Effects of lipopolysaccharide on maturation of bovine oocyte <i>in vitro</i> and its possible mechanisms

Zhao, Shanjiang; Pang, Yuxin; Zhao, Xiao‐Fan; Du, Weihua; Huang, Hao; Zhu, Huabin

doi:10.18632/oncotarget.13965

Cited by 29 publications

(20 citation statements)

References 51 publications

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“…Previous data suggest that exposure of COCs to either LPS or TNF‐α reduces progression to the blastocyst stage of development by 16 or 8 percentage points, respectively (Soto et al, ). Our work here and by others have demonstrated alterations in the machinery and status of the epigenome of the oocyte following exposure to LPS (Zhao et al, ). We hope that future experimentation will be able to evaluate the epigenetics and phenotype of cattle conceived following oocyte exposures.…”

Section: Discussionsupporting

confidence: 73%

“…In addition, we observed an LPS‐mediated increase in transcript abundance of the histone deacetylase HDAC1 , suggesting possible dysregulation of histone posttranslational modifications. Interestingly, it has been reported that oocytes matured in the presence of LPS have reduced DNA methylation (5‐mC) and histone H3 lysine 9 dimethylation (H3K9me2), whereas histone H3 lysine 4 dimethylation (H3K4me2) is increased (Zhao et al, ). It is interesting to postulate if the altered transcripts involved in epigenetic programing observed here may affect enduring epigenetic marks that could affect the phenotype of subsequent offspring.…”

Section: Discussionmentioning

confidence: 99%

“…Uterine infections are common in cows, and subsequently LPS accumulates in follicular fluid, altering the microenvironment of oocyte development (Herath et al, 2007;Piersanti et al, 2019). In vitro maturation (IVM) of bovine cumulus-oocyte complexes (COCs) in the presence of LPS increases failure of the meiotic cell cycle (Bromfield & Sheldon, 2011;Zhao et al, 2017), and subsequently decreases blastocyst development (Soto, Natzke, & Hansen, 2003b). Similarly in human in vitro production (IVP) of embryos, the presence of LPS culture medium reduces clinical pregnancy (Fishel, Jackson, Webster, & Faratian, 1988;Nagata & Shirakawa, 1996;Snyman & Van der Merwe, 1986).…”

mentioning

confidence: 99%

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Lipopolysaccharide and tumor necrosis factor‐alpha alter gene expression of oocytes and cumulus cells during bovine in vitro maturation

Piersanti

Santos

Sheldon

et al. 2019

Molecular Reproduction Devel

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Communication between the oocyte and cumulus facilitates oocyte growth, cell cycle regulation, and metabolism. This communication is mediated by direct contact between oocytes and cumulus cells, and soluble secreted molecules. Secreted molecules involved in this process are known inflammatory mediators. Lipopolysaccharide (LPS) is detected in follicular fluid and is associated with reduced fertility, whereas accumulation of inflammatory mediators in follicular fluid, including tumor necrosis factor-α (TNF-α), is associated with female infertility. Maturation of oocytes in the presence of LPS or TNF-α reduces meiotic maturation and the capacity to develop to the blastocyst. Here we evaluated the abundance of 92 candidate genes involved immune function, epigenetic modifications, embryo development, oocyte secreted factors, apoptosis, cell cycle, and cell signaling in bovine cumulus cells or zona-free oocytes after exposure to LPS or TNF-α during in vitro maturation. We hypothesize that LPS or TNF-α will alter the abundance of transcripts in oocytes and cumulus cell in a cell type dependent manner. Exposure to LPS altered abundance of 31 transcripts in oocytes (including ACVR1V, BMP15, DNMT3A) and 12 transcripts in cumulus cells (including AREG, FGF4, PIK3IP1). Exposure to TNF-α altered 1 transcript in oocytes (IGF2) and 4 transcripts in cumulus cells (GJA1, PLD2, PTGER4, STAT1). Cumulus expansion was reduced after exposure to LPS or TNF-α. Exposing COCs to LPS had a marked effect on expression of targeted transcripts in oocytes. We propose that altered oocyte transcript abundance is associated with reduced meiotic maturation and embryo development observed in oocytes cultured in LPS or TNF-α.

