Kinesin-2: A family of heterotrimeric and homodimeric motors with diverse intracellular transport functions

Annual Review of Cell and Developmental Biology

Volumn 29, Issue , 2013, Pages 443-469

  Scholey, Jonathan M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cilium biogenesis; heterotrimeric kinesin 2; homodimeric kinesin 2; intracellular transport; microtubule based motor proteins

Indexed keywords

HETEROTRIMERIC KINESIN 2; HOMODIMERIC KINESIN 2; KINESIN 2; OLIGOMER; PROTEIN KAP; UNCLASSIFIED DRUG; KINESIN; MOLECULAR MOTOR;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CYTOKINESIS; DIMERIZATION; EUKARYOTE; INTRACELLULAR TRANSPORT; MITOSIS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN SUBUNIT; REVIEW; RNA TRANSPORT; ANIMAL; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR EVOLUTION; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; EVOLUTION, MOLECULAR; HUMANS; KINESIN; MOLECULAR MOTOR PROTEINS;

EID: 84885774512     PISSN: 10810706     EISSN: 15308995     Source Type: Book Series    
DOI: 10.1146/annurev-cellbio-101512-122335     Document Type: Review

References (154)

1. AizawaH, Sekine Y, Takemura R, Zhang Z, NangakuM,HirokawaN. 1992. Kinesin family in murine central nervous system. J. Cell Biol. 119:1287-96
2. Avasthi P,Watt CB, Williams DS, Le YZ, Li S, et al. 2009. Trafficking of membrane proteins to cone but not rod outer segments is dependent on heterotrimeric kinesin-II. J. Neurosci. 29:14287-98
3. Awan A, BernsteinM, Hamasaki T, Satir P. 2004. Cloning and characterization of Kin5, a novel Tetrahymena ciliary kinesin II. Cell Motil. Cytoskelet. 58:1-9
4. Berezuk MA, Schroer TA. 2004. Fractionation and characterization of kinesin II species in vertebrate brain. Traffic 5:503-13
5. Berezuk MA, Schroer TA. 2007. Dynactin enhances the processivity of kinesin-2. Traffic 8:124-29
6. Betley JN, Heinrich B, Vernos I, Sardet C, Prodon F, Deshler JO. 2004. Kinesin II mediates Vg1 mRNA transport in Xenopus oocytes. Curr. Biol. 14:219-24
7. Bieling P, Kronja I, Surrey T. 2010. Microtubule motility on reconstituted meiotic chromatin. Curr. Biol. 20:763-69
8. Brown CL, Maier KC, Stauber T, Ginkel LM, Wordeman L, et al. 2005. Kinesin-2 is a motor for late endosomes and lysosomes. Traffic 6:1114-24
9. Brown JM, Marsala C, Kosoy R, Gaertig J. 1999. Kinesin-II is preferentially targeted to assembling cilia and is required for ciliogenesis and normal cytokinesis in Tetrahymena. Mol. Biol. Cell 10:3081-96
10. Brunnbauer M, Dombi R, Ho TH, Schliwa M, Rief M, Okten Z. 2012. Torque generation of kinesin motors is governed by the stability of the neck domain. Mol. Cell 46:147-58
11. Brunnbauer M, Mueller-Planitz F, Kosem S, Ho TH, Dombi R, et al. 2010. Regulation of a heterodimeric kinesin-2 through an unprocessive motor domain that is turned processive by its partner. Proc. Natl. Acad. Sci. USA 107:10460-65
12. Burghoorn J, Dekkers MP, Rademakers S, de Jong T, Willemsen R, Jansen G. 2007. Mutation of the MAP kinase DYF-5 affects docking and undocking of kinesin-2 motors and reduces their speed in the cilia of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 104:7157-62
