Landscape Phage: Evolution from Phage Display to Nanobiotechnology

The development of phage engineering technology has led to the construction of a novel type of phage display library—a collection of nanofiber materials with diverse molecular landscapes accommodated on the surface of phage particles. These new nanomaterials, called the “landscape phage”, serve as a huge resource of diagnostic/detection probes and versatile construction materials for the preparation of phage-functionalized biosensors and phage-targeted nanomedicines. Landscape-phage-derived probes interact with biological threat agents and generate detectable signals as a part of robust and inexpensive molecular recognition interfaces introduced in mobile detection devices. The use of landscape-phage-based interfaces may greatly improve the sensitivity, selectivity, robustness, and longevity of these devices. In another area of bioengineering, landscape-phage technology has facilitated the development and testing of targeted nanomedicines. The development of high-throughput phage selection methods resulted in the discovery of a variety of cancer cell-associated phages and phage proteins demonstrating natural proficiency to self-assemble into various drug- and gene-targeting nanovehicles. The application of this new “phage-programmed-nanomedicines” concept led to the development of a number of cancer cell-targeting nanomedicine platforms, which demonstrated anticancer efficacy in both in vitro and in vivo experiments. This review was prepared to attract the attention of chemical scientists and bioengineers seeking to develop functionalized nanomaterials and use them in different areas of bioscience, medicine, and engineering.

[1]  P. Král,et al.  Structure and dynamics of highly PEG-ylated sterically stabilized micelles in aqueous media. , 2011, Journal of the American Chemical Society.

[2]  Hongwei Song,et al.  Selective photothermal therapy for breast cancer with targeting peptide modified gold nanorods. , 2012, Dalton transactions.

[3]  Phage Display for Generating Peptide Reagents , 2008, Current protocols in protein science.

[4]  G. Weiss,et al.  Virus-Enabled Biosensor for Human Serum Albumin. , 2017, Analytical chemistry.

[5]  L. Sandakhchiev,et al.  [Production of a viable variant of the M13 phage with a foreign peptide inserted into the basic coat protein]. , 1989, Doklady Akademii nauk SSSR.

[6]  James D. Watson,et al.  Phage and the origins of molecular biology : the centennial edition , 2007 .

[7]  G. Cesareni,et al.  Modifying filamentous phage capsid: limits in the size of the major capsid protein. , 1995, Journal of molecular biology.

[8]  Tao Wang,et al.  Paclitaxel-loaded polymeric micelles modified with MCF-7 cell-specific phage protein: enhanced binding to target cancer cells and increased cytotoxicity. , 2010, Molecular pharmaceutics.

[9]  Valery A Petrenko,et al.  Detection of biological threats. A challenge for directed molecular evolution. , 2004, Journal of microbiological methods.

[10]  I-Hsuan Chen,et al.  Landscape phage probes for Salmonella typhimurium. , 2005, Journal of microbiological methods.

[11]  V. Petrenko,et al.  Promiscuous tumor targeting phage proteins. , 2016, Protein engineering, design & selection : PEDS.

[12]  Srinivas Sista,et al.  Highly sensitive phage-based biosensor for the detection of β-galactosidase , 2007 .

[13]  V. Petrenko,et al.  A Label-Free Electrochemical Impedance Cytosensor Based on Specific Peptide-Fused Phage Selected from Landscape Phage Library , 2016, Scientific Reports.

[14]  V. Petrenko,et al.  Magnetostrictive Microcantilever as an Advanced Transducer for Biosensors , 2007, Sensors.

[15]  V. Petrenko,et al.  Targeted delivery of siRNA into breast cancer cells via phage fusion proteins. , 2013, Molecular pharmaceutics.

[16]  A M Eroshkin,et al.  Mutations in fd phage major coat protein modulate affinity of the displayed peptide. , 2009, Protein engineering, design & selection : PEDS.

[17]  Structure of a foreign peptide displayed on the surface of bacteriophage M13. , 1994, Journal of molecular biology.

[18]  V. Petrenko,et al.  Bio-mimetic Nanostructure Self-assembled from Au@Ag Heterogeneous Nanorods and Phage Fusion Proteins for Targeted Tumor Optical Detection and Photothermal Therapy , 2014, Scientific Reports.

