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Novel Zn2+-binding sites in human transthyretin: implications for amyloidogenesis and retinol-binding protein recognition.

Palmieri Lde C, Lima LM, Freire JB, Bleicher L, Polikarpov I, Almeida FC, Foguel D
J Biol Chem 285 31731-41 (2010)
Related entries: 3did, 3gps, 3grb, 3grg

Cited: 30 times
EuropePMC logo PMID: 20659897

Abstract

Human transthyretin (TTR) is a homotetrameric protein involved in several amyloidoses. Zn(2+) enhances TTR aggregation in vitro, and is a component of ex vivo TTR amyloid fibrils. We report the first crystal structure of human TTR in complex with Zn(2+) at pH 4.6-7.5. All four structures reveal three tetra-coordinated Zn(2+)-binding sites (ZBS 1-3) per monomer, plus a fourth site (ZBS 4) involving amino acid residues from a symmetry-related tetramer that is not visible in solution by NMR. Zn(2+) binding perturbs loop E-α-helix-loop F, the region involved in holo-retinol-binding protein (holo-RBP) recognition, mainly at acidic pH; TTR affinity for holo-RBP decreases ∼5-fold in the presence of Zn(2+). Interestingly, this same region is disrupted in the crystal structure of the amyloidogenic intermediate of TTR formed at acidic pH in the absence of Zn(2+). HNCO and HNCA experiments performed in solution at pH 7.5 revealed that upon Zn(2+) binding, although the α-helix persists, there are perturbations in the resonances of the residues that flank this region, suggesting an increase in structural flexibility. While stability of the monomer of TTR decreases in the presence of Zn(2+), which is consistent with the tertiary structural perturbation provoked by Zn(2+) binding, tetramer stability is only marginally affected by Zn(2+). These data highlight structural and functional roles of Zn(2+) in TTR-related amyloidoses, as well as in holo-RBP recognition and vitamin A homeostasis.

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Articles - 3dgd mentioned but not cited (5)

  1. Novel Zn2+-binding sites in human transthyretin: implications for amyloidogenesis and retinol-binding protein recognition. Palmieri Lde C, Lima LM, Freire JB, Bleicher L, Polikarpov I, Almeida FC, Foguel D. J Biol Chem 285 31731-31741 (2010)
  2. Copper mediated amyloid-β binding to Transthyretin. Ciccone L, Fruchart-Gaillard C, Mourier G, Savko M, Nencetti S, Orlandini E, Servent D, Stura EA, Shepard W. Sci Rep 8 13744 (2018)
  3. The 3DGD: a database of genome 3D structure. Li C, Dong X, Fan H, Wang C, Ding G, Li Y. Bioinformatics 30 1640-1642 (2014)
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  2. THE IMS PARADOX: A PERSPECTIVE ON STRUCTURAL ION MOBILITY-MASS SPECTROMETRY. McCabe JW, Hebert MJ, Shirzadeh M, Mallis CS, Denton JK, Walker TE, Russell DH. Mass Spectrom Rev 40 280-305 (2021)
  3. Transthyretin: From Structural Stability to Osteoarticular and Cardiovascular Diseases. Wieczorek E, Ożyhar A. Cells 10 1768 (2021)
  4. The interaction of zinc with the multi-functional plasma thyroid hormone distributor protein, transthyretin: evolutionary and cross-species comparative aspects. Yamauchi K. Biometals 34 423-437 (2021)

Articles citing this publication (19)

