Antifreeze proteins (AFPs) are a class of polypeptides that permit organismal survival in sub-freezing environments. The purpose of this study was to investigate the effect of AFP supplementation on immature mouse oocyte vitrification. Germinal vesicle-stage oocytes were vitrified using a two-step exposure to equilibrium and vitrification solution in the presence or absence of 500 ng/mL of AFP III. After warming, oocyte survival, in vitro maturation, fertilization, and embryonic development up to the blastocyst stage were assessed. Spindle and chromosome morphology, membrane integrity, and the expression levels of several genes were assessed in in vitro matured oocytes. The rate of blastocyst formation was significantly higher and the number of caspase-positive blastomeres was significantly lower in the AFP-treated group compared with the untreated group. The proportion of oocytes with intact spindles/chromosomes and stable membranes was also significantly higher in the AFP group. The AFP group showed increased Mad2, Hook-1, Zar1, Zp1, and Bcl2 expression and lower Eg5, Zp2, Caspase6, and Rbm3 expression compared with the untreated group. Supplementation of the vitrification medium with AFP has a protective effect on immature mouse oocytes, promoting their resistance to chilling injury. AFPs may preserve spindle forming ability and membrane integrity at GV stage. The fertilization and subsequent developmental competence of oocytes may be associated with the modulation of Zar1, Zp1/Zp2, Bcl2, Caspase6, and Rbm3.
References
[1]
Ubaldi F, Anniballo R, Romano S, Baroni E, Albricci L, et al. (2010) Cumulative ongoing pregnancy rate achieved with oocyte vitrification and cleavage stage transfer without embryo selection in a standard infertility program. Hum Reprod 25: 1199–1205.
[2]
Cobo A, Meseguer M, Remohi J, Pellicer A (2010) Use of cryo-banked oocytes in an ovum donation programme: a prospective, randomized, controlled, clinical trial. Hum Reprod 25: 2239–2246.
[3]
Cobo A, Romero JL, Perez S, de los Santos MJ, Meseguer M, et al. (2010) Storage of human oocytes in the vapor phase of nitrogen. Fertil Steril 94: 1903–1907.
[4]
Nagy ZP, Chang CC, Shapiro DB, Bernal DP, Kort HI, et al. (2009) The efficacy and safety of human oocyte vitrification. Semin Reprod Med 27: 450–455.
[5]
Smith GD, Serafini PC, Fioravanti J, Yadid I, Coslovsky M, et al. (2010) Prospective randomized comparison of human oocyte cryopreservation with slow-rate freezing or vitrification. Fertil Steril 94: 2088–2095.
[6]
Rao GD, Chian RC, Son WS, Gilbert L, Tan SL (2004) Fertility preservation in women undergoing cancer treatment. Lancet 363: 1829–1830.
[7]
Isachenko E, Rahimi G, Isachenko V, Nawroth F (2004) In-vitro maturation of germinal-vesicle oocytes and cryopreservation in metaphase I/II: a possible additional option to preserve fertility during ovarian tissue cryopreservation. Reprod Biomed Online 8: 553–557.
[8]
Cooper A, Paynter SJ, Fuller BJ, Shaw RW (1998) Differential effects of cryopreservation on nuclear or cytoplasmic maturation in vitro in immature mouse oocytes from stimulated ovaries. Hum Reprod 13: 971–978.
[9]
Isachenko EF, Nayudu PL (1999) Vitrification of mouse germinal vesicle oocytes: effect of treatment temperature and egg yolk on chromatin and spindle normality and cumulus integrity. Hum Reprod 14: 400–408.
[10]
Toth TL, Lanzendorf SE, Sandow BA, Veeck LL, Hassen WA, et al. (1994) Cryopreservation of human prophase I oocytes collected from unstimulated follicles. Fertil Steril 61: 1077–1082.
[11]
Toth TL, Baka SG, Veeck LL, Jones HW , Muasher S, et al. (1994) Fertilization and in vitro development of cryopreserved human prophase I oocytes. Fertil Steril 61: 891–894.
[12]
Son WY, Park SE, Lee KA, Lee WS, Ko JJ, et al. (1996) Effects of 1,2-propanediol and freezing-thawing on the in vitro developmental capacity of human immature oocytes. Fertil Steril 66: 995–999.
[13]
Yeh Y, Feeney RE (1996) Antifreeze Proteins: Structures and Mechanisms of Function. Chem Rev 96: 601–618.
[14]
Fletcher GL, Hew CL, Davies PL (2001) Antifreeze proteins of teleost fishes. Annu Rev Physiol 63: 359–390.
[15]
Arav A, Rubinsky B, Fletcher G, Seren E (1993) Cryogenic protection of oocytes with antifreeze proteins. Mol Reprod Dev 36: 488–493.
[16]
Payne SR, Oliver JE, Upreti GC (1994) Effect of antifreeze proteins on the motility of ram spermatozoa. Cryobiology 31: 180–184.
[17]
Madura JD, Baran K, Wierzbicki A (2000) Molecular recognition and binding of thermal hysteresis proteins to ice. J Mol Recognit 13: 101–113.
[18]
Rubinsky B, Arav A, Mattioli M, Devries AL (1990) The effect of antifreeze glycopeptides on membrane potential changes at hypothermic temperatures. Biochem Biophys Res Commun 173: 1369–1374.
[19]
Habibi A, Farrokhi N, Moreira da Silva F, Bettencourt BF, Bruges-Armas J, et al. (2010) The effects of vitrification on gene expression in mature mouse oocytes by nested quantitative PCR. J Assist Reprod Genet 27: 599–604.
