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Published in: Reproductive Biology and Endocrinology 1/2015

Open Access 01-12-2015 | Research

Conjugated linoleic acid improves oocyte cryosurvival through modulation of the cryoprotectants influx rate

Authors: Joana E. Matos, Carla C. Marques, Teresa F. Moura, Maria C. Baptista, Antonio E. M. Horta, Graça Soveral, Rosa M. L. N. Pereira

Published in: Reproductive Biology and Endocrinology | Issue 1/2015

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Abstract

Background

In cryopreservation, oocytes are subjected to extreme hyperosmotic conditions, inducing large volume changes that, along with an abrupt temperature drop, interfere with their developmental competence. Our objectives in this work were to find conditions enabling an increase in oocyte cryosurvival and subsequent development.

Methods

Abattoir-derived bovine oocytes were cultured without (Control group) or with trans-10,cis-12 conjugated linoleic acid isomer (CLA group). Comparative observations were made for 1) the oocyte developmental competence after exposure to cryoprotectants followed or not by vitrification/warming, 2) the oocyte membrane permeability to water (using the non-permeant cryoprotectant sucrose) and 3) the oocyte membrane permeability to two cryoprotectants (ethylene glycol, EG, and dimethyl sulfoxide, DMSO). Mature oocytes cultured with or without CLA and vitrified/warmed or only exposed to cryoprotectants without vitrification were subjected to in vitro fertilization; embryo culture proceeded until the blastocyst stage. The oocyte membrane permeabilities to water and cryoprotectants were estimated using mature oocytes subjected to hyperosmotic challenges. For water permeability, 200 mM sucrose was used, whereas for the cryoprotectant permeability, a 10 % solution of both EG and DMSO was used. The data were analyzed using the MIXED procedure and Student’s T-test.

Results

CLA supplementation improves the developmental competence of vitrified/warmed and cryoprotectants exposed oocytes (p < 0.01) and reduces their membrane permeability to water (37 %, p < 0.001) and to cryoprotectants (42 %, p < 0.001).

