Ultrastructure and mitochondrial numbers in pre- and postpubertal pig oocytes
Hanne Skovsgaard Pedersen A E , Henrik Callesen A , Peter Løvendahl B , Fenghua Chen C , Jens Randel Nyengaard C , Nanett Kvist Nikolaisen D , Peter Holm D and Poul Hyttel DA Department of Animal Science, Aarhus University, Blichers Allé 20, DK-8830 Tjele, Denmark.
B Department of Molecular Biology and Genetics, Aarhus University, Blichers Allé 20, DK-8830 Tjele, Denmark.
C Stereology and Electron Microscopy Laboratory, Centre for Stochastic Geometry and Advanced Bioimaging, Aarhus University, Nørrebrogade 44, DK-8000 Aarhus C, Denmark.
D Department of Veterinary Clinical and Animal Science, University of Copenhagen, Dyrlægevej 16, DK-1870 Frederiksberg C, Denmark.
E Corresponding author. Email: hanne.skovsgaard@agrsci.dk
Reproduction, Fertility and Development 28(5) 586-598 https://doi.org/10.1071/RD14220
Submitted: 19 June 2014 Accepted: 19 August 2014 Published: 25 September 2014
Abstract
Prepubertal pig oocytes are associated with lower developmental competence. The aim of this experiment was to conduct an exhaustive survey of oocyte ultrastructure and to use a design-unbiased stereological approach to quantify the numerical density and total number of mitochondria in oocytes with different diameters from pre- and postpubertal pigs. The ultrastructure of smaller prepubertal immature oocytes indicated active cells in close contact with cumulus cells. The postpubertal oocytes were more quiescent cell types. The small prepubertal oocytes had a lower total mitochondrial number, but no differences were observed in mitochondrial densities between groups. Mature postpubertal oocytes adhered to the following characteristics: presence of metaphase II, lack of contact between cumulus cells and oocyte, absence of rough endoplasmic reticulum and Golgi complexes, peripheral location of cortical granules and central localisation of mitochondria, vesicles and lipid droplets. Prepubertal oocytes displayed more variation. The ultrastructure of large pre- and postpubertal oocytes was compatible with higher developmental competence, whereas that of smaller prepubertal oocytes could explain their reduced capacity. The higher number of mitochondria in large pre- and postpubertal oocytes could have an influence on oocyte competence, by increasing the pool of mitochondria available for early embryonic development.
Additional keywords: mitochondria, oocyte quality, stereology, transmission electron microscopy.
References
Al-Mashhadi, R. H., Sørensen, C. B., Kragh, P. M., Christoffersen, C., Mortensen, M. B., Tolbod, L. P., Thim, T., Du, Y., Li, J., and Liu, Y. (2013). Familial hypercholesterolemia and atherosclerosis in cloned minipigs created by DNA transposition of a human PCSK9 gain-of-function mutant. Science Translational Medicine 5, 166ra1.| Familial hypercholesterolemia and atherosclerosis in cloned minipigs created by DNA transposition of a human PCSK9 gain-of-function mutant.Crossref | GoogleScholarGoogle Scholar | 23283366PubMed |
Bagg, M. A., Vassena, R., Papasso-Brambilla, E., Grupen, C. G., Armstrong, D. T., and Gandolfi, F. (2004). Changes in ovarian, follicular and oocyte morphology immediately after the onset of puberty are not accompanied by an increase in oocyte developmental competence in the pig. Theriogenology 62, 1003–1011.
| Changes in ovarian, follicular and oocyte morphology immediately after the onset of puberty are not accompanied by an increase in oocyte developmental competence in the pig.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2czos1CrsA%3D%3D&md5=00585a9c7f37c13e8c9bbbe959cb58beCAS | 15289043PubMed |
Bagg, M. A., Nottle, M. B., Armstrong, D. T., and Grupen, C. G. (2007). Relationship between follicle size and oocyte developmental competence in prepubertal and adult pigs. Reprod. Fertil. Dev. 19, 797–803.
