class A beta-lactamases; hybrid enzymes; polyglutamine model protein; epitope mapping; antigen display; immunodetection; phage display; difficult to express protein; de novo antigen
Abstract :
[en] Designing hybrid proteins is a major aspect of protein engineering and covers a very wide range of applications frombasic research
to medical applications. This review focuses on the use of class A 𝛽-lactamases as versatile scaffolds to design hybrid enzymes
(referred to as 𝛽-lactamase hybrid proteins, BHPs) in which an exogenous peptide, protein or fragment thereof is inserted at
various permissive positions.We discuss how BHPs can be specifically designed to create bifunctional proteins, to produce and to
characterize proteins that are otherwise difficult to express, to determine the epitope of specific antibodies, to generate antibodies
against nonimmunogenic epitopes, and to better understand the structure/function relationship of proteins.
Research center :
CIP - Centre d'Ingénierie des Protéines - ULiège
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Huynen, Céline ; Université de Liège - ULiège > Département des sciences de la vie > Enzymologie et repliement des protéines
Filée, Patrice; Progénosis
Matagne, André ; Université de Liège - ULiège > Département des sciences de la vie > Enzymologie et repliement des protéines
Galleni, Moreno ; Université de Liège - ULiège > Département des sciences de la vie > Macromolécules biologiques
Dumoulin, Mireille ; Université de Liège - ULiège > Département des sciences de la vie > Enzymologie et repliement des protéines
Language :
English
Title :
Class A β -Lactamases as Versatile Scaffolds to Create Hybrid Enzymes: Applications from Basic Research to Medicine
Publication date :
28 August 2013
Journal title :
BioMed Research International
ISSN :
2314-6133
eISSN :
2314-6141
Publisher :
Hindawi
Volume :
2013
Pages :
16
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE] PAI Région wallonne [BE]
Beguin P., Hybrid enzymes. Current Opinion in Biotechnology 1999 10 336 340
Collinet B., Hervé M., Pecorari F., Minard P., Eder O., Desmadril M., Functionally accepted insertions of proteins within protein domains. Journal of Biological Chemistry 2000 275 23 17428 17433 2-s2.0-0034625370 10.1074/jbc.M000666200
Betton J.-M., Jacob J. P., Hofnung M., Broome-Smith J. K., Creating a bifunctional protein by insertion of β -lactamase into the maltodextrin-binding protein. Nature Biotechnology 1997 15 12 1276 1279 2-s2.0-0030696198
Martin J. L., Bardwell J. C. A., Kuriyan J., Crystal structure of the DsbA protein required for disulphide bond formation in vivo. Nature 1993 365 6445 464 468 2-s2.0-0027373949 10.1038/365464a0
Delarue M., Poch O., Tordo N., Moras D., Argos P., An attempt to unify the structure of polymerases. Protein Engineering 1990 3 6 461 467 2-s2.0-0025040632
Levine M., Muirhead H., Stammers D. K., Stuart D. I., Structure of pyruvate kinase and similarities with other enzymes: possible implications for protein taxonomy and evolution. Nature 1978 271 5646 626 630 2-s2.0-0017813889
Jones S., Stewart M., Michie A., Swindells M. B., Orengo C., Thornton J. M., Domain assignment for protein structures using a consensus approach: characterization and analysis. Protein Science 1998 7 2 233 242 2-s2.0-0031889752
Bannister D., Popovic B., Sridharan S., Giannotta F., Filée P., Yilmaz N., Minter R., Epitope mapping and key amino acid identification of anti-CD22 immunotoxin CAT-8015 using hybrid-lactamase display. Protein Engineering, Design and Selection 2011 24 4 351 360 2-s2.0-79952645843 10.1093/protein/gzq114
