Home LiteratureArticle Details
PMID: 20855501 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

The cell biology of vision.

The Journal of cell biology ·Vol. 190 ·No. 6 ·2010-09-20 ·Pages 953-63

Sung CH, Chuang JZ

Abstract

Humans possess the remarkable ability to perceive color, shape, and motion, and to differentiate between light intensities varied by over nine orders of magnitude. Phototransduction--the process in which absorbed photons are converted into electrical responses--is the first stage of visual processing, and occurs in the outer segment, the light-sensing organelle of the photoreceptor cell. Studies of genes linked to human inherited blindness have been crucial to understanding the biogenesis of the outer segment and membrane-trafficking of photoreceptors.

MeSH Terms
Animals Cellular Senescence Eye/cytology Humans Morphogenesis Retinal Rod Photoreceptor Cells/cytology,ultrastructure Rhodopsin/metabolism Vision, Ocular/physiology
Chemicals
Rhodopsin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Sung Ching-Hwa
Dyson Vision Research Institute, Department of Ophthalmology, Weill Cornell Medical College, New York, NY 10065, USA. [email protected]
Chuang Jen-Zen
References (99)
99 references, click to expand
  1. Submicroscopic organization of retinal cones of the rabbit.
    J Biophys Biochem Cytol. 1958 Nov 25;4(6):743-6 PMID: 13610938
  2. Phototransduction motifs and variations.
    Cell. 2009 Oct 16;139(2):246-64 PMID: 19837030
  3. The outer segment serves as a default destination for the trafficking of membrane proteins in photoreceptors.
    J Cell Biol. 2008 Nov 3;183(3):485-98 PMID: 18981232
  4. Chloride intracellular channel 4 is critical for the epithelial morphogenesis of RPE cells and retinal attachment.
    Mol Biol Cell. 2010 Sep 1;21(17):3017-28 PMID: 20610659
  5. Progressive photoreceptor degeneration, outer segment dysplasia, and rhodopsin mislocalization in mice with targeted disruption of the retinitis pigmentosa-1 (Rp1) gene.
    Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5698-703 PMID: 11960024
  6. Rod outer segment disk shedding in rat retina: relationship to cyclic lighting.
    Science. 1976 Dec 3;194(4269):1071-4 PMID: 982063
  7. Morphogenesis of the photoreceptor outer segment during postnatal development in the mouse (BALB/c) retina.
    Cell Tissue Res. 1992 Jul;269(1):39-48 PMID: 1423483
  8. A novel Usher protein network at the periciliary reloading point between molecular transport machineries in vertebrate photoreceptor cells.
    Hum Mol Genet. 2008 Jan 1;17(1):71-86 PMID: 17906286
  9. Transcriptome analysis of the retina.
    Genome Biol. 2002 Jul 30;3(8):REVIEWS1022 PMID: 12186651
  10. Procion yellow: a marker dye for outer segment disc patency and for rod renewal.
    Exp Eye Res. 1976 Aug;23(2):139-48 PMID: 61886
  11. Photoreceptor peripherin is the normal product of the gene responsible for retinal degeneration in the rds mouse.
    Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):723-6 PMID: 1992463
  12. Light and temperature modulated staining of the rod outer segment distal tips with Lucifer yellow.
    Invest Ophthalmol Vis Sci. 1985 May;26(5):628-35 PMID: 2581915
  13. Impaired photoreceptor protein transport and synaptic transmission in a mouse model of Bardet-Biedl syndrome.
    Vision Res. 2007 Dec;47(27):3394-407 PMID: 18022666
  14. FOVEAL RECEPTORS OF THE MONKEY RETINA: FINE STRUCTURE.
    Science. 1965 Jan 1;147(3653):57-9 PMID: 14224526
  15. Parallel processing in the mammalian retina.
    Nat Rev Neurosci. 2004 Oct;5(10):747-57 PMID: 15378035
  16. Freeze-fracture studies of photoreceptor membranes: new observations bearing upon the distribution of cholesterol.
    J Cell Biol. 1983 Sep;97(3):749-55 PMID: 6411740
  17. Kinetics of rod outer segment renewal in the developing mouse retina.
    J Cell Biol. 1973 Sep;58(3):650-61 PMID: 4747920
  18. Microtubules and actin filaments in teleost visual cone elongation and contraction.
    J Supramol Struct. 1976;5(3):257-75 PMID: 1035780
  19. Disulfide-mediated oligomerization of Peripherin/Rds and Rom-1 in photoreceptor disk membranes. Implications for photoreceptor outer segment morphogenesis and degeneration.
    J Biol Chem. 2000 Feb 25;275(8):5370-8 PMID: 10681511
  20. Intersegmental fusion in vertebrate rod photoreceptors. Rod cell structure revisited.
    Invest Ophthalmol Vis Sci. 1995 Aug;36(9):1918-33 PMID: 7635665
  21. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells.
