Elevated non-esteri fied fatty acid concentrations during in vitro murine follicle growth alter follicular physiology and reduce oocyte developmental competence

Fertility and Sterility

Volumn 102, Issue 6, 2014, Pages 1769-1776.e1

  Valckx, Sara D M ^a   Van Hoeck, Veerle ^a   Arias Alvarez, Maria ^a   Maillo, Veronica ^b   Lopez Cardona, Angela P ^b,c   Gutierrez Adan, Alfonso ^b   Berth, Mario ^d   Cortvrindt, Rita ^e   Bols, Peter E J ^a   Leroy, Jo L M R ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b INIA   (Spain)

^c UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^d Algemeen Medisch Laboratorium   (Belgium)

^e EggCentris Besloten Vennootschap Met Beperkte Aansprakelijkheid   (Belgium)

Author keywords

Folliculogenesis; Metabolic disorder; NEFA; Obesity; Oocyte developmental competence

Indexed keywords

ESTRADIOL; INHIBIN B; MESSENGER RNA; OLEIC ACID; PALMITIC ACID; PROGESTERONE; STEARIC ACID; FATTY ACID; INHIBIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLASTOCYST; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENERGY METABOLISM; EXPERIMENTAL STUDY; FATTY ACID BLOOD LEVEL; FATTY ACID METABOLISM; FEMALE; GENE EXPRESSION; GRANULOSA CELL; HORMONE RELEASE; IN VITRO STUDY; LIPOLYSIS; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OOCYTE DEVELOPMENT; OVARY FOLLICLE DEVELOPMENT; OXIDATIVE STRESS; PRIORITY JOURNAL; PROGESTERONE SYNTHESIS; STEROID METABOLISM; STEROIDOGENESIS; ZYGOTE; ANIMAL; BIOSYNTHESIS; CELL CULTURE; DRUG EFFECTS; METABOLISM; OOCYTE; OVARY FOLLICLE; OVULATION; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; FATTY ACIDS, NONESTERIFIED; FEMALE; INHIBINS; MALE; MICE; OOCYTES; OVARIAN FOLLICLE; OVULATION; PROGESTERONE;

EID: 84921989262     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2014.08.018     Document Type: Article

References (36)

