Phage display: Concept, innovations, applications and future

Biotechnology Advances

Volumn 28, Issue 6, 2010, Pages 849-858

  Pande, Jyoti ^a   Szewczyk, Magdalena M ^a   Grover, Ashok K ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Antibodies; Caloxin; Enzyme inhibitors; Peptide display; Protein protein interactions; Receptors; Vaccines

Indexed keywords

ALLOSTERIC SITE; BIOPANNING; CALOXIN; COMMONLY USED; DRUG DESIGN; ENZYME INHIBITORS; EPITOPE MAPPING; FILAMENTOUS PHAGE; G PROTEIN; HIGH AFFINITY LIGANDS; PHAGE CLONES; PHAGE DISPLAY; PHAGE LIBRARIES; PHAGE PARTICLES; PROTEIN-PROTEIN INTERACTIONS; RAPID ISOLATION; RECEPTORS; THERAPEUTIC TARGETS; VACCINE DEVELOPMENT;

ANTIBODIES; BINDING SITES; BIOCHEMISTRY; COLUMN CHROMATOGRAPHY; ENZYMES; LIBRARIES; LIGANDS; VACCINES;

PEPTIDES;

PEPTIDE; PEPTIDE LIBRARY;

ANTIBODY; CHROMATOGRAPHY; ENZYME ACTIVITY; FUTURE PROSPECT; INHIBITOR; INNOVATION; LIGAND; PEPTIDE; PROTEIN; RECOMBINATION; VACCINE;

BACTERIOPHAGE; METABOLISM; MUTAGENESIS; PROTEIN BINDING; REVIEW;

BACTERIOPHAGES; MUTAGENESIS; PEPTIDE LIBRARY; PEPTIDES; PROTEIN BINDING;

EID: 77957017501     PISSN: 07349750     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biotechadv.2010.07.004     Document Type: Review

References (118)