[20]
Musacchio A, Hardwick KG (2002) The spindle checkpoint: structural insights into dynamic signalling. Nat Rev Mol Cell Biol 3: 731–741.
[21]
Wang WH, Sun QY (2006) Meiotic spindle, spindle checkpoint and embryonic aneuploidy. Front Biosci 11: 620–636.
[22]
Wang JZ, Sui HS, Miao DQ, Liu N, Zhou P, et al. (2009) Effects of heat stress during in vitro maturation on cytoplasmic versus nuclear components of mouse oocytes. Reproduction 137: 181–189.
[23]
Jo JW, Jee BC, Lee JR, Suh CS (2011) Effect of antifreeze protein supplementation in vitrification medium on mouse oocyte developmental competence. Fertil Steril.
[24]
Hagan I, Yanagida M (1990) Novel potential mitotic motor protein encoded by the fission yeast cut7+ gene. Nature 347: 563–566.
[25]
Hoyt MA, He L, Loo KK, Saunders WS (1992) Two Saccharomyces cerevisiae kinesin-related gene products required for mitotic spindle assembly. J Cell Biol 118: 109–120.
[26]
Blangy A, Lane HA, d’Herin P, Harper M, Kress M, et al. (1995) Phosphorylation by p34cdc2 regulates spindle association of human Eg5, a kinesin-related motor essential for bipolar spindle formation in vivo. Cell 83: 1159–1169.
[27]
Castillo A, Justice MJ (2007) The kinesin related motor protein, Eg5, is essential for maintenance of pre-implantation embryogenesis. Biochem Biophys Res Commun 357: 694–699.
[28]
Castillo A, Morse HC , Godfrey VL, Naeem R, Justice MJ (2007) Overexpression of Eg5 causes genomic instability and tumor formation in mice. Cancer Res 67: 10138–10147.
[29]
Simpson F, Martin S, Evans TM, Kerr M, James DE, et al. (2005) A novel hook-related protein family and the characterization of hook-related protein 1. Traffic 6: 442–458.
[30]
Hamatani T, Falco G, Carter MG, Akutsu H, Stagg CA, et al. (2004) Age-associated alteration of gene expression patterns in mouse oocytes. Hum Mol Genet 13: 2263–2278.
[31]
Tong ZB, Gold L, Pfeifer KE, Dorward H, Lee E, et al. (2000) Mater, a maternal effect gene required for early embryonic development in mice. Nat Genet 26: 267–268.
[32]
Christians E, Davis AA, Thomas SD, Benjamin IJ (2000) Maternal effect of Hsf1 on reproductive success. Nature 407: 693–694.
[33]
Wu X, Viveiros MM, Eppig JJ, Bai Y, Fitzpatrick SL, et al. (2003) Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat Genet 33: 187–191.
[34]
Blomberg LA, Long EL, Sonstegard TS, Van Tassell CP, Dobrinsky JR, et al. (2005) Serial analysis of gene expression during elongation of the peri-implantation porcine trophectoderm (conceptus). Physiol Genomics 20: 188–194.
[35]
Wassarman PM (1988) Zona pellucida glycoproteins. Annu Rev Biochem 57: 415–442.
[36]
Wassarman PM (1988) Fertilization in mammals. Sci Am 259: 78–84.
[37]
Hinsch E, Groeger S, Oehninger S, Hinsch KD (2003) Localization and functional importance of a conserved zona pellucida 2 protein domain in the human and bovine ovary using monoclonal anti-ZP2 peptide antibodies. Theriogenology 60: 1331–1344.
[38]
Wrenzycki C, Herrmann D, Carnwath JW, Niemann H (1999) Alterations in the relative abundance of gene transcripts in preimplantation bovine embryos cultured in medium supplemented with either serum or PVA. Mol Reprod Dev 53: 8–18.
[39]
Yang MY, Rajamahendran R (2002) Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro. Anim Reprod Sci 70: 159–169.
[40]
Izawa M, Nguyen PH, Kim HH, Yeh J (1998) Expression of the apoptosis-related genes, caspase-1, caspase-3, DNA fragmentation factor, and apoptotic protease activating factor-1, in human granulosa cells. Fertil Steril 70: 549–552.
[41]
Exley GE, Tang C, McElhinny AS, Warner CM (1999) Expression of caspase and BCL-2 apoptotic family members in mouse preimplantation embryos. Biol Reprod 61: 231–239.
[42]
Nishiyama H, Itoh K, Kaneko Y, Kishishita M, Yoshida O, et al. (1997) A glycine-rich RNA-binding protein mediating cold-inducible suppression of mammalian cell growth. J Cell Biol 137: 899–908.
[43]
Zhou KW, Zheng XM, Yang ZW, Zhang L, Chen HD (2009) Overexpression of CIRP may reduce testicular damage induced by cryptorchidism. Clin Invest Med 32: E103–111.
[44]
Handyside AH, Hunter S (1984) A rapid procedure for visualising the inner cell mass and trophectoderm nuclei of mouse blastocysts in situ using polynucleotide-specific fluorochromes. J Exp Zool 231: 429–434.
[45]
Huang JY, Chen HY, Tan SL, Chian RC (2007) Effect of choline-supplemented sodium-depleted slow freezing versus vitrification on mouse oocyte meiotic spindles and chromosome abnormalities. Fertil Steril 88: 1093–1100.
[46]
Somfai T, Dinnyes A, Sage D, Marosan M, Carnwath JW, et al. (2006) Development to the blastocyst stage of parthenogenetically activated in vitro matured porcine oocytes after solid surface vitrification (SSV). Theriogenology 66: 415–422.