Salivary Gland Proteome Analysis Reveals Modulation of Anopheline Unique Proteins in Insensitive Acetylcholinesterase Resistant Anopheles gambiae Mosquitoes

Abstract

Insensitive acetylcholinesterase resistance due to a mutation in the acetylcholinesterase (ace) encoding ace-1 gene confers cross-resistance to organophosphate and carbamate insecticides in Anopheles gambiae populations from Central and West Africa. This mutation is associated with a strong genetic cost revealed through alterations of some life history traits but little is known about the physiological and behavioural changes in insects bearing the ace-1R allele. Comparative analysis of the salivary gland contents between An. gambiae susceptible and ace-1R resistant strains was carried out to charaterize factors that could be involved in modifications of blood meal process, trophic behaviour or pathogen interaction in the insecticide-resistant mosquitoes. Differential analysis of the salivary gland protein profiles revealed differences in abundance for several proteins, two of them showing major differences between the two strains. These two proteins identified as saglin and TRIO are salivary gland-1 related proteins, a family unique to anopheline mosquitoes, one of them playing a crucial role in salivary gland invasion by Plasmodium falciparum sporozoites. Differential expression of two other proteins previously identified in the Anopheles sialome was also observed. The differentially regulated proteins are involved in pathogen invasion, blood feeding process, and protection against oxidation, relevant steps in the outcome of malaria infection. Further functional studies and insect behaviour experiments would confirm the impact of the modification of the sialome composition on blood feeding and pathogen transmission abilities of the resistant mosquitoes. The data supports the hypothesis of alterations linked to insecticide resistance in the biology of the primary vector of human malaria in Africa.

Overexpression of Two Members of D7 Salivary Genes Family is Associated with Pyrethroid Resistance in the Malaria Vector Anopheles Funestus s.s. but Not in Anopheles Gambiae in Cameroon

“…Indeed, because mosquitoes develop different resistance mechanisms to carbamates and pyrethroids, the impact of the resistance to one family could be different to what observed for the other. However, the down-regulation of D7 family genes observed in our study is in accordance with results of previous studies after comparative proteomic analysis of expressed proteins in bendiocarb susceptible and resistant mosquitoes [46,47]. Indeed, in these studies conducted in Culex quinquefasciatus [48] and An.…”

“…Indeed, in these studies conducted in Culex quinquefasciatus [48] and An. gambiae [47], the D7 long form (the sole member of D7 family protein detected) presented lower expression in the resistant strain than the susceptible strain. Globally, it appears that the pattern of how insecticide resistance is associated to the differential expression of D7 family genes remained unclear.…”

Protein expression in female salivary glands of pyrethroid-susceptible and resistant strains of Aedes aegypti mosquitoes

“…aegypti salivary gland extract enhances dengue pathogenesis after infection [ 16 ]. In previous studies, differential expression of salivary gland proteins between insecticide-susceptible and resistant strains of Culex quinquefasciatus [ 17 ], Anopheles gambiae [ 18 ] and Anopheles stephensi [ 19 ] has been reported. Regarding insecticide resistant mosquitoes in Thailand, no report of differentially expressed salivary gland proteins between susceptible and insecticide-resistant Ae.…”

Differential protein expression in the midgut of Culex quinquefasciatus mosquitoes induced by the insecticide temephos

“…Overall, an increasing number of studies have compared differentially expressed proteins in vector mosquitoes, but these refer to proteins from the salivary glands (Cornelie et al , ; Vijay et al , ) or from the whole larval body (Wang et al , ), rather than the midgut. The studies cited above identified proteins that differ from those reported herein.…”