Sperm phenotypic characteristics and oviduct binding ability are altered in breeding bulls with high sperm DNA fragmentation index

Nag, Pranab Kumar; Kumaresan, A.; Akshaya, Sivamanikandan; Manimaran, A.; Rajendran, D.; Paul, Nilendu; Sharma, Ankur; Karuthadurai, Thirumalaisamy; Kaustubh, Saraf; Jeyakumar, Sakthivel; Ramesha, K. P.

doi:10.1016/j.theriogenology.2021.06.006

Cited by 16 publications

(13 citation statements)

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“…Several reasons are attributed to the decreased fertility of cryopreserved semen, primarily damage that occurs in spermatozoa during cryopreservation (cryodamage), which alters its fertilising potential ( Cormier et al, 1997 ; Watson, 2000 ; Yeste, 2016 ). The process of cryopreservation results in the death of almost 50% of spermatozoa, while the remaining sperm population shows altered functional competencies ( Kumaresan et al, 2011 ; Kumaresan et al, 2012 ; Singh et al, 2016 ; Kumaresan et al, 2017 ; Saraf et al, 2019 ; Rather et al, 2020 ; Vignesh et al, 2020 ; Nag et al, 2021 ), which might be linked to the reduced fertility of cryopreserved semen. However, the fertility of cryopreserved semen subjected to sperm selection methods (for the selection of viable, active, and phenotypically normal spermatozoa) was also not as good as that of fresh semen, although some improvement in fertility was observed ( Said and Land, 2011 ; Marzano et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Cryopreservation process alters the expression of genes involved in pathways associated with the fertility of bull spermatozoa

et al. 2022

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In bovines, cryopreserved semen is used for artificial insemination; however, the fertility of cryopreserved semen is far lower than that of fresh semen. Although cryopreservation alters sperm phenotypic characteristics, its effect on sperm molecular health is not thoroughly understood. The present study applied next-generation sequencing to investigate the effect of cryopreservation on the sperm transcriptomic composition of bull spermatozoa. While freshly ejaculated bull spermatozoa showed 14,280 transcripts, cryopreserved spermatozoa showed only 12,375 transcripts. Comparative analysis revealed that 241 genes were upregulated, 662 genes were downregulated, and 215 genes showed neutral expression in cryopreserved spermatozoa compared to fresh spermatozoa. Gene ontology analysis indicated that the dysregulated transcripts were involved in nucleic acid binding, transcription-specific activity, and protein kinase binding involving protein autophosphorylation, ventricular septum morphogenesis, and organ development. Moreover, the dysregulated genes in cryopreserved spermatozoa were involved in pathways associated with glycogen metabolism, MAPK signalling, embryonic organ morphogenesis, ectodermal placode formation, and regulation of protein auto-phosphorylation. These findings suggest that the cryopreservation process induced alterations in the abundance of sperm transcripts related to potential fertility-associated functions and pathways, which might partly explain the reduced fertility observed with cryopreserved bull spermatozoa.

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Section: Introductionmentioning

confidence: 99%

Cryopreservation process alters the expression of genes involved in pathways associated with the fertility of bull spermatozoa

et al. 2022

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“…A plethora of in vitro studies supports this narrative (see Table 2). Overall, they show that OECs preferentially bind uncapacitated sperm [64,93,100,101] with higher DNA integrity [102,103]. Some of the differences observed between bound and free-swimming sperm were detected only after 3 minute of incubation [93].…”

Section: Boar Ex Vivo Oviduct Explantmentioning

confidence: 89%

Sperm selection by the oviduct: perspectives for male fertility and assisted reproductive technologies

