Virus-like particle formation in Drosophila melanogaster germ cells suggests a complex translational regulation of the retrotransposon cycle and new mechanisms inhibiting transposition.
Transposition of 1731, a Drosophila melanogaster LTR retrotransposon, was investigated in reproductive organs by RNA, protein and VLP distribution during its life cycle. We detected 1731 transcription in oogonia but not in spermatogonia; in all cells during oogenesis but only in primary spermatocytes; and in ovarian cytoplasm but both in nuclei and cytoplasm of primary spermatocytes. By confocal scanning, we showed that whereas Gag protein appeared in all cytoplasms during oogenesis, in testes Gag detection began in late premeiotic primary spermatocytes and increased in elongating spermatids suggesting distinct mechanisms of 1731 transcription and translation regulation. By electron microscopy, we did not detect 1731 VLPs in ovaries, suggesting a complex post-translational control blocking VLP assembly and transposition. Interestingly, in testes we discovered VLP aggregates in cystic cytoplasm of maturing partially individualized spermatids. In testes, we observed two delays in 1731 product expressions, suggesting a complex temporal control mechanism. Transcriptional/translational delay may be determined by accumulation of 1731 RNAs in primary spermatocyte nuclei. Translational/VLP assembly delay may be determined by post-transductional mechanisms controlling +1 frameshift and Pol-protein degradation. Our results indicated two differential mechanisms inhibiting 1731 transposition in Drosophila melanogaster ovaries and testes. In addition, we proposed a new mechanism for transposition control at the cell cycle level.
Rachidi
M
M
EA 3508 Université Paris 7-Denis Diderot, Paris, France. mrachidi@9online.fr
Lopes
C
C
Benichou
J-C
JC
Hellio
R
R
Maisonhaute
C
C
D000818:Animals; D004331:Drosophila melanogaster / Q000648:ultrastructure / Q000821:virology*; D020077:Endogenous Retroviruses / Q000235:genetics* / Q000302:isolation & purification / Q000648:ultrastructure; D005260:Female; D015686:Gene Products, env / Q000235:genetics; D007150:Immunohistochemistry; D017403:In Situ Hybridization; D008297:Male; D010053:Ovary / Q000648:ultrastructure; D018626:Retroelements; D020079:Terminal Repeat Sequences / Q000235:genetics; D013737:Testis / Q000648:ultrastructure
D015686:Gene Products, env; D018626:Retroelements