The kinesin motor KIF3A is a component of the presynaptic ribbon in vertebrate photoreceptors

Journal of Neuroscience

Volumn 19, Issue 3, 1999, Pages 1027-1037

  Muresan, Virgil ^a   Lyass, Asya ^a   Schnapp, Bruce J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Bipolar cell; Connecting cilium axoneme; Intracellular traffic; Kinesin related motor KIF3A; Photoreceptor cell; Retina; Ribbon synapse

Indexed keywords

KINESIN; POLYPEPTIDE;

ANIMAL CELL; ARTICLE; AXONEME; CELL FRACTIONATION; CENTRIOLE; GENE EXPRESSION; IMMUNOELECTRON MICROSCOPY; MALE; NONHUMAN; PHOTORECEPTOR; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; RAT; RETINA; SYNAPSE VESICLE; VERTEBRATE;

EID: 0033080905     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-03-01027.1999     Document Type: Article

References (71)

1. Afshar K, Barton N R, Hawley RS, Goldstein LSB (1995) DNA binding and meiotic chromosomal localization of the Drosophila nod kinesin-like protein. Cell 81:129-138.
2. Bachman KM, Balkema GW (1993) Developmental expression of a synaptic ribbon antigen (B16) in mouse retina. J Comp Neurol 333:109-117.
3. Balkema GW (1991) A synaptic antigen (B16) is localized in retinal synaptic ribbons. J Comp Neurol 312:573-583.
4. Barthel LK, Raymond PA (1990) Improved method for obtaining 3-μm cryosections for immunocytochemistry. J Histochem Cytochem 38:1383-1388.
5. Beech PL, Pagh-Roehl K, Noda Y, Hirokawa N, Burnside B, Rosenbaum JL (1996) Localization of kinesin superfamily proteins to the connecting cilium of fish photoreceptors. J Cell Sci 109:889-897.
6. Besharse JC (1982) The daily light-dark cycle and rhythmic metabolism in the photoreceptor-pigment epithelial complex. Prog Ret Res 1:81-124.
7. Besharse JC (1986) Photosensitive membrane turnover: differentiated membrane domains and cell-cell interactions. In: The retina: a model for cell biological studies, Part I (Adler R, Farber D, eds), pp 297-352. New York: Academic.
8. Besharse JC, Horst CJ (1990) The photoreceptor connecting cilium. A model for the transition zone. In: Ciliary and flagellar membranes (Bloodgood RA, ed), pp 389-417. New York: Plenum.
9. Brady ST, Pfister KK, Bloom GS (1990) A monoclonal antibody against kinesin inhibits both anterograde and retrograde fast axonal transport in squid axoplasm. Proc Natl Acad Sci USA 87:1061-1065.
10. Braekevelt CR, Hollenberg M (1970) The development of the retina of the albino rat. Am J Anat 127:281-301.
11. Brandstatter JH, Wassle H, Betz H, Morgans CW (1996) The plasma membrane protein SNAP-25, but not syntaxin, is present at photoreceptor and bipolar cell synapses in the rat retina. Eur J Neurosci 8:823-828.
12. Burns ME, Augustine GJ (1995) Synaptic structure and function: dynamic organization yields architectural precision. Cell 83:187-194.
13. Chamberlain LH, Burgoyne RD (1996) Identification of a novel cysteine string protein variant and expression of cysteine string proteins in non-neuronal cells. J Biol Chem 271:7320-7323.
14. Cole DG, Cande WZ, Baskin RJ, Skoufias DA, Hogan CJ, Scholey JM (1992) Isolation of sea urchin egg kinesin-related protein using peptide antibodies. J Cell Sci 101:291-301.
15. Cole DG, Chinn SW, Wedaman KP, Hall K, Vuong T, Scholey JM (1993) Novel heterotrimeric kinesin-related protein purified from sea urchin eggs. Nature (Lond) 366:268-270.
16. Cole DG, Diener DR, Himelblau AL, Beech PL, Fuster JC, Rosenbaum JL (1998) Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J Cell Biol 141:993-1008.
17. Coy DL, Howard J (1994) Organelle transport and sorting in axons. Curr Opin Neurobiol 4:662-667.
18. Dowling JE (1987) The retina: an approachable part of the brain. Cambridge, MA: Harvard UP.
19. Dowling JE, Boycott BB (1966) Organization of the primate retina: electron microscopy. Proc R Soc Lond B Biol Sci 166:80-111.
20. Flock A (1964) Structure of the macula utriculi with special reference to directional interplay of sensory responses as revealed by morphological polarization. J Cell Biol 22:413-431.
