GLH-1/Vasa represses neuropeptide expression and drives spermiogenesis in the C. elegans germline

Rochester, Jesse D.; Min, Hyemin; Gajjar, Gita A.; Sharp, Catherine S.; Maki, Nathaniel J.; Rollins, Jarod; Keiper, Brett D.; Graber, Joel H.; Updike, Dustin L.

doi:10.1016/j.ydbio.2022.10.003

Cited by 3 publications

(3 citation statements)

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“…Germ cells that fail at totipotency are relegated to somatic fates with ensuing germline mortality and sterility ( Updike et al, 2014 ). Oocytes that have disrupted P granules mis-appropriately express neuropeptide and sperm genes ( Campbell and Updike, 2015 ; Rochester et al, 2022 ). The 3′ untranslated (UTR) regions of mRNAs are sufficient to regulate expression in most germ cells; however, sperm-expressed genes require 5′ UTRs to specify correct expression patterns ( Shim, 1999 ; Merritt et al, 2008 ; del Castillo-Olivares et al, 2009 ; Kulkarni et al, 2012 ; Ragle et al, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

RNAi-dependent expression of sperm genes in ADL chemosensory neurons is required for olfactory responses in Caenorhabditis elegans

Ow,

Nishiguchi,

Dar

et al. 2024

Front. Mol. Biosci.

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Environmental conditions experienced early in the life of an animal can result in gene expression changes later in its life history. We have previously shown that C. elegans animals that experienced the developmentally arrested and stress resistant dauer stage (postdauers) retain a cellular memory of early-life stress that manifests during adulthood as genome-wide changes in gene expression, chromatin states, and altered life history traits. One consequence of developmental reprogramming in C. elegans postdauer adults is the downregulation of osm-9 TRPV channel gene expression in the ADL chemosensory neurons resulting in reduced avoidance to a pheromone component, ascr#3. This altered response to ascr#3 requires the principal effector of the somatic nuclear RNAi pathway, the Argonaute (AGO) NRDE-3. To investigate the role of the somatic nuclear RNAi pathway in regulating the developmental reprogramming of ADL due to early-life stress, we profiled the mRNA transcriptome of control and postdauer ADL in wild-type and nrde-3 mutant adults. We found 711 differentially expressed (DE) genes between control and postdauer ADL neurons, 90% of which are dependent upon NRDE-3. Additionally, we identified a conserved sequence that is enriched in the upstream regulatory sequences of the NRDE-3-dependent differentially expressed genes. Surprisingly, 214 of the ADL DE genes are considered “germline-expressed”, including 21 genes encoding the Major Sperm Proteins and two genes encoding the sperm-specific PP1 phosphatases, GSP-3 and GSP-4. Loss of function mutations in gsp-3 resulted in both aberrant avoidance and attraction behaviors. We also show that an AGO pseudogene, Y49F6A.1 (wago-11), is expressed in ADL and is required for ascr#3 avoidance. Overall, our results suggest that small RNAs and reproductive genes program the ADL mRNA transcriptome during their developmental history and highlight a nexus between neuronal and reproductive networks in calibrating animal neuroplasticity.

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Section: Discussionmentioning

confidence: 99%

RNAi-dependent expression of sperm genes in ADL chemosensory neurons is required for olfactory responses in Caenorhabditis elegans

Ow,

Nishiguchi,

Dar

et al. 2024

Front. Mol. Biosci.

