Oxygen-Regulated Gene Expression in Bovine Blastocysts1
Abstract
Oxygen concentrations used during in vitro embryo culture can influence embryo development, cell numbers, and gene expression. Here we propose that the preimplantation bovine embryo possesses a molecular mechanism for the detection of, and response to, oxygen, mediated by a family of basic helix-loop-helix transcription factors, the hypoxia-inducible factors (HIFs). Day 5 compacting bovine embryos were cultured under different oxygen tensions (2%, 7%, 20%) and the effect on the expression of oxygen-regulated genes, development, and cell number allocation and HIFalpha protein localization were examined. Bovine in vitro-produced embryos responded to variations in oxygen concentration by altering gene expression. GLUT1 expression was higher following 2% oxygen culture compared with 7% and 20% cultured blastocysts. HIF mRNA expression (HIF1alpha, HIF2alpha) was unaltered by oxygen concentration. HIF2alpha protein was predominantly localized to the nucleus of blastocysts. In contrast, HIF1alpha protein was undetectable at any oxygen concentration or in the presence of the HIF protein stabilizer desferrioxamine (DFO), despite being detectable in cumulus cells following normal maturation conditions, acute anoxic culture, or in the presence of DFO. Oxygen concentration also significantly altered inner cell mass cell proportions at the blastocyst stage. These results suggest that oxygen can influence gene expression in the bovine embryo during postcompaction development and that these effects may be mediated by HIF2alpha.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Animal studies have confirmed that HIFs are expressed at the blastocyst stage of development and are essential for normal placental development.
“Animal studies have confirmed that HIFs are expressed at the blastocyst stage of development (243), and that they are essential for normal placental development.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [243]
Cites
Wang, G. L., Jiang, B. H., Rue, E. A., & Semenza, G. L. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.12.5510 · Cited by 6,212 · see citing works
Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene
Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O’Shea, K. S., Powell-Braxton, L., Hillan, K. J., & Moore, M. W. (1996) · Nature · doi:10.1038/380439a0 · Cited by 3,624 · see citing works
A conserved family of prolyl-4-hydroxylases that modify HIF
Bruick, R. K., & McKnight, S. L. (2001) · Science · doi:10.1126/science.1066373 · Cited by 2,549 · see citing works
Cellular and developmental control of O <sub>2</sub> homeostasis by hypoxia-inducible factor 1α
Iyer, N. V., Kotch, L. E., Agani, F., Leung, S. W., Laughner, E., Wenger, R. H., Gassmann, M., Gearhart, J. D., Lawler, A. M., Yu, A. Y., et al. (1998) · Genes & Development · doi:10.1101/gad.12.2.149 · Cited by 2,476 · see citing works
Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1.
Semenza, G., Roth, P. H., Fang, H. M., & Wang, G. L. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)31580-6 · Cited by 1,892 · see citing works
Molecular and Biological Properties of the Vascular Endothelial Growth Factor Family of Proteins
Ferrara, N., Houck, K. A., Jakeman, L. B., & LEUNG, D. W. (1992) · Endocrine Reviews · doi:10.1210/edrv-13-1-18 · Cited by 1,655 · see citing works
HIF‐1α is required for solid tumor formation and embryonic vascularization
Ryan, H. E., Lo, J., & Johnson, R. S. (1998) · The EMBO Journal · doi:10.1093/emboj/17.11.3005 · Cited by 1,579 · see citing works
Asparagine Hydroxylation of the HIF Transactivation Domain: A Hypoxic Switch
Lando, D., Peet, D. J., Whelan, D. A., Gorman, J. J., & Whitelaw, M. L. (2002) · Science · doi:10.1126/science.1068592 · Cited by 1,558 · see citing works
Guerin, P. J. (2001) · Human Reproduction Update · doi:10.1093/humupd/7.2.175 · Cited by 1,419 · see citing works
HIF-1 and mechanisms of hypoxia sensing
Semenza, G. L. (2001) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(00)00194-0 · Cited by 1,267 · see citing works
Jiang, B. H., Semenza, G. L., Bauer, C., & Marti, H. H. (1996) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1996.271.4.c1172 · Cited by 1,213 · see citing works
Hypoxia-inducible factor 1: master regulator of O2 homeostasis
Semenza, G. L. (1998) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(98)80016-6 · Cited by 1,092 · see citing works
SUCCESSFUL CULTURE IN VITRO OF SHEEP AND CATTLE OVA
