Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-23T14:58:29.703Z Has data issue: false hasContentIssue false

Analysis of Heterogeneous Mitochondria Distribution in Somatic Cell Nuclear Transfer Porcine Embryos

Published online by Cambridge University Press:  16 September 2008

Zhisheng Zhong
Affiliation:
Department of Veterinary Pathobiology, University of Missouri-Columbia, Columbia, MO 65211, USA
Yanhong Hao
Affiliation:
Division of Animal Science, University of Missouri-Columbia, Columbia, MO 65211, USA
Rongfeng Li
Affiliation:
Division of Animal Science, University of Missouri-Columbia, Columbia, MO 65211, USA
Lee Spate
Affiliation:
Division of Animal Science, University of Missouri-Columbia, Columbia, MO 65211, USA
David Wax
Affiliation:
Division of Animal Science, University of Missouri-Columbia, Columbia, MO 65211, USA
Qing-Yuan Sun
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, P.R. China
Randall S. Prather
Affiliation:
Division of Animal Science, University of Missouri-Columbia, Columbia, MO 65211, USA
Heide Schatten*
Affiliation:
Department of Veterinary Pathobiology, University of Missouri-Columbia, Columbia, MO 65211, USA
*
Corresponding author. E-mail: [email protected]
Get access

Abstract

We previously reported that translocation of mitochondria from the oocyte cortex to the perinuclear area indicates positive developmental potential that was reduced in porcine somatic cell nuclear transfer (SCNT) embryos compared to in vitro–fertilized (IVF) embryos (Katayama, M., Zhong, Z.-S., Lai, L., Sutovsky, P., Prather, R.S. & Schatten, H. (2006). Dev Biol299, 206–220.). The present study is focused on distribution of donor cell mitochondria in intraspecies (pig oocytes; pig fetal fibroblast cells) and interspecies (pig oocytes; mouse fibroblast cells) reconstructed embryos by using either pig fibroblasts with mitochondria-stained MitoTracker CMXRos or YFP-mitochondria 3T3 cells (pPhi-Yellow-mito) as donor cells. Transmission electron microscopy was employed for ultrastructural analysis of pig oocyte and donor cell mitochondria. Our results revealed donor cell mitochondrial clusters around the donor nucleus that gradually dispersed into the ooplasm at 3 h after SCNT. Donor-derived mitochondria distributed into daughter blastomeres equally (82.8%) or unequally (17.2%) at first cleavage. Mitochondrial morphology was clearly different between donor cells and oocytes in which various complex shapes and configurations were seen. These data indicate that (1) unequal donor cell mitochondria distribution is observed in 17.2% of embryos, which may negatively influence development; and (2) complex mitochondrial morphologies are observed in IVF and SCNT embryos, which may influence mitochondrial translocation and affect development.

