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

Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):14928-33. doi: 10.1073/pnas.0802355105. Epub 2008 Sep 22.

Abstract

Evolutionary 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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Chickens / genetics
  • Chickens / metabolism
  • Elephants / genetics
  • Elephants / metabolism
  • Endometrium / metabolism*
  • Evolution, Molecular*
  • Female
  • Gene Expression Regulation, Developmental*
  • Homeodomain Proteins / genetics*
  • Homeodomain Proteins / metabolism
  • Humans
  • Mice
  • Molecular Sequence Data
  • Opossums / genetics
  • Opossums / metabolism
  • Placenta / metabolism
  • Pregnancy / genetics*
  • Prolactin / genetics*
  • Promoter Regions, Genetic
  • Selection, Genetic

Substances

  • HOXA11 protein, human
  • Homeodomain Proteins
  • Prolactin