"Splicing up" drug discovery. Cell-based expression and screening of genetically-encoded libraries of backbone-cyclized polypeptides

Advanced Drug Delivery Reviews

Volumn 61, Issue 11, 2009, Pages 908-917

  Sancheti, Harshkumar ^a   Camarero, Julio A ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Cyclic peptide; Cyclotides; Expressed Protein Ligation; Genetically encoded libraries; Intein; Native Chemical Ligation; Trans peptidation

Indexed keywords

CYCLIC PEPTIDE; CYCLOTIDES; EXPRESSED PROTEIN LIGATION; GENETICALLY-ENCODED LIBRARIES; INTEIN; NATIVE CHEMICAL LIGATION; TRANS-PEPTIDATION;

AMINES; BIOCHEMISTRY; BIOSYNTHESIS; CELL MEMBRANES; DNA; GENETIC ENGINEERING; LIBRARIES; NUCLEIC ACIDS; PEPTIDES;

POLYPEPTIDES;

ALPHA THIOESTER; ANTIINFECTIVE AGENT; CYCLOPEPTIDE; CYCLOTIDE; CYSTEINE; ENDOPEPTIDASE CLPX; INTEIN; POLYPEPTIDE; PROTEIN SH3; PROTEINASE; PSEUDOSTELLARIN F; RECOMBINANT DNA; RETROVIRUS VECTOR; SORTASE; STAPHYLOCOCCUS AUREUS SORTASE A; THIOESTER; UNCLASSIFIED DRUG;

ALLERGY; AMINO TERMINAL SEQUENCE; ANTIBACTERIAL ACTIVITY; ASTHMA; BACTERIAL CELL; CELL SCREENING; CYCLIZATION; DRUG DELIVERY SYSTEM; ENZYME MECHANISM; ESCHERICHIA COLI; EXPRESSED PROTEIN LIGATION; GENE LIBRARY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NATIVE CHEMICAL LIGATION; NONHUMAN; NONRIBOSOMAL PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN PROCESSING; RECOMBINANT DNA TECHNOLOGY; REVIEW; TRANS SPLICING; TRANSPEPTIDATION; VIRAL GENE DELIVERY SYSTEM;

DRUG DISCOVERY; PEPTIDE LIBRARY; PEPTIDES; PEPTIDES, CYCLIC; PROTEIN SPLICING; RECOMBINANT PROTEINS;

EID: 70349439112     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.addr.2009.07.003     Document Type: Review

References (79)

