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Substance P in the fish gut: Mechanism of action and release on distension
98 SUBSTANCE P DISTENSION
IN
THE
FISH
GUT: M E C H A N I S M OF A C T I O N AND R E L E A S E ON
J. JENSEN, A.-C. JONSSON and S. H O L M G R E N Comparative Neuroscience Unit, Department U n i v e r s i t y of G6teborg, G6teborg, Sweden.
of
Zoophysiology,
Nerve fibres and endocrine cells c o n t a i n i n g a substance P- (SP) like peptide have been d e m o n s t r a t e d in the g a s t r o i n t e s t i n a l canal of several fish species. However, the actual function and the m e c h a n i s m of action of this peptide in the fish gut is less w e l l known. In all species we have studied so far SP is found to have an e x c i t a t o r y action on gut preparations, but the m e c h a n i s m s of action appear to vary between organs and species. Thus, in the gut of the spiny dogfish, Squalus acanthias, SP acts d i r e c t l y on the smooth m u s c l e cells (i), while in the stomach of the rainbow trout, Salmo gairdneri, the e x c i t a t o r y effect of exogenous SP can be c o r r e l a t e d to a release of 5-hydroxytryptamine as well as, w h e n using high concentrations, a direct effect on smooth muscle (2). In v a s c u l a r l y perfused p r e p a r a t i o n s of the intestine of the cod, Gadus morhua, SP in low c o n c e n t r a t i o n s appears to exert its effect via both c h o l i n e r g i c and serotonergic pathways in addition to a direct effect o b t a i n e d w i t h high c o n c e n t r a t i o n s of SP (3). Experiments p e r f o r m e d on the v a s c u l a r l y p e r f u s e d stomach of the cod show that the contractions produced by SP is u n a f f e c t e d by t r e a t m e n t w i t h atropine, m e t h y s e r g i d e or tetrodotoxin, s u g g e s t i n g the p r e s e n c e of only a direct effect of SP in the cod stomach. This finding points to an interesting difference between the action of SP in the cod stomach and the rainbow trout stomach where an a d d i t i o n a l pathway via serotonergic neurons is present. It also shows that the pathways may be different between the stomach and the intestine in the same species. In studies of the effect of SP on a p h y l o g e n e t i c a l l y i n t e r e s t i n g species, the south american lungfish (Lepidosiren paradoxa) SP was found to p r o d u c e dose-dependent contractions on circular m u s c l e strip preparations from the intestine. The contractions were u n a f f e c t e d by treatment w i t h atropine, m e t h y s e r g i d e or tetrodotoxin, indicating an action d i r e c t l y on the smooth m u s c l e cells only similar to the situation in the gut of the spiny dogfish. It m a y be hypothesized that the direct action of SP o b s e r v e d in all fish species s t u d i e d so far is a general and primitive mechanism. Experiments w i t h the v a s c u l a r l y p e r f u s e d rainbow trout stomach have shown that m e c h a n i c a l d i s t e n s i o n initiates a c o n t r a c t i l e a c t i v i t y which is b l o c k e d by tetrodotoxin as well as by a c o m b i n a t i o n of serotonergic and cholinergic antagonists (4). P r e l i m i n a r y results now show that SP-like m a t e r i a l is c o n t i n u o u s l y r e l e a s e d from the stomach into the vascular perfusate. On m e c h a n i c a l d i s t e n s i o n of the stomach an increase in the outflow of i m m u n o r e a c t i v e m a t e r i a l is observed further i n d i c a t i n g the involvement of a SP-like peptide in the e x c i t a t o r y control of the rainbow trout stomach. i. H o l m g r e n S (1985) Mol 2. H o l m g r e n S, Grove DJ, 3. J e n s e n J, Holmgren 20:25-33 4. Grove DJ, H o l m g r e n S,
Physiol 8:119-130 N i l s s o n S (1985) N e u r o s c i e n c e 14:683-693 S, J6nsson A-C (1987) J A u t o n o m N e r v Syst to be p u b l i s h e d
IN
THE
FISH
GUT: M E C H A N I S M OF A C T I O N AND R E L E A S E ON
J. JENSEN, A.-C. JONSSON and S. H O L M G R E N Comparative Neuroscience Unit, Department U n i v e r s i t y of G6teborg, G6teborg, Sweden.
