A Comprehensive Review on Phage Therapy and Phage-Based Drug Development
Abstract
:1. Introduction
2. Updated Mechanisms of Phage Action
2.1. Phage Adsorption and Receptor Recognition
2.2. Genome Injection and Host Takeover
2.3. Replication Strategies
2.4. Phage-Encoded Toxins and Enzymes
2.5. Horizontal Gene Transfer and Phage Therapy
2.6. Phage-Host Co-Evolution
2.7. Immune System Interactions
2.8. Synthetic and Recombinant Phages
2.9. Phage Delivery Systems
2.10. Regulatory and Ethical Considerations
3. Phage Therapy for Drug-Resistant Bacterial Infections
3.1. The Growing Threat of Antibiotic Resistance
3.2. Mechanisms and Advantages of Phage Therapy
3.3. Targeting Specific Drug-Resistant Bacteria
3.4. Enhancing Therapeutic Potential by Engineered Phages
3.5. Phage Therapy in Combination with Antibiotics
3.6. Regulatory and Safety Considerations
4. Phage-Based Treatments for Biofilm-Generating Bacteria
4.1. Mechanisms of Phage Action Against Biofilms
4.2. Advantages of Phage-Based Biofilm Treatments
4.3. Case Studies and Applications
4.4. Challenges and Future Directions
5. Phage Therapy for Intracellular Bacteria
5.1. Mechanisms of Phage Action Against Intracellular Bacteria
5.2. Advantages of Phage Therapy for Intracellular Bacterial Infections
5.3. Case Studies and Applications
5.4. Challenges and Future Directions
6. Phage-Based Vaccines
6.1. Principles of Phage-Based Vaccine Design
6.2. Mechanisms of Immune Stimulation
6.3. Applications of Phage-Based Vaccines
6.4. Challenges and Future Directions
7. Phage Therapy as Anti-Cancer Agents
7.1. Mechanisms of Phage-Mediated Anti-Cancer Activity
7.2. Development of Phage-Based Cancer Therapies
7.3. Applications of Phage-Based Cancer Therapies
7.4. Challenges and Future Directions
8. Phages as Drug Delivery Systems (DDS)
8.1. Principles of Phage-Based Drug Delivery
8.2. Engineering of Phage Vectors for Drug Delivery
8.3. Applications of Phage-Based Drug Delivery Systems
8.4. Challenges and Future Directions
9. Phage-Display Technology in Drug Discovery
9.1. Applications in Drug Discovery
9.2. Recent Advances in Phage Display for Drug Discovery
9.3. Challenges and Future Directions
10. Safety and Regulatory Considerations
10.1. Safety Considerations
10.2. Regulatory Frameworks
11. Challenges and Future Directions
11.1. Standardization and Regulatory Considerations
11.2. Therapeutic and Technological Challenges
11.3. Future Directions
12. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Phage-Enabled Techniques and Their Applications in Modern Medicine and Biotechnology | Relevant Strategies and Methodologies | References |
---|---|---|
1. Gene-Targeted Bacterial Killing |
| [17,18,19,20,21] |
2. Delivery of Antimicrobial Genes |
| [22,23,24,25] |
3. Phage-Mediated Antimicrobial Agent Delivery |
| [26,27,28,29] |
4. Strict Lytic Cycle Maintenance |
| [30] |
5. Inhibition of Biofilm Formation |
| [31,32,33] |
6. Modification of Phage Host Range |
| [34,35,36,37,38,39] |
7. Strategies to Overcome Phage Resistance |
| [24,40] |
8. In Vivo Phage Stabilization |
| [41,42,43,44,45] |
9. Enhancing Antibiotic Sensitivity |
| [46,47,48,49] |
10. Endotoxin Shock Suppression |
| [50,51] |
11. Phage-Based Vaccines |
| [52,53,54,55,56,57,58] |
12. Phage in Gene Therapy Applications |
| [59,60] |
13. Phage-Mediated Virus Suppression |
| [61] |
14. Phage for Diagnostic Applications |
| [62] |
15. Phage-Assisted Bone Regeneration |
| [63,64] |
16. Phage-Assisted Skin Regeneration |
| [65] |
17. Phage-Assisted Nerve Regeneration |
| [66,67] |
Status | Completed or Terminated | On Going or Not Yet Recruiting | ||||||||
---|---|---|---|---|---|---|---|---|---|---|
Phase | Pre-Clinical or Case Study | Phase | Pre-Clinical or Case Study | Phase | ||||||
I | I/II | II | II/III | III | I/II | II | III | |||
