Tropomyosin and Troponin Are Required for Ovarian Contraction in theCaenorhabditis elegansReproductive System

Abstract

Ovulation in the nematode Caenorhabditis elegans is coordinated by interactions between the somatic gonad and germ cells. Myoepithelial sheath cells of the proximal ovary are smooth muscle-like cells, but the regulatory mechanism of their contraction is unknown. We show that contraction of the ovarian muscle requires tropomyosin and troponin, which are generally major actin-linked regulators of contraction of striated muscle. RNA interference of tropomyosin or troponin C caused sterility by inhibiting ovarian contraction that is required for expelling mature oocytes into the spermatheca where fertilization takes place, thus causing accumulation of endomitotic oocytes in the ovary. Tropomyosin and troponin C were associated with actin filaments in the myoepithelial sheath, and the association of troponin C with actin was dependent on tropomyosin. A mutation in the actin depolymerizing factor/cofilin gene suppressed the ovulation defects by RNA interference of tropomyosin or troponin C. These results strongly suggest that tropomyosin and troponin are the actin-linked regulators for contraction of ovarian muscle in the C. elegans reproductive system.

Structural components of the nonstriated contractile apparatuses in the Caenorhabditis elegans gonadal myoepithelial sheath and their essential roles for ovulation

“…2D-F) were specifically expressed in the myoepithelial sheath. We previously demonstrated that PAT-10 troponin C and Ce-kettin, a large immunoglobulinlike repeat protein, were also specific in the myoepithelial sheath (Ono and Ono, 2004;Ono et al, 2006). We found that the monoclonal antibody MH42 against UNC-89, a large obscurin-like thick-filament-associated protein (Benian et al, 1996), specifically stained the proximal myoepithelial sheath (Fig.…”

“…2J-R). In addition, we previously reported that Ce-tropomyosin was expressed in the proximal myoepithelial sheath and the sper- matheca (Ono and Ono, 2004). All of these structural proteins, except for actin, were not significantly detected in the germline as observed at different focal planes (data not shown).…”

“…This finding suggests that the thin filaments in the myoepithelial sheath may have variable length and that the filament ends may not be tightly aligned. We have previously shown that tropomyosin (CeTM) and PAT-10 troponin C localize to the thin filaments in the myoepithelial sheath (Ono and Ono, 2004). Ce-kettin (MH44 antigen) also localizes to the thin filaments in the myoepithelial sheath, but it is limited to a narrow region near the dense bodies (Ono et al, 2005.…”

“…Troponin and tropomyosin function as actin-linked Ca 2ϩ sensors in the thin filaments of the myoepithelial sheath cells and are required for ovulation (Myers et al, 1996;Ono and Ono, 2004). Thus, these nonstriated muscle cells are atypical, as troponin is generally expressed in striated muscle.…”

“…Ovulation is perturbed by disturbing functions of several structural proteins, including MUP-2 troponin T (Myers et al, 1996), PAT-10 troponin C (Ono and Ono, 2004), LEV-11 tropomyosin (Ono and Ono, 2004), PAT-3 ␤-integrin , talin (Cram et al, 2003), PAT-4 integrin-linked kinase (Xu et al, 2006), and UNC-112 Mig-2 (Xu et al, 2006). However, overall organization and molecular components of the contractile apparatuses of the myoepithelial sheath are not clearly understood.…”