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2001 | 48 | 4 | 807-827
Article title

3D Domain swapping, protein oligomerization, and amyloid formation.

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Abstracts
EN
In 3D domain swapping, first described by Eisenberg, a structural element of a monomeric protein is replaced by the same element from another subunit. This process requires partial unfolding of the closed monomers that is then followed by adhesion and reconstruction of the original fold but from elements contributed by different subunits. If the interactions are reciprocal, a closed-ended dimer will be formed, but the same phenomenon has been suggested as a mechanism for the formation of open-ended polymers as well, such as those believed to exist in amyloid fibrils. There has been a rapid progress in the study of 3D domain swapping. Oligomers higher than dimers have been found, the monomer-dimer equilibrium could be controlled by mutations in the hinge element of the chain, a single protein has been shown to form more than one domain-swapped structure, and recently, the possibility of simultaneous exchange of two structural domains by a single molecule has been demonstrated. This last discovery has an important bearing on the possibility that 3D domain swapping might be indeed an amyloidogenic mechanism. Along the same lines is the discovery that a protein of proven amyloidogenic properties, human cystatin C, is capable of 3D domain swapping that leads to oligomerization. The structure of do-main-swapped human cystatin C dimers explains why a naturally occurring mutant of this protein has a much higher propensity for aggregation, and also suggests how this same mechanism of 3D domain swapping could lead to an open-ended polymer that would be consistent with the cross-β structure, which is believed to be at the heart of the molecular architecture of amyloid fibrils.
Publisher

Year
Volume
48
Issue
4
Pages
807-827
Physical description
Dates
published
2001
received
2001-09-18
accepted
2001-10-26
Contributors
  • Department of Crystallography, Faculty of Chemistry, Adam Mickiewicz University, Poznań, Poland
References
  • Abrahamson, M., Barrett, A.J., Salvesen, G. & Grubb, A. (1986) Isolation of six cysteine proteinase inhibitors from human urine. Their physicochemical and enzyme kinetic properties and concentrations in biological fluids. J. Biol. Chem. 261, 11282-11289.
  • Abrahamson, M. & Grubb, A. (1994) Increased body temperature accelerates aggregation of the Leu->Gln mutant cystatin C, the amyloid-forming protein in hereditary cystatin C amyloid angiopathy. Proc. Natl. Acad. Sci. U.S.A. 91, 1416-1420.
  • Adinolfi, S., Piccoli, R., Sica, F. & Mazzarella, L. (1996) BS-RNase tetramers: An example of domain-swapped oligomers. FEBS Lett. 398, 326-332.
  • Alvarez-Fernandez, M., Barrett, A.J., Gerhartz, B., Dando, P.M., Ni, J. & Abrahamson, M. (1999) Inhibition of mammalian legumain by some cystatins is due to a novel second reactive site. J. Biol. Chem. 274, 19195-19203.
  • Barrett, A.J., Fritz, H., Grubb, A., Isemura, S., Jarvinen, M., Katunuma, N., Machleidt, W., Muller-Esterl, W., Sasaki, M. & Turk, V. (1986) Nomenclature and classification of the proteins homologous with the cysteine-proteinase inhibitor chicken cystatin. Biochem. J. 236, 312.
  • Beintema, J.J., Wietzes, P., Weickmann, J.L. & Glitz, D.G. (1984) The amino acid sequence of human pancreatic ribonuclease. Anal. Biochem. 136, 48-64.
  • Bennett, M.J., Choe, S. & Eisenberg, D.S. (1994) Domain swapping: Entangling alliances between proteins. Proc. Natl. Acad. Sci. U.S.A. 91, 3127-3131.
  • Bennett, M.J., Schlunegger, M.P. & Eisenberg, D. (1995) 3D Domain swapping: A mechanism for oligomer assembly. Protein Sci. 4, 2455-2468.
