Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography

Journal of Cell Biology

Volumn 177, Issue 5, 2007, Pages 917-925

  Nickell, Stephan ^a   Park, Paul S H ^b   Baumeister, Wolfgang ^a   Palczewski, Krzysztof ^b  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CRYOELECTRON TOMOGRAPHY; MOUSE; NERVE CELL; NONHUMAN; PHOTOTRANSDUCTION; PRIORITY JOURNAL; RETINA; RETINA ROD OUTER SEGMENT; TOMOGRAPHY; VITRIFICATION;

ANIMALS; CRYOELECTRON MICROSCOPY; IMAGING, THREE-DIMENSIONAL; MICE; ROD OUTER SEGMENTS;

MAMMALIA; MURINAE;

EID: 34249884786     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200612010     Document Type: Article

References (85)

1. Andreucci, D., P. Bisegna, G. Caruso, H.E. Hamm, and E. DiBenedetto. 2003. Mathematical model of the spatio-temporal dynamics of second messengers in visual transduction. Biophys. J. 85:1358-1376.
2. Arshavsky, V.Y., T.D. Lamb, and E.N. Pugh Jr. 2002. G proteins and phototransduction. Annu. Rev. Physiol. 64:153-187.
3. Batra-Safferling, R., K. Abarca-Heidemann, H.G. Korschen, C. Tziatzios, M. Stoldt, I. Budyak, D. Willbold, H. Schwalbe, J. Klein-Seetharaman, and U.B. Kaupp. 2006. Glutamic acid-rich proteins of rod photoreceptors are natively unfolded. J. Biol. Chem. 281:1449-1460.
4. Batten, M.L., Y. Imanishi, D.C. Tu, T. Doan, L. Zhu, J. Pang, L. Glushakova, A.R. Moise, W. Baehr, R.N. Van Gelder, et al. 2005. Pharmacological and rAAV gene therapy rescue of visual functions in a blind mouse model of Leber congenital amaurosis. PLoS Med. 2:e333.
5. Blaurock, A.E., and M.H. Wilkins. 1969. Structure of frog photoreceptor membranes. Nature. 223:906-909.
6. Blaurock, A.E., and M.H. Wilkins. 1972. Structure of retinal photoreceptor membranes. Nature. 236:313-314.
7. Brown, P.K., I.R. Gibbons, and G. Wald. 1963. The visual cells and visual pigment of the mudpuppy, Necturus. J. Cell Biol. 19:79-106.
8. Chang, B., N.L. Hawes, R.E. Hurd, M.T. Davisson, S. Nusinowitz, and J.R. Heckenlively. 2002. Retinal degeneration mutants in the mouse. Vision Res. 42:517-525.
9. Clark, A.W., and D. Branton. 1968. Fracture faces in frozen outer segments from the guinea pig retina. Z. Zellforsch. Mikrosk. Anat. 91:586-603.
10. Cohen, A.I. 1960. The ultrastructure of the rods of the mouse retina. Am. J. Anat. 107:23-48.
11. Cohen, A.I. 1961. The fine structure of the extrafoveal receptors of the Rhesus monkey. Exp. Eye Res. 1:128-136.
12. Cohen, A.I. 1963. The fine structure of the visual receptors of the pigeon. Exp. Eye Res. 2:88-97.
13. Cohen, A.I. 1964. Some observations on the fine structure of the retinal receptors of the American gray squirrel. Invest. Ophthalmol. 3:198-216.
14. Cohen, A.I. 1968. New evidence supporting the linkage to extracellular space of outer segment saccules of frog cones but not rods. J. Cell Biol. 37:424-444.
15. Cohen, A.I. 1971. Electron microscope observations on form changes in photoreceptor outer segments and their saccules in response to osmotic stress. J. Cell Biol. 48:547-565.
16. Corless, J.M. 1972. Lamellar structure of bleached and unbleached rod photoreceptor membranes. Nature. 237:229-231.
17. Corless, J.M., and T.G. Schneider. 1987. Patterns of interdisk connections within the lamellar domains of retinal rod outer segment disks: observations relevant to the axial propagation of incisures. Exp. Eye Res. 45:883-905.
18. Corless, J.M., R.D. Fetter, and M.J. Costello. 1987a. Structural features of the terminal loop region of frog retinal rod outer segment disk membranes: I. Organization of lipid components. J. Comp. Neurol. 257:1-8.
