Isolation and characterization of a diuretic peptide common to the house fly and stable fly

doi:10.1016/0196-9781(94)90059-0

Peptides

Volume 15, Issue 6, 1994, Pages 971-979

https://doi.org/10.1016/0196-9781(94)90059-0 Get rights and content

Abstract

An identical CRF-related diuretic peptide (Musca-DP) was isolated and characterized from whole-body extracts of the house fly, Musca domestica, and stable fly, Stomoxys calcitrans. The peptide stimulates cyclic AMP production in Manduca sexta Malpighian tubules and increases the rate of fluid secretion by isolated Musca domestica tubules. The 44-residue peptide, with a mol.wt. of 5180, is amidated, and has the primary structure: NKPSLSIVNPLDVLRQRLLLEIARRQMKENTRQVELNRAILKNV-NH₂. Musca-DP has a high percentage of sequence identity with other characterized CRF-related insect diuretic peptides.

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Can BRET-based biosensors be used to characterize G-protein mediated signaling pathways of an insect GPCR, the Schistocerca gregaria CRF-related diuretic hormone receptor?
2020, Insect Biochemistry and Molecular Biology
Citation Excerpt :
While the physiological role of Schgr-DH was previously investigated in S. gregaria (Van Wielendaele et al., 2012), its receptor was never molecularly characterized. Moreover, this newly characterized receptor, Schgr-CFR-DHR, was also chosen as a proof-of-principle, since it is well-documented that CRF-DHs exert effects on their cellular targets through their interaction with receptors belonging to the secretin receptor-related GPCR family (family B), for which cAMP has been identified to act as an intracellular second messenger of CRF-DH in numerous insects, both in vivo and in vitro (Audsley et al., 1995; Baldwin et al., 2001; Clottens et al., 1994; Hector et al., 2009; Johnson et al., 2004; Lee et al., 2016; Reagan, 1996; Tobe et al., 2005). In addition, the production of primary urine is dependent on cAMP, which increases cationic transport (such as K+ and Na+) into the Malpighian tubules (Beyenbach, 1995; O'Donnell et al., 1996).
G protein-coupled receptors (GPCRs) are membrane-bound receptors that are considered prime candidates for the development of novel insect pest management strategies. However, the molecular signaling properties of insect GPCRs remain poorly understood. In fact, most studies on insect GPCR signaling are limited to analysis of fluctuations in the secondary messenger molecules calcium (Ca²⁺) and/or cyclic adenosine monophosphate (cAMP). In the current study, we characterized a corticotropin-releasing factor-related diuretic hormone (CRF-DH) receptor of the desert locust, Schistocerca gregaria. This Schgr-CRF-DHR is mainly expressed in the nervous system and in brain-associated endocrine organs. The neuropeptide Schgr-CRF-DH induced Ca²⁺-dependent aequorin-based bioluminescent responses in CHO cells co-expressing this receptor with the promiscuous Gα₁₆ protein. Furthermore, when co-expressed with the cAMP-dependent bioluminescence resonance energy transfer (BRET)-based CAMYEL biosensor in HEK293T cells, this receptor elicited dose-dependent agonist-induced responses with an EC₅₀ in the nanomolar range (4.02 nM). In addition, we tested if vertebrate BRET-based G protein biosensors, can also be used to detect direct Gα protein subunit activation by an insect GPCR. Therefore, we analyzed ten different human BRET-based G protein biosensors, representing members of all four Gα protein subfamilies; Gα_s, Gα_i/o, Gα_q/11 and Gα_12/13. Our data demonstrate that stimulation of Schgr-CRF-DHR by Schgr-CRF-DH can dose-dependently activate Gα_i/o and Gα_s biosensors, while no significant effects were observed with the Gα_q/11 and Gα_12/13 biosensors. Our study paves the way for future biosensor-based studies to analyze the signaling properties of insect GPCRs in both fundamental science and applied research contexts.
Isolation and characterization of the corticotropin-releasing factor-related diuretic hormone receptor in Rhodnius prolixus
2016, Cellular Signalling
Citation Excerpt :
Since then, other CRF/DHs have been sequenced from Periplaneta americana[14], L. migratoria[15], Drosophila melanogaster[16], R. prolixus[17]and a second CRF/DH from M. sexta[18]. CRF/DHs have been shown to increase fluid excretion in vivo and in vitro and to increase cAMP content in MTs [14,15,19,20]. Besides diuretic effects, CRF/DH has been shown to induce satiety in M. sexta and Schistocerca gregaria[21,22], initiate pre-ecdysis behavior in M. sextra[23] retard reproduction in Schistocerca gregaria[22], modulate normal rest: activity rhythms, as well as control sperm ejection and storage in D. melanogaster[24,25].
Rhodnius prolixus, the vector of human Chagas disease, is a hemipteran insect that undergoes rapid post-feeding diuresis following ingestion of a blood meal that can be up to 10 times its initial body weight. Corticotropin-releasing factor-related diuretic hormone (Rhopr-CRF/DH) and serotonin are neurohormones that are synergistic in increasing rates of fluid secretion by Malpighian tubules during this rapid post-feeding diuresis. A Rhopr-CRF/DH receptor transcript has now been isolated and characterized from fifth instar R. prolixus. The receptor is a family B1 (secretin) G protein-coupled receptor (GPCR) and was deorphaned in a heterologous cellular system using Chinese hamster ovary (CHO) cells stably expressing a promiscuous G-protein (Gα16). This assay was also used to demonstrate the presence of Rhopr-CRF/DH in the haemolymph of R. prolixus in response to blood-gorging. Two additional cell lines were used in this heterologous assay to verify that the cyclic adenosine monophosphate (cAMP) pathway and not the inositol triphosphate (IP₃) pathway was stimulated upon activation of the receptor. Lastly, quantitative PCR demonstrated strong receptor expression in digestive tissues, upper Malpighian tubules and reproductive tissues. Identification of the Rhopr-CRF/DH receptor now provides tools for a more detailed understanding into the precise coordination of diuresis and other physiological processes in R. prolixus.
