Rapid nitric oxide-mediated S-nitrosylation of estrogen receptor: regulation of estrogen-dependent gene transcription

Proc Natl Acad Sci U S A. 2005 Feb 15;102(7):2632-6. doi: 10.1073/pnas.0409854102. Epub 2005 Feb 7.

Abstract

Nitric oxide (NO) and estrogen receptor (ER) are both important mediators of signal transduction in cardiovascular and reproductive tissues. In this study, we evaluated NO-mediated S-nitrosylation of ER and assessed the effect of this structural modification on transcription-related functions of ER. We have found selective inhibitory effects of NO on specific binding of ER to specific estrogen-responsive elements (ERE) that can be reversed in the presence of the reducing agent, DTT, thus suggesting that S-nitrosylation of thiolate-zinc centers may occur within the ER molecule. Furthermore, we examined inhibitory effects of NO on ER-dependent transcriptional activity by using an ERE-driven reporter gene system. By monitoring biophysical changes in the structure of NO-treated or untreated human recombinant ERalpha,we obtained evidence for the formation of S-nitrosothiols in the ER molecule. In addition, we have detected specific S-nitrosylation of cysteine residues within the ER molecule by immunodetection of S-nitrosocysteine moieties in ER. Collectively, these findings suggest an important physiological role for NO in modification of human ER structure by S-nitrosylation, an effect that leads, in turn, to impaired DNA-binding activity of ER and subsequent blockade of estrogen-dependent gene transcription. Thus, NO-induced S-nitrosylation of ER can occur at cysteine residues that coordinate Zn2+ within the two major DNA-binding Zn-finger domains of ER, resulting in selective inhibition of DNA-binding at specific ERE. This cross-communication between NO and ER may favor activation of rapid (nongenomic) signaling pathways and subsequent modulation of downstream genomic activity.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Binding Sites / genetics
  • COS Cells
  • Cell Line
  • Cysteine / analogs & derivatives*
  • Cysteine / metabolism
  • DNA / genetics
  • DNA / metabolism
  • Endoplasmic Reticulum / metabolism
  • Estrogen Receptor alpha / chemistry
  • Estrogen Receptor alpha / metabolism
  • Estrogens / metabolism*
  • Genes, Reporter
  • Humans
  • Models, Biological
  • Nitric Oxide / metabolism*
  • Nitric Oxide / pharmacology
  • Receptors, Estrogen / chemistry
  • Receptors, Estrogen / metabolism*
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • S-Nitrosothiols / metabolism
  • Signal Transduction
  • Transcription, Genetic* / drug effects
  • Transfection

Substances

  • Estrogen Receptor alpha
  • Estrogens
  • Receptors, Estrogen
  • Recombinant Proteins
  • S-Nitrosothiols
  • Nitric Oxide
  • DNA
  • S-nitrosocysteine
  • Cysteine