Selective destruction of a host blood cell type by a parasitoid wasp.

Abstract

Foreign objects that enter the hemocoel of Drosophila melanogaster larvae are encapsulated by one type of blood cell, the lamellocyte, yet eggs of the parasitoid wasp Leptopilina heterotoma remain unencapsulated in D. melano. gaster larval hosts that have many lamellocytes. Here we demonstrate that shortly after a female wasp oviposits in the hemocoel the lamellocytes undergo morphological changes and lose their adhesiveness. These affected blood cells are eventually destroyed as the parasitoid egg continues its development. The factor responsible for lamellocyte destruction, lamellolysin, is contained in an accessory gland of the female reproductive system and is injected along with the egg into the host hemocoel.Lamellolysin does not alter the morphology or the defense functions of the other types of blood cells in the host.Large foreign bodies entering the hemocoel of an insect are encapsulated by the circulating blood cells and permanently sealed in melanized cellular capsules. Thus, the successful development of a parasitoid wasp egg in the hemocoel of an insect host depends upon its ability to avoid encapsulation by its host's blood cells. Some parasitoid wasp eggs have special surface features so that they do not arouse a host defense response (1, 2). Other wasps actively interfere with host blood cell function when they oviposit. In the latter category are the ichneumonids that coinfect their hosts with viruses during oviposition so that the host's immune system as well as its growth are influenced (3-5). When melanotic tumor (symbol, tu) mutant larvae of Drosophila melanogaster are parasitized by some strains of the cynipid wasp, Leptopilina heterotoma (formerly, Pseudeucoila bochei), the encapsulation of host aberrant tissues to form the inert black masses known as melanotic tumors is blocked together with the inhibition of encapsulation of the wasp eggs (6, 7). The hemocytes of parasitized and unparasitized insect hosts have been compared (8-10), but how the host's immune system is suppressed by parasitoid wasps has not been elucidated.In this report we describe the loss of adhesiveness and eventual destruction of the type of blood cell that encapsulates foreign bodies. We also demonstrate that the factor responsible for suppression of encapsulation in the host is present in the reservoir associated with an accessory gland of the female wasp reproductive system. MATERIALS AND METHODS Insects. A sex-linked, temperature-sensitive melanotic tumor mutant of D. melanogaster, tu(J)Sz's, which develops melanotic masses in the posterior fat body when the larvae are grown at 26°C but not at 18°C (11), was used for the experiments. Larvae were raised at 26°C on cream of wheat/ molasses medium seeded with live yeast. Two autosomal recessive melanotic tumor mutations, tu(2)W and tu(2)bw (12, 13), were used to confirm that the effects of parasitization on lamellocytes are not strain specific. For exposure to female wasps, early third instar larvae were rinsed with distilled H20 and transferred to filter pa...

Lamellocyte differentiation in Drosophila larvae parasitized by Leptopilina

“…1). As reported in earlier studies (5,14,15), no lamellocytes were found adhering to L. heterotoma eggs, but L. boulardi eggs were encapsulated by lameUocytes. The lamellocytes in hosts with L. boulardi eggs were normal in shape, but elongated lamellocytes as well as the normal, discoidal lamellocytes were present in hemolymph samples from hosts with L. heterotoma eggs (Table 1, Fig.…”

“…However, the fate of the newly differentiated lameUocytes differs in the hosts with L. heterotoma and L. boulardi eggs. Newly differentiated lamellocytes encapsulate L. boulardi eggs, but the induced lameUocytes in the hosts with L. heterotoma eggs are incapacitated and destroyed in the same manner as reported previously for lamellocytes present in melanotic tumor larvae at the time of parasitization (5,14). Thus, the virus-like particles of L. heterotoma females function to destroy lameUocytes produced in the host, not to block the differentiation of lamellocytes.…”

“…Lamellocytes are discoidal blood cells with sticky surfaces (3,4). In melanotic tumor larvae parasitized by Leptopilina heterotoma, a cynipid wasp, the lamellocytes lose their surface adhesiveness and become bipolar cells (5). These modified lamellocytes are incapa-ble of forming capsules and are eventually destroyed so the parasitoid eggs in the host hemocoel develop unmolested by the type of host blood cell potentially harmful to them.…”

“…It has been demonstrated recently that the destructive factor for host lamellocytes is a virus-like particle from an accessory gland of the female wasp's reproductive system (6). No detrimental effects on the plasmatocytes and crystal cells of parasitized hosts have been observed (5), suggesting that the virus-like particles injected into the host along with eggs by the parasitoid female selectively destroy host lamellocytes.…”

Tissue specificity of a baculovirus-expressed, basement membrane-degrading protease in larvae of Heliothis virescens

“…Cellular defense is mediated by the phagocytic activities of plasmatocytes (Hoffmann and Reichhart, 2002;Rizki and Rizki, 1984) A characteristic manifestation of the phagocytosis and encapsulation response in insects is melanization. The pigment appears on the surface of the cuticle where the pathogen breaches the integument, as well as on and very near the surfaces of organisms that have invaded the hemocoel of the host Nappi and Christensen, 2005).…”