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First published online March 28, 2008
Journal of Experimental Biology 211, 1270-1280 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.012005
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Changes in the control of gastric motor activity during metamorphosis in the amphibian Xenopus laevis, with special emphasis on purinergic mechanisms

Monika Sundqvist* and Susanne Holmgren

Department of Zoophysiology, Göteborg University, SE 405 30 Göteborg, Sweden


Figure 1
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  		Fig. 1. (A) Mean force developed in gastric smooth muscle under basal conditions in prometamorphic (Promet.), metamorphic (Met.) and juvenile Xenopus. Statistical significance was calculated using a one-way ANOVA followed by Bonferroni's post hoc test (N=28). (B) Concentration-dependent increase in mean force in response to carbachol (CCh). Statistically significant increase was obtained at >=1 µmol l–1 at all stages (N=6). (C) Concentration-dependent increase in mean force in response to neurokinin A (NKA). A statistically significant increase was obtained at >=0.1 µmol l–1 for prometamorphosis (N=7) and metamorphosis (N=8), and at >=1 µmol l–1 for juveniles (N=6). For concentration–response curves, statistical analysis was performed using repeated measures one-way ANOVA followed by Dunnett's post hoc test. Control value prior to administration of agonist is denoted C on the x-axis. (D) Effect of 300 µmol l–1 N-nitro-L-arginine methyl ester hydrochloride (L-NAME) administered 20–30 min prior to measurements in prometamorphosis (N=7), metamorphosis (N=8) and juveniles (N=9). Asterisk indicates a statistically significant difference, P<0.05. (E,F) Representative traces of the response to L-NAME (300 µmol l–1) in (E) metamorphic tissues and (F) juvenile tissues.

 

Figure 2
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  		Fig. 2. Responses to 5-hydroxytryptamine (5-HT, serotonin) in stomach muscle. (A) Concentration-dependent effect on mean force in response to 5-HT. A statistically significant decrease was obtained at >=0.01 µmol l–1 in prometamorphosis (N=10) and at >=10 µmol l–1 in juveniles (N=8). There was no effect during metamorphosis (N=7). For concentration–response curves, statistical analysis was performed using repeated measures one-way ANOVA followed by Dunnett's post hoc test. (B) Representative trace of the response to an excitatory concentration of 5-HT (1 µmol l–1) in juveniles. (C) Representative trace of the response to an inhibitory concentration of 5-HT (1 µmol l–1) in juveniles. (D) Relaxing effect of 5-HT (1 µmol l–1) in the presence and absence of the 5-HT receptor antagonist methysergide (Meth., 10 µmol l–1) in prometamorphic (N=4) and juvenile (N=5) stomach muscle strips. (E) Contracting effect of 5-HT (0.1–1 µmol l–1) in the presence and absence of the 5-HT receptor antagonist methysergide (10 µmol l–1) in juvenile (N=12) stomach muscle strips. Statistical analysis was performed using repeated measures one-way ANOVA followed by Bonferroni's post hoc test. Asterisk indicates a statistically significant difference, P<0.05.

 

Figure 3
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  		Fig. 3. Responses to ATP in stomach muscle preparations. (A) Concentration-dependent mean force response to ATP. A statistically significant decrease was obtained at >=3 µmol l–1 in prometamorphosis (N=10) and at >=300 µmol l–1 in juveniles (N=10). There was no effect in metamorphic tissues (N=8). Control value prior to administration of agonist is denoted C. Statistical analysis was performed using repeated measures one-way ANOVA followed by Dunnett's post hoc test. (B,C) Representative traces of the response to ATP in (B) prometamorphic tissues and (C) juvenile tissues (concentrations are in µmol l–1). (D) Representative trace of the response to a single high concentration of ATP (1000 µmol l–1).

 

Figure 4
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  		Fig. 4. (A,B) Responses to adenosine 5'-triphosphate (ATP) in the absence and presence of the ectonucleotidase inhibitor 6-N,N-diethyl-D-β,{gamma}-dibromomethylene ATP (ARL67156, 100 µmol l–1) in (A) prometamorphic tissues (N=8) and in (B) juveniles (N=9). A statistically significant difference between responses was obtained at >=0.01 µmol l–1 in prometamorphosis and between 1 and 10 µmol l–1 in juveniles. (C,D) Responses to ATP in the absence and presence of the A1 receptor antagonist 1,3-dipropyl-8-cyclopentylxanthine (DPCPX) in (C) prometamorphic tissues (1 µmol l–1, N=9) and in (D) juveniles (3 µmol l–1, N=8). A statistically significant difference between responses was obtained between 3 and 30 µmol l–1 in prometamorphic tissues but not at all in juvenile tissues. Control value prior to administration of antagonist or enzyme blocker is denoted C1 and that prior to ATP administration as C2 on the x-axis (A–D). Statistical significance for ARL67156/DPCPX effects was calculated using Student's unpaired t-test for each concentration.