Ruth N., Quinting B., Mainil J., Hallet B., Frère J.-M., Huygen K., Galleni M., Creating hybrid proteins by insertion of exogenous peptides into permissive sites of a class A β -lactamase. FEBS Journal 2008 275 20 5150 5160 2-s2.0-52449127994 10.1111/j.1742-4658.2008.06646.x
Vandevenne M., Filee P., Scarafone N., Cloes B., Gaspard G., Yilmaz N., Dumoulin M., François J.-M., Frère J.-M., Galleni M., The Bacillus licheniformis BlaP β -lactamase as a model protein scaffold to study the insertion of protein fragments. Protein Science 2007 16 10 2260 2271 2-s2.0-34748920256 10.1110/ps.072912407
Chevigné A., Yilmaz N., Gaspard G., Giannotta F., François J. M., Frère J. M., Galleni M., Filée P., Use of bifunctional hybrid β -lactamases for epitope mapping and immunoassay development. Journal of Immunological Methods 2007 320 1-2 81 93 2-s2.0-33847359217 10.1016/j.jim.2006.12.009
Vandevenne M., Gaspard G., Belgsir E. M., Ramnath M., Cenatiempo Y., Marechal D., Dumoulin M., Frere J.-M., Matagne A., Galleni M., Filee P., Effects of monopropanediamino- β -cyclodextrin on the denaturation process of the hybrid protein BlaPChBD. Biochimica et Biophysica Acta 2011 1814 9 1146 1153 2-s2.0-79959764395 10.1016/j.bbapap.2011.05.007
Vandevenne M., Gaspard G., Yilmaz N., Giannotta F., Frère J. M., Galleni M., Filée P., Rapid and easy development of versatile tools to study protein/ligand interactions. Protein Engineering, Design and Selection 2008 21 7 443 451 2-s2.0-45849090688 10.1093/protein/gzn021
Ruth N., Mainil J., Roupie V., Frère J.-M., Galleni M., Huygen K., DNA vaccination for the priming of neutralizing antibodies against non-immunogenic STa enterotoxin from enterotoxigenic Escherichia coli. Vaccine 2005 23 27 3618 3627 2-s2.0-18044386165 10.1016/j.vaccine.2004.11.080
Zervosen A., Saegerman C., Antoniotti I., Robert B., Ruth N., Collard A., Schynts F., Galleni M., Mercuri P. S., Characterization of the cattle serum antibody responses against TEM β -lactamase and the nonimmunogenic Escherichia coli heat-stable enterotoxin (STaI). FEMS Immunology and Medical Microbiology 2008 54 3 319 329 2-s2.0-56049083043 10.1111/j.1574-695X.2008. 00482.x
Scarafone N., Pain C., Fratamico A., Gaspard G., Yilmaz N., Filée P., Galleni M., Matagne A., Dumoulin M., Amyloid-like fibril formation by polyq proteins: a critical balance between the polyq length and the constraints imposed by the host protein. PLoS One 2012 7 3 2-s2.0-84857936144 10.1371/journal.pone.0031253 e31253
Ambler R. P., Coulson A. F. W., Frere J.-M., Ghuysen J.-M., Joris B., Forsman M., Levesque R. C., Tiraby G., Waley S. G., A standard numbering scheme for the class A β -lactamases. Biochemical Journal 1991 276 1 269 270 2-s2.0-0025870126
Knox J. R., Moews P. C., -Lactamase of Bacillus licheniformis 749/C. Refinement at 2 Å resolution and analysis of hydration. Journal of Molecular Biology 1991 220 2 435 455 2-s2.0-0025923511
Fonze E., Charlier P., To'th Y., Vermeire M., Raquet X., Dubus A., Frere J. M., TEM1 beta-lactamase structure solved by molecular replacement and refined structure of the S235A mutant. Acta Crystallographica D 1995 51 5 682 694 2-s2.0-0028870390 10.1107/S0907444994014496
Hallet B., Sherratt D. J., Hayes F., Pentapeptide scanning mutagenesis: random insertion of a variable five amino acid cassette in a target protein. Nucleic Acids Research 1997 25 9 1866 1867 2-s2.0-0030825248 10.1093/nar/25.9.1866
