Allatostatin modulates skeletal muscle performance in crustaceans through pre‐ and postsynaptic effects

Abstract

Allatostatins, originally identified in insects as peptide inhibitors of juvenile hormone biosynthesis, are regarded as potent inhibitory regulators of intestinal muscles in insects and crustaceans. However, accumulating data indicate that allatostatins might also be involved in modulation of skeletal neuromuscular events. We show that most ganglia of two isopod crustaceans (Idotea baltica and I. emarginata) contain pairs of large, allatostatin-immunoreactive motor neurons which supply several segmental muscles. Among them are the dorsal extensor muscles, of which some fibres receive immunoreactive, varicose innervation. We demonstrate, on identified muscle fibres, that allatostatin exerts a twofold inhibitory effect: it reduces contractions of single voltage-clamped fibres, and it decreases the amplitude of evoked excitatory junctional currents recorded from individual release boutons. No change in excitation-contraction threshold or in passive membrane parameters was observed. As the amplitude of miniature currents generated by spontaneously released single transmitter quanta was not changed, the inhibitory effect of the peptide on junctional currents must be of presynaptic origin. Supportive results were obtained on leg muscles of the crab Eriphia spinifrons, where allatostatin decreased evoked synaptic currents by reducing the mean number of transmitter quanta released by presynaptic depolarization without affecting the amplitudes of currents generated by single quanta. This effect of allatostatin was similar for two functionally different neurons, the slow and the fast closer excitor. The data show that allatostatin occurs in identified motor neurons of Idotea and exerts complementary pre- and postsynaptic modulatory effects which reduce muscle responses. Thus, allatostatin counteracts the effects of another neuropeptide, proctolin, which is also present in Idotea and causes potentiating effects on the same muscle fibres.

Inter-animal variability in the effects of C-type allatostatin on the cardiac neuromuscular system in the lobster Homarus americanus

“…In contrast to our predictions, the peptide did not alter contraction in response to constant stimulation in any of the preparations, indicating that C-AST does not directly modulate either muscle contraction or the neuromuscular junction. This contrasts with the effects of A-ASTs, which have been shown to modulate muscle contraction both pre-and postsynaptically (Jorge-Rivera and Marder, 1997;Kreissl et al, 1999). Although there were no direct effects of C-AST on muscle contraction, we found that C-AST's ability to decrease contraction amplitude was in fact due to an indirect effect at the neuromuscular junction; namely, a decrease in facilitation resulting from the decreased cycle frequency, as has been seen in other studies of this system (Mahadevan et al, 2004) as well as other crustacean neuromuscular systems (Jorge-Rivera et al, 1998;Mercier and Wilkins, 1984;Morris and Hooper, 1998).…”

“…The effects of a given neuromodulator on a specific pattern generator often vary somewhat among animals, but most studies have focused on mean responses, and have reported similarities in the direction of these effects across the animal population Kreissl et al, 1999;Mercier et al, 2003;Richards et al, 2003;Stevens et al, 2008;Stevens et al, 2009). While a number of factors could potentially underlie the quantitative variability in responses across animals, differences in response to a given modulator have most often been attributed to the 'state' of the system; this in turn is often reflected in the starting parameters of the pattern, notably cycle frequency (Dickinson et al, 2001;Fu et al, 2007;Medler and Hulme, 2009;Nadim et al, 2008;Nagy and Dickinson, 1983;Nusbaum and Marder, 1989b;Sargeant, 2007).…”

“…Second, stretch-sensitive dendrites on the neurons of the CG are thought to play a generally excitatory role (Alexandrowicz, 1932;Garcia-Crescioni et al, 2010;Sakurai and Wilkens, 2003). While there is considerable evidence indicating that crustacean neuromuscular junction (Kreissl et al, 1999;Stevens et al, 2009) and muscle, including cardiac muscle (Dickinson, 1995;Kravitz et al, 1984;Kreissl et al, 1999;Stevens et al, 2009), are modulated, it is not yet clear whether the feedback pathways themselves are likewise subject to modulation.…”

Identification of SYWKQCAFNAVSCFamide: a broadly conserved crustacean C-type allatostatin-like peptide with both neuromodulatory and cardioactive properties

“…cockroaches, crickets and termites (Stay and Tobe, 2007). A-type peptides have also been found in a number of crustaceans (Duve et al, 1997;Dircksen et al, 1999;Duve et al, 2002;Huybrechts et al, 2003;Fu et al, 2005;Yasuda-Kamatani and Yasuda, 2006;Yin et al, 2006;Christie et al, 2008a;Ma et al, 2008;Gard et al, 2009;Ma et al, 2009), where they have been shown to function as locally released and/or hormonally delivered neuro/myomodulators (Skiebe and Schneider, 1994;Jorge-Rivera and Marder, 1997;Jorge-Rivera et al, 1998;Dircksen et al, 1999;Kreissl et al, 1999;Birmingham et al, 2003;Billimoria et al, 2006;Cruz-Bermúdez and Marder, 2007). Molecular, biochemical and mass spectral analyses have shown that multiple isoforms of A-type peptides are common in both insect and crustacean species, with multiple peptides encoded by the known arthropod A-AST prepro-hormones (e.g.…”

The neuropeptide proctolin potentiates contractions and reduces cGMP concentration via a PKC-dependent pathway

“…techniques To expose the extensor muscle (for anatomical details, see Kreissl et al, 1999), the preparation was pinned with the ventral side exposed in a Sylgard-coated dish. Sternites with attached flexor muscles and the ventral nerve cord were removed.…”