  1. Identification of beta-amyloid-binding sites on transthyretin. Du J, Cho PY, Yang DT, Murphy RM. Protein Eng Des Sel 25 337-345 (2012)
  2. Fourier Transform-Ion Mobility-Orbitrap Mass Spectrometer: A Next-Generation Instrument for Native Mass Spectrometry. Poltash ML, McCabe JW, Shirzadeh M, Laganowsky A, Clowers BH, Russell DH. Anal Chem 90 10472-10478 (2018)
  3. Transthyretin is a metallopeptidase with an inducible active site. Liz MA, Leite SC, Juliano L, Saraiva MJ, Damas AM, Bur D, Sousa MM. Biochem J 443 769-778 (2012)
  4. Native IM-Orbitrap MS: Resolving What Was Hidden. Poltash ML, McCabe JW, Shirzadeh M, Laganowsky A, Russell DH. Trends Analyt Chem 124 115533 (2020)
  5. New insights into the metal-induced oxidative degradation pathways of transthyretin. Poltash ML, Shirzadeh M, McCabe JW, Moghadamchargari Z, Laganowsky A, Russell DH. Chem Commun (Camb) 55 4091-4094 (2019)
  6. A new crystal form of human transthyretin obtained with a curcumin derived ligand. Polsinelli I, Nencetti S, Shepard W, Ciccone L, Orlandini E, Stura EA. J Struct Biol 194 8-17 (2016)
  7. Human TTR conformation altered by rhenium tris-carbonyl derivatives. Ciccone L, Policar C, Stura EA, Shepard W. J Struct Biol 195 353-364 (2016)
  8. Structural evidence for native state stabilization of a conformationally labile amyloidogenic transthyretin variant by fibrillogenesis inhibitors. Zanotti G, Cendron L, Folli C, Florio P, Imbimbo BP, Berni R. FEBS Lett 587 2325-2331 (2013)
  9. Zinc binding regulates amyloid-like aggregation of GAPR-1. Sheng J, Olrichs NK, Geerts WJ, Li X, Rehman AU, Gadella BM, Kaloyanova DV, Helms JB. Biosci Rep 39 BSR20182345 (2019)
  10. Characterization of little skate (Leucoraja erinacea) recombinant transthyretin: Zinc-dependent 3,3',5-triiodo-l-thyronine binding. Suzuki S, Kasai K, Yamauchi K. Gen Comp Endocrinol 217-218 43-53 (2015)
  11. Structural Analysis of the Effect of a Dual-FLAG Tag on Transthyretin. Shirzadeh M, Poltash ML, Laganowsky A, Russell DH. Biochemistry 59 1013-1022 (2020)
  12. Characterization of Oncorhynchus mykiss 5-hydroxyisourate hydrolase/transthyretin superfamily: evolutionary and functional analyses. Kasai K, Nishiyama N, Yamauchi K. Gene 531 326-336 (2013)
  13. Characteristics of the brown hagfish Paramyxine atami transthyretin: Metal ion-dependent thyroid hormone binding. Suzuki S, Kasai K, Nishiyama N, Ishihara A, Yamauchi K. Gen Comp Endocrinol 249 1-14 (2017)
  14. Sequential Molecular Events of Functional Trade-Offs in 5-Hydroxyisourate Hydrolase Before and After Gene Duplication Led to the Evolution of Transthyretin During Chordate Diversification. Yamauchi K, Kasai K. J Mol Evol 86 457-469 (2018)
  15. Calcium Binds to Transthyretin with Low Affinity. Cantarutti C, Mimmi MC, Verona G, Mandaliti W, Taylor GW, Mangione PP, Giorgetti S, Bellotti V, Corazza A. Biomolecules 12 1066 (2022)
  16. Controlling dissociation channels of gas-phase protein complexes using charge manipulation. Fegan SK, Thachuk M. J Am Soc Mass Spectrom 25 722-728 (2014)
  17. A molecular basis for tetramer destabilization and aggregation of transthyretin Ala97Ser. Wang YS, Huang CH, Liou GG, Hsueh HW, Liang CT, Tseng HC, Huang SJ, Chao CC, Hsieh ST, Tzeng SR. Protein Sci 32 e4610 (2023)
  18. Allosteric activation of human α-thrombin through exosite 2 by suramin analogs. Cargnelutti MT, Marques AF, Esser D, Monteiro RQ, Kassack MU, Lima LM. Arch Biochem Biophys 520 36-41 (2012)
  19. Linking Gas-Phase and Solution-Phase Protein Unfolding via Mobile Proton Simulations. Eldrid C, Cragnolini T, Ben-Younis A, Zou J, Raleigh DP, Thalassinos K. Anal Chem 94 16113-16121 (2022)


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