1. Hruby V.J., and Al-Obeidi F. Emerging approaches in the molecular design of receptor-selective peptide ligands: conformational, topographical and dynamic considerations. J. Biochem. 268 (1990) 249-262
2. Rizo J., and Gierasch L.M. Constrained peptides: models of bioactive peptides and protein substructures. Ann. Rev. Biochem. 61 (1992) 387-418
3. Camarero J.A., and Muir T.W. Chemoselective backbone cyclization of unprotected peptides. Chem. Soc. Chem. Comm. 1997 (1997) 1369-1370
4. Zhang L., and Tam J.P. Synthesis and application of unprotected cyclic peptides as building blocks for peptide dendrimers. J. Am. Chem. Soc. 119 (1997) 2363-2370
5. Camarero J.A., Pavel J., and Muir T.W. chemical synthesis of a circular protein domain: evidence for folding-assisted cyclization. Angew. Chem. Int. Ed. 37 (1998) 347-349
6. Shao Y., Lu W.Y., and Kent S.B.H. A novel method to synthesize cyclic peptides. Tetrahedron Lett. 39 (1998) 3911-3914
7. Camarero J.A., Cotton G.J., Adeva A., and Muir T.W. Chemical ligation of unprotected peptides directly form a solid support. J. Pept. Res. 51 (1998) 303-316
8. Trauger J.W., Kohli R.M., Mootz H.D., Marahiel M.A., and Walsh C.T. Peptide cyclization catalysed by the thioesterase domain of tyrocidine synthetase. Nature 407 (2000) 215-218
9. Kohli R.M., Walsh C.T., and Burkart M.D. Biomimetic synthesis and optimization of cyclic peptide antibiotics. Nature 418 (2002) 658-661
10. Walsh C.T. Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 303 (2004) 1805-1810
11. Camarero J.A., and Muir T.W. Biosynthesis of a head-to-tail cyclized protein with improved biological activity. J. Am. Chem. Soc. 121 (1999) 5597-5598
12. Scott C.P., Abel-Santos E., Wall M., Wahnon D., and Benkovic S.J. Production of cyclic peptides and proteins in vivo. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 13638-13643
13. Evans T.C., Benner J., and Xu M.-Q. The cyclization and polymerization of bacterially expressed proteins using modified self-splicing inteins. J. Biol. Chem. 274 (1999) 18359-18381
14. Camarero J.A., Fushman D., Cowburn D., and Muir T.W. Peptide chemical ligation inside living cells: in vivo generation of a circular protein domain. Bioorg. Med. Chem. 9 (2001) 2479-2484
15. Iwai H., Lingel A., and Pluckthun A. Cyclic green fluorescent protein produced in vivo using an artificially split PI-PfuI intein from Pyrococcus furiosus. J. Biol. Chem. 276 (2001) 16548-16554
16. Abel-Santos E., Scott C.P., and Benkovic S.J. Use of inteins for the in vivo production of stable cyclic peptide libraries in E. coli. Methods Mol. Biol. 205 (2003) 281-294
17. Noren C.J., Wang J.M., and Perler F.B. Dissecting the chemistry of protein splicing and its applications. Angew. Chem. Int. Ed. 39 (2000) 451-456
18. Suter B., Auerbach D., and Stagljar I. Yeast-based functional genomics and proteomics technologies: the first 15 years and beyond. Biotechniques 40 (2006) 625-644
19. Wu H., Hu Z., and Liu X.Q. Protein trans-splicing by a split intein encoded in a split DnaE gene of Synechocystis sp. PCC6803. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 9226-9231
20. Evans Jr. T.C., Martin D., Kolly R., Panne D., Sun L., Ghosh I., Chen L., Benner J., Liu X.Q., and Xu M.Q. Protein trans-splicing and cyclization by a naturally split intein from the dnaE gene of Synechocystis species PCC6803. J. Biol. Chem. 275 (2000) 9091-9094
21. Dawson P.E., Muir T.W., Clark-Lewis I., and Kent S.B.H. Synthesis of proteins by native chemical ligation. Science 266 (1994) 776-779
22. Dawson P.E., and Kent S.B. Synthesis of native proteins by chemical ligation. Annu. Rev. Biochem. 69 (2000) 923-960
23. Tam J.P., Lu Y.A., Liu C.F., and Shao J. Peptide synthesis using unprotected peptides through orthogonal coupling methods. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 12485-12489
24. Evans Jr. T.C., and Xu M.Q. Intein-mediated protein ligation: harnessing nature's escape artists. Biopolymers 51 (1999) 333-342
25. Camarero J.A., and Muir T.W. Native chemical ligation of polypeptides. Curr. Prot. Prot. Sci. (1999) 1-21
26. Muir T.W. Semisynthesis of proteins by expressed protein ligation. Annu. Rev. Biochem. 72 (2003) 249-289
27. Wieland T., Bokelmann E., Bauer L., Lang H.U., and Lau H. Polypeptide synthesis. VIII. Formation of sulfur containing peptides by intramolecular migration of aminoacyl groups. Liebigs Ann. Chem. 583 (1953) 129
28. Wieland T. Sulfur in biomimetic peptide synthesis. In: Jaeniche v.D.K. (Ed). The Roots of Modern Biochemistry (1988), Walter de Gruyter & Co., Berlin, New York 213-221
29. Muir T.W., Sondhi D., and Cole P.A. Expressed protein ligation: a general method for protein engineering. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 6705-6710
