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PMID: 22278980 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Loss of genomic imprinting in mouse embryos with fast rates of preimplantation development in culture.

Biology of reproduction ·Vol. 86 ·No. 5 ·2012-05-00 ·Pages 143, 1-16

Market Velker BA, Denomme MM, Mann MR

Abstract

Currently, the stage of embryo development has been proposed as one of many criteria for identifying healthy embryos in infertility clinics with the fastest embryos being highlighted as the healthiest. However the validity of this as an accurate criterion with respect to genomic imprinting is unknown. Given that embryo development in culture generally requires an extra day compared to in vivo development, we hypothesized that loss of imprinting correlates with slower rates of embryonic development. To evaluate this, embryos were recovered at the 2-cell stage, separated into four groups based on morphological stage at two predetermined time points, and cultured to blastocysts. We examined cell number, embryo volume, embryo sex, imprinted Snrpn and H19 methylation, imprinted Snrpn, H19, and Cdkn1c expression, and expression of genes involved in embryo metabolism-Atp1a1, Slc2a1, and Mapk14-all within the same individual embryo. Contrary to our hypothesis, we observed that faster developing embryos exhibited greater cell numbers and embryo volumes as well as greater perturbations in genomic imprinting and metabolic marker expression. Embryos with slower rates of preimplantation development were most similar to in vivo derived embryos, displaying similar cell numbers, embryo volumes, Snrpn and H19 imprinted methylation, H19 imprinted expression, and Atp1a1 and Slc2a1 expression. We conclude that faster development rates in vitro are correlated with loss of genomic imprinting and aberrant metabolic marker expression. Importantly, we identified a subset of in vitro cultured embryos that, according to the parameters evaluated, are very similar to in vivo derived embryos and thus are likely most suitable for embryo transfer.

MeSH Terms
Animals Cyclin-Dependent Kinase Inhibitor p57/metabolism DNA Methylation/physiology Embryo Culture Techniques Embryonic Development/genetics Female Gene Expression Regulation, Developmental/physiology Genomic Imprinting Glucose Transporter Type 1/metabolism Male Mice Mice, Inbred C57BL Mitogen-Activated Protein Kinase 14/metabolism Pregnancy Sodium-Potassium-Exchanging ATPase/metabolism snRNP Core Proteins/metabolism
Chemicals
Cdkn1c protein, mouse Cyclin-Dependent Kinase Inhibitor p57 Glucose Transporter Type 1 Slc2a1 protein, mouse snRNP Core Proteins Mitogen-Activated Protein Kinase 14 Atp1a1 protein, mouse Sodium-Potassium-Exchanging ATPase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Market Velker Brenna A
Departments of Obstetrics & Gynecology, and Biochemistry, University of Western Ontario, Schulich School of Medicine and Dentistry, London, Ontario, Canada.
Denomme Michelle M
Mann Mellissa R W
References (79)
79 references, click to expand
  1. Beckwith-Wiedemann syndrome and assisted reproduction technology (ART).
    J Med Genet. 2003 Jan;40(1):62-4 PMID: 12525545
  2. Roles of Na,K-ATPase in early development and trophectoderm differentiation.
    Semin Nephrol. 2005 Sep;25(5):352-5 PMID: 16139691
  3. Another case of imprinting defect in a girl with Angelman syndrome who was conceived by intracytoplasmic semen injection.
    Am J Hum Genet. 2003 Jan;72(1):218-9 PMID: 12549484
  4. Glucose transporters in preimplantation development.
    Rev Reprod. 1998 May;3(2):77-81 PMID: 9685185
  5. Epigenetics and human disease: translating basic biology into clinical applications.
    CMAJ. 2006 Jan 31;174(3):341-8 PMID: 16446478
  6. Glucose transporter expression is developmentally regulated in in vitro derived bovine preimplantation embryos.
    Mol Reprod Dev. 2001 Nov;60(3):370-6 PMID: 11599048
  7. Mitogen-activated protein kinase (MAPK) pathways mediate embryonic responses to culture medium osmolarity by regulating Aquaporin 3 and 9 expression and localization, as well as embryonic apoptosis.
    Hum Reprod. 2009 Jun;24(6):1373-86 PMID: 19258345
  8. In vitro fertilization may increase the risk of Beckwith-Wiedemann syndrome related to the abnormal imprinting of the KCN1OT gene.
