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Linkage via K27 Bestows Ubiquitin Chains with Unique Properties among Polyubiquitins.

Castañeda CA, Dixon EK, Walker O, Chaturvedi A, Nakasone MA, Curtis JE, Reed MR, Krueger S, Cropp TA, Fushman D
Structure 24 423-36 (2016)
Cited: 33 times
EuropePMC logo PMID: 26876099

Abstract

Polyubiquitination, a critical protein post-translational modification, signals for a diverse set of cellular events via the different isopeptide linkages formed between the C terminus of one ubiquitin (Ub) and the ɛ-amine of K6, K11, K27, K29, K33, K48, or K63 of a second Ub. We assembled di-ubiquitins (Ub2) comprising every lysine linkage and examined them biochemically and structurally. Of these, K27-Ub2 is unique as it is not cleaved by most deubiquitinases. As this remains the only structurally uncharacterized lysine linkage, we comprehensively examined the structures and dynamics of K27-Ub2 using nuclear magnetic resonance, small-angle neutron scattering, and in silico ensemble modeling. Our structural data provide insights into the functional properties of K27-Ub2, in particular that K27-Ub2 may be specifically recognized by K48-selective receptor UBA2 domain from proteasomal shuttle protein hHR23a. Binding studies and mutagenesis confirmed this prediction, further highlighting structural/recognition versatility of polyubiquitins and the potential power of determining function from elucidation of conformational ensembles.

Articles - 5ujl mentioned but not cited (1)

  1. K27-linked ubiquitylation promotes p97 substrate processing and is essential for cell proliferation. Shearer RF, Typas D, Coscia F, Schovsbo S, Kruse T, Mund A, Mailand N. EMBO J 41 e110145 (2022)


Reviews citing this publication (10)

  1. The recognition of ubiquitinated proteins by the proteasome. Grice GL, Nathan JA. Cell Mol Life Sci 73 3497-3506 (2016)
  2. Playing with the Molecules of Life. Young DD, Schultz PG. ACS Chem Biol 13 854-870 (2018)
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  4. RAP80, ubiquitin and SUMO in the DNA damage response. Lombardi PM, Matunis MJ, Wolberger C. J Mol Med (Berl) 95 799-807 (2017)
  5. The diversity of linkage-specific polyubiquitin chains and their role in synaptic plasticity and memory formation. Musaus M, Navabpour S, Jarome TJ. Neurobiol Learn Mem 174 107286 (2020)
  6. Structural Insights into Ankyrin Repeat-Containing Proteins and Their Influence in Ubiquitylation. Kane EI, Spratt DE. Int J Mol Sci 22 E609 (2021)
  7. Segmental and site-specific isotope labelling strategies for structural analysis of posttranslationally modified proteins. Vogl DP, Conibear AC, Becker CFW. RSC Chem Biol 2 1441-1461 (2021)
  8. Acute Myeloid Leukemia-Related Proteins Modified by Ubiquitin and Ubiquitin-like Proteins. Park SS, Baek KH. Int J Mol Sci 23 514 (2022)
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Articles citing this publication (22)