Type
Biological Applications
Copyright
Copyright © Microscopy Society of America 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abeydeera, L.R., Wang, W.H., Prather, R.S. & Day, B.N. (1998). Maturation in vitro of pig oocytes in protein-free culture media: Fertilization and subsequent embryo development in vitro. Biol Reprod 58, 13161320.CrossRefGoogle ScholarPubMed
Au, H.-K., Yeh, T.-S., Kao, S.-H., Tzeng, C.-R. & Hsieh, R.-H. (2005). Abnormal mitochondrial structure in human unfertilized oocytes and arrested embryos. Ann NY Acad Sci 1042, 177185.CrossRefGoogle ScholarPubMed
Calarco, P.G. (1995). Polarization of mitochondria in the unfertilized mouse oocytes. Dev Genet 16, 3646.CrossRefGoogle Scholar
Calarco, P.G. & McLaren, A. (1976). Ultrastructural observations of preimplantation stages of the sheep. J Embryol Exp Morph 36, 609622.Google ScholarPubMed
Chen, D-Y., Wen, D-C., Zhang, Y-P., Sun, Q-Y., Han, Z-M., Liu, Z-H., Shi, P., Li, J-S., Xiangyu, J-G., Lian, L., Kou, Z-H., Wu, Y-Q., Chen, Y-C., Wang, P-Y. & Zhang, H-M. (2002). Interspecies implantation and mitochondria fate of panda-rabbit cloned embryos. Biol Repro 67, 637642.CrossRefGoogle ScholarPubMed
Cran, D.G. (1985). Qualitative and quantitative structural changes during pig oocyte maturation. J Reprod Fertil (Suppl) 38, 4962.Google Scholar
Ferreira, C.R., Meirelles, F.V., Yamazaki, W., Chiaratti, M.R., Méo, S.C., Perecin, F., Smith, L.C. & Garcia, J.M. (2007). The kinetics of donor cell mtDNA in embryonic and somatic donor cell-derived bovine embryos. Cloning Stem Cells 9(4), 618629.CrossRefGoogle ScholarPubMed
Han, Y.-M., Abeydeera, L.R., Kim, J.-H., Moon, H.-B., Cabot, R.A., Day, B.N. & Prather, R.S. (1999a). Growth retardation of inner cell mass cells in polyspermic porcine embryos produced in vitro. Biol Reprod 60, 11101113.CrossRefGoogle ScholarPubMed
Han, Y.M., Wang, W.H., Abeydeera, L.R., Petersen, A.L., Kim, J.H., Murphy, C., Day, B.N. & Prather, R.S. (1999b). Pronuclear localization before the first cell division determines ploidy of polyspermic pig embryos. Biol Reprod 61, 13401346.CrossRefGoogle Scholar
Hao, Y., Lai, L., Mao, J., Im, G.-S., Bonk, A. & Prather, R. (2003). Apoptosis and in vitro development of preimplantation porcine embryos derived in vitro or by nuclear transfer. Biol Reprod 69, 501507.CrossRefGoogle ScholarPubMed
Hiendleder, S., Prelle, K., Brüggerhoff, K., Reichenack, H.-D., Wenigerkind, H., Bebbere, D., Stojkoviv, M., Müller, S., Brem, G., Zakhartchenko, V. & Wolf, E. (2004). Nuclear-cytoplasmic interactions affect in utero developmental capacity, phenotype, and cellular metabolism of bovine nuclear transfer fetuses. Biol Reprod 70, 11961205.CrossRefGoogle ScholarPubMed
Katayama, M., Zhong, Z.-S., Lai, L., Sutovsky, P., Prather, R.S. & Schatten, H. (2006). Mitochondria distribution and microtubule organization in fertilized and cloned porcine embryos: Implications for developmental potential. Dev Biol 299, 206220.CrossRefGoogle ScholarPubMed
Krause, W.J., Charlson, E.J., Sherman, D.M. & Day, B.N. (1992). Three-dimensional reconstruction using a computer graphics system: Application to mitochondrial aggregates in porcine oocytes, zygotes, and early embryos using a personal computer. Zool Anz 229, 2136.Google Scholar
Lai, L., Park, K.W., Cheong, H.T., Kühholzer, B., Samuel, M., Bonk, A., Im, G.S., Rieke, A., Day, B.N., Murphy, C.N., Carter, D.B. & Prather, R.S. (2002). Transgenic pig expressing the enhanced green fluorescent protein produced by nuclear transfer using colchicine-treated fibroblasts as donor cells. Mol Reprod Dev 62(3), 300306.CrossRefGoogle ScholarPubMed
