Sphingoshine-1-Phosphate Enhances Meiotic Maturation and Further Embryonic Development in Pigs

  • Lee, Hyo-Sang (Development and Differentiation Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Koo, Deog-Bon (Department of Biotechnology, College of Engineering, Daegu University)
  • Received : 2012.08.28
  • Accepted : 2012.09.17
  • Published : 2012.09.30

Abstract

Sphingosine-1-phosphate (S1P) has a many function involved proliferation, differentiation and survival of many cells. In this study, to investigate whether S1P improve the developmental competence of porcine embryos, 50 nM of S1P were supplemented during in vitro maturation (with EGF or without EGF) medium and/or in vitro culture (IVC) medium. Addition of S1P was significantly increased the rate of oocytes reaching metaphase II (MII) compared to the control (83.5 vs. 64.1%) in without EGF medium, but not with EGF medium (89.5 vs. 84.6%). When treated with $1{\mu}M$ of N1N-dimethylsphingosine (DMS), a sphingosine kinase inhibitor which is blocked endogenous generation of S1P, the meiotic progression rates to MII stage (without EGF: 45.2 and with EGF: 66.7%) were significantly decreased and degeneration rates (without EGF: 51.2 and with EGF: 30.1%) were increased in both medium compared to control group during IVM periods. Also, the rates of blastocyst formation was significantly increased in the S1P treated group compared to control group (29.0 vs. 19.2%) of EGF supplemented medium, whereas there were no effect in the EGF free medium (9.0 vs. 10.5%). After 12 h IVM, the phosphorylation of ERK1 and ERK2, which is major signaling pathway of MAP kinase, were increased in the S1P group than that of control or DMS group. When supplemented of S1P during IVC, the rates of blastocyst formation and total cell number (30.2% and 40.6) were significantly increased in S1P-treated group compared with control (20.1% and 32.5), DMS (12.3% and 25.1), and S1P plus DMS group (24.7% and 33.6). The percentage of apoptosis nuclei in the S1P group was significantly decreased than other groups. Also, the rates of blastocyst formation (26.7 vs. 14%) and total cell number (42.8 vs. 32.5) were significantly increased in the S1P group than those of control group when S1P added during the entire IVM and IVC periods. Taken together, our results indicate that S1P supplementation in IVM and/or IVC medium affects beneficial effect of meiotic maturation and subsequent developmental competence of porcine embryos.

Keywords

References

  1. Chen XY, Li QW, Zhang SS, Han ZS, Zhao R, Wu SY, Huang J (2007): Effects of ovarian cortex cell co-culture during in vitro maturation on porcine oocytes maturation, fertilization and embryo development. Anim Reprod Sci 99:306-316. https://doi.org/10.1016/j.anireprosci.2006.05.007
  2. Cuvillier O, Pirianov G, Kleuser B, Vanek PG, Coso OA, Gutkind S, Spiegel S (1996): Suppression of ceramide- mediated programmed cell death by sphingosine- 1-phosphate. Nature 381:800-803. https://doi.org/10.1038/381800a0
  3. Ding J, Foxcroft GR (1994): Epidermal growth factor enhances oocyte maturation in pigs. Mol Reprod Dev 39:30-40. https://doi.org/10.1002/mrd.1080390106
  4. Edsall LC, Pirianov GG, Spiegel S (1997): Involvement of sphingosine 1-phosphate in nerve growth factor-mediated neuronal survival and differentiation. J Neurosci 17:6952-6960.
