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Early vertebrate origin of CTCFL, a CTCF paralog, revealed by proximity-guided shark genome scaffolding.

ABSTRACT: The nuclear protein CCCTC-binding factor (CTCF) contributes as an insulator to chromatin organization in diverse animals. The gene encoding this protein has a paralog which was first identified to be expressed exclusively in the testis in mammals and designated as CTCFL (also called BORIS). CTCFL orthologs were reported only among amniotes, and thus CTCFL was once thought to have arisen in the amniote lineage. In this study, we identified elasmobranch CTCFL orthologs, and investigated its origin with the aid of a shark genome assembly improved by proximity-guided scaffolding. Our analysis employing evolutionary interpretation of syntenic gene location suggested an earlier timing of the gene duplication between CTCF and CTCFL than previously thought, that is, around the common ancestor of extant vertebrates. Also, our transcriptomic sequencing revealed a biased expression of the catshark CTCFL in the testis, suggesting the origin of the tissue-specific localization in mammals more than 400 million years ago. To understand the historical process of the functional consolidation of the long-standing chromatin regulator CTCF, its additional paralogs remaining in some of the descendant lineages for spatially restricted transcript distribution should be taken into consideration.

SUBMITTER: Kadota M

PROVIDER: S-EPMC7471279 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Early vertebrate origin of CTCFL, a CTCF paralog, revealed by proximity-guided shark genome scaffolding.

Kadota Mitsutaka M Yamaguchi Kazuaki K Hara Yuichiro Y Kuraku Shigehiro S

Scientific reports 20200903 1

The nuclear protein CCCTC-binding factor (CTCF) contributes as an insulator to chromatin organization in diverse animals. The gene encoding this protein has a paralog which was first identified to be expressed exclusively in the testis in mammals and designated as CTCFL (also called BORIS). CTCFL orthologs were reported only among amniotes, and thus CTCFL was once thought to have arisen in the amniote lineage. In this study, we identified elasmobranch CTCFL orthologs, and investigated its origin ...[more]

PMID: 32884037

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Project description:BACKGROUND: CTCF is a highly conserved and essential zinc finger protein expressed in virtually all cell types. In conjunction with cohesin, it organizes chromatin into loops, thereby regulating gene expression and epigenetic events. The function of CTCFL or BORIS, the testis-specific paralog of CTCF, is less clear. RESULTS: Using immunohistochemistry on testis sections and fluorescence-based microscopy on intact live seminiferous tubules, we show that CTCFL is only transiently present during spermatogenesis, prior to the onset of meiosis, when the protein co-localizes in nuclei with ubiquitously expressed CTCF. CTCFL distribution overlaps completely with that of Stra8, a retinoic acid-inducible protein essential for the propagation of meiosis. We find that absence of CTCFL in mice causes sub-fertility because of a partially penetrant testicular atrophy. CTCFL deficiency affects the expression of a number of testis-specific genes, including Gal3st1 and Prss50. Combined, these data indicate that CTCFL has a unique role in spermatogenesis. Genome-wide RNA expression studies in ES cells expressing a V5- and GFP-tagged form of CTCFL show that genes that are downregulated in CTCFL-deficient testis are upregulated in ES cells. These data indicate that CTCFL is a male germ cell gene regulator. Furthermore, genome-wide DNA-binding analysis shows that CTCFL binds a consensus sequence that is very similar to that of CTCF. However, only ~3,700 out of the ~5,700 CTCFL- and ~31,000 CTCF-binding sites overlap. CTCFL binds promoters with loosely assembled nucleosomes, whereas CTCF favors consensus sites surrounded by phased nucleosomes. Finally, an ES cell-based rescue assay shows that CTCFL is functionally different from CTCF. CONCLUSIONS: Our data suggest that nucleosome composition specifies the genome-wide binding of CTCFL and CTCF. We propose that the transient expression of CTCFL in spermatogonia and preleptotene spermatocytes serves to occupy a subset of promoters and maintain the expression of male germ cell genes.

Project description:BackgroundVasopressin and oxytocin are mammalian neurohypophysial hormones with distinct functions. Vasopressin is involved mainly in osmoregulation and oxytocin is involved primarily in parturition and lactation. Jawed vertebrates contain at least one homolog each of vasopressin and oxytocin, whereas only a vasopressin-family hormone, vasotocin, has been identified in jawless vertebrates. The genes encoding vasopressin and oxytocin are closely linked tail-to-tail in eutherian mammals whereas their homologs in chicken, Xenopus and coelacanth (vasotocin and mesotocin) are linked tail-to-head. In contrast, their pufferfish homologs, vasotocin and isotocin, are located on the same strand of DNA with isotocin located upstream of vasotocin and separated by five genes. These differences in the arrangement of the two genes in different bony vertebrate lineages raise questions about their origin and ancestral arrangement. To trace the origin of these genes, we have sequenced BAC clones from the neurohypophysial gene loci in a cartilaginous fish, the elephant shark (Callorhinchus milii), and in a jawless vertebrate, the Japanese lamprey (Lethenteron japonicum). We have also analyzed the neurohypophysial hormone gene locus in an invertebrate chordate, the amphioxus (Branchiostoma floridae).ResultsThe elephant shark neurohypophysial hormone genes encode vasotocin and oxytocin, and are linked tail-to-head like their homologs in coelacanth and non-eutherian tetrapods. Besides the hypothalamus, the two genes are also expressed in the ovary. In addition, the vasotocin gene is expressed in the kidney, rectal gland and intestine. These expression profiles indicate a paracrine role for the two hormones. The lamprey locus contains a single neurohypophysial hormone gene, the vasotocin. The synteny of genes in the lamprey locus is conserved in elephant shark, coelacanth and tetrapods but disrupted in teleost fishes. The amphioxus locus encodes a single neurohypophysial hormone, designated as [Ile4]vasotocin.ConclusionThe vasopressin- and oxytocin-family of neurohypophysial hormones evolved in a common ancestor of jawed vertebrates through tandem duplication of the ancestral vasotocin gene. The duplicated genes were linked tail-to-head like their homologs in elephant shark, coelacanth and non-eutherian tetrapods. In contrast to the conserved linkage of the neurohypophysial genes in these vertebrates, the neurohypophysial hormone gene locus has experienced extensive rearrangements in the teleost lineage.

Dataset Information

Early vertebrate origin of CTCFL, a CTCF paralog, revealed by proximity-guided shark genome scaffolding.

Publications

Early vertebrate origin of CTCFL, a CTCF paralog, revealed by proximity-guided shark genome scaffolding.

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