13. Chu P-J, Rivera JF, Arnold DB. 2006. A role for Kif17 in transport of Kv4.2. J. Biol. Chem. 281:365-73
14. Cole DG, Cande WZ, Baskin RJ, Skoufias DA, Hogan CJ, Scholey JM. 1992. Isolation of a sea urchin egg kinesin-related protein using peptide antibodies. J. Cell Sci. 101(Pt. 2):291-301
15. Cole DG, Chinn SW, Wedaman KP, Hall K, Vuong T, Scholey JM. 1993. Novel heterotrimeric kinesinrelated protein purified from sea urchin eggs. Nature 366:268-70
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. Corbit KC, Shyer AE, DowdleWE, Gaulden J, Singla V, et al. 2008. Kif3a constrains ?-catenin-dependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Nat. Cell Biol. 10:70-76
18. Cyr JL, Pfister KK, Bloom GS, Slaughter CA, Brady ST. 1991. Molecular genetics of kinesin light chains: generation of isoforms by alternative splicing. Proc. Natl. Acad. Sci. USA 88:10114-18
19. de Cuevas M, Tao T, Goldstein LS. 1992. Evidence that the stalk of Drosophila kinesin heavy chain is an a-helical coiled coil. J. Cell Biol. 116:957-65
20. De Marco V, Burkhard P, Le Bot N, Vernos I, Hoenger A. 2001. Analysis of heterodimer formation by Xklp3A/B, a newly cloned kinesin-II from Xenopus laevis. EMBO J. 20:3370-79
21. De Marco V, De Marco A, Goldie KN, Correia JJ, Hoenger A. 2003. Dimerization properties of a Xenopus laevis kinesin-II carboxy-terminal stalk fragment. EMBO Rep. 4:717-22
22. Deacon SW, Nascimento A, Serpinskaya AS, Gelfand VI. 2005. Regulation of bidirectional melanosome transport by organelle bound MAP kinase. Curr. Biol. 15:459-63
23. Deacon SW, Serpinskaya AS, Vaughan PS, Lopez Fanarraga M, Vernos I, et al. 2003. Dynactin is required for bidirectional organelle transport. J. Cell Biol. 160:297-301
24. Dishinger JF, Kee HL, Jenkins PM, Fan S, Hurd TW, et al. 2010. Ciliary entry of the kinesin-2 motor KIF17 is regulated by importin-?2 and RanGTP. Nat. Cell Biol. 12:703-10
25. Doodhi H, Ghosal D, Krishnamurthy M, Jana SC, Shamala D, et al. 2009. KAP, the accessory subunit of kinesin-2, binds the predicted coiled-coil stalk of the motor subunits. Biochemistry 48:2248-60
26. Doodhi H, Jana SC, Devan P, Mazumdar S, Ray K. 2012. Biochemical and molecular dynamic simulation analysis of a weak coiled coil association between kinesin-II stalks. PLoS ONE 7:e45981
27. Drummond IA. 2012. Cilia functions in development. Curr. Opin. Cell Biol. 24:24-30
28. Evans JE, Snow JJ, Gunnarson AL, Ou G, Stahlberg H, et al. 2006. Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans. J. Cell Biol. 172:663-69
29. Fan J, Beck KA. 2004. A role for the spectrin superfamily member Syne-1 and kinesin II in cytokinesis. J. Cell Sci. 117:619-29
30. Fan S, Hurd TW, Liu CJ, Straight SW, Weimbs T, et al. 2004. Polarity proteins control ciliogenesis via kinesin motor interactions. Curr. Biol. 14:1451-61
31. Gaudin R, de Alencar BC, Jouve M, Berre S, Le Bouder E, et al. 2012. Critical role for the kinesin KIF3A in the HIV life cycle in primary human macrophages. J. Cell Biol. 199:467-79
32. Gindhart JG Jr, Goldstein LS. 1996. Armadillo repeats in the SpKAP115 subunit of kinesin-II. Trends Cell Biol. 6:415-16
33. Ginkel LM,Wordeman L. 2000. Expression and partial characterization of kinesin-related proteins in differentiating and adult skeletal muscle. Mol. Biol. Cell 11:4143-58
