Home LiteratureArticle Details
PMID: 22461414 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Effect of glucose concentration during in vitro culture of mouse embryos on development to blastocyst, success of embryo transfer, and litter sex ratio.

Molecular reproduction and development ·Vol. 79 ·No. 5 ·2012-05-00 ·Pages 329-36

Bermejo-Alvarez P, Roberts RM, Rosenfeld CS

Abstract

A high-glucose concentration in the reproductive tract during early development may result in aberrant embryo or fetal development, with effects that could have a greater impact on one sex than the other. Here, we determine if a high-glucose concentration impacts embryo development and pregnancy outcomes in a sex-specific manner in the mouse. Zygotes were cultured in potassium simple optimized medium, which typically contains 0.2 mM D-glucose, with and without additional glucose supplementation to a concentration of 28 mM. Zygote cleavage and blastocyst rate did not differ between treatments, but total and trophectoderm cell counts were reduced in blastocysts cultured in a high glucose. No differences between sexes nor inner cell mass cell number were observed within each treatment. Blastocysts developed in both media were transferred to recipients. The percentage of blastocysts resulting in viable pups was significantly reduced when the blastocysts were cultured in 28 mM glucose (74 ± 4%, controls vs. 55.8 ± 7.1%, 28 mM glucose), but conceptus loss affected both sexes equally as litter sex ratio did not differ between treatments (52.7% and 52.2% males for controls and high glucose, respectively). Pup body weight at birth was higher for males than females, but was not affected by earlier culture in high glucose. In conclusion, in vitro culture in medium with a glucose concentration approximating that of diabetic serum reduces total and trophectoderm cell numbers at the blastocyst stage and conceptus development to term, but these detrimental effects are not sex-specific.

