Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2017-0027
Animal Reproduction (AR)
Original Article

Human exhaled air can efficiently support in vitro maturation of porcine oocytes and subsequent early embryonic development

Zubing Cao; Di Gao; Tengteng Xu; Xu Tong; Yiqing Wang; Yunsheng Li; Fugui Fang; Jianping Ding; Xiaorong Zhang; Yunhai Zhang

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Abstract

Air phase is an indispensable environmental factor affecting oocyte maturation and early embryo development. Human exhaled air was previously proved to be a reliable and inexpensive atmosphere that sustains normal early development of mouse and bovine embryos. However, whether human exhaled air can support in vitro maturation (IVM) of porcine oocytes is not yet known. To evaluate the feasibility of maturing oocytes in human exhaled air, we examined oocyte morphology, BMP15 expression, nuclear and cytoplasmic maturation. We found that cumulus expansion status, expression levels of BMP15 important for cumulus expansion and the rate of first polar body emission were similar among human exhaled air, 5% O2 or 20% O2 in air after IVM of 44 h. Furthermore, the percentage of metaphase II (MII) oocytes showing normal cortical and sub-membranous localization of cortical granules and diffused mitochondrial distribution patterns is comparable among groups. The cleavage, blastocyst rate and total cell number were not apparently different for parthenogenetic activated and somatic cloned embryos derived from MII oocytes matured in three air phases, suggesting oocytes matured in human exhaled air obtain normal developmental competence. Taken together, human exhaled air can efficiently support in vitro maturation of porcine oocytes and subsequent early embryonic development.

Keywords

human exhaled air, pig, oocyte maturation, somatic cell nuclear transfer, early embryo

References

Adam AA , Takahashi Y , Katagiri S , Nagano M . 2004 . Effects of oxygen tension in the gas atmosphere during in vitro maturation, in vitro fertilization and in vitro culture on the efficiency of in vitro production of mouse embryos . Jpn J Vet Res , 52 : 77 - 84 .

Bavister BD . 1995 . Culture of preimplantation embryos: facts and artifacts . Hum Reprod Update , 1 : 91 - 148 .

Bavister BD , Poole KA . 2005 . Duration and temperature of culture medium equilibration affect frequency of blastocyst development . Reprod Biomed Online , 10 : 124 - 129 .

Brevini TA , Vassena R , Francisci C , Gandolfi F . 2005 . Role of adenosine triphosphate, active mitochondria, and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes . Biol Reprod , 72 : 1218 - 1223 .

Brevini TA , Cillo F , Antonini S , Gandolfi F . 2007 . Cytoplasmic remodelling and the acquisition of developmental competence in pig oocytes . Anim Reproduction Sci , 98 : 23 - 38 .

Buccione R , Vanderhyden BC , Caron PJ , Eppig JJ . 1990 . FSH-induced expansion of the mouse cumulus oophorus in vitro is dependent upon a specific factor(s) secreted by the oocyte . Dev Biol , 138 : 16 - 25 .

Cao Z , Li Y , Chen Z , Wang H , Zhang M , Zhou N , Wu R , Ling Y , Fang F , Li N , Zhang Y. 2015 . Genome-Wide Dynamic Profiling of Histone Methylation during Nuclear Transfer-Mediated Porcine Somatic Cell Reprogramming . PloS one , 10 : e0144897 .

Cao Z , Zhou N , Zhang Y , Wu R , Li Y , Li N. 2014 . Dynamic reprogramming of 5-hydroxymethylcytosine during early porcine embryogenesis . Theriogenology , 81 : 496 - 508 .

Chen J , Torcia S , Xie F , Lin CJ , Cakmak H , Franciosi F , Horner K , Onodera C , Song JS , Cedars MI , Ramalho-Santos M , Conti M . 2013 . Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes . Nat Cell Biol , 15 : 1415 - 1423 .

