Cleft lip and palate results from Hedgehog signaling antagonism in the mouse: Phenotypic characterization and clinical implications

Birth Defects Res A Clin Mol Teratol. 2010 Apr;88(4):232-40. doi: 10.1002/bdra.20656.

Abstract

Background: The Hedgehog (Hh) pathway provides inductive signals critical for developmental patterning of the brain and face. In humans and in animal models interference with this pathway yields birth defects, among the most well-studied of which fall within the holoprosencephaly (HPE) spectrum.

Methods: Timed-pregnant C57Bl/6J mice were treated with the natural Hh signaling antagonist cyclopamine by subcutaneous infusion from gestational day (GD) 8.25 to 9.5, or with a potent cyclopamine analog, AZ75, administered by oral gavage at GD 8.5. Subsequent embryonic morphogenesis and fetal central nervous system (CNS) phenotype were respectively investigated by scanning electron microscopy and high resolution magnetic resonance imaging (MRI).

Results: In utero Hh signaling antagonist exposure induced a spectrum of craniofacial and brain malformations. Cyclopamine exposure caused lateral cleft lip and palate (CLP) defects attributable to embryonic deficiency of midline and lower medial nasal prominence tissue. The CLP phenotype was accompanied by olfactory bulb hypoplasia and anterior pituitary aplasia, but otherwise grossly normal brain morphology. AZ75 exposure caused alobar and semilobar HPE with associated median facial deficiencies. An intermediate phenotype of median CLP was produced infrequently by both drug administration regimens.

Conclusions: The results of this study suggest that interference with Hh signaling should be considered in the CLP differential and highlight the occurrence of CNS defects that are expected to be present in a cohort of patients having CLP. This work also illustrates the utility of fetal MRI-based analyses and establishes a novel mouse model for teratogen-induced CLP.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Abnormalities, Drug-Induced / embryology
  • Abnormalities, Drug-Induced / etiology*
  • Abnormalities, Drug-Induced / physiopathology
  • Abnormalities, Multiple / chemically induced*
  • Abnormalities, Multiple / embryology
  • Abnormalities, Multiple / physiopathology
  • Administration, Oral
  • Animals
  • Cells, Cultured / drug effects
  • Cleft Lip / chemically induced*
  • Cleft Lip / embryology
  • Cleft Lip / physiopathology
  • Cleft Palate / chemically induced*
  • Cleft Palate / embryology
  • Cleft Palate / physiopathology
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Female
  • Fetal Resorption / chemically induced
  • Fetus / drug effects
  • Fetus / ultrastructure
  • Hedgehog Proteins / antagonists & inhibitors*
  • Hedgehog Proteins / physiology
  • Holoprosencephaly / chemically induced*
  • Holoprosencephaly / embryology
  • Holoprosencephaly / physiopathology
  • Maternal Exposure / adverse effects*
  • Mice
  • Mice, Inbred C57BL
  • Microscopy, Electron, Scanning
  • NIH 3T3 Cells / drug effects
  • Olfactory Bulb / abnormalities*
  • Olfactory Bulb / embryology
  • Phenotype
  • Pituitary Gland, Anterior / abnormalities*
  • Pituitary Gland, Anterior / embryology
  • Veratrum Alkaloids / administration & dosage
  • Veratrum Alkaloids / pharmacology
  • Veratrum Alkaloids / toxicity*

Substances

  • Hedgehog Proteins
  • Veratrum Alkaloids
  • cyclopamine