Chemical modification of lysine residues in lysozyme may dramatically influence its amyloid fibrillation

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1804, Issue 4, 2010, Pages 714-722

  Morshedi, Dina ^a,b   Ebrahim Habibi, Azadeh ^c   Moosavi Movahedi, Ali Akbar ^b   Nemat Gorgani, Mohsen ^b,d  

^a NATIONAL INSTITUTE OF GENETIC ENGINEERING AND BIOTECHNOLOGY   (Iran)

^b UNIVERSITY OF TEHRAN   (Iran)

^c TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acetylation; Amorphous aggregate; Amyloid fibrillation; Chemical modification; Citraconylation; Lysozyme

Indexed keywords

AMYLOID; LYSINE; LYSOZYME;

ACETYLATION; ARTICLE; CHEMICAL MODIFICATION; CONFORMATION; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; THROMBOCYTE AGGREGATION INHIBITION;

ACETIC ANHYDRIDES; ACETYLATION; AMYLOID; ANIMALS; CHICKENS; CITRACONIC ANHYDRIDES; FEMALE; HYDROGEN-ION CONCENTRATION; KINETICS; LYSINE; MICROSCOPY, ELECTRON, TRANSMISSION; MURAMIDASE; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; SPECTROMETRY, FLUORESCENCE;

EID: 76849089849     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2009.11.012     Document Type: Article

References (82)

