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Tolerance of lamb and mouse oocytes to cryoprotectants during vitrification

Published online by Cambridge University Press:  07 December 2018

Jaqueline Sudiman Open the ORCID record for Jaqueline Sudiman [Opens in a new window] ,
Alice Lee ,
Kheng Ling Ong ,
Wu Zi Yuan ,
Sarah Jansen ,
Peter Temple-Smith ,
Mulyoto Pangestu  and
Sally Catt
Jaqueline Sudiman*
Affiliation:
Obstetrics and Gynaecology Department, Monash Medical Centre, 246 Clayton Road, Victoria, Australia
Alice Lee
Affiliation:
Obstetrics and Gynaecology Department, Monash Medical Centre, 246 Clayton Road, Victoria, Australia
Kheng Ling Ong
Affiliation:
Obstetrics and Gynaecology Department, Monash Medical Centre, 246 Clayton Road, Victoria, Australia
Wu Zi Yuan
Affiliation:
Obstetrics and Gynaecology Department, Monash Medical Centre, 246 Clayton Road, Victoria, Australia
Sarah Jansen
Affiliation:
Obstetrics and Gynaecology Department, Monash Medical Centre, 246 Clayton Road, Victoria, Australia
Peter Temple-Smith
Affiliation:
Obstetrics and Gynaecology Department, Monash Medical Centre, 246 Clayton Road, Victoria, Australia
Mulyoto Pangestu
Affiliation:
Obstetrics and Gynaecology Department, Monash Medical Centre, 246 Clayton Road, Victoria, Australia
Sally Catt
Affiliation:
Obstetrics and Gynaecology Department, Monash Medical Centre, 246 Clayton Road, Victoria, Australia
*
Address for correspondence: Jaqueline Sudiman. Monash Institute of Medical Research, Obstetrics and Gynaecology Department, Udayana University, Denpasar, Bali, Indonesia. Tel: +62 82283387245. E-mail: j_sudiman@yahoo.com
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Summary

Mouse and lamb oocytes were vitrified with, or exposed to, different cryoprotectants and evaluated for their effects on their survival and developmental competence after in vitro fertilization (IVF) and activation treatments. Control oocytes remained untreated, whilst the remainder were exposed to three different combinations of vitrification solutions [dimethyl sulfoxide (DMSO) + ethylene glycol (EG), EG only, or propanediol (PROH) + EG] and either vitrified or left unfrozen (exposed groups). Oocytes in the control and vitrified groups underwent IVF and developmental competence was assessed to the blastocyst stage. In lambs, survival rate in vitrified oocytes was significantly lower than for oocytes in the exposed groups (P <0.05). Blastocyst development was low in vitrified oocytes compared with controls (<6% vs 38.9%, P <0.01). Parthenogenetic activation was more prevalent in vitrified lamb oocytes compared with controls (P <0.05). No evidence of zona pellucida hardening or cortical granule exocytosis could account for reduced fertilization rates in vitrified lamb oocytes. Mouse oocytes demonstrated a completely different response to lamb oocytes, with survival and parthenogenetic activation rates unaffected by the vitrification process. Treatment of mouse oocytes with DMSO + EG yielded significantly higher survival and cleavage rates than treatment with PROH + EG (87.8% and 51.7% vs 32.7% and 16.7% respectively, P <0.01), however cleavage rate for vitrified oocytes remained lower than for the controls (51.7% vs 91.7%, P <0.01) as did mean blastocyst cell number (33 ± 3.1 vs 42 ± 1.5, P <0.05). From this study, it is clear that lamb and mouse show different tolerances to cryoprotectants commonly used in vitrification procedures, and careful selection and testing of species-compatible cryoprotectants is required when vitrifying oocytes to optimize survival and embryo development.

Keywords

CryoprotectantsEmbryo developmentLamb oocytesMouse oocytesParthenogenesisVitrification
Type
Research Article
Information
Zygote , Volume 27 , Issue 1 , February 2019 , pp. 36 - 45
Copyright
© Cambridge University Press 2018 

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Footnotes

*

Affiliated to the Obstetrics and Gynaecology Department, Udayana University, Denpasar, Bali, Indonesia.