Moore J. T., Davis S. T., Dev I. K., The development of β -lactamase as a highly versatile genetic reporter for eukaryotic cells. Analytical Biochemistry 1997 247 2 203 209 2-s2.0-0031149894 10.1006/abio.1997.2092
Zlokarnik G., Negulescu P. A., Knapp T. E., Mere L., Burres N., Feng L., Whitney M., Roemer K., Tsien R. Y., Quantitation of transcription and clonal selection of single living cells with β -lactamase as reporter. Science 1998 279 5347 84 88 2-s2.0-0032472195 10.1126/science.279.5347.84
Oosterom J., van Doornmalen E. J. P., Lobregt S., Blomenröhr M., Zaman G. J. R., High-throughput screening using β -lactamase reporter-gene technology for identification of low-molecular-weight antagonists of the human gonadotropin releasing hormone receptor. Assay and Drug Development Technologies 2005 3 2 143 154 2-s2.0-20544445672 10.1089/adt.2005.3.143
Vandevenne M., Galleni M., Filee P., How to make a good use of a "Bad Enzyme": utilisation of efficient beta-lactamase for the benefits of biochemical research. Beta-Lactamases 2011 New York, NY, USA Nova Science
Jelsch C., Mourey L., Masson J.-M., Samama J.-P., Crystal structure of Escherichia coli TEM1 β -lactamase at 1.8 Å resolution. Proteins 1993 16 4 364 383 2-s2.0-0027275788
Moews P. C., Knox J. R., Dideberg O., Charlier P., Frere J.-M., β -Lactamase of Bacillus licheniformis 749/C at 2 Å resolution. Proteins 1990 7 2 156 171 2-s2.0-0025271184
Charpentier X., Oswald E., Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 β -lactamase as a new fluorescence-based reporter. Journal of Bacteriology 2004 186 16 5486 5495 2-s2.0-3843065509 10.1128/JB.186.16.5486-5495.2004
Matagne A., Misselyn-Bauduin A.-M., Joris B., Erpicum T., Granier B., Frere J.-M., The diversity of the catalytic properties of class A β -lactamases. Biochemical Journal 1990 265 1 131 146 2-s2.0-0025091910
Wu X.-C., Lee W., Tran L., Wong S.-L., Engineering a Bacillus subtilis expression-secretion system with a strain deficient in six extracellular proteases. Journal of Bacteriology 1991 173 16 4952 4958 2-s2.0-0026338822
Veith B., Herzberg C., Steckel S., Feesche J., Maurer K. H., Ehrenreich P., Bäumer S., Henne A., Liesegang H., Merkl R., Ehrenreich A., Gottschalk G., The complete genome sequence of Bacillus licheniformis DSM13, an organism with great industrial potential. Journal of Molecular Microbiology and Biotechnology 2004 7 4 204 211 2-s2.0-4644259296 10.1159/000079829
Tjoelker L. W., Gosting L., Frey S., Hunter C. L., Le Trong H., Steiner B., Brammer H., Gray P. W., Structural and functional definition of the human chitinase chitin- binding domain. Journal of Biological Chemistry 2000 275 1 514 520 2-s2.0-0034614497 10.1074/jbc.275.1.514
Hollak C. E. M., Van Weely S., Van Oers M. H. J., Aerts J. M. F. G., Marked elevation of plasma chitotriosidase activity. A novel hallmark of Gaucher disease. Journal of Clinical Investigation 1994 93 3 1288 1292 2-s2.0-0028220472
Boot R. G., Van Achterberg T. A. E., Van Aken B. E., Renkema G. H., Jacobs M. J. H. M., Aerts J. M. F. G., De Vries C. J. M., Strong induction of members of the chitinase family of proteins in atherosclerosis: chitotriosidase and human cartilage gp-39 expressed in lesion macrophages. Arteriosclerosis, Thrombosis, and Vascular Biology 1999 19 3 687 694 2-s2.0-0032975495
Overdijk B., Van Steijn G. J., Human serum contains a chitinase: identification of an enzyme, formerly described as 4-metbylumbelliferyl-tetra-N- acetylchitotetraoside hydrolase (MU-TACT hydrolase). Glycobiology 1994 4 6 797 803 2-s2.0-0028566913
