Skip to main content
Top
Published in: Journal of Assisted Reproduction and Genetics 1/2013

01-01-2013 | Embryo Biology

Effect of sperm entry on blastocyst development after in vitro fertilization and intracytoplasmic sperm injection — mouse model

Authors: Karolina Piotrowska-Nitsche, Anthony W. S. Chan

Published in: Journal of Assisted Reproduction and Genetics | Issue 1/2013

Login to get access

Abstract

Purpose

To investigate whether in vitro fertilization (IVF) and intracytoplasmic sperm injection (ICSI), influence the embryo’s development and its quality using the mouse as a model.

Methods

Assisted fertilization was performed using ICSI and IVF. Fluorescent beads were adhered to the fertilization cone or place of previous sperm injection in the natural mated (NM), IVF and ICSI embryos, respectively. Embryo examination was carried out at the two-cell and blastocyst stage to determine the position of fluorescent bead. Protein expression was detected by fluorescence immunocytochemical staining and confocal microscopic imaging of blastocysts.

Results

IVF and ICSI embryos developed at rates comparable to NM group. Embryos show similar expression patterns of two transcription factors, Oct4 and Cdx2. The most preferred place for spermatozoa attachment was the equatorial site of the egg, whether fertilization occurred in vitro or under natural conditions. We also link the sperm entry position (SEP) to embryo morphology and the number of cells at the blastocyst stage, with no influence of the method of fertilization.