1. Augustine-Rauch K.A., Zhang Q.J., Leonard J.L., Chadderton A., Welsh M.J., Rami H.K., et al. Evidence for a molecular mechanism of teratogenicity of SB-236057, a 5-HT1B receptor inverse agonist that alters axial formation. Birth Defects Res A Clin Mol Teratol 2004, 70:789-807.
2. Barbas C.F., Kang A.S., Lerner R.A., Benkovic S.J. Assembly of combinatorial antibody libraries on phage surfaces: the gene III site. Proc Natl Acad Sci USA 1991, 88:7978-7982.
3. Basha S., Rai P., Poon V., Saraph A., Gujraty K., Go M.Y., et al. Polyvalent inhibitors of anthrax toxin that target host receptors. Proc Natl Acad Sci USA 2006, 103:13509-13513.
4. Benhar I. Biotechnological applications of phage and cell display. Biotechnol Adv 2001, 19:1-33.
5. Berggard T., Linse S., James P. Methods for the detection and analysis of protein-protein interactions. Proteomics 2007, 7:2833-2842.
6. Bonetto S., Carlavan I., Baty D. Isolation and characterization of antagonist and agonist peptides to the human melanocortin 1 receptor. Peptides 2005, 26:2302-2313.
7. Bottger V., Bottger A. Epitope mapping using phage display peptide libraries. Methods Mol Biol 2009, 524:181-201.
8. Bratkovic T. Progress in phage display: evolution of the technique and its applications. Cell Mol Life Sci 2010, 67:749-767.
9. Burritt J.B., Quinn M.T., Jutila M.A., Bond C.W., Jesaitis A.J. Topological mapping of neutrophil cytochrome b epitopes with phage-display libraries. J Biol Chem 1995, 270:16974-16980.
10. Caberoy N.B., Zhou Y., Alvarado G., Fan X., Li W. Efficient identification of phosphatidylserine-binding proteins by ORF phage display. Biochem Biophys Res Commun 2009, 386:197-201.
11. Caberoy N.B., Zhou Y., Jiang X., Alvarado G., Li W. Efficient identification of tubby-binding proteins by an improved system of T7 phage display. J Mol Recognit 2010, 23:74-83.
12. Cardinale A., Biocca S. The potential of intracellular antibodies for therapeutic targeting of protein-misfolding diseases. Trends Mol Med 2008, 14:373-380.
13. Carter D.M., Miousse I.R., Gagnon J.N., Martinez E., Clements A., Lee J., et al. Interactions between TonB from Escherichia coli and the periplasmic protein FhuD. J Biol Chem 2006, 281:35413-35424.
14. Chaudhary J., Walia M., Matharu J., Escher E., Grover A.K. Caloxin: a novel plasma membrane Ca2+ pump inhibitor. Am J Physiol Cell Physiol 2001, 280:C1027-C1030.
15. Clackson T., Wells J.A. In vitro selection from protein and peptide libraries. Trends Biotechnol 1994, 12:173-184.
16. Collins J., Horn N., Wadenback J., Szardenings M. Cosmix-plexing: a novel recombinatorial approach for evolutionary selection from combinatorial libraries. J Biotechnol 2001, 74:317-338.
17. Cortese R., Monaci P., Nicosia A., Luzzago A., Felici F., Galfre G., et al. Identification of biologically active peptides using random libraries displayed on phage. Curr Opin Biotechnol 1995, 6:73-80.
18. Crowe J.E., Gilmour P.S., Murphy B.R., Chanock R.M., Duan L., Pomerantz R.J., et al. Isolation of a second recombinant human respiratory syncytial virus monoclonal antibody fragment (Fab RSVF2-5) that exhibits therapeutic efficacy in vivo. J Infect Dis 1998, 177:1073-1076.
19. Deshayes K., Schaffer M.L., Skelton N.J., Nakamura G.R., Kadkhodayan S., Sidhu S.S. Rapid identification of small binding motifs with high-throughput phage display: discovery of peptidic antagonists of IGF-1 function. Chem Biol 2002, 9:495-505.
20. Diamond S.L. Methods for mapping protease specificity. Curr Opin Chem Biol 2007, 11:46-51.
21. El Zoeiby A., Sanschagrin F., Darveau A., Brisson J.R., Levesque R.C. Identification of novel inhibitors of Pseudomonas aeruginosa MurC enzyme derived from phage-displayed peptide libraries. J Antimicrob Chemother 2003, 51:531-543.
22. Engberg J., Andersen P.S., Nielsen L.K., Dziegiel M., Johansen L.K., Albrechtsen B. Phage-display libraries of murine and human antibody Fab fragments. Mol Biotechnol 1996, 6:287-310.
23. Evans E.R., Sutton J.M., Gravett A., Shone C.C. Analysis of the substrate recognition domain determinants of botulinum type B toxin using phage display. Toxicon 2005, 46:446-453.
