Potent and specific inhibition of glycosidases by small artificial binding proteins (Affitins)

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Correa, Agustín ^a,b   Pacheco, Sabino ^b,c,d   Mechaly, Ariel E ^a,b   Obal, Gonzalo ^a   Béhar, Ghislaine ^b,c,d   Mouratou, Barbara ^b,c,d   Oppezzo, Pablo ^a   Alzari, Pedro M ^b   Pecorari, Frédéric ^b,c,d  

^a INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

^b CNRS   (France)

^c Team 12   (France)

^d UNIVERSITÉ DE NANTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AFFITIN; BACTERIAL ENZYME; GLYCOSIDASE; GLYCOSIDASE INHIBITOR; LYSOZYME; PROTEIN CELD; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BETA GLUCOSIDASE; CARRIER PROTEIN; CELC PROTEIN, BACTERIA; ENZYME INHIBITOR; MULTIPROTEIN COMPLEX; OLIGONUCLEOTIDE;

ARTICLE; BINDING AFFINITY; CATALYSIS; CLOSTRIDIUM THERMOCELLUM; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG POTENCY; DRUG PROTEIN BINDING; DRUG PURIFICATION; DRUG STABILITY; EGG; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; NONHUMAN; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; THERMOSTABILITY; AMINO ACID SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; CALORIMETRY; CHEMICAL STRUCTURE; CHEMISTRY; CHICKEN; CRYSTALLOGRAPHY; DNA SEQUENCE; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROCEDURES; PROTEIN ENGINEERING; X RAY DIFFRACTION;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; BETA-GLUCOSIDASE; CALORIMETRY; CARRIER PROTEINS; CHICKENS; CLOSTRIDIUM THERMOCELLUM; CRYSTALLOGRAPHY; ENZYME INHIBITORS; ESCHERICHIA COLI; GLYCOSIDE HYDROLASES; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; MURAMIDASE; OLIGONUCLEOTIDES; PROTEIN ENGINEERING; SEQUENCE ANALYSIS, DNA; SUBSTRATE SPECIFICITY; X-RAY DIFFRACTION;

EID: 84901281489     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097438     Document Type: Article

References (53)

