Tubulin transport by IFT is upregulated during ciliary growth by a cilium-autonomous mechanism

Journal of Cell Biology

Volumn 208, Issue 2, 2015, Pages 223-237

  Craft, Julie M ^a   Harris, J Aaron ^a   Hyman, Sebastian ^a   Kner, Peter ^b   Lechtreck, Karl F ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b University of Georgia   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; GREEN FLUORESCENT PROTEIN; PROTEIN TAG; TUBULIN; VEGETABLE PROTEIN;

ARTICLE; CELL GROWTH; CELL LEVEL; CHLAMYDOMONAS; CILIARY GROWTH; CONTROLLED STUDY; DIFFUSION; EUKARYOTIC FLAGELLUM; INTRACELLULAR TRANSPORT; INTRAFLAGELLAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN TRANSPORT; STEADY STATE; UPREGULATION; CHLAMYDOMONAS REINHARDTII; FLAGELLUM; METABOLISM; PHYSIOLOGY; PROTEIN MULTIMERIZATION; ULTRASTRUCTURE;

CHLAMYDOMONAS;

CHLAMYDOMONAS REINHARDTII; CILIA; DIFFUSION; FLAGELLA; PLANT PROTEINS; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; TUBULIN; UP-REGULATION;

EID: 84921822477     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201409036     Document Type: Article

References (78)

1. Ahmed, N.T., C. Gao, B.F. Lucker, D.G. Cole, and D.R. Mitchell. 2008. ODA16 aids axonemal outer row dynein assembly through an interaction with the intraflagellar transport machinery. J. Cell Biol. 183: 313-322. http://dx.doi.org/10.1083/jcb.200802025
2. Al-Bassam, J., and F. Chang. 2011. Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP. Trends Cell Biol. 21: 604-614. http://dx.doi.org/10.1016/j.tcb.2011.06.007
3. Barsel, S.E., D.E. Wexler, and P.A. Lefebvre. 1988. Genetic analysis of longflagella mutants of Chlamydomonas reinhardtii. Genetics. 118:637-648.
4. Belzile, O., C.I. Hernandez-Lara, Q. Wang, and W.J. Snell. 2013. Regulated membrane protein entry into flagella is facilitated by cytoplasmic microtubules and does not require IFT. Curr. Biol. 23: 1460-1465. http://dx.doi.org/10.1016/j.cub.2013.06.025
5. Berman, S.A., N.F. Wilson, N.A. Haas, and P.A. Lefebvre. 2003. A novel MAP kinase regulates flagellar length in Chlamydomonas. Curr. Biol. 13: 1145-1149. http://dx.doi.org/10.1016/S0960-9822(03)00415-9
6. Bhogaraju, S., L. Cajanek, C. Fort, T. Blisnick, K. Weber, M. Taschner, N. Mizuno, S. Lamla, P. Bastin, E.A. Nigg, and E. Lorentzen. 2013. Molecular basis of tubulin transport within the cilium by IFT74 and IFT81. Science. 341: 1009-1012. http://dx.doi.org/10.1126/science.1240985
7. Bhogaraju, S., K. Weber, B.D. Engel, K.F. Lechtreck, and E. Lorentzen. 2014. Getting tubulin to the tip of the cilium: one IFT train, many different tubulin cargo-binding sites? BioEssays. 36:463-467. http://dx.doi.org/10.1002/bies.201400007
8. Blacque, O.E., M.J. Reardon, C. Li, J. McCarthy, M.R. Mahjoub, S.J. Ansley, J.L. Badano, A.K. Mah, P.L. Beales, W.S. Davidson, et al. 2004. Loss of C. elegans BBS-7 and BBS-8 protein function results in cilia defects and compromised intraflagellar transport. Genes Dev. 18: 1630-1642. http://dx.doi.org/10.1101/gad.1194004