  • Bjarnadottir, M., Nilsson, C., Lindstrom, V., Westman, A., Davidsson, P., Thormodsson, F., Blondal, H., Gudmundsson, G. & Grubb, A. (2001)The cerebral hemorrhage-producing cystatin C variant (L68Q) in extracellular fluids. Amyloid 8, 1-10.
  • Blake, C. & Serpell, L. (1996)Synchrotron X-ray studies suggest that the core of the transthyretin amyloid fibril is a continuous β-sheet helix. Structure 4, 989-998.
  • Bode, W., Engh, R., Musil, D., Thiele, U., Huber, R., Karshnikov, A., Brzin, J., Kos, J. & Turk, V. (1988) The 2.0 Å X-ray crystal structure of chicken egg white cystatin and its possible mode of interaction with cysteine proteinases. EMBO J. 7, 2593-2599.
  • Booth, D.R., Sunde, M., Bellotti, V., Robinson, C.V., Hutchinson, W.L., Fraser, P.E., Hawkins, P.N., Dobson, C.M., Radford, S.E., Blake, C.C. & Pepys, M.B. (1997) Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis. Nature 385, 787-793.
  • Chiti, F., Taddei, N., Bucciantini, M., White, P., Ramponi, G. & Dobson, C.M. (2000) Mutational analysis of the propensity for amyloid formation by a globular protein. EMBO J. 19, 1441-1449.
  • Cohen, A.S. (1986) General introduction and a brief history of the amyloid fibril; in Amyloidosis (Marrink, J. & Van Rijvijk, M.H., eds.) pp. 3-19, Nijhoff, Dordrecht.
  • Cohen, A.S. & Calkins, E. (1959) Electron microscopic observation on a fibrous component in amyloid of diverse origins. Nature 183, 1202-1203.
  • Cohen, A.S., Shirahamata, T. & Skinner, M. (1982) Electron microscopy of amyloid; in Electron Microscopy of Proteins (Harris, J.R., ed.) vol. 3, pp. 165-205, Academic Press, New York.
  • Cohen, F.E. & Prusiner, S.B. (1998) Pathologic conformations of prion proteins. Annu. Rev. Biochem. 67, 793-819.
  • Crestfield, A.M., Stein, W.H. & Moore, S. (1962) On the aggregation of bovine pancreatic ribonuclease. Arch. Biochem. Biophys. 1 (Suppl.), 217-222.
  • Crestfield, A.M., Stein, W.H. & Moore, S. (1963) Properties and conformation of the histidine residues at the active site of ribonuclease. J. Biol. Chem. 238, 2421-2428.
  • D'Alessio, G. (1999) Evolution of oligomeric proteins. Eur. J. Biochem. 266, 699-708.
  • Dieckmann, T., Mitschang, L., Hofmann, M., Kos, J., Turk, V., Auerswald, E.A., Jaenicke, R. & Oschkinat, H. (1993) The structure of native phosphorylated chicken cystatin and of recombinant unphosphorylated variant in solution. J. Mol. Biol. 234, 1048-1059.
  • Dobson, C.M. (1999) Protein misfolding, evolution and disease. Trends Biochem. Sci. 24, 329-332.
  • Ekiel, I. & Abrahamson, M. (1996) Folding-related dimerization of human cystatin C. J. Biol. Chem. 271, 1314-1321.
  • Ekiel, I., Abrahamson, M., Fulton, D.B., Lindahl, P., Storer, A.C., Levadoux, W., Lafrance, M., Labelle, S., Pomerleau, Y., Groleau, D., LeSauteur, L. & Gehring, K. (1997) NMR structural studies of human cystatin C dimers and monomers. J. Mol. Biol. 271, 266-277.
  • Engh, R.A., Dieckmann, T., Bode, W., Auerswald, E.A., Turk, V., Huber, R. & Oschkinat, H. (1993) Conformational variability of chicken cystatin. Comparison of structures determined by X-ray diffraction and NMR spectroscopy. J. Mol. Biol. 234, 1060-1069.
  • Gerhartz, B., Ekiel, I. & Abrahamson, M. (1998) Two stable unfolding intermediates of the disease-causing L68Q variant of human cystatin C. Biochemistry 37, 17309-17317.
