Myoinhibitory neuropeptides in the American cockroach☆
Introduction
The neuropeptide pattern in neurohaemal organs of the American cockroach, Periplaneta americana, was intensively investigated in the last few years. Hereby, we concentrated on myotropic neuropeptides of the retrocerebral complex and abdominal perisympathetic organs which are the major neurohaemal release sites of the brain/subesophageal ganglion and ventral nerve cord, respectively. Two general conclusions can be drawn from these studies. Firstly, members of all myostimulatory neuropeptide families which were initially isolated from head extracts of Leucophaea maderae [12] are also present in considerable amounts in the corpora cardiaca/allata complex (CC/CA) of the American cockroach. This fact supports the idea that these peptides will be released into the circulation. Secondly, the abdominal perisympathetic organs (PSOs) were found to contain a neuropeptide pattern totally different from that of the retrocerebral complex. Altogether, not less than five different neuropeptide families with myostimulatory properties were identified from neurohaemal organs of the American cockroach, namely kinins, sulfakinins, pyrokinins, corazonin, and periviscerokinins [27].
A detailed knowledge of the structures and the distribution of myotropins in neurohaemal organs of P. americana makes it possible to investigate fluctuations in the amount of these peptides during development and certain physiological events. Muscle activity, however, can also be influenced by myoinhibitory neurohormones. For an understanding of the coordinated action of myotropic neurohormones it is therefore necessary to include myostimulatory peptides, as well as myoinhibitors. No myoinhibitory peptides have been reported from the American cockroach thus far. To fill this gap, we isolated and identified myoinhibitors from neurohaemal organs of P. americana. These putative hormones include leucomyosuppressin (LMS), initially isolated from L. maderae [11] and a novel member of myoinhibitory peptides (Pea-MIP). The efficacy of the different myoinhibitors of the American cockroach in visceral muscle assays is compared. During these experiments we also tested allatostatins which were known to inhibit spontaneous activity of the foregut of Leucophaea maderae [6].
Section snippets
Animals
Cockroaches were reared under a 12-h light, 12-h dark photoperiod at a constant temperature of 28°C. Only adult males four to six weeks after their last moult were used throughout the experiments. They were fed rat food pellets and had free access to water.
Bioassays
The assays on the isolated visceral muscles were performed as previously described [20]. The insect saline (pH 7.25) contained NaCl (8.19 g/liter), KCl (0.37 g/liter), CaCl2 (0.56 g/liter), MgCl2 × 6H2O (0.2 g/liter), glucose (0.9 g/liter)
Isolation and structural elucidation of leucomyosuppressin
An extract of 800 CC/CA was chromatographed on an Alphasil C18 column with TFA as organic modifier. The resulting fractions between 10 and 50 min were collected manually and then tested for myotropic activity on different visceral muscles, namely the hyperneural muscle, heart, and hindgut. The purification of peptides with myostimulatory properties has been described elsewhere (see 27). Only one fraction (Fig. 1 ) clearly inhibited the activity of isolated heart and hindgut. This fraction was
Discussion
The only myoinhibitor, which was highly effective in all visceral muscle assays used during this study, was LMS. Action, biologically active core sequence, and distribution of this peptide was extensively investigated in blaberoid cockroaches [1], [3], [5], [9], [16], [17], [18]. LMS seems to be conservative not only in its function as myoinhibitor in insects but also in its sequence which is obviously highly conserved in cockroaches and related insect orders. These properties resemble those of
Acknowledgements
We thank Mrs. Virginia Johnson (Protein Technologies Laboratory, Texas A & M University, College Station) for excellent sequence analysis; Mrs. Renate Winkler, Mrs. Erika Krause and Mrs. Ch. Raue (Institut für Allgemeine Zoologie und Tierphysiologie Jena, Germany) for perfect technical assistance. This study was supported with a post-doc fellowship of the German Academy of Science Leopoldina (LPD 1997, to RP) and grants from Deutsche Forschungsgemeinschaft (Predel 595/1–1,2; Eckert 122/4–1).
References (38)
- et al.
Molecular characterization of the inhibitory myotropic peptide leucomyosuppressin
Peptides
(1997) - et al.
The identification of two myoinhibitory peptides, with sequence similarities to the galanins, isolated from the ventral nerve cord of Manduca sexta
Regul Peptides
(1995) - et al.
