Bovine cumulus cells protect maturing oocytes from increased fatty acid levels by massive intracellular lipid storage

Biology of Reproduction

Volumn 88, Issue 6, 2013, Pages

  Aardema, Hilde ^a   Lolicato, Francesca ^b   van de Lest, Chris H A ^b   Brouwers, Jos F ^b   Vaandrager, Arie B ^b   van Tol, Helena T A ^a   Roelen, Bernard A J ^a   Vos, Peter L A M ^a   Helms, J Bernd ^b   Gadella, Bart M ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Cows; Embryo culture; In vitro fertilization; In vitro maturation; IVF; IVM; Oocyte follicle interactions; Ruminants

Indexed keywords

FATTY ACID; OLEIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLASTOCYST; CELL INTERACTION; CELL PROTECTION; CONTROLLED STUDY; COW; CUMULUS CELL; FERTILIZATION IN VITRO; LIPID STORAGE; NONHUMAN; OOCYTE MATURATION; OVARY FOLLICLE CELL; PRIORITY JOURNAL;

COWS; EMBRYO CULTURE; IN VITRO FERTILIZATION; IN VITRO MATURATION; IVF; IVM; OOCYTE-FOLLICLE INTERACTIONS; RUMINANTS;

ANIMALS; BLASTOCYST; CATTLE; CELLS, CULTURED; CUMULUS CELLS; EMBRYO CULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; FATTY ACIDS; FEMALE; FERTILIZATION IN VITRO; FOLLICULAR FLUID; LIPID METABOLISM; OOCYTES; OOGENESIS;

EID: 84882286703     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.106062     Document Type: Article

References (56)