9. Borisy, G.G., and E.W. Taylor. 1967. The mechanism of action of colchicine. Binding of colchincine-3H to cellular protein. J. Cell Biol. 34: 525-533. http://dx.doi.org/10.1083/jcb.34.2.525
10. Breslow, D.K., E.F. Koslover, F. Seydel, A.J. Spakowitz, and M.V. Nachury. 2013. An in vitro assay for entry into cilia reveals unique properties of the soluble diffusion barrier. J. Cell Biol. 203: 129-147. http://dx.doi.org/10.1083/jcb.201212024
11. Brust-Mascher, I., G. Ou, and J.M. Scholey. 2013. Measuring rates of intraflagellar transport along Caenorhabditis elegans sensory cilia using fluorescence microscopy. Methods Enzymol. 524: 285-304. http://dx.doi.org/10.1016/B978-0-12-397945-2.00016-0
12. Cao, M., D. Meng, L. Wang, S. Bei, W.J. Snell, and J. Pan. 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: 12337-12342. http://dx.doi.org/10.1073/pnas.1302364110
13. Chan, Y.H., and W.F. Marshall. 2012. How cells know the size of their organelles. Science. 337: 1186-1189. http://dx.doi.org/10.1126/science.1223539
14. Cole, D.G., D.R. Diener, A.L. Himelblau, P.L. Beech, J.C. Fuster, and J.L. Rosenbaum. 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. http://dx.doi.org/10.1083/jcb.141.4.993
15. Collingridge, P., C. Brownlee, and G.L. Wheeler. 2013. Compartmentalized calcium signaling in cilia regulates intraflagellar transport. Curr. Biol. 23: 2311-2318. http://dx.doi.org/10.1016/j.cub.2013.09.059
16. Craige, B., C.C. Tsao, D.R. Diener, Y. Hou, K.F. Lechtreck, J.L. Rosenbaum, and G.B. Witman. 2010. CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content. J. Cell Biol. 190: 927-940. http://dx.doi.org/10.1083/jcb.201006105
17. Deane, J.A., D.G. Cole, E.S. Seeley, D.R. Diener, and J.L. Rosenbaum. 2001. Localization of intraflagellar transport protein IFT52 identifies basal body transitional fibers as the docking site for IFT particles. Curr. Biol. 11: 1586-1590. http://dx.doi.org/10.1016/S0960-9822(01)00484-5
18. Dentler, W. 2005. Intraflagellar transport (IFT) during assembly and disassembly of Chlamydomonas flagella. J. Cell Biol. 170: 649-659. http://dx.doi.org/10.1083/jcb.200412021
19. Desai, A., and T.J. Mitchison. 1997. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13: 83-117. http://dx.doi.org/10.1146/annurev.cellbio.13.1.83
20. Duan, J., and M.A. Gorovsky. 2002. Both carboxy-terminal tails of alpha- and beta-tubulin are essential, but either one will suffice. Curr. Biol. 12: 313-316. http://dx.doi.org/10.1016/S0960-9822(02)00651-6
21. Engel, B.D., W.B. Ludington, and W.F. Marshall. 2009. Intraflagellar transport particle size scales inversely with flagellar length: revisiting the balancepoint length control model. J. Cell Biol. 187: 81-89. http://dx.doi.org/10.1083/jcb.200812084
22. Euteneuer, U., and J.R. McIntosh. 1981. Polarity of some motility-related micro tubules. Proc. Natl. Acad. Sci. USA. 78: 372-376. http://dx.doi.org/10.1073/pnas.78.1.372
23. Gaertig, J., and D. Wloga. 2008. Ciliary tubulin and its post-translational modifications. Curr. Top. Dev. Biol. 85: 83-113. http://dx.doi.org/10.1016/S0070-2153(08)00804-1