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“…The overwhelming evidence suggests that the inheritance of gene regulation states is coordinated in the germline P granules [ 280 ]. The absence of germline P granules results in the ectopic expression of somatic genes in the germ line [ 308 , 309 ], and a recent study showed that P granules are important for the ability of RNAi components, particularly PRG-1 and HRDE-1, to distinguish “self” from “non-self” transcripts exiting the nucleus [ 310 ]. Thus, it seems likely that P granules function in the germ line to facilitate which transcripts should be expressed, which should be silenced, and which should be transgenerationally silenced.…”

Section: Progress On Open Questions In Epigenetic Inheritance Biologymentioning

confidence: 99%

Inheritance of Stress Responses via Small Non-Coding RNAs in Invertebrates and Mammals

Ow,

Hall

2023

Epigenomes

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While reports on the generational inheritance of a parental response to stress have been widely reported in animals, the molecular mechanisms behind this phenomenon have only recently emerged. The booming interest in epigenetic inheritance has been facilitated in part by the discovery that small non-coding RNAs are one of its principal conduits. Discovered 30 years ago in the Caenorhabditis elegans nematode, these small molecules have since cemented their critical roles in regulating virtually all aspects of eukaryotic development. Here, we provide an overview on the current understanding of epigenetic inheritance in animals, including mice and C. elegans, as it pertains to stresses such as temperature, nutritional, and pathogenic encounters. We focus on C. elegans to address the mechanistic complexity of how small RNAs target their cohort mRNAs to effect gene expression and how they govern the propagation or termination of generational perdurance in epigenetic inheritance. Presently, while a great amount has been learned regarding the heritability of gene expression states, many more questions remain unanswered and warrant further investigation.

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“…Relevant to the cholesterol efflux, C. elegans [ 52 ] and murine [ 60 ] MKAs might have a common role in spermatids and spermatozoa, respectively. Moreover, RNA helicases contained in germ granules likely act during male germ cell functions in C. elegans and mice; GLH-1, a homolog of the germline-specific Vasa/DDX4 DEAD-box RNA helicase, represses spermatogenic expression during oogenesis in C. elegans , while it promotes MSP expression to drive spermiogenesis and sperm motility [ 61 ]. In mice, the mouse Vasa homolog gene Mvh is involved in proliferation and differentiation of male germ cells [ 62 ].…”

Section: Conclusion and Future Perspectivesmentioning

confidence: 99%

Spermiogenesis in Caenorhabditis elegans: An Excellent Model to Explore the Molecular Basis for Sperm Activation

2023

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C. elegans spermiogenesis converts non-motile spermatids into motile, fertilization-competent spermatozoa. Two major events include the building of a pseudopod required for motility and fusion of membranous organelles (MOs)—intracellular secretory vesicles—with the spermatid plasma membrane required for the proper distribution of sperm molecules in mature spermatozoa. The mouse sperm acrosome reaction—a sperm activation event occurring during capacitation—is similar to MO fusion in terms of cytological features and biological significance. Moreover, C. elegans fer-1 and mouse Fer1l5, both encoding members of the ferlin family, are indispensable for MO fusion and acrosome reaction, respectively. Genetics-based studies have identified many C. elegans genes involved in spermiogenesis pathways; however, it is unclear whether mouse orthologs of these genes are involved in the acrosome reaction. One significant advantage of using C. elegans for studying sperm activation is the availability of in vitro spermiogenesis, which enables combining pharmacology and genetics for the assay. If certain drugs can activate both C. elegans and mouse spermatozoa, these drugs would be useful probes to explore the mechanism underlying sperm activation in these two species. By analyzing C. elegans mutants whose spermatids are insensitive to the drugs, genes functionally relevant to the drugs’ effects can be identified.

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GLH-1/Vasa represses neuropeptide expression and drives spermiogenesis in the C. elegans germline

Cited by 3 publications

References 63 publications

RNAi-dependent expression of sperm genes in ADL chemosensory neurons is required for olfactory responses in Caenorhabditis elegans

RNAi-dependent expression of sperm genes in ADL chemosensory neurons is required for olfactory responses in Caenorhabditis elegans

Inheritance of Stress Responses via Small Non-Coding RNAs in Invertebrates and Mammals

Spermiogenesis in Caenorhabditis elegans: An Excellent Model to Explore the Molecular Basis for Sperm Activation

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