Association of salivary acetylcholinesterase with arthropod vectors of disease

Authors: Temeyer, Kevin; Schlechte, Kristie; Olafson, Pia; Drolet, Barbara; Tidwell, Jason; Osbrink, Weste; Showler, Allan; GROSS, AARON - Virginia Tech; Perez De Leon, Adalberto - Beto

Submitted to: Journal of Medical Entomology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/4/2020
Publication Date: 5/27/2020
Citation: Temeyer, K.B., Schlechte, K.G., Olafson, P.U., Drolet, B.S., Tidwell, J.P., Osbrink, W.L., Showler, A., Gross, A., Perez De Leon, A.A. 2020. Association of salivary acetylcholinesterase with arthropod vectors of disease. Journal of Medical Entomology. https://doi.org/10.1093/jme/tjaa096.
DOI: https://doi.org/10.1093/jme/tjaa096

Interpretive Summary: Ticks, mosquitoes and other blood-feeding parasites sometimes actively transmit pathogenic organisms to humans and animals, resulting in disease. These vector-borne diseases can be very serious, including malaria, yellow fever, West Nile virus, Zika virus, Lyme disease, and many others, and are responsible for over a million deaths worldwide annually. Saliva of some of these blood-feeding parasites may alter the immune response of the host animal in a manner that promotes pathogen transmission, establishment and disease progression within the host. Scientists in the U.S. Department of Agriculture report the discovery of an enzyme present in the saliva of ticks, mosquitoes, sand flies, and midges that may participate in altering the host immune response to parasite blood-feeding. It is expected that this new knowledge may enable further studies to understand the mechanisms responsible for altering the host immune responses and develop new technologies to protect people and animals from vector-borne diseases.

Technical Abstract: Acetylcholinesterase (AChE) was previously reported to be present in saliva of the southern cattle tick, Rhipicephalus (Boophilus) microplus (Canestrini), with proposed potential functions to 1) reduce acetylcholine toxicity during rapid engorgement, 2) modulate host immune responses, and 3) to influence pathogen transmission and establishment in the host. Potential modulation of host immune responses might include participation in salivary-assisted transmission and establishment of pathogens in the host as has been reported for a number of arthropod vector-borne diseases. If the hypothesis that tick salivary AChE may alter host immune responses is correct, we reasoned that similar cholinesterase activities might be present in saliva of additional arthropod vectors. Here, we report the presence of AChE-like activity in the saliva of southern cattle ticks, Rhipicephalus (Boophilus) microplus; the lone star tick, Amblyomma americanum (Linnaeus); Asian tiger mosquitoes, Aedes albopictus (Skuse); sand flies, Phlebotomus papatasi (Scopoli); and biting midges, Culicoides sonorensis Wirth and Jones. Salivary AChE-like activity was not detected for horn flies Haematobia irritans (L.), stable flies Stomoxys calcitrans (L.), and house flies Musca domestica L. Salivary cholinesterase (ChE) activities of arthropod vectors of disease-causing agents exhibited various Michaelis-Menten KM values that were each lower than the KM value of bovine serum AChE. A lower KM value is indicative of higher affinity for substrate and is consistent with a hypothesized role in localized depletion of host tissue acetylcholine potentially modulating host immune responses at the arthropod bite site that may favor ectoparasite blood-feeding and alter host defensive responses against pathogen transmission and establishment.