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Structural basis of tubulin detyrosination by the vasohibin-SVBP enzyme complex.

Wang N, Bosc C, Ryul Choi S, Boulan B, Peris L, Olieric N, Bao H, Krichen F, Chen L, Andrieux A, Olieric V, Moutin MJ, Steinmetz MO, Huang H
Nat Struct Mol Biol 26 571-582 (2019)
Related entries: 6j4o, 6j4p, 6j4q, 6j4s, 6j4u, 6j4v

Cited: 24 times
EuropePMC logo PMID: 31235911

Abstract

Vasohibins are tubulin tyrosine carboxypeptidases that are important in neuron physiology. We examined the crystal structures of human vasohibin 1 and 2 in complex with small vasohibin-binding protein (SVBP) in the absence and presence of different inhibitors and a C-terminal α-tubulin peptide. In combination with functional data, we propose that SVBP acts as an activator of vasohibins. An extended groove and a distinctive surface residue patch of vasohibins define the specific determinants for recognizing and cleaving the C-terminal tyrosine of α-tubulin and for binding microtubules, respectively. The vasohibin-SVBP interaction and the ability of the enzyme complex to associate with microtubules regulate axon specification of neurons. Our results define the structural basis of tubulin detyrosination by vasohibins and show the relevance of this process for neuronal development. Our findings offer a unique platform for developing drugs against human conditions with abnormal tubulin tyrosination levels, such as cancer, heart defects and possibly brain disorders.

Articles - 6qby mentioned but not cited (1)

  1. VASH1-SVBP and VASH2-SVBP generate different detyrosination profiles on microtubules. Ramirez-Rios S, Choi SR, Sanyal C, Blum TB, Bosc C, Krichen F, Denarier E, Soleilhac JM, Blot B, Janke C, Stoppin-Mellet V, Magiera MM, Arnal I, Steinmetz MO, Moutin MJ. J Cell Biol 222 e202205096 (2023)


Reviews citing this publication (8)

  1. The tubulin code and its role in controlling microtubule properties and functions. Janke C, Magiera MM. Nat Rev Mol Cell Biol 21 307-326 (2020)
  2. The Tubulin Code in Microtubule Dynamics and Information Encoding. Roll-Mecak A. Dev Cell 54 7-20 (2020)
  3. Tubulin post-translational modifications control neuronal development and functions. Moutin MJ, Bosc C, Peris L, Andrieux A. Dev Neurobiol 81 253-272 (2021)
  4. The Tubulin Code in Mitosis and Cancer. Lopes D, Maiato H. Cells 9 E2356 (2020)
  5. Posttranslational modifications of the cytoskeleton. MacTaggart B, Kashina A. Cytoskeleton (Hoboken) 78 142-173 (2021)
  6. Post-translational modifications of tubulin: their role in cancers and the regulation of signaling molecules. Wattanathamsan O, Pongrakhananon V. Cancer Gene Ther 30 521-528 (2023)
  7. The microtubule cytoskeleton: An old validated target for novel therapeutic drugs. Lafanechère L. Front Pharmacol 13 969183 (2022)
  8. The Emerging Roles of Axonemal Glutamylation in Regulation of Cilia Architecture and Functions. Yang WT, Hong SR, He K, Ling K, Shaiv K, Hu J, Lin YC. Front Cell Dev Biol 9 622302 (2021)

Articles citing this publication (15)

