Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene

Autores
Santangelo, A.M.; De Souza, F.S.J.; Franchini, L.F.; Bumaschny, V.F.; Low, M.J.; Rubinstein, M.
Año de publicación
2007
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The proopiomelanocortin gene (POMC) is expressed in the pituitary gland and the ventral hypothalamus of all jawed vertebrates, producing several bioactive peptides that function as peripheral hormones or central neuropeptides, respectively. We have recently determined that mouse and human POMC expression in the hypothalamus is conferred by the action of two 5′ distal and unrelated enhancers, nPE1 and nPE2. To investigate the evolutionary origin of the neuronal enhancer nPE2, we searched available vertebrate genome databases and determined that nPE2 is a highly conserved element in placentals, marsupials, and monotremes, whereas it is absent in nonmammalian vertebrates. Following an in silico paleogenomic strategy based on genome-wide searches for paralog sequences, we discovered that opossum and wallaby nPE2 sequences are highly similar to members of the superfamily of CORE-short interspersed nucleotide element (SINE) retroposons, in particular to MAR1 retroposons that are widely present in marsupial genomes. Thus, the neuronal enhancer nPE2 originated from the exaptation of a CORE-SINE retroposon in the lineage leading to mammals and remained under purifying selection in all mammalian orders for the last 170 million years. Expression studies performed in transgenic mice showed that two nonadjacent nPE2 subregions are essential to drive reporter gene expression into POMC hypothalamic neurons, providing the first functional example of an exapted enhancer derived from an ancient CORE-SINE retroposon. In addition, we found that this CORE-SINE family of retroposons is likely to still be active in American and Australian marsupial genomes and that several highly conserved exonic, intronic and intergenic sequences in the human genome originated from the exaptation of CORESINE retroposons. Together, our results provide clear evidence of the functional novelties that transposed elements contributed to their host genomes throughout evolution. © 2007 Santangelo et al.
Fil:Santangelo, A.M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fil:Rubinstein, M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fuente
PLoS Genet. 2007;3(10):1813-1826
Materia
proopiomelanocortin
animal experiment
animal tissue
article
brain nerve cell
computer model
embryo
enhancer region
female
gene expression
genetic conservation
genetic database
genetic line
genome analysis
hypothalamus
intron
mammalian genetics
marsupial
molecular evolution
monotremate
mouse
multigene family
newborn
nonhuman
physical anthropology
placenta
reporter gene
retroposon
short interspersed repeat
transposon
vertebrate
Animals
Base Sequence
Computational Biology
Consensus Sequence
Conserved Sequence
Embryonic Development
Enhancer Elements (Genetics)
Evolution, Molecular
Gene Expression Regulation, Developmental
Genomics
Mammals
Mice
Mice, Transgenic
Molecular Sequence Data
Neurons
Opossums
Paleontology
Pro-Opiomelanocortin
Sequence Alignment
Sequence Analysis, DNA
Sequence Deletion
Short Interspersed Nucleotide Elements
Didelphidae
Eutheria
Gnathostomata (vertebrate)
Mammalia
Metatheria
Monotremata
Mus musculus
Vertebrata
Nivel de accesibilidad
acceso abierto
Condiciones de uso
http://creativecommons.org/licenses/by/2.5/ar
Repositorio
Biblioteca Digital (UBA-FCEN)
Institución
Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
OAI Identificador
paperaa:paper_15537390_v3_n10_p1813_Santangelo

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oai_identifier_str paperaa:paper_15537390_v3_n10_p1813_Santangelo
network_acronym_str BDUBAFCEN
repository_id_str 1896
network_name_str Biblioteca Digital (UBA-FCEN)
