Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons

Autores
Franchini, L.F.; López-Leal, R.; Nasif, S.; Beati, P.; Gelman, D.M.; Low, M.J.; De Souza, F.J.S.; Rubinstein, M.
Año de publicación
2011
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The proopiomelanocortin gene (POMC) is expressed in a group of neurons present in the arcuate nucleus of the hypothalamus. Neuron-specific POMC expression in mammals is conveyed by two distal enhancers, named nPE1 and nPE2. Previous transgenic mouse studies showed that nPE1 and nPE2 independently drive reporter gene expression to POMC neurons. Here, we investigated the evolutionary mechanisms that shaped not one but two neuron- specific POMC enhancers and tested whether nPE1 and nPE2 drive identical or complementary spatiotemporal expression patterns. Sequence comparison among representative genomes of most vertebrate classes and mammalian orders showed that nPE1 is a placental novelty. Using in silico paleogenomics we found that nPE1 originated from the exaptation of a mammalian- apparent LTR retrotransposon sometime between the metatherian/ eutherian split (147 Mya) and the placental mammal radiation (≈90 Mya). Thus, the evolutionary origin of nPE1 differs, in kind and time, from that previously demonstrated for nPE2, which was exapted from a CORE-short interspersed nucleotide element (SINE) retroposon before the origin of prototherians, 166 Mya. Transgenic mice expressing the fluorescent markers tomato and EGFP driven by nPE1 or nPE2, respectively, demonstrated coexpression of both reporter genes along the entire arcuate nucleus. The onset of reporter gene expression guided by nPE1 and nPE2 was also identical and coincidental with the onset of Pomc expression in the presumptive mouse diencephalon. Thus, the independent exaptation of two unrelated retroposons into functional analogs regulating neuronal POMC expression constitutes an authentic example of convergent molecular evolution of cell-specific enhancers.
Fil:Gelman, D.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
Proc. Natl. Acad. Sci. U. S. A. 2011;108(37):15270-15275
Materia
Obesity
Retroposition
Retrotransposition
Satiety
Shadow enhancer
enhanced green fluorescent protein
proopiomelanocortin
animal cell
animal experiment
arcuate nucleus
article
convergent evolution
diencephalon
evolutionary adaptation
fluorescence analysis
gene
gene expression
gene sequence
human
human cell
mammal
molecular evolution
mouse
nerve cell
nonhuman
nPE1 gene
nPE2 gene
placenta
placental mammals
priority journal
reporter gene
retroposon
tomato
transgenic mouse
vertebrate
Animals
Base Sequence
Enhancer Elements, Genetic
Evolution, Molecular
Female
Gene Expression Regulation, Developmental
Genes, Reporter
Humans
Mammals
Mice
Mice, Transgenic
Molecular Sequence Data
Neurons
Phylogeny
Placenta
Pregnancy
Pro-Opiomelanocortin
Retroelements
Time Factors
Eutheria
Lycopersicon esculentum
Mammalia
Mus musculus
Mya
Prototheria
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_00278424_v108_n37_p15270_Franchini

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oai_identifier_str paperaa:paper_00278424_v108_n37_p15270_Franchini
network_acronym_str BDUBAFCEN
repository_id_str 1896
network_name_str Biblioteca Digital (UBA-FCEN)
spelling Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposonsFranchini, L.F.López-Leal, R.Nasif, S.Beati, P.Gelman, D.M.Low, M.J.De Souza, F.J.S.Rubinstein, M.ObesityRetropositionRetrotranspositionSatietyShadow enhancerenhanced green fluorescent proteinproopiomelanocortinanimal cellanimal experimentarcuate nucleusarticleconvergent evolutiondiencephalonevolutionary adaptationfluorescence analysisgenegene expressiongene sequencehumanhuman cellmammalmolecular evolutionmousenerve cellnonhumannPE1 genenPE2 geneplacentaplacental mammalspriority journalreporter generetroposontomatotransgenic mousevertebrateAnimalsBase SequenceEnhancer Elements, GeneticEvolution, MolecularFemaleGene Expression Regulation, DevelopmentalGenes, ReporterHumansMammalsMiceMice, TransgenicMolecular Sequence DataNeuronsPhylogenyPlacentaPregnancyPro-OpiomelanocortinRetroelementsTime FactorsEutheriaLycopersicon