Tubulin cofactors and Arl2 are cage-like chaperones that regulate the soluble αβ-tubulin pool for microtubule dynamics

eLife

Volumn 4, Issue JULY2015, 2015, Pages

  Nithianantham, Stanley ^a   Le, Sinh ^a   Seto, Elbert ^a   Jia, Weitao ^a   Leary, Julie ^a   Corbett, Kevin D ^b,c   Moore, Jeffrey K ^d   Al Bassam, Jawdat ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; ARL2 GUANOSINE TRIPHOSPHATASE PROTEIN; BETA TUBULIN; CHAPERONE; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; PEPTIDES AND PROTEINS; TUBULIN BINDING COFACTOR C; TUBULIN BINDING COFACTOR D; TUBULIN BINDING COFACTOR E; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ARF3 PROTEIN, S CEREVISIAE; CIN1 PROTEIN, S CEREVISIAE; MICROTUBULE ASSOCIATED PROTEIN; PAC2 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; TBCC PROTEIN, S CEREVISIAE; TBCD PROTEIN, S CEREVISIAE; TBCE PROTEIN, HUMAN; TUBULIN;

ARTICLE; CELL STRUCTURE; CYTOLOGY; ELECTRON MICROSCOPY; ENZYME ACTIVITY; HOMEOSTASIS; HUMAN; MICROTUBULE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN HYDROLYSIS; X RAY CRYSTALLOGRAPHY; METABOLISM; PHYSIOLOGY; PROTEIN MULTIMERIZATION; SACCHAROMYCES CEREVISIAE;

ADP-RIBOSYLATION FACTORS; MICROSCOPY, ELECTRON; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MOLECULAR CHAPERONES; PROTEIN MULTIMERIZATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TUBULIN;

EID: 84939516782     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.08811.001     Document Type: Article

References (65)

1. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica. Section D, Biological Crystallography 66: 213-221. doi: 10. 1107/S0907444909052925.
2. Akhmanova A, Steinmetz MO. 2008. Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nature Reviews Molecular Cell Biology 9: 309-322. doi: 10. 1038/nrm2369.
3. Alushin GM, Lander GC, Kellogg EH, Zhang R, Baker D, Nogales E. 2014. High-resolution microtubule structures reveal the structural transitions in alphabeta-tubulin upon GTP hydrolysis. Cell 157: 1117-1129. doi: 10. 1016/j. cell. 2014. 03. 053.
4. Amberg DC, Burke DJ, Strathern JN. 2005. Methods in Yeast Genetics. New York: Cold Spring Harbor Laboratory Press.
5. Antoshechkin I, Han M. 2002. The C. elegans evl-20 gene is a homolog of the small GTPase ARL2 and regulates cytoskeleton dynamics during cytokinesis and morphogenesis. Developmental Cell 2: 579-591. doi: 10. 1016/S1534-5807(02)00146-6.
6. Archer JE, Magendantz M, Vega LR, Solomon F. 1998. Formation and function of the Rbl2p-beta-tubulin complex. Molecular and Cellular Biology 18: 1757-1762.
7. Bhamidipati A, Lewis SA, Cowan NJ. 2000. ADP ribosylation factor-like protein 2 (Arl2) regulates the interaction of tubulin-folding cofactor D with native tubulin. The Journal of Cell Biology 149: 1087-1096. doi: 10. 1083/jcb. 149. 5. 1087.
8. Brouhard GJ, Rice LM. 2014. The contribution of alphabeta-tubulin curvature to microtubule dynamics. The Journal of Cell Biology 207: 323-334. doi: 10. 1083/jcb. 201407095.
9. Caplow M, Fee L. 2002. Dissociation of the tubulin dimer is extremely slow, thermodynamically very unfavorable, and reversible in the absence of an energy source. Molecular Biology of the Cell 13: 2120-2131. doi: E01-10-0089.
10. Cleveland DW. 1989. Autoregulated control of tubulin synthesis in animal cells. Current Opinion in Cell Biology 1: 10-14. doi: 10. 1016/S0955-0674(89)80030-4.
11. Cleveland DW, Kirschner MW, Cowan NJ. 1978. Isolation of separate mRNAs for alpha-and beta-tubulin and characterization of the corresponding in vitro translation products. Cell 15: 1021-1031. doi: 10. 1016/0092-8674 (78)90286-6.
12. Cook A, Fernandez E, Lindner D, Ebert J, Schlenstedt G, Conti E. 2005a. The exportin Cse1 in its cargo-free, cytoplasmic state. RCSB Protein Data Bank 1Z3H. http://www. rcsb. org/pdb/explore. do?structureId=1z3h.
13. Cook A, Fernandez E, Lindner D, Ebert J, Schlenstedt G, Conti E. 2005b. The structure of the nuclear export receptor Cse1 in its cytosolic state reveals a closed conformation incompatible with cargo binding. Molecular Cell 18: 355-367. doi: 10. 1016/j. molcel. 2005. 03. 021.
14. Elie-Caille C, Severin F, Helenius J, Howard J, Muller DJ, Hyman AA. 2007. Straight GDP-tubulin protofilaments form in the presence of taxol. Current Biology 17: 1765-1770. doi: 10. 1016/j. cub. 2007. 08. 063.
15. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallographica. Section D, Biological Crystallography 66: 486-501. doi: 10. 1107/S0907444910007493.
16. Feierbach B, Nogales E, Downing KH, Stearns T. 1999. Alf1p, a CLIP-170 domain-containing protein, is functionally and physically associated with alpha-tubulin. The Journal of Cell Biology 144: 113-124. doi: 10. 1083/jcb. 144. 1. 113.
17. Fleming JA, Vega LR, Solomon F. 2000. Function of tubulin binding proteins in vivo. Genetics 156: 69-80.
18. Fleming JR, Morgan RE, Fyfe PK, Kelly SM, Hunter WN. 2013a. Trypansoma brucei tubulin binding cofactor B CAPGly domain. RCSB Protein Data Bank 4B6M. http://www. rcsb. org/pdb/explore/explore. do?structureId=4B6M.
19. Fleming JR, Morgan RE, Fyfe PK, Kelly SM, Hunter WN. 2013b. Architecture of Trypanosoma brucei Tubulin-Binding cofactor B. RCSB Protein Data Bank 4B6W. http://www. rcsb. org/pdb/explore/explore. do? structureId=4B6W.
20. Fleming JR, Morgan RE, Fyfe PK, Kelly SM, Hunter WN. 2013c. The architecture of Trypanosoma brucei tubulinbinding cofactor B and implications for function. The FEBS Journal 280: 3270-3280. doi: 10. 1111/febs. 12308.
21. Garcia-Mayoral MF, Castano R, Fanarraga ML, Zabala JC, Rico M, Bruix M. 2011. The solution structure of the Nterminal domain of human tubulin binding cofactor C reveals a platform for tubulin interaction. PLoS ONE 6: e25912. doi: 10. 1371/journal. pone. 0025912.
22. Grigorieff N. 2007. FREALIGN: high-resolution refinement of single particle structures. Journal of Structural Biology 157: 117-125. doi: 10. 1016/j. jsb. 2006. 05. 004.
23. Hanzal-Bayer M, Renault L, Roversi P, Wittinghofer A, Hillig RC. 2002a. Complex of Arl2 and PDE delta, Crystal Form 2 (SeMet). RCSB Protein Data Bank 1KSJ. http://www. rcsb. org/pdb/explore/explore. do?structureId=1KSJ.