Conclusions

IVF and ICSI, do not compromise in vitro pre-implantation development. Additional data, related to sperm entry, could offer further criteria to predict embryos that will implant successfully. Based on embryo morphology, developmental rate and protein expression level of key transcription factors, our results support the view that ART techniques, such as IVF and ICSI, do not perturb embryonic development or quality.
Appendix
Available only for authorised users
Literature
1.
go back to reference Amor DJ, Halliday J. A review of known imprinting syndromes and their association with assisted reproduction technologies. Hum Reprod. 2008;23(12):2826–34.PubMedCrossRef Amor DJ, Halliday J. A review of known imprinting syndromes and their association with assisted reproduction technologies. Hum Reprod. 2008;23(12):2826–34.PubMedCrossRef
2.
go back to reference Andersen AN, Goossens V, Ferraretti AP, Bhattacharya S, Felberbaum R, de Mouzon J, et al. Assisted reproductive technology in Europe, 2004: results generated from European registers by ESHRE. Hum Reprod. 2008;23:756–71.PubMedCrossRef Andersen AN, Goossens V, Ferraretti AP, Bhattacharya S, Felberbaum R, de Mouzon J, et al. Assisted reproductive technology in Europe, 2004: results generated from European registers by ESHRE. Hum Reprod. 2008;23:756–71.PubMedCrossRef
3.
go back to reference Avery S, Blayney M. Effect of the position of the meiotic spindle on the outcome of intracytoplasmic sperm injection. Hum Fertil (Camb). 2003;6:19–22.CrossRef Avery S, Blayney M. Effect of the position of the meiotic spindle on the outcome of intracytoplasmic sperm injection. Hum Fertil (Camb). 2003;6:19–22.CrossRef
4.
go back to reference Beck F, Erler T, Russell A, James R. Expression of Cdx-2 in the mouse embryo and placenta: possible role in patterning of the extra-embryonic membranes. Dev Dyn. 1995;204:219–27.PubMedCrossRef Beck F, Erler T, Russell A, James R. Expression of Cdx-2 in the mouse embryo and placenta: possible role in patterning of the extra-embryonic membranes. Dev Dyn. 1995;204:219–27.PubMedCrossRef
5.
go back to reference Black M, Liu DY, Bourne H, Baker HW. Comparison of outcomes of conventional intracytoplasmic sperm injection (ICSI) and ICSI using sperm bound to the zona pellucida of immature oocytes. Fertil Steril. 2010;93:672–4.PubMedCrossRef Black M, Liu DY, Bourne H, Baker HW. Comparison of outcomes of conventional intracytoplasmic sperm injection (ICSI) and ICSI using sperm bound to the zona pellucida of immature oocytes. Fertil Steril. 2010;93:672–4.PubMedCrossRef
6.
go back to reference Brezinova J, Oborna I, Svobodova M, Fingerova H. Evaluation of day one embryo quality and IVF outcome – a comparison of two scoring systems. Reprod Biol Endocrinol. 2009;3:7–9. Brezinova J, Oborna I, Svobodova M, Fingerova H. Evaluation of day one embryo quality and IVF outcome – a comparison of two scoring systems. Reprod Biol Endocrinol. 2009;3:7–9.
7.
go back to reference Bridges PJ, Jeoung M, Kim H, Kim JH, Lee DR, Ko C, Baker DJ. Methodology matters: IVF versus ICSI and embryonic gene expression. Reprod Biomed. 2011. Online May 8:Epub ahead of print Bridges PJ, Jeoung M, Kim H, Kim JH, Lee DR, Ko C, Baker DJ. Methodology matters: IVF versus ICSI and embryonic gene expression. Reprod Biomed. 2011. Online May 8:Epub ahead of print
8.
go back to reference Center for Disease Control and Prevention (2008) “ART National Report”, November Center for Disease Control and Prevention (2008) “ART National Report”, November
9.
go back to reference Chawengsaksophak K, James R, Hammond VE, Kontgen F, Beck F. Homeosis and intestinal tumours in Cdx-2 mutant mice. Nature. 1997;386:84–7.PubMedCrossRef Chawengsaksophak K, James R, Hammond VE, Kontgen F, Beck F. Homeosis and intestinal tumours in Cdx-2 mutant mice. Nature. 1997;386:84–7.PubMedCrossRef
