Retained Acetylated Histone Four in Bull Sperm Associated With Fertility

Bull fertility, ability of the sperm to fertilize and activate the egg and support embryo development, is vital for cattle reproduction and production. Even though majority of histones are replaced by protamines, some histones are retained in sperm. It is known that chromatin remodeling during sperm...

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Main Authors: Muhammet Rasit Ugur, Naseer Ahmad Kutchy, Erika Bezerra de Menezes, Asma Ul-Husna, Bethany Peyton Haynes, Alper Uzun, Abdullah Kaya, Einko Topper, Arlindo Moura, Erdogan Memili
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-07-01
Series:Frontiers in Veterinary Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fvets.2019.00223/full
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author Muhammet Rasit Ugur
Naseer Ahmad Kutchy
Naseer Ahmad Kutchy
Erika Bezerra de Menezes
Asma Ul-Husna
Bethany Peyton Haynes
Alper Uzun
Alper Uzun
Alper Uzun
Abdullah Kaya
Einko Topper
Arlindo Moura
Erdogan Memili
author_facet Muhammet Rasit Ugur
Naseer Ahmad Kutchy
Naseer Ahmad Kutchy
Erika Bezerra de Menezes
Asma Ul-Husna
Bethany Peyton Haynes
Alper Uzun
Alper Uzun
Alper Uzun
Abdullah Kaya
Einko Topper
Arlindo Moura
Erdogan Memili
author_sort Muhammet Rasit Ugur
collection DOAJ
description Bull fertility, ability of the sperm to fertilize and activate the egg and support embryo development, is vital for cattle reproduction and production. Even though majority of histones are replaced by protamines, some histones are retained in sperm. It is known that chromatin remodeling during spermatogenesis results in dynamic changes in sperm chromatin structure through post-translational modifications (PTM) of sperm histones, which are important for regulation of gene expression. However, amounts of sperm Histone 4 (H4), its acetylated form (H4 acetyl), and to what extent these molecular attributes influence sperm chromatin structure and bull fertility are unknown. These gaps in the knowledge base are important because they are preventing advances in the fundamental science of bovine male gamete and improvement of bull fertility. The objective of this study was to test the hypothesis that expression dynamics as well as PTM of sperm H4 are associated with bull fertility. Flow cytometry was utilized to quantify H4 and H4 acetylated form in sperm from seven high and seven low fertility Holstein bulls. The results indicated that the average number of cells with H4 or H4 acetyl expression in high and low fertility bull sperm were 34.6 ± 20.4, 1.88 ± 1.8, 15.2 ± 20.8, and 1.4 ± 1.2, respectively. However, the sperm enriched in both H4 and H4 acetyl were different between high and low fertility groups (3.5 ± 0.6; 1.8 ± 0.8; P = 0.043). The localization and detection of H4 and H4 acetylation were measured by immunocytochemistry which revealed that H4 and H4 acetylation were equally distributed in the sperm head of high and low fertility sires. Western blotting results confirmed the presence of the H4 and its acetylated form in the sperm. Bioinformatics studies demonstrated that H4 is highly conserved among mammalians, and have significant gene ontology on spermatogenesis, early embryo implantation, and sperm capacitation. The results are significant because it demonstrates the replacement of canonical histone H4 into modified H4 acetylation in sperm and regulate its dynamics which is crucial for bull fertility and reproductive biotechnology. These findings advance fundamental science of mammalian early development and reproductive biotechnology.