MeSH Terms
Animals Blastocyst/drug effects,metabolism,physiology Embryo Culture Techniques Embryo Transfer Embryo, Mammalian/drug effects,metabolism,physiology Embryonic Development Female Glucose/metabolism,pharmacology Hyperglycemia Male Mice Pregnancy Sex Ratio Zygote/growth & development
Chemicals
Glucose
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Bermejo-Alvarez P
Bond Life Sciences Center, University of Missouri, Columbia, Missouri 65211, USA. [email protected]
Roberts R M
Rosenfeld C S
References (52)
52 references, click to expand
  1. Differential gene expression profile in bovine blastocysts resulting from hyperglycemia exposure during early cleavage stages.
    Biol Reprod. 2012 Feb 29;86(2):50 PMID: 22075474
  2. Transcriptional sexual dimorphism during preimplantation embryo development and its consequences for developmental competence and adult health and disease.
    Reproduction. 2011 May;141(5):563-70 PMID: 21339284
  3. Can bovine in vitro-matured oocytes selectively process X- or Y-sorted sperm differentially?
    Biol Reprod. 2008 Oct;79(4):594-7 PMID: 18579751
  4. Diabetic embryopathy in C57BL/6J mice. Altered fetal sex ratio and impact of the splotch allele.
    Diabetes. 2001 May;50(5):1193-9 PMID: 11334426
  5. Metabolism of the viable mammalian embryo: quietness revisited.
    Mol Hum Reprod. 2008 Dec;14(12):667-72 PMID: 19019836
  6. Toxic effects of hyperglycemia are mediated by the hexosamine signaling pathway and o-linked glycosylation in early mouse embryos.
    Biol Reprod. 2010 Apr;82(4):751-8 PMID: 20032283
  7. Comparison of gene expression in male and female mouse blastocysts revealed imprinting of the X-linked gene, Rhox5/Pem, at preimplantation stages.
    Curr Biol. 2006 Jan 24;16(2):166-72 PMID: 16431368
  8. Transcriptional sexual dimorphism in elongating bovine embryos: implications for XCI and sex determination genes.
    Reproduction. 2011 Jun;141(6):801-8 PMID: 21411694
  9. Dose-response effects of glucose, insulin, and glucagon on mouse pre-embryo development.
    Metabolism. 1991 Jun;40(6):566-70 PMID: 1865820
  10. Maternal diabetes impairs gastrulation and insulin and IGF-I receptor expression in rabbit blastocysts.
    Endocrinology. 2010 Sep;151(9):4158-67 PMID: 20631000
  11. Glucose metabolism in pregnancy and embryogenesis.
    Curr Opin Endocrinol Diabetes Obes. 2007 Dec;14(6):488-93 PMID: 17982357
  12. Effect of diabetes mellitus on mouse pre-implantation embryo development.
    J Reprod Fertil. 1991 Nov;93(2):325-32 PMID: 1787451
  13. Nutrient concentrations in murine follicular fluid and the female reproductive tract.
    Theriogenology. 2005 Sep 1;64(4):992-1006 PMID: 16054501
  14. Differential expression of two genes located on the X chromosome between male and female in vitro-produced bovine embryos at the blastocyst stage.
    Mol Reprod Dev. 2000 Feb;55(2):146-51 PMID: 10618653
  15. Increased number of cells and metabolic activity in male human preimplantation embryos following in vitro fertilization.
    J Reprod Fertil. 1995 May;104(1):165-71 PMID: 7636798
  16. Evidence that glucose is not always an inhibitor of mouse preimplantation development in vitro.
    Hum Reprod. 2001 Jan;16(1):153-163 PMID: 11139555
  17. Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro.
    Reprod Fertil Dev. 2001;13(5-6):361-5 PMID: 11833931
  18. Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts.
    Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3394-9 PMID: 20133684
  19. In vitro production and nuclear transfer affect dosage compensation of the X-linked gene transcripts G6PD, PGK, and Xist in preimplantation bovine embryos.
    Biol Reprod. 2002 Jan;66(1):127-34 PMID: 11751274
  20. Mitochondrial function and redox state in mammalian embryos.
    Semin Cell Dev Biol. 2009 May;20(3):346-53 PMID: 19530278
  21. Blastocyst transfer does not cause a sex-ratio imbalance.
    Fertil Steril. 2009 Oct;92(4):1302-1305 PMID: 18996516
  22. Impact of hyperglycemia on early embryo development and embryopathy: in vitro experiments using a mouse model.
    Hum Reprod. 2007 Dec;22(12):3059-68 PMID: 17933753
  23. Effects of D-glucose concentration, D-fructose, and inhibitors of enzymes of the pentose phosphate pathway on the development and sex ratio of bovine blastocysts.
    Mol Reprod Dev. 2005 Oct;72(2):201-7 PMID: 15968626
  24. One-cell zygote transfer from diabetic to nondiabetic mouse results in congenital malformations and growth retardation in offspring.
    Endocrinology. 2008 Feb;149(2):466-9 PMID: 18039778
  25. Preimplantation development in the streptozotocin-induced diabetic mouse.
    Reprod Fertil Dev. 1990;2(4):407-12 PMID: 2217897
  26. Quantitative measurement of transcript levels throughout human preimplantation development: analysis of hypoxanthine phosphoribosyl transferase.
