Parental diet-induced obesity leads to retarded early mouse embryo development and altered carbohydrate utilisation by the blastocyst
Natalie K. Binder A , Megan Mitchell B and David K. Gardner A CA Department of Zoology, University of Melbourne, Parkville 3010, Victoria, Australia.
B Discipline of Obstetrics and Gynecology, The Robinson Institute, University of Adelaide, Adelaide, SA 5006, Australia.
C Corresponding author. Email: david.gardner@unimelb.edu.au
Reproduction, Fertility and Development 24(6) 804-812 https://doi.org/10.1071/RD11256
Submitted: 4 October 2011 Accepted: 3 December 2011 Published: 2 February 2012
Abstract
Maternal obesity results in reproductive complications, whereas the impact of paternal obesity is unclear. In the present study, the effects of parental obesity on preimplantation embryo cell cycle length and carbohydrate utilisation were investigated. Maternal and paternal obesity were assessed independently by deriving zygotes from normal or obese C57BL/6 female mice mated with normal Swiss male mice (maternal obesity), or from normal Swiss female mice mated with normal or obese C57BL/6 male mice (paternal obesity). Zygotes were cultured in vitro and development was then assessed by time-lapse microscopy and metabolism determined using ultramicrofluorescence. Maternal obesity was associated with a significant delay in precompaction cell cycle kinetics from the 1-cell stage. A significant increase in glucose consumption by embryos from obese compared with normal females occurred after compaction, although glycolysis remained unchanged. Similarly, paternal obesity led to significant delays in cell cycle progression during preimplantation embryo development. However, this developmental delay was observed from the second cleavage stage onwards, following embryonic genome activation. Blastocysts from obese males showed disproportionate changes in carbohydrate metabolism, with significantly increased glycolysis. Overall, metabolic changes were not inhibitory to blastocyst formation; however, blastocyst cell numbers were significantly lower when either parent was obese. These data suggest that both maternal and paternal obesity significantly impacts preimplantation embryo physiology.
Additional keywords: high fat diet, maternal, metabolism, nutrition, paternal, preimplantation.
References
Aggerholm, A. S., Thulstrup, A. M., Toft, G., Ramlau-Hansen, C. H., and Bonde, J. P. (2008). Is overweight a risk factor for reduced semen quality and altered serum sex hormone profile? Fertil. Steril. 90, 619–626.| Is overweight a risk factor for reduced semen quality and altered serum sex hormone profile?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtF2qsb7K&md5=ce350f18d1a3f5204f3a464b1e4eae2fCAS | 18068160PubMed |
Avise, J. C., Lansman, R. A., and Shade, R. O. (1979). The use of restriction endonucleases to measure mitochondrial DNA sequence relatedness in natural populations. I. Population structure and evolution in the genus Peromyscus. Genetics 92, 279–295.
| 1:CAS:528:DyaE1MXlt1Wgsr4%3D&md5=59f30d1da5cf70c1ffaad36f5e7be40fCAS | 499767PubMed |
Bakos, H. W., Mitchell, M., Setchell, B. P., and Lane, M. (2010). The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model. Int. J. Androl. 34, 402–410.
| The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model.Crossref | GoogleScholarGoogle Scholar | 20649934PubMed |
Bakos, H. W., Henshaw, R. C., Mitchell, M., and Lane, M. (2011). Paternal body mass index is associated with decreased blastocyst development and reduced live birth rates following assisted reproductive technology. Fertil. Steril. 95, 1700–1704.
| Paternal body mass index is associated with decreased blastocyst development and reduced live birth rates following assisted reproductive technology.Crossref | GoogleScholarGoogle Scholar | 21145051PubMed |
Bellance, N., Benard, G., Furt, F., Begueret, H., Smolkova, K., Passerieux, E., Delage, J. P., Baste, J. M., Moreau, P., and Rossignol, R. (2009). Bioenergetics of lung tumors: alteration of mitochondrial biogenesis and respiratory capacity. Int. J. Biochem. Cell. Biol. 41, 2566–2577.
| Bioenergetics of lung tumors: alteration of mitochondrial biogenesis and respiratory capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlGhsrvN&md5=ef9cc337f4a23ea79d92a116ce96d18dCAS | 19712747PubMed |
Bellver, J., Rossal, L. P., Bosch, E., Zuniga, A., Corona, J. T., Melendez, F., Gomez, E., Simon, C., Remohi, J., and Pellicer, A. (2003). Obesity and the risk of spontaneous abortion after oocyte donation. Fertil. Steril. 79, 1136–1140.