Tervit, H. R., Whittingham, D. G., & ROWSON, L. E. A. (1972) · Reproduction · doi:10.1530/jrf.0.0300493 · Cited by 1,008 · see citing works
Signal transduction to hypoxia-inducible factor 1
Semenza, G. L. (2002) · Biochemical Pharmacology · doi:10.1016/s0006-2952(02)01168-1 · Cited by 860 · see citing works
Differential Transcriptional Regulation of the Two Vascular Endothelial Growth Factor Receptor Genes
Gerber, H.-P., Condorelli, F., Park, J., & Ferrara, N. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.38.23659 · Cited by 794 · see citing works
Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits
Fischer, B. M., & Bavister, B. D. (1993) · Reproduction · doi:10.1530/jrf.0.0990673 · Cited by 775 · see citing works
Wang, G., & Semenza, G. (1993) · Blood · doi:10.1182/blood.v82.12.3610.3610 · Cited by 766 · see citing works
Widespread, hypoxia‐inducible expression of HIF‐2α in distinct cell populations of different organs
Wiesener, M. S., Jürgensen, J. S., Rosenberger, C., Scholze, C. K., Hörstrup, J. H., Warnecke, C., Mandriota, S. J., Bechmann, I., Frei, U. A., Pugh, C. W., et al. (2002) · The FASEB Journal · doi:10.1096/fj.02-0445fje · Cited by 741 · see citing works
Stroka, D., Burkhardt, T., Desbaillets, I., Wenger, R. H., Neil, D., Bauer, C., GASSMANN, M., & Candinas, D. (2001) · The FASEB Journal · doi:10.1096/fj.01-0125com · Cited by 716 · see citing works
Caniggia, I., Mostachfi, H., Winter, J., Gassmann, M., Lye, S. J., Kuliszewski, M., & Post, M. (2000) · Journal of Clinical Investigation · doi:10.1172/jci8316 · Cited by 644 · see citing works
Wiesener, M. S., Turley, H., Allen, W. E., Willam, C., Eckardt, K., Talks, K., Wood, S. M., Gatter, K. C., Harris, A. L., Pugh, C. W., et al. (1998) · Blood · doi:10.1182/blood.v92.7.2260 · Cited by 629 · see citing works
Gu, Y.-Z., Moran, S. M., Hogenesch, J. B., Wartman, L. D., & Bradfield, C. A. (1998) · Europe PMC (PubMed Central) · Cited by 577 · see citing works
Niemann, H. J., & Wrenzycki, C. (2000) · Theriogenology · doi:10.1016/s0093-691x(99)00237-x · Cited by 475 · see citing works
Zhong, H., & Simons, J. W. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.0815 · Cited by 473 · see citing works
Peng, J., Zhang, L., Drysdale, L., & Fong, G.-H. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.140087397 · Cited by 460 · cited 1× · see citing works
“5, developing severe vascular defects in both the yolk sac and embryo proper [32], suggesting that HIFs are regulators of critical developmental processes associated with normal postimplantation embryo development.”
BackgroundLazzari, G., Wrenzycki, C., Herrmann, D., Duchi, R., Kruip, T. A. M., Niemann, H., & Galli, C. (2002) · Biology of Reproduction · doi:10.1095/biolreprod.102.004481 · Cited by 401 · see citing works
Protection against tissue damage in vivo by desferrioxamine: What is its mechanism of action?
Halliwell, B. B. (1989) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(89)90145-7 · Cited by 378 · see citing works
Johnson, M. H., & Nasr‐Esfahani, M. H. (1994) · BioEssays · doi:10.1002/bies.950160105 · Cited by 342 · see citing works
Oxygen uptake and carbohydrate metabolism by in vitro derived bovine embryos
Thompson, J. G., Partridge, R. J., Houghton, F. D., Cox, C. I., & Leese, H. J. (1996) · Reproduction · doi:10.1530/jrf.0.1060299 · Cited by 333 · see citing works
Self-citationREDOX regulation of early embryo development
Harvey, A. J., Kind, K. L., & Thompson, J. G. (2002) · Reproduction · doi:10.1530/rep.0.1230479 · Cited by 332 · see citing works
Self-citationWrenzycki, C., Herrmann, D., Keskintepe, L., Martins, A., Sirisathien, S., Brackett, B. G., & Niemann, H. J. (2001) · Human Reproduction · doi:10.1093/humrep/16.5.893 · Cited by 328 · see citing works
Effect of oxygen concentration on in-vitro development of preimplantation sheep and cattle embryos
Thompson, J. G., Simpson, A. C., Pugh, P. A., Donnelly, P. E., & Tervit, H. R. (1990) · Reproduction · doi:10.1530/jrf.0.0890573 · Cited by 323 · see citing works
Self-citationElvert, G., Kappel, A., Heidenreich, R., Englmeier, U., Lanz, S., Acker, T., Rauter, M., Plate, K. H., Sieweke, M. H., Breier, G., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211298200 · Cited by 272 · see citing works
Role of Prolyl Hydroxylation in Oncogenically Stabilized Hypoxia-inducible Factor-1α
Chan, D. A., Sutphin, P. D., Denko, N. C., & Giaccia, A. J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206922200 · Cited by 264 · see citing works
The hypoxia-inducible factors: key transcriptional regulators of hypoxic responses
