Comprehensive functional analysis reveals that acrosome integrity and viability are key variables distinguishing artificial insemination bulls of varying fertility

Bernecic, Naomi C.; Donnellan, E.M.; O’Callaghan, Elena; Kupisiewicz, Kasia; O’Meara, C.M.; Weldon, K; Lonergan, P.; Kenny, David A.; Fair, Seán

doi:10.3168/jds.2021-20319

Cited by 26 publications

(34 citation statements)

References 52 publications

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“…However, although such relationships were certainly less likely to be observed when using a single ejaculate, the fact that they were found could indicate a consistent relationship with fertility that should be confirmed by further studies. In agreement with our study, Bernecic et al [15] have described that acrosome integrity, together with viability, were the only sperm attributes that were significantly different between high-and low-fertility bulls. Unlike our work, the evaluation of the acrosome integrity in this study was carried out using PNA, which showed a lower sensitivity than that of the ISAS3Fun technique.…”

Section: Discussionsupporting

confidence: 93%

“…The analysis of frozen/thawed doses of a single ejaculate per bull and the selection of more males per fertility group in the current study would probably reduce the chances of finding differences in more sperm quality parameters. In fact, Bernecic et al [ 15 ] observed that both viability and acrosome integrity could serve as bull fertility biomarkers in the field, while Kjaestad et al [ 17 ] described an association between sperm motility and velocity with bull fertility.…”

Section: Discussionmentioning

confidence: 99%

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Ability of the ISAS3Fun Method to Detect Sperm Acrosome Integrity and Its Potential to Discriminate between High and Low Field Fertility Bulls

Yániz

Palacín

Silvestre

et al. 2021

Biology

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The objective of the present study was to investigate whether fertility differences in bulls are reflected in variations of sperm quality when analysing only one ejaculate per male. Two experiments were performed. In the first experiment, frozen semen samples from 20 adult bulls were tested; 10 bulls had high field fertility and 10 bulls had low field fertility. Analyses of sperm motility, membrane integrity, and membrane–acrosome integrity with the ISAS3Fun method were performed. Sperm morphometry of the fluorescence sperm subpopulations obtained with the ISAS3Fun method was also analysed. Significant differences between high- and low-fertility groups were only found with the ISAS3Fun technique, specifically in sperm acrosome integrity, the proportion of spermatozoa with an intact acrosome and damaged membrane, and in sperm head width of spermatozoa with intact structures. Discriminant analyses allowed us to correctly classify 90% of sperm samples in their fertility group using sperm quality parameters. Given that only the results obtained with the ISAS3Fun technique were related to bull fertility, we performed a second experiment aimed to validate the efficacy of this technique to detect the acrosomal integrity of bull spermatozoa, comparing them with the conventional FITC-PNA/propidium iodide (PNA/PI) combination under capacitating conditions. The results indicated that the ISAS3Fun combination provided an accurate assessment of both viability and acrosomal integrity for ejaculated spermatozoa, while the PNA/PI combination underestimated the extension of acrosomal damage due to false negatives. It was concluded that the simultaneous assessment of sperm plasma membranes and acrosome integrity with the ISAS3Fun method is precise and seems to have a greater potential to discriminate between high- and low-fertility bulls than more conventional in vitro sperm quality tests.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Ability of the ISAS3Fun Method to Detect Sperm Acrosome Integrity and Its Potential to Discriminate between High and Low Field Fertility Bulls

Yániz

Palacín

Silvestre

et al. 2021

Biology

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“…Despite rigorous assessments of sperm quality before semen is released, bulls used in AI still exhibit significant variation in field fertility. Numerous studies by our group and others have investigated aspects of sperm function in an attempt to explain divergent fertility in populations of AI bulls segregated based on pregnancy per AI (Sellem et al, 2015;Bernecic et al, 2021;Donnellan et al, 2022). Results tend to be rather inconsistent, probably a reflection of the multifactorial nature of sire subfertility as mentioned above and the fact that such AI bulls tend to be of high to medium fertility rather than being truly "low fertile" in terms of the extremes of fertility given that their semen has already undergone pre-freeze and post-thaw quality control checks.…”

Section: Discussionmentioning

confidence: 99%

118 Influence of sire fertility status on conceptus-induced transcriptomic response of the bovine endometrium

O’Callaghan

Sánchez

Rabaglino

et al. 2021

Reprod. Fertil. Dev.