1. Skovronsky D.M., Lee V.M., and Trojanowski J.Q. Neurodegenerative diseases: new concepts of pathogenesis and their therapeutic implications. Annu. Rev. Pathol. 1 (2006) 151-170
2. Chiti F., and Dobson C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75 (2006) 333-366
3. Bucciantini M., Giannoni E., Chiti F., Baroni F., Formigli L., Zurdo J., Taddei N., Ramponi G., Dobson C.M., and Stefani M. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416 (2002) 507-511
4. Wang J.Z., Grundke-Iqbal I., and Iqbal K. Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration. Eur. J. Neurosci. 25 (2007) 59-68
5. Iqbal K., and Grundke-Iqbal I. Alzheimer neurofibrillary degeneration: significance, etiopathogenesis, therapeutics and prevention. J. Cell. Mol. Med. 12 (2007) 38-55
6. Iwatsubo T. Pathological biochemistry of alpha-synucleinopathy. Neuropathology 27 (2007) 474-478
7. Dias W.B., and Hart G.W. O-GlcNAc modification in diabetes and Alzheimer's disease. Mol. Biosyst. 3 (2007) 766-772
8. Takeuchi M., Sato T., Takino J., Kobayashi Y., Furuno S., Kikuchi S., and Yamagishi S. Diagnostic utility of serum or cerebrospinal fluid levels of toxic advanced glycation end-products (TAGE) in early detection of Alzheimer's disease. Med. Hypotheses 69 (2007) 1358-1366
9. Bergstrom A.L., Chabry J., Bastholm L., and Heegaard P.M. Oxidation reduces the fibrillation but not the neurotoxicity of the prion peptide PrP106-126. Biochim. Biophys. Acta. 1774 (2007) 1118-1127
10. Johansson A.S., Bergquist J., Volbracht C., Paivio A., Leist M., Lannfelt L., and Westlind-Danielsson A. Attenuated amyloid-beta aggregation and neurotoxicity owing to methionine oxidation. Neuroreport 18 (2007) 559-563
11. Sacksteder C.A., Qian W.J., Knyushko T.V., Wang H., Chin M.H., Lacan G., Melega W.P., Camp II D.G., Smith R.D., Smith D.J., Squier T.C., and Bigelow D.J. Endogenously nitrated proteins in mouse brain: links to neurodegenerative disease. Biochemistry 45 (2006) 8009-8022
12. Castegna A., Thongboonkerd V., Klein J.B., Lynn B., Markesbery W.R., and Butterfield D.A. Proteomic identification of nitrated proteins in Alzheimer's disease brain. J. Neurochem. 85 (2003) 1394-1401
13. Giasson B.I., Duda J.E., Murray I.V., Chen Q., Souza J.M., Hurtig H.I., Ischiropoulos H., Trojanowski J.Q., and Lee V.M. Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 290 (2000) 985-989
14. Reynolds M.R., Berry R.W., and Binder L.I. Nitration in neurodegeneration: deciphering the "hows" "nYs". Biochemistry 46 (2007) 7325-7336
15. Ha C., Ryu J., and Park C.B. Metal ions differentially influence the aggregation and deposition of Alzheimer's beta-amyloid on a solid template. Biochemistry 46 (2007) 6118-6125
16. Naylor R., Hill A.F., and Barnham K.J. Neurotoxicity in Alzheimer's disease: is covalently crosslinked Abeta responsible?. Eur. Biophys. J. 37 (2008) 265-268
17. Zawia N.H., and Basha M.R. Environmental risk factors and the developmental basis for Alzheimer's disease. Rev. Neurosci. 16 (2005) 325-337
18. Paik S.R., Shin H.J., Lee J.H., Chang C.S., and Kim J. Copper(II)-induced self-oligomerization of alpha-synuclein. Biochem. J. 340 Pt. 3 (1999) 821-828
19. El-Agnaf O.M., Paleologou K.E., Greer B., Abogrein A.M., King J.E., Salem S.A., Fullwood N.J., Benson F.E., Hewitt R., Ford K.J., Martin F.L., Harriott P., Cookson M.R., and Allsop D. A strategy for designing inhibitors of alpha-synuclein aggregation and toxicity as a novel treatment for Parkinson's disease and related disorders. FASEB J. 18 (2004) 1315-1317
20. Gaeta A., and Hider R.C. The crucial role of metal ions in neurodegeneration: the basis for a promising therapeutic strategy. Br. J. Pharmacol. 146 (2005) 1041-1059
21. Honson N.S., Jensen J.R., Darby M.V., and Kuret J. Potent inhibition of tau fibrillization with a multivalent ligand. Biochem. Biophys. Res. Commun. 363 (2007) 229-234
22. Qin Z., Hu D., Han S., Reaney S.H., Di Monte D.A., and Fink A.L. Effect of 4-hydroxy-2-nonenal modification on alpha-synuclein aggregation. J. Biol. Chem. 282 (2007) 5862-5870