Conclusions

: By slowing the fluxes of water and of permeant cryoprotectants, CLA contributed to improved oocyte cryosurvival and post-thawed viability. This isomer supplementation to the maturation media should be considered when designing new protocols for oocyte cryopreservation.
Literature
1.
go back to reference Pereira RM, Marques CC. Animal oocyte and embryo cryopreservation. Cell Tissue Bank. 2008;9:267–77.PubMedCrossRef Pereira RM, Marques CC. Animal oocyte and embryo cryopreservation. Cell Tissue Bank. 2008;9:267–77.PubMedCrossRef
3.
go back to reference Agca Y, Liu J, McGrath JJ, Peter AT, Critser ES, Critser JK. Membrane permeability characteristics of metaphase II mouse oocytes at various temperatures in the presence of Me2SO. Cryobiology. 1998;36:287–300.PubMedCrossRef Agca Y, Liu J, McGrath JJ, Peter AT, Critser ES, Critser JK. Membrane permeability characteristics of metaphase II mouse oocytes at various temperatures in the presence of Me2SO. Cryobiology. 1998;36:287–300.PubMedCrossRef
4.
go back to reference Agca Y, Liu J, Peter AT, Critser ES, Critser JK. Effect of developmental stage on bovine oocyte plasma membrane water and cryoprotectant permeability characteristics. Mol Reprod Dev. 1998;49:408–15.PubMedCrossRef Agca Y, Liu J, Peter AT, Critser ES, Critser JK. Effect of developmental stage on bovine oocyte plasma membrane water and cryoprotectant permeability characteristics. Mol Reprod Dev. 1998;49:408–15.PubMedCrossRef
5.
go back to reference De Santis L, Coticchio G, Paynter S, Albertini D, Hutt K, Cino I, et al. Permeability of human oocytes to ethylene glycol and their survival and spindle configurations after slow cooling cryopreservation. Hum Reprod. 2007;22:2776–83.PubMedCrossRef De Santis L, Coticchio G, Paynter S, Albertini D, Hutt K, Cino I, et al. Permeability of human oocytes to ethylene glycol and their survival and spindle configurations after slow cooling cryopreservation. Hum Reprod. 2007;22:2776–83.PubMedCrossRef
6.
go back to reference Martins AP, Lopes PA, Martins SV, Madeira A, Santos NC, Prates JA, et al. Conjugated linoleic acid reduces permeability and fluidity of adipose plasma membranes from obese Zucker rats. Biochem Biophys Res Commun. 2010;398:199–204.PubMedCrossRef Martins AP, Lopes PA, Martins SV, Madeira A, Santos NC, Prates JA, et al. Conjugated linoleic acid reduces permeability and fluidity of adipose plasma membranes from obese Zucker rats. Biochem Biophys Res Commun. 2010;398:199–204.PubMedCrossRef
8.
go back to reference Veth MJ, Bauman DE, Koch W, Mann GE, Pfeiffer AM, Butler WR. Efficacy of conjugated linoleic acid for improving reproduction: A multi-study analysis in early-lactation dairy cows. J Dairy Sci. 2009;92:2662–9.PubMedCrossRef Veth MJ, Bauman DE, Koch W, Mann GE, Pfeiffer AM, Butler WR. Efficacy of conjugated linoleic acid for improving reproduction: A multi-study analysis in early-lactation dairy cows. J Dairy Sci. 2009;92:2662–9.PubMedCrossRef
9.
go back to reference Pereira RM, Baptista MC, Vasques MI, Horta AEM, Portugal PV, Bessa RJB, et al. Cryosurvival of bovine blastocysts is enhanced by culture with trans-10, cis-12 conjugated linoleic acid. Anim Reprod Sci. 2007;98:293–301.PubMedCrossRef Pereira RM, Baptista MC, Vasques MI, Horta AEM, Portugal PV, Bessa RJB, et al. Cryosurvival of bovine blastocysts is enhanced by culture with trans-10, cis-12 conjugated linoleic acid. Anim Reprod Sci. 2007;98:293–301.PubMedCrossRef
10.
go back to reference Pereira RM, Carvalhais I, Pimenta J, Baptista MC, Vasques MI, Horta AEM, et al. Biopsied and vitrified bovine embryos viability is improved by trans-10, cis-12 conjugated linoleic acid supplementation during in vitro embryo culture. Anim Reprod Sci. 2008;106:322–32.PubMedCrossRef Pereira RM, Carvalhais I, Pimenta J, Baptista MC, Vasques MI, Horta AEM, et al. Biopsied and vitrified bovine embryos viability is improved by trans-10, cis-12 conjugated linoleic acid supplementation during in vitro embryo culture. Anim Reprod Sci. 2008;106:322–32.PubMedCrossRef
11.
go back to reference Lapa M, Marques CC, Alves SP, Vasques MI, Baptista MC, Carvalhais I, et al. Effect of trans-10 cis-12 conjugated linoleic acid on bovine oocyte competence and fatty acid composition. Reprod Dom Anim. 2011;46:904–10.CrossRef Lapa M, Marques CC, Alves SP, Vasques MI, Baptista MC, Carvalhais I, et al. Effect of trans-10 cis-12 conjugated linoleic acid on bovine oocyte competence and fatty acid composition. Reprod Dom Anim. 2011;46:904–10.CrossRef