spelling Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin geneSantangelo, A.M.De Souza, F.S.J.Franchini, L.F.Bumaschny, V.F.Low, M.J.Rubinstein, M.proopiomelanocortinanimal experimentanimal tissuearticlebrain nerve cellcomputer modelembryoenhancer regionfemalegene expressiongenetic conservationgenetic databasegenetic linegenome analysishypothalamusintronmammalian geneticsmarsupialmolecular evolutionmonotrematemousemultigene familynewbornnonhumanphysical anthropologyplacentareporter generetroposonshort interspersed repeattransposonvertebrateAnimalsBase SequenceComputational BiologyConsensus SequenceConserved SequenceEmbryonic DevelopmentEnhancer Elements (Genetics)Evolution, MolecularGene Expression Regulation, DevelopmentalGenomicsMammalsMiceMice, TransgenicMolecular Sequence DataNeuronsOpossumsPaleontologyPro-OpiomelanocortinSequence AlignmentSequence Analysis, DNASequence DeletionShort Interspersed Nucleotide ElementsDidelphidaeEutheriaGnathostomata (vertebrate)MammaliaMetatheriaMonotremataMus musculusVertebrataThe proopiomelanocortin gene (POMC) is expressed in the pituitary gland and the ventral hypothalamus of all jawed vertebrates, producing several bioactive peptides that function as peripheral hormones or central neuropeptides, respectively. We have recently determined that mouse and human POMC expression in the hypothalamus is conferred by the action of two 5′ distal and unrelated enhancers, nPE1 and nPE2. To investigate the evolutionary origin of the neuronal enhancer nPE2, we searched available vertebrate genome databases and determined that nPE2 is a highly conserved element in placentals, marsupials, and monotremes, whereas it is absent in nonmammalian vertebrates. Following an in silico paleogenomic strategy based on genome-wide searches for paralog sequences, we discovered that opossum and wallaby nPE2 sequences are highly similar to members of the superfamily of CORE-short interspersed nucleotide element (SINE) retroposons, in particular to MAR1 retroposons that are widely present in marsupial genomes. Thus, the neuronal enhancer nPE2 originated from the exaptation of a CORE-SINE retroposon in the lineage leading to mammals and remained under purifying selection in all mammalian orders for the last 170 million years. Expression studies performed in transgenic mice showed that two nonadjacent nPE2 subregions are essential to drive reporter gene expression into POMC hypothalamic neurons, providing the first functional example of an exapted enhancer derived from an ancient CORE-SINE retroposon. In addition, we found that this CORE-SINE family of retroposons is likely to still be active in American and Australian marsupial genomes and that several highly conserved exonic, intronic and intergenic sequences in the human genome originated from the exaptation of CORESINE retroposons. Together, our results provide clear evidence of the functional novelties that transposed elements contributed to their host genomes throughout evolution. © 2007 Santangelo et al.Fil:Santangelo, A.M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.Fil:Rubinstein, M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.2007info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12110/paper_15537390_v3_n10_p1813_SantangeloPLoS Genet. 2007;3(10):1813-1826reponame:Biblioteca Digital (UBA-FCEN)instname:Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturalesinstacron:UBA-FCENenginfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by/2.5/ar2025-09-29T13:43:03Zpaperaa:paper_15537390_v3_n10_p1813_SantangeloInstitucionalhttps://digital.bl.fcen.uba.ar/Universidad públicaNo correspondehttps://digital.bl.fcen.uba.ar/cgi-bin/oaiserver.cgiana@bl.fcen.uba.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:18962025-09-29 13:43:04.621Biblioteca Digital (UBA-FCEN) - Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturalesfalse
dc.title.none.fl_str_mv Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene
title Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene
spellingShingle Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene
Santangelo, A.M.
