Transitions in histone variants during sea urchin spermatogenesis

Poccia, Dominic; Simpson, Marcia V.; Green, G.R.

doi:10.1016/0012-1606(87)90181-3

Cited by 65 publications

(38 citation statements)

References 17 publications

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“…While the CS histones are expressed in oogenesis and early development (references 35 and 47 and this study), the sperm H2B and H1 proteins are synthesized exclusively during spermatogenesis (13,54). These sperm histones are first expressed in spermatogonia and subsequently function as normal histones in transcription and replication during meiosis due to the fact that their basic N-terminal extensions are phosphorylated and thus neutralized (52). At the late spermatid stage, these N-terminal sequences become dephosphorylated (52) and subsequently stabilize the highly condensed and transcriptionally inert chromatin of the mature sperm by strong ionic interaction with linker DNA (30,36).…”

Section: Discussionmentioning

confidence: 76%

The Five Cleavage-Stage (CS) Histones of the Sea Urchin Are Encoded by a Maternally Expressed Family of Replacement Histone Genes: Functional Equivalence of the CS H1 and Frog H1M (B4) Proteins

Mandl

Brandt

Superti‐Furga

et al. 1997

Molecular and Cellular Biology

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The cleavage-stage (CS) histones of the sea urchin are known to be maternally expressed in the egg, have been implicated in chromatin remodeling of the male pronucleus following fertilization, and are the only histone variants present in embryonic chromatin up to the four-cell stage. With the help of partial peptide sequence information, we have isolated and identified CS H1, H2A, H2B, H3, and H4 cDNAs from egg poly(A) ؉ mRNA of the sea urchin Psammechinus miliaris. All five CS proteins correspond to replacement histone variants which are encoded by replication-independent genes containing introns, poly(A) addition signals, and long nontranslated sequences. Transcripts of the CS histone genes could be detected only during oogenesis and in development up to the early blastula stage. The CS proteins, with the exception of H4, are unique histones which are distantly related in sequence to the early, late, and sperm histone subtypes of the sea urchin. In contrast, the CS H1 protein displays highest sequence homology with the H1M (B4) histone of Xenopus laevis. Both H1 proteins are replacement histone variants with very similar developmental expression profiles in their respective species, thus indicating that the frog H1M (B4) gene is a vertebrate homolog of the CS H1 gene. These data furthermore suggest that the CS histones are of ancient evolutionary origin and may perform similar conserved functions during oogenesis and early development in different species.Histones are basic proteins that associate with each other and nuclear DNA to form the nucleosome. This basic unit of chromatin consists of two molecules each of the core histones H2A, H2B, H3, and H4, while the H1 protein interacts both with the histone octamer and with linker DNA and is responsible for packaging nucleosomes into higher-order structures. The core histones H3 and H4 are almost invariant in evolution. The less well conserved H2A and H2B proteins often occur as different subtypes within the same organism, while the H1 protein is the most variable of all histones (reviewed in reference 66).The expression of the majority of histone genes is tightly coupled to DNA synthesis by specific transcriptional and posttranscriptional mechanisms. These so-called replication histone genes code for mRNAs with short 5Ј and 3Ј untranslated regions; they lack introns and polyadenylation sequences but instead end in a 3Ј-terminal palindrome (11, 34) that serves as a recognition sequence for U7 snRNP-mediated 3Ј processing of histone pre-mRNA (5). A minor group of histone genes is expressed at a basal level throughout the cell cycle in proliferating cells and at a reduced but significant rate in quiescent cells, where their proteins gradually replace the replicationdependent histones in the chromatin (73, 74). These so-called replacement histone genes contain introns, code for polyadenylated mRNA with long untranslated sequences, and are thus classical RNA polymerase II transcription units (9,22,68).The sea urchin genome contains four distinct histone gene familie...