23. Dear D.V., Young D.S., Kazlauskaite J., Meersman F., Oxley D., Webster J., Pinheiro T.J., Gill A.C., Bronstein I., and Lowe C.R. Effects of post-translational modifications on prion protein aggregation and the propagation of scrapie-like characteristics in vitro. Biochim. Biophys. Acta 1774 (2007) 792-802
24. Maleknia S.D., Reixach N., and Buxbaum J.N. Oxidation inhibits amyloid fibril formation of transthyretin. FEBS J. 273 (2006) 5400-5406
25. Na C.H., Jeon S.H., Zhang G., Olson G.L., and Chae C.B. Inhibition of amyloid beta-peptide production by blockage of beta-secretase cleavage site of amyloid precursor protein. J. Neurochem. 101 (2007) 1583-1595
26. Abedini A., Meng F., and Raleigh D.P. A single-point mutation converts the highly amyloidogenic human islet amyloid polypeptide into a potent fibrillization inhibitor. J. Am. Chem. Soc. 129 (2007) 11300-11301
27. Karsai A., Nagy A., Kengyel A., Martonfalvi Z., Grama L., Penke B., and Kellermayer M.S. Effect of lysine-28 side-chain acetylation on the nanomechanical behavior of Alzheimer amyloid beta25-35 fibrils. J. Chem. Inf. Model 45 (2005) 1641-1646
28. Shibata H., Kamada H., Kobayashi-Nishibata K., Yoshioka Y., Nishibata T., Abe Y., Nomura T., Nabeshi H., Minowa K., Mukai Y., Nakagawa S., Mayumi T., Tsunoda S., and Tsutsumi Y. Role of amino acid residue 90 in bioactivity and receptor binding capacity of tumor necrosis factor mutants. Biochim. Biophys. Acta 1774 (2007) 1029-1035
29. Min J., Allali-Hassani A., Nady N., Qi C., Ouyang H., Liu Y., MacKenzie F., Vedadi M., and Arrowsmith C.H. L3MBTL1 recognition of mono- and dimethylated histones. Nat. Struct. Mol. Biol. 14 (2007) 1229-1230
30. Knappe M., Bodevin S., Selinka H.C., Spillmann D., Streeck R.E., Chen X.S., Lindahl U., and Sapp M. Surface-exposed amino acid residues of HPV16 L1 protein mediating interaction with cell surface heparan sulfate. J. Biol. Chem. 282 (2007) 27913-27922
31. Okumura N., Seki T., and Ariga T. Cell surface-bound plasminogen regulates hepatocyte proliferation through a uPA-dependent mechanism. Biosci. Biotechnol. Biochem. 71 (2007) 1542-1549
32. Rose K., Kriha D., Pallast S., Junker V., Klumpp S., and Krieglstein J. Basic fibroblast growth factor: lysine 134 is essential for its neuroprotective activity. Neurochem. Int. 51 (2007) 25-31
33. Wilmarth P.A., Tanner S., Dasari S., Nagalla S.R., Riviere M.A., Bafna V., Pevzner P.A., and David L.L. Age-related changes in human crystallins determined from comparative analysis of post-translational modifications in young and aged lens: does deamidation contribute to crystallin insolubility?. J. Proteome Res. 5 (2006) 2554-2566
34. Floor E., Maples A.M., Rankin C.A., Yaganti V.M., Shank S.S., Nichols G.S., O'Laughlin M., Galeva N.A., and Williams T.D. A one-carbon modification of protein lysine associated with elevated oxidative stress in human substantia nigra. J. Neurochem. 97 (2006) 504-514
35. Smirnovas V., Winter R., Funck T., and Dzwolak W. Thermodynamic properties underlying the alpha-helix-to-beta-sheet transition, aggregation, and amyloidogenesis of polylysine as probed by calorimetry, densimetry, and ultrasound velocimetry. J. Phys. Chem. B. 109 (2005) 19043-19045
36. Masuda T., Ide N., and Kitabatake N. Effects of chemical modification of lysine residues on the sweetness of lysozyme. Chem. Senses 30 (2005) 253-264
37. Gharibyan A.L., Zamotin V., Yanamandra K., Moskaleva O.S., Margulis B.A., Kostanyan I.A., and Morozova-Roche L.A. Lysozyme amyloid oligomers and fibrils induce cellular death via different apoptotic/necrotic pathways. J. Mol. Biol. 365 (2007) 1337-1349
38. Chiti F., Calamai M., Taddei N., Stefani M., Ramponi G., and Dobson C.M. Studies of the aggregation of mutant proteins in vitro provide insights into the genetics of amyloid diseases. Proc. Natl. Acad. Sci. U. S. A. 99 Suppl. 4 (2002) 16419-16426
39. Schmitt A., Schmitt J., Munch G., and Gasic-Milencovic J. Characterization of advanced glycation end products for biochemical studies: side chain modifications and fluorescence characteristics. Anal. Biochem. 338 (2005) 201-215