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spelling doaj.art-4e8676e082ab404c96fddee4f2e1841a2022-12-22T03:42:27ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692019-07-01610.3389/fvets.2019.00223458113Retained Acetylated Histone Four in Bull Sperm Associated With FertilityMuhammet Rasit Ugur0Naseer Ahmad Kutchy1Naseer Ahmad Kutchy2Erika Bezerra de Menezes3Asma Ul-Husna4Bethany Peyton Haynes5Alper Uzun6Alper Uzun7Alper Uzun8Abdullah Kaya9Einko Topper10Arlindo Moura11Erdogan Memili12Department of Animal and Dairy Sciences, Mississippi State University, Starkville, MS, United StatesDepartment of Animal and Dairy Sciences, Mississippi State University, Starkville, MS, United StatesDepartment of Genetics, School of Medicine, Yale University, New Haven, CT, United StatesDepartment of Animal and Dairy Sciences, Mississippi State University, Starkville, MS, United StatesDepartment of Zoology, Pir Mehr Ali Shah-Arid Agriculture University, Rawalpindi, PakistanDepartment of Animal and Dairy Sciences, Mississippi State University, Starkville, MS, United StatesWarren Alpert Medical School of Brown University, Providence, RI, United StatesDepartment of Pediatrics, Women and Infants Hospital of Rhode Island, Providence, RI, United StatesCenter for Computational Molecular Biology, Brown University, Providence, RI, United StatesDepartment of Reproduction and Artificial Insemination, Selcuk University, Konya, TurkeyURUS Group LP, Madison, WI, United StatesDepartment of Animal Science, Federal University of Ceará, Fortaleza, BrazilDepartment of Animal and Dairy Sciences, Mississippi State University, Starkville, MS, United StatesBull fertility, ability of the sperm to fertilize and activate the egg and support embryo development, is vital for cattle reproduction and production. Even though majority of histones are replaced by protamines, some histones are retained in sperm. It is known that chromatin remodeling during spermatogenesis results in dynamic changes in sperm chromatin structure through post-translational modifications (PTM) of sperm histones, which are important for regulation of gene expression. However, amounts of sperm Histone 4 (H4), its acetylated form (H4 acetyl), and to what extent these molecular attributes influence sperm chromatin structure and bull fertility are unknown. These gaps in the knowledge base are important because they are preventing advances in the fundamental science of bovine male gamete and improvement of bull fertility. The objective of this study was to test the hypothesis that expression dynamics as well as PTM of sperm H4 are associated with bull fertility. Flow cytometry was utilized to quantify H4 and H4 acetylated form in sperm from seven high and seven low fertility Holstein bulls. The results indicated that the average number of cells with H4 or H4 acetyl expression in high and low fertility bull sperm were 34.6 ± 20.4, 1.88 ± 1.8, 15.2 ± 20.8, and 1.4 ± 1.2, respectively. However, the sperm enriched in both H4 and H4 acetyl were different between high and low fertility groups (3.5 ± 0.6; 1.8 ± 0.8; P = 0.043). The localization and detection of H4 and H4 acetylation were measured by immunocytochemistry which revealed that H4 and H4 acetylation were equally distributed in the sperm head of high and low fertility sires. Western blotting results confirmed the presence of the H4 and its acetylated form in the sperm. Bioinformatics studies demonstrated that H4 is highly conserved among mammalians, and have significant gene ontology on spermatogenesis, early embryo implantation, and sperm capacitation. The results are significant because it demonstrates the replacement of canonical histone H4 into modified H4 acetylation in sperm and regulate its dynamics which is crucial for bull fertility and reproductive biotechnology. These findings advance fundamental science of mammalian early development and reproductive biotechnology.https://www.frontiersin.org/article/10.3389/fvets.2019.00223/fullacetylationepigeneticshistone 4fertilitysperm
spellingShingle Muhammet Rasit Ugur
Naseer Ahmad Kutchy
Naseer Ahmad Kutchy
Erika Bezerra de Menezes
Asma Ul-Husna
Bethany Peyton Haynes
Alper Uzun
Alper Uzun
Alper Uzun
Abdullah Kaya
Einko Topper
Arlindo Moura
Erdogan Memili
Retained Acetylated Histone Four in Bull Sperm Associated With Fertility
Frontiers in Veterinary Science
acetylation
epigenetics
histone 4
fertility
sperm
title Retained Acetylated Histone Four in Bull Sperm Associated With Fertility
title_full Retained Acetylated Histone Four in Bull Sperm Associated With Fertility
title_fullStr Retained Acetylated Histone Four in Bull Sperm Associated With Fertility
title_full_unstemmed Retained Acetylated Histone Four in Bull Sperm Associated With Fertility
title_short Retained Acetylated Histone Four in Bull Sperm Associated With Fertility
title_sort retained acetylated histone four in bull sperm associated with fertility
topic acetylation
epigenetics
histone 4
fertility
sperm
url https://www.frontiersin.org/article/10.3389/fvets.2019.00223/full
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