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

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

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...

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Published in:Frontiers in veterinary science Vol. 9; p. 993561
Main Authors: Donnellan, Eimear M., Perrier, Jean-Philippe, Keogh, Kate, Štiavnická, Miriam, Collins, Caitríona M., Dunleavy, Elaine M., Sellem, Eli, Bernecic, Naomi C., Lonergan, Patrick, Kenny, David A., Fair, Sean
Format: Journal Article
Language:English
Published: Frontiers Media S.A 05-10-2022
Subjects:
bovine
male fertility
miRNA
RNA
spermatozoa
Veterinary Science
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Abstract 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.
AbstractList 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.
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.
Author Donnellan, Eimear M.
Kenny, David A.
Keogh, Kate
Fair, Sean
Lonergan, Patrick
Štiavnická, Miriam
Dunleavy, Elaine M.
Collins, Caitríona M.
Bernecic, Naomi C.
Perrier, Jean-Philippe
Sellem, Eli
AuthorAffiliation 5 ALLICE, Innovation and Development , Paris , France
1 Laboratory of Animal Reproduction, Department of Biological Sciences, Biomaterials Research Cluster, Faculty of Science and Engineering, School of Natural Sciences, Bernal Institute, University of Limerick , Limerick , Ireland
3 Technical University of the Shannon , Athlone, Co. Westmeath , Ireland
2 Animal and Bioscience Research Department, Animal and Grassland Research and Innovation Centre , Teagasc , Ireland
6 School of Agriculture and Food Science, University College Dublin , Dublin , Ireland
4 Centre for Chromosome Biology, Biomedical Sciences, National University of Ireland , Galway , Ireland
AuthorAffiliation_xml – name: 2 Animal and Bioscience Research Department, Animal and Grassland Research and Innovation Centre , Teagasc , Ireland
– name: 6 School of Agriculture and Food Science, University College Dublin , Dublin , Ireland
– name: 3 Technical University of the Shannon , Athlone, Co. Westmeath , Ireland
– name: 4 Centre for Chromosome Biology, Biomedical Sciences, National University of Ireland , Galway , Ireland
– name: 1 Laboratory of Animal Reproduction, Department of Biological Sciences, Biomaterials Research Cluster, Faculty of Science and Engineering, School of Natural Sciences, Bernal Institute, University of Limerick , Limerick , Ireland
– name: 5 ALLICE, Innovation and Development , Paris , France
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Copyright Copyright © 2022 Donnellan, Perrier, Keogh, Štiavnická, Collins, Dunleavy, Sellem, Bernecic, Lonergan, Kenny and Fair. 2022 Donnellan, Perrier, Keogh, Štiavnická, Collins, Dunleavy, Sellem, Bernecic, Lonergan, Kenny and Fair
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Present address: Jean-Philippe Perrier, INSERM U1209, CNRS UMR 5309, Institute for Advanced Biosciences, Université Grenoble Alpes, Grenoble, France
This article was submitted to Animal Reproduction - Theriogenology, a section of the journal Frontiers in Veterinary Science
Reviewed by: Karl Kerns, Iowa State University, United States; Rajan Iyyappan, National Institute of Environmental Health Sciences (NIEHS), United States
Edited by: M. Sofia Ortega, University of Wisconsin-Madison, United States
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Snippet Bulls used in artificial insemination, with apparently normal semen quality, can vary significantly in their field fertility. This study aimed to characterize...
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SubjectTerms bovine
male fertility
miRNA
RNA
spermatozoa
Veterinary Science
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Title Identification of differentially expressed mRNAs and miRNAs in spermatozoa of bulls of varying fertility
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