Differential expression of BMP inhibitors gremlin and noggin in Hydra suggests distinct roles during budding and patterning of tentacles

Dev Dyn. 2020 Dec;249(12):1470-1485. doi: 10.1002/dvdy.238. Epub 2020 Sep 9.

Abstract

Background: Mechanisms regulating BMP and Wnt pathways and their interactions are not well studied in Hydra.

Results: We report identification of BMP inhibitor gremlin, comparison of its expression with that of noggin and possible antagonism between Wnt and BMP signaling in Hydra. Gremlin is expressed in body column with high levels in budding region and in early buds. Noggin, on the other hand, is expressed in the hypostome, base of tentacles, lower body column, and basal disc. During budding, noggin is expressed at the sites of tentacle emergence. This was confirmed in ectopic tentacles in polyps treated with alsterpaullone (ALP), a GSK-3β inhibitor that leads to upregulation of Wnt pathway. RT-PCR data show that upregulation of Wnt is accompanied by downregulation of bmp 5-8b though noggin and gremlin remain unaltered till 24 hours.

Conclusions: Different expression patterns of gremlin and noggin suggest their roles in budding and patterning of tentacles, respectively. Further, bmp 5-8b inhibition by activated Wnt signaling does not directly involve noggin and gremlin in Hydra. Our data suggest that Wnt/BMP antagonism may have evolved early for defining the oral-aboral axis, while the involvement of BMP antagonists during axial patterning is a recent evolutionary acquisition within the Bilateria lineage.

Keywords: BMP; Wnt; evolution; gremlin; hydra; noggin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biological Evolution
  • Body Patterning / genetics*
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Hydra / embryology*
  • Hydra / metabolism
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / metabolism*
  • Wnt Signaling Pathway / physiology

Substances

  • Carrier Proteins
  • Intercellular Signaling Peptides and Proteins
  • noggin protein