References

Albarracin, JL, Morato, R, Izquierdo, D and Mogas, T (2005) Vitrification of calf oocytes: effects of maturation stage and prematuration treatment on the nuclear and cytoskeletal components of oocytes and their subsequent development. Mol Reprod Dev 72, 239–249.Google Scholar
Ali, A and Sirard, MA (2002) The effects of 17beta-estradiol and protein supplement on the response to purified and recombinant follicle stimulating hormone in bovine oocytes. Zygote 10, 65–71.Google Scholar
Arav, A and Zvi, R (2008) Do chilling injury and heat stress share the same mechanism of injury in oocytes? Mol Cell Endocrinol, 282, 150–152.Google Scholar
Attanasio, L, Boccia, L, Vajta, G, Kuwayama, M, Campanile, G, Zicarelli, L, Neglia, G and Gasparrini, B (2010) Cryotop vitrification of buffalo (Bubalus bubalis) in in vitro matured oocytes: effects of cryoprotectant concentrations and warming procedures. Reprod Domest Anim 45, 997–1002.Google Scholar
Begin, I, Bhatia, B, Baldassarre, H, Dinnyes, A and Keefer, CL (2003) Cryopreservation of goat oocytes and in in vivo derived 2- to 4-cell embryos using the cryoloop (CLV) and solid-surface vitrification (SSV) methods. Theriogenology 59, 1839–1850.Google Scholar
Bernardini, L, Martini, E, Geraedts, JP, Hopman, AH, Lanteri, S, Conte, N and Capitanio, GL (1997) Comparison of gonosomal aneuploidy in spermatozoa of normal fertile men and those with severe male factor detected by in-situ hybridization. Mol Hum Reprod 3, 431–438.Google Scholar
Berthelot-Ricou, A, Perrin, J, di Giorgio, C, de Meo, M, Botta, A and Courbiere, B (2013) Genotoxicity assessment of mouse oocytes by comet assay before vitrification and after warming with three vitrification protocols. Fertil Steril 100, 882–888.Google Scholar
Cao, YX, Xing, Q, Li, L, Cong, L, Zhang, ZG, Wei, ZL and Zhou, P (2009) Comparison of survival and embryonic development in human oocytes cryopreserved by slow-freezing and vitrification. Fertil Steril 92, 1306–1311.Google Scholar
Cao, X, Li, J, Xue, H, Wang, S, Zhaow, W, Du, Z, Yang, Y and Yue, Z (2017) Effect of vitrification on meiotic maturation, mitochondrial distribution and glutathione synthesis in immature silver fox cumulus oocyte complexes. Theriogenology 15, 104–111.Google Scholar
Chang, CC, Shapiro, DB, Bernal, DP, Wright, G, Kort, HI and Nagy, ZP (2008) Two successful pregnancies obtained following oocyte vitrification and embryo re-vitrification. Reprod Biomed Online 16, 346–349.Google Scholar
Cobo, A, Castello, D, Vallejo, B, Albert, C, de los Santos, JM and Remohi, J (2013a) Outcome of cryotransfer of embryos developed from vitrified oocytes: double vitrification has no impact on delivery rates. Fertil Steril 99, 1623–1630.Google Scholar
Cobo, A, Garcia-Velasco, JA, Domingo, J, Remohi, J and Pellicer, A (2013b) Is vitrification of oocytes useful for fertility preservation for age-related fertility decline and in cancer patients? Fertil Steril 99, 1485–1495.Google Scholar
Ducibella, T, Anderson, E, Albertini, DF, Aalberg, J and Rangarajan, S (1988) Quantitative studies of changes in cortical granule number and distribution in the mouse oocyte during meiotic maturation. Dev Biol 130, 184–197.Google Scholar
Fahy, GM, Wowk, B, Wu, J and Paynter, S (2004) Improved vitrification solutions based on the predictability of vitrification solution toxicity. Cryobiology 48, 22–35.Google Scholar
Fernandez-Gonzalez, L and Jewgenow, K (2016) Cryopreservation of feline oocytes by vitrification using commercial kits and slush nitrogen technique. Reprod Domest Anim 51 (Suppl 3), 1–5.Google Scholar