30. Severinov K., and Muir T.W. Expressed protein ligation, a novel method for studying protein-protein interactions in transcription. J. Biol. Chem. 273 (1998) 16205-16209
31. Evans T.C., Benner J., and Xu M.-Q. Semisynthesis of cytotoxic proteins using a modified protein splicing element. Protein Sci. 7 (1998) 2256-2264
32. Xu M.-Q., and Perler F.B. The mechanism of protein splicing and its modulation by mutation. EMBO J. 15 (1996) 5146-5153
33. Chong S., Mersha F.B., Comb D.G., Scott M.E., Landry D., Vence L.M., Perler F.B., Benner J., Kucera R.B., Hirvonen C.A., Pelletier J.J., Paulus H., and Xu M.Q. Single-column purification of free recombinant proteins using a self-cleavable affinity tag derived from a protein splicing element. Gene 192 (1997) 271-281
34. Chong S., Montenello G.E., Zhang A., Cantor E.J., Liao W., Xu M.-Q., and Benner J. Utilizing the C-terminal cleavage activity of a protein splicing element to purify recombinant proteins in a single chromatographic step. Nucleic Acid Res. 26 (1998) 5109-5115
35. Hirel P.H., Schmitter M.J., Dessen P., Fayat G., and Blanquet S. 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. U. S. A. 86 (1989) 8247-8251
36. Dwyer M.A., Lu W., Dwyer J.J., and Kossiakoff A.A. Biosynthetic phage display: a novel protein engineering tool combining chemical and genetic diversity. Chem. Biol. 7 (2000) 263-274
37. Iwai H., and Pluckthum A. Circular b-lactamase: stability enhancement by cyclizing the backbone. FEBS Lett. (1999) 166-172
38. Cotton G.J., Ayers B., Xu R., and Muir T.W. Insertion of a synthetic peptide into a recombinant protein framework; a protein biosensor. J. Am. Chem. Soc. 121 (1999) 1100-1101
39. Erlandson D.A., Chytil M., and Verdine G.L. The leucine zipper domain controls the orientation of AP-1 in the NFAT•AP-1•DNA complex. Chem. Biol. 3 (1996) 981-991
40. Tolbert T.J., and Wong C.-H. New methods for proteomic research: preparation of proteins with N-terminal cysteines for labeling and conjugation. Angew. Chem. Int. Ed. Engl. 41 (2002) 2171-2174
41. Evans T.C., Benner J., and Xu M.-Q. The in vitro ligation of bacterially expressed proteins using an intein from Methanobacterium thermoautotrophicum. J. Biol. Chem. 274 (1999) 3923-3926
42. Southworth M.W., Amaya K., Evans T.C., Xu M.Q., and Perler F.B. Purification of proteins fused to either the amino or carboxy terminus of the Mycobacterium xenopi gyrase A intein. Biotechniques 27 (1999) 110-114, 116, 118-120
43. Mathys S., Evans T.C., Chute I.C., Wu H., Chong S., Benner J., Liu X.Q., and Xu M.Q. 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 (1999) 1-13
44. Liu D., Xu R., Dutta K., and Cowburn D. N-terminal cysteinyl proteins can be prepared using thrombin cleavage. FEBS Lett. 582 (2008) 1163-1167
45. Dalbey R.E., Lively M.O., Bron S., and van Dijl J.M. The chemistry and enzymology of the type I signal peptidases. Protein Sci. 6 (1997) 1129-1138
46. Paetzel M., Dalbey R.E., and Strynadka N.C. Crystal structure of a bacterial signal peptidase apoenzyme: implications for signal peptide binding and the Ser-Lys dyad mechanism. J. Biol. Chem. 277 (2002) 9512-9519
47. Hauser P.S., and Ryan R.O. Expressed protein ligation using an N-terminal cysteine containing fragment generated in vivo from a pelB fusion protein. Protein Expr. Purif. 54 (2007) 227-233
48. Camarero J.A., Fushman D., Sato S., Giriat I., Cowburn D., Raleigh D.P., and Muir T.W. Rescuing a destabilized protein fold through backbone cyclization. J. Mol. Biol. 308 (2001) 1045-1062
49. Camarero J.A., Kimura R.H., Woo Y.H., Shekhtman A., and Cantor J. Biosynthesis of a fully functional cyclotide inside living bacterial cells. Chembiochem 8 (2007) 1363-1366
50. Craik D.J., Daly N.L., Bond T., and Waine C. Plant cyclotides: a unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif. J. Mol. Biol. 294 (1999) 1327-1336
51. Greenwood K.P., Daly N.L., Brown D.L., Stow J.L., and Craik D.J. The cyclic cystine knot miniprotein MCoTI-II is internalized into cells by macropinocytosis. Int. J. Biochem. Cell Biol. 39 (2007) 2252-2264
52. Craik D.J., Simonsen S., and Daly N.L. The cyclotides: novel macrocyclic peptides as scaffolds in drug design. Curr. Opin. Drug Discov. Dev. 5 (2002) 251-260
53. Kimura R.H., Tran A.T., and Camarero J.A. Biosynthesis of the cyclotide Kalata B1 by using protein splicing. Angew. Chem. Int. Ed. Engl. 45 (2006) 973-976
54. Saleh L., and Perler F.B. Protein splicing in cis and in trans. Chem. Rec. 6 (2006) 183-193
55. Xu M.Q., and Evans Jr. T.C. Recent advances in protein splicing: manipulating proteins in vitro and in vivo. Curr. Opin. Biotechnol. 16 (2005) 440-446
56. Naumann T.A., Savinov S.N., and Benkovic S.J. Engineering an affinity tag for genetically encoded cyclic peptides. Biotechnol. Bioeng. 92 (2005) 820-830
