Treatment with cyclic adenosine monophosphate modulators prior to in vitro maturation alters the lipid composition and transcript profile of bovine cumulus–oocyte complexes and blastocysts

Razza, E. M.; Sudano, Mateus José; Fontes, P. K.; Franchi, F; Belaz, K. R. A.; Santos, Pedro César dos; Castilho, A. C. S.; Rocha, Daniele F. O.; Eberlin, Marcos N.; Machado, Marcela Aparecida Guerreiro; Nogueira, Marcelo Fábio Gouveia

doi:10.1071/rd17335

Cited by 17 publications

(22 citation statements)

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“…Gene expression analysis of bovine oocytes was performed using Applied BiosystemsTaqMan Assays, specific for Bos taurus species as previously described by Razza et al 44 , 45 . A total of 96 candidate genes were analyzed (Table 1 ).…”

Section: Methodsmentioning

confidence: 99%

“…COCs were inseminated with 1 × 10 6 sperm/mL at 38.5 °C and 5% CO 2 in humidified air. After 18 h IVF, presumptive zygotes were denuded by 5 min vortexing in pre-IVF medium and washed three times in modified potassium simplex optimization medium (KSOM medium -Embryomax) supplemented with 10% (v/v) FBS, 1.25 µg/mL gentamicin, and 4 µl/mL non-essential amino Gene expression analysis of bovine oocytes was performed using Applied BiosystemsTaqMan Assays, specific for Bos taurus species as previously described by Razza et al 44,45 . A total of 96 candidate genes were analyzed (Table 1).…”

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confidence: 99%

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Autophagy is a pro-survival adaptive response to heat shock in bovine cumulus-oocyte complexes

Latorraca

Feitosa

Mariano

et al. 2020

Sci Rep

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Autophagy is a physiological mechanism that can be activated under stress conditions. However, the role of autophagy during oocyte maturation has been poorly investigated. Therefore, this study characterized the role of autophagy on developmental competence and gene expression of bovine oocytes exposed to heat shock (HS). Cumulus-oocyte-complexes (COCs) were matured at Control (38.5 °C) and HS (41 °C) temperatures in the presence of 0 and 10 mM 3-methyladenine (3MA; autophagy inhibitor). Western blotting analysis revealed that HS increased autophagy marker LC3-II/LC3-I ratio in oocytes. However, there was no effect of temperature for oocytes matured with 3MA. On cumulus cells, 3MA reduced LC3-II/LC3-I ratio regardless of temperature. Inhibition of autophagy during IVM of heat-shocked oocytes (3MA-41 °C) reduced cleavage and blastocyst rates compared to standard in vitro matured heat-shocked oocytes (IVM-41 °C). Therefore, the magnitude of HS detrimental effects was greater in the presence of autophagy inhibitor. Oocyte maturation under 3MA-41 °C reduced mRnA abundance for genes related to energy metabolism (MTIF3), heat shock response (HSF1), and oocyte maturation (HAS2 and GREM1). In conclusion, autophagy is a stress response induced on heat shocked oocytes. inhibition of autophagy modulated key functional processes rendering the oocyte more susceptible to the deleterious effects of heat shock. Autophagy is a programmed lysosomal process that degrades damaged or unnecessary cellular proteins, lipids, DNA, RNA, and organelles for recycling amino acids, fatty acids, and nucleosides to act as cellular building blocks for anabolic processes 1-3. This event is involved in development, differentiation, immunity, aging, and cell death 2. The autophagy pathway can be triggered by different stress conditions in order to restore homeostasis as a prosurvival adaptive response to stress. For example, autophagy can be induced by diseases 4-6 and environmental factors such as nutrient deprivation 7,8 , high temperature 9-11 , oxidative stress 12,13 , hypoxia 14,15 , and toxins 16-18. There are three autophagy types described in mammalian cells: chaperone-mediated autophagy, macroautophagy, and microautophagy 1. In the chaperone-mediated autophagy, heat shock cognate 70 complex (Hsc70 complex) directs abnormal proteins that have KFERQ-like motifs exposed to lysosome-mediated degradation. On the other hand, during microautophagy the lysosome membrane invaginates, thus capturing a small portion of the cytoplasm to be degraded 2. Macroautophagy is the best-understood type of autophagy, which is mediated by double-membrane vesicles that transport abnormal proteins and organelles through the cytoplasm (i.e., autophagosomes). The autophagosome membrane fuses to lysosomes to breakdown the transported material 2. During embryonic development, autophagy is first induced after fertilization to clear sperm-born material that is not necessary for further embryogenesis 19-21. In turn, autophagy is also associated with abundance of maternal...

