FLA8/KIF3B phosphorylation regulates kinesin-II interaction with IFT-B to control IFT entry and turnaround

Developmental Cell

Volumn 30, Issue 5, 2014, Pages 585-597

  Liang, Yinwen ^a   Pang, Yunong ^a   Wu, Qiong ^a   Hu, Zhangfeng ^a   Han, Xue ^a   Xu, Yisheng ^a   Deng, Haiteng ^a   Pan, Junmin ^a  

^a TSINGHUA UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CRCDPK1 PROTEIN; IFT B PROTEIN; KIF3B PROTEIN; KINESIN 2; KINESIN II MOTOR SUBUNIT FLA8; PROTEIN KINASE; UNCLASSIFIED DRUG; CALCIUM BINDING PROTEIN; KINESIN; KINESIN-II; VEGETABLE PROTEIN;

ARTICLE; CELL TRANSPORT; CHLAMYDOMONAS REINHARDTII; CONTROLLED STUDY; FLAGELLUM; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INTRAFLAGELLAR TRANSPORT; KINETOSOME; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; AMINO ACID SEQUENCE; ANIMAL; EUKARYOTIC FLAGELLUM; GENE EXPRESSION REGULATION; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PHYSIOLOGY; SEQUENCE HOMOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

CHLAMYDOMONAS;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM-BINDING PROTEINS; CHLAMYDOMONAS REINHARDTII; CILIA; FLAGELLA; GENE EXPRESSION REGULATION, PLANT; KINESIN; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PLANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84908645677     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.07.019     Document Type: Article

References (49)