[19]  J. Marvin,et al.  Antibody Humanization and Affinity Maturation Using Phage Display , 2005 .

[20]  V. Petrenko,et al.  Diversity and censoring of landscape phage libraries. , 2009, Protein engineering, design & selection : PEDS.

[21]  Tao Wang,et al.  Cytoplasmic delivery of liposomes into MCF-7 breast cancer cells mediated by cell-specific phage fusion coat protein. , 2010, Molecular pharmaceutics.

[22]  Bernard R. Glick,et al.  Molecular biotechnology : principles and applications ofrecombinant DNA , 2010 .

[23]  V. Petrenko,et al.  Paradigm shift in bacteriophage-mediated delivery of anticancer drugs: from targeted ‘magic bullets’ to self-navigated ‘magic missiles’ , 2017, Expert opinion on drug delivery.

[24]  V. Petrenko,et al.  Phages from landscape libraries as substitute antibodies. , 2000, Protein engineering.

[25]  Dong-Joo Kim,et al.  Phage immobilized magnetoelastic sensor for the detection of Salmonella typhimurium. , 2007, Journal of microbiological methods.

[26]  Tao Wang,et al.  On the mechanism of targeting of phage fusion protein-modified nanocarriers: only the binding peptide sequence matters. , 2011, Molecular pharmaceutics.

[27]  R. Perham,et al.  Factors limiting display of foreign peptides on the major coat protein of filamentous bacteriophage capsids and a potential role for leader peptidase , 1998, FEBS letters.

[28]  V. Petrenko,et al.  Identifying Diagnostic Peptides for Lyme Disease through Epitope Discovery , 2001, Clinical Diagnostic Laboratory Immunology.

[29]  W. H. Gaylord Molecular Biology of Bacterial Viruses , 1964, The Yale Journal of Biology and Medicine.

[30]  S. Sidhu Phage display in biotechnology and drug discovery , 2005 .

[31]  Tao Wang,et al.  Enhanced binding and killing of target tumor cells by drug-loaded liposomes modified with tumor-specific phage fusion coat protein. , 2010, Nanomedicine.

[32]  S. Sillankorva,et al.  Bacteriophage Therapy , 2018, Methods in Molecular Biology.

[33]  V. Petrenko,et al.  Paclitaxel-Loaded PEG-PE–Based Micellar Nanopreparations Targeted with Tumor-Specific Landscape Phage Fusion Protein Enhance Apoptosis and Efficiently Reduce Tumors , 2014, Molecular Cancer Therapeutics.

[34]  V. Petrenko,et al.  Landscape phages and their fusion proteins targeted to breast cancer cells. , 2012, Protein engineering, design & selection : PEDS.

[35]  I-Hsuan Chen,et al.  Affinity-selected filamentous bacteriophage as a probe for acoustic wave biodetectors of Salmonella typhimurium. , 2006, Biosensors & bioelectronics.

[36]  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.

[37]  R. Perham,et al.  New vectors for peptide display on the surface of filamentous bacteriophage. , 1996, Gene.

[38]  Valery A Petrenko,et al.  Phage display for detection of biological threat agents. , 2003, Journal of microbiological methods.

[39]  Bryan A. Chin,et al.  Detection of Bacillus anthracis spores in liquid using phage-based magnetoelastic micro-resonators , 2007 .

[40]  C Nave,et al.  Molecular models and structural comparisons of native and mutant class I filamentous bacteriophages Ff (fd, f1, M13), If1 and IKe. , 1994, Journal of molecular biology.

[41]  D. Marvin,et al.  Role of capsid structure and membrane protein processing in determining the size and copy number of peptides displayed on the major coat protein of filamentous bacteriophage. , 1996, Journal of molecular biology.

[42]  V. Petrenko,et al.  Vectors and Modes of Display , 2005 .

[43]  L. Castagnoli,et al.  Construction, Exploitation and Evolution of a New Peptide Library Displayed at High Density by Fusion to the Major Coat Protein of Filamentous Phage , 1997, Biological chemistry.

