The combination treatment of cholesterol‐loaded methyl‐β‐cyclodextrin and methyl‐β‐cyclodextrin significantly improves the fertilization capacity of vitrified bovine oocytes by protecting fertilization protein JUNO

Tang, Hao; Zhang, Peipei; Huang, Hao; Du, Weihua; Pang, Yuxin; Zhao, Shanjiang; Zou, Huiying; Zhu, Huabin; Wang, Yu; Li, Shujing; Zhao, Xiao‐Fan

doi:10.1111/rda.13890

Cited by 9 publications

(3 citation statements)

References 61 publications

(81 reference statements)

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“…In addition, preloading of cholesterol into the MBCD facilitates the insertion of cholesterol into the sperm membrane and inhibits the cryoinjury that occurs during sperm cryopreservation and thawing [62]. Combination treatment with cholesterol-loaded MBCD and MBCD significantly improves the fertilization capacity of bovine vitrified oocytes [63]. In this study, we showed that DMACD was useful for inducing sperm capacitation, and it could also be applicable for several reproductive engineering techniques, such as sperm cryopreservation and oocyte vitrification.…”

Section: Discussionmentioning

confidence: 83%

Dimethyl-α-cyclodextrin induces capacitation by removing phospholipids from the plasma membrane of mouse sperm

Nakao

Ito

Sakoh

et al. 2023

Biology of Reproduction

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Capacitation is an important event in the completion of fertilization by mammalian sperm. Cholesterol efflux is a trigger of capacitation. In general, cholesterol acceptors of albumin and β-cyclodextrins are used to induce capacitation during in vitro fertilization. Previously, we reported that methyl-β-cyclodextrin (MBCD), which is composed of seven glucoses, had a higher ability to induce capacitation than bovine serum albumin (BSA) in frozen–thawed mouse sperm. Comparison of albumin and cyclodextrins is helpful for understanding the mechanism of capacitation. In this study, we examined the effects of albumin, MBCD, and a different type of cyclodextrin, dimethyl-α-cyclodextrin (DMACD), which is composed of six glucoses, on several events of sperm capacitation. We showed that DMACD induced sperm capacitation and promoted fertilization ability. The time required to increase the fertilization rate differed among BSA, MBCD, and DMACD. BSA and MBCD enhanced cholesterol and phospholipid efflux, whereas DMACD enhanced only phospholipid efflux. BSA, MBCD, and DMACD increased sperm membrane fluidity, rearrangement of the lipid raft, and the acrosome reaction. These findings suggest that phospholipid efflux is a novel trigger of capacitation. Increasing the choice of sperm capacitation inducers may be useful for improving in vitro fertilization (IVF) techniques not only in mice, but also in various species in which it has been difficult to produce embryos by IVF.

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Section: Discussionmentioning

confidence: 83%

Dimethyl-α-cyclodextrin induces capacitation by removing phospholipids from the plasma membrane of mouse sperm

Nakao

Ito

Sakoh

et al. 2023

Biology of Reproduction

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“…Data were normalized to the expression level of reference genes. The primers are shown in Table 1 (Hao et al, 2021), and data were analysed using the comparative Ct (2 −ΔΔCt ) method (Livak & Schmittgen, 2001).…”

Section: Methodsmentioning

confidence: 99%

Study on the expression patterns and function of JUNO and CD9 in bovine oocytes during in vitro maturation

Yang

Tang

Yang

et al. 2022

Reprod Domestic Animals

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Fertilization proteins JUNO and CD9 play vital roles in sperm-egg fusion, but little is known about their expression patterns during in vitro maturation (IVM) and their function during in vitro fertilization (IVF) of bovine oocytes. In this study, qRT-PCR and immunofluorescence staining were used to detect the mRNA and protein expression levels of JUNO and CD9 genes in bovine oocytes and cumulus cells. Then, fertilization rate of MII oocytes treated with (i) JUNO antibody (1, 5 and 25 μg/ml) or (ii) CD9 antibody (1, 5 and 25 μg/ml) or (iii) CD9 antibody (5 μg/ml) + JUNO antibody (5 μg/ml) were recorded. Our results showed that the mRNA and protein expression levels of JUNO and CD9 genes significantly increased from bovine GV oocytes to MII oocytes, and similar mRNA expression patterns of JUNO and CD9 were also detected in cumulus cells. All groups of oocytes treated with CD9 antibody or JUNO antibody showed significantly decreased fertilization rates (p < .05). Particularly, the fertilization ability of oocytes treated with CD9 antibody (5 μg/ml) + JUNO antibody (5 μg/ml) sharply decreased to 3.48 ± 0.11%. In conclusion, our study revealed the expression levels of JUNO and CD9 genes in oocytes and cumulus cells increased during IVM of bovine oocytes, with JUNO protein playing a major role in the fertilization of bovine oocytes.