    Mol Hum Reprod. 2001 Feb;7(2):147-54 PMID: 11160840
  27. Glucose and glutamine metabolism in pre-attachment cattle embryos in relation to sex and stage of development.
    J Reprod Fertil. 1991 Sep;93(1):125-32 PMID: 1920281
  28. Glucose controls sex-related growth rate differences of bovine embryos produced in vitro.
    J Reprod Fertil. 1996 Mar;106(2):169-72 PMID: 8699398
  29. Developmental kinetics and gene expression in male and female bovine embryos produced in vitro with sex-sorted spermatozoa.
    Reprod Fertil Dev. 2010;22(2):426-36 PMID: 20047728
  30. Decreased expression of fibroblast growth factor-4 and associated dysregulation of trophoblast differentiation in mouse blastocysts exposed to high D-glucose in vitro.
    Diabetologia. 2001 Oct;44(10):1318-25 PMID: 11692181
  31. Genes that escape from X inactivation.
    Hum Genet. 2011 Aug;130(2):237-45 PMID: 21614513
  32. Increased cell death in rat blastocysts exposed to maternal diabetes in utero and to high glucose or tumor necrosis factor-alpha in vitro.
    Development. 1997 Dec;124(23):4827-36 PMID: 9428419
  33. Low oxygen tension during IVM improves bovine oocyte competence and enhances anaerobic glycolysis.
    Reprod Biomed Online. 2010 Mar;20(3):341-9 PMID: 20093090
  34. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes.
    PLoS One. 2010 Apr 09;5(4):e10074 PMID: 20404917
  35. Effect of duration of oocyte maturation on the kinetics of cleavage, embryo yield and sex ratio in cattle.
    Reprod Fertil Dev. 2008;20(6):734-40 PMID: 18671921
  36. Hyperglycemia induces apoptosis in pre-implantation embryos through cell death effector pathways.
    Nat Med. 1998 Dec;4(12):1421-4 PMID: 9846581
  37. Hyperglycemia-induced apoptosis affects sex ratio of bovine and murine preimplantation embryos.
    Mol Reprod Dev. 2003 Jun;65(2):180-7 PMID: 12704729
  38. Utero-tubal transfer of mouse embryos.
    Genesis. 2001 Jun;30(2):77-81 PMID: 11416867
  39. A differential autophagic response to hyperglycemia in the developing murine embryo.
    Reproduction. 2011 May;141(5):607-15 PMID: 21367963
  40. Altered sex ratio in offspring of mothers with insulin-dependent diabetes mellitus.
    Lancet. 1998 Feb 14;351(9101):497-8 PMID: 9482447
  41. Can mammalian mothers influence the sex of their offspring peri-conceptually?
    Reproduction. 2010 Sep;140(3):425-33 PMID: 20591970
  42. Sex and development in bovine in-vitro fertilized embryos.
    Theriogenology. 1991 May;35(5):953-63 PMID: 16726963
  43. Glucose consumption of single post-compaction human embryos is predictive of embryo sex and live birth outcome.
    Hum Reprod. 2011 Aug;26(8):1981-6 PMID: 21572086
  44. Mouse Y-specific repeats isolated by whole chromosome representational difference analysis.
    Genomics. 1996 Sep 1;36(2):349-53 PMID: 8812464
  45. Effects of streptozotocin- and alloxan-induced diabetes mellitus on mouse follicular and early embryo development.
    J Reprod Fertil. 1989 May;86(1):1-10 PMID: 2526873
  46. Experimental diabetes impairs rat embryo development during the preimplantation period.
    Diabetologia. 1990 Apr;33(4):187-91 PMID: 2347432
  47. Experimental IUGR and later diabetes.
    J Intern Med. 2007 May;261(5):437-52 PMID: 17444883
  48. Peri-implantation embryopathy induced by maternal diabetes.
    J Reprod Fertil Suppl. 2000;55:129-39 PMID: 10889842
  49. Sexual dimorphism among bovine embryos in their ability to make the transition to expanded blastocyst and in the expression of the signaling molecule IFN-tau.
    Proc Natl Acad Sci U S A. 2001 Aug 14;98(17):9677-82 PMID: 11481449
  50. Sex ratios of offspring of patients with breast cancer and other endocrine related cancers.
    Int J Cancer. 2006 Dec 1;119(11):2710-1; author reply 2712 PMID: 17004247
  51. Effect of pH and CO2 concentration on glucose metabolism by rat adipose tissue in vitro.
    Am J Physiol. 1968 Sep;215(3):582-6 PMID: 5670996
  52. Sex-related differences in developmental rates of bovine embryos produced and cultured in vitro.
    Mol Reprod Dev. 1992 Apr;31(4):249-52 PMID: 1571158
Article Info
Journal
Molecular reproduction and development
Abbr.
Mol Reprod Dev
ISSN
1098-2795
Published
2012-05-00
Epub
2012-00-29
Pages
329-36
Language
English
Region
United States
NLM ID
8903333
PMCID
PMC4243512
Subset
IM
Grants
NICHD NIH HHS · HD21896 · United States
NICHD NIH HHS · R01 HD044042-01A2 · United States
NICHD NIH HHS · R01 HD044042 · United States
NICHD NIH HHS · HD 44042 · United States
NICHD NIH HHS · R37 HD021896 · United States
NICHD NIH HHS · R01 HD021896-19 · United States
NIEHS NIH HHS · RC1 ES018195 · United States
NICHD NIH HHS · R01 HD021896 · United States
NIEHS NIH HHS · RC1 ES018195-01 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]