Dynamic integrated analysis of DNA methylation and gene expression profiles in in vivo and in vitro fertilized mouse post-implantation extraembryonic and placental tissues

Molecular Human Reproduction

Volumn 22, Issue 7, 2016, Pages 485-498

  Tan, Kun ^a   Zhang, Zhenni ^a   Miao, Kai ^a   Yu, Yong ^a   Sui, Linlin ^a   Tian, Jianhui ^a   An, Lei ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

DNA methylation; Gene expression; In vitro fertilization; Mouse; Placentation

Indexed keywords

ACTIN; LAMININ; TRANSCRIPTION FACTOR ETS; WNT2 PROTEIN; TRANSCRIPTOME;

ACTIN FILAMENT; ACTIN POLYMERIZATION; AMINO ACID METABOLISM; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLASTOCYST; CONTROLLED STUDY; CYTOSKELETON; DNA DETERMINATION; DNA INTEGRATION; DNA METHYLATION; DOWN REGULATION; ECTODERM; EMBRYO DEVELOPMENT; EMBRYO MEMBRANE; EMBRYO TRANSFER; ENERGY METABOLISM; EPIDIDYMIS; FEMALE; FERTILIZATION IN VITRO; GASTRULATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC TRANSDUCTION; GENOME-WIDE ASSOCIATION STUDY; HEMATOPOIESIS; HIGH THROUGHPUT SEQUENCING; HISTOPATHOLOGY; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; INFERTILITY THERAPY; MOUSE; NONHUMAN; OOCYTE; PHENOTYPE; PLACENTA DISORDER; PLACENTA TISSUE; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTION; RNA SEQUENCE; SUPEROVULATION; TRANSLATION REGULATION; UPREGULATION; ANIMAL; CYTOLOGY; GENETICS; IN VITRO FERTILIZATION; MALE; METABOLISM; NIDATION; PHYSIOLOGY; PLACENTA; PREGNANCY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BLASTOCYST; DNA METHYLATION; EMBRYO IMPLANTATION; FEMALE; FERTILIZATION IN VITRO; IMMUNOPRECIPITATION; MALE; MICE; PLACENTA; PREGNANCY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTOME;

EID: 84978731979     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gaw028     Document Type: Article

References (67)