Overdijk B., Van Steijn G. J., Odds F. C., Chitinase levels in guinea pig blood are increased after systemic infection with Aspergillus fumigatus. Glycobiology 1996 6 6 627 634 2-s2.0-0029854392 10.1093/glycob/6.6.627
Dumoulin M., Last A. M., Desmyter A., Decanniere K., Canet D., Larsson G., Spencer A., Archer D. B., Sasse J., Muyldermans S., Wyns L., Redfield C., Matagne A., Robinson C. V., Dobson C. M., A camelid antibody fragment inhibits the formation of amyloid fibrils by human lysozyme. Nature 2003 424 6950 783 788 2-s2.0-0042467574 10.1038/nature01870
De Genst E., Chan P., Pardon E., Hsu S. T., Kumita J., Christodoulou J., Menzer L., Chirgadze D., Robinson C., Muyldermans S., Matagne A., Wyns L., Dobson C. M., Dumoulin M., A nanobody binding to non-amyloidogenic regions of the protein human lysozyme enhances partial unfolding but inhibits amyloid fibril formation. Journal of Physical Chemistry. In press
Gershoni J. M., Roitburd-Berman A., Siman-Tov D. D., Freund N. T., Weiss Y., Epitope mapping: the first step in developing epitope-based vaccines. BioDrugs 2007 21 3 145 156 2-s2.0-34249725007 10.2165/00063030-200721030-00002
Obungu V. H., Gelfanova V., Rathnachalam R., Bailey A., Sloan-Lancaster J., Huang L., Determination of the mechanism of action of anti-FasL antibody by epitope mapping and homology modeling. Biochemistry 2009 48 30 7251 7260 2-s2.0-70350712762 10.1021/bi900296g
Paterson Y., Englander S. W., Roder H., An antibody binding site on cytochrome c defined by hydrogen exchange and two-dimensional NMR. Science 1990 249 4970 755 759 2-s2.0-0025142485
Reineke U., Volkmer-Engert R., Schneider-Mergener J., Applications of peptide arrays prepared by the spot-technology. Current Opinion in Biotechnology 2001 12 1 59 64 2-s2.0-0035823285 10.1016/S0958-1669(00)00178-6
Smith G. P., Scott J. K., Libraries of peptides and proteins displayed on filamentous phage. Methods in Enzymology 1993 217 228 257 2-s2.0-0027266779
Zwick M. B., Shen J., Scott J. K., Phage-displayed peptide libraries. Current Opinion in Biotechnology 1998 9 4 427 436 2-s2.0-0032146224 10.1016/S0958-1669(98)80017-7
Williams S. C., Badley R. A., Davis P. J., Puijk W. C., Meloen R. H., Identification of epitopes within beta lactoglobulin recognised by polyclonal antibodies using phage display and PEPSCAN. Journal of Immunological Methods 1998 213 1 1 17 2-s2.0-0031817073 10.1016/S0022-1759(98)00022-2
Van Zonneveld A.-J., Identification of functional interaction sites on proteins using bacteriophage-displayed random epitope libraries. Gene 1995 167 1-2 49 52 2-s2.0-0029584350 10.1016/0378-1119(95)00614-1
Wang L.-F., Du Plessis D. H., White J. R., Hyatt A. D., Eaton B. T., Use of a gene-targeted phage display random epitope library to map an antigenic determinant on the bluetongue virus outer capsid protein VP5. Journal of Immunological Methods 1995 178 1 1 12 2-s2.0-0028801675 10.1016/0022-1759(94) 00235-O
Smith G. P., Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 1985 228 4705 1315 1317 2-s2.0-0021818675
Rodi D. J., Makowski L., Phage-display technology-finding a needle in a vast molecular haystack. Current Opinion in Biotechnology 1999 10 1 87 93 2-s2.0-0032901290 10.1016/S0958-1669(99)80016-0
Clackson T., Hoogenboom H. R., Griffiths A. D., Winter G., Making antibody fragments using phage display libraries. Nature 1991 352 6336 624 628 2-s2.0-0025835310 10.1038/352624a0
Pande J., Szewczyk M. M., Grover A. K., Phage display: concept, innovations, applications and future. Biotechnology Advances 2010 28 6 849 858 2-s2.0-77957017501 10.1016/j.biotechadv.2010.07.004
