A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila.
PIWI-interacting RNAs (piRNAs) silence retrotransposons in Drosophila germ lines by associating with the PIWI proteins Argonaute 3 (AGO3), Aubergine (Aub) and Piwi. piRNAs in Drosophila are produced from intergenic repetitive genes and piRNA clusters by two systems: the primary processing pathway and the amplification loop. The amplification loop occurs in a Dicer-independent, PIWI-Slicer-dependent manner. However, primary piRNA processing remains elusive. Here we analysed piRNA processing in a Drosophila ovarian somatic cell line where Piwi, but not Aub or AGO3, is expressed; thus, only the primary piRNAs exist. In addition to flamenco, a Piwi-specific piRNA cluster, traffic jam (tj), a large Maf gene, was determined as a new piRNA cluster. piRNAs arising from tj correspond to the untranslated regions of tj messenger RNA and are sense-oriented. piRNA loading on to Piwi may occur in the cytoplasm. zucchini, a gene encoding a putative cytoplasmic nuclease, is required for tj-derived piRNA production. In tj and piwi mutant ovaries, somatic cells fail to intermingle with germ cells and Fasciclin III is overexpressed. Loss of tj abolishes Piwi expression in gonadal somatic cells. Thus, in gonadal somatic cells, tj gives rise simultaneously to two different molecules: the TJ protein, which activates Piwi expression, and piRNAs, which define the Piwi targets for silencing.
Saito
Kuniaki
K
Keio University School of Medicine, Tokyo 160-8582, Japan.
Inagaki
Sachi
S
Mituyama
Toutai
T
Kawamura
Yoshinori
Y
Ono
Yukiteru
Y
Sakota
Eri
E
Kotani
Hazuki
H
Asai
Kiyoshi
K
Siomi
Haruhiko
H
Siomi
Mikiko C
MC
D000818:Animals; D060565:Argonaute Proteins; D015816:Cell Adhesion Molecules, Neuronal / Q000378:metabolism; D002460:Cell Line; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D004331:Drosophila melanogaster / Q000235:genetics / Q000378:metabolism*; D004722:Endoribonucleases / Q000378:metabolism; D005260:Female; D017344:Genes, Insect / Q000235:genetics; D056426:Genetic Loci / Q000235:genetics; D051473:Maf Transcription Factors, Large / Q000235:genetics / Q000378:metabolism*; D008297:Male; D010053:Ovary / Q000166:cytology / Q000378:metabolism; D010641:Phenotype; D011518:Proto-Oncogene Proteins / Q000235:genetics / Q000378:metabolism*; D012313:RNA / Q000096:biosynthesis / Q000235:genetics / Q000378:metabolism*; D034622:RNA Interference; D012323:RNA Processing, Post-Transcriptional; D034743:RNA-Induced Silencing Complex / Q000235:genetics / Q000378:metabolism*; D013737:Testis / Q000166:cytology / Q000378:metabolism
D060565:Argonaute Proteins; D015816:Cell Adhesion Molecules, Neuronal; D029721:Drosophila Proteins; C061565:Fas3 protein, Drosophila; D051473:Maf Transcription Factors, Large; D011518:Proto-Oncogene Proteins; D034743:RNA-Induced Silencing Complex; C116498:piwi protein, Drosophila; C480048:tj protein, Drosophila; D012313:RNA; D004722:Endoribonucleases; C521347:Zuc protein, Drosophila