10.
go back to reference Cruz M, Garrido N, Herrero J, Pérez-Cano I, Muñoz M, Meseguer M. Timing of cell division in human cleavage-stage embryos is linked with blastocyst formation and quality. Reprod Biomed Online. 2012;25(4):371–81.PubMedCrossRef Cruz M, Garrido N, Herrero J, Pérez-Cano I, Muñoz M, Meseguer M. Timing of cell division in human cleavage-stage embryos is linked with blastocyst formation and quality. Reprod Biomed Online. 2012;25(4):371–81.PubMedCrossRef
11.
go back to reference Ebner T, Moser M, Sommergruber M, Tews G. Selection based on morphological assessment of oocytes and embryos at different stages of preimplantation development: a review. Hum Reprod Update. 2003;9(3):251–62.PubMedCrossRef Ebner T, Moser M, Sommergruber M, Tews G. Selection based on morphological assessment of oocytes and embryos at different stages of preimplantation development: a review. Hum Reprod Update. 2003;9(3):251–62.PubMedCrossRef
12.
go back to reference Ecker DJ, Stein P, Xu Z, Williams CJ, Kopf GS, Bilker WB, et al. Long-term effects of culture of preimplantation mouse embryos on behavior. Proc Natl Acad Sci USA. 2004;101:1595–600.PubMedCrossRef Ecker DJ, Stein P, Xu Z, Williams CJ, Kopf GS, Bilker WB, et al. Long-term effects of culture of preimplantation mouse embryos on behavior. Proc Natl Acad Sci USA. 2004;101:1595–600.PubMedCrossRef
13.
go back to reference Evans JP, Foster JA, McAvey BA, Gerton GL, Kopf GS, Schultz RM. Effects of perturbation of cell polarity on molecular markers of sperm-egg binding sites on mouse eggs. Biol Reprod. 2000;62:76–84.PubMedCrossRef Evans JP, Foster JA, McAvey BA, Gerton GL, Kopf GS, Schultz RM. Effects of perturbation of cell polarity on molecular markers of sperm-egg binding sites on mouse eggs. Biol Reprod. 2000;62:76–84.PubMedCrossRef
14.
go back to reference Foresta C, Garolla A, Bartoloni L, Bettella A, Ferlin A. Genetic abnormalities among severely oligospermic men who are candidates for intracytoplasmic sperm injection. J Clin Endocrinol Metab. 2005;90:152–6.PubMedCrossRef Foresta C, Garolla A, Bartoloni L, Bettella A, Ferlin A. Genetic abnormalities among severely oligospermic men who are candidates for intracytoplasmic sperm injection. J Clin Endocrinol Metab. 2005;90:152–6.PubMedCrossRef
15.
go back to reference Fortunato A, Tosti E. The impact of in vitro fertilization on health of the children: an update. Eur J Obstet Gynecol Reprod Biol. 2011;154(2):125–9.PubMedCrossRef Fortunato A, Tosti E. The impact of in vitro fertilization on health of the children: an update. Eur J Obstet Gynecol Reprod Biol. 2011;154(2):125–9.PubMedCrossRef
16.
go back to reference Gardner DK, Schoolcraft WB. Towards reproductive certainty: infertility and genetics beyond. In: Jansen R, Mortimer D, editors. In vitro culture of human blastocysts. Carnforth: Parthenon Press; 1999. p. 378–88. Gardner DK, Schoolcraft WB. Towards reproductive certainty: infertility and genetics beyond. In: Jansen R, Mortimer D, editors. In vitro culture of human blastocysts. Carnforth: Parthenon Press; 1999. p. 378–88.
17.
go back to reference Giritharan G, Talbi S, Donjacour A, Di Sebastiano F, Dobson AT, Rinaudo PF. Effect of in vitro fertilization on gene expression and development of mouse preimplantation embryos. Reproduction. 2007;134(1):63–72.PubMedCrossRef Giritharan G, Talbi S, Donjacour A, Di Sebastiano F, Dobson AT, Rinaudo PF. Effect of in vitro fertilization on gene expression and development of mouse preimplantation embryos. Reproduction. 2007;134(1):63–72.PubMedCrossRef
18.