Bracken, C. P., Whitelaw, M. L., & Peet, D. J. (2003) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-003-2370-y · Cited by 255 · see citing works
Effects of oxygen toxicity on early development of mouse embryos
Umaoka, Y., Noda, Y., Narimoto, K., & Mori, T. (1992) · Molecular Reproduction and Development · doi:10.1002/mrd.1080310106 · Cited by 223 · see citing works
Granulocyte–macrophage colony-stimulating factor promotes human blastocyst development in vitro
Sjöblom, C., Wikland, M., & Robertson, S. A. (1999) · Human Reproduction · doi:10.1093/humrep/14.12.3069 · Cited by 209 · see citing works
Bertolini, M., Mason, J. B., Beam, S. W., Carneiro, G. F., Sween, M. L., Kominek, D. J., Moyer, A. L., Famula, T. R., Sainz, R. D., & Anderson, G. B. (2002) · Theriogenology · doi:10.1016/s0093-691x(02)00935-4 · Cited by 204 · see citing works
Thompson, J. G., Mcnaughton, C., Gasparrini, B., McGowan, L., & Tervit, H. (2000) · Reproduction · doi:10.1530/reprod/118.1.47 · Cited by 192 · see citing works
Self-citationSoom, A. V., Boerjan, M. L., Bols, P. E. J., Vanroose, G., Lein, A., Coryn, M., & de Kruif, A. (1997) · Biology of Reproduction · doi:10.1095/biolreprod57.5.1041 · Cited by 188 · see citing works
Dibbens, J. A., Miller, D. L., Damert, A., Risau, W., Vadas, M. A., & Goodall, G. J. (1999) · Molecular Biology of the Cell · doi:10.1091/mbc.10.4.907 · Cited by 179 · see citing works
Pabon, J. E., Findley, W. E., & Gibbons, W. E. (1989) · Fertility and Sterility · doi:10.1016/s0015-0282(16)60688-x · Cited by 178 · see citing works
Khurana, N. K., & Niemann, H. J. (2000) · Theriogenology · doi:10.1016/s0093-691x(00)00387-3 · Cited by 168 · see citing works
Similarities and differences between the vascular endothelial growth factor (VEGF) splice variants
Neufeld, G., Cohen, T., Gitay-Goren, H., Gluzman‐Poltorak, Z., Tessler, S., Sharon, R., Gengrinovitch, S., & Levi, B.-Z. (1996) · Cancer and Metastasis Reviews · doi:10.1007/bf00437467 · Cited by 164 · see citing works
Batt, P. A., Gardner, D. K., & Cameron, A. (1991) · Reproduction Fertility and Development · doi:10.1071/rd9910601 · Cited by 151 · see citing works
Human assisted conception: a cautionary tale. Lessons from domestic animals
Leese, H. J., Donnay, I., & Thompson, J. G. (1998) · Human Reproduction · doi:10.1093/humrep/13.suppl_4.184 · Cited by 145 · see citing works
Self-citationHypoxia-inducible factor-1α is regulated at the post-mRNA level
Wenger, R. H., Kvietiko, I., Rolfs, A., Gassmann, M., & Marti, H. H. (1997) · Kidney International · doi:10.1038/ki.1997.79 · Cited by 139 · see citing works
Yaseen, M., Wrenzycki, C., Herrmann, D., Carnwath, J., & Niemann, H. J. (2001) · Reproduction · doi:10.1530/rep.0.1220601 · Cited by 117 · see citing works
Wrenzycki, C., Herrmann, D., Carnwath, J. W., & Niemann, H. J. (1998) · Reproduction · doi:10.1530/jrf.0.1120387 · Cited by 109 · see citing works
Vonnahme, K. A., Wilson, M. E., & Ford, S. P. (2001) · Biology of Reproduction · doi:10.1095/biolreprod64.6.1821 · Cited by 108 · see citing works
Scharte, M., Han, X., Bertges, D. J., Fink, M. P., & Delude, R. L. (2003) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00076.2002 · Cited by 89 · see citing works
Krüssel, J.-S. (2001) · Molecular Human Reproduction · doi:10.1093/molehr/7.1.57 · Cited by 76 · see citing works
Diabetes and Preimplantation Events of Embryogenesis
Moley, K. (1999) · Seminars in Reproductive Medicine · doi:10.1055/s-2007-1016221 · Cited by 69 · see citing works
Pantaleon, M., Ryan, J. P., Gil, M., & Kaye, P. L. (2001) · Biology of Reproduction · doi:10.1095/biolreprod64.4.1247 · Cited by 69 · see citing works
Self-citationDevelopment of one-cell ovine embryos in two culture media under two gas atmospheres
Betterbed, B., & Wright, R. W. (1985) · Theriogenology · doi:10.1016/0093-691x(85)90026-3 · Cited by 65 · see citing works
Byatt‐Smith, J. G. B., Leese, H. J., & Gosden, R. G. (1991) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a137258 · Cited by 59 · see citing works
Marti, H. H., Katschinski, D. M., Wagner, K. F., Schäffer, L., Stier, B., & Wenger, R. H. (2002) · Molecular Endocrinology · doi:10.1210/mend.16.2.0786 · Cited by 51 · see citing works
Bernardi, M. L., Fléchon, J. E., & Delouis, C. (1996) · Reproduction · doi:10.1530/jrf.0.1060161 · Cited by 51 · see citing works
Krüssel, J.-S., Behr, B. R., Hirchenhain, J., Wen, Y., Milki, A. A., Cupisti, S., Bielfeld, P., & Polan, M. L. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01581-8 · Cited by 43 · see citing works
