The antidiuretic neurohormone RhoprCAPA-2 downregulates fluid transport across the anterior midgut in the blood-feeding insect Rhodnius prolixus

Ianowski, Juan P.; Paluzzi, Jean‐Paul; Brugge, V.A. Te; Orchard, Ian

doi:10.1152/ajpregu.00208.2009

Cited by 32 publications

(26 citation statements)

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“…In this study, we show expression data for a CAPA receptor homolog in R. prolixus that correlates with the physiological roles identified previously in the MTs (9) and anterior midgut (4,11). Interestingly, we have identified that additional tissues that comprise the alimentary canal contain appreciable levels of CAPA receptor expression, namely in oesophagus posterior midgut, and hindgut, suggesting additional targets for the endogenous CAPA peptides.…”

Section: Discussionsupporting

confidence: 86%

“…The capa-r1 expressed receptor was activated by low concentrations of RhoprCAPA-α2 with an EC 50 value comparable to that determined for other heterologously expressed CAPA receptors (13,14); however, this EC 50 value does not match the observed in vitro potency observed for RhoprCAPA-α2, which lies in the low nanomolar range (4,9), and this difference may be a result of poor coupling of the receptor to the calcium mobilization pathway leading to nonoptimal activation of the aequorin reporter. In support of this prediction, our recent physiological results suggest that calcium is not involved in eliciting the natural RhoprCAPA-α2 inhibitory effect on the anterior midgut (4); thus, the endogenous receptor coupling in vivo differs from that in our heterologous expression system.…”

Section: Discussionmentioning

confidence: 65%

“…In dipterans, it is unknown if these peptides regulate any other tissue in addition to the MTs. In R. prolixus, we have recently shown that the antidiuretic hormone, RhoprCAPA-α2(-β2), is also a potent inhibitor of anterior midgut absorption stimulated by 5-HT (4,11).…”

Section: Discussionmentioning

confidence: 99%

“…The parasitic protozoan, Trypanosoma cruzi, is transmitted to humans in the urine, and so diuresis controls the transmission of Chagas' disease. Neurohormones control hemolymph salt and water homeostasis by acting on the anterior midgut and MTs (3,4). The insect CAPA peptides, some of which are also referred to as periviscerokinins, usually contain the consensus carboxy terminal sequence FPRV-NH 2 .…”

mentioning

confidence: 99%

“…Each gene codes for three peptides, two of them being CAPArelated peptides and the third being a pyrokinin-related peptide. The second encoded peptide in each prepropeptide, Rhopr-CAPA-α2(-β2), is identical in sequence in each paralog (9,10) and has been shown to directly inhibit 5HT-stimulated secretion by the MTs (9, 10), as well as absorption of water and ions by the anterior midgut (4,11). The availability of completed insect genomes has made the identification of receptors for these neuroendocrine factors more feasible.…”

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confidence: 99%

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Isolation, expression analysis, and functional characterization of the first antidiuretic hormone receptor in insects

Paluzzi

Park

Nachman

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Diuresis following blood-gorging in Rhodnius prolixus is the major process leading to the transmission of Chagas' disease. We have cloned the cDNA of the first receptor known to be involved in an antidiuretic strategy in insects, a strategy that prevents diuresis. This receptor belongs to the insect CAPA receptor family known in other insects to be activated by peptides encoded within the capability gene. We characterize the expression profile in fifthinstars and find expression is localized to the alimentary canal. Highest transcript levels are found in Malpighian tubules and the anterior midgut, which are known targets of the antidiuretic hormone, RhoprCAPA-α2. Two transcripts were identified, capa-r1 and capa-r2; however, the latter encodes an atypical G proteincoupled receptor lacking a region ranging between the first and second transmembrane domain. Our heterologous expression assay revealed the expressed capa-r1 receptor is activated by Rhopr-CAPA-α2 (EC 50 = 385nM) but not by RhoprCAPA-α1. Structural analogs of the inactive RhoprCAPA-α1 were capable of activating the expressed capa-r1 receptor, confirming the importance of the C-terminal consensus sequence common to CAPA-related peptides. In addition, this receptor has some sensitivity to the pyrokininrelated peptide, RhoprCAPA-αPK1, but with an efficacy ≈40-fold less than RhoprCAPA-α2. Other peptides belonging to the PRXamide superfamily were inactive on the capa-r1 receptor. Taken together, the neuroendocrinological relevance of this receptor in facilitating the antidiuretic strategy in R. prolixus may make this receptor a useful target for development of agonists or antagonists that could help influence the transmission of Chagas' disease that occurs during diuresis in this medically important insectdisease vector.CAPA | Chagas' | G protein-coupled receptor | neurohormone | neuropeptide A major physiological process that allows insects to adopt a variety of feeding strategies and environmental niches is their ability to regulate water and ion composition in their hemolymph. This process involves control over primary urine production via the insect kidney equivalent, the Malpighian (renal) tubules (MTs) and, in a number of insects, the reabsorption of essential salts and water from the hindgut before the final excretae is voided. Insect neurohormones, including peptides and biogenic amines, together with their cognate receptors, carry out an essential role in these and related physiological processes, and numerous neuroendocrine factors regulating fluid and ion balance in insects have been described (see ref.