19. Corless, J.M., R.D. Fetter, O.B. Zampighi, M.J. Costello, and D.L. Wall-Buford. 1987b. Structural features of the terminal loop region of frog retinal rod outer segment disk membranes: II. Organization of the terminal loop complex. J. Comp. Neurol. 257:9-23.
20. Daemen, F.J. 1973. Vertebrate rod outer segment membranes. Biochim. Biophys. Acta. 300:255-288.
21. Dalke, C., and J. Graw. 2005. Mouse mutants as models for congenital retinal disorders. Exp. Eye Res. 81:503-512.
22. De Robertis, E., and A. Lasansky. 1958. Submicroscopic organization of retinal cones of the rabbit. J. Biophys. Biochem. Cytol. 4:743-746.
23. Dejneka, N.S., T.S. Rex, and J. Bennett. 2003. Gene therapy and animal models for retinal disease. Dev. Ophthalmol. 37:188-198.
24. Dierksen, K., D. Typke, R. Hegerl, J. Walz, E. Sackmann, and W. Baumeister. 1995. Three-dimensional structure of lipid vesicles embedded in vitreous ice and investigated by automated electron tomography. Biophys. J. 68:1416-1422.
25. Dowling, J.E. 1965. Foveal receptors of the monkey retina: fine structure. Science. 147:57-59.
26. Dubochet, J., M. Adrian, J.J. Chang, J.C. Homo, J. Lepault, A.W. McDowall, and P. Schultz. 1988. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21:129-228.
27. Falk, G., and P. Fatt. 1969. Distinctive properties of the lamellar and disk-edge structures of the rod outer segment. J. Ultrastruct. Res. 28:41-60.
28. Falk, G., and P. Fatt. 1973. Changes in structure of the disks of retinal rods in hypotonic solutions. J. Cell Sci. 13:787-797.
29. Filipek, S., R.E. Stenkamp, D.C. Teller, and K. Palczewski. 2003. G protein-coupled receptor rhodopsin: a prospectus. Annu. Rev. Physiol. 65:851-879.
30. Finean, J.B., F.S. Sjostrand, and E. Steinmann. 1953. Submicroscopic organisation of some layered lipoprotein structures (nerve myelin, retinal rods, and chloroplasts). Exp. Cell Res. 5:557-559.
31. Fotiadis, D., Y. Liang, S. Filipek, D.A. Saperstein, A. Engel, and K. Palczewski. 2003. Atomic-force microscopy: Rhodopsin dimers in native disc membranes. Nature. 421:127-128.
32. Frangakis, A.S., J. Bohm, F. Forster, S. Nickell, D. Nicastro, D. Typke, R. Hegerl, and W. Baumeister. 2002. Identification of macromolecular complexes in cryoelectron tomograms of phantom cells. Proc. Natl. Acad. Sci. USA. 99:14153-14158.
33. Godfrey, A.J. 1973. A study of the ultrastructure of visual cell outer segment membranes. J. Ultrastruct. Res. 43:228-246.
34. Goldberg, A.F., and R.S. Molday. 2000. Expression and characterization of peripherin/rds-rom-1 complexes and mutants implicated in retinal degenerative diseases. Methods Enzymol. 316:671-687.
35. Gras, W.J., and C.R. Worthington. 1969. X-ray analysis of retinal photoreceptors. Proc. Natl. Acad. Sci. USA. 63:233-238.
36. Grimm, R., D. Typke, M. Barmann, and W. Baumeister. 1996. Determination of the inelastic mean free path in ice by examination of tilted vesicles and automated most probable loss imaging. Ultramicroscopy. 63:169-179.
37. Grimm, R., H. Singh, R. Rachel, D. Typke, W. Zillig, and W. Baumeister. 1998. Electron tomography of ice-embedded prokaryotic cells. Biophys. J. 74:1031-1042.
38. Grunewald, K., O. Medalia, A. Gross, A.C. Steven, and W. Baumeister. 2003. Prospects of electron cryotomography to visualize macromolecular complexes inside cellular compartments: implications of crowding. Biophys. Chem. 100:577-591.
39. Heller, J., T.J. Ostwald, and D. Bok. 1971. The osmotic behavior of rod photoreceptor outer segment discs. J. Cell Biol. 48:633-649.
40. Henderson, R. 2004. Realizing the potential of electron cryo-microscopy. Q. Rev. Biophys. 37:3-13.
41. Holcman, D., and J.I. Korenbrot. 2004. Longitudinal diffusion in retinal rod and cone outer segment cytoplasm: the consequence of cell structure. Biophys. J. 86:2566-2582.