Tscheudschilsuren, G., Aust, G., Nieber, K., Schilling, N., & Spanel‐Borowski, K. (2002) · Microvascular Research · doi:10.1006/mvre.2001.2346 · Cited by 33 · see citing works
Down-regulation of Hypoxia-inducible Factor-2 in PC12 Cells by Nerve Growth Factor Stimulation
Naranjo‐Suarez, S., Castellanos, M. C., Álvarez-Tejado, M., Vara, A., Landázuri, M. O., & del Peso, L. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304079200 · Cited by 33 · see citing works
Beneficial effects of culturing rabbit zygotes to blastocysts in 5% oxygen and 10% carbon dioxide
Farrell, P. B., & Foote, R. H. (1995) · Reproduction · doi:10.1530/jrf.0.1030127 · Cited by 26 · see citing works
Hara, S., Kobayashi, C., & Imura, N. (1999) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/s0167-4781(99)00048-2 · Cited by 19 · see citing works
Incorporation of glucose by the sheep conceptus between days 13 and 19 of pregnancy
Wales, R. G., Cuneo, C. L., & Waugh, E. (1989) · Reproduction Fertility and Development · doi:10.1071/rd9890137 · Cited by 10 · see citing works
Expression of VEGF-system mRNAs in mouse blastocysts is not affected by in vitro culture
Ingmann, S. C., Hirchenhain, J., Huse, I., Hess, A. P., Bielfeld, P., & Krüssel, J.-S. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03946-8 · Cited by 4 · see citing works
Wales, R. G., & Waugh, E. (1993) · Reproduction Fertility and Development · doi:10.1071/rd9930201 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The role of oxygen availability in embryonic development and stem cell function
Simon, M. C., & Keith, B. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2354 · Cited by 966 · see citing works
Covello, K. L., Kehler, J., Yu, H., Gordan, J. D., Arsham, A. M., Hu, C., Labosky, P. A., Simon, M. C., & Keith, B. (2006) · Genes & Development · doi:10.1101/gad.1399906 · Cited by 818 · see citing works
Low O 2 tensions and the prevention of differentiation of hES cells
Ezashi, T., Das, P., & Roberts, R. M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501283102 · Cited by 804 · see citing works
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
Mitochondrial Regulation of Cell Cycle and Proliferation
Arciuch, V. G. A., Elguero, M. E., Poderoso, J. J., & Carreras, M. C. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.4085 · Cited by 428 · see citing works
Forristal, C. E., Wright, K. L., Hanley, N. A., Oreffo, R. O. C., & Houghton, F. D. (2009) · Reproduction · doi:10.1530/rep-09-0300 · Cited by 396 · see citing works
Could oxidative stress influence the in-vitro maturation of oocytes?
Combelles, C. M. H., Gupta, S., & Agarwal, A. K. (2009) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)60038-7 · Cited by 314 · see citing works
Metabolism of the viable mammalian embryo: quietness revisited
Leese, H. J., Baumann, C. G., Brison, D. R., McEvoy, T. G., & Sturmey, R. G. (2008) · Molecular Human Reproduction · doi:10.1093/molehr/gan065 · Cited by 270 · see citing works
Lonergan, P., Fair, T., Corcoran, D., & Evans, A. C. O. (2005) · Theriogenology · doi:10.1016/j.theriogenology.2005.09.028 · Cited by 262 · see citing works
Oxidative Stress and Redox Regulation on In Vitro Development of Mammalian Embryos
Takahashi, M. (2012) · Journal of Reproduction and Development · doi:10.1262/jrd.11-138n · Cited by 255 · see citing works
Hypoxia and stem cell‐based engineering of mesenchymal tissues
Ma, T., Grayson, W. L., Fröhlich, M., & Vunjak‐Novakovic, G. (2009) · Biotechnology Progress · doi:10.1002/btpr.128 · Cited by 231 · see citing works
Effects of oxygen tension on gene expression in preimplantation mouse embryos
Rinaudo, P. F., Giritharan, G., Talbi, S., Dobson, A. T., & Schultz, R. M. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.05.017 · Cited by 210 · see citing works
Wrenzycki, C., Herrmann, D., Lucas‐Hahn, A., Korsawe, K., Lemme, E., & Niemann, H. (2004) · Reproduction Fertility and Development · doi:10.1071/rd04109 · Cited by 195 · see citing works
Meintjes, M., Chantilis, S. J., Douglas, J. D., Rodriguez, A. J., Guerami, A. R., Bookout, D. M., Barnett, B. D., & Madden, J. D. (2008) · Human Reproduction · doi:10.1093/humrep/den368 · Cited by 169 · see citing works
Modulation of neuronal stem cell differentiation by hypoxia and reactive oxygen species
Vieira, H. L. A., Alves, P. M., & Vercelli, A. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.01.007 · Cited by 165 · see citing works
Gardner, D. K., & Harvey, A. J. (2015) · Reproduction Fertility and Development · doi:10.1071/rd14421 · Cited by 162 · see citing works
Self-citationGardner, D. K. (2015) · BioEssays · doi:10.1002/bies.201400155 · Cited by 157 · see citing works