[44]  Jamie K. Scott,et al.  Beyond phage display: non-traditional applications of the filamentous bacteriophage as a vaccine carrier, therapeutic biologic, and bioconjugation scaffold , 2015, Front. Microbiol..

[45]  J. Fastrez,et al.  Construction and exploitation in model experiments of functional selection of a landscape library expressed from a phagemid. , 2002, Gene.

[46]  Carlos F. Barbas,et al.  Phage display: a Laboratory manual , 2014 .

[47]  V. Petrenko,et al.  Delivery of siRNA into breast cancer cells via phage fusion protein-targeted liposomes. , 2011, Nanomedicine : nanotechnology, biology, and medicine.

[48]  V. Petrenko,et al.  Diagnostic probes for Bacillus anthracis spores selected from a landscape phage library. , 2004, Clinical chemistry.

[49]  Frederic A. Fellouse,et al.  Methods for the construction of phage-displayed libraries , 2005 .

[50]  V. Petrenko,et al.  Combinatorial synthesis and screening of cancer cell-specific nanomedicines targeted via phage fusion proteins , 2015, Front. Microbiol..

[51]  T. Clackson,et al.  Making antibody fragments using phage display libraries , 1991, Nature.

[52]  G. P. Smith,et al.  A new filamentous phage cloning vector: fd-tet. , 1980, Gene.

[53]  G. Winter,et al.  Phage antibodies: filamentous phage displaying antibody variable domains , 1990, Nature.

[54]  Valery A Petrenko,et al.  Gold nanoprobe functionalized with specific fusion protein selection from phage display and its application in rapid, selective and sensitive colorimetric biosensing of Staphylococcus aureus. , 2016, Biosensors & bioelectronics.

[55]  F. Felici,et al.  Selection of antibody ligands from a large library of oligopeptides expressed on a multivalent exposition vector. , 1991, Journal of molecular biology.

[56]  Valery A Petrenko,et al.  Phage as a molecular recognition element in biosensors immobilized by physical adsorption. , 2007, Biosensors & bioelectronics.

[57]  F. Felici,et al.  Uptake and intracellular fate of phage display vectors in mammalian cells. , 1999, Biochimica et biophysica acta.

[58]  V. Petrenko,et al.  Double-targeted polymersomes and liposomes for multiple barrier crossing. , 2016, International journal of pharmaceutics.

[59]  I-Hsuan Chen,et al.  Phage-Based Magnetoelastic Wireless Biosensors for Detecting Bacillus Anthracis Spores , 2007, IEEE Sensors Journal.

[60]  Y. Kan,et al.  Antibodies to human fetal erythroid cells from a nonimmune phage antibody library , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[61]  V. Petrenko,et al.  Selection of Lung Cancer-Specific Landscape Phage for Targeted Drug Delivery. , 2016, Combinatorial chemistry & high throughput screening.

[62]  G. Stent,et al.  Phage and the Origins of Molecular Biology , 2000 .

[63]  H. J. Baker,et al.  Cell targeted phagemid rescued by preselected landscape phage. , 2004, Gene.

[64]  V. Petrenko,et al.  Humoral immune responses against gonadotropin releasing hormone elicited by immunization with phage-peptide constructs obtained via phage display. , 2015, Journal of biotechnology.

[65]  Tao Wang,et al.  In vitro optimization of liposomal nanocarriers prepared from breast tumor cell specific phage fusion protein , 2011, Journal of drug targeting.

[66]  V. Petrenko,et al.  Landscape phage fusion protein-mediated targeting of nanomedicines enhances their prostate tumor cell association and cytotoxic efficiency. , 2010, Nanomedicine : nanotechnology, biology, and medicine.

[67]  V. Petrenko,et al.  Peptide microarray with ligands at high density based on symmetrical carrier landscape phage for detection of cellulase. , 2014, Analytical chemistry.

[68]  V. Petrenko,et al.  Sensitive colorimetric immunoassay of Vibrio parahaemolyticus based on specific nonapeptide probe screening from a phage display library conjugated with MnO2 nanosheets with peroxidase-like activity. , 2018, Nanoscale.

