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

Open Access 01-12-2015 | Research

The effect of lysophosphatidic acid during in vitro maturation of bovine cumulus–oocyte complexes: cumulus expansion, glucose metabolism and expression of genes involved in the ovulatory cascade, oocyte and blastocyst competence

Authors: Dorota Boruszewska, Emilia Sinderewicz, Ilona Kowalczyk-Zieba, Katarzyna Grycmacher, Izabela Woclawek-Potocka

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

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Abstract

Background

In the cow, lysophosphatidic acid (LPA) acts as an auto-/paracrine factor, through its receptors LPAR1-4, on oocytes and cumulus cells during in vitro maturation (IVM). The aim of the present work was to determine the effect of LPA during IVM of bovine oocytes on: 1) oocyte maturation; 2) apoptosis of COCs; 3) expression of genes involved in developmental competence and apoptosis in bovine oocytes and subsequent blastocysts; 4) cumulus expansion and expression of genes involved in the ovulatory cascade in cumulus cells; 5) glucose metabolism and expression of genes involved in glucose utilization in cumulus cells; 6) cleavage and blastocyst rates on Day 2 and Day 7 of in vitro culture, respectively.

Methods

Cumulus-oocyte complexes (COCs) were matured in vitro in the presence or absence of LPA (10−5M) for 24h. Following maturation, we determined: oocyte maturation stage, cumulus expansion, COCs apoptosis and glucose and lactate levels in the maturation medium. Moreover, COCs were either used for gene expression analysis or fertilized in vitro. The embryos were cultured until Day 7 to assess cleavage and blastocyst rates. Oocytes, cumulus cells and blastocysts were used for gene expression analysis.

Results

Supplementation of the maturation medium with LPA enhanced oocyte maturation rates and stimulated the expression of developmental competence-related factors (OCT4, SOX2, IGF2R) in oocytes and subsequent blastocysts. Moreover, LPA reduced the occurrence of apoptosis in COCs and promoted an antiapoptotic balance in the transcription of genes involved in apoptosis (BAX and BCL2) either in oocytes or blastocysts. LPA increased glucose uptake by COCs via augmentation of GLUT1 expression in cumulus cells as well as stimulating lactate production via the enhancement of PFKP expression in cumulus cells. LPA did not affect cumulus expansion as visually assessed, however, it stimulated upstream genes of cumulus expansion cascade, AREG and EREG.