    Am J Hum Genet. 2003 May;72(5):1338-41 PMID: 12772698
  9. Analysis of the sex ratio in preimplantation embryos from B6.K1 and B6.K2 Ped gene congenic mice.
    J Assist Reprod Genet. 2006 Jul-Aug;23(7-8):321-8 PMID: 16902830
  10. A formula for scoring human embryo growth rates in in vitro fertilization: its value in predicting pregnancy and in comparison with visual estimates of embryo quality.
    J In Vitro Fert Embryo Transf. 1986 Oct;3(5):284-95 PMID: 3783014
  11. Long-term effects of culture of preimplantation mouse embryos on behavior.
    Proc Natl Acad Sci U S A. 2004 Feb 10;101(6):1595-600 PMID: 14747652
  12. Predictive value of embryo grading for embryos with known outcomes.
    Fertil Steril. 2010 Feb;93(2):658-62 PMID: 19410247
  13. Temporal and spatial regulation of H19 imprinting in normal and uniparental mouse embryos.
    Development. 1995 Dec;121(12):4195-202 PMID: 8575319
  14. Factors affecting the time of formation of the mouse blastocoele.
    J Embryol Exp Morphol. 1977 Oct;41:79-92 PMID: 591880
  15. Selective loss of imprinting in the placenta following preimplantation development in culture.
    Development. 2004 Aug;131(15):3727-35 PMID: 15240554
  16. Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior.
    Proc Natl Acad Sci U S A. 2004 Apr 20;101(16):5880-5 PMID: 15079084
  17. Choosing a culture medium: making informed choices.
    Fertil Steril. 2008 Sep;90(3):473-83 PMID: 18847602
  18. Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19.
    Am J Hum Genet. 2003 Jan;72(1):156-60 PMID: 12439823
  19. Early cleavage of in-vitro fertilized human embryos to the 2-cell stage: a novel indicator of embryo quality and viability.
    Hum Reprod. 1997 Jul;12(7):1531-6 PMID: 9262291
  20. Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage.
    Nat Biotechnol. 2010 Oct;28(10):1115-21 PMID: 20890283
  21. Glucose transporter GLUT1 mRNA expression in the ontogeny of glucose incorporation in mouse preimplantation embryos.
    Biochem Biophys Res Commun. 1994 Mar 30;199(3):1525-31 PMID: 8147898
  22. The direct measurement of embryogenic volume and nucleo-cytoplasmic ratio during mouse pre-implantation development.
    Reproduction. 2004 Nov;128(5):527-35 PMID: 15509698
  23. Mouse preimplantation embryo responses to culture medium osmolarity include increased expression of CCM2 and p38 MAPK activation.
    BMC Dev Biol. 2007 Jan 10;7:2 PMID: 17214902
  24. Aberrant fetal growth and development after in vitro culture of sheep zygotes.
    J Reprod Fertil. 1999 May;116(1):177-86 PMID: 10505068
  25. Blastocyst embryo transfer is the primary determinant for improved outcomes in oocyte donation cycles.
    J Obstet Gynaecol Res. 2010 Apr;36(2):357-63 PMID: 20492388
  26. Heat shock protein 1 and the mitogen-activated protein kinase 14 pathway are important for mouse trophoblast stem cell differentiation.
    Biol Reprod. 2007 May;76(5):884-91 PMID: 17267699
  27. Role of fatty acids in energy provision during oocyte maturation and early embryo development.
    Reprod Domest Anim. 2009 Sep;44 Suppl 3:50-8 PMID: 19660080
  28. PCR sexing and developmental rate differences in preimplantation mouse embryos fertilized and cultured in vitro.
    Mol Reprod Dev. 1993 Jun;35(2):121-6 PMID: 8318217
  29. Development of preimplantation mouse embryos in vivo and in vitro.
    Aust J Biol Sci. 1982;35(2):187-93 PMID: 7126059
  30. Metabolism of the preimplantation mammalian embryo.
    Oxf Rev Reprod Biol. 1991;13:35-72 PMID: 1845337
  31. Cleavage anomalies in early human embryos and survival after prolonged culture in-vitro.
    Hum Reprod. 2000 Dec;15(12):2634-43 PMID: 11098037
  32. The epigenetic imprinting defect of patients with Beckwith-Wiedemann syndrome born after assisted reproductive technology is not restricted to the 11p15 region.