24. Fack F., Hügle-Dörr B., Song D., Queitsch I., Petersen G., Bautz E.K. Epitope mapping by phage display: random versus gene-fragment libraries. J Immunol Methods 1997, 206:43-52.
25. Faix P.H., Burg M.A., Gonzales M., Ravey E.P., Baird A., Larocca D. Phage display of cDNA libraries: enrichment of cDNA expression using open reading frame selection. Biotechniques 2004, 36:1018-1029.
26. Finucane M.D., Tuna M., Lees J.H., Woolfson D.N. Core-directed protein design. I. An experimental method for selecting stable proteins from combinatorial libraries. Biochemistry 1999, 38:11604-11612.
27. Fisch I., Kontermann R.E., Finnern R., Hartley O., Soler-Gonzalez A.S., Griffiths A.D., et al. A strategy of exon shuffling for making large peptide repertoires displayed on filamentous bacteriophage. Proc Natl Acad Sci USA 1996, 93:7761-7766.
28. Fleming T.J., Sachdeva M., Delic M., Beltzer J., Wescott C.R., Devlin M., et al. Discovery of high-affinity peptide binders to BLyS by phage display. J Mol Recognit 2005, 18:94-102.
29. Förster-Waldl E., Riemer A.B., Dehof A.K., Neumann D., Brämswig K., Boltz-Nitulescu G., et al. Isolation and structural analysis of peptide mimotopes for the disialoganglioside GD2, a neuroblastoma tumor antigen. Mol Immunol 2005, 42(3):319-325.
30. Fuh G., Pisabarro M.T., Li Y., Quan C., Lasky L.A., Sidhu S.S. Analysis of PDZ domain-ligand interactions using carboxyl-terminal phage display. J Biol Chem 2000, 275:21486-21491.
31. Fuh G., Sidhu S.S. Efficient phage display of polypeptides fused to the carboxy-terminus of the M13 gene-3 minor coat protein. FEBS Lett 2000, 480:231-234.
32. Geysen H.M., Mason T.J., Rodda S.J. Cognitive features of continuous antigenic determinants. J Mol Recognit 1988, 1:32-41.
33. Gujraty K., Sadacharan S., Frost M., Poon V., Kane R.S., Mogridge J. Functional characterization of peptide-based anthrax toxin inhibitors. Mol Pharm 2005, 2:367-372.
34. Hekim C., Leinonen J., Narvanen A., Koistinen H., Zhu L., Koivunen E., et al. Novel peptide inhibitors of human kallikrein 2. J Biol Chem 2006, 281:12555-12560.
35. Hertveldt K., Belien T., Volckaert G. General M13 phage display: M13 phage display in identification and characterization of protein-protein interactions. Methods Mol Biol 2009, 502:321-339.
36. Hessling J., Lohse M.J., Klotz K.N. Peptide G protein agonists from a phage display library. Biochem Pharmacol 2003, 65:961-967.
37. Hiraga K., Soga I., Dansereau J.T., Pereira B., Derbyshire V., Du Z., et al. Selection and structure of hyperactive inteins: peripheral changes relayed to the catalytic center. J Mol Biol 2009, 393:1106-1117.
38. Hoess R.H. Protein design and phage display. Chem Rev 2001, 101:3205-3218.
39. Hoogenboom H.R. Selecting and screening recombinant antibody libraries. Nat Biotechnol 2005, 23(9):1105-1116.
40. Hoogenboom H.R., Griffiths A.D., Johnson K.S., Chiswell D.J., Hudson P., Winter G. Multi-subunit proteins on the surface of filamentous phage: methodologies for displaying antibody (Fab) heavy and light chains. Nucleic Acids Res 1991, 19:4133-4137.
41. Huang J., Gutteridge A., Honda W., Kanehisa M. MIMOX: a web tool for phage display based epitope mapping. BMC Bioinform 2006, 7:451.
42. James K.J., Hancock M.A., Gagnon J.N., Coulton J.W. TonB Interacts with BtuF, the Escherichia coli periplasmic binding protein for cyanocobalamin. Biochemistry 2009, 48:9212-9220.
43. Jespers L.S., Messens J.H., De Keyser A., Eeckhout D., Van den Brande I., Gansemans Y.G., et al. Surface expression and ligand-based selection of cDNAs fused to filamentous phage gene VI. Biotechnology (NY) 1995, 13:378-382.
44. Kay B.K., Kasanov J., Yamabhai M. Screening phage-displayed combinatorial peptide libraries. Methods 2001, 24:240-246.
45. Kehoe J.W., Kay B.K. Filamentous phage display in the new millennium. Chem Rev 2005, 105:4056-4072.
46. Kiewitz A., Wolfes H. Mapping of protein-protein interactions between c-myb and its coactivator CBP by a new phage display technique. FEBS Lett 1997, 415:258-262.
47. Kitov P.I., Sadowska J.M., Mulvey G., Armstrong G.D., Ling H., Pannu N.S., et al. Shiga-like toxins are neutralized by tailored multivalent carbohydrate ligands. Nature 2000, 403:669-672.
