An env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus.

Abstract

The gypsy element of Drosophila differs from most LTR retrotransposons in containing a third open reading frame that resembles retroviral env genes. The protein encoded by ORF3 is glycosylated and processed, like all retroviral envelope proteins. The protein is expressed at high levels in fly strains in which gypsy elements are active. In these strains the protein is found primarily in viral particles. When larvae of fly strains in which gypsy is normally inactive are exposed to sucrose gradient fractions containing these particles, a high level of gypsy insertion activity is observed in their progeny. Thus, gypsy has the expected properties of an insect retrovirus. [Key Words: Drosophila; mutagenesis; transposable element; insect retrovirus] Received May 6, 1994; revised version accepted July 11, 1994.The gypsy element of Drosophila melanogaster has been classified traditionally as a long terminal repeat (LTR) retrotransposon; however, it is one of a small group of LTR retrotransposons from insects that are unusual in that they contain three open reading frames (ORFs). In these retroelements, the first two ORFs correspond to retroviral gag and poi, whereas ORF3 is of unknown function but corresponds in size and genomic location to retroviral env (Fig. 1). All elements with three ORFs described so far are from insects, either Drosophila or the lepidopteran Trichoplusia ni. Recent results have shown that in two elements encoding an ORF3, gypsy and tom, a subgenomic mRNA similar in structure to retroviral env mRNAs can be found (P61isson et al. 1994;Tanda et al. 1994). In the case of gypsy, this transcript is observed only in certain strains in which gypsy transpositional activity is high (P41isson et al. 1994). The primary sequences of the encoded ORF3 proteins of these elements are quite variable and show no obvious similarity to retroviral Env proteins. However, retroviral Env proteins are themselves very variable in primary sequence. Like retroviral Env proteins, the proteins encoded by "retrotransposon" ORF3s contain a putative transmembrane domain near their carboxyl terminus, multiple putative N-glycosylation sites, and putative protease cleavage sites (resembling the cleavage sites in a variety of retroviral Env proteins) at conserved positions (Fig. 1 }. These features of gypsy and the other ORF3-containing insect retrotransposons have prompted the suggestion that these elements may represent endogenous insect retro- viruses (Boeke 1988;Boeke and Corces 1989;Coffin 1993).To address the question of whether gypsy represents a virus or a transposon more directly, we have turned to the use of Drosophila strains that show genetic instabilities associated with high-frequency insertion by gypsy elements. These strains are characterized by a large number of full-length gypsy elements in the euchromatin, appearance of gypsy insertion mutations at high frequency, and the presence of both large amounts of gypsy full-length RNA and spliced ORF3 mRNA (P61isson et al. 1994; N. Prud'homme, M. Gans, M. Masson, C. Ter...

Activation of transcription and retrotransposition of a novel retroelement, Steamer , in neoplastic hemocytes of the mollusk Mya arenaria

“…Those elements that do encode envelope proteins [such as ZAM (37) and gypsy itself (38)] can act as infectious retroviruses and can transmit from cell to cell and from one animal to another, perhaps with the help of cellular vesicle trafficking machinery (37)(38)(39). However, such infection events may take place even without the use of the envelope protein encoded by the element (40), and in these cases an envelope-like protein from the cell, or from a complementing retroelement, may provide the functionality in trans.…”

Revisiting horizontal transfer of transposable elements in Drosophila

“…In D. melanogaster, the gypsy virus-like particles are capable of efficiently infecting the germ line of strains devoid of active gypsy, and a high level of insertion activity is observed in their progeny (Song et al, 1994). Its infectious properties result from the expression of the env gene, encoding a protein responsible for its infectivity (Kim et al, 1994;Song et al, 1994;Teysset et al, 1998;Chalvet et al, 1999).…”

Evolutionary conservation and molecular characteristics of repetitive sequences of Drosophila koepferae

“…Horizontal transmission may be invoked to explain the similarity among active copies (Mizrokhi & Mazo, 1991). Recent evidence suggesting that Gypsy may behave as an infectious virus (Kim et at., 1994;Song et a!., 1994) makes this hypothesis very attractive. The characterization of active elements in other species will eventually explain the evolutionary history of this element.…”