    J Med Genet. 2006 Dec;43(12):902-7 PMID: 16825435
  33. The quiet embryo hypothesis: molecular characteristics favoring viability.
    Mol Reprod Dev. 2007 Oct;74(10):1345-53 PMID: 17342740
  34. Regulation of blastocyst formation.
    Front Biosci. 2001 May 01;6:D708-30 PMID: 11333210
  35. Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes.
    Biol Reprod. 2001 Mar;64(3):918-26 PMID: 11207209
  36. p38 mitogen-activated protein kinase (MAPK) first regulates filamentous actin at the 8-16-cell stage during preimplantation development.
    Biol Cell. 2005 Aug;97(8):629-40 PMID: 15850458
  37. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo.
    Biol Reprod. 2000 Jun;62(6):1526-35 PMID: 10819752
  38. The impact of embryo quality and quantity on implantation and the establishment of viable pregnancies.
    J In Vitro Fert Embryo Transf. 1987 Aug;4(4):218-22 PMID: 3625001
  39. DNA damage and metabolic activity in the preimplantation embryo.
    Hum Reprod. 2009 Jan;24(1):81-91 PMID: 18835872
  40. Beckwith-Wiedemann syndrome and IVF: a case-control study.
    Am J Hum Genet. 2004 Sep;75(3):526-8 PMID: 15284956
  41. Generation and culturing of precursor cells and neuroblasts from embryonic and adult central nervous system.
    Methods Enzymol. 1995;254:20-37 PMID: 8531687
  42. In utero programming of cardiovascular disease.
    Theriogenology. 2000 Jan 15;53(2):555-74 PMID: 10735050
  43. p38 MAPK signaling during murine preimplantation development.
    Dev Biol. 2004 Apr 1;268(1):76-88 PMID: 15031106
  44. Side-by-side comparison of five commercial media systems in a mouse model: suboptimal in vitro culture interferes with imprint maintenance.
    Biol Reprod. 2010 Dec;83(6):938-50 PMID: 20702853
  45. Dissection of culture media for embryos: the most important and less important components and characteristics.
    Reprod Fertil Dev. 2008;20(1):9-18 PMID: 18154693
  46. Embryo viability and metabolism: obeying the quiet rules.
    Hum Reprod. 2007 Dec;22(12):3047-50 PMID: 17956925
  47. Cryopreservation of mouse embryos affects later embryonic development possibly through reduced expression of the glucose transporter GLUT1.
    Mol Reprod Dev. 1997 Dec;48(4):496-500 PMID: 9364444
  48. [Embryo quality evaluation according to the speed of the first cleavage after conventional IVF].
    Ceska Gynekol. 2006 Mar;71(2):105-10 PMID: 16649410
  49. Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development.
    Theriogenology. 2000 Jan 1;53(1):21-34 PMID: 10735059
  50. Facilitated glucose transporters play a crucial role throughout mouse preimplantation embryo development.
    Hum Reprod. 2001 Jun;16(6):1229-36 PMID: 11387297
  51. Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner.
    Hum Mol Genet. 2010 Jan 1;19(1):36-51 PMID: 19805400
  52. Blastocyst versus cleavage stage transfer in in vitro fertilization: differences in neonatal outcome?
    Fertil Steril. 2010 Oct;94(5):1680-3 PMID: 20137785
  53. Intracytoplasmic sperm injection may increase the risk of imprinting defects.
    Am J Hum Genet. 2002 Jul;71(1):162-4 PMID: 12016591
  54. Growth rate of human preimplantation embryos is sex dependent after ICSI but not after IVF.
    Hum Reprod. 2005 Feb;20(2):484-91 PMID: 15591088
  55. Embryonic origins of health: long-term effects of IVF in human and livestock.
    Theriogenology. 2000 Jan 15;53(2):537-47 PMID: 10735048
  56. p38 MAPK in development and cancer.
    Cell Cycle. 2006 Apr;5(8):824-8 PMID: 16627995
  57. Epidermal growth factor stimulation of trophoblast differentiation requires MAPK11/14 (p38 MAP kinase) activation.
    Biol Reprod. 2005 Dec;73(6):1282-8 PMID: 16120828
  58. Transfer of a selected single blastocyst optimizes the chance of a healthy term baby: a retrospective population based study in Australia 2004-2007.