Li, R., Lai, L., Wax, D., Hao, Y., Murphy, C.N., Rieke, A., Samuel, M., Linville, M.L., Korte, S.W., Evans, R.W., Turk, J.R., Kang, J.X., Witt, W.T., Dai, Y. & Prather, R.S. (2006). Cloned transgenic swine via in vitro production and cryopreservation. Biol Reprod 75, 226230.CrossRefGoogle ScholarPubMed
Murakami, M., Otoi, T., Wongsrikeao, P., Agung, B., Sambuu, R. & Suzuki, T. (2005). Development of interspecies cloned embryos in yak and dog. Cloning Stem Cells 7(2), 7781.CrossRefGoogle ScholarPubMed
Petters, R.M. & Wells, K.D. (1993). Culture of pig embryos. J Reprod Fertil Suppl 48, 6173.Google ScholarPubMed
Prather, R.S. (2007). Nuclear remodeling and nuclear reprogramming for making transgenic pigs by nuclear transfer. In Somatic Cell Nuclear Transfer, Sutovsky, P. (Ed.), Landes Bioscience. Adv Exp Med Biol 591, 113.CrossRefGoogle Scholar
Prather, R.S., Hawley, R.J., Carter, D.B., Lai, L. & Greenstein, J.L. (2003). Transgenic swine for biomedicine and agriculture. Theriogenol 59, 115123.CrossRefGoogle ScholarPubMed
Schatten, H., Prather, R.S. & Sun, Q.-Y. (2005). The significance of mitochondria for embryo development in cloned farm animals. Mitochondrion 5, 303321.CrossRefGoogle ScholarPubMed
Schatten, H., Ripple, M., Balczon, R., Weindruch, R. & Taylor, M. (2000a). Androgen and taxol cause cell type specific alterations of centrosome and DNA organization in androgen-responsive LNCaP and androgen-independent prostate cancer cells. J Cell Biochem 76, 463477.3.0.CO;2-S>CrossRefGoogle Scholar
Schatten, H. & Ris, H. (2002). Unconventional specimen preparation techniques using high resolution low voltage field emission scanning electron microscopy to study cell motility, host cell invasion, and internal structures in Toxoplasma gondii. Microsc Microanal 8, 94103.CrossRefGoogle ScholarPubMed
Schatten, H. & Ris, H. (2004). Three-dimensional imaging of Toxoplasma gondii—Host cell membrane interactions. Microsc Microanal 10, 580585.CrossRefGoogle Scholar
Schatten, H., Wiedemeier, A., Taylor, M., Lubahn, D., Greenberg, M.N., Besch-Williford, C., Rosenfeld, C., Day, K. & Ripple, M. (2000b). Centrosome-centriole abnormalities are markers for abnormal cell divisions and cancer in the transgenic adenocarcinoma mouse prostate (TRAMP) model. Biol Cell 92, 331340.CrossRefGoogle ScholarPubMed
Senger, P.L. & Saacke, R.G. (1970). Unusual mitochondria of the bovine oocyte. J Cell Biol 46, 405408.CrossRefGoogle ScholarPubMed
Squirrell, J.M., Lane, M. & Bavister, B.D. (2001). Altering intracellular pH disrupts development and cellular organization in preimplantation hamster embryos. Biol Reprod 64, 18451854.CrossRefGoogle ScholarPubMed
Squirrell, J.M., Schramm, R.D., Paprocki, M., Wokosin, D.L. & Bavister, B.D. (2003). Imaging mitochondrial organization in living primate oocytes and embryos using multiphoton microscopy. Microsc Microanal 9, 190201.CrossRefGoogle ScholarPubMed
Squirrell, J.M., Wokosin, D.L., Bavister, B.D. & White, J.G. (1999). Long-term multiphoton fluorescence imaging of mammalian embryos does not compromise viability. Nature Biotechn 17, 763767.CrossRefGoogle Scholar
Steinborn, R., Schinogl, P., Wells, D.N., Bergthaler, A., Müller, M. & Brem, G. (2002). Coexistence of Bos taurus and B. indicus mitochondrial DNA in nuclear transfer-derived somatic cattle clones. Genetics 162, 823829.CrossRefGoogle Scholar