Legendre D., Soumillion P., Fastrez J., Engineering a regulatable enzyme for homogeneous immunoassays. Nature Biotechnology 1999 17 1 67 72 2-s2.0-0032956429 10.1038/5243
Du X., Beers R., FitzGerald D. J., Pastan I., Differential cellular internalization of anti-CD19 and -CD22 immunotoxins results in different cytotoxic activity. Cancer Research 2008 68 15 6300 6305 2-s2.0-51049120495 10.1158/0008-5472.CAN-08-0461
Clark E. A., CD22, a B cell-specific receptor, mediates adhesion and signal transduction. Journal of Immunology 1993 150 11 4715 4718 2-s2.0-0027241438
Crocker P. R., Varki A., Siglecs, sialic acids and innate immunity. Trends in Immunology 2001 22 6 337 342 2-s2.0-0034913685 10.1016/S1471-4906(01) 01930-5
May A. P., Robinson R. C., Vinson M., Crocker P. R., Jones E. Y., Crystal structure of the N-terminal domain of sialoadhesin in complex with 3′ sialyllactose at 1.85 Å resolution. Molecular Cell 1998 1 5 719 728 2-s2.0-0032037915
Mussai F., Campana D., Bhojwani D., Stetler-Stevenson M., Steinberg S. M., Wayne A. S., Pastan I., Cytotoxicity of the anti-CD22 immunotoxin HA22 (CAT-8015) against paediatric acute lymphoblastic leukaemia: research paper. British Journal of Haematology 2010 150 3 352 358 2-s2.0-77954566553 10.1111/j.1365-2141.2010.08251.x
Alderson R. F., Kreitman R. J., Chen T., Yeung P., Herbst R., Fox J., Pastan I., CAT-8015: a second-generation pseudomonas exotoxin a-based immunotherapy targeting CD22-expressing hematologic malignancies. Clinical Cancer Research 2009 15 3 832 839 2-s2.0-61349115036 10.1158/1078-0432.CCR-08- 1456
DiJoseph J. F., Popplewell A., Tickle S., Ladyman H., Lawson A., Kunz A., Khandke K., Armellino D. C., Boghaert E. R., Hamann P. R., Zinkewich-Peotti K., Stephens S., Weir N., Damle N. K., Antibody-targeted chemotherapy of B-cell lymphoma using calicheamicin conjugated to murine or humanized antibody against CD22. Cancer Immunology, Immunotherapy 2005 54 1 11 24 2-s2.0-19944426031 10.1007/s00262-004-0572-2
Leclerc C., Lo-Man R., Charbit A., Martineau P., Clement J. M., Hofnung M., Immunogenicity of viral B- and T-cell epitopes expressed in recombinant bacterial proteins. International Reviews of Immunology 1994 11 2 123 132 2-s2.0-0028002691
Holland R. E., Some infectious causes of diarrhea in young farm animals. Clinical Microbiology Reviews 1990 3 4 345 375 2-s2.0-0025066262
Nagy B., Fekete P. Z., Enterotoxigenic Escherichia coli (ETEC) in farm animals. Veterinary Research 1999 30 2-3 259 284 2-s2.0-0033091983
Gariépy J., Judd A. K., Schoolnik G. K., Importance of disulfide bridges in the structure and activity of Escherichia coli enterotoxin ST1b. Proceedings of the National Academy of Sciences of the United States of America 1987 84 24 8907 8911 2-s2.0-0023460826
Moseley S. L., Hardy J. W., Huq M. I., Isolation and nucleotide sequence determination of a gene encoding a heat-stable enterotoxin of Escherichia coli. Infection and Immunity 1983 39 3 1167 1174 2-s2.0-0020656141
Lockwood D. E., Robertson D. C., Development of a competitive enzyme-linked immunosorbent assay (ELISA) for Escherichia coli heat-stable enterotoxin (ST(a)). Journal of Immunological Methods 1984 75 2 295 307 2-s2.0-0021674360 10.1016/0022-1759(84)90113-3
Svennerholm A.-M., Wikstrom M., Lindblad M., Holmgren J., Monoclonal antibodies against Escherichia coli heat-stable toxin (STa) and their use in a diagnostic ST ganglioside GM1-enzyme-linked immunosorbent assay. Journal of Clinical Microbiology 1986 24 4 585 590 2-s2.0-0022459288
