Gene Expression and Protein Synthesis in Mitochondria Enhance the Duration of High-Speed Linear Motility in Boar Sperm

Zhu, Zhendong; Umehara, Takashi; Okazaki, Tetsuji; Goto, Masaaki; Fujita, Yöko; Hoque, S. A. Masudul; Kawai, Tomoko; Zeng, Wenxian; Shimada, M.

doi:10.3389/fphys.2019.00252

Cited by 64 publications

(84 citation statements)

References 56 publications

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“…This is likely because mature human spermatozoa use glucose and fructose as primary source of ATP. As shown in boar semen, mitochondrial transcription, unlike nuclear transcription, appears fully active and is dependent on ATP [45]. Therefore, it is possible that what we see as an increase of mitochondrial tsRNA is a result of more full-length mitochondrial tRNA caused by sugar-dependent gene transcription.…”

Section: Paralleled Shift In Sperm Motility and Tsrnamentioning

confidence: 61%

Human sperm displays rapid responses to diet

et al. 2019

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The global rise in obesity and steady decline in sperm quality are two alarming trends that have emerged during recent decades. In parallel, evidence from model organisms shows that paternal diet can affect offspring metabolic health in a process involving sperm tRNAderived small RNA (tsRNA). Here, we report that human sperm are acutely sensitive to nutrient flux, both in terms of sperm motility and changes in sperm tsRNA. Over the course of a 2-week diet intervention, in which we first introduced a healthy diet followed by a diet rich in sugar, sperm motility increased and stabilized at high levels. Small RNA-seq on repeatedly sampled sperm from the same individuals revealed that tsRNAs were up-regulated by eating a high-sugar diet for just 1 week. Unsupervised clustering identified two independent pathways for the biogenesis of these tsRNAs: one involving a novel class of fragments with specific cleavage in the T-loop of mature nuclear tRNAs and the other exclusively involving mitochondrial tsRNAs. Mitochondrial involvement was further supported by a similar up-regulation of mitochondrial rRNA-derived small RNA (rsRNA). Notably, the changes in sugarsensitive tsRNA were positively associated with simultaneous changes in sperm motility and negatively associated with obesity in an independent clinical cohort. This rapid response to a dietary intervention on tsRNA in human sperm is attuned with the paternal intergenerational metabolic responses found in model organisms. More importantly, our findings suggest shared diet-sensitive mechanisms between sperm motility and the biogenesis of tsRNA, which provide novel insights about the interplay between nutrition and male reproductive health.

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Section: Paralleled Shift In Sperm Motility and Tsrnamentioning

confidence: 61%

Human sperm displays rapid responses to diet

et al. 2019

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“…TLR7 was detected in sperm tail but TLR8 expressed in the midpiece of sperm, which localized in mitochondria, indicating that the activation of TLR8 directly suppressed mitochondrial activity, and TLR7 inhibited hexokinase activity (Fig 5). In our previous study, ATP production in mitochondria regulated the progressive motility in sperm, and the system was independent on glycolysis [40]. Because sperm motility and ATP level were much decreased by the treatment with R848 as compared with those by R837, it is estimated that both TLR7 and TLR8 would regulate ATP generation, which impacts on sperm motility.…”

Section: Discussionmentioning

confidence: 99%

“…Sperm mitochondrial activity was measured with MitoPT JC-1 Assay Kit (911, ImmunoChemistry Technologies, llc.) according to Zhu and colleagues (2019) [40]. Briefly, sperm samples were incubated with 500 μL 1x working solution at 37 °C for 30 min in dark, the mitochondrial activity was analyzed by flow cytometry using a filter with a bandwidth of 574/26 nm (Attune NxT Acoustic Focusing Cytometer, Invitrogen) and measured as the mean fluorescence intensity (MFI) of JC-1 orange aggregates.…”

Section: Methodsmentioning

confidence: 99%

Activation of Toll-like receptor 7/8 encoded by the X chromosome alters sperm motility and provides a novel simple technology for sexing sperm

