Troponin I controls ovulatory contraction of non-striated actomyosin networks in the C. elegans somatic gonad

Abstract

SummaryThe myoepithelial sheath of the Caenorhabditis elegans somatic gonad has non-striated actomyosin networks that provide contractile forces during ovulation, a process in which a mature oocyte is expelled from the ovary. Troponin T and troponin C are known regulators of contraction of the myoepithelial sheath. These are two of the three components of the troponin complex that is generally considered as a striated-muscle-specific regulator of actomyosin contraction. Here, we report identification of troponin I as the third component of the troponin complex that regulates ovulatory contraction of the myoepithelial sheath. C. elegans has four genes encoding troponin-I isoforms. We found that tni-1 and unc-27 (also known as tni-2) encode two major troponin-I isoforms in the myoepithelial sheath. Combination of RNA interference and mutation of tni-1 and unc-27 resulted in loss of the troponin-I protein in the gonad and caused sterility due to defective contraction of the myoepithelial sheath. Troponin-I-depleted gonads were hypercontracted, which is consistent with the function of troponin I as an inhibitor of actomyosin contraction. Troponin I was associated with nonstriated actin networks in a tropomyosin-dependent manner. Our results demonstrate that troponin I regulates contraction of nonstriated actomyosin networks and is an essential cytoskeletal component of the C. elegans reproductive system.

Sea Lily Muscle Lacks a Troponin-Regulatory System, While it Contains Paramyosin

“…Deficiency of troponin in the echinoderm muscles seemed strange, as troponin is detectable not only in the muscles of chordates but also in the muscles of many protostomes. Moreover, troponin has been detected in actin filament networks in non-striated muscle of the tardigrades (water bears) (Obinata et al, 2011) and in gonad myoepithelial cells of nematodes (Ono and Ono, 2004;Obinata et al, 2010), suggesting the possibility that troponin is involved in the regulation of a variety of motile cells. In this study, we focused on an isocrinid sea lily (stalked crinoid), a taxon that constitutes the most basal group of extant echinoderms (Rouse et al, 2013) and a member of subphylum Pelmatozoa, to clarify whether troponin is lacking from the beginning of the evolution of echinoderms.…”

Detection of a troponin I-like protein in non-striated muscle of the tardigrades (water bears)

“…polyclonal antibody that was raised against Ascaris troponin I 21 specifically recognizes nematode TnI in Ascaris 21 and C. elegans. 12,22 As shown in figure 1a, the antibody reacted specifically with a single band of roughly 31 kDa in the tardigrade extracts ( fig. 1a, lane 2).…”

“…In C. elegans, four TnI isoforms are present and differentially expressed in the pharynx and body wall muscle. 12,24,25 Likewise, tardigrades may have multiple muscle-type-specific TnI isoforms, and a pharynx-specific isoform might not be recognized by the anti-Ascaris TnI antibody. It is also possible that the tardigrade pharynx uses a regulatory system for contraction that is independent of troponin.…”

“…In these cells, actin and myosin are organized in non-striated filamentous networks, and troponin C and troponin I are associated with actin filaments. 11,12 Their contraction is tightly coupled with oocyte maturation and troponin plays an essential role for the contractile regulation. [11][12][13] Furthermore, TnI is involved in the regulation of chromosomal stability and cell polarity in early Drosophila embryos.…”

“…11,12 Their contraction is tightly coupled with oocyte maturation and troponin plays an essential role for the contractile regulation. [11][12][13] Furthermore, TnI is involved in the regulation of chromosomal stability and cell polarity in early Drosophila embryos. 14 These observations suggest that troponin may play important roles not only in striated muscles but also in non-striated muscle or even in non-muscle cells.…”