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Sperm Transcripts Associated With Odorant Binding and Olfactory Transduction Pathways Are Altered in Breeding Bulls Producing Poor-Quality Semen

Spermatozoa carries a reservoir of mRNAs regulating sperm functions and fertilizing potential. Although it is well recognized that a considerable proportion of high genetic merit breeding bulls produce poor-quality semen, the transcriptomic alterations in spermatozoa from such bulls are not understo...

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Autores principales: Karuthadurai, Thirumalaisamy, Das, Dayal Nitai, Kumaresan, Arumugam, Sinha, Manish Kumar, Kamaraj, Elango, Nag, Pradeep, Ebenezer Samuel King, John Peter, Datta, Tirtha Kumar, Manimaran, Ayyasamy, Jeyakumar, Sakthivel, Ramesha, Kerekoppa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8902071/
https://www.ncbi.nlm.nih.gov/pubmed/35274020
http://dx.doi.org/10.3389/fvets.2022.799386
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author Karuthadurai, Thirumalaisamy
Das, Dayal Nitai
Kumaresan, Arumugam
Sinha, Manish Kumar
Kamaraj, Elango
Nag, Pradeep
Ebenezer Samuel King, John Peter
Datta, Tirtha Kumar
Manimaran, Ayyasamy
Jeyakumar, Sakthivel
Ramesha, Kerekoppa
author_facet Karuthadurai, Thirumalaisamy
Das, Dayal Nitai
Kumaresan, Arumugam
Sinha, Manish Kumar
Kamaraj, Elango
Nag, Pradeep
Ebenezer Samuel King, John Peter
Datta, Tirtha Kumar
Manimaran, Ayyasamy
Jeyakumar, Sakthivel
Ramesha, Kerekoppa
author_sort Karuthadurai, Thirumalaisamy
collection PubMed
description Spermatozoa carries a reservoir of mRNAs regulating sperm functions and fertilizing potential. Although it is well recognized that a considerable proportion of high genetic merit breeding bulls produce poor-quality semen, the transcriptomic alterations in spermatozoa from such bulls are not understood. In the present study, comparative high-throughput transcriptomic profiling of spermatozoa from good and poor-quality semen-producing bulls was carried out to identify the transcripts associated with semen quality. Using next-generation sequencing (NGS), we identified 11,632 transcripts in Holstein Friesian bull spermatozoa; after total hit normalization, a total of 544 transcripts were detected, of which 185 transcripts were common to both good and poor-quality semen, while 181 sperm transcripts were unique to good quality semen, and 178 transcripts were unique to poor-quality semen. Among the co-expressed transcripts, 31 were upregulated, while 108 were downregulated, and 46 were neutrally expressed in poor-quality semen. Bioinformatics analysis revealed that the dysregulated transcripts were predominantly involved in molecular function, such as olfactory receptor activity and odor binding, and in biological process, such as detection of chemical stimulus involved in sensory perception, sensory perception of smell, signal transduction, and signal synaptic transmission. Since a majority of the dysregulated transcripts were involved in the olfactory pathway (85% of enriched dysregulated genes were involved in this pathway), the expression of selected five transcripts associated with this pathway (OR2T11, OR10S1, ORIL3, OR5M11, and PRRX1) were validated using real-time qPCR, and it was found that their transcriptional abundance followed the same trend as observed in NGS; the sperm transcriptional abundance of OR2T11 and OR10S1 differed significantly (p < 0.05) between good and poor-quality semen. It is concluded that poor-quality semen showed altered expression of transcripts associated with olfactory receptors and pathways indicating the relationship between olfactory pathway and semen quality in bulls.
