Home LiteratureArticle Details
PMID: 20889529 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Effect of ICSI on gene expression and development of mouse preimplantation embryos.

Human reproduction (Oxford, England) ·Vol. 25 ·No. 12 ·2010-12-00 ·Pages 3012-24

Giritharan G, Li MW, Di Sebastiano F, De Sebastiano F, Esteban FJ, Horcajadas JA, Lloyd KC, Donjacour A, Maltepe E, Rinaudo PF

Abstract

In vitro culture (IVC) and IVF of preimplantation mouse embryos are associated with changes in gene expression. It is however not known whether ICSI has additional effects on the transcriptome of mouse blastocysts. We compared gene expression and development of mouse blastocysts produced by ICSI and cultured in Whitten's medium (ICSI(WM)) or KSOM medium with amino acids (ICSI(KSOMaa)) with control blastocysts flushed out of the uterus on post coital Day 3.5 (in vivo). In addition, we compared gene expression in embryos generated by IVF or ICSI using WM. Global pattern of gene expression was assessed using the Affymetrix 430 2.0 chip. Blastocysts from ICSI fertilization have a reduction in the number of trophoblastic and inner cell mass cells compared with embryos generated in vivo. Approximately 1000 genes are differentially expressed between ICSI blastocyst and in vivo blastocysts; proliferation, apoptosis and morphogenetic pathways are the most common pathways altered after IVC. Unexpectedly, expression of only 41 genes was significantly different between embryo cultured in suboptimal conditions (WM) or optimal conditions (KSOM(aa)). Our results suggest that fertilization by ICSI may play a more important role in shaping the transcriptome of the developing mouse embryo than the culture media used.

