Ets-2 and C/EBP-beta are important mediators of ovine trophoblast Kunitz domain protein-1 gene expression in trophoblast

BMC Mol Biol. 2007 Feb 27:8:14. doi: 10.1186/1471-2199-8-14.

Abstract

Background: The trophoblast Kunitz domain proteins (TKDPs) constitute a highly expressed, placenta-specific, multigene family restricted to ruminant ungulates and characterized by a C-terminal "Kunitz" domain, preceded by one or more unique N-terminal domains. TKDP-1 shares an almost identical expression pattern with interferon-tau, the "maternal recognition of pregnancy protein" in ruminants. Our goal here has been to determine whether the ovine (ov) Tkdp-1 and IFNT genes possess a similar transcriptional code.

Results: The ovTkdp-1 promoter has been cloned and characterized. As with the IFNT promoter, the Tkdp-1 promoter is responsive to Ets-2, and promoter-driven reporter activity can be increased over 700-fold in response to over-expression of Ets-2 and a constitutively active form of protein Kinase A (PKA). Unexpectedly, the promoter element of Tkdp-1 responsible for this up-regulation, unlike that of the IFNT, does not bind Ets-2. However, mutation of a CCAAT/enhancer binding element within this control region not only reduced basal transcriptional activity, but prevented Ets-2 as well as cyclic adenosine 5'-monophosphate (cAMP)/PKA and Ras/mitogen-activated protein kinase (MAPK) responsiveness. In vitro binding experiments and in vivo protein-protein interaction assays implicated CCAAT/enhancer binding protein-beta (C/EBP-beta) as involved in up-regulating the Tkdp-1 promoter activity. A combination of Ets-2 and C/EBP-beta can up-regulate expression of the minimal Tkdp-1 promoter as much as 930-fold in presence of a cAMP analog. An AP-1-like element adjacent to the CCAAT enhancer, which binds Jun family members, is required for basal and cAMP/ C/EBP-beta-dependent activation of the gene, but not for Ets-2-dependent activity.

Conclusion: This paper demonstrates how Ets-2, a key transcription factor for trophoblast differentiation and function, can control expression of two genes (Tkdp-1 and IFNT) having similar spatial and temporal expression patterns via very different mechanisms.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Base Pairing
  • Binding Sites
  • CCAAT-Enhancer-Binding Protein-beta / genetics
  • CCAAT-Enhancer-Binding Protein-beta / metabolism*
  • Choriocarcinoma / enzymology
  • Choriocarcinoma / genetics
  • Choriocarcinoma / pathology
  • Cyclic AMP / metabolism
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Female
  • Gene Expression Regulation*
  • Humans
  • Interferon Type I / genetics
  • Interferon Type I / metabolism
  • Mice
  • Mitogen-Activated Protein Kinases / metabolism
  • NIH 3T3 Cells
  • Pregnancy
  • Pregnancy Proteins / genetics
  • Pregnancy Proteins / metabolism
  • Promoter Regions, Genetic / genetics
  • Protein Binding
  • Proto-Oncogene Protein c-ets-2 / genetics
  • Proto-Oncogene Protein c-ets-2 / metabolism*
  • Proto-Oncogene Proteins p21(ras) / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Sheep / genetics*
  • Transcription Factor AP-1 / genetics
  • Transcription, Genetic
  • Trophoblasts / metabolism*
  • Trypsin Inhibitors / genetics*
  • Trypsin Inhibitors / metabolism

Substances

  • CCAAT-Enhancer-Binding Protein-beta
  • Interferon Type I
  • Pregnancy Proteins
  • Proto-Oncogene Protein c-ets-2
  • RNA, Messenger
  • Transcription Factor AP-1
  • Trypsin Inhibitors
  • interferon tau
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases
  • Mitogen-Activated Protein Kinases
  • Proto-Oncogene Proteins p21(ras)