Conclusions

Supplementation of the maturation medium with LPA improves oocyte maturation rates, decreases extent of apoptosis in COCs and sustains the expression of developmental competence related factors during oocyte maturation and subsequently affects gene expression profile at the blastocyst stage. We also demonstrate that LPA directs glucose metabolism toward the glycolytic pathway during IVM.
Literature
1.
Van de Leemput EE, Vos PL, Zeinstra EC, Bevers MM, Van der Weijden GC, Dieleman SJ. Improved in vitro embryo development using in vivo matured oocytes from heifers superovulated with a controlled preovulatory LH surge. Theriogenology. 1999;52:335–49.CrossRefPubMed
2.
Sirard MA, Richard F, Blondin P, Robert C. Contribution of the oocyte to embryo quality. Theriogenology. 2006;65:126–36.CrossRefPubMed
3.
Rizos D, Ward F, Duffy P, Boland MP, Lonergan P. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev. 2002;61:234–48.CrossRefPubMed
4.
Ulloa SM, Heinzmann J, Herrmann D, Timmermann B, Baulain U, Großfeld R, et al. Effects of different oocyte retrieval and in vitro maturation systems on bovine embryo development and quality. Zygote. 2014;15:1–11.
5.
Jarvis AA, Cain C, Dennis EA. Purification and characterization of a lysophospholipase from human amnionic membranes. J Biol Chem. 1984;259:15188–95.PubMed
6.
Tokumura A, Miyake M, Nishioka Y, Yamano S, Aono T, Fukuzawa K. Production of lysophosphatidic acids by lysophospholipase D in human follicular fluids of in vitro fertilization patients. Biol Reprod. 1999;61:195–9.CrossRefPubMed
7.
Hinokio K, Yamano S, Nakagawa K, Iraharaa M, Kamada M, Tokumura A, et al. Lysophosphatidic acid stimulates nuclear and cytoplasmic maturation of golden hamster immature oocytes in vitro via cumulus cells. Life Sci. 2002;70:759–67.CrossRefPubMed
8.
Komatsu J, Yamano S, Kuwahara A, Tokumura A, Irahara M. The signaling pathways linking to lysophosphatidic acid-promoted meiotic maturation in mice. Life Sci. 2006;79:506–11.CrossRefPubMed
9.
Liszewska E, Reinaud P, Billon-Denis E, Dubois O, Robin P, Charpigny G. Lysophosphatidic acid signaling during embryo development in sheep: involvement in prostaglandin synthesis. Endocrinology. 2009;150:422–34.CrossRefPubMed
10.
Woclawek-Potocka I, Kowalczyk-Zieba I, Skarzynski DJ. Lysophosphatidic acid action during early pregnancy in the cow: in vivo and in vitro studies. J Reprod Dev. 2010;56:411–20.CrossRefPubMed
11.
Woclawek-Potocka I, Komiyama J, Saulnier-Blache JS, Brzezicka E, Bah MM, Okuda K, et al. Lysophosphatic acid modulates prostaglandin secretion in the bovine uterus. Reproduction. 2009;137:95–105.CrossRefPubMed
12.
Kowalczyk-Zieba I, Boruszewska D, Saulnier-Blache JS, Lopes Da Costa L, Jankowska K, Skarzynski DJ, et al. Lysophosphatidic acid action in the bovine corpus luteum -an in vitro study. J Reprod Dev. 2012;58:661–71.CrossRefPubMed
13.
Boruszewska D, Sinderewicz E, Kowalczyk-Zieba I, Skarzynski DJ, Woclawek-Potocka I. Influence of lysophosphatidic acid on estradiol production and follicle stimulating hormone action in bovine granulosa cells. Reprod Biol. 2013;13:344–7.CrossRefPubMed
14.
Boruszewska D, Torres AC, Kowalczyk-Zieba I, Diniz P, Batista M, Lopes-da-Costa L, et al. The effect of lysophosphatidic acid during in vitro maturation of bovine oocytes: embryonic development and mRNA abundances of genes involved in apoptosis and oocyte competence. Mediat Inflamm. 2014;2014:670670.CrossRef
15.
Torres AC, Boruszewska D, Batista M, Kowalczyk-Zieba I, Diniz P, Sinderewicz E, et al. Lysophosphatidic acid signaling in late cleavage and blastocyst stage bovine embryos. Mediat Inflamm. 2014;2014:678968.CrossRef
16.
Boiani M, Eckardt S, Schöler HR, McLaughlin KJ. Oct4 distribution and level in mouse clones: consequences for pluripotency. Genes Dev. 2002;16:1209–19.CrossRefPubMedCentralPubMed
17.
Keramari M, Razavi J, Ingman KA, Patsch C, Edenhofer F, Ward CM, et al. Sox2 is essential for formation of trophectoderm in the preimplantation embryo. PLoS One. 2010;5, e13952.CrossRefPubMedCentralPubMed
18.
Matsui M, Takahashi Y, Hishinuma M, Kanagawa H. Stimulation of the development of bovine embryos by insulin and insulin-like growth factor-I (IGF-I) is mediated through the IGF-I receptor. Theriogenology. 1997;48:605–16.CrossRefPubMed
19.