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Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

Autophagy is a pro-survival adaptive response to heat shock in bovine cumulus-oocyte complexes

Latorraca

Feitosa

Mariano

et al. 2020

Sci Rep

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“…There are several options of drugs that can be used to stimulate a gradual chromatin transition while maintaining gap junctions open during prematuration culture. The most effective drugs reported in the literature are those that prevent a decrease in the level of intra‐oocyte cyclic adenosine monophosphate (cAMP) levels by stimulating cAMP synthesis, such as forskolin, or by inhibiting the phosphodiesterase, an enzyme that degrades cAMP, such as cilostamide, milrinone or 3‐isobutyl‐1‐methyl‐xanthine (Albuz et al, ; Dall'Acqua, da Leão, Rocha‐Frigoni, Gottardi, & Mingoti, ; Dieci et al, ; Franciosi et al, ; Mehlmann, ; Razza et al, ). More recently, the natriuretic peptide precursor C (NPPC) has also been investigated, as this drug indirectly prevents the decrease in cAMP levels by stimulating cyclic guanosine monophosphate (cGMP) synthesis (Franciosi et al, ).…”

Section: Introductionmentioning

confidence: 99%

Differences in embryonic gene expression and quality indicate the benefit of epidermal growth factor receptor inhibitor during prematuration to improve competence in bovine oocytes

Dall’Acqua

Nunes

Silva

et al. 2019

Reprod Domestic Animals

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ContentsThe epidermal growth factor receptor (EGFR) pathway is directly involved in oocyte meiotic resumption induced by a gonadotropic stimulus. Here, we used an EGFR inhibitor (AG1478) to inhibit spontaneous meiosis resumption in bovine oocytes (EGFR− group) during 8 hr prematuration and assessed the competence of such oo- cytes for embryonic development, apoptosis and gene expression in comparison withControl group which was not prematured. Data are presented as mean ± SEM.Blastocysts rate on day 7 (40.81%, averaged) and hatching rate on day 9 (77.35%, averaged) were unaffected by treatment (p > 0.05). Similarly, treatment did not affect (p > 0.05) the total cell number on day 7 (119.05, averaged) and on day 9 (189.5, averaged). Apoptosis was reduced (p < 0.05) in EGFR− group day 7-embryos compared to Control group (3.7% ± 1.0 vs. 5.2% ± 0.8). Abundance of several transcripts was upregulated (p < 0.05) in EGFR− group, including genes related to embryo development and quality (NANOG and RPLP0), epigenetic regulation (H2AFZ), apoptosis (BID) and stress response (GPX4 and HIF1A). Taken together, the results presented here demonstrated a reduction in the apoptosis index and upregulation of NANOG, H2AFZ and RPLP0 mRNA levels, which are related to embryonic development. Our data suggest that temporary meiosis blockage with EGFR inhibitor during prematuration culture of bovine oocytes may be an interesting strategy to improve embryo quality. K E Y W O R D S apoptosis, embryo development, in vitro maturation | 667 CHEDIEK DALL'ACQUA Et AL.

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“…Meiosis blockade before maturation has been suggested as an alternative because it allows oocytes to have additional culture time without suffering modification such as pre-maturation. Blockade of meiosis can be induced by various strategies including increased cAMP, protein synthesis, or inhibition of phosphorylation (Razza et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…Such inhibitors have been added for 24 h to IVM medium, preserving bovine oocyte viability without compromising embryonic development (Kubelka et al, 2000;Lonergan et al, 2000;Mermillod et al, 2000;Ferreira et al, 2009;Quetglas et al, 2011). However, different usage times of these drugs have not been described in the literature (Maziero et al, 2016;Paschoal et al, 2017;Razza et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Treatment with roscovitine and butyrolactone I prior to in vitro maturation alters blastocyst production

Maziero

Guaitolini

Paschoal

et al. 2019

Zygote

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SummaryThis study evaluated the effects of oocyte meiosis inhibitors roscovitine (ROS) and butyrolactone I (BL-I) on in vitro production of bovine embryos. Bovine oocytes were maintained in pre in vitro maturation (pre-IVM) with 25 µM ROS or 100 µM BL-I for 24 h to delay meiosis and for 24 h in in vitro maturation (IVM). Following this treatment, the nuclear maturation index was evaluated. All embryos degenerated following this procedure. In the second set of experiments, oocytes were maintained for 6 or 12 h in pre-IVM with the following three treatments: ROS (25 µM or 12.5 µM), BL-I (100 µM or 50 µM) or a combination of both drugs (6.25 µM ROS and 12.5 µM BL-I). Oocytes were cultivated for 18 or 12 h in IVM. When a meiosis-inducing agent was used during pre-IVM for 24 h, more degenerated oocytes were observed at the end of the IVM period. This effect decreased when the meiotic blocking period was reduced to 6 or 12 h. No significant differences were observed in the blastocyst production rate of oocytes in pre-IVM for 6 h with ROS, BL-I, or ROS + BL-I compared with that of the control group (P > 0.05). However, inhibition of oocytes for 12 h resulted in decreased embryo production compared with that in the controls (P < 0.05). There was no difference in the post-vitrification embryo re-expansion rate between the study groups, showing that the meiotic inhibition for 6 or 12 h did not alter the embryo cryopreservation process.

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Treatment with cyclic adenosine monophosphate modulators prior to in vitro maturation alters the lipid composition and transcript profile of bovine cumulus–oocyte complexes and blastocysts

Cited by 17 publications

References 75 publications

Autophagy is a pro-survival adaptive response to heat shock in bovine cumulus-oocyte complexes

Autophagy is a pro-survival adaptive response to heat shock in bovine cumulus-oocyte complexes

Differences in embryonic gene expression and quality indicate the benefit of epidermal growth factor receptor inhibitor during prematuration to improve competence in bovine oocytes

Treatment with roscovitine and butyrolactone I prior to in vitro maturation alters blastocyst production

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