Expressed protein ligation: A resourceful tool to study protein structure and function

Cellular and Molecular Life Sciences

Volumn 66, Issue 24, 2009, Pages 3909-3922

  Berrade, Luis ^a   Camarero, Julio A ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Chemical ligation; Circular polypeptides; Intein; Isotopic labeling; Post translational modifications; Protein thioesters; Protein splicing

Indexed keywords

AMINO ACID; CYSTEINE; HYDROLASE; ISOTOPE; METHIONINE; METHIONYL AMINOPEPTIDASE;

AMINO TERMINAL SEQUENCE; BIOPHYSICAL EQUIPMENT; CARBOXY TERMINAL SEQUENCE; CHEMICAL ANALYSIS; CHEMICAL COMPOSITION; CLINICAL ASSESSMENT TOOL; CYCLIZATION; EXPRESSED PROTEIN LIGATION; GLYCOSYLATION; HUMAN; NUCLEAR MAGNETIC RESONANCE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN IMMOBILIZATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEIN STRUCTURE, FUNCTION AND VARIABILITY; PROTEIN SYNTHESIS; REVIEW; SPECTROSCOPY; TECHNOLOGY; TRANSESTERIFICATION;

MODELS, CHEMICAL; MOLECULAR STRUCTURE; PEPTIDES; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEINS;

EID: 70849134554     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-009-0122-3     Document Type: Review

References (126)

1. CP Hackenberger D Schwarzer 2008 Chemoselective ligation and modification strategies for peptides and proteins Angew Chem Int Ed Engl 47 10030 10074 1:CAS:528:DC%2BD1MXislSitA%3D%3D 19072788
2. Camarero JA (2006) New developments for the site-specific attachment of proteins to surfaces. Biophys Rev Lett 1:1-28
3. PE Dawson TW Muir I Clark-Lewis SBH Kent 1994 Synthesis of proteins by native chemical ligation Science 266 776 779 1:CAS:528:DyaK2MXitVGgtrw%3D 7973629
4. JP Tam YA Lu CF Liu J Shao 1995 Peptide synthesis using unprotected peptides through orthogonal coupling methods Proc Natl Acad Sci USA 92 12485 12489 1:CAS:528:DyaK28Xhtl2rsQ%3D%3D 8618926
5. Wieland T, Bokelmann E, Bauer L, Lang HU, Lau H (1953) Polypeptide synthesis. VIII. Formation of sulfur containing peptides by intramolecular migration of aminoacyl groups. Liebigs Ann Chem 583:129-149
6. Wieland T (1988) Sulfur in biomimetic peptide synthesis. In: Kleinkauf Jaeniche VD (eds) The roots of modern biochemistry. Walter de Gruyter, Berlin, pp 213-221
7. SB Kent 2009 Total chemical synthesis of proteins Chem Soc Rev 38 338 351 1:CAS:528:DC%2BD1MXksVSntL8%3D 19169452
8. DA Erlanson M Chytil GL Verdine 1996 The leucine zipper domain controls the orientation of AP-1 in the NFAT•AP-1•DNA complex Chem Biol 3 981 991 1:CAS:528:DyaK2sXmslKrtA%3D%3D 9000009
9. TW Muir D Sondhi PA Cole 1998 Expressed protein ligation: a general method for protein engineering Proc Natl Acad Sci USA 95 6705 6710 1:CAS:528:DyaK1cXjslyntLg%3D 9618476
10. TC Evans J Benner M-Q Xu 1999 The in Vitro ligation of bacterially expressed proteins using an intein from Metanobacterium thermoautotrophicum J Biol Chem 274 3923 3926 1:CAS:528:DyaK1MXhslahtLw%3D 9933578
11. RR Flavell TW Muir 2009 Expressed protein ligation (EPL) in the study of signal transduction, ion conduction, and chromatin biology Acc Chem Res 42 107 116 1:CAS:528:DC%2BD1cXht1Ohs7nM 18939858
12. JP Pellois TW Muir 2006 Semisynthetic proteins in mechanistic studies: using chemistry to go where nature can't Curr Opin Chem Biol 10 487 491 1:CAS:528:DC%2BD28Xps1Olurs%3D 16935551
