Crescerin uses a TOG domain array to regulate microtubules in the primary cilium

Molecular Biology of the Cell

Volumn 26, Issue 23, 2015, Pages 4248-4264

  Das, Alakananda ^a,b   Dickinson, Daniel J ^a,b   Wood, Cameron C ^a   Goldstein, Bob ^a,b   Slep, Kevin C ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TUBULIN; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; CAENORHABDITIS ELEGANS; CRESCERIN PROTEIN FAMILY; CRYSTAL STRUCTURE; EUKARYOTIC FLAGELLUM; HOMOLOGOUS RECOMBINATION; IN VITRO STUDY; MICROTUBULE; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; AMINO ACID SEQUENCE; ANIMAL; COMPARATIVE STUDY; CONSERVED SEQUENCE; GENETICS; METABOLISM; MOLECULAR MODEL; MOUSE; NERVE CELL; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CILIA; CONSERVED SEQUENCE; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MODELS, MOLECULAR; NEURONS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; TUBULIN;

EID: 84947104535     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-08-0603     Document Type: Article

References (64)

1. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. (2010). PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66, 213-221.
2. Afonine PV, Grosse-Kunstleve RW, Echols N, Headd JJ, Moriarty NW, Mustyakimov M, Terwilliger TC, Urzhumtsev A, Zwart PH, Adams PD (2012). Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr D Biol Crystallogr 68, 352-367.
3. Akhmanova A, Hoogenraad CC, Drabek K, Stepanova T, Dortland B, Verkerk T, Vermeulen W, Burgering BM, De Zeeuw CI, Grosveld F, Galjart N (2001). CLASPs are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104, 923-935.
4. Al-Bassam J, Chang F (2011). Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP. Trends Cell Biol 21, 604-614.
5. Al-Bassam J, Kim H, Brouhard G, van Oijen A, Harrison SC, Chang F (2010). CLASP promotes microtubule rescue by recruiting tubulin dimers to the microtubule. Dev Cell 19, 245-258.
6. Al-Bassam J, Larsen NA, Hyman AA, Harrison SC (2007). Crystal structure of a TOG domain: conserved features of XMAP215/Dis1-family TOG domains and implications for tubulin binding. Structure 15, 355-362.
7. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990). Basic local alignment search tool. J Mol Biol 215, 403-410.
8. Ayaz P, Ye X, Huddleston P, Brautigam CA, Rice LM (2012). A TOG: αβ-tubulin complex structure reveals conformation-based mechanisms for a microtubule polymerase. Science 337, 857-860.
9. Bacaj T, Lu Y, Shaham S (2008). The conserved proteins CHE-12 and DYF-11 are required for sensory cilium function in Caenorhabditis elegans. Genetics 178, 989-1002.
10. Bargmann CI (2006). Chemosensation in C. elegans. WormBook 2009 (Oct25), 1-29.
11. Bargmann CI, Horvitz HR (1991). Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7, 729-742.
12. Bhogaraju S, Cajanek L, Fort C, Blisnick T, Weber K, Taschner M, Mizuno N, Lamla S, Bastin P, Nigg EA, Lorentzen E (2013). Molecular basis of tubulin transport within the cilium by IFT74 and IFT81. Science 341, 1009-1012.
13. Brittle AL, Ohkura H (2005). Mini spindles, the XMAP215 homologue, suppresses pausing of interphase microtubules in Drosophila. EMBO J 24, 1387-1396.
14. Buchan DWA, Minneci F, Nugent TCO, Bryson K, Jones DT (2013). Scalable web services for the PSIPRED Protein Analysis Workbench. Nucleic Acids Res 41, W349-W357.
15. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC (2010). MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66, 12-21.
16. Christensen ST, Pedersen S F, Satir P, Veland IR, Schneider L (2008). The primary cilium coordinates signaling pathways in cell cycle control and migration during development and tissue repair. Curr Top Dev Biol 85, 261-301.
17. Cole C, Barber JD, Barton GJ (2008). The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36, W197-W201.