Sanchez J., Svennerholm A.-M., Holmgren J., Genetic fusion of a non-toxic heat-stable enterotoxin-related decapeptide antigen to cholera toxin B-subunit. FEBS Letters 1988 241 1-2 110 114 2-s2.0-0024272945 10.1016/0014-5793(88)81041- X
Klipstein F. A., Engert R. F., Clements J. D., Houghten R. A., Vaccine for enterotoxigenic Escherichia coli based on synthetic heat-stable toxin crossed-linked to the B subunit of heat-labile toxin. Journal of Infectious Diseases 1983 147 2 318 326 2-s2.0-0020684865
Batisson I., Der Vartanian M., Contribution of defined amino acid residues to the immunogenicity of recombinant Escherichia coli heat-stable enterotoxin fusion proteins. FEMS Microbiology Letters 2000 192 2 223 229 2-s2.0-0034669389 10.1016/S0378-1097(00)00439-0
Sanchez J., Argotte R., Buelna A., Engineering of cholera toxin A-subunit for carriage of epitopes at its amino end. FEBS Letters 1997 401 1 95 97 2-s2.0-0031027372 10.1016/S0014-5793(96)01445-7
Aitken R., Hirst T. R., Recombinant enterotoxins as vaccines against Escherichia coli -mediated diarrhoea. Vaccine 1993 11 2 227 233 2-s2.0-0027466064 10.1016/0264-410X(93)90022-P
Sanchez J., Uhlin B. E., Grundstrom T., Immunoactive chimeric ST-LT enterotoxins of Escherichia coli generated by in vitro gene fusion. FEBS Letters 1986 208 2 194 198 2-s2.0-0022974852
Pereira C. M., Guth B. E., Sbrogio-Almeida M. E., Castilho B. A., Antibody response against Escherichia coli heat-stable enterotoxin expressed as fusions to flagellin. Microbiology 2001 147 4 861 867 2-s2.0-0035047438
Wu C.-M., Chung T.-C., Mice protected by oral immunization with Lactobacillus reuteri secreting fusion protein of Escherichia coli enterotoxin subunit protein. FEMS Immunology and Medical Microbiology 2007 50 3 354 365 2-s2.0-34447285246 10.1111/j.1574-695X.2007.00255.x
Hands S. L., Wyttenbach A., Neurotoxic protein oligomerisation associated with polyglutamine diseases. Acta Neuropathologica 2010 120 4 419 437 2-s2.0-77956184558 10.1007/s00401-010-0703-0
Zoghbi H. Y., Orr H. T., Glutamine repeats and neurodegeneration. Annual Review of Neuroscience 2000 23 217 247 2-s2.0-0034094873 10.1146/annurev.neuro. 23.1.217
Orr H. T., Zoghbi H. Y., Trinucleotide repeat disorders. Annual Review of Neuroscience 2007 30 575 621 2-s2.0-34547692622 10.1146/annurev.neuro.29. 051605.113042
Ross C. A., Intranuclear neuronal inclusions: a common pathogenic mechanism for glutamine-repeat neurodegenerative diseases? Neuron 1997 19 6 1147 1150 2-s2.0-0031446233 10.1016/S0896-6273(00)80405-5
Wetzel R., Alvarado M. R., Kelly J. W., Dobson C. M., Misfolding and aggregation in Huntington disease and other expanded Polyglutamine repeat diseases. Protein Misfolding Diseases 2010 New York, NY, USA Wiley 305 324
Ordway J. M., Tallaksen-Greene S., Gutekunst C.-A., Bernstein E. M., Cearley J. A., Wiener H. W., Dure L. S. IV, Lindsey R., Hersch S. M., Jope R. S., Albin R. L., Detloff P. J., Ectopically expressed CAG repeats cause intranuclear inclusions and a progressive late onset neurological phenotype in the mouse. Cell 1997 91 6 753 763 2-s2.0-0031469707 10.1016/S0092-8674(00)80464- X
Chen Y. W., Stott K., Perutz M. F., Crystal structure of a dimeric chymotrypsin inhibitor 2 mutant containing an inserted glutamine repeat. Proceedings of the National Academy of Sciences of the United States of America 1999 96 4 1257 1261 2-s2.0-0000522537 10.1073/pnas.96.4.1257
Gordon-Smith D. J., Carbajo R. J., Stott K., Neuhaus D., Solution studies of chymotrypsin inhibitor-2 glutamine insertion mutants show no interglutamine interactions. Biochemical and Biophysical Research Communications 2001 280 3 855 860 2-s2.0-0034814752 10.1006/bbrc.2000.4196