24. Gard, D.L., and M.W. Kirschner. 1987. Microtubule assembly in cytoplasmic extracts of Xenopus oocytes and eggs. J. Cell Biol. 105: 2191-2201. http://dx.doi.org/10.1083/jcb.105.5.2191
25. Goehring, N.W., and A.A. Hyman. 2012. Organelle growth control through limiting pools of cytoplasmic components. Curr. Biol. 22: R330-R339. http://dx.doi.org/10.1016/j.cub.2012.03.046
26. Hao, L., M. Thein, I. Brust-Mascher, G. Civelekoglu-Scholey, Y. Lu, S. Acar, B. Prevo, S. Shaham, and J.M. Scholey. 2011. Intraflagellar transport delivers tubulin isotypes to sensory cilium middle and distal segments. Nat. Cell Biol. 13: 790-798. http://dx.doi.org/10.1038/ncb2268
27. Hilton, L.K., K. Gunawardane, J.W. Kim, M.C. Schwarz, and L.M. Quarmby. 2013. The kinases LF4 and CNK2 control ciliary length by feedback regulation of assembly and disassembly rates. Curr. Biol. 23: 2208-2214. http://dx.doi.org/10.1016/j.cub.2013.09.038
28. Hou, Y., H. Qin, J.A. Follit, G.J. Pazour, J.L. Rosenbaum, and G.B. Witman. 2007. Functional analysis of an individual IFT protein: IFT46 is required for transport of outer dynein arms into flagella. J. Cell Biol. 176: 653-665. http://dx.doi.org/10.1083/jcb.200608041
29. Howard, J. 2001. Mechanics of motor proteins and the cytoskeleton. Sinauer Associates, Publishers, Sunderland, Mass. 67 pp.
30. Huang, K., D.R. Diener, A. Mitchell, G.J. Pazour, G.B. Witman, and J.L. Rosenbaum. 2007. Function and dynamics of PKD2 in Chlamydomonas reinhardtii flagella. J. Cell Biol. 179: 501-514. http://dx.doi.org/10.1083/jcb.200704069
31. Johnson, K.A., and J.L. Rosenbaum. 1992. Polarity of flagellar assembly in Chlamydomonas. J. Cell Biol. 119: 1605-1611. http://dx.doi.org/10.1083/jcb.119.6.1605
32. Kee, H.L., and K.J. Verhey. 2013. Molecular connections between nuclear and ciliary import processes. Cilia. 2: 11. http://dx.doi.org/10.1186/2046-2530-2-11
33. Kee, H.L., J.F. Dishinger, T.L. Blasius, C.J. Liu, B. Margolis, and K.J. Verhey. 2012. A size-exclusion permeability barrier and nucleoporins characterize a ciliary pore complex that regulates transport into cilia. Nat. Cell Biol. 14: 431-437. http://dx.doi.org/10.1038/ncb2450
34. King, S.M., and G.B. Witman. 1990. Localization of an intermediate chain of outer arm dynein by immunoelectron microscopy. J. Biol. Chem. 265: 19807-19811.
35. Ko, H.W., R.X. Norman, J. Tran, K.P. Fuller, M. Fukuda, and J.T. Eggenschwiler. 2010. Broad-minded links cell cycle-related kinase to cilia assembly and hedgehog signal transduction. Dev. Cell. 18: 237-247. http://dx.doi.org/10.1016/j.devcel.2009.12.014
36. Kozminski, K.G., K.A. Johnson, P. Forscher, and J.L. Rosenbaum. 1993. A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc. Natl. Acad. Sci. USA. 90: 5519-5523. http://dx.doi.org/10.1073/pnas.90.12.5519
37. Kozminski, K.G., P.L. Beech, and J.L. Rosenbaum. 1995. The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. J. Cell Biol. 131: 1517-1527. http://dx.doi.org/10.1083/jcb.131.6.1517