proopiomelanocortin
animal experiment
animal tissue
article
brain nerve cell
computer model
embryo
enhancer region
female
gene expression
genetic conservation
genetic database
genetic line
genome analysis
hypothalamus
intron
mammalian genetics
marsupial
molecular evolution
monotremate
mouse
multigene family
newborn
nonhuman
physical anthropology
placenta
reporter gene
retroposon
short interspersed repeat
transposon
vertebrate
Animals
Base Sequence
Computational Biology
Consensus Sequence
Conserved Sequence
Embryonic Development
Enhancer Elements (Genetics)
Evolution, Molecular
Gene Expression Regulation, Developmental
Genomics
Mammals
Mice
Mice, Transgenic
Molecular Sequence Data
Neurons
Opossums
Paleontology
Pro-Opiomelanocortin
Sequence Alignment
Sequence Analysis, DNA
Sequence Deletion
Short Interspersed Nucleotide Elements
Didelphidae
Eutheria
Gnathostomata (vertebrate)
Mammalia
Metatheria
Monotremata
Mus musculus
Vertebrata
title_short Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene
title_full Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene
title_fullStr Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene
title_full_unstemmed Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene
title_sort Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene
dc.creator.none.fl_str_mv Santangelo, A.M.
De Souza, F.S.J.
Franchini, L.F.
Bumaschny, V.F.
Low, M.J.
Rubinstein, M.
author Santangelo, A.M.
author_facet Santangelo, A.M.
De Souza, F.S.J.
Franchini, L.F.
Bumaschny, V.F.
Low, M.J.
Rubinstein, M.
author_role author
author2 De Souza, F.S.J.
Franchini, L.F.
Bumaschny, V.F.
Low, M.J.
Rubinstein, M.
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv proopiomelanocortin
animal experiment
animal tissue
article
brain nerve cell
computer model
embryo
enhancer region
female
gene expression
genetic conservation
genetic database
genetic line
genome analysis
hypothalamus
intron
mammalian genetics
marsupial
molecular evolution
monotremate
mouse
multigene family
newborn
nonhuman
physical anthropology
placenta
reporter gene
retroposon
short interspersed repeat
transposon
vertebrate
Animals
Base Sequence
Computational Biology
Consensus Sequence
Conserved Sequence
Embryonic Development
Enhancer Elements (Genetics)
Evolution, Molecular
Gene Expression Regulation, Developmental
Genomics
Mammals
Mice
Mice, Transgenic
Molecular Sequence Data
Neurons
Opossums
Paleontology
Pro-Opiomelanocortin
Sequence Alignment
Sequence Analysis, DNA
Sequence Deletion
Short Interspersed Nucleotide Elements
Didelphidae
Eutheria
Gnathostomata (vertebrate)
Mammalia
Metatheria
Monotremata
Mus musculus
Vertebrata
topic proopiomelanocortin
animal experiment
animal tissue
article
brain nerve cell
computer model
embryo
enhancer region
female
gene expression
genetic conservation
genetic database
genetic line
genome analysis
hypothalamus
intron
mammalian genetics
marsupial
molecular evolution
monotremate
mouse
multigene family
newborn
nonhuman
physical anthropology
placenta
reporter gene
retroposon
short interspersed repeat
transposon
vertebrate
Animals
Base Sequence
Computational Biology
Consensus Sequence
Conserved Sequence
Embryonic Development
Enhancer Elements (Genetics)
Evolution, Molecular
Gene Expression Regulation, Developmental
Genomics
Mammals
Mice
Mice, Transgenic
Molecular Sequence Data
Neurons
Opossums
Paleontology
Pro-Opiomelanocortin
Sequence Alignment
Sequence Analysis, DNA
Sequence Deletion
Short Interspersed Nucleotide Elements
Didelphidae
Eutheria
Gnathostomata (vertebrate)
Mammalia
Metatheria
Monotremata
Mus musculus
Vertebrata
dc.description.none.fl_txt_mv The proopiomelanocortin gene (POMC) is expressed in the pituitary gland and the ventral hypothalamus of all jawed vertebrates, producing several bioactive peptides that function as peripheral hormones or central neuropeptides, respectively. We have recently determined that mouse and human POMC expression in the hypothalamus is conferred by the action of two 5′ distal and unrelated enhancers, nPE1 and nPE2. To investigate the evolutionary origin of the neuronal enhancer nPE2, we searched available vertebrate genome databases and determined that nPE2 is a highly conserved element in placentals, marsupials, and monotremes, whereas it is absent in nonmammalian vertebrates. Following an in silico paleogenomic strategy based on genome-wide searches for paralog sequences, we discovered