1. Boden G, Shulman GI. Free fatty acids in obesity and type 2 diabetes: defining their role in the development of insulin resistance and beta-cell dysfunction. Eur J Clin Invest 2002;32:14-23.
2. Mooradian AD, Haas MJ, Wehmeier KR, Wong NCW. Obesity-related changes in high-density lipoprotein metabolism. Obesity 2008;16:1152-60.
3. Cnop M, Hannaert JC, Hoorens A, Eizirik DL, Pipeleers DG. Inverse relationship between cytotoxicity of free fatty acids in pancreatic islet cells and cellular triglyceride accumulation. Diabetes 2001;50:1771-7.
4. Lu ZH, Mu YM, Wang BA, Li XL, Lu JM, Li JY, et al. Saturated free fatty acids, palmitic acid and stearic acid, induce apoptosis by stimulation of ceramide generation in rat testicular Leydig cell. Biochem Biophys Res Commun 2003;303:1002-7.
5. Zhang LY, Keung W, Samokhvalov V, Wang W, Lopaschuk GD. Role of fatty acid uptake and fatty acid beta-oxidation in mediating insulin resistance in heart and skeletal muscle. Biochim Biophys Acta 2010;1801:1-22.
6. Leroy JLMR, Vanholder T, Delanghe JR, Opsomer G, Van Soom A, Bols PEJ, et al. Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early post partum. Theriogenology 2004;62:1131-43.
7. Valckx SD, De Pauw I, De Neubourg D, Inion I, Berth M, Fransen E, et al. BMIrelated metabolic composition of the follicular fluid of women undergoing assisted reproductive treatment and the consequences for oocyte and embryo quality. Hum Reprod 2012;27:3531-9.
8. Valckx SD, Arias-Alvarez M, De Pauw I, Fievez V, Vlaeminck B, Fransen E, et al. Fatty acid composition of the follicular fluid of normal weight, overweight and obese women undergoing assisted reproductive treatment: a descriptive cross-sectional study. Reprod Biol Endocrinol 2014;12:13.
9. Vanholder T, Leroy JL, Soom AV, Opsomer G, Maes D, Coryn M, et al. Effect of non-esteri fied fatty acids on bovine granulosa cell steroidogenesis and proliferation in vitro. Anim Reprod Sci 2005;87:33-44.
10. Vanholder T, Leroy JL, Van Soom A, Maes D, Coryn A, Fiers T, et al. Effect of non-esteri fied fatty acids on bovine theca cell steroidogenesis and proliferation in vitro. Anim Reprod Sci 2006;92:51-63.
11. Mu YM, Yanase T, Nishi Y, Tanaka A, Saito M, Jin CH, et al. Saturated FFAs, palmitic acid and stearic acid, induce apoptosis in human granulosa cells. Endocrinology 2001;142:3590-7.
12. Jungheim ES, Macones GA, Odem RR, Patterson BW, Lanzendorf SE, Ratts VS, et al. Associations between free fatty acids, cumulus oocyte complex morphology and ovarian function during in vitro fertilization. Fertil Steril 2011;95:1970-4.
13. Van Hoeck V, Sturmey RG, Bermejo-Alvarez P, Rizos D, Gutierrez-Adan A, Leese HJ, et al. Elevated non-esteri fied fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS One 2011;6:e23183.
14. Leroy JLMR, Vanholder T, Mateusen B, Christophe A, Opsomer G, de Kruif A, et al. Non-esterified fatty acids in follicular fl uid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 2005;130:485-95.
15. Aardema H, Vos PLAM, Lolicato F, Roelen BAJ, Knijn HM, Vaandrager AB, et al. Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol Reprod 2011;85:62-9.
16. Jorritsma R, Cesar ML, Hermans JT, Kruitwagen CLJJ, Vos PLAM, Kruip TAM. Effects of non-esterified fatty acids on bovine granulosa cells and developmental potential of oocytes in vitro. Anim Reprod Sci 2004;81:225-35.
17. Smitz JEJ, Cortvrindt RG. The earliest stages of folliculogenesis in vitro. Reproduction 2002;123:185-202.
18. Cortvrindt R, Smitz J, Van Steirteghem AC. In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simpli fied culture system. Hum Reprod 1996;11:2656-66.
19. Adriaens I, Cortvrindt R, Smitz J. Differential fsh exposure in preantral follicle culture has marked effects on folliculogenesis and oocyte developmental competence. Hum Reprod 2004;19:398-408.
20. Van Hoeck V, Rizos D, Gutierrez-Adan A, Pintelon I, Jorssen E, Dufort I, et al. Interaction between differential gene expression profile and phenotype in bovine blastocysts originating from oocytes exposed to elevated non-esterified fatty acid concentrations. Reprod Fertil Dev 2013;23 Epub ahead of print.
21. Van Hoeck V, Leroy JL, Arias Alvarez M, Rizos D, Gutierrez-Adan A, Schnorbusch K, et al. Oocyte developmental failure in response to elevated nonesteri fied fatty acid concentrations: mechanistic insights. Reproduction 2013;145:33-44.
22. Eitel K, Staiger H, Brendel MD, Brandhorst D, Bretzel RG, Haring HU, et al. Different role of saturated and unsaturated fatty acids in beta-cell apoptosis. Biochem Biophys Res Commun 2002;299:853-6.
23. Van Cruchten S, Van den Broeck W. Morphological and biochemical aspects of apoptosis, oncosis and necrosis. Anat Histol Embryol 2002;31:214-23.
24. Mihm M, Baker PJ, Fleming LM, Monteiro AM, O'Shaughnessy PJ. Differentiation of the bovinedominant follicle fromthe cohort upregulatesmrna expression for new tissue development genes. Reproduction 2008;135:253-65.
25. Fair T, Lonergan P. The role of progesterone in oocyte acquisition of developmental competence. Reprod Domest Anim 2012;47:142-7.
26. Lenie S, Smitz J. Steroidogenesis-disrupting compounds can be effectively studied for major fertility-related endpoints using in vitro cultured mouse follicles. Toxicol Lett 2009;185:143-52.
27. Smitz J, Cortvrindt R. Inhibin a and b secretion in mouse preantral follicle culture. Hum Reprod 1998;13:927-35.
28. Amsterdam A, Dantes A, Selvaraj N, Aharoni D. Apoptosis in steroidogenic cells: structure-function analysis. Steroids 1997;62:207-11.
29. Kerental I, Suh BS, Dantes A, Lindner S, Oren M, Amsterdam A. Involvement of p53 expression in camp-mediated apoptosis in immortalized granulosacells. Exp Cell Res 1995;218:283-95.
30. Elnashar AM. Progesterone rise on the day of hcg administration (premature luteinization) in ivf: an overdue update. J Assist Reprod Genet 2010;27:149-55.
31. Pasquali R, Patton L, Gambineri A. Obesity and infertility. Curr Opin Endocrinol Diabetes Obes 2007;14:482-7.
32. Van Soom A, Mateusen B, Leroy J, De Kruif A. Assessment of mammalian embryo quality: What can we learn from embryo morphology? Reprod Biomed Online 2003;7:664-70.
33. Holm P, Booth PJ, Callesen H. Kinetics of early in vitro development of bovine in vivo- and in vitro-derived zygotes produced and/or cultured in chemically defined or serum-containing media. Reproduction 2002;123:553-65.
34. Seshagiri PB, Sen Roy S, Sireesha G, Rao RP. Cellular and molecular regulation of mammalian blastocyst hatching. J Reprod Immunol 2009;83:79-84.
35. Thomas M, Jain S, Kumar GP, Laloraya M. A programmed oxyradical burst causes hatching of mouse blastocysts. J Cell Sci 1997;110:1597-602.
36. Cortvrindt RG, Smitz JEJ. Follicle culture in reproductive toxicology: a tool for in-vitro testing of ovarian function? Hum Reprod Update 2002;8:243-54.