1. Metwally M, Cutting R, Tipton A, Skull J, Ledger WL, Li TC. Effect of increased body mass index on oocyte and embryo quality in IVF patients. Reprod Biomed Online 2007; 15:532-538.
2. Robker RL, Wu LL, Yang X. Inflammatory pathways linking obesity and ovarian dysfunction. J Reprod Immunol 2011; 88:142-148.
3. Jungheim ES, Macones GA, Odem RR, Patterson BW, Lanzendorf SE, Ratts VS, Moley KH. Associations between free fatty acids, cumulus oocyte complex morphology and ovarian function during in vitro fertilization. Fertil Steril 2011; 95:1970-1974.
4. Yang X, Wu LL, Chura LR, Liang X, Lane M, Norman RJ, Robker RL. Exposure to lipid-rich follicular fluid is associated with endoplasmic reticulum stress and impaired oocyte maturation in cumulus-oocyte complexes. Fertil Steril 2012; 97:1438-1443.
5. Walther TC. Farese RV Jr. Lipid droplets and cellular lipid metabolism. Annu Rev Biochem 2012; 81:687-714.
6. Cusi K. Role of obesity and lipotoxicity in the development of nonalcoholic steatohepatitis: pathophysiology and clinical implications. Gastroenterology 2012; 142:711-725. e6.
7. Leroy JL, Vanholder T, Mateusen B, Christophe A, Opsomer G, de Kruif A, Genicot G, Van Soom A. Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 2005; 130:485-495.
8. 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; 50:1771-1777.
9. Listenberger LL, Han X, Lewis SE, Cases S, Farese RVJr, Ory DS, Schaffer JE. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci U S A 2003; 100:3077-3082.
10. Mishra R, Simonson MS. Saturated free fatty acids and apoptosis in microvascular mesangial cells: palmitate activates pro-apoptotic signaling involving caspase 9 and mitochondrial release of endonuclease G. Cardiovasc Diabetol 2005; 4:2.
11. Coll T, Eyre E, Rodriguez-Calvo R, Palomer X, Sanchez RM, Merlos M, Laguna JC, Vazquez-Carrera M. Oleate reverses palmitate-induced insulin resistance and inflammation in skeletal muscle cells. J Biol Chem 2008; 283:11107-11116.
12. Henique C, Mansouri A, Fumey G, Lenoir V, Girard J, Bouillaud F, Prip- Buus C, Cohen I. Increased mitochondrial fatty acid oxidation is sufficient to protect skeletal muscle cells from palmitate-induced apoptosis. J Biol Chem 2010; 285:36818-36827.
13. Maedler K, Spinas GA, Dyntar D, Moritz W, Kaiser N, Donath MY. Distinct effects of saturated and monounsaturated fatty acids on beta-cell turnover and function. Diabetes 2001; 50:69-76.
14. Listenberger LL, Ory DS, Schaffer JE. Palmitate-induced apoptosis can occur through a ceramide-independent pathway. J Biol Chem 2001; 276: 14890-14895.
15. Aardema H, Vos PL, Lolicato F, Roelen BA, Knijn HM, Vaandrager AB, Helms JB, Gadella BM. Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol Reprod 2011; 85:62-69.
16. Wu LL, Dunning KR, Yang X, Russell DL, Lane M, Norman RJ, Robker RL. High-fat diet causes lipotoxicity responses in cumulus-oocyte complexes and decreased fertilization rates. Endocrinology 2010; 151: 5438-5445.
17. Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update 2008; 14:159-177.
18. Albertini DF, Combelles CM, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 2001; 121:647-653.
19. Mu YM, Yanase T, Nishi Y, Tanaka A, Saito M, Jin CH, Mukasa C, Okabe T, Nomura M, Goto K, Nawata H. Saturated FFAs, palmitic acid and stearic acid, induce apoptosis in human granulosa cells. Endocrinology 2001; 142:3590-3597.
20. Ferguson EM, Leese HJ. A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development. Mol Reprod Dev 2006; 73:1195-1201.
21. Sturmey RG, O'Toole PJ, Leese HJ. Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte. Reproduction 2006; 132:829-837.
22. Dunning KR, Cashman K, Russell DL, Thompson JG, Norman RJ, Robker RL. Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol Reprod 2010;
23. Jorritsma R, de Groot MW, Vos PL, Kruip TA, Wensing T, Noordhuizen JP. Acute fasting in heifers as a model for assessing the relationship between plasma and follicular fluid NEFA concentrations. Theriogenology 2003; 60:151-161.
24. Britt JH. Impacts of early postpartum metabolism on follicular development and fertility. The Bovine Proceedings 1992; 24:39-43.
25. Walters AH, Bailey TL, Pearson RE, Gwazdauskas FC. Parity-related changes in bovine follicle and oocyte populations, oocyte quality, and hormones to 90 days postpartum. J Dairy Sci 2002; 85:824-832.
26. van Knegsel AT, van den Brand H, Dijkstra J, Tamminga S, Kemp B. Effect of dietary energy source on energy balance, production, metabolic disorders and reproduction in lactating dairy cattle. Reprod Nutr Dev 2005; 45:665-688.
27. Butler WR. Energy balance relationships with follicular development, ovulation and fertility in postpartum dairy cows. Livestock Production Science 2003; 83:211-218.
28. Thompson JG, Partridge RJ, Houghton FD, Cox CI, Leese HJ. Oxygen uptake and carbohydrate metabolism by in vitro derived bovine embryos. J Reprod Fertil 1996; 106:299-306.
29. Schroder UJ, Staufenbiel R. Invited review: methods to determine body fat reserves in the dairy cow with special regard to ultrasonographic measurement of backfat thickness. J Dairy Sci 2006; 89:1-14.
30. Pieterse MC, Vos PL, Kruip TA, Wurth YA, van Beneden TH, Willemse AH, Taverne MA. Transvaginal ultrasound guided follicular aspiration of bovine oocytes. Theriogenology 1991; 35:857-862.