Ross C. A., Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders. Neuron 2002 35 5 819 822 2-s2.0-0037194897 10.1016/S0896-6273(02)00872-3
Bauer P. O., Nukina N., The pathogenic mechanisms of polyglutamine diseases and current therapeutic strategies. Journal of Neurochemistry 2009 110 6 1737 1765 2-s2.0-69949170793 10.1111/j.1471-4159.2009.06302.x
Penney J. B. Jr., Vonsattel J.-P., MacDonald M. E., Gusella J. F., Myers R. H., CAG repeat number governs the development rate of pathology in huntington's disease. Annals of Neurology 1997 41 5 689 692 2-s2.0-0030919726 10.1002/ana.410410521
Davies S. W., Turmaine M., Cozens B. A., DiFiglia M., Sharp A. H., Ross C. A., Scherzinger E., Wanker E. E., Mangiarini L., Bates G. P., Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 1997 90 3 537 548 2-s2.0-18544410106 10.1016/S0092-8674(00)80513-9
Bulone D., Masino L., Thomas D. J., San Biagio P. L., Pastore A., The interplay between polyQ and protein context delays aggregation by forming a reservoir of protofibrils. PLoS One 2006 1 1, article e111 2-s2.0-35648992125 10.1371/journal.pone.0000111
Nozaki K., Onodera O., Takano H., Tsuji S., Amino acid sequences flanking polyglutamine stretches influence their potential for aggregate formation. NeuroReport 2001 12 15 3357 3364 2-s2.0-0035968933
Bhattacharyya A., Thakur A. K., Chellgren V. M., Thiagarajan G., Williams A. D., Chellgren B. W., Creamer T. P., Wetzel R., Oligoproline effects on polyglutamine conformation and aggregation. Journal of Molecular Biology 2006 355 3 524 535 2-s2.0-28944446477 10.1016/j.jmb.2005.10.053
Masino L., Kelly G., Leonard K., Trottier Y., Pastore A., Solution structure of polyglutamine tracts in GST-polyglutamine fusion proteins. FEBS Letters 2002 513 2-3 267 272 2-s2.0-0037181179 10.1016/S0014-5793(02)02335-9
Robertson A. L., Bate M. A., Buckle A. M., Bottomley S. P., The rate of polyQ-mediated aggregation is dramatically affected by the number and location of surrounding domains. Journal of Molecular Biology 2011 413 4 879 887 2-s2.0-80054855376 10.1016/j.jmb.2011.09.014
Robertson A. L., Bottomley S. P., Towards the treatment of polyglutamine diseases: the modulatory role of protein context. Current Medicinal Chemistry 2010 17 27 3058 3068 2-s2.0-77955647254 10.2174/092986710791959800
Tobelmann M. D., Murphy R. M., Location trumps length: polyglutamine-mediated changes in folding and aggregation of a host protein. Biophysical Journal 2011 100 11 2773 2782 2-s2.0-79960320014 10.1016/j.bpj.2011.04.028
Chow M. K. M., Ellisdon A. M., Cabrita L. D., Bottomley S. P., Purification of Polyglutamine Proteins1. Methods in Enzymology 2006 413 1 19 2-s2.0-33749516084 10.1016/S0076-6879(06)13001-3
Tanaka M., Morishima I., Akagi T., Hashikawa T., Nukina N., Intra- and intermolecular β -pleated sheet formation in glutamine-repeat inserted myoglobin as a model for polyglutamine diseases. Journal of Biological Chemistry 2001 276 48 45470 45475 2-s2.0-0035976971 10.1074/jbc.M107502200
Aachmann F. L., Otzen D. E., Larsen K. L., Wimmer R., Structural background of cyclodextrin-protein interactions. Protein Engineering 2003 16 12 905 912 2-s2.0-1442359491
Irie T., Uekama K., Cyclodextrins in peptide and protein delivery. Advanced Drug Delivery Reviews 1999 36 1 101 123 2-s2.0-0033105151 10.1016/S0169-409X(98)00057-X
Szejtli J., Introduction and general overview of cyclodextrin chemistry. Chemical Reviews 1998 98 5 1743 1754 2-s2.0-0346461917
