Functional analysis of a G protein‐coupled receptor from the Southern cattle tick <i>Boophilus microplus</i> (Acari: Ixodidae) identifies it as the first arthropod myokinin receptor

Holmes, Steven P.; Barhoumi, Roula; Nachman, Ronald J.; Pietrantonio, Patricia V.

doi:10.1046/j.1365-2583.2003.00384.x

Cited by 60 publications

(63 citation statements)

References 71 publications

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“…G, heterotrimeric Gprotein; PLC, phospholipase C; IP3, inositol (1,4,5)-trisphosphate. Data from Yu and Beyenbach, 2002. 3854 snails (Lymnaea stagnalis), cattle ticks (Boophilus microplus) and the fruit fly have a sequence consistent with a G-protein coupled receptor (Radford et al, 2002;Holmes et al, 2003). Furthermore, AlF4 -, a known activator of G-proteins, duplicates the effects of leucokinin in Aedes Malpighian tubules (Yu and Beyenbach, 2001).…”

Section: Transport In Malpighian Tubulesmentioning

confidence: 93%

Transport mechanisms of diuresis in Malpighian tubules of insects

Beyenbach

2003

Journal of Experimental Biology

173

169

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SUMMARYWe have studied Malpighian tubules of Aedes aegypti using a variety of methods: Ramsay fluid secretion assay, electron probe analysis of secreted fluid, in vitro microperfusion and two-electrode voltage clamp. Collectively, these methods have allowed us to elucidate transepithelial transport mechanisms under control conditions and in the presence of diuretic peptides. Mosquito natriuretic peptide (MNP), a corticotropin-releasing factor (CRF)-like diuretic peptide, selectively increases transepithelial secretion of NaCl and water, meeting the NaCl loads of the blood meal. The intracellular messenger of MNP is cAMP, which increases the Na+ conductance and activates the Na+/K+/2Cl--cotransporter in the basolateral membrane of principal cells. Leucokinin non-selectively increases transepithelial NaCl and KCl secretion, which may deal with hemolymph volume expansions or reduce the flight pay load upon eclosion from the aquatic habitat. The non-selective NaCl and KCl diuresis stems from the increase in septate junctional Cl- conductance activated by leucokinin using Ca2+ as second messenger. Fundamental to diuretic mechanisms are powerful epithelial transport mechanisms in the distal segment of the Malpighian tubules, where transepithelial secretion rates can exceed the capacity of mammalian glomerular kidneys in the renal turnover of the extracellular fluid compartment. In conjunction with powerful epithelial transport mechanisms driven by the V-type H+-ATPase, diuretic hormones enable hematophagous and probably also phytophagous insects to deal with enormous dietary loads, thereby contributing to the evolutionary success of insects.

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Section: Transport In Malpighian Tubulesmentioning

confidence: 93%

Transport mechanisms of diuresis in Malpighian tubules of insects

Beyenbach

2003

Journal of Experimental Biology

173

169

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“…The protein sequences of the Lymnaea stagnalis L. (Cox et al, 1997) and Boophilus microplus Canestrini (Holmes et al, 2003) leucokinin-like receptors were also used to confirm the sequence match. The BLOSUM62 matrix (default settings) was used for all BLAST analysis as above.…”

Section: Methodsmentioning

confidence: 99%

“…The protein sequences of the known leucokinin-like receptors, the Drosophila LKR (CG10626; Radford et al, 2002), the lymnokinin receptor (GenBank accession AAD11810; Cox et al, 1997), the B. microplus receptor (AAF72891; Holmes et al, 2003) and the putative A. stephensi receptor (Fig.·3) were aligned using the CLUSTAL X program (Thompson et al, 1994). The sequence alignment was annotated using BioEdit (Hall, 1999) (Fig.·4).…”

Section: Alignment and Comparison Of The Known Leucokinin Receptorsmentioning

confidence: 99%

Functional characterisation of theAnophelesleucokinins and their cognate G-protein coupled receptor

Radford

Terhzaz

Cabrero

et al. 2004

Journal of Experimental Biology

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Drosophila leucokinin was also found to activate the Anopheles receptor with a similar EC 50 value to Anopheles leucokinin I. However, when the Anopheles peptides were applied to the Drosophila receptor, only Anopheles leucokinin I and II elicited a rise in [Ca 2+ ] i . This suggests that the Anopheles receptor has a broader specificity for leucokinin ligands than the Drosophila receptor.Antisera raised against the Anopheles receptor identified a doublet of approx. 65 and 72·kDa on western blots, consistent with the presence of four N-glycosylation sites within the receptor sequence, and the known glycosylation of the receptor in Drosophila. In Anopheles tubules, as in Drosophila, the receptor was localised to the stellate cells.Thus we provide the first identification of Anopheles mosquito leucokinins (Anopheles leucokinins) and a cognate leucokinin receptor, characterise their interaction and show that Dipteran leucokinin signalling is closely conserved between Drosophila and Anopheles.