2019

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In most mammals, the male to female sex ratio of offspring is about 50% because half of the sperm contain either the Y chromosome or X chromosome. In mice, the Y chromosome encodes fewer than 700 genes, whereas the X chromosome encodes over 3,000 genes. Although overall gene expression is lower in sperm than in somatic cells, transcription is activated selectively in round spermatids. By regulating the expression of specific genes, we hypothesized that the X chromosome might exert functional differences in sperm that are usually masked during fertilization. In this study, we found that Toll-like receptors 7/8 (TLR7/ 8) coding the X chromosome were expressed by approximately 50% of the round spermatids in testis and in approximately 50% of the epididymal sperm. Especially, TLR7 was localized to the tail, and TLR8 was localized to the midpiece. Ligand activation of TLR7/8 selectively suppressed the mobility of the X chromosome-bearing sperm (X-sperm) but not the Y-sperm without altering sperm viability or acrosome formation. The difference in sperm motility allowed for the separation of Y-sperm from X-sperm. Following in vitro fertilization using the ligand-selected high-mobility sperm, 90% of the embryos were XY male. Likewise, 83% of the pups obtained following embryo transfer were XY males. Conversely, the TLR7/8-activated, slow mobility sperm produced embryos and pups that were 81% XX females. Therefore, the functional differences between Y-sperm and X-sperm motility were revealed and related to different gene expression patterns, specifically TLR7/8 on X-sperm. Activation of Toll-like receptor 7/8 encoded by the X chromosome alters sperm motility and provides a novel simple technology for sexing sperm. PLoS Biol 17(8): e3000398. https://doi.including the nuclear condensation, acrosome formation, and the elongation of the sperm flagella [3,4]. As indicated by studies using knockout mouse models, the morphological changes associated with spermiogenesis are associated with the expression of various genes, including Tekt, Tnp, and Gba2 in the round spermatids [5][6][7]. Thus, active gene transcription occurs on chromosomes, including sex chromosomes, in haploid male germ cells, and some of them are essential for cell survival [8]. Using the cytoplasmic bridges between spermatids, cytoplasm including RNAs and proteins are shared to rescue Y chromosome bearing sperm (Y-sperm) [8,9]. It has been reported that the bridge works in spermatid at early stage of spermiogenesis, and the high levels of RNA polymerase II are detected in this stage [10,11]. However, RNA polymerase II is still detected in later stages of spermiogenesis [11], indicating that the unique features of sperm can be distinguished not only by the presence of the X or Y chromosome but also by expression of distinct genes encoded by each sex chromosome.However, mouse Y chromosome encodes fewer than 700 genes, whereas mouse X chromosome encodes over 3,000 genes [12,13]. The X chromosome contains some unique genes, such as Taz encoding tafazzin that is a t...

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“…Western blot (WB) analyses was performed as described previously [59] with some modifications. Briefly, total protein was extracted from sperm in sodium dodecyl sulfate (SDS) sample buffer.…”

Section: Western Blot Analysismentioning

confidence: 99%

miR-26a is Involved in Glycometabolism and Affects Boar Sperm Viability by Targeting PDHX

Wang

Liang

Chang

et al. 2020

Cells

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miR-26a is associated with sperm metabolism and can affect sperm motility and apoptosis. However, how miR-26a affects sperm motility remains largely unknown. Our previous study indicated that the PDHX gene is predicted to be a potential target of miR-26a, which is responsible for pyruvate oxidative decarboxylation which is considered as a key step for connecting glycolysis with oxidative phosphorylation. In this study, we first reported a potential relationship between miR-26a and PDHX and their expressions in fresh, frozen-thawed, and epididymal boar sperm. Then, sperm viability and survival were determined after transfection of miR-26a. mRNA and protein expression level of PDHX in the liquid-preserved boar sperm after transfection were also determined by RT-qPCR and Western Blot (WB). Our results showed that expression level of PDHX was significantly increased during sperm transit from epididymal caput to corpus and cauda. Similarly, expression of PDHX was significantly higher (P < 0.05) in fresh sperm as compared to epididymal cauda and frozen-thawed sperm. However, the expression of miR-26a in epididymal corpus sperm was significantly higher (P < 0.05) than that of caput and cauda sperm. Furthermore, after transfection of boar sperm with miR-26a mimic and inhibitor under liquid storage, the lowest and highest sperm viability was observed in miR-26a mimic and inhibitor treatment (P < 0.05), respectively. The protein levels of PDHX, after 24 and 48 h of transfection of miR-26a mimics and inhibitor, were notably decreased and increased (P < 0.05), respectively, as compared to negative control (NC) group. In conclusion, the novel and enticing findings of our study provide a reasonable evidence that miR-26a via PDHX, a link between glycolysis and oxidative phosphorylation, could regulate the glycometabolic pathway which eventually affect boar sperm viability and survival.

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Gene Expression and Protein Synthesis in Mitochondria Enhance the Duration of High-Speed Linear Motility in Boar Sperm

Cited by 64 publications

References 56 publications

Human sperm displays rapid responses to diet

Human sperm displays rapid responses to diet

Activation of Toll-like receptor 7/8 encoded by the X chromosome alters sperm motility and provides a novel simple technology for sexing sperm

miR-26a is Involved in Glycometabolism and Affects Boar Sperm Viability by Targeting PDHX

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