Myotropic Activities of Tick Pyrokinin Neuropeptides and Analog in Feeding Tissues of Hard Ticks (Ixodidae).

Caixing Xiong,Juan P Wulff,Patricia V Pietrantonio,Ronald J Nachman

doi:10.3389/fphys.2021.826399

Caixing Xiong, Juan P Wulff + Show 2 more

Open Access

https://doi.org/10.3389/fphys.2021.826399

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Abstract

Neuropeptides regulate many important physiological processes in animals. The G protein-coupled receptors of corresponding small neuropeptide ligands are considered promising targets for controlling arthropod pests. Pyrokinins (PKs) are pleiotropic neuropeptides that, in some insect species, stimulate muscle contraction and modulate pheromone biosynthesis, embryonic diapause, and feeding behavior. However, their function remains unknown in ticks. In this study, we reported the myotropic activity of tick endogenous PKs and a PK agonist analog, PK-PEG8 (MS[PEG8]-YFTPRLa), on feeding tissues of two tick species representing the family Ixodidae lineages, namely, Prostriata (Ixodes scapularis) and Metastriata (Rhipicephalus sanguineus). First, we predicted the sequences of two periviscerokinins (PVK), one with a derived ending RNa and five PKs encoded by the CAPA peptide precursor from R. sanguineus and found the encoded PKs were identical to those of R. microplus identified previously. The pharynx-esophagus of both tick species responded with increased contractions to 10 μM of the endogenous PK as well as to PK-PEG8 but not to the scrambled PK peptide, as expected. A dose-dependent myotropic activity of the PK-PEG8 was found for both tick species, validating the analog activity previously found in the pyrokinin recombinant receptor assay. In agreement with the tissue activity elicited, we quantified the relative transcript abundance of R. sanguineus PK receptor in unfed female ticks and found it was the highest in the feeding tissues extracted from the capitulum and lowest in the reproductive tissue. This is the first report of the activity of pyrokinins in ticks. These findings strongly indicate the potential role of PKs in regulating tick blood feeding and therefore, making the tick PK receptor a potential target for interference.

Highlights

G protein-coupled receptors (GPCRs) are promising novel targets for tick control (Pietrantonio et al, 2018)
To identify the capa gene from R. sanguineus, a BLASTn search was performed on NCBI against the R. sanguineus nucleotide collection using the capa cDNA sequence we previously cloned from R. microplus (GenBank accession number MZ686950) (Xiong et al, 2021b)
The amino acid sequences of these seven neuropeptides encoded by the Rhisa-CAPA precursor are Myotropic Activity of Pyrokinins in R. sanguineus

Summary

Introduction

G protein-coupled receptors (GPCRs) are promising novel targets for tick control (Pietrantonio et al, 2018). In contrast to the rapid advance in the identification of ligands and GPCRs by means of omics tools, studies on the physiological function of tick neuropeptides are still limited. Such knowledge is essential for selecting GPCRs for screening synthetic chemical libraries and for understanding the mode of action of novel chemistries. PKs from the American cockroach, Periplaneta americana, show myostimulatory activity on several tissues such as the hyperneural muscle, hindgut, foregut, and oviducts (Predel and Nachman, 2001), and pyrokinins increase the contraction in the heart muscle of Drosophila (Meng et al, 2002). PKs accelerate pupariation in the flesh fly (Nachman et al, 2006)

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