Meiotic synthesis of testis histones in the rat.

Brock, William A.; Trostle, Patricia K.; Meistrich, Marvin L.

doi:10.1073/pnas.77.1.371

Cited by 55 publications

(31 citation statements)

References 27 publications

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“…Although it had been generally believed that there was negligible histone synthesis during spermiogenesis [24], recent studies of ssH2B [6] and other histone transcripts [20] showed that histones can be synthesized in round spermatids. The absence of ssH2B protein in pachytene spermatocytes and its appearance in round spermatids indicated that this histone variant is synthesized in round spermatids.…”

Section: Discussionmentioning

confidence: 99%

Stage-Specific Distribution of the Spermatid-Specific Histone 2b in the Rat Testis1

Unni

Zhang

Kangasniemi

et al. 1995

Biology of Reproduction

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Male germ cells contain a number of histone variants, most of which are synthesized during either the mitotic or the meiotic stages of spermatogenesis. A spermatid-specific H2B (ssH2B) variant has been identified in mouse round spermatids that has an additional 12 amino acids at its carboxyl terminus as compared to somatic H2Bs. Until now, the presence of this protein in other mammals has not been known. Northern blot analysis using an oligonucleotide probe complementary to a unique coding region of the C-terminus of mouse ssH2B showed that mRNA encoding this protein was present in isolated rat round spermatids. Furthermore, immunoblot analysis of basic nuclear proteins from round spermatids probed with an anti-ssH2B antiserum that recognizes the novel peptide sequence indicated that the protein was present in round spermatids but not in pachytene spermatocytes. The ssH2B comigrated with H2A.X by acid-urea (2.5 M) PAGE and migrated slightly more slowly than TH2B by acid-urea-Triton PAGE. When seminiferous tubules were microdissected stage-specifically and basic nuclear proteins were immunoblotted, ssH2B was detected in tubule sections of stages II-VI. It reached a maximum level in stages VII-VIII and then decreased to minimal levels in stages XIII-I. Since ssH2B was not detected in pachytene spermatocytes, the stage-specific levels of ssH2B corresponded to the respective steps of spermatids present in the tubules. While ssH2B constituted a relatively small amount (approximately 2%) of total H2B protein in round spermatids, its presence in both the mouse and the rat suggests that its function may be conserved in mammalian spermatogenic cells.

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Section: Discussionmentioning

confidence: 99%

Stage-Specific Distribution of the Spermatid-Specific Histone 2b in the Rat Testis1

Unni

Zhang

Kangasniemi

et al. 1995

Biology of Reproduction

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“…Variations in each core histone may provide functional modulation in chromatin organization. In murine and human spermatogenic cells, testis-specific or enriched core histones, with the exception of H4, appear in chromatin at different stages during spermatogenesis (Brock et al, 1980;Meistrich et al, 1985;Doenecke et al, 1997b).…”

Section: Nucleosomal Core Histonesmentioning

confidence: 99%

Male germline-specific histones in mouse and man

Churikov

Zalenskaya

Zalensky³

2004

Cytogenet Genome Res

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In mice and humans, the production of male gametes is a result of a complex multistep process of stem cell differentiation. The final product, the mature spermatozoon, is designed for the safe delivery of a haploid copy of the paternal genetic information to the oocyte in a structural state suitable for zygote formation and embryogenesis. A remarkable structural reorganization of chromosomes in germline cells during mammalian spermatogenesis has been characterized. The most important steps are connected with the recombination events during meiosis and the final packaging of the haploid genome in the genetically inert, compacted nucleus of the sperm. Underlying the changes in chromatin organization is the appearance of testis-specific histones. Although the existence of such histones has been known for decades, their exact functions still are not established. Deciphering of the mouse and human genomes has allowed a more detailed description of the organization and regulation of the testis-specific histone genes. In addition, it has facilitated the discovery of previously unknown proteins. This review summarizes contemporary information on these germline-specific/enriched histones in both the mouse and human and outlines early achievements in the identification of their functions.

