Gudu, an Armadillo repeat-containing protein, is required for spermatogenesis in Drosophila

Cheng, Wen Ming; Ip, Y. Tony; Xu, Zuoshang

doi:10.1016/j.gene.2013.08.080

Cited by 35 publications

(24 citation statements)

References 27 publications

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“…Among this conserved set are several with established reproductive phenotypes in Drosophila. This includes proteins associated with sperm individualization, including cullin3 (Cul3) and SKP1-related A (SkpA), which acts in cullin-dependent E3 ubiquitin ligase complex required for caspase activity in sperm individualization [ 54 ], gudu, an Armadillo repeat containing protein [ 55 ], and porin (mentioned previously) [ 48 ]. Two proteins involved in sperm motility were also identified: dynein axonemal heavy chain 3 (dnah3) [ 56 ] and an associated microtubule-binding protein growth arrest specific protein 8 (Gas8) [ 57 ].…”

Section: Resultsmentioning

confidence: 99%

Contrasting patterns of evolutionary constraint and novelty revealed by comparative sperm proteomic analysis in Lepidoptera

et al. 2017

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BackgroundRapid evolution is a hallmark of reproductive genetic systems and arises through the combined processes of sequence divergence, gene gain and loss, and changes in gene and protein expression. While studies aiming to disentangle the molecular ramifications of these processes are progressing, we still know little about the genetic basis of evolutionary transitions in reproductive systems. Here we conduct the first comparative analysis of sperm proteomes in Lepidoptera, a group that exhibits dichotomous spermatogenesis, in which males produce a functional fertilization-competent sperm (eupyrene) and an incompetent sperm morph lacking nuclear DNA (apyrene). Through the integrated application of evolutionary proteomics and genomics, we characterize the genomic patterns potentially associated with the origination and evolution of this unique spermatogenic process and assess the importance of genetic novelty in Lepidopteran sperm biology.ResultsComparison of the newly characterized Monarch butterfly (Danaus plexippus) sperm proteome to those of the Carolina sphinx moth (Manduca sexta) and the fruit fly (Drosophila melanogaster) demonstrated conservation at the level of protein abundance and post-translational modification within Lepidoptera. In contrast, comparative genomic analyses across insects reveals significant divergence at two levels that differentiate the genetic architecture of sperm in Lepidoptera from other insects. First, a significant reduction in orthology among Monarch sperm genes relative to the remainder of the genome in non-Lepidopteran insect species was observed. Second, a substantial number of sperm proteins were found to be specific to Lepidoptera, in that they lack detectable homology to the genomes of more distantly related insects. Lastly, the functional importance of Lepidoptera specific sperm proteins is broadly supported by their increased abundance relative to proteins conserved across insects.ConclusionsOur results identify a burst of genetic novelty amongst sperm proteins that may be associated with the origin of heteromorphic spermatogenesis in ancestral Lepidoptera and/or the subsequent evolution of this system. This pattern of genomic diversification is distinct from the remainder of the genome and thus suggests that this transition has had a marked impact on lepidopteran genome evolution. The identification of abundant sperm proteins unique to Lepidoptera, including proteins distinct between specific lineages, will accelerate future functional studies aiming to understand the developmental origin of dichotomous spermatogenesis and the functional diversification of the fertilization incompetent apyrene sperm morph.Electronic supplementary materialThe online version of this article (10.1186/s12864-017-4293-2) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Contrasting patterns of evolutionary constraint and novelty revealed by comparative sperm proteomic analysis in Lepidoptera

et al. 2017

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“…A previous study demonstrated that dysfunction of ARMC4 , a paralog to ARMC3 , impairs physiological function of the cilia and sperm flagella in humans [ 33 ]. Proper function of Gudu , a gene highly homologous to ARMC4 , is essential for an undisturbed spermatogenesis in Drosophila melanogaster [ 34 ]. Our investigations also evidenced an impaired spermatogenesis in bulls homozygous for the frameshift mutation in ARMC3 .…”

Section: Discussionmentioning

confidence: 99%

A frameshift mutation in ARMC3 is associated with a tail stump sperm defect in Swedish Red (Bos taurus) cattle

