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The structure of the complex between α-tubulin, TBCE and TBCB reveals a tubulin dimer dissociation mechanism.

Serna M, Carranza G, Martín-Benito J, Janowski R, Canals A, Coll M, Zabala JC, Valpuesta JM
J Cell Sci 128 1824-34 (2015)
Cited: 19 times
EuropePMC logo PMID: 25908846

Abstract

Tubulin proteostasis is regulated by a group of molecular chaperones termed tubulin cofactors (TBC). Whereas tubulin heterodimer formation is well-characterized biochemically, its dissociation pathway is not clearly understood. Here, we carried out biochemical assays to dissect the role of the human TBCE and TBCB chaperones in α-tubulin-β-tubulin dissociation. We used electron microscopy and image processing to determine the three-dimensional structure of the human TBCE, TBCB and α-tubulin (αEB) complex, which is formed upon α-tubulin-β-tubulin heterodimer dissociation by the two chaperones. Docking the atomic structures of domains of these proteins, including the TBCE UBL domain, as we determined by X-ray crystallography, allowed description of the molecular architecture of the αEB complex. We found that heterodimer dissociation is an energy-independent process that takes place through a disruption of the α-tubulin-β-tubulin interface that is caused by a steric interaction between β-tubulin and the TBCE cytoskeleton-associated protein glycine-rich (CAP-Gly) and leucine-rich repeat (LRR) domains. The protruding arrangement of chaperone ubiquitin-like (UBL) domains in the αEB complex suggests that there is a direct interaction of this complex with the proteasome, thus mediating α-tubulin degradation.

Reviews citing this publication (3)

  1. Genetic causes of hypomagnesemia, a clinical overview. Viering DHHM, de Baaij JHF, Walsh SB, Kleta R, Bockenhauer D. Pediatr Nephrol 32 1123-1135 (2017)
  2. An Emerging Role for Tubulin Isotypes in Modulating Cancer Biology and Chemotherapy Resistance. Parker AL, Teo WS, McCarroll JA, Kavallaris M. Int J Mol Sci 18 E1434 (2017)
  3. A conceptual view at microtubule plus end dynamics in neuronal axons. Voelzmann A, Hahn I, Pearce SP, Sánchez-Soriano N, Prokop A. Brain Res Bull 126 226-237 (2016)

Articles citing this publication (16)

