Complex Compound Inheritance of Lethal Lung Developmental Disorders Due to Disruption of the TBX-FGF Pathway

Am J Hum Genet. 2019 Feb 7;104(2):213-228. doi: 10.1016/j.ajhg.2018.12.010. Epub 2019 Jan 10.

Abstract

Primary defects in lung branching morphogenesis, resulting in neonatal lethal pulmonary hypoplasias, are incompletely understood. To elucidate the pathogenetics of human lung development, we studied a unique collection of samples obtained from deceased individuals with clinically and histopathologically diagnosed interstitial neonatal lung disorders: acinar dysplasia (n = 14), congenital alveolar dysplasia (n = 2), and other lethal lung hypoplasias (n = 10). We identified rare heterozygous copy-number variant deletions or single-nucleotide variants (SNVs) involving TBX4 (n = 8 and n = 2, respectively) or FGF10 (n = 2 and n = 2, respectively) in 16/26 (61%) individuals. In addition to TBX4, the overlapping ∼2 Mb recurrent and nonrecurrent deletions at 17q23.1q23.2 identified in seven individuals with lung hypoplasia also remove a lung-specific enhancer region. Individuals with coding variants involving either TBX4 or FGF10 also harbored at least one non-coding SNV in the predicted lung-specific enhancer region, which was absent in 13 control individuals with the overlapping deletions but without any structural lung anomalies. The occurrence of rare coding variants involving TBX4 or FGF10 with the putative hypomorphic non-coding SNVs implies a complex compound inheritance of these pulmonary hypoplasias. Moreover, they support the importance of TBX4-FGF10-FGFR2 epithelial-mesenchymal signaling in human lung organogenesis and help to explain the histopathological continuum observed in these rare lethal developmental disorders of the lung.

Keywords: 17q23.1q23.2 recurrent deletion; 5p12 deletion; T-box transcription factor 4; aplasia of lacrimal and salivary glands; fibroblast growth factor 10; lacrimoauriculodentodigital (LAAD) syndrome; lung hypoplasia; neonatal lung disease.

Publication types

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

MeSH terms

  • DNA Copy Number Variations / genetics
  • Female
  • Fibroblast Growth Factor 10 / genetics*
  • Fibroblast Growth Factor 10 / metabolism
  • Gene Expression Regulation
  • Gestational Age
  • Humans
  • Infant, Newborn
  • Infant, Newborn, Diseases / genetics*
  • Infant, Newborn, Diseases / metabolism
  • Infant, Newborn, Diseases / mortality*
  • Infant, Newborn, Diseases / pathology
  • Lung / embryology
  • Lung / growth & development
  • Lung Diseases / genetics*
  • Lung Diseases / metabolism
  • Lung Diseases / mortality*
  • Lung Diseases / pathology
  • Male
  • Maternal Inheritance
  • Organogenesis
  • Paternal Inheritance
  • Pedigree
  • Polymorphism, Single Nucleotide / genetics
  • Receptor, Fibroblast Growth Factor, Type 2 / metabolism
  • Signal Transduction / genetics*
  • T-Box Domain Proteins / genetics*
  • T-Box Domain Proteins / metabolism

Substances

  • FGF10 protein, human
  • Fibroblast Growth Factor 10
  • T-Box Domain Proteins
  • TBX4 protein, human
  • FGFR2 protein, human
  • Receptor, Fibroblast Growth Factor, Type 2