Heart-specific ablation of Prkar1a causes failure of heart development and myxomagenesis

Circulation. 2008 Mar 18;117(11):1414-22. doi: 10.1161/CIRCULATIONAHA.107.759233. Epub 2008 Mar 3.

Abstract

Background: Protein kinase A signaling has long been known to play an important role in cardiac function. Dysregulation of the protein kinase A system, caused by mutation of the protein kinase A regulatory subunit gene PRKAR1A, causes the inherited tumor syndrome Carney complex, which includes cardiac myxomas as one of its cardinal features. Mouse models of this genetic defect have been unsatisfactory because homozygote null animals die early in development and heterozygotes do not exhibit a cardiac phenotype.

Methods and results: To study the cardiac-specific effects resulting from complete loss of Prkar1a, we used cre-lox technology to generate mice lacking this protein specifically in cardiomyocytes. Conditional knockout mice died at day 11.5 to 12.5 of embryogenesis with thin-walled, dilated hearts. These hearts showed elevated protein kinase A activity and decreased cardiomyocyte proliferation before demise. Analysis of the expression of transcription factors required for cardiogenesis revealed downregulation of key cardiac transcription factors such as the serum response factor, Gata4, and Nkx2-5. Although heart wall thickness was reduced overall, specific areas exhibited morphological changes consistent with myxomatous degeneration in the walls of knockout hearts.

Conclusions: Loss of Prkar1a from the heart causes a failure of proper myocardial development with subsequent cardiac failure and embryonic demise. These changes appear to be due to suppression of cardiac-specific transcription by increased protein kinase A activity. These biochemical changes lead to myxoma-like changes, indicating that these mice may be a good model with which to study the formation of these tumors.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis
  • Cell Division
  • Cyclic AMP-Dependent Protein Kinase RIalpha Subunit / deficiency*
  • Cyclic AMP-Dependent Protein Kinase RIalpha Subunit / genetics
  • Cyclic AMP-Dependent Protein Kinase RIalpha Subunit / physiology
  • Cyclic AMP-Dependent Protein Kinases / physiology
  • Down-Regulation
  • Fetal Death / enzymology
  • Fetal Death / genetics
  • Fetal Heart / enzymology
  • Fetal Heart / pathology*
  • Fetal Heart / ultrastructure
  • Genes, Lethal
  • Heart Neoplasms / genetics*
  • Heart Neoplasms / pathology
  • Integrases
  • Mice
  • Mice, Knockout
  • Models, Animal
  • Myocytes, Cardiac / enzymology
  • Myxoma / genetics*
  • Myxoma / pathology
  • Neoplastic Syndromes, Hereditary / enzymology
  • Neoplastic Syndromes, Hereditary / genetics
  • Organ Specificity
  • Transcription Factors / biosynthesis
  • Transcription Factors / genetics

Substances

  • Cyclic AMP-Dependent Protein Kinase RIalpha Subunit
  • Prkar1a protein, mouse
  • Transcription Factors
  • Cyclic AMP-Dependent Protein Kinases
  • Cre recombinase
  • Integrases