Pseudocatalytic Antiaggregation Activity of Antibodies: Immunoglobulins can Influence α-Synuclein Aggregation at Substoichiometric Concentrations

Molecular Neurobiology

Volumn 53, Issue 3, 2016, Pages 1949-1958

  Breydo, Leonid ^a,b   Morgan, Dave ^a,b   Uversky, Vladimir N ^a,b,c,d,e  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^d INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

^e INSTITUTE OF CYTOLOGY   (Russian Federation)

Author keywords

Antibodies; Parkinson s disease; Protein aggregation; Synuclein

Indexed keywords

ALPHA SYNUCLEIN; ALPHA SYNUCLEIN ANTIBODY; ANTIBODY; UNCLASSIFIED DRUG; PROTEIN AGGREGATE; THIAZOLE DERIVATIVE; THIOFLAVINE;

ARTICLE; CIRCULAR DICHROISM; CONCENTRATION (PARAMETERS); CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG ACTIVITY; PROTEIN AGGREGATION; PROTEIN PROTEIN INTERACTION; PSEUDOCATALYTIC ANTIAGGREGATION ACTIVITY; SUBSTOICHIOMETRIC CONCENTRATION; BIOASSAY; BIOCATALYSIS; CHEMISTRY; DRUG EFFECTS; FLUORESCENCE; KINETICS; METABOLISM; PROTEINOSIS; ULTRASTRUCTURE;

ALPHA-SYNUCLEIN; ANTIBODIES; BIOCATALYSIS; BIOLOGICAL ASSAY; CIRCULAR DICHROISM; FLUORESCENCE; KINETICS; PROTEIN AGGREGATES; PROTEIN AGGREGATION, PATHOLOGICAL; THIAZOLES;

EID: 84961162986     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-015-9148-8     Document Type: Article

References (37)