  1. Ubiquitin Modulates Liquid-Liquid Phase Separation of UBQLN2 via Disruption of Multivalent Interactions. Dao TP, Kolaitis RM, Kim HJ, O'Donovan K, Martyniak B, Colicino E, Hehnly H, Taylor JP, Castañeda CA. Mol Cell 69 965-978.e6 (2018)
  2. ALS-Linked Mutations Affect UBQLN2 Oligomerization and Phase Separation in a Position- and Amino Acid-Dependent Manner. Dao TP, Martyniak B, Canning AJ, Lei Y, Colicino EG, Cosgrove MS, Hehnly H, Castañeda CA. Structure 27 937-951.e5 (2019)
  3. Atomistic modelling of scattering data in the Collaborative Computational Project for Small Angle Scattering (CCP-SAS). Perkins SJ, Wright DW, Zhang H, Brookes EH, Chen J, Irving TC, Krueger S, Barlow DJ, Edler KJ, Scott DJ, Terrill NJ, King SM, Butler PD, Curtis JE. J Appl Crystallogr 49 1861-1875 (2016)
  4. Branching via K11 and K48 Bestows Ubiquitin Chains with a Unique Interdomain Interface and Enhanced Affinity for Proteasomal Subunit Rpn1. Boughton AJ, Krueger S, Fushman D. Structure 28 29-43.e6 (2020)
  5. Structure of hRpn10 Bound to UBQLN2 UBL Illustrates Basis for Complementarity between Shuttle Factors and Substrates at the Proteasome. Chen X, Ebelle DL, Wright BJ, Sridharan V, Hooper E, Walters KJ. J Mol Biol 431 939-955 (2019)
  6. Practical Chemical Synthesis of Atypical Ubiquitin Chains by Using an Isopeptide-Linked Ub Isomer. Tang S, Liang LJ, Si YY, Gao S, Wang JX, Liang J, Mei Z, Zheng JS, Liu L. Angew Chem Int Ed Engl 56 13333-13337 (2017)
  7. LATS1 but not LATS2 represses autophagy by a kinase-independent scaffold function. Tang F, Gao R, Jeevan-Raj B, Wyss CB, Kalathur RKR, Piscuoglio S, Ng CKY, Hindupur SK, Nuciforo S, Dazert E, Bock T, Song S, Buechel D, Morini MF, Hergovich A, Matthias P, Lim DS, Terracciano LM, Heim MH, Hall MN, Christofori G. Nat Commun 10 5755 (2019)
  8. Porcine RING Finger Protein 114 Inhibits Classical Swine Fever Virus Replication via K27-Linked Polyubiquitination of Viral NS4B. Zhang Y, Zhang H, Zheng GL, Yang Q, Yu S, Wang J, Li S, Li LF, Qiu HJ. J Virol 93 e01248-19 (2019)
  9. A diubiquitin-based photoaffinity probe for profiling K27-linkage targeting deubiquitinases. Tan XD, Pan M, Gao S, Zheng Y, Shi J, Li YM. Chem Commun (Camb) 53 10208-10211 (2017)
  10. Mechanistic insights into enhancement or inhibition of phase separation by different polyubiquitin chains. Dao TP, Yang Y, Presti MF, Cosgrove MS, Hopkins JB, Ma W, Loh SN, Castañeda CA. EMBO Rep 23 e55056 (2022)
  11. Towards a molecular basis of ubiquitin signaling: A dual-scale simulation study of ubiquitin dimers. Berg A, Kukharenko O, Scheffner M, Peter C. PLoS Comput Biol 14 e1006589 (2018)
  12. Deubiquitinating enzymes and the proteasome regulate preferential sets of ubiquitin substrates. Trulsson F, Akimov V, Robu M, van Overbeek N, Berrocal DAP, Shah RG, Cox J, Shah GM, Blagoev B, Vertegaal ACO. Nat Commun 13 2736 (2022)
  13. Branched ubiquitin chain binding and deubiquitination by UCH37 facilitate proteasome clearance of stress-induced inclusions. Song A, Hazlett Z, Abeykoon D, Dortch J, Dillon A, Curtiss J, Martinez SB, Hill CP, Yu C, Huang L, Fushman D, Cohen RE, Yao T. Elife 10 e72798 (2021)
  14. Characterization of the deubiquitination activity and substrate specificity of the chicken ubiquitin-specific protease 1/USP associated factor 1 complex. Zheng H, Wang M, Zhao C, Wu S, Yu P, Lü Y, Wang T, Ai Y. PLoS One 12 e0186535 (2017)
  15. Conformational and functional characterization of artificially conjugated non-canonical ubiquitin dimers. Schneider T, Berg A, Ulusoy Z, Gamerdinger M, Peter C, Kovermann M. Sci Rep 9 19991 (2019)
  16. Unveiling the Structural and Dynamic Nature of the Ubiquitin Code. Di Lello P, Hymowitz SG. Structure 24 498-499 (2016)
  17. Diubiquitin-Based NMR Analysis: Interactions Between Lys6-Linked diUb and UBA Domain of UBXN1. Shahul Hameed D, van Tilburg GBA, Merkx R, Flierman D, Wienk H, El Oualid F, Hofmann K, Boelens R, Ovaa H. Front Chem 7 921 (2019)
  18. Electrostatic and steric effects underlie acetylation-induced changes in ubiquitin structure and function. Kienle SM, Schneider T, Stuber K, Globisch C, Jansen J, Stengel F, Peter C, Marx A, Kovermann M, Scheffner M. Nat Commun 13 5435 (2022)
  19. Exploring Polyubiquitin as a Flexible Multiple-Ligand Binding Platform. Fushman D. Structure 25 1-3 (2017)
  20. A high-field cellular DNP-supported solid-state NMR approach to study proteins with sub-cellular specificity. Beriashvili D, Yao R, D'Amico F, Krafčíková M, Gurinov A, Safeer A, Cai X, Mulder MPC, Liu Y, Folkers GE, Baldus M. Chem Sci 14 9892-9899 (2023)
  21. Mechanism of selective recognition of Lys48-linked polyubiquitin by macrocyclic peptide inhibitors of proteasomal degradation. Lemma B, Zhang D, Vamisetti GB, Wentz BG, Suga H, Brik A, Lubkowski J, Fushman D. Nat Commun 14 7212 (2023)
  22. Processing of the ribosomal ubiquitin-like fusion protein FUBI-eS30/FAU is required for 40S maturation and depends on USP36. van den Heuvel J, Ashiono C, Gillet LC, Dörner K, Wyler E, Zemp I, Kutay U. Elife 10 e70560 (2021)


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