42. Jeon, C.J., E. Strettoi, and R.H. Masland. 1998. The major cell populations of the mouse retina. J. Neurosci. 18:8936-8946.
43. Kajimura, N., Y. Harada, and J. Usukura. 2000. High-resolution freeze-etching replica images of the disk and the plasma membrane surfaces in purified bovine rod outer segments. J. Electron Microsc. (Tokyo). 49:691-697.
44. Kedzierski, W., S. Nusinowitz, D. Birch, G. Clarke, R.R. McInnes, D. Bok, and G.H. Travis. 2001. Deficiency of rds/peripherin causes photoreceptor death in mouse models of digenic and dominant retinitis pigmentosa. Proc. Natl. Acad. Sci. USA. 98:7718-7723.
45. Korenbrot, J.I., D.T. Brown, and R.A. Cone. 1973. Membrane characteristics and osmotic behavior of isolated rod outer segments. J. Cell Biol. 56:389-398.
46. Korschen, H.G., M. Beyermann, F. Muller, M. Heck, M. Vantler, K.W. Koch, R. Kellner, U. Wolfrum, C. Bode, K.P. Hofmann, and U.B. Kaupp. 1999. Interaction of glutamic-acid-rich proteins with the cGMP signalling pathway in rod photoreceptors. Nature. 400:761-766.
47. Kota, P., P.J. Reeves, U.L. Rajbhandary, and H.G. Khorana. 2006. Opsin is present as dimers in COS1 cells: identification of amino acids at the dimeric interface. Proc. Natl. Acad. Sci. USA. 103:3054-3059.
48. Krebs, W., and H. Kuhn. 1977. Structure of isolated bovine rod outer segment membranes. Exp. Eye Res. 25:511-526.
49. Lamb, T.D., and E.N. Pugh Jr. 1992. A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. J. Physiol. 449:719-758.
50. Lasansky, A., and E. De Robertis. 1960. Electron microscopy of retinal photoreceptors. The use of chromation following formaldehyde fixation as a complementary technique to osmium tetroxide fixation. J. Biophys. Biochem. Cytol. 7:493-498.
51. Leeson, T.S. 1970. Rat retinal rods: freeze-fracture replication of outer segments. Can. J. Ophthalmol. 5:91-107.
52. Liang, Y., D. Fotiadis, S. Filipek, D.A. Saperstein, K. Palczewski, and A. Engel. 2003. Organization of the G protein-coupled receptors rhodopsin and opsin in native membranes. J. Biol. Chem. 278:21655-21662.
53. Liang, Y., D. Fotiadis, T. Maeda, A. Maeda, A. Modzelewska, S. Filipek, D.A. Saperstein, A. Engel, and K. Palczewski. 2004. Rhodopsin signaling and organization in heterozygote rhodopsin knockout mice. J. Biol. Chem. 279:48189-48196.
54. Loewen, C.J., and R.S. Molday. 2000. Disulfide-mediated oligomerization of Peripherin/Rds and Rom-1 in photoreceptor disk membranes. Implications for photoreceptor outer segment morphogenesis and degeneration. J. Biol. Chem. 275:5370-5378.
55. Lucic, V., F. Forster, and W. Baumeister. 2005. Structural studies by electron tomography: from cells to molecules. Annu. Rev. Biochem. 74:833-865.
56. Mansoor, S.E., K. Palczewski, and D.L. Farrens. 2006. Rhodopsin self-associates in asolectin liposomes. Proc. Natl. Acad. Sci. USA. 103:3060-3065.
57. Missotten, L. 1964. Ultrastructure of ocular tissue. Bull. Soc. Belge Ophtalmol. 136:3-204.
58. Miyaguchi, K., C.H. Kuo, N. Miki, and P.H. Hashimoto. 1992. Topography of opsin within disk and plasma membranes revealed by a rapid-freeze deepetch technique. J. Neurocytol. 21:807-819.
59. Moody, M.F., and J.D. Robertson. 1960. The fine structure of some retinal photoreceptors. J. Biophys. Biochem. Cytol. 7:87-92.
60. Nickell, S., R. Hegerl, W. Baumeister, and R. Rachel. 2003. Pyrodictium cannulae enter the periplasmic space but do not enter the cytoplasm, as revealed by cryo-electron tomography. J. Struct. Biol. 141:34-42.
61. Nickell, S., F. Forster, A. Linaroudis, W.D. Net, F. Beck, R. Hegerl, W. Baumeister, and J.M. Plitzko. 2005. TOM software toolbox: acquisition and analysis for electron tomography. J. Struct. Biol. 149:227-234.
