Overlapping genes in the human and mouse genomes

Department of Computer Science, Virginia Tech, Blacksburg, USA.
BMC Genomics (Impact Factor: 3.99). 02/2008; 9(1):169. DOI: 10.1186/1471-2164-9-169
Source: PubMed


Increasing evidence suggests that overlapping genes are much more common in eukaryotic genomes than previously thought. In this study we identified and characterized the overlapping genes in a set of 13,484 pairs of human-mouse orthologous genes.
About 10% of the genes under study are overlapping genes, the majority of which are different-strand overlaps. The majority of the same-strand overlaps are embedded forms, whereas most different-strand overlaps are not embedded and in the convergent transcription orientation. Most of the same-strand overlapping gene pairs show at least a tenfold difference in length, much larger than the length difference between non-overlapping neighboring gene pairs. The length difference between the two different-strand overlapping genes is less dramatic. Over 27% of the different-strand-overlap relationships are shared between human and mouse, compared to only approximately 8% conservation for same-strand-overlap relationships. More than 96% of the same-strand and different-strand overlaps that are not shared between human and mouse have both genes located on the same chromosomes in the species that does not show the overlap. We examined the causes of transition between the overlapping and non-overlapping states in the two species and found that 3' UTR change plays an important role in the transition.
Our study contributes to the understanding of the evolutionary transition between overlapping genes and non-overlapping genes and demonstrates the high rates of evolutionary changes in the un-translated regions.

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    • "A study in human cells correlated the expression of the RevErb messenger to the regulation of erbAa2 mRNA splicing (Hastings et al., 1997; Salato et al., 2010) via an mRNA-mRNA interaction. In this case, at least 600 additional overlapping coding genes have been identified (Sanna et al., 2008). We wished to address the question of the fate of 3 0 -overlapping messengers in the model organism Saccharomyces cerevisiae , where hundreds of 3 0 -overlapping mRNA result from convergent gene transcription and can theoretically form mRNA duplexes (Pelechano et al., 2013; Wilkening et al., 2013). "
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    ABSTRACT: Transcriptome analyses have revealed that convergent gene transcription can produce many 3'-overlapping mRNAs in diverse organisms. Few studies have examined the fate of 3'-complementary mRNAs in double-stranded RNA-dependent nuclear phenomena, and nothing is known about the cytoplasmic destiny of 3'-overlapping messengers or their impact on gene expression. Here, we demonstrate that the complementary tails of 3'-overlapping mRNAs can interact in the cytoplasm and promote post-transcriptional regulatory events including no-go decay (NGD) in Saccharomyces cerevisiae. Genome-wide experiments confirm that these messenger-interacting mRNAs (mimRNAs) form RNA duplexes in wild-type cells and thus have potential roles in modulating the mRNA levels of their convergent gene pattern under different growth conditions. We show that the post-transcriptional fate of hundreds of mimRNAs is controlled by Xrn1, revealing the extent to which this conserved 5'-3' cytoplasmic exoribonuclease plays an unexpected but key role in the post-transcriptional control of convergent gene expression.
    Full-text · Article · Sep 2015 · Cell Reports
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    • "Eukaryotic genomes harbor an abundance of overlapping genes (Sanna et al. 2008; Soldà et al. 2008). In most cases, overlapping genes involve a noncoding gene feature (intron or untranslated region) from one gene and part of the CDS from another gene, whereas only a small fraction of overlapping gene pairs involve two CDSs (“CDS-CDS overlap”). "
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    ABSTRACT: Orphan genes are defined as genes which lack detectable similarity to genes in other species and therefore no clear signals of common descant (i.e. homology) can be inferred. Orphans are an enigmatic portion of the genome since their origin and function are mostly unknown and they typically make up 10 to 30% of all genes in a genome. Several case studies demonstrated that orphans can contribute to lineage-specific adaptation. Here, we study orphan genes by comparing thirty arthropod genomes, focusing in particular on seven recently sequenced ant genomes. This setup allows analyzing a major metazoan taxon and a comparison between social Hymenoptera (ants, bees) and non-social Diptera (flies, mosquitoes). First, we find that recently split lineages undergo accelerated genomic reorganization, including the rapid gain of many orphan genes. Second, between the two insect orders Hymenoptera and Diptera, orphan genes are more abundant and emerge more rapidly in Hymenoptera, in particular in leaf-cutter ants With respect to intra-genomic localization, we find that ant orphan genes show little clustering which suggests that orphan genes in ants are scattered uniformly over the genome and between non-orphan genes. Finally, our results indicate that the genetic mechanisms creating orphan genes - such as gene duplication, frame shift fixation, creation of overlapping genes, horizontal gene transfer and exaptation of transposable elements - act at different rates in insects, primates, and plants. In Formicidae, the majority of orphan genes has their origin in intergenic regions, pointing to a high rate of de novo gene formation or generalized gene loss, and support a recently proposed dynamic model of frequent gene birth and death.
    Full-text · Article · Jan 2013 · Genome Biology and Evolution
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    • "That may be a reason why gene-overlap events go on and off during the evolutionary course, such as the overlap of MINK1 and CHRNE [44]. Importantly, most overlapping genes are new or lineage-specific [9] [10] [11], and nested ones are further reported as tissue-specific genes [37]. These all address the need and significance of investigating overlapping genes. "
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    ABSTRACT: Overlapping genes are pairs of adjacent genes whose genomic regions partially overlap. They are notable by their potential intricate regulation, such as cis-regulation of nested gene-promoter configurations, and post-transcriptional regulation of natural antisense transcripts. The originations and consequent detailed regulation remain obscure. Herein, we propose a unified framework comprising biological classification rules followed by extensive analyses, namely, exon-sharing analysis, a human-mouse conservation study, and transcriptome analysis of hundreds of microarrays and transcriptome sequencing data (mRNA-Seq). We demonstrate that the tail-to-tail architecture would result from sharing functional elements in 3'-untranslated regions (3'-UTRs) of pre-existing genes. Dissimilarly, we illustrate that the other gene overlaps would originate from a new gene arising in a pre-existing gene locus. Interestingly, these types of coupled overlapping genes may influence each other synergistically or competitively during transcription, depending on the promoter configurations. This framework discloses distinctive characteristics of overlapping genes to be a foundation for a further comprehensive understanding of them.
    Full-text · Article · Jul 2012 · Genomics
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