Sexual Preferences in Nutrient Utilization Regulate Oxygen Consumption and Reactive Oxygen Species Generation in Schistosoma mansoni: Potential Implications for Parasite Redox Biology
نویسندگان
چکیده
Schistosoma mansoni, one of the causative agents of human schistosomiasis, has a unique antioxidant network that is key to parasite survival and a valuable chemotherapeutic target. The ability to detoxify and tolerate reactive oxygen species increases along S. mansoni development in the vertebrate host, suggesting that adult parasites are more exposed to redox challenges than young stages. Indeed, adult parasites are exposed to multiple redox insults generated from blood digestion, activated immune cells, and, potentially, from their own parasitic aerobic metabolism. However, it remains unknown how reactive oxygen species are produced by S. mansoni metabolism, as well as their biological effects on adult worms. Here, we assessed the contribution of nutrients and parasite gender to oxygen utilization pathways, and reactive oxygen species generation in whole unpaired adult S. mansoni worms. We also determined the susceptibilities of both parasite sexes to a pro-oxidant challenge. We observed that glutamine and serum importantly contribute to both respiratory and non-respiratory oxygen utilization in adult worms, but with different proportions among parasite sexes. Analyses of oxygen utilization pathways revealed that respiratory rates were high in male worms, which contrast with high non-respiratory rates in females, regardless nutritional sources. Interestingly, mitochondrial complex I-III activity was higher than complex IV specifically in females. We also observed sexual preferences in substrate utilization to sustain hydrogen peroxide production towards glucose in females, and glutamine in male worms. Despite strikingly high oxidant levels and hydrogen peroxide production rates, female worms were more resistant to a pro-oxidant challenge than male parasites. The data presented here indicate that sexual preferences in nutrient metabolism in adult S. mansoni worms regulate oxygen utilization and reactive oxygen species production, which may differently contribute to redox biology among parasite sexes.
منابع مشابه
Role of oxygen reactive species in Schistosoma mansoni egg-induced granulomatous inflammation.
The role of oxygen reactive species in granulomatous hypersensitivity was explored using a model of pulmonary granulomas induced by intravenous injection of eggs from the parasite Schistosoma mansoni. Macrophages from sychronously developing lesions spontaneously released significant quantities of superoxide anion (26 nmoles/10(6)/2h) by 8 days of development. In contrast, the non-T cell foreig...
متن کاملOxidative Stress and its Role in Female Infertility and Assisted Reproduction: Clinical Implications
Reactive oxygen species (ROS) are involved in physiological functions and act as mediators in various signaling processes. Elevated or sustained generation of free radicals and non radical species derived from free radicals can lead to an imbalance in the intracellular redox homeostasis. Normally, any excess levels of reactive radical and nonradical species generated are intercepted by antioxid...
متن کاملAn example of molecular co-evolution: reactive oxygen species (ROS) and ROS scavenger levels in Schistosoma mansoni/Biomphalaria glabrata interactions.
The co-evolution between hosts and parasites involves huge reciprocal selective pressures on both protagonists. However, relatively few reports have evaluated the impact of these reciprocal pressures on the molecular determinants at the core of the relevant interaction, such as the factors influencing parasitic virulence and host resistance. Here, we address this question in a host-parasite mod...
متن کاملSchistosome serine protease inhibitors: parasite defense or homeostasis?
Serpins are a structurally conserved family of macromolecular inhibitors found in numerous biological systems. The completion and annotation of the genomes of Schistosoma mansoni and Schistosoma japonicum has enabled the identification by phylogenetic analysis of two major serpin clades. S. mansoni shows a greater multiplicity of serpin genes, perhaps reflecting adaptation to infection of a hum...
متن کاملImpact of Reactive Oxygen Species on Spermatozoa: ABalancing Act between Beneficial and Detrimental Effects
Reactive oxygen species (ROS)plays an important role in sperm motility. The physiological generation at low concentration induces beneficial effects on sperm functions and plays a significant role in sperm metabolism. Meanwhile, the excessive generation of reactive oxygen species can overwhelm protective mechanism and triggers changes in lipid and protein layers of sperm plasma membrane, which ...
متن کامل