go back to reference Giritharan G, Li MW, De Sebastiano F, Esteban FJ, Horcajadas JA, Lloyd KC, et al. Effect of ICSI on gene expression and development of mouse preimplantation embryos. Hum Reprod. 2010;25(12):3012–24.PubMedCrossRef Giritharan G, Li MW, De Sebastiano F, Esteban FJ, Horcajadas JA, Lloyd KC, et al. Effect of ICSI on gene expression and development of mouse preimplantation embryos. Hum Reprod. 2010;25(12):3012–24.PubMedCrossRef
19.
go back to reference Gray D, Plusa B, Piotrowska K, Na J, Tom B, Glover DM, et al. First cleavage of the mouse embryo responds to egg geometry that reflects the position of sperm entry. Curr Biol. 2004;9:397–405.CrossRef Gray D, Plusa B, Piotrowska K, Na J, Tom B, Glover DM, et al. First cleavage of the mouse embryo responds to egg geometry that reflects the position of sperm entry. Curr Biol. 2004;9:397–405.CrossRef
20.
go back to reference Hvidtjørn D, Grove J, Schendel D, Vaeth M, Ernst E, Nielsen L, et al. ‘Vanishing embryo syndrome’ in IVF/ICSI. Hum Reprod. 2005;20:2550–1.PubMedCrossRef Hvidtjørn D, Grove J, Schendel D, Vaeth M, Ernst E, Nielsen L, et al. ‘Vanishing embryo syndrome’ in IVF/ICSI. Hum Reprod. 2005;20:2550–1.PubMedCrossRef
21.
go back to reference Jones Jr HW, Jones GS, Andrews MC, Acosta AA, Bundren C, Garcia J, et al. The program for in vitro fertilization at Norfolk. Fertil Steril. 1982;38:14–21.PubMed Jones Jr HW, Jones GS, Andrews MC, Acosta AA, Bundren C, Garcia J, et al. The program for in vitro fertilization at Norfolk. Fertil Steril. 1982;38:14–21.PubMed
22.
go back to reference Kimber SJ, Sneddon SF, Bloor DJ, El-Bareg AM, Hawkhead JA, Metcalfe AD, et al. Expression of genes involved in early cell fate decisions in human embryos and their regulation by growth factors. Reproduction. 2008;135:635–47.PubMedCrossRef Kimber SJ, Sneddon SF, Bloor DJ, El-Bareg AM, Hawkhead JA, Metcalfe AD, et al. Expression of genes involved in early cell fate decisions in human embryos and their regulation by growth factors. Reproduction. 2008;135:635–47.PubMedCrossRef
23.
go back to reference Kimura Y, Yanagimachi R. Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development. 1995;121(8):2397–405.PubMed Kimura Y, Yanagimachi R. Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development. 1995;121(8):2397–405.PubMed
24.
go back to reference Klemetti R, Gissler M, Sevón T, Koivurova S, Ritvanen A, Hemminki E. Children born after assisted fertilization have an increased rate of major congenital anomalies. Fertil Steril. 2005;84:1300–7.PubMedCrossRef Klemetti R, Gissler M, Sevón T, Koivurova S, Ritvanen A, Hemminki E. Children born after assisted fertilization have an increased rate of major congenital anomalies. Fertil Steril. 2005;84:1300–7.PubMedCrossRef
25.
go back to reference Kohda T, Ogonuki N, Inoue K, Furuse T, Kaneda H, Suzuki T, et al. Intracytoplasmic sperm injection induces transcriptome perturbation without any transgenerational effect. Biochem Biophys Res Commun. 2011;410(2):282–8.PubMedCrossRef Kohda T, Ogonuki N, Inoue K, Furuse T, Kaneda H, Suzuki T, et al. Intracytoplasmic sperm injection induces transcriptome perturbation without any transgenerational effect. Biochem Biophys Res Commun. 2011;410(2):282–8.PubMedCrossRef
26.
go back to reference Liu F, Qiu Y, Zou Y, Deng ZH, Liu DY. Use of zona pellucida-bound sperm for intracytoplasmic sperm injection produces higher embryo quality and implantation than conventional intracytoplasmic sperm injection. Fertil Steril. 2011;95(2):815–8.PubMedCrossRef Liu F, Qiu Y, Zou Y, Deng ZH, Liu DY. Use of zona pellucida-bound sperm for intracytoplasmic sperm injection produces higher embryo quality and implantation than conventional intracytoplasmic sperm injection. Fertil Steril. 2011;95(2):815–8.PubMedCrossRef
27.
