Evolution of phage display technology: from discovery to application

Abstract Phage display technology as a selection-based system is an attractive method for evolution of new biological drugs. Unique ability of phage libraries for displaying proteins on bacteriophage surfaces enable them to make a major contribution in diverse fields of researches related to the diagnosis and therapy of diseases. One of the great challenges facing researchers is the modification of phage display technology and the development of new applications. This article reviews the molecular basis of phage display library, and summarizes the novel and specific applications of this technique in the field of biological drugs development including therapeutic antibodies, peptides, vaccines, and catalytic antibodies.

[1]  A M Lesk,et al.  Structural repertoire of the human VH segments. , 1992, Journal of molecular biology.

[2]  G. P. Smith,et al.  Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. , 1985, Science.

[3]  N. Tikunova,et al.  Phage Display on the Base of Filamentous Bacteriophages: Application for Recombinant Antibodies Selection , 2009, Acta naturae.

[4]  L. Goulart,et al.  Theranostic applications of phage display to control leishmaniasis: selection of biomarkers for serodiagnostics, vaccination, and immunotherapy. , 2015, Revista da Sociedade Brasileira de Medicina Tropical.

[5]  R. Massey,et al.  Catalytic hydrolysis of vasoactive intestinal peptide by human autoantibody , 1989, Regulatory Peptides.

[6]  J. George,et al.  AMG 531, a thrombopoiesis-stimulating protein, for chronic ITP. , 2006, The New England journal of medicine.

[7]  Andrew D. Griffiths,et al.  By–Passing Immunization: Building High Affinity Human Antibodies by Chain Shuffling , 1992, Bio/Technology.

[8]  A. Gargouri,et al.  Biocatalysts: beautiful creatures. , 2012, Biochemical and biophysical research communications.

[9]  K. Janda,et al.  Identification and characterization of single chain anti-cocaine catalytic antibodies. , 2007, Journal of molecular biology.

[10]  Use of Phage Display technology in development of canine visceral leishmaniasis vaccine using synthetic peptide trapped in sphingomyelin/cholesterol liposomes , 2015, Parasites & Vectors.

[11]  D R Burton,et al.  In vitro evolution of a neutralizing human antibody to human immunodeficiency virus type 1 to enhance affinity and broaden strain cross-reactivity. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Simon J. Henderson,et al.  Monoclonal antibody therapeutics: history and future. , 2012, Current opinion in pharmacology.

[13]  D. Landry,et al.  Anti-Cocaine Catalytic Antibodies: A Synthetic Approach to Improved Antibody Diversity. , 1996 .

[14]  L. Riechmann,et al.  The C-Terminal Domain of TolA Is the Coreceptor for Filamentous Phage Infection of E. coli , 1997, Cell.

[15]  Daqing Yang,et al.  Peptide mimics of peptidoglycan are vaccine candidates and protect mice from infection with Staphylococcus aureus. , 2011, Journal of medical microbiology.

[16]  A. Limaye,et al.  Invasive Pseudomonas aeruginosa infections: high rate of recurrence and mortality after hematopoietic cell transplantation , 2007, Bone Marrow Transplantation.

[17]  O. Favorova,et al.  Catalytic Antibodies: New Characters in the Protein Repertoire , 2002 .

[18]  S. Bishop-Hurley,et al.  Phage-displayed peptides selected for binding to Campylobacter jejuni are antimicrobial. , 2010, Protein engineering, design & selection : PEDS.

[19]  I. Tomlinson,et al.  Antibody fragments from a ‘single pot’ phage display library as immunochemical reagents. , 1994, The EMBO journal.

[20]  Mingshi Yang,et al.  Novel Formulation Approaches for Peptide and Protein Injectables , 2009 .

[21]  J. Berzofsky,et al.  Phase I Study of GC1008 (Fresolimumab): A Human Anti-Transforming Growth Factor-Beta (TGFβ) Monoclonal Antibody in Patients with Advanced Malignant Melanoma or Renal Cell Carcinoma , 2014, PloS one.

[22]  P. T. Jones,et al.  Isolation of high affinity human antibodies directly from large synthetic repertoires. , 1994, The EMBO journal.

[23]  G. Winter,et al.  Mimicking somatic hypermutation: affinity maturation of antibodies displayed on bacteriophage using a bacterial mutator strain. , 1996, Journal of molecular biology.

[24]  J. Mach,et al.  New inhibitors of Helicobacter pylori urease holoenzyme selected from phage-displayed peptide libraries. , 1999, European journal of biochemistry.