Liu HC, He ZY, Mele CA, Veeck LL, Davis OK, Rosenwaks Z. Expression of IGFs and their receptors is a potential marker for embryo quality. Am J Reprod Immunol. 1997;38:237–45.CrossRefPubMed
20.
Rekik W, Dufort I, Sirard MA. Analysis of the gene expression pattern of bovine blastocysts at three stages of development. Mol Reprod Dev. 2011;78:226–40.CrossRefPubMed
21.
Yang MY, Rajamahendran R. Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro. Anim Reprod Sci. 2002;70:159–69.CrossRefPubMed
22.
Tanghe S, Van Soom A, Nauwynck H, Coryn M, de Kruif A. Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev. 2002;61:414–24.CrossRefPubMed
23.
Tesfaye D, Ghanem N, Carter F, Fair T, Sirard MA, Hoelker M, et al. Gene expression profile of cumulus cells derived from cumulus–oocyte complexes matured either in vivo or in vitro. Reprod Fertil Dev. 2009;21:451–61.CrossRefPubMed
24.
Assidi M, Dieleman SJ, Sirard MA. Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence. Reproduction. 2010;140:835–52.CrossRefPubMed
25.
Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science. 2004;303:682–4.CrossRefPubMed
26.
Ashkenazi H, Cao X, Motola S, Popliker M, Conti M, Tsafriri A. Epidermal growth factor family members: endogenous mediators of the ovulatory response. Endocrinology. 2005;146:77–84.CrossRefPubMed
27.
Shimada M, Hernandez-Gonzalez I, Gonzalez-Robayna I, Richards JS. Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol. 2006;20:1352–65.CrossRefPubMed
28.
Nautiyal J, Steel JH, Rosell MM, Nikolopoulou E, Lee K, Demayo FJ, et al. The nuclear receptor cofactor receptor-interacting protein 140 is a positive regulator of amphiregulin expression and cumulus cell-oocyte complex expansion in the mouse ovary. Endocrinology. 2010;151:2923–32.CrossRefPubMedCentralPubMed
29.
Salustri A, Yanagishita M, Hascall VC. Synthesis and accumulation of hyaluronic acid and proteoglycans in the mouse cumulus cell-oocyte complex during follicle-stimulating hormone-induced mucification. J Biol Chem. 1989;264:13840–7.PubMed
30.
Chen L, Wert SE, Hendrix EM, Russell PT, Cannon M, Larsen WJ. Hyaluronic acid synthesis and gap junction endocytosis are necessary for normal expansion of the cumulus mass. Mol Reprod Dev. 1990;26:236–47.CrossRefPubMed
31.
Schoenfelder M, Einspanier R. Expression of hyaluronan synthases and corresponding hyaluronan receptors is differentially regulated during oocyte maturation in cattle. Biol Reprod. 2003;69:269–77.CrossRefPubMed
32.
Wang Q, Chi MM, Schedl T, Moley KH. An intercellular pathway for glucose transport into mouse oocytes. Am J Physiol Endocrinol Metab. 2012;302:E1511–8.CrossRefPubMedCentralPubMed
33.
Marshall DL, Bacote V, Traxinger RR. Discovery of a metabolic pathway mediating glucose-induced desenitization of the glucose transport system. J Biol Chem. 1991;266:4706–12.PubMed
34.
Cetica P, Pintos L, Dalvit G, Beconi M. Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction. 2002;124:675–81.CrossRefPubMed
35.
Cetica PD, Pintos LN, Dalvit GC, Beconi MT. Effect of lactate dehydrogenase activity and isoenzyme localization in bovine oocytes and utilization of oxidative substrates on in vitro maturation. Theriogenology. 1999;51:541–50.CrossRefPubMed
36.
Stringfellow DA, Seidel SM. Manual of IETS 3rd edn. Savoy, IL, USA. Int Embryo Transfer Soc. 1998;106–7.
37.
Jensen J, Ørntoft T. Normalization of real-time quantitative RT-PCR data: a model based variance estimation approach to identify genes suited for normalization- applied to bladder- and colon-cancer data-sets. Cancer Res. 2004;64:5245–50.CrossRefPubMed
38.
39.
Kobayashi K, Yamashita S, Hoshi H. Influence of epidermal growth factor and transforming growth factor-a on in vitro maturation of cumulus cell-enclosed bovine oocytes in a defined medium. J Reprod Fertil. 1994;100:439–46.CrossRefPubMed
40.
Jo JW, Jee BC, Suh CS, Kim SH. Addition of lysophosphatidic acid to mouse oocyte maturation media can enhance fertilization and developmental competence. Hum Reprod. 2014;29:234–41.CrossRefPubMed
41.
Zhang JY, Jiang Y, Lin T, Kang JW, Lee JE, Jin DI. Lysophosphatidic acid improves porcine oocyte maturation and embryo development in vitro. Mol Reprod Dev. 2015;82:66–77.CrossRefPubMed
42.
Watson AJ, De Sousa P, Caveney A, Barcrodt LC, Natale D, Urquhart J, et al. Impact of bovine maturation media on oocyte transcript levels, blastocyst development, cell number, and apoptosis. Biol Reprod. 2000;62:355–64.CrossRefPubMed
43.