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Section: Discussionmentioning

confidence: 76%

The Five Cleavage-Stage (CS) Histones of the Sea Urchin Are Encoded by a Maternally Expressed Family of Replacement Histone Genes: Functional Equivalence of the CS H1 and Frog H1M (B4) Proteins

Mandl

Brandt

Superti‐Furga

et al. 1997

Molecular and Cellular Biology

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“…S-P tetrapeptides which closely resemble those in wheat H2A are repeated several times in the N-terminal regions of sea urchin sperm histones Sp H 1 and Sp H2B (21,22). These S-P tetrapeptides are selectively phosphorylated during spermatogenesis, and again after fertilization, thus reducing DNA-binding during periods of nuclear activity (7,15,16). In mature sperm cells, S-P tetrapeptides are fully dephosphorylated to maximize binding of the N-terminal regions to linker DNA between nucleosomes, thus stabilizing the condensed sperm chromatin (8).…”

Section: Discussionmentioning

confidence: 99%

“…3). The Sp H2B N-terminal S-P tetrapeptides are selectively phosphorylated during spermatogenesis, become dephosphorylated late in spermiogenesis, and then are rephosphorylated immediately after fertilization (7,13,15,16). Although several seine residues representing potential phosphorylation sites are present in the N-terminal region of wheat H2B, phosphorylation of wheat and alfalfa H2B variants was not detected by the autoradiogram (Fig.…”

Section: P_mentioning

confidence: 95%

Phosphorylation of Plant H2A Histones

Green¹,

Gustavsen²,

Poccia³

1990

Plant Physiol.

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Phosphorylation of wheat (Triticum aestivum) and alfalfa (Medicago sativa) H2A histone variants was examined during early seedling growth. The C-terminal regions of wheat H2A variants contain multiple S-P tetrapeptides (senne-proline adjacent to a pair of basic amino acids) which resemble known phosphorylation sites in histones from other species. Phosphorylation of nucleosomal core histones was assessed by autoradiography of proteins labeled in vivo with 32pi and resolved by two-dimensional polyacrylamide gel electrophoresis, and phosphorylation sites were mapped by cleaving in vivo labeled H2A variants with Nbromosuccinimide. Essentially all phosphorylation of nucleosomal core histones in wheat and alfalfa seedlings occurred within the C-terminal peptides obtained from wheat and alfalfa H2A variants. A hypothesis accounting for the presence of large H2A and H2B histone variants in plants and phosphorylation of plant H2A C-terminal regions is proposed. The utility of S-P tetrapeptides for modulation of DNA-protein interactions is discussed.H2A and H2B histone variants from wheat contain long N-and C-terminal regions, rich in basic amino acids, hydroxyamino acids, proline and alanine (5,17,18). These regions resemble the DNA-binding 'head' and 'tail' regions of HI histones (1). Located periodically in the C-terminal regions of wheat H2A variants are two or three S-P tetrapeptides (serineproline adjacent to a pair of basic amino acids) (17, 18). Similar S-P tetrapeptides are known phosphorylation sites in the C-terminal regions of vertebrate HI histones (reviewed in Poccia [ 13]) and in the long N-terminal regions of sea urchin sperm HI and H2B histone variants, Sp HI and Sp H2B (7, 16).These observations prompted a study of nucleosomal core histone phosphorylation in early seedlings, during a period of rapid cell growth which follows a protracted period of nuclear quiescence. The results show that nearly all nucleosomal histone phosphorylation occurs within C-terminal peptides obtained from H2A histone variants, suggesting that S-P tetrapeptides are the primary sites ofphosphorylation, as they are in the sea urchin sperm variants Sp HI and Sp H2B. By analogy with Sp H1 and Sp H2B, we propose a hypothesis which accounts for the presence of large H2A and H2B histone variants in plants and C-terminal phosphorylation of the H2A variants. MATERIALS AND METHODSGermination, Seedling Growth, and Radiolabeling Seeds ofalfalfa (Medicago sativa) and hard red spring wheat (Triticum aestivum) were purchased from local grocery stores and germinated in Petri dishes on filter paper wetted with distilled water. After 48 h at 22°C, germinated seedlings (2 g, 2-4 mm in length) were transferred to fresh filter paper and wetted with 0.1 mCi/mL 32Pi (orthophosphate in carrier free aqueous solution; Amersham). Seedlings were incubated for an additional 24 h, after which endosperm or cotyledon tissues were removed. The seedlings were washed with cold water to remove residual 32Pi. Subsequent steps were at OC. Histone IsolationW...