[25]  Hennie R. Hoogenboom,et al.  Guiding the Selection of Human Antibodies from Phage Display Repertoires to a Single Epitope of an Antigen , 1994, Bio/Technology.

[26]  A. Malmborg,et al.  The Phage Infection Process: a Functional Role for the Distal Linker Region of Bacteriophage Protein 3 , 2000, Journal of Virology.

[27]  J. Tabernero,et al.  Necitumumab, a fully human IgG1 mAb directed against the EGFR for the potential treatment of cancer. , 2010, Current opinion in investigational drugs.

[28]  P. Tak,et al.  MOR103, a human monoclonal antibody to granulocyte–macrophage colony-stimulating factor, in the treatment of patients with moderate rheumatoid arthritis: results of a phase Ib/IIa randomised, double-blind, placebo-controlled, dose-escalation trial , 2014, Annals of the rheumatic diseases.

[29]  N. Peppas,et al.  Is the oral route possible for peptide and protein drug delivery? , 2006, Drug discovery today.

[30]  K. Duan,et al.  Protective efficacy of a peptide derived from a potential adhesin of Pseudomonas aeruginosa against corneal infection. , 2016, Experimental eye research.

[31]  E. H. Cohen,et al.  Generation of high-affinity human antibodies by combining donor-derived and synthetic complementarity-determining-region diversity , 2005, Nature Biotechnology.

[32]  N. Mishra,et al.  Catalytic antibodies as potential therapeutics , 2009 .

[33]  P. Carter,et al.  Alternative molecular formats and therapeutic applications for bispecific antibodies. , 2015, Molecular immunology.

[34]  M. Rothenberg,et al.  Inhibition of human interleukin‐13‐induced respiratory and oesophageal inflammation by anti‐human‐interleukin‐13 antibody (CAT‐354) , 2005, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[35]  Iftach Yacoby,et al.  Targeting Antibacterial Agents by Using Drug-Carrying Filamentous Bacteriophages , 2006, Antimicrobial Agents and Chemotherapy.

[36]  J. Fastrez,et al.  Phage display as a tool for the directed evolution of enzymes. , 2003, Trends in biotechnology.

[37]  K. Kelly,et al.  Phase 2 study of mapatumumab, a fully human agonistic monoclonal antibody which targets and activates the TRAIL receptor-1, in patients with advanced non-small cell lung cancer. , 2008, Lung cancer.

[38]  D. Landry,et al.  A catalytic antibody against cocaine prevents cocaine's reinforcing and toxic effects in rats. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[39]  D. Marvin,et al.  Structure of the capsid of Pf3 filamentous phage determined from X-ray fibre diffraction data at 3.1 A resolution. , 1998, Journal of molecular biology.

[40]  P. Michetti,et al.  Vaccination against Helicobacter pylori - an old companion of man , 2001, Expert opinion on biological therapy.

[41]  L. Pauling.  Antibodies and specific biological forces. , 1948, Endeavour.

[42]  B. Shen,et al.  A novel peptide isolated from phage library to substitute a complex system for a vaccine against staphylococci infection. , 2006, Vaccine.

[43]  Dirk Ponsel,et al.  High Affinity, Developability and Functional Size: The Holy Grail of Combinatorial Antibody Library Generation , 2011, Molecules.

[44]  R. Stahel,et al.  Human agonistic TRAIL receptor antibodies Mapatumumab and Lexatumumab induce apoptosis in malignant mesothelioma and act synergistically with cisplatin , 2007, Molecular Cancer.

[45]  R. E. Webster.  CHAPTER 1 – Biology of the Filamentous Bacteriophage , 1996 .

[46]  Ishtiaq Qadri,et al.  Bacteriophages and their implications on future biotechnology: a review , 2012, Virology Journal.

[47]  M. Fanger,et al.  Bispecific antibodies. , 1992, Critical reviews in immunology.

[48]  M. Rowley,et al.  Phage display for epitope determination: a paradigm for identifying receptor-ligand interactions. , 2004, Biotechnology annual review.

[49]  A. Pini,et al.  Design and Use of a Phage Display Library , 1998, The Journal of Biological Chemistry.

[50]  A. Kimball,et al.  Safety and efficacy of ABT-874, a fully human interleukin 12/23 monoclonal antibody, in the treatment of moderate to severe chronic plaque psoriasis: results of a randomized, placebo-controlled, phase 2 trial. , 2008, Archives of dermatology.

[51]  B. Blagoev,et al.  Agonism and Antagonism at the Insulin Receptor , 2012, PloS one.