| Obesity and the risk of spontaneous abortion after oocyte donation.Crossref | GoogleScholarGoogle Scholar | 12738508PubMed |
Bellver, J., Ayllon, Y., Ferrando, M., Melo, M., Goyri, E., Pellicer, A., Remohi, J., and Meseguer, M. (2010). Female obesity impairs in vitro fertilization outcome without affecting embryo quality. Fertil. Steril. 93, 447–454.
| Female obesity impairs in vitro fertilization outcome without affecting embryo quality.Crossref | GoogleScholarGoogle Scholar | 19171335PubMed |
Carrell, D. T., Jones, K. P., Peterson, C. M., Aoki, V., Emery, B. R., and Campbell, B. R. (2001). Body mass index is inversely related to intrafollicular HCG concentrations, embryo quality and IVF outcome. Reprod. Biomed. Online 3, 109–111.
| Body mass index is inversely related to intrafollicular HCG concentrations, embryo quality and IVF outcome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXos1GktLg%3D&md5=9fa81fff982bb3978f5fdd7c135974b2CAS | 12513872PubMed |
Chavarro, J. E., Toth, T. L., Wright, D. L., Meeker, J. D., and Hauser, R. (2009). Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic. Fertil. Steril. 93, 2222–2231.
| Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic.Crossref | GoogleScholarGoogle Scholar | 19261274PubMed |
Dokras, A., Baredziak, L., Blaine, J., Syrop, C., VanVoorhis, B. J., and Sparks, A. (2006). Obstetric outcomes after in vitro fertilization in obese and morbidly obese women. Obstet. Gynecol. 108, 61–69.
| Obstetric outcomes after in vitro fertilization in obese and morbidly obese women.Crossref | GoogleScholarGoogle Scholar | 16816057PubMed |
Fedorcsák, P., Storeng, R., Dale, P. O., Tanbo, T., and Åbyholm, T. (2000). Obesity is a risk factor for early pregnancy loss after IVF or ICSI. Acta Obstet. Gynecol. Scand. 79, 43–48.
| Obesity is a risk factor for early pregnancy loss after IVF or ICSI.Crossref | GoogleScholarGoogle Scholar | 10646815PubMed |
Fedorcsák, P., Dale, P. O., Storeng, R., Ertzeid, G., Bjercke, S., Oldereid, N., Omland, A. K., Åbyholm, T., and Tanbo, T. (2004). Impact of overweight and underweight on assisted reproduction treatment. Hum. Reprod. 19, 2523–2528.
| Impact of overweight and underweight on assisted reproduction treatment.Crossref | GoogleScholarGoogle Scholar | 15319380PubMed |
Fejes, I., Koloszar, S., Szollosi, J., Zavaczki, Z., and Pal, A. (2005). Is semen quality affected by male body fat distribution? Andrologia 37, 155–159.
| Is semen quality affected by male body fat distribution?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MnjvFajtg%3D%3D&md5=51171eaf1e30e97868a33d059aa0dc65CAS | 16266392PubMed |
Gardner, D. K. (1998). Changes in requirements and utilization of nutrients during mammalian preimplantation embryo development and their significance in embryo culture. Theriogenology 49, 83–102.
| Changes in requirements and utilization of nutrients during mammalian preimplantation embryo development and their significance in embryo culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFCrtA%3D%3D&md5=4d390ae6295e6e5bd79a63fc3e781115CAS | 10732123PubMed |
Gardner, D. K., and Lane, M. (2007). Embryo culture systems. In ‘In Vitro Fertilization: A Practical Approach’. (Ed. D. K. Gardner.) pp. 221–282. (Informa Healthcare: New York.)