34. Goldstein LS, Yang Z. 2000. Microtubule-based transport systems in neurons: The roles of kinesins and dyneins. Annu. Rev. Neurosci. 23:39-71
35. Guillaud L, Setou M, Hirokawa N. 2003. KIF17 dynamics and regulation of NR2B trafficking in hippocampal neurons. J. Neurosci. 23:131-40
36. Guillaud L, Wong R, Hirokawa N. 2008. Disruption of KIF17-Mint1 interaction by CaMKII-dependent phosphorylation: A molecular model of kinesin-cargo release. Nat. Cell Biol. 10:19-29
37. Hammond JW, Blasius TL, Soppina V, CaiD, Verhey KJ. 2010. Autoinhibition of the kinesin-2 motor KIF17 via dual intramolecular mechanisms. J. Cell Biol. 189:1013-25
38. Hao L, Efimenko E, Swoboda P, Scholey JM. 2011a. The retrograde IFT machinery of C. elegans cilia: Two IFT dynein complexes? PLoS ONE 6:e20995
39. Hao L,Thein M, Brust-Mascher I, Civelekoglu-ScholeyG, Lu Y, et al. 2011b. Intraflagellar transport delivers tubulin isotypes to sensory cilium middle and distal segments. Nat. Cell Biol. 13:790-98
40. Haraguchi K, Hayashi T, Jimbo T, Yamamoto T, Akiyama T. 2006. Role of the kinesin-2 family protein, KIF3, during mitosis. J. Biol. Chem. 281:4094-99
41. Hendricks AG, Holzbaur EL, Goldman YE. 2012. Force measurements on cargoes in living cells reveal collective dynamics of microtubule motors. Proc. Natl. Acad. Sci. USA 109:18447-52
42. Henson JH, Cole DG, Terasaki M, Rashid D, Scholey JM. 1995. Immunolocalization of the heterotrimeric kinesin-related protein KRP(85/95) in themitotic apparatus of sea urchin embryos. Dev. Biol. 171:182-94
43. Hirokawa N. 2000. Stirring up development with the heterotrimeric kinesin KIF3. Traffic 1:29-34
44. Hirokawa N, Noda Y, Tanaka Y, Niwa S. 2009. Kinesin superfamily motor proteins and intracellular transport. Nat. Rev. Mol. Cell Biol. 10:682-96
45. Hirokawa N, Pfister KK, Yorifuji H, Wagner MC, Brady ST, Bloom GS. 1989. Submolecular domains of bovine brain kinesin identified by electron microscopy andmonoclonal antibody decoration. Cell 56:867-78
46. Hirokawa N, Tanaka Y, Okada Y. 2012. Cilia, KIF3 molecular motor and nodal flow. Curr. Opin. Cell Biol. 24:31-39
47. Hoeng JC, Dawson SC, House SA, Sagolla MS, Pham JK, et al. 2008. High-resolution crystal structure and in vivo function of a kinesin-2 homologue in Giardia intestinalis. Mol. Biol. Cell 19:3124-37
48. Huang B, RifkinMR, Luck DJ. 1977. Temperature-sensitive mutations affecting flagellar assembly and function in Chlamydomonas reinhardtii. J. Cell Biol. 72:67-85
49. Huang CF, Banker G. 2011. The translocation selectivity of the kinesins that mediate neuronal organelle transport. Traffic 13:549-64
50. Huang CJ, Huang CC, Chang CC. 2012. Association of the testis-specific TRIM/RBCC protein RNF33/TRIM60 with the cytoplasmicmotor proteins KIF3A and KIF3B. Mol. Cell. Biochem. 360:121-31
51. Imanishi M, Endres NF, Gennerich A, Vale RD. 2006. Autoinhibition regulates the motility of the C. Elegans intraflagellar transport motor OSM-3. J. Cell Biol. 174:931-37
52. Insinna C, Besharse JC. 2008. Intraflagellar transport and the sensory outer segment of vertebrate photoreceptors. Dev. Dyn. 237:1982-92
