Programmable polyproteams built using twin peptide superglues

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 5, 2016, Pages 1202-1207

  Veggiani, Gianluca ^a   Nakamura, Tomohiko ^a,b   Brenner, Michael D ^a   Gayet, Raphaël V ^a,c   Yan, Jun ^d   Robinson, Carol V ^d   Howarth, Mark ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b LOC Development Department   (Japan)

^c UNIVERSITÉ DE LYON   (France)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; DEATH RECEPTOR; DEATH RECEPTOR 5; EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR RECEPTOR; MALTOSE BINDING PROTEIN; PEPTIDE; POLYPROTEIN; SPYTAG PEPTIDE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; ADHESIVE AGENT;

AMIDATION; ARTICLE; CANCER CELL; CELL CULTURE; CELL DEATH; CELL VIABILITY; COVALENT BOND; CYTOTOXICITY; ELECTROPHORESIS; ELECTROSPRAY MASS SPECTROMETRY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; STREPTOCOCCUS PNEUMONIAE; THERMOSTABILITY; CHEMISTRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; SIGNAL TRANSDUCTION;

ADHESINS, BACTERIAL; ADHESIVES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; PEPTIDES; SIGNAL TRANSDUCTION; STREPTOCOCCUS PNEUMONIAE;

EID: 84956923057     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1519214113     Document Type: Article

References (69)