57. Tavassoli A., and Benkovic S.J. Split-intein mediated circular ligation used in the synthesis of cyclic peptide libraries in E. coli. Natl. Protoc. 2 (2007) 1126-1133
58. Scott C.P., Abel-Santos E., Jones A.D., and Benkovic S.J. Structural requirements for the biosynthesis of backbone cyclic peptide libraries. Chem. Biol. 8 (2001) 801-815
59. Hackeng T.M., Griffin J.H., and Dawson P.E. Protein synthesis by native chemical ligation: expanded scope by using straightforward methodology. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 10063-10078
60. Hackeng T.M., Griffin J.H., and Dawson P.E. Protein synthesis by native chemical ligation: expanded scope by using straightforward methodology. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 10068-10073
61. Marraffini L.A., Dedent A.C., and Schneewind O. Sortases and the art of anchoring proteins to the envelopes of gram-positive bacteria. Microbiol. Mol. Biol. Rev. 70 (2006) 192-221
62. Mazmanian S.K., Liu G., Ton-That H., and Schneewind O. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285 (1999) 760-763
63. Mao H., Hart S.A., Schink A., and Pollok B.A. Sortase-mediated protein ligation: a new method for protein engineering. J. Am. Chem. Soc. 126 (2004) 2670-2671
64. Tsukiji S., and Nagamune T. Sortase-mediated ligation: a gift from Gram-positive bacteria to protein engineering. Chembiochem 10 (2009) 787-798
65. Parthasarathy R., Subramanian S., and Boder E.T. Sortase A as a novel molecular "stapler" for sequence-specific protein conjugation. Bioconjug. Chem. 18 (2007) 469-476
66. Saska I., and Craik D.J. Protease-catalysed protein splicing: a new post-translational modification?. Trends Biochem. Sci. 33 (2008) 363-368
67. Gillon A.D., Saska I., Jennings C.V., Guarino R.F., Craik D.J., and Anderson M.A. Biosynthesis of circular proteins in plants. Plant J. 53 (2008) 505-515
68. Saska I., Gillon A.D., Hatsugai N., Dietzgen R.G., Hara-Nishimura I., Anderson M.A., and Craik D.J. An asparaginyl endopeptidase mediates in vivo protein backbone cyclization. J. Biol. Chem. 282 (2007) 29721-29728
69. Kinsella T.M., Ohashi C.T., Harder A.G., Yam G.C., Li W., Peelle B., Pali E.S., Bennett M.K., Molineaux S.M., Anderson D.A., Masuda E.S., and Payan D.G. Retrovirally delivered random cyclic peptide libraries yield inhibitors of interleukin-4 signaling in human B cells. J. Biol. Chem. 277 (2002) 37512-37518
70. Cheng L., Naumann T.A., Horswill A.R., Hong S.J., Venters B.J., Tomsho J.W., Benkovic S.J., and Keiler K.C. Discovery of antibacterial cyclic peptides that inhibit the ClpXP protease. Protein Sci. 16 (2007) 1535-1542
71. Tavassoli A., Lu Q., Gam J., Pan H., Benkovic S.J., and Cohen S.N. Inhibition of HIV budding by a genetically selected cyclic peptide targeting the Gag-TSG101 interaction. ACS Chem. Biol. 3 (2008) 757-764
72. Tavassoli A., and Benkovic S.J. Genetically selected cyclic-peptide inhibitors of AICAR transformylase homodimerization. Angew. Chem. Int. Ed. Engl. 44 (2005) 2760-2763
73. Horswill A.R., Savinov S.N., and Benkovic S.J. A systematic method for identifying small-molecule modulators of protein-protein interactions. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 15591-15596
74. Hernandez J.F., Gagnon J., Chiche L., Nguyen T.M., Andrieu J.P., Heitz A., Trinh Hong T., Pham T.T., and Le Nguyen D. Squash trypsin inhibitors from Momordica cochinchinensis exhibit an atypical macrocyclic structure. Biochemistry 39 (2000) 5722-5730
75. Felizmenio-Quimio M.E., Daly N.L., and Craik D.J. Circular proteins in plants: solution structure of a novel macrocyclic trypsin inhibitor from Momordica cochinchinensis. J. Biol. Chem. 276 (2001) 22875-22882
76. Luckett S., Garcia R.S., Barker J.J., Konarev A.V., Shewry P.R., Clarke A.R., and Brady R.L. High-resolution structure of a potent, cyclic proteinase inhibitor from sunflower seeds. J. Mol. Biol. 290 (1999) 525-533
77. Korsinczky M.L., Schirra H.J., Rosengren K.J., West J., Condie B.A., Otvos L., Anderson M.A., and Craik D.J. Solution structures by 1H NMR of the novel cyclic trypsin inhibitor SFTI-1 from sunflower seeds and an acyclic permutant. J. Mol. Biol. 311 (2001) 579-591
78. Wang W., Mulakala C., Ward S.C., Jung G., Luong H., Pham D., Waring A.J., Kaznessis Y., Lu W., Bradley K.A., and Lehrer R.I. Retrocyclins kill bacilli and germinating spores of Bacillus anthracis and inactivate anthrax lethal toxin. J. Biol. Chem. 281 (2006) 32755-32764
79. Gallo S.A., Wang W., Rawat S.S., Jung G., Waring A.J., Cole A.M., Lu H., Yan X., Daly N.L., Craik D.J., Jiang S., Lehrer R.I., and Blumenthal R. Theta-defensins prevent HIV-1 Env-mediated fusion by binding gp41 and blocking 6-helix bundle formation. J. Biol. Chem. 281 (2006) 18787-18792