Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-19T00:13:12.875Z Has data issue: false hasContentIssue false
  • English
  • Français

Modulation of lipid metabolism through multiple pathways during oocyte maturation and embryo culture in bovine

Published online by Cambridge University Press:  18 August 2021

Clara Slade Oliveira Open the ORCID record for Clara Slade Oliveira [Opens in a new window] ,
Viviane Luzia da Silva Feuchard ,
Sheila Costa de Souza Marques  and
Naiara Zoccal Saraiva Open the ORCID record for Naiara Zoccal Saraiva [Opens in a new window]
Clara Slade Oliveira*
Affiliation:
Animal Reproduction Laboratory, Santa Monica Experimental Station, Embrapa Dairy Cattle, Fazenda Santa Monica Road, Barao de Juparana, Valença, RJ, Brazil
Viviane Luzia da Silva Feuchard
Affiliation:
Animal Reproduction Laboratory, Santa Monica Experimental Station, Embrapa Dairy Cattle, Fazenda Santa Monica Road, Barao de Juparana, Valença, RJ, Brazil
Sheila Costa de Souza Marques
Affiliation:
Animal Reproduction Laboratory, Santa Monica Experimental Station, Embrapa Dairy Cattle, Fazenda Santa Monica Road, Barao de Juparana, Valença, RJ, Brazil
Naiara Zoccal Saraiva
Affiliation:
Animal Reproduction Laboratory, Embrapa Dairy Cattle, 610 Eugenio do Nascimento Ave., Juiz de Fora, MG, Brazil
*
Author for correspondence: Clara Slade Oliveira, Animal Reproduction Laboratory, Santa Monica Experimental Station, Embrapa Dairy Cattle, Fazenda Santa Monica Road, Barao de Juparana, Valença, RJ, 27640–000Brazil. E-mail: clara.oliveira@embrapa.br
Get access Rights & Permissions [Opens in a new window]

Abstract

Lipid accumulation occurs in cultured embryos and is associated with reduced cryotolerance. Here we report the use of a multiple pathway lipid modulator cocktail (l-carnitine, linoleic acid and forskolin) to improve cryosurvival. First, we stained oocytes and embryos with Oil Red to examine the time course of lipid accumulation during in vitro fertilization (IVF) and embryo culture. Then we evaluated the effects of the lipid modulators cocktail on lipid content, developmental rates and survival after vitrification. In our conditions, lipid accumulation was detected (P < 0.05) at the end of in vitro maturation (IVM) and after 4 days of embryo culture (D4-D5). In experiment 1, we used lipid modulator cocktail during IVM. Reduced (P < 0.05) lipid accumulation was detected in oocytes (Control: 49.9 ± 1.6, Lip. Mod. IVM: 45.0 ± 1.8) but no changes were present at blastocyst stage (Control: 62.4 ± 2.6, Lip. Mod. IVM: 66.8 ± 2.7). Treated oocytes presented decreased (P < 0.05) blastocyst rates and lower (P < 0.05) re-expansion after vitrification. In experiment 2, lipid modulators cocktail was used during embryo culture (from D4–D7 or D6–D7). Treatment had an effect on lipid metabolism, as lipid content was increased (P < 0.05) in D7 blastocysts in treated groups (Control: 52.7 ± 3.1a, D4: 65.9 ± 2.6b, D6: 78.1 ± 2.7b). However, no effect was present for cleavage, blastocyst and cryosurvival rates. No difference was detected in mean cell number comparing the three groups (Control: 78.9 ± 9.6, D4: 82.6 ± 16.5, D6: 68.3 ± 7.8), but apoptosis rate was increased (P < 0.05) in vitrified-warmed blastocysts from treated groups (Control: 14.77*, D4: 22.28, D6: 22.22). We concluded that the combined use of lipid modulators was efficient to promote changes in lipid content of oocytes and embryos in bovine, but those changes did not reflect positively on embryo development or cryosurvival.

