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

Biology of Reproduction

Volumn 86, Issue 5, 2012, Pages

  Velker, Brenna A Market ^a,b   Denomme, Michelle M ^a,b   Mann, Mellissa R W ^a,b  

^a WESTERN UNIVERSITY   (Canada)

^b CHILDREN S HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

Dna methylation; Genomic imprinting; In vitro culture; Metabolic genes; Mouse embryo; Preimplantation development

Indexed keywords

ATP1A1 PROTEIN; BIOLOGICAL MARKER; CYCLIN DEPENDENT KINASE INHIBITOR 1C; GLUCOSE TRANSPORTER 1; HISTONE; MITOCHONDRIAL RIBOSOMAL PROTEIN L1; MITOGEN ACTIVATED PROTEIN KINASE 14; PROTEIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ATP1A1 PROTEIN, MOUSE; CDKN1C PROTEIN, MOUSE; SLC2A1 PROTEIN, MOUSE; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL COUNT; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO TRANSFER; FEMALE; HISTONE METHYLATION; MALE; MOUSE; NONHUMAN; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DETERMINATION; ANIMAL; C57BL MOUSE; DNA METHYLATION; EMBRYO CULTURE; GENE EXPRESSION REGULATION; GENETICS; GENOME IMPRINTING; METABOLISM; PHYSIOLOGY; PREGNANCY;

ANIMALS; CYCLIN-DEPENDENT KINASE INHIBITOR P57; DNA METHYLATION; EMBRYO CULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOMIC IMPRINTING; GLUCOSE TRANSPORTER TYPE 1; MALE; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE 14; PREGNANCY; SNRNP CORE PROTEINS; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 84864015171     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.096602     Document Type: Article

References (82)

