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

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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 expre...

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Autores principales:	Santangelo, A.M., De Souza, F.S.J., Franchini, L.F., Bumaschny, V.F., Low, M.J., Rubinstein, M.
Formato:	Artículo publishedVersion
Lenguaje:	Inglés
Publicado:	2007
Materias:	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
Acceso en línea:	http://hdl.handle.net/20.500.12110/paper_15537390_v3_n10_p1813_Santangelo
Aporte de:	Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA) de Universidad de Buenos Aires

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spelling	paperaa:paper_15537390_v3_n10_p1813_Santangelo2023-06-12T16:50:44Z Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene PLoS Genet. 2007;3(10):1813-1826 Santangelo, A.M. De Souza, F.S.J. Franchini, L.F. Bumaschny, V.F. Low, M.J. Rubinstein, 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 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. 2007 info:eu-repo/semantics/article info:ar-repo/semantics/artículo info:eu-repo/semantics/publishedVersion application/pdf eng info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/2.5/ar http://hdl.handle.net/20.500.12110/paper_15537390_v3_n10_p1813_Santangelo
institution	Universidad de Buenos Aires
institution_str	I-28
repository_str	R-134
collection	Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA)
language	Inglés
orig_language_str_mv	eng
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
spellingShingle	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 Santangelo, A.M. De Souza, F.S.J. Franchini, L.F. Bumaschny, V.F. Low, M.J. Rubinstein, M. Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene
topic_facet	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
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.
format	Artículo Artículo publishedVersion
author	Santangelo, A.M. De Souza, F.S.J. Franchini, L.F. Bumaschny, V.F. Low, M.J. Rubinstein, M.
author_facet	Santangelo, A.M. De Souza, F.S.J. Franchini, L.F. Bumaschny, V.F. Low, M.J. Rubinstein, M.
author_sort	Santangelo, A.M.
title	Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene
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
publishDate	2007
url	http://hdl.handle.net/20.500.12110/paper_15537390_v3_n10_p1813_Santangelo
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Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene

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