The Role of Hypoxia in Stem Cell Differentiation and Therapeutics
Abdollahi, H., Harris, L. J., Zhang, P., McIlhenny, S. E., Srinivas, V., Tulenko, T. N., & DiMuzio, P. J. (2009) · Journal of Surgical Research · doi:10.1016/j.jss.2009.09.057 · Cited by 157 · see citing works
Ex vivo early embryo development and effects on gene expression and imprinting
Gardner, D. K., & Lane, M. (2005) · Reproduction Fertility and Development · doi:10.1071/rd04103 · Cited by 150 · see citing works
Lonergan, T. A., Bavister, B. D., & Brenner, C. A. (2007) · Mitochondrion · doi:10.1016/j.mito.2007.05.002 · Cited by 143 · see citing works
Hardy, M. L. M., Day, M. L., & Morris, M. B. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph182111374 · Cited by 132 · see citing works
Permanent embryo arrest: molecular and cellular concepts
Betts, D. H., & Madan, P. (2008) · Molecular Human Reproduction · doi:10.1093/molehr/gan035 · Cited by 131 · see citing works
Hypoxia‐inducible factors in stem cells and cancer
Mazumdar, J., Dondeti, V. R., & Simon, M. C. (2009) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2009.00963.x · Cited by 127 · see citing works
Preimplantation embryo programming: transcription, epigenetics, and culture environment
Duranthon, V., Watson, A. J., & Lonergan, P. (2008) · Reproduction · doi:10.1530/rep-07-0324 · Cited by 123 · see citing works
The role of oxygen in ruminant preimplantation embryo development and metabolism
Harvey, A. J. (2006) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2006.10.008 · Cited by 123 · see citing works
Self-citationImpact of the IVF laboratory environment on human preimplantation embryo phenotype
Gardner, D. K., & Kelley, R. L. (2017) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174417000368 · Cited by 122 · see citing works
Identification of Oxygen-Sensitive Transcriptional Programs in Human Embryonic Stem Cells
Westfall, S. D., Sachdev, S., Das, P., Hearne, L. B., Hannink, M., Roberts, R. M., & Ezashi, T. (2008) · Stem Cells and Development · doi:10.1089/scd.2007.0240 · Cited by 121 · see citing works
Yang, W., Wang, P., Cao, P., Wang, S., Yang, Y., Huimin, S., & Nashun, B. (2021) · Epigenetics & Chromatin · doi:10.1186/s13072-021-00431-6 · Cited by 118 · see citing works
Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells
Blerkom, J. V. (2008) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)60463-4 · Cited by 117 · see citing works
The control of mtDNA replication during differentiation and development
John, J. C. S. (2013) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2013.10.036 · Cited by 113 · see citing works
Corrêa, G. A., Rumpf, R., Mundim, T. C. D., Franco, M. M., & Dode, M. A. N. (2007) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2007.02.002 · Cited by 104 · see citing works
Oxygen Regulation in Development: Lessons from Embryogenesis towards Tissue Engineering
Fathollahipour, S., Patil, P. S., & Leipzig, N. D. (2018) · Cells Tissues Organs · doi:10.1159/000493162 · Cited by 101 · see citing works
Lopes, A. S., Madsen, S. E., Ramsing, N. B., Løvendahl, P., Greve, T., & Callesen, H. (2006) · Human Reproduction · doi:10.1093/humrep/del404 · Cited by 98 · see citing works
Predictive factors for embryo implantation potential
Borini, A., Lagalla, C., Cattoli, M., Sereni, E., Sciajno, R., Flamigni, C., & Coticchio, G. (2005) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)61675-6 · Cited by 97 · see citing works
Feil, D., Lane, M., Roberts, C. T., Kelley, R. L., Edwards, L. J., Thompson, J. G., & Kind, K. L. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2005.102681 · Cited by 90 · see citing works
Self-citationBalasubramanian, S., Son, W. J., Kumar, B. M., Ock, S. A., Yoo, J. G., Im, G., Choe, S. Y., & Rho, G. (2007) · Theriogenology · doi:10.1016/j.theriogenology.2007.05.044 · Cited by 90 · see citing works
Lopes, A. S., Larsen, L. H., Ramsing, N. B., Løvendahl, P., Räty, M., Peippo, J., Greve, T., & Callesen, H. (2005) · Reproduction · doi:10.1530/rep.1.00703 · Cited by 89 · see citing works
Oxygen‐regulated expression of GLUT‐1, GLUT‐3, and VEGF in the mouse blastocyst
Kind, K. L., Collett, R. A., Harvey, A. J., & Thompson, J. G. (2004) · Molecular Reproduction and Development · doi:10.1002/mrd.20183 · Cited by 87 · see citing works
Self-citationGad, A. Y., Besenfelder, U., Rings, F., Ghanem, N., Salilew‐Wondim, D., Hossain, M. M., Tesfaye, D., Lonergan, P., Becker, A., Cinar, U., et al. (2011) · Human Reproduction · doi:10.1093/humrep/der110 · Cited by 87 · see citing works