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Section: Discussionsupporting

confidence: 86%

Section: Discussionmentioning

confidence: 65%

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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Isolation, expression analysis, and functional characterization of the first antidiuretic hormone receptor in insects

Paluzzi

Park

Nachman

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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EFFECTS OF DIURETIC HORMONE 31, DROSOKININ, AND ALLATOSTATIN A ON TRANSEPITHELIAL K⁺TRANSPORT AND CONTRACTION FREQUENCY IN THE MIDGUT AND HINDGUT OF LARVALDrosophila melanogaster

Vanderveken

O’Donnell

2014

Arch Insect Biochem Physiol

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Recent studies have identified paracrine and endocrine cells in the midgut of larval Drosophila melanogaster as well as midgut and hindgut receptors for multiple neuropeptides implicated in the control of fluid and ion balance. Although the effects of diuretic factors on fluid secretion by isolated Malpighian tubules of D. melanogaster have been examined extensively, relatively little is known about the effects of such factors on gut peristalsis or ion transport across the gut. We have measured the effects of diuretic hormone 31 (DH31), drosokinin and allatostatin A (AST-A) on both K(+) transport and muscle contraction frequency in the isolated gut of larval D. melanogaster. K(+) absorption across the gut was measured using K(+) -selective microelectrodes and the scanning ion-selective electrode technique. Allatostatin A (AST-A; 1 μM) increased K(+) absorption across the anterior midgut but reduced K(+) absorption across the copper cells and large flat cells of the middle midgut. AST-A strongly inhibited gut contractions in the anterior midgut but had no effect on contractions of the pyloric sphincter induced by proctolin. DH31 (1 μM) increased the contraction frequency in the anterior midgut, but had no effect on K(+) flux across the anterior, middle, or posterior midgut or across the ileum. Drosokinin (1 μM) did not affect either contraction frequency or K(+) flux across any of the gut regions examined. Possible functions of AST-A, DH31, and drosokinin in regulating midgut physiology are discussed.

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Osmoregulation and Excretion

Larsen

Deaton

Onken

et al. 2014

Comprehensive Physiology

185

141

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The article discusses advances in osmoregulation and excretion with emphasis on how multicellular animals in different osmotic environments regulate their milieu intérieur. Mechanisms of energy transformations in animal osmoregulation are dealt with in biophysical terms with respect to water and ion exchange across biological membranes and coupling of ion and water fluxes across epithelia. The discussion of functions is based on a comparative approach analyzing mechanisms that have evolved in different taxonomic groups at biochemical, cellular and tissue levels and their integration in maintaining whole body water and ion homeostasis. The focus is on recent studies of adaptations and newly discovered mechanisms of acclimatization during transitions of animals between different osmotic environments. Special attention is paid to hypotheses about the diversity of cellular organization of osmoregulatory and excretory organs such as glomerular kidneys, antennal glands, Malpighian tubules and insect gut, gills, integument and intestine, with accounts on experimental approaches and methods applied in the studies. It is demonstrated how knowledge in these areas of comparative physiology has expanded considerably during the last two decades, bridging seminal classical works with studies based on new approaches at all levels of anatomical and functional organization. A number of as yet partially unanswered questions are emphasized, some of which are about how water and solute exchange mechanisms at lower levels are integrated for regulating whole body extracellular water volume and ion homeostasis of animals in their natural habitats. © 2014 American Physiological Society.

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The antidiuretic neurohormone RhoprCAPA-2 downregulates fluid transport across the anterior midgut in the blood-feeding insect Rhodnius prolixus

Cited by 32 publications

References 57 publications

Isolation, expression analysis, and functional characterization of the first antidiuretic hormone receptor in insects

Isolation, expression analysis, and functional characterization of the first antidiuretic hormone receptor in insects

EFFECTS OF DIURETIC HORMONE 31, DROSOKININ, AND ALLATOSTATIN A ON TRANSEPITHELIAL K⁺TRANSPORT AND CONTRACTION FREQUENCY IN THE MIDGUT AND HINDGUT OF LARVALDrosophila melanogaster

Osmoregulation and Excretion

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The antidiuretic neurohormone RhoprCAPA-2 downregulates fluid transport across the anterior midgut in the blood-feeding insect Rhodnius prolixus

Cited by 32 publications

References 57 publications

Isolation, expression analysis, and functional characterization of the first antidiuretic hormone receptor in insects

Isolation, expression analysis, and functional characterization of the first antidiuretic hormone receptor in insects

EFFECTS OF DIURETIC HORMONE 31, DROSOKININ, AND ALLATOSTATIN A ON TRANSEPITHELIAL K+TRANSPORT AND CONTRACTION FREQUENCY IN THE MIDGUT AND HINDGUT OF LARVALDrosophila melanogaster

Osmoregulation and Excretion

Contact Info

Product

Resources

About

EFFECTS OF DIURETIC HORMONE 31, DROSOKININ, AND ALLATOSTATIN A ON TRANSEPITHELIAL K⁺TRANSPORT AND CONTRACTION FREQUENCY IN THE MIDGUT AND HINDGUT OF LARVALDrosophila melanogaster