53. Insinna C, HumbyM, Sedmak T,Wolfrum U, Besharse JC. 2009. Different roles for KIF17 and kinesin II in photoreceptor development and maintenance. Dev. Dyn. 238:2211-22
54. Ishikawa H, Marshall WF. 2011. Ciliogenesis: building the cell's antenna. Nat. Rev. Mol. Cell Biol. 12:222-34
55. Jana SC, Girotra M, Ray K. 2011. Heterotrimeric kinesin-II is necessary and sufficient to promote different stepwise assembly of morphologically distinct bipartite cilia in Drosophila antenna. Mol. Biol. Cell 22:769-81
56. Jaulin F, Kreitzer G. 2010. KIF17 stabilizes microtubules and contributes to epithelial morphogenesis by acting at MT plus ends with EB1 and APC. J. Cell Biol. 190:443-60
57. Jenkins PM, Hurd TW, Zhang L, McEwen DP, Brown RL, et al. 2006. Ciliary targeting of olfactory CNG channels requires the CNGB1b subunit and the kinesin-2 motor protein, KIF17. Curr. Biol. 16:1211-16
58. Jimbo T, Kawasaki Y, Koyama R, Sato R, Takada S, et al. 2002. Identification of a link between the tumour suppressor APC and the kinesin superfamily. Nat. Cell Biol. 4:323-27
59. Jimeno D, Feiner L, Lillo C, Teofilo K, Goldstein LS, et al. 2006. Analysis of kinesin-2 function in photoreceptor cells using synchronous Cre-loxP knockout of Kif3a with RHO-Cre. Investig. Ophthalmol. Vis. Sci. 47:5039-46
60. Jolly AL, Gelfand VI. 2011. Bidirectional intracellular transport: utility and mechanism. Biochem. Soc. Trans. 39:1126-30
61. Keil R, Kiessling C, Hatzfeld M. 2009. Targeting of p0071 to the midbody depends on KIF3. J. Cell Sci. 122:1174-83
62. Khan ML, Ali MY, Siddiqui ZK, Shakir MA, Ohnishi H, et al. 2000. C. elegans KLP-11/OSM-3/KAP-1: orthologs of the sea urchin kinesin-II, and mouse KIF3A/KIFB/KAP3 kinesin complexes. DNA Res. 7:121-25
63. Kodani A, Sirerol-Piquer MS, Seol A, Garcia-Verdugo JM, Reiter JF. 2013. Kif3a interacts with dynactin subunit p150Glued to organize centriole subdistal appendages. EMBO J. 32:597-607
64. Kolpakova-Hart E, JinninM,Hou B, FukaiN,Olsen BR. 2007. Kinesin-2 controls development and patterning of the vertebrate skeleton by Hedgehog-and Gli3-dependent mechanisms. Dev. Biol. 309:273-84
65. 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. 131:1517-27
66. Kural C, Serpinskaya AS, Chou YH, Goldman RD, Gelfand VI, Selvin PR. 2007. Tracking melanosomes inside a cell to study molecular motors and their interaction. Proc. Natl. Acad. Sci. USA 104:5378-82
67. Laib JA, Marin JA, Bloodgood RA, Guilford WH. 2009. The reciprocal coordination and mechanics of molecular motors in living cells. Proc. Natl. Acad. Sci. USA 106:3190-95
68. Larson AG, Landahl EC, Rice SE. 2009. Mechanism of cooperative behaviour in systems of slow and fast molecular motors. Phys. Chem. Chem. Phys. 11:4890-98
69. Lawrence CJ, Dawe RK, Christie KR, Cleveland DW, Dawson SC, et al. 2004. A standardized kinesin nomenclature. J. Cell Biol. 167:19-22
70. Le Bot N, Antony C, White J, Karsenti E, Vernos I. 1998. Role of xklp3, a subunit of the Xenopus kinesin II heterotrimeric complex, in membrane transport between the endoplasmic reticulum and the Golgi apparatus. J. Cell Biol. 143:1559-73