that opossum and wallaby nPE2 sequences are highly similar to members of the superfamily of CORE-short interspersed nucleotide element (SINE) retroposons, in particular to MAR1 retroposons that are widely present in marsupial genomes. Thus, the neuronal enhancer nPE2 originated from the exaptation of a CORE-SINE retroposon in the lineage leading to mammals and remained under purifying selection in all mammalian orders for the last 170 million years. Expression studies performed in transgenic mice showed that two nonadjacent nPE2 subregions are essential to drive reporter gene expression into POMC hypothalamic neurons, providing the first functional example of an exapted enhancer derived from an ancient CORE-SINE retroposon. In addition, we found that this CORE-SINE family of retroposons is likely to still be active in American and Australian marsupial genomes and that several highly conserved exonic, intronic and intergenic sequences in the human genome originated from the exaptation of CORESINE retroposons. Together, our results provide clear evidence of the functional novelties that transposed elements contributed to their host genomes throughout evolution. © 2007 Santangelo et al.
Fil:Santangelo, A.M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fil:Rubinstein, M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
description The proopiomelanocortin gene (POMC) is expressed in the pituitary gland and the ventral hypothalamus of all jawed vertebrates, producing several bioactive peptides that function as peripheral hormones or central neuropeptides, respectively. We have recently determined that mouse and human POMC expression in the hypothalamus is conferred by the action of two 5′ distal and unrelated enhancers, nPE1 and nPE2. To investigate the evolutionary origin of the neuronal enhancer nPE2, we searched available vertebrate genome databases and determined that nPE2 is a highly conserved element in placentals, marsupials, and monotremes, whereas it is absent in nonmammalian vertebrates. Following an in silico paleogenomic strategy based on genome-wide searches for paralog sequences, we discovered that opossum and wallaby nPE2 sequences are highly similar to members of the superfamily of CORE-short interspersed nucleotide element (SINE) retroposons, in particular to MAR1 retroposons that are widely present in marsupial genomes. Thus, the neuronal enhancer nPE2 originated from the exaptation of a CORE-SINE retroposon in the lineage leading to mammals and remained under purifying selection in all mammalian orders for the last 170 million years. Expression studies performed in transgenic mice showed that two nonadjacent nPE2 subregions are essential to drive reporter gene expression into POMC hypothalamic neurons, providing the first functional example of an exapted enhancer derived from an ancient CORE-SINE retroposon. In addition, we found that this CORE-SINE family of retroposons is likely to still be active in American and Australian marsupial genomes and that several highly conserved exonic, intronic and intergenic sequences in the human genome originated from the exaptation of CORESINE retroposons. Together, our results provide clear evidence of the functional novelties that transposed elements contributed to their host genomes throughout evolution. © 2007 Santangelo et al.
publishDate 2007
dc.date.none.fl_str_mv 2007
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12110/paper_15537390_v3_n10_p1813_Santangelo
url http://hdl.handle.net/20.500.12110/paper_15537390_v3_n10_p1813_Santangelo
dc.language.none.fl_str_mv eng
language eng
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
http://creativecommons.org/licenses/by/2.5/ar
eu_rights_str_mv openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/2.5/ar
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv PLoS Genet. 2007;3(10):1813-1826
reponame:Biblioteca Digital (UBA-FCEN)
instname:Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
instacron:UBA-FCEN
reponame_str Biblioteca Digital (UBA-FCEN)
collection Biblioteca Digital (UBA-FCEN)
instname_str Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
instacron_str UBA-FCEN
institution UBA-FCEN
repository.name.fl_str_mv Biblioteca Digital (UBA-FCEN) - Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
repository.mail.fl_str_mv ana@bl.fcen.uba.ar
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