1. Kiessling LL, Gestwicki JE, Strong LE (2006) Synthetic multivalent ligands as probes of signal transduction. Angew Chem Int Ed Engl 45(15):2348-2368.
2. Bachmann MF, Jennings GT (2010) Vaccine delivery: A matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol 10(11):787-796.
3. Gradišar H, et al. (2013) Design of a single-chain polypeptide tetrahedron assembled from coiled-coil segments. Nat Chem Biol 9(6):362-366.
4. Fletcher JM, et al. (2013) Self-Assembling cages from coiled-coil peptide modules. Science 340(6132):595-599.
5. Zaher HS, Green R (2009) Fidelity at the molecular level: Lessons from protein synthesis. Cell 136(4):746-762.
6. Baneyx F, Mujacic M (2004) Recombinant protein folding and misfolding in Escherichia coli. Nat Biotechnol 22(11):1399-1408.
7. Fairhead M, et al. (2014) SpyAvidin hubs enable precise and ultrastable orthogonal nanoassembly. J Am Chem Soc 136(35):12355-12363.
8. Pengo P, et al. (2010) Solid-phase preparation of protein complexes. J Mol Recognit 23(6):551-558.
9. Arfi Y, Shamshoum M, Rogachev I, Peleg Y, Bayer EA (2014) Integration of bacterial lytic polysaccharide monooxygenases into designer cellulosomes promotes enhanced cellulose degradation. Proc Natl Acad Sci USA 111(25):9109-9114.
10. Russell J, Colpitts T, Holets-McCormack S, Spring T, Stroupe S (2004) Defined protein conjugates as signaling agents in immunoassays. Clin Chem 50(10):1921-1929.
11. Rossi EA, Goldenberg DM, Chang CH (2012) Complex and defined biostructures with the dock-And-lock method. Trends Pharmacol Sci 33(9):474-481.
12. Patterson DM, Nazarova LA, Prescher JA (2014) Finding the right (bioorthogonal) chemistry. ACS Chem Biol 9(3):592-605.
13. Merrifield RB (1963) Solid phase peptide synthesis. 1. The synthesis of a tetrapeptide. J Am Chem Soc 85(14):2149-2154.
14. Marshall GR (2003) Solid-phase synthesis: A paradigm shift. J Pept Sci 9(9):534-544.
15. Cheloha RW, Maeda A, Dean T, Gardella TJ, Gellman SH (2014) Backbone modification of a polypeptide drug alters duration of action in vivo. Nat Biotechnol 32(7):653-655.
16. Letsinger RL, Mahadevan V (1965) Oligonucleotide synthesis on a polymer support. J Am Chem Soc 87:3526-3527.
17. Kosuri S, Church GM (2014) Large-scale de novo DNA synthesis: Technologies and applications. Nat Methods 11(5):499-507.
18. Raibaut L, et al. (2013) Highly efficient solid phase synthesis of large polypeptides by iterative ligations of bis(2-sulfanylethyl)amido (SEA) peptide segments. Chem Sci (Camb) 4(10):4061-4066.
19. Jbara M, Seenaiah M, Brik A (2014) Solid phase chemical ligation employing a rink amide linker for the synthesis of histone H2B protein. Chem Commun (Camb) 50(83):12534-12537.
20. Delebecque CJ, Lindner AB, Silver PA, Aldaye FA (2011) Organization of intracellular reactions with rationally designed RNA assemblies. Science 333(6041):470-474.
21. Chen R, et al. (2014) Biomolecular scaffolds for enhanced signaling and catalytic efficiency. Curr Opin Biotechnol 28:59-68.
22. Modica JA, Skarpathiotis S, Mrksich M (2012) Modular assembly of protein building blocks to create precisely defined megamolecules. ChemBioChem 13(16):2331-2334.
23. Huh WK, et al. (2003) Global analysis of protein localization in budding yeast. Nature 425(6959):686-691.
24. Zakeri B, Howarth M (2010) Spontaneous intermolecular amide bond formation between side chains for irreversible peptide targeting. J Am Chem Soc 132(13):4526-4527.
25. Veggiani G, Zakeri B, Howarth M (2014) Superglue from bacteria: Unbreakable bridges for protein nanotechnology. Trends Biotechnol 32(10):506-512.
26. Zakeri B, et al. (2012) Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. Proc Natl Acad Sci USA 109(12):E690-E697.
27. Bedbrook CN, et al. (2015) Genetically encoded spy peptide fusion system to detect plasma membrane-localized proteins in vivo. Chem Biol 22(8):1108-1121.
28. Izoré T, et al. (2010) Structural basis of host cell recognition by the pilus adhesin from Streptococcus pneumoniae. Structure 18(1):106-115.
29. Yancey PH (2004) Compatible and counteracting solutes: Protecting cells from the Dead Sea to the deep sea. Sci Prog 87(Pt 1):1-24.
30. Radzicka A, Wolfenden R (1996) Rates of uncatalyzed peptide bond hydrolysis in neutral solution and the transition state affinities of proteases. J Am Chem Soc 118(26):6105-6109.
31. Telmer PG, Shilton BH (2003) Insights into the conformational equilibria of maltosebinding protein by analysis of high affinity mutants. J Biol Chem 278(36):34555-34567.
32. Walker IH, Hsieh PC, Riggs PD (2010) Mutations in maltose-binding protein that alter affinity and solubility properties. Appl Microbiol Biotechnol 88(1):187-197.
33. Wikman M, et al. (2004) Selection and characterization of HER2/neu-binding affibody ligands. Protein Eng Des Sel 17(5):455-462.
34. ZhangWB, Sun F, Tirrell DA, Arnold FH (2013) Controlling macromolecular topology with genetically encoded SpyTag-SpyCatcher chemistry. J Am Chem Soc 135(37):13988-13997.
35. Holland PM (2014) Death receptor agonist therapies for cancer, which is the right TRAIL? Cytokine Growth Factor Rev 25(2):185-193.
36. Huet HA, et al. (2014) Multivalent nanobodies targeting death receptor 5 elicit superior tumor cell killing through efficient caspase induction. MAbs 6(6):1560-1570.
37. Kang HJ, Baker EN (2011) Intramolecular isopeptide bonds: Protein crosslinks built for stress? Trends Biochem Sci 36(4):229-237.