| Relationship between follicle size and oocyte developmental competence in prepubertal and adult pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVWhtrzN&md5=2b788f96fba86cf4ceab3a9a58ddd9afCAS | 17897582PubMed |
Bavister, B. D., and Squirrell, J. M. (2000). Mitochondrial distribution and function in oocytes and early embryos. Hum. Reprod. 15, 189–198.
| Mitochondrial distribution and function in oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar | 11041524PubMed |
Brevini, T. A. L., Vassena, R., Francisci, C., and 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.
| Role of adenosine triphosphate, active mitochondria and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslSntrc%3D&md5=592ca1e16a62ed71ecc86d4c3d95722aCAS |
Cotterill, M., Harris, S. E., Fernandez, E. C., Lu, J., Huntriss, J. D., Campbell, B. K., and Picton, H. M. (2013). The activity and copy number of mitochondrial DNA in ovine oocytes throughout oogenesis in vivo and during oocyte maturation in vitro. Mol. Hum. Reprod. 19, 444–450.
| The activity and copy number of mitochondrial DNA in ovine oocytes throughout oogenesis in vivo and during oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVCqurfP&md5=83c0ff882f100661f2396a96c24ff9cdCAS | 23468533PubMed |
Cran, D. G. (1985). Qualitative and quantitative structural changes during pig oocyte maturation. J. Reprod. Fertil. 74, 237–245.
| Qualitative and quantitative structural changes during pig oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXks1GhsLs%3D&md5=e6114739f1149c071190a77a27d2fc54CAS | 4020770PubMed |
Cran, D. G., and Cheng, W. T. K. (1985). Changes in cortical granules during porcine oocyte maturation. Gamete Res. 11, 311–319.
| Changes in cortical granules during porcine oocyte maturation.Crossref | GoogleScholarGoogle Scholar |
Crozet, N., Motlik, J., and Szollosi, D. (1981). Nucleolar fine structure and RNA synthesis in porcine oocytes during the early stages of antrum formation. Biol. Cell 41, 35–42.
| 1:CAS:528:DyaL3MXlt1Olsrs%3D&md5=786ab50786104e630d2b5711dc2169f2CAS |
Cummins, J. M. (2001). Epigenetic and experimental modifications in early mammalian development: part I: mitochondria: potential roles in embryogenesis and nucleocytoplasmic transfer. Hum. Reprod. Update 7, 217–228.
| Epigenetic and experimental modifications in early mammalian development: part I: mitochondria: potential roles in embryogenesis and nucleocytoplasmic transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisFymsL8%3D&md5=e03d433dee67ced75bc48b8bcc921251CAS | 11284664PubMed |
Eisele, J. C., Schaefer, I. M., Nyengaard, J. R., Post, H., Liebetanz, D., Brüel, A., and Mühlfeld, C. (2008). Effect of voluntary exercise on number and volume of cardiomyocytes and their mitochondria in the mouse left ventricle. Basic Res. Cardiol. 103, 12–21.
| Effect of voluntary exercise on number and volume of cardiomyocytes and their mitochondria in the mouse left ventricle.Crossref | GoogleScholarGoogle Scholar | 18004633PubMed |
El Shourbagy, S. H., Spikings, E. C., Freitas, M., and St John, J. C. (2006). Mitochondria directly influence fertilisation outcome in the pig. Reproduction 131, 233–245.
| Mitochondria directly influence fertilisation outcome in the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFalsL4%3D&md5=f0457ff7daef9cacf24b578829b3d4e2CAS | 16452717PubMed |
Endo, M., Kimura, K., Kuwayama, T., Monji, Y., and Iwata, H. (2012). Effect of oestradiol during culture of bovine oocyte–granulosa cell complexes on the mitochondrial DNA copies of oocytes and telomere length of granulosa cells. Zygote 12, 1–9.
| Effect of oestradiol during culture of bovine oocyte–granulosa cell complexes on the mitochondrial DNA copies of oocytes and telomere length of granulosa cells.Crossref | GoogleScholarGoogle Scholar |
Fair, T., Hyttel, P., Greve, T., and Boland, M. (1996). Nucleus structure and transcriptional activity in relation to oocyte diameter in cattle. Mol. Reprod. Dev. 43, 503–512.
