Carbonylated proteins are eliminated during reproduction in C. elegans

Abstract

Summary Oxidatively damaged proteins accumulate with age in many species (Stadtman (1992) Science257, 1220–1224). This means that damage must be reset at the time of reproduction. To visualize this resetting in the roundworm Caenorhabditis elegans, a novel immunofluorescence technique that allows the detection of carbonylated proteins in situ was developed. The application of this technique revealed that carbonylated proteins are eliminated during C. elegans reproduction. This purging occurs abruptly within the germline at the time of oocyte maturation. Surprisingly, the germline was markedly more oxidized than the surrounding somatic tissues. Because distinct mechanisms have been proposed to explain damage elimination in yeast and mice (Aguilaniu et al. (2003) Science299, 1751–1753; Hernebring et al. (2006) Proc Natl Acad Sci USA103, 7700–7705), possible common mechanisms between worms and one of these systems were tested. The results show that, unlike in yeast (Aguilaniu et al. (2003) Science299, 1751–1753; Erjavec et al. (2008) Proc Natl Acad Sci USA105, 18764–18769), the elimination of carbonylated proteins in worms does not require the presence of the longevity‐ensuring gene, SIR‐2.1. However, similar to findings in mice (Hernebring et al. (2006) Proc Natl Acad Sci USA103, 7700–7705), proteasome activity in the germline is required for the resetting of carbonylated proteins during reproduction in C. elegans. Thus, oxidatively damaged proteins are eliminated during reproduction in worms through the proteasome. This finding suggests that the resetting of damaged proteins during reproduction is conserved, therefore validating the use of C. elegans as a model to study the molecular basis of damage elimination.

Effects of aging and reproduction on protein quality control in soma and gametes of Drosophila melanogaster

“…This is in line with other studies, which demonstrate that the germline, like the soma, displays aging-related features, including increased oxidative damage (Goudeau & Aguilaniu, 2010). For example, the function of D. melanogaster germline stem cells declines upon aging, and this can, in part, be counteracted by overproduction of superoxide dismutase (Pan et al, 2007).…”

Mitochondrial Function Is Required for Secretion of DAF-28/Insulin in C. elegans

“…We measured the relative amount of carbonylated proteins which result from protein oxidation in emv(RNAi)- treated and tomm-40(RNAi) -treated larvae of similar ages (Figure 4C). The levels of carbonylated proteins in worms is an indirect measure of its redox status, since proteins that are oxidized become irreversibly carbonylated [34] and since the carbonylation status in worms is not reset until embryogenesis [35]. Using this assay we could detect no significant difference between lysates from emv(RNAi) and tomm-40(RNAi) animal.…”

A lysosomal switch triggers proteostasis renewal in the immortal C. elegans germ lineage

“…Studies in C. elegans have suggested that damage-clearance mechanisms in the germline may prevent parental damage from being transmitted to progeny5. In the C. elegans hermaphrodite, germ cells form a developmental gradient, with mature oocytes located proximally, near the sperm (Fig.…”

“…1a). Protein carbonylation, a form of oxidative damage, is high in immature distal germ cells, but decreases in sperm-proximal oocytes5. This decrease is likely to be signalled by sperm-derived ‘major sperm proteins’ (MSPs), which trigger meiotic maturation in nearby oocytes2,6 (Fig.…”