Staphylococcus aureus | 1 | 2 | 1 | 1 | 3 | 3 | 3 | |||
Coagulase-negative Staphylococci | 1 | 3 | ||||||||
Pseudomonas aeruginosa | 2 | 1 | 4 | 1 | 1 | 1 | 3 | 1 | ||
Escherichia coli | 2 | 3 | 1 | 1 | 1 | 2 | 2 | 1 | 1 | |
Enterococcus spp. | 1 | 1 | 1 | 2 | 1 | |||||
Klebsiella | 1 | 1 | 1 | 1 | 1 | 2 | ||||
Acinetobacter baumannii | 1 | 1 | 1 | 1 | ||||||
Streptococcus | 1 | 1 | ||||||||
Proteus | 1 | 1 | 1 | |||||||
Non-tuberculosis Mycobacteria | 1 | 1 | ||||||||
Achromobacter xylosoxidans | 1 | 1 | ||||||||
Stenotrophomonas maltophilia | 1 | 1 | ||||||||
Bacteroides fragilis | 1 | 1 | ||||||||
Shigella | 1 |
Challenges in Phage Therapy | Conventional Approach | Synthetic Approach | |
---|---|---|---|
1 | Narrow host range | The use of phage cocktail [111,112] | Genetic manipulation of receptor-binding protein [30,34] |
2 | Emergence of phage-resistant bacteria | Phage cocktail; combined therapy of antibiotic and phage [113,114] | Genetic manipulation of receptor-binding protein [115]; incorporation of small RNAs or CRISPR-Cas system to silence antibiotic resistance determinant [17,49] or delivery of genes encoding proteins to sensitize bacteria against antibiotics [116] |
3 | Necessitate identification of phage with therapeutic effect against patients’ isolates (personalized medicine) | Establish phage biobanks (isolating large phage collections) [117] | Engineering of phage tail fibers to alter host range [35,36,38] |
4 | Rapid clearance by reticuloendothelial system (RES) | Multiple phage dosing [118] | Phage capsid protein mutagenesis [41]; PEGylation of phage particles [43] |
5 | Phage pharmacokinetics (bioavailability through oral administration) | Pharmacological neutralization of gastric acid [119] | Encapsulation of phage in nanoparticles [120,121] |
6 | Limited accessibility to biofilm-producing bacteria | Use only phages with intrinsic biofilm-degrading properties [122,123], or combined therapy using phage and biofilm-degrading enzymes [124] | Engineered phages expressing biofilm-degrading enzymes [31] |
7 | Difficulties in defining pharmacokinetics (e.g., MIC) | Standardize routes and dosages of administration (required specified combinations of phage-host for each infection) [125] | Generation of non-proliferative anti-bacterial phage capsids [17] |
8 | Safety concern: risk of horizontal gene transfer | The use of phage-derived endolysin [126] | Development of well-characterized, non-propagating phages [127], introduction of antibacterial cargo using phagemids [128,129] or phage-inducible chromosomal islands (PICIs) [20] |
9 | Presence of potential hazardous genes in phage genome (toxin, virulence, antibiotic resistance genes, etc.) | Obligate virulent phage is preferred in therapy [113]; whole-genome analysis should be done in the first place | Custom-made phage can be generated easily using current techniques [30,34,130]; the use of self-destructive engineered phage (conjugation to gold nanorods) [29] |
10 | Low purity and potential toxin contamination in phage preparation | Purification by CsCl density gradient and ion exchange column [113] or affinity chromatography [131] | The use of cell-free system (cell-free-transcription-translation, TXTL) for phage production [130] |
Study | Target Bacteria | Phage (Dosages) | Antibiotic (Dosages) | References | |
---|---|---|---|---|---|
1 | Racenis et al., 2023 | Multidrug-resistant P. aeruginosa | Phages PNM and PT07 (Titer of 107 PFU/mL) | Ceftazidime/Avibactam (2.5 g) and Amikacin (750 mg) | [133] |
2 | Kebriaei et al., 2023 | Methicillin-resistant S. aureus (MRSA) strains and their daptomycin-nonsusceptible vancomycin-intermediate (DNS-VISA) | Phages Intesti13, Sb-1, and Romulus (107 PFU/well) | Daptomycin, vancomycin, and ceftaroline at 0.5× MBIC or 1× MBIC | [105] |
