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A redox signalling globin is essential for reproduction in Caenorhabditis elegans.

ABSTRACT: Moderate levels of reactive oxygen species (ROS) are now recognized as redox signalling molecules. However, thus far, only mitochondria and NADPH oxidases have been identified as cellular sources of ROS in signalling. Here we identify a globin (GLB-12) that produces superoxide, a type of ROS, which serves as an essential signal for reproduction in C. elegans. We find that GLB-12 has an important role in the regulation of multiple aspects in germline development, including germ cell apoptosis. We further describe how GLB-12 displays specific molecular, biochemical and structural properties that allow this globin to act as a superoxide generator. In addition, both an intra- and extracellular superoxide dismutase act as key partners of GLB-12 to create a transmembrane redox signal. Our results show that a globin can function as a driving factor in redox signalling, and how this signal is regulated at the subcellular level by multiple control layers.

SUBMITTER: De Henau S

PROVIDER: S-EPMC4686822 | biostudies-literature | 2015 Dec

REPOSITORIES: biostudies-literature

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A redox signalling globin is essential for reproduction in Caenorhabditis elegans.

De Henau Sasha S Tilleman Lesley L Vangheel Matthew M Luyckx Evi E Trashin Stanislav S Pauwels Martje M Germani Francesca F Vlaeminck Caroline C Vanfleteren Jacques R JR Bert Wim W Pesce Alessandra A Nardini Marco M Bolognesi Martino M De Wael Karolien K Moens Luc L Dewilde Sylvia S Braeckman Bart P BP

Nature communications 20151201

Moderate levels of reactive oxygen species (ROS) are now recognized as redox signalling molecules. However, thus far, only mitochondria and NADPH oxidases have been identified as cellular sources of ROS in signalling. Here we identify a globin (GLB-12) that produces superoxide, a type of ROS, which serves as an essential signal for reproduction in C. elegans. We find that GLB-12 has an important role in the regulation of multiple aspects in germline development, including germ cell apoptosis. We ...[more]

PMID: 26621324

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Project description:In Caenorhabditis elegans, the binding of Piwi protein to a non-coding RNA form, called piRNA, has been found to be important to both reproductive and aging processes. As the biosynthesis of piRNA is modulated by mitochondrial function, it is likely that the interaction between mitochondrial function and piRNA expression plays an unknown, yet important, role in reproductive and aging processes because both processes are known to be affected by declines in mitochondrial quality and activity. While the relationship between reproduction and longevity is not characterized in full, the optimality theory of aging and the disposable soma theory suggest that a trade-off between energy and resources is needed for reproductive and aging maintenance. In this study, the influence of mitochondrial variations, via a respiratory chain complex IV (COX1) polymorphism, on piRNA expression was examined in relation to the reproductive and aging outcomes of C. elegans. The COX1 polymorphism in mitochondria was found to affect the number of piRNAs expressed, the development of germ cells, and the length of the lifespan of the nematodes. Interestingly, more than two-thirds of the piRNA expression changes associated with the mitochondrial variation were found to also be affected by age. A gene ontology analysis of the altered piRNA species found that the piRNAs affected by mitochondrial variation and age were linked to genes known to have roles in reproductive and developmental function. Moreover, a piRNA-lncRNA-mRNA regulatory network based on the differential expression patterns of piRNA related to the mitochondrial variation was constructed to further identify potential gene targets with functional interactions. Similarly, this network identified genes involved in reproduction, development, and aging processes. These findings provide new insight into understanding how mitochondrial variations may regulate piRNA expression and may influence the underlying molecular mechanisms that affect reproduction and aging.

Dataset Information

A redox signalling globin is essential for reproduction in Caenorhabditis elegans.

Publications

A redox signalling globin is essential for reproduction in Caenorhabditis elegans.

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