Pausch¹,

Venhoranta²,

Wurmser³

et al. 2016

BMC Genet

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BackgroundArtificial insemination is widely used in many cattle breeding programs. Semen samples of breeding bulls are collected and closely examined immediately after collection at artificial insemination centers. Only ejaculates without anomalous findings are retained for artificial insemination. Although morphological aberrations of the spermatozoa are a frequent reason for discarding ejaculates, the genetic determinants underlying poor semen quality are scarcely understood.ResultsA tail stump sperm defect was observed in three bulls of the Swedish Red cattle breed. The spermatozoa of affected bulls were immotile because of severely disorganized tails indicating disturbed spermatogenesis. We genotyped three affected bulls and 18 unaffected male half-sibs at 46,035 SNPs and performed homozygosity mapping to map the fertility disorder to an 8.42 Mb interval on bovine chromosome 13. The analysis of whole-genome re-sequencing data of an affected bull and 300 unaffected animals from eleven cattle breeds other than Swedish Red revealed a 1 bp deletion (Chr13: 24,301,425 bp, ss1815612719) in the eleventh exon of the armadillo repeat containing 3-encoding gene (ARMC3) that was compatible with the supposed recessive mode of inheritance. The deletion is expected to alter the reading frame and to induce premature translation termination (p.A451fs26). The mutated protein is shortened by 401 amino acids (46 %) and lacks domains that are likely essential for normal protein function.ConclusionsWe report the phenotypic and genetic characterization of a sterilizing tail stump sperm defect in the Swedish Red cattle breed. Exploiting high-density genotypes and massive re-sequencing data enabled us to identify the most likely causal mutation for the fertility disorder in bovine ARMC3. Our results provide the basis for monitoring the mutated variant in the Swedish Red cattle population and for the early identification of infertile animals.Electronic supplementary materialThe online version of this article (doi:10.1186/s12863-016-0356-7) contains supplementary material, which is available to authorized users.

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“…To our knowledge, this is proved for the first time that circRNA is essential for oocyte maturation and early embryo development. It is previously reported that Gudu is the Drosophila homolog of mammalian ARMC4 which is the host gene of circARMC4 and has been shown to be required for spermatogenesis, but not female fertility (Cheng et al, 2013), predicting that circARMC4 could be involved in the regulation of mammalian reproduction. Besides, miRNA-378 bound by circARMC4 is a negative regulator of porcine oocyte maturation and early embryo development (Pan et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Circular RNA profiling in the oocyte and cumulus cells reveals thatcircARMC4is essential for porcine oocyte maturation

Cao

Gao

et al. 2019

Preprint

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Thousands of circular RNAs (circRNAs) have been recently discovered in cumulus cells and oocytes from several species. However, the expression and function of circRNA during porcine oocyte meiotic maturation have been never examined. Here, we separately identified 7,067 and 637 circRNAs in both the cumulus cell and the oocyte via deep sequencing and bioinformatic analysis. Further analysis revealed that a faction of circRNAs is differentially expressed (DE) in a developmental stage-specific manner. The host genes of DE circRNAs are markedly enriched to multiple signaling pathways associated with cumulus cell function and oocyte maturation. Additionally, most DE circRNAs harbor several miRNA targets, suggesting that these DE circRNAs potentially act as miRNA sponge. Importantly, we found that maternal circARMC4 knockdown by siRNA microinjection caused a severely impaired chromosome alignment, and significantly inhibited first polar body extrusion and early embryo development. Taken together, these results demonstrate for the first time that circRNAs are abundantly and dynamically expressed in a developmental stage-specific manner in cumulus cells and oocytes, and maternally expressed circARMC4 is essential for porcine oocyte meiotic maturation and early embryo development.

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Gudu, an Armadillo repeat-containing protein, is required for spermatogenesis in Drosophila

Cited by 35 publications

References 27 publications

Contrasting patterns of evolutionary constraint and novelty revealed by comparative sperm proteomic analysis in Lepidoptera

Contrasting patterns of evolutionary constraint and novelty revealed by comparative sperm proteomic analysis in Lepidoptera

A frameshift mutation in ARMC3 is associated with a tail stump sperm defect in Swedish Red (Bos taurus) cattle

Circular RNA profiling in the oocyte and cumulus cells reveals thatcircARMC4is essential for porcine oocyte maturation

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