Keywords

CryopreservationEmbryo cultureIn vitro maturationLipid accumulationVitrification
Type
Research Article
Information
Zygote , Volume 30 , Issue 2 , April 2022 , pp. 258 - 266
Copyright
© The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aardema, H, Vos, PLAM, Lolicato, F, Roelen, BAJ, Knijn, HM, Vaandrager, AB, Helms, JB and Gadella, BM (2011). Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol Reprod 85, 62–9.CrossRefGoogle ScholarPubMed
Abe, H, Yamashita, S, Satoh, T and Hoshi, H (2002). Accumulation of cytoplasmic lipid droplets in bovine embryos and cryotolerance of embryos developed in different culture systems using serum-free or serum-containing media. Mol Reprod Dev 61, 57–66.CrossRefGoogle ScholarPubMed
Absalón-Medina, VA, Bedford-Guaus, SJ, Gilbert, RO, Siqueira, LC, Esposito, G, Schneider, A, Cheong, SH and Butler, WR (2014). The effects of conjugated linoleic acid isomers cis-9,trans-11 and trans-10,cis-12 on in vitro bovine embryo production and cryopreservation. J Dairy Sci 97, 6164–76.CrossRefGoogle ScholarPubMed
Al Darwich, A, Perreau, C, Petit, MH, Papillier, P, Dupont, J, Guillaume, D, Mermillod, P and Guignot, F (2010). Effect of PUFA on embryo cryoresistance, gene expression and AMPKα phosphorylation in IVF-derived bovine embryos. Prostaglandins Other Lipid Mediat 93(1–2), 30–6.CrossRefGoogle ScholarPubMed
Bertevello, PS, Teixeira-Gomes, AP, Seyer, A, Vitorino Carvalho, AV, Labas, V, Blache, MC, Banliat, C, Cordeiro, LAV, Duranthon, V, Papillier, P, Maillard, V, Elis, S and Uzbekova, S (2018). Lipid identification and transcriptional analysis of controlling enzymes in bovine ovarian follicle. Int J Mol Sci 19, 3261.CrossRefGoogle ScholarPubMed
Carro, M, Buschiazzo, J, Ríos, GL, Oresti, GM and Alberio, RH (2013). Linoleic acid stimulates neutral lipid accumulation in lipid droplets of maturing bovine oocytes. Theriogenology 79, 687–94.CrossRefGoogle ScholarPubMed
Carro, T, Taneyhill, LA and Ann Ottinger, M (2013). The effects of an environmentally relevant 58-congener polychlorinated biphenyl (PCB) mixture on cardiac development in the chick embryo. Environ Toxicol Chem 32, 1317–24.Google ScholarPubMed
Chankitisakul, V, Somfai, T, Inaba, Y, Techakumphu, M and Nagai, T (2013). Supplementation of maturation medium with L-carnitine improves cryo-tolerance of bovine in vitro matured oocytes. Theriogenology 79, 590–8.CrossRefGoogle ScholarPubMed
de Lima, MR, Saraiva, NZ, Oliveira, CS and Garcia, JM (2017). The use of linoleic acid in in vitro culture of bovine embryos and its effects on production and survival to vitrification. Anim Reprod 14, 894.Google Scholar
Del Collado, M, Saraiva, NZ, Lopes, FL, Gaspar, RC, Padilha, LC, Costa, RR, Rossi, GF, Vantini, R and Garcia, JM (2015). Influence of bovine serum albumin and fetal bovine serum supplementation during in vitro maturation on lipid and mitochondrial behaviour in oocytes and lipid accumulation in bovine embryos. Reprod Fertil Dev doi: 10.1071/RD15067.CrossRefGoogle Scholar
del Collado, M, Da Silveira, JC, Oliveira, MLF, Alves, BMSM, Simas, RC, Godoy, AT, Coelho, MB, Marques, LA, Carriero, MM, Nogueira, MFG, Eberlin, MN, Silva, LA, Meirelles, FV and Perecin, F (2017). In vitro maturation impacts cumulus–oocyte complex metabolism and stress in cattle. Reproduction 154, 881–93.CrossRefGoogle ScholarPubMed
Dunning, KR, Anastasi, MR, Zhang, VJ, Russell, DL and Robker, RL (2014). Regulation of fatty acid oxidation in mouse cumulus–oocyte complexes during maturation and modulation by PPAR agonists. PLoS One 9, e87327.CrossRefGoogle ScholarPubMed