| Nucleus structure and transcriptional activity in relation to oocyte diameter in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitVGjsL8%3D&md5=5d653b8f79b66f5ac57c167ff0d30b62CAS | 9052942PubMed |
Fair, T., Hulshof, S. C. J., Hyttel, P., Greve, T., and Boland, M. (1997). Oocyte ultrastructure in bovine primordial to early tertiary follicles. Anat. Embryol. (Berl.) 195, 327–336.
| Oocyte ultrastructure in bovine primordial to early tertiary follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3mtFOrtg%3D%3D&md5=aa13b101791b48d8151b54b781836c6eCAS | 9108198PubMed |
Gomes, L. C., Benedetto, G. D., and Scorrano, L. (2011). During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 13, 589–598.
| During autophagy mitochondria elongate, are spared from degradation and sustain cell viability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsFGmurc%3D&md5=bab054656e2d0e93a04e0fae9f575f5dCAS | 21478857PubMed |
Grupen, C. G., McIlfatrick, S. M., Ashman, R. J., Boquest, A. C., Armstrong, D. T., and Nottle, M. B. (2003). Relationship between donor animal age, follicular fluid steroid content and oocyte developmental competence in the pig. Reprod. Fertil. Dev. 15, 81–87.
| Relationship between donor animal age, follicular fluid steroid content and oocyte developmental competence in the pig.Crossref | GoogleScholarGoogle Scholar | 12895404PubMed |
Gundersen, H. J. G. (1988). The nucleator. J. Microsc. 151, 3–21.
| The nucleator.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M%2FlsFOqsg%3D%3D&md5=30274cc4598ea881055c622a81991055CAS |
Gundersen, H. J. G., and Jensen, E. B. (1987). The efficiency of systematic sampling in stereology and its prediction. J. Microsc. 147, 229–263.
| The efficiency of systematic sampling in stereology and its prediction.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c7hvVyltA%3D%3D&md5=3da1533b2ccfb7598bdfba92900e0433CAS |
Gundersen, H. J. G., Bagger, P., Bendtsen, T. F., Evans, S. M., Korbo, L., Marcussen, N., Møller, A., Nielsen, K., Nyengaard, J. R., and Pakkenberg, B. (1988). The new stereological tools: disector, fractionator, nucleator and point-sampled intercepts and their use in pathological research and diagnosis. APMIS 96, 857–881.
| The new stereological tools: disector, fractionator, nucleator and point-sampled intercepts and their use in pathological research and diagnosis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M%2FltVKitA%3D%3D&md5=ba12a89f3eeea40aa6b8329d127cd4b2CAS |
Gupta, M. K., Uhm, S. J., and Lee, H. T. (2008). Sexual maturity and reproductive phase of oocyte donor influence the developmental ability and apoptosis of cloned and parthenogenetic porcine embryos. Anim. Reprod. Sci. 108, 107–121.
| Sexual maturity and reproductive phase of oocyte donor influence the developmental ability and apoptosis of cloned and parthenogenetic porcine embryos.Crossref | GoogleScholarGoogle Scholar | 17869033PubMed |
Homa, S. T., Carroll, J., and Swann, K. (1993). Fertilisation and early embryology: the role of calcium in mammalian oocyte maturation and egg activation. Hum. Reprod. 8, 1274–1281.
| 1:STN:280:DyaK2c%2FhtlemtA%3D%3D&md5=eeddbe391dc7d533b159f18a9fd73ecbCAS | 8408526PubMed |
Hunter, M. G. (2000). Oocyte maturation and ovum quality in pigs. Rev. Reprod. 5, 122–130.
| Oocyte maturation and ovum quality in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsleiu7k%3D&md5=949b173fb745a6b5c3108b852815cb03CAS | 10864857PubMed |
Hyttel, P., and Madsen, I. (1987). Rapid method to prepare mammalian oocytes and embryos for transmission electron microscopy. Acta Anat. (Basel) 129, 12–14.
