Abundant corneal gelsolin in Zebrafish and the 'four-eyed' fish, Anableps anableps: possible analogy with multifunctional lens crystallins

Exp Eye Res. 2004 Dec;79(6):949-56. doi: 10.1016/j.exer.2004.04.002.

Abstract

The cornea accumulates high proportions (can be up to 50%) of taxon-specific, water-soluble, cytoplasmic proteins (often enzymes) that have been considered analogous to the multifunctional lens crystallins. We have shown that gelsolin (an actin-severing protein) is the major water-soluble corneal protein of the zebrafish (Danio rerio) and the 'four-eyed' fish (Anableps anableps). Each Anableps eye contains one lens, an aquatic ventral cornea with an epithelium comprising 5-7 cell layers, and an air-exposed flatter dorsal cornea with an epithelium comprising >20 cell layers and appreciably enriched with glycogen. Gelsolin accounts for 38 and 21% of the dorsal and ventral cornea, respectively, suggesting that the abundance of gelsolin in the cornea is not incompatible with its function in air. The thicker, glycogen-enriched, air-exposed dorsal cornea may protect against UV irradiation and desiccation. Gelsolin comprises approximately 50% of the 5 cell-layer thick aquatic corneal epithelium of zebrafish. Reported zebrafish ESTs have indicated the presence of a second gelsolin gene in this species. We show by RT-PCR that the abundant corneal gelsolin (also expressed weakly in lens) (C/L-gelsolin) is also expressed in early development and differs from a ubiquitously expressed gelsolin (U-gelsolin) that is not specialized for cornea. Microinjection tests showed that overexpression of C/L-gelsolin dorsalizes the embryo and can lead to axis duplication, while interruption of C/L-gelsolin expression with a specific morpholino oligonucleotide ventralizes the embryo and interferes with brain and eye development. The evidence that C/L-gelsolin participates in the bone morphogenetic protein (BMP)/Smad dorsal-ventral signaling pathway is reviewed. Finally, we speculate that soluble C/L-gelsolin:actin complexes in the cornea may be analogous to soluble alphaA:alphaB-crystallin complexes in the lens. Together, our data are consistent with an analogy between the abundance of gelsolin in fish corneas and taxon-specific multifunctional crystallins in lenses.

MeSH terms

  • Animals
  • Cornea / anatomy & histology
  • Cornea / metabolism*
  • Crystallins / genetics
  • Crystallins / metabolism*
  • Fishes / anatomy & histology
  • Fishes / metabolism*
  • Gelsolin / metabolism*
  • Gene Expression
  • In Situ Hybridization
  • Lens, Crystalline / metabolism
  • RNA, Messenger / genetics
  • Reverse Transcriptase Polymerase Chain Reaction / methods
  • Zebrafish / anatomy & histology
  • Zebrafish / metabolism

Substances

  • Crystallins
  • Gelsolin
  • RNA, Messenger