21. Goodson HV, Valetti C, Kreis TE (1997) Motors and membrane traffic. Curr Opin Cell Biol 9:18-28.
22. Grabs D, Bergmann M, Urban M, Post A, Gratzl M (1996) Rab3 proteins and SNAP-25, essential components of the exocytosis machinery in conventional synapses, are absent from ribbon synapses of the mouse retina. Eur J Neurosci 8:162-168.
23. Gray EG, Pease HL (1971) On understanding the organization of the retinal receptor synapses. Brain Res 35:1-15.
24. (85/ 95) in the mitotic apparatus of sea urchin embryos. Dev Biol 171:182-194.
25. Henson JH, Cole DG, Roesener CD, Capuano S, Mendola RJ, Scholey JM (1997) The heterotrimeric motor protein kinesin-II localizes to the midpiece and flagellum of sea urchin and sand dollar sperm. Cell Motil Cytoskeleton 38:29-37.
26. Hermes B, Reuss S, Vollrath L (1992) Synaptic ribbons, spheres and intermediate structures in the developing retina. Int J Dev Neurosci 10:215-223.
27. Hirokawa N (1998) Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279:519-526.
28. Hopsu VK, Arstila AU (1964) An apparent somato-somatic synaptic structure in the pineal gland of the rat. Exp Cell Res 37:484-487.
29. Kolb H (1979) The inner plexiform layer in the retina of the cat: electron microscopic observations. J Neurocytol 8:295-329.
30. Kondo S, Sato-Yoshitake R, Noda Y, Aizawa H, Nakata T, Matsuura Y, Hirokawa N (1994) KIF3A is a new microtubule-based anterograde motor in the nerve axon. J Cell Biol 125:1095-1107.
31. Kozminski KG, Beech PL, Rosenbaum JL (1995) The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. J Cell Biol 131:1517-1527.
32. Lagnado L, Gomis A, Job C (1996) Continuous vesicle cycling in the synaptic terminal of retinal bipolar cells. Neuron 17:957-967.
33. Mandell JW, Townes-Anderson E, Czernik AJ, Cameron R, Greengard P, De Camilli P (1990) Synapsins in the vertebrate retina: absence from ribbon synapses and heterogeneous distribution among conventional synapses. Neuron 5:19-33.
34. Matthews G (1996) Synaptic exocytosis and endocytosis: capacitance measurements. Curr Opin Neurobiol 6:358-364.
35. McArdle CB, Dowling JE, Masland RH (1977) Development of outer segments and synapses in the rabbit retina. J Comp Neurol 175:253-274.
36. Morgans CW, Brandstatter JH, Kellerman J, Betz H, Wassle H (1996) A SNARE complex containing syntaxin 3 is present in ribbon synapses of the retina. J Neurosci 16:6713-6721.
37. Morris RL, Scholey JM (1997) Heterotrimeric kinesin-II is required for the assembly of motile 9 + 2 ciliary axonemes on sea urchin embryos. J Cell Biol 138:1009-1022.
38. Muresan V, Besharse JC (1994) Complex intermolecular interactions maintain a stable linkage between the photoreceptor connecting cilium axoneme and plasma membrane. Cell Motil Cytoskeleton 28:213-230.
39. Muresan V, Joshi HC, Besharse JC (1993) γ-Tubulin in differentiated cell types: localization in the vicinity of basal bodies in retinal photoreceptors and ciliated epithelia. J Cell Sci 104:1229-1237.
40. Muresan V, Godek CP, Reese TS, Schnapp BJ (1996) Plus-end motors override minus-end motors during transport of squid axon vesicles on microtubules. J Cell Biol 135:383-397.
41. Muresan V, Bendala-Tufanisco E, Hollander BA, Besharse JC (1997) Evidence for kinesin-related proteins associated with the axoneme of retinal photoreceptors. Exp Eye Res 64:895-903.
42. Muresan V, Abramson T, Lyass A, Winter D, Porro E, Hong F, Chamberlin NL, Schnapp BJ (1998) KIF3C and KIF3A form a novel neuronal heteromeric kinesin that associates with membrane vesicles. Mol Biol Cell 9:637-652.
43. Nakagawa T, Tanaka Y, Matsuoka E, Kondo S, Okada Y, Noda Y, Kanai Y, Hirokawa N (1997) Identification and classification of 16 new kinesin superfamily (KIF) proteins in mouse genome. Proc Natl Acad Sci USA 94:9654-9659.
44. Nislow C, Lombillo VA, Kuriyama R, McIntosh JR (1992) A plus-end-directed motor enzyme that moves antiparallel microtubules in vitro localizes to the interzone of mitotic spindles. Nature 359:543-547.
