γ-Crystallins of the chicken lens: remnants of an ancient vertebrate gene family in birds

FEBS J. 2016 Apr;283(8):1516-30. doi: 10.1111/febs.13689. Epub 2016 Mar 11.

Abstract

γ-Crystallins, abundant proteins of vertebrate lenses, were thought to be absent from birds. However, bird genomes contain well-conserved genes for γS- and γN-crystallins. Although expressed sequence tag analysis of chicken eye found no transcripts for these genes, RT-PCR detected spliced transcripts for both genes in chicken lens, with lower levels in cornea and retina/retinal pigment epithelium. The level of mRNA for γS in chicken lens was relatively very low even though the chicken crygs gene promoter had lens-preferred activity similar to that of mouse. Chicken γS was detected by a peptide antibody in lens, but not in other ocular tissues. Low levels of γS and γN proteins were detected in chicken lens by shotgun mass spectroscopy. Water-soluble and water-insoluble lens fractions were analyzed and 1934 proteins (< 1% false discovery rate) were detected, increasing the known chicken lens proteome 30-fold. Although chicken γS is well conserved in protein sequence, it has one notable difference in leucine 16, replacing a surface glutamine conserved in other γ-crystallins, possibly affecting solubility. However, L16 and engineered Q16 versions were both highly soluble and had indistinguishable circular dichroism, tryptophan fluorescence and heat stability (melting temperature Tm ~ 65 °C) profiles. L16 has been present in birds for over 100 million years and may have been adopted for a specific protein interaction in the bird lens. However, evolution has clearly reduced or eliminated expression of ancestral γ-crystallins in bird lenses. The conservation of genes for γS- and γN-crystallins suggests they may have been preserved for reasons unrelated to the bulk properties of the lens.

Keywords: crystallin; evolution; eye; promoter; protein folding; proteomics.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Base Sequence
  • Blotting, Western
  • Chickens / genetics*
  • Chickens / metabolism
  • Circular Dichroism
  • Eye / metabolism*
  • Lens, Crystalline / chemistry
  • Lens, Crystalline / metabolism*
  • Mice
  • Molecular Sequence Data
  • Multigene Family*
  • Phylogeny
  • Promoter Regions, Genetic / genetics
  • Proteome
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sequence Homology, Nucleic Acid
  • Spectrometry, Fluorescence
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
  • Vertebrates / genetics*
  • Vertebrates / metabolism
  • gamma-Crystallins / chemistry
  • gamma-Crystallins / genetics*
  • gamma-Crystallins / metabolism

Substances

  • Proteome
  • RNA, Messenger
  • gamma-Crystallins