1. Bischoff H (1995) The mechanism of alpha-glucosidase inhibition in the management of diabetes. Clin Invest Med 18: 303-311.
2. Hruska KS, LaMarca ME, Scott CR, Sidransky E (2008) Gaucher disease: mutation and polymorphism spectrum in the glucocerebrosidase gene (GBA). Hum Mutat 29: 567-583. (Pubitemid 351614580)
3. Spearman MA, Ballon BC, Gerrard JM, Greenberg AH, Wright JA (1991) The inhibition of platelet aggregation of metastatic H-ras-transformed 10T1/2 fibroblasts with castanospermine, an N-linked glycoprotein processing inhibitor. Cancer Lett 60: 185-191.
4. Zhu Z, Zheng T, Homer RJ, Kim YK, Chen NY, et al. (2004) Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science 304: 1678-1682. (Pubitemid 38765861)
5. Leeson PD, Springthorpe B (2007) The influence of drug-like concepts on decision-making in medicinal chemistry. Nat Rev Drug Discov 6: 881-890. (Pubitemid 350042396)
6. Gloster TM, Vocadlo DJ (2012) Developing inhibitors of glycan processing enzymes as tools for enabling glycobiology. Nat Chem Biol 8: 683-694.
7. Moorthy NS, Ramos MJ, Fernandes PA (2012) Studies on alpha-glucosidase inhibitors development: magic molecules for the treatment of carbohydrate mediated diseases. Mini Rev Med Chem 12: 713-720.
8. Cheng AC, Coleman RG, Smyth KT, Cao Q, Soulard P, et al. (2007) Structure-based maximal affinity model predicts small-molecule druggability. Nat Biotechnol 25: 71-75. (Pubitemid 46087905)
9. Carlson HA, Smith RD, Khazanov NA, Kirchhoff PD, Dunbar JB Jr., et al. (2008) Differences between high- and low-affinity complexes of enzymes and nonenzymes. J Med Chem 51: 6432-6441.
10. Jones S, Thornton JM (1996) Principles of protein-protein interactions. Proc Natl Acad Sci U S A 93: 13-20. (Pubitemid 26038096)
11. Transue TR, De Genst E, Ghahroudi MA, Wyns L, Muyldermans S (1998) Camel single-domain antibody inhibits enzyme by mimicking carbohydrate substrate. Proteins 32: 515-522. (Pubitemid 28380790)
12. Binz HK, Amstutz P, Pluckthun A (2005) Engineering novel binding proteins from nonimmunoglobulin domains. Nat Biotechnol 23: 1257-1268. (Pubitemid 41486853)
13. Gebauer M, Skerra A (2009) Engineered protein scaffolds as next-generation antibody therapeutics. Curr Opin Chem Biol 13: 245-255.
14. Stoop AA, Craik CS (2003) Engineering of a macromolecular scaffold to develop specific protease inhibitors. Nat Biotechnol 21: 1063-1068. (Pubitemid 37064736)
15. Desmyter A, Transue TR, Ghahroudi MA, Thi MH, Poortmans F, et al. (1996) Crystal structure of a camel single-domain VH antibody fragment in complex with lysozyme. Nat Struct Biol 3: 803-811. (Pubitemid 26303407)
16. De Genst E, Silence K, Decanniere K, Conrath K, Loris R, et al. (2006) Molecular basis for the preferential cleft recognition by dromedary heavy-chain antibodies. Proceedings of the National Academy of Sciences of the United States of America 103: 4586-4591.
17. Stanfield RL, Dooley H, Flajnik MF, Wilson IA (2004) Crystal structure of a shark single-domain antibody V region in complex with lysozyme. Science 305: 1770-1773. (Pubitemid 39249643)
18. Steemson JD, Baake M, Rakonjac J, Arcus VL, Liddament MT (2014) Tracking Molecular Recognition at the Atomic Level with a New Protein Scaffold Based on the OB-Fold. PLoS One 9: e86050.
19. Mouratou B, Schaeffer F, Guilvout I, Tello-Manigne D, Pugsley AP, et al. (2007) Remodeling a DNA-binding protein as a specific in vivo inhibitor of bacterial secretin PulD. Proc Natl Acad Sci U S A 104: 17983-17988. (Pubitemid 350210807)
20. Pecorari F, Alzari PM (2008) OB-fold used as scaffold for engineering new specific binders. Patent Publication Nos WO2008068637 (A3), EP2099817 (A2).
21. Krehenbrink M, Chami M, Guilvout I, Alzari PM, Pecorari F, et al. (2008) Artificial binding proteins (Affitins) as probes for conformational changes in secretin PulD. J Mol Biol 383: 1058-1068.
22. Buddelmeijer N, Krehenbrink M, Pecorari F, Pugsley AP (2009) Type II secretion system secretin PulD localizes in clusters in the Escherichia coli outer membrane. J Bacteriol 191: 161-168.
23. Behar G, Bellinzoni M, Maillasson M, Paillard-Laurance L, Alzari PM, et al. (2013) Tolerance of the archaeal Sac7d scaffold protein to alternative library designs: characterization of anti-immunoglobulin G Affitins. Protein Eng Des Sel 26: 267-275.
24. Miranda FF, Brient-Litzler E, Zidane N, Pecorari F, Bedouelle H (2011) Reagentless fluorescent biosensors from artificial families of antigen binding proteins. Biosens Bioelectron 26: 4184-4190.
