Octopamine-MAPK-SKN-1 signaling suppresses mating-induced oxidative stress in Caenorhabditis elegans gonads to protect fertility

Tsai, Yi‐Hung; Lin, Yu-Chun; Lee, Ying-Hue

doi:10.1016/j.isci.2023.106162

Cited by 5 publications

(3 citation statements)

References 62 publications

(70 reference statements)

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“…In contrast, AMNP, a tardigrade-specific peroxidase, was highly expressed in males, suggesting enhanced protection against oxidative stress. Similar observations have been made in the sperm of many animals (94, 95). Together, the sex-biased expression of anhydrobiosis genes may provide protection for sex-specific tissues.…”

Section: Discussionsupporting

confidence: 86%

Sexual dimorphism in the tardigradeParamacrobiotus metropolitanustranscriptome

Sugiura,

Yoshida,

Hayashi

et al. 2024

Preprint

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Background In gonochoristic animals, the sex determination pathway induces different morphological and behavioral features that can be observed between sexes, a condition known as sexual dimorphism. While many components of this sex differentiation cascade shows high levels of diversity, factors such as the Doublesex-Mab-3-related transcription factor (DMRT) are highly conserved throughout animals. Species of the phylum Tardigrada exhibits remarkable diversity in morphology and behavior between sexes, suggesting a pathway regulating such dimorphism. Despite the wealth of genomic and zoological knowledge accumulated in recent studies, the sexual differences in tardigrades genomes have not been identified. In this study, we focused on the gonochoristic species Paramacrobiotus metropolitanus and employed omics analyses to unravel the molecular basis of sexual dimorphism. Results Transcriptome analysis between sex identified numerous differentially expressed genes, of which approximately 2,000 male-biased genes were focused on 29 non-male-specific genomic loci. From these regions, we identified two Macrobiotidae family specific DMRT paralogs, which were significantly upregulated in males and lacked sex specific splicing variants. Furthermore, phylogenetic analysis indicated all tardigrade genomes lacks the doublesex ortholog, suggesting doublesex emerged after the divergence of Tardigrada. In contrast to sex-specific expression, no evidence of genomic difference between the sexes were found. We also identified several anhydrobiosis genes exhibiting sex-biased expression, possibly suggesting a mechanism for protection of sex specific tissues against extreme stress. Conclusions This study provides a comprehensive analysis for analyzing the genetic differences between sexes in tardigrades. The existence of male-biased, but not male-specific, genomic loci and identification of the family specific male-biased DMRT subfamily would provide the foundation for understanding the sex determination cascade. In addition, sex-biased expression of several tardigrade-specific genes which are involved their stress tolerance suggests a potential role in protecting sex-specific tissue and gametes.

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Section: Discussionsupporting

confidence: 86%

Sexual dimorphism in the tardigradeParamacrobiotus metropolitanustranscriptome

Sugiura,

Yoshida,

Hayashi

et al. 2024

Preprint

View full text Add to dashboard Cite

show abstract

“…In contrast, AMNP, a tardigrade-specific peroxidase, was highly expressed in males, suggesting enhanced protection against oxidative stress. Similar observations have been made in the sperm of many animals [ 95 , 96 ]. Together, the sex-biased expression of anhydrobiosis genes may provide protection for sex-specific tissues.…”

