Effect of exogenous DMNPE-caged ATP on in vitro-matured bovine oocytes prior to parthenogenetic activation, fertilisation and nuclear transfer
Jun Xue A B , Melissa A. Cooney A B , Vanessa J. Hall A B , Natasha A. Korfiatis A B , R. Tayfur Tecirlioglu A B , Andrew J. French A B and Nancy T. Ruddock A B CA Monash Institute of Reproduction and Development, Monash University, 27–31 Wright Street, Clayton, Vic. 3168, Australia.
B Cooperative Research Centre for Innovative Dairy Products, Melbourne, Vic. 3000, Australia.
C Corresponding author. Email: nancy.ruddock@med.monash.edu.au
Reproduction, Fertility and Development 16(8) 781-786 https://doi.org/10.1071/RD04055
Submitted: 1 June 2004 Accepted: 14 November 2004 Published: 13 January 2005
Abstract
Adenosine triphosphate (ATP) plays an important role during fertilisation of the mammalian oocyte through its ability to alter the frequency and duration of calcium oscillations. It has also been shown that higher ATP levels correlate with increased developmental competence in bovine and human oocytes. During somatic cell nuclear transfer (NT), the incoming nucleus is remodelled extensively, undoubtedly using a variety of ATP-dependent enzymes. The aim of the present study was to determine whether additional exogenous ATP influences activation of parthenogenetic (PA), in vitro-fertilised (IVF) or cloned (NT) in vitro-matured bovine oocytes. Blastocyst development and cell numbers in PA embryos were found to increase in a dose-dependent manner following the photorelease of 0, 50, 100, 500 and 1000 μm DMNPE-caged ATP (adenosine 5′-triphosphate, P3-(1-(4,5-dimethoxy-2-nitrophenyl)ethyl) ester, disodium salt). No cleavage was found following release of 2 and 5 mm DMNPE-caged ATP or with DMNPE-caged ATP (not photoreleased). There were also no differences in blastocyst rates or cell numbers between the control group and groups treated with caged, but not photoreleased, ATP. The addition of exogenous ATP before IVF or to NT couplets did not result in a significant increase in blastocyst development or cell number. Embryo transfer is necessary to determine whether exogenous ATP can positively affect reprogramming, resulting in higher cloned pregnancy rates or live-term births.
Extra keyword: in vitro fertilisation.
Acknowledgments
The authors gratefully acknowledge the support of The Cooperative Research Centre (CRC) for Innovative Dairy Products. The authors also thank Drs Wendy Dean and Justin St John as well as Mr George Thouas for their valuable input and discussion. We appreciate the assistance of Genetics Australia Co-operative Ltd, Bacchus Marsh, Victoria, for oocyte supply and animal care and Dr Garey Dawson and laboratory staff (Southern Cross Pathology Australia, Monash Medical Centre, Southern Health, Clayton, Victoria) for cytogenetic analyses.
Ammini, C. V. , and Hauswirth, W. W. (1999). Mitochondrial gene expression is regulated at the level of transcription during early embryogenesis of Xenopus laevis. J. Biol. Chem. 274, 6265–6271.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Brad, A. M. , Bormann, C. L. , Swain, J. E. , Durkin, R. E. , Johnson, A. E. , Clifford, A. L. , and Krisher, R. L. (2003). Glutathione and adenosine triphosphate content of in vivo and in vitro matured porcine oocytes. Mol. Reprod. Dev. 64, 492–498.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chi, M. M. , Manchester, J. K. , Yang, V. C. , Curato, A. D. , Strickler, R. C. , and Lowry, O. H. (1988). Contrast in the levels of metabolic enzymes in human and mouse ova. Biol. Reprod. 39, 295–307.
| PubMed |
Cummins, J. M. (2001). Cytoplasmic inheritance and its implications for animal biotechnology. Theriogenology 55, 1381–1399.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Daniels, R. , Hall, V. J. , French, A. J. , Korfiatis, N. A. , and Trounson, A. O. (2001). Comparison of gene transcription in cloned bovine embryos produced by different nuclear transfer techniques. Mol. Reprod. Dev. 60, 281–288.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dumollard, R. , Hammar, K. , Porterfield, M. , Smith, P. J. , Cibert, C. , Rouviere, C. , and Sardet, C. (2003). Mitochondrial respiration and Ca2+ waves are linked during fertilization and meiosis completion. Development 130, 683–692.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fissore, R. A. , Kurokawa, M. , Knott, J. , Zhang, M. , and Smyth, J. (2002). Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction 124, 745–754.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Håkelien, A.-M. , Landsverk, H. B. , Robl, J. M. , Skålhegg, B. S. , and Collas, P. (2002). Reprogramming fibroblasts to express T-cell functions using cell extracts. Nat. Biotechnol. 20, 460–466.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hall, V. J. , Korfiatis, N. A. , Lewis, I. M. , Trounson, A. O. , and French, A. J. (2001). The effect of FGF4 addition on IVP bovine embryo development. Soc. Reprod. Biol. 32, 49.