MeSH Terms
Animals Blastocyst/metabolism DNA-Binding Proteins/biosynthesis Embryo Culture Techniques Embryonic Development Female Gene Expression Profiling Gene Expression Regulation, Developmental Histone Deacetylase 6 Histone Deacetylases/biosynthesis Histone-Lysine N-Methyltransferase Mice Myeloid-Lymphoid Leukemia Protein/biosynthesis Protein Array Analysis Sperm Injections, Intracytoplasmic Transcription Factors/biosynthesis
Chemicals
DNA-Binding Proteins Smarca1 protein, mouse Transcription Factors Myeloid-Lymphoid Leukemia Protein Histone-Lysine N-Methyltransferase Kmt2b protein, mouse Hdac6 protein, mouse Histone Deacetylase 6 Histone Deacetylases
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Giritharan G
Department of Obstetric, Gynecology and Reproductive Sciences, University of California, San Francisco, San Francisco, CA 94143, USA.
Li M W
Di Sebastiano F
De Sebastiano F
Esteban F J
Horcajadas J A
Lloyd K C K
Donjacour A
Maltepe E
Rinaudo P F
References (61)
61 references, click to expand
  1. HDAC6-induced premature chromatin compaction in mouse oocytes and fertilised eggs.
    Zygote. 2003 Nov;11(4):323-8 PMID: 15085732
  2. The solute carrier family SLC10: more than a family of bile acid transporters regarding function and phylogenetic relationships.
    Naunyn Schmiedebergs Arch Pharmacol. 2006 Mar;372(6):413-31 PMID: 16541252
  3. The risk of major birth defects after intracytoplasmic sperm injection and in vitro fertilization.
    N Engl J Med. 2002 Mar 7;346(10):725-30 PMID: 11882727
  4. Human endometrial side population cells exhibit genotypic, phenotypic and functional features of somatic stem cells.
    PLoS One. 2010 Jun 24;5(6):e10964 PMID: 20585575
  5. Effects of oxygen tension on gene expression in preimplantation mouse embryos.
    Fertil Steril. 2006 Oct;86(4 Suppl):1252-65, 1265.e1-36 PMID: 17008149
  6. Developmental effects of sublethal mitochondrial injury in mouse oocytes.
    Biol Reprod. 2006 May;74(5):969-77 PMID: 16452460
  7. Manipulation of SMARCA2 and SMARCA4 transcript levels in porcine embryos differentially alters development and expression of SMARCA1, SOX2, NANOG, and EIF1.
    Reproduction. 2009 Jan;137(1):23-33 PMID: 18845624
  8. Interleukin 11 inhibits human trophoblast invasion indicating a likely role in the decidual restraint of trophoblast invasion during placentation.
    Biol Reprod. 2009 Feb;80(2):302-10 PMID: 18987331
  9. Clinical and molecular genetic features of Beckwith-Wiedemann syndrome associated with assisted reproductive technologies.
    Hum Reprod. 2009 Mar;24(3):741-7 PMID: 19073614
  10. A novel member of a zinc transporter family is defective in acrodermatitis enteropathica.
    Am J Hum Genet. 2002 Jul;71(1):66-73 PMID: 12032886
  11. Calcium-dependent and -independent interactions of the S100 protein family.
    Biochem J. 2006 Jun 1;396(2):201-14 PMID: 16683912
  12. Rank-based methods as a non-parametric alternative of the T-statistic for the analysis of biological microarray data.
    J Bioinform Comput Biol. 2005 Oct;3(5):1171-89 PMID: 16278953
  13. Comparison of in-vitro development of embryos originating from either conventional in-vitro fertilization or intracytoplasmic sperm injection.
    Hum Reprod. 2000 Feb;15(2):402-9 PMID: 10655313
  14. Preterm birth and low birth weight among in vitro fertilization singletons: a systematic review and meta-analyses.
    Eur J Obstet Gynecol Reprod Biol. 2009 Oct;146(2):138-48 PMID: 19577836
  15. 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
  16. Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta.
    Dev Biol. 2002 Oct 15;250(2):358-73 PMID: 12376109
  17. 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
  18. Mouse pregnancy-specific glycoproteins: tissue-specific expression and evidence of association with maternal vasculature.
    Reproduction. 2006 Apr;131(4):721-32 PMID: 16595723
  19. Low and very low birth weight in infants conceived with use of assisted reproductive technology.
    N Engl J Med. 2002 Mar 7;346(10):731-7 PMID: 11882728
  20. Assessment of three generations of mice derived by ICSI using freeze-dried sperm.
    Zygote. 2009 Aug;17(3):239-51 PMID: 19416557
  21. Analysis of gene transcription alterations at the blastocyst stage related to the long-term consequences of in vitro culture in mice.
    Reproduction. 2009 Feb;137(2):271-83 PMID: 19017722
  22. ICSI-generated mouse zygotes exhibit altered calcium oscillations, inositol 1,4,5-trisphosphate receptor-1 down-regulation, and embryo development.
    Mol Hum Reprod. 2003 Sep;9(9):523-33 PMID: 12900511
  23. Intracellular calcium oscillations and activation in horse oocytes injected with stallion sperm extracts or spermatozoa.
    Reproduction. 2003 Oct;126(4):489-99 PMID: 14525531
  24. Syntenic organization of the mouse distal chromosome 7 imprinting cluster and the Beckwith-Wiedemann syndrome region in chromosome 11p15.5.
    Hum Mol Genet. 1998 Jul;7(7):1149-59 PMID: 9618174
  25. RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo.
    Dev Biol. 2005 Jul 1;283(1):40-57 PMID: 15975430
  26. Mouse preimplantation embryos developed from oocytes injected with round spermatids or spermatozoa have similar but distinct patterns of early messenger RNA expression.
    Biol Reprod. 2003 Oct;69(4):1170-6 PMID: 12773410
  27. Tetraspanin functions and associated microdomains.
    Nat Rev Mol Cell Biol. 2005 Oct;6(10):801-11 PMID: 16314869
  28. Long-term effects of mouse intracytoplasmic sperm injection with DNA-fragmented sperm on health and behavior of adult offspring.
    Biol Reprod. 2008 Apr;78(4):761-72 PMID: 18199884
  29. Tumor suppressor p53 protein is a new target for the metastasis-associated Mts1/S100A4 protein: functional consequences of their interaction.