Ciray, H. N., Aksoy, T., Yaramanci, K., Karayaka, I., & Bahçeci, M. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.07.1707 · Cited by 82 · see citing works
Factors influencing in vitro embryo production
Camargo, L. S. A., Viana, J. H. M., de Sa, W. F., Ferreira, A. M., Ramos, A. A., & Filho, V. R. V. (2006) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) · Cited by 81 · see citing works
Pluripotent Stem Cell Metabolism and Mitochondria: Beyond ATP
Lees, J. G., Gardner, D. K., & Harvey, A. J. (2017) · Stem Cells International · doi:10.1155/2017/2874283 · Cited by 80 · see citing works
Self-citationEmbryo catheter loading and embryo culture techniques: results of a worldwide web-based survey
Christianson, M. S., Zhao, Y., Shoham, G., Granot, I., Safran, A., Khafagy, A. M., Leong, M. K. H., & Shoham, Z. (2014) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-014-0250-z · Cited by 80 · see citing works
The embryonic stress response to in vitro culture: insight from genomic analysis
Cagnone, G., & Sirard, M. (2016) · Reproduction · doi:10.1530/rep-16-0391 · Cited by 75 · see citing works
Embryo Mitochondrial DNA Depletion Is Reversed During Early Embryogenesis in Cattle1
Chiaratti, M. R., Bressan, F. F., Ferreira, C. R., Caetano, A. R., Smith, L. C., Vercesi, A. E., & Meirelles, F. V. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.109.077776 · Cited by 73 · see citing works
Quantification of embryo quality by respirometry
Lopes, A. S., Greve, T., & Callesen, H. (2006) · Theriogenology · doi:10.1016/j.theriogenology.2006.09.026 · Cited by 71 · see citing works
The Preimplantation Embryo: Handle with Care
Watkins, A. J., Papenbrock, T., & Fleming, T. P. (2008) · Seminars in Reproductive Medicine · doi:10.1055/s-2008-1042956 · Cited by 61 · see citing works
Metaboloepigenetic Regulation of Pluripotent Stem Cells
Harvey, A. J., Rathjen, J., & Gardner, D. K. (2015) · Stem Cells International · doi:10.1155/2016/1816525 · Cited by 61 · see citing works
Self-citationOxygen concentration and preimplantation development
Bavister, B. D. (2004) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)61630-6 · Cited by 60 · see citing works
IVF/ICSI outcomes after culture of human embryos at low oxygen tension: a meta-analysis
Sobrinho, D. B. G., Oliveira, J. B. A., Petersen, C. G., Mauri, A. L., Silva, L. F., Massaro, F. C., Baruffi, R. L. R., Cavagna, M., & Franco, J. G., Jr. (2011) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-9-143 · Cited by 59 · see citing works
Essential role of glucose transporter GLUT3 for post-implantation embryonic development
Schmidt, S., Hommel, A., Gawlik, V., Augustin, R., Junicke, N., Florian, S., Richter, M., Walther, D. J., Montag, D., Joost, H., et al. (2008) · Journal of Endocrinology · doi:10.1677/joe-08-0262 · Cited by 59 · see citing works
Short-term exposure to hydrogen peroxide during oocyte maturation improves bovine embryo development
Vandaele, L., Thys, M., Bijttebier, J., Langendonckt, A. V., Donnay, I., Maes, D., Meyer, E., & Soom, A. V. (2009) · Reproduction · doi:10.1530/rep-09-0430 · Cited by 58 · see citing works
Hiendleder, S., Zakhartchenko, V., & Wolf, E. (2004) · Reproduction Fertility and Development · doi:10.1071/rd04115 · Cited by 58 · see citing works
Ma, Y.-Y., Chen, H., & Tzeng, C. (2017) · Journal of Ovarian Research · doi:10.1186/s13048-017-0344-1 · Cited by 57 · see citing works
Lapointe, J., Kimmins, S., MacLaren, L. A., & Bilodeau, J. (2005) · Endocrinology · doi:10.1210/en.2004-1373 · Cited by 56 · see citing works
Lopes, A. S., Wrenzycki, C., Ramsing, N. B., Herrmann, D., Niemann, H., Løvendahl, P., Greve, T., & Callesen, H. (2007) · Theriogenology · doi:10.1016/j.theriogenology.2007.04.055 · Cited by 54 · see citing works
Kelley, R. L., & Gardner, D. K. (2017) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2017.02.001 · Cited by 52 · see citing works
Developmental assessment of human vitrified-warmed blastocysts based on oxygen consumption
Yamanaka, M., Hashimoto, S., Amo, A., Ito‐Sasaki, T., Abé, H., & Morimoto, Y. (2011) · Human Reproduction · doi:10.1093/humrep/der324 · Cited by 51 · see citing works
Oxygen tension affects histone remodeling of in vitro–produced embryos in a bovine model
Gaspar, R. C., Arnold, D. R., Corrêa, C. A. P., da Rocha, C. V., Penteado, J. C. T., del Collado, M., Vantini, R., Garcia, J. M., & Lopes, F. L. (2015) · Theriogenology · doi:10.1016/j.theriogenology.2015.01.002 · Cited by 50 · see citing works
Reactive oxygen species in reproduction: harmful, essential or both?
