Abstract
Invertebrate retinas contain hexagonal arrays of microvilli that form the honeycomb structure of rhabdome photoreceptors. The largest and most crystalline rhabdomes are found in the squid retina, and we have taken advantage of their unique properties to derive a model for the electron density distribution in microvillar membranes using low angle X-ray diffraction combined with correlation averaging of electron microscope images. The model electron density map, calculated to a resolution of approximately 35 A, shows an unusually high protein content in the membranes. This may be associated with a dense meshwork of membrane junctions between neighboring microvilli as revealed by electron microscope image analysis. Membrane pair contacts are resolved as two or more strands of density crossing the membranes. The microvilli are also linked together by Y-shaped junctions at their three-way contacts. These two sorts of junctions link the membranes into a three-dimensional array and partition them into a mosaic of deformable and rigid domains. This arrangement maintains a remarkable degree of long-range order in squid rhabdomes, and may be responsible for the alignment of rhodopsin molecules. The structural order observed is necessary for these photoreceptors to achieve their high sensitivity to the plane of polarized light. Rhodopsin constitutes about one-half the microvillar protein. The remaining proteins, which can be divided into approximately equal detergent-soluble and insoluble fractions, could account for the composition of the new structures described.
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Selected References
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- Caspar D. L., Goodenough D. A., Makowski L., Phillips W. C. Gap junction structures. I. Correlated electron microscopy and x-ray diffraction. J Cell Biol. 1977 Aug;74(2):605–628. doi: 10.1083/jcb.74.2.605. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chabre M. X-ray diffraction studies of retinal rods. I. Structure of the disc membrane, effect of illumination. Biochim Biophys Acta. 1975 Mar 25;382(3):322–335. doi: 10.1016/0005-2736(75)90274-6. [DOI] [PubMed] [Google Scholar]
- Fernandez H. R., Nickel E. E. Ultrastructural and molecular characteristics of crayfish photoreceptor membranes. J Cell Biol. 1976 Jun;69(3):721–732. doi: 10.1083/jcb.69.3.721. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldsmith T. H., Wehner R. Restrictions on rotational and translational diffusion of pigment in the membranes of a rhabdomeric photoreceptor. J Gen Physiol. 1977 Oct;70(4):453–490. doi: 10.1085/jgp.70.4.453. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hewat E. A., Cusack S., Ruigrok R. W., Verwey C. Low resolution structure of the influenza C glycoprotein determined by electron microscopy. J Mol Biol. 1984 May 15;175(2):175–193. doi: 10.1016/0022-2836(84)90473-x. [DOI] [PubMed] [Google Scholar]
- Johnson E. C., Robinson P. R., Lisman J. E. Cyclic GMP is involved in the excitation of invertebrate photoreceptors. Nature. 1986 Dec 4;324(6096):468–470. doi: 10.1038/324468a0. [DOI] [PubMed] [Google Scholar]
- Kirschner D. A., Hollingshead C. J. Processing for electron microscopy alters membrane structure and packing in myelin. J Ultrastruct Res. 1980 Nov;73(2):211–232. doi: 10.1016/s0022-5320(80)90125-2. [DOI] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Makowski L., Caspar D. L., Phillips W. C., Goodenough D. A. Gap junction structures. II. Analysis of the x-ray diffraction data. J Cell Biol. 1977 Aug;74(2):629–645. doi: 10.1083/jcb.74.2.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
- O'Tousa J. E., Baehr W., Martin R. L., Hirsh J., Pak W. L., Applebury M. L. The Drosophila ninaE gene encodes an opsin. Cell. 1985 Apr;40(4):839–850. doi: 10.1016/0092-8674(85)90343-5. [DOI] [PubMed] [Google Scholar]
