Core Histones Are Constituents of the Perinuclear Theca of Murid Spermatozoa: An Assessment of Their Synthesis and Assembly during Spermiogenesis and Function after Gametic Fusion
The perinuclear theca (PT) of the eutherian sperm head is a cytoskeletal-like structure that houses proteins involved in important cellular processes during spermiogenesis and fertilization. Building upon our novel discovery of non-nuclear histones in the bovine PT, we sought to investigate whether...
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MDPI AG
2021-07-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/22/15/8119 |
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| author | Lauren E. Hamilton Morgan Lion Luis Aguila João Suzuki Genevieve Acteau Nicole Protopapas Wei Xu Peter Sutovsky Mark Baker Richard Oko |
| author_facet | Lauren E. Hamilton Morgan Lion Luis Aguila João Suzuki Genevieve Acteau Nicole Protopapas Wei Xu Peter Sutovsky Mark Baker Richard Oko |
| author_sort | Lauren E. Hamilton |
| collection | DOAJ |
| description | The perinuclear theca (PT) of the eutherian sperm head is a cytoskeletal-like structure that houses proteins involved in important cellular processes during spermiogenesis and fertilization. Building upon our novel discovery of non-nuclear histones in the bovine PT, we sought to investigate whether this PT localization was a conserved feature of eutherian sperm. Employing cell fractionation, immunodetection, mass spectrometry, qPCR, and intracytoplasmic sperm injections (ICSI), we examined the localization, developmental origin, and functional potential of histones from the murid PT. Immunodetection localized histones to the post-acrosomal sheath (PAS) and the perforatorium (PERF) of the PT but showed an absence in the sperm nucleus. MS/MS analysis of selectively extracted PT histones indicated that predominately core histones (i.e., H3, H3.3, H2B, H2A, H2AX, and H4) populate the murid PT. These core histones appear to be <i>de novo</i>-synthesized in round spermatids and assembled via the manchette during spermatid elongation. Mouse ICSI results suggest that early embryonic development is delayed in the absence of PT-derived core histones. Here, we provide evidence that core histones are <i>de novo</i>-synthesized prior to PT assembly and deposited in PT sub-compartments for subsequent involvement in chromatin remodeling of the male pronucleus post-fertilization. |
| first_indexed | 2024-03-10T09:15:26Z |
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| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T09:15:26Z |
| publishDate | 2021-07-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-e42d1103e99b4488876a640e2791a2762023-11-22T05:43:31ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-07-012215811910.3390/ijms22158119Core Histones Are Constituents of the Perinuclear Theca of Murid Spermatozoa: An Assessment of Their Synthesis and Assembly during Spermiogenesis and Function after Gametic FusionLauren E. Hamilton0Morgan Lion1Luis Aguila2João Suzuki3Genevieve Acteau4Nicole Protopapas5Wei Xu6Peter Sutovsky7Mark Baker8Richard Oko9Department of Biomedical and Molecular Sciences, Queen’s University, Botterell Hall, 18 Stuart Street, Kingston, ON K7L 3N6, CanadaDepartment of Biomedical and Molecular Sciences, Queen’s University, Botterell Hall, 18 Stuart Street, Kingston, ON K7L 3N6, CanadaCenter for Research in Reproduction and Fertility, Department of Veterinary Sciences, Université de Montreal, St. Hyacinthe, QC J2S 2M2, CanadaCenter for Research in Reproduction and Fertility, Department of Veterinary Sciences, Université de Montreal, St. Hyacinthe, QC J2S 2M2, CanadaDepartment of Biomedical and Molecular Sciences, Queen’s University, Botterell Hall, 18 Stuart Street, Kingston, ON K7L 3N6, CanadaDepartment of Biomedical and Molecular Sciences, Queen’s University, Botterell Hall, 18 Stuart Street, Kingston, ON K7L 3N6, CanadaDepartment of Biomedical and Molecular Sciences, Queen’s University, Botterell Hall, 18 Stuart Street, Kingston, ON K7L 3N6, CanadaDivision of Animal Science, College of Agriculture, Food and Natural Resources, University of Missouri, Columbia, MO 65211, USASchool of Environmental and Life Science, University of Newcastle, Callaghan, NSW 2308, AustraliaDepartment of Biomedical and Molecular Sciences, Queen’s University, Botterell Hall, 18 Stuart Street, Kingston, ON K7L 3N6, CanadaThe perinuclear theca (PT) of the eutherian sperm head is a cytoskeletal-like structure that houses proteins involved in important cellular processes during spermiogenesis and fertilization. Building upon our novel discovery of non-nuclear histones in the bovine PT, we sought to investigate whether this PT localization was a conserved feature of eutherian sperm. Employing cell fractionation, immunodetection, mass spectrometry, qPCR, and intracytoplasmic sperm injections (ICSI), we examined the localization, developmental origin, and functional potential of histones from the murid PT. Immunodetection localized histones to the post-acrosomal sheath (PAS) and the perforatorium (PERF) of the PT but showed an absence in the sperm nucleus. MS/MS analysis of selectively extracted PT histones indicated that predominately core histones (i.e., H3, H3.3, H2B, H2A, H2AX, and H4) populate the murid PT. These core histones appear to be <i>de novo</i>-synthesized in round spermatids and assembled via the manchette during spermatid elongation. Mouse ICSI results suggest that early embryonic development is delayed in the absence of PT-derived core histones. Here, we provide evidence that core histones are <i>de novo</i>-synthesized prior to PT assembly and deposited in PT sub-compartments for subsequent involvement in chromatin remodeling of the male pronucleus post-fertilization.https://www.mdpi.com/1422-0067/22/15/8119histonesgamete biologyspermiogenesismicrotubular manchettespermatozoaperinuclear theca |
| spellingShingle | Lauren E. Hamilton Morgan Lion Luis Aguila João Suzuki Genevieve Acteau Nicole Protopapas Wei Xu Peter Sutovsky Mark Baker Richard Oko Core Histones Are Constituents of the Perinuclear Theca of Murid Spermatozoa: An Assessment of Their Synthesis and Assembly during Spermiogenesis and Function after Gametic Fusion International Journal of Molecular Sciences histones gamete biology spermiogenesis microtubular manchette spermatozoa perinuclear theca |
| title | Core Histones Are Constituents of the Perinuclear Theca of Murid Spermatozoa: An Assessment of Their Synthesis and Assembly during Spermiogenesis and Function after Gametic Fusion |
| title_full | Core Histones Are Constituents of the Perinuclear Theca of Murid Spermatozoa: An Assessment of Their Synthesis and Assembly during Spermiogenesis and Function after Gametic Fusion |
| title_fullStr | Core Histones Are Constituents of the Perinuclear Theca of Murid Spermatozoa: An Assessment of Their Synthesis and Assembly during Spermiogenesis and Function after Gametic Fusion |
| title_full_unstemmed | Core Histones Are Constituents of the Perinuclear Theca of Murid Spermatozoa: An Assessment of Their Synthesis and Assembly during Spermiogenesis and Function after Gametic Fusion |
| title_short | Core Histones Are Constituents of the Perinuclear Theca of Murid Spermatozoa: An Assessment of Their Synthesis and Assembly during Spermiogenesis and Function after Gametic Fusion |
| title_sort | core histones are constituents of the perinuclear theca of murid spermatozoa an assessment of their synthesis and assembly during spermiogenesis and function after gametic fusion |
| topic | histones gamete biology spermiogenesis microtubular manchette spermatozoa perinuclear theca |
| url | https://www.mdpi.com/1422-0067/22/15/8119 |
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