Fraser, LR (1984) Mouse sperm capacitation in vitro involves loss of a surface-associated inhibitory component. J Reprod Fertil 72, 373–384.Google Scholar
Fuku, E, Xia, L and Downey, BR (1995) Ultrastructural changes in bovine oocytes cryopreserved by vitrification. Cryobiology 32, 139–156.Google Scholar
Gautam, SK, Verma, V, Palta, P, Chauhan, MS and Manik, RS (2008) Effect of type of cryoprotectant on morphology and developmental competence of in vitro-matured buffalo (Bubalus bubalis) oocytes subjected to slow freezing or vitrification. Reprod Fertil Dev 20, 490–496.Google Scholar
George, MA and Johnson, MH (1993) Use of fetal bovine serum substitutes for the protection of the mouse zona pellucida against hardening during cryoprotectant addition. Hum Reprod 8, 1898–1900.Google Scholar
Ghetler, Y, Skutelsky, E, Ben Nun, I, Ben Dor, L, Amihai, D and Shalgi, R (2006) Human oocyte cryopreservation and the fate of cortical granules. Fertil Steril 86, 210–216.Google Scholar
Gomez, MC, Catt, JW, Gillan, L, Evans, G and Maxwell, WM (1997) Effect of culture, incubation and acrosome reaction of fresh and frozen–thawed ram spermatozoa for in vitro fertilization and intracytoplasmic sperm injection. Reprod Fertil Dev 9, 665–673.Google Scholar
Gook, DA, Osborn, SM and Johnston, WI (1993) Cryopreservation of mouse and human oocytes using 1,2-propanediol and the configuration of the meiotic spindle. Hum Reprod 8, 1101–1109.Google Scholar
Griffiths, TA, Murdoch, AP and Herbert, M (2000) Embryonic development in vitro is compromised by the ICSI procedure. Hum Reprod 15, 1592–1596.Google Scholar
Han, BS and Gao, JL (2013) Effects of chemical combinations on the parthenogenetic activation of mouse oocytes. Exp Therapeut Med 5, 1281–1288.Google Scholar
Huang, JY, Chen, HY, Park, JY, Tan, SL and Chian, RC (2008) Comparison of spindle and chromosome configuration in in vitro- and in vivo-matured mouse oocytes after vitrification. Fertil Steril 90, 1424–1432.Google Scholar
Hyttel, P, Vajta, G and Callesen, H (2000) Vitrification of bovine oocytes with the open pulled straw method: ultrastructural consequences. Mol Reprod Dev 56, 80–88.Google Scholar
Jones, A, Van Blerkom, J, Davis, P and Toledo, AA (2004) Cryopreservation of metaphase II human oocytes effects mitochondrial membrane potential: implications for developmental competence. Hum Reprod 19, 1861–1866.Google Scholar
Kishigami, S and Wakayama, T (2007) Efficient strontium-induced activation of mouse oocytes in standard culture media by chelating calcium. J Reprod Dev 53, 1207–1215.Google Scholar
Kuwayama, M, Vajta, G, Kato, O and Leibo, SP (2005) Highly efficient vitrification method for cryopreservation of human oocytes. Reprod Biomed Online 11, 300–308.Google Scholar
Lane, M and Gardner, DK (2001) Vitrification of mouse oocytes using a nylon loop. Mol Reprod Dev 58, 342–347.Google Scholar
Larman, MG and Gardner, DK (2014) Ultrarapid vitrification of mouse oocytes and embryos. Methods Mol Biol 1092, 153–165.Google Scholar
Larman, MG, Katz-Jaffe, MG, Sheehan, CB and Gardner, DK (2007) 1,2-propanediol and the type of cryopreservation procedure adversely affect mouse oocyte physiology. Hum Reprod 22, 250–259.Google Scholar
Lee, SH, Ahuja, KK, Gilburt, DJ and Whittingham, DG (1988) The appearance of glycoconjugates associated with cortical granule release during mouse fertilization. Development 102, 595–604.Google Scholar