71. Levi V, Serpinskaya AS, Gratton E, Gelfand V. 2006. Organelle transport along microtubules in Xenopus melanophores: Evidence for cooperation between multiple motors. Biophys. J. 90:318-27
72. Li X, Lipowsky R, Kierfeld, J. 2013. Bifurcation of velocity distributions in cooperative transport of filaments by fast and slow motors. Biophys. J. 104:666-76
73. Lopes VS, Jimeno D, Khanobdee K, Song X, Chen B, et al. 2010. Dysfunction of heterotrimeric kinesin-2 in rod photoreceptor cells and the role of opsin mislocalization in rapid cell death. Mol. Biol. Cell 21:4076-88
74. Lukong KE, Richard S. 2008. Breast tumor kinase BRK requires kinesin-2 subunit KAP3A in modulation of cell migration. Cell. Signal. 20:432-42
75. Malicki J. 2012. Who drives the ciliary highway? BioArchitecture 2:111-17
76. Malicki J, Besharse JC. 2012. Kinesin-2 family motors in the unusual photoreceptor cilium. Vis. Res. 75:33-36
77. MarandeW, Kohl L. 2011. Flagellar kinesins in protists. Future Microbiol. 6:231-46
78. Marshall WF. 2008. The cell biological basis of ciliary disease. J. Cell Biol. 180:17-21
79. Marszalek JR, Goldstein LS. 2000. Understanding the functions of kinesin-II. Biochim. Biophys. Acta 1496:142-50
80. Marszalek JR, Liu X, Roberts EA, Chui D, Marth JD, et al. 2000. Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102:175-87
81. Marszalek JR, Ruiz-Lozano P, Roberts E, Chien KR,Goldstein LS. 1999. Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc. Natl. Acad. Sci. USA 96:5043-48
82. Mattie FJ, Stackpole MM, Stone MC, Clippard JR, Rudnick DA, et al. 2010. Directed microtubule growth, +TIPs, and kinesin-2 are required for uniform microtubule polarity in dendrites. Curr. Biol. 20:2169-77
83. Messitt TJ,Gagnon JA, Kreiling JA, PrattCA, Yoon YJ, Mowry KL. 2008. Multiple kinesinmotors coordinate cytoplasmic RNA transport on a subpopulation of microtubules in Xenopus oocytes. Dev. Cell 15:426-36
84. MillerMS, Esparza JM, Lippa AM, LuxFGIII, Cole DG, Dutcher SK. 2005. Mutant kinesin-2motor subunits increase chromosome loss. Mol. Biol. Cell 16:3810-20
85. Morris RL, Hoffman MP, Obar RA, McCafferty SS, Gibbons IR, et al. 2006. Analysis of cytoskeletal and motility proteins in the sea urchin genome assembly. Dev. Biol. 300:219-37
86. 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. 138:1009-22
87. Jolly AL, Gelfand VI. 2011. Bidirectional intracellular transport: utility and mechanism. Biochem. Soc. Trans. 39:1126-30
88. Keil R, Kiessling C, Hatzfeld M. 2009. Targeting of p0071 to the midbody depends on KIF3. J. Cell Sci. 122:1174-83
89. Khan ML, Ali MY, Siddiqui ZK, Shakir MA, Ohnishi H, et al. 2000. C. elegans KLP-11/OSM-3/KAP-1: orthologs of the sea urchin kinesin-II, and mouse KIF3A/KIFB/KAP3 kinesin complexes. DNA Res. 7:121-25
90. Kodani A, Sirerol-Piquer MS, Seol A, Garcia-Verdugo JM, Reiter JF. 2013. Kif3a interacts with dynactin subunit p150Glued to organize centriole subdistal appendages. EMBO J. 32:597-607
91. Kolpakova-Hart E, JinninM,Hou B, FukaiN,Olsen BR. 2007. Kinesin-2 controls development and patterning of the vertebrate skeleton by Hedgehog-and Gli3-dependent mechanisms. Dev. Biol. 309:273-84
92. 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. 131:1517-27
