Consensus design of a NOD receptor leucine rich repeat domain with binding affinity for a muramyl dipeptide, a bacterial cell wall fragment

Protein Science

Volumn 23, Issue 6, 2014, Pages 790-800

  Parker, Rachael ^a   Mercedes Camacho, Ana ^a   Grove, Tijana Z ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Binding scaffold; Consensus design; Leucine rich repeat; MDP; NOD; Repeat protein

Indexed keywords

BINDING PROTEIN; CLRR2 PROTEIN; MURAMYL DIPEPTIDE; NOD PROTEIN; PROTEIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; LEUCINE; N ACETYLMURAMYLALANYL DEXTRO ISOGLUTAMINE; PEPTIDOGLYCAN; PROTEIN BINDING;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL CELL WALL; BINDING AFFINITY; CAPPING PHENOMENON; CIRCULAR DICHROISM; COMPLEMENTARITY DETERMINING REGION; CONSENSUS SEQUENCE; CONTROLLED STUDY; FLUORESCENCE SPECTROSCOPY; HUGO GENE NOMENCLATURE; HUMAN; INNATE IMMUNITY; LEUCINE RICH REPEAT; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT; TANDEM REPEAT; CELL WALL; CHEMISTRY; METABOLISM;

ACETYLMURAMYL-ALANYL-ISOGLUTAMINE; CARRIER PROTEINS; CELL WALL; LEUCINE; PEPTIDOGLYCAN; PROTEIN BINDING; PROTEINS;

EID: 84904169024     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2461     Document Type: Article

References (57)