Coticchio G , Dal Canto M , Mignini Renzini M , Guglielmo MC , Brambillasca F , Turchi D , Novara PV , Fadini R . 2015 . Oocyte maturation: gamete-somatic cells interactions, meiotic resumption, cytoskeletal dynamics and cytoplasmic reorganization . Hum Reprod Update , 21 : 427 - 454 .

Dumollard R , Duchen M , Carroll J. 2007 . The role of mitochondrial function in the oocyte and embryo . Curr Top Dev Biol , 77 : 21 - 49 .

Fischer B , Bavister BD . 1993 . Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits . J Reprod Fertil , 99 : 673 - 679 .

Gilchrist RB , Thompson JG . 2007 . Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology , 67 : 6 - 15 .

Howe K , FitzHarris G. 2013 . Recent insights into spindle function in mammalian oocytes and early embryos . Biol Reprod , 89 : 1 - 9 .

Hu MW , Wang ZB , Teng Y , Jiang ZZ , Ma XS , Hou N , Cheng X , Schatten H , Xu X , Yang X , Sun QY . 2015 . Loss of protein phosphatase 6 in oocytes causes failure of meiosis II exit and impaired female fertility . J Cell Sci , 128 : 3769 - 3780 .

Huan Y , Xie B , Liu S , Kong Q , Liu Z. 2015 . A novel role for DNA methyltransferase 1 in regulating oocyte cytoplasmic maturation in pigs . PloS one , 10 : e0127512 .

Iwamoto M , Onishi A , Fuchimoto D , Somfai T , Takeda K , Tagami T , Hanada H , Noguchi J , Kaneko H , Nagai T , Kikuchi K. 2005 . Low oxygen tension during in vitro maturation of porcine follicular oocytes improves parthenogenetic activation and subsequent development to the blastocyst stage . Theriogenology , 63 : 1277 - 1289 .

Kang JT , Atikuzzaman M , Kwon DK , Park SJ , Kim SJ , Moon JH , Koo OJ , Jang G , Lee BC . 2012 . Developmental competence of porcine oocytes after in vitro maturation and in vitro culture under different oxygen concentrations . Zygote , 20 : 1 - 8 .

Kong Q , Xie B , Li J , Huan Y , Huang T , Wei R , Lv J , Liu S , Liu Z. 2014 . Identification and characterization of an oocyte factor required for porcine nuclear reprogramming . J Biol Chem , 289 : 6960 - 6968 .

Krisher RL . 2004 . The effect of oocyte quality on development . J Anim Sci , 82 ( E-Suppl ): E14 - 23 .

Li HK , Kuo TY , Yang HS , Chen LR , Li SS , Huang HW . 2008 . Differential gene expression of bone morphogenetic protein 15 and growth differentiation factor 9 during in vitro maturation of porcine oocytes and early embryos . Anim Reprod Sci , 103 : 312 - 322 .

Lonergan P , Rizos D , Gutierrez-Adan A , Fair T , Boland MP . 2003 . Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns . Reprod Domest Anim , 38 : 259 - 267 .

MacLennan M , Crichton JH , Playfoot CJ , Adams IR . 2015 . Oocyte development, meiosis and aneuploidy . Semin Cell Dev Biol , 45 : 68 - 76 .

McNatty KP , Smith P , Moore LG , Reader K , Lun S , Hanrahan JP , Groome NP , Laitinen M , Ritvos O , Juengel JL . 2005 . Oocyte-expressed genes affecting ovulation rate . Mol Cell Endocrinol , 234 : 57 - 66 .

Miyamoto K , Nagai K , Kitamura N , Nishikawa T , Ikegami H , Binh NT , Tsukamoto S , Matsumoto M , Tsukiyama T , Minami N , Yamada M , Ariga H , Miyake M , Kawarasaki T , Matsumoto K , Imai H . 2011 . Identification and characterization of an oocyte factor required for development of porcine nuclear transfer embryos . Proc Natl Acad Sci U S A , 108 : 7040 - 7045 .

Park JI , Hong JY , Yong HY , Hwang WS , Lim JM , Lee ES . 2005 . High oxygen tension during in vitro oocyte maturation improves in vitro development of porcine oocytes after fertilization . Anim Reprod Sci , 87 : 133 - 141 .