48. Knittelfelder R., Riemer A.B., Jensen-Jarolim E. Mimotope vaccination-from allergy to cancer. Expert Opin Biol Ther 2009, 9:493-506.
49. Koide A., Wojcik J., Gilbreth R.N., Reichel A., Piehler J., Koide S. Accelerating phage-display library selection by reversible and site-specific biotinylation. Protein Eng Des Sel 2009, 22:685-690.
50. Koolpe M., Burgess R., Dail M., Pasquale E.B. EphB receptor-binding peptides identified by phage display enable design of an antagonist with ephrin-like affinity. J Biol Chem 2005, 280:17301-17311.
51. Lamboy J.A., Arter J.A., Knopp K.A., Der D., Overstreet C.M., Palermo E.F., et al. Phage wrapping with cationic polymers eliminates nonspecific binding between M13 phage and high pI target proteins. J Am Chem Soc 2009, 131:16454-16460.
52. Lane D.P., Stephen C.W. Epitope mapping using bacteriophage peptide libraries. Curr Opin Immunol 1993, 5:268-271.
53. Lehmann A. Ecallantide (DX-88), a plasma kallikrein inhibitor for the treatment of hereditary angioedema and the prevention of blood loss in on-pump cardiothoracic surgery. Expert Opin Biol Ther 2008, 8:1187-1199.
54. Li B., Xi H., Diehl L., Lee W.P., Sturgeon L., Chinn J., et al. Improving therapeutic efficacy of a complement receptor by structure-based affinity maturation. J Biol Chem 2009, 284:35605-35611.
55. Li W., Caberoy N.B. New perspective for phage display as an efficient and versatile technology of functional proteomics. Appl Microbiol Biotechnol 2009, 85:909-919.
56. Ling J., Liao H., Clark R., Wong M.S., Lo D.D. Structural constraints for the binding of short peptides to claudin-4 revealed by surface plasmon resonance. J Biol Chem 2008, 283:30585-30595.
57. Lowman H.B. Bacteriophage display and discovery of peptide leads for drug development. Annu Rev Biophys Biomol Struct 1997, 26:401-424.
58. Lunder M., Bratkovic T., Urleb U., Kreft S., Strukelj B. Ultrasound in phage display: a new approach to nonspecific elution. Biotechniques 2008, 44:893-900.
59. Maeda H., Sahara H., Mori Y., Torigo T., Kamiguchi K., Tamura Y., et al. Biological heterogeneity of the peptide-binding motif of the 70-kDa heat shock protein by surface plasmon resonance analysis. J Biol Chem 2007, 282:26956-26962.
60. Malik S., Ghosh M., Bonacci T.M., Tall G.G., Smrcka A.V. Ric-8 enhances G protein betagamma-dependent signaling in response to betagamma-binding peptides in intact cells. Mol Pharmacol 2005, 68:129-136.
61. Malmborg A.C., Duenas M., Ohlin M., Soderlind E., Borrebaeck C.A. Selection of binders from phage displayed antibody libraries using the BIAcore biosensor. J Immunol Methods 1996, 198:51-57.
62. Mandava S., Makowski L., Devarapalli S., Uzubell J., Rodi D.J. RELIC-a bioinformatics server for combinatorial peptide analysis and identification of protein-ligand interaction sites. Proteomics 2004, 4:1439-1460.
63. Marks C., Marks J.D. Phage libraries-a new route to clinically useful antibodies. N Engl J Med 1996, 335:730-733.
64. Marks J.D., Hoogenboom H.R., Bonnert T.P., McCafferty J., Griffiths A.D., Winter G. By-passing immunization. Human antibodies from V-gene libraries displayed on phage. J Mol Biol 1991, 222:581-597.
65. Matsubara T., Ishikawa D., Taki T., Okahata Y., Sato T. Selection of ganglioside GM1-binding peptides by using a phage library. FEBS Lett 1999, 456:253-256.
66. Matthews D.J., Wells J.A. Substrate phage: selection of protease substrates by monovalent phage display. Science 1993, 260:1113-1117.
67. Mayrose I., Shlomi T., Rubinstein N.D., Gershoni J.M., Ruppin E., Sharan R., et al. Epitope mapping using combinatorial phage-display libraries: a graph-based algorithm. Nucleic Acids Res 2007, 35:69-78.
68. Mcconnell S.J., Uveges A.J., Fowlkes D.M., Spinella D.G. Construction and screening of M13 phage libraries displaying long random peptides. Mol Divers 1996, 1:165-176.
69. Mcgregor D. Selection of proteins and peptides from libraries displayed on filamentous bacteriophage. Mol Biotechnol 1996, 6:155-162.