    J Biol Chem. 2001 Jun 22;276(25):22699-708 PMID: 11278647
  30. Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR.
    Biol Proced Online. 2006;8:175-93 PMID: 17242735
  31. Trophectoderm-specific expression of the X-linked Bex1/Rex3 gene in preimplantation stage mouse embryos.
    Mol Reprod Dev. 2002 Mar;61(3):281-7 PMID: 11835573
  32. Glycogen storage disease type Ib.
    Eur J Pediatr. 1983 Sep;140(4):283-8 PMID: 6313372
  33. Bypassing spermiogenesis for several generations does not have detrimental consequences on the fertility and neurobehavior of offspring: a study using the mouse.
    J Assist Reprod Genet. 1999 Jul;16(6):315-24 PMID: 10394528
  34. Ott, a mouse X-linked multigene family expressed specifically during meiosis.
    Hum Mol Genet. 1996 Aug;5(8):1139-48 PMID: 8842733
  35. Structure and function of cationic amino acid transporters (CATs).
    J Membr Biol. 2006;213(2):67-77 PMID: 17417706
  36. Predictive value of human chorionic gonadotrophin in the outcome of early pregnancy after in-vitro fertilization and spontaneous conception.
    Hum Reprod. 1994 Aug;9(8):1550-5 PMID: 7527424
  37. A comparison of meta-analysis methods for detecting differentially expressed genes in microarray experiments.
    Bioinformatics. 2008 Feb 1;24(3):374-82 PMID: 18204063
  38. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo.
    Biol Reprod. 2000 Jun;62(6):1526-35 PMID: 10819752
  39. The evolution, regulation, and function of placenta-specific genes.
    Annu Rev Cell Dev Biol. 2008;24:159-81 PMID: 18616428
  40. Intracytoplasmic sperm injection in the bovine induces abnormal [Ca2+]i responses and oocyte activation.
    Reprod Fertil Dev. 2006;18(1-2):39-51 PMID: 16478601
  41. Metabolism of the viable mammalian embryo: quietness revisited.
    Mol Hum Reprod. 2008 Dec;14(12):667-72 PMID: 19019836
  42. Luteogenic hormones act through a vascular endothelial growth factor-dependent mechanism to up-regulate alpha 5 beta 1 and alpha v beta 3 integrins, promoting the migration and survival of human luteinized granulosa cells.
    Am J Pathol. 2007 May;170(5):1561-72 PMID: 17456762
  43. Enhanced insulin sensitivity of gene-targeted mice lacking functional KCNQ1.
    Am J Physiol Regul Integr Comp Physiol. 2009 Jun;296(6):R1695-701 PMID: 19369585
  44. Targeted deletion of fatty acid transport protein-4 results in early embryonic lethality.
    J Biol Chem. 2003 Dec 5;278(49):49512-6 PMID: 14512415
  45. Congenital malformations in 4224 children conceived after IVF.
    Hum Reprod. 2002 Aug;17(8):2089-95 PMID: 12151442
  46. Complementation cloning identifies CDG-IIc, a new type of congenital disorders of glycosylation, as a GDP-fucose transporter deficiency.
    Nat Genet. 2001 May;28(1):73-6 PMID: 11326280
  47. Gene expression in the preimplantation embryo: in-vitro developmental changes.
    Reprod Biomed Online. 2005 May;10(5):607-16 PMID: 15949218
  48. Cytochrome c oxidase of mammals contains a testes-specific isoform of subunit VIb--the counterpart to testes-specific cytochrome c?
    Mol Reprod Dev. 2003 Sep;66(1):8-16 PMID: 12874793
  49. Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts.
    Reprod Biomed Online. 2001;3(1):25-29 PMID: 12513888
  50. Intracytoplasmic sperm injection may increase the risk of imprinting defects.
    Am J Hum Genet. 2002 Jul;71(1):162-4 PMID: 12016591
  51. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes.
    N Engl J Med. 2004 Feb 12;350(7):664-71 PMID: 14960743
  52. Histone H2AX-dependent GABA(A) receptor regulation of stem cell proliferation.
    Nature. 2008 Jan 24;451(7177):460-4 PMID: 18185516
  53. Comparison of Ca2+ and CaMKII responses in IVF and ICSI in the mouse.
    Mol Hum Reprod. 2007 Apr;13(4):265-72 PMID: 17327267
  54. Transforming growth factor beta (TGFB) signaling is activated during porcine implantation: proposed role for latency-associated peptide interactions with integrins at the conceptus-maternal interface.
    Reproduction. 2010 Feb;139(2):465-78 PMID: 19920116
  55. Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption.
    Cell. 2006 Dec 1;127(5):917-28 PMID: 17129779
  56. Effects of embryo culture on global pattern of gene expression in preimplantation mouse embryos.
    Reproduction. 2004 Sep;128(3):301-11 PMID: 15333781
  57. Transgene insertion induced dominant male sterility and rescue of male fertility using round spermatid injection.
    Biol Reprod. 2002 Mar;66(3):726-34 PMID: 11870080
  58. Increased apoptosis and skewed differentiation in mouse embryonic stem cells lacking the histone methyltransferase Mll2.
    Mol Biol Cell. 2007 Jun;18(6):2356-66 PMID: 17429066
  59. Effect of in vitro fertilization on gene expression and development of mouse preimplantation embryos.
    Reproduction. 2007 Jul;134(1):63-72 PMID: 17641089
  60. Cardiometabolic differences in children born after in vitro fertilization: follow-up study.
    J Clin Endocrinol Metab. 2008 May;93(5):1682-8 PMID: 18285409
  61. Coordinate expression of splice variants of the murine pregnancy-specific glycoprotein (PSG) gene family during placental development.
    Eur J Biochem. 1996 Dec 1;242(2):280-7 PMID: 8973644
Article Info
Journal
Human reproduction (Oxford, England)
Abbr.
Hum Reprod
ISSN
1460-2350
Published
2010-12-00
Epub
2010-00-01
Pages
3012-24
Language
English
Region
England
NLM ID
8701199
PMCID
PMC2989873
Subset
IM
Grants
NCI NIH HHS · P30 CA093373 · United States
NICHD NIH HHS · R01 HD062803 · United States
NIH HHS · U42 OD012210 · United States
NICHD NIH HHS · 1U54HD055764 · United States
Corrections
ErratumIn
-
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]