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Early histone H4 acetylation during chromatin remodeling in equine spermatogenesis.
Abstract: Chromatin remodeling during spermatogenesis culminates in the exchange of nucleosomes for transition proteins and protamines as an important part of spermatid development to give rise to healthy sperm. Comparative immunofluorescence analyses of equine and murine testis histological sections were used to characterize nucleoprotein exchange in the stallion. Histone H4 hyperacetylation is considered a key event of histone removal during the nucleoprotein transition to a protamine-based sperm chromatin structure. In the stallion, but not the mouse, H4 was already highly acetylated in lysine residues K5, K8, and K12 in round spermatids almost immediately after meiotic division. Time courses of transition protein 1 (TP1), protamine 1, H2A histone family member Z (H2AFZ), and testis-specific histone H2B variant (TH2B) expression in stallion spermatogenesis were similar to the mouse where protamine 1 and TP1 were only expressed in elongating spermatids much later in spermatid development. The additional acetylation of H4 in K16 position (H4K16ac) was detected during a brief phase of spermatid elongation in both species, concomitant with the phosphorylation of the noncanonical histone variant H2AFX resulting from DNA strand break-mediated DNA relaxation. The results suggest that H4K16 acetylation, which is dependent on DNA damage signaling, may be more important for nucleosome replacement in spermiogenesis than indicated by data obtained in rodents and highlight the value of the stallion as an alternative animal model for investigating human spermatogenesis. A revised classification system of the equine spermatogenic cycle for simplified comparison with the mouse is proposed to this end.
© The Author(s) 2017. Published by Oxford University Press on behalf of Society for the Study of Reproduction. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Publication Date: 2017-12-01 PubMed ID: 29186293DOI: 10.1093/biolre/iox159Google Scholar: Lookup The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research paper focuses on the chromatin remodeling process in spermatogenesis for equines (horses) and compares it to the process in murine (mice). Specifically, it studies how the histone H4 acetylation, a crucial component in the development of spermatids, occurs much earlier in horses than in mice. This earlier acetylation could make the horse a valuable alternative model for investigating human spermatogenesis.
Methodology and Focus
- The researchers conducted a comparative analysis of equine and murine testis histological sections to understand the nucleoprotein exchange in stallions.
- The emphasis was on the acetylation of histone H4, considered a key process in histone removal during the transition from nucleoprotein to a protamine-based sperm chromatin structure, a critical step for spermatid development.
Findings
- In stallions, unlike mice, it was found that the histone H4 was highly acetylated in lysine residues K5, K8, and K12 in round spermatids, happening nearly immediately post-meiotic division.
- Findings on the time course of transition protein 1 (TP1), protamine 1, H2A histone family member Z (H2AFZ), and testis-specific histone H2B variant (TH2B) expression in stallion spermatogenesis resembled the findings for mice. Here, the expression of protamine 1 and TP1 only occurred in elongating spermatids, a much later stage of spermatid development.
- A notable additional acetylation of H4 in the K16 position (H4K16ac) was discovered during a brief phase of spermatid elongation for both species. This has connections with DNA strand break-mediated DNA relaxation, enabled through the phosphorylation of the noncanonical histone variant H2AFX.
Implications
- The results suggest that the sperm chromatin structure’s remodeling in stallions might be more deeply influenced by H4K16 acetylation than in rodents.
- This raises the potential of using horses as an alternative animal model for studying human spermatogenesis.
- Researchers also propose a revised classification system for the equine spermatogenic cycle for simplified comparison to mice.
All in all, this research provides vital insights into the spermatogenesis process in different mammalian species, emphasizing the role of histone H4 acetylation and suggesting an alternative model for studying human reproductive biology.
Cite This Article
APA
Ketchum CC, Larsen CD, McNeil A, Meyer-Ficca ML, Meyer RG.
(2017).
Early histone H4 acetylation during chromatin remodeling in equine spermatogenesis.
Biol Reprod, 98(1), 115-129.
https://doi.org/10.1093/biolre/iox159 Publication
Researcher Affiliations
- Department of Animal, Dairy and Veterinary Sciences, College of Agriculture and Applied Sciences, Utah Experimental Station, Utah State University, Logan, Utah, USA.
- Utah Experimental Station, Utah State University, Logan, Utah, USA.
- School of Veterinary Medicine (Washington-Idaho-Montana-Utah Regional Veterinary Medical Program, WIMU), Utah State University, Logan, Utah, USA.
- Department of Animal, Dairy and Veterinary Sciences, College of Agriculture and Applied Sciences, Utah Experimental Station, Utah State University, Logan, Utah, USA.
- Department of Animal, Dairy and Veterinary Sciences, College of Agriculture and Applied Sciences, Utah Experimental Station, Utah State University, Logan, Utah, USA.