1. Bowman P, McLaren A. Viability and growth of mouse embryos after in vitro culture and fusion. J Embryol Exp Morphol 1970; 23:693-704.
2. Harlow GM, Quinn P. Development of preimplantation mouse embryos in vivo and in vitro. Aust J Biol Sci 1982; 35:187-193.
3. Biggers JD, Summers MC. Choosing a culture medium: making informed choices. Fertil Steril 2008; 90:473-483.
4. Gardner DK. Dissection of culture media for embryos: the most important and less important components and characteristics. Reprod Fertil Dev 2008; 20:9-18.
5. Sasaki H, Ferguson-Smith AC, Shum AS, Barton SC, Surani MA. Temporal and spatial regulation of H19 imprinting in normal and uniparental mouse embryos. Development 1995; 121:4195-4202.
6. Sinclair KD, McEvoy TG, Maxfield EK, Maltin CA, Young LE, Wilmut I, Broadbent PJ, Robinson JJ. Aberrant fetal growth and development after in vitro culture of sheep zygotes. J Reprod Fertil 1999; 116:177-186.
7. Barker DJ. In utero programming of cardiovascular disease. Theriogenology 2000; 53:555-574.
8. Boerjan ML, den Daas JH, Dieleman SJ. Embryonic origins of health: long-term effects of IVF in human and livestock. Theriogenology 2000; 53:537-547.
9. Doherty AS, Mann MR, Tremblay KD, Bartolomei MS, Schultz RM. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod 2000; 62:1526-1535.
10. Khosla S, Dean W, Brown D, Reik W, Feil R. Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol Reprod 2001; 64:918-926.
11. Summers MC, Biggers JD. Chemically defined media and the culture of mammalian preimplantation embryos: historical perspective and current issues. Hum Reprod Update 2003; 9:557-582.
12. Ecker DJ, Stein P, Xu Z, Williams CJ, Kopf GS, Bilker WB, Abel T, Schultz RM. Long-term effects of culture of preimplantation mouse embryos on behavior. Proc Natl Acad Sci U S A 2004; 101:1595-1600.
13. Fernandez-Gonzalez R, Moreira P, Bilbao A, Jimenez A, Perez-Crespo M, Ramirez MA, Rodriguez De Fonseca F, Pintado B, Gutierrez-Adan A. 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; 101:5880-5885.
14. Rinaudo P, Schultz RM. Effects of embryo culture on global pattern of gene expression in preimplantation mouse embryos. Reproduction 2004; 128:301-311.
15. Niemann H, Wrenzycki C. Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development. Theriogenology 2000; 53:21-34.
16. Mann MR Lee SS, Doherty AS, Verona RI, Nolen LD, Schultz RM, Bartolomei MS. Selective loss of imprinting in the placenta following preimplantation development in culture. Development 2004; 131: 3727-3735.
17. Market-Velker BA, Fernandes AD, Mann MR. Side-by-side comparison of five commercial media systems in a mouse model: suboptimal in vitro culture interferes with imprint maintenance. Biol Reprod 2010; 83: 938-950.
18. Verona RI, Mann MRW, Bartolomei MS. Genomic imprinting: intricacies of epigenetic regulation in clusters. Annu Rev Cell Dev Biol 2003; 19: 237-259.
19. Rodenhiser D, Mann M. Epigenetics and human disease: translating basic biology into clinical applications. CMAJ 2006; 174:341-348.
20. Cox GF, Burger J, Lip V, Mau UA, Sperling K, Wu BL, Horsthemke B. Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am J Hum Genet 2002; 71:162-164.
21. DeBaun MR, Niemitz EL, Feinberg AP. Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19. Am J Hum Genet 2003; 72:156-160.
22. Maher ER, Brueton LA, Bowdin SC, Luharia A, Cooper W, Cole TR, Macdonald F, Sampson JR, Barratt CL, Reik W, Hawkins MM. Beckwith-Wiedemann syndrome and assisted reproduction technology (ART). J Med Genet 2003; 40:62-64.
23. Gicquel C, Gaston V, Mandelbaum J, Siffroi JP, Flahault A, Le Bouc Y. 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; 72:1338-1341.
24. Orstavik KH, Eiklid K, van der Hagen CB, Spetalen S, Kierulf K, Skjeldal O, Buiting K. Another case of imprinting defect in a girl with Angelman syndrome who was conceived by intracytoplasmic semen injection. Am J Hum Genet 2003; 72:218-219.
25. Halliday J, Oke K, Breheny S, Algar E, Amor DJ. Beckwith-Wiedemann syndrome and IVF: a case-control study. Am J Hum Genet 2004; 75: 526-528.
26. Chang AS, Moley KH, Wangler M, Feinberg AP, Debaun MR. Association between Beckwith-Wiedemann syndrome and assisted reproductive technology: a case series of 19 patients. Fertil Steril 2005; 83:349-354.
27. Ludwig M, Katalinic A, Gross S, Sutcliffe A, Varon R, Horsthemke B. Increased prevalence of imprinting defects in patients with Angelman syndrome born to subfertile couples. J Med Genet 2005; 42:289-291.
28. Sutcliffe AG, Peters CJ, Bowdin S, Temple K, Reardon W, Wilson L, Clayton-Smith J, Brueton LA, Bannister W, Maher ER. Assisted reproductive therapies and imprinting disorders-a preliminary British survey. Hum Reprod 2006; 21:1009-1011.