12.
go back to reference Vajta G, Holm P, Kuwayama M, Booth PJ, Jacobsen H, Greve T, et al. Open Pulled Straw vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Mol Reprod Dev. 1998;51:53–8.PubMedCrossRef Vajta G, Holm P, Kuwayama M, Booth PJ, Jacobsen H, Greve T, et al. Open Pulled Straw vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Mol Reprod Dev. 1998;51:53–8.PubMedCrossRef
13.
go back to reference Stringfellow DA, Seidel SM. Manual of the International Embryo Transfer Society. Savoy II. USA: Inc: International Embryo Transfer Society; 1998. Stringfellow DA, Seidel SM. Manual of the International Embryo Transfer Society. Savoy II. USA: Inc: International Embryo Transfer Society; 1998.
14.
go back to reference Campos E, Moura TF, Oliva A, Leandro P, Soveral G. Lack of Aquaporin 3 in bovine erythrocyte membranes correlates with low glycerol permeation. Biochem Biophys Res Commun. 2011;408:477–81.PubMedCrossRef Campos E, Moura TF, Oliva A, Leandro P, Soveral G. Lack of Aquaporin 3 in bovine erythrocyte membranes correlates with low glycerol permeation. Biochem Biophys Res Commun. 2011;408:477–81.PubMedCrossRef
15.
go back to reference Jin B, Kawai Y, Hara T, Takeda S, Seki S, Nakata Y, et al. Pathway for the movement of water and cryoprotectants in bovine oocytes and embryos. Biol Reprod. 2011;85:834–47.PubMedCrossRef Jin B, Kawai Y, Hara T, Takeda S, Seki S, Nakata Y, et al. Pathway for the movement of water and cryoprotectants in bovine oocytes and embryos. Biol Reprod. 2011;85:834–47.PubMedCrossRef
16.
go back to reference Kuwayama M, Vajta G, Kato O, Leibo SP. Highly efficient vitrification method for cryopreservation of human oocytes. Reprod BioMed Online. 2005;11:300–8.PubMedCrossRef Kuwayama M, Vajta G, Kato O, Leibo SP. Highly efficient vitrification method for cryopreservation of human oocytes. Reprod BioMed Online. 2005;11:300–8.PubMedCrossRef
17.
go back to reference Vieira AD, Forell F, Feltrin C, Rodrigues JL. Calves born after direct transfer of vitrified bovine in vitro-produced blastocysts derived from vitrified immature oocytes. Reprod Dom Anim. 2008;43:314–8.CrossRef Vieira AD, Forell F, Feltrin C, Rodrigues JL. Calves born after direct transfer of vitrified bovine in vitro-produced blastocysts derived from vitrified immature oocytes. Reprod Dom Anim. 2008;43:314–8.CrossRef
18.
go back to reference Dıez C, Munoz M, Caamano JN, Gomez E. Cryopreservation of the bovine oocyte: current status and perspectives. Reprod Dom Anim. 2012;47:76–83.CrossRef Dıez C, Munoz M, Caamano JN, Gomez E. Cryopreservation of the bovine oocyte: current status and perspectives. Reprod Dom Anim. 2012;47:76–83.CrossRef
19.
go back to reference Diez C, Duque P, Gomez E, Hidalgo CO, Tamargo C, Rodrıguez A, et al. Bovine oocyte vitrification before or after meiotic arrest: effects on ultrastructure and developmental ability. Theriogenology. 2005;64:317–33.PubMedCrossRef Diez C, Duque P, Gomez E, Hidalgo CO, Tamargo C, Rodrıguez A, et al. Bovine oocyte vitrification before or after meiotic arrest: effects on ultrastructure and developmental ability. Theriogenology. 2005;64:317–33.PubMedCrossRef
20.
go back to reference Morató R, Izquierdo D, Paramio MT, Mogas T. Cryotops versus open pulled straws as carriers for the cryopreservation of bovine oocytes: effects on spindle and chromosome configuration and embryo development. Cryobiology. 2008;57:137–41.PubMedCrossRef Morató R, Izquierdo D, Paramio MT, Mogas T. Cryotops versus open pulled straws as carriers for the cryopreservation of bovine oocytes: effects on spindle and chromosome configuration and embryo development. Cryobiology. 2008;57:137–41.PubMedCrossRef
21.
go back to reference Prentice JR, Singh J, Dochi O, Anzar M. Factors affecting nuclear maturation, cleavage and embryo development of vitrified bovine cumulus-oocyte complexes. Theriogenology. 2011;75:602–9.PubMedCrossRef Prentice JR, Singh J, Dochi O, Anzar M. Factors affecting nuclear maturation, cleavage and embryo development of vitrified bovine cumulus-oocyte complexes. Theriogenology. 2011;75:602–9.PubMedCrossRef
22.
