twin, a CCR4 homolog, regulates cyclin poly(A) tail length to permit Drosophila oogenesis.
Cyclins regulate progression through the cell cycle. Control of cyclin levels is essential in Drosophila oogenesis for the four synchronous divisions that generate the 16 cell germ line cyst and for ensuring that one cell in each cyst, the oocyte, is arrested in meiosis, while the remaining fifteen cells become polyploid nurse cells. Changes in cyclin levels could be achieved by regulating transcription, translation or protein stability. The proteasome limits cyclin protein levels in the Drosophila ovary, but the mechanisms regulating RNA turnover or translation remain largely unclear. Here, we report the identification of twin, a homolog of the yeast CCR4 deadenylase. We show that twin is important for the number and synchrony of cyst divisions and oocyte fate. Consistent with the deadenylase activity of CCR4 in yeast, our data suggest that Twin controls germ line cyst development by regulating poly(A) tail lengths of several targets including Cyclin A (CycA) RNA. twin mutants exhibit very low expression of Bag-of-marbles (Bam), a regulator of cyst division, indicating that Twin/Ccr4 activity is necessary for wild-type Bam expression. Lowering the levels of CycA or increasing the levels of Bam suppresses the defects we observe in twin ovaries, implicating CycA and Bam as downstream effectors of Twin. We propose that Twin/Ccr4 functions during early oogenesis to coordinate cyst division, oocyte fate specification and egg chamber maturation.
Morris
Jason Z
JZ
Developmental Genetics Program, Department of Cell Biology, The Skirball Institute and Howard Hughes Medical Institute, NYU School of Medicine, New York, NY 10016, USA.
Hong
Amy
A
Lilly
Mary A
MA
Lehmann
Ruth
R
D000241:Adenosine / Q000378:metabolism*; D000595:Amino Acid Sequence; D000818:Animals; D016213:Cyclins / Q000096:biosynthesis* / Q000235:genetics; D004330:Drosophila / Q000235:genetics / Q000378:metabolism*; D029721:Drosophila Proteins / Q000096:biosynthesis / Q000235:genetics / Q000378:metabolism*; D005260:Female; D005786:Gene Expression Regulation; D008969:Molecular Sequence Data; D009866:Oogenesis / Q000235:genetics / Q000502:physiology*; D011108:Polymers / Q000378:metabolism*; D012333:RNA, Messenger / Q000378:metabolism; D012260:Ribonucleases / Q000235:genetics / Q000378:metabolism*; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics
D016213:Cyclins; D029721:Drosophila Proteins; D011108:Polymers; D012333:RNA, Messenger; D029701:Saccharomyces cerevisiae Proteins; C091674:bam protein, Drosophila; C069424:polyadenosine; C078657:CCR4 protein, S cerevisiae; D012260:Ribonucleases; C500128:twin protein, Drosophila; D000241:Adenosine