13. V Muralidharan TW Muir 2006 Protein ligation: an enabling technology for the biophysical analysis of proteins Nat Methods 3 429 438 1:CAS:528: DC%2BD28XkvVWksrw%3D 16721376
14. S Tsukiji T Nagamune 2009 Sortase-mediated ligation: a gift from Gram-positive bacteria to protein engineering Chembiochem 10 787 798 1:CAS:528:DC%2BD1MXktVajt7o%3D 19199328
15. L Saleh FB Perler 2006 Protein splicing in cis and in trans Chem Rec 6 183 193 1:CAS:528:DC%2BD28XptlymsLs%3D 16900466
16. TC Evans Jr MQ Xu 1999 Intein-mediated protein ligation: harnessing nature's escape artists Biopolymers 51 333 342 1:CAS:528:DC%2BD3cXhsVOisrg%3D 10685044
17. Camarero JA, Muir TW (1999) Native chemical ligation of polypeptides. Curr Protoc Protein Sci 15:18.4.1-18.4.21
18. PE Dawson SB Kent 2000 Synthesis of native proteins by chemical ligation Annu Rev Biochem 69 923 960 1:CAS:528:DC%2BD3cXnt1ajurc%3D 10966479
19. TW Muir 2003 Semisynthesis of proteins by expressed protein ligation Annu Rev Biochem 72 249 289 1:CAS:528:DC%2BD3sXntFSgtLs%3D 12626339
20. TM Hackeng JH Griffin PE Dawson 1999 Protein synthesis by native chemical ligation: expanded scope by using straightforward methodology Proc Natl Acad Sci USA 96 10068 10073 1:CAS:528:DyaK1MXlvFegsLw%3D 10468563
21. H Hojo S Aimoto 1991 Polypeptide Synthesis Using the S-Alkyl Thioester of a Partially Protected Peptide Segment. Synthesis of the DNA-Binding Domain of c-Myb Protein (142-193)-NH2 Bull Chem Soc Jpn 64 111 117 1:CAS:528: DyaK3MXhvVKjt7c%3D
22. JA Camarero GJ Cotton A Adeva TW Muir 1998 Chemical ligation of unprotected peptides directly form a solid support J Pept Res 51 303 316 1:CAS:528:DyaK1cXitFaiu7o%3D 9560006
23. JA Camarero A Adeva TW Muir 2000 3-Thiopropionic acid as a highly versatile multidetachable thioester resin linker Int J Pept Res Ther 7 17 21 1:CAS:528:DC%2BD3cXhtFertLc%3D
24. M Huse MN Holford J Kuriyan TW Muir 2000 Semisynthesis of hyperphosphorylated type I TGF beta receptor: addressing the mechanism of kinase activation J Am Chem Soc 122 8337 8338 1:CAS:528:DC%2BD3cXlslWksrY%3D
25. aThioesters: application to the total chemical synthesis of a glycoprotein by native chemical ligation. J Am Chem Soc 121:11684-11689
26. Tolbert TJ, Wong C-H (2000) Intein-mediated synthesis of proteins containing carbohydrates and other molecular probes. J Am Chem Soc 122:5421-5428
27. Miller JS, Dudkin VY, Lyon GJ, Muir TW, Danishefsky SJ (2003) Toward fully synthetic N-linked glycoproteins. Angew Chem Int Ed 42:431-434
28. JA Camarero AR Mitchell 2005 Synthesis of proteins by native chemical ligation using Fmoc-based chemistry Protein Pept Lett 12 723 728 1:CAS:528:DC%2BD2MXhtFOrt7nN 16305540
29. Ingenito R, Bianchi E, Fattori D, Pessi A (1999) Solid phase synthesis of peptide C-terminal thioesters by Fmoc/t-Bu chemistry Source. J Am Chem Soc 121:11369-11374
30. JA Camarero BJ Hackel JJ de Yoreo AR Mitchell 2004 Fmoc-based synthesis of peptide alpha-thioesters using an aryl hydrazine support J Org Chem 69 4145 4151 1:CAS:528:DC%2BD2cXktValsr0%3D 15176841
31. JB Blanco-Canosa PE Dawson 2008 An efficient Fmoc-SPPS approach for the generation of thioester peptide precursors for use in native chemical ligation Angew Chem Int Ed Engl 47 6851 6855 1:CAS:528:DC%2BD1cXhtV2iurjK 18651678
32. T Kawakami S Aimoto 2009 Peptide ligation via the in situ transformation of an amide into a thioester at a cysteine residue Adv Exp Med Biol 611 117 118 19400119