esculentumMammaliaMus musculusMyaPrototheriaVertebrataThe proopiomelanocortin gene (POMC) is expressed in a group of neurons present in the arcuate nucleus of the hypothalamus. Neuron-specific POMC expression in mammals is conveyed by two distal enhancers, named nPE1 and nPE2. Previous transgenic mouse studies showed that nPE1 and nPE2 independently drive reporter gene expression to POMC neurons. Here, we investigated the evolutionary mechanisms that shaped not one but two neuron- specific POMC enhancers and tested whether nPE1 and nPE2 drive identical or complementary spatiotemporal expression patterns. Sequence comparison among representative genomes of most vertebrate classes and mammalian orders showed that nPE1 is a placental novelty. Using in silico paleogenomics we found that nPE1 originated from the exaptation of a mammalian- apparent LTR retrotransposon sometime between the metatherian/ eutherian split (147 Mya) and the placental mammal radiation (≈90 Mya). Thus, the evolutionary origin of nPE1 differs, in kind and time, from that previously demonstrated for nPE2, which was exapted from a CORE-short interspersed nucleotide element (SINE) retroposon before the origin of prototherians, 166 Mya. Transgenic mice expressing the fluorescent markers tomato and EGFP driven by nPE1 or nPE2, respectively, demonstrated coexpression of both reporter genes along the entire arcuate nucleus. The onset of reporter gene expression guided by nPE1 and nPE2 was also identical and coincidental with the onset of Pomc expression in the presumptive mouse diencephalon. Thus, the independent exaptation of two unrelated retroposons into functional analogs regulating neuronal POMC expression constitutes an authentic example of convergent molecular evolution of cell-specific enhancers.Fil:Gelman, D.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.2011info: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_00278424_v108_n37_p15270_FranchiniProc. Natl. Acad. Sci. U. S. A. 2011;108(37):15270-15275reponame: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/ar2025-09-29T13:42:57Zpaperaa:paper_00278424_v108_n37_p15270_FranchiniInstitucionalhttps://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 13:42:59.026Biblioteca Digital (UBA-FCEN) - Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturalesfalse
dc.title.none.fl_str_mv Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons
title Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons
spellingShingle Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons
Franchini, L.F.
Obesity
Retroposition
Retrotransposition
Satiety
Shadow enhancer
enhanced green fluorescent protein
proopiomelanocortin
animal cell
animal experiment
arcuate nucleus
article
convergent evolution
diencephalon
evolutionary adaptation
fluorescence analysis
gene
gene expression
gene sequence
human
human cell
mammal
molecular evolution
mouse
nerve cell
nonhuman
nPE1 gene
nPE2 gene
placenta
placental mammals
priority journal
reporter gene
retroposon
tomato
transgenic mouse
vertebrate
Animals
Base Sequence
Enhancer Elements, Genetic
Evolution, Molecular
Female
Gene Expression Regulation, Developmental
Genes, Reporter
Humans
Mammals
Mice
Mice, Transgenic
Molecular Sequence Data
Neurons
Phylogeny
Placenta
Pregnancy
Pro-Opiomelanocortin
Retroelements
Time Factors
Eutheria
Lycopersicon esculentum
Mammalia
Mus musculus
Mya
Prototheria
Vertebrata
title_short Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons
title_full Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons
title_fullStr Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons
title_full_unstemmed Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons
title_sort Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons
dc.creator.none.fl_str_mv Franchini, L.F.
López-Leal, R.
Nasif, S.
Beati, P.
Gelman, D.M.
Low, M.J.
De Souza, F.J.S.
Rubinstein, M.
author Franchini, L.F.
author_facet Franchini, L.F.
López-Leal, R.
Nasif, S.
Beati, P.
Gelman, D.M.
Low, M.J.
De Souza, F.J.S.
Rubinstein, M.
author_role author
author2 López-Leal, R.
Nasif, S.
Beati, P.
Gelman, D.M.
Low, M.J.
De Souza, F.J.S.
Rubinstein, M.