  5. Fan HY, Sun QY (2004): Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol Reprod 70: 535-547. https://doi.org/10.1095/biolreprod.103.022830
  6. Grupen CG, Nagashima H, Nottle MB (1997): Role of epidermal growth factor and insulin-like growth factor-I on porcine oocyte maturation and embryonic development in vitro. Reprod Fertil Dev 9:571- 575. https://doi.org/10.1071/R96115
  7. Halliwell B (1978): Superoxide-dependent formation of hydroxyl radicals in the presence of iron chelates: is it a mechanism for hydroxyl radical production in biochemical systems? FEBS Lett 92:321- 326. https://doi.org/10.1016/0014-5793(78)80779-0
  8. Hsu CJ, Holmes SD, Hammond JM (1987): Ovarian epidermal growth factor-like activity. Concentrations in porcine follicular fluid during follicular enlargement. Biochem Biophys Res Commun 147: 242-247. https://doi.org/10.1016/S0006-291X(87)80112-2
  9. Inoue M, Naito K, Nakayama T, Sato E (1998): Mitogen- activated protein kinase translocates into the germinal vesicle and induces germinal vesicle breakdown in porcine oocytes. Biol Reprod 58:130-136. https://doi.org/10.1095/biolreprod58.1.130
  10. Kim DS, Hwang ES, Lee JE, Kim SY, Kwon SB, Park KC (2003): Sphingosine-1-phosphate decreases melanin synthesis via sustained ERK activation and subsequent MITF degradation. J Cell Sci 116:1699- 1706. https://doi.org/10.1242/jcs.00366
  11. Kim HS, Lee GS, Hyun SH, Lee SH, Nam DH, Jeong YW, Hwang WS (2004): Improved in vitro development of porcine embryos with different energy substrates and serum. Theriogenology 61:1381- 1393. https://doi.org/10.1016/j.theriogenology.2003.08.012
  12. Kim JH, Lee SH, Kim S, Jeong YW, Koo OJ, Hashem MD, Hwang WS (2006): Embryotrophic effects of ethylenediaminetetraacetic acid and hemoglobin on in vitro porcine embryos development. Theriogenology 66:449-455. https://doi.org/10.1016/j.theriogenology.2005.12.008
  13. Kitagawa Y, Suzuki K, Yoneda A, Watanabe T (2004): Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS), and DNA fragmentation in porcine embryos. Theriogenology 62:1186- 1197. https://doi.org/10.1016/j.theriogenology.2004.01.011
  14. Koo DB, Kang YK, Choi YH, Park JS, Han SK, Park IY, Han YM (2000): In vitro development of reconstructed porcine oocytes after somatic cell nuclear transfer. Biol Reprod 63:986-992. https://doi.org/10.1095/biolreprod63.4.986
  15. Kun Z, Shaohua W, Yufang M, Yankun L, Hengxi W, Xiuzhu S, Ning L (2007): Effects of leptin supplementation in in vitro maturation medium on meiotic maturation of oocytes and preimplantation development of parthenogenetic and cloned embryos in pigs. Anim Reprod Sci 101:85-96. https://doi.org/10.1016/j.anireprosci.2006.08.021
  16. Labbe JC, Capony JP, Caput D, Cavadore JC, Derancourt J, Kaghad M, Doree M (1989): MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B. Embo J 8:3053-3058.
  17. Lee JY, Hannun YA, Obeid LM (1996): Ceramide inactivates cellular protein kinase Calpha. J Biol Chem 271:13169-13174. https://doi.org/10.1074/jbc.271.22.13169
  18. Maupas-Schwalm F, Auge N, Robinet C, Cambus JP, Parsons SJ, Salvayre R, Negre-Salvayre A (2004): The sphingomyelin/ceramide pathway is involved in ERK1/2 phosphorylation, cell proliferation, and uPAR overexpression induced by tissue-type plasminogen activator. Faseb J 18:1398-1400. https://doi.org/10.1096/fj.03-1123fje
  19. McEvoy TG, Coull GD, Broadbent PJ, Hutchinson JS, Speake BK (2000): Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J Reprod Fertil 118: 163-170.
  20. Meyer zu Heringdorf D, Lass H, Kuchar I, Alemany R, Guo Y, Schmidt M, Jakobs KH (1999): Role of sphingosine kinase in $Ca^{(2+)}$signalling by epidermal growth factor receptor. FEBS Lett 461: 217-222. https://doi.org/10.1016/S0014-5793(99)01463-5
  21. Moor RM, Mattioli M, Ding J, Nagai T (1990): Maturation of pig oocytes in vivo and in vitro. J Reprod Fertil Suppl 40:197-210.
