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
- Institución
- Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
- OAI Identificador
- paperaa:paper_00278424_v108_n37_p15270_Franchini
Ver los metadatos del registro completo
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network_name_str |
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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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1844618736287350784 |
score |
13.070432 |