| Rapid method to prepare mammalian oocytes and embryos for transmission electron microscopy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s3psFSjsA%3D%3D&md5=b48f3da56977bb717277bc358c14e807CAS | 3618092PubMed |
Hyttel, P., Callesen, H., and Greve, T. (1986a). Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. J. Reprod. Fertil. 76, 645–656.
| Ultrastructural features of preovulatory oocyte maturation in superovulated cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL287pvFyrtQ%3D%3D&md5=f498e05ee3506d5187fafeb02bc16e55CAS | 3084771PubMed |
Hyttel, P., Xu, K. P., Smith, S., and Greve, T. (1986b). Ultrastructure of in vitro oocyte maturation in cattle. J. Reprod. Fertil. 78, 615–625.
| Ultrastructure of in vitro oocyte maturation in cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s7ht1equg%3D%3D&md5=9fdb4142278b2841aaed1902f2bf4d63CAS | 3806520PubMed |
Hyttel, P., Fair, T., Callesen, H., and Greve, T. (1997). Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47, 23–32.
| Oocyte growth, capacitation and final maturation in cattle.Crossref | GoogleScholarGoogle Scholar |
Ikeda, K., and Takahashi, Y. (2003). Comparison of maturational and developmental parameters of oocytes recovered from prepubertal and adult pigs. Reprod. Fertil. Dev. 15, 215–221.
| Comparison of maturational and developmental parameters of oocytes recovered from prepubertal and adult pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntV2msLc%3D&md5=e46238f2d7502ac208d1a147a928f16bCAS | 12921696PubMed |
Iwata, H., Goto, H., Tanaka, H., Sakaguchi, Y., Kimura, K., Kuwayama, T., and Monji, Y. (2011). Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod. Fertil. Dev. 23, 424–432.
| Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjt12nt7s%3D&md5=20070ec4ad3390158e2aba4099fe27f1CAS | 21426860PubMed |
Kacinskis, M. Á., Lucci, C. M., Luque, M. C. A., and Báo, S. N. (2005). Morphometric and ultrastructural characterization of Bos indicus preantral follicles. Anim. Reprod. Sci. 87, 45–57.
| Morphometric and ultrastructural characterization of Bos indicus preantral follicles.Crossref | GoogleScholarGoogle Scholar | 15885440PubMed |
Kim, J., You, J., Hyun, S. H., Lee, G., Lim, J., and Lee, E. (2010). Developmental competence of morphologically poor oocytes in relation to follicular size and oocyte diameter in the pig. Mol. Reprod. Dev. 77, 330–339.
| 1:CAS:528:DC%2BC3cXisFemtrY%3D&md5=f7e0cdd818a5439f3ce98002edec7dffCAS | 20029826PubMed |
Kruip, T. A. M., Cran, D. G., Van Beneden, T. H., and Dieleman, S. J. (1983). Structural changes in bovine oocytes during final maturation in vivo. Gamete Res. 8, 29–47.
| Structural changes in bovine oocytes during final maturation in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlvVyisLc%3D&md5=05dc9456cce4c4433ad5010691c38cd1CAS |
Lee, H. C., and Wei, Y. H. (2005). Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress. Int. J. Biochem. Cell Biol. 37, 822–834.
| Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVKisbw%3D&md5=072123e7ad2194528a946923aeebd1a6CAS | 15694841PubMed |
Li, J., Pedersen, H. S., Li, R., Adamsen, J., Liu, Y., Schmidt, M., Purup, S., and Callesen, H. (2014). Developmental potential of pig embryos reconstructed by use of sow versus pre-pubertal gilt oocytes after somatic cell nuclear transfer. Zygote 22, 356–365.
| 23331714PubMed |
Lucas, X., Martinez, E. A., Roca, J., Vazquez, J. M., Gil, M. A., Pastor, L. M., and Alabart, J. L. (2002). Relationship between antral follicle size, oocyte diameters and nuclear maturation of immature oocytes in pigs. Theriogenology 58, 871–885.