    Hum Reprod. 2010 Aug;25(8):1996-2005 PMID: 20519249
  59. Aquaporin proteins in murine trophectoderm mediate transepithelial water movements during cavitation.
    Dev Biol. 2003 Apr 15;256(2):342-54 PMID: 12679107
  60. Effects of embryo culture on global pattern of gene expression in preimplantation mouse embryos.
    Reproduction. 2004 Sep;128(3):301-11 PMID: 15333781
  61. Assisted reproductive therapies and imprinting disorders--a preliminary British survey.
    Hum Reprod. 2006 Apr;21(4):1009-11 PMID: 16361294
  62. Clinical and biological parameters influencing implantation: score to determine number of embryos to transfer.
    Reprod Biomed Online. 2006 Apr;12(4):453-9 PMID: 16740218
  63. Sex-related growth rate differences in mouse preimplantation embryos in vivo and in vitro.
    Mol Reprod Dev. 1995 Jan;40(1):56-61 PMID: 7702870
  64. Quiet please, do not disturb: a hypothesis of embryo metabolism and viability.
    Bioessays. 2002 Sep;24(9):845-9 PMID: 12210521
  65. The effect on human sex ratio at birth by assisted reproductive technology (ART) procedures--an assessment of babies born following single embryo transfers, Australia and New Zealand, 2002-2006.
    BJOG. 2010 Dec;117(13):1628-34 PMID: 20875033
  66. Comparative analysis of pregnancy rates after the transfer of early dividing embryos versus slower dividing embryos.
    Hum Reprod. 2004 May;19(5):1155-62 PMID: 15044410
  67. An unusual subcellular localization of GLUT1 and link with metabolism in oocytes and preimplantation mouse embryos.
    Biol Reprod. 2001 Apr;64(4):1247-54 PMID: 11259273
  68. Genomic imprinting: intricacies of epigenetic regulation in clusters.
    Annu Rev Cell Dev Biol. 2003;19:237-59 PMID: 14570570
  69. ATP-dependent chromatin remodeling: genetics, genomics and mechanisms.
    Cell Res. 2011 Mar;21(3):396-420 PMID: 21358755
  70. Clinical and molecular genetic features of Beckwith-Wiedemann syndrome associated with assisted reproductive technologies.
    Hum Reprod. 2009 Mar;24(3):741-7 PMID: 19073614
  71. Early cleavage is a valuable addition to existing embryo selection parameters: a study using single embryo transfers.
    Hum Reprod. 2004 Sep;19(9):2103-8 PMID: 15243008
  72. Factors predicting IVF treatment outcome: a multivariate analysis of 5310 cycles.
    Reprod Biomed Online. 2005 May;10(5):645-9 PMID: 15949224
  73. Expression pattern of oxygen and stress-responsive gene transcripts at various developmental stages of in vitro and in vivo preimplantation bovine embryos.
    Theriogenology. 2007 Jul 15;68(2):265-75 PMID: 17559922
  74. Association between Beckwith-Wiedemann syndrome and assisted reproductive technology: a case series of 19 patients.
    Fertil Steril. 2005 Feb;83(2):349-54 PMID: 15705373
  75. Increased prevalence of imprinting defects in patients with Angelman syndrome born to subfertile couples.
    J Med Genet. 2005 Apr;42(4):289-91 PMID: 15805153
  76. Cell volume regulation in oocytes and early embryos: connecting physiology to successful culture media.
    Hum Reprod Update. 2010 Mar-Apr;16(2):166-76 PMID: 19825850
  77. Human blastocyst culture in IVF: current laboratory applications in reproductive medicine practice.
    Rom J Morphol Embryol. 2010;51(3):441-5 PMID: 20809018
  78. Chemically defined media and the culture of mammalian preimplantation embryos: historical perspective and current issues.
    Hum Reprod Update. 2003 Nov-Dec;9(6):557-82 PMID: 14714592
  79. Viability and growth of mouse embryos after in vitro culture and fusion.
    J Embryol Exp Morphol. 1970 Jun;23(3):693-704 PMID: 5473306
Article Info
Journal
Biology of reproduction
Abbr.
Biol Reprod
ISSN
1529-7268
Published
2012-05-00
Epub
2012-00-10
Pages
143, 1-16
Language
English
Region
United States
NLM ID
0207224
PMCID
PMC4480067
Subset
IM
Grants
Canadian Institutes of Health Research · Canada
Corrections
CommentIn
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