Control of organ shape by a secreted metalloprotease in the nematode Caenorhabditis elegans

Nature. 1999 Jun 10;399(6736):586-90. doi: 10.1038/21196.

Abstract

The molecular controls governing organ shape are poorly understood. In the nematode Caenorhabditis elegans, the gonad acquires a U-shape by the directed migration of a specialized 'leader' cell, which is located at the tip of the growing gonadal 'arm'. The gon-1 gene is essential for gonadal morphogenesis: in gon-1 mutants, no arm elongation occurs and somatic gonadal structures are severely malformed. Here we report that gon-1 encodes a secreted protein with a metalloprotease domain and multiple thrombospondin type-1-like repeats. This motif architecture is typical of a small family of genes that include bovine procollagen I N-protease (P1NP), which cleaves collagen, and murine ADAMTS-1, the expression of which correlates with tumour cell progression. We find that gon-1 is expressed in two sites, leader cells and muscle, and that expression in each site has a unique role in forming the gonad. We speculate that GON-1 controls morphogenesis by remodelling basement membranes and that regulation of its activity is crucial for achieving organ shape.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans / anatomy & histology
  • Caenorhabditis elegans / embryology*
  • Caenorhabditis elegans / enzymology*
  • Caenorhabditis elegans Proteins*
  • Chromosome Mapping
  • Cloning, Molecular
  • Female
  • Gene Expression
  • Genes, Helminth
  • Gonads / embryology
  • Helminth Proteins / chemistry
  • Helminth Proteins / genetics
  • Helminth Proteins / physiology*
  • Male
  • Metalloendopeptidases / chemistry
  • Metalloendopeptidases / genetics
  • Metalloendopeptidases / physiology*
  • Molecular Sequence Data
  • Morphogenesis / genetics
  • Morphogenesis / physiology
  • Mutagenesis, Site-Directed
  • Sequence Homology, Amino Acid
  • Thrombospondin 1 / chemistry
  • Transgenes

Substances

  • Caenorhabditis elegans Proteins
  • Helminth Proteins
  • Thrombospondin 1
  • GON-1 protein, C elegans
  • Metalloendopeptidases