| Relationship between antral follicle size, oocyte diameters and nuclear maturation of immature oocytes in pigs.Crossref | GoogleScholarGoogle Scholar |
Luo, Y., Li, J., Liu, Y., Lin, L., Du, Y., Li, S., Yang, H., Vajta, G., Callesen, H., Bolund, L., and Sørensen, C. B. (2011). High efficiency of BRCA1 knockout using rAAV-mediated gene targeting: developing a pig model for breast cancer. Transgenic Res. 20, 975–988.
| High efficiency of BRCA1 knockout using rAAV-mediated gene targeting: developing a pig model for breast cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFKrt7%2FL&md5=1c3fe6319836c2a5c4d8620e8578442aCAS | 21181439PubMed |
Marchal, R., Feugang, J. M., Perreau, C., Venturi, E., Terqui, M., and Mermillod, P. (2001). Meiotic and developmental competence of prepubertal and adult swine oocytes. Theriogenology 56, 17–29.
| Meiotic and developmental competence of prepubertal and adult swine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlslaktro%3D&md5=7f31dd269e66bb17c9581f0a129e53aaCAS | 11467513PubMed |
Marchal, R., Vigneron, C., Perreau, C., Bali-Papp, A., and Mermillod, P. (2002). Effect of follicular size on meiotic and developmental competence of porcine oocytes. Theriogenology 57, 1523–1532.
| Effect of follicular size on meiotic and developmental competence of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zhtFykug%3D%3D&md5=f85cf371ecb0b233e6b7a5763e279715CAS | 12054210PubMed |
May-Panloup, P., Chretién, M., Malthiery, Y., and Reynier, P. (2007). Mitochondrial DNA in the oocyte and the developing embryo. Curr. Top. Dev. Biol. 77, 51–83.
| Mitochondrial DNA in the oocyte and the developing embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1Gltbw%3D&md5=3cb245a25fe94091b056b23608e280a1CAS | 17222700PubMed |
Motlik, J., Crozet, N., and Fulka, J. (1984). Meiotic competence in vitro of pig oocytes isolated from early antral follicles. J. Reprod. Fertil. 72, 323–328.
| Meiotic competence in vitro of pig oocytes isolated from early antral follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M%2Fot1yitg%3D%3D&md5=e737cfc49619330190dcd1c34a127df0CAS | 6392543PubMed |
Müller-Höcker, J., Schäfer, S., Weis, S., Münscher, C., and Strowitzki, T. (1996). Morphological–cytochemical and molecular genetic analyses of mitochondria in isolated human oocytes in the reproductive age. Mol. Hum. Reprod. 2, 951–958.
| Morphological–cytochemical and molecular genetic analyses of mitochondria in isolated human oocytes in the reproductive age.Crossref | GoogleScholarGoogle Scholar | 9237239PubMed |
Nyengaard, J. R. (1999). Steriological methods and their application in kidney research. J. Am. Soc. Nephrol. 10, 1100–1123.
| 1:STN:280:DyaK1M3kslKmug%3D%3D&md5=ba4f30654383fb47817cca953d439387CAS | 10232698PubMed |
O’Brien, J. K., Dwarte, D., Ryan, J. P., Maxwell, W. M. C., and Evans, G. (2000). Comparison of in vitro maturation, in vitro fertilisation, metabolism and ultrastructure of oocytes from prepubertal and adult pigs. Reprod. Domest. Anim. 35, 101–107.
| Comparison of in vitro maturation, in vitro fertilisation, metabolism and ultrastructure of oocytes from prepubertal and adult pigs.Crossref | GoogleScholarGoogle Scholar |
Pawlak, P., Cieslak, A., Warzych, E., Zejden, Z., Szumacher-Strabel, M., Molinska-Glura, M., and Lechniak, D. (2012). No single way to explain cytoplasmic maturation of oocytes from prepubertal and cyclic gilts. Theriogenology 78, 2020–2030.
