Maybe repressed mRNAs are not stored in the chromatoid body in mammalian spermatids

Kleene, Kenneth C.; Cullinane, Danielle Louise

doi:10.1530/rep-11-0113

Cited by 10 publications

(12 citation statements)

References 52 publications

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“…The high levels of polysomal Ldhc mRNA in both gradients validate the integrity of the polysomes and suggest that YBX2 is not an important repressor of the Ldhc mRNA. Kleene & Cullinane (2011)). We used an in situ hybridization protocol in which 24-48 tiled 20-base oligonucleotides specific for individual RNA species are 5 0 end labeled with fluorochromes (Raj et al 2008).…”

Section: Depletion Of Ybx2 Results In Premature Recruitment Of the Prmentioning

confidence: 99%

“…6A, B, C, D, H and I). The relatively strong RNA-FISH signals in the chromatoid body can be explained by the fact that the chromatoid body represents !0.4% of the volume of the cytoplasm (Kleene & Cullinane 2011). This number can be used to calculate that if 5% of an mRNA was in chromatoid body and 95% of that mRNA was in the cytoplasm, the concentration of the mRNA would be 13-fold higher in the chromatoid body.…”

Section: Depletion Of Ybx2 Results In Premature Recruitment Of the Prmentioning

confidence: 99%

“…The prematurely translated Smcp mRNA in Ybx2-null round spermatids is also concentrated in the chromatoid body. Evidently, sequestration in the chromatoid body is not sufficient for prolonged repression, and sucrose gradient analysis suggests that free-mRNPs and polysomes are present in the general cytoplasm (reviewed in Kleene & Cullinane (2011)). The transitory localization of repressed mRNAs in the chromatoid body is clearly demonstrated by the first detection of the Tnp2 and Prm2 mRNAs simultaneously in the chromatoid body and the cytoplasm (Saunders et al 1992, Fukuda et al 2013.…”

Section: Discussionmentioning

confidence: 99%

“…However, it is unclear whether the chromatoid body functions as a remodeling center, which regulates the interactions of RBPs and miRNAs with mRNAs, or a realization center, which carries out the consequences of these interactions. An especially relevant question here is whether translationally repressed free-mRNPs are formed and stored in the chromatoid body or formed in the chromatoid body and stored in the general cytoplasm (reviewed in Kleene & Cullinane (2011)). …”

Section: Introductionmentioning

confidence: 99%

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Mechanisms of translational repression of the Smcp mRNA in round spermatids

Cullinane¹,

Chowdhury²,

Kleene³

2015

Reproduction

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The protamine 1 (Prm1) and sperm mitochondria-associated, cysteine-rich protein (Smcp) mRNAs exemplify a widespread pattern of mRNA-specific regulation of mRNA translation in post-meiotic spermatogenic cells, spermatids. Both mRNAs are transcribed and initially stored in free-mRNPs in early spermatids, and translated on polysomes in late spermatids. In this study, we demonstrate that the 5 0 and 3 0 -UTRs and the 3 0 terminus of the Smcp 3 0 -UTR are required for normal repression of the Smcp mRNA in transgenic mice. RNA affinity chromatography and mass spectrometry sequencing identified Y-box protein 2 (YBX2/MSY2) as the major protein that interacts with the 3 0 terminus of the Smcp 3 0 -UTR and a Y-box recognition sequence, GCCACCU, in the translation control element that is necessary for Prm1 mRNA repression. Depletion of YBX2 in Ybx2-null mice prematurely activates Prm1 and Smcp mRNA translation in early spermatids. Fluorescent in situ hybridization reveals that the Smcp intron, the Smcp mRNA, and both Smcp-Gfp transgenic mRNAs are strongly concentrated in the chromatoid body, and that theYbx2-null mutation does not eliminate the Smcp mRNA from the chromatoid body. This and previous findings suggest that the Smcp pre-mRNA is spliced and associates with YBX2 in the chromatoid body, and that repressed free-mRNPs are stored in the general cytoplasm. As YBX2 is the predominant protein in testis free-mRNPs, it likely represses many mRNAs in early spermatids. The mechanisms by which YBX2 represses the Smcp and Prm1 mRNAs are relevant to reproductive medicine because mutations in the human YBX2 gene correlate with abnormal protamine expression and male infertility.

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Section: Depletion Of Ybx2 Results In Premature Recruitment Of the Prmentioning

confidence: 99%

Section: Depletion Of Ybx2 Results In Premature Recruitment Of the Prmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Mechanisms of translational repression of the Smcp mRNA in round spermatids

Cullinane¹,

Chowdhury²,

Kleene³

2015

Reproduction

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“…In this context, it is interesting to note the existence of the chromatoid body, a germ cell-specific RNA processing center suggested to be involved in the sequestration and translation repression of several mRNAs during spermiogenesis (Kotaja & Sassone-Corsi 2007) and whose RNA and protein content was recently analyzed (Meikar et al 2014). However, the direct contribution of this organelle to translational regulation remains to be clearly demonstrated (for review, see Kleene & Cullinane (2011)). …”

Section: Correlating Transcription and Translation Rates During Spermmentioning

confidence: 99%

Linking transcriptomics and proteomics in spermatogenesis

Chalmel¹,

Rolland²

2015

Reproduction

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Spermatogenesis is a complex and tightly regulated process leading to the continuous production of male gametes, the spermatozoa. This developmental process requires the sequential and coordinated expression of thousands of genes, including many that are testisspecific. The molecular networks underlying normal and pathological spermatogenesis have been widely investigated in recent decades, and many high-throughput expression studies have studied genes and proteins involved in male fertility. In this review, we focus on studies that have attempted to correlate transcription and translation during spermatogenesis by comparing the testicular transcriptome and proteome. We also discuss the recent development and use of new transcriptomic approaches that provide a better proxy for the proteome, from both qualitative and quantitative perspectives. Finally, we provide illustrations of how testis-derived transcriptomic and proteomic data can be integrated to address new questions and how the 'proteomics informed by transcriptomics' technique, by combining RNA-seq and MS-based proteomics, can contribute significantly to the discovery of new protein-coding genes or new protein isoforms expressed during spermatogenesis.Reproduction (2015) 150 R149-R157

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Roles of RNA-binding Proteins and Post-transcriptional Regulation in Driving Male Germ Cell Development in the Mouse

Licatalosi

2016

Advances in Experimental Medicine and Biology

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Tissue development and homeostasis are dependent on highly regulated gene expression programs in which cell-specific combinations of regulatory factors determine which genes are expressed and the post-transcriptional fate of the resulting RNA transcripts. Post-transcriptional regulation of gene expression by RNA-binding proteins has critical roles in tissue development—allowing individual genes to generate multiple RNA and protein products, and the timing, location, and abundance of protein synthesis to be finely controlled. Extensive post-transcriptional regulation occurs during mammalian gametogenesis, including high levels of alternative mRNA expression, stage-specific expression of mRNA variants, broad translational repression, and stage-specific activation of mRNA translation. In this chapter, an overview of the roles of RNA-binding proteins and the importance of post-transcriptional regulation in male germ cell development in the mouse is presented.

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Maybe repressed mRNAs are not stored in the chromatoid body in mammalian spermatids

Cited by 10 publications

References 52 publications

Mechanisms of translational repression of the Smcp mRNA in round spermatids

Mechanisms of translational repression of the Smcp mRNA in round spermatids

Linking transcriptomics and proteomics in spermatogenesis

Roles of RNA-binding Proteins and Post-transcriptional Regulation in Driving Male Germ Cell Development in the Mouse

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