Getting tubulin to the tip of the cilium: One IFT train, many different tubulin cargo-binding sites?

BioEssays

Volumn 36, Issue 5, 2014, Pages 463-467

  Bhogaraju, Sagar ^a   Weber, Kristina ^a   Engel, Benjamin D ^a   Lechtreck, Karl Ferdinand ^b   Lorentzen, Esben ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Cilia; Ciliogenesis; Flagella; Intraflagellar transport (IFT); Tubulin

Indexed keywords

CARRIER PROTEIN; INTRAFLAGELLAR TRANSPORT 74 PROTEIN; INTRAFLAGELLAR TRANSPORT 81 PROTEIN; MOLECULAR MOTOR; TUBULIN; UNCLASSIFIED DRUG; CYTOSKELETON PROTEIN; PROTEIN BINDING;

ARTICLE; BINDING KINETICS; BINDING SITE; CELL FUNCTION; EUKARYOTIC FLAGELLUM; MICROTUBULE; NONHUMAN; PROTEIN BINDING; PROTEIN PURIFICATION; PROTEIN TRANSPORT; ANIMAL; CHEMISTRY; HUMAN; METABOLISM; PROTEIN TERTIARY STRUCTURE; TRANSPORT AT THE CELLULAR LEVEL;

EUKARYOTA;

ANIMALS; BINDING SITES; BIOLOGICAL TRANSPORT; CILIA; CYTOSKELETAL PROTEINS; HUMANS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TUBULIN;

EID: 84897958996     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201400007     Document Type: Article

References (55)