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“…In midpachytene cells, the ubiquitinated H2A distributes to the entire nucleus and then in late pachytene cells concentrates again to the sex body (Baarends et al, 1999a). Such ubiquitination of histone H2A during pachytene may facilitate the substitution of somatic histones by testis specific isotypes that are synthesized in these cells (Poccia et al, 1987;Meistrich, 1989;Drabent et al, 1996). In addition, it is now well established that histone ubiquitination can regulate transcription of specific genes (Zhang, 2003).…”

Section: The E3mentioning

confidence: 99%

“…Ubiquitinated histone H3 and testes-specific H3 (TH3) were first identified in a study of rat spermatogenesis, with the highest level in elongated spermatids (Chen et al, 1998). Ubiquitination may be required for somatic histones replacement by testis specific histones during meiosis (Poccia et al, 1987;Meistrich, 1989;Drabent et al, 1996) and for the subsequent substitution of most histones by transition proteins, which are later replaced by protamines during spermiogenesis (Mills et al, 1977;Meistrich, 1989). This latter substitution of histones is critical for normal chromatin condensation in spermatids.…”

Section: Introductionmentioning

confidence: 99%

Regulated expression of the ubiquitin protein ligase, E3^Histone/LASU1/Mule/ARF‐BP1/HUWE1, during spermatogenesis

Liu

Miao

Xia

et al. 2007

Developmental Dynamics

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A ubiquitin protein ligase (E3), E3Histone /LASU1 (Mule/ARF-BP1/HUWE1), was recently identified that mediates ubiquitination of core histones, the Mcl-1 anti-apoptotic protein, and the p53 tumor suppressor protein. However, the expression of E3 Histone /LASU1 remains poorly studied. Because we identified E3 Histone /LASU1 from the testis, we explored its regulation during spermatogenesis. In the first wave of rat spermatogenesis, E3Histone /LASU1 mRNA and protein had peak expression at days 10 and 20, respectively, and decreased with age. Consistent with these findings, immunohistochemistry revealed that E3 Histone /LASU1 was highly expressed in nuclei from spermatogonia to mid-pachytene spermatocytes. There was no obvious staining in spermatids, when histones are ubiquitinated and degraded.

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Transitions in histone variants during sea urchin spermatogenesis

Cited by 65 publications

References 17 publications

The Five Cleavage-Stage (CS) Histones of the Sea Urchin Are Encoded by a Maternally Expressed Family of Replacement Histone Genes: Functional Equivalence of the CS H1 and Frog H1M (B4) Proteins

The Five Cleavage-Stage (CS) Histones of the Sea Urchin Are Encoded by a Maternally Expressed Family of Replacement Histone Genes: Functional Equivalence of the CS H1 and Frog H1M (B4) Proteins

Phosphorylation of Plant H2A Histones

Regulated expression of the ubiquitin protein ligase, E3^Histone/LASU1/Mule/ARF‐BP1/HUWE1, during spermatogenesis

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Transitions in histone variants during sea urchin spermatogenesis

Cited by 65 publications

References 17 publications

The Five Cleavage-Stage (CS) Histones of the Sea Urchin Are Encoded by a Maternally Expressed Family of Replacement Histone Genes: Functional Equivalence of the CS H1 and Frog H1M (B4) Proteins

The Five Cleavage-Stage (CS) Histones of the Sea Urchin Are Encoded by a Maternally Expressed Family of Replacement Histone Genes: Functional Equivalence of the CS H1 and Frog H1M (B4) Proteins

Phosphorylation of Plant H2A Histones

Regulated expression of the ubiquitin protein ligase, E3Histone/LASU1/Mule/ARF‐BP1/HUWE1, during spermatogenesis

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Regulated expression of the ubiquitin protein ligase, E3^Histone/LASU1/Mule/ARF‐BP1/HUWE1, during spermatogenesis