40. Frare E., Mossuto M.F., Polverino de Laureto P., Dumoulin M., Dobson C.M., and Fontana A. Identification of the core structure of lysozyme amyloid fibrils by proteolysis. J. Mol. Biol. 361 (2006) 551-561
41. Choudhary C., Kumar C., Gnad F., Nielsen M.L., Rehman M., Walther T.C., Olsen J.V., and Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325 (2009) 834-840
42. Arnaudov L.N., and de Vries R. Thermally induced fibrillar aggregation of hen egg white lysozyme. Biophys. J. 88 (2005) 515-526
43. Honig B., and Yang A.S. Free energy balance in protein folding. Adv. Protein Chem. 46 (1995) 27-58
44. Kim H.J., Chatani E., Goto Y., and Paik S.R. Seed-dependent accelerated fibrillation of alpha-synuclein induced by periodic ultrasonication treatment. J. Microbiol. Biotechnol. 17 (2007) 2027-2032
45. Shashilov V., Xu M., Ermolenkov V.V., Fredriksen L., and Lednev I.K. Probing a fibrillation nucleus directly by deep ultraviolet Raman spectroscopy. J. Am. Chem. Soc. 129 (2007) 6972-6973
46. Uversky V.N., and Fink A.L. Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim. Biophys. Acta 1698 (2004) 131-153
47. Bemporad F., Plakoutsi G., Calamai M., Taddei N., Dobson C.M., and Chiti F. Evidence for a mechanism of amyloid formation involving molecular reorganization within native-like precursor aggregates. J. Mol. Biol. 351 (2005) 910-922
48. Bhattacharyya A.M., Thakur A.K., and Wetzel R. Polyglutamine aggregation nucleation: thermodynamics of a highly unfavorable protein folding reaction. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 15400-15405
49. Ecroyd H., Koudelka T., Thorn D.C., Williams D.M., Devlin G., Hoffmann P., and Carver J.A. Dissociation from the oligomeric state is the rate-limiting step in fibril formation by kappa-casein. J. Biol. Chem. 283 (2008) 9012-9022
50. Pace C.N., Grimsley G.R., and Scholtz J.M. Protein ionizable groups: pK values and their contribution to protein stability and solubility. J. Biol. Chem. 284 (2009) 13285-13289
51. Scandurra R., Consalvi V., Chiaraluce R., Politi L., and Engel P.C. Protein thermostability in extremophiles. Biochimie 80 (1998) 933-941
52. Karshikoff A., and Ladenstein R. Ion pairs and the thermotolerance of proteins from hyperthermophiles: a "traffic rule" for hot roads. Trends Biochem. Sci. 26 (2001) 550-556
53. Missimer J.H., Steinmetz M.O., Baron R., Winkler F.K., Kammerer R.A., Daura X., and van Gunsteren W.F. Configurational entropy elucidates the role of salt-bridge networks in protein thermostability. Protein Sci. 16 (2007) 1349-1359
54. Tidor B., and Hendsch Z.S. Do salt bridges stabilize proteins? A continuum electrostatic analysis. Protein Sci. 3 2 (1994) 211-226 Feb
55. Schaefer M., van Vlijmen H.W., and Karplus M. Electrostatic contributions to molecular free energies in solution. Adv. Protein Chem. 51 (1998) 1-57
56. Pfeil W., and Privalov P.L. Thermodynamic investigations of proteins. III. Thermodynamic description of lysozyme. Biophys. Chem. 4 (1976) 41-50
57. Schmittschmitt J.P., and Scholtz J.M. The role of protein stability, solubility, and net charge in amyloid fibril formation. Protein Sci. 12 (2003) 2374-2378
58. Yang Y., and Hamaguchi K. Hydrolysis of 4-methylumbelliferyl N-acetyl-chitotetraoside catalyzed by hen lysozyme. J. Biochem. 88 (1980) 829-836
59. Tracz S.M., Abedini A., Driscoll M., and Raleigh D.P. Role of aromatic interactions in amyloid formation by peptides derived from human amylin. Biochemistry 43 (2004) 15901-15908
60. Bemporad F., Taddei N., Stefani M., and Chiti F. Assessing the role of aromatic residues in the amyloid aggregation of human muscle acylphosphatase. Protein Sci. 15 (2006) 862-870
61. Wu C., Lei H., and Duan Y. The role of Phe in the formation of well-ordered oligomers of amyloidogenic hexapeptide (NFGAIL) observed in molecular dynamics simulations with explicit solvent. Biophys. J. 88 (2005) 2897-2906
62. Stryer L. The interaction of a naphthalene dye with apomyoglobin and apohemoglobin. A fluorescent probe of non-polar binding sites. J. Mol. Biol. 13 (1965) 482-495