38. Kuchka, M.R., and J.W. Jarvik. 1987. Short-Flagella Mutants of Chlamydomonas reinhardtii. Genetics. 115:685-691.
39. Lechtreck, K.F. 2013. In vivo imaging of IFT in Chlamydomonas flagella. Methods Enzymol. 524: 265-284. http://dx.doi.org/10.1016/B978-0-12-397945-2.00015-9
40. Lechtreck, K.F., E.C. Johnson, T. Sakai, D. Cochran, B.A. Ballif, J. Rush, G.J. Pazour, M. Ikebe, and G.B. Witman. 2009. The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella. J. Cell Biol. 187: 1117-1132. http://dx.doi.org/10.1083/jcb.200909183
41. Lechtreck, K.F., J.M. Brown, J.L. Sampaio, J.M. Craft, A. Shevchenko, J.E. Evans, and G.B. Witman. 2013. Cycling of the signaling protein phospholipase D through cilia requires the BBSome only for the export phase. J. Cell Biol. 201: 249-261. http://dx.doi.org/10.1083/jcb.201207139
42. Lefebvre, P.A. 1995. Flagellar amputation and regeneration in Chlamydomonas. Methods Cell Biol. 47: 3-7. http://dx.doi.org/10.1016/S0091-679X(08)60782-7
43. Lefebvre, P.A. 2009. Flagellar length control. In The Chlamydomonas sourcebook, Vol. 3: Cell motility and behavior. E.H. Harris and G.B. Witmann, editors. Elsevier, Amsterdam, 115-129.
44. Lin, Y.C., P. Niewiadomski, B. Lin, H. Nakamura, S.C. Phua, J. Jiao, A. Levchenko, T. Inoue, R. Rohatgi, and T. Inoue. 2013. Chemically inducible diffusion trap at cilia reveals molecular sieve-like barrier. Nat. Chem. Biol. 9: 437-443. http://dx.doi.org/10.1038/nchembio.1252
45. Ludington, W.B., L.Z. Shi, Q. Zhu, M.W. Berns, and W.F. Marshall. 2012. Organelle size equalization by a constitutive process. Curr. Biol. 22: 2173-2179. http://dx.doi.org/10.1016/j.cub.2012.09.040
46. Ludington, W.B., K.A. Wemmer, K.F. Lechtreck, G.B. Witman, and W.F. Marshall. 2013. Avalanche-like behavior in ciliary import. Proc. Natl. Acad. Sci. USA. 110: 3925-3930. http://dx.doi.org/10.1073/pnas.1217354110
47. Luo, M., M. Cao, Y. Kan, G. Li, W. Snell, and J. Pan. 2011. The phosphorylation state of an aurora-like kinase marks the length of growing flagella in Chlamydomonas. Curr. Biol. 21: 586-591. http://dx.doi.org/10.1016/j.cub.2011.02.046
48. Mahjoub, M.R., and T. Stearns. 2012. Supernumerary centrosomes nucleate extra cilia and compromise primary cilium signaling. Curr. Biol. 22: 1628-1634. http://dx.doi.org/10.1016/j.cub.2012.06.057
49. Mahjoub, M.R., M.L. Trapp, and L.M. Quarmby. 2005. NIMA-related kinases defective in murine models of polycystic kidney diseases localize to primary cilia and centrosomes. J. Am. Soc. Nephrol. 16: 3485-3489. http://dx.doi.org/10.1681/ASN.2005080824
50. Marshall, W.F., and J.L. Rosenbaum. 2001. Intraflagellar transport balances continuous turnover of outer doublet microtubules: implications for flagellar length control. J. Cell Biol. 155: 405-414. http://dx.doi.org/10.1083/jcb.200106141
51. Marshall, W.F., H. Qin, M. Rodrigo Brenni, and J.L. Rosenbaum. 2005. Flagellar length control system: testing a simple model based on intraflagellar transport and turnover. Mol. Biol. Cell. 16: 270-278. http://dx.doi.org/10.1091/mbc.E04-07-0586
52. Mueller, J., C.A. Perrone, R. Bower, D.G. Cole, and M.E. Porter. 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: 1341-1354. http://dx.doi.org/10.1091/mbc.E04-10-0931