70. Mclafferty M.A., Kent R.B., Ladner R.C., Markland W. M13 bacteriophage displaying disulfide-constrained microproteins. Gene 1993, 128:29-36.
71. Molina-Lopez J., Sanschagrin F., Levesque R.C. A peptide inhibitor of MurA UDP-N-acetylglucosamine enolpyruvyl transferase: the first committed step in peptidoglycan biosynthesis. Peptides 2006, 27:3115-3121.
72. Molinkova D., Skladal P., Celer V. In vitro neutralization of equid herpesvirus 1 mediated by recombinant antibodies. J Immunol Methods 2008, 333:186-191.
73. Naz R.K. Status of contraceptive vaccines. Am J Reprod Immunol 2009, 61:11-18.
74. Newton J., Deutscher S.L. Phage peptide display. Handb Exp Pharmacol 2008, 145-163.
75. O'Neil K.T., Hoess R.H., Jackson S.A., Ramachandran N.S., Mousa S.A., DeGrado W.F. Identification of novel peptide antagonists for GPIIb/IIIa from a conformationally constrained phage peptide library. Proteins 1992, 14:509-515.
76. Pande J., Mallhi K.K., Grover A.K. A novel plasma membrane Ca(2+)-pump inhibitor: caloxin 1A1. Eur J Pharmacol 2005, 508:1-6.
77. Pande J., Mallhi K.K., Grover A.K. Role of third extracellular domain of plasma membrane Ca2+-Mg2+-ATPase based on the novel inhibitor caloxin 3A1. Cell Calcium 2005, 37:245-250.
78. Pande J., Mallhi K.K., Sawh A., Szewczyk M.M., Simpson F., Grover A.K. Aortic smooth muscle and endothelial plasma membrane Ca2+ pump isoforms are inhibited differently by the extracellular inhibitor caloxin 1b1. Am J Physiol Cell Physiol 2006, 290:C1341-C1349.
79. Pande J., Szewczyk M.M., Kuszczak I., Grover S., Escher E., Grover A.K. Functional effects of caloxin 1c2, a novel engineered selective inhibitor of plasma membrane Ca(2+)-pump isoform 4, on coronary artery. J Cell Mol Med 2008, 12:1049-1060.
80. Paradis-Bleau C., Beaumont M., Boudreault L., Lloyd A., Sanschagrin F., Bugg T.D., et al. Selection of peptide inhibitors against the Pseudomonas aeruginosa MurD cell wall enzyme. Peptides 2006, 27:1693-1700.
81. Paradis-Bleau C., Lloyd A., Sanschagrin F., Clarke T., Blewett A., Bugg T.D., et al. Phage display-derived inhibitor of the essential cell wall biosynthesis enzyme MurF. BMC Biochem 2008, 9:33.
82. Paradis-Bleau C., Lloyd A., Sanschagrin F., Maaroufi H., Clarke T., Blewett A., et al. Pseudomonas aeruginosa MurE amide ligase: enzyme kinetics and peptide inhibitor. Biochem J 2009, 421:263-272.
83. Park J.P., Cropek D.M., Banta S. High affinity peptides for the recognition of the heart disease biomarker troponin I identified using phage display. Biotechnol Bioeng 2009, 105:678-686.
84. Paschke M. Phage display systems and their applications. Appl Microbiol Biotechnol 2006, 70:2-11.
85. Pershad K., Pavlovic J.D., Graslund S., Nilsson P., Colwill K., Karatt-Vellatt A., et al. Generating a panel of highly specific antibodies to 20 human SH2 domains by phage display. Protein Eng Des Sel 2010, 4:279-288.
86. Philibert P., Stoessel A., Wang W., Sibler A.P., Bec N., Larroque C., et al. A focused antibody library for selecting scFvs expressed at high levels in the cytoplasm. BMC Biotechnol 2007, 7:81.
87. Pini A., Bracci L. Phage display of antibody fragments. Curr Protein Pept Sci 2000, 1:155-169.
88. Ponsard I., Galleni M., Soumillion P., Fastrez J. Selection of metalloenzymes by catalytic activity using phage display and catalytic elution. Chembiochem 2001, 2:253-259.
89. Ratnikov B., Cieplak P., Smith J.W. High throughput substrate phage display for protease profiling. Methods Mol Biol 2009, 539:93-114.
90. Rodi D.J., Janes R.W., Sanganee H.J., Holton R.A., Wallace B.A., Makowski L. Screening of a library of phage-displayed peptides identifies human bcl-2 as a taxol-binding protein. J Mol Biol 1999, 285:197-203.
91. Sandman K.E., Tardiff D.F., Neely L.A., Noren C.J. Revised Escherichia coli selenocysteine insertion requirements determined by in vivo screening of combinatorial libraries of SECIS variants. Nucleic Acids Res 2003, 31:2234-2241.
92. Sblattero D., Bradbury A. Exploiting recombination in single bacteria to make large phage antibody libraries. Nat Biotechnol 2000, 18:75-80.
93. Sche P.P., Mckenzie K.M., White J.D., Austin D.J. Display cloning: functional identification of natural product receptors using cDNA-phage display. Chem Biol 1999, 6:707-716.
