Three-dimensional structure of an invertebrate rhodopsin and basis for ordered alignment in the photoreceptor membrane.
Invertebrate rhodopsins activate a G-protein signalling pathway in microvillar photoreceptors. In contrast to the transducin-cyclic GMP phosphodiesterase pathway found in vertebrate rods and cones, visual transduction in cephalopod (squid, octopus, cuttlefish) invertebrates is signalled via Gq and phospholipase C. Squid rhodopsin contains the conserved residues of the G-protein coupled receptor (GPCR) family, but has only 35% identity with mammalian rhodopsins. Unlike vertebrate rhodopsins, cephalopod rhodopsin is arranged in an ordered lattice in the photoreceptor membranes. This organization confers sensitivity to the plane of polarized light and also provides the optimal orientation of the linear retinal chromophores in the cylindrical microvillar membranes for light capture. Two-dimensional crystals of squid rhodopsin show a rectilinear arrangement that is likely to be related to the alignment of rhodopsins in vivo.Here, we present a three-dimensional structure of squid rhodopsin determined by cryo-electron microscopy of two-dimensional crystals. Docking the atomic structure of bovine rhodopsin into the squid density map shows that the helix packing and extracellular plug structure are conserved. In addition, there are two novel structural features revealed by our map. The linear lattice contact appears to be made by the transverse C-terminal helix lying on the cytoplasmic surface of the membrane. Also at the cytoplasmic surface, additional density may correspond to a helix 5-6 loop insertion found in most GPCRs relative to vertebrate rhodopsins. The similarity supports the conservation in structure of rhodopsins (and other G-protein-coupled receptors) from phylogenetically distant organisms. The map provides the first indication of the structural basis for rhodopsin alignment in the microvillar membrane.
Davies
A
A
Crystallography Department, Birkbeck College, Malet Street, London, WC1E 7HX, UK.
Gowen
B E
BE
Krebs
A M
AM
Schertler
G F
GF
Saibil
H R
HR
D000818:Animals; D002417:Cattle; D002462:Cell Membrane / Q000737:chemistry* / Q000378:metabolism / Q000648:ultrastructure*; D020285:Cryoelectron Microscopy; D003460:Crystallization; D049832:Decapodiformes / Q000737:chemistry* / Q000166:cytology; D019143:Evolution, Molecular; D020962:Heterotrimeric GTP-Binding Proteins / Q000378:metabolism; D008958:Models, Molecular; D017956:Photoreceptor Cells, Invertebrate / Q000166:cytology* / Q000378:metabolism / Q000648:ultrastructure*; D011487:Protein Conformation; D011956:Receptors, Cell Surface / Q000737:chemistry / Q000378:metabolism / Q000648:ultrastructure; D012243:Rhodopsin / Q000737:chemistry* / Q000378:metabolism / Q000648:ultrastructure*
D011956:Receptors, Cell Surface; D012243:Rhodopsin; D020962:Heterotrimeric GTP-Binding Proteins