33. Gesquièe J-C, Diesis E, Tartar A (1990) Conversion of N-terminal cysteine to thiazolidine carboxylic acid during hydrogen fluoride deparotection of peptides containing N-bom protected histidine. J Chem Soc Chem Commun 20:1402-1403
34. BL Pentelute ZP Gates JL Dashnau JM Vanderkooi SB Kent 2008 Mirror image forms of snow flea antifreeze protein prepared by total chemical synthesis have identical antifreeze activities J Am Chem Soc 130 9702 9707 1:CAS:528: DC%2BD1cXotFyitb4%3D 18598026
35. K Severinov TW Muir 1998 Expressed protein ligation, a novel method for studying protein-protein interactions in transcription J Biol Chem 273 16205 16209 1:CAS:528:DyaK1cXkt1Gju7o%3D 9632677
36. TC Evans J Benner M-Q Xu 1998 Semisynthesis of cytotoxic proteins using a modified protein splicing element Protein Sci 7 2256 2264 1:CAS:528: DyaK1cXnt1GrsLg%3D 9827992
37. M-Q Xu FB Perler 1996 The mechanism of protein splicing and its modulation by mutation EMBO J 15 5146 5153 1:CAS:528:DyaK28XmsVeitbk%3D 8895558
38. S Chong FB Mersha DG Comb ME Scott D Landry LM Vence FB Perler J Benner RB Kucera CA Hirvonen JJ Pelletier H Paulus MQ Xu 1997 Single-column purification of free recombinant proteins using a self-cleavable affinity tag derived from a protein splicing element Gene 192 271 281 1:CAS:528: DyaK2sXjsVers7k%3D 9224900
39. S Chong GE Montello A Zhang EJ Cantor W Liao M-Q Xu J Benner 1998 Utilizing the C-terminal cleavage activity of a protein splicing element to purify recombinant proteins in a single chromatographic step Nucleic Acid Res 26 5109 5115 1:CAS:528:DyaK1cXnvF2jtbc%3D 9801307
40. FI Valiyaveetil R MacKinnon TW Muir 2002 Semisynthesis and folding of the potassium channel KcsA J Am Chem Soc 124 9113 9120 1:CAS:528: DC%2BD38XltFCqurY%3D 12149015
41. JA Camarero A Shektman E Campbell M Chlenov TM Gruber DA Bryant SA Darst D Cowburn TW Muir 2002 Autoregulation of a bacterial sigma factor explored using segmental isotopic labeling and NMR Proc Natl Acad Sci USA 99 8536 8541 1:CAS:528:DC%2BD38XltF2hsro%3D 12084914
42. PH Hirel MJ Schmitter P Dessen G Fayat S Blanquet 1989 Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the side-chain length of the penultimate amino acid Proc Natl Acad Sci USA 86 8247 8251 1:CAS:528:DyaK3cXktFyh 2682640
43. MA Dwyer W Lu JJ Dwyer AA Kossiakoff 2000 Biosynthetic phage display: a novel protein engineering tool combining chemical and genetic diversity Chem Biol 7 263 274 1:CAS:528:DC%2BD3cXisFynur8%3D 10780926
44. Iwai H, Pluckthun A (1999) Circular b-lactamase: stability enhancement by cyclizing the backbone. FEBS Lett 459:166-172
45. JA Camarero D Fushman D Cowburn TW Muir 2001 Peptide chemical ligation inside living cells: in vivo generation of a circular protein domain Bioorg Med Chem 9 2479 2484 1:CAS:528:DC%2BD3MXmslaru78%3D 11553489
46. Cotton GJ, Ayers B, Xu R, Muir TW (1999) Insertion of a synthetic peptide into a recombinant protein framework; a protein biosensor. J Am Chem Soc 121:1100-1101
47. TJ Tolbert C-H Wong 2002 New methods for proteomic research: preparation of proteins with N-terminal cysteines for labeling and conjugation Angew Chem Int Ed Engl 41 2171 2174 1:CAS:528:DC%2BD38XltVWgtbg%3D 19746634
48. D Liu R Xu K Dutta D Cowburn 2008 N-terminal cysteinyl proteins can be prepared using thrombin cleavage FEBS Lett 582 1163 1167 1:CAS:528: DC%2BD1cXjs1Kht7w%3D 18331839
