Thyroid hormone induces a time-dependent opsin switch in the retina of salmonid fishes

Invest Ophthalmol Vis Sci. 2009 Jun;50(6):3024-32. doi: 10.1167/iovs.08-2713. Epub 2009 Feb 14.

Abstract

Purpose: To determine the role of thyroid hormone in inducing the UV (SWS1)-to-blue (SWS2) opsin switch in the retina of two salmonid fishes, the coho salmon (Oncorhynchus kisutch) and the rainbow trout (O. mykiss).

Methods: Fish were treated with thyroid hormone (T(4)) or the vehicle solution (0.1 M NaOH, control), exogenously or by intraocular injection, at different life history stages. Microspectrophotometry and in situ hybridization with riboprobes against the SWS1 and SWS2 opsins were used to reveal the dynamics of opsin expression in treated and control animals. To assess whether thyroid hormone induced differentiation of retinal progenitor cells into cones, treated and control fish were injected intraocularly with bromodeoxyuridine (BrdU) and the number of proliferating cells in the outer nuclear layer (ONL) determined. These observations were accompanied by histologic counts of cone densities.

Results: Thyroid hormone induced a reversible UV-to-blue opsin switch in differentiated single cones of juvenile salmonids (alevin and parr stages), but failed to exert any effect in the retina of older fish (smolt stage). The switch progressed from the ventral to the dorsal retina in clockwise fashion. Thyroid hormone did not induce cone density changes or alterations in the number of BrdU-labeled cells, which were the same in control and treated animals.

Conclusions: Thyroid hormone induces a UV (SWS1)-to-blue (SWS2) opsin switch in the retina of young salmonid fishes that is identical with that occurring during natural development. The switch occurs in differentiated photoreceptors, is reversible (maintained by thyroid hormone exposure), and can be induced only before its natural onset. Thyroid hormone did not cause changes in the number of proliferating cells in the ONL. These results conform to the dynamics of thyroid hormone-induced opsin expression in the mouse and are consistent with the opsin plasticity found in differentiated photoreceptors of the fruit fly, Drosophila melanogaster. This work establishes a role for thyroid hormone in triggering opsin switches in the vertebrate retina.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bromodeoxyuridine / metabolism
  • Cell Count
  • Cell Differentiation / drug effects
  • Cell Proliferation / drug effects
  • Cone Opsins / metabolism*
  • In Situ Hybridization
  • Microspectrophotometry
  • Oncorhynchus kisutch
  • Oncorhynchus mykiss
  • RNA, Messenger / metabolism
  • Retinal Cone Photoreceptor Cells / cytology
  • Retinal Cone Photoreceptor Cells / drug effects*
  • Retinal Cone Photoreceptor Cells / metabolism*
  • Thyroxine / pharmacology*
  • Time Factors

Substances

  • Cone Opsins
  • RNA, Messenger
  • Bromodeoxyuridine
  • Thyroxine