1. Ishikawa H, Marshall WF. 2011. Ciliogenesis: building the cell's antenna. Nat Rev Mol Cell Biol 12: 222-34.
2. Pazour G, Dickert BL, Vucica Y, Seeley ES, et al. 2000. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene Tg737, are required for assembly of cilia and flagella. J Cell Biol 151: 709-18.
3. Hildebrandt F, Benzing T, Katsanis N. 2011. Ciliopathies. N Engl J Med 364: 1533-43.
4. Breslow DK, Koslover EF, Seydel F, Spakowitz AJ, et al. 2013. An in vitro assay for entry into cilia reveals unique properties of the soluble diffusion barrier. J Cell Biol 203: 129-47.
5. Hu Q, Nelson WJ. 2011. Ciliary diffusion barrier: the gatekeeper for the primary cilium compartment. Cytoskeleton 68: 313-24.
6. Kozminski KG, Johnson KA, Forscher P, Rosenbaum JL. 1993. A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc Natl Acad Sci USA 90: 5519-23.
7. Cole DG, Diener DR, Himelblau AL, Beech PL, et al. 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.
8. 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.
9. Walther Z, Vashishtha M, Hall JL. 1994. The Chlamydomonas FLA10 gene encodes a novel kinesin-homologous protein. J Cell Biol 126: 175-88.
10. Pazour GJ, Dickert BL, Witman GB. 1999. The DHC1b (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly. J Cell Biol 144: 473-81.
11. Porter ME, Bower R, Knott JA, Byrd P, et al. 1999. Cytoplasmic dynein heavy chain 1b is required for flagellar assembly in Chlamydomonas. Mol Biol Cell 10: 693-712.
12. Perrone CA, Tritschler D, Taulman P, Bower R, et al. 2003. A novel dynein light intermediate chain colocalizes with the retrograde motor for intraflagellar transport at sites of axoneme assembly in Chlamydomonas and mammalian cells. Mol Biol Cell 14: 2041-56.
13. Hou Y, Pazour GJ, Witman GB. 2004. A dynein light intermediate chain, D1bLIC, is required for retrograde intraflagellar transport. Mol Biol Cell 15: 4382-94.
14. Engel BD, Ishikawa H, Wemmer KA, Geimer S, et al. 2012. The role of retrograde intraflagellar transport in flagellar assembly, maintenance, and function. J Cell Biol 199: 151-67.
15. Piperno G, Siuda E, Henderson S, Segil M, et al. 1998. Distinct mutants of retrograde intraflagellar transport (IFT) share similar morphological and molecular defects. J Cell Biol 143: 1591-601.
16. Lucker BF, Behal RH, Qin H, Siron LC, et al. 2005. Characterization of the intraflagellar transport complex B core: direct interaction of the IFT81 and IFT74/72 subunits. J Biol Chem 280: 27688-96.
17. Iomini C, Babaev-Khaimov V, Sassaroli M, Piperno G. 2001. Protein particles in Chlamydomonas flagella undergo a transport cycle consisting of four phases. J Cell Biol 153: 13-24.
18. Pedersen LB, Geimer S, Rosenbaum JL. 2006. Dissecting the molecular mechanisms of intraflagellar transport in Chlamydomonas. Curr Biol 16: 450-9.
19. Buisson J, Chenouard N, Lagache T, Blisnick T, et al. 2013. Intraflagellar transport proteins cycle between the flagellum and its base. J Cell Sci 126: 327-38.
20. Ludington WB, Wemmer KA, Lechtreck KF, Witman GB, et al. 2013. Avalanche-like behavior in ciliary import. Proc Natl Acad Sci USA 110: 3925-30.
21. Pigino G, Geimer S, Lanzavecchia S, Paccagnini E, et al. 2009. Electron-tomographic analysis of intraflagellar transport particle trains in situ. J Cell Biol 187: 135-48.
22. Engel BD, Ludington WB, Marshall WF. 2009. Intraflagellar transport particle size scales inversely with flagellar length: revisiting the balance-point length control model. J Cell Biol 187: 81-9.
23. Bhogaraju S, Cajanek L, Fort C, Blisnick T, et al. 2013. Molecular basis of tubulin transport within the cilium by IFT74 and IFT81. Science 341: 1009-12.
24. Nicastro D, Fu X, Heuser T, Tso A, et al. 2011. Cryo-electron tomography reveals conserved features of doublet microtubules in flagella. Proc Natl Acad Sci USA 108: E845-53.
25. Johnson KA, Rosenbaum JL. 1992. Polarity of flagellar assembly in Chlamydomonas. J Cell Biol 119: 1605-11.
26. Marshall WF, Rosenbaum JL. 2001. Intraflagellar transport balances continuous turnover of outer doublet microtubules: implications for flagellar length control. J Cell Biol 155: 405-14.
27. Wren KN, Craft JM, Tritschler D, Schauer A, et al. 2013. A differential cargo-loading model of ciliary length regulation by IFT. Curr Biol 23: 2463-71.
28. Song L, Dentler W. 2001. Flagellar protein dynamics in Chlamydomonas. J Biol Chem 276: 29754-63.
29. Stephens RE. 1997. Synthesis and turnover of embryonic sea urchin ciliary proteins during selective inhibition of tubulin synthesis and assembly. Mol Biol Cell 8: 2187-98.