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Obesity
Retroposition
Retrotransposition
Satiety
Shadow enhancer
enhanced green fluorescent protein
proopiomelanocortin
animal cell
animal experiment
arcuate nucleus
article
convergent evolution
diencephalon
evolutionary adaptation
fluorescence analysis
gene
gene expression
gene sequence
human
human cell
mammal
molecular evolution
mouse
nerve cell
nonhuman
nPE1 gene
nPE2 gene
placenta
placental mammals
priority journal
reporter gene
retroposon
tomato
transgenic mouse
vertebrate
Animals
Base Sequence
Enhancer Elements, Genetic
Evolution, Molecular
Female
Gene Expression Regulation, Developmental
Genes, Reporter
Humans
Mammals
Mice
Mice, Transgenic
Molecular Sequence Data
Neurons
Phylogeny
Placenta
Pregnancy
Pro-Opiomelanocortin
Retroelements
Time Factors
Eutheria
Lycopersicon esculentum
Mammalia
Mus musculus
Mya
Prototheria
Vertebrata
topic Obesity
Retroposition
Retrotransposition
Satiety
Shadow enhancer
enhanced green fluorescent protein
proopiomelanocortin
animal cell
animal experiment
arcuate nucleus
article
convergent evolution
diencephalon
evolutionary adaptation
fluorescence analysis
gene
gene expression
gene sequence
human
human cell
mammal
molecular evolution
mouse
nerve cell
nonhuman
nPE1 gene
nPE2 gene
placenta
placental mammals
priority journal
reporter gene
retroposon
tomato
transgenic mouse
vertebrate
Animals
Base Sequence
Enhancer Elements, Genetic
Evolution, Molecular
Female
Gene Expression Regulation, Developmental
Genes, Reporter
Humans
Mammals
Mice
Mice, Transgenic
Molecular Sequence Data
Neurons
Phylogeny
Placenta
Pregnancy
Pro-Opiomelanocortin
Retroelements
Time Factors
Eutheria
Lycopersicon esculentum
Mammalia
Mus musculus
Mya
Prototheria
Vertebrata
dc.description.none.fl_txt_mv The proopiomelanocortin gene (POMC) is expressed in a group of neurons present in the arcuate nucleus of the hypothalamus. Neuron-specific POMC expression in mammals is conveyed by two distal enhancers, named nPE1 and nPE2. Previous transgenic mouse studies showed that nPE1 and nPE2 independently drive reporter gene expression to POMC neurons. Here, we investigated the evolutionary mechanisms that shaped not one but two neuron- specific POMC enhancers and tested whether nPE1 and nPE2 drive identical or complementary spatiotemporal expression patterns. Sequence comparison among representative genomes of most vertebrate classes and mammalian orders showed that nPE1 is a placental novelty. Using in silico paleogenomics we found that nPE1 originated from the exaptation of a mammalian- apparent LTR retrotransposon sometime between the metatherian/ eutherian split (147 Mya) and the placental mammal radiation (≈90 Mya). Thus, the evolutionary origin of nPE1 differs, in kind and time, from that previously demonstrated for nPE2, which was exapted from a CORE-short interspersed nucleotide element (SINE) retroposon before the origin of prototherians, 166 Mya. Transgenic mice expressing the fluorescent markers tomato and EGFP driven by nPE1 or nPE2, respectively, demonstrated coexpression of both reporter genes along the entire arcuate nucleus. The onset of reporter gene expression guided by nPE1 and nPE2 was also identical and coincidental with the onset of Pomc expression in the presumptive mouse diencephalon. Thus, the independent exaptation of two unrelated retroposons into functional analogs regulating neuronal POMC expression constitutes an authentic example of convergent molecular evolution of cell-specific enhancers.
Fil:Gelman, D.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 a group of neurons present in the arcuate nucleus of the hypothalamus. Neuron-specific POMC expression in mammals is conveyed by two distal enhancers, named nPE1 and nPE2. Previous transgenic mouse studies showed that nPE1 and nPE2 independently drive reporter gene expression to POMC neurons. Here, we investigated the evolutionary mechanisms that shaped not one but two neuron- specific POMC enhancers and tested whether nPE1 and nPE2 drive identical or complementary spatiotemporal expression patterns. Sequence comparison among representative genomes of most vertebrate classes and mammalian orders showed that nPE1 is a placental novelty. Using in silico paleogenomics we found that nPE1 originated from the exaptation of a mammalian- apparent LTR retrotransposon sometime between the metatherian/ eutherian split (147 Mya) and the placental mammal radiation (≈90 Mya). Thus, the evolutionary origin of nPE1 differs, in kind and time, from that previously demonstrated for nPE2, which was exapted from a CORE-short interspersed nucleotide element (SINE) retroposon before the origin of prototherians, 166 Mya. Transgenic mice expressing the fluorescent markers tomato and EGFP driven by nPE1 or nPE2, respectively, demonstrated coexpression of both reporter genes along the entire arcuate nucleus. The onset of reporter gene expression guided by nPE1 and nPE2 was also identical and coincidental with the onset of Pomc expression in the presumptive mouse diencephalon. Thus, the independent exaptation of two unrelated retroposons into functional analogs regulating neuronal POMC expression constitutes an authentic example of convergent molecular evolution of cell-specific enhancers.
publishDate 2011
dc.date.none.fl_str_mv 2011
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_00278424_v108_n37_p15270_Franchini
url http://hdl.handle.net/20.500.12110/paper_00278424_v108_n37_p15270_Franchini
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 Proc. Natl. Acad. Sci. U. S. A. 2011;108(37):15270-15275
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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