Distinct structural changes in wild-type and amyloidogenic chicken cystatin caused by disruption of C95–C115 disulfide bond

Journal of Biomolecular Structure and Dynamics

Volumn 34, Issue 12, 2016, Pages 2679-2687

  Chong, Xiaoying ^a   Lu, Xian ^a   Wang, Yu ^a   Chang, Alan K ^a   Xu, Linan ^b   Wang, Na ^a   Sun, Yonghui ^a   Jones, Gary W ^b   Song, Youtao ^a   Song, Yong Bo ^c   He, Jianwei ^a  

^a LIAONING UNIVERSITY   (China)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^c SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

amyloid; cystatin; disulfide bond; Eps1; molecular chaperone; molecular dynamics simulation

Indexed keywords

AMYLOID PROTEIN; CYSTATIN C; CYSTEINE; DISULFIDE; EPS1 PROTEIN; PROTEIN DISULFIDE ISOMERASE; UNCLASSIFIED DRUG; CYSTATIN; CYSTATIN, EGG-WHITE;

AMINO ACID SUBSTITUTION; ARTICLE; CHICKEN; COMPUTER MODEL; CONTROLLED STUDY; DISULFIDE BOND; EPS1 GENE; GENE; HYDROPHOBICITY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; VASCULAR AMYLOIDOSIS; WILD TYPE; CHEMICAL PHENOMENA; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR MODEL; POINT MUTATION; PROTEIN CONFORMATION; STRUCTURE ACTIVITY RELATION;

CYSTATINS; DISULFIDES; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; POINT MUTATION; PROTEIN CONFORMATION; PROTEIN STABILITY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84958057543     PISSN: 07391102     EISSN: 15380254     Source Type: Journal    
DOI: 10.1080/07391102.2015.1126796     Document Type: Article

References (45)