go back to reference Chankitisakul V, Somfai T, Inaba Y, Techakumphu M, Nagai T. Supplementation of maturation medium with L-carnitine improves cryo-tolerance of bovine in vitro matured oocytes. Theriogenology. 2013;79:590–8.PubMedCrossRef Chankitisakul V, Somfai T, Inaba Y, Techakumphu M, Nagai T. Supplementation of maturation medium with L-carnitine improves cryo-tolerance of bovine in vitro matured oocytes. Theriogenology. 2013;79:590–8.PubMedCrossRef
23.
go back to reference Kasai M, Ito K, Edashige K. Morphological appearance of the cryopreserved mouse blastocyst as a tool to identify the type of cryoinjury. Hum Reprod. 2002;17:1863–74.PubMedCrossRef Kasai M, Ito K, Edashige K. Morphological appearance of the cryopreserved mouse blastocyst as a tool to identify the type of cryoinjury. Hum Reprod. 2002;17:1863–74.PubMedCrossRef
24.
go back to reference Gualtieri R, Iaccarino M, Mollo V, Prisco M, Iaccarino S, Talevi R. Slow cooling of human oocytes: ultrastructural injuries and apoptotic status. Fertil Steril. 2009;91:1023–34.PubMedCrossRef Gualtieri R, Iaccarino M, Mollo V, Prisco M, Iaccarino S, Talevi R. Slow cooling of human oocytes: ultrastructural injuries and apoptotic status. Fertil Steril. 2009;91:1023–34.PubMedCrossRef
25.
go back to reference Marques CC, Galvão A, Baptista MC, Prates EG, Horta AEM, Ferreira-Dias G, et al. Effect of trans-10, cis-12 conjugated linoleic acid on bovine and porcine oocyte prostaglandins and lipid content during maturation. Reprod Dom Anim. 2013;48:106. Marques CC, Galvão A, Baptista MC, Prates EG, Horta AEM, Ferreira-Dias G, et al. Effect of trans-10, cis-12 conjugated linoleic acid on bovine and porcine oocyte prostaglandins and lipid content during maturation. Reprod Dom Anim. 2013;48:106.
26.
go back to reference Prates EG, Alves S, Marques CC, Baptista MC, Horta AEM, Bessa RJB, et al. Fatty acid composition of porcine cumulus oocyte complexes (COC) during maturation: effect of the lipid modulators trans-10, cis-12 conjugated linoleic acid and forskolin. In Vitro Cell Dev Biol Animal. 2013;49:335–45.CrossRef Prates EG, Alves S, Marques CC, Baptista MC, Horta AEM, Bessa RJB, et al. Fatty acid composition of porcine cumulus oocyte complexes (COC) during maturation: effect of the lipid modulators trans-10, cis-12 conjugated linoleic acid and forskolin. In Vitro Cell Dev Biol Animal. 2013;49:335–45.CrossRef
27.
go back to reference Tavares Batista R, Raposo N, Campos P, Pereira M, Camargo L, Carvalho B, et al. Trans-10, cis-12 conjugated linoleic acid reduces neutral lipid content and may affect cryotolerance of in vitro-produced crossbred bovine embryos. J Anim Sci Biotechnol. 2014;5:33.CrossRef Tavares Batista R, Raposo N, Campos P, Pereira M, Camargo L, Carvalho B, et al. Trans-10, cis-12 conjugated linoleic acid reduces neutral lipid content and may affect cryotolerance of in vitro-produced crossbred bovine embryos. J Anim Sci Biotechnol. 2014;5:33.CrossRef
28.
go back to reference Romão R, Marques CC, Baptista MC, Barbas JP, Horta AEM, Bettencourt E, Carolino N, Pereira RMLN.. Cryopreservation of in vitro produced sheep embryos: effect of different protocols of lipid reduction. Theriogenology 2015, in press,1-9. Romão R, Marques CC, Baptista MC, Barbas JP, Horta AEM, Bettencourt E, Carolino N, Pereira RMLN.. Cryopreservation of in vitro produced sheep embryos: effect of different protocols of lipid reduction. Theriogenology 2015, in press,1-9.
29.
go back to reference Hochi S, Kimura K, Hanada A. Effect of linoleic acid-albumin in the culture medium on freezing sensivity of in vitro-produced bovine morulae. Theriogenology. 1999;52:497–504.PubMedCrossRef Hochi S, Kimura K, Hanada A. Effect of linoleic acid-albumin in the culture medium on freezing sensivity of in vitro-produced bovine morulae. Theriogenology. 1999;52:497–504.PubMedCrossRef
30.
go back to reference Karlssona JOM, Szurekb EA, Higginsc AZ, Leeb SR, Eroglu A. Optimization of cryoprotectant loading into murine and human oocytes. Cryobiology. 2014;68:18–28.CrossRef Karlssona JOM, Szurekb EA, Higginsc AZ, Leeb SR, Eroglu A. Optimization of cryoprotectant loading into murine and human oocytes. Cryobiology. 2014;68:18–28.CrossRef
Metadata
Title
Conjugated linoleic acid improves oocyte cryosurvival through modulation of the cryoprotectants influx rate
Authors
Joana E. Matos
Carla C. Marques
Teresa F. Moura
Maria C. Baptista
Antonio E. M. Horta
Graça Soveral
Rosa M. L. N. Pereira
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2015
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-015-0059-3

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