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“…In the spermatogenic lineage of mammals, the synthesis of replication-dependent variants has not been detected later than the pachytene stage of meiosis (8). Most testis-specific variants are synthesized in spermatogonia and spermatocytes and ultimately replace replication-dependent variants in the chromatin of spermatocytes.…”

mentioning

confidence: 99%

Expression of replication-dependent histone genes in avian spermatids involves an alternate pathway of mRNA 3'-end formation.

Challoner¹,

Moss²,

Groudine³

1989

Mol. Cell. Biol.

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In somatic cells the expression of replication-dependent histone genes is coupled to the S phase of the cell cycle. However, we have found a number of novel H2a, H2b, and H3 poly(A)+ RNA species in avian haploid round spermatids. The spermatid-specific H2a and H2b 0.8-kilobase RNAs are transcribed from a subset of the replication-dependent H2a and H2b gene families. Two cDNAs derived from the spermatid-specific H2b transcripts were isolated and sequenced. The structures of these cDNAs reveal that the spermatid-specific RNAs are identical to the 0.5-kilobase poly(A)-H2b mRNAs expressed in proliferating somatic cells, except for the addition of poly(A) at the 3' ends. The site of poly(A) addition in the spermatid-specific RNAs is located 26 to 28 nucleotides 3' of the poly(A)-H2b mRNA terminus. Thus, the hairpin structures and purine-rich elements required for the U7 small nuclear ribonucleoprotein-mediated cleavage reaction that generates the 3' ends of poly(A)-H2b mRNAs are not utilized in spermatids and are retained in the poly(A)+ H2b RNAs.In higher eucaryotes the predominant class of histone proteins consists of replication-dependent variants that are synthesized during the S phase of the mitotic cell cycle. The expression of mRNAs encoding these proteins is coupled to DNA replication by a variety of transcriptional and posttranscriptional regulatory mechanisms. First, cells undergoing DNA replication sustain a three-to fivefold increase in the rate of histone transcription (18,29). This increase occurs through the interaction of several promoter-proximal sequences with trans-acting regulatory factors (16,21,50). Second, recent experiments suggest that the 3' processing of histone primary transcripts can contribute to the cell cycle regulation of the mature mRNAs. During the S phase the poly(A)-3' termini of histone mRNAs are produced by an endonucleolytic cleavage reaction involving an Sm subtype small nuclear ribonucleoprotein (snRNP) containing the U7 small nuclear RNA (15,40,51). This reaction requires a hairpin structure formed by a conserved hyphenated symmetrical dyad element immediately 5' of the cleavage site in the histone pre-mRNA, as well as a more distal purine-rich sequence (3-5). If cells are arrested in Gi, the amount of U7 snRNP remains relatively constant, but histone mRNA precursors accumulate as a heat-labile regulatory factor necessary for 3' processing becomes limiting (22,35). Third, there is an increase in the rate of histone mRNA degradation when cells progress from S to G2 or when DNA synthesis is inhibited (48,49). This specific degradation of histone mRNA requires the hairpin structure at the 3' terminus of the molecule (33, 41); consequently, degradation initiates at the 3' end of the histone mRNA and proceeds toward the 5' end (45).The less prevalent replacement and tissue-specific variant histones are not subject to the cell cycle regulation that governs the expression of replication-dependent variants. Since steady-state levels of replacement variant transcripts typically do no...

show abstract

Meiotic synthesis of testis histones in the rat.

Cited by 55 publications

References 27 publications

Stage-Specific Distribution of the Spermatid-Specific Histone 2b in the Rat Testis1

Stage-Specific Distribution of the Spermatid-Specific Histone 2b in the Rat Testis1

Male germline-specific histones in mouse and man

Expression of replication-dependent histone genes in avian spermatids involves an alternate pathway of mRNA 3'-end formation.

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