Hymenolepis diminuta: metacestode-induced reduction in the synthesis of the yolk protein, vitellogenin, in the fat body of Tenebrio molitor

Abstract

Vitellogenin synthesis by the fat body has been monitored using in vitro culture and immunoprecipitation. This system was found to be efficient for measuring vitellogenin production in both non-infected Tenebrio molitor and those infected with Hymenolepis diminuta. In fat bodies from infected beetles, vitellogenin production was decreased by up to 75% (day 24 post-infection) and, at all times investigated, vitellogenin synthesis was significantly below control levels (days 3-30 post-infection). Incubating fat bodies from control insects with isolated metacestodes indicated that this may be a direct effect by the parasite which is developmental stage-specific. Stage II, but not Stage III-IV, not heat-killed parasites could bring about this decrease in vitellogenin. In addition, these effects may be density dependent within the range of 2-20 parasites per fat body; only 2 metacestodes were necessary to cause a significant decrease. Since metacestodes do not take up vitellogenin, nor limit the amount of [14C]leucine available to the fat body for vitellogenin production, it is conceivable that the parasite produces a potent inhibitor of vitellogenin synthesis, or a molecule which induces cells within the fat body.

Direct manipulation of insect reproduction by agents of parasite origin

“…Metacestodes are known to possess uptake sites for several monosaccharides and amino acids (Arme 1988) but cannot use Vg itself (Webb & Hurd 1996). As they compete directly for amino acids circulating in the haemolymph, all host tissues could be depleted of nutrients.…”

“…14 C]L-leucine (0.25 mCi, total volume 120 ml; Webb & Hurd 1996). After incubation, 2 Â RIPA (radioimmunoprecipitation assay) bu¡er was added (0.3 M NaCl, 0.02 M Tris^HCl, 2% (by volume) Triton X-100, 0.2% (by mass) sodium dodecyl sulphate (SDS), 0.05 M sodium deoxycholate, pH 7.7; 120 ml) and the tissue disrupted by sonication (less than 25 s).…”

“…Egg production is retarded on two levels. In the fat body, synthesis of the yolk protein vitellogenin (Vg) is reduced (Hurd & Arme 1986b;Webb & Hurd 1996) and in the ovary, uptake of Vg is hindered (Hurd & Arme 1987a;Webb et al 1997); eggs are therefore protein de¢cient and lack viability (Hurd & Arme 1986a,b).…”

A γ-glutamyl transpeptidase of Aphidius ervi venom induces apoptosis in the ovaries of host aphids

“…Both in this experimental model system and in other parasitoids attacking adults, the castration appears to be a key strategy for a successful biochemical redirection of the host resources, as reproduction represents the main metabolic sink to switch off in order to increase the host nutritional suitability for the developing parasitoid progeny (Pennacchio and Strand, 2006). The disruption of the host reproductive activity is a common theme also in some true parasites of insects, such as, for example, in the case of the rat tapeworm Hymenolepsis diminuta, infecting Tenebrio molitor beetles, which show selective downregulation of vitellogenin, but not of other proteins, and a re-distribution of nitrogenderived nutrients more favourable both to the host and the parasite (Webb and Hurd, 1996;Hurd, 1998Hurd, , 2001Warr et al, 2004).…”

The effect of Plasmodium yoelii nigeriensis infection on ovarian protein accumulation by Anopheles stephensi

“…Other parasite-insect associations we have studied Webb and Hurd 1996) have also led us to conclude that a parasite-induced reduction in insect egg production is unlikely to be caused directly by competition for nutrients between the parasite and the developing eggs. Parasites may interact directly or indirectly with vector vitellogenesis via ''modulator molecules'' of parasite or host origin.…”