1. Amann KJ, Pollard TD. Cellular regulation of actin network assembly. Curr Biol 2000;10:R728-R730.
2. Audic S, Claverie JM. The significance of digital gene expression profiles. Genome Res 1997;7:986-995.
3. Barker DJ, Bull AR, Osmond C, Simmonds SJ. Fetal and placental size and risk of hypertension in adult life. BMJ 1990;301:259-262.
4. Bergh T, Ericson A, Hillensjo T, Nygren KG,Wennerholm UB. Deliveries and children born after in-vitro fertilisation in Sweden 1982-95: a retrospective cohort study. Lancet 1999;354:1579-1585.
5. Bestor TH, Edwards JR, Boulard M. Notes on the role of dynamic DNA methylation in mammalian development. Proc Natl Acad Sci USA 2015; 112:6796-6799.
6. Bloise E, Lin W, Liu X, Simbulan R, Kolahi KS, Petraglia F, Maltepe E, Donjacour A, Rinaudo P. Impaired placental nutrient transport in mice generated by in vitro fertilization. Endocrinology 2012;153:3457-3467.
7. Bondareva AA, Capecchi MR, Iverson SV, LiY, Lopez NI, Lucas O, MerrillGF, Prigge JR, Siders AM,WakamiyaMet al. Effects of thioredoxin reductase-1 deletion on embryogenesis and transcriptome. Free Radic Biol Med 2007; 43:911-923.
8. Borgel J, Guibert S, Li Y, Chiba H, Schubeler D, Sasaki H, Forne T,Weber M. Targets and dynamics of promoter DNA methylation during early mouse development. Nat Genet 2010;42:1093-1100.
9. Bracken CP, Li X, Wright JA, Lawrence DM, Pillman KA, Salmanidis M, Anderson MA, Dredge BK, Gregory PA, Tsykin A et al. Genome-wide identification of miR-200 targets reveals a regulatory network controlling cell invasion. EMBO J 2014;33:2040-2056.
10. Carlevaro MF, Albini A, Ribatti D, Gentili C, Benelli R, Cermelli S, Cancedda R, Cancedda FD. Transferrin promotes endothelial cell migration and invasion: implication in cartilage neovascularization. J Cell Biol 1997;136:1375-1384.
11. Ceelen M, van Weissenbruch MM, Vermeiden JP, van Leeuwen FE, Delemarre-van de Waal HA. Cardiometabolic differences in children born after in vitro fertilization: follow-up study. J Clin Endocrinol Metab 2008;93:1682-1688.
12. Chan SW, Henderson IR, Jacobsen SE. Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 2005;6:351-360.
13. Chen S, Sun FZ, Huang X, Wang X, Tang N, Zhu B, Li B. Assisted reproduction causes placental maldevelopment and dysfunction linked to reduced fetal weight in mice. Sci Rep 2015;5:10596.
14. Coan PM, Angiolini E, Sandovici I, Burton GJ, Constancia M, Fowden AL. Adaptations in placental nutrient transfer capacity to meet fetal growth demands depend on placental size in mice. J Physiol 2008;586:4567-4576.
15. Damdimopoulou PE, Miranda-Vizuete A, Arner ES, Gustafsson JA, Damdimopoulos AE. The human thioredoxin reductase-1 splice variant TXNRD1_v3 is an atypical inducer of cytoplasmic filaments and cell membrane filopodia. Biochim Biophys Acta 2009;1793:1588-1596.
16. de Waal E, Mak W, Calhoun S, Stein P, Ord T, Krapp C, Coutifaris C, Schultz RM, Bartolomei MS. In vitro culture increases the frequency of stochastic epigenetic errors at imprinted genes in placental tissues from mouse concepti produced through assisted reproductive technologies. Biol Reprod 2014;90:22.
17. de Waal E, Vrooman LA, Fischer E, Ord T, Mainigi MA, Coutifaris C, Schultz RM, Bartolomei MS. The cumulative effect of assisted reproduction procedures on placental development and epigenetic perturbations in a mouse model. Hum Mol Genet 2015;24:6975-6985.
18. Delle Piane L, Lin W, Liu X, Donjacour A, Minasi P, Revelli A, Maltepe E, Rinaudo PF. Effect of the method of conception and embryo transfer procedure on mid-gestation placenta and fetal development in an IVF mouse model. Hum Reprod 2010;25:2039-2046.
19. Desforges M, Sibley CP. Placental nutrient supply and fetal growth. Int J Dev Biol 2010;54:377-390.
20. Deshmukh RS, Ostrup O, Ostrup E, Vejlsted M, Niemann H, Lucas-Hahn A, Petersen B, Li J, Callesen H, Hyttel P. DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilization, parthenogenetic activation and somatic cell nuclear transfer. Epigenetics 2011;6:177-187.
21. Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T,Wang H. Molecular cues to implantation. Endocr Rev 2004;25:341-373.
22. Donjacour A, Liu X, Lin W, Simbulan R, Rinaudo PF. In vitro fertilization affects growth and glucose metabolism in a sex-specific manner in an outbred mouse model. Biol Reprod 2014;90:80.
