Interactions between host biogenic amines and sand fly salivary yellow-related proteins

Tatiana Spitzova,Nikola Polanska,Luisa Poctova,Petr Volf,Vera Volfova,Petra Sumova

doi:10.1186/s13071-020-04105-2

Abstract

BackgroundDuring blood feeding, sand flies inoculate salivary proteins that interact with the host haemostatic system. The blocking of biogenic amines such as serotonin and histamine helps to limit vasodilatation and clot formation, and thus enables the insect to finish the blood-feeding process. In sand flies, an amine-binding ability is known only for the yellow-related proteins of Phlebotomus and Lutzomyia vectors, but not yet for members of the genus Sergentomyia.MethodsThe ability of Phlebotomus argentipes and Sergentomyia schwetzi recombinant yellow-related salivary proteins to bind histamine and serotonin was measured by microscale thermophoresis. Both sand fly species were also fed through a chicken-skin membrane on blood mixed with histamine or serotonin in order to check the effects of biogenic amines on sand fly fitness. Additionally, fecundity and mortality were compared in two groups of P. argentipes females fed on repeatedly-bitten and naive hamsters, respectively.ResultsThe P. argentipes recombinant yellow-related protein PagSP04 showed high binding affinity to serotonin and low affinity to histamine. No binding activity was detected for two yellow-related proteins of S. schwetzi. Elevated concentrations of serotonin significantly reduced the amount of eggs laid by P. argentipes when compared to the control. The fecundity of S. schwetzi and the mortality of both sand fly species were not impaired after the experimental membrane feeding. Additionally, there were no differences in oviposition or mortality between P. argentipes females fed on immunized or naive hamsters.ConclusionsOur results suggest that in natural conditions sand flies are able to cope with biogenic amines or anti-saliva antibodies without any influence on their fitness. The serotonin binding by salivary yellow-related proteins may play an important role in Phlebotomus species feeding on mammalian hosts, but not in S. schwetzi, which is adapted to reptiles.

Highlights

During blood feeding, sand flies inoculate salivary proteins that interact with the host haemostatic system
Proteins of this family are found exclusively in insects and are abundant in phlebotomine sialomes with high variability in the number of yellowrelated protein (YRP) among different sand fly species [1, 8]; they show a similar structure with some intraspecific modifications that influence the ligand-binding abilities [9]
The main aims of the study were (i) to compare the ability of P. argentipes and S. schwetzi yellow-related proteins to bind biogenic amines, histamine and serotonin; (ii) to clarify if the fecundity and mortality of P. argentipes and S. schwetzi could be affected by biogenic amines present in blood using membrane feeding; and (iii) to study if high levels of anti-P. argentipes saliva antibodies in repeatedly-bitten hamsters interfere with P. argentipes fecundity and mortality

Summary

Introduction

Sand flies inoculate salivary proteins that interact with the host haemostatic system. During blood-feeding they inoculate salivary proteins into the skin that counteract the host haemostatic system [1] Biogenic amines, such as, histamine and serotonin, Spitzova et al Parasites Vectors (2020) 13:237. The ability to bind host biogenic amines has only been described for the family of salivary yellow-related proteins (YRPs) [6, 7]. Proteins of this family are found exclusively in insects and are abundant in phlebotomine sialomes with high variability in the number of YRPs among different sand fly species [1, 8]; they show a similar structure with some intraspecific modifications that influence the ligand-binding abilities [9]. These antibodies could have an impact on sand fly fecundity and mortality [10,11,12]; other studies have not found any significant effects [13,14,15]

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