49. PS Hauser RO Ryan 2007 Expressed protein ligation using an N-terminal cysteine containing fragment generated in vivo from a pelB fusion protein Protein Expr Purif 54 227 233 1:CAS:528:DC%2BD2sXlvVOqsL4%3D 17493830
50. RE Dalbey MO Lively S Bron JM van Dijl 1997 The chemistry and enzymology of the type I signal peptidases Protein Sci 6 1129 1138 1:CAS:528: DyaK2sXktVylsbY%3D 9194173
51. M Paetzel RE Dalbey NC Strynadka 2002 Crystal structure of a bacterial signal peptidase apoenzyme: implications for signal peptide binding and the Ser-Lys dyad mechanism J Biol Chem 277 9512 9519 1:CAS:528:DC%2BD38Xitl2ktL4%3D 11741964
52. Southworth MW, Amaya K, Evans TC, Xu MQ, Perler FB (1999) Purification of proteins fused to either the amino or carboxy terminus of the Mycobacterium xenopi gyrase A intein. Biotechniques 27:110-114, 116, 118-120
53. S Mathys TC Evans IC Chute H Wu S Chong J Benner XQ Liu MQ Xu 1999 Characterization of a self-splicing mini-intein and its conversion into autocatalytic N- and C-terminal cleavage elements: facile production of protein building blocks for protein ligation Gene 231 1 13 1:CAS:528:DyaK1MXjsFCrurY%3D 10231563
54. A Watzke M Gutierrez-Rodriguez M Kohn R Wacker H Schroeder R Breinbauer J Kuhlmann K Alexandrov CM Niemeyer RS Goody H Waldmann 2006 A generic building block for C- and N-terminal protein-labeling and protein-immobilization Bioorg Med Chem 14 6288 6306 1:CAS:528:DC%2BD28XosVOhs7k%3D 16725326
55. A Watzke M Kohn M Gutierrez-Rodriguez R Wacker H Schroder R Breinbauer J Kuhlmann K Alexandrov CM Niemeyer RS Goody H Waldmann 2006 Site-selective protein immobilization by staudinger ligation Angew Chem Int Ed Engl 45 1408 1412 1:CAS:528:DC%2BD28XitF2qt7Y%3D 16440394
56. PC Lin SH Ueng MC Tseng JL Ko KT Huang SC Yu AK Adak YJ Chen CC Lin 2006 Site-specific protein modification through Cu(I)-catalyzed 1, 2, 3-triazole formation and its implementation in protein microarray fabrication Angew Chem Int Ed Engl 45 4286 4290 1:CAS:528:DC%2BD28XmsFWqt7w%3D 16739151
57. J Kalia RT Raines 2006 Reactivity of intein thioesters: appending a functional group to a protein Chembiochem 7 1375 1383 1:CAS:528: DC%2BD28Xpslajsr4%3D 16897799
58. JA Camarero Y Kwon MA Coleman 2004 Chemoselective attachment of biologically active proteins to surfaces by expressed protein ligation and its application for "protein chip" fabrication J Am Chem Soc 126 14730 14731 1:CAS:528:DC%2BD2cXovVKgtr0%3D 15535692
59. A Girish H Sun DS Yeo GY Chen TK Chua SQ Yao 2005 Site-specific immobilization of proteins in a microarray using intein-mediated protein splicing Bioorg Med Chem Lett 15 2447 2451 1:CAS:528:DC%2BD2MXjslyrtLo%3D 15863295
60. Camarero JA, Muir TW (1999) Biosynthesis of a head-to-tail cyclized protein with improved biological activity. J Am Chem Soc 121:5597-5598
61. RH Kimura AT Tran JA Camarero 2006 Biosynthesis of the cyclotide Kalata B1 by using protein splicing Angew Chem Int Ed Engl 45 973 976 1:CAS:528:DC%2BD28XhsFKmsbY%3D 16381044
62. JA Camarero RH Kimura YH Woo A Shekhtman J Cantor 2007 Biosynthesis of a fully functional cyclotide inside living bacterial cells Chembiochem 8 1363 1366 1:CAS:528:DC%2BD2sXps1alt7k%3D 17590879
63. FI Valiyaveetil M Leonetti TW Muir R Mackinnon 2006 Ion selectivity in a semisynthetic K+ channel locked in the conductive conformation Science 314 1004 1007 1:CAS:528:DC%2BD28XhtFyqtLjL 17095703
