Replacement of nucleosomal histones by histone H1-like proteins during spermiogenesis in Cnidaria: Evolutionary implications

Rocchini, Corinne; Marx, Roswitha M.; Carosfeld, Joachim Schnorr von; Kasinsky, Harold E.; Rosenberg, Ellen; Sommer, Freya; Ausió, Juan

doi:10.1007/bf02198850

Cited by 29 publications

(31 citation statements)

References 14 publications

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“…(36) Further evidence for the vertical evolution of SNBPs can be obtained from the exclusive presence of H-type SNBPs in sponges (45) and the presence of RI histone H1-related PL proteins (PL-I) in the sperm of different cnidarians. (46,47) Furthermore, SNBPs of the PL-and P-types are more prevalent in the sperm of taxonomic groups located on the upper phylogenetic branches of bilaterian evolution, (14,48) as shown in Fig. 2.…”

Section: Mechanisms Of Long-term Evolution Of Sperm Nuclear Basic Promentioning

confidence: 96%

Origin and evolution of chromosomal sperm proteins

Eirín‐López

Ausió

2009

BioEssays

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In the eukaryotic cell, DNA compaction is achieved through its interaction with histones, constituting a nucleoprotein complex called chromatin. During metazoan evolution, the different structural and functional constraints imposed on the somatic and germinal cell lines led to a unique process of specialization of the sperm nuclear basic proteins (SNBPs) associated with chromatin in male germ cells. SNBPs encompass a heterogeneous group of proteins which, since their discovery in the nineteenth century, have been studied extensively in different organisms. However, the origin and controversial mechanisms driving the evolution of this group of proteins has only recently started to be understood. Here, we analyze in detail the histone hypothesis for the vertical parallel evolution of SNBPs, involving a "vertical" transition from a histone to a protamine-like and finally protamine types (H --> PL --> P), the last one of which is present in the sperm of organisms at the uppermost tips of the phylogenetic tree. In particular, the common ancestry shared by the protamine-like (PL)- and protamine (P)-types with histone H1 is discussed within the context of the diverse structural and functional constraints acting upon these proteins during bilaterian evolution.

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Section: Mechanisms Of Long-term Evolution Of Sperm Nuclear Basic Promentioning

confidence: 96%

Origin and evolution of chromosomal sperm proteins

Eirín‐López

Ausió

2009

BioEssays

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“…The idea that sperm basic chromatin proteins originated from histones was originally proposed by Subirana et al (30). This hypothesis has since been refined by Ausio and co-workers to suggest that such proteins arose from a primitive histone H1, and it is supported by their extensive biochemical analysis of sperm nuclear proteins from a wide variety of lower eukaryotes (31)(32)(33). The isolation and characterization of winter flounder clone 2B provides evidence in vertebrates that specialized sperm chromatin proteins have evolved from the N-terminal tail of a progenitor linker histone.…”

Section: Fig 4 Genomic Clone 2b Contains 32-amino Acid Repeatsmentioning

confidence: 85%

The High Molecular Weight Chromatin Proteins of Winter Flounder Sperm Are Related to an Extreme Histone H1 Variant