31. Bungartz L, Niemann H. Assessment of the presence of a dominant follicle and selection of dairy cows suitable for superovulation by a single ultrasound examination. J Reprod Fertil 1994; 101:583-591.
32. Knijn H, Fokker W, van der Weijden G, Dieleman S, Vos P. Effects of superovulation with oFSH and norgestomet/GnRH-controlled release of the LH surge on hormone concentrations, and yield of oocytes and embryos at specific developmental stages. Reprod Domest Anim 2012; 47: 177-183.
33. Vos PL, Bevers MM, Willemse AH, Dieleman SJ. Effects of suppression by a progesterone-releasing intravaginal device and subsequent induction by GnRH of the preovulatory LH surge on follicular function in PMSG/ PG-treated heifers. J Reprod Fertil 1994; 101:43-49.
34. Dieleman SJ, Bevers MM. Effects of monoclonal antibody against PMSG administered shortly after the preovulatory LH surge on time and number of ovulations in PMSG/PG-treated cows. J Reprod Fertil 1987; 81: 533-542.
35. Dieleman SJ, Bevers MM, Poortman J, van Tol HT. Steroid and pituitary hormone concentrations in the fluid of preovulatory bovine follicles relative to the peak of LH in the peripheral blood. J Reprod Fertil 1983; 69:641-649.
36. van Tol HT, van Eerdenburg FJ, Colenbrander B, Roelen BA. Enhancement of Bovine oocyte maturation by leptin is accompanied by an upregulation in mRNA expression of leptin receptor isoforms in cumulus cells. Mol Reprod Dev 2008; 75:578-587.
37. Goovaerts IG, Leroy JL, Jorssen EP, Bols PE. Noninvasive bovine oocyte quality assessment: possibilities of a single oocyte culture. Theriogenology 2010; 74:1509-1520.
38. Balboula AZ, Yamanaka K, Sakatani M, Hegab AO, Zaabel SM, Takahashi M. Intracellular cathepsin B activity is inversely correlated with the quality and developmental competence of bovine preimplantation embryos. Mol Reprod Dev 2010; 77:1031-1039.
39. Van Hoeck V, Sturmey RG, Bermejo-Alvarez P, Rizos D, Gutierrez-Adan A, Leese HJ, Bols PE, Leroy JL. Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS One 2011; 6:e23183.
40. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959; 37:911-917.
41. Rouser G, Fleischer S, Yamamoto A. Two dimensional thin layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 1970; 5:494-496.
42. Manini P, Andreoli R, Careri M, Elviri L, Musci M. Atmospheric pressure chemical ionization liquid chromatography/mass spectrometry in cholesterol oxide determination and characterization. Rapid Commun Mass Spectrom 1998; 12:883-889.
43. Brouwers JF, Gadella BM, van Golde LM, Tielens AG. Quantitative analysis of phosphatidylcholine molecular species using HPLC and light scattering detection. J Lipid Res 1998; 39:344-353.
44. Aitzemüller K. Recent progress in the high performance liquid chromatography of lipids. Prog Lipid Res 1982; 21:171-193.
45. Kates M. Techniques of lipidology: isolation, analysis and identification of lipids In: Burdon RH, and Van Knippenberg PH (eds.), Laboratory Techniques in Biochemistry and Molecular Biology, 2nd ed. Amsterdam: Elsevier; 1986; 125.
46. Smith CA, Want EJ, O'Maille G, Abagyan R, Siuzdak G. XCMS: Processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem 2006; 78: 779-787.
47. Pinheiro J, Bates D, DebRoy S, Sarkar D, the R Development Core Team. Linear and Nonlinear Mixed Effects Models. R Package Version 3.1101. 2011.
48. Jorritsma R, Wensing T, Kruip TA, Vos PL, Noordhuizen JP. Metabolic changes in early lactation and impaired reproductive performance in dairy cows. Vet Res 2003; 34:11-26.
49. Rukkwamsuk T, Geelen MJ, Kruip TA, Wensing T. Interrelation of fatty acid composition in adipose tissue, serum, and liver of dairy cows during the development of fatty liver postpartum. J Dairy Sci 2000; 83:52-59.
50. Moreau C, Froment P, Tosca L, Moreau V, Dupont J. Expression and regulation of the SCD2 desaturase in the rat ovary. Biol Reprod 2006; 74: 75-87.
51. Fragouli E, Wells D. Transcriptomic analysis of follicular cells provides information on the chromosomal status and competence of unfertilized oocytes. Expert Rev Mol Diagn 2012; 12:1-4.
52. Fatehi AN, Roelen BA, Colenbrander B, Schoevers EJ, Gadella BM, Bevers MM, van den Hurk R. Presence of cumulus cells during in vitro fertilization protects the bovine oocyte against oxidative stress and improves first cleavage but does not affect further development. Zygote 2005; 13:177-185.
53. Tatemoto H, Sakurai N, Muto N. Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during In vitro maturation: role of cumulus cells. Biol Reprod 2000; 63:805-810.
54. Merton JS, de Roos AP, Koenen EP, Roelen BA, Vos PL, Mullaart E, Knijn HM. Bovine OPU-derived oocytes can be matured in vitro for 16- 28 h with similar developmental capacity. Reprod Domest Anim 2012; 47: 1037-1042.
55. Wu LL, Russell DL, Norman RJ, Robker RL. Endoplasmic reticulum (ER) stress in cumulus-oocyte complexes impairs pentraxin-3 secretion, mitochondrial membrane potential (DWm), and embryo development. Mol Endocrinol 2012; 26:562-573.
56. Jungheim ES, Schoeller EL, Marquard KL, Louden ED, Schaffer JE, Moley KH. Diet-induced obesity model: abnormal oocytes and persistent growth abnormalities in the offspring. Endocrinology 2010; 151: 4039-4046.