Characterization of peripherin/rds and rom-1 transport in rod photoreceptors of transgenic and knockout animals

Invest Ophthalmol Vis Sci. 2006 May;47(5):2150-60. doi: 10.1167/iovs.05-0919.

Abstract

Purpose: Peripherin/rds and rom-1 have structural roles in morphogenesis and stabilization of the outer segment, but little is known about their transport and sorting to the rod outer segment. Peripherin/rds and rom-1 trafficking were studied in several knockout and transgenic animal models.

Methods: Rod outer segment formation and distribution of peripherin/rds and rom-1 were examined by immunohistochemistry, electron microscopy, and molecular biological methods in wild-type, rhodopsin-knockout, and peripherin/rds-knockout mice. C-terminally truncated peripherin/rds (Xper38)-GFP chimeric protein sorting was followed by immunofluorescence microscopy in transgenic Xenopus.

Results: In developing wild-type photoreceptors, peripherin/rds was detected exclusively in the distal tip of the connecting cilium in advance of outer segment formation. Rhodopsin-knockout mice failed to create normal rod outer segments and instead, elaborated membranous protrusions at the distal cilium tip. Peripherin/rds and rom-1 localized to this ciliary membrane in rhodopsinless photoreceptors. In transgenic Xenopus, a C-terminally truncated peripherin/rds-GFP fusion predominantly localized to its normal location within disc rims. In developing rds mice, rom-1 accumulated primarily in distal ciliary membranes.

Conclusions: Peripherin/rds transport and localization are polarized to the site of outer segment morphogenesis before disc formation in developing photoreceptors. Peripherin/rds and rom-1 trafficking is maintained in rhodopsin-knockouts, suggesting that rim proteins and rhodopsin have separate transport pathways. The presence of truncated peripherin/rds-GFP in the outer segment supports previous evidence that peripherin/rds mice form homotetramers for outer segment targeting. The finding that rom-1 transports to the outer segment domain in rds mice suggests that rom-1 may possess its own sorting and transport signals.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Eye Proteins / genetics
  • Eye Proteins / metabolism*
  • Fluorescent Antibody Technique, Indirect
  • Gene Silencing / physiology
  • Green Fluorescent Proteins / metabolism
  • Intermediate Filament Proteins / genetics
  • Intermediate Filament Proteins / metabolism*
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Knockout
  • Mice, Transgenic
  • Microscopy, Electron, Scanning
  • Microscopy, Immunoelectron
  • Morphogenesis
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Peripherins
  • Protein Transport
  • RNA, Messenger / metabolism
  • Rats
  • Recombinant Fusion Proteins / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Rhodopsin / genetics
  • Rod Cell Outer Segment / metabolism*
  • Rod Cell Outer Segment / ultrastructure
  • Tetraspanins
  • Transcription, Genetic
  • Xenopus Proteins
  • Xenopus laevis

Substances

  • Eye Proteins
  • Intermediate Filament Proteins
  • Membrane Glycoproteins
  • Membrane Proteins
  • Nerve Tissue Proteins
  • PRPH protein, Xenopus
  • Peripherins
  • Prph2 protein, mouse
  • Prph2 protein, rat
  • RNA, Messenger
  • Recombinant Fusion Proteins
  • Rom1 protein, mouse
  • Tetraspanins
  • Xenopus Proteins
  • Green Fluorescent Proteins
  • Rhodopsin