3 | Altamirano et al., 2022 | A. baumannii AB900 | Phages øFG02 (range: 102–108 PFU/mL) | Ceftazidime (range: 1–512 mg/mL) | [135] |
4 | Cano et al., 2021 | K. pneumoniae complex KpJH46 | Phage KpJH46Φ2(6.3 × 1010 phages in 50 mL for a total of 40 doses) | Minocycline, 100 mg | [136] |
5 | Morales et al., 2020 | S. aureus | Three Myoviridae bacteriophages AB-SA01 (109 PFU/mL) | lucloxacillin, Cefazolin, Vancomycin, Ciprofloxacin, Rifampicin | [137] |
6 | Jault et al., 2019 | P. aeruginosa | cocktail of 12 natural lytic anti-P. aeruginosa bacteriophages (PP1131; 1 × 106 PFU]/mL) | 1% sulfadiazine silver emulsion cream | [138] |
7 | Osman et al., 2023 | MDR A. baumannii | Multiple phage cocktails (C2P24, AC4, C2P21, and C1P12) | Minocycline | [139] |
Phage | Functional Peptide Display/Cargo | Tumor Type | Mode of Therapy | Preclinical Model | Therapy Outcome | References |
---|---|---|---|---|---|---|
M13 | WDC-2 phage displaying melanoma cell targeting peptide TRTKLPRLHLQS | Melanoma | Immunomodulatory | Subcutaneous B16-F10 tumor model in mice | Delayed tumor growth and increased survival | [197] |
λ Phage | Display of human ASPH-derived proteins | Hepatocellular carcinoma | Immunotherapy—Delivery of antigen for vaccine effect | Prophylactic vaccination schedule in BNL HCC subcutaneous model | Prophylactic and therapeutic immunization significantly delayed HCC growth and progression | [201] |
Hybrid M13/AAV | RGD4C peptide CDCRGDCFC that binds to αvβ3 integrin cell surface receptor on Glioblastoma | Glioblastoma | Gene therapy—Grp78 expression | Intracranial implantation of U87 glioblastoma cells | Suppressed the growth of orthotopic glioblastoma | [209] |
M13 phage | Fusobacterium nucleatum binding M13 phages | Colorectal cancer | Immunomodulatory | Orthotopic CT26 murine model | Precise scavenging of pro-tumor bacteria of Fusobacterium nucleatum, thereby blocking immunosuppressive myeloid-derived suppressor cells augmentation in the tumor microenvironment. | [28] |
2nd generation M13 vector | CDCRGDCFC (RGD4C) ligand that binds to αvβ3 integrin | Chondrosarcoma | Gene therapy–tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) expression | Subcutaneous implantation of SW1353-GFP-Luc cells | Decreased tumor size with nil side effects | [210] |
TPA (transmorphic phage/AAV) | Tumour targeting ligand, CDCRGDCFC (RGD4C) | Hepatocellular carcinoma | Therapeutic gene cassette that expresses TRAIL | N/A | Selective and efficient delivery of the tmTRAIL gene to HCC cells that induced apoptotic death of HCC cells | [211] |
Transmorphic phage/AAV, TPA | Double-cyclic tumour-targeting ligand, RGD4C ligand | Medulloblastoma | Delivering transgene expressing the tumor necrosis factor-alpha (TNFα) | Subcutaneous Daoy medulloblastoma xenograft mice model | Selective tumor homing, targeted tumor expression of TNFα, apoptosis, and destruction of the tumor vasculature | [212] |
M13/AAV | RGD4C ligand on the pIII minor coat protein for targeted therapy Histidine-rich endosomal escape peptide, H5WYG | Chondrosarcoma | Delivery of TNFα transgene | Subcutaneously established SW1353 xenograft in athymic mice | Complete elimination of tumor growth and eradication of the tumor size and tumor viability | [213] |
M13 bacteriophage | Chemical cross-linking and biomineralization of palladium nanoparticles | Breast cancer | Delivery of palladium nanoparticle for photothermal therapy and NLG919, a nontoxic IDO1-selective inhibitor | Subcutaneous breast cancer model using 4T1 cells | Induced immunogenic death of tumor cells with down-regulated IDO1 expression | [214] |
M13 | Fn-binding phages | Colon carcinoma | Immunomodulatory and reversing chemoresistance | Caecum implantation of CT26 cells in BALB/c mice | Modulated gut microbiota to augment chemotherapeutic effect | [215] |