Section: Discussionsupporting

confidence: 85%

Sexual dimorphism in the tardigrade Paramacrobiotus metropolitanus transcriptome

Sugiura,

Yoshida,

Hayashi

et al. 2024

Zoological Lett

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Background In gonochoristic animals, the sex determination pathway induces different morphological and behavioral features that can be observed between sexes, a condition known as sexual dimorphism. While many components of this sex differentiation cascade show high levels of diversity, factors such as the Doublesex-Mab-3-Related Transcription factor (DMRT) are widely conserved across animal taxa. Species of the phylum Tardigrada exhibit remarkable diversity in morphology and behavior between sexes, suggesting a pathway regulating this dimorphism. Despite the wealth of genomic and zoological knowledge accumulated in recent studies, the sexual differences in tardigrades genomes have not been identified. In the present study, we focused on the gonochoristic species Paramacrobiotus metropolitanus and employed omics analyses to unravel the molecular basis of sexual dimorphism. Results Transcriptome analysis between sex-identified specimens revealed numerous differentially expressed genes, of which approximately 2,000 male-biased genes were focused on 29 non-male-specific genomic loci. From these regions, we identified two Macrobiotidae family specific DMRT paralogs, which were significantly upregulated in males and lacked sex specific splicing variants. Furthermore, phylogenetic analysis indicated all tardigrade genomes lack the doublesex ortholog, suggesting doublesex emerged after the divergence of Tardigrada. In contrast to sex-specific expression, no evidence of genomic differences between the sexes was found. We also identified several anhydrobiosis genes that exhibit sex-biased expression, suggesting a possible mechanism for protection of sex-specific tissues against extreme stress. Conclusions This study provides a comprehensive analysis for analyzing the genetic differences between sexes in tardigrades. The existence of male-biased, but not male-specific, genomic loci and identification of the family specific male-biased DMRT subfamily provides the foundation for understanding the sex determination cascade. In addition, sex-biased expression of several tardigrade-specific genes which are involved their stress tolerance suggests a potential role in protecting sex-specific tissue and gametes.

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“…Octopamine has higher scavenging ability on the 2,2-diphenyl-1-picrylhydrazyl free radical, superoxide anion free radical, and hydroxyl free radical than its tyramine precursor (Bour et al, 2003). Octopamine activates the Gq-coupled octopamine receptor SER-3 and mitogen-activated protein kinase pathway, which promotes glutathione biosynthesis and protects nematodes from mating-induced ROS (Tsai et al, 2023). Conversely, PBDEs affect thyroid function and oxidative stress, which are key contributors for the pathogenesis of TC (Zhou et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

Identification of serum metabolites associated with polybrominated diphenyl ethers (PBDEs) exposure in papillary thyroid carcinoma: A case–control study

Song,

Liu,

Peng

et al. 2024

Preprint

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Thyroid cancer (TC) is the most common endocrine cancer with a sharply increasing incidence worldwide in recent years. Multiple factors including genetics, radiation, iodine, autoimmune disease, and exposure to environmental endocrine–disrupting chemicals (EDCs) may be related to the incidence of TC. Polybrominated diphenyl ethers (PBDEs) have been extensively used in electronic production, soft furnishings, fabrics, and paints as flame retardants since the 1980s. As a typical EDCs, high PBDEs exposure is associated with an increased risk of TC. However, interference with the metabolic signature in PBDEs exposure–related TC has not been studied. In this study, eight congeners of PBDEs were determined in serum from 111 patents with papillary thyroid cancer (PTC) and 111 healthy participants based on case–control epidemiology using gas chromatography–atmospheric pressure chemical ionization–tandem mass spectrometry (GC-APCI-MS/MS). Based on the tertile distribution of total PBDEs concentrations in 59 participants, metabolomics analysis was performed by ultra-high performance liquid chromatography coupled to hybrid quadrupole-Orbitrap MS. The 29 identified metabolites were correlated with PBDEs exposure (Partial correlation analysis, P < 0.05). Furthermore, (+/-)-octopamine and 5-hydroxyindole, which modify the actions of neurotransmitters, were identified as potentially disturbed metabolite markers of TC upon PBDEs exposure. The PBDEs disturbed the glycerophospholipids, sphingolipids, and taurine and hypotaurine metabolism, which showed that neurotransmitters, oxidative stress, and inflammation were the sensitive pathways in PTC. These are the first findings on metabolic disturbance in PTC associated with PBDEs exposure by MS nontargeted metabolomics.

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Octopamine-MAPK-SKN-1 signaling suppresses mating-induced oxidative stress in Caenorhabditis elegans gonads to protect fertility

Cited by 5 publications

References 62 publications

Sexual dimorphism in the tardigradeParamacrobiotus metropolitanustranscriptome

Sexual dimorphism in the tardigradeParamacrobiotus metropolitanustranscriptome

Sexual dimorphism in the tardigrade Paramacrobiotus metropolitanus transcriptome

Identification of serum metabolites associated with polybrominated diphenyl ethers (PBDEs) exposure in papillary thyroid carcinoma: A case–control study

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