Gardner, D. K., and Leese, H. J. (1987). Assessment of embryo viability prior to transfer by the noninvasive measurement of glucose uptake. J. Exp. Zool. 242, 103–105.
| Assessment of embryo viability prior to transfer by the noninvasive measurement of glucose uptake.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s3ltlShtQ%3D%3D&md5=1eab58a4ac77b7fc8266c6a7f6f8d860CAS | 3598508PubMed |
Gardner, D. K., and Leese, H. J. (1990). Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro. J. Reprod. Fertil. 88, 361–368.
| Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhsFCks7Y%3D&md5=226b7fea334710e3d03927dbded64fd1CAS | 2313649PubMed |
Garesse, R., and Vallejo, C. G. (2001). Animal mitochondrial biogenesis and function: a regulatory cross-talk between two genomes. Gene 263, 1–16.
| Animal mitochondrial biogenesis and function: a regulatory cross-talk between two genomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXht1Okur0%3D&md5=5ae1abad167b3daf0df671af06ef5c90CAS | 11223238PubMed |
Giles, R. E., Blanc, H., Cann, H. M., and Wallace, D. C. (1980). Maternal inheritance of human mitochondrial DNA. Proc. Natl Acad. Sci. USA 77, 6715–6719.
| Maternal inheritance of human mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXivVSksw%3D%3D&md5=00427adb50255914cd2ed280ef4454d1CAS | 6256757PubMed |
Hammoud, A. O., Wilde, N., Gibson, M., Parks, A., Carrell, D. T., and Meikle, A. W. (2008). Male obesity and alteration in sperm parameters. Fertil. Steril. 90, 2222–2225.
| Male obesity and alteration in sperm parameters.Crossref | GoogleScholarGoogle Scholar | 18178190PubMed |
Honnma, H., Endo, T., Kiya, T., Shimizu, A., Nagasawa, K., Baba, T., Fujimoto, T., Henmi, H., Kitajima, Y., Manase, K., Ishioka, S., Ito, E., and Saito, T. (2010). Remarkable features of ovarian morphology and reproductive hormones in insulin-resistant Zucker fatty (fa/fa) rats. Reprod. Biol. Endocrinol. 8, 73–81.
| Remarkable features of ovarian morphology and reproductive hormones in insulin-resistant Zucker fatty (fa/fa) rats.Crossref | GoogleScholarGoogle Scholar | 20576113PubMed |
Igosheva, N., Abramov, A. Y., Poston, L., Eckert, J. J., Fleming, T. P., Duchen, M. R., and McConnell, J. (2010). Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS ONE 5, e10074.
| Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes.Crossref | GoogleScholarGoogle Scholar | 20404917PubMed |
James, P. T., Rigby, N., and Leach, R. (2004). The obesity epidemic, metabolic syndrome and future prevention strategies. Eur. J. Cardiovasc. Prev. Rehabil. 11, 3–8.
| The obesity epidemic, metabolic syndrome and future prevention strategies.Crossref | GoogleScholarGoogle Scholar | 15167200PubMed |
Jensen, T. K., Andersson, A. M., Jorgensen, N., Andersen, A. G., Carlsen, E., Petersen, J. H., and Skakkebaek, N. E. (2004). Body mass index in relation to semen quality and reproductive hormones among 1,558 Danish men. Fertil. Steril. 82, 863–870.
| Body mass index in relation to semen quality and reproductive hormones among 1,558 Danish men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvFOjtrg%3D&md5=9bd46bc85c6a272f3acc53390b63d0c6CAS | 15482761PubMed |
Kenigsberg, S., Bentov, Y., Chalifa-Caspi, V., Potashnik, G., Ofir, R., and Birk, O. S. (2009). Gene expression microarray profiles of cumulus cells in lean and overweight-obese polycystic ovary syndrome patients. Mol. Hum. Reprod. 15, 89–103.
| Gene expression microarray profiles of cumulus cells in lean and overweight-obese polycystic ovary syndrome patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1OntLg%3D&md5=74202c80e36a49eac86ec2aaf0ced9dbCAS | 19141487PubMed |
Kort, H. I., Massey, J. B., Elsner, C. W., Mitchell-Leef, D., Shapiro, D. B., Witt, M. A., and Roudebush, W. E. (2006). Impact of body mass index values on sperm quantity and quality. J. Androl. 27, 450–452.
| Impact of body mass index values on sperm quantity and quality.Crossref | GoogleScholarGoogle Scholar | 16339454PubMed |
Ku, S. Y., Kim, S. D., Jee, B. C., Suh, C. S., Choi, Y. M., Kim, J. G., Moon, S. Y., and Kim, S. H. (2006). Clinical efficacy of body mass index as predictor of in vitro fertilization and embryo transfer outcomes. J. Korean Med. Sci. 21, 300–303.