Pocar P , Brevini TA , Perazzoli F , Cillo F , Modina S , Gandolfi F . 2001 . Cellular and molecular mechanisms mediating the effects of polychlorinated biphenyls on oocyte developmental competence in cattle . Mol Reprod Dev , 60 : 535 - 541 .

Roberts R , Franks S , Hardy K. 2002 . Culture environment modulates maturation and metabolism of human oocytes . Hum Reprod , 17 : 2950 - 2956 .

Sha W , Xu BZ , Li M , Liu D , Feng HL , Sun QY . 2010 . Effect of gonadotropins on oocyte maturation in vitro: an animal model . Fertil Steril , 93 : 1650 - 1661 .

Sun QY , Nagai T . 2003 . Molecular mechanisms underlying pig oocyte maturation and fertilization . J Reprod Dev , 49 : 347 - 359 .

Sun QY , Wu GM , Lai L , Park KW , Cabot R , Cheong HT , Day BN , Prather RS , Schatten H . 2001 . Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction , 122 : 155 - 163 .

Swain JE . 2010 . Optimizing the culture environment in the IVF laboratory: impact of pH and buffer capacity on gamete and embryo quality . Reprod Biomed Online , 21 : 6 - 16 .

Tarkowski AK , Wroblewska J . 1967 . Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage . J Embryol Exp Morphol , 18 : 155 - 180 .

Torner H , Brussow KP , Alm H , Ratky J , Pohland R , Tuchscherer A , Kanitz W . 2004 . Mitochondrial aggregation patterns and activity in porcine oocytes and apoptosis in surrounding cumulus cells depends on the stage of pre-ovulatory maturation . Theriogenology , 61 : 1675 - 1689 .

Vajta G , Holm P , Greve T , Callesen H. 1997 . The submarine incubation system, a new tool for in vitro embryo culture: a technique report . Theriogenology , 48 : 1379 - 1385 .

Van Blerkom J , Runner MN . 1984 . Mitochondrial reorganization during resumption of arrested meiosis in the mouse oocyte . Am J Anat , 171 : 335 - 355 .

Wang Q , Sun QY . 2007 . Evaluation of oocyte quality: morphological, cellular and molecular predictors . Reprod Ferti Dev , 19 : 1 - 12 .

Watson AJ . 2007 . Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence . J Anim Sci , 85 : E1 - 3 .

Wessel GM , Conner SD , Berg L . 2002 . Cortical granule translocation is microfilament mediated and linked to meiotic maturation in the sea urchin oocyte . Development , 129 : 4315 - 4325 .

Wrenzycki C , Stinshoff H. 2013 . Maturation environment and impact on subsequent developmental competence of bovine oocytes . Reprod Domest Anim , 48 ( Suppl 1 ): 38 - 43 .

Yan C , Wang P , DeMayo J , DeMayo FJ , Elvin JA , Carino C , Prasad SV , Skinner SS , Dunbar BS , Dube JL , Celeste AJ , Matzuk MM . 2001 . Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function . Mol Endocrinol , 15 : 854 - 866 .

Yang CR , Miao DQ , Zhang QH , Guo L , Tong JS , Wei Y , Huang X , Hou Y , Schatten H , Liu Z , Sun QY . 2010 . Short-term preservation of porcine oocytes in ambient temperature: novel approaches . PloS one , 5 : e14242 .

Zhang X , Miao Y , Zhao JG , Spate L , Bennett MW , Murphy CN , Schatten H , Prather RS . 2010 . Porcine oocytes denuded before maturation can develop to the blastocyst stage if provided a cumulous cell-derived coculture system . J Anim Sci , 88 : 2604 - 2610 .

Zheng Z , Zhao MH , Jia JL , Heo YT , Cui XS , Oh JS , Kim NH . 2013 . Knockdown of maternal homeobox transcription factor SEBOX gene impaired early embryonic development in porcine parthenotes . J Reprod Dev , 59 : 557 - 562 .

 

 

 

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