Gene function and expression level influence the insertion/fixation dynamics of distinct transposon families in mammalian introns

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

Background: Transposable elements (TEs) represent more than 45% of the human and mouse genomes. Both parasitic and mutualistic features have been shown to apply to the host-TE relationship but a comprehensive scenario of the forces driving TE fixation within mammalian genes is still missing. Results: We show that intronic multispecies conserved sequences (MCSs) have been affecting TE integration frequency over time. We verify that a selective economizing pressure has been acting on TEs to decrease their frequency in highly expressed genes. After correcting for GC content, MCS density and intron size, we identified TE-enriched and TE-depleted gene categories. In addition to developmental regulators and transcription factors, TE-depleted regions encompass loci that might require subtle regulation of transcript levels or precise activation timing, such as growth factors, cytokines, hormones, and genes involved in the immune response. The latter, despite having reduced frequencies of most TE types, are significantly enriched in mammalian-wide interspersed repeats (MIRs). Analysis of orthologous genes indicated that MIR over-representation also occurs in dog and opossum immune response genes, suggesting, given the partially independent origin of MIR sequences in eutheria and metatheria, the evolutionary conservation of a specific function for MIRs located in these loci. Consistently, the core MIR sequence is over-represented in defense response genes compared to the background intronic frequency. Conclusion: Our data indicate thatgene function, expression level, and sequence conservation influence TE insertion/fixation in mammalian introns. Moreover, we provide the first report showing that a specific TE family is evolutionarily associated with a gene function category.

Original languageEnglish
Article numberR120
JournalGenome Biology
Volume7
Issue number12
DOIs
Publication statusPublished - Dec 20 2006

Fingerprint

DNA Transposable Elements
transposons
Introns
fixation
introns
Gene Expression
gene
genes
Genes
immune response
conserved sequences
Conserved Sequence
family
Opossums
Marsupialia
hormone
loci
Base Composition
opossums
genome

ASJC Scopus subject areas

  • Genetics
  • Cell Biology
  • Ecology, Evolution, Behavior and Systematics

Cite this

@article{c83e7eabfdc848b995cc291ad87361cd,
title = "Gene function and expression level influence the insertion/fixation dynamics of distinct transposon families in mammalian introns",
abstract = "Background: Transposable elements (TEs) represent more than 45{\%} of the human and mouse genomes. Both parasitic and mutualistic features have been shown to apply to the host-TE relationship but a comprehensive scenario of the forces driving TE fixation within mammalian genes is still missing. Results: We show that intronic multispecies conserved sequences (MCSs) have been affecting TE integration frequency over time. We verify that a selective economizing pressure has been acting on TEs to decrease their frequency in highly expressed genes. After correcting for GC content, MCS density and intron size, we identified TE-enriched and TE-depleted gene categories. In addition to developmental regulators and transcription factors, TE-depleted regions encompass loci that might require subtle regulation of transcript levels or precise activation timing, such as growth factors, cytokines, hormones, and genes involved in the immune response. The latter, despite having reduced frequencies of most TE types, are significantly enriched in mammalian-wide interspersed repeats (MIRs). Analysis of orthologous genes indicated that MIR over-representation also occurs in dog and opossum immune response genes, suggesting, given the partially independent origin of MIR sequences in eutheria and metatheria, the evolutionary conservation of a specific function for MIRs located in these loci. Consistently, the core MIR sequence is over-represented in defense response genes compared to the background intronic frequency. Conclusion: Our data indicate thatgene function, expression level, and sequence conservation influence TE insertion/fixation in mammalian introns. Moreover, we provide the first report showing that a specific TE family is evolutionarily associated with a gene function category.",
author = "Manuela Sironi and Giorgia Menozzi and Comi, {Giacomo P.} and Matteo Cereda and Rachele Cagliani and Nereo Bresolin and Uberto Pozzoli",
year = "2006",
month = "12",
day = "20",
doi = "10.1186/gb-2006-7-12-r120",
language = "English",
volume = "7",
journal = "Genome Biology",
issn = "1474-760X",
publisher = "BioMed Central Ltd.",
number = "12",

}

TY - JOUR

T1 - Gene function and expression level influence the insertion/fixation dynamics of distinct transposon families in mammalian introns

AU - Sironi, Manuela

AU - Menozzi, Giorgia

AU - Comi, Giacomo P.

AU - Cereda, Matteo

AU - Cagliani, Rachele

AU - Bresolin, Nereo

AU - Pozzoli, Uberto

PY - 2006/12/20

Y1 - 2006/12/20

N2 - Background: Transposable elements (TEs) represent more than 45% of the human and mouse genomes. Both parasitic and mutualistic features have been shown to apply to the host-TE relationship but a comprehensive scenario of the forces driving TE fixation within mammalian genes is still missing. Results: We show that intronic multispecies conserved sequences (MCSs) have been affecting TE integration frequency over time. We verify that a selective economizing pressure has been acting on TEs to decrease their frequency in highly expressed genes. After correcting for GC content, MCS density and intron size, we identified TE-enriched and TE-depleted gene categories. In addition to developmental regulators and transcription factors, TE-depleted regions encompass loci that might require subtle regulation of transcript levels or precise activation timing, such as growth factors, cytokines, hormones, and genes involved in the immune response. The latter, despite having reduced frequencies of most TE types, are significantly enriched in mammalian-wide interspersed repeats (MIRs). Analysis of orthologous genes indicated that MIR over-representation also occurs in dog and opossum immune response genes, suggesting, given the partially independent origin of MIR sequences in eutheria and metatheria, the evolutionary conservation of a specific function for MIRs located in these loci. Consistently, the core MIR sequence is over-represented in defense response genes compared to the background intronic frequency. Conclusion: Our data indicate thatgene function, expression level, and sequence conservation influence TE insertion/fixation in mammalian introns. Moreover, we provide the first report showing that a specific TE family is evolutionarily associated with a gene function category.

AB - Background: Transposable elements (TEs) represent more than 45% of the human and mouse genomes. Both parasitic and mutualistic features have been shown to apply to the host-TE relationship but a comprehensive scenario of the forces driving TE fixation within mammalian genes is still missing. Results: We show that intronic multispecies conserved sequences (MCSs) have been affecting TE integration frequency over time. We verify that a selective economizing pressure has been acting on TEs to decrease their frequency in highly expressed genes. After correcting for GC content, MCS density and intron size, we identified TE-enriched and TE-depleted gene categories. In addition to developmental regulators and transcription factors, TE-depleted regions encompass loci that might require subtle regulation of transcript levels or precise activation timing, such as growth factors, cytokines, hormones, and genes involved in the immune response. The latter, despite having reduced frequencies of most TE types, are significantly enriched in mammalian-wide interspersed repeats (MIRs). Analysis of orthologous genes indicated that MIR over-representation also occurs in dog and opossum immune response genes, suggesting, given the partially independent origin of MIR sequences in eutheria and metatheria, the evolutionary conservation of a specific function for MIRs located in these loci. Consistently, the core MIR sequence is over-represented in defense response genes compared to the background intronic frequency. Conclusion: Our data indicate thatgene function, expression level, and sequence conservation influence TE insertion/fixation in mammalian introns. Moreover, we provide the first report showing that a specific TE family is evolutionarily associated with a gene function category.

UR - http://www.scopus.com/inward/record.url?scp=34249752804&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=34249752804&partnerID=8YFLogxK

U2 - 10.1186/gb-2006-7-12-r120

DO - 10.1186/gb-2006-7-12-r120

M3 - Article

VL - 7

JO - Genome Biology

JF - Genome Biology

SN - 1474-760X

IS - 12

M1 - R120

ER -