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“…Studies using bovine, ovine and porcine eggs demonstrated that rising UC cholesterol levels transiently during vitrification preserves oocyte lipid rafts organization and quality, resulting in improved maturation, viability, fertilization, and early development rates after thawing ( Buschiazzo et al, 2017 ; Atalla et al, 2018 ; Chen et al, 2019 ). In a recent paper, Hao et al showed that the level of JUNO, a glycosylphosphatidylinositol (GPI)-anchored protein expressed on the egg surface that is essential for female fertility ( Bianchi et al, 2014 ), was significantly reduced in bovine eggs by vitrification ( Hao et al, 2021 ). The successive treatment of MβCD-Chol/MβCD before/after cryopreservation preserved oocyte JUNO levels and significantly improved fertilization capacity.…”

Section: Introductionmentioning

confidence: 99%

Implications of High-Density Cholesterol Metabolism for Oocyte Biology and Female Fertility

Arias

Quiroz

Santander

et al. 2022

Front. Cell Dev. Biol.

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Cholesterol is an essential component of animal cells. Different regulatory mechanisms converge to maintain adequate levels of this lipid because both its deficiency and excess are unfavorable. Low cell cholesterol content promotes its synthesis and uptake from circulating lipoproteins. In contrast, its excess induces the efflux to high-density lipoproteins (HDL) and their transport to the liver for excretion, a process known as reverse cholesterol transport. Different studies suggest that an abnormal HDL metabolism hinders female fertility. HDL are the only lipoproteins detected in substantial amounts in follicular fluid (FF), and their size and composition correlate with embryo quality. Oocytes obtain cholesterol from cumulus cells via gap junctions because they cannot synthesize cholesterol de novo and lack HDL receptors. Recent evidence has supported the possibility that FF HDL play a major role in taking up excess unesterified cholesterol (UC) from the oocyte. Indeed, genetically modified mouse models with disruptions in reverse cholesterol transport, some of which show excessive circulating UC levels, exhibit female infertility. Cholesterol accumulation can affect the egg´s viability, as reported in other cell types, and activate the plasma membrane structure and activity of membrane proteins. Indeed, in mice deficient for the HDL receptor Scavenger Class B Type I (SR-B1), excess circulating HDL cholesterol and UC accumulation in oocytes impairs meiosis arrest and hinders the developmental capacity of the egg. In other cells, the addition of cholesterol activates calcium channels and dysregulates cell death/survival signaling pathways, suggesting that these mechanisms may link altered HDL cholesterol metabolism and infertility. Although cholesterol, and lipids in general, are usually not evaluated in infertile patients, one study reported high circulating UC levels in women showing longer time to pregnancy as an outcome of fertility. Based on the evidence described above, we propose the existence of a well-regulated and largely unexplored system of cholesterol homeostasis controlling traffic between FF HDL and oocytes, with significant implications for female fertility.

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The combination treatment of cholesterol‐loaded methyl‐β‐cyclodextrin and methyl‐β‐cyclodextrin significantly improves the fertilization capacity of vitrified bovine oocytes by protecting fertilization protein JUNO

Cited by 9 publications

References 61 publications

Dimethyl-α-cyclodextrin induces capacitation by removing phospholipids from the plasma membrane of mouse sperm

Dimethyl-α-cyclodextrin induces capacitation by removing phospholipids from the plasma membrane of mouse sperm

Study on the expression patterns and function of JUNO and CD9 in bovine oocytes during in vitro maturation

Implications of High-Density Cholesterol Metabolism for Oocyte Biology and Female Fertility

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