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J. Biol. Chem., Vol. 281, Issue 4, 1935-1942, January 27, 2006

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Function and Evolution of a Mosquito Salivary Protein Family^*

From the Section of Vector Biology, Laboratory of Malaria and Vector Research, NIAID, National Institutes of Health, Bethesda, Maryland 20852

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.

Received for publication, September 21, 2005 , and in revised form, November 14, 2005.

^* This work was funded by the Division of Intramural Research, NIAID, National Institutes of Health. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S1–S3 and supplemental Tables S1 and S2.

¹ Both authors contributed equally to this work.

² To whom correspondence should be addressed: NIAID/LMVR, 12735 Twinbrook Pkwy., Rm. 2E32D, Rockville, MD 20852. Tel.: 301-496-9389; Fax: 301-480-2571; E-mail: jribeiro{at}niaid.nih.gov.

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