An unusual myosuppressin from the blood-feeding bug<i>Rhodnius prolixus</i>

Lee, Dohee; Taufique, Hamza; Silva, Rosa da; Lange, Angela B.

doi:10.1242/jeb.067447

Cited by 38 publications

(29 citation statements)

References 37 publications

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“…However, the cardioacceleratory properties of FLPs are not universal. Depending on the N-terminal sequence of the peptide, and the insect being tested, some FLPs are cardioacceletatory (Cuthbert and Evans, 1989;Robb and Evans, 1990;Duve et al, 1993;Duttlinger et al, 2003), some are cardiodeceleratory (Cuthbert and Evans, 1989;Robb and Evans, 1990;Nichols et al, 1999;Lee et al, 2012), some have complex effects that are dependent on the presence of other molecules (Nichols, 2006), and yet others have no effect on heart physiology (Duve et al, 1993;Nichols et al, 1999;Nichols, 2006). In the present study, we confirm the cardioacceleratory activity of SALDKNFMRFamide and FMRFamide, and for the first time show in a holometabolous insect that FLPs accelerate the antennal APOs.…”

Section: Discussionmentioning

confidence: 99%

CCAP and FMRFamide-like peptides accelerate the contraction rate of the antennal accessory pulsatile organs (auxiliary hearts) of mosquitoes

Suggs

Jones

Murphree

et al. 2016

Journal of Experimental Biology

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Insects rely on specialized accessory pulsatile organs (APOs), also known as auxiliary hearts, to propel hemolymph into their antennae. In most insects, this is accomplished via the pulsations of a pair of ampulla located in the head, each of which propels hemolymph across an antenna via an antennal vessel. Once at the distal end of the appendage, hemolymph returns to the head via the antennal hemocoel. Although the structure of the antennal hearts has been elucidated in various insect orders, their hormonal modulation has only been studied in cockroaches and other hemimetabolous insects within the superorder Polyneoptera, where proctolin and FMRFamide-like peptides accelerate the contraction rate of these auxiliary hearts. Here, we assessed the hormonal modulation of the antennal APOs of mosquitoes, a group of holometabolous (Endopterygota) insects within the order Diptera. We show that crustacean cardioactive peptide (CCAP), FMRFamide and SALDKNFMRFamide increase the contraction rate of the antennal APOs and the heart of Anopheles gambiae. Both antennal hearts are synchronously responsive to these neuropeptides, but their contractions are asynchronous with the contraction of the heart. Furthermore, we show that these neuropeptides increase the velocity and maximum acceleration of hemolymph within the antennal space, suggesting that each contraction is also more forceful. To our knowledge, this is the first report demonstrating that hormones of a holometabolous insect modulate the contraction dynamics of an auxiliary heart, and the first report that shows that the hormones of any insect accelerate the velocity of hemolymph in the antennal space.

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Section: Discussionmentioning

confidence: 99%

CCAP and FMRFamide-like peptides accelerate the contraction rate of the antennal accessory pulsatile organs (auxiliary hearts) of mosquitoes

Suggs

Jones

Murphree

et al. 2016

Journal of Experimental Biology

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“…In other insects, the heart contracts in a myogenic manner (Jones, 1977;Dulcis et al, 2001;Sláma and Lukáš, 2011), but several neurohormones and neurotransmitters affect the speed and directionality of heart contractions (Johnson et al, 1997;Nichols, 2006;Lee et al, 2012;Setzu et al, 2012). Among the cardiostimulatory neurohormones is crustacean cardioactive peptide (CCAP), a cyclic amidated nonapeptide that is produced in a broad range of organisms, including crabs (Stangier et al, 1987), crayfish (Chung et al, 2006), lobsters (Chung et al, 2006), ticks (Simo et al, 2009), mites (Christie et al, 2011) and all sequenced insect lineages (Cheung et al, 1992;Furuya et al, 1993;Riehle et al, 2002;Park et al, 2003;Sakai et al, 2004;Predel et al, 2010;, which suggests that CCAP was produced by the ancestral arthropod.…”

Section: Introductionmentioning

confidence: 99%

Cardioacceleratory function of the neurohormone CCAP in the mosquito Anopheles gambiae

