Function and evolution of a mosquito salivary protein family.
Saliva of blood-sucking arthropods contains a complex and diverse mixture of antihemostatic, antiinflammatory, and immunomodulatory compounds. The D7 salivary family of proteins is abundantly expressed in blood-feeding Diptera and is distantly related to the odorant-binding protein superfamily. In mosquitoes, two subfamilies exist, the long and short D7 proteins. Ticks and kissing bugs evolved salivary lipocalins that act as efficient scavengers of biogenic amines, and a similar function was postulated for the D7 proteins. Accordingly, we expressed the five members of the small D7 family of the African malaria vector Anopheles gambiae and a D7 long form from Aedes aegypti and showed by isothermal microcalorimetry, a modified and very sensitive non-equilibrium chromatography/spectrum distortion method, and by smooth muscle bioassay that four of these five short D7 proteins and the D7 long form bind serotonin with high affinity, as well as histamine and norepinephrine. The nonbinding D7 protein is poorly expressed in the salivary glands and appears to be on the path to becoming a pseudogene. Scavenging of host amines would antagonize their vasoconstrictor, platelet-aggregating, and pain-inducing properties. It appears that counteracting biogenic amines is of strong adaptive value in the convergent evolution of arthropods to hematophagy. This adaptation has been solved independently in ticks, bugs, and mosquitoes by co-option of either member of the lipocalin or, as shown here, by the odorant-binding protein families.
Calvo
Eric
E
Section of Vector Biology, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases/NIH, 12735 Twinbrook Parkway, Rockville, MD 20852, USA.
Mans
Ben J
BJ
Andersen
John F
JF
Ribeiro
José M C
JM
D000330:Aedes; D000595:Amino Acid Sequence; D000818:Animals; D000852:Anopheles / Q000378:metabolism; D001681:Biological Assay; D001777:Blood Coagulation; D002151:Calorimetry; D002352:Carrier Proteins / Q000737:chemistry; D002845:Chromatography; D009033:Culicidae; D018076:DNA, Complementary / Q000378:metabolism; D006632:Histamine / Q000737:chemistry; D007303:Insect Vectors; D054835:Lipocalin 1; D008957:Models, Genetic; D008969:Molecular Sequence Data; D005810:Multigene Family; D009638:Norepinephrine / Q000737:chemistry; D010802:Phylogeny; D016133:Polymerase Chain Reaction; D011485:Protein Binding; D011994:Recombinant Proteins / Q000737:chemistry; D012471:Salivary Proteins and Peptides / Q000737:chemistry* / Q000235:genetics*; D017386:Sequence Homology, Amino Acid; D012701:Serotonin / Q000737:chemistry; D014466:Ultraviolet Rays
D002352:Carrier Proteins; D018076:DNA, Complementary; D054835:Lipocalin 1; D011994:Recombinant Proteins; D012471:Salivary Proteins and Peptides; D012701:Serotonin; D006632:Histamine; D009638:Norepinephrine