Steinborn, R., Schinogl, P., Zakhartchenko, V., Achmann, R., Schernthaner, W., Stojkovic, M., Wolf, E., Müller, M. & Brem, G. (2000). Mitochondrial DNA heteroplasmy in cloned cattle produced by fetal and adult cell cloning. Nature Gen 25, 255257.CrossRefGoogle ScholarPubMed
St. John, J.C., Lloyd, R.E.I., Bowles, E.J., Thomas, E.C. & Shourbagy, S.E. (2004). The consequences of nuclear transfer for mammalian foetal development and offspring survival. A mitochondrial DNA perspective. Reproduction 127, 631641.CrossRefGoogle ScholarPubMed
Sun, Q.-Y, Wu, G.M., Lai, L., Park, K.W., Day, B., Prather, R.S. & Schatten, H. (2001). Translocation of active mitochondria during porcine oocyte maturation, fertilization and early embryo development in vitro. Reproduc 122, 155163.CrossRefGoogle ScholarPubMed
Sutovsky, P. (2004). Degradation of paternal mitochondria after fertilization: Implications for heteroplasmy, assisted reproductive technologies and mtDNA inheritance. Reprod Bio Med 8, 2433.Google ScholarPubMed
Sutovsky, P., McCauley, T.C., Sutovsky, M. & Day, B.N. (2003). Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG 132. Biol Reprod 68, 17931800.CrossRefGoogle Scholar
Sutovsky, P., Moreno, R.D., Ramalho-Santos, J., Dominko, T., Simerly, C. & Schatten, G. (1999). Ubiquitin tag for sperm mitochondria. Nature 402, 371372.CrossRefGoogle ScholarPubMed
Szöllösi, D. (1972). Changes of some cell organelles during oogenesis in mammals. In Oogenesis, Biggars, J.D. & Schuetz, A.W. (Ed.), pp. 4764. Baltimore, MD: University Press.Google Scholar
Takeda, K., Tasai, M., Iwamoto, M., Akita, T., Tagami, T., Nirasawa, K., Hanada, H. & Onishi, A. (2006). Transmission of mitochondrial DNA in pigs and progeny derived from nuclear transfer of Meishan pig fibroblast cells. Mol Repro Dev 73, 306312.CrossRefGoogle ScholarPubMed
Uhm, S.J., Gupta, M.K., Kim, T. & Lee, H.T. (2007). Expression of enhanced green fluorescent protein in porcine- and bovine-cloned embryos following interspecies somatic cell nuclear transfer of fibroblasts transfected by retrovirus vector. Mol Repro Dev 74, 15381547.CrossRefGoogle ScholarPubMed
Ullmann, S.L. & Butcher, L. (1996). Mammalian oocyte organelles with special reference to pleomorphic mitochondria and vacuole formation in marsupials. Reprod Fertil Dev 8, 491508.CrossRefGoogle ScholarPubMed
Van Blerkom, J., Davis, P. & Alexander, S. (2000). Differential mitochondrial distribution in human pronuclear embryos leads to disproportionate inheritance between blastomeres: Relationship to microtubular organization, ATP content and competence. Human Reproduction 15, 26212633.CrossRefGoogle ScholarPubMed
Van Blerkom, J., Davis, P. & Lee, J. (1995). ATP content of human oocytes and developmental potential and outcome after in vitro fertilization and embryo transfer. Human Reproduction 10, 415424.CrossRefGoogle ScholarPubMed
Zhong, Z., Spate, L., Hao, Y., Li, R., Lai, L., Katayama, M., Sun, Q.Y., Prather, R.S. & Schatten, H. (2007). Remodeling of centrosomes in intraspecies and interspecies nuclear transfer porcine embryos. Cell Cycle 6(12), 15101521.CrossRefGoogle ScholarPubMed
Zhong, Z.-S., Zhang, G., Meng, X.-Q., Zhang, Y.-L., Chen, D.-Y., Schatten, H. & Sun, Q.-Y. (2005). Function of donor cell centrosome in intraspecies and interspecies nuclear transfer embryos. Exp Cell Res 306, 3546.CrossRefGoogle ScholarPubMed