Water Homeostasis and Osmoregulation as Targets in the Control of Insect Pests
2013, Advances in Insect Physiology
Citation Excerpt :
Later, CRF-like peptides in other insect species were reported. Identical peptide sequences were isolated and identified in the house fly Musca domestica and the stable fly Stomoxys calcitrans (Clottens et al., 1994), and an almost identical sequence of the above dipterans was described for D. melanogaster (Drome-DH44) neuropeptide (Cabrero et al., 2002). Two CRF-like DH peptides, isolated from T. molitor (Tenmo-DH37 and Tenmo-DH47) (Furuya et al., 1995, 1998), are highly potent neurohormones stimulating diuresis in isolated MTs at EC50 values of 12 and 27 nM, respectively (Wiehart et al., 2002), and two similar DHs (DH37 and DH47) were isolated from the closely related T. castaneum species (Li et al., 2008).
Insects, which are characterized by a comparative large surface area versus a relative small size, are generally challenged by osmotic stresses and, in particular, when exposed to hot, dry, salty and freezing environments. Furthermore, insects feeding on large volumes of fluids such as blood, phloem-sap or nectar confront a different type of osmotic challenges. The digestive tract and associated Malpighian tubules are the major organs active in alleviating such challenges. Various passive and active transepithelial transport facilitators, such as pumps, ion exchangers, co-transporters and ion and water channels (aquaporins), are under the hormonal control by biogenic amines and various neuropeptides. Interaction of the neurohormones with their respective receptors induces cascade pathways that trigger diuretic or antidiuretic responses. Since water homeostasis and osmoregulation are crucial for the survival of insects, the elaborate physiological mechanisms that have evolved in maintaining balance of water and electrolytes are potential targets for interference. Synthesis of metabolically and environmentally biostable neuropeptidergic analogs in combination with receptor assay-guided structure–activity studies could be instrumental in discovering highly potent molecular leads that are vital in generating efficient and selective insect control agents.
Hormones Controlling Homeostasis in Insects
2012, Insect Endocrinology
This chapter discusses the hormonal controllers of the supply of endogenous metabolic energy and the hormonal control of fluid and electrolyte balance. Due to the wide variety of environmental niches inhabited by insects, the mechanisms for control of homeostasis may show considerable variation between genera, although basic underlying themes are conserved. Insects are an extremely ancient grouping of organisms, with short life spans and frequently multiple generations per year. This rapid rate of evolution is reflected in differences in the nature of main substrates used as metabolic fuels for flight; in considerable interspecific diversity in structure between hormones in certain families that regulate homeostasis, especially diuretic hormones; and also in differences in which family of diuretic hormones appears to dominate as the major controllers of fluid excretion between different genera. It has also become apparent that signal transduction pathways for a given family of homeostatic hormones may differ between genera.
Hormones Controlling Homeostasis in Insects
2011, Insect Endocrinology
This chapter discusses the hormonal controllers of the supply of endogenous metabolic energy and the hormonal control of fluid and electrolyte balance. Due to the wide variety of environmental niches inhabited by insects, the mechanisms for control of homeostasis may show considerable variation between genera, although basic underlying themes are conserved. Insects are an extremely ancient grouping of organisms, with short life spans and frequently multiple generations per year. This rapid rate of evolution is reflected in differences in the nature of main substrates used as metabolic fuels for flight; in considerable interspecific diversity in structure between hormones in certain families that regulate homeostasis, especially diuretic hormones; and also in differences in which family of diuretic hormones appears to dominate as the major controllers of fluid excretion between different genera. It has also become apparent that signal transduction pathways for a given family of homeostatic hormones may differ between genera.
Phylogeny of the corticotropin-releasing factor family of peptides in the metazoa
2006, General and Comparative Endocrinology
The corticotropin-releasing factor (CRF) family of peptides consists of four distinct paralogs found on separate chromosomes in vertebrates. Among invertebrates, the family has been relatively well characterized in the insects where at least 2 or 3 paralogs, a CRF-binding protein ortholog and a CRF receptor variant have been found. The conservation of structure and function of this system in insects imply that the CRF system evolved in ancestral species well before the Precambrian explosion. The CRF family peptides association with diuresis and feeding may have developed early in its evolution. However, CRF’s role in the hypothalamo–pituitary–adrenal axis and regulation of the glucocorticoids in association with energy metabolism appears to have developed in the chordate lineage.