29. Kidder GM, Watson AJ. Roles of Na, K-ATPase in early development and trophectoderm differentiation. Semin Nephrol 2005; 25:352-355.
30. Pantaleon M, Kaye PL. Glucose transporters in preimplantation development. Rev Reprod 1998; 3:77-81.
31. Augustin R, Pocar P, Navarrete-Santos A, Wrenzycki C, Gandolfi F, Niemann H, Fischer B. Glucose transporter expression is developmentally regulated in in vitro derived bovine preimplantation embryos. Mol Reprod Dev 2001; 60:370-376.
32. Natale DR, Paliga AJ, Beier F, D'Souza SJ, Watson AJ. p38 MAPK signaling during murine preimplantation development. Dev Biol 2004; 268:76-88.
33. Paliga AJ, Natale DR, Watson AJ. p38 mitogen-activated protein kinase (MAPK) first regulates filamentous actin at the 8-16-cell stage during preimplantation development. Biol Cell 2005; 97:629-640.
34. Fong B, Watson PH, Watson AJ. Mouse preimplantation embryo responses to culture medium osmolarity include increased expression of CCM2 and p38 MAPK activation. BMC Dev Biol 2007; 7:2.
35. Johnstone ED, Sibley CP, Lowen B, Guilbert LJ. Epidermal growth factor stimulation of trophoblast differentiation requires MAPK11/14 (p38 MAP kinase) activation. Biol Reprod 2005; 73:1282-1288.
36. Winger QA, Guttormsen J, Gavin H, Bhushan F. Heat shock protein 1 and the mitogen-activated protein kinase 14 pathway are important for mouse trophoblast stem cell differentiation. Biol Reprod 2007; 76:884-891.
37. Market-Velker BA, Zhang L, Magri LS, Bonvissuto AC, Mann MR. Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Hum Mol Genet 2010; 19: 36-51.
38. Smith R, McLaren A. Factors affecting the time of formation of the mouse blastocoele. J Embryol Exp Morphol 1977; 41:79-92.
39. Whitten WK. Nutrient requirements for the culture of preimplantation mouse embryo in vitro. Adv Biosci 1971; 6:129-139.
40. R Development Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria; 2011.
41. Ray J, Raymon HK, Gage FH. Generation and culturing of precursor cells and neuroblasts from embryonic and adult central nervous system. Methods Enzymol 1995; 254:20-37.
42. Dumoulin JC, Derhaag JG, Bras M, Van Montfoort AP, Kester AD, Evers JL, Geraedts JP, Coonen E. Growth rate of human preimplantation embryos is sex dependent after ICSI but not after IVF. Hum Reprod 2005; 20:484-491.
43. Dean JH, Chapman MG, Sullivan EA. 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; 117:1628-1634.
44. Valdivia RP, Kunieda T, Azuma S, Toyoda Y. PCR sexing and developmental rate differences in preimplantation mouse embryos fertilized and cultured in vitro. Mol Reprod Dev 1993; 35:121-126.
45. Peippo J, Bredbacka P. Sex-related growth rate differences in mouse preimplantation embryos in vivo and in vitro. Mol Reprod Dev 1995; 40: 56-61.
46. Byrne MJ, Newmark JA, Warner CM. Analysis of the sex ratio in preimplantation embryos from B6.K1 and B6.K2 Ped gene congenic mice. J Assist Reprod Genet 2006; 23:321-328.
47. Leese HJ. Quiet please, do not disturb: a hypothesis of embryo metabolism and viability. Bioessays 2002; 24:845-849.
48. Lim D, Bowdin SC, Tee L, Kirby GA, Blair E, Fryer A, Lam W, Oley C, Cole T, Brueton LA, Reik W, Macdonald F, Maher ER. Clinical and molecular genetic features of Beckwith-Wiedemann syndrome associated with assisted reproductive technologies. Hum Reprod 2009; 24:741-747.
49. Rossignol S, Steunou V, Chalas C, Kerjean A, Rigolet M, Viegas-Pequignot E, Jouannet P, Le Bouc Y, Gicquel C. 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; 43:902-907.
50. Morita Y, Tsutsumi O, Oka Y, Taketani Y. Glucose transporter GLUT1 mRNA expression in the ontogeny of glucose incorporation in mouse preimplantation embryos. Biochem Biophys Res Commun 1994; 199: 1525-1531.
51. Uechi H, Tsutsumi O, Morita Y, Taketani Y. Cryopreservation of mouse embryos affects later embryonic development possibly through reduced expression of the glucose transporter GLUT1. Mol Reprod Dev 1997; 48: 496-500.
52. Pantaleon M, Ryan JP, Gil M, Kaye PL. An unusual subcellular localization of GLUT1 and link with metabolism in oocytes and preimplantation mouse embryos. Biol Reprod 2001; 64:1247-1254.
53. Leppens-Luisier G, Urner F, Sakkas D. Facilitated glucose transporters play a crucial role throughout mouse preimplantation embryo development. Hum Reprod 2001; 16:1229-1236.
54. Balasubramanian S, Son WJ, Kumar BM, Ock SA, Yoo JG, Im GS, Choe SY, Rho GJ. Expression pattern of oxygen and stress-responsive gene transcripts at various developmental stages of in vitro and in vivo preimplantation bovine embryos. Theriogenology 2007; 68:265-275.