1. Allen J.J., Lazerwith S.E., Shokat K.M. Bio-orthogonal affinity purification of direct kinase substrates. J.Am. Chem. Soc. 2005, 127:5288-5289.
2. Allen J.J., Li M., Brinkworth C.S., Paulson J.L., Wang D., Hübner A., Chou W.H., Davis R.J., Burlingame A.L., Messing R.O., et al. A semisynthetic epitope for kinase substrates. Nat. Methods 2007, 4:511-516.
3. Baker S.A., Freeman K., Luby-Phelps K., Pazour G.J., Besharse J.C. IFT20 links kinesin II with a mammalian intraflagellar transport complex that is conserved in motile flagella and sensory cilia. J.Biol. Chem. 2003, 278:34211-34218.
4. Berman S.A., Wilson N.F., Haas N.A., Lefebvre P.A. A novel MAP kinase regulates flagellar length in Chlamydomonas. Curr. Biol. 2003, 13:1145-1149.
5. Besschetnova T.Y., Kolpakova-Hart E., Guan Y., Zhou J., Olsen B.R., Shah J.V. Identification of signaling pathways regulating primary cilium length and flow-mediated adaptation. Curr. Biol. 2010, 20:182-187.
6. Burghoorn J., Dekkers M.P., Rademakers S., de Jong T., Willemsen R., Jansen G. 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 2007, 104:7157-7162.
7. Cao M., Meng D., Wang L., Bei S., Snell W.J., Pan J. Activation loop phosphorylation of a protein kinase is a molecular marker of organelle size that dynamically reports flagellar length. Proc. Natl. Acad. Sci. USA 2013, 110:12337-12342.
8. Chan Y.H., Marshall W.F. How cells know the size of their organelles. Science 2012, 337:1186-1189.
9. Chaya T., Omori Y., Kuwahara R., Furukawa T. ICK is essential for cell type-specific ciliogenesis and the regulation of ciliary transport. EMBO J. 2014, 33:1227-1242.
10. 2+. J.Cell Biol. 1991, 115:1651-1659.
11. Cole D.G., Chinn S.W., Wedaman K.P., Hall K., Vuong T., Scholey J.M. Novel heterotrimeric kinesin-related protein purified from sea urchin eggs. Nature 1993, 366:268-270.
12. Collingridge P., Brownlee C., Wheeler G.L. Compartmentalized calcium signaling in cilia regulates intraflagellar transport. Curr. Biol. 2013, 23:2311-2318.
13. Corbalan-Garcia S., Gómez-Fernández J.C. Signaling through C2 domains: more than one lipid target. Biochim. Biophys. Acta 2014, 1838:1536-1547.
14. Deane J.A., Cole D.G., Seeley E.S., Diener D.R., Rosenbaum J.L. Localization of intraflagellar transport protein IFT52 identifies basal body transitional fibers as the docking site for IFT particles. Curr. Biol. 2001, 11:1586-1590.
15. Dorn K.V., Hughes C.E., Rohatgi R. A Smoothened-Evc2 complex transduces the Hedgehog signal at primary cilia. Dev. Cell 2012, 23:823-835.
16. Dutcher S.K., Li L., Lin H., Meyer L., Giddings T.H., Kwan A.L., Lewis B.L. Whole-Genome Sequencing to Identify Mutants and Polymorphisms in Chlamydomonas reinhardtii. G3 (Bethesda) 2012, 2:15-22.
17. Engel B.D., Ludington W.B., Marshall W.F. Intraflagellar transport particle size scales inversely with flagellar length: revisiting the balance-point length control model. J.Cell Biol. 2009, 187:81-89.
18. Engel B.D., Ishikawa H., Wemmer K.A., Geimer S., Wakabayashi K., Hirono M., Craige B., Pazour G.J., Witman G.B., Kamiya R., Marshall W.F. The role of retrograde intraflagellar transport in flagellar assembly, maintenance, and function. J.Cell Biol. 2012, 199:151-167.
19. Fan Z.C., Behal R.H., Geimer S., Wang Z., Williamson S.M., Zhang H., Cole D.G., Qin H. Chlamydomonas IFT70/CrDYF-1 is a core component of IFT particle complex B and is required for flagellar assembly. Mol. Biol. Cell 2010, 21:2696-2706.
20. Francescatto L., Rothschild S.C., Myers A.L., Tombes R.M. The activation of membrane targeted CaMK-II in the zebrafish Kupffer's vesicle is required for left-right asymmetry. Development 2010, 137:2753-2762.
21. Goetz S.C., Anderson K.V. The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet. 2010, 11:331-344.
22. Guillaud L., Wong R., Hirokawa N. Disruption of KIF17-Mint1 interaction by CaMKII-dependent phosphorylation: a molecular model of kinesin-cargo release. Nat. Cell Biol. 2008, 10:19-29.
23. Imanishi M., Endres N.F., Gennerich A., Vale R.D. Autoinhibition regulates the motility of the C. elegans intraflagellar transport motor OSM-3. J.Cell Biol. 2006, 174:931-937.
24. Lefebvre P.A., Nordstrom S.A., Moulder J.E., Rosenbaum J.L. Flagellar elongation and shortening in Chlamydomonas. IV. Effects of flagellar detachment, regeneration, and resorption on the induction of flagellar protein synthesis. J.Cell Biol. 1978, 78:8-27.