24. Hanzal-Bayer M, Renault L, Roversi P, Wittinghofer A, Hillig RC. 2002b. The complex of Arl2-GTP and PDE delta: from structure to function. The EMBO Journal 21: 2095-2106. doi: 10. 1093/emboj/21. 9. 2095.
25. Hoyt MA, Macke JP, Roberts BT, Geiser JR. 1997. Saccharomyces cerevisiae PAC2 functions with CIN1, 2 and 4 in a pathway leading to normal microtubule stability. Genetics 146: 849-857.
26. Hoyt MA, Stearns T, Botstein D. 1990. Chromosome instability mutants of Saccharomyces cerevisiae that are defective in microtubule-mediated processes. Molecular and Cellular Biology 10: 223-234.
27. Jin S, Pan L, Liu Z, Wang Q, Xu Z, Zhang YQ. 2009. Drosophila Tubulin-specific chaperone E functions at neuromuscular synapses and is required for microtubule network formation. Development 136: 1571-1581. doi: 10. 1242/dev. 029983.
28. Kuhnel K, Veltel S, Schlichting I, Wittinghofer A. 2006. Crystal structure of the human retinitis pigmentosa 2 protein and its interaction with Arl3. Structure 14: 367-378. doi: 10. 1016/j. str. 2005. 11. 008.
29. Lacefield S, Magendantz M, Solomon F. 2006. Consequences of defective tubulin folding on heterodimer levels, mitosis and spindle morphology in Saccharomyces cerevisiae. Genetics 173: 635-646. doi: 10. 1534/genetics. 105. 055160.
30. Leonard M, Song BD, Ramachandran R, Schmid SL. 2005. Robust colorimetric assays for dynamin's basal and stimulated GTPase activities. Methods in Enzymology 404: 490-503. doi: 10. 1016/S0076-6879(05)04043-7.
31. Lewis SA, Tian G, Cowan NJ. 1997. The alpha-and beta-tubulin folding pathways. Trends in Cell Biology 7: 479-484. doi: 10. 1016/S0962-8924(97)01168-9.
32. Lowe J, Li H, Downing KH, Nogales E. 2001. Refined structure of alpha-beta tubulin from zinc-induced sheets stabilized with taxol. RCSB Protein Data Bank 1JFF. http://www. rcsb. org/pdb/explore/explore. do? structureId=1JFF.
33. Lundin VF, Leroux MR, Stirling PC. 2010. Quality control of cytoskeletal proteins and human disease. Trends in Biochemical Sciences 35: 288-297. doi: 10. 1016/j. tibs. 2009. 12. 007.
34. Lyumkis D, Brilot AF, Theobald DL, Grigorieff N. 2013. Likelihood-based classification of cryo-EM images using FREALIGN. Journal of Structural Biology 183: 377-388. doi: 10. 1016/j. jsb. 2013. 07. 005.
35. Mori R, Toda T. 2013. The dual role of fission yeast Tbc1/cofactor C orchestrates microtubule homeostasis in tubulin folding and acts as a GAP for GTPase Alp41/Arl2. Molecular Biology of the Cell 24: 1713-1724. S1711-1718. doi: 10. 1091/mbc. E12-11-0792.
36. Moore JK, Sept D, Cooper JA. 2009. Neurodegeneration mutations in dynactin impair dynein-dependent nuclear migration. Proceedings of the National Academy of Sciences of USA 106: 5147-5152. doi: 10. 1073/pnas. 0810828106.
37. Newman LE, Zhou CJ, Mudigonda S, Mattheyses AL, Paradies E, Marobbio CM, Kahn RA. 2014. The ARL2 GTPase is required for mitochondrial morphology, motility, and maintenance of ATP levels. PLoS ONE 9: e99270. doi: 10. 1371/journal. pone. 0099270.
38. Nogales E, Whittaker M, Milligan RA, Downing KH. 1999. High-resolution model of the microtubule. Cell 96: 79-88. doi: 10. 1016/S0092-8674(00)80961-7.
39. Paciucci R. 1994. Role of 300 kDa complexes as intermediates in tubulin folding and dimerization: characterization of a 25 kDa cytosolic protein involved in the GTP-dependent release of monomeric tubulin. The Biochemical Journal 301: 105-110.
40. Park BS, Song DH, Kim HM, Choi B-S, Lee H, Lee J-O. 2009a. Crystal structure of the human TLR4-human MD-2-E. coli LPS Ra complex. RCSB Protein Data Bank 3FXI. http://www. rcsb. org/pdb/explore/explore. do? structureId=3FXI.
41. Park BS, Song DH, Kim HM, Choi BS, Lee H, Lee JO. 2009b. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458: 1191-1195. doi: 10. 1038/nature07830.
42. Parvari R, Hershkovitz E, Grossman N, Gorodischer R, Loeys B, Zecic A, Mortier G, Gregory S, Sharony R, Kambouris M, Sakati N, Meyer BF, Al Aqeel AI, Al Humaidan AK, Al Zanhrani F, Al Swaid A, Al Othman J, Diaz GA, Weiner R, Khan KT, Gordon R, Gelb BD, HRD/Autosomal Recessive Kenny-Caffey SyndromeConsortium. 2002. Mutation of TBCE causes hypoparathyroidism-retardation-dysmorphism and autosomal recessive Kenny-Caffey syndrome. Nature Genetics 32: 448-452. doi: 10. 1038/ng1012.
43. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. Journal of Computational Chemistry 25: 1605-1612. doi: 10. 1002/jcc. 20084.
44. Prasad AR, Luduena RF, Horowitz PM. 1986. Bis(8-anilinonaphthalene-1-sulfonate) as a probe for tubulin decay. Biochemistry 25: 739-742. doi: 10. 1021/bi00351a035.
45. Powell HR, Johnson O, Leslie AG. 2013. Autoindexing diffraction images with iMosflm. Acta Crystallographica. Section D, Biological Crystallography 69: 1195-1203. doi: 10. 1107/S0907444912048524.