go back to reference Macas E, Imthurn B, Rosselli M, Keller PJ. The chromosomal complements of multipronuclear human zygotes resulting from intracytoplasmic sperm injection. Hum Reprod. 1996;11:2496–501.PubMedCrossRef Macas E, Imthurn B, Rosselli M, Keller PJ. The chromosomal complements of multipronuclear human zygotes resulting from intracytoplasmic sperm injection. Hum Reprod. 1996;11:2496–501.PubMedCrossRef
28.
go back to reference Mann MR, Lee SS, Doherty AS, Verona RI, Nolen LD, Schultz RM, et al. Selective loss of imprinting in the placenta following preimplantation development in culture. Development. 2004;131(15):3727–35.PubMedCrossRef Mann MR, Lee SS, Doherty AS, Verona RI, Nolen LD, Schultz RM, et al. Selective loss of imprinting in the placenta following preimplantation development in culture. Development. 2004;131(15):3727–35.PubMedCrossRef
29.
go back to reference Martin-Du Pan RC, Sakkas D, Stalberg A, Bianchi PG, de Boccard G, Campana A. Treatment of male sterility using intra-oocytic sperm injection: critical evaluation. Schweiz Med Wochenschr. 1995;125:1483–8.PubMed Martin-Du Pan RC, Sakkas D, Stalberg A, Bianchi PG, de Boccard G, Campana A. Treatment of male sterility using intra-oocytic sperm injection: critical evaluation. Schweiz Med Wochenschr. 1995;125:1483–8.PubMed
30.
go back to reference Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct-4. Cell. 1998;95:379–91.PubMedCrossRef Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct-4. Cell. 1998;95:379–91.PubMedCrossRef
31.
go back to reference Olson CK, Keppler-Noreuil KM, Romitti PA, Budelier WT, Ryan G, Sparks AE, et al. In vitro fertilization is associated with an increase in major birth defects. Fertil Steril. 2005;84:1308–15.PubMedCrossRef Olson CK, Keppler-Noreuil KM, Romitti PA, Budelier WT, Ryan G, Sparks AE, et al. In vitro fertilization is associated with an increase in major birth defects. Fertil Steril. 2005;84:1308–15.PubMedCrossRef
32.
go back to reference Ozil JP, Banrezes B, Tóth S, Pan H, Schultz RM. Ca2+ oscillatory pattern in fertilized mouse eggs affects gene expression and development to term. Dev Biol. 2006;300(534–544):51. Ozil JP, Banrezes B, Tóth S, Pan H, Schultz RM. Ca2+ oscillatory pattern in fertilized mouse eggs affects gene expression and development to term. Dev Biol. 2006;300(534–544):51.
33.
go back to reference Paes Almeida Ferreira de Braga D, Iaconelli Jr A, Sávio C, de Figueira R, Madaschi C, Semião-Francisco L, et al. Outcome of ICSI using zona pellucida-bound spermatozoa and conventionally selected spermatozoa. Reprod Biomed Online. 2009;19:802–7.PubMedCrossRef Paes Almeida Ferreira de Braga D, Iaconelli Jr A, Sávio C, de Figueira R, Madaschi C, Semião-Francisco L, et al. Outcome of ICSI using zona pellucida-bound spermatozoa and conventionally selected spermatozoa. Reprod Biomed Online. 2009;19:802–7.PubMedCrossRef
34.
go back to reference Palermo G, Joris H, Devroey P, Van Steirteghem AC. Induction of acrosome reaction in human spermatozoa used for subzonal insemination. Hum Reprod. 1992;7:248–54.PubMed Palermo G, Joris H, Devroey P, Van Steirteghem AC. Induction of acrosome reaction in human spermatozoa used for subzonal insemination. Hum Reprod. 1992;7:248–54.PubMed
35.
go back to reference Palmieri SL, Peter W, Hess H, Scholer HR. Oct-4 transcription factor is differently expressed in the mouse embryo during establishment of the first two extraembryonic cell lineages involved in implantation. Dev Biol. 1994;166:259–67.PubMedCrossRef Palmieri SL, Peter W, Hess H, Scholer HR. Oct-4 transcription factor is differently expressed in the mouse embryo during establishment of the first two extraembryonic cell lineages involved in implantation. Dev Biol. 1994;166:259–67.PubMedCrossRef
