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

Reproductive Biology and Endocrinology

Izabela Woclawek-Potocka¹  Katarzyna Grycmacher¹  Ilona Kowalczyk-Zieba¹  Emilia Sinderewicz¹  Dorota Boruszewska¹ 

[1] Department of Reproductive Immunology and Pathology, Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, Tuwima 10, Olsztyn, 10-748, Poland

关键词: Blastocyst competence;    Apoptosis;    Glucose metabolism;    Cumulus expansion;    Embryo;    Cumulus cells;    In vitro maturation;    Oocyte;    Lysophosphatidic acid;    Cow;   

Others  :  1216420
DOI  :  10.1186/s12958-015-0044-x

 received in 2015-01-09, accepted in 2015-05-12,  发布年份 2015

【 摘 要 】

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.

【 授权许可】

   
2015 Boruszewska et al.; licensee BioMed Central.

【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

Fig. 5.

Fig. 6.

Fig. 7.

Fig. 8.

【 参考文献 】

• [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.
• [2]Sirard MA, Richard F, Blondin P, Robert C. Contribution of the oocyte to embryo quality. Theriogenology. 2006; 65:126-36.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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: Article ID e13952
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [38]Zhao S, Fernald RD. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol. 2005; 12:1047-64.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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: Article ID e4109
• [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: Article ID e34110
• [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.
• [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.
• [48]Goissis MD, Cibelli JB. Functional characterization of SOX2 in bovine preimplantation embryos. Biol Reprod. 2014; 90:30.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [72]Blobel CP. ADAMs: key components in EGFR signalling and development. Nat Rev Mol Cell Biol. 2005; 6:32-43.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.