Estévez‐Lao

Boyce

Honegger

et al. 2013

Journal of Experimental Biology

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SUMMARYCrustacean cardioactive peptide (CCAP) is a highly conserved arthropod neurohormone that is involved in ecdysis, hormone release and the modulation of muscle contractions. Here, we determined the CCAP gene structure in the malaria mosquito Anopheles gambiae, assessed the developmental expression of CCAP and its receptor and determined the role that CCAP plays in regulating mosquito cardiac function. RACE sequencing revealed that the A. gambiae CCAP gene encodes a neuropeptide that shares 100% amino acid identity with all sequenced CCAP peptides, with the exception of Daphnia pulex. Quantitative RT-PCR showed that expression of CCAP and the CCAP receptor displays a bimodal distribution, with peak mRNA levels in second instar larvae and pupae. Injection of CCAP revealed that augmenting hemocoelic CCAP levels in adult mosquitoes increases the anterograde and retrograde heart contraction rates by up to 28%, and increases intracardiac hemolymph flow velocities by up to 33%. Partial CCAP knockdown by RNAi had the opposite effect, decreasing the mosquito heart rate by 6%. Quantitative RT-PCR experiments showed that CCAP mRNA is enriched in the head region, and immunohistochemical experiments in newly eclosed mosquitoes detected CCAP in abdominal neurons and projections, some of which innervated the heart, but failed to detect CCAP in the abdomens of older mosquitoes. Instead, in older mosquitoes CCAP was detected in the pars lateralis, the subesophageal ganglion and the corpora cardiaca. In conclusion, CCAP has a potent effect on mosquito circulatory physiology, and thus heart physiology in this dipteran insect is under partial neuronal control. Supplementary material available online at

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“…The myosuppressin of R. prolixus is the first FMRFamide‐like peptide with a FMRFamide C ‐terminal motif to be found outside of the dipterans and the only myosuppressin without an FLRFamide C‐terminal motif, and even with these structural differences it is still capable of inhibiting both visceral and cardiac muscle (Lee et al ., ). Using a functional receptor assay we were able to use structural analogues of RhoprMS to help determine the importance of the methionine in position 8 and also to determine the minimum sequence needed to bind to the receptor.…”

Section: Discussionmentioning

confidence: 97%

“…Previously, Lee et al . () have shown that RhoprMS inhibits the frequency and amplitude of contractions of the anterior midgut and hindgut, while also decreasing the heartbeat rate. These three tissues were found to express the RhoprMSR, particularly the anterior midgut, which consistently had the highest expression of the peripheral tissues.…”

Section: Discussionmentioning

confidence: 98%

“…The recently sequenced Rhodnius prolixus myosuppressin (RhoprMS) has a unique peptide sequence from other myosuppressins consisting of pQDIDHVFMRFamide (i.e. where X3 is an isoleucine instead of valine and X8 is methionine instead of leucine; Lee et al, 2012). Despite these differences, RhoprMS is still functionally a myoinhibitory peptide decreasing heart rate, and inhibiting anterior midgut and hindgut contractions in R. prolixus (Lee et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

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Identification, characterization and expression of a receptor for the unusual myosuppressin in the blood‐feeding bug, Rhodnius prolixus

Lee

James

Lange

2014

Insect Molecular Biology

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Myosuppressins are a family of the FMRFamide-like peptides. They have been characterized in many insects and shown to inhibit visceral muscle contraction. Rhodnius prolixus possesses an unusual myosuppressin in that the typical FLRFamide C-terminal motif is unique and ends with FMRFamide. In the present study, we isolated the cDNA sequence for the R. prolixus receptor for this unusual myosuppressin (RhoprMSR). Quantitative PCR indicates high relative transcript expression of RhoprMSR in the central nervous system and also supports the previously described physiological effects of RhoprMS on the digestive system, with expression of the RhoprMSR transcript in the midgut and hindgut. Expression of the RhoprMSR transcript was also found in the female and male reproductive system of 5th instar nymphs, with transcript expression greater in the female reproductive tissues. No expression was found in the salivary glands or Malpighian tubules. A functional receptor expression assay confirmed that the cloned RhoprMSR is indeed activated by RhoprMS (half maximum effective concentration = 42.7 nM). Structure-activity studies based upon both functional receptor assays and physiological assays showed the importance of the HVFMRFamide moiety, as further N-terminal truncation removed all activity.

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An unusual myosuppressin from the blood-feeding bugRhodnius prolixus

Cited by 38 publications

References 37 publications

CCAP and FMRFamide-like peptides accelerate the contraction rate of the antennal accessory pulsatile organs (auxiliary hearts) of mosquitoes

CCAP and FMRFamide-like peptides accelerate the contraction rate of the antennal accessory pulsatile organs (auxiliary hearts) of mosquitoes

Cardioacceleratory function of the neurohormone CCAP in the mosquito Anopheles gambiae

Identification, characterization and expression of a receptor for the unusual myosuppressin in the blood‐feeding bug, Rhodnius prolixus

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