36.
go back to reference Piotrowska K, Zernicka-Goetz M. Role for sperm in spatial patterning of the early mouse embryo. Nature. 2001;409:517–21.PubMedCrossRef Piotrowska K, Zernicka-Goetz M. Role for sperm in spatial patterning of the early mouse embryo. Nature. 2001;409:517–21.PubMedCrossRef
37.
go back to reference Piotrowska K, Zernicka-Goetz M. Early patterning of the mouse embryo–contributions of sperm and egg. Development. 2002;129(24):5803–13.PubMedCrossRef Piotrowska K, Zernicka-Goetz M. Early patterning of the mouse embryo–contributions of sperm and egg. Development. 2002;129(24):5803–13.PubMedCrossRef
38.
go back to reference Piotrowska-Nitsche K, Yang SH, Banta H, Chan AWS. Assisted fertilization and embryonic axis formation in higher primates. Reprod Biomed Online. 2009;18:382–90.PubMedCrossRef Piotrowska-Nitsche K, Yang SH, Banta H, Chan AWS. Assisted fertilization and embryonic axis formation in higher primates. Reprod Biomed Online. 2009;18:382–90.PubMedCrossRef
39.
go back to reference Plusa B, Piotrowska K, Zernicka-Goetz M. The first cleavage plane of the mouse zygote passes close by the sperm entry point defined by several labelling techniques. Genesis. 2002;32:193–8.PubMedCrossRef Plusa B, Piotrowska K, Zernicka-Goetz M. The first cleavage plane of the mouse zygote passes close by the sperm entry point defined by several labelling techniques. Genesis. 2002;32:193–8.PubMedCrossRef
40.
go back to reference Qiao J, Chen Y, Yan LY, Yan J, Liu P, Sun QY. Changes in histone methylation during human oocyte maturation and IVF- or ICSI-derived embryo development. Fertil Steril. 2010;93(5):1628–36.PubMedCrossRef Qiao J, Chen Y, Yan LY, Yan J, Liu P, Sun QY. Changes in histone methylation during human oocyte maturation and IVF- or ICSI-derived embryo development. Fertil Steril. 2010;93(5):1628–36.PubMedCrossRef
41.
go back to reference Rienzi L, Ubaldi F, Martinez F, Iacobelli M, Minasi MG, Ferrero S, et al. Relationship between meiotic spindle location with regard to the polar body position and oocyte developmental potential after ICSI. Hum Reprod. 2003;18:1289–93.PubMedCrossRef Rienzi L, Ubaldi F, Martinez F, Iacobelli M, Minasi MG, Ferrero S, et al. Relationship between meiotic spindle location with regard to the polar body position and oocyte developmental potential after ICSI. Hum Reprod. 2003;18:1289–93.PubMedCrossRef
42.
go back to reference Rinaudo P, Schultz RM. Effects of embryo culture on global pattern of gene expression in preimplantation mouse embryos. Reproduction. 2004;128(3):301–11.PubMedCrossRef Rinaudo P, Schultz RM. Effects of embryo culture on global pattern of gene expression in preimplantation mouse embryos. Reproduction. 2004;128(3):301–11.PubMedCrossRef
43.
go back to reference Rinaudo P, Giritharan G, Talbi S, Dobson AT, Schultz RM. Effects of oxygen tension on gene expression in preimplantation mouse embryos. Fertil Steril. 2006;86(4 Suppl):1252–65.PubMed Rinaudo P, Giritharan G, Talbi S, Dobson AT, Schultz RM. Effects of oxygen tension on gene expression in preimplantation mouse embryos. Fertil Steril. 2006;86(4 Suppl):1252–65.PubMed
44.
go back to reference Ruiz de Assin R, Clavero A, Gonzalvo MC, Ramírez JP, Zamora S, Fernández A, et al. Comparison of methods to determine the assigned value in an external quality control programme for embryo evaluation. Reprod Biomed Online. 2009;19:824–9.PubMedCrossRef Ruiz de Assin R, Clavero A, Gonzalvo MC, Ramírez JP, Zamora S, Fernández A, et al. Comparison of methods to determine the assigned value in an external quality control programme for embryo evaluation. Reprod Biomed Online. 2009;19:824–9.PubMedCrossRef
45.
