Malaria Plasmodium agent induces alteration in the head proteome of their Anopheles mosquito host

Abstract

Despite increasing evidence of behavioural manipulation of their vectors by pathogens, the underlying mechanisms causing infected vectors to act in ways that benefit pathogen transmission remain enigmatic in most cases. Here, 2-D DIGE coupled with MS were employed to analyse and compare the head proteome of mosquitoes (Anopheles gambiae sensu stricto (Giles)) infected with the malarial parasite (Plasmodium berghei) with that of uninfected mosquitoes. This approach detected altered levels of 12 protein spots in the head of mosquitoes infected with sporozoites. These proteins were subsequently identified using MS and functionally classified as belonging to metabolic, synaptic, molecular chaperone, signalling, and cytoskeletal groups. Our results indicate an altered energy metabolism in the head of sporozoite-infected mosquitoes. Some of the up-/down-regulated proteins identified, such as synapse-associated protein, 14-3-3 protein and calmodulin, have previously been shown to play critical roles in the CNS of both invertebrates and vertebrates. Furthermore, a heat shock response (HSP 20) and a variation of cytoarchitecture (tropomyosins) have been shown. Discovery of these proteins sheds light on potential molecular mechanisms that underlie behavioural modifications and offers new insights into the study of intimate interactions between Plasmodium and its Anopheles vector.

What can parasitoid wasps teach us about decision-making in insects?

“…Such proteins can then be extracted and their mass and amino acid sequence can be determined via mass spectrophotometry and aligned against available databases. Pioneer proteomics studies on manipulated hosts have been carried out on seven arthropod hostparasite associations, among which two Orthoptera-hairworm associations Biron et al, 2006;Lefevre et al, 2007). These studies have contributed to the discovery of candidate genes and of biochemical pathways altered in host CNS during the parasite manipulation for three aberrant host behaviours: suicidal behaviour, increase in probing rate and alteration of evasive behaviour.…”

Host–parasite molecular cross-talk during the manipulative process of a host by its parasite

“…The Journal of Experimental Biology 216 (1) (Lefèvre et al, 2007a;Lefèvre et al, 2007b). For the two dipteran species, the qualitative proteome of G. palpalis gambiensis responded rather more strongly to its manipulative trypanosome species compared with A. gambiae manipulated by its malaria species (Fig.3A) (Lefèvre et al, 2007a;Lefèvre et al, 2007b).…”

“…Hurd, 2003;Jenni et al, 1980;Lefèvre and Thomas, 2008;Molyneux and Jefferies, 1986;Roberts, 1981). Two parasito-proteomics studies were done on two insect-vector-parasite associations to improve understanding of the proximate cause(s) leading to the alteration of the insect vector behaviour: (1) the mosquito Anopheles gambiae Giles (Diptera, Culicidae) parasitized by a malaria parasite, Plasmodium berghei (Haemosporida, Plasmodiidae) (Lefèvre et al, 2007a), and (2) the tsetse fly Glossina palpalis gambiensis (Vanderplank) (Diptera, Glossinidae), parasitized by the sleeping sickness parasite, Trypanosoma brucei brucei (Kinetoplastida, Trypanosomatidae) (Lefèvre et al, 2007b). These studies provided evidence that the parasites can indeed induce alteration in the head proteome of their insect vectors…”

Proteomics of Anopheles gambiae

“…Interestingly, few studies have been undertaken to demonstrate the existence of a general manipulative mechanism by which the parasite manipulate the host central nervous system. A 2-D DIGE coupled with MS was used to analyse and compare the head proteome of A. gambiae infected with Plasmodium berghei with that of uninfected mosquitoes [48]. This approach allowed detecting modulations of 12 protein spots in the head of mosquitoes infected with sporozoites.…”