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Bull sperm SWATH-MS-based proteomics reveals link between high fertility and energy production, motility structures, and sperm-oocyte interaction. Quantitation

ABSTRACT: Prediction of male or semen fertility potential remains a persistent challenge that has yet to be fully resolved. This work analyzed several in vitro parameters and proteome of spermatozoa in bulls cataloged as high (HF; n=5) and low field (LF; n=5) fertility after more than a thousand artificial inseminations. Sperm motility was evaluated by Computer-Assisted Sperm Analysis. Sperm viability, mitochondrial membrane potential (MMP), and reactive oxygen species (mROS) of spermatozoa were assessed by flow cytometry. Proteome was evaluated by SWATH-MS procedure. Spermatozoa of HF bulls showed significantly higher total motility than the LF group (41.4% vs. 29.7%). Rates of healthy sperm (live, high MMP, and low mROS) for HF and LF bull groups were 49% and 43%, respectively (p > 0.05). Spermatozoa of HF bulls showed higher presence of differentially abundant proteins (DAPs) related to both energy production (COX7C), mainly OXPHOS pathway, and to the development of structures linked with the motility process (TPPP2, SSMEM1 and SPAG16). Furthermore, we observed that EQTN, together with other DAPs related to the interaction with the oocyte, were overrepresented in HF bull spermatozoa. The biological processes related to protein processing, catabolism, and protein folding were found to be overrepresented in LF bull sperm in which the HSP90AA1 chaperone was identified as the most DAP

INSTRUMENT(S): TripleTOF 6600

ORGANISM(S): Bos Taurus (bovine)

TISSUE(S): Semen

SUBMITTER: Luz Valero

LAB HEAD: Miguel A. Silvestre

PROVIDER: PXD042286 | Pride | 2023-10-18

REPOSITORIES: Pride

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Bull Sperm SWATH-MS-Based Proteomics Reveals Link between High Fertility and Energy Production, Motility Structures, and Sperm-Oocyte Interaction.

Gacem Sabrina S Castello-Ruiz María M Hidalgo Carlos O CO Tamargo Carolina C Santolaria Pilar P Soler Carles C Yániz Jesús L JL Silvestre Miguel A MA

Journal of proteome research 20231002 11

The prediction of male or semen fertility potential remains a persistent challenge that has yet to be fully resolved. This work analyzed several in vitro parameters and proteome of spermatozoa in bulls cataloged as high- (HF; n = 5) and low-field (LF; n = 5) fertility after more than a thousand artificial inseminations. Sperm motility was evaluated by computer-assisted sperm analysis. Sperm viability, mitochondrial membrane potential (MMP) and reactive oxygen species (mROS) ...[more]

PMID: 37782577

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Project description:Abstract Buffalo bulls are the backbone of Indian dairy industry, and the quality of semen donating bulls determine the overall production efficiency of buffalo dairy farms. Seminal plasma (SP) of bulls harbor millions of lipid bilayer nanovesicles known as extracellular vesicles (EVs). These EVs carry a heterogenous cargo of essential biomolecules including fertility associated proteins which contribute to the fertilizing potential of spermatozoa. In this study, we explored various parameters of EVs such as size, concentration and the complete proteome profiles of SP EVs from two distinct fertility groups in order to unravel the differentially abundant proteins that potentially affect the overall fertility of bulls. Through Dynamic Light Scattering (DLS) it was found that the purified EVs were present in 7 to 14 size exclusion chromatographic (SEC) fractions with sizes ranging from 145 to 256 nm in the high fertile (HF) and low fertile (LF) bulls. Nanoparticle Tracking Analysis (NTA) confirmed the size of seminal EVs up to 200 nm, and concentrations varying from 2.84 to 6.82 × 1011 and 3.57 to 7.74 × 1011 particles per ml in HF and LF bulls, respectively across all the fractions. No significant difference was observed in the size and concentration of seminal EVs between the HF and LF groups. We identified a total of 1862 and 1807 proteins in seminal EVs of HF and LF bulls, respectively using high throughput LC-MS/MS approach. Out of these total proteins, 1754 proteins were common in both the groups and about 87 proteins were highly abundant in HF group while 1292 were less abundant as compared to LF bulls. Gene ontology (GO) analysis, revealed that the highly abundant proteins in HF group were mainly part of the nucleus and involved in nucleosome assembly along with DNA binding. In addition, highly abundant proteins in EVs of HF group were found to be involved in spermatogenesis, motility, acrosome reaction, capacitation, gamete fusion, and cryotolerance. Two highly abundant proteins of HF EVs, namely protein disulfide-isomerase A4 (PDIA4) and gelsolin (GSN), were successfully immunolocalized on spermatozoa, indicating that these proteins might be transferred to spermatozoa through EVs. The proteins; PDIA4 and GSN are intricately associated with sperm-oocyte fusion and acrosome reaction, respectively, thus they are vital for regulating the fertilizing capacity of sperm. Our evidences clearly support that the protein repertoires in EVs and subsequently their presence on sperm, are strongly associated with sperm functions. Altogether, the current investigation clearly indicates that SPEVs possess crucial protein repertoires which are essential for enhancing the sperm fertilizing capacity.

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