Reduced NODAL signaling strength via mutation of several pathway members including FOXH1 is linked to human heart defects and holoprosencephaly

Am J Hum Genet. 2008 Jul;83(1):18-29. doi: 10.1016/j.ajhg.2008.05.012. Epub 2008 Jun 5.

Abstract

Abnormalities of embryonic patterning are hypothesized to underlie many common congenital malformations in humans including congenital heart defects (CHDs), left-right disturbances (L-R) or laterality, and holoprosencephaly (HPE). Studies in model organisms suggest that Nodal-like factors provide instructions for key aspects of body axis and germ layer patterning; however, the complex genetics of pathogenic gene variant(s) in humans are poorly understood. Here we report our studies of FOXH1, CFC1, and SMAD2 and summarize our mutational analysis of three additional components in the human NODAL-signaling pathway: NODAL, GDF1, and TDGF1. We identify functionally abnormal gene products throughout the pathway that are clearly associated with CHD, laterality, and HPE. Abnormal gene products are most commonly detected in patients within a narrow spectrum of isolated conotruncal heart defects (minimum 5%-10% of subjects), and far less commonly in isolated laterality or HPE patients (approximately 1% for each). The difference in the mutation incidence between these groups is highly significant. We show that apparent gene dosage discrepancies between humans and model organisms can be reconciled by considering a broader combination of sequence variants. Our studies confirm that (1) the genetic vulnerabilities inferred from model organisms with defects in Nodal signaling are indeed analogous to humans; (2) the molecular analysis of an entire signaling pathway is more complete and robust than that of individual genes and presages future studies by whole-genome analysis; and (3) a functional genomics approach is essential to fully appreciate the complex genetic interactions necessary to produce these effects in humans.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Body Patterning / genetics
  • Case-Control Studies
  • Codon / genetics
  • Cohort Studies
  • DNA Mutational Analysis
  • Embryo, Nonmammalian / abnormalities
  • Epidermal Growth Factor / genetics
  • Forkhead Transcription Factors / chemistry
  • Forkhead Transcription Factors / genetics*
  • GPI-Linked Proteins
  • Growth Differentiation Factor 1
  • Heart Defects, Congenital / embryology
  • Heart Defects, Congenital / genetics*
  • Holoprosencephaly / genetics*
  • Humans
  • Intercellular Signaling Peptides and Proteins / genetics
  • Membrane Glycoproteins / genetics
  • Models, Biological
  • Molecular Sequence Data
  • Mutation
  • Neoplasm Proteins / genetics
  • Nodal Protein
  • Pilot Projects
  • Sequence Homology, Amino Acid
  • Signal Transduction*
  • Smad2 Protein / genetics
  • Transforming Growth Factor beta / genetics*
  • Zebrafish / embryology
  • Zebrafish / genetics

Substances

  • CFC1 protein, human
  • Codon
  • FOXH1 protein, human
  • Forkhead Transcription Factors
  • GDF1 protein, human
  • GPI-Linked Proteins
  • Growth Differentiation Factor 1
  • Intercellular Signaling Peptides and Proteins
  • Membrane Glycoproteins
  • NODAL protein, human
  • Neoplasm Proteins
  • Nodal Protein
  • SMAD2 protein, human
  • Smad2 Protein
  • TDGF1 protein, human
  • Transforming Growth Factor beta
  • Epidermal Growth Factor