    Proc Natl Acad Sci U S A. 1997 Nov 11;94(23):12425-30 PMID: 9356465
  22. The renewal of photoreceptor cell outer segments.
    J Cell Biol. 1967 Apr;33(1):61-72 PMID: 6033942
  23. Role of subunit assembly in autosomal dominant retinitis pigmentosa linked to mutations in peripherin 2.
    Novartis Found Symp. 2004;255:95-112; discussion 113-6, 177-8 PMID: 14750599
  24. Essential role of nephrocystin in photoreceptor intraflagellar transport in mouse.
    Hum Mol Genet. 2009 May 1;18(9):1566-77 PMID: 19208653
  25. Mutant prominin 1 found in patients with macular degeneration disrupts photoreceptor disk morphogenesis in mice.
    J Clin Invest. 2008 Aug;118(8):2908-16 PMID: 18654668
  26. Responses of retinal rods to single photons.
    J Physiol. 1979 Mar;288:613-34 PMID: 112243
  27. Photoreceptor IFT complexes containing chaperones, guanylyl cyclase 1 and rhodopsin.
    Traffic. 2009 Jun;10(6):648-63 PMID: 19302411
  28. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis.
    Cell. 2007 Jun 15;129(6):1201-13 PMID: 17574030
  29. Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4.
    EMBO J. 2009 Feb 4;28(3):183-92 PMID: 19153612
  30. Digenic retinitis pigmentosa due to mutations at the unlinked peripherin/RDS and ROM1 loci.
    Science. 1994 Jun 10;264(5165):1604-8 PMID: 8202715
  31. Intraflagellar transport.
    Nat Rev Mol Cell Biol. 2002 Nov;3(11):813-25 PMID: 12415299
  32. ENERGY, QUANTA, AND VISION.
    J Gen Physiol. 1942 Jul 20;25(6):819-40 PMID: 19873316
  33. Rom-1 is required for rod photoreceptor viability and the regulation of disk morphogenesis.
    Nat Genet. 2000 May;25(1):67-73 PMID: 10802659
  34. Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa.
    Nat Genet. 2000 Nov;26(3):270-1 PMID: 11062461
  35. Loss of the cholesterol-binding protein prominin-1/CD133 causes disk dysmorphogenesis and photoreceptor degeneration.
    J Neurosci. 2009 Feb 18;29(7):2297-308 PMID: 19228982
  36. Analysis of a zebrafish dync1h1 mutant reveals multiple functions for cytoplasmic dynein 1 during retinal photoreceptor development.
    Neural Dev. 2010 Apr 22;5:12 PMID: 20412557
  37. Disc morphogenesis in vertebrate photoreceptors.
    J Comp Neurol. 1980 Apr 1;190(3):501-8 PMID: 6771304
  38. SARA-regulated vesicular targeting underlies formation of the light-sensing organelle in mammalian rods.
    Cell. 2007 Aug 10;130(3):535-47 PMID: 17693260
  39. Overexpression of rhodopsin alters the structure and photoresponse of rod photoreceptors.
    Biophys J. 2009 Feb;96(3):939-50 PMID: 19186132
  40. Rhodopsin transport in the membrane of the connecting cilium of mammalian photoreceptor cells.
    Cell Motil Cytoskeleton. 2000 Jun;46(2):95-107 PMID: 10891855
  41. Surfaces of rod photoreceptor disk membranes: integral membrane components.
    J Cell Biol. 1982 Nov;95(2 Pt 1):487-500 PMID: 6815210
  42. FAPP2 is involved in the transport of apical cargo in polarized MDCK cells.
    J Cell Biol. 2005 Aug 15;170(4):521-6 PMID: 16103222
  43. Some observations on the ultrastructure and morphogenesis of photoreceptors.
    J Gen Physiol. 1960 Jul;43(6)Suppl:1-13 PMID: 13814989
  44. Microtubule polarity and distribution in teleost photoreceptors.
    J Neurosci. 1988 Jul;8(7):2371-80 PMID: 3249231
  45. A photoreceptor-specific cadherin is essential for the structural integrity of the outer segment and for photoreceptor survival.
    Neuron. 2001 Dec 6;32(5):775-86 PMID: 11738025
  46. Peripherin. A rim-specific membrane protein of rod outer segment discs.
    Invest Ophthalmol Vis Sci. 1987 Jan;28(1):50-61 PMID: 2433249
  47. Further studies on the question of the patency of saccules in outer segments of vertebrate photoreceptors.
    Vision Res. 1970 Jun;10(6):445-53 PMID: 4099086
  48. Membrane assembly in retinal photoreceptors. III. Distinct membrane domains of the connecting cilium of developing rods.
