Sperm DNA Integrity and Male Fertility in Farm Animals: A Review

Kumaresan, A.; Gupta, Mohua Das; Datta, Tirtha Kumar; Morrell, Jane M.

doi:10.3389/fvets.2020.00321

Cited by 77 publications

(57 citation statements)

References 182 publications

(161 reference statements)

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“…The GWAS has been previously used to aid the identification of genetic variants underlying reduced male reproductive performance as well as of candidate genes for semen traits in human [ 22 , 30 ], livestock [ 30 , 31 ], as well as in more suitable animal models, as pigs [ 14 , 15 ]. In either case, the rationale behind was to improve the identification of males suffering from idiophatic sub/infertility, despite providing ejaculates with values considered “within normal limits” [ 32 , 33 ].…”

Section: Discussionmentioning

confidence: 99%

“…This unexplained subfertility had led to calls over the years for more sophisticated semen analyses, aiding elimination of clearly subfertile sires [ 12 ]. Considering that the spermatozoa carries intact, healthy attributes that could define fertility when retrospectively related to the observed sire fertility [ 12 ], novel methods include omics of spermatozoa [ 13 , 14 , 15 ] and seminal plasma (SP, [ 7 ]), which is a trend also used in human andrology [ 16 ]. However, reliable prognosis for fertility in either species has remained elusive, often because the definition of fertility levels for a given male must indeed consider a plethora of confounding factors, including number of inseminated spermatozoa, intercourse frequency and, in pigs, an even number of females undergoing AI, number of AIs per oestrus, seasonality, the systems used to detect oestrus, farm characteristics, AI procedures, etc.…”

Section: Introductionmentioning

confidence: 99%

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Sperm Methylome Profiling Can Discern Fertility Levels in the Porcine Biomedical Model

Pértille

Álvarez‐Rodríguez

Silva

et al. 2021

IJMS

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A combined Genotyping By Sequencing (GBS) and methylated DNA immunoprecipitation (MeDIP) protocol was used to identify—in parallel—genetic variation (Genomic-Wide Association Studies (GWAS) and epigenetic differences of Differentially Methylated Regions (DMR) in the genome of spermatozoa from the porcine animal model. Breeding boars with good semen quality (n = 11) and specific and well-documented differences in fertility (farrowing rate, FR) and prolificacy (litter size, LS) (n = 7) in artificial insemination programs, using combined FR and LS, were categorized as High Fertile (HF, n = 4) or Low Fertile (LF, n = 3), and boars with Unknown Fertility (UF, n = 4) were tested for eventual epigenetical similarity with those fertility-proven. We identified 165,944 Single Nucleotide Polymorphisms (SNPs) that explained 14–15% of variance among selection lines. Between HF and LF individuals (n = 7, 4 HF and 3 LF), we identified 169 SNPs with p ≤ 0.00015, which explained 58% of the variance. For the epigenetic analyses, we considered fertility and period of ejaculate collection (late-summer and mid-autumn). Approximately three times more DMRs were observed in HF than in LF boars across these periods. Interestingly, UF boars were clearly clustered with one of the other HF or LF groups. The highest differences in DMRs between HF and LF experimental groups across the pig genome were located in the chr 3, 9, 13, and 16, with most DMRs being hypermethylated in LF boars. In both HF and LF boars, DMRs were mostly hypermethylated in late-summer compared to mid-autumn. Three overlaps were detected between SNPs (p ≤ 0.0005, n = 1318) and CpG sites within DMRs. In conclusion, fertility levels in breeding males including FR and LS can be discerned using methylome analyses. The findings in this biomedical animal model ought to be applied besides sire selection for andrological diagnosis of idiopathic sub/infertility.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Sperm Methylome Profiling Can Discern Fertility Levels in the Porcine Biomedical Model

Pértille

Álvarez‐Rodríguez

Silva

et al. 2021

IJMS

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“…The main task of the sperm cell is to deliver the paternal genome to an oocyte during fertilization. Sperm DNA integrity is crucial for successful fertilization and subsequent embryo development (Kumaresan et al, 2020). The sperm cell has a unique chromatin structure where most of the histones are replaced by smaller proteins, called protamines, during spermatogenesis (Champroux et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Sperm chromatin integrity and DNA methylation in Norwegian Red bulls of contrasting fertility