| No single way to explain cytoplasmic maturation of oocytes from prepubertal and cyclic gilts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFSltrbK&md5=7bb14d30c1cd4438a57abffb6cf35c26CAS | 23043949PubMed |
Pedersen, H. S., Løvendahl, P., Nikolaisen, N. K., Holm, P., Hyttel, P., Nyengaard, J. R., Chen, F., and Callesen, H. (2014). Mitochondrial dynamics in pre- and post-pubertal pig oocytes before and after in vitro maturation. Reprod. Fertil. Dev. 26, 189–190.
| Mitochondrial dynamics in pre- and post-pubertal pig oocytes before and after in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvV2mur3J&md5=4da18fe823e675256eb01c2ab243fc9dCAS |
Pedersen, H. S., Løvendahl, P., Larsen, K., Madsen, L. B., and Callesen, H. (2014). mtDNA copy number in oocytes of different sizes from individual pre- and post-pubertal pigs. Reprod. Fertil. Dev. , .
Petr, J., Rozinek, J., Hruban, V., Jílek, F., Sedmíková, M., Vanourková, Z., and Nemecek, Z. (2001). Ultrastructural localisation of calcium deposits during in vitro culture of pig oocytes. Mol. Reprod. Dev. 58, 196–204.
| Ultrastructural localisation of calcium deposits during in vitro culture of pig oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjslOiuw%3D%3D&md5=d867a97196092da8f95c87b6b6d7dc96CAS | 11139232PubMed |
Pikó, L., and Matsumoto, L. (1976). Number of mitochondria and some properties of mitochondrial DNA in the mouse egg. Dev. Biol. 49, 1–10.
| Number of mitochondria and some properties of mitochondrial DNA in the mouse egg.Crossref | GoogleScholarGoogle Scholar | 943339PubMed |
Rambold, A. S., Kostelecky, B., and Lippincott-Schwartz, J. (2011). Together we are stronger. Fusion protects mitochondria from autophagosomal degradation. Autophagy 7, 1568–1569.
| Together we are stronger. Fusion protects mitochondria from autophagosomal degradation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xks1ygsbs%3D&md5=4a99bfe9a40811fed82e8b3cb038ffceCAS | 22024745PubMed |
Reader, K. L., Cox, N. R., Stanton, J. L., and Juengel, J. L. (2014). Mitochondria and vesicles differ between adult and prepubertal sheep oocytes during IVM. Reprod. Fertil. Dev. , .
| Mitochondria and vesicles differ between adult and prepubertal sheep oocytes during IVM.Crossref | GoogleScholarGoogle Scholar | 25155366PubMed |
Reynier, P., May-Panloup, P., Chrétien, M. F., Morgan, C. J., Jean, M., Savagner, F., Barrière, P., and Malthièry, Y. (2001). Mitochondrial DNA content affects the fertilisability of human oocytes. Mol. Hum. Reprod. 7, 425–429.
| Mitochondrial DNA content affects the fertilisability of human oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1CqsLg%3D&md5=d992edf173ed21a2847ca52be9e660caCAS | 11331664PubMed |
Rube, D. A., and Van der Bliek, M. (2004). Mitochondrial morphology is dynamic and varied. Mol. Cell. Biochem. 256-257, 331–339.
| Mitochondrial morphology is dynamic and varied.Crossref | GoogleScholarGoogle Scholar |
Shoubridge, E. A., and Wai, T. (2007). Mitochondrial DNA and the mammalian oocyte. Curr. Top. Dev. Biol. 77, 87–111.
| Mitochondrial DNA and the mammalian oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1Gltbo%3D&md5=a09ddf3fff46478c618e646e90a97f7bCAS | 17222701PubMed |
Spikings, E. C., Alderson, J., and John, J. C. S. (2007). Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development. Biol. Reprod. 76, 327–335.
| Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFWqtLs%3D&md5=0f25b8f56ab93bc97019011eacb1cf48CAS | 17035641PubMed |
Sterio, D. C. (1984). The unbiased estimation of number and sizes of arbitrary particles using the disector. J. Microsc. 134, 127–136.
