Cellular Immune Response Involving Multinucleated Giant Hemocytes with Two-Step Genome Amplification in the Drosophilid <b><i>Zaprionus indianus</i></b>

Abstract

Previously, a novel cell type, the multinucleated giant hemocyte (MGH) was identified in the ananassae subgroup of Drosophilidae. These cells share several features with mammalian multinucleated giant cells, a syncytium of macrophages formed during granulomatous inflammation. We were able to show that MGHs also differentiate in Zaprionus indianus, an invasive species belonging to the vittiger subgroup of the family, highly resistant to a large number of parasitoid wasp species. We have classified the MGHs of Z. indianus as giant hemocytes belonging to a class of cells which also include elongated blood cells carrying a single nucleus and anuclear structures. They are involved in encapsulating parasites, originate from the lymph gland, can develop by cell fusion, and generally carry many nuclei, while possessing an elaborated system of canals and sinuses, resulting in a spongiform appearance. Their nuclei are all transcriptionally active and show accretion of genetic material. Multinucleation and accumulation of the genetic material in the giant hemocytes represents a two-stage amplification of the genome, while their spongy ultrastructure substantially increases the contact surface with the extracellular space. These features may furnish the giant hemocytes with a considerable metabolic advantage, hence contributing to the mechanism of the effective immune response.Insect Stocks and Culturing Z. indianus strain #1 and strain #3 [20] were kindly provided by Bálint Z. Kacsoh (University of Pennsylvania, USA). Stocks were kept at 25 ° C on standard yeast-cornmeal food. The experiments were done with both strains. As the antigen manifestation and all tested parameters were the same in the two stocks, the re-Genome Amplification during the Cellular Immune Response of Drosophila 259

Broad Ultrastructural and Transcriptomic Changes Underlie the Multinucleated Giant Hemocyte Mediated Innate Immune Response against Parasitoids

“…Similar to our previous observations in Z. indianus [ 13 ], we found an MDBS in D. ananassae MGHs, which appeared to contribute to the formation of an electron-dense layer along the attachment site with the parasitoid. The well-organized, lamellar structure of this electron-dense layer likely facilitates strong and stable attachment of MGHs to parasitoids, encapsulation, and possibly degradation.…”

“…Subsequently, these elongated cells fuse with each other and form the terminally differentiated MGHs, which have the capacity to encapsulate invaders [ 12 ]. Previously, in Z. indianus , we found that MGHs carry relatively few vesicles and possess a sponge-like overall ultrastructure formed by an irregular cytoplasmic canalicular system [ 13 ]. By contrast, our current analysis of D. ananassae MGHs revealed a large number of diverse vesicular systems and a canalicular organization which is mostly localized at the cell periphery.…”

“…Previously, we found that in species of the ananassae subgroup and in Zaprionus indianus belonging to the vittiger subgroup of Drosophilidae , the immune response is highly effective and remarkably different from that in D. melanogaster [ 12 , 13 ]. In these species, after infection by parasitoids, giant cells possessing several nuclei, termed as multinucleated giant hemocytes (MGHs), differentiate and encapsulate the invader [ 12 ].…”

“…Similar to lamellocytes, MGHs encapsulate parasitoid wasp eggs and larvae, but do not participate in bacterial phagocytosis, the process of which is mediated by plasmatocytes [ 12 , 13 ]. However, MGHs are highly motile, and their presence is associated with a remarkably efficient protection against parasitoid wasps [ 12 , 13 , 23 , 24 ]. In addition, 1 key step of the immune protection is different between MGHs and lamellocytes.…”

Once upon a Time

“…In the last article published in this issue Gyöngyi Cinege and colleagues carried out functional and developmental analysis of hemocyte subsets and immune compartments. To this end, the authors examined cellular immune re-sponses involving multinucleated giant hemocytes from Zaprionus indianus, an Afrotropical drosophilid species [13]. The authors concluded that the unique features of the cell-mediated immunity of this species provides clues towards the understanding of the immune response accomplished by multinucleated giant hemocytes.…”