53. Omran, H. 2010. NPHP proteins: gatekeepers of the ciliary compartment. J. Cell Biol. 190: 715-717. http://dx.doi.org/10.1083/jcb.201008080
54. Özgül, R.K., A.M. Siemiatkowska, D. Yücel, C.A. Myers, R.W. Collin, M.N. Zonneveld, A. Beryozkin, E. Banin, C.B. Hoyng, L.I. van den Born, et al. European Retinal Disease Consortium. 2011. Exome sequencing and cis-regulatory mapping identify mutations in MAK, a gene encoding a regulator of ciliary length, as a cause of retinitis pigmentosa. Am. J. Hum. Genet. 89: 253-264. http://dx.doi.org/10.1016/j.ajhg.2011.07.005
55. Pasquale, S.M., and U.W. Goodenough. 1987. Cyclic AMP functions as a primary sexual signal in gametes of Chlamydomonas reinhardtii. J. Cell Biol. 105: 2279-2292. http://dx.doi.org/10.1083/jcb.105.5.2279
56. Pedigo, S., and R.C. Williams Jr. 2002. Concentration dependence of variability in growth rates of microtubules. Biophys. J. 83: 1809-1819. http://dx.doi.org/10.1016/S0006-3495(02)73946-5
57. Phirke, P., E. Efimenko, S. Mohan, J. Burghoorn, F. Crona, M.W. Bakhoum, M. Trieb, K. Schuske, E.M. Jorgensen, B.P. Piasecki, et al. 2011. Transcriptional profiling of C. elegans DAF-19 uncovers a ciliary baseassociated protein and a CDK/CCRK/LF2p-related kinase required for intraflagellar transport. Dev. Biol. 357: 235-247. http://dx.doi.org/10.1016/j.ydbio.2011.06.028
58. Preitner, N., J. Quan, D.W. Nowakowski, M.L. Hancock, J. Shi, J. Tcherkezian, T.L. Young-Pearse, and J.G. Flanagan. 2014. APC is an RNA-binding protein, and its interactome provides a link to neural development and microtubule assembly. Cell. 158: 368-382. http://dx.doi.org/10.1016/j.cell.2014.05.042
59. Qian, H., M.P. Sheetz, and E.L. Elson. 1991. Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. Biophys. J. 60: 910-921. http://dx.doi.org/10.1016/S0006-3495(91)82125-7
60. Qin, H., D.R. Diener, S. Geimer, D.G. Cole, and J.L. Rosenbaum. 2004. Intraflagellar transport (IFT) cargo: IFT transports flagellar precursors to the tip and turnover products to the cell body. J. Cell Biol. 164: 255-266. http://dx.doi.org/10.1083/jcb.200308132
61. Rasala, B.A., D.J. Barrera, J. Ng, T.M. Plucinak, J.N. Rosenberg, D.P. Weeks, G.A. Oyler, T.C. Peterson, F. Haerizadeh, and S.P. Mayfield. 2013. Expanding the spectral palette of fluorescent proteins for the green microalga Chlamydomonas reinhardtii. Plant J. 74: 545-556. http://dx.doi.org/10.1111/tpj.12165
62. Rosenbaum, J.L., and G.B. Witman. 2002. Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3: 813-825. http://dx.doi.org/10.1038/nrm952
63. Rosenbaum, J.L., J.E. Moulder, and D.L. Ringo. 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: 600-619. http://dx.doi.org/10.1083/jcb.41.2.600
64. Sbalzarini, I.F., and P. Koumoutsakos. 2005. Feature point tracking and trajectory analysis for video imaging in cell biology. J. Struct. Biol. 151: 182-195. http://dx.doi.org/10.1016/j.jsb.2005.06.002
65. Shaner, N.C., G.G. Lambert, A. Chammas, Y. Ni, P.J. Cranfill, M.A. Baird, B.R. Sell, J.R. Allen, R.N. Day, M. Israelsson, et al. 2013. A bright monomeric green fluorescent protein derived from Branchiostoma lanceolatum. Nat. Methods. 10: 407-409. http://dx.doi.org/10.1038/nmeth.2413