1. M.Abrahamson, & A.Grubb, (1994). Increased body temperature accelerates aggregation of the Leu-68–>Gln mutant cystatin C, the amyloid-forming protein in hereditary cystatin C amyloid angiopathy. Proceedings of the National Academy of Sciences, 91, 1416–1420.10.1073/pnas.91.4.1416
2. M.Abrahamson, A.J.Barrett, G.Salvesen, & A.Grubb, (1986). Isolation of six cysteine proteinase inhibitors from human urine. Their physicochemical and enzyme kinetic properties and concentrations in biological fluids. Journal of Biological Chemistry, 261, 11282–11289.
3. M.Abrahamson, S.Jonsdottir, I.Olafsson, O.Jensson, & A.Grubb, (1992). Hereditary cystatin C amyloid angiopathy:Identification of the disease-causing mutation and specific diagnosis by polymerase chain reaction based analysis. Human Genetics, 89, 377–380.
4. M.Alvarez-Fernandez, A.J.Barrett, B.Gerhartz, P.M.Dando, J.Ni, & M.Abrahamson, (1999). Inhibition of mammalian legumain by some cystatins is due to a novel second reactive site. Journal of Biological Chemistry, 274, 19195–19203.10.1074/jbc.274.27.19195
5. A.Ben-Zvi, E.A.Miller, & R.I.Morimoto, (2009). Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proceedings of the National Academy of Sciences, 106, 14914–14919. doi:0902882106[pii]10.1073/pnas.0902882106
6. W.M.Berhanu, & A.E.Masunov, (2012). Controlling the aggregation and rate of release in order to improve insulin formulation:Molecular dynamics study of full-length insulin amyloid oligomer models. Journal of Molecular Modeling, 18, 1129–1142. doi:10.1007/s00894-011-1123-3
7. W.M.Berhanu, & A.E.Masunov, (2014). Full length amylin oligomer aggregation:Insights from molecular dynamics simulations and implications for design of aggregation inhibitors. Journal of Biomolecular Structure and Dynamics, 32, 1651–1669. doi:10.1080/07391102.2013.832635
8. M.Bjarnadottir, C.Nilsson, V.Lindstrom, A.Westman, P.Davidsson, F.Thormodsson, & A.Grubb, (2001). The cerebral hemorrhage-producing cystatin C variant (L68Q) in extracellular fluids. Amyloid, 8(1), 1–10.10.3109/13506120108993809
9. I.Bjoerk, & K.Ylinenjaervi, (1992). Different roles of the two disulfide bonds of the cysteine proteinase inhibitor, chicken cystatin, for the conformation of the active protein. Biochemistry, 31, 8597–8602.10.1021/bi00151a029
10. W.Bode, R.Engh, D.Musil, U.Thiele, R.Huber, A.Karshikov, & V.Turk, (1988). The 2.0 A X-ray crystal structure of chicken egg white cystatin and its possible mode of interaction with cysteine proteinases. EMBO Journal, 7, 2593–2599.
11. E.Cohen, J.F.Paulsson, P.Blinder, T.Burstyn-Cohen, D.Du, G.Estepa, & A.Dillin, (2009). Reduced IGF-1 signaling delays age-associated proteotoxicity in mice. Cell, 139, 1157–1169. doi:S0092-8674(09)01426-3[pii]10.1016/j.cell.2009.11.014
12. B.C.Cunningham, & J.A.Wells, (1989). High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis. Science, 244, 1081–1085.10.1126/science.2471267
13. F.Demontis, & N.Perrimon, (2010). FOXO/4E-BP signaling in drosophila muscles regulates organism-wide proteostasis during aging. Cell, 143, 813–825. doi:S0092-8674(10)01143-8[pii]10.1016/j.cell.2010.10.007
14. J.F.Dice, (1993). Cellular and molecular mechanisms of aging. Physiological Reviews, 73, 149–159.
15. G.Dubin, (2005). Proteinaceous cysteine protease inhibitors. Cellular and Molecular Life Sciences, 62, 653–669. doi:10.1007/s00018-004-4445-9
16. I.Ekiel, M.Abrahamson, D.B.Fulton, P.Lindahl, A.C.Storer, W.Levadoux, & K.Gehring, (1997). NMR structural studies of human cystatin C dimers and monomers. Journal of Molecular Biology, 271, 266–277. doi:S0022-2836(97)91150-5[pii]10.1006/jmbi.1997.1150
17. S.M.Greenberg, (1998). Cerebral amyloid angiopathy:Prospects for clinical diagnosis and treatment. Neurology, 51, 690–694.10.1212/WNL.51.3.690
18. A.O.Grubb, (2000). Cystatin C–properties and use as diagnostic marker. Advances in Clinical Chemistry, 35, 63–99.
19. G.Gudmundsson, J.Hallgrímsson, T.A.Jonasson, & O.Bjarnason, (1972). Hereditary cerebral hemorrhage with amyloidosis. Brain, 95, 387–404.10.1093/brain/95.2.387
20. T.Hansson, C.Oostenbrink, & W.van Gunsteren, (2002). Molecular dynamics simulations. Current Opinion in Structural Biology, 12, 190–196.10.1016/S0959-440X(02)00308-1
21. J.He, T.Sakamoto, Y.Song, A.Saito, A.Harada, H.Azakami, & A.Kato, (2005). Effect of EPS1 gene deletion in Saccharomyces cerevisiae on the secretion of foreign proteins which have disulfide bridges. FEBS Letters, 579, 2277–2283. doi:10.1016/j.febslet.2005.03.019
22. J.He, Y.Song, N.Ueyama, A.Harada, H.Azakami, & A.Kato, (2005). Characterization of recombinant amyloidogenic chicken cystatin mutant I66Q expressed in yeast. Journal of Biochemistry, 137, 477–485. doi:10.1093/jb/mvi064
23. J.He, Y.Song, N.Ueyama, A.Saito, H.Azakami, & A.Kato, (2006). Prevention of amyloid fibril formation of amyloidogenic chicken cystatin by site-specific glycosylation in yeast. Protein Science, 15, 213–222. doi:15/2/213[pii]10.1110/ps.051753306
24. J.He, L.Xu, Z.Zou, N.Ueyama, H.Li, A.Kato, & Y.Song, (2013). Molecular dynamics simulation to investigate the impact of disulfide bond formation on conformational stability of chicken cystatin I66Q mutant. Journal of Biomolecular Structure and Dynamics, 31, 1101–1110. doi:10.1080/07391102.2012.721498