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“…Periviscerokinin was the first conserved neuropeptide identified in ticks by using matrix-assisted laser desorption/ionization-time of flight (MALDI-TOF) analysis of single neurons (Neupert et al, 2005). Molecular cloning and functional analysis of the Gprotein-coupled receptor for a kinin-like peptide in the southern cattle tick, Boophilus microplus, further suggested that ticks produce multiple neuropeptides and receptors similar to those identified in other arthropods (Holmes et al, 2000(Holmes et al, , 2003Taneja-Bageshwar et al, 2006). We recently described the complex neuroendocrine network present in the central and peripheral nervous systems of the hard tick, Rhipicephalus appendiculatus, by using 15 different antibodies that recognize various neuropeptides (Šimo et al, 2009).…”

mentioning

confidence: 99%

Two novel neuropeptides in innervation of the salivary glands of the black‐legged tick, Ixodes scapularis: Myoinhibitory peptide and SIFamide

Šimo

Žitňan

Park

2009

J of Comparative Neurology

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The peptidergic signaling system is an ancient cell-cell communication mechanism that is involved in numerous behavioral and physiological events in multicellular organisms. We identified two novel neuropeptides in the neuronal projections innervating the salivary glands of the blacklegged tick, Ixodes scapularis (Say, 1821). Myoinhibitory peptide (MIP) and SIFamide immunoreactivities were colocalized in the protocerebral cells and their projections terminating on specific cells of salivary gland acini (types II and III). Immunoreactive substances were identified by matrix-assisted laser desorption/ionization-time of flight (MALDITOF) analysis: a 1,321.6-Da peptide with the sequence typical for MIP (ASDWNRLSGMWamide) and a 1,395.7-Da SIFamide (AYRKPPFNGSIFamide), which are highly conserved among arthropods. Genes encoding these peptides were identified in the available Ixodes genome and expressed sequence tag (EST) database. In addition, the cDNA encoding the MIP prepropeptide was isolated by rapid amplification of cDNA ends (RACE). In this report, we describe the anatomical structure of specific central neurons innervating salivary gland acini and identify different neuropeptides and their precursors expressed by these neurons. Our data provide evidence for neural control of salivary gland by MIP and SIFamide from the synganglion, thus leading a basis for functional studies of these two distinct classes of neuropeptides. Keywords neuropeptide; myoinhibitory peptide; MIP; SIFamide; MALDI; synganglion; salivary glands Ticks are obligatory external parasites that feed on the blood of mammals, birds, and reptiles and often transmit pathogenic viruses, Rickettsiae, bacteria, and protozoa. Tick-borne diseases cause substantial economic loss in the animal industry and present risks for human health. The black-legged tick, Ixodes scapularis, transmits the most important tick-borne pathogen, Borrelia burgdorferi, which causes Lyme disease. More than 20,000 new cases are reported per year in the United States, in 46 states. This species also transmits other diseases, including human babesiosis Babesia microti and human granulocytic ehrlichiosis.Salivary secretions of ticks are essential during feeding for manipulation and suppression of host defense responses and might represent key components in the transmission of (Binnington, 1978;Coons and Roshdy, 1973;Krolak et al., 1982). Each type of acinus contains multiple cell types, including different types of secretory and epithelial cells (Balashov et al., 1983;Sauer et al., 1995;Sonenshine, 1993). Studies with transmission electron microscopy have discovered that axon terminals reach the basal region of the acini, indicating that there is neuronal control of the salivary glands (Balashov et al., 1983; Coons and Alberti, 1999). Recently, we have described the neuroanatomy of peptidergic cells in the nervous system, including the neurons and axonal projections that innervate tick salivary glands (Šimo et al., 2009).Previous immunohistochemical studies have indica...

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Functional analysis of a G protein‐coupled receptor from the Southern cattle tick Boophilus microplus (Acari: Ixodidae) identifies it as the first arthropod myokinin receptor

Cited by 60 publications

References 71 publications

Transport mechanisms of diuresis in Malpighian tubules of insects

Transport mechanisms of diuresis in Malpighian tubules of insects

Functional characterisation of theAnophelesleucokinins and their cognate G-protein coupled receptor

Two novel neuropeptides in innervation of the salivary glands of the black‐legged tick, Ixodes scapularis: Myoinhibitory peptide and SIFamide

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