Testis-Specific Histone Variant H3t Gene Is Essential for Entry into Spermatogenesis

Cellular differentiation is associated with dynamic chromatin remodeling in establishing a cell-type-specific epigenomic landscape. Here, we find that mouse testis-specific and replication-dependent histone H3 variant H3t is essential for very early stages of spermatogenesis. H3t gene deficiency lea...

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Main Authors: Jun Ueda, Akihito Harada, Takashi Urahama, Shinichi Machida, Kazumitsu Maehara, Masashi Hada, Yoshinori Makino, Jumpei Nogami, Naoki Horikoshi, Akihisa Osakabe, Hiroyuki Taguchi, Hiroki Tanaka, Hiroaki Tachiwana, Tatsuma Yao, Minami Yamada, Takashi Iwamoto, Ayako Isotani, Masahito Ikawa, Taro Tachibana, Yuki Okada, Hiroshi Kimura, Yasuyuki Ohkawa, Hitoshi Kurumizaka, Kazuo Yamagata
Format: Article
Language:English
Published: Elsevier 2017-01-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124716317727
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author Jun Ueda
Akihito Harada
Takashi Urahama
Shinichi Machida
Kazumitsu Maehara
Masashi Hada
Yoshinori Makino
Jumpei Nogami
Naoki Horikoshi
Akihisa Osakabe
Hiroyuki Taguchi
Hiroki Tanaka
Hiroaki Tachiwana
Tatsuma Yao
Minami Yamada
Takashi Iwamoto
Ayako Isotani
Masahito Ikawa
Taro Tachibana
Yuki Okada
Hiroshi Kimura
Yasuyuki Ohkawa
Hitoshi Kurumizaka
Kazuo Yamagata
author_facet Jun Ueda
Akihito Harada
Takashi Urahama
Shinichi Machida
Kazumitsu Maehara
Masashi Hada
Yoshinori Makino
Jumpei Nogami
Naoki Horikoshi
Akihisa Osakabe
Hiroyuki Taguchi
Hiroki Tanaka
Hiroaki Tachiwana
Tatsuma Yao
Minami Yamada
Takashi Iwamoto
Ayako Isotani
Masahito Ikawa
Taro Tachibana
Yuki Okada
Hiroshi Kimura
Yasuyuki Ohkawa
Hitoshi Kurumizaka
Kazuo Yamagata
author_sort Jun Ueda
collection DOAJ
description Cellular differentiation is associated with dynamic chromatin remodeling in establishing a cell-type-specific epigenomic landscape. Here, we find that mouse testis-specific and replication-dependent histone H3 variant H3t is essential for very early stages of spermatogenesis. H3t gene deficiency leads to azoospermia because of the loss of haploid germ cells. When differentiating spermatogonia emerge in normal spermatogenesis, H3t appears and replaces the canonical H3 proteins. Structural and biochemical analyses reveal that H3t-containing nucleosomes are more flexible than the canonical nucleosomes. Thus, by incorporating H3t into the genome during spermatogonial differentiation, male germ cells are able to enter meiosis and beyond.
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spelling doaj.art-06d1e957ec7a424ab096f2a87b360b822022-12-22T00:13:56ZengElsevierCell Reports2211-12472017-01-0118359360010.1016/j.celrep.2016.12.065Testis-Specific Histone Variant H3t Gene Is Essential for Entry into SpermatogenesisJun Ueda0Akihito Harada1Takashi Urahama2Shinichi Machida3Kazumitsu Maehara4Masashi Hada5Yoshinori Makino6Jumpei Nogami7Naoki Horikoshi8Akihisa Osakabe9Hiroyuki Taguchi10Hiroki Tanaka11Hiroaki Tachiwana12Tatsuma Yao13Minami Yamada14Takashi Iwamoto15Ayako Isotani16Masahito Ikawa17Taro Tachibana18Yuki Okada19Hiroshi Kimura20Yasuyuki Ohkawa21Hitoshi Kurumizaka22Kazuo Yamagata23Center for Education in Laboratory Animal Research, Chubu University, Kasugai, Aichi 487-8501, JapanDivision of Transcriptomics, Medical Institute of Bioregulation, Kyushu University, Fukuoka 812-8582, JapanLaboratory of Structural Biology, Graduate School of Advanced Science & Engineering, Waseda University, Tokyo 162-8480, JapanLaboratory of Structural Biology, Graduate School of Advanced Science & Engineering, Waseda University, Tokyo 162-8480, JapanDivision of Transcriptomics, Medical Institute of Bioregulation, Kyushu University, Fukuoka 812-8582, JapanLaboratory of Pathology and Development, Institute of Molecular and Cellular Biosciences, University of Tokyo, Tokyo 113-0032, JapanLaboratory of Pathology and Development, Institute of Molecular and Cellular Biosciences, University of Tokyo, Tokyo 113-0032, JapanDivision of Transcriptomics, Medical Institute of Bioregulation, Kyushu University, Fukuoka 812-8582, JapanLaboratory of Structural Biology, Graduate School of Advanced