Histone H1 and evolution of sperm nuclear basic proteins.

The Three Main Groups of Sperm Nucleus Basic Proteins (SNBPs) In early studies on the chemical composition of the cell nucleus, it was found that the nucleic acid initially called “nuclein” (1) could form salt-like linkages with two different complexing substances, referred to as “protamine” (2) and “histone” (3). By the end of the nineteenth century, the true protein nature of these complexing substances had been established (3, 4). Early characterization of the nucleoprotein complexes (chromatin) showed that whereas the major chromatin proteins from somatic cells consisted of histones, the protein composition of chromatin from sperm cells consisted of either histones (as in carp (5)) or protamines (as in salmon (2)). Further progress on the chemical characterization of the SNBPs revealed a large degree of compositional variability and structural heterogeneity (6–8), which contrasts with the evolutionarily conserved chemical nature and low structure variability of histones from somatic cells (9). An early attempt to classify the SNBPs was carried out by David Bloch in 1969 (10). In this classification (see Fig. 1), Bloch distinguished among the following types: Salmo type (arginine-rich protamines from fish, “monoprotamines”), mousegrasshopper type (containing –SH groups, “stable protamines”), Mytilus type (intermediate between histones and protamines), Rana type (histones), and crab type (no basic proteins in the large uncondensed nucleus such that DNA appears essentially naked). However, the heterogeneity of the SNBPs and the phylogenetically scattered nature of the organisms for which SNBP information was available masked any evidence of an evolutionary relationship among these proteins. As more information has become available a clearer understanding of the possible mechanisms underlying SNBP variability has started to emerge (11). In recent years, studies have been designed to gather information about the SNBPs from different groups of phylogenetically related organisms (12, 13). The result of this phylogenetically based approach has proved to be rewarding not only for providing a better insight into the classification of these proteins but also for providing a deeper understanding of their evolution. Based on current information, SNBPs can be grouped in three main categories: histone type (H type); protamine type (P type); and protamine-like (PL type) (12) (see Fig. 1). The first group of SNBPs in this classification, histone type (H type), basically corresponds to Bloch’s Rana type. It consists of histones that are compositionally and structurally related to the histones that are found in the nuclei of somatic cells (Fig. 2, lanes H and Fig. 3, panel 1). This group includes sperm-specific variants mainly for histones H1 and H2B (spH1, spH2B) such as those present in the sperm of echinoderms (14–16). The second group of SNBPs, the protamine type (P type) (Fig. 2, lanes P), consists of arginine-rich (Arg $ 30 mol %) highly basic proteins (His 1 Lys 1 Arg 5 45–80 mol %, Ser 1 Thr 1 Gly 5 10–25 mol %) (17) of relatively small molecular mass (approximately 4000 # Mr # 10,000) (Fig. 3, panels 4 and 5). This group includes the Salmo and mouse type of Bloch’s classification. During spermiogenesis, these proteins replace the majority of the germinal somatic-like histones that are present at the onset of spermatogenesis, and they are the main SNBPs found in mature sperm. The protamine-like (PL) type is the third group of proteins of this classification (8, 12, 18) (Fig. 2, lanes PL) and is the most structurally heterogeneous group. This group is equivalent to the Mytilus type in Bloch’s classification. It consists of basic proteins having an arginine 1 lysine content that usually amounts to at least 35–50 mol % (12). All of the proteins from this group are closely related to molecules from the histone H1 family (12, 19, 20). Although initially described in bivalve molluscs (19, 20) (Fig. 2, lanes 4–6 and Fig. 3, panels 2 and 3), these SNBPs are widespread throughout the animal kingdom. The PL proteins have been identified in phylogenetically distant groups such as in the phylum Cnidaria (21, 22) (Fig. 2, lane 3) and in chordates (23) and vertebrates (24). The PL proteins replace most of the histone components during spermiogenesis, although to a smaller extent than the proteins of the P type (12). In most instances, PL proteins coexist in the mature sperm with a full histone complement (19, 25) amounting to 20–25% of the total SNBPs. Despite the apparent structural variability of SNBPs (Fig. 1), most of the SNBPs characterized so far can be classified within these three protein types (12).