66. Sharma, N., Z.A. Kosan, J.E. Stallworth, N.F. Berbari, and B.K. Yoder. 2011. Soluble levels of cytosolic tubulin regulate ciliary length control. Mol. Biol. Cell. 22: 806-816. http://dx.doi.org/10.1091/mbc.E10-03-0269
67. Shih, S.M., B.D. Engel, F. Kocabas, T. Bilyard, A. Gennerich, W.F. Marshall, and A. Yildiz. 2013. Intraflagellar transport drives flagellar surface motility. eLife. 2: e00744. http://dx.doi.org/10.7554/eLife.00744
68. Silflow, C.D., and J.L. Rosenbaum. 1981. Multiple α- and β-tubulin genes in Chlamydomonas and regulation of tubulin mRNA levels after deflagellation. Cell. 24: 81-88. http://dx.doi.org/10.1016/0092-8674(81)90503-1
69. Srayko, M., A. Kaya, J. Stamford, and A.A. Hyman. 2005. Identification and characterization of factors required for microtubule growth and nucleation in the early C. elegans embryo. Dev. Cell. 9: 223-236. http://dx.doi.org/10.1016/j.devcel.2005.07.003
70. Tam, L.W., N.F. Wilson, and P.A. Lefebvre. 2007. A CDK-related kinase regulates the length and assembly of flagella in Chlamydomonas. J. Cell Biol. 176: 819-829. http://dx.doi.org/10.1083/jcb.200610022
71. Tam, L.W., P.T. Ranum, and P.A. Lefebvre. 2013. CDKL5 regulates flagellar length and localizes to the base of the flagella in Chlamydomonas. Mol. Biol. Cell. 24: 588-600. http://dx.doi.org/10.1091/mbc.E12-10-0718
72. Tammachote, R., C.J. Hommerding, R.M. Sinders, C.A. Miller, P.G. Czarnecki, A.C. Leightner, J.L. Salisbury, C.J. Ward, V.E. Torres, V.H. Gattone II, and P.C. Harris. 2009. Ciliary and centrosomal defects associated with mutation and depletion of the Meckel syndrome genes MKS1 and MKS3. Hum. Mol. Genet. 18: 3311-3323. http://dx.doi.org/10.1093/hmg/ddp272
73. Wang, L., T. Piao, M. Cao, T. Qin, L. Huang, H. Deng, T. Mao, and J. Pan. 2013. Flagellar regeneration requires cytoplasmic microtubule depolymerization and kinesin-13. J. Cell Sci. 126: 1531-1540. http://dx.doi.org/10.1242/jcs.124255
74. Williams, C.L., C. Li, K. Kida, P.N. Inglis, S. Mohan, L. Semenec, N.J. Bialas, R.M. Stupay, N. Chen, O.E. Blacque, et al. 2011. MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. J. Cell Biol. 192: 1023-1041. http://dx.doi.org/10.1083/jcb.201012116
75. Witman, G.B. 1975. The site of in vivo assembly of flagellar microtubules. Ann. N. Y. Acad. Sci. 253: 178-191. http://dx.doi.org/10.1111/j.1749-6632.1975.tb19199.x
76. Witman, G.B. 1986. Isolation of Chlamydomonas flagella and flagellar axonemes. Methods Enzymol. 134: 280-290. http://dx.doi.org/10.1016/0076-6879(86)34096-5
77. Wren, K.N., J.M. Craft, D. Tritschler, A. Schauer, D.K. Patel, E.F. Smith, M.E. Porter, P. Kner, and K.F. Lechtreck. 2013. A differential cargo-loading model of ciliary length regulation by IFT. Curr. Biol. 23: 2463-2471. http://dx.doi.org/10.1016/j.cub.2013.10.044
78. Ye, F., D.K. Breslow, E.F. Koslover, A.J. Spakowitz, W.J. Nelson, and M.V. Nachury. 2013. Single molecule imaging reveals a major role for diffusion in the exploration of ciliary space by signaling receptors. eLife. 2: e00654. http://dx.doi.org/10.7554/eLife.00654