38. Shi X, et al. (2012) Quantitative fluorescence labeling of aldehyde-Tagged proteins for single-molecule imaging. Nat Methods 9(5):499-503.
39. Shah NH, Muir TW (2014) Inteins: Nature's gift to protein chemists. Chem Sci (Camb) 5(1):446-461.
40. Rashidian M, Dozier JK, Distefano MD (2013) Enzymatic labeling of proteins: Techniques and approaches. Bioconjug Chem 24(8):1277-1294.
41. Popp MWL, Ploegh HL (2011) Making and breaking peptide bonds: Protein engineering using sortase. Angew Chem Int Ed Engl 50(22):5024-5032.
42. Carvajal-Vallejos P, Pallissé R, Mootz HD, Schmidt SR (2012) Unprecedented rates and efficiencies revealed for new natural split inteins from metagenomic sources. J Biol Chem 287(34):28686-28696.
43. Chang TK, Jackson DY, Burnier JP, Wells JA (1994) Subtiligase: A tool for semisynthesis of proteins. Proc Natl Acad Sci USA 91(26):12544-12548.
44. Sasmal PK, et al. (2012) Catalytic azide reduction in biological environments. ChemBioChem 13(8):1116-1120.
45. van den Bosch SM, et al. (2013) Evaluation of strained alkynes for Cu-free click reaction in live mice. Nucl Med Biol 40(3):415-423.
46. Versteegen RM, Rossin R, ten Hoeve W, Janssen HM, Robillard MS (2013) Click to release: Instantaneous doxorubicin elimination upon tetrazine ligation. Angew Chem Int Ed Engl 52(52):14112-14116.
47. Aerni HR, ShifmanMA, Rogulina S, O'Donoghue P, Rinehart J (2015) Revealing the amino acid composition of proteins within an expanded genetic code. Nucleic Acids Res 43(2):e8.
48. Schneider T, et al. (2014) Dissecting ubiquitin signaling with linkage-defined and protease resistant ubiquitin chains. Angew Chem Int Ed Engl 53(47):12925-12929.
49. Trang VH, et al. (2012) Nonenzymatic polymerization of ubiquitin: Single-step synthesis and isolation of discrete ubiquitin oligomers. Angew Chem Int Ed Engl 51(52):13085-13088.
50. Moyal T, Bavikar SN, Karthikeyan SV, Hemantha HP, Brik A (2012) Polymerization behavior of a bifunctional ubiquitin monomer as a function of the nucleophile site and folding conditions. J Am Chem Soc 134(38):16085-16092.
51. Krueger AT, Kroll C, Sanchez E, Griffith LG, Imperiali B (2014) Tailoring chimeric ligands for studying and biasing ErbB receptor family interactions. Angew Chem Int Ed Engl 53(10):2662-2666.
52. Dushek O, Goyette J, van der Merwe PA (2012) Non-catalytic tyrosine-phosphorylated receptors. Immunol Rev 250(1):258-276.
53. Shaw A, et al. (2014) Spatial control of membrane receptor function using ligand nanocalipers. Nat Methods 11(8):841-846.
54. Chen AY, et al. (2014) Synthesis and patterning of tunable multiscale materials with engineered cells. Nat Mater 13(5):515-523.
55. Sun F, Zhang WB, Mahdavi A, Arnold FH, Tirrell DA (2014) Synthesis of bioactive protein hydrogels by genetically encoded SpyTag-SpyCatcher chemistry. Proc Natl Acad Sci USA 111(31):11269-11274.
56. Botyanszki Z, Tay PK, Nguyen PQ, Nussbaumer MG, Joshi NS (2015) Engineered catalytic biofilms: Site-specific enzyme immobilization onto E. coli curli nanofibers. Biotechnol Bioeng 112(10):2016-2024.
57. Fierer JO, Veggiani G, Howarth M (2014) SpyLigase peptide-peptide ligation polymerizes affibodies to enhance magnetic cancer cell capture. Proc Natl Acad Sci USA 111(13):E1176-E1181.
58. Kuhlman B, Yang HY, Boice JA, Fairman R, Raleigh DP (1997) An exceptionally stable helix from the ribosomal protein L9: Implications for protein folding and stability. J Mol Biol 270(5):640-647.
59. Li L, Fierer JO, Rapoport TA, HowarthM(2014) Structural analysis and optimization of the covalent association between SpyCatcher and a peptide Tag. J Mol Biol 426(2):309-317.
60. Eigenbrot C, Ultsch M, Dubnovitsky A, Abrahmsén L, Härd T (2010) Structural basis for high-Affinity HER2 receptor binding by an engineered protein. Proc Natl Acad Sci USA 107(34):15039-15044.
61. Friedman M, et al. (2007) Phage display selection of Affibody molecules with specific binding to the extracellular domain of the epidermal growth factor receptor. Protein Eng Des Sel 20(4):189-199.
62. Li J, et al. (2010) Selection of affibody molecules to the ligand-binding site of the insulin-like growth factor-1 receptor. Biotechnol Appl Biochem 55(2):99-109.
63. Lendel C, Dogan J, Härd T (2006) Structural basis for molecular recognition in an affibody:affibody complex. J Mol Biol 359(5):1293-1304.
64. Veggiani G, de Marco A (2011) Improved quantitative and qualitative production of single-domain intrabodies mediated by the co-expression of Erv1p sulfhydryl oxidase. Protein Expr Purif 79(1):111-114.
65. Fairhead M, Howarth M (2015) Site-specific biotinylation of purified proteins using BirA. Methods Mol Biol 1266:171-184.
66. Castaño-Cerezo S, Bernal V, Röhrig T, Termeer S, Cánovas M (2015) Regulation of acetate metabolism in Escherichia coli BL21 by protein N(e)-lysine acetylation. Appl Microbiol Biotechnol 99(8):3533-3545.
67. Geoghegan KF, et al. (1999) Spontaneous alpha-N-6-phosphogluconoylation of a "His tag" in Escherichia coli: The cause of extra mass of 258 or 178 Da in fusion proteins. Anal Biochem 267(1):169-184.
68. Pringle SD, et al. (2007) An investigation of the mobility separation of some peptide and protein ions using a new hybrid quadrupole/travelling wave IMS/oa-ToF instrument. Int J Mass Spectrom 261(1):1-12.
69. Hernández H, Robinson CV (2007) Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry. Nat Protoc 2(3):715-726.