Protamine 1 to protamine 2 ratio correlates with dynamic aspects of DNA fragmentation in human sperm

García-Peiró, Agustín; Martínez-Heredia, Juan; Oliver-Bonet, María; Abad, Carlos; Amengual, M. J.; Navarro, J.; Jones, Céline; Coward, Kevin; Gosálvez, Jaime; Benet, Jordi

doi:10.1016/j.fertnstert.2010.06.053

Cited by 94 publications

(73 citation statements)

References 38 publications

(48 reference statements)

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“…On the other hand, a number of studies have reported that protamine deficiency could also deteriorate chromatin tight packaging and increase susceptibility to external stress resulting in increased risk of higher sperm DNA damage (Oliva, 2006;Garcia-Peiro et al, 2011;Ni et al, 2014). To date, the most common methods to analyze protamine deficiency are CMA3 staining and protamine ratio, which were proved to be closely associated with sperm DNA damage (Aoki et al, 2005b;Nili et al, 2009;Tavalaee et al, 2009;Garcia-Peiro et al, 2011;Manochantr et al, 2012;Ni et al, 2014). Therefore, we also systematically analyzed the association between protamine deficiency and sperm DNA damage in this meta-analysis.…”

Section: Discussionmentioning

confidence: 99%

“…A total of nine studies with 633 patients and 463 controls in the first part, which fulfilled all of the inclusion criteria, were considered for the analysis. Five of the studies were prospective (de Mateo et al, 2009;Garcia-Peiro et al, 2011;Rogenhofer et al, 2013;Ni et al, 2014;Savadi-Shiraz et al, 2015) and four were retrospective (Mengual et al, 2003;Aoki et al, 2005aAoki et al, , 2006aSteger et al, 2008). Four studies used real-time RT-qPCR (mRNA) (Steger et al, 2008;Rogenhofer et al, 2013;Ni et al, 2014;Savadi-Shiraz et al, 2015) and five studies employed PAGE (protein) (Mengual et al, 2003;Aoki et al, 2005aAoki et al, , 2006ade Mateo et al, 2009;Garcia-Peiro et al, 2011) to calculate the protamine ratio.…”

Section: Study Design Characteristicsmentioning

confidence: 99%

“…Four studies used real-time RT-qPCR (mRNA) (Steger et al, 2008;Rogenhofer et al, 2013;Ni et al, 2014;Savadi-Shiraz et al, 2015) and five studies employed PAGE (protein) (Mengual et al, 2003;Aoki et al, 2005aAoki et al, , 2006ade Mateo et al, 2009;Garcia-Peiro et al, 2011) to calculate the protamine ratio. When comparing the differences in the protamine ratio between experimental and control groups, two studies compared normozoospermic healthy donors with subfertile patients (Steger et al, 2008;Savadi-Shiraz et al, 2015), five studies compared proven fertile donors with subfertile patients (Mengual et al, 2003;Aoki et al, 2005aAoki et al, , 2006ade Mateo et al, 2009;Garcia-Peiro et al, 2011), one study compared groups of men contributing to successful fertilization with those involved in fertilization failure after IVF and ICSI treatment (Rogenhofer et al, 2013), and one study compared spontaneous pregnant couples with non-pregnant couples (Ni et al, 2014). In the second part, the total number of studies included in the review was 12 comprising of 845 participants.…”

Section: Study Design Characteristicsmentioning

confidence: 99%

“…In the second part, the total number of studies included in the review was 12 comprising of 845 participants. Eight of the studies were prospective (De Iuliis et al, 2009;Tarozzi et al, 2009;Tavalaee et al, 2009;Razavi et al, 2010;Garcia-Peiro et al, 2011;Ni et The studies scored well on the Newcastle-Ottawa Quality Assessment Scale. Four studies scored up to 8 and five studies scored 7 in the first part, while in the second part one study scored 8, eight studies scored 7, and three studies scored 6.…”

Section: Study Design Characteristicsmentioning

confidence: 99%

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The impact of sperm protamine deficiency and sperm DNA damage on human male fertility: a systematic review and meta-analysis

et al. 2016

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SUMMARYExisting literature suggests evidence that protamine deficiency is related to DNA damage and male fertility. In this meta-analysis, we analyzed the relationship between the ratio of protamine-1 and protamine-2 with male fertility and the association of protamine deficiency with sperm DNA damage. Quality of available cohort studies was evaluated using the Newcastle-Ottawa Scale checklist. Summary effect estimates with 95% confidence intervals (CI) were derived using a random effects model. The effect of the protamine ratio on male fertility was analyzed in nine studies demonstrating a significantly higher value of the protamine ratio in subfertile men (n = 633) when compared with controls (n = 453, SMD = 0.46, 95% CI 0.25-0.66, Z = 4.42, p < 0.00001). Both protamine mRNA (SMD = 0.45, 95% CI 0.11-0.79, Z = 2.63, p = 0.009) and protein ratio (SMD = 0.46, 95% CI 0.25-0.68, Z = 4.22, p < 0.0001) showed significantly increased values in subfertile patients. The association between protamine deficiency and DNA damage was analyzed in 12 studies (n = 845) exhibiting a combined overall correlation coefficient (COR) of 0.53 (95% CI 0.28-0.71, Z = 3.87, p < 0.001). Protamine deficiency measured by CMA3 staining was significantly associated with sperm DNA damage (COR = 0.71, 95% CI 0.48-0.85, Z = 4.87, p < 0.001), whereas the P1/P2 ratio was not (COR = 0.17, 95% CI À0.16 to 0.46, Z = 0.99, p = 0.33). It is concluded that the protamine ratio represents a suitable biomarker for the assessment of sperm quality and protamine deficiency is closely related with sperm DNA damage.