25. Vasella A, Davies GJ, Bohm M (2002) Glycosidase mechanisms. Curr Opin Chem Biol 6: 619-629. (Pubitemid 35284193)
26. Mouratou B, Behar G, Paillard-Laurance L, Colinet S, Pecorari F (2012) Ribosome display for the selection of Sac7d scaffolds. Methods Mol Biol 805: 315-331.
27. Kabsch W (2010) Xds. Acta Crystallogr D Biol Crystallogr 66: 125-132.
28. Evans PR (2011) An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr D Biol Crystallogr 67: 282-292.
29. McCoy AJ (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr D Biol Crystallogr 63: 32-41.
30. Bricogne G BE, Brandl M., Flensburg C., Keller P., Paciorek W., Roversi P SA, Smart O.S., Vonrhein C., Womack T.O (2011) BUSTER version 2.11.1. Cambridge, United Kingdom: Global Phasing Ltd.
31. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132. (Pubitemid 41742764)
32. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255. (Pubitemid 27235885)
33. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-383.
34. DeLano WL (2002) The PyMOL Molecular Graphics System.
35. Laskowski RA, Swindells MB (2011) LigPlot+ : multiple ligand-protein interaction diagrams for drug discovery. J Chem Inf Model 51: 2778-2786.
36. Lawrence MC, Colman PM (1993) Shape complementarity at protein/protein interfaces. Journal of Molecular Biology 234: 946-950. (Pubitemid 24027225)
37. Correa AC, Ortega CO, Obal GO, Alzari PA, Vincentelli RV, et al. (2014) Generation of a vector suite for protein solubility screening. Frontiers in Microbiology 5: 1-9.
38. Peng J, Wang W, Jiang Y, Liu M, Zhang H, et al. (2011) Enhanced soluble expression of a thermostable cellulase from Clostridium thermocellum in Escherichia coli. Curr Microbiol 63: 523-530.
39. Chauvaux S, Beguin P, Aubert JP (1992) Site-directed mutagenesis of essential carboxylic residues in Clostridium thermocellum endoglucanase CelD. J Biol Chem 267: 4472-4478.
40. Juy MA, Adolfo G.; Alzari, Pedro M.; Poljak, Roberta J.; Claeyssens, Marc; Béguin, Pierre; Aubert, Jean-Paul (1992) Three-dimensional structure of a thermostable bacterial cellulase. Nature 357: 89-91.
41. Davies GJ, Gloster TM, Henrissat B (2005) Recent structural insights into the expanding world of carbohydrate-active enzymes. Curr Opin Struct Biol 15: 637-645. (Pubitemid 41668519)
42. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233-238.
43. Koide A, Wojcik J, Gilbreth RN, Hoey RJ, Koide S (2012) Teaching an old scaffold new tricks: monobodies constructed using alternative surfaces of the FN3 scaffold. J Mol Biol 415: 393-405.
44. Dimitrov DS, Marks JD (2009) Therapeutic antibodies: current state and future trends-is a paradigm change coming soon? Methods Mol Biol 525: 1-27, xiii.
45. Dimitrov DS (2012) Therapeutic proteins. Methods Mol Biol 899: 1-26.
46. Investigators O- (1999) Effects of recombinant hirudin (lepirudin) compared with heparin on death, myocardial infarction, refractory angina, and revascularisation procedures in patients with acute myocardial ischaemia without ST elevation: a randomised trial. Lancet 353: 429-438.
47. Wurch T, Pierre A, Depil S (2012) Novel protein scaffolds as emerging therapeutic proteins: from discovery to clinical proof-of-concept. Trends Biotechnol 30: 575-582.
48. Williams A, Baird LG (2003) DX-88 and HAE: a developmental perspective. Transfus Apher Sci 29: 255-258. (Pubitemid 37315589)
49. Attucci S, Gauthier A, Korkmaz B, Delepine P, Martino MF, et al. (2006) EPI-hNE4, a proteolysis-resistant inhibitor of human neutrophil elastase and potential anti-inflammatory drug for treating cystic fibrosis. J Pharmacol Exp Ther 318: 803-809. (Pubitemid 44061254)
50. Tolcher AW, Sweeney CJ, Papadopoulos K, Patnaik A, Chiorean EG, et al. (2011) Phase I and pharmacokinetic study of CT-322 (BMS-844203), a targeted Adnectin inhibitor of VEGFR-2 based on a domain of human fibronectin. Clin Cancer Res 17: 363-371.
51. Campochiaro PA, Channa R, Berger BB, Heier JS, Brown DM, et al. (2012) Treatment of Diabetic Macular Edema With a Designed Ankyrin Repeat Protein That Binds Vascular Endothelial Growth Factor: A Phase 1/2 Study. Am J Ophthalmol.
52. Wojcik J, Hantschel O, Grebien F, Kaupe I, Bennett KL, et al. (2010) A potent and highly specific FN3 monobody inhibitor of the Abl SH2 domain. Nat Struct Mol Biol 17: 519-527.
53. Gilbreth RN, Truong K, Madu I, Koide A, Wojcik JB, et al. (2011) Isoform-specific monobody inhibitors of small ubiquitin-related modifiers engineered using structure-guided library design. Proc Natl Acad Sci U S A 108: 7751-7756.