| Clinical efficacy of body mass index as predictor of in vitro fertilization and embryo transfer outcomes.Crossref | GoogleScholarGoogle Scholar | 16614518PubMed |
Kupka, M. S., Gnoth, C., Buehler, K., Dahncke, W., and Kruessel, J. S. (2011). Impact of female and male obesity on IVF/ICSI: results of 700,000 ART-cycles in Germany. Gynecol. Endocrinol. 27, 144–149.
| Impact of female and male obesity on IVF/ICSI: results of 700,000 ART-cycles in Germany.Crossref | GoogleScholarGoogle Scholar | 20540669PubMed |
Lane, M., and Gardner, D. K. (1996). Selection of viable mouse blastocysts prior to transfer using a metabolic criterion. Hum. Reprod. 11, 1975–1978.
| 1:STN:280:DyaK2s%2FnvFensA%3D%3D&md5=6ad9e838f56101844adb92da30960e52CAS | 8921074PubMed |
Lane, M., and Gardner, D. K. (1997). Differential regulation of mouse embryo development and viability by amino acids. J. Reprod. Fertil. 109, 153–164.
| Differential regulation of mouse embryo development and viability by amino acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhs1Gls78%3D&md5=645c813d18faa617931f8383ef5c9cb7CAS | 9068427PubMed |
Lane, M., and Gardner, D. K. (2000). Lactate regulates pyruvate uptake and metabolism in the preimplantation mouse embryo. Biol. Reprod. 62, 16–22.
| Lactate regulates pyruvate uptake and metabolism in the preimplantation mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhslKmtA%3D%3D&md5=665e252f57f432fb11889d034fd40344CAS | 10611062PubMed |
Lane, M., and Gardner, D. K. (2003). Ammonium induces aberrant blastocyst differentiation, metabolism, pH regulation, gene expression and subsequently alters fetal development in the mouse. Biol. Reprod. 69, 1109–1117.
| Ammonium induces aberrant blastocyst differentiation, metabolism, pH regulation, gene expression and subsequently alters fetal development in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsV2nsr8%3D&md5=752647a0cb5eecb57d1f4d8172084a91CAS | 12773416PubMed |
Lane, M., and Gardner, D. K. (2004). Preparation of gametes, in vitro maturation, in vitro fertilization, embryo recovery and transfer. In ‘A Laboratory Guide to the Mammalian Embryo’. (Eds D. K. Gardner, M. Lane and A. J. Watson.) pp. 24–40. (Oxford University Press: New York.)
Lashen, H., Fear, K., and Sturdee, D. W. (2004). Obesity is associated with increased risk of first trimester and recurrent miscarriage: matched case-control study. Hum. Reprod. 19, 1644–1646.
| Obesity is associated with increased risk of first trimester and recurrent miscarriage: matched case-control study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2czhvVOrsQ%3D%3D&md5=ca652ebae325bbaaa85062a3751a6a1dCAS | 15142995PubMed |
Latham, K. E., and Schultz, R. M. (2001). Embryonic genome activation. Front. Biosci. 6, d748–d759.
| Embryonic genome activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlslKhuro%3D&md5=e3e03911202b8b49e9c33ab55861643bCAS | 11401780PubMed |
Leese, H. J., and Barton, A. M. (1984). Pyruvate and glucose uptake by mouse ova and preimplantation embryos. J. Reprod. Fertil. 72, 9–13.
| Pyruvate and glucose uptake by mouse ova and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXmt1Ols7k%3D&md5=3f1aff4831ec9f7914961ec9f0f30be1CAS | 6540809PubMed |
Loveland, J. B., McClamrock, H. D., Malinow, A. M., and Sharara, F. I. (2001). Increased body mass index has a deleterious effect on in vitro fertilization outcome. J. Assist. Reprod. Genet. 18, 382–386.
| Increased body mass index has a deleterious effect on in vitro fertilization outcome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvlsVWlsg%3D%3D&md5=b5ddad4a4a09fed2b44f43d6433eacc3CAS | 11499322PubMed |
Magnusdottir, E. V., Thorsteinsson, T., Thorsteinsdottir, S., Heimisdottir, M., and Olafsdottir, K. (2005). Persistent organochlorines, sedentary occupation, obesity and human male subfertility. Hum. Reprod. 20, 208–215.