Watson¹,

Davies

1998

Journal of Biological Chemistry

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Unlike mammals, birds, and most other fishes, winter flounder completes spermatogenesis without replacing its germ cell histones with protamines. Instead, during spermiogenesis, these fish produce a family of high molecular weight (80,000 -200,000) basic nuclear proteins (HM r BNPs) that bind to sperm chromatin containing the normal complement of histones. These large, basic proteins are built up of tandem iterations of oligopeptide repeats that contain phosphorylatable DNA-binding motifs. Although the HM r BNPs have no obvious homology to histones, protamines, or other sperm-specific chromatin proteins, we report here the isolation of a clone (2B) from a winter flounder genomic DNA library that establishes a link between the HM r BNPs and histone H1. The 2B sequence contains an open reading frame, which, when conceptually translated, encodes a 265-residue protein. At its N terminus the translation product contains numerous simple repeats that match the oligopeptides contained within the HM r BNPs. Unexpectedly, the C terminus of the putative protein shows 66% identity and 76% conservation to the histone H1 globular domain. This connection suggests that the HM r BNPs may have originated from the extended N-terminal tail region of a testis-specific, H1-like linker histone.In almost all eukaryotic cells, histones have a fundamental role in organizing and condensing DNA (1, 2). It is therefore not surprising that the sequences of the core histones (H2A, H2B, H3, and H4) are extremely well conserved and contain many basic residues. The fifth histone (H1), which may or may not sit outside the nucleosomal core (3), is the longest, most variable, and most lysine-rich member of the histone family. The structure of histone H1 can be subdivided into three domains: a variable N-terminal region of 35-40 residues with a net positive charge followed by a well conserved globular domain of 80 residues (4), which is thought to interact with both core histones and nucleosomal DNA, and a very basic C-terminal tail of ϳ90 residues, 90% of which is lysine, alanine, and proline.Most organisms possess more than one tissue-or stagespecific histone H1 variant (5, 6). For example, sperm-specific histone H1 variants (H1T) are commonly found in mammals (6), amphibians (7), and invertebrates (8, 9). H1Ts typically have a shorter C-terminal domain and tails that contain a higher proportion of positively charged residues (usually Arg) than their somatic counterparts, as well as a greater number of phosphorylation sites (6). However, the sperm-specific H1 of sea urchin (SpH1) is longer than its somatic counterpart at both ends due to N-and C-terminal extensions composed of tetrapeptide repeats (SPXB, where X is usually basic, and B is K or R) (10).This trend to increased basicity and a higher arginine content in sperm-specific histones may facilitate condensation of the DNA into the sperm nucleus. In fact, the switch from somatic to sperm chromatin can be accomplished using a variety of proteins. One strategy used by some vertebrates and many ...

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“…In contrast, African clawed frog spermatozoa appeared to be fairly resistant to DNA fragmentation (Pollock et al 2015). Although cysteine residues have been reported in the protamine-like proteins and H1 histones of some bivalve molluscs (Zhang et al 1999), anemones (Rocchini et al 1996) and tunicates (Saperas et al 1992;Zhang et al 1999), Yokota (et al 1991 claim that none of the SNBPs of African clawed frog spermatozoa contained cysteine, despite amino acid sequence analysis revealing molar percentages up to 0.8% in seven of the eight proteins examined. While it is possible that the negligible levels of cysteine residues observed in African clawed frog spermatozoa may contribute to the stabilisation of the sperm chromatin, it seems more likely to be a function of the high arginine content of the SNBPs (up to 41.2%; Yokota et al 1991) in this species.…”

Section: Amphibian Sperm Nuclear Basic Proteins (Snbps)mentioning

confidence: 96%

“…and prototherian mammals examined thus far do not appear to contain any cysteine residues in their sperm protamine and therefore lack the capacity for disulphide bonding to stabilise the sperm chromatin (Cortés-Gutiérrez et al 2014b;Johnston et al 2015). While generally uncommon, cysteine residues have been reported in the histone variants of the grey short-tailed opossum (Monodelphis domestica; Johnston et al 2015), as well as in some lower vertebrates (Saperas et al 1992;Rocchini et al 1996;Zhang et al 1999), indicating the possibility of histone-mediated disulphide bonds in these species. Hence, alternative stabilising mechanisms are likely to function in these species but much further investigation is required.…”