64. KA Scheibner Z Zhang PA Cole 2003 Merging fluorescence resonance energy transfer and expressed protein ligation to analyze protein-protein interactions Anal Biochem 317 226 232 1:CAS:528:DC%2BD3sXjvFWnur0%3D 12758261
65. V Muralidharan J Cho M Trester-Zedlitz L Kowalik BT Chait DP Raleigh TW Muir 2004 Domain-specific incorporation of noninvasive optical probes into recombinant proteins J Am Chem Soc 126 14004 14012 1:CAS:528: DC%2BD2cXot1Kqtbo%3D 15506763
66. Romanelli A, Shekhtman A, Cowburn D, Muir TW (2004) Semisynthesis of a segmental isotopically labeled protein splicing precursor: NMR evidence for an unusual peptide bond at the N-extein-intein junction. Proc Natl Acad Sci USA 101:6397-6402
67. LL Anderson GR Marshall E Crocker SO Smith TJ Baranski 2005 Motion of carboxyl terminus of Galpha is restricted upon G protein activation A solution NMR study using semisynthetic Galpha subunits. J Biol Chem 280 31019 31026 1:CAS:528:DC%2BD2MXpsVCmtLs%3D
68. F Vitali A Henning FC Oberstrass Y Hargous SD Auweter M Erat FH Allain 2006 Structure of the two most C-terminal RNA recognition motifs of PTB using segmental isotope labeling EMBO J 25 150 162 1:CAS:528:DC%2BD28Xis1Khsw%3D%3D 16362043
69. L Skrisovska FH Allain 2008 Improved segmental isotope labeling methods for the NMR study of multidomain or large proteins: application to the RRMs of Npl3p and hnRNP L J Mol Biol 375 151 164 1:CAS:528:DC%2BD2sXhtlylu73K 17936301
70. RS Goody T Durek H Waldmann L Brunsveld K Alexandrov 2005 Application of protein semisynthesis for the construction of functionalized posttranslationally modified rab GTPases Methods Enzymol 403 29 42 1:CAS:528:DC%2BD2sXmt1Sntb4%3D 16473575
71. L Brunsveld J Kuhlmann K Alexandrov A Wittinghofer RS Goody H Waldmann 2006 Lipidated ras and rab peptides and proteins-synthesis, structure, and function Angew Chem Int Ed Engl 45 6622 6646 1:CAS:528:DC%2BD28XhtFCltLnF 17031879
72. G Reuther KT Tan A Vogel C Nowak K Arnold J Kuhlmann H Waldmann D Huster 2006 The lipidated membrane anchor of full length N-Ras protein shows an extensive dynamics as revealed by solid-state NMR spectroscopy J Am Chem Soc 128 13840 13846 1:CAS:528:DC%2BD28XhtVajtrbM 17044712
73. JA Camarero 2008 Recent developments in the site-specific immobilization of proteins onto solid supports Biopolymers 90 450 458 1:CAS:528: DC%2BD1cXls1agsLw%3D 17618518
74. ML Lesaicherre M Uttamchandani GY Chen SQ Yao 2002 Developing site-specific immobilization strategies of peptides in a microarray Bioorg Med Chem Lett 12 2079 2083 1:CAS:528:DC%2BD38XlsVeksrg%3D 12127508
75. Govindaraju T, Jonkheijm P, Gogolin L, Schroeder H, Becker CF, Niemeyer CM, Waldmann H (2008) Surface immobilization of biomolecules by click sulfonamide reaction. Chem Commun (Camb) 32:3723-3725
76. Camarero JA, Kwon Y (2008) Traceless and site-specific attachment of proteins onto solid supports. Int J Pept Res Ther 14:351-357
77. ML Lesaicherre RY Lue GY Chen Q Zhu SQ Yao 2002 Intein-mediated biotinylation of proteins and its application in a protein microarray J Am Chem Soc 124 8768 8769 1:CAS:528:DC%2BD38XkvFCltrY%3D 12137509
78. RY Lue GY Chen Y Hu Q Zhu SQ Yao 2004 Versatile protein biotinylation strategies for potential high-throughput proteomics J Am Chem Soc 126 1055 1062 1:CAS:528:DC%2BD2cXkt1eqtA%3D%3D 14746473