of
Zoophysiology,
Nerve fibres and endocrine cells c o n t a i n i n g a substance P- (SP) like peptide have been d e m o n s t r a t e d in the g a s t r o i n t e s t i n a l canal of several fish species. However, the actual function and the m e c h a n i s m of action of this peptide in the fish gut is less w e l l known. In all species we have studied so far SP is found to have an e x c i t a t o r y action on gut preparations, but the m e c h a n i s m s of action appear to vary between organs and species. Thus, in the gut of the spiny dogfish, Squalus acanthias, SP acts d i r e c t l y on the smooth m u s c l e cells (i), while in the stomach of the rainbow trout, Salmo gairdneri, the e x c i t a t o r y effect of exogenous SP can be c o r r e l a t e d to a release of 5-hydroxytryptamine as well as, w h e n using high concentrations, a direct effect on smooth muscle (2). In v a s c u l a r l y perfused p r e p a r a t i o n s of the intestine of the cod, Gadus morhua, SP in low c o n c e n t r a t i o n s appears to exert its effect via both c h o l i n e r g i c and serotonergic pathways in addition to a direct effect o b t a i n e d w i t h high c o n c e n t r a t i o n s of SP (3). Experiments p e r f o r m e d on the v a s c u l a r l y p e r f u s e d stomach of the cod show that the contractions produced by SP is u n a f f e c t e d by t r e a t m e n t w i t h atropine, m e t h y s e r g i d e or tetrodotoxin, s u g g e s t i n g the p r e s e n c e of only a direct effect of SP in the cod stomach. This finding points to an interesting difference between the action of SP in the cod stomach and the rainbow trout stomach where an a d d i t i o n a l pathway via serotonergic neurons is present. It also shows that the pathways may be different between the stomach and the intestine in the same species. In studies of the effect of SP on a p h y l o g e n e t i c a l l y i n t e r e s t i n g species, the south american lungfish (Lepidosiren paradoxa) SP was found to p r o d u c e dose-dependent contractions on circular m u s c l e strip preparations from the intestine. The contractions were u n a f f e c t e d by treatment w i t h atropine, m e t h y s e r g i d e or tetrodotoxin, indicating an action d i r e c t l y on the smooth m u s c l e cells only similar to the situation in the gut of the spiny dogfish. It m a y be hypothesized that the direct action of SP o b s e r v e d in all fish species s t u d i e d so far is a general and primitive mechanism. Experiments w i t h the v a s c u l a r l y p e r f u s e d rainbow trout stomach have shown that m e c h a n i c a l d i s t e n s i o n initiates a c o n t r a c t i l e a c t i v i t y which is b l o c k e d by tetrodotoxin as well as by a c o m b i n a t i o n of serotonergic and cholinergic antagonists (4). P r e l i m i n a r y results now show that SP-like m a t e r i a l is c o n t i n u o u s l y r e l e a s e d from the stomach into the vascular perfusate. On m e c h a n i c a l d i s t e n s i o n of the stomach an increase in the outflow of i m m u n o r e a c t i v e m a t e r i a l is observed further i n d i c a t i n g the involvement of a SP-like peptide in the e x c i t a t o r y control of the rainbow trout stomach. i. H o l m g r e n S (1985) Mol 2. H o l m g r e n S, Grove DJ, 3. J e n s e n J, Holmgren 20:25-33 4. Grove DJ, H o l m g r e n S,
Physiol 8:119-130 N i l s s o n S (1985) N e u r o s c i e n c e 14:683-693 S, J6nsson A-C (1987) J A u t o n o m N e r v Syst to be p u b l i s h e d