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spelling pubmed-89020712022-03-09 Sperm Transcripts Associated With Odorant Binding and Olfactory Transduction Pathways Are Altered in Breeding Bulls Producing Poor-Quality Semen Karuthadurai, Thirumalaisamy Das, Dayal Nitai Kumaresan, Arumugam Sinha, Manish Kumar Kamaraj, Elango Nag, Pradeep Ebenezer Samuel King, John Peter Datta, Tirtha Kumar Manimaran, Ayyasamy Jeyakumar, Sakthivel Ramesha, Kerekoppa Front Vet Sci Veterinary Science Spermatozoa carries a reservoir of mRNAs regulating sperm functions and fertilizing potential. Although it is well recognized that a considerable proportion of high genetic merit breeding bulls produce poor-quality semen, the transcriptomic alterations in spermatozoa from such bulls are not understood. In the present study, comparative high-throughput transcriptomic profiling of spermatozoa from good and poor-quality semen-producing bulls was carried out to identify the transcripts associated with semen quality. Using next-generation sequencing (NGS), we identified 11,632 transcripts in Holstein Friesian bull spermatozoa; after total hit normalization, a total of 544 transcripts were detected, of which 185 transcripts were common to both good and poor-quality semen, while 181 sperm transcripts were unique to good quality semen, and 178 transcripts were unique to poor-quality semen. Among the co-expressed transcripts, 31 were upregulated, while 108 were downregulated, and 46 were neutrally expressed in poor-quality semen. Bioinformatics analysis revealed that the dysregulated transcripts were predominantly involved in molecular function, such as olfactory receptor activity and odor binding, and in biological process, such as detection of chemical stimulus involved in sensory perception, sensory perception of smell, signal transduction, and signal synaptic transmission. Since a majority of the dysregulated transcripts were involved in the olfactory pathway (85% of enriched dysregulated genes were involved in this pathway), the expression of selected five transcripts associated with this pathway (OR2T11, OR10S1, ORIL3, OR5M11, and PRRX1) were validated using real-time qPCR, and it was found that their transcriptional abundance followed the same trend as observed in NGS; the sperm transcriptional abundance of OR2T11 and OR10S1 differed significantly (p < 0.05) between good and poor-quality semen. It is concluded that poor-quality semen showed altered expression of transcripts associated with olfactory receptors and pathways indicating the relationship between olfactory pathway and semen quality in bulls. Frontiers Media S.A. 2022-02-22 /pmc/articles/PMC8902071/ /pubmed/35274020 http://dx.doi.org/10.3389/fvets.2022.799386 Text en Copyright © 2022 Karuthadurai, Das, Kumaresan, Sinha, Kamaraj, Nag, Ebenezer Samuel King, Datta, Manimaran, Jeyakumar and Ramesha. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Veterinary Science
Karuthadurai, Thirumalaisamy
Das, Dayal Nitai
Kumaresan, Arumugam
Sinha, Manish Kumar
Kamaraj, Elango
Nag, Pradeep
Ebenezer Samuel King, John Peter
Datta, Tirtha Kumar
Manimaran, Ayyasamy
Jeyakumar, Sakthivel
Ramesha, Kerekoppa
Sperm Transcripts Associated With Odorant Binding and Olfactory Transduction Pathways Are Altered in Breeding Bulls Producing Poor-Quality Semen
title Sperm Transcripts Associated With Odorant Binding and Olfactory Transduction Pathways Are Altered in Breeding Bulls Producing Poor-Quality Semen
title_full Sperm Transcripts Associated With Odorant Binding and Olfactory Transduction Pathways Are Altered in Breeding Bulls Producing Poor-Quality Semen
title_fullStr Sperm Transcripts Associated With Odorant Binding and Olfactory Transduction Pathways Are Altered in Breeding Bulls Producing Poor-Quality Semen
title_full_unstemmed Sperm Transcripts Associated With Odorant Binding and Olfactory Transduction Pathways Are Altered in Breeding Bulls Producing Poor-Quality Semen
title_short Sperm Transcripts Associated With Odorant Binding and Olfactory Transduction Pathways Are Altered in Breeding Bulls Producing Poor-Quality Semen
title_sort sperm transcripts associated with odorant binding and olfactory transduction pathways are altered in breeding bulls producing poor-quality semen
topic Veterinary Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8902071/
https://www.ncbi.nlm.nih.gov/pubmed/35274020
http://dx.doi.org/10.3389/fvets.2022.799386
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