79. K Holland-Nell AG Beck-Sickinger 2007 Specifically immobilised Aldo/Keto reductase AKR1A1 shows a dramatic increase in activity relative to the randomly immobilised enzyme Chembiochem 8 1071 1076 1:CAS:528:DC%2BD2sXntlCqsr8%3D 17508367
80. VJ Hruby F Al-Obeidi 1990 Emerging approaches in the molecular design of receptor-selective peptide ligands: conformational, topographical and dynamic considerations J Biochem 268 249 262 1:CAS:528:DyaK3cXktFOqs7Y%3D
81. J Rizo LM Gierasch 1992 Constrained peptides: models of bioactive peptides and protein substructures Annu Rev Biochem 61 387 418 1:CAS:528:DyaK3sXjsVCmuw%3D%3D 1497316
82. Camarero JA, Muir TW (1997) Chemoselective backbone cyclization of unprotected peptides. J Chem Soc Chem Comm 27:1369-1370
83. Zhang L, Tam JP (1997) Synthesis and application of unprotected cyclic peptides as building blocks for peptide dendrimers. J Am Chem Soc 119:2363-2370
84. Camarero JA, Pavel J, Muir TW (1998) Chemical synthesis of a circular protein domain: evidence for folding-assisted cyclization. Angew Chem Int Ed 37:347-349
85. Y Shao WY Lu SBH Kent 1998 A novel method to synthesize cyclic peptides Tetrahedron Lett 39 3911 3914 1:CAS:528:DyaK1cXjsVyjt7Y%3D
86. TC Evans J Benner M-Q Xu 1999 The cyclization and polymerization of bacterially expressed proteins using modified sef-splicing inteins J Biol Chem 274 18359 18363 1:CAS:528:DyaK1MXktF2rur8%3D 10373440
87. JA Camarero D Fushman S Sato I Giriat D Cowburn DP Raleigh TW Muir 2001 Rescuing a destabilized protein fold through backbone cyclization J Mol Biol 308 1045 1062 1:CAS:528:DC%2BD3MXjsVGitLw%3D 11352590
88. DJ Craik NL Daly T Bond C Waine 1999 Plant cyclotides: a unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif J Mol Biol 294 1327 1336 1:CAS:528:DyaK1MXnvFaqsLs%3D 10600388
89. KP Greenwood NL Daly DL Brown JL Stow DJ Craik 2007 The cyclic cystine knot miniprotein MCoTI-II is internalized into cells by macropinocytosis Int J Biochem Cell Biol 39 2252 2264 1:CAS:528:DC%2BD2sXhtFWgsL3O 17693122
90. DJ Craik S Simonsen NL Daly 2002 The cyclotides: novel macrocyclic peptides as scaffolds in drug design Curr Opin Drug Discov Devel 5 251 260 1:CAS:528:DC%2BD38XksFGqtLg%3D 11926131
91. M Salzmann K Pervushin G Wider H Senn K Wuthrich 1998 TROSY in triple-resonance experiments: new perspectives for sequential NMR assignment of large proteins Proc Natl Acad Sci USA 95 13585 13590 1:CAS:528: DyaK1cXnsVGgsLc%3D 9811843
92. R Xu B Ayers D Cowburn TW Muir 1999 Chemical ligation of folded recombinant proteins; segmental isotopic labeling of domains for NMR studies Proc Natl Acad Sci USA 96 388 393 1:CAS:528:DyaK1MXmtlCgsg%3D%3D 9892643
93. W Zhao Y Zhang C Cui Q Li J Wang 2008 An efficient on-column expressed protein ligation strategy: application to segmental triple labeling of human apolipoprotein E3 Protein Sci 17 736 747 1:CAS:528:DC%2BD1cXksVGrsb8%3D 18305193
94. SA Tatulian S Qin AH Pande X He 2005 Positioning membrane proteins by novel protein engineering and biophysical approaches J Mol Biol 351 939 947 1:CAS:528:DC%2BD2MXns1Wlurw%3D 16055150
95. RR Flavell P Kothari M Bar-Dagan M Synan S Vallabhajosula JM Friedman TW Muir G Ceccarini 2008 Site-specific (18)F-labeling of the protein hormone leptin using a general two-step ligation procedure J Am Chem Soc 130 9106 9112 1:CAS:528:DC%2BD1cXns1SqurY%3D 18570424
96. RR Flavell M Huse M Goger M Trester-Zedlitz J Kuriyan TW Muir 2002 Efficient semisynthesis of a tetraphosphorylated analogue of the Type I TGFbeta receptor Org Lett 4 165 168 1:CAS:528:DC%2BD3MXpt1Cnsr0%3D 11796041