    J Neurosci. 1985 Apr;5(4):1035-48 PMID: 3156973
  49. The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance.
    J Cell Biol. 2002 Apr 1;157(1):103-13 PMID: 11916979
  50. The carboxyl-terminal domain is essential for rhodopsin transport in rod photoreceptors.
    Vision Res. 2002 Feb;42(4):417-26 PMID: 11853757
  51. Circadian nature of rod outer segment disc shedding in the rat.
    Invest Ophthalmol Vis Sci. 1980 Apr;19(4):407-11 PMID: 7358492
  52. Plasticity of retinal ribbon synapses.
    Microsc Res Tech. 1996 Dec 15;35(6):472-87 PMID: 9016450
  53. Peripherin/rds influences membrane vesicle morphology. Implications for retinopathies.
    J Biol Chem. 2000 May 5;275(18):13191-4 PMID: 10747861
  54. Functional dissection of Rab GTPases involved in primary cilium formation.
    J Cell Biol. 2007 Jul 30;178(3):363-9 PMID: 17646400
  55. Transgenic animal studies of human retinal disease caused by mutations in peripherin/rds.
    Adv Exp Med Biol. 2006;572:141-6 PMID: 17249567
  56. Trafficking of membrane proteins to cone but not rod outer segments is dependent on heterotrimeric kinesin-II.
    J Neurosci. 2009 Nov 11;29(45):14287-98 PMID: 19906976
  57. Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans.
    J Cell Biol. 2006 Feb 27;172(5):663-9 PMID: 16492809
  58. Bbs2-null mice have neurosensory deficits, a defect in social dominance, and retinopathy associated with mislocalization of rhodopsin.
    Proc Natl Acad Sci U S A. 2004 Nov 23;101(47):16588-93 PMID: 15539463
  59. Prevention of rod disk shedding by detachment from the retinal pigment epithelium.
    Invest Ophthalmol Vis Sci. 1987 Jan;28(1):184-7 PMID: 3804649
  60. A role for the Tubby-like protein 1 in rhodopsin transport.
    Invest Ophthalmol Vis Sci. 2001 Aug;42(9):1955-62 PMID: 11481257
  61. Morphogenesis of the retinal rods; an electron microscope study.
    J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):209-18 PMID: 13357544
  62. Dark adaptation and the retinoid cycle of vision.
    Prog Retin Eye Res. 2004 May;23(3):307-80 PMID: 15177205
  63. Rhodopsin's carboxy-terminal cytoplasmic tail acts as a membrane receptor for cytoplasmic dynein by binding to the dynein light chain Tctex-1.
    Cell. 1999 Jun 25;97(7):877-87 PMID: 10399916
  64. Myosin VIIa participates in opsin transport through the photoreceptor cilium.
    J Neurosci. 1999 Aug 1;19(15):6267-74 PMID: 10414956
  65. Proteomics of photoreceptor outer segments identifies a subset of SNARE and Rab proteins implicated in membrane vesicle trafficking and fusion.
    Mol Cell Proteomics. 2008 Jun;7(6):1053-66 PMID: 18245078
  66. Identification of an outer segment targeting signal in the COOH terminus of rhodopsin using transgenic Xenopus laevis.
    J Cell Biol. 2000 Dec 25;151(7):1369-80 PMID: 11134067
  67. Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors.
    Cell. 2000 Jul 21;102(2):175-87 PMID: 10943838
  68. Mutant rab8 Impairs docking and fusion of rhodopsin-bearing post-Golgi membranes and causes cell death of transgenic Xenopus rods.
    Mol Biol Cell. 2001 Aug;12(8):2341-51 PMID: 11514620
  69. Photoreceptor number and outer segment disk membrane surface area in the retina of the rat: stereological data for whole organ and average photoreceptor cell.
    J Neurocytol. 1997 Jan;26(1):53-61 PMID: 9154529
  70. Timing and computation in inner retinal circuitry.
    Annu Rev Physiol. 2007;69:271-90 PMID: 17059359
  71. A rhodopsin gene mutation responsible for autosomal dominant retinitis pigmentosa results in a protein that is defective in localization to the photoreceptor outer segment.
    J Neurosci. 1994 Oct;14(10):5818-33 PMID: 7523628
  72. The renewal of protein in retinal rods and cones.
    J Cell Biol. 1968 Oct;39(1):169-84 PMID: 5692679
  73. Usher syndrome: molecular links of pathogenesis, proteins and pathways.
    Hum Mol Genet. 2006 Oct 15;15 Spec No 2:R262-70 PMID: 16987892
  74. RP1 is required for the correct stacking of outer segment discs.
    Invest Ophthalmol Vis Sci. 2003 Oct;44(10):4171-83 PMID: 14507858
  75. The cytoplasmic tail of rhodopsin acts as a novel apical sorting signal in polarized MDCK cells.
    J Cell Biol. 1998 Sep 7;142(5):1245-56 PMID: 9732285
  76. 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 PMID: 16639027
  77. A knockin mouse model of the Bardet-Biedl syndrome 1 M390R mutation has cilia defects, ventriculomegaly, retinopathy, and obesity.
    Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19422-7 PMID: 18032602
  78. The oligogenic properties of Bardet-Biedl syndrome.
    Hum Mol Genet. 2004 Apr 1;13 Spec No 1:R65-71 PMID: 14976158
  79. Development and degeneration of retina in rds mutant mice: ultraimmunohistochemical localization of opsin.
    Exp Eye Res. 1987 Mar;44(3):347-61 PMID: 2954840
  80. Intraflagellar transport genes are essential for differentiation and survival of vertebrate sensory neurons.
    Neuron. 2004 Jun 10;42(5):703-16 PMID: 15182712
  81. An outer segment localization signal at the C terminus of the photoreceptor-specific retinol dehydrogenase.
    J Neurosci. 2004 Mar 17;24(11):2623-32 PMID: 15028754
  82. Rod photoreceptors dissociated from the adult rabbit retina.
    J Neurosci. 1988 Jan;8(1):320-31 PMID: 3339415
  83. Transgenic expression of a GFP-rhodopsin COOH-terminal fusion protein in zebrafish rod photoreceptors.
    Vis Neurosci. 2002 May-Jun;19(3):257-64 PMID: 12392175
  84. Neuronal cell types.
    Curr Biol. 2004 Jul 13;14(13):R497-500 PMID: 15242626
  85. Intraflagellar transport molecules in ciliary and nonciliary cells of the retina.
    J Cell Biol. 2010 Apr 5;189(1):171-86 PMID: 20368623
  86. Outer segment disc shedding and phagocytosis in the outer retina.
    Trans Ophthalmol Soc U K. 1983;103 ( Pt 4):397-404 PMID: 6380008
  87. Photoreceptor membrane proteins, phototransduction, and retinal degenerative diseases. The Friedenwald Lecture.
    Invest Ophthalmol Vis Sci. 1998 Dec;39(13):2491-513 PMID: 9856758
  88. Photoreceptor outer segments: accelerated membrane renewal in rods after exposure to light.
    Science. 1977 Apr 29;196(4289):536-8 PMID: 300504
  89. The homodimeric kinesin, Kif17, is essential for vertebrate photoreceptor sensory outer segment development.
    Dev Biol. 2008 Apr 1;316(1):160-70 PMID: 18304522
  90. The retinitis pigmentosa GTPase regulator (RPGR)- interacting protein: subserving RPGR function and participating in disk morphogenesis.
    Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):3965-70 PMID: 12651948
  91. Usher syndrome: animal models, retinal function of Usher proteins, and prospects for gene therapy.
    Vision Res. 2008 Feb;48(3):433-41 PMID: 17936325
  92. Development and degeneration of retina in rds mutant mice: photoreceptor abnormalities in the heterozygotes.
    Exp Eye Res. 1985 Dec;41(6):701-20 PMID: 3830736
  93. Mechanisms underlying development of visual maps and receptive fields.
    Annu Rev Neurosci. 2008;31:479-509 PMID: 18558864
  94. Rhodopsin trafficking and its role in retinal dystrophies.
    Int Rev Cytol. 2000;195:215-67 PMID: 10603577
  95. Nephronophthisis-associated ciliopathies.
    J Am Soc Nephrol. 2007 Jun;18(6):1855-71 PMID: 17513324
  96. Ankyrin-G promotes cyclic nucleotide-gated channel transport to rod photoreceptor sensory cilia.
    Science. 2009 Mar 20;323(5921):1614-7 PMID: 19299621
  97. The role of subunit assembly in peripherin-2 targeting to rod photoreceptor disk membranes and retinitis pigmentosa.
    Mol Biol Cell. 2003 Aug;14(8):3400-13 PMID: 12925772
  98. Turnover of mouse photoreceptor outer segments in constant light and darkness.
    Invest Ophthalmol Vis Sci. 1979 Oct;18(10):1019-24 PMID: 478775
  99. Mouse photoreceptor synaptic ribbons lose and regain material in response to illumination changes.
    Eur J Neurosci. 2004 Mar;19(6):1559-71 PMID: 15066152
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
1540-8140
Published
2010-09-20
Pages
953-63
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC3101587
Subset
IM
Grants
NEI NIH HHS · EY11307 · United States
NEI NIH HHS · R24 EY015656 · United States
NEI NIH HHS · R01 EY011307 · United States
NEI NIH HHS · EY015656 · United States
NEI NIH HHS · EY016805 · United States
NEI NIH HHS · R01 EY016805 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]