1. Bertram L, Tanzi RE (2005) The genetic epidemiology of neurodegenerative disease. J Clin Invest 115(6):1449–1457
2. Breydo L, Wu JW, Uversky VN (2012) Alpha-synuclein misfolding and Parkinson’s disease. Biochim Biophys Acta 1822(2):261–285
3. Uversky VN, Eliezer D (2009) Biophysics of Parkinson’s disease: structure and aggregation of alpha-synuclein. Curr Protein Pept Sci 10(5):483–499
4. Uversky VN (2008) Alpha-synuclein misfolding and neurodegenerative diseases. Curr Protein Pept Sci 9(5):507–540
5. Uversky VN (2007) Neuropathology, biochemistry, and biophysics of alpha-synuclein aggregation. J Neurochem 103(1):17–37
6. Uversky VN (2003) A protein-chameleon: conformational plasticity of alpha-synuclein, a disordered protein involved in neurodegenerative disorders. J Biomol Struct Dyn 21(2):211–234
7. Bae EJ, Lee HJ, Rockenstein E, Ho DH, Park EB, Yang NY, Desplats P, Masliah E, Lee SJ (2012) Antibody-aided clearance of extracellular alpha-synuclein prevents cell-to-cell aggregate transmission. J Neurosci Off J Soc Neurosci 32(39):13454–13469
8. Masliah E, Rockenstein E, Mante M, Crews L, Spencer B, Adame A, Patrick C, Trejo M, Ubhi K, Rohn TT, Mueller-Steiner S, Seubert P, Barbour R, McConlogue L, Buttini M, Games D, Schenk D (2011) Passive immunization reduces behavioral and neuropathological deficits in an alpha-synuclein transgenic model of Lewy body disease. PLoS One 6(4):e19338
9. Lindstrom V, Ihse E, Fagerqvist T, Bergstrom J, Nordstrom E, Moller C, Lannfelt L, Ingelsson M (2014) Immunotherapy targeting alpha-synuclein, with relevance for future treatment of Parkinson’s disease and other Lewy body disorders. Immunotherapy 6(2):141–153
10. Nasstrom T, Goncalves S, Sahlin C, Nordstrom E, Screpanti Sundquist V, Lannfelt L, Bergstrom J, Outeiro TF, Ingelsson M (2011) Antibodies against alpha-synuclein reduce oligomerization in living cells. PLoS One 6(10):e27230
11. Lee HJ, Bae EJ, Lee SJ (2014) Extracellular alpha–synuclein-a novel and crucial factor in Lewy body diseases. Nat Rev Neurol 10(2):92–98
12. Hard T, Lendel C (2012) Inhibition of amyloid formation. J Mol Biol 421(4–5):441–465
13. Habicht G, Haupt C, Friedrich RP, Hortschansky P, Sachse C, Meinhardt J, Wieligmann K, Gellermann GP, Brodhun M, Gotz J, Halbhuber KJ, Rocken C, Horn U, Fandrich M (2007) Directed selection of a conformational antibody domain that prevents mature amyloid fibril formation by stabilizing Abeta protofibrils. Proc Natl Acad Sci U S A 104(49):19232–19237
14. Ladiwala AR, Bhattacharya M, Perchiacca JM, Cao P, Raleigh DP, Abedini A, Schmidt AM, Varkey J, Langen R, Tessier PM (2012) Rational design of potent domain antibody inhibitors of amyloid fibril assembly. Proc Natl Acad Sci U S A 109(49):19965–19970
15. Wang XP, Zhang JH, Wang YJ, Feng Y, Zhang X, Sun XX, Li JL, Du XT, Lambert MP, Yang SG, Zhao M, Klein WL, Liu RT (2009) Conformation-dependent single-chain variable fragment antibodies specifically recognize beta-amyloid oligomers. FEBS Lett 583(3):579–584
16. Lafaye P, Achour I, England P, Duyckaerts C, Rougeon F (2009) Single-domain antibodies recognize selectively small oligomeric forms of amyloid beta, prevent Abeta-induced neurotoxicity and inhibit fibril formation. Mol Immunol 46(4):695–704
17. Dumoulin M, Last AM, Desmyter A, Decanniere K, Canet D, Larsson G, Spencer A, Archer DB, Sasse J, Muyldermans S, Wyns L, Redfield C, Matagne A, Robinson CV, Dobson CM (2003) A camelid antibody fragment inhibits the formation of amyloid fibrils by human lysozyme. Nature 424(6950):783–788
18. Legleiter J, Lotz GP, Miller J, Ko J, Ng C, Williams GL, Finkbeiner S, Patterson PH, Muchowski PJ (2009) Monoclonal antibodies recognize distinct conformational epitopes formed by polyglutamine in a mutant huntingtin fragment. J Biol Chem 284(32):21647–21658
19. McLaurin J, Cecal R, Kierstead ME, Tian X, Phinney AL, Manea M, French JE, Lambermon MH, Darabie AA, Brown ME, Janus C, Chishti MA, Horne P, Westaway D, Fraser PE, Mount HT, Przybylski M, St George-Hyslop P (2002) Therapeutically effective antibodies against amyloid-beta peptide target amyloid-beta residues 4–10 and inhibit cytotoxicity and fibrillogenesis. Nat Med 8(11):1263–1269
