Mistrafficking of prenylated proteins causes retinitis pigmentosa 2

FASEB J. 2015 Mar;29(3):932-42. doi: 10.1096/fj.14-257915. Epub 2014 Nov 24.

Abstract

The retinitis pigmentosa 2 polypeptide (RP2) functions as a GTPase-activating protein (GAP) for ARL3 (Arf-like protein 3), a small GTPase. ARL3 is an effector of phosphodiesterase 6 Δ (PDE6D), a prenyl-binding protein and chaperone of prenylated protein in photoreceptors. Mutations in the human RP2 gene cause X-linked retinitis pigmentosa (XLRP) and cone-rod dystrophy (XL-CORD). To study mechanisms causing XLRP, we generated an RP2 knockout mouse. The Rp2h(-/-) mice exhibited a slowly progressing rod-cone dystrophy simulating the human disease. Rp2h(-/-) scotopic a-wave and photopic b-wave amplitudes declined at 1 mo of age and continued to decline over the next 6 mo. Prenylated PDE6 subunits and G-protein coupled receptor kinase 1 (GRK1) were unable to traffic effectively to the Rp2h(-/-) outer segments. Mechanistically, absence of RP2 GAP activity increases ARL3-GTP levels, forcing PDE6D to assume a predominantly "closed" conformation that impedes binding of lipids. Lack of interaction disrupts trafficking of PDE6 and GRK1 to their destination, the photoreceptor outer segments. We propose that hyperactivity of ARL3-GTP in RP2 knockout mice and human patients with RP2 null alleles leads to XLRP resembling recessive rod-cone dystrophy.

Keywords: ARL3; PDE6D; RP2; XLRP; rod-cone dystrophy.

Publication types

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

MeSH terms

  • ADP-Ribosylation Factors / metabolism*
  • Animals
  • Antibody Formation
  • Caenorhabditis elegans / growth & development
  • Caenorhabditis elegans / metabolism
  • Cilia / metabolism
  • Cyclic Nucleotide Phosphodiesterases, Type 6 / metabolism*
  • Electroretinography
  • Eye Proteins / physiology*
  • Female
  • G-Protein-Coupled Receptor Kinase 1 / metabolism*
  • GTP-Binding Proteins
  • Guanosine Triphosphate / metabolism
  • Humans
  • Immunoblotting
  • Immunoenzyme Techniques
  • Intracellular Signaling Peptides and Proteins / physiology*
  • Membrane Proteins / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Photoreceptor Cells, Vertebrate / metabolism
  • Protein Prenylation*
  • Protein Transport
  • Rabbits
  • Retinitis Pigmentosa / metabolism*
  • Retinitis Pigmentosa / pathology

Substances

  • Eye Proteins
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • RP2 protein, human
  • Guanosine Triphosphate
  • G-Protein-Coupled Receptor Kinase 1
  • Grk1 protein, mouse
  • Cyclic Nucleotide Phosphodiesterases, Type 6
  • GTP-Binding Proteins
  • Arl3 protein, mouse
  • ADP-Ribosylation Factors

Supplementary concepts

  • Retinitis Pigmentosa 2