23. Driver AM, Penagaricano F, Huang W, Ahmad KR, Hackbart KS, Wiltbank MC, Khatib H. RNA-Seq analysis uncovers transcriptomic variations between morphologically similar in vivo-and in vitro-derived bovine blastocysts. BMC Genomics 2012;13:118.
24. Elshourbagy NA, Near JC, Kmetz PJ, Wells TN, Groot PH, Saxty BA, Hughes SA, Franklin M, Gloger IS. Cloning and expression of a human ATP-citrate lyase cDNA. Eur J Biochem 1992;204:491-499.
25. Eriksdotter-NilssonM, Bjorklund H,Olson L. Laminin immunohistochemistry: a simple method to visualize and quantitate vascular structures in the mammalian brain. J NeurosciMethods 1986;17:275-286.
26. Fauque P, Mondon F, Letourneur F, Ripoche MA, Journot L, Barbaux S, Dandolo L, Patrat C, Wolf JP, Jouannet P et al. In vitro fertilization and embryo culture strongly impact the placental transcriptome in the mouse model. PLoS One 2010a;5:e9218.
27. Fauque P, RipocheMA,Tost J, Journot L, Gabory A, Busato F, Le Digarcher A, Mondon F, Gut I, Jouannet P et al. Modulation of imprinted gene network in placenta results in normal development of in vitro manipulated mouse embryos. Hum Mol Genet 2010b;19:1779-1790.
28. Fernandez-Gonzalez R, de Dios Hourcade J, Lopez-Vidriero I, Benguria A, De Fonseca FR, Gutierrez-Adan A. Analysis of gene transcription alterations at the blastocyst stage related to the long-term consequences of in vitro culture in mice. Reproduction 2009;137:271-283.
29. Feuer SK, Donjacour A, Simbulan RK, LinW, Liu X, Maltepe E, Rinaudo PF. Sexually dimorphic effect of in vitro fertilization (IVF) on adult mouse fat and liver metabolomes. Endocrinology 2014;155:4554-4567.
30. Gambardella L, Hemberger M, Hughes B, Zudaire E, Andrews S, Vermeren S. PI3K signaling through the dual GTPase-activating protein ARAP3 is essential for developmental angiogenesis. Sci Signal 2010;3:ra76.
31. Giritharan G, Talbi S, Donjacour A, Di Sebastiano F, DobsonAT, Rinaudo PF. Effect of in vitro fertilization on gene expression and development of mouse preimplantation embryos. Reproduction 2007;134:63-72.
32. Haavaldsen C, Tanbo T, Eskild A. Placental weight in singleton pregnancies with and without assisted reproductive technology: a population study of 536,567 pregnancies. Hum Reprod 2012;27:576-582.
33. Hansen M, Kurinczuk JJ, Milne E, de Klerk N, Bower C. Assisted reproductive technology and birth defects: a systematic review and meta-analysis. Hum Reprod Update 2013;19:330-353.
34. Hemberger M, Cross JC. Genes governing placental development. Trends Endocrinol Metab 2001;12:162-168.
35. Karp NA, Spencer M, Lindsay H, O'Dell K, Lilley KS. Impact of replicate types on proteomic expression analysis. J Proteome Res 2005;4:1867-1871.
36. KeslerCT, Pereira ER, Cui CH, Nelson GM, Masuck DJ, BaishJW, Padera TP. Angiopoietin-4 increases permeability of blood vessels and promotes lymphatic dilation. FASEB J 2015;29:3668-3677.
37. Klemetti R, Sevon T, Gissler M, Hemminki E. Health of children born as a result of in vitro fertilization. Pediatrics 2006;118:1819-1827.
38. Liu D, Bei D, Parmar H, Matus A. Activity-regulated, cytoskeleton-associated protein (Arc) is essential for visceral endoderm organization during early embryogenesis. Mech Dev 2000;92:207-215.
39. Liu Y, Zhou QX, Hou YY, Lu B, Yu C, Chen J, Ling QL, Cao J, Chi ZQ, Xu L et al. Actin polymerization-dependent increase in synaptic Arc/Arg3.1 expression in the amygdala is crucial for the expression of aversive memory associated with drug withdrawal. J Neurosci 2012;32: 12005-12017.
40. Moreau V, Frischknecht F, Reckmann I, Vincentelli R, Rabut G, Stewart D, Way M. A complex of N-WASP and WIP integrates signalling cascades that lead to actin polymerization. Nat Cell Biol 2000;2: 441-448.
41. Nagy A, Gerstenstein M, Vintersten K, Behringer R. Manipulating the Mouse Embryo-A Laboratory Manual, 3rd edn. Plainview, NY, USA: Cold Spring Harbor Press, 2003.
42. Nelissen EC, van Montfoort AP, Dumoulin JC, Evers JL. Epigenetics and the placenta. Hum Reprod Update 2011;17:397-417.
43. Nelissen EC, Dumoulin JC, Daunay A, Evers JL, Tost J, van Montfoort AP. Placentas from pregnancies conceived by IVF/ICSI have a reduced DNA methylation level at the H19 and MEST differentially methylated regions. Hum Reprod 2013;28:1117-1126.