- School of Veterinary Medicine (Washington-Idaho-Montana-Utah Regional Veterinary Medical Program, WIMU), Utah State University, Logan, Utah, USA.
- Department of Animal, Dairy and Veterinary Sciences, College of Agriculture and Applied Sciences, Utah Experimental Station, Utah State University, Logan, Utah, USA.
- Utah Experimental Station, Utah State University, Logan, Utah, USA.
- School of Veterinary Medicine (Washington-Idaho-Montana-Utah Regional Veterinary Medical Program, WIMU), Utah State University, Logan, Utah, USA.
MeSH Terms
- Acetylation
- Animals
- Chromatin Assembly and Disassembly / physiology
- Histones / genetics
- Histones / metabolism
- Horses / physiology
- Male
- Spermatogenesis / physiology
- Spermatozoa / physiology
Citations
This article has been cited 12 times.- Moritz L, Schon SB, Rabbani M, Sheng Y, Agrawal R, Glass-Klaiber J, Sultan C, Camarillo JM, Clements J, Baldwin MR, Diehl AG, Boyle AP, O'Brien PJ, Ragunathan K, Hu YC, Kelleher NL, Nandakumar J, Li JZ, Orwig KE, Redding S, Hammoud SS. Sperm chromatin structure and reproductive fitness are altered by substitution of a single amino acid in mouse protamine 1. Nat Struct Mol Biol 2023 Aug;30(8):1077-1091.
- Li T, Wang H, Ma K, Wu Y, Qi X, Liu Z, Li Q, Zhang Y, Ma Y. Identification and functional characterization of developmental-stage-dependent piRNAs in Tibetan sheep testes. J Anim Sci 2023 Jan 3;101.
- Tan H, Wang W, Zhou C, Wang Y, Zhang S, Yang P, Guo R, Chen W, Zhang J, Ye L, Cui Y, Ni T, Zheng K. Single-cell RNA-seq uncovers dynamic processes orchestrated by RNA-binding protein DDX43 in chromatin remodeling during spermiogenesis. Nat Commun 2023 Apr 29;14(1):2499.
- Odroniec A, Olszewska M, Kurpisz M. Epigenetic markers in the embryonal germ cell development and spermatogenesis. Basic Clin Androl 2023 Feb 23;33(1):6.
- Moritz L, Hammoud SS. The Art of Packaging the Sperm Genome: Molecular and Structural Basis of the Histone-To-Protamine Exchange. Front Endocrinol (Lausanne) 2022;13:895502.
- Cruz A, Sullivan DB, Doty KF, Hess RA, Canisso IF, Reddi PP. Acrosomal marker SP-10 (gene name Acrv1) for staging of the cycle of seminiferous epithelium in the stallion. Theriogenology 2020 Oct 15;156:214-221.
- Chioccarelli T, Pierantoni R, Manfrevola F, Porreca V, Fasano S, Chianese R, Cobellis G. Histone Post-Translational Modifications and CircRNAs in Mouse and Human Spermatozoa: Potential Epigenetic Marks to Assess Human Sperm Quality. J Clin Med 2020 Feb 27;9(3).
- Wang T, Gao H, Li W, Liu C. Essential Role of Histone Replacement and Modifications in Male Fertility. Front Genet 2019;10:962.
- Yu L, Xie R, Tian T, Zheng L, Tang L, Cai S, Ma Z, Yang T, Han B, Yang Q. Suberoylanilide hydroxamic acid upregulates histone acetylation and activates endoplasmic reticulum stress to induce apoptosis in HepG2 liver cancer cells. Oncol Lett 2019 Oct;18(4):3537-3544.
- Firouzabadi AM, Fesahat F, Seifati SM. Dynamic architecture of mammalian paternal chromatin: histone-to-protamine exchange and post-fertilization reprogramming. Epigenetics Chromatin 2025 Dec 7;18(1):83.
- Porreca V, Chioccarelli T, Albano F, Nittoli V, Ricci G, Ambrosino C, Chianese R, Mele VG, Migliaccio A, Stornaiuolo M, Suglia A, Cobellis G, Manfrevola F. SIRT1 retention in elongating spermatids interferes with histone displacement by counteracting MOF-dependent H4K16 acetylation. Front Cell Dev Biol 2025;13:1524919.
- Kaltsas A, Markou E, Kyrgiafini MA, Zikopoulos A, Symeonidis EN, Dimitriadis F, Zachariou A, Sofikitis N, Chrisofos M. Oxidative-Stress-Mediated Epigenetic Dysregulation in Spermatogenesis: Implications for Male Infertility and Offspring Health. Genes (Basel) 2025 Jan 17;16(1).
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