Sagirkaya H, Misirlioglu M, Kaya A, First NL, Parrish JJ, Memili E. Developmental potential of bovine oocytes cultured in different maturation and culture conditions. Anim Reprod Sci. 2007;101:225–40.CrossRefPubMed
44.
Foygel K, Choi B, Jun S, Leong DE, Lee A, Wong CC, et al. A novel and critical role for Oct4 as a regulator of the maternal-embryonic transition. PLoS One. 2008;3, e4109.CrossRefPubMedCentralPubMed
45.
Khan DR, Dubé D, Gall L, Peynot N, Ruffini S, Laffont L, et al. Expression of pluripotency master regulators during two key developmental transitions: EGA and early lineage specification in the bovine embryo. PLoS One. 2012;7, e34110.CrossRefPubMedCentralPubMed
46.
Gendelman M, Roth Z. In vivo vs. in vitro models for studying the effects of elevated temperature on the GV stage oocyte, subsequent developmental competence and gene expression. Anim Reprod Sci. 2012;134:125–34.CrossRefPubMed
47.
Gendelman M, Aroyo A, Yavin S, Roth Z. Seasonal effects on gene expression, cleavage timing, and developmental competence of bovine preimplantation embryos. Reproduction. 2010;140:73–82.CrossRefPubMed
48.
Goissis MD, Cibelli JB. Functional characterization of SOX2 in bovine preimplantation embryos. Biol Reprod. 2014;90:30.CrossRefPubMed
49.
Wang LM, Feng HL, Ma YZ, Cang M, Li HJ, Yan Z, et al. Expression of IGF receptors and its ligands in bovine oocytes and preimplantation embryos. Anim Reprod Sci. 2009;114:99–108.CrossRefPubMed
50.
Yaseen MA, Wrenzycki C, Herrmann D, Carnwath JW, Niemann H. Changes in the relative abundance of mRNA transcripts for insulin-like growth factor (IGF-I and IGF-II) ligands and their receptors (IGF-IR/IGF-IIR) in preimplantation bovine embryos derived from different in vitro systems. Reproduction. 2001;122:601–10.CrossRefPubMed
51.
Klein C, Bauersachs S, Ulbrich SE, Einspanier R, Meyer HHD, Schmidt SEM, et al. Monozygotic twin model reveals novel embryo-induced transcriptome changes of bovine endometrium in the pre-attachment period. Biol Reprod. 2006;74:253–64.CrossRefPubMed
52.
Mansouri-Attia N, Aubert J, Reinaud P, Giraud-Delville C, Taghouti G, Galio L, et al. Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation. Physiol Genomics. 2009;39:14–27.CrossRefPubMed
53.
El-Sayed A, Hoelker M, Rings F, Salilew D, Jennen D, Tholen E, et al. Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients. Physiol Genomics. 2006;28:84–96.CrossRefPubMed
54.
Ghanem N, Salilew-Wondim D, Gad A, Tesfaye D, Phatsara C, Tholen E, et al. Bovine blastocysts with developmental competence to term share similar expression of developmentally important genes although derived from different culture environments. Reproduction. 2011;142:551–64.CrossRefPubMed
55.
Gjørret JO, Knijn HM, Dieleman SJ, Avery B, Larsson LI, Maddox-Hyttel P. Chronology of apoptosis in bovine embryos produced in vivo and in vitro. Biol Reprod. 2003;69:1193–200.CrossRefPubMed
56.
Bilodeau-Goeseels S, Panich P. Effects of oocyte quality on development and transcriptional activity in early bovine embryos. Anim Reprod Sci. 2002;71:143–55.CrossRefPubMed
57.
Lonergan P, Rizos D, Kanka J, Nemcova L, Mbaye AM, Kingston M, et al. Temporal sensitivity of bovine embryos to culture environment after fertilization and the implications for blastocyst quality. Reproduction. 2003;126:337–46.CrossRefPubMed
58.
Yuan YQ, Van Soom A, Leroy JL, Dewulf J, Van Zeveren A, de Kruif A, et al. Apoptosis in cumulus cells, but not in oocytes, may influence bovine embryonic developmental competence. Theriogenology. 2005;63:2147–63.CrossRefPubMed
59.
Melka MG, Rings F, Hölker M, Tholen E, Havlicek V, Besenfelder U, et al. Expression of apoptosis regulatory genes and incidence of apoptosis in different morphological quality groups of in vitro-produced bovine pre-implantation embryos. Reprod Domest Anim. 2010;45:915–21.PubMed
60.
Byrne AT, Southgate J, Brison DR, Leese HJ. Analysis of apoptosis in the preimplantation bovine embryo using TUNEL. J Reprod Fertil. 1999;117:97–105.CrossRefPubMed
61.
Fukui Y, Sakuma Y. Maturation of bovine oocytes cultured in vitro: relation to ovarian activity, follicular size and the presence or absence of cumulus cells. Biol Reprod. 1980;22:669–73.PubMed
62.
Fatehi AN, Zeinstra EC, Kooij RV, Colenbrander B, Bevers MM. Effect of cumulus cell removal of in vitro matured bovine oocytes prior to in vitro fertilization on subsequent cleavage rate. Theriogenology. 2002;57:1347–55.CrossRefPubMed