30. Qin H, Diener DR, Geimer S, Cole DG, et al. 2004. Intraflagellar transport (IFT) cargo: IFT transports flagellar precursors to the tip and turnover products to the cell body. J Cell Biol 164: 255-66.
31. Hao L, Thein M, Brust-Mascher I, Civelekoglu-Scholey G, et al. 2011. Intraflagellar transport delivers tubulin isotypes to sensory cilium middle and distal segments. Nat Cell Biol 13: 790-8.
32. Ciferri C, Pasqualato S, Screpanti E, Varetti G, et al. 2008. Implications for kinetochore-microtubule attachment from the structure of an engineered Ndc80 complex. Cell 133: 427-39.
33. Korenbaum E, Rivero F. 2002. Calponin homology domains at a glance. J Cell Sci 115: 3543-5.
34. Schou KB, Andersen JS, Pedersen LB. 2014. A divergent calponin homology (NN-CH) domain defines a novel family: implications for evolution of ciliary IFT complex B proteins. Bioinformatics, in press, doi: 10.1093/bioinformatics/btt661.
35. van Dam TJP, Townsend MJ, Turk M, Schlessinger A, et al. 2013. Evolution of modular intraflagellar transport from a coatomer-like progenitor. Proc Natl Acad Sci USA 110: 6943-8.
36. Rosenbaum JL, Moulder JE, Ringo DL. 1969. Flagellar elongation and shortening in Chlamydomonas: the use of cycloheximide and colchicine to study the synthesis and assembly of flagellar proteins. J Cell Biol 41: 600-19.
37. Mueller J, Perrone CA, Bower R, Cole DG, et al. 2005. The FLA3 KAP subunit is required for localization of kinesin-2 to the site of flagellar assembly and processive anterograde intraflagellar transport. Mol Biol Cell 16: 1341-54.
38. Dentler W. 2005. Intraflagellar transport (IFT) during assembly and disassembly of Chlamydomonas flagella. J Cell Biol 170: 649-59.
39. Marshall WF, Qin H, Rodrigo Brenni M, Rosenbaum JL. 2005. Flagellar length control system: testing a simple model based on intraflagellar transport and turnover. Mol Biol Cell 16: 270-8.
40. Bhogaraju S, Engel BD, Lorentzen E. 2013. Intraflagellar transport complex structure and cargo interactions. Cilia 2: 10.
41. Taschner M, Bhogaraju S, Lorentzen E. 2012. Architecture and function of IFT complex proteins in ciliogenesis. Differentiation 83: S12-S22.
42. Ling L, Goeddel DV. 2000. MIP-T3, a novel protein linking tumor necrosis factor receptor-associated factor 3 to the microtubule network. J Biol Chem 275: 23852-60.
43. Guo C-W, Xiong S, Liu G, Wang Y-F, et al. 2010. Proteomic analysis reveals novel binding partners of MIP-T3 in human cells. Proteomics 10: 2337-47.
44. Li J, Sun Z. 2011. Qilin is essential for cilia assembly and normal kidney development in zebrafish. PLoS One 6: e27365.
45. Omori Y, Zhao C, Saras A, Mukhopadhyay S, et al. 2008. Elipsa is an early determinant of ciliogenesis that links the IFT particle to membrane-associated small GTPase Rab8. Nat Cell Biol 10: 437-4.
46. Ou G, Qin H, Rosenbaum JL, Scholey JM. 2005. The PKD protein qilin undergoes intraflagellar transport. Curr Biol 15: R410-R411.
47. Ahmed NT, Gao C, Lucker BF, Cole DG, et al. 2008. ODA16 aids axonemal outer row dynein assembly through an interaction with the intraflagellar transport machinery. J Cell Biol 183: 313-22.
48. Hou Y, Qin H, Follit JA, Pazour GJ, et al. 2007. Functional analysis of an individual IFT protein: IFT46 is required for transport of outer dynein arms into flagella. J Cell Biol 176: 653-65.
49. Bui KH, Yagi T, Yamamoto R, Kamiya R, et al. 2012. Polarity and asymmetry in the arrangement of dynein and related structures in the Chlamydomonas axoneme. J Cell Biol 198: 913-25.
50. Luo M, Cao M, Kan Y, Li G, et al. 2011. The phosphorylation state of an aurora-like kinase marks the length of growing flagella in Chlamydomonas. Curr Biol 21: 586-91.
51. Cao M, Meng D, Wang L, Bei S, et al. 2013. Activation loop phosphorylation of a protein kinase is a molecular marker of organelle size that dynamically reports flagellar length. Proc Natl Acad Sci USA 110: 12337-42.
52. Tam LW, Wilson NF, Lefebvre PA. 2007. A CDK-related kinase regulates the length and assembly of flagella in Chlamydomonas. J Cell Biol 176: 819-29.
53. Hilton LK, Gunawardane K, Kim JW, Schwarz MC, et al. 2013. The kinases LF4 and CNK2 control ciliary length by feedback regulation of assembly and disassembly rates. Curr Biol 23: 2208-14.
54. Berman SA, Wilson NF, Haas NA, Lefebvre PA. 2003. A Novel MAP kinase regulates flagellar length in Chlamydomonas. Curr Biol 13: 1145-9.
55. Baker SA, Freeman K, Luby-Phelps K, Pazour GJ, et al. 2003. IFT20 links kinesin II with a mammalian intraflagellar transport complex that is conserved in motile flagella and sensory cilia. J Biol Chem 278: 34211-8.