[69]  V. Petrenko,et al.  Design of specific immunogens using filamentous phage as the carrier. , 1993, Gene.

[70]  T. S. Lim,et al.  Phage Display , 2018, Methods in Molecular Biology.

[71]  G. P. Smith,et al.  A library of organic landscapes on filamentous phage. , 1996, Protein engineering.

[72]  V. Petrenko,et al.  Phage display selection of peptides that affect prostate carcinoma cells attachment and invasion , 2001, The Prostate.

[73]  R. Ladner,et al.  Design, construction and function of a multicopy display vector using fusions to the major coat protein of bacteriophage M13. , 1991, Gene.

[74]  E. Kaestner Vectors: a survey of molecular cloning vectors and their uses. , 1988, Biotechnology.

[75]  G. P. Smith,et al.  Alpha-helically constrained phage display library. , 2002, Protein engineering.

[76]  Phage Libraries for Developing Antibody-Targeted Diagnostics and Vaccines , 2005 .

[77]  T. Lu,et al.  Genetically Engineered Phages: a Review of Advances over the Last Decade , 2016, Microbiology and Molecular Reviews.

[78]  V. Petrenko,et al.  Specific ligands for classical swine fever virus screened from landscape phage display library. , 2014, Antiviral research.

[79]  F. Theil,et al.  Unraveling the Effect of Immunogenicity on the PK/PD, Efficacy, and Safety of Therapeutic Proteins , 2016, Journal of immunology research.

[80]  Jeroen Lammertyn,et al.  Affinity comparison of p3 and p8 peptide displaying bacteriophages using surface plasmon resonance. , 2013, Analytical chemistry.

[81]  J. Scott,et al.  Searching for peptide ligands with an epitope library. , 1990, Science.

[82]  Va Petrenko Evolution of phage display: from bioactive peptides to bioselective nanomaterials. , 2008, Expert opinion on drug delivery.

[83]  T. Franklin The Molecular Basis of Antibiotic Action , 1973 .

[84]  G. P. Smith,et al.  Antibody-selectable filamentous fd phage vectors: affinity purification of target genes. , 1988, Gene.

[85]  V. Petrenko,et al.  Specific probe selection from landscape phage display library and its application in enzyme-linked immunosorbent assay of free prostate-specific antigen. , 2014, Analytical chemistry.

[86]  V. Petrenko,et al.  Enhanced tumor delivery and antitumor activity in vivo of liposomal doxorubicin modified with MCF-7-specific phage fusion protein. , 2014, Nanomedicine : nanotechnology, biology, and medicine.

[87]  R. Barrett,et al.  Peptides on phage: a vast library of peptides for identifying ligands. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[88]  V. Petrenko,et al.  Landscape phage ligands for PC3 prostate carcinoma cells. , 2010, Protein engineering, design & selection : PEDS.

[89]  V. Petrenko,et al.  Selected landscape phage probe as selective recognition interface for sensitive total prostate-specific antigen immunosensor. , 2018, Biosensors & bioelectronics.

[90]  C. W. Hilbers,et al.  Solution structure of the M13 major coat protein in detergent micelles: a basis for a model of phage assembly involving specific residues. , 1998, Journal of molecular biology.

[91]  Valery A. Petrenko,et al.  Landscape phage as a molecular recognition interface for detection devices , 2008, Microelectron. J..

[92]  V A Petrenko,et al.  Phage protein‐targeted cancer nanomedicines , 2014, FEBS letters.

[93]  D. Marvin,et al.  Structure and assembly of filamentous bacteriophages. , 2014, Progress in biophysics and molecular biology.

[94]  V. Petrenko,et al.  Optimization of Landscape Phage Fusion Protein-Modified Polymeric PEG-PE Micelles for Improved Breast Cancer Cell Targeting. , 2012, Journal of nanomedicine & nanotechnology.

[95]  V. Petrenko,et al.  Liposomes targeted by fusion phage proteins. , 2009, Nanomedicine : nanotechnology, biology, and medicine.

[96]  T. Quinn,et al.  α-Helically constrained phage display library , 2002 .