20. Subramanian S, Madhavadas S, Balasubramanian P (2009) Influence of conformational antibodies on dissociation of fibrillar amyloid beta (A beta 1–42) in vitro. Indian J Exp Biol 47(5):309–313
21. Mamikonyan G, Necula M, Mkrtichyan M, Ghochikyan A, Petrushina I, Movsesyan N, Mina E, Kiyatkin A, Glabe CG, Cribbs DH, Agadjanyan MG (2007) Anti-abeta1 11 antibody binds to different beta-amyloid species, inhibits fibril formation, and disaggregates preformed fibrils but not the most toxic oligomers. J Biol Chem 282(31):22376–22386
22. Solomon B, Koppel R, Frankel D, Hanan-Aharon E (1997) Disaggregation of Alzheimer beta-amyloid by site-directed mAb. Proc Natl Acad Sci U S A 94(8):4109–4112
23. Buell AK, Galvagnion C, Gaspar R, Sparr E, Vendruscolo M, Knowles TP, Linse S, Dobson CM (2014) Solution conditions determine the relative importance of nucleation and growth processes in alpha-synuclein aggregation. Proc Natl Acad Sci U S A
24. Holmes BB, DeVos SL, Kfoury N, Li M, Jacks R, Yanamandra K, Ouidja MO, Brodsky FM, Marasa J, Bagchi DP, Kotzbauer PT, Miller TM, Papy-Garcia D, Diamond MI (2013) Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc Natl Acad Sci U S A 110(33):E3138–E3147
25. Bolen DW, Rose GD (2008) Structure and energetics of the hydrogen-bonded backbone in protein folding. Annu Rev Biochem 77:339–362
26. Canchi DR, Garcia AE (2013) Cosolvent effects on protein stability. Annu Rev Phys Chem 64:273–293
27. Giasson BI, Jakes R, Goedert M, Duda JE, Leight S, Trojanowski JQ, Lee VM (2000) A panel of epitope-specific antibodies detects protein domains distributed throughout human alpha-synuclein in Lewy bodies of Parkinson’s disease. J Neurosci Res 59(4):528–533
28. Necula M, Kayed R, Milton S, Glabe CG (2007) Small molecule inhibitors of aggregation indicate that amyloid beta oligomerization and fibrillization pathways are independent and distinct. J Biol Chem 282(14):10311–10324
29. Breydo L, Reddy KD, Piai A, Felli IC, Pierattelli R, Uversky VN (2014) The crowd you’re in with: effects of different types of crowding agents on protein aggregation. Biochim Biophys Acta 1844(2):346–357
30. Uversky VN, Li J, Fink AL (2001) Evidence for a partially folded intermediate in alpha-synuclein fibril formation. J Biol Chem 276(14):10737–10744
31. Wu JW, Breydo L (2014) Conformation-dependent antibodies as tools for characterization of amyloid protein aggregates. In: Uversky VN, Lyubchenko YL (eds) Bionanoimaging in protein misfolding and aggregation. Elsevier, New York
32. Morgado I, Wieligmann K, Bereza M, Ronicke R, Meinhardt K, Annamalai K, Baumann M, Wacker J, Hortschansky P, Malesevic M, Parthier C, Mawrin C, Schiene-Fischer C, Reymann KG, Stubbs MT, Balbach J, Gorlach M, Horn U, Fandrich M (2012) Molecular basis of beta-amyloid oligomer recognition with a conformational antibody fragment. Proc Natl Acad Sci U S A 109(31):12503–12508
33. Haupt C, Morgado I, Kumar ST, Parthier C, Bereza M, Hortschansky P, Stubbs MT, Horn U, Fandrich M (2011) Amyloid fibril recognition with the conformational B10 antibody fragment depends on electrostatic interactions. J Mol Biol 405(2):341–348
34. Sultan A, Raman B, Rao Ch M, Tangirala R (2013) The extracellular chaperone haptoglobin prevents serum fatty acid-promoted amyloid fibril formation of beta2-microglobulin, resistance to lysosomal degradation, and cytotoxicity. J Biol Chem 288(45):32326–32342
35. Mansson C, Kakkar V, Monsellier E, Sourigues Y, Harmark J, Kampinga HH, Melki R, Emanuelsson C (2014) DNAJB6 is a peptide-binding chaperone which can suppress amyloid fibrillation of polyglutamine peptides at substoichiometric molar ratios. Cell Stress Chaperones 19(2):227–239
36. Knight SD, Presto J, Linse S, Johansson J (2013) The BRICHOS domain, amyloid fibril formation, and their relationship. Biochemistry 52(43):7523–7531
37. Luo J, Warmlander SK, Graslund A, Abrahams JP (2014) Non-chaperone proteins can inhibit aggregation and cytotoxicity of Alzheimer amyloid beta peptide. J Biol Chem 289(40):27766–27775