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Section: Discussionsupporting

confidence: 73%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Lipopolysaccharide and tumor necrosis factor‐alpha alter gene expression of oocytes and cumulus cells during bovine in vitro maturation

Piersanti

Santos

Sheldon

et al. 2019

Molecular Reproduction Devel

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“…The active states of lipopolysaccharide, tumor necrosis factor (TNF), and phorbol myristate acetate (PMA) were predicted in the aged oocytes based on the expression changes of their downstream genes in our dataset (Additional file 1: Figure S2). Exposure to lipopolysaccharide was reported to inhibit the maturation potential of bovine oocytes by affecting cell cycle, cytoskeletal dynamics, oxidative stress, and epigenetic modifications [20]. In porcine and cattle, TNF could inhibit the maturation of oocytes from GV to MII stage and increase the proportion of oocytes with abnormal chromosome alignment and cytoskeleton structure [21,22].…”

Section: Decoding Transcriptional Dynamics During Oocyte Agingmentioning

confidence: 99%

Simultaneous transcriptome and methylome profiles of single mouse oocytes provide novel insights on maturation and aging

Yan

Cao

Liao

et al. 2020

Preprint

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Background: Advanced maternal aging has become a worldwide public health issue that contributes to female fertility decline and significant risk to embryo development. Despite transcriptional and epigenetic alterations reported in oocyte maturation and development, the dynamics of gene expression and DNA dynamics associated with aging remain elusive. Here we generated simultaneous transcriptome and methylome profiles of mouse oocytes during aging and maturation at single-cell and single-base resolution to examine key biological processes and identify the key targets for novel treatment options. Results:. We report the dynamics in transcriptome and DNA methylome in mouse oocytes during maternal aging and oocyte maturation. Age-associated gene expression changes showed mitochondrial dysfunction in GV oocytes and defects of chromosome segregation and spindle assembly in MII oocytes. EIF2 signaling protein synthesis pathway was also impaired during aged oocyte maturation. Moreover, distinctive DNA methylation patterns were demonstrated during maternal aging in GV and MII oocytes. A positive correlation between gene expression and methylation in gene body was characterized. Furthermore, we identified several promising biomarkers, including IL-7, to assess oocyte quality, which are potential therapeutic targets for improve oocyte maturation. More importantly, we built the first mouse oocyte maturation and age prediction model using transcriptome data and validated its feasibility in published data. Conclusions: This work provides a better understanding of molecular and cellular mechanisms during mouse oocyte aging, points a new direction of oocyte quality assessment, and paves the way for developing novel treatments to improve oocyte maturation and quality in the future.

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“…At the mitosis stage, gene expression could be propagated by the histone acetylation, the level of H3K4me2 was increased, but the DNA methylation (5-mC) and H3K9me2 were decreased (Zhao et al, 2017), while the misexpression could be caused by the aberrant H3K4me3 and H3K27me3 (Xu et al, 2017). If the discharge of the PB1 is suppressed, the level of H3K4me2 will increase, while the level of 5mC and H3K9me2 will decrease (Zhao et al, 2017).…”

Section: Figmentioning

confidence: 99%

The Effect of Epigenetic Changes on the Extrusion of the First Polar Body in Pig Oocytes DuringIn VitroMaturation

Qian

et al. 2019

Cellular Reprogramming

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The present study was designed to investigate the comprehensive function of maternal factors of primordial germ cell 7 (PGC7) and POU5F1-POU class 5 homeobox 1 (OCT4), as well as the epigenetic modification roles on the mitosis for the extrusion of first polar body (PB1) in pig maturated oocytes. First, the common distribution of histone modifications, including H3K4me2, H3K27me3, H3K9me2, and H4K12ac and DNA methylation, were detected at the high level in the nucleus. However, only one part of the chromosome was higher methylated or acetylated when the mitosis happened to extrude the PB1. When the mitosis was inhibited by the cytochalasin B (CB) treatment, the expression of PGC7, OCT4, DNA methyltransferase1 (DNMT1), DNA methyltransferase3b (DNMT3b), tet methylcytosine dioxygenase 1 (TET1), tet methylcytosine dioxygenase 2 (TET2), and tet methylcytosine dioxygenase 3 (TET3) could be inhibited (p < 0.01), and no concentrated expression of the PGC7 and OCT4 was observed on the chromosome, but the levels of H3K9me2 and H4K12ac were higher. In addition, when the trichostatin A was performed on the in vitro maturation, the extrusion of the PB1 was inhibited too. And the histone methylation (H3K9me2 and H3K27me3) could be detected all the time with relative higher level and no demethylation could be observed. However, the expression of PGC7 and OCT4 was lower in the chromosome. It might indicate that the maternal factor of PGC7 and histone modification that included H4K12ac and H3K9me2 could regulate the extrusion of the PB1 and play an important role in the maturation of pig oocytes.

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Effects of lipopolysaccharide on maturation of bovine oocyte in vitro and its possible mechanisms

Cited by 29 publications

References 51 publications

Lipopolysaccharide and tumor necrosis factor‐alpha alter gene expression of oocytes and cumulus cells during bovine in vitro maturation

Lipopolysaccharide and tumor necrosis factor‐alpha alter gene expression of oocytes and cumulus cells during bovine in vitro maturation

Simultaneous transcriptome and methylome profiles of single mouse oocytes provide novel insights on maturation and aging

The Effect of Epigenetic Changes on the Extrusion of the First Polar Body in Pig Oocytes DuringIn VitroMaturation

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