Chromatin remodelling initiation during human spermiogenesis

被引:43
作者
de Vries, Marieke [1 ]
Ramos, Liliana [1 ]
Housein, Zjwan [1 ]
de Boer, Peter [1 ]
机构
[1] Radboud Univ Nijmegen, Med Ctr, Dept Obstet & Gynaecol, NL-6500 HB Nijmegen, Netherlands
关键词
Spermiogenesis; Chromatin remodelling; Human;
D O I
10.1242/bio.2012844
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
During the last phase of spermatogenesis, spermiogenesis, haploid round spermatids metamorphose towards spermatozoa. Extensive cytoplasmic reduction and chromatin remodelling together allow a dramatic decrease of cellular, notably nuclear volume. DNA packing by a nucleosome based chromatin structure is largely replaced by a protamine based one. At the cytoplasmic level among others the acrosome and perinuclear theca (PNT) are formed. In this study we describe the onset of chromatin remodelling to occur concomitantly with acrosome and PNT development. In spread human round spermatid nuclei, we show development of a DAPI-intense doughnut-like structure co-localizing with the acrosomal sac and sub acrosomal PNT. At this structure we observe the first gradual decrease of nucleosomes and several histones. Histone post-translational modifications linked to chromatin remodelling such as H4K8ac and H4K16ac also delineate the doughnut, that is furthermore marked by H3K9me2. During the capping phase of acrosome development, the size of the doughnut-like chromatin domain increases, and this area often is marked by uniform nucleosome loss and the first appearance of transition protein 2 and protamine 1. In the acrosome phase at nuclear elongation, chromatin remodelling follows the downward movement of the marginal ring of the acrosome. Our results indicate that acrosome development and chromatin remodelling are interacting processes. In the discussion we relate chromatin remodelling to the available data on the nuclear envelope and the linker of nucleoskeleton and cytoskeleton (LINC) complex of spermatids, suggesting a signalling route for triggering chromatin remodelling. (C) 2012. Published by The Company of Biologists Ltd.
引用
收藏
页码:446 / 457
页数:12
相关论文
共 92 条
[1]  
Albig W, 1996, HUM GENET, V97, P486
[2]  
Alsheimer M, 1998, J CELL SCI, V111, P2227
[3]   Histone ubiquitination and chromatin remodeling in mouse spermatogenesis [J].
Baarends, WM ;
Hoogerbrugge, TW ;
Roest, HP ;
Ooms, M ;
Vreeburg, J ;
Hoeijmakers, JHJ ;
Grootegoed, JA .
DEVELOPMENTAL BIOLOGY, 1999, 207 (02) :322-333
[4]   The protamine family of sperm nuclear proteins [J].
Balhorn, Rod .
GENOME BIOLOGY, 2007, 8 (09)
[5]   IMMUNOELECTRON MICROSCOPIC DISTRIBUTION OF HISTONE-H2B AND HISTONE-H3 AND PROTAMINES IN THE COURSE OF MOUSE SPERMIOGENESIS [J].
BIGGIOGERA, M ;
MULLER, S ;
COURTENS, JL ;
FAKAN, S ;
ROMANINI, MGM .
MICROSCOPY RESEARCH AND TECHNIQUE, 1992, 20 (03) :259-267
[6]   A new insight into male genome reprogramming by histone variants and histone code [J].
Boussouar, Faycal ;
Rousseaux, Sophie ;
Khochbin, Saadi .
CELL CYCLE, 2008, 7 (22) :3499-3502
[7]   Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa [J].
Brykczynska, Urszula ;
Hisano, Mizue ;
Erkek, Serap ;
Ramos, Liliana ;
Oakeley, Edward J. ;
Roloff, Tim C. ;
Beisel, Christian ;
Schuebeler, Dirk ;
Stadler, Michael B. ;
Peters, Antoine H. F. M. .
NATURE STRUCTURAL & MOLECULAR BIOLOGY, 2010, 17 (06) :679-U47
[8]   The aetiology of sperm protamine abnormalities and their potential impact on the sperm epigenome [J].
Carrell, Douglas T. ;
Emery, Benjamin R. ;
Hammoud, Sue .
INTERNATIONAL JOURNAL OF ANDROLOGY, 2008, 31 (06) :537-545
[9]   Characterization of aneuploidy rates, protamine levels, ultrastructure, and functional ability of round-headed sperm from two siblings and implications for intracytoplasmic sperm injection [J].
Carrell, DT ;
Emery, BR ;
Liu, LH .
FERTILITY AND STERILITY, 1999, 71 (03) :511-516
[10]   Changes in intranuclear chromatin architecture induce bipolar nuclear localization of histone variant H1T2 in male haploid spermatids [J].
Catena, Raffaella ;
Ronfani, Lorenza ;
Sassone-Corsi, Paolo ;
Davidson, Irwin .
DEVELOPMENTAL BIOLOGY, 2006, 296 (01) :231-238