Levi Setti, PE, Porcu, E, Patrizio, P, Vigiliano, V, de Luca, R, d’Aloja, P, Spoletini, R and Scaravelli, G (2014) Human oocyte cryopreservation with slow freezing versus vitrification. Results from the National Italian Registry data, 2007–2011. Fertil Steril 102, 90–5 e92.Google Scholar
Liang, YY, Srirattana, K, Phermthai, T, Somfai, T, Nagai, T and Parnpai, R (2012) Effects of vitrification cryoprotectant treatment and cooling method on the viability and development of buffalo oocytes after intracytoplasmic sperm injection. Cryobiology 65, 151–156.Google Scholar
Loutradi, KE, Kolibianakis, EM, Venetis, CA, Papanikolaou, EG, Pados, G, Bontis, I and Tarlatzis, BC (2008) Cryopreservation of human embryos by vitrification or slow freezing: a systematic review and meta-analysis. Fertil Steril 90, 186–193.Google Scholar
Manna, C, Rienzi, L, Greco, E, Sbracia, M, Rahman, A, Poverini, R, Siracusa, G and De Felici, M (2001) Zona pellucida solubility and cortical granule complements in human oocytes following assisted reproductive techniques. Zygote 9, 201–210.Google Scholar
Marco-Jimenez, F, Berlinguer, F and Leoni, GG (2012) Effect of “ice blocker” in solutions for vitrification of in vitro matured ovine oocytes. CryoLett 33, 41–44.Google Scholar
Maro, B, Johnson, MH, Pickering, SJ and Flach, G (1984) Changes in actin distribution during fertilization of the mouse egg. J Embryol Exp Morphol 81, 211–237.Google Scholar
Miyara, F, Aubriot, FX, Glissant, A, Nathan, C, Douard, S, Stanovici, A, Herve, F, Dumont-Hassan, M, LeMeur, A, Cohen-Bacrie, P and Debey, P (2003) Multiparameter analysis of human oocytes at metaphase II stage after IVF failure in non-male infertility. Hum Reprod 18, 1494–1503.Google Scholar
Mullen, SF (ed.) (2007) Oncofertility. Springer, New York.Google Scholar
Palermo, G, Joris, H, Devroey, P and Van Steirteghem, AC (1992) Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 340, 17–18.Google Scholar
Palermo, GD, Neri, QV, Takeuchi, T and Rosenwaks, Z (2009) ICSI: where we have been and where we are going. Semin Reprod Med 27, 191–201.Google Scholar
Papis, K, Shimizu, M and Izaike, Y (2000) Factors affecting the survivability of bovine oocytes vitrified in droplets. Theriogenology 54, 651–658.Google Scholar
Pukazhenthi, BS and Wildt, DE (2004) Which reproductive technologies are most relevant to studying, managing and conserving wildlife? Reprod Fertil Dev 16, 33–46.Google Scholar
Quinn, PJ (1985) A lipid-phase separation model of low-temperature damage to biological membranes. Cryobiology 22, 128–146.Google Scholar
Schalkoff, ME, Oskowitz, SP and Powers, RD (1989) Ultrastructural observations of human and mouse oocytes treated with cryopreservatives. Biol Reprod 40, 379–393.Google Scholar
Shaw, JM and Jones, GM (2003) Terminology associated with vitrification and other cryopreservation procedures for oocytes and embryos. Hum Reprod Update 9, 583–605.Google Scholar
Shaw, JM and Trounson, AO (1989) Parthenogenetic activation of unfertilized mouse oocytes by exposure to 1,2-propanediol is influenced by temperature, oocyte age, and cumulus removal. Gamete Res 24, 269–279.Google Scholar
Somfai, T, Ozawa, M, Noguchi, J, Kaneko, H, Kuriani Karja, NW, Farhudin, M, Dinnyes, A, Nagai, T and Kikuchi, K (2007) Developmental competence of in vitro-fertilized porcine oocytes after in vitro maturation and solid surface vitrification: effect of cryopreservation on oocyte antioxidative system and cell cycle stage. Cryobiology 55, 115–126.Google Scholar