45. Perin MS, Johnston PA, Ozcelik T, Jahn R, Francke U, Südhof TC (1991) Structural and functional conservation of synaptotagmin (p65) in Drosophila and humans. J Biol Chem 266:615-622.
46. Perkins LA, Hedgecock EM, Thomson JN, Culotti JG (1986) Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 117:456-487.
47. Pfister KK, Wagner MC, Stenoien DA, Brady ST, Bloom GS (1989) Monoclonal antibodies to kinesin heavy and light chains stain vesicle-like structures, but not microtubules, in cultured cells. J Cell Biol 108:1453-1463.
48. Rao-Mirotznik R, Harkins AB, Buchsbaum G, Sterling P (1995) Mammalian rod terminal: architecture of a binary synapse. Neuron 14:561-569.
49. 85/95. J Mol Biol 252:157-162.
50. Raviola E, Gilula NB (1975) Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. J Cell Biol 65:192-222.
51. Redburn D (1988) Transmitter systems in the outer plexiform layer of the mammalian retina. Neurosci Res [Suppl] 8:S127-S136.
52. Sawin KE, Mitchison TJ, Wordeman LG (1992) Evidence for kinesin-related proteins in the mitotic apparatus using peptide antibodies. J Cell Sci 101:303-313.
53. Schaeffer SF, Raviola E (1978) Membrane recycling in the cone cell endings of the turtle retina. J Cell Biol 79:802-825.
54. Schaeffer SF, Raviola E, Heuser JE (1982) Membrane specializations in the outer plexiform layer of the turtle retina. J Comp Neurol 204:253-267.
55. Schmitz F, Bechmann M, Drenckhahn D (1996) Purification of synaptic ribbons, structural components of the photoreceptor active zone complex. J Neurosci 16:7109-7116.
56. Scholey JM (1996) Kinesin-II, a membrane traffic motor in axons, axonemes, and spindles. J Cell Biol 133:1-4.
57. Sjöstrand FS (1953) The ultrastructure of the retinal rod synapse of the guinea pig eye. J Appl Physiol 24:1422.
58. Sjöstrand FS (1998) Structure determines function of the retina, a neural center. 1. The synaptic ribbon complex. J Submicrosc Cytol Pathol 30:1-29.
59. Tabish M, Siddiqui ZK, Nishikawa K, Siddiqui SS (1995) Exclusive expression of C. elegans osm-3 kinesin gene in chemosensory neurons open to the external environment. J Mol Biol 247:377-389.
60. Troutt LL, Burnside B (1988) Microtubule polarity and distribution in teleost photoreceptors. J Neurosci 8:2371-2380.
61. Ulrich B, Südhof TC (1994) Distribution of synaptic markers in the retina: implications for synaptic vesicle traffic in ribbon synapses. J Physiol (Lond) 88:249-257.
62. Vale RD, Reese TS, Shcetz MP (1985) Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42:39-50.
63. Vashishtha M, Walther Z, Hall JL (1996) The kinesin-homologous protein encoded by the Chlamydomonas FLA10 gene is associated with basal bodies and centrioles. J Cell Sci 109:541-549.
64. Vernos I, Raats J, Hirano T, Heasman J, Karsenti E, Wylie C (1995) Xk1p1, a chromosomal Xenopits kinesin-like protein essential for spindle organization and chromosome positioning. Cell 81:117-127.
65. von Gersdorff H, Matthews G (1994) Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367:735-739.
66. von Gersdorff H, Matthews G (1997) Depletion and replenishment of vesicle pools at a ribbon-type synaptic terminal. J Neurosci 17:1919-1927.
67. 85/95) complex. J Cell Biol 132:371-380.
68. Yamazaki H, Nakata T, Okada Y, Hirokawa N (1995) KIF3A/B: a heterodimeric kinesin superfamily protein that works as a microtubule plus end-directed motor for membrane organelle transport. J Cell Biol 130:1387-1399.
69. Yamazaki H, Nakata T, Okada Y, Hirokawa N (1996) Cloning and characterization of KAP3: a novel kinesin superfamily-associated protein of KIF3A/3B. Proc Natl Acad Sci USA 93:8443-8448.
70. Yang Z, Goldstein LSB (1998) Characterization of the KIF3C neural kinesin-like motor from mouse. Mol Biol Cell 9:249-261.
71. Yen TJ, Li G, Schaar BT, Szilak I, Cleveland DW (1992) CENP-E is a putative kinetochore motor that accumulates just before mitosis. Nature 359:536-539.