62. Nickell, S., C. Kofler, A.P. Leis, and W. Baumeister. 2006. A visual approach to proteomics. Nat. Rev. Mol. Cell Biol. 7:225-230.
63. Nilsson, S.E. 1965. The ultrastructure of the receptor outer segments in the retina of the leopard frog (Rana Pipiens). J. Ultrastruct. Res. 12:207-231.
64. Nir, I., and M.O. Hall. 1974. The ultrastructure of lipid-depleted rod photoreceptor membranes. J. Cell Biol. 63:587-598.
65. Nir, I., and D.C. Pease. 1973. Ultrastructural aspects of discs in rod outer segments. Exp. Eye Res. 16:173-182.
66. Nir, I., and D.C. Pease. 1975. Substructure in rod photoreceptor membranes. Anat. Rec. 182:15-27.
67. Palczewski, K. 2006. G protein-coupled receptor rhodopsin. Annu. Rev. Biochem. 75:743-767.
68. Papermaster, D.S., B.G. Schneider, M.A. Zorn, and J.P. Kraehenbuhl. 1978. Immunocytochemical localization of a large intrinsic membrane protein to the incisures and margins of frog rod outer segment disks. J. Cell Biol. 78:415-425.
69. Park, P.S.-H., S. Filipek, J.W. Wells, and K. Palczewski. 2004. Oligomerization of G protein-coupled receptors: past, present, and future. Biochemistry. 43:15643-15656.
70. Peet, J.A., A. Bragin, P.D. Calvert, S.S. Nikonov, S. Mani, X. Zhao, J.C. Besharse, E.A. Pierce, B.E. Knox, and E.N. Pugh Jr. 2004. Quantification of the cytoplasmic spaces of living cells with EGFP reveals arrestin-EGFP to be in disequilibrium in dark adapted rod photoreceptors. J. Cell Sci. 117:3049-3059.
71. Poetsch, A., L.L. Molday, and R.S. Molday. 2001. The cGMP-gated channel and related glutamic acid-rich proteins interact with peripherin-2 at the rim region of rod photoreceptor disc membranes. J. Biol. Chem. 276:48009-48016.
72. 2+-binding proteins in the retina. Trends Neurosci. 19:547-554.
73. Roof, D.J., and J.E. Heuser. 1982. Surfaces of rod photoreceptor disk membranes: integral membrane components. J. Cell Biol. 95:487-500.
74. Rosenkranz, J. 1970. On the fine structure of the frog's rod outer segments, observed by the freeze-etching technique. Z. Zellforsch. Mikrosk. Anat. 111:228-262.
75. Rosenkranz, J. 1977. New aspects of the ultrastructure of frog rod outer segments. Int. Rev. Cytol. 50:25-158.
76. Sjostrand, F.S. 1949. An electron microscope study of the retinal rods of the guinea pig eye. J. Cell. Comp. Physiol. 33:383-403.
77. Sjostrand, F.S. 1953. The ultrastructure of the outer segments of rods and cones of the eye as revealed by the electron microscope. J. Cell. Comp. Physiol. 42:15-44.
78. Sjostrand, F.S., and S.E. Nilsson. 1964. The structure of the rabbit retina as revealed by electron microscopy. In The Rabbit in Eye Research. J.H. Prince, editor. Charles C. Thomas, Springfield, IL. 449-513.
79. Tanuj Sapra, K., P.S. Park, S. Filipek, A. Engel, D.J. Muller, and K. Palczewski. 2006. Detecting molecular interactions that stabilize native bovine rhodopsin. J. Mol. Biol. 358:255-269.
80. Tonosaki, A., M. Yamasaki, H. Washioka, and J. Mizoguchi. 1980. Complementary freeze fracture methods applied to cattle disk membranes. Arch. Histol. Jpn. 43:115-126.
81. Townes-Anderson, E., R.F. Dacheux, and E. Raviola. 1988. Rod photoreceptors dissociated from the adult rabbit retina. J. Neurosci. 8:320-331.
82. Usukura, J., and E. Yamada. 1981. Molecular organization of the rod outer segment. A deep-etching study with rapid freezing using unfixed frog retina. Biomed. Res. 2:177-193.
83. Wald, G., P.K. Brown, and I.R. Gibbons. 1963. The problem of visual excitation. J. Opt. Soc. Am. 53:20-35.
84. Webb, N.G. 1972. X-ray diffraction from outer segments of visual cells in intact eyes of the frog. Nature. 235:44-46.
85. Wolken, J.J. 1957. A comparative study of photoreceptors. Trans. NY Acad. Sci. 19:315-327.