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Vol. 14, No. 20, pp. 2596-2609, October 15, 2000

RESEARCH PAPER
CPEB proteins control two key steps in spermatogenesis in C. elegans

Cameron Luitjens,1 Maria Gallegos,1,4,6 Brian Kraemer,2,5,6 Judith Kimble,2,3 and Marvin Wickens2,7

1 Program in Cell and Molecular Biology, 2 Department of Biochemistry, and 3 Howard Hughes Medical Institute, University of Wisconsin, Madison, Wisconsin 53706, USA

Cytoplasmic polyadenylation element binding (CPEB) proteins bind to and regulate the translation of specific mRNAs. CPEBs from Xenopus, Drosophila, and Spisula participate in oogenesis. In this report, we examine the biological roles of all identifiable CPEB homologs in a single organism, Caenorhabditis elegans. We find four homologs in the C. elegans genome: cbp-1, cpb-2, cpb-3, and fog-1. Surprisingly, two homologs, CPB-1 and FOG-1, have key functions in spermatogenesis and are dispensable for oogenesis. CPB-2 and CPB-3 also appear not to be required for oogenesis. CPB-1 is essential for progression through meiosis: cpb-1(RNAi) spermatocytes fail to undergo the meiotic cell divisions. CPB-1 protein is present in the germ line just prior to overt spermatogenesis; once sperm differentiation begins, CPB-1 disappears. CPB-1 physically interacts with FBF, another RNA-binding protein and 3' UTR regulator. In addition to its role in controlling the sperm/oocyte switch, we find that FBF also appears to be required for spermatogenesis, consistent with its interaction with CPEB. A second CPEB homolog, FOG-1, is required for specification of the sperm fate. The fog-1 gene produces fog-1(L) and fog-1(S) transcripts. The fog-1(L) RNA is enriched in animals making sperm and is predicted to encode a larger protein; fog-1(S) RNA is enriched in animals making oocytes and is predicted to encode a smaller protein. The relative abundance of the two mRNAs is controlled temporally during germ-line development and by the sex determination pathway in a fashion that suggests that the fog-1(L) species encodes the active form. In sum, our results demonstrate that, in C. elegans, two CPEB proteins have distinct functions in the germ line, both in spermatogenesis: FOG-1 specifies the sperm cell fate and CPB-1 executes that decision.

[Key Words: CPEB proteins; C. elegans; spermatogenesis; FOG-1; CPB-1; translational control]


Present addresses: 4University of California, Department of Anatomy, San Francisco, CA 94143-0452, USA

5 Seattle VA Medical Center, University of Washington, Seattle, WA 98108, USA.

6 These authors contributed equally to this work.

7 Corresponding author.


GENES & DEVELOPMENT 14:2596-2609 © 2000 by Cold Spring Harbor Laboratory Press  ISSN 0890-9369/00 $5.00

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