93. Kural C, Serpinskaya AS, Chou YH, Goldman RD, Gelfand VI, Selvin PR. 2007. Tracking melanosomes inside a cell to study molecular motors and their interaction. Proc. Natl. Acad. Sci. USA 104:5378-82
94. Laib JA, Marin JA, Bloodgood RA, Guilford WH. 2009. The reciprocal coordination and mechanics of molecular motors in living cells. Proc. Natl. Acad. Sci. USA 106:3190-95
95. Larson AG, Landahl EC, Rice SE. 2009. Mechanism of cooperative behaviour in systems of slow and fast molecular motors. Phys. Chem. Chem. Phys. 11:4890-98
96. Lawrence CJ, Dawe RK, Christie KR, Cleveland DW, Dawson SC, et al. 2004. A standardized kinesin nomenclature. J. Cell Biol. 167:19-22
97. Le Bot N, Antony C, White J, Karsenti E, Vernos I. 1998. Role of xklp3, a subunit of the Xenopus kinesin II heterotrimeric complex, in membrane transport between the endoplasmic reticulum and the Golgi apparatus. J. Cell Biol. 143:1559-73
98. Levi V, Serpinskaya AS, Gratton E, Gelfand V. 2006. Organelle transport along microtubules in Xenopus melanophores: Evidence for cooperation between multiple motors. Biophys. J. 90:318-27
99. Li X, Lipowsky R, Kierfeld, J. 2013. Bifurcation of velocity distributions in cooperative transport of filaments by fast and slow motors. Biophys. J. 104:666-76
100. Lopes VS, Jimeno D, Khanobdee K, Song X, Chen B, et al. 2010. Dysfunction of heterotrimeric kinesin-2 in rod photoreceptor cells and the role of opsin mislocalization in rapid cell death. Mol. Biol. Cell 21:4076-88
101. Lukong KE, Richard S. 2008. Breast tumor kinase BRK requires kinesin-2 subunit KAP3A in modulation of cell migration. Cell. Signal. 20:432-42
102. Malicki J. 2012. Who drives the ciliary highway? BioArchitecture 2:111-17
103. Malicki J, Besharse JC. 2012. Kinesin-2 family motors in the unusual photoreceptor cilium. Vis. Res. 75:33-36
104. MarandeW, Kohl L. 2011. Flagellar kinesins in protists. Future Microbiol. 6:231-46
105. Marshall WF. 2008. The cell biological basis of ciliary disease. J. Cell Biol. 180:17-21
106. Marszalek JR, Goldstein LS. 2000. Understanding the functions of kinesin-II. Biochim. Biophys. Acta 1496:142-50
107. Marszalek JR, Liu X, Roberts EA, Chui D, Marth JD, et al. 2000. Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102:175-87
108. Marszalek JR, Ruiz-Lozano P, Roberts E, Chien KR,Goldstein LS. 1999. Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc. Natl. Acad. Sci. USA 96:5043-48
109. Mattie FJ, Stackpole MM, Stone MC, Clippard JR, Rudnick DA, et al. 2010. Directed microtubule growth, +TIPs, and kinesin-2 are required for uniform microtubule polarity in dendrites. Curr. Biol. 20:2169-77
110. Messitt TJ,Gagnon JA, Kreiling JA, PrattCA, Yoon YJ, Mowry KL. 2008. Multiple kinesinmotors coordinate cytoplasmic RNA transport on a subpopulation of microtubules in Xenopus oocytes. Dev. Cell 15:426-36
111. MillerMS, Esparza JM, Lippa AM, LuxFGIII, Cole DG, Dutcher SK. 2005. Mutant kinesin-2motor subunits increase chromosome loss. Mol. Biol. Cell 16:3810-20
112. Morris RL, Hoffman MP, Obar RA, McCafferty SS, Gibbons IR, et al. 2006. Analysis of cytoskeletal and motility proteins in the sea urchin genome assembly. Dev. Biol. 300:219-37
113. 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. 138:1009-22