Hewitson, L. , Simerly, C. , Dominko, T. , and Schatten, G. (2000). Cellular and molecular events after in vitro fertilization and intracytoplasmic sperm injection. Theriogenology 53, 95–104.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Holm, P. , Booth, P. J. , Schmidt, M. H. , Greve, T. , and Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum proteins. Theriogenology 52, 683–700.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Leese, H. J. (1991). Metabolism of the preimplantation mammalian embryo. Oxf. Rev. Reprod. Biol. 13, 35–72.
| PubMed |
Liu, L. , Hammar, K. , Smith, P. J. S. , Inoue, S. , and Keefe, D. L. (2001). Mitochondrial modulation of signaling at the initiation of development. Cell Calcium 30, 423–433.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mak, D.-O. D. , McBride, S. , and Foskett, J. K. (1999). ATP regulation of type I inositol 1,4,5-triphosphate receptor channel gating by allosteric tuning of Ca2+ activation. J. Biol. Chem. 274, 22 231–22 237.
| Crossref | GoogleScholarGoogle Scholar |
Reynier, P. , May-Panloup, P. , Chretien, M. F. , Morgan, C. J. , Jean, M. , Savagner, F. , Barriere, P. , and Malthiery, Y. (2001). Mitochondrial DNA content affects the fertilizability of human oocytes. Mol. Hum. Reprod. 7, 425–429.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rieger, D. (1997). Batch analysis of the ATP content of bovine sperm, oocytes, and early embryos using a scintillation counter to measure the chemiluminescence produced by the luciferin-luciferase reaction. Anal. Biochem. 246, 67–70.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Saunders, C. M. , Larman, M. G. , Parrington, J. , Cox, L. J. , Royse, J. , Blayney, L. M. , Swann, K. , and Lai, F. A. (2002). PLCζ: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129, 3533–3544.
| PubMed |
Shepard, A. , and Borejdo, J. (2004). Correlation between mechanical and enzymatic events in contracting skeletal muscle fiber. Biochemistry 43, 2804–2811.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stojkovic, M. , Machado, S. A. , Stojkovic, P. , Zakhartchenko, V. , Hutzler, P. , Gonzalves, 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 fertilization and culture. Biol. Reprod. 64, 904–909.
| PubMed |
Sutovsky, P. , and Schatten, G. (2000). Paternal contributions to the mammalian zygote: fertilization after sperm–egg fusion. Int. Rev. Cytol. 195, 1–65.
| PubMed |
Tecirlioglu, R. T. , French, A. J. , Lewis, I. M. , Vajta, G. , Korfiatis, N. A. , Hall, V. J. , Ruddock, N. T. , Cooney, M. A. , and Trounson, A. O. (2003). Birth of a cloned calf derived from a vitrified hand-made (HMC) embryo. Reprod. Fertil. Dev. 15, 361–366.
| Crossref | GoogleScholarGoogle Scholar |
Thompson, J. G. (2000). In vitro culture and embryo metabolism of cattle and sheep embryos: a decade of achievement. Anim. Reprod. Sci. 60–61, 263–275.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Thouas, G. A. , Korfiatis, N. A. , French, A. J. , Jones, G. M. , and Trounson, A. O. (2001). Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod. BioMed. Online 3, 25–29.
| PubMed |
Trimarchi, J. R. , Liu, L. , Porterfield, D. M. , Smith, P. J. S. , and Keefe, D. L. (2000). Oxidative phosphorylation-dependent and -independent oxygen consumption by individual preimplantation mouse embryos. Biol. Reprod. 62, 1866–1874.
| PubMed |
Van Blerkom, J. , Davis, P. , and Lee, J. (1995). ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum. Reprod. 10, 415–424.
| PubMed |
Van Blerkom, J. , Davis, P. , and Alexander, S. (2003). Inner mitochondrial membrane potential (ΔΨm), cytoplasmic ATP content and free Ca2+ levels in metaphase II mouse oocytes. Hum. Reprod. 18, 2429–2440.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