  22. Morbeck DE, Flowers WL, Britt JH (1993): Response of porcine granulosa cells isolated from primary and secondary follicles to FSH, 8-bromo-cAMP and epidermal growth factor in vitro. J Reprod Fertil 99: 577-584. https://doi.org/10.1530/jrf.0.0990577
  23. Morita Y, Perez GI, Paris F, Miranda SR, Ehleiter D, Haimovitz-Friedman A, Tilly JL (2000): Oocyte apoptosis is suppressed by disruption of the acid sphingomyelinase gene or by sphingosine-1-phosphate therapy. Nat Med 6:1109-1114. https://doi.org/10.1038/80442
  24. Nebreda AR, Ferby I (2000): Regulation of the meiotic cell cycle in oocytes. Curr Opin Cell Biol 12: 666-675. https://doi.org/10.1016/S0955-0674(00)00150-2
  25. O'Keefe SJ, Kiessling AA, Cooper GM (1991): The c-mos gene product is required for cyclin B accumulation during meiosis of mouse eggs. Proc Natl Acad Sci 88:7869-7872. https://doi.org/10.1073/pnas.88.17.7869
  26. Ohashi S, Naito K, Sugiura K, Iwamori N, Goto S, Naruoka H, Tojo H (2003): Analyses of mitogenactivated protein kinase function in the maturation of porcine oocytes. Biol Reprod 68:604-609. https://doi.org/10.1095/biolreprod.102.008334
  27. Okajima F (2002): Plasma lipoproteins behave as carriers of extracellular sphingosine 1-phosphate: is this an atherogenic mediator or an anti-atherogenic mediator? Biochim Biophys Acta 1582:132-137. https://doi.org/10.1016/S1388-1981(02)00147-6
  28. Olivera A, Spiegel S (1993): Sphingosine-1-phosphate as second messenger in cell proliferation induced by PDGF and FCS mitogens. Nature 365:557-560. https://doi.org/10.1038/365557a0
  29. Otala M, Suomalainen L, Pentikainen MO, Kovanen P, Tenhunen M, Erkkila K, Dunkel L (2004): Protection from radiation-induced male germ cell loss by sphingosine-1-phosphate. Biol Reprod 70:759-767. https://doi.org/10.1095/biolreprod.103.021840
  30. Paris F, Perez GI, Fuks Z, Haimovitz-Friedman A, Nguyen H, Bose M, Kolesnick R (2002): Sphingosine 1-phosphate preserves fertility in irradiated female mice without propagating genomic damage in offspring. Nat Med 8:901-902. https://doi.org/10.1038/nm0902-901
  31. Perez GI, Jurisicova A, Matikainen T, Moriyama T, Kim MR, Takai Y, Tilly JL (2005): A central role for ceramide in the age-related acceleration of apoptosis in the female germline. FASEB J 19:860-862. https://doi.org/10.1096/fj.04-2903fje
  32. Perez GI, Knudson CM, Leykin L, Korsmeyer SJ, Tilly JL (1997): Apoptosis-associated signaling pathways are required for chemotherapy-mediated female germ cell destruction. Nat Med 3:1228-1232. https://doi.org/10.1038/nm1197-1228
  33. Prather RS, Hawley RJ, Carter DB, Lai L, Greenstein JL (2003): Transgenic swine for biomedicine and agriculture. Theriogenology 59:115-123. https://doi.org/10.1016/S0093-691X(02)01263-3
  34. Prochazka R, Srsen V, Nagyova E, Miyano T, Flechon JE (2000): Developmental regulation of effect of epidermal growth factor on porcine oocyte-cumulus cell complexes: nuclear maturation, expansion, and F-actin remodeling. Mol Reprod Dev 56: 63-73. https://doi.org/10.1002/(SICI)1098-2795(200005)56:1<63::AID-MRD8>3.0.CO;2-D
  35. Pyne S, Pyne NJ (2000): Sphingosine 1-phosphate signalling in mammalian cells. Biochem J 349:385- 402. https://doi.org/10.1042/0264-6021:3490385
  36. Rakhit S, Conway AM, Tate R, Bower T, Pyne NJ, Pyne S (1999): Sphingosine 1-phosphate stimulation of the p42/p44 mitogen-activated protein kinase pathway in airway smooth muscle. Role of endothelial differentiation gene 1, c-Src tyrosine kinase and phosphoinositide 3-kinase. Biochem J 338:643-649. https://doi.org/10.1042/0264-6021:3380643