  • Glenner, G.G. (1980a) Amyloid deposits and amyloidosis - the β-fibrilloses 1. N. Engl. J. Med. 302, 1283-1292.
  • Glenner, G.G. (1980b) Amyloid deposits and amyloidosis - the β-fibrilloses 2. N. Engl. J. Med. 302, 1333-1343.
  • Glenner, G.G., Eanes, E.D. & Page, D.L. (1972) The relation of the properties of congo red-stained amyloid fibrils to the β-conformation. J. Histochem. Cytochem. 20, 821-826.
  • Grubb, A. (2000) Cystatin C-- properties and use as diagnostic marker. Adv. Clin. Chem. 35, 63-99.
  • Janowski, R., Kozak, M., Jankowska, E., Grzonka, Z., Grubb, A., Abrahamson, M. & Jaskolski, M. (2001) Human cystatin C, an amyloidogenic protein, dimerizes through three-dimensional domain swapping. Nat. Struct. Biol. 8, 316-320.
  • Klafki, H.-W., Pick, A.I., Pardowitz, I., Cole, T., Awni, L.A., Barnikol, H.V., Mayer, F., Kratzin, H.D. & Hilschmann, N. (1993) Reduction of disulfide bonds in an amyloidogenic Bence Jones protein leads to formation of amyloid-like fibrils in vitro. Biol. Chem. Hoppe- Seyler 374, 1117-1122.
  • Kozak, M., Jankowska, E., Janowski, R., Grzonka, Z., Grubb, A., Alvarez-Fernandez, M., Abrahamson, M. & Jaskólski, M. (1999) Expression of a selenomethionyl derivative and preliminary crystallographicstudies of human cystatin C. Acta Crystallogr. D Biol Crystallogr. 55, 1939-1942.
  • Liu, Y., Hart, P.J., Schlunegger, M.P. & Eisenberg, D. (1998) The crystal structure of a 3D domain-swapped dimer of RNase A at 2.1 Å resolution. Proc. Natl. Acad. Sci. U.S.A. 95, 3437-3442.
  • Liu, Y., Gotte, G., Libonati, M. & Eisenberg, D. (2001) A domain-swapped RNase A dimer with implications for amyloid formation. Nat. Struct. Biol. 8, 211-214.
  • Mazzarella, L., Capasso, S., Demasi, D., Di Lorenzo, G., Mattia, C.A. & Zagari, A. (1993) Bovine seminal ribonuclease: Structure at 1.9 Å resolution. Acta Crystallogr. D Biol Crystallogr 49, 389-402.
  • McPherson, A. (1998) Crystallization of Biological Macromolecules. Cold Spring Harbor Laboratory Press, New York.
  • Miers, H.A. & Isaac, F. (1907) The spontaneous crystallization of binary mixtures: Experiments on salol and betol. Proc. Roy. Soc. Lond. A 79, 322.
  • Minor, D.L., Jr. & Kim, P.S. (1996) Context-dependent secondary structure formation of a designed protein sequence. Nature 380, 730-734.
  • Murray, A.J., Head, J.G., Barker, J.J. & Brady, R.L. (1998) Engineering an intertwined form of CD2 for stability and assembly. Nature Struct. Biol. 5, 778-782.
  • Murray, A.J., Lewis, S.J., Barclay, A.N. & Brady, R.L. (1995) One sequence, two folds: A metastable structure of CD2. Proc. Natl. Acad. Sci. U.S.A. 92, 7337-7341.
  • Ogihara, N.L., Ghirlanda, G., Bryson, J.W., Gingery, M., DeGardo, W.F. & Eisenberg, D. (2001) Design of three-dimensional domain-swapped dimers and fibrous oligomers. Proc. Natl. Acad. Sci. U.S.A. 98, 1404-1409.
  • Olafsson, I. & Grubb, A. (2000) Hereditary cystatin C amyloid angiopathy. Amyloid 7, 70-79.