Ferguson, EM and Leese, HJ (1999). Triglyceride content of bovine oocytes and early embryos. J Reprod Fertil 116, 373–8.Google ScholarPubMed
Fu, XW, Wu, GQ, Li, JJ, Hou, YP, Zhou, GB, Lun-Suo, L-S, Wang, YP and Zhu, SE (2011). Positive effects of forskolin (stimulator of lipolysis) treatment on cryosurvival of in vitro matured porcine oocytes. Theriogenology 75, 268–75.Google ScholarPubMed
Garcia, JM, de Lima, MR, Saraiva, NZ and Oliveira, CS (2017). Evaluation of L-carnitine supplementation on the production and vitrification of bovine embryos produced in vitro . Anim Reprod 14, 881.Google Scholar
Hizaki, H, Segi, E, Sugimoto, Y, Hirose, M, Saji, T, Ushikubi, F, Matsuoka, T, Noda, Y, Tanaka, T, Yoshida, N, Narumiya, S and Ichikawa, A (1999). Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP. Proc Natl Acad Sci USA 96, 10501–6.Google ScholarPubMed
Hochi, S, Kimura, K and Hanada, A (1999). Effect of linoleic acid-albumin in the culture medium on freezing sensitivity of in vitro-produced bovine morulae. Theriogenology 52, 497–504.CrossRefGoogle ScholarPubMed
Karaşahin, T (2019). The effect of oleic and linoleic acid addition to the culture media on bovine embryonic development following vitrification. Polish J Vet Sci 22, 661–6.Google Scholar
Kim, JY, Kinoshita, M, Ohnishi, M and Fukui, Y (2001). Lipid and fatty acid analysis of fresh and frozen–thawed immature and in vitro matured bovine oocytes. Reproduction 122, 131–8.CrossRefGoogle ScholarPubMed
Men, H, Agca, Y, Riley, LK and Critser, JK (2006). Improved survival of vitrified porcine embryos after partial delipation through chemically stimulated lipolysis and inhibition of apoptosis. Theriogenology 66, 2008–16.CrossRefGoogle ScholarPubMed
Oliveira, CS, Saraiva, NZ, de Lima, MR, Oliveira, LZ, Serapião, RV, Garcia, JM, Borges, CAV and Camargo, LSA (2016). Cell death is involved in sexual dimorphism during preimplantation development. Mech Dev 139, 42–50.Google ScholarPubMed
Paczkowski, M, Schoolcraft, WB and Krisher, RL (2014). Fatty acid metabolism during maturation affects glucose uptake and is essential to oocyte competence. Reproduction 148, 429–39.Google ScholarPubMed
Paschoal, DM, Sudano, MJ, Guastali, MD, Dias Maziero, RR, Crocomo, LF, Oña Magalhães, LC, Da Silva Rascado, T, Martins, A and Da Cruz Landim-Alvarenga, F (2014). Forskolin effect on the cryosurvival of in vitro-produced bovine embryos in the presence or absence of fetal calf serum. Zygote 22, 146–57.CrossRefGoogle ScholarPubMed
Paschoal, DM, Sudano, MJ, Schwarz, KRL, Maziero, RRD, Guastali, MD, Crocomo, LF, Magalhães, LCO, Martins, A, Leal, CLV and Landim-Alvarenga, FDC (2017). Cell apoptosis and lipid content of in vitro–produced, vitrified bovine embryos treated with forskolin. Theriogenology 87, 108–14.CrossRefGoogle ScholarPubMed
Paula-Lopes, FF, Lima, RS, Satrapa, RA and Barros, CM (2013). Physiology and Endocrinology Symposium: Influence of cattle genotype (Bos indicus vs. Bos taurus) on oocyte and preimplantation embryo resistance to increased temperature. J Anim Sci 91, 1143–53.Google ScholarPubMed
Pereira, RM, Baptista, MC, Vasques, MI, Horta, AEM, Portugal, PV, Bessa, RJB, Silva, JCe, Pereira, MS and Marques, CC (2007). Cryosurvival of bovine blastocysts is enhanced by culture with trans-10 cis-12 conjugated linoleic acid (10t,12c CLA). Anim Reprod Sci 98(3–4), 293–301.CrossRefGoogle Scholar