63.
Patel OV, Bettegowda A, Ireland JJ, Coussens PM, Lonergan P, Smith GW. Functional genomics studies of oocyte competence: evidence that reduced transcript abundance for follistatin is associated with poor developmental competence of bovine oocytes. Reproduction. 2007;133:95–106.CrossRefPubMed
64.
Lee KB, Bettegowda A, Wee G, Ireland JJ, Smith GW. Molecular determinants of oocyte competence: potential functional role for maternal (oocyte-derived) follistatin in promoting bovine early embryogenesis. Endocrinology. 2009;150:2463–71.CrossRefPubMed
65.
Bettegowda A, Patel OV, Lee KB, Park KE, Salem M, Yao J, et al. Identification of novel bovine cumulus cell molecular markers predictive of oocyte competence: functional and diagnostic implications. Biol Reprod. 2008;79:301–9.CrossRefPubMed
66.
Assidi M, Dufort I, Ali A, Hamel M, Algriany O, Dielemann S, et al. Identification of potential markers of oocyte competence expressed in bovine cumulus cells cultured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro. Biol Reprod. 2008;79:209–22.CrossRefPubMed
67.
McKenzie LJ, Pangas SA, Carson SA, Kovanci E, Cisneros P, Buster JE, et al. Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. Hum Reprod. 2004;19:2869–74.CrossRefPubMed
68.
Blondin P, Sirard MA. Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Mol Reprod Dev. 1995;41:54–62.CrossRefPubMed
69.
Hizaki H, Segi E, Sugimoto Y, Hirose M, Saji T, Ushikubi F, et al. Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP(2). Proc Natl Acad Sci U S A. 1999;96:10501–6.CrossRefPubMedCentralPubMed
70.
Li Q, Jimenez-Krassel F, Ireland JJ, Smith GW. Gene expression profiling of bovine preovulatory follicles: gonadotropin surge and prostanoid-dependent up-regulation of genes potentially linked to the ovulatory process. Reproduction. 2009;137:297–307.CrossRefPubMed
71.
Peschon JJ, Slack JL, Reddy P, Stocking KL, Sunnarborg SW, Lee DC, et al. An essential role for ectodomain shedding in mammalian development. Science. 1998;282:1281–4.CrossRefPubMed
72.
Blobel CP. ADAMs: key components in EGFR signalling and development. Nat Rev Mol Cell Biol. 2005;6:32–43.CrossRefPubMed
73.
Sugimura S, Ritter LJ, Sutton-McDowall ML, Mottershead DG, Thompson JG. Amphiregulin co-operates with bone morphogenetic protein 15 to increase bovine oocyte developmental competence: effects on gap junction-mediated metabolite supply. Mol Hum Reprod. 2014;20:499–513.CrossRefPubMed
74.
Steeves TE, Gardner DK. Metabolism of glucose, pyruvate, and glutamine during the maturation of oocytes derived from pre-pubertal and adult cows. Mol Reprod Dev. 1999;54:92–101.CrossRefPubMed
75.
Rose-Hellekant TA, Libersky-Williamson EA, Bavister BD. Energy substrates and amino acids provided during in vitro maturation of bovine oocytes alter acquisition of developmental competence. Zygote. 1998;6:285–94.CrossRefPubMed
76.
Saito T, Hiroi M, Kato T. Development of glucose utilization studied in single oocytes and preimplantation embryos from mice. Biol Reprod. 1994;50:266–70.CrossRefPubMed
77.
Sutton-McDowall ML, Gilchrist RB, Thompson JG. Cumulus expansion and glucose utilisation by bovine cumulus-oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone. Reproduction. 2004;128:313–9.CrossRefPubMed
78.
Augustin R, Pocar P, Navarrete-Santos A, Wrenzycki C, Gandolfi F, Niemann H, et al. Glucose transporter expression is developmentally regulated in in vitro derived bovine preimplantation embryos. Mol Reprod Dev. 2001;60:370–6.CrossRefPubMed
79.
Bertolini M, Beam SW, Shim H, Bertolini LR, Moyer AL, Famula TR, et al. Growth, development, and gene expression by in vivo- and in vitro-produced day 7 and 16 bovine embryos. Mol Reprod Dev. 2002;63:318–28.CrossRefPubMed
80.
Sutton ML, Cetica PD, Beconi MT, Kind KL, Gilchrist RB, Thompson JG. Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes. Reproduction. 2003;126:27–34.CrossRefPubMed
Metadata
Title
The effect of lysophosphatidic acid during in vitro maturation of bovine cumulus–oocyte complexes: cumulus expansion, glucose metabolism and expression of genes involved in the ovulatory cascade, oocyte and blastocyst competence
Authors
Dorota Boruszewska
Emilia Sinderewicz
Ilona Kowalczyk-Zieba
Katarzyna Grycmacher
Izabela Woclawek-Potocka
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/s12958-015-0044-x

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