44. Nie J, An L, Miao K, Hou Z, Yu Y, Tan K, Sui L, He S, Liu Q, Lei X et al. Comparative analysis of dynamic proteomic profiles between in vivo and in vitro produced mouse embryos during postimplantation period. J Proteome Res 2013;12:3843-3856.
45. Oliver VF, Miles HL, Cutfield WS, Hofman PL, Ludgate JL, Morison IM. Defects in imprinting and genome-wide DNA methylation are not common in the in vitro fertilization population. Fertil Steril 2012; 97:147-153 e147.
46. Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003;112:453-465.
47. Racowsky C. High rates of embryonic loss, yet high incidence of multiple births in human ART: is this paradoxical? Theriogenology 2002; 57:87-96.
48. Ramesh N, Anton IM, Hartwig JH, Geha RS. WIP, a protein associated with Wiskott-Aldrich syndrome protein, induces actin polymerization and redistribution in lymphoid cells. Proc Natl Acad Sci USA 1997; 94:14671-14676.
49. Reefhuis J, Honein MA, Schieve LA, Correa A, Hobbs CA, Rasmussen SA; National Birth Defects Prevention Study. Assisted reproductive technology and major structural birth defects in the United States. Hum Reprod 2009;24:360-366.
50. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001;293:1089-1093.
51. Ren L, Wang Z, An L, Zhang Z, Tan K, Miao K, Tao L, Cheng L, Zhang Z, Yang M et al. Dynamic comparisons of high-resolution expression profiles highlighting mitochondria-related genes between in vivo and in vitro fertilized early mouse embryos. Hum Reprod 2015;30: 2892-2911.
52. Rinkenberger J, Werb Z. The labyrinthine placenta. Nat Genet 2000; 25:248-250.
53. Rivera RM, Stein P, Weaver JR, Mager J, Schultz RM, Bartolomei MS. Manipulations of mouse embryos prior to implantation result in aberrant expression of imprinted genes on day 9.5 of development. Hum Mol Genet 2008;17:1-14.
54. Rossant J, Cross JC. Placental development: lessons from mouse mutants. Nat Rev Genet 2001;2:538-548.
55. Rugh R. The Mouse: Its Reproduction and Development. Oxford, UK: Oxford Science Publications, 1968.
56. Sakian S, Louie K,Wong EC, Havelock J, Kashyap S, Rowe T, Taylor B, Ma S. Altered gene expression of H19 and IGF2 in placentas from ART pregnancies. Placenta 2015;36:1100-1105.
57. Schieve LA, Meikle SF, Ferre C, PetersonHB, Jeng G, Wilcox LS.Lowand very low birth weight in infants conceived with use of assisted reproductive technology. N Engl J Med 2002;346:731-737.
58. Seckl JR, Holmes MC.Mechanisms of disease: glucocorticoids, their placental metabolism and fetal 'programming' of adult pathophysiology. Nat Clin Pract Endocrinol Metab 2007;3:479-488.
59. Serman L, Dodig D. Impact ofDNAmethylation on trophoblast function. Clin Epigenetics 2011;3:7.
60. Servick K. Unsettled questions trail IVF's success. Science 2014;345:744-746.
61. Sui L, An L, Tan K,Wang Z,Wang S, Miao K, Ren L, Tao L, He S, Yu Y et al. Dynamic proteomic profiles of in vivo-and in vitro-produced mouse postimplantation extraembryonic tissues and placentas. Biol Reprod 2014;91:155.
62. Tan K, An L,Wang SM,Wang XD, Zhang ZN, Miao K, Sui LL, He SZ, Nie JZ, WuZH et al. Actin disorganization plays a vital role in impaired embryonic development of in vitro-produced mouse preimplantation embryos. PLoS One 2015;10:e0130382.
63. Tan K, Wang Z, Zhang Z, An L, Tian J. IVF affects embryonic development in a sex-biased manner in mice. Reproduction 2016;151: 443-453.
64. Valenzuela DM, Griffiths JA, Rojas J, Aldrich TH, Jones PF, Zhou H, McClain J, Copeland NG, Gilbert DJ, Jenkins NA et al. Angiopoietins 3 and 4: diverging gene counterparts in mice and humans. Proc Natl Acad Sci USA 1999;96:1904-1909.
65. Vallet JL, McNeel AK, Miles JR, Freking BA. Placental accommodations for transport and metabolism during intra-uterine crowding in pigs. J Anim Sci Biotechnol 2014;5:55.
66. Walentin K, Hinze C, Werth M, Haase N, Varma S, Morell R, Aue A, Potschke E, Warburton D, Qiu A et al. A Grhl2-dependent gene network controls trophoblast branching morphogenesis. Development 2015;142:1125-1136.
67. Wen J, Jiang J, Ding C, Dai J, Liu Y, Xia Y, Liu J, Hu Z. Birth defects in children conceived by in vitro fertilization and intracytoplasmic sperm injection: a meta-analysis. Fertil Steril 2012;97:1331-1337 e1331-1334.