| Persistent organochlorines, sedentary occupation, obesity and human male subfertility.Crossref | GoogleScholarGoogle Scholar | 15567884PubMed |
Metwally, M., Cutting, R., Tipton, A., Skull, J., Ledger, W. L., and Li, T. C. (2007). Effect of increased body mass index on oocyte and embryo quality in IVF patients. Reprod. Biomed. Online 15, 532–538.
| Effect of increased body mass index on oocyte and embryo quality in IVF patients.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2sjgslWruw%3D%3D&md5=043ef347bc927560a430eb11ba152889CAS | 18044034PubMed |
Metwally, M., Ong, K. J., Ledger, W. L., and Li, T. C. (2008). Does high body mass index increase the risk of miscarriage after spontaneous and assisted conception? A meta-analysis of the evidence. Fertil. Steril. 90, 714–726.
| Does high body mass index increase the risk of miscarriage after spontaneous and assisted conception? A meta-analysis of the evidence.Crossref | GoogleScholarGoogle Scholar | 18068166PubMed |
Minge, C. E., Bennett, B. D., Norman, R. J., and Robker, R. L. (2008). Peroxisome proliferator-activated receptor-gamma agonist rosiglitazone reverses the adverse effects of diet-induced obesity on oocyte quality. Endocrinology 149, 2646–2656.
| Peroxisome proliferator-activated receptor-gamma agonist rosiglitazone reverses the adverse effects of diet-induced obesity on oocyte quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Gmsb%2FO&md5=f2989d225f5874bc6f4976c3d425701bCAS | 18276752PubMed |
Mitchell, M., Bakos, H. W., and Lane, M. (2011). Paternal diet-induced obesity impairs embryo development and implantation in the mouse. Fertil. Steril. 95, 1349–1353.
| Paternal diet-induced obesity impairs embryo development and implantation in the mouse.Crossref | GoogleScholarGoogle Scholar | 21047633PubMed |
Nichols, J. E., Crane, M. M., Higdon, H. L., Miller, P. B., and Boone, W. R. (2003). Extremes of body mass index reduce in vitro fertilization pregnancy rates. Fertil. Steril. 79, 645–647.
| Extremes of body mass index reduce in vitro fertilization pregnancy rates.Crossref | GoogleScholarGoogle Scholar | 12620460PubMed |
Ogden, C. L., Carroll, M. D., Curtin, L. R., McDowell, M. A., Tabak, C. J., and Flegal, K. M. (2006). Prevalence of overweight and obesity in the United States, 1999–2004. JAMA 295, 1549–1555.
| Prevalence of overweight and obesity in the United States, 1999–2004.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt12itrk%3D&md5=864df5264850b2e62aac375394e40995CAS | 16595758PubMed |
Pauli, E. M., Legro, R. S., Demers, L. M., Kunselman, A. R., Dodson, W. C., and Lee, P. A. (2008). Diminished paternity and gonadal function with increasing obesity in men. Fertil. Steril. 90, 346–351.
| Diminished paternity and gonadal function with increasing obesity in men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVGlsLvM&md5=ab9b73e252977e4828bdc6c5945fc1c0CAS | 18291378PubMed |
Qin, D. D., Yuan, W., Zhou, W. J., Cui, Y. Q., Wu, J. Q., and Gao, E. S. (2007). Do reproductive hormones explain the association between body mass index and semen quality? Asian J. Androl. 9, 827–834.
| Do reproductive hormones explain the association between body mass index and semen quality?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVWrtLbL&md5=dac9fc0aa73f0ea3bdf84fe31aea39d0CAS | 17968470PubMed |
Ramlau-Hansen, C. H., Thulstrup, A. M., Nohr, E. A., Bonde, J. P., Sorensen, T. I., and Olsen, J. (2007). Subfecundity in overweight and obese couples. Hum. Reprod. 22, 1634–1637.
| Subfecundity in overweight and obese couples.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2szgvFamtQ%3D%3D&md5=87355adfd51a3b1a8ca7b0b8eb293d8eCAS | 17344224PubMed |
Renard, J. P., Philippon, A., and Menezo, Y. (1980). In-vitro uptake of glucose by bovine blastocysts. J. Reprod. Fertil. 58, 161–164.
| In-vitro uptake of glucose by bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXptFKrsg%3D%3D&md5=2f877cc741454be790c7c8ac882c4c00CAS | 7359473PubMed |
Robker, R. L., Akison, L. K., Bennett, B. D., Thrupp, P. N., Chura, L. R., Russell, D. L., Lane, M., and Norman, R. J. (2009). Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women. J. Clin. Endocrinol. Metab. 94, 1533–1540.
| Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvVCqtrw%3D&md5=cb174acbd4167b38a5ea1c840b92bc21CAS | 19223519PubMed |
Seshagiri, P. B., and Bavister, B. D. (1991). Glucose and phosphate inhibit respiration and oxidative metabolism in cultured hamster eight-cell embryos: evidence for the ‘crabtree effect’. Mol. Reprod. Dev. 30, 105–111.
| Glucose and phosphate inhibit respiration and oxidative metabolism in cultured hamster eight-cell embryos: evidence for the ‘crabtree effect’.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmslKmsrg%3D&md5=01a7b918dfacbd3421976cbd0256f599CAS | 1954025PubMed |
Taylor, K. D., and Piko, L. (1995). Mitochondrial biogenesis in early mouse embryos: expression of the mRNAs for subunits IV, Vb, and VIIc of cytochrome c oxidase and subunit 9 (P1) of H(+)-ATP synthase. Mol. Reprod. Dev. 40, 29–35.
| Mitochondrial biogenesis in early mouse embryos: expression of the mRNAs for subunits IV, Vb, and VIIc of cytochrome c oxidase and subunit 9 (P1) of H(+)-ATP synthase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXivFyrsrg%3D&md5=18c97d2d4183c5c7e781593c99e9cc98CAS | 7535541PubMed |
van der Steeg, J. W., Steures, P., Eijkemans, M. J., Habbema, J. D., Hompes, P. G., Burggraaff, J. M., Oosterhuis, G. J., Bossuyt, P. M., van der Veen, F., and Mol, B. W. (2008). Obesity affects spontaneous pregnancy chances in subfertile, ovulatory women. Hum. Reprod. 23, 324–328.
| Obesity affects spontaneous pregnancy chances in subfertile, ovulatory women.Crossref | GoogleScholarGoogle Scholar | 18077317PubMed |
van Swieten, E. C., van der Leeuw-Harmsen, L., Badings, E. A., and van der Linden, P. J. (2005). Obesity and clomiphene challenge test as predictors of outcome of in vitro fertilization and intracytoplasmic sperm injection. Gynecol. Obstet. Invest. 59, 220–224.
| Obesity and clomiphene challenge test as predictors of outcome of in vitro fertilization and intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 15753618PubMed |
Villamor, E., and Cnattingius, S. (2006). Interpregnancy weight change and risk of adverse pregnancy outcomes: a population-based study. Lancet 368, 1164–1170.
| Interpregnancy weight change and risk of adverse pregnancy outcomes: a population-based study.Crossref | GoogleScholarGoogle Scholar | 17011943PubMed |
Virant-Klun, I., Tomazevic, T., and Meden-Vrtovec, H. (2002). Sperm single-stranded DNA, detected by acridine orange staining, reduces fertilization and quality of ICSI-derived embryos. J. Assist. Reprod. Genet. 19, 319–328.
| Sperm single-stranded DNA, detected by acridine orange staining, reduces fertilization and quality of ICSI-derived embryos.Crossref | GoogleScholarGoogle Scholar | 12168732PubMed |
Wale, P. L., and Gardner, D. K. (2010). Time-lapse analysis of mouse embryo development in oxygen gradients. Reprod. Biomed. Online 21, 402–410.
| Time-lapse analysis of mouse embryo development in oxygen gradients.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cfgtVGnsQ%3D%3D&md5=6d6d3581e8fb224ed9b483bcafd137e3CAS | 20691637PubMed |
Wang, J. X., Davies, M., and Norman, R. J. (2000). Body mass and probability of pregnancy during assisted reproduction treatment: retrospective study. BMJ 321, 1320–1321.
| Body mass and probability of pregnancy during assisted reproduction treatment: retrospective study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FmsVKjtA%3D%3D&md5=b2d927213ba4f42ad1634a3e86392f44CAS | 11090515PubMed |
Wittemer, C., Ohl, J., Bailly, M., Bettahar-Lebugle, K., and Nisand, I. (2000). Does body mass index of infertile women have an impact on IVF procedure and outcome? J. Assist. Reprod. Genet. 17, 547–552.
| Does body mass index of infertile women have an impact on IVF procedure and outcome?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M3jt1GntA%3D%3D&md5=dff94de529959d40dd40b610aeffd6c6CAS | 11209534PubMed |