| The unbiased estimation of number and sizes of arbitrary particles using the disector.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c3kt1yjtw%3D%3D&md5=abe673c2704ac89396b17215728722f0CAS | 6737468PubMed |
Stojkovic, M., Machado, S. A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Goncalves, P. B., and Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilisation and culture. Biol. Reprod. 64, 904–909.
| Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilisation and culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsVKjtrk%3D&md5=0d1a08b5bcdd8b3387833fe9afb4cda4CAS | 11207207PubMed |
Sun, Q. Y., Wu, G. M., Lai, L., Park, K. W., Cabot, R., Cheong, H. T., Day, B. N., Prather, R. S., and Schatten, H. (2001). Translocation of active mitochondria during pig oocyte maturation, fertilisation and early embryo development in vitro. Reproduction 122, 155–163.
| Translocation of active mitochondria during pig oocyte maturation, fertilisation and early embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVGis7g%3D&md5=f53b1a86b5042ba936eb70f04c388dd1CAS | 11425340PubMed |
Sun, M. G., Williams, J., Munoz-Pinedo, C., Perkins, G. A., Brown, J. M., Ellisman, M. H., Green, D. R., and Frey, T. G. (2007). Correlated three-dimensional light and electron microscopy reveals transformation of mitochondria during apoptosis. Nat. Cell Biol. 9, 1057–1065.
| Correlated three-dimensional light and electron microscopy reveals transformation of mitochondria during apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpslGju70%3D&md5=dc84348c6ce478c7d4dc0348dd06bebbCAS | 17721514PubMed |
Torner, H., Brüssow, K. P., Alm, H., Ratky, J., Pöhland, R., Tuchscherer, A., and 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.
| Mitochondrial aggregation patterns and activity in porcine oocytes and apoptosis in surrounding cumulus cells depends on the stage of pre-ovulatory maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhslWnu70%3D&md5=e7eb594309d6256c41190aad9a44d127CAS | 15019463PubMed |
Wang, W. H., Sun, Q. Y., Hosoe, M., Shioya, Y., and Day, B. N. (1997). Quantified analysis of cortical granule distribution and exocytosis of porcine oocytes during meiotic maturation and activation. Biol. Reprod. 56, 1376–1382.
| Quantified analysis of cortical granule distribution and exocytosis of porcine oocytes during meiotic maturation and activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtlGrtbY%3D&md5=5d992fc9ae67ada13ba94c7c121d0841CAS | 9166688PubMed |
Yaffe, M. P. (1999). Dynamic mitochondria. Nat. Cell Biol. 1, E149–E150.
| Dynamic mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvVersLY%3D&md5=f7a077b53685a6e91a1e92b757276302CAS | 10559975PubMed |
Youle, R. J., and Van der Bliek, A. M. (2012). Mitochondrial fission, fusion and stress. Science 337, 1062–1065.
| Mitochondrial fission, fusion and stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Grtr7L&md5=85a9df5b622bdc3ec7d6938ac77724cdCAS | 22936770PubMed |
Zeng, H. T., Ren, Z., Yeung, W. S., Shu, Y. M., Xu, Y. W., Zhuang, G. L., and Liang, X. Y. (2007). Low mitochondrial DNA and ATP contents contribute to the absence of birefringent spindle imaged with PolScope in in vitro-matured human oocytes. Hum. Reprod. 22, 1681–1686.
| Low mitochondrial DNA and ATP contents contribute to the absence of birefringent spindle imaged with PolScope in in vitro-matured human oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1ejtL0%3D&md5=6ce6e465347f40947ac47c9481cd1fd6CAS | 17449512PubMed |
Zick, M., Rabl, R., and Reichert, A. S. (2009). Cristae formation – linking ultrastructure and function of mitochondria. Biochim. Biophys. Acta 1793, 5–19.
| Cristae formation – linking ultrastructure and function of mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVWrtL3F&md5=252c3b9a032ee23c3dc36e7b7c625db3CAS | 18620004PubMed |