[52]  Chien-Hsun Wu,et al.  Advancement and applications of peptide phage display technology in biomedical science , 2016, Journal of Biomedical Science.

[53]  N. Ponomarenko,et al.  Creation of catalytic antibodies metabolizing organophosphate compounds , 2012, Biochemistry (Moscow).

[54]  D. Ray,et al.  Replication of bacteriophage M13. II. The role of replicative forms in single-strand synthesis. , 1969, Journal of molecular biology.

[55]  R. Lock,et al.  Cell-division inhibitors: new insights for future antibiotics , 2008, Nature Reviews Drug Discovery.

[56]  Helen X. Chen,et al.  A phase II study of cixutumumab (IMC-A12, NSC742460) in advanced hepatocellular carcinoma. , 2014, Journal of hepatology.

[57]  H R Hoogenboom,et al.  By-passing immunization. Human antibodies from V-gene libraries displayed on phage. , 1991, Journal of molecular biology.

[58]  G. Oster,et al.  Theoretical studies of clonal selection: minimal antibody repertoire size and reliability of self-non-self discrimination. , 1979, Journal of theoretical biology.

[59]  V. Sperandio,et al.  Anti-virulence strategies to combat bacteria-mediated disease , 2010, Nature Reviews Drug Discovery.

[60]  W. Jencks.  Catalysis in chemistry and enzymology , 1969 .

[61]  P. Appelbaum.  Microbiology of antibiotic resistance in Staphylococcus aureus. , 2007, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[62]  D. Eeckhout,et al.  Surface Expression and Ligand-Based Selection of cDNAs Fused to Filamentous Phage Gene VI , 1995, Bio/Technology.

[63]  McGraw-Hill, New York. , 2022 .

[64]  A. Friboulet,et al.  Catalytic antibodies and their applications in biotechnology: state of the art , 2014, Biotechnology Letters.

[65]  Wang Jing-lin,et al.  In vitro selection and evolution of functional proteins by using ribosome display , 2003 .

[66]  H R Hoogenboom,et al.  By-passing immunisation. Human antibodies from synthetic repertoires of germline VH gene segments rearranged in vitro. , 1992, Journal of molecular biology.

[67]  Samuel I. Miller,et al.  Use of Phage Display To Identify Potential Pseudomonas aeruginosa Gene Products Relevant to Early Cystic Fibrosis Airway Infections , 2005, Infection and Immunity.

[68]  D R Burton,et al.  CDR walking mutagenesis for the affinity maturation of a potent human anti-HIV-1 antibody into the picomolar range. , 1995, Journal of molecular biology.

[69]  E. Zorrilla,et al.  Catalytic antibody degradation of ghrelin increases whole-body metabolic rate and reduces refeeding in fasting mice , 2008, Proceedings of the National Academy of Sciences.

[70]  R. Herbst,et al.  Safety, pharmacokinetics, and antitumor activity of AMG 386, a selective angiopoietin inhibitor, in adult patients with advanced solid tumors. , 2009, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[71]  Paul J Conroy,et al.  A tale of two specificities: bispecific antibodies for therapeutic and diagnostic applications , 2013, Trends in Biotechnology.

[72]  Tristan J. Vaughan,et al.  Human Antibodies with Sub-nanomolar Affinities Isolated from a Large Non-immunized Phage Display Library , 1996, Nature Biotechnology.

[73]  S. Bishop-Hurley,et al.  Development of Anti-Infectives Using Phage Display: Biological Agents against Bacteria, Viruses, and Parasites , 2012, Antimicrobial Agents and Chemotherapy.

[74]  Yamei Gao,et al.  Identification and evaluation of a novel peptide binding to the cell surface of Staphylococcus aureus. , 2013, Microbiological research.

[75]  Antibody Proteases: Induction of Catalytic Response , 2002, Biochemistry (Moscow).

[76]  V. Buneva,et al.  Antibodies from the sera of HIV‐infected patients efficiently hydrolyze all human histones , 2016, Journal of molecular recognition : JMR.

[77]  N. Haigwood,et al.  New recombinant vaccines based on the use of prokaryotic antigen-display systems , 2004, Expert review of vaccines.

[78]  N. Dunn,et al.  Genetic organization and functional analysis of a novel phage abortive infection system, AbiL, from Lactococcus lactis. , 1999, Journal of biotechnology.

[79]  Hennie R. Hoogenboom,et al.  A Large Non-immunized Human Fab Fragment Phage Library That Permits Rapid Isolation and Kinetic Analysis of High Affinity Antibodies* , 1999, The Journal of Biological Chemistry.