  1. α-tubulin tail modifications regulate microtubule stability through selective effector recruitment, not changes in intrinsic polymer dynamics. Chen J, Kholina E, Szyk A, Fedorov VA, Kovalenko I, Gudimchuk N, Roll-Mecak A. Dev Cell 56 2016-2028.e4 (2021)
  2. MARK4 controls ischaemic heart failure through microtubule detyrosination. Yu X, Chen X, Amrute-Nayak M, Allgeyer E, Zhao A, Chenoweth H, Clement M, Harrison J, Doreth C, Sirinakis G, Krieg T, Zhou H, Huang H, Tokuraku K, Johnston DS, Mallat Z, Li X. Nature 594 560-565 (2021)
  3. Defective tubulin detyrosination causes structural brain abnormalities with cognitive deficiency in humans and mice. Pagnamenta AT, Heemeryck P, Martin HC, Bosc C, Peris L, Uszynski I, Gory-Fauré S, Couly S, Deshpande C, Siddiqui A, Elmonairy AA, WGS500 Consortium, Genomics England Research Consortium, Jayawant S, Murthy S, Walker I, Loong L, Bauer P, Vossier F, Denarier E, Maurice T, Maurice T, Barbier EL, Deloulme JC, Taylor JC, Taylor JC, Blair EM, Andrieux A, Moutin MJ. Hum Mol Genet 28 3391-3405 (2019)
  4. Depletion of Vasohibin 1 Speeds Contraction and Relaxation in Failing Human Cardiomyocytes. Chen CY, Salomon AK, Caporizzo MA, Curry S, Kelly NA, Bedi K, Bogush AI, Krämer E, Schlossarek S, Janiak P, Moutin MJ, Carrier L, Margulies KB, Prosser BL. Circ Res 127 e14-e27 (2020)
  5. Cryo-EM structure of VASH1-SVBP bound to microtubules. Li F, Li Y, Ye X, Gao H, Shi Z, Luo X, Rice LM, Yu H. Elife 9 e58157 (2020)
  6. Leishmania-infected macrophages release extracellular vesicles that can promote lesion development. Gioseffi A, Hamerly T, Van K, Zhang N, Dinglasan RR, Yates PA, Kima PE. Life Sci Alliance 3 e202000742 (2020)
  7. Tubulin tyrosination regulates synaptic function and is disrupted in Alzheimer's disease. Peris L, Parato J, Qu X, Soleilhac JM, Lanté F, Kumar A, Pero ME, Martínez-Hernández J, Corrao C, Falivelli G, Payet F, Gory-Fauré S, Bosc C, Blanca Ramirez M, Sproul A, Brocard J, Di Cara B, Delagrange P, Buisson A, Goldberg Y, Moutin MJ, Bartolini F, Andrieux A. Brain 145 2486-2506 (2022)
  8. Structural insights into tubulin detyrosination by vasohibins-SVBP complex. Liu X, Wang H, Zhu J, Xie Y, Liang X, Chen Z, Feng Y, Zhang Y. Cell Discov 5 65 (2019)
  9. CPR-C4 is a highly conserved novel protease from the Candidate Phyla Radiation with remote structural homology to human vasohibins. Cornish KAS, Lange J, Aevarsson A, Pohl E. J Biol Chem 298 101919 (2022)
  10. Identification and classification of papain-like cysteine proteinases. Ozhelvaci F, Steczkiewicz K. J Biol Chem 299 104801 (2023)
  11. Tubulin engineering by semi-synthesis reveals that polyglutamylation directs detyrosination. Ebberink E, Fernandes S, Hatzopoulos G, Agashe N, Chang PH, Guidotti N, Reichart TM, Reymond L, Velluz MC, Schneider F, Pourroy C, Janke C, Gönczy P, Fierz B, Aumeier C. Nat Chem 15 1179-1187 (2023)
  12. Interplay between stochastic enzyme activity and microtubule stability drives detyrosination enrichment on microtubule subsets. Tang Q, Sensale S, Bond C, Xing J, Qiao A, Hugelier S, Arab A, Arya G, Lakadamyali M. Curr Biol 33 5169-5184.e8 (2023)
  13. Structure-based virtual screening identifies small-molecule inhibitors of O-fucosyltransferase SPINDLY in Arabidopsis. Aizezi Y, Zhao H, Zhang Z, Bi Y, Yang Q, Guo G, Zhang H, Guo H, Jiang K, Wang ZY. Plant Cell 36 497-509 (2024)
  14. Targeting Vasohibins to Promote Axon Regeneration. Gobrecht P, Gebel J, Hilla A, Gisselmann G, Fischer D. J Neurosci 44 e2031232024 (2024)
  15. The crystal structure of the tetrameric human vasohibin-1-SVBP complex reveals a variable arm region within the structural core. Ikeda A, Urata S, Ando T, Suzuki Y, Sato Y, Nishino T. Acta Crystallogr D Struct Biol 76 993-1000 (2020)


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