25. Liang Y., Pan J. Regulation of flagellar biogenesis by a calcium dependent protein kinase in Chlamydomonas reinhardtii. PLoS ONE 2013, 8:e69902.
26. Liu Q., Tan G., Levenkova N., Li T., Pugh E.N., Rux J.J., Speicher D.W., Pierce E.A. The proteome of the mouse photoreceptor sensory cilium complex. Mol. Cell. Proteomics 2007, 6:1299-1317.
27. Ludington W.B., Wemmer K.A., Lechtreck K.F., Witman G.B., Marshall W.F. Avalanche-like behavior in ciliary import. Proc. Natl. Acad. Sci. USA 2013, 110:3925-3930.
28. Luo M., Cao M., Kan Y., Li G., Snell W., Pan J. The phosphorylation state of an aurora-like kinase marks the length of growing flagella in Chlamydomonas. Curr. Biol. 2011, 21:586-591.
29. Mahjoub M.R., Qasim Rasi M., Quarmby L.M. A NIMA-related kinase, Fa2p, localizes to a novel site in the proximal cilia of Chlamydomonas and mouse kidney cells. Mol. Biol. Cell 2004, 15:5172-5186.
30. Marshall W.F., Qin H., Rodrigo Brenni M., Rosenbaum J.L. Flagellar length control system: testing a simple model based on intraflagellar transport and turnover. Mol. Biol. Cell 2005, 16:270-278.
31. Molnar A., Bassett A., Thuenemann E., Schwach F., Karkare S., Ossowski S., Weigel D., Baulcombe D. Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. Plant J. 2009, 58:165-174.
32. Omori Y., Chaya T., Katoh K., Kajimura N., Sato S., Muraoka K., Ueno S., Koyasu T., Kondo M., Furukawa T. Negative regulation of ciliary length by ciliary male germ cell-associated kinase (Mak) is required for retinal photoreceptor survival. Proc. Natl. Acad. Sci. USA 2010, 107:22671-22676.
33. Ou G., Blacque O.E., Snow J.J., Leroux M.R., Scholey J.M. Functional coordination of intraflagellar transport motors. Nature 2005, 436:583-587.
34. Pazour G.J., Agrin N., Leszyk J., Witman G.B. Proteomic analysis of a eukaryotic cilium. J.Cell Biol. 2005, 170:103-113.
35. Pedersen L.B., Rosenbaum J.L. Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr. Top. Dev. Biol. 2008, 85:23-61.
36. Pedersen L.B., Miller M.S., Geimer S., Leitch J.M., Rosenbaum J.L., Cole D.G. Chlamydomonas IFT172 is encoded by FLA11, interacts with CrEB1, and regulates IFT at the flagellar tip. Curr. Biol. 2005, 15:262-266.
37. Rosenbaum J.L., Witman G.B. Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 2002, 3:813-825.
38. Rosenbaum J.L., Moulder J.E., Ringo D.L. Flagellar elongation and shortening in Chlamydomonas. The use of cycloheximide and colchicine to study the synthesis and assembly of flagellar proteins. J.Cell Biol. 1969, 41:600-619.
39. Rothschild S.C., Francescatto L., Drummond I.A., Tombes R.M. CaMK-II is a PKD2 target that promotes pronephric kidney development and stabilizes cilia. Development 2011, 138:3387-3397.
40. Satish Tammana T.V., Tammana D., Diener D.R., Rosenbaum J. Centrosomal protein CEP104 (Chlamydomonas FAP256) moves to the ciliary tip during ciliary assembly. J.Cell Sci. 2013, 126:5018-5029.
41. Scholey J.M. Intraflagellar transport motors in cilia: moving along the cell's antenna. J.Cell Biol. 2008, 180:23-29.
42. Scholey J.M. Kinesin-2: a family of heterotrimeric and homodimeric motors with diverse intracellular transport functions. Annu. Rev. Cell Dev. Biol. 2013, 29:443-469.
43. Tam L.W., Wilson N.F., Lefebvre P.A. A CDK-related kinase regulates the length and assembly of flagella in Chlamydomonas. J.Cell Biol. 2007, 176:819-829.
44. Tam L.W., Ranum P.T., Lefebvre P.A. CDKL5 regulates flagellar length and localizes to the base of the flagella in Chlamydomonas. Mol. Biol. Cell 2013, 24:588-600.
45. Verhey K.J., Hammond J.W. Traffic control: regulation of kinesin motors. Nat. Rev. Mol. Cell Biol. 2009, 10:765-777.
46. Wang L., Piao T., Cao M., Qin T., Huang L., Deng H., Mao T., Pan J. Flagellar regeneration requires cytoplasmic microtubule depolymerization and kinesin-13. J.Cell Sci. 2013, 126:1531-1540.
47. Wei Q., Zhang Y., Li Y., Zhang Q., Ling K., Hu J. The BBSome controls IFT assembly and turnaround in cilia. Nat. Cell Biol. 2012, 14:950-957.
48. 2+-calmodulin-dependent protein kinases IV and II reveals shared and distinctive features. J.Biol. Chem. 1998, 273:3166-3172.
49. Yang Y., Roine N., Mäkelä T.P. CCRK depletion inhibits glioblastoma cell proliferation in a cilium-dependent manner. EMBO Rep. 2013, 14:741-747.