63. Plakoutsi G., Bemporad F., Calamai M., Taddei N., Dobson C.M., and Chiti F. Evidence for a mechanism of amyloid formation involving molecular reorganisation within native-like precursor aggregates. J. Mol. Biol. 351 (2005) 910-922
64. Fung S.Y., Keyes C., Duhamel J., and Chen P. Concentration effect on the aggregation of a self-assembling oligopeptide. Biophys. J. 85 (2003) 537-548
65. Powers E.T., and Powers D.L. The kinetics of nucleated polymerizations at high concentrations: amyloid fibril formation near and above the "supercritical concentration". Biophys. J. 91 (2006) 122-132
66. Khajeh K., Naderi-Manesh H., Ranjbar B., Moosavi-Movahedi A., and Nemat-Gorgani M. Chemical modification of lysine residues in Bacillus alpha-amylases: effect on activity and stability. Enzyme Microb. Technol. 28 (2001) 543-549
67. Kammerer R.A., Kostrewa D., Zurdo J., Detken A., Garcia-Echeverria C., Green J.D., Muller S.A., Meier B.H., Winkler F.K., Dobson C.M., and Steinmetz M.O. Exploring amyloid formation by a de novo design. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 4435-4440
68. Ahern T.J., and Klibanov A.M. Analysis of processes causing thermal inactivation of enzymes. Methods Biochem. Anal. 33 (1988) 91-127
69. Volkin D.B., and Klibanov A.M. Thermal destruction processes in proteins involving cystine residues. J. Biol. Chem. 262 (1987) 2945-2950
70. Kudou M., Shiraki K., Fujiwara S., Imanaka T., and Takagi M. Prevention of thermal inactivation and aggregation of lysozyme by polyamines. FEBS J. 270 (2003) 4547-4554
71. Knubovets T., Osterhout J.J., Connolly P.J., and Klibanov A.M. Structure, thermostability, and conformational flexibility of hen egg-white lysozyme dissolved in glycerol. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 1262-1267
72. Babu K.R., and Bhakuni V. Ionic-strength-dependent transition of hen egg-white lysozyme at low pH to a compact state and its aggregation on thermal denaturation. Eur. J. Biochem. 245 (1997) 781-789
73. Qin Z., Hu D., Zhu M., and Fink A.L. Structural characterization of the partially folded intermediates of an immunoglobulin light chain leading to amyloid fibrillation and amorphous aggregation. Biochemistry 46 (2007) 3521-3531
74. Zhou R., Eleftheriou M., Royyuru A.K., and Berne B.J. Destruction of long-range interactions by a single mutation in lysozyme. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 5824-5829
75. Fernandez-Escamilla A.M., Rousseau F., Schymkowitz J., and Serrano L. Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat. Biotechnol. 22 (2004) 1302-1306
76. Conchillo-Sole O., de Groot N.S., Aviles F.X., Vendrell J., Daura X., and Ventura S. AGGRESCAN: a server for the prediction and evaluation of "hot spots" of aggregation in polypeptides. BMC Bioinformatics 8 (2007) 65
77. Ventura S., Zurdo J., Narayanan S., Parreno M., and Mangues R. Short amino acid stretches can mediate amyloid formation in globular proteins: the Src homology 3 (SH3) case. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 7258-7263
78. Lopez-Jaramillo F.J., Perez-Banderas F., Hernandez-Mateo F., and Santoyo-Gonzalez F. Production, crystallization and X-ray characterization of chemically glycosylated hen egg-white lysozyme. Acta. Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 61 (2005) 435-438
79. Morshedi D., Rezaei-Ghaleh N., Ebrahim-Habibi A., Ahmadian S., and Nemat-Gorgani M. Inhibition of amyloid fibrillation of lysozyme by indole derivatives-possible mechanism of action. Febs J. 274 (2007) 6415-6425
80. Aune K.C., and Tanford C. Thermodynamics of the denaturation of lysozyme by guanidine hydrochloride. I. Dependence on pH at 25 degrees. Biochemistry 8 (1969) 4579-4585
81. Nilsson M.R. Techniques to study amyloid fibril formation in vitro. Methods 34 (2004) 151-160
82. Klunk W.E., Pettegrew J.W., and Abraham D.J. Quantitative evaluation of Congo red binding to amyloid-like proteins with a beta-pleated sheet conformation. J. Histochem. Cytochem. 37 (1989) 1273-1281