Science & Engineering, Waseda University, Tokyo 162-8480, JapanLaboratory of Structural Biology, Graduate School of Advanced Science & Engineering, Waseda University, Tokyo 162-8480, JapanLaboratory of Structural Biology, Graduate School of Advanced Science & Engineering, Waseda University, Tokyo 162-8480, JapanLaboratory of Structural Biology, Graduate School of Advanced Science & Engineering, Waseda University, Tokyo 162-8480, JapanLaboratory of Structural Biology, Graduate School of Advanced Science & Engineering, Waseda University, Tokyo 162-8480, JapanResearch and Development Center, Fuso Pharmaceutical Industries, Ltd., Osaka 536-8523, JapanCenter for Education in Laboratory Animal Research, Chubu University, Kasugai, Aichi 487-8501, JapanCenter for Education in Laboratory Animal Research, Chubu University, Kasugai, Aichi 487-8501, JapanCenter for Genetic Analysis of Biological Responses, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita 565-0871, JapanCenter for Genetic Analysis of Biological Responses, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita 565-0871, JapanDepartment of Bioengineering, Graduate School of Engineering, Osaka City University, Osaka 558-8585, JapanLaboratory of Pathology and Development, Institute of Molecular and Cellular Biosciences, University of Tokyo, Tokyo 113-0032, JapanGraduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259 Nagatsuta-cho, Midori-ku, Yokohama 226-8501, JapanDivision of Transcriptomics, Medical Institute of Bioregulation, Kyushu University, Fukuoka 812-8582, JapanLaboratory of Structural Biology, Graduate School of Advanced Science & Engineering, Waseda University, Tokyo 162-8480, JapanCenter for Genetic Analysis of Biological Responses, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita 565-0871, JapanCellular differentiation is associated with dynamic chromatin remodeling in establishing a cell-type-specific epigenomic landscape. Here, we find that mouse testis-specific and replication-dependent histone H3 variant H3t is essential for very early stages of spermatogenesis. H3t gene deficiency leads to azoospermia because of the loss of haploid germ cells. When differentiating spermatogonia emerge in normal spermatogenesis, H3t appears and replaces the canonical H3 proteins. Structural and biochemical analyses reveal that H3t-containing nucleosomes are more flexible than the canonical nucleosomes. Thus, by incorporating H3t into the genome during spermatogonial differentiation, male germ cells are able to enter meiosis and beyond.http://www.sciencedirect.com/science/article/pii/S2211124716317727histone variantspermatogenesisnucleosomechromatincrystal structureepigeneticstestesmeiosisspermatogonial differentiationspermatozoa
spellingShingle Jun Ueda
Akihito Harada
Takashi Urahama
Shinichi Machida
Kazumitsu Maehara
Masashi Hada
Yoshinori Makino
Jumpei Nogami
Naoki Horikoshi
Akihisa Osakabe
Hiroyuki Taguchi
Hiroki Tanaka
Hiroaki Tachiwana
Tatsuma Yao
Minami Yamada
Takashi Iwamoto
Ayako Isotani
Masahito Ikawa
Taro Tachibana
Yuki Okada
Hiroshi Kimura
Yasuyuki Ohkawa
Hitoshi Kurumizaka
Kazuo Yamagata
Testis-Specific Histone Variant H3t Gene Is Essential for Entry into Spermatogenesis
Cell Reports
histone variant
spermatogenesis
nucleosome
chromatin
crystal structure
epigenetics
testes
meiosis
spermatogonial differentiation
spermatozoa
title Testis-Specific Histone Variant H3t Gene Is Essential for Entry into Spermatogenesis
title_full Testis-Specific Histone Variant H3t Gene Is Essential for Entry into Spermatogenesis
title_fullStr Testis-Specific Histone Variant H3t Gene Is Essential for Entry into Spermatogenesis
title_full_unstemmed Testis-Specific Histone Variant H3t Gene Is Essential for Entry into Spermatogenesis
title_short Testis-Specific Histone Variant H3t Gene Is Essential for Entry into Spermatogenesis
title_sort testis specific histone variant h3t gene is essential for entry into spermatogenesis
topic histone variant
spermatogenesis
nucleosome
chromatin
crystal structure
epigenetics
testes
meiosis
spermatogonial differentiation
spermatozoa
url http://www.sciencedirect.com/science/article/pii/S2211124716317727
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