94. Schumacher T.N., Mayr L.M., Minor D.L., Milhollen M.A., Burgess M.W., Kim P.S. Identification of D-peptide ligands through mirror-image phage display. Science 1996, 271:1854-1857.
95. Scott J.K., Smith G.P. Searching for peptide ligands with an epitope library. Science 1990, 249:386-390.
96. Sidhu S.S. Phage display in pharmaceutical biotechnology. Curr Opin Biotechnol 2000, 11:610-616.
97. Smith G.P. Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 1985, 228:1315-1317.
98. Smith G.P., Petrenko V.A. Phage Display. Chem Rev 1997, 97:391-410.
99. Smith G.P., Scott J.K. Libraries of peptides and proteins displayed on filamentous phage. Methods Enzymol 1993, 217:228-257.
100. Stephen C.W., Helminen P., Lane D.P. Characterisation of epitopes on human p53 using phage-displayed peptide libraries: insights into antibody-peptide interactions. J Mol Biol 1995, 248:58-78.
101. Sternberg N., Hamilton D. Bacteriophage P1 site-specific recombination. I. Recombination between loxP sites. J Mol Biol 1981, 150:467-486.
102. Takakusagi Y., Takakusagi K., Kuramochi K., Kobayashi S., Sugawara F., Sakaguchi K. Identification of C10 biotinylated camptothecin (CPT-10-B) binding peptides using T7 phage display screen on a QCM device. Bioorg Med Chem 2007, 15:7590-7598.
103. Thie H., Voedisch B., Dubel S., Hust M., Schirrmann T. Affinity maturation by phage display. Methods Mol Biol 2009, 525:309-322.
104. Tian F., Tsao M.L., Schultz P.G. A phage display system with unnatural amino acids. J Am Chem Soc 2004, 126:15962-15963.
105. van Houten N.E., Zwick M.B., Menendez A., Scott J.K. Filamentous phage as an immunogenic carrier to elicit focused antibody responses against a synthetic peptide. Vaccine 2006, 24:4188-4200.
106. Vanwetswinkel S., Avalle B., Fastrez J. Selection of beta-lactamases and penicillin binding mutants from a library of phage displayed TEM-1 beta-lactamase randomly mutated in the active site omega-loop. J Mol Biol 2000, 295:527-540.
107. Verhaert R.M., Beekwilder J., Olsthoorn R., Duin J., Quax W.J. Phage display selects for amylases with improved low pH starch-binding. J Biotechnol 2002, 96:103-118.
108. von Schantz L., Gullfot F., Scheer S., Filonova L., Cicortas G.L., Flint J.E., et al. Affinity maturation generates greatly improved xyloglucan-specific carbohydrate binding modules. BMC Biotechnol 2009, 9:92.
109. Voss M., Lettau M., Janssen O. Identification of SH3 domain interaction partners of human FasL (CD178) by phage display screening. BMC Immunol 2009, 10:53.
110. Wang L.F., Yu M. Epitope mapping using phage-display random fragment libraries. Methods Mol Biol 2009, 524:315-332.
111. Waterhouse P., Griffiths A.D., Johnson K.S., Winter G. Combinatorial infection and in vivo recombination: a strategy for making large phage antibody repertoires. Nucleic Acids Res 1993, 21:2265-2266.
112. Watkins N.A., Ouwehand W.H. Introduction to antibody engineering and phage display. Vox Sang 2000, 78:72-79.
113. Williams A., Baird L.G. DX-88 and HAE: a developmental perspective. Transfus Apher Sci 2003, 29:255-258.
114. Williamson P., Matthews R. Development of neutralising human recombinant antibodies to pertussis toxin. FEMS Immunol Med Microbiol 1999, 23:313-319.
115. Woiwode T.F., Haggerty J.E., Katz R., Gallop M.A., Barrett R.W., Dower W.J., et al. Synthetic compound libraries displayed on the surface of encoded bacteriophage. Chem Biol 2003, 10:847-858.
116. Zhang M.Y., Dimitrov D.S. Sequential antigen panning for selection of broadly cross-reactive HIV-1-neutralizing human monoclonal antibodies. Methods Mol Biol 2009, 562:143-154.
117. Zhikui L., Changcun G., Yongzhan N., Fengtian H, Xingling R., Shujun L., et al. Screening and identification of recombinant anti-idiotype antibodies against gastric cancer and colon cancer monoclonal antibodies by a phage-displayed single-chain variable fragment library. J Biomol Screen 2010, 15:308-313.
118. Zhou Y, Marks J.D. Identification of target and function specific antibodies for effective drug delivery. Methods Mol Biol 2009, 525:145-160.