55. Sturmey RG, Reis A, Leese HJ, McEvoy TG. Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod Domest Anim 2009; 44:50-58.
56. Hargreaves DC, Crabtree GR. ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res 2011; 21:396-420.
57. Aiken CE, Swoboda PP, Skepper JN, Johnson MH. The direct measurement of embryogenic volume and nucleo-cytoplasmic ratio during mouse pre-implantation development. Reproduction 2004; 128:527-535.
58. Baltz JM, Tartia AP. Cell volume regulation in oocytes and early embryos: connecting physiology to successful culture media. Hum Reprod Update 2010; 16:166-167.
59. Bradham C, McClay DR. p38 MAPK in development and cancer. Cell Cycle 2006; 5:824-828.
60. Bell CE, Lariviere NM, Watson PH, Watson AJ. 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; 24: 1373-1386.
61. Watson AJ, Barcroft LC. Regulation of blastocyst formation. Front Biosci 2001; 6:D708-D730.
62. Barcroft LC, Offenberg H, Thomsen P, Watson AJ. Aquaporin proteins in murine trophectoderm mediate transepithelial water movements during cavitation. Dev Biol 2003; 256:342-354.
63. Leese HJ, Sturmey RG, Baumann CG, McEvoy TG. Embryo viability and metabolism: obeying the quiet rules. Hum Reprod 2007; 22:3047-3050.
64. Leese HJ. Metabolism of the preimplantation mammalian embryo. Oxf Rev Reprod Biol 1991; 13:35-72.
65. Baumann CG, Morris DG, Sreenan JM, Leese HJ. The quiet embryo hypothesis: molecular characteristics favoring viability. Mol Reprod Dev 2007; 74:1345-1353.
66. Sturmey RG, Hawkhead JA, Barker EA, Leese HJ. DNA damage and metabolic activity in the preimplantation embryo. Hum Reprod 2009; 24: 81-91.
67. Kallen B, Finnstrom O, Lindam A, Nilsson E, Nygren KG, Olausson PO. Blastocyst versus cleavage stage transfer in in vitro fertilization: differences in neonatal outcome? Fertil Steril 2010; 94:1680-1683.
68. Min JK, Hughes E, Young D, Gysler M, Hemmings R, Cheung AP, Goodrow GJ, Senikas V, Wong BC, Sierra S, Carranza-Mamane B, Chase A, et al. Elective single embryo transfer following in vitro fertilization. J Obstet Gynaecol Can 2010; 32:363-377.
69. Porat N, Boehnlein LM, Barker MA, Kovacs P, Lindheim SR. Blastocyst embryo transfer is the primary determinant for improved outcomes in oocyte donation cycles. J Obstet Gynaecol Res 2010; 36:357-363.
70. Sills ES, Palermo GD. Human blastocyst culture in IVF: current laboratory applications in reproductive medicine practice. Rom J Morphol Embryol 2010; 51:441-445.
71. Wang YA, Kovacs G, Sullivan EA. 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; 25:1996-2005.
72. Elizur SE, Lerner-Geva L, Levron J, Shulman A, Bider D, Dor J. Factors predicting IVF treatment outcome: a multivariate analysis of 5310 cycles. Reprod Biomed Online 2005; 10:645-649.
73. Lesourd F, Parant O, Clouet-Delannoy M, Parinaud J. Clinical and biological parameters influencing implantation: score to determine number of embryos to transfer. Reprod Biomed Online 2006; 12:453-459.
74. Shoukir Y, Campana A, Farley T, Sakkas D. Early cleavage of in-vitrofertilized human embryos to the 2-cell stage: a novel indicator of embryo quality and viability. Hum Reprod 1997; 12:1531-1536.
75. Van Montfoort AP, Dumoulin JC, Kester AD, Evers JL. Early cleavage is a valuable addition to existing embryo selection parameters: a study using single embryo transfers. Hum Reprod 2004; 19:2103-2108.
76. Claman P, Armant DR, Seibel MM, Wang TA, Oskowitz SP, Taymor ML. The impact of embryo quality and quantity on implantation and the establishment of viable pregnancies. J In Vitro Fert Embryo Transf 1987; 4:218-222.
77. Windt ML, Kruger TF, Coetzee K, Lombard CJ. Comparative analysis of pregnancy rates after the transfer of early dividing embryos versus slower dividing embryos. Hum Reprod 2004; 19:1155-1162.
78. Biezinova J, Svobodova M, Oborna I, Fingerova H, Dosta J, Krskova M. Embryo quality evaluation according to the speed of the first cleavage after conventional IVF [in Czech]. Ceska Gynekol 2006; 71:105-110.
79. Cummins JM, Breen TM, Harrison KL, Shaw JM, Wilson LM, Hennessey JF. 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; 3: 284-295.
80. Alikani M, Calderon G, Tomkin G, Garrisi J, Kokot M, Cohen J. Cleavage anomalies in early human embryos and survival after prolonged culture invitro. Hum Reprod 2000; 15:2634-2643.
81. Weitzman VN, Schnee-Riesz J, Benadiva C, Nulsen J, Siano L, Maier D. Predictive value of embryo grading for embryos with known outcomes. Fertil Steril 2010; 93:658-662.
82. Wong CC, Loewke KE, Bossert NL, Behr B, De Jonge CJ, Baer TM, Reijo Pera RA. Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat Biotechnol 2010; 28:1115-1121.