114. Sarpal R, Todi SV, Sivan-Loukianova E, Shirolikar S, Subramanian N, et al. 2003. Drosophila KAP interacts with the kinesin II motor subunit KLP64D to assemble chordotonal sensory cilia, but not sperm tails. Curr. Biol. 13:1687-96
115. Scholey JM. 1996. Kinesin-II, a membrane traffic motor in axons, axonemes, and spindles. J. Cell Biol. 133:1-4
116. Scholey JM. 2003. Intraflagellar transport. Annu. Rev. Cell Dev. Biol. 19:423-43
117. Schroeder HW III, Hendricks AG, Ikeda K, Shuman H, Rodionov V, et al. 2012. Force-dependent detachment of kinesin-2 biases track switching at cytoskeletal filament intersections. Biophys. J. 103:48-58
118. SetouM,Nakagawa T, SeogDH, Hirokawa N. 2000. Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288:1796-802
119. Sfakianos J, Togawa A, Maday S, Hull M, Pypaert M, et al. 2007. Par3 functions in the biogenesis of the primary cilium in polarized epithelial cells. J. Cell Biol. 179:1133-40
120. Shakir MA, Fukushige T, Yasuda H, Miwa J, Siddiqui SS. 1993. C. elegans osm-3 gene mediating osmotic avoidance behaviour encodes a kinesin-like protein. Neuroreport 4:891-94
121. Shastry S, Hancock WO. 2010. Neck linker length determines the degree of processivity in kinesin-1 and kinesin-2 motors. Curr. Biol. 20:939-43
122. Shi S-H, Cheng T, Jan LY, Jan YN. 2004. APC and GSK-3β are involved in mPar3 targeting to the nascent axon and establishment of neuronal polarity. Curr. Biol. 14:2025-32
123. Shimizu K, Kawabe H, Minami S, Honda T, Takaishi K, et al. 1996. SMAP, an Smg GDS-associating protein having arm repeats and phosphorylated by Src tyrosine kinase. J. Biol. Chem. 271:27013-17
124. Signor D, Wedaman KP, Orozco JT,Dwyer ND, Bargmann CI, et al. 1999a. Role of a classDHC1b dynein in retrograde transport of IFT motors and IFT raft particles along cilia, but not dendrites, in chemosensory neurons of living Caenorhabditis elegans. J. Cell Biol. 147:519-30
125. Signor D, Wedaman KP, Rose LS, Scholey JM. 1999b. Two heteromeric kinesin complexes in chemosensory neurons and sensory cilia of Caenorhabditis elegans. Mol. Biol. Cell 10:345-60
126. Snezhko A, Barlan K, Aranson IS, Gelfand VI. 2010. Statistics of active transport in Xenopus melanophores cells. Biophys. J. 99:3216-23
127. Snow JJ, Ou G, Gunnarson AL,Walker MR, Zhou HM, et al. 2004. Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. Nat. Cell Biol. 6:1109-13
128. Stauber T, Simpson JC, Pepperkok R, Vernos I. 2006. A role for kinesin-2 in COPI-dependent recycling between the ER and the Golgi complex. Curr. Biol. 16:2245-51
129. 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. 247:377-89
130. Takeda S, YamazakiH, SeogDH, Kanai Y,Terada S,HirokawaN. 2000. Kinesin superfamily protein 3 (KIF3) motor transports fodrin-associating vesicles important for neurite building. J. Cell Biol. 148:1255-65
131. Tanuma N, Nomura M, Ikeda M, Kasugai I, Tsubaki Y, et al. 2009. Protein phosphatase Dusp26 associates with KIF3 motor and promotes N-cadherin-mediated cell-cell adhesion. Oncogene 28:752-61
132. Tarabeux J, Champagne N, Brustein E, Hamdan FF, Gauthier J, et al. 2010. De novo truncating mutation in kinesin 17 associated with schizophrenia. Biol. Psychiatry 68:649-56