M13 | Peptide (SYPIPDT) that is able to bind the epidermal growth factor receptor (EGFR) Chemical conjugation of Rose Bengal (RB) photosensitizing molecules on the capsid surface | Epidermoid carcinoma | Photodynamic therapy | N/A | M13EGFR–RB derivatives generated intracellular reactive oxygen species activated by an ultralow intensity white light irradiation, thereby killing the cancer cells | [216] |
T7 | Cancer homing peptide pep42 (CTVALPGGYVRVC) targeting the grp78 on cancer cells | Melanoma | Mammalian expression cassette of the cytokine granulocyte macrophage-colony stimulating factor (GM-CSF) | Subcutaneous B16F10 xenografts | Inhibited tumor growth by 72% compared to the untreated control. | [217] |
M13 | Engineered to display the EC and TM domains of human HER2 (ECTM phages) or its splice variant Δ16HER2 | Breast carcinoma | Immunotherapy-Delivery of antigen for vaccine effect | Δ16HER2-expressing epithelial tumor cell lines mice | Anti-HER2 vaccination induced a significant anti-HER2 antibody response and controls tumor growth. | [218] |
M13 | Display of anti-CD40 DARPin into the gene of the pIII coat protein for CD40 targeting | Colon adenocarcinoma | Immunotherapy—In situ vaccines | Subcutaneous MC38 xenografts | Significant accumulation of the phages and activation of DCs at the tumor site, reversing the immunosuppressive tumor microenvironment | [219] |
λ Phage | Tumor selectivity of the cargo, apoptin | Breast Carcinoma | Gene therapy | BT-474 cells subcutaneous xenograft | Implanted BT-474 human breast tumor successfully responded to the systemic and local injection of untargeted recombinant λ NBPs | [220] |
λ Phage | Display of displaying a HER2/neu derived peptide GP2 | Breast carcinoma | Immunotherapy—Delivery of antigen for vaccine effect | Subcutaneous TUBO cell implant | Robust CTL response against HER2/neu-positive tumor challenge in both prophylactic and therapeutic settings | [221] |
T4-AAV | RGD peptide (CDCRGDCFC), a cell surface targeting ligand, when fused to the tip of Hoc fiber | HEK293T | Gene delivery, Protein Delivery & Genome editing | N/A | Delivered full-length dystrophin gene and performed genome editing, gene recombination, gene replacement, gene expression, and gene silencing. | [222] |
T4 | Display of Catalase protein on phage heads Chemically coupled chlorin e6 (Ce6), a photosensitizer | Breast cancer | Photodynamic therapy | Subcutaneous 4T1 cancer cell model | Relieved tumor hypoxia and enabled Ce6 to produce ROS for effective tumor inhibition | [223] |
T7 phage | Display of neoepitopes derived from mutated proteins of melanoma tumor cells | Melanoma | Immunotherapy—Delivery of neoepitopes for vaccine effect | Subcutaneous B16F10 xenografts | Rapid production of vaccines that can deliver mutated peptides and stimulate an appropriate B cell response | [224] |
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Cui, L.; Watanabe, S.; Miyanaga, K.; Kiga, K.; Sasahara, T.; Aiba, Y.; Tan, X.-E.; Veeranarayanan, S.; Thitiananpakorn, K.; Nguyen, H.M.; et al. A Comprehensive Review on Phage Therapy and Phage-Based Drug Development. Antibiotics 2024, 13, 870. https://doi.org/10.3390/antibiotics13090870
Cui L, Watanabe S, Miyanaga K, Kiga K, Sasahara T, Aiba Y, Tan X-E, Veeranarayanan S, Thitiananpakorn K, Nguyen HM, et al. A Comprehensive Review on Phage Therapy and Phage-Based Drug Development. Antibiotics. 2024; 13(9):870. https://doi.org/10.3390/antibiotics13090870
Chicago/Turabian StyleCui, Longzhu, Shinya Watanabe, Kazuhiko Miyanaga, Kotaro Kiga, Teppei Sasahara, Yoshifumi Aiba, Xin-Ee Tan, Srivani Veeranarayanan, Kanate Thitiananpakorn, Huong Minh Nguyen, and et al. 2024. "A Comprehensive Review on Phage Therapy and Phage-Based Drug Development" Antibiotics 13, no. 9: 870. https://doi.org/10.3390/antibiotics13090870