Stachecki, JJ and Cohen, J (2004) An overview of oocyte cryopreservation. Reprod Biomed Online 9, 152–163.Google Scholar
Succu, S, Bebbere, D, Bogliolo, L, Ariu, F, Fois, S, Leoni, GG, Berlinguer, F, Naitana, S and Ledda, S (2008) Vitrification of in vitro matured ovine oocytes affects in vitro pre-implantation development and mRNA abundance. Mol Reprod Dev 75, 538–546.Google Scholar
Succu, S, Leoni, GG, Bebbere, D, Berlinguer, F, Mossa, F, Bogliolo, L, Madeddu, M, Ledda, S and Naitana, S (2007a) Vitrification devices affect structural and molecular status of in vitro matured ovine oocytes. Mol Reprod Dev 74, 1337–1344.Google Scholar
Succu, S, Leoni, GG, Berlinguer, F, Madeddu, M, Bebbere, D, Mossa, F, Bogliolo, L, Ledda, S and Naitana, S (2007b) Effect of vitrification solutions and cooling upon in vitro matured prepubertal ovine oocytes. Theriogenology 68, 107–114.Google Scholar
Summers, MC, Bhatnagar, PR, Lawitts, JA and Biggers, JD (1995) Fertilization in vitro of mouse ova from inbred and outbred strains: complete preimplantation embryo development in glucose-supplemented KSOM. Biol Reprod 53, 431–437.Google Scholar
Tervit, HR, Whittingham, DG and Rowson, LE (1972) Successful culture in vitro of sheep and cattle ova. J Reprod Fertil 30, 493–497.Google Scholar
Tian, SJ, Yan, CL, Yang, HX, Zhou, GB, Yang, ZQ and Zhu, SE (2007) Vitrification solution containing DMSO and EG can induce parthenogenetic activation of in vitro matured ovine oocytes and decrease sperm penetration. Anim Reprod Sci 101, 365–371.Google Scholar
Tong, XH, Wu, LM, Jin, RT, Luo, LH, Luan, HB and Liu, YS (2012) Fertilization rates are improved after IVF if the corona radiata is left intact in vitrified-warmed human oocytes. Hum Reprod 27, 3208–3214.Google Scholar
Tong, XH, Wu, LM, Jin, RT, Luan, HB and Liu, YS (2013) Human oocyte vitrification with corona radiata, in autologous follicular fluid supplemented with ethylene glycol, preserves conventional IVF potential: birth of four healthy babies. Reprod Fertil Dev 26, 1001–1006.Google Scholar
Vajta, G (2000) Vitrification of the oocytes and embryos of domestic animals. Anim Reprod Sci 60–61, 357–364.Google Scholar
Vajta, G, Holm, P, Kuwayama, M, Booth, PJ, Jacobsen, H, Greve, T and Callesen, H (1998) Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Mol Reprod Dev 51, 53–58.Google Scholar
Van der Elst, J, Van den Abbeel, E, Nerinckx, S and Van Steirteghem, A (1992) Parthenogenetic activation pattern and microtubular organization of the mouse oocyte after exposure to 1,2-propanediol. Cryobiology 29, 549–562.Google Scholar
Veeck, LL, Amundson, CH, Brothman, LJ, DeScisciolo, C, Maloney, MK, Muasher, SJ and Jones, HW Jr (1993) Significantly enhanced pregnancy rates per cycle through cryopreservation and thaw of pronuclear stage oocytes. Fertil Steril 59, 1202–1207.Google Scholar
Veeck, LL, Bodine, R, Clarke, RN, Berrios, R, Libraro, J, Moschini, RM, Zaninovic, N and Rosenwaks, Z (2004) High pregnancy rates can be achieved after freezing and thawing human blastocysts. Fertil Steril 82, 1418–1427.Google Scholar
Wood, MJ, Whittingham, DG and Lee, SH (1992) Fertilization failure of frozen mouse oocytes is not due to premature cortical granule release. Biol Reprod, 46, 1187–1195.Google Scholar
Wusteman, MC, Pegg, DE, Robinson, MP, Wang, LH and Fitch, P (2002) Vitrification medium: toxicity, permeability, and dielectric properties. Cryobiology 44, 24–37.Google Scholar