25. H.H.Heidtmann, U.Salge, M.Abrahamson, M.Bencina, L.Kastelic, N.Kopitar-Jerala, & T.T.Lah, (1997). Cathepsin B and cysteine proteinase inhibitors in human lung cancer cell lines. Clinical and Experimental Metastasis, 15, 368–381.10.1023/A:1018494020001
26. R.Janowski, M.Kozak, E.Jankowska, Z.Grzonka, A.Grubb, M.Abrahamson, & M.Jaskolski, (2001). Human cystatin C, an amyloidogenic protein, dimerizes through three-dimensional domain swapping. Nature Structural Biology, 8, 316–320. doi:10.1038/86188
27. R.Janowski, M.Abrahamson, A.Grubb, & M.Jaskolski, (2004). Domain swapping in N-truncated human cystatin C. Journal of Molecular Biology, 341, 151–160. doi:10.1016/j.jmb.2004.06.013
28. O.Jensson, G.Gudmundsson, A.Arnason, H.Blöndal, I.Petursdottir, L.Thorsteinsson, & B.Frangione, (1987). Hereditary cystatin C (γ-trace) amyloid angiopathy of the CNS causing cerebral hemorrhage. Acta Neurologica Scandinavica, 76, 102–114.10.1111/ane.1987.76.issue-2
29. W.Kabsch, & C.Sander, (1983). Dictionary of protein secondary structure:Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577–2637. doi:10.1002/bip.360221211
30. S.A.Kaeser, M.C.Herzig, J.Coomaraswamy, E.Kilger, M.L.Selenica, D.T.Winkler, & M.Jucker, (2007). Cystatin C modulates cerebral β-amyloidosis. Nature Genetics, 39, 1437–1439. doi:10.1038/ng.2007.23
31. D.L.Labovitz, & R.L.Sacco, (2001). Intracerebral hemorrhage:Update. Current Opinion in Neurology, 14, 103–108.10.1097/00019052-200102000-00016
32. E.Levy, C.Lopez-Otin, J.Ghiso, D.Geltner, & B.Frangione, (1989). Stroke in Icelandic patients with hereditary amyloid angiopathy is related to a mutation in the cystatin C gene, an inhibitor of cysteine proteases. Journal of Experimental Medicine, 169, 1771–1778.10.1084/jem.169.5.1771
33. Y.M.Lin, H.L.Liu, J.H.Zhao, C.H.Huang, H.W.Fang, Y.Ho, & W.Y.Chen, (2007). Molecular dynamics simulations to investigate the domain swapping mechanism of human cystatin C. Biotechnology Progress, 23, 577–584. doi:10.1021/bp060380d
34. H.Lofberg, A.O.Grubb, E.K.Nilsson, O.Jensson, G.Gudmundsson, H.Blondal, & L.Thorsteinsson, (1987). Immunohistochemical characterization of the amyloid deposits and quantitation of pertinent cerebrospinal fluid proteins in hereditary cerebral hemorrhage with amyloidosis. Stroke, 18, 431–440.10.1161/01.STR.18.2.431
35. B.Ma, & R.Nussinov, (2006). Simulations as analytical tools to understand protein aggregation and predict amyloid conformation. Current Opinion in Chemical Biology, 10, 445–452. doi:10.1016/j.cbpa.2006.08.018
36. A.A.Pakula, V.B.Young, & R.T.Sauer, (1986). Bacteriophage lambda cro mutations:Effects on activity and intracellular degradation. Proceedings of the National Academy of Sciences, 83, 8829–8833.10.1073/pnas.83.23.8829
37. S.Rodziewicz-Motowidlo, M.Wahlbom, X.Wang, J.Łągiewka, R.Janowski, M.Jaskólski, & Z.Grzonka, (2006). Checking the conformational stability of cystatin C and its L68Q variant by molecular dynamics studies:Why is the L68Q variant amyloidogenic? Journal of Structural Biology, 154, 68–78. doi:10.1016/j.jsb.2005.11.015
38. A.Sanders, C.Jeremy Craven, L.D.Higgins, S.Giannini, M.J.Conroy, A.M.Hounslow, & R.A.Staniforth, (2004). Cystatin forms a tetramer through structural rearrangement of domain-swapped dimers prior to amyloidogenesis. Journal of Molecular Biology, 336, 165–178. doi:S0022283603015043[pii]
39. H.A.Scheraga, M.Khalili, & A.Liwo, (2007). Protein-folding dynamics:Overview of molecular simulation techniques. Annual Review of Physical Chemistry, 58, 57–83. doi:10.1146/annurev.physchem.58.032806.104614
40. V.Stoka, M.Nycander, B.Lenarčič, C.Labriola, J.J.Cazzulo, I.Björk, & V.Turk, (1995). Inhibition of cruzipain, the major cysteine proteinase of the protozoan parasite, Trypanosoma cruzi, by proteinase inhibitors of the cystatin superfamily. FEBS Letters, 370, 101–104. doi:0014-5793(95)00798-E[pii]
41. Y.F.Yang, K.C.Cheng, P.H.Tsai, C.C.Liu, T.R.Lee, & P.C.Lyu, (2009). Alanine substitutions of noncysteine residues in the cysteine-stabilized αβ motif. Protein Science, 18, 1498–1506. doi:10.1002/pro.164
42. W.Ye, W.Wang, C.Jiang, Q.Yu, & H.Chen, (2013). Molecular dynamics simulations of amyloid fibrils:An in silico approach. Acta Biochimica et Biophysica Sinica, 45, 503–508. doi:10.1093/abbs/gmt026
43. Y.Yu, Y.Wang, J.He, Y.Liu, H.Li, H.Zhang, & Y.Song, (2010). Structural and dynamic properties of a new amyloidogenic chicken cystatin mutant I108T. Journal of Biomolecular Structure and Dynamics, 27, 641–649. doi:c4299/Structural-and-Dynamic-Properties-of-a-New-Amyloidogenic-Chicken-Cystatin-Mutant-I108T-641-650-p17766.html[pii]10.1080/07391102.2010.10508578
44. Y.Yu, X.Liu, J.He, M.Zhang, H.Li, D.Wei, & Y.Song, (2012). Appendant structure plays an important role in amyloidogenic cystatin dimerization prior to domain swapping. Journal of Biomolecular Structure and Dynamics, 30, 102–112. doi:10.1080/07391102.2012.674282
45. J.H.Zhao, H.L.Liu, Y.F.Liu, H.Y.Lin, H.W.Fang, Y.Ho, & W.B.Tsai, (2009). Molecular dynamics simulations to investigate the aggregation behaviors of the Aß(17–42) oligomers. Journal of Biomolecular Structure and Dynamics, 26, 481–490. doi:10.1080/07391102.2009.10507263