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Section: Discussionmentioning

confidence: 99%

Section: Study Design Characteristicsmentioning

confidence: 99%

Section: Study Design Characteristicsmentioning

confidence: 99%

Section: Study Design Characteristicsmentioning

confidence: 99%

See 2 more Smart Citations

The impact of sperm protamine deficiency and sperm DNA damage on human male fertility: a systematic review and meta-analysis

et al. 2016

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“…26,27 Additionally, the sensitivity (true positive) and specificity (1: false positive) of using SDF as a predictor of pregnancy varies among different laboratories and is likely to be dependent on the type of ART employed and the varying skill of individual clinicians (see, for example, Tables 3 and 4 in Zini and Sigman 28 and Zini 29 ). This inconsistency is probably due to the fact that the genesis of SDF in the male is not a consequence of a single factor but of a series of inter-related events including defective spermatogenesis during chromatin remodelling, the interaction of spermatozoa with oxidative stress, exposure to bacterial infections, the presence of chromosomal abnormalities, 30 constitutive genetic conditions, 31,32 genomic modifications, such as telomere-shortening 33 or environmental stress. 34 The predictive value of SDF is also influenced by the quality and competence of the oocyte, and the capacity of the female gamete to repair sperm DNA damage following syngamy.…”

Section: Introductionmentioning

confidence: 99%

Can DNA fragmentation of neat or swim-up spermatozoa be used to predict pregnancy following ICSI of fertile oocyte donors?

Gosálvez

Caballero²,

López‐Fernández³

et al. 2013

Asian J Androl

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This study compared the potential of assessing sperm DNA fragmentation (SDF) from neat semen and the subsequent swim-up (SU) procedure to predict pregnancy when conducting ICSI of fertile donor oocytes. Infertile females (n581) were transferred embryos resulting from intracytoplasmic sperm injection (ICSI) of their partner's spermatozoa and proven donor oocytes. This model normalized the impact of female factor in putative sperm DNA repair. Semen was blindly assessed for SDF using Halosperm immediately following ejaculation (NS) and after swim-up at the time of ICSI fertilisation. There was a decrease in SDF values of the ejaculated semen sample following the swim-up protocol (P50.000). Interestingly, pregnancy could be equally predicted from SDF values derived from either neat or swim-up semen samples. Receiver operator curves and the derived Youden's indices determined SDF cutoff values for NS and SU of 24.8% and 17.5%, respectively. Prediction of pregnancy from NS SDF had a sensitivity of 75% and a specificity of 69%, whereas for SU SDF was 78% and 73%, respectively. While increased levels of SDF negatively impact reproductive outcome, we have shown that a reduction in SDF following sperm selection using ICSI with proven donor oocytes is not mandatory for achieving pregnancy. This suggests that a certain level of DNA damage that is not detectable using current technologies could be impacting on the relative success of assisted reproductive technology (ART) procedures. Consequently, we propose a modification of the so called 'iceberg model' as a possible rationale for understanding the role of SDF in reproductive outcome.

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Relationships between the dynamics of iatrogenic DNA damage and genomic design in mammalian spermatozoa from eleven species

Gosálvez

López‐Fernández

Fernández

et al. 2011

Molecular Reproduction Devel

129

110

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The dynamic onset of DNA fragmentation in mammalian sperm populations varies widely in different species when the spermatozoa are incubated in vitro at body temperature for several hours, and recent studies have shown that the dynamic rate of DNA fragmentation within a species has considerable predictive value in terms of fertility. The reasons for such variation are unclear, but here we show that differences in protamine sequence and identity could be partially responsible. Sets of 10 normal semen samples from 11 species (ram, goat, boar, white-tailed deer, rabbit, human, domestic and Spanish fighting bull, horse, donkey, rhinoceros, and koala) were cryopreserved, thawed, diluted in an appropriate extender for each species, and then incubated for 4 hr at 37 °C. Semen samples from human infertility patients were also included for comparison with the donors. DNA fragmentation analysis was undertaken immediately after thawing (t(0)) and after 4 hr (t(4)) using the Halomax/Halosperm procedure, and the differences in DNA fragmentation between t(0) and t(4) were examined in the context of the respective protamine genomes. The expression of protamine 2 in a species significantly enhanced the likelihood of sperm DNA fragmentation; greater numbers of cysteine residues in protamine 1 tended to confer increased sperm DNA stability, and there were logical evolutionary relationships between species in terms of their sperm DNA stability. Human spermatozoa from infertility patients exhibited considerably higher DNA instability than the normal semen donors, a difference that could be indirectly attributed to unbalanced protamine 1-to-protamine 2 ratios.

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Protamine 1 to protamine 2 ratio correlates with dynamic aspects of DNA fragmentation in human sperm

Cited by 94 publications

References 38 publications

The impact of sperm protamine deficiency and sperm DNA damage on human male fertility: a systematic review and meta-analysis

The impact of sperm protamine deficiency and sperm DNA damage on human male fertility: a systematic review and meta-analysis

Can DNA fragmentation of neat or swim-up spermatozoa be used to predict pregnancy following ICSI of fertile oocyte donors?

Relationships between the dynamics of iatrogenic DNA damage and genomic design in mammalian spermatozoa from eleven species

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