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Vol. 20, Issue 17, 3888-3895, September 1, 2009

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Caenorhabditis elegans FOS-1 and JUN-1 Regulate plc-1 Expression in the Spermatheca to Control Ovulation

Susan M. Hiatt^*, Holli M. Duren^*, Y. John Shyu^*, Ronald E. Ellis, Naoki Hisamoto, Kunihiro Matsumoto, Ken-ichi Kariya, Tom K. Kerppola^||, and Chang-Deng Hu^*

*Department of Medicinal Chemistry and Molecular Pharmacology, School of Pharmacy and Pharmaceutical Sciences, Purdue University, West Lafayette, IN 47907; Department of Molecular Biology, School of Osteopathic Medicine, University of Medicine and Dentistry of New Jersey, Stratford, NJ 08084; Division of Biological Science, Graduate School of Science, Institute for Advanced Research, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan; Division of Cell Biology, Graduate School of Medicine, University of the Ryukyus, Nishihara-cho, Okinawa 903-0215, Japan; and ^||Howard Hughes Medical Institute and Department of Biological Chemistry, University of Michigan Medical School, Ann Arbor, MI 48109

Submitted August 13, 2008; Revised June 17, 2008; Accepted June 23, 2009
Monitoring Editor: William P. Tansey

Fos and Jun are components of activator protein-1 (AP-1) and play crucial roles in the regulation of many cellular, developmental, and physiological processes. Caenorhabditis elegans fos-1 has been shown to act in uterine and vulval development. Here, we provide evidence that C. elegans fos-1 and jun-1 control ovulation, a tightly regulated rhythmic program in animals. Knockdown of fos-1 or jun-1 blocks dilation of the distal spermathecal valve, a critical step for the entry of mature oocytes into the spermatheca for fertilization. Furthermore, fos-1 and jun-1 regulate the spermathecal-specific expression of plc-1, a gene that encodes a phospholipase C (PLC) isozyme that is rate-limiting for inositol triphosphate production and ovulation, and overexpression of PLC-1 rescues the ovulation defect in fos-1(RNAi) worms. Unlike fos-1, regulation of ovulation by jun-1 requires genetic interactions with eri-1 and lin-15B, which are involved in the RNA interference pathway and chromatin remodeling, respectively. At least two isoforms of jun-1 are coexpressed with fos-1b in the spermatheca, and different AP-1 dimers formed between these isoforms have distinct effects on the activation of a reporter gene. These findings uncover a novel role for FOS-1 and JUN-1 in the reproductive system and establish C. elegans as a model for studying AP-1 dimerization.

Address correspondence to: Chang-Deng Hu (cdhu{at}pharmacy.purdue.edu)