  • Park, C. & Raines, R.T. (2000) Dimer formation by a “monomeric” protein. Protein Sci. 9, 2026-2033.
  • Pei, X.Y., Holliger, P., Murzin, A.G. & Williams, R.L. (1997) The 2.0-Å resolution crystal structure of a trimeric antibody fragment with noncognate VH-VL domain pairs shows a rearrangement of VH CDR3. Proc. Natl. Acad. Sci. U.S.A. 94, 9637-9642.
  • Perutz, M.F. (1997) Mutations make enzymes polymerize. Nature 385, 773-774.
  • Perutz, M.F. (1999) Glutamine repeats and neurodegenerative diseases: Molecular aspects. Trends. Biochem. Sci. 24, 58-63.
  • Perutz, M.F., Johnson, T., Suzuki, M. & Finch, J.T. (1994) Glutamine repeats as polar zippers: Their possible role in inherited neurodegene rative diseases. Proc. Natl. Acad. Sci. U.S.A. 91, 5355-5358.
  • Piccoli, R., Tamburrini, M., Piccialli, G., Di Donato, A., Parente, A. & D'Alessio, G. (1992) The dual-mode quaternary structure of seminal RNase. Proc. Natl. Acad. Sci. U.S.A. 89, 1870-1874.
  • Piccoli, R., Di Gaetano, S., De Lorenzo, C., Grauso, M., Monaco, C., Spalletti-Cernia, D., Laccetti, P., Cinatl, J., Matousek, J. & D'Alessio, G. (1999) A dimeric mutant of human pancreatic ribonuclease with selective cytotoxicity toward malignant cells. Proc. Natl. Acad. Sci. U.S.A. 96, 7768-7773.
  • Rawlings, N.D. & Barrett, A.J. (1990) Evolution of proteins of the cystatin superfamily. J. Mol. Evol. 30, 60-71.
  • Schlunegger, M.P., Bennett, M.J. & Eisenberg, D. (1997) Oligomer formation by 3D domain swapping: A model for protein assembly and misassembly; in Advances in Protein Chemistry (Richards, F.M., Eisenberg, D.S. & Kim, P.S., eds.) vol. 50, pp. 61-122, Academic Press, New York.
  • Sipe, J.D. & Cohen, A.S. (2000) Review: history of the amyloid fibril. J. Struct. Biol. 130, 88-98.
  • Sunde, M. & Blake, C.C.F. (1998) From the globular to the fibrous state: Protein structure and structural conversion in amyloid formation. Quat. Rev. Biophys. 31, 1-39.
  • Sunde, M., Serpell, L.C., Bartlam, M., Fraser, P.E., Pepys, M.B. & Blake, C.C.F. (1997) Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J. Mol. Biol. 273, 729-739.
  • Teplow, D.B. (1998) Structural and kinetic features of amyloid β-protein fibrillogenesis. Amyloid 5, 121-142.
  • Wlodawer, A., Bott, R. & Sjolin, L. (1982) The refined crystal structure of ribonuclease A at 2.0 Å resolution. J. Biol. Chem. 257, 1325-1332.
  • Wlodawer, A., Svansson, L.A., Sjolin, L. & Gilliland, G.L. (1988) Structure of phosphate-free ribonuclease A refined at 1.26 Å resolution. Biochemistry 27, 2705-2717.
  • Knaus, K.J., Morillas, M., Swietnicki, W., Malone, M., Surewicz, W.K. & Yee, V.C. (2001) Crystal structure of the human prion protein reveals a mechanism for oligomerization. Nat. Struct. Biol. 8, 770-774.
  • Staniforth, R.A., Giannini, S., Higgins, L.D., Conroy, M.J., Hounslow, A.M., Jerala, R., Craven, C.J. & Waltho, J.P. (2001) Three-dimensional domain swapping in the folded and molten-globule states of cystatins, an amyloid-forming structural superfamily. EMBO J. 20, 4774-4781.
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bwmeta1.element.bwnjournal-article-abpv48i4p807kz
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