133. Teng J, Rai T, Tanaka Y, Takei Y, Nakata T, et al. 2005. The KIF3 motor transports N-cadherin and organizes the developing neuroepithelium. Nat. Cell Biol. 7:474-82
134. Trivedi D, Colin E, Louie CM, Williams DS. 2012. Live-cell imaging evidence for the ciliary transport of rod photoreceptor opsin by heterotrimeric kinesin-2. J. Neurosci. 32:10587-93
135. Tuma MC, Zill A, Le Bot N, Vernos I, Gelfand V. 1998. Heterotrimeric kinesin II is the microtubule motor protein responsible for pigment dispersion in Xenopus melanophores. J. Cell Biol. 143:1547-58
136. Vale RD. 2003. The molecular motor toolbox for intracellular transport. Cell 112:467-80
137. Vale RD, Reese TS, SheetzMP. 1985. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42:39-50
138. Verhey KJ, Dishinger J, Kee HL. 2011a. Kinesin motors and primary cilia. Biochem. Soc. Trans. 39:1120-25
139. Verhey KJ,KaulN, Soppina V. 2011b. Kinesin assembly andmovement in cells. Annu. Rev. Biophys. 40:267-88
140. Vukajlovic M, Dietz H, Schliwa M, Okten Z. 2011. How kinesin-2 forms a stalk. Mol. Biol. Cell 22:4279-87
141. Walther Z, Vashishtha M, Hall JL. 1994. The Chlamydomonas FLA10 gene encodes a novel kinesinhomologous protein. J. Cell Biol. 126:175-88
142. Wang Q, Pan J, Snell WJ. 2006. Intraflagellar transport particles participate directly in cilium-generated signaling in Chlamydomonas. Cell 125:549-62
143. Washbourne P, Bennett JE, McAllister AK. 2002. Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nat. Neurosci. 5:751-59
144. WedamanKP, MeyerDW,Rashid DJ, ColeDG,Scholey JM. 1996. Sequence and submolecular localization of the 115-kD accessory subunit of the heterotrimeric kinesin-II (KRP85/95) complex. J. Cell Biol. 132:371-80
145. Wei Q, Zhang Y, Li Y, Zhang Q, Ling K, Hu J. 2012. The BBSome controls IFT assembly and turnaround in cilia. Nat. Cell Biol. 14:950-57
146. Wickstead B, Gull K. 2006. A 'holistic' kinesin phylogeny reveals new kinesin families and predicts protein functions. Mol. Biol. Cell 17:1734-43
147. Wickstead B, Gull K, Richards TA. 2010. Patterns of kinesin evolution reveal a complex ancestral eukaryote with a multifunctional cytoskeleton. BMC Evol. Biol. 10:110
148. Williams DS. 2002. Transport to the photoreceptor outer segment by myosin VIIa and kinesin II. Vis. Res. 42:455-62
149. Wong RW, Setou M, Teng J, Takei Y, Hirokawa N. 2002. Overexpression of motor protein KIF17 enhances spatial and working memory in transgenic mice. Proc. Natl. Acad. Sci. USA 99:14500-5
150. 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 93:8443-48
151. Yang JT, Laymon RA, Goldstein LS. 1989. A three-domain structure of kinesin heavy chain revealed byDNA sequence and microtubule binding analyses. Cell 56:879-89
152. Yang Z, Goldstein LS. 1998. Characterization of the KIF3C neural kinesin-like motor from mouse. Mol. Biol. Cell 9:249-61
153. Yin X, Takei Y, Kido MA, Hirokawa N. 2011. Molecular motor KIF17 is fundamental for memory and learning via differential support of synaptic NR2A/2B levels. Neuron 70:310-25
154. Zhao C, Omori Y, Brodowska K, Kovach P, Malicki J. 2012. Kinesin-2 family in vertebrate ciliogenesis. Proc. Natl. Acad. Sci. USA 109:2388-93