46. Radcliffe PA, Hirata D, Vardy L, Toda T. 1999. Functional dissection and hierarchy of tubulin-folding cofactor homologues in fission yeast. Molecular Biology of the Cell 10: 2987-3001. doi: 10. 1091/mbc. 10. 9. 2987.
47. Radcliffe PA, Vardy L, Toda T. 2000. A conserved small GTP-binding protein Alp41 is essential for the cofactordependent biogenesis of microtubules in fission yeast. FEBS Letters 468: 84-88. doi: 10. 1016/S0014-5793(00) 01202-3.
48. Sackett DL, Knutson JR, Wolff J. 1990. Hydrophobic surfaces of tubulin probed by time-resolved and steady-state fluorescence of nile red. The Journal of Biological Chemistry 265: 14899-14906.
49. Sackett DL, Lippoldt RE. 1991. Thermodynamics of reversible monomer-dimer association of tubulin. Biochemistry 30: 3511-3517. doi: 10. 1021/bi00228a023.
50. Serna M, Carranza G, Martín-Benito J, Janowski R, Canals A, Coll M, Zabala JC, Valpuesta JM. 2015. The structure of the complex between alpha-tubulin, TBCE and TBCB reveals a tubulin dimer dissociation mechanism. Journal of Cell Science 128: 1824-1834. doi: 10. 1242/jcs. 167387.
51. Shaikh TR, Gao H, Baxter WT, Asturias FJ, Boisset N, Leith A, Frank J. 2008. SPIDER image processing for singleparticle reconstruction of biological macromolecules from electron micrographs. Nature Protocols 3: 1941-1974. doi: 10. 1038/nprot. 2008. 156.
52. Sorzano CO, Marabini R, Velazquez-Muriel J, Bilbao-Castro JR, Scheres SH, Carazo JM, Pascual-Montano A. 2004. XMIPP: a new generation of an open-source image processing package for electron microscopy. Journal of Structural Biology 148: 194-204. doi: 10. 1016/j. jsb. 2004. 06. 006.
53. Stearns T. 1990. The yeast microtubule cytoskeleton: genetic approaches to structure and function. Cell Motility and the Cytoskeleton 15: 1-6. doi: 10. 1002/cm. 970150102.
54. Steinborn K, Maulbetsch C, Priester B, Trautmann S, Pacher T, Geiges B, Küttner F, Lepiniec L, Stierhof YD, Schwarz H, Jürgens G, Mayer U. 2002. The Arabidopsis PILZ group genes encode tubulin-folding cofactor orthologs required for cell division but not cell growth. Genes & Development 16: 959-971. doi: 10. 1101/gad. 221702.
55. Tan S, Kern RC, Selleck W. 2005. The pST44 polycistronic expression system for producing protein complexes in Escherichia coli. Protein Expression and Purification 40: 385-395. doi: 10. 1016/j. pep. 2004. 12. 002.
56. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, Rees I, Ludtke SJ. 2007. EMAN2: an extensible image processing suite for electron microscopy. Journal of Structural Biology 157: 38-46. doi: 10. 1016/j. jsb. 2006. 05. 009.
57. Tarazona MP, Saiz E. 2003. Combination of SEC/MALS experimental procedures and theoretical analysis for studying the solution properties of macromolecules. Journal of Biochemical and Biophysical Methods 56: 95-116. doi: 10. 1016/S0165-022X(03)00075-7.
58. Terwilliger TC, Berendzen J. 1999. Automated MAD and MIR structure solution. Acta Crystallographica. Section D, Biological Crystallography 55: 849-861. doi: 10. 1107/S0907444999000839.
59. Tian G, Bhamidipati A, Cowan NJ, Lewis SA. 1999. Tubulin folding cofactors as GTPase-activating proteins. GTP hydrolysis and the assembly of the alpha/beta-tubulin heterodimer. The Journal of Biological Chemistry 274: 24054-24058. doi: 10. 1074/jbc. 274. 34. 24054.
60. Tian G, Cowan NJ. 2013. Tubulin-specific chaperones: components of a molecular machine that assembles the alpha/beta heterodimer. Methods in Cell Biology 115: 155-171. doi: 10. 1016/B978-0-12-407757-7. 00011-6.
61. Tian G, Huang Y, Rommelaere H, Vandekerckhove J, Ampe C, Cowan NJ. 1996. Pathway leading to correctly folded beta-tubulin. Cell 86: 287-296. doi: 10. 1016/S0092-8674(00)80100-2.
62. Tian G, Lewis SA, Feierbach B, Stearns T, Rommelaere H, Ampe C, Cowan NJ. 1997. Tubulin subunits exist in an activated conformational state generated and maintained by protein cofactors. The Journal of Cell Biology 138: 821-832. doi: 10. 1083/jcb. 138. 4. 821.
63. Tian G, Thomas S, Cowan NJ. 2010. Effect of TBCD and its regulatory interactor Arl2 on tubulin and microtubule integrity. Cytoskeleton 67: 706-714. doi: 10. 1002/cm. 20480.
64. Veltel S, Gasper R, Eisenacher E, Wittinghofer A. 2008. The retinitis pigmentosa 2 gene product is a GTPase-activating protein for Arf-like 3. Nature Structural & Molecular Biology 15: 373-380. doi: 10. 1038/nsmb. 1396.
65. Wang W, Ding J, Allen E, Zhu P, Zhang L, Vogel H, Yang Y. 2005. Gigaxonin interacts with tubulin folding cofactor B and controls its degradation through the ubiquitin-proteasome pathway. Current Biology 15: 2050-2055. doi: 10. 1016/j. cub. 2005. 10. 052.