Molecular cloning and functional characterization of the upstream rat atrial natriuretic peptide promoter

J Hypertens. 2002 Feb;20(2):219-28. doi: 10.1097/00004872-200202000-00011.

Abstract

Objective: The upregulation of left ventricular atrial natriuretic peptide (ANP) serves as a molecular marker of cardiac hypertrophy. The precise mechanisms underlying this gene induction are unclear, since the presently cloned 3.6 kilo base (kb) rat ANP promoter failed to substantially induce coupled reporter genes in chronically hypertrophied hearts. The aim of this study was to clone and to functionally analyse the upstream ANP promoter.

Design: Upstream of the known ANP promoter, a 1.5 kb segment was cloned by the promoter walker method and found to harbour a putative CCAAT-binding site as well as multiple putative transcription factor binding sites. This newly cloned segment was ligated with a reporter gene, in vivo transfected into rat myocardium, and analysed under basal conditions or after stimulation with both acute (isovolumetric contractions in the Langendorff apparatus) and chronic wall stress (aortic banding).

Results: Reporter gene constructs carrying the newly cloned segment conferred only little promoter activity. In hearts exposed to acute wall stress, the previously cloned 3.6 kb ANP promoter as well as a constitutive promoter (pGL3 promoter vector) were active but markedly suppressed after extension with the newly cloned upstream promoter (-88.1 and -85.5%; P < 0.05 respectively). Site directed mutagenesis of two AP-2 transcription factor binding sites (base pairs -3946 to -3954 or -4192 to -4200) eliminated this silencing effect. In hearts with chronic pressure overload hypertrophy as well as in normal, unstimulated hearts the activity of the 3.6 kb ANP promoter was weak and also abolished after ligation with the 1.5 kb upstream segment. Moreover, both putative AP-2 binding sites within the upstream rat ANP promoter bound specifically to nuclear proteins of unstimulated, acute and chronic pressure overloaded hearts as demonstrated by electrophoresis mobility shift assays.

Conclusion: Novel silencer elements were cloned, localized to two AP-2 binding sites in the upstream ANP promoter, and functionally characterized. Given that the putative upregulation of left ventricular ANP by the extensively studied 3.6 kb proximal promoter region is substantially diminished by the newly cloned segment, the functional significance of regulatory elements within the proximal promoter region should be re-evaluated. The molecular mechanism causing ANP mRNA induction in left ventricular hypertrophy remains obscure.

Publication types

  • Comparative Study
  • Evaluation Study

MeSH terms

  • Animals
  • Atrial Natriuretic Factor / genetics*
  • Atrial Natriuretic Factor / metabolism
  • Blood Pressure / genetics
  • Body Weight / genetics
  • Cloning, Molecular / methods*
  • DNA / metabolism
  • Gene Expression Regulation / genetics
  • Hypertrophy, Left Ventricular / genetics
  • Promoter Regions, Genetic / genetics*
  • Protein Binding / genetics
  • RNA, Messenger / genetics
  • Rats
  • Transcription, Genetic / genetics
  • Transcriptional Activation
  • Ventricular Function*

Substances

  • RNA, Messenger
  • Atrial Natriuretic Factor
  • DNA