Cumulative effects of PDVs and other virulence factors on host immunity

PDVs constitute a component of the parasitoid arsenal to overcome the host immune response but other factors are also involved. The eggs of C. rubecula are deposited in caterpillars of P. rapae and are protected from encapsulation during their early embryogenesis by calyx-fluid glycoproteins (Asgari et al, 1996). Among them, the ovarian protein Crp32 coats the eggs and the viral particles and provides protection during the short temporal window necessary to the expression of viral genes (Asgari et al, 1998). Some venom proteins of C. rubecula were shown to inhibit melanin formation when added to host haemolymph (Asgari et al., 2003a, 2003b) during the early phase of parasitiza-tion. A small venom peptide of 1.5 kDa is required for the expression of CrBV genes in host haemo-cytes (Zhang et al., 2004). This peptide could facilitate virus chromatin restructuring, uncoating of genomic DNA, or expression of CrBV genes at the transcriptional level. This finding confirmed earlier reports which established that venom of C. rubecula was indirectly necessary for the protection of the parasitoid eggs from encapsulation (Kitano, 1982). Indeed, once expressed in host haemocytes, the PDV of C. rubecula induces profound modifications of cell-surface properties, actin cytoskeleton structure, and adhesion capacities of the immune cells within 6 h of their injection into hosts (Asgari et al., 1996). In this system, a combination of factors thus provides a synergistic effect and ensures short-term and long-term protection to the developing para-sitoid. In the closely related species Cotesia kariyai, venom is also required for successful parasitism (Wago and Tanaka, 1989) and combined injections of C. kariyai bracovirus (CkBV) and venom induced apoptosis of circulating haemocytes in the host P. separata (Teramoto and Tanaka, 2004). In the late stages of parasitism, the parasitoid larvae are protected by teratocytes, cells that derive from their extraembryonic serosa, and which do not divide inside the host's haemolymph but undergo a considerable increase in size. These cells release a yet-to-be-identified inhibitor of PO activity (Tanaka and Wago, 1990). In Cotesia melanoscela, the venom is required for the uncoating and persistence of viral DNA but not for viral entry into host cells (Stoltz et al., 1988). In other braconid models, the venom is not strictly necessary for the function of bracoviruses but can increase their impact on host physiology. This is notably the case for the venom of M. demolitor, which amplifies the effects of MdBV on the immune system and the development of the host P. includens (Strand, 1994). In most ichneumo-nid wasps, PDVs and venoms appear to act independently (Stoltz and Guzo, 1986; Asgari, 2006).

In the ichneumonid wasp Tranosema rostrale an uncommon association between the PDVs and the egg chorion has been reported (Cusson et al., 1998). The authors suggested that the delivery of the virus to specific host tissues could be enhanced by the fact that the virus lodges in the fine hairlike projections of the egg chorion. This example is evocative of some non-PDV-carrying parasitoids, in which structural properties of the egg chorion avoid encapsulation (Prevost et al., 2005).

In the ichneumonid wasp C. sonorensis, venom, ovarian proteins, and PDVs co-operatively protect parasitoid eggs and larvae by disrupting the host encapsulation response and other aspects of innate immunity (Edson et al., 1981; Li and Webb, 1994; Webb and Luckhart, 1994; Luckhart and Webb, 1996; Webb, 1998). During parasitization by C. sono-rensis encapsulation is transiently inhibited by ovarian proteins, and in the longer term by PDVs. The ability of PDVs to establish a persistent infection of parasitized hosts determines the host range of this wasp (Cui et al, 2000). Interestingly, Webb and Summers (1990) have revealed the existence of antigenic and sequence homologies between some proteins of the viral envelope of CsIV and venom proteins of C. sonorensis. According to the authors, expression of venom-related viral genes would enhance the survival of parasite eggs.

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