- Paulsen R., Zinkler D., Delmelle M. Architecture and dynamics of microvillar photoreceptor membranes of a cephalopod. Exp Eye Res. 1983 Jan;36(1):47–56. doi: 10.1016/0014-4835(83)90088-x. [DOI] [PubMed] [Google Scholar]
- Perrelet A., Baumann F. Evidence for extracellular space in the rhabdome of the honeybee drone eye. J Cell Biol. 1969 Mar;40(3):825–830. doi: 10.1083/jcb.40.3.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roof D. J., Heuser J. E. Surfaces of rod photoreceptor disk membranes: integral membrane components. J Cell Biol. 1982 Nov;95(2 Pt 1):487–500. doi: 10.1083/jcb.95.2.487. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saibil H. R. A light-stimulated increase of cyclic GMP in squid photoreceptors. FEBS Lett. 1984 Mar 26;168(2):213–216. doi: 10.1016/0014-5793(84)80248-3. [DOI] [PubMed] [Google Scholar]
- Saibil H. R. An ordered membrane-cytoskeleton network in squid photoreceptor microvilli. J Mol Biol. 1982 Jul 5;158(3):435–456. doi: 10.1016/0022-2836(82)90208-x. [DOI] [PubMed] [Google Scholar]
- Saibil H. R., Michel-Villaz M. Squid rhodopsin and GTP-binding protein crossreact with vertebrate photoreceptor enzymes. Proc Natl Acad Sci U S A. 1984 Aug;81(16):5111–5115. doi: 10.1073/pnas.81.16.5111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saxton W. O., Baumeister W. The correlation averaging of a regularly arranged bacterial cell envelope protein. J Microsc. 1982 Aug;127(Pt 2):127–138. doi: 10.1111/j.1365-2818.1982.tb00405.x. [DOI] [PubMed] [Google Scholar]
- Schinz R. H., Lo M. V., Larrivee D. C., Pak W. L. Freeze-fracture study of the Drosophila photoreceptor membrane: mutations affecting membrane particle density. J Cell Biol. 1982 Jun;93(3):961–967. doi: 10.1083/jcb.93.3.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Szuts E. Z., Wood S. F., Reid M. S., Fein A. Light stimulates the rapid formation of inositol trisphosphate in squid retinas. Biochem J. 1986 Dec 15;240(3):929–932. doi: 10.1042/bj2400929. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Unwin P. N., Ennis P. D. Two configurations of a channel-forming membrane protein. Nature. 1984 Feb 16;307(5952):609–613. doi: 10.1038/307609a0. [DOI] [PubMed] [Google Scholar]
- Vandenberg C. A., Montal M. Light-regulated biochemical events in invertebrate photoreceptors. 1. Light-activated guanosinetriphosphatase, guanine nucleotide binding, and cholera toxin catalyzed labeling of squid photoreceptor membranes. Biochemistry. 1984 May 22;23(11):2339–2347. doi: 10.1021/bi00306a003. [DOI] [PubMed] [Google Scholar]
- Vandenberg C. A., Montal M. Light-regulated biochemical events in invertebrate photoreceptors. 2. Light-regulated phosphorylation of rhodopsin and phosphoinositides in squid photoreceptor membranes. Biochemistry. 1984 May 22;23(11):2347–2352. doi: 10.1021/bi00306a004. [DOI] [PubMed] [Google Scholar]
- White R. H. The effect of light and light deprivation upon the ultrastructure of the larval mosquito eye. II. The rhabdom. J Exp Zool. 1967 Dec;166(3):405–425. doi: 10.1002/jez.1401660313. [DOI] [PubMed] [Google Scholar]
- Wilkins M. H., Blaurock A. E., Engelman D. M. Bilayer structure in membranes. Nat New Biol. 1971 Mar 17;230(11):72–76. doi: 10.1038/newbio230072a0. [DOI] [PubMed] [Google Scholar]
- Yoshioka T., Inoue H., Takagi M., Hayashi F., Amakawa T. The effect of isobutylmethylxanthine on the photoresponse and phosphorylation of phosphatidylinositol in octopus retina. Biochim Biophys Acta. 1983 Jan 4;755(1):50–55. doi: 10.1016/0304-4165(83)90271-4. [DOI] [PubMed] [Google Scholar]
- de Couet H. G., Stowe S., Blest A. D. Membrane-associated actin in the rhabdomeral microvilli of crayfish photoreceptors. J Cell Biol. 1984 Mar;98(3):834–846. doi: 10.1083/jcb.98.3.834. [DOI] [PMC free article] [PubMed] [Google Scholar]