  37. Rani CS, Wang F, Fuior E, Berger A, Wu J, Sturgill TW, Spiegel S (1997). Divergence in signal transduction pathways of platelet-derived growth factor (PDGF) and epidermal growth factor (EGF) receptors. Involvement of sphingosine 1-phosphate in PDGF but not EGF signaling. J Biol Chem 272:10777- 10783. https://doi.org/10.1074/jbc.272.16.10777
  38. Roth Z, Hansen PJ (2004): Sphingosine 1-phosphate protects bovine oocytes from heat shock during maturation. Biol Reprod 71:2072-2078. https://doi.org/10.1095/biolreprod.104.031989
  39. Roy SK, Greenwald GS (1991): Mediation of follicle- stimulating hormone action on follicular deoxyribonucleic acid synthesis by epidermal growth factor. Endocrinology 129: 1903-1908. https://doi.org/10.1210/endo-129-4-1903
  40. Spiegel S, Milstien S (2003): Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 4:397-407. https://doi.org/10.1038/nrm1103
  41. Spiteller G (2001): Peroxidation of linoleic acid and its relation to aging and age dependent diseases. Mech Ageing Dev 122:617-657. https://doi.org/10.1016/S0047-6374(01)00220-2
  42. Sukocheva O, Wadham C, Holmes A, Albanese N, Verrier E, Feng F, Xia P (2006): Estrogen transactivates EGFR via the sphingosine 1-phosphate receptor Edg-3: the role of sphingosine kinase-1. J Cell Biol 173:301-310. https://doi.org/10.1083/jcb.200506033
  43. Sun QY, Lai L, Bonk A, Prather RS, Schatten H (2001): Cytoplasmic changes in relation to nuclear maturation and early embryo developmental potential of porcine oocytes: effects of gonadotropins, cumulus cells, follicular size, and protein synthesis inhibition. Mol Reprod Dev 59:192-198. https://doi.org/10.1002/mrd.1022
  44. Suomalainen L, Hakala JK, Pentikainen V, Otala M, Erkkila K, Pentikainen MO, Dunkel L (2003): Sphingosine- 1-phosphate in inhibition of male germ cell apoptosis in the human testis. J Clin Endocrinol Metab 88:5572-5579. https://doi.org/10.1210/jc.2003-030776
  45. Tanimoto T, Lungu AO, Berk BC (2004): Sphingosine 1-phosphate transactivates the platelet-derived growth factor beta receptor and epidermal growth factor receptor in vascular smooth muscle cells. Circ Res 94:1050-1058. https://doi.org/10.1161/01.RES.0000126404.41421.BE
  46. Tellier E, Negre-Salvayre A, Bocquet B, Itohara S, Hannun YA, Salvayre R, Auge, N (2007): Role for furin in tumor necrosis factor alpha-induced activation of the matrix metalloproteinase/sphingolipid mitogenic pathway. Mol Cell Biol 27:2997-3007. https://doi.org/10.1128/MCB.01485-06
  47. Vaughan TJ, James PS, Pascall JC, Brown KD (1992): Expression of the genes for TGF alpha, EGF and the EGF receptor during early pig development. Development 116:663-669.
  48. von Otte S, Paletta JR, Becker S, Konig S, Fobker M, Greb RR, Nofer JR (2006): Follicular fluid high density lipoprotein-associated sphingosine 1-phosphate is a novel mediator of ovarian angiogenesis. J Biol Chem 281:5398-5405. https://doi.org/10.1074/jbc.M508759200
  49. Wang WH, Abeydeera LR, Han YM, Prather RS, Day BN (1999): Morphologic evaluation and actin filament distribution in porcine embryos produced in vitro and in vivo. Biol Reprod 60:1020-1028. https://doi.org/10.1095/biolreprod60.4.1020
  50. Wehrend A, Meinecke B (2001). Kinetics of meiotic progression, M-phase promoting factor (MPF) and mitogen-activated protein kinase (MAP kinase) activities during in vitro maturation of porcine and bovine oocytes: species specific differences in the length of the meiotic stages. Anim Reprod Sci 66: 175-184. https://doi.org/10.1016/S0378-4320(01)00094-X
  51. Xia P, Gamble JR, Rye KA, Wang L, Hii CS, Cockerill P, Vadas MA (1998): Tumor necrosis factor-alpha induces adhesion molecule expression through the sphingosine kinase pathway. Proc Natl Acad Sci 95:14196-14201. https://doi.org/10.1073/pnas.95.24.14196