1. Boersma YL, Pluckthun A (2011) DARPins and other repeat protein scaffolds: Advances in engineering and applications. Curr Opin Biotechnol 22:849-857
2. Lofblom J, Frejd FY, Stahl S (2011) Non-immunoglobulin based protein scaffolds. Curr Opin Biotechnol 22: 843-848
3. Yoshimura H, Inaguma A, Yamada T, Ozawa T (2012) Fluorescent probes for imaging endogenous beta-actin mRNA in living cells using fluorescent protein-tagged pumilio. ACS Chem Biol 7:999-1005
4. Filipovska A, Razif MF, Nygard KK, Rackham O (2011) A universal code for RNA recognition by PUF proteins. Nat Chem Biol 7:425-427
5. Hong X, Ma MZ, Gildersleeve JC, Chowdhury S, Barchi JJ, Jr, Mariuzza RA, Murphy MB, Mao L, Pancer Z (2013) Sugar-binding proteins from fish: Selection of high affinity "lambodies" that recognize biomedically relevant glycans. ACS Chem Biol 8:152-160
6. Garg A, Lohmueller JJ, Silver PA, Armel TZ (2012) Engineering synthetic TAL effectors with orthogonal target sites. Nucleic Acids Res 40:7584-7595
7. Fujimoto YK, Green DF (2012) Carbohydrate recognition by the antiviral lectin cyanovirin-N. J Am Chem Soc 134:19639-19651
8. Woodrum BW, Maxwell JD, Bolia A, Ozkan SB, Ghirlanda G (2013) The antiviral lectin cyanovirin-N: probing multivalency and glycan recognition through experimental and computational approaches. Biochem Soc Trans 41:1170-1176
9. Zheng H, Wang F, Wang Q, Gao JM (2011) Cofactorfree detection of phosphatidylserine with cyclic peptides mimicking lactadherin. J Am Chem Soc 133: 15280-15283
10. Mak ANS, Bradley P, Cernadas RA, Bogdanove AJ, Stoddard BL (2012) The crystal structure of TAL effector PthXo1 bound to its DNA target. Science 335:716-719
11. Mak AN-S, Bradley P, Bogdanove AJ, Stoddard BL (2013) TAL effectors: function, structure, engineering and applications. Curr Opin Struct Biol 23:93-99
12. Gebauer M, Skerra A (2009) Engineered protein scaffolds as next-generation antibody therapeutics. Curr Opin Chem Biol 13:245-255
13. Cummings RD (2009) The repertoire of glycan determinants in the human glycome. Mol Biosyst 5:1087-1104
14. Binz HK, Amstutz P, Kohl A, Stumpp MT, Briand C, Forrer P, Grutter MG, Pluckthun A (2004) High-affinity binders selected from designed ankyrin repeat protein libraries. Nat Biotechnol 22:575-582
15. Cortajarena AL, Kajander T, Pan W, Cocco MJ, Regan L (2004) Protein design to understand peptide ligand recognition by tetratricopeptide repeat proteins. Protein Eng Des Sel 17:399-409
16. Varadamsetty G, Tremmel D, Hansen S, Parmeggiani F, Pluckthun A (2012) Designed Armadillo repeat proteins: library generation, characterization and selection of peptide binders with high specificity. J Mol Biol 424: 68-87
17. Seeger MA, Zbinden R, Flutsch A, Gutte PGM, Engeler S, Roschitzki-Voser H, Grutter MG (2013) Design, construction, and characterization of a second-generation DARPin library with reduced hydrophobicity. Protein Sci 22:1239-1257
18. Luo M, Velikovsky CA, Yang X, Siddiqui MA, Hong X, Barchi JJ, Jr., Gildersleeve JC, Pancer Z, Mariuzza RA (2013) Recognition of the Thomsen-Friedenreich pancarcinoma carbohydrate antigen by a lamprey variable lymphocyte receptor. J Biol Chem 288:23597-23606
19. Wezner-Ptasinska M, Krowarsch D, Otlewski J (2011) Design and characteristics of a stable protein scaffold for specific binding based on variable lymphocyte receptor sequences. Biochim Biophys Acta 1814:1140-1145
20. Lee SC, Park K, Han J, Lee JJ, Kim HJ, Hong S, Heu W, Kim YJ, Ha JS, Lee SG, Cheong HK, Jeon YH, Kim D, Kim HS (2012) Design of a binding scaffold based on variable lymphocyte receptors of jawless vertebrates by module engineering. Proc Natl Acad Sci U S A 109: 3299-3304
21. Cortajarena AL, Liu TY, Hochstrasser M, Regan L (2010) Designed proteins to modulate cellular networks. ACS Chem Biol 5:545-552
22. Grove TZ, Cortajarena AL, Regan L (2008) Ligand binding by repeat proteins: natural and designed. Curr Opin Struct Biol 18:507-515
23. Grove TZ, Forster J, Pimienta G, Dufresne E, Regan L (2012) A modular approach to the design of proteinbased smart gels. Biopolymers 97:508-517
24. Grove TZ, Hands M, Regan L (2010) Creating novel proteins by combining design and selection. Protein Eng Des Sel 23:449-455
25. Grove TZ, Osuji CO, Forster JD, Dufresne ER, Regan L (2010) Stimuli-responsive smart gels realized via modular protein design. J Am Chem Soc 132:14024-14026
26. Jackrel ME, Valverde R, Regan L (2009) Redesign of a protein-peptide interaction: Characterization and applications. Protein Sci 18:762-774
27. Mosavi LK, Cammett TJ, Desrosiers DC, Peng ZY (2004) The ankyrin repeat as molecular architecture for protein recognition. Protein Sci 13:1435-1448