go back to reference Santos F, Hyslop L, Stojkovic P, Leary C, Murdoch A, Reik W, et al. Evaluation of epigenetic marks in human embryos derived from IVF and ICSI. Hum Reprod. 2010;25(9):2387–95.PubMedCrossRef Santos F, Hyslop L, Stojkovic P, Leary C, Murdoch A, Reik W, et al. Evaluation of epigenetic marks in human embryos derived from IVF and ICSI. Hum Reprod. 2010;25(9):2387–95.PubMedCrossRef
46.
go back to reference Scholer HR, Hatzopoulous AK, Balling R, Suzuki N, Gruss P. A family of octamer-specific proteins present during mouse embryogenesis: evidence for germ-line specific expression of an Oct factor. EMBO J. 1989;8:2543–50.PubMed Scholer HR, Hatzopoulous AK, Balling R, Suzuki N, Gruss P. A family of octamer-specific proteins present during mouse embryogenesis: evidence for germ-line specific expression of an Oct factor. EMBO J. 1989;8:2543–50.PubMed
47.
go back to reference Scott L. The biological basis of non-invasive strategies for selection of human oocytes and embryos. Hum Reprod Update. 2003;9:237–49.PubMedCrossRef Scott L. The biological basis of non-invasive strategies for selection of human oocytes and embryos. Hum Reprod Update. 2003;9:237–49.PubMedCrossRef
48.
go back to reference Silva CP, Kommineni K, Oldenbourg R, Keefe DL. The first polar body does not predict accurately the location of the metaphase II meiotic spindle in mammalian oocytes. Fertil Steril. 1999;71:719–21.PubMedCrossRef Silva CP, Kommineni K, Oldenbourg R, Keefe DL. The first polar body does not predict accurately the location of the metaphase II meiotic spindle in mammalian oocytes. Fertil Steril. 1999;71:719–21.PubMedCrossRef
49.
go back to reference Steptoe P, Edwards RG. Birth after the reimplantation of a Human Embryo. The Lancet. 1978;312(8085):366.CrossRef Steptoe P, Edwards RG. Birth after the reimplantation of a Human Embryo. The Lancet. 1978;312(8085):366.CrossRef
50.
go back to reference Tesarik J, Rolet F, Brami C, Sedbon E, Thorel J, Tibi C, et al. Spermatid injection into human oocytes. II. Clinical application in the treatment of infertility due to non-obstructive azoospermia. Hum Reprod. 1996;11(4):780–3.PubMedCrossRef Tesarik J, Rolet F, Brami C, Sedbon E, Thorel J, Tibi C, et al. Spermatid injection into human oocytes. II. Clinical application in the treatment of infertility due to non-obstructive azoospermia. Hum Reprod. 1996;11(4):780–3.PubMedCrossRef
51.
go back to reference Turan N, Katari S, Gerson LF, Chalian R, Foster MW, Gaughan JP, et al. Inter- and intra-individual variation in allele-specific DNA methylation and gene expression in children conceived using assisted reproductive technology. PLoS Genet. 2010;6(7):e1001033.PubMedCrossRef Turan N, Katari S, Gerson LF, Chalian R, Foster MW, Gaughan JP, et al. Inter- and intra-individual variation in allele-specific DNA methylation and gene expression in children conceived using assisted reproductive technology. PLoS Genet. 2010;6(7):e1001033.PubMedCrossRef
52.
go back to reference Wong CC, Loewke KE, Bossert NL, Behr B, De Jonge CJ, Baer TM, et al. Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat Biotechnol. 2010;28(10):1115–21.PubMedCrossRef Wong CC, Loewke KE, Bossert NL, Behr B, De Jonge CJ, Baer TM, et al. Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat Biotechnol. 2010;28(10):1115–21.PubMedCrossRef
Metadata
Title
Effect of sperm entry on blastocyst development after in vitro fertilization and intracytoplasmic sperm injection — mouse model
Authors
Karolina Piotrowska-Nitsche
Anthony W. S. Chan
Publication date
01-01-2013
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 1/2013
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-012-9896-6

Other articles of this Issue 1/2013

Journal of Assisted Reproduction and Genetics 1/2013 Go to the issue