Comparative effects of leucomyosuppressin on the visceral muscle systems of the cockroach Leucophaea maderae
Comp Biochem Physiol C
(1991) - et al.
Characterization of the gene for leucomyosuppressin and its expression in the brain of the cockroach Diploptera punctata
Insect Biochem Molec Biol
(1996) - et al.
A family of neuropeptides that inhibit juvenile hormone biosysnthesis in the cricket, Gryllus bimaculatus
J Biol Chem
(1995) - et al.
Structure-activity relationships for inhibitory insect myosuppressinscontrast with the stimulatory sulfakinins
Peptides
(1993) - et al.
Isolation and structural elucidation of two pyrokinins from the retrocerebral complex of the American cockroach
Peptides
(1997) - et al.
Isolation and structural elucidation of eight kinins from the retrocerebral complex of the American cockroach
Regul Peptides
(1997) - et al.
Isolation of periviscerokinin-2 from the abdominal perisympathetic organs of the American cockroach, Periplaneta americana
Peptides
(1998) - et al.
Allatostatins from retrocerebral complex and antennal pulsatile organ of the American cockroach, Periplaneta americana, aided by matrix-assisted laser desorption/ionization-time-of-flight mass spectrometry
Regul Peptides
(1999)
Isolation, identification and synthesis of locustamyoinhibiting peptide (Lom-MIP), a novel biologically active neuropeptide from Locusta migratoria
Regul Peptides
Immunocytochemical distribution of locustamyoinhibiting peptide (Lom-MIP) in the nervous system of Locusta migratoria
Regul Peptides
Peptides in the locusts, Locusta migratoria and Schistocerca gregaria
Peptides
Modulation of cardiac rhythm by allatostatins in the cockroach Blattella germanica (L.) (Dictyoptera, Blattellidae)
J Ins Physiol
Comparison of the allatostatin neuropeptide precursors in the distantly related cockroaches Periplaneta americana and Diploptera punctata
Eur J Biochem
Innervation of the foregut of the cockroach Leucophaea maderae and inhibition of spontaneous contractile activity by callatostatin neuropeptides
Physiol Entomol
Periviscerokinin-like immunoreactivity in the nervous system of the American cockroach
Cell Tissue Res
In situ hybridization analysis of leucomyosuppressin mRNA expression in the cockroach, Diploptera punctata
J Comp Neurol
Cited by (105)
The combination of NlMIP and Gαi/q coupled-receptor NlA10 promotes abdominal vibration production in female Nilaparvata lugens (Stål)
2023, Journal of Integrative AgricultureFeeding-modulating neuropeptides and peptide hormones in insects
2019, Advances in Insect PhysiologyCitation Excerpt :AST-C derived from the FrG has an inhibitory activity on foregut contraction in L. oleracea (Audsley et al., 2001). LMS inhibited foregut contraction in P. americana (Predel et al., 2001b), L. maderaea (Cook and Wagner, 1991), and B. germanica (Aguilar et al., 2004). In P. americana, AST-C also exhibited inhibitory activity on foregut contraction (Predel et al., 2001b).
Myotropic activity of allatostatins in tenebrionid beetles
2018, NeuropeptidesCitation Excerpt :Allatostatins from all three groups exhibit strong myoinhibitory properties towards the visceral muscles of insects. FGL/ASTs regulate the contractile activity of the gut muscles and heart (Audsley et al., 2005; Duve et al., 2000; Duve et al., 1999; Hergarden et al., 2012; Vilaplana et al., 1999), MIP/ASTs act as myoinhibitors of the ovary and hindgut muscles (Blackburn et al., 2001; Blackburn et al., 1995; Lange et al., 2012; Predel et al., 2001; Schoofs et al., 1991; Sedra et al., 2015) and PISCF/ASTs are potent myoinhibitors of the foregut and heart contractions (Matthews et al., 2007; Price et al., 2002). However little is known about the activity of allatostatins and their myoactivity in beetles, the largest insect order.
Discovery and structure-activity relationships of pyrazolodiazepine derivatives as the first small molecule agonists of the Drosophila sex peptide receptor
2015, Bioorganic and Medicinal ChemistryFunctional characterization and expression analysis of the myoinhibiting peptide receptor in the Chagas disease vector, Rhodnius prolixus
2015, Molecular and Cellular Endocrinology