97. JJ Ottesen M Huse MD Sekedat TW Muir 2004 Semisynthesis of phosphovariants of Smad2 reveals a substrate preference of the activated T beta RI kinase Biochemistry 43 5698 5706 1:CAS:528:DC%2BD2cXjtlCnsro%3D 15134444
98. JW Wu M Hu J Chai J Seoane M Huse C Li DJ Rigotti S Kyin TW Muir R Fairman J Massague Y Shi 2001 Crystal structure of a phosphorylated Smad2. Recognition of phosphoserine by the MH2 domain and insights on Smad function in TGF-beta signaling Mol Cell 8 1277 1289 1:CAS:528:DC%2BD38XivFGmsg%3D%3D 11779503
99. M Huse TW Muir L Xu YG Chen J Kuriyan J Massague 2001 The TGF beta receptor activation process: an inhibitor- to substrate-binding switch Mol Cell 8 671 682 1:CAS:528:DC%2BD3MXnslGmt7w%3D 11583628
100. BY Qin SS Lam JJ Correia K Lin 2002 Smad3 allostery links TGF-beta receptor kinase activation to transcriptional control Genes Dev 16 1950 1963 1:CAS:528:DC%2BD38XmtFalu7c%3D 12154125
101. BM Chacko BY Qin A Tiwari G Shi S Lam LJ Hayward M De Caestecker K Lin 2004 Structural basis of heteromeric smad protein assembly in TGF-beta signaling Mol Cell 15 813 823 1:CAS:528:DC%2BD2cXnvFyhs7g%3D 15350224
102. T Durek K Alexandrov RS Goody A Hildebrand I Heinemann H Waldmann 2004 Synthesis of fluorescently labeled mono- and diprenylated Rab7 GTPase J Am Chem Soc 126 16368 16378 1:CAS:528:DC%2BD2cXhtVansrnL 15600338
103. L Brunsveld A Watzke T Durek K Alexandrov RS Goody H Waldmann 2005 Synthesis of functionalized rab GTPases by a combination of solution- or solid-phase lipopeptide synthesis with expressed protein ligation Chemistry 11 2756 2772 1:CAS:528:DC%2BD2MXktVCls7s%3D 15729676
104. A Rak O Pylypenko T Durek A Watzke S Kushnir L Brunsveld H Waldmann RS Goody K Alexandrov 2003 Structure of Rab GDP-dissociation inhibitor in complex with prenylated YPT1 GTPase Science 302 646 650 1:CAS:528:DC%2BD3sXotlWqt7c%3D 14576435
105. O Pylypenko A Rak T Durek S Kushnir BE Dursina NH Thomae AT Constantinescu L Brunsveld A Watzke H Waldmann RS Goody K Alexandrov 2006 Structure of doubly prenylated Ypt1:GDI complex and the mechanism of GDI-mediated Rab recycling EMBO J 25 13 23 1:CAS:528:DC%2BD28Xis1Kgsw%3D%3D 16395334
106. Z Guo YW Wu D Das C Delon J Cramer S Yu S Thuns N Lupilova H Waldmann L Brunsveld RS Goody K Alexandrov W Blankenfeldt 2008 Structures of RabGGTase-substrate/product complexes provide insights into the evolution of protein prenylation EMBO J 27 2444 2456 1:CAS:528:DC%2BD1cXhtFWlurzN 18756270
107. T Kouzarides 2007 Chromatin modifications and their function Cell 128 693 705 1:CAS:528:DC%2BD2sXis12ju7Y%3D 17320507
108. MA Shogren-Knaak CJ Fry CL Peterson 2003 A native peptide ligation strategy for deciphering nucleosomal histone modifications J Biol Chem 278 15744 15748 1:CAS:528:DC%2BD3sXjt1ehsr8%3D 12595522
109. M Shogren-Knaak H Ishii JM Sun MJ Pazin JR Davie CL Peterson 2006 Histone H4-K16 acetylation controls chromatin structure and protein interactions Science 311 844 847 1:CAS:528:DC%2BD28XhtFylsLY%3D 16469925 (Pubitemid 43228847)
110. S He D Bauman JS Davis A Loyola K Nishioka JL Gronlund D Reinberg F Meng N Kelleher DG McCafferty 2003 Facile synthesis of site-specifically acetylated and methylated histone proteins: reagents for evaluation of the histone code hypothesis Proc Natl Acad Sci USA 100 12033 12038 1:CAS:528:DC%2BD3sXotlGltb0%3D 14530408