  1. Tubulin cofactors and Arl2 are cage-like chaperones that regulate the soluble αβ-tubulin pool for microtubule dynamics. Nithianantham S, Le S, Seto E, Jia W, Leary J, Corbett KD, Moore JK, Al-Bassam J. Elife 4 (2015)
  2. TBCE Mutations Cause Early-Onset Progressive Encephalopathy with Distal Spinal Muscular Atrophy. Sferra A, Baillat G, Rizza T, Barresi S, Flex E, Tasca G, D'Amico A, Bellacchio E, Ciolfi A, Caputo V, Cecchetti S, Torella A, Zanni G, Diodato D, Piermarini E, Niceta M, Coppola A, Tedeschi E, Martinelli D, Dionisi-Vici C, Nigro V, Dallapiccola B, Compagnucci C, Tartaglia M, Haase G, Bertini E. Am J Hum Genet 99 974-983 (2016)
  3. A Trimer Consisting of the Tubulin-specific Chaperone D (TBCD), Regulatory GTPase ARL2, and β-Tubulin Is Required for Maintaining the Microtubule Network. Francis JW, Newman LE, Cunningham LA, Kahn RA. J Biol Chem 292 4336-4349 (2017)
  4. Dysregulation of a novel miR-1825/TBCB/TUBA4A pathway in sporadic and familial ALS. Helferich AM, Brockmann SJ, Reinders J, Deshpande D, Holzmann K, Brenner D, Andersen PM, Petri S, Thal DR, Michaelis J, Otto M, Just S, Ludolph AC, Danzer KM, Freischmidt A, Weishaupt JH. Cell Mol Life Sci 75 4301-4319 (2018)
  5. Colchicine Blocks Tubulin Heterodimer Recycling by Tubulin Cofactors TBCA, TBCB, and TBCE. Nolasco S, Bellido J, Serna M, Carmona B, Soares H, Zabala JC. Front Cell Dev Biol 9 656273 (2021)
  6. Microtubule dynamics at low temperature: evidence that tubulin recycling limits assembly. Li G, Moore JK. Mol Biol Cell 31 1154-1166 (2020)
  7. The chaperonin CCT controls T cell receptor-driven 3D configuration of centrioles. Martin-Cofreces NB, Chichon FJ, Calvo E, Torralba D, Bustos-Moran E, Dosil SG, Rojas-Gomez A, Bonzon-Kulichenko E, Lopez JA, Otón J, Sorrentino A, Zabala JC, Vernos I, Vazquez J, Valpuesta JM, Sanchez-Madrid F. Sci Adv 6 eabb7242 (2020)
  8. Tubulin Dimer Reversible Dissociation: AFFINITY, KINETICS, AND DEMONSTRATION OF A STABLE MONOMER. Montecinos-Franjola F, Schuck P, Sackett DL. J Biol Chem 291 9281-9294 (2016)
  9. Acetylated α-tubulin K394 regulates microtubule stability to shape the growth of axon terminals. Saunders HAJ, Johnson-Schlitz DM, Jenkins BV, Volkert PJ, Yang SZ, Wildonger J. Curr Biol 32 614-630.e5 (2022)
  10. Native mass spectrometry analyses of chaperonin complex TRiC/CCT reveal subunit N-terminal processing and re-association patterns. Collier MP, Moreira KB, Li KH, Chen YC, Itzhak D, Samant R, Leitner A, Burlingame A, Frydman J. Sci Rep 11 13084 (2021)
  11. Tubulin Folding Cofactor TBCB is a Target of the Salmonella Effector Protein SseK1. Araujo-Garrido JL, Baisón-Olmo F, Bernal-Bayard J, Romero F, Ramos-Morales F. Int J Mol Sci 21 E3193 (2020)
  12. Cancer Conformational Landscape Shapes Tumorigenesis. Bamberger C, Diedrich J, Martìnez-Bartholomé S, Yates JR. J Proteome Res 21 1017-1028 (2022)
  13. Tubulin-folding cofactor E deficiency promotes vascular dysfunction by increased endoplasmic reticulum stress. Efentakis P, Molitor M, Kossmann S, Bochenek ML, Wild J, Lagrange J, Finger S, Jung R, Karbach S, Schäfer K, Schulz A, Wild P, Münzel T, Wenzel P. Eur Heart J 43 488-500 (2022)
  14. Expanding the Phenotypic Spectrum of Kenny-Caffey Syndrome. Schigt H, Bald M, van der Eerden BCJ, Gal L, Ilenwabor BP, Konrad M, Levine MA, Li D, Mache CJ, Mackin S, Perry C, Rios FJ, Schlingmann KP, Storey B, Trapp CM, Verkerk AJMH, Zillikens MC, Touyz RM, Hoorn EJ, Hoenderop JGJ, de Baaij JHF. J Clin Endocrinol Metab 108 e754-e768 (2023)
  15. Genome-Wide Analysis of Tubulin Gene Family in Cassava and Expression of Family Member FtsZ2-1 during Various Stress. Li S, Cao P, Wang C, Guo J, Zang Y, Wu K, Ran F, Liu L, Wang D, Min Y. Plants (Basel) 10 668 (2021)
  16. High Expression of Microtubule-associated Protein TBCB Predicts Adverse Outcome and Immunosuppression in Acute Myeloid Leukemia. Wang B, Wang W, Li Q, Guo T, Yang S, Shi J, Yuan W, Chu Y. J Cancer 14 1707-1724 (2023)


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