Jamil, M., Debbarh, H., Aboulmaouahib, S., Filali, O. A., Mounaji, K., Zarqaoui, M., Saadani, B., Louanjli, N., & Cadi, R. (2020) · Zygote · doi:10.1017/s0967199420000179 · Cited by 50 · see citing works
Podkalicka, P., Stępniewski, J., Mucha, O., Kachamakova‐Trojanowska, N., Dulak, J., & Łoboda, A. (2020) · Biomolecules · doi:10.3390/biom10121614 · Cited by 49 · see citing works
Differential expression of oxygen‐regulated genes in bovine blastocysts
Harvey, A. J., Santos, A. N., Kirstein, M., Kind, K. L., Fischer, B., & Thompson, J. G. (2006) · Molecular Reproduction and Development · doi:10.1002/mrd.20617 · Cited by 47 · see citing works
Self-citationThompson, J. G. (2006) · Journal of Reproduction and Development · doi:10.1262/jrd.17089 · Cited by 46 · see citing works
Self-citationPost‐hatching development of in vitro bovine embryos from day 7 to 14 in vivo versus in vitro
Machado, G. M., Ferreira, A. R., Pivato, I., Fidelis, A. A. G., Sprícigo, J. F. W., Paulini, F., Lucci, C. M., Franco, M. M., & Dode, M. A. N. (2013) · Molecular Reproduction and Development · doi:10.1002/mrd.22230 · Cited by 45 · see citing works
Choi, B.-I., Harvey, A. J., & Green, M. P. (2016) · Scientific Reports · doi:10.1038/srep29318 · Cited by 45 · see citing works
Self-citationWang, Y., Liu, X., Huang, W., Liang, J., & Chen, Y. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108303 · Cited by 44 · see citing works
Finger, B. J., Harvey, A. J., Green, M. P., & Gardner, D. K. (2015) · Human Reproduction · doi:10.1093/humrep/dev142 · Cited by 44 · see citing works
Self-citationOxygen as a Master Regulator of Human Pluripotent Stem Cell Function and Metabolism
Nit, K., Tyszka‐Czochara, M., & Bobis‐Wozowicz, S. (2021) · Journal of Personalized Medicine · doi:10.3390/jpm11090905 · Cited by 42 · see citing works
Culture systems for bovine embryos
Feugang, J. M., Camargo, O., & Memili, E. (2008) · Livestock Science · doi:10.1016/j.livsci.2008.06.019 · Cited by 42 · see citing works
Gibbons, J. R., Hewitt, E. A., & Gardner, D. K. (2006) · Cloning and Stem Cells · doi:10.1089/clo.2006.8.117 · Cited by 38 · see citing works
Rho, G., Balasubramanian, S., Kim, D., Son, W. J., Cho, S., Kim, J. H., Mohana kumar, B., & Choe, S. (2006) · Molecular Reproduction and Development · doi:10.1002/mrd.20502 · Cited by 38 · see citing works
Bomfim, M. M., Andrade, G. M., del Collado, M., Sangalli, J. R., Fontes, P. K., Nogueira, M. F. G., Meirelles, F. V., da Silveira, J. C., & Perecin, F. (2017) · Molecular Reproduction and Development · doi:10.1002/mrd.22929 · Cited by 38 · see citing works
López-Anguita, N., Gassaloglu, S. I., Stötzel, M., Typou, M., Virta, I., Hetzel, S., Buschow, R., Koksal, B., Atilla, D., Maitschke-Rajasekharan, R., et al. (2022) · Development · doi:10.1242/dev.200679 · Cited by 37 · see citing works
Preimplantation embryotoxicity after mouse embryo exposition to reactive oxygen species
Cebral, E., Carrasco, I., Vantman, D., & Smith, R. (2007) · Biocell · doi:10.32604/biocell.2007.31.051 · Cited by 37 · see citing works
Romek, M., Gajda, B., Rolka, M., & Smorąg, Z. (2010) · Reproduction in Domestic Animals · doi:10.1111/j.1439-0531.2010.01691.x · Cited by 36 · see citing works
Harvey, A. J., Kind, K. L., & Thompson, J. G. (2007) · Biology of Reproduction · doi:10.1095/biolreprod.106.058826 · Cited by 36 · see citing works
Self-citationKelley, R. L., & Gardner, D. K. (2016) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2016.08.003 · Cited by 35 · see citing works
Yadav, A. K., Singh, K., Singh, M. K., Saini, N., Palta, P., Manik, R., Singla, S., Upadhyay, R. C., & Chauhan, M. (2013) · Reproduction in Domestic Animals · doi:10.1111/rda.12175 · Cited by 35 · see citing works
Yao, Y., Lu, Y., Chen, W., Jiang, Y., Cheng, T., Ma, Y., Lu, L., & Dai, W. H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086620 · Cited by 34 · see citing works
Kelley, R. L., & Gardner, D. K. (2019) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2019.03.102 · Cited by 34 · see citing works
Comparison of 2, 5, and 20 % O2 on the development of post-thaw human embryos
Yang, Y., Xu, Y., Ding, C., Khoudja, R., Lin, M., Awonuga, A. O., Dai, J., Puscheck, E. E., Rappolee, D. A., & Zhou, C. (2016) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-016-0693-5 · Cited by 33 · see citing works
Camargo, L. S. A., Powell, A. M., Filho, V. R. D. V., & Wall, R. J. (2005) · Reproduction Fertility and Development · doi:10.1071/rd04128 · Cited by 33 · see citing works
Lee, S. H., Lee, M. Y., & Han, H. J. (2008) · Cell Proliferation · doi:10.1111/j.1365-2184.2008.00516.x · Cited by 33 · see citing works
Cellular and molecular changes associated with fish oocyte ageing
Samarin, A. M., Samarin, A. M., & Policar, T. (2018) · Reviews in Aquaculture · doi:10.1111/raq.12249 · Cited by 32 · see citing works
Gardner, D. K., Kuramoto, T., Tanaka, M., Mitzumoto, S., Montag, M. H. M., & Yoshida, A. (2020) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2020.01.026 · Cited by 32 · see citing works
Parental Effects on Epigenetic Programming in Gametes and Embryos of Dairy Cows
Wu, C., & Sirard, M. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.557846 · Cited by 32 · see citing works
Houghton, F. D. (2020) · Reproduction · doi:10.1530/rep-20-0322 · Cited by 31 · see citing works
Inner Cell Mass Localization of NANOG Precedes OCT3/4 in Rhesus Monkey Blastocysts
Harvey, A. J., Armant, D. R., Bavister, B. D., Nichols, S. M., & Brenner, C. A. (2009) · Stem Cells and Development · doi:10.1089/scd.2009.0122 · Cited by 31 · see citing works
Self-citationAssessment of three generations of mice derived by ICSI using freeze-dried sperm
Li, M., Willis, B., Griffey, S. M., Spearow, J. L., & Lloyd, K. C. K. (2009) · Zygote · doi:10.1017/s0967199409005292 · Cited by 31 · see citing works
Palasz, A. T., Breña, P. B., Martínez, M. F., Pérez‐Garnelo, S. S., Ramírez, M. Á., Gutiérrez‐Adán, A., & de la Fuente, J. (2008) · Zygote · doi:10.1017/s0967199407004467 · Cited by 29 · see citing works
Distinct profiles of human embryonic stem cell metabolism and mitochondria identified by oxygen
Lees, J. G., Rathjen, J., Sheedy, J. R., Gardner, D. K., & Harvey, A. J. (2015) · Reproduction · doi:10.1530/rep-14-0633 · Cited by 27 · see citing works
Self-citationIntrinsic factors affecting apoptosis in bovine in vitro produced embryos.