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ArticleIsolation and characterization of a diuretic peptide common to the house fly and stable fly

Abstract

Ion and water transport across epithelia

Metabolic pathways of the isolated Malpighian tubules of the blowfly functioning in an artificial medium

J. Insect Physiol.

Urine formation by the Malpighian tubules of Calliphora. I Cations

J. Exp. Biol.

Urine formation by the Malpighian tubules of Calliphora. II Anions

J. Exp. Biol.

Isolation and identification of a new diuretic peptide from the tobacco hornworm, Manduca sexta

Biochem. Biophys. Res. Commun.

Fluid secretion by single isolated Malpighian tubules of the house cricket, Acheta domesticus, and their response to diuretic hormone

Physiol. Entomol.

An evaluation of the role of cyclic AMP as an intracellular second messenger in Malpighian tubules of the house cricket, Acheta domesticus

J. Insect Physiol.

The diuretic activity of cephalomyotropic neuropeptides, the achetakinins, on isolated Malpighian tubules of the house cricket, Acheta domesticus

J. Insect Physiol.

Diuretic peptides in the house cricket, Acheta domesticus (L.): A possible dual control of Malpighian tubules

Fluid secretion by isolated Malpighian tubules of the house fly Musca domestica

J. Insect Physiol.

Diuresis in the tsetse fly Glossina austeni

J. Exp. Biol.

The control of diuresis in the tsetse fly Glossina austeni: A preliminary investigation of the diuretic hormone

J. Exp. Biol.

Leucokinins, a new family of ion transport stimulators and inhibitors in insect Malpighian tubules

Life Sci.

Isolation and amino acid sequence of urotensin I, a vasoactive and ACTH-releasing neuropeptide, from the carp (Cyprinus carpio) urophysis

Peptides

Inhibition of desert locust (Schistocerca gregaria) Malpighian tubule fluid secretion by destruxins, cyclic peptide from the insect pathogenic fungus Metarhizium anisopliae

J. Insect Physiol.

Isolation and identification of a diuretic hormone from the tobacco hornworm, Manduca sexta

Isolation and characterization of a diuretic peptide from Acheta domesticus. Evidence for a family of insect diuretic peptides

Biol. Chem. Hoppe Seyler

Article
Isolation and characterization of a diuretic peptide common to the house fly and stable fly