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Article: Adaptive changes in the transcription factor HoxA-11 are essential for the evolution of pregnancy in mammals

TitleAdaptive changes in the transcription factor HoxA-11 are essential for the evolution of pregnancy in mammals
Authors
KeywordsEvolution of development
Functional divergence
Molecular evolution
trans-regulatory evolution
Issue Date2008
PublisherNational Academy of Sciences. The Journal's web site is located at http://www.pnas.org
Citation
Proceedings Of The National Academy Of Sciences Of The United States Of America, 2008, v. 105 n. 39, p. 14928-14933 How to Cite?
AbstractEvolutionary change in gene regulation can result from changes in cis-regulatory elements, leading to differences in the temporal and spatial expression of genes or in the coding region of transcription factors leading to novel functions or both. Although there is a growing body of evidence supporting the importance of cis-regulatory evolution, examples of protein-mediated evolution of novel developmental pathways have not been demonstrated. Here, we investigate the evolution of prolactin (PRL) expression in endometrial cells, which is essential for placentation/pregnancy in eutherian mammals and is a direct regulatory target of the transcription factor HoxA-11. Here, we show that (i) endometrial PRL expression is a derived feature of placental mammals, (ii) the PRL regulatory gene HoxA-11 experienced a period of strong positive selection in the stem-lineage of eutherian mammals, and (iii) only HoxA-11 proteins from placental mammals, including the reconstructed ancestral eutherian gene, are able to up-regulate PRL from the promoter used in endometrial cells. In contrast, HoxA-11 from the reconstructed therian ancestor, opossum, platypus, and chicken are unable to up-regulate PRL expression. These results demonstrate that the evolution of novel gene expression domains is not only mediated by the evolution of cis-regulatory elements but can also require evolutionary changes of transcription factor proteins themselves. © 2008 by The National Academy of Sciences of the USA.
Persistent Identifierhttp://hdl.handle.net/10722/60687
ISSN
2015 Impact Factor: 9.423
2015 SCImago Journal Rankings: 6.883
PubMed Central ID
ISI Accession Number ID
Funding AgencyGrant Number
John Templeton Foundation
Funding Information:

We thank Dr. J.J. Roth for assistance in making expression constructs and tissue culture and Dr. T. Williams for help with immunocytochemistry. We also thank Dr. K. Smith (Duke University, Durham, NC) for providing pregnant opossum uterus samples and Dr. D. Wildman (Wayne State University, Detroit, MI) for providing RACE ready cDNA from elephant placenta. This work was supported by a grant from the John Templeton Foundation.

References

 

DC FieldValueLanguage
dc.contributor.authorLynch, VJen_HK
dc.contributor.authorTanzer, Aen_HK
dc.contributor.authorWang, Yen_HK
dc.contributor.authorLeung, FCen_HK
dc.contributor.authorGellersen, Ben_HK
dc.contributor.authorEmera, Den_HK
dc.contributor.authorWagner, GPen_HK
dc.date.accessioned2010-05-31T04:16:31Z-
dc.date.available2010-05-31T04:16:31Z-
dc.date.issued2008en_HK
dc.identifier.citationProceedings Of The National Academy Of Sciences Of The United States Of America, 2008, v. 105 n. 39, p. 14928-14933en_HK
dc.identifier.issn0027-8424en_HK
dc.identifier.urihttp://hdl.handle.net/10722/60687-
dc.description.abstractEvolutionary change in gene regulation can result from changes in cis-regulatory elements, leading to differences in the temporal and spatial expression of genes or in the coding region of transcription factors leading to novel functions or both. Although there is a growing body of evidence supporting the importance of cis-regulatory evolution, examples of protein-mediated evolution of novel developmental pathways have not been demonstrated. Here, we investigate the evolution of prolactin (PRL) expression in endometrial cells, which is essential for placentation/pregnancy in eutherian mammals and is a direct regulatory target of the transcription factor HoxA-11. Here, we show that (i) endometrial PRL expression is a derived feature of placental mammals, (ii) the PRL regulatory gene HoxA-11 experienced a period of strong positive selection in the stem-lineage of eutherian mammals, and (iii) only HoxA-11 proteins from placental mammals, including the reconstructed ancestral eutherian gene, are able to up-regulate PRL from the promoter used in endometrial cells. In contrast, HoxA-11 from the reconstructed therian ancestor, opossum, platypus, and chicken are unable to up-regulate PRL expression. These results demonstrate that the evolution of novel gene expression domains is not only mediated by the evolution of cis-regulatory elements but can also require evolutionary changes of transcription factor proteins themselves. © 2008 by The National Academy of Sciences of the USA.en_HK
dc.languageengen_HK
dc.publisherNational Academy of Sciences. The Journal's web site is located at http://www.pnas.orgen_HK
dc.relation.ispartofProceedings of the National Academy of Sciences of the United States of Americaen_HK
dc.subjectEvolution of developmenten_HK
dc.subjectFunctional divergenceen_HK
dc.subjectMolecular evolutionen_HK
dc.subjecttrans-regulatory evolutionen_HK
dc.subject.meshEndometrium - metabolism-
dc.subject.meshEvolution, Molecular-
dc.subject.meshGene Expression Regulation, Developmental-
dc.subject.meshHomeodomain Proteins - genetics - metabolism-
dc.subject.meshPregnancy - genetics-
dc.titleAdaptive changes in the transcription factor HoxA-11 are essential for the evolution of pregnancy in mammalsen_HK
dc.typeArticleen_HK
dc.identifier.openurlhttp://library.hku.hk:4550/resserv?sid=HKU:IR&issn=0027-8424&volume=105&issue=39&spage=14928&epage=14933&date=2008&atitle=Adaptive+changes+in+the+transcription+factor+HoxA-11+are+essential+for+the+evolution+of+pregnancy+in+mammals-
dc.identifier.emailWang, Y: cdwyj@yahoo.comen_HK
dc.identifier.emailLeung, FC: fcleung@hkucc.hku.hken_HK
dc.identifier.authorityWang, Y=rp00801en_HK
dc.identifier.authorityLeung, FC=rp00731en_HK
dc.description.naturelink_to_OA_fulltext-
dc.identifier.doi10.1073/pnas.0802355105en_HK
dc.identifier.pmid18809929-
dc.identifier.pmcidPMC2567470-
dc.identifier.scopuseid_2-s2.0-54449095844en_HK
dc.identifier.hkuros166176en_HK
dc.relation.referenceshttp://www.scopus.com/mlt/select.url?eid=2-s2.0-54449095844&selection=ref&src=s&origin=recordpageen_HK
dc.identifier.volume105en_HK
dc.identifier.issue39en_HK
dc.identifier.spage14928en_HK
dc.identifier.epage14933en_HK
dc.identifier.isiWOS:000261914300021-
dc.publisher.placeUnited Statesen_HK
dc.identifier.f10001146915-
dc.identifier.scopusauthoridLynch, VJ=8309259000en_HK
dc.identifier.scopusauthoridTanzer, A=8833025700en_HK
dc.identifier.scopusauthoridWang, Y=36062525200en_HK
dc.identifier.scopusauthoridLeung, FC=7103078633en_HK
dc.identifier.scopusauthoridGellersen, B=7003531313en_HK
dc.identifier.scopusauthoridEmera, D=25622104600en_HK
dc.identifier.scopusauthoridWagner, GP=7404372801en_HK
dc.identifier.citeulike3332325-

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