28. Stumpp MT, Forrer P, Binz HK, Pluckthun A (2003) Designing repeat proteins: modular leucine-rich repeat protein libraries based on the mammalian ribonuclease inhibitor family. J Mol Biol 332:471-487
29. Kumar H, Kawai T, Akira S (2009) Pathogen recognition in the innate immune response. Biochem J 420: 1-16
30. Istomin AY, Godzik A (2009) Understanding diversity of human innate immunity receptors: Analysis of surface features of leucine-rich repeat domains in NLRs and TLRs. BMC Immunol 10:48
31. Wang Y, Liu L, Davies DR, Segal DM (2010) Dimerization of Toll-like receptor 3 (TLR3) is required for ligand binding. J Biol Chem 285:36836-36841
32. Mariathasan S, Monack DM (2007) Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat Rev Immunol 7:31-40
33. Kobe B, Deisenhofer J (1994) The leucine-rich repeat: A versatile binding motif. Trends Biochem Sci 19:415-421
34. Kajander T, Cortajarena AL, Regan L (2006) Consensus design as a tool for engineering repeat proteins. Methods Mol Biol 340:151-170
35. Magliery TJ, Regan L (2005) Sequence variation in ligand binding sites in proteins. BMC Bioinform 6:240
36. Magliery TJ, Regan L (2004) Beyond consensus: Statistical free energies reveal hidden interactions in the design of a TPR motif. J Mol Biol 343:731-745
37. Johnson G, Wu TT (2001) Kabat Database and its applications: future directions. Nucleic Acids Res 29: 205-206
38. Forrer P, Binz HK, Stumpp MT, Pluckthun A (2004) Consensus design of repeat proteins. Chembiochem 5: 183-189
39. Magliery TJ, Lavinder JJ, Sullivan BJ (2011) Protein stability by number: high-throughput and statistical approaches to one of protein science's most difficult problems. Curr Opin Chem Biol 15:443-451
40. Sullivan BJ, Durani V, Magliery TJ (2011) Triosephosphate isomerase by consensus design: dramatic differences in physical properties and activity of related variants. J Mol Biol 413:195-208
41. Jackrei ME, Valverde R, Regan L (2009) Redesign of a protein-peptide interaction: Characterization and applications. Protein Sci 18:762-774
42. Kajander T, Cortajarena AL, Regan L (2006) Consensus design as a tool for engineering repeat proteins. Methods Mol Biol 340:151-170
43. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: A sequence logo generator. Genome Res 14: 1188-1190
44. Kloss E, Courtemanche N, Barrick D (2008) Repeatprotein folding: new insights into origins of cooperativity, stability, and topology. Arch Biochem Biophys 469: 83-99
45. Pancer Z, Amemiya CT, Ehrhardt GR, Ceitlin J, Gartland GL, Cooper MD (2004) Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430:174-180
46. Wingfield PT, Palmer I, Liang S-M (2001) Folding and Purification of Insoluble (Inclusion Body) Proteins from Escherichia coli. Current Protocols in Protein Science. Coligan JE, Dunn BM, Ploegh HL, Speicher DW, Wingfield PT, Eds. John Wiley & Sons, Inc., New York, pp 6.5.1-6.5.27
47. Sreerama N, Venyaminov SY, Woody RW (1999) Estimation of the number of alpha-helical and beta-strand segments in proteins using circular dichroism spectroscopy. Protein Sci 8:370-380
48. Sreerama N, Woody RW (2004) Computation and analysis of protein circular dichroism spectra. Methods Enzymol 383:318-351
49. Kobe B, Kajava AV (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11:725-732
50. Wu S, Zhang Y (2008) MUSTER: Improving protein sequence profile-profile alignments by using multiple sources of structure information. Proteins 72:547-556
51. Hong M, Yoon SI, Wilson IA (2012) Structure and functional characterization of the RNA-binding element of the NLRX1 innate immune modulator. Immunity 36: 337-347
52. Courtemanche N, Barrick D (2008) Folding thermodynamics and kinetics of the leucine-rich repeat domain of the virulence factor Internalin B. Protein Sci 17:43-53
53. Kloss E, Barrick D (2008) Thermodynamics, kinetics, and salt dependence of folding of YopM, a large leucine-rich repeat protein. J Mol Biol 383:1195-1209
54. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124:783-801
55. Grimes CL, Ariyananda Lde Z, Melnyk JE, O'Shea EK (2012) The innate immune protein Nod2 binds directly to MDP, a bacterial cell wall fragment. J Am Chem Soc 134:13535-13537
56. Inohara N, Ogura Y, Fontalba A, Gutierrez O, Pons F, Crespo J, Fukase K, Inamura S, Kusumoto S, Hashimoto M, Foster SJ, Moran AP, Fernandez-Luna JL, Nunez G (2003) Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J Biol Chem 278:5509-5512
57. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. (2005) The proteomics protocols handbook. Totowa, NJ: Humana Press.