111. C Chatterjee RK McGinty JP Pellois TW Muir 2007 Auxiliary-mediated site-specific peptide ubiquitylation Angew Chem Int Ed Engl 46 2814 2818 1:CAS:528:DC%2BD2sXksleitbo%3D 17366504
112. RK McGinty J Kim C Chatterjee RG Roeder TW Muir 2008 Chemically ubiquitylated histone H2B stimulates hDot1L-mediated intranucleosomal methylation Nature 453 812 816 1:CAS:528:DC%2BD1cXmvVGmsLw%3D 18449190
113. H Hojo Y Nakahara 2007 Recent progress in the field of glycopeptide synthesis Biopolymers 88 308 324 1:CAS:528:DC%2BD2sXksVWltbs%3D 17278124
114. LA Marcaurelle LS Mizoue J Wilken L Oldham SB Kent TM Handel CR Bertozzi 2001 Chemical synthesis of lymphotactin: a glycosylated chemokine with a C-terminal mucin-like domain Chemistry 7 1129 1132 1:CAS:528: DC%2BD3MXhvVegu7k%3D 11303872
115. CP Hackenberger CT Friel SE Radford B Imperiali 2005 Semisynthesis of a glycosylated Im7 analogue for protein folding studies J Am Chem Soc 127 12882 12889 1:CAS:528:DC%2BD2MXpt1Whtrg%3D 16159282
116. D Macmillan CR Bertozzi 2004 Modular assembly of glycoproteins: towards the synthesis of GlyCAM-1 by using expressed protein ligation Angew Chem Int Ed Engl 43 1355 1359 1:CAS:528:DC%2BD2cXivFSqtbc%3D 15368405
117. FI Valiyaveetil M Sekedat R MacKinnon TW Muir 2006 Structural and functional consequences of an amide-to-ester substitution in the selectivity filter of a potassium channel J Am Chem Soc 128 11591 11599 1:CAS:528: DC%2BD28XnvFOqsrc%3D 16939283
118. D Schwarzer PA Cole 2005 Protein semisynthesis and expressed protein ligation: chasing a protein's tail Curr Opin Chem Biol 9 561 569 1:CAS:528:DC%2BD2MXht1aqu7bM 16226484
119. Algire MA, Maag D, Lorsch JR (2005) Pi release from eIF2, not GTP hydrolysis, is the step controlled by start-site selection during eukaryotic translation initiation. Mol Cell 20:251-262
120. D Maag CA Fekete Z Gryczynski JR Lorsch 2005 A conformational change in the eukaryotic translation preinitiation complex and release of eIF1 signal recognition of the start codon Mol Cell 17 265 275 1:CAS:528: DC%2BD2MXht12lt70%3D 15664195
121. LM Szewczuk MK Tarrant V Sample WJ Drury 3rd J Zhang PA Cole 2008 Analysis of serotonin N-acetyltransferase regulation in vitro and in live cells using protein semisynthesis Biochemistry 47 10407 10419 1:CAS:528: DC%2BD1cXhtVOmtrnI 18771288
122. N Xie EN Elangwe S Asher YG Zheng 2009 A dual-mode fluorescence strategy for screening HAT modulators Bioconjug Chem 20 360 366 1:CAS:528: DC%2BD1MXlvFyitw%3D%3D 19146394
123. Woo Y-H, Camarero JA (2006) Interfacing 'Hard' and 'Soft' matter with exquisite chemical control. Curr Nanosci 2:93-103
124. CF Becker Y Marsac P Hazarika J Moser RS Goody CM Niemeyer 2007 Functional immobilization of the small GTPase Rab6A on DNA-Gold nanoparticles by using a site-specifically attached poly(ethylene glycol) linker and thiol place-exchange reaction Chembiochem 8 32 36 1:CAS:528:DC%2BD2sXhtFCnu7Y%3D 17121405
125. DJ Craik M Cemazar NL Daly 2006 The cyclotides and related macrocyclic peptides as scaffolds in drug design Curr Opin Drug Discov Dev 9 251 260 1:CAS:528:DC%2BD28XislSmtL4%3D
126. MG Paulick AR Wise MB Forstner JT Groves CR Bertozzi 2007 Synthetic analogues of glycosylphosphatidylinositol-anchored proteins and their behavior in supported lipid bilayers J Am Chem Soc 129 11543 11550 1:CAS:528: DC%2BD2sXptl2lt7c%3D 17715922