 

Figure 5
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  		Fig. 5. (A) Concentration-dependent decrease in mean force in response to adenosine. A statistically significant decrease was obtained at >=10 µmol l–1 in prometamorphosis (N=12), at >=100 µmol l–1 in metamorphosis (N=6) and at >=300 µmol l–1 in juveniles (N=12). (B) Concentration-dependent decrease in mean force in response to N6-cyclopentyladenosine (CPA) in prometamorphosis (N=8), metamorphosis (N=11) and juveniles (N=10). Statistically significant decrease obtained at >=1 µmol l–1 for all stages. Control value prior to administration of agonist is denoted C on the x-axis. Statistical analysis was performed using repeated measures one-way ANOVA followed by Dunnett's post hoc test (A,B). (C) Effect of adenosine in the presence and absence of the A1 receptor antagonist DPCPX (1 µmol l–1) in prometamorphic (100 µmol l–1 adenosine, N=4) and juvenile (1000 µmol l–1 adenosine, N=9) stomach muscle strips. Statistical analysis was performed using repeated measures one-way ANOVA followed by Bonferroni's post hoc test. Asterisk indicates P<0.05. (D) Effects of the adenosine kinase inhibitor 4-amino-5-(3-bromophenyl)-7-(6-morpholino-pyridin-3-yl)pyrido[2,3-d]pyrimidine (ABT-702, 1 µmol l–1) on mean force developed under control conditions in prometamorphic (N=7) and juvenile (N=10) tissues. Statistical significance was calculated using Student's t-test for paired observations. Asterisk indicates P<0.05.

 

Figure 6
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  		Fig. 6. Responses to uridine 5'-triphosphate (UTP) in stomach muscle preparations. (A) Concentration-dependent response of mean force to UTP. A statistically significant decrease was obtained at >=10 µmol l–1 in prometamorphosis (N=9) and in juvenile tissues at 1000 µmol l–1 (N=12). In metamorphic tissues a significant increase was obtained at >=30 µmol l–1 (N=6). Control value prior to administration of agonist is denoted C on the x-axis. Statistical analysis was performed using repeated measures one-way ANOVA followed by Dunnett's post hoc test. (B–D) Representative traces of the response to UTP in (B) prometamorphic tissues, (C) metamorphic tissues and (D) juvenile tissues (concentrations in µmol l–1).

 

Figure 7
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  		Fig. 7. (A,B) Representative trace of the tetrodotoxin (TTX)-insensitive responses to UTP (100 µmol l–1) in (A) prometamorphic stomach and (B) metamorphic stomach. (C) Representative trace of the partially TTX-sensitive response to UTP (100 µmol l–1) in juvenile stomach. (D,E) TTX (1 µmol l–1) blocks the UTP-induced decrease in frequency (D, N=9) but not the increase in mean force (E, N=6) in juvenile stomach. (F) L-NAME (300 µmol l–1) blocks the UTP-induced decrease in frequency (N=5) in juvenile stomach. Statistical analysis was performed using repeated measures one-way ANOVA followed by Bonferroni's post hoc test. Asterisk indicates P<0.05. W, wash-out.

 

Figure 8
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  		Fig. 8. Responses to adenosine 5'-[{gamma}-thio]-triphosphate (ATP{gamma}S) and {alpha}-β-methyleneadenosine 5'-triphosphate ({alpha}-β-MeATP) in stomach muscle preparations. (A) Concentration-dependent increase in mean force in response to ATP{gamma}S. A statistically significant increase was obtained at >=30 µmol l–1 in prometamorphic (N=7), at >=100 µmol l–1 (N=9) in metamorphic and at 300 µmol l–1 in juvenile tissues (N=15). (B) Concentration-dependent increase in mean force in response to {alpha}-β-MeATP. Statistically significant increase obtained at >=10 µmol l–1 in prometamorphic (N=8) and at >=30 µmol l–1 (N=6) in metamorphic and juvenile tissues (N=10). Control value prior to administration of agonist is denoted C on the x-axis. Statistical analysis was performed using repeated measures one-way ANOVA followed by Dunnett's post hoc test. (C) Effect of {alpha}-β-MeATP in the presence and absence of the P2 receptor antagonist pyridoxalphosphate-6-azophenyl-2',4'-disulphonic acid (PPADS, 100 µmol l–1) in prometamorphic (10 µmol l–1 {alpha}-β-MeATP, N=7) and juvenile (30 µmol l–1 {alpha}-β-MeATP, N=8) stomach strips. Statistical analysis was performed using repeated measures one-way ANOVA followed by Bonferroni's post hoc test. Asterisk indicates P<0.05.

 

Figure 9
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  		Fig. 9. A schematic overview of the different receptors indicated in this study to be present in the gut at prometamorphosis, metamorphosis and juvenile stages. Most receptors seem to be directly situated on the smooth muscle. Plus sign indicates excitatory neuron, whereas minus sign indicates inhibitory neuron. Black receptors indicate excitatory effects while grey receptors indicate inhibitory effects. For possible receptor subtypes see discussion. M, muscarinic receptor; NK, neurokinin receptor. Other abbreviations as previously used in the text.

 

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© The Company of Biologists Ltd 2008