Soto-Heras

Sakkas

Miller

2023

Biology of Reproduction

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The contribution of sperm to embryogenesis is gaining attention with up to 50% of infertility cases being attributed to a paternal factor. The traditional methods used in assisted reproductive technologies (ART) for selecting and assessing sperm quality are mainly based on motility and viability parameters. However, other sperm characteristics, including DNA integrity, have major consequences for successful live birth. In natural reproduction, sperm navigate the male and female reproductive tract to reach and fertilize the egg. During transport, sperm encounter many obstacles that dramatically reduce the number arriving at the fertilization site. In humans, the number of sperm is reduced from tens of millions in the ejaculate to hundreds in the Fallopian tube (oviduct). Whether this sperm population has higher fertilization potential is not fully understood, but several studies in animals indicate that many defective sperm do not advance to the site of fertilization. Moreover, the oviduct plays a key role in fertility by modulating sperm transport, viability, and maturation, providing sperm that are ready to fertilize at the appropriate time. Here we present evidence of sperm selection by the oviduct with emphasis on the mechanisms of selection and the sperm characteristics selected. Considering the sperm parameters that are essential for healthy embryonic development, we discuss the use of novel in vitro sperm selection methods that mimic physiological conditions. We propose that insight gained from understanding how the oviduct selects sperm can be translated to ART to yield high fertilization, embryonic development, and pregnancy rates.

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“…Karoui and co-authors found a negative association between bull fertility and sperm DNA fragmentation using the halo test ( 78 ). DNA integrity is essential for bovine embryonic development ( 79 ), and DFI is negatively correlated with sperm binding index and conception rates ( 80 ). Interestingly, the sperm viability and motility become affected earlier than DNA, and occurrence of single-stranded DNA breaks happens in parallel with chromatin decondensation and deprotamination ( 81 ).…”

Section: Discussionmentioning

confidence: 99%

Systematic review and meta-analysis of cryopreserved bovine sperm assessment: harnessing imaging flow cytometry for multi-parametric analysis

Umirbaeva,

Kurenkov,

Makhanbetova

et al. 2024

Front. Vet. Sci.

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Cryopreservation of sperm is an essential technique in assisted reproduction in cattle. The objective of the study was to systematically review and synthesize the literature on bull semen quality evaluation based on the comparison of morphological and metabolic parameters of cryopreserved bovine spermatozoa such as DNA integrity, mitochondrial status, plasma membrane alterations, total motility, and morphology (% of abnormal cells). The electronic databases PubMed, Web of Sciences, Scopus, and Google Scholar were searched up to December 2023. Studies and references were included if they reported the following parameters: DNA integrity, mitochondrial status, plasma membrane alterations, total motility, and morphological aberrations (% of abnormal cells) for conventional cryopreserved bovine spermatozoa. After an electronic search, out of 1,526 original studies, only 40 were included in the meta-analysis. Standardized mean differences (SMD) with 95% confidence intervals were estimated for the chosen studies, and a meta-analysis was performed using a random effects model. The tau-squared (tau2) and inconsistency index (I2) quantified heterogeneity among different studies. The regression analysis for the evaluated parameters showed a positive correlation between mitochondrial membrane potential (MMP), total motility, and abnormal morphology and a negative correlation between DNA fragmentation index (DFI) and total motility and MMP. Moreover, subgroup analysis demonstrated similar associations for dairy and non-dairy bull breeds, albeit with lower I2 values. The presence of publication bias was confirmed by Egger’s test, except for the MMP parameter. A multi-parametric analysis of morphological and metabolic parameters can address the existing limitations of cryopreserved bovine spermatozoa quality assessment. Combining imaging flow cytometry (IFC) with standardization of sperm pre-processing and optimization of the experimental protocols may help to differentiate sperm from cellular debris and cytoplasmic droplets of similar size and alleviate limitations demonstrated by conventional sperm analysis.

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Sperm phenotypic characteristics and oviduct binding ability are altered in breeding bulls with high sperm DNA fragmentation index

Cited by 16 publications

References 61 publications

Cryopreservation process alters the expression of genes involved in pathways associated with the fertility of bull spermatozoa

Cryopreservation process alters the expression of genes involved in pathways associated with the fertility of bull spermatozoa

Sperm selection by the oviduct: perspectives for male fertility and assisted reproductive technologies

Systematic review and meta-analysis of cryopreserved bovine sperm assessment: harnessing imaging flow cytometry for multi-parametric analysis

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