Vandaele, L., & Soom, A. V. (2011) · PubMed · Cited by 27 · see citing works
Oxygen modulates human embryonic stem cell metabolism in the absence of changes in self-renewal
Harvey, A. J., Rathjen, J., Yu, L. J., & Gardner, D. K. (2014) · Reproduction Fertility and Development · doi:10.1071/rd14013 · Cited by 26 · see citing works
Self-citationDirect effects of hypoxia and nitric oxide on ecdysone secretion by insect prothoracic glands
DeLalio, L. J., Dion, S. M., Bootes, A. M., & Smith, W. A. (2015) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2015.02.009 · Cited by 24 · see citing works
Mechanism of resveratrol on the promotion of induced pluripotent stem cells
Ding, D.-F., Li, X., Xu, H., Wang, Z., Liang, Q., Li, C., & Wang, Y. (2013) · Journal of Chinese Integrative Medicine · doi:10.3736/jintegrmed2013039 · Cited by 23 · see citing works
Sánchez‐Ajofrín, I., Iniesta‐Cuerda, M., Sánchez‐Calabuig, M. J., Peris‐Frau, P., Martín‐Maestro, A., Ortiz, J. A., Fernández-Santos, M. R., Garde, J. J., Gutiérrez‐Adán, A., & Soler, A. J. (2020) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2020.106279 · Cited by 23 · see citing works
Predicting embryo quality: mRNA expression and the preimplantation embryo
Corcoran, D., Fair, T., & Lonergan, P. (2005) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)60842-5 · Cited by 22 · see citing works
Simintiras, C. A., Sánchez, J. M., McDonald, M., O’Callaghan, E., Aburima, A. A., & Lonergan, P. (2021) · Biology of Reproduction · doi:10.1093/biolre/ioab021 · Cited by 21 · see citing works
Belli, M., Antonouli, S., Palmerini, M. G., Bianchi, S., Bernardi, S., Khalili, M. A., Donfrancesco, O., Nottola, S. A., & Macchiarelli, G. (2020) · Systems Biology in Reproductive Medicine · doi:10.1080/19396368.2020.1754961 · Cited by 21 · see citing works
Rlim-Dependent and -Independent Pathways for X Chromosome Inactivation in Female ESCs
Wang, F., McCannell, K. N., Bošković, A., Zhu, X., Shin, J., Yu, J., Gallant, J., Byron, M., Lawrence, J. B., Zhu, L. J., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.12.004 · Cited by 21 · see citing works
- Authors
- Harvey, A. J., Kind, K. L., Pantaleon, M., Armstrong, D. T., & Thompson, J. G.
- Affiliations
- Queen Elizabeth Hospital (AU)
- The University of Queensland (AU)
- Corresponding author
- Harvey, A.J.
- Venue
- Biology of Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2004-10-01
- Volume
- 71
- Issue
- 4
- Pages
- 1108-1119
- ISSN
- 0006-3363 (ISSN-L)
- 1529-7268
- OpenAlex
- W2154875545
- Cited by
- 189
- References
- 66
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 4 · 2023: 2 · 2022: 14 · 2021: 6 · 2020: 15 · 2019: 4 · 2018: 4 · 2017: 10 · 2016: 6 · 2015: 13 · 2014: 4 · 2013: 13 · 2012: 9
- FWCI
- 12.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biology of Reproduction (publishedVersion)
- PubMed (publishedVersion)
- BioOne Complete (BioOne) (submittedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- Funders
- Medical Research Council
- National Health and Medical Research Council (157941)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Reproductive Physiology in Livestock
- Keywords
- oxygen regulation, bovine blastocyst, hypoxia-inducible factor, HIF-1α, HIF-2α, GLUT1, embryo culture, oxygen partial pressure, deferoxamine, inner cell mass, bHLH transcription factors, embryonic development, cumulus cells
- MeSH terms
- Endothelial PAS Domain-Containing Protein 1, Animals, Blastocyst, Cattle, Monosaccharide Transport Proteins, Oxygen, RNA, Messenger, Tissue Distribution, Transcription Factors, Gene Expression Regulation, Developmental, Vascular Endothelial Growth Factor A, Embryo Culture Techniques, Embryonic Development, Glucose Transporter Type 1, Basic Helix-Loop-Helix Proteins, Hypoxia-Inducible Factor 1, alpha Subunit
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review