Narud

Khezri

Zeremichael

et al. 2021

Molecular Reproduction Devel

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In this study, the complexity of chromatin integrity was investigated in frozen‐thawed semen samples from 37 sires with contrasting fertility, expressed as 56‐day non‐return rates (NR56). Protamine deficiency, thiols, and disulfide bonds were assessed and compared with previously published data for DNA fragmentation index (DFI) and high DNA stainability (HDS). In addition, in vitro embryo development and sperm DNA methylation were assessed using semen samples from 16 of these bulls. The percentages of DFI and HDS were negatively associated with NR56 and cleavage rate and positively associated with sperm protamine deficiency (p < 0.05). Significant differences in cleavage and blastocyst rates were observed between bulls of high and low NR56. However, once fertilization occurred, further development into blastocysts was not associated with NR56. The differential methylation analysis showed that spermatozoa from bulls of low NR56 were hypermethylated compared to bulls of high NR56. Pathway analysis showed that genes annotated to differentially methylated cytosines could participate in different biological pathways and have important biological roles related to bull fertility. In conclusion, sperm cells from Norwegian Red bulls of inferior fertility have less compact chromatin structure, higher levels of DNA damage, and are hypermethylated compared with bulls of superior fertility.

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“…In artificial breeding, it is well-understood that sperm must possess some functionalities for successful fertilization of oocyte, which include, but not restricted to, motility to reach the site of fertilization ( 42 ) functional membrane integrity to establish sperm–oviduct reservoir ( 4 , 5 , 43 ) and sperm–oocyte binding ( 44 ) and intact non-reacted acrosome for sperm penetration into the oocyte ( 5 ). Additionally, it has been reported that sperm DNA integrity ( 45 ) and status of lipid peroxidation ( 4 , 46 ) are also related to male fertility. In the present study, we observed that sperm motility, membrane, and acrosomal integrity were significantly higher, while the status of protamination and lipid peroxidation were significantly lower in high- compared to low-fertile buffalo bulls.…”

Section: Discussionmentioning

confidence: 99%

Transcriptomic Profiling of Buffalo Spermatozoa Reveals Dysregulation of Functionally Relevant mRNAs in Low-Fertile Bulls

et al. 2021

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Although, it is known that spermatozoa harbor a variety of RNAs that may influence embryonic development, little is understood about sperm transcriptomic differences in relation to fertility, especially in buffaloes. In the present study, we compared the differences in sperm functional attributes and transcriptomic profile between high- and low-fertile buffalo bulls. Sperm membrane and acrosomal integrity were lower (P < 0.05), while protamine deficiency and lipid peroxidation were higher (P < 0.05) in low- compared to high-fertile bulls. Transcriptomic analysis using mRNA microarray technology detected a total of 51,282 transcripts in buffalo spermatozoa, of which 4,050 transcripts were differentially expressed, and 709 transcripts were found to be significantly dysregulated (P < 0.05 and fold change >1) between high- and low-fertile bulls. Majority of the dysregulated transcripts were related to binding activity, transcription, translation, and metabolic processes with primary localization in the cell nucleus, nucleoplasm, and in cytosol. Pathways related to MAPK signaling, ribosome pathway, and oxidative phosphorylation were dysregulated in low-fertile bull spermatozoa. Using bioinformatics analysis, we observed that several genes related to sperm functional attributes were significantly downregulated in low-fertile bull spermatozoa. Validation of the results of microarray analysis was carried out using real-time qPCR expression analysis of selected genes (YBX1, ORAI3, and TFAP2C). The relative expression of these genes followed the same trend in both the techniques. Collectively, this is the first study to report the transcriptomic profile of buffalo spermatozoa and to demonstrate the dysregulation of functionally relevant transcripts in low-fertile bull spermatozoa. The results of the present study open up new avenues for understanding the etiology for poor fertility in buffalo bulls and to identify fertility biomarkers.

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Sperm DNA Integrity and Male Fertility in Farm Animals: A Review

Cited by 77 publications

References 182 publications

Sperm Methylome Profiling Can Discern Fertility Levels in the Porcine Biomedical Model

Sperm Methylome Profiling Can Discern Fertility Levels in the Porcine Biomedical Model

Sperm chromatin integrity and DNA methylation in Norwegian Red bulls of contrasting fertility

Transcriptomic Profiling of Buffalo Spermatozoa Reveals Dysregulation of Functionally Relevant mRNAs in Low-Fertile Bulls

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