Section: Chromatin Remodelling In Mammalian Spermatozoamentioning

confidence: 99%

“…While it is possible that the negligible levels of cysteine residues observed in African clawed frog spermatozoa may contribute to the stabilisation of the sperm chromatin, it seems more likely to be a function of the high arginine content of the SNBPs (up to 41.2%; Yokota et al 1991) in this species. Interestingly, DNA fragmentation was only revealed in common dunnart (Sminthopsis murina; Johnston et al 2015) spermatozoa following exposure to aggressive protein lysis and a high concentration of a disulphide bondreducing agent (1.0 M β-mercaptoethanol), despite possessing cysteine-free protamines; this phenomenon prompted the authors to suggest that the cysteine residues associated with some histones/histone variants, as seen in some lower vertebrates (Saperas et al 1992;Rocchini et al 1996;Zhang et al 1999), could potentially establish disulphide bonds in species that retain high levels of histones in their mature spermatozoa. Yet, the sperm chromatin of zebrafish characterised solely by somatic histones and a nucleosomal core structure (Ausio et al 2014), is among the most susceptible to rapid DNA fragmentation.…”

Section: Amphibian Sperm Nuclear Basic Proteins (Snbps)mentioning

confidence: 99%

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Amphibian sperm DNA fragmentation

Pollock¹

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There are extremely limited studies that have investigated DNA fragmentation in amphibians and even less information exists pertaining to DNA fragmentation in the spermatozoa.A DNA fragmentation assay applied and validated for amphibian spermatozoa would not only provide the first evidence of this phenomenon in a new major taxon, but also prove a valuable tool for developing improvements in ART used in the captive propagation of threatened and endangered species. Consequently, the fundamental aim of this project was the development and validation of the sperm chromatin dispersion (SCD) test for amphibian spermatozoa with the purpose of investigating the dynamic behaviour of amphibian sperm DNA in response to cryopreservation.The SCD test was first applied to African clawed frog (Xenopus laevis) as an amphibian sperm model using a species-specific modified lysing solution for protein depletion. Sperm DNA fragmentation (SDF) was assessed immediately following activation of sperm motility (T0) and again after one hour and 24 hours of incubation in order to produce a range of spermatozoa with differing levels of DNA damage. The SCD procedure resulted in the production of three nuclear morphotypes; amphibian sperm morphotype 1 (ASM-1) and ASM-2 showed no evidence of DNA damage, whereas ASM-3 spermatozoa were highly fragmented with large halos of dispersed DNA fragments and a reduced nuclear core. Levels of SDF revealed by the SCD test were highly correlated with results produced using in situ nick hybridisation with DNA-specific molecular probes (ISNT) and the double comet assay (r = 0.9613). The alkaline step of the double-comet assay revealed the extensive presence of structural single-stranded DNA breaks (SSB) and provided grounds for the suggestion that alkali labile sites (ALS) are a constitutive feature of African clawed frog sperm chromatin.SDF is a dynamic process and has been shown to increase with incubation at room temperature as well as following cryopreservation. However, the mechanisms of DNA cryoinjury and the resulting effect on the potential reproductive output of ART remain open to interpretation.Consequently, dynamic changes to the basal level of DNA fragmentation were examined in fresh African clawed frog spermatozoa in comparison with the post-thaw integrity of cryopreserved (-80 °C) and frozen (-20 °C) sperm DNA. SDF was examined initially at T0 and over incubation of up to 60 minutes. The difference in SDF was only marginal for fresh, frozen (-20 °C) and cryopreserved (-80 °C) spermatozoa examined at the onset of the experiment immediately upon thawing, however, a significant increase (p = 0.004) in SDF, albeit of a low magnitude, was observed in activated ii cryopreserved (-80 °C) spermatozoa following incubation. Although African clawed frog spermatozoa appeared to be highly resistant to cryopreservation-induced DNA damage, cryopreserved-thawed spermatozoa yielded a significantly lower (p = 0.0065) fertilisation rate than fresh spermatozoa.In order to provide further insight into cryo...

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Replacement of nucleosomal histones by histone H1-like proteins during spermiogenesis in Cnidaria: Evolutionary implications

Cited by 29 publications

References 14 publications

Origin and evolution of chromosomal sperm proteins

Origin and evolution of chromosomal sperm proteins

The High Molecular Weight Chromatin Proteins of Winter Flounder Sperm Are Related to an Extreme Histone H1 Variant

Amphibian sperm DNA fragmentation

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