18. Craft JM, Harris JA, Hyman S, Kner P, Lechtreck KF (2015). Tubulin transport by IFT is upregulated during ciliary growth by a cilium-autonomous mechanism. J Cell Biol 208, 223-237.
19. Currie JD, Stewman S, Schimizzi G, Slep KC, Ma A, Rogers SL (2011). The microtubule lattice and plus-end association of Drosophila Mini spindles is spatially regulated to fine-tune microtubule dynamics. Mol Biol Cell 22, 4343-4361.
20. De La Mora-Rey T, Guenther BD, Finzel BC (2013). The structure of the TOG-like domain of Drosophila melanogaster Mast/Orbit. Acta Crystallogr F Struct Biol Cryst Commun 69, 723-729.
21. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard J F, Guindon S, Lefort V, Lescot M, et al. (2008). Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36, W465-W469.
22. Dickinson DJ, Ward JD, Reiner DJ, Goldstein B (2013). Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat Methods 10, 1028-1034.
23. Drabek K, van Ham M, Stepanova T, Draegestein K, van Horssen R, Sayas CL, Akhmanova A, Ten Hagen T, Smits R, Fodde R, et al. (2006). Role of CLASP2 in microtubule stabilization and the regulation of persistent motility. Curr Biol 16, 2259-2264.
24. Fox JN, Currie JD, Rogers SL, Slep KC (2014). The XMAP215 family drives microtubule polymerization using a structurally diverse TOG array. Mol Biol Cell 25, 2375-2392.
25. Grosse-Kunstleve RW, Adams PD (2003). Substructure search procedures for macromolecular structures. Acta Crystallogr D Biol Crystallogr 59, 1966-1973.
26. Hao L, Thein M, Brust-Mascher I, Civelekoglu-Scholey G, Lu Y, Acar S, Prevo B, Shaham S, Scholey JM (2011). Intraflagellar transport delivers tubulin isotypes to sensory cilium middle and distal segments. Nat Cell Biol 13, 790-798.
27. Hoey DA, Downs ME, Jacobs CR (2012). The mechanics of the primary cilium: an intricate structure with complex function. J Biomech 45, 17-26.
28. Holm L, Rosenström P (2010). DALI server: conservation mapping in 3D. Nucleic Acids Res 38, W545-W549.
29. Ishikawa T (2012). Structural biology of cytoplasmic and axonemal dyneins. J Struct Biol 179, 229-234.
30. Jensen-Smith HC, Ludueña RF, Hallworth R (2003). Requirement for the betaI and betaIV tubulin isotypes in mammalian cilia. Cell Motil. Cytoskeleton 55, 213-220.
31. Jones DT (1999). Protein secondary structure prediction based on positionspecific scoring matrices. J Mol Biol 292, 195-202.
32. Kim E, Sun L, Gabel CV, Fang-Yen C (2013). Long-term imaging of Caenorhabditis elegans using nanoparticle-mediated immobilization. PLoS One 8, 1-6.
33. Kobayashi D, Takeda H (2012). Ciliary motility: the components and cytoplasmic preassembly mechanisms of the axonemal dyneins. Differentiation 83, S23-S29.
34. Leano JB, Rogers SL, Slep KC (2013). A cryptic TOG domain with a distinct architecture underlies CLASP-dependent bipolar spindle formation. Structure 21, 939-950.
35. Ludington WB, Ishikawa H, Serebrenik YV, Ritter A, Hernandez-Lopez RA, Gunzenhauser J, Kannegaard E, Marshall WF (2015). A systematic comparison of mathematical models for inherent measurement of ciliary length: how a cell can measure length and volume. Biophys J 108, 1361-1379.
36. Luo L, Wen Q, Ren J, Hendricks M, Gershow M, Qin Y, Greenwood J, Soucy ER, Klein M, Smith-Parker HK, et al. (2014). Dynamic encoding of perception, memory, and movement in a C. elegans chemotaxis circuit. Neuron 82, 1115-1128.
37. Marshall WF (2008). The cell biological basis of ciliary disease. J Cell Biol 180, 17-21.
38. Marshall W F, Nonaka S (2006). Cilia: tuning in to the cell's antenna. Curr Biol 16, R604-R614.
39. Marshall WF, Rosenbaum JL (2001). Intraflagellar transport balances continuous turnover of outer doublet microtubules: Implications for flagellar length control. J Cell Biol 155, 405-414.
40. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007). Phaser crystallographic software. J Appl Crystallogr 40, 658-674.
41. Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991). Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10, 3959-3970.
42. Moriarty NW, Grosse-Kunstleve RW, Adams PD (2009). Electronic ligand builder and optimization workbench (eLBOW): A tool for ligand coordinate and restraint generation. Acta Crystallogr D Biol Crystallogr 65, 1074-1080.
43. Mukhopadhyay S, Lu Y, Shaham S, Sengupta P (2008). Sensory signalingdependent remodeling of olfactory cilia architecture in C. elegans. Dev Cell 14, 762-774.
44. Otwinowski Z, Minor W (1997). Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276, 307-326.
45. Patel K, Nogales E, Heald R (2012). Multiple domains of human CLASP contribute to microtubule dynamics and organization in vitro and in Xenopus egg extracts. Cytoskeleton 69, 155-165.
46. Péchart I, Kann ML, Levilliers N, Bré MH, Fouquet JP (1999). Composition and organization of tubulin isoforms reveals a variety of axonemal models. Biol Cell 91, 685-697.
47. Perkins LA, Hedgecock EM, Thomson JN, Culotti JG (1986). Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 117, 456-487.
48. Rich DR, Clark AL (2012). Chondrocyte primary cilia shorten in response to osmotic challenge and are sites for endocytosis. Osteoarthritis. Cartilage 20, 923-930.
49. Satir P, Christensen ST (2007). Overview of structure and function of mammalian cilia. Annu Rev Physiol 69, 377-400.
50. Satir P, Christensen ST (2008). Structure and function of mammalian cilia. Histochem Cell Biol 129, 687-693.
51. Scholey JM (2003). Intraflagellar transport. Annu Rev Cell Dev Biol 19, 423-443.
52. Scholey JM (2008). Intraflagellar transport motors in cilia: moving along the cell's antenna. J Cell Biol 180, 23-29.
53. Slep KC (2009). The role of TOG domains in microtubule plus end dynamics. Biochem Soc Trans 37, 1002-1006.
54. Slep KC, Vale RD (2007). Structural basis of microtubule plus end tracking by XMAP215, CLIP-170, and EB1. Mol Cell 27, 976-991.
55. Sousa A, Reis R, Sampaio P, Sunkel CE (2007). The Drosophila CLASP homologue, Mast/Orbit regulates the dynamic behaviour of interphase microtubules by promoting the pause state. Cell Motil Cytoskeleton 64, 605-620.
56. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30, 2725-2729.
57. Terwilliger T (2004). SOLVE and RESOLVE: automated structure solution, density modification, and model building. J Synchrotron Radiat 11, 49-52.
58. Terwilliger TC, Grosse-Kunstleve RW, Afonine PV, Moriarty NW, Adams PD, Read RJ, Zwart PH, Hung LW (2008). Iterative-build OMIT maps: map improvement by iterative model building and refinement without model bias. Acta Crystallogr D Biol Crystallogr 64, 515-524.
59. Terwilliger TC, Grosse-Kunstleve RW, Afonine PV, Moriarty NW, Zwart PH, Hung LW, Read RJ, Adams PD (2007). Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Acta Crystallogr D Biol Crystallogr 64, 61-69.
60. Tilney LG, Gibbins JR (1968). Differential effects of antimitotic agents on the stability and behavior of cytoplasmic and ciliary microtubules. Protoplasma 65, 167-179.
61. Veland IR, Awan A, Pedersen LB, Yoder BK, Christensen ST (2009). Primary cilia and signaling pathways in mammalian development, health and disease. Nephron Physiol 111, p39-53.
62. Ward S (1973). Chemotaxis by the nematode Caenorhabditis elegans: identification of attractants and analysis of the response by use of mutants. Proc Natl Acad Sci USA 70, 817-821.
63. Widlund PO, Stear JH, Pozniakovsky A, Zanic M, Reber S, Brouhard GJ, Hyman AA, Howard J (2011). XMAP215 polymerase activity is built by combining multiple tubulin-binding TOG domains and a basic latticebinding region. Proc Natl Acad Sci USA 108, 2741-2746.
64. Zwart PH, Grosse-Kunstleve RW, Adams PD (2005). Xtriage and Fest: automatic assessment of X-ray data and substructure structure factor estimation. CCP4 Newsl 43, 27-35.