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The aim was to examine the effect of sire fertility status on conceptus-induced changes in the bovine endometrial transcriptome. To generate elongated conceptuses, Day 7 blastocysts produced in vitro using frozen-thawed sperm from Holstein Friesian bulls (3 High fertility, HF and 3 Low fertility, LF) were transferred in groups of 5-10 into synchronized heifers (n = 7 heifers per bull) and recovered following slaughter on Day 15. Day 15 endometrial explants recovered from the uterine horn ipsilateral to the corpus luteum were recovered from synchronized cyclic heifers (n = 4). Explants from each heifer were co-cultured for 6 h in RPMI medium alone (Control) or with 100 ng/ml ovine recombinant interferon tau (IFNT) or with a single conceptus from each HF or LF bull. After 6 h, explants were snap frozen and stored at −80 °C. Extracted mRNA was subjected to RNA-seq and the resulting data were analyzed with R software. The numbers of differentially expressed genes (DEG; FDR<0.05) were: HF vs. Control: 956; LF vs. Control: 1021; IFNT vs. Control: 1301; HF vs. LF: 2. Unsurprisingly, the majority of DEG (658) were common to all comparisons and were related to IFNT-induced changes in the endometrium. Prior to applying the adjusted p-value, there were 700 DEG between HF and LF, with 191 and 509 genes more expressed in HF or LF, respectively (p < 0.05). Overrepresentation analysis of KEGG pathways (FDR<0.05), revealed that DEG with higher expression in LF were involved in cell cycle and proteolysis, while those upregulated DEG by HF conceptuses were strongly associated with immune process pathways, such as TNF, NFkappa B, cytokine-cytokine receptor interaction, and TLR signaling. These pathways were also enriched by DEG upregulated by IFNT compared to the Control. Furthermore, only the HF, and not the LF group, affected the expression of most genes in these pathways (p < 0.05) according to a negative binomial regression model. Finally, a weighted gene co-expression network analysis revealed two clusters of co-expressed genes associated with the HF conceptuses (p < 0.05), which were also enriched for the aforementioned pathways. In conclusion, HF conceptuses, similar to IFNT

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“…However, despite various multivariate and statistical approaches being developed, no single test nor combination of tests can reliably and consistently predict field fertility. This is evident from the work of both Sellem, et al ( 3 ) and Bernecic, et al ( 4 ) which could explain approximately 40 and 47%, respectively, of the variation in Holstein bull fertility through the assessment of flow cytometry and CASA-based parameters. A recent study by Narud, et al ( 5 ) increased the explained variation in bull field fertility to 59% by adding the measurement of intracellular metabolites and selected trace elements (such as amino acids, Fe and Zn) in the spermatozoa of Norwegian Red Bulls ( 5 ).…”

Section: Introductionmentioning

confidence: 91%

Identification of differentially expressed mRNAs and miRNAs in spermatozoa of bulls of varying fertility

et al. 2022

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Bulls used in artificial insemination, with apparently normal semen quality, can vary significantly in their field fertility. This study aimed to characterize the transcriptome of spermatozoa from high (HF) and low (LF) fertility bulls at the mRNA and miRNA level in order to identify potential novel markers of fertility. Holstein-Friesian bulls were assigned to either the HF or LF group (n = 10 per group) based on an adjusted national fertility index from a minimum of 500 inseminations. Total RNA was extracted from a pool of frozen-thawed spermatozoa from three different ejaculates per bull, following which mRNA-seq and miRNA-seq were performed. Six mRNAs and 13 miRNAs were found differentially expressed (P < 0.05, FC > 1.5) between HF and LF bulls. Of particular interest, the gene pathways targeted by the 13 differentially expressed miRNAs were related to embryonic development and gene expression regulation. Previous studies reported that disruptions to protamine 1 mRNA (PRM1) had deleterious consequences for sperm chromatin structure and fertilizing ability. Notably, PRM1 exhibited a higher expression in spermatozoa from LF than HF bulls. In contrast, Western Blot analysis revealed a decrease in PRM1 protein abundance for spermatozoa from LF bulls; this was not associated with increased protamine deficiency (measured by the degree of chromatin compaction) or DNA fragmentation, as assessed by flow cytometry analyses. However, protamine deficiency was positively and moderately correlated with the percentage of spermatozoa with DNA fragmentation, irrespective of fertility group. This study has identified potential biomarkers that could be used for improving semen quality assessments of bull fertility.

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Comprehensive functional analysis reveals that acrosome integrity and viability are key variables distinguishing artificial insemination bulls of varying fertility

Cited by 26 publications

References 52 publications

Ability of the ISAS3Fun Method to Detect Sperm Acrosome Integrity and Its Potential to Discriminate between High and Low Field Fertility Bulls

Ability of the ISAS3Fun Method to Detect Sperm Acrosome Integrity and Its Potential to Discriminate between High and Low Field Fertility Bulls

118 Influence of sire fertility status on conceptus-induced transcriptomic response of the bovine endometrium

Identification of differentially expressed mRNAs and miRNAs in spermatozoa of bulls of varying fertility

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