the hypothesis that the bladder receives a purinergic excitatory innervation.

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“…It was shown in 1974 that adenine nucleotides induce prostaglandin (PG) synthesis [517] and, soon after, evidence was presented that PGs were responsible for the rebound contractions of the guinea-pig taenia coli that follow stimulation of purinergic inhibitory nerves [114]. Since then, evidence has accumulated that PGs are generated in bladder smooth muscle as a result of purinergic neurotransmitter activity.…”

Section: Involvement Of Prostaglandins In Purinergic Signallingmentioning

confidence: 99%

Purinergic signalling in the urinary tract in health and disease

Burnstock

2013

Purinergic Signalling

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142

149

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Purinergic signalling is involved in a number of physiological and pathophysiological activities in the lower urinary tract. In the bladder of laboratory animals there is parasympathetic excitatory cotransmission with the purinergic and cholinergic components being approximately equal, acting via P2X1 and muscarinic receptors, respectively. Purinergic mechanosensory transduction occurs where ATP, released from urothelial cells during distension of bladder and ureter, acts on P2X3 and P2X2/3 receptors on suburothelial sensory nerves to initiate the voiding reflex, via low threshold fibres, and nociception, via high threshold fibres. In human bladder t h e p u r i n e rg i c c o m p o n e n t o f p a r a s y m p a t h e t i c cotransmission is less than 3 %, but in pathological conditions, such as interstitial cystitis, obstructed and neuropathic bladder, the purinergic component is increased to 40 %. Other pathological conditions of the bladder have been shown to involve purinoceptor-mediated activities, including multiple sclerosis, ischaemia, diabetes, cancer and bacterial infections. In the ureter, P2X7 receptors have been implicated in inflammation and fibrosis. Purinergic therapeutic strategies are being explored that hopefully will be developed and bring benefit and relief to many patients with urinary tract disorders.

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Evidence that prostaglandin is responsible for the ‘rebound contraction’ following stimulation of non-adrenergic, non-cholinergic (‘purinergic’) inhibitory nerves

Cited by 140 publications

References 8 publications

Muscularis mucosae contraction evokes colonic secretion via prostaglandin synthesis and nerve stimulation

Muscularis mucosae contraction evokes colonic secretion via prostaglandin synthesis and nerve stimulation

EFFECTS OF ADENOSINE 5′‐TRIPHOSPHATE (ATP) AND Β‐γ‐METHYLENE ATP ON THE RAT URINARY BLADDER

Purinergic signalling in the urinary tract in health and disease

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