Journal Article

Periviscerokinin (Cap2b; CAPA) receptor silencing in females of Rhipicephalus microplus reduces survival, weight and reproductive output

Lohmeyer, Kimberly H., Pietrantonio, Patricia V., Schlechte, Kristie G., Temeyer, Kevin B., Tidwell, Jason P., Wulff, Juan P.

2022

Overview

Background The cattle fever tick, Rhipicephalus ( Boophilus ) microplus , is a vector of pathogens causative of babesiosis and anaplasmosis, both highly lethal bovine diseases that affect cattle worldwide. In Ecdysozoa, neuropeptides and their G-protein-coupled receptors play a critical integrative role in the regulation of all physiological processes. However, the physiological activity of many neuropeptides is still unknown in ticks. Periviscerokinins (CAP 2b /PVKs) are neuropeptides associated with myotropic and diuretic activities in insects. These peptides have been identified only in a few tick species, such as Ixodes ricinus , Ixodes scapularis and R. microplus, and their cognate receptor only characterized for the last two. Methods Expression of the periviscerokinin receptor ( Rhimi-CAP 2b R ) was investigated throughout the developmental stages of R. microplus and silenced by RNA interference (RNAi) in the females. In a first experiment, three double-stranded (ds) RNAs, named ds680-805, ds956-1109 and ds1102-1200, respectively, were tested in vivo. All three caused phenotypic effects, but only the last one was chosen for subsequent experiments. Resulting RNAi phenotypic variables were compared to those of negative controls, both non-injected and dsRNA beta-lactamase-injected ticks, and to positive controls injected with beta-actin dsRNA. Rhimi-CAP 2b R silencing was verified by quantitative reverse-transcriptase PCR in whole females and dissected tissues. Results Rhimi-CAP 2b R transcript expression was detected throughout all developmental stages . Rhimi-CAP 2b R silencing was associated with increased female mortality, decreased weight of surviving females and of egg masses, a delayed egg incubation period and decreased egg hatching ( P  < 0.05). Conclusions CAP 2b /PVKs appear to be associated with the regulation of female feeding, reproduction and survival. Since the Rhimi-CAP 2b R loss of function was detrimental to females, the discovery of antagonistic molecules of the CAP 2b /PVK signaling system should cause similar effects. Our results point to this signaling system as a promising target for tick control. Graphical Abstract

• Publisher: BioMed Central,BioMed Central Ltd,Springer Nature B.V,BMC
• Subject: Actin / Analysis / Anaplasmosis / Arachnids / Asian blue tick / Babesiosis / Biomedical and Life Sciences / Biomedicine / CAPA gene / Cardioacceleratory peptide 2b (CAP2b)/periviscerokinins (PVK) neuropeptide family / Care and treatment / Cattle / Cattle fever tick / Cloning / Developmental stages / Diagnosis / Diuretics / Dosage and administration / Double-stranded RNA / egg incubation / Eggs / Entomology / Experiments / Females / Fever / G protein-coupled receptors / Gene expression / Hatching / Hormones / Incubation / Incubation period / Infectious Diseases / Insects / Ixodes ricinus / Ixodes scapularis / Laboratories / Livestock / mortality / Muscle proteins / Neuropeptides / Nucleotide sequence / Parasitology / Pathogens / Peptides / Pesticides / phenotype / Physiology / Polyvinyl carbazole / Receptors / reproductive performance / reverse transcriptase polymerase chain reaction / Rhipicephalus microplus / Risk factors / RNA interference / RNA-mediated interference / Signalling systems / Southern cattle tick / species / Survival / tick control / Tick-borne diseases / Ticks / Tropical Medicine / Veterinary Medicine/Veterinary Science / Virology / Weight / Weight reduction / β Lactamase