Time-dependent localization of high- and low-sulfated keratan sulfates in the song nuclei of developing zebra finches

Eur J Neurosci. 2015 Nov;42(9):2716-25. doi: 10.1111/ejn.13073. Epub 2015 Oct 26.

Abstract

Keratan sulfate proteoglycans (KSPGs) and chondroitin sulfate proteoglycans (CSPGs) consist of a protein core with covalently attached glycosaminoglycan side chain. Although CSPGs are known to regulate the end of the critical period, the role of KSPGs in brain development remains unclear. Young male zebra finches memorise song templates during development. The brain regions that are responsible for song learning, known as song nuclei, are recognized as a suitable model for the study of brain development. To understand the potential role of KSPGs, here we examined the localization of KSs with different degrees of sulfation in the brain of developing male zebra finches. Exclusively in the song nuclei, an increase in expression of 5-D-4-positive (5-D-4(+)) high-sulfated KS started after hatching, and reached a plateau at the end of the sensory period, during which the young bird listens to and memorises the song of an adult tutor. By contrast, weak and ubiquitous expression of BCD-4(+) low-sulfated KS remained unchanged until the end of the sensory period, and first increased in the song nuclei at the end of the sensorimotor period, during which the young bird produces plastic songs. Immunoblot analysis showed that phosphacan was a common core protein of 5-D-4(+) KS and BCD-4(+) KS. Finally, we confirmed that the sulfotransferase responsible for the synthesis of high-sulfated KS was exclusively localised in the song nuclei. Our observations suggest that time-dependent localization of KSPGs with different sulfation patterns in the song nuclei may underlie song learning in developing male zebra finches.

Keywords: glycosaminoglycan; phosphacan; sensory motor period; sensory period.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Avian Proteins / metabolism
  • Brain / growth & development*
  • Brain / metabolism*
  • Carbohydrate Sulfotransferases
  • Chondroitin Sulfate Proteoglycans / metabolism
  • Female
  • Finches
  • High Vocal Center / growth & development
  • High Vocal Center / metabolism
  • Keratan Sulfate / chemistry
  • Keratan Sulfate / metabolism*
  • Male
  • Proteoglycans / chemistry
  • Proteoglycans / metabolism*
  • Sulfotransferases / metabolism

Substances

  • Avian Proteins
  • Chondroitin Sulfate Proteoglycans
  • Proteoglycans
  • Keratan Sulfate
  • Sulfotransferases