Paternal influence of sperm DNA integrity on early embryonic development

Lee, Simon; Murphy, Kristin; Shamsi, Monis Bilal; Liu, L.; Emery, Benjamin R.; Aston, Kenneth I.; Hotaling, James M.; Carrell, Douglas T.

doi:10.1093/humrep/deu228

Cited by 235 publications

(204 citation statements)

References 67 publications

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“…It is well known that dysfunction in the sperm negatively affects the development of embryos [12,51,52]. The present study supports the hypothesis that the impact of male infertility may be related not only to zygote and early cleavage-stage morphological abnormalities (early paternal effect) but also to poor developmental competence which in turn might lead to implantation failure due to disorganization of the chromatin and/or a high level of sperm DNA fragmentation.…”

Section: Discussionsupporting

confidence: 87%

The impact of paternal factors on cleavage stage and blastocyst development analyzed by time-lapse imaging—a retrospective observational study

Neyer

Zintz

Stecher

et al. 2015

J Assist Reprod Genet

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Purpose Various time-lapse studies have postulated embryo selection criteria based on early morphokinetic markers. However, late paternal effects are mostly not visible before embryonic genome activation. The primary objective of this retrospective study was to investigate whether those early morphokinetic algorithms investigated by time-lapse imaging are reliable enough to allow for the accurate selection of those embryos that develop into blastocysts, while of course taking into account the correlation with the type of injected spermatozoa. Methods During a period of 18 months, a total of 461 MII oocytes from 43 couples with severe male factor infertility and previous Bexternal^IVF failures after cleavage-stage embryo transfer (ET) were fertilized by intracytoplasmic morphologically selected sperm injection (IMSI). Thereof, 373 embryos were monitored in a time-lapse incubator until ET on day 5. Blastocyst outcome in combination with three previously postulated MKc (cc2: t3-t2, 5-12 h; t3, 35-40 h; t5, 48-56 h) and the morphology of the selected sperm were analyzed. Results A significant increase in the rate of blastocysts (54.0 vs. 36.3 %; P<0.01) and top blastocysts (25.3 vs. 10.8 %; P<0.001) was observed in the group of those meeting all three morphokinetic criteria (MKc3). However, MKc3 were only met in 23.3 % of all embryos. Moreover, TBR was influenced by the type of injected spermatozoa. In both groups, TBR decreased dramatically (MKc3, 35.0 vs. 17.0 %; MKc<3, 14.2 vs. 8.4 %) when class II/III sperm instead of class I were injected. Conclusion Early morphokinetic parameters might give some predictive information but fail to serve as a feasible selective tool for the prediction of blastocyst development given the influence of the type of spermatozoa injected.

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Section: Discussionsupporting

confidence: 87%

The impact of paternal factors on cleavage stage and blastocyst development analyzed by time-lapse imaging—a retrospective observational study

Neyer

Zintz

Stecher

et al. 2015

J Assist Reprod Genet

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“…One of the critical factors that is known to play an important role in pregnancy and subsequent embryo development is sperm DNA integrity [Kumar et al 2013;Menezo 2006;Puscheck and Jeyendran 2007;Sakkas and Alvarez 2010;Simon et al 2014]. The deleterious effect of fragmented paternal DNA on embryonic viability and progression of pregnancy has been experimentally shown in mouse models [Ahmadi and Ng 1999] and similar results were also observed in human patients who opt for assisted reproductive technologies such as IVF and ICSI [Lin et al 2008;Muriel et al 2006;Robinson et al 2012;Tandara et al 2014;Tesarik et al 2004;Wdowiak et al 2015;Zhao et al 2014;Zini et al 2008].…”

Section: Introductionmentioning

confidence: 90%

Histone retention, protein carbonylation, and lipid peroxidation in spermatozoa: Possible role in recurrent pregnancy loss

Mohanty

Swain

Goswami

et al. 2016

Systems Biology in Reproductive Medicine

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Contribution from a defective paternal genome has been attributed to be an important cause for spontaneous recurrent pregnancy loss (RPL). Increased oxidative stress results in decreased detoxification and is a cause for damage to chromatin, proteins, and membrane lipids. The present study aimed to explore if there is a significant relationship between retained histones due to defective packaging of DNA in spermatozoa and oxidative stress. RPL patients (n=16) with a history of ≥2 embryo losses before the 20th week of gestation and no female factor abnormality, and fertile healthy volunteers (n=20) as controls were included in the study. A significant difference in the levels of protein carbonylation and lipid peroxidation together with an increased retention of histones in the experimental groups was noticed. Histone carrying sites for oxidative modification such as arginine and lysine might be responsible for disturbing the paternal epigenomic control during early stages of embryonic differentiation leading to abortion. ARTICLE HISTORY

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“…Moreover, it is possible that altered sperm DNA integrity has an impact on early embryonic development according to studies reporting a reduction of embryo morphokinetic parameters [45,46], a reduced implantation rate, [47] and a poor embryo's post-implantation development resulting in pregnancy loss [48]. The study of Sivanarayana et al [49] showed that sperms with abnormal forms (elongated, thin, round, pyri, amorphous, micro-, and macro-forms) and abnormal motility parameters were significantly associated with a higher DNA fragmentation index [49].…”

Section: Dna Fragmentationmentioning

confidence: 99%

The Impact of Aging on Fertility: Similarities and Differences between Ovaries and Testes

Albu¹,

Albu²

2017

Testes and Ovaries - Functional and Clinical Differences and Similarities

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The increasing age seems to have a negative impact on reproductive functions not only in women but also in men. Therefore, our aim was to review the data available in the literature regarding the impact of advancing age on fertility and the mechanisms underlying this association in both genders. The available data suggest that the effects of age on ovarian function cause a decrease in fertility starting 13 years before menopause. Statistics show that 10% of women will have a decreased fertility starting with the age of 30. The impact of age on ovary is due to both decreased number and quality of the oocytes, resulting in a high rate of chromosomal aneuploidy in the embryo and mitochondria dysfunction. Assisted reproductive technologies aiming to identify competent embryo were created but for the moment the results are unsatisfactory. On the other hand, in men, the semen quality and testicular function were found to gradually decrease with age and most of the studies also describe a negative impact on fertility. The mechanisms underlying decreased fertility are mainly genetic and epigenetics changes. However, if the effects of age on male fertility in men can be overcome by assisted reproductive technologies is not clear yet as the results of the studies are inconsistent.

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Paternal influence of sperm DNA integrity on early embryonic development

Abstract: N/A.

Cited by 235 publications

References 67 publications

The impact of paternal factors on cleavage stage and blastocyst development analyzed by time-lapse imaging—a retrospective observational study

The impact of paternal factors on cleavage stage and blastocyst development analyzed by time-lapse imaging—a retrospective observational study

Histone retention, protein carbonylation, and lipid peroxidation in spermatozoa: Possible role in recurrent pregnancy loss

The Impact of Aging on Fertility: Similarities and Differences between Ovaries and Testes

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