Phongnimitr, T, Liang, Y, Srirattana, K, Panyawai, K, Sripunya, N, Treetampinich, C and Parnpai, R (2013). Effect of L-carnitine on maturation, cryo-tolerance and embryo developmental competence of bovine oocytes. Anim Sci J 84, 719–25.Google ScholarPubMed
Razza, EM, Sudano, MJ, Fontes, PK, Franchi, FF, Belaz, KRA, Santos, PH, Castilho, ACS, Rocha, DFO, Eberlin, MN, Machado, MF and Nogueira, MFG (2018). 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. Reprod Fertil Dev 30, 1314–28.CrossRefGoogle ScholarPubMed
Sanches, BV, Marinho, LSR, Filho, BDO, Pontes, JHF, Basso, AC, Meirinhos, MLG, Silva-Santos, KC, Ferreira, CR and Seneda, MM (2013). Cryosurvival and pregnancy rates after exposure of IVF-derived Bos indicus embryos to forskolin before vitrification. Theriogenology 80, 372–7.CrossRefGoogle ScholarPubMed
Seidel, GE (2006). Modifying oocytes and embryos to improve their cryopreservation. Theriogenology 65, 228–35.CrossRefGoogle ScholarPubMed
Sovernigo, TC, Adona, PR, Monzani, PS, Guemra, S, Barros, FDA, Lopes, FG and Leal, CLV (2017). Effects of supplementation of medium with different antioxidants during in vitro maturation of bovine oocytes on subsequent embryo production. Reprod Domest Anim 52, 561–9.CrossRefGoogle ScholarPubMed
Sudano, MJ, Santos, VG, Tata, A, Ferreira, CR, Paschoal, DM, Machado, R, Buratini, J, Eberlin, MN and Landim-Alvarenga, FDC (2012). Phosphatidylcholine and sphingomyelin profiles vary in Bos taurus indicus and Bos taurus taurus in vitro- and in vivo-produced blastocysts. Biol Reprod 87, 130.CrossRefGoogle ScholarPubMed
Sudano, MJ, Rascado, TDS, Tata, A, Belaz, KRA, Santos, VG, Valente, RS, Mesquita, FS, Ferreira, CR, Araújo, JP, Eberlin, MN and Landim-Alvarenga, FDC (2016). Lipidome signatures in early bovine embryo development. Theriogenology 86, 472–84.e1.CrossRefGoogle ScholarPubMed
Sutton-McDowall, ML, Feil, D, Robker, RL, Thompson, JG and Dunning, KR (2012). Utilization of endogenous fatty acid stores for energy production in bovine preimplantation embryos. Theriogenology 77, 1632–41.Google ScholarPubMed
Takahashi, T, Inaba, Y, Somfai, T, Kaneda, M, Geshi, M, Nagai, T and Manabe, N (2013). Supplementation of culture medium with L-carnitine improves development and cryotolerance of bovine embryos produced in vitro. Reprod Fertil Dev 25, 589–99.CrossRefGoogle ScholarPubMed
Tominaga, K, Shimizu, M, Ooyama, S and Izaike, Y (2000). Effect of lipid polarization by centrifugation at different developmental stages on post-thaw survival of bovine in vitro produced 16-cell embryos. Theriogenology 53, 1669–80.CrossRefGoogle ScholarPubMed
Vajta, G, Holm, P, Kuwayama, M, Booth, PJ, Jacobsen, H, Greve, T and Callesen, H (1998). Open Pulled Straw (OPS) vitrification: A new way to reduce cryoinjuries of bovine ova and embryos. Mol Reprod Dev 51, 53–58.Google ScholarPubMed
Valsangkar, D and Downs, SM (2013). A requirement for fatty acid oxidation in the hormone-induced meiotic maturation of mouse oocytes. Biol Reprod 89, 43.Google ScholarPubMed
Viana, J (2019). Statistics of embryo production and transfer in domestic farm animals. Embryo Technol. Newsletter-IETS, 2018.Google Scholar
Ya, R and Downs, SM (2013). Suppression of chemically induced and spontaneous mouse oocyte activation by AMP-activated protein kinase. Biol Reprod 88, 70.CrossRefGoogle ScholarPubMed
Zolini, AM, Carrascal-Triana, E, Ruiz de King, A, Hansen, PJ, Alves Torres, CA and Block, J (2019). Effect of addition of l-carnitine to media for oocyte maturation and embryo culture on development and cryotolerance of bovine embryos produced in vitro . Theriogenology 133, 135–43.CrossRefGoogle ScholarPubMed