[80]  F. Panza,et al.  Monoclonal antibodies against β-amyloid (Aβ) for the treatment of Alzheimer's disease: the Aβ target at a crossroads , 2011, Expert opinion on biological therapy.

[81]  G. Bodey,et al.  Infections caused by Pseudomonas aeruginosa. , 1983, Reviews of infectious diseases.

[82]  W. Wickner.  Asymmetric orientation of phage M13 coat protein in Escherichia coli cytoplasmic membranes and in synthetic lipid vesicles. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[83]  P. Model,et al.  Location of filamentous phage minor coat proteins in phage and in infected cells. , 1995, Journal of molecular biology.

[84]  Igor Fisch,et al.  Selection of Human Single Chain Fv Antibody Fragments Binding and Inhibiting Helicobacter pylori Urease , 2000, Tumor Biology.

[85]  A. Maranhão,et al.  Antibody Phage Display Libraries: Contributions to Oncology , 2012, International journal of molecular sciences.

[86]  Benjamin Wu,et al.  Pharmacokinetics of Peptide-Fc fusion proteins. , 2014, Journal of pharmaceutical sciences.

[87]  Kobra Omidfar,et al.  Advances in phage display technology for drug discovery , 2015, Expert opinion on drug discovery.

[88]  Hai Yu,et al.  In vitro affinity maturation and characterization of anti-P24 antibody for HIV diagnostic assay. , 2015, Journal of biochemistry.

[89]  D. Menezes-Souza,et al.  Mimotope-Based Vaccines of Leishmania infantum Antigens and Their Protective Efficacy against Visceral Leishmaniasis , 2014, PloS one.

[90]  R. Lerner,et al.  Making artificial antibodies: a format for phage display of combinatorial heterodimeric arrays. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[91]  Jane Wilton,et al.  The remarkable flexibility of the human antibody repertoire; isolation of over one thousand different antibodies to a single protein, BLyS. , 2003, Journal of molecular biology.

[92]  G. Winter,et al.  Combinatorial infection and in vivo recombination: a strategy for making large phage antibody repertoires. , 1993, Nucleic acids research.

[93]  M. Waldor,et al.  Filamentous phage integration requires the host recombinases XerC and XerD , 2002, Nature.

[94]  C. Van de Wiele,et al.  Quality specifications for peptide drugs: a regulatory‐pharmaceutical approach , 2009, Journal of peptide science : an official publication of the European Peptide Society.

[95]  G. Winter,et al.  Selection of phage antibodies by binding affinity. Mimicking affinity maturation. , 1992, Journal of molecular biology.

[96]  Gnanasambandan Ramanathan,et al.  Renin gene rs1464816 polymorphism contributes to chronic kidney disease progression in ADPKD , 2016, Journal of Biomedical Science.

[97]  C. Kummerfeldt,et al.  Raxibacumab: potential role in the treatment of inhalational anthrax , 2014, Infection and drug resistance.

[98]  J. Molina-López,et al.  A peptide inhibitor of MurA UDP-N-acetylglucosamine enolpyruvyl transferase: The first committed step in peptidoglycan biosynthesis , 2006, Peptides.

[99]  Franklin Peale,et al.  Variants of the Antibody Herceptin That Interact with HER2 and VEGF at the Antigen Binding Site , 2009, Science.

[100]  J. Arends,et al.  Selection of Recombinant, Library-Derived Antibody Fragments against p24 for Human Immunodeficiency Virus Type 1 Diagnostics , 1998, Clinical Diagnostic Laboratory Immunology.

[101]  D. Landry,et al.  Antibody-catalyzed degradation of cocaine. , 1993, Science.

[102]  P. Hofschneider,et al.  M 13 BACTERIOPHAGE LIBERATION FROM INTACT BACTERIA AS REVEALED BY ELECTRON MICROSCOPY. , 1963, Journal of molecular biology.

[103]  S. Dübel,et al.  Mating antibody phage display with proteomics. , 2004, Trends in biotechnology.

[104]  R. Perham,et al.  Multiple display of foreign peptides on a filamentous bacteriophage. Peptides from Plasmodium falciparum circumsporozoite protein as antigens. , 1991, Journal of molecular biology.

[105]  P G Schultz,et al.  Selective chemical catalysis by an antibody. , 1986, Science.

[106]  T. Hoffmann,et al.  Peptide therapeutics: current status and future directions. , 2015, Drug discovery today.