Evolving Horizons: Adenovirus Vectors’ Timeless Influence on Cancer, Gene Therapy and Vaccines
Abstract
:1. Introduction
2. Biology, Species Types, Infection and Toxicity
3. Recombinant Adenoviruses: Safety, Modifications, Advantages, and Disadvantages
- (i)
- First-generation adenovirus (FGAdV) vectors: These vectors remove the E1 and E3 regions, allowing for increased cargo capacity by eliminating non-essential genetic information. These vectors cannot replicate on their own and rely on packaging cells, such as human embryonic kidney 293 cells expressing E1 protein, for production. The vector is capable of carrying up to 8.2 kb of foreign DNA cargo with higher immunogenicity [44]. These were used in certain earlier gene therapies. Vaccines often use FGAdV to trigger an apt immune response Modifications of early genes mostly depends on specific application.
- (ii)
- Conditionally replicating adenovirus (C-RAdV) vectors: These modified viral vectors involve the removal of E1 and/or E2 units that make it replication-deficient [45]. The vector is capable of replicating selectively in tumor cells, but not in normal cells, due to their abnormal retinoblastoma protein [46]. The engineering of tumor-specific gene promoters into the AdV genome is used to control the induction of viral replication to construct C-RAvD, which is regularly used in oncolytic virotherapy.
- (iii)
- Second-generation adenovirus (SGAdV) vectors: This generation of adenovirus was created to hold more genetic material (up to 12 Kb). The FGAdVs, despite E1 region deletion, induce strong host immune responses due to E1A-like factors in human cells. The SGAdV with E2 and E4 deletions was created to address this, but it still triggers host immune responses, resulting in reduced transgene expression in target cells [47]. More gene deletion was created by removing genes such as E2 and/or E4, in combination with E1 and E4 gene deletions. These are used in certain gene therapies for genetic disorders, vaccines, and certain types of cancers.
- (iv)
- Third-generation adenovirus (TGAdV) vectors: FGAdV and SGAdV vectors, despite E1–E4 region deletion, exhibit substantial immunogenicity and cytotoxicity. To accommodate larger therapeutic genes, third-generation adenovirus vectors were developed by removing the entire native adenovirus genome except for essential elements, thus raising the cargo limit to 36 kb. These ‘gutless adenovirus vectors’ enable high-level gene expression with minimal immune response. Production requires a co-introduced ‘helper adenovirus,’ but contamination concerns have led to the development of contamination-free methods using plasmids as helpers [48]. Incorporating stuffer DNA for efficient encapsidation in third-generation vectors has variable effects on transduction efficiency, with conflicting reports in the literature. These vectors do not have many regulatory genes and also do not have genetic elements, such as packing signals [48,49]. These gutless and safer vectors are regularly used in certain gene therapies for genetic disorders, vaccines, and certain types of cancers.
4. Recombinant Adenovirus Vector Production Methods
- (i)
- The traditional method/homologous recombination: The classical method for obtaining E1-deleted rAdVs involves homologous recombination of two DNA vectors. One vector contains a sequence mapping to the gene of interest at the left end of the adenovirus genome, while the other carries a sequence overlapping the 3′ viral segment and extending to the adenovirus genome’s right ITRs. This method is mostly used for generating FGAdV. This recombination process takes place in E-1-expressing cells such as HEK-293 cells. However, this laborious method is very inefficient in terms of recombination events and time consumption [50].
- (ii)
- Cre-LoxP-mediated recombination: To overcome limitations of the classical method, a Cre-lox site-specific recombination approach was developed. It involves three components: (a) a recombinant adenovirus with two loxP sites; (b) a shuttle vector containing ITR, an expression cassette, a packaging signal, and a loxP site; and (c) a 293-Cre cell line expressing Cre-recombinase. Transfection of the shuttle vector, containing the gene of interest and viral DNA, into a 293-Cre cell creates an adenovirus genome capable of replication, but it cannot be packaged. Recombination occurs between the loxP sites of the generated adenovirus genome and the shuttle vector, yielding the desired recombinant adenovirus. One drawback is the presence of parental adenovirus in the preparation, which persists even after multiple passages in 293-Cre cells, requiring careful recombinant virus verification [47,51].
- (iii)
- The AdEasy approach: This method employs HEK 293 cells to minimize homologous recombination issues, leveraging recombination in microorganisms such as yeast and bacterial cells. For instance, the AdEasy system aids in recovering the recombinant E. coli clone, primarily by introducing expression cassettes into the E1 region. After purifying recombinant plasmid DNA, it releases the viral chromosome and is subsequently transfected into the cell line. This system predominantly relies on E. coli rather than mammalian cells, benefiting from the bacterial machinery’s homologous capabilities [2,47].
- (iv)
- Use of Helper AdV for making TGAdV: The genome size of a virion should be within the range of 27.7–37 kb for proper packaging [52]. As discussed earlier third generational AdV/gutless AdV are helper-dependent adenovirus vector. TGAdV genomes include a noncoding eukaryotic ‘stuffer’, adenovirus ITRs, and a packaging signal [53]. In contrast, the helper virus (HV) lacks E1 and contains a packaging signal flanked by loxP sites. Infecting 293-Cre cells allows for the removal of the packaging signal from the helper virus genome, making it unpackageable but still capable of DNA replication, complementing TGAdV genome replication and encapsidation. An alternative TGAdV production system based on FLP/FRT site-specific recombination has also been developed, with similar results [54]. During packaging, helper virus contamination can be reduced via the Cre/LoxP or FLP/FRT systems if necessary [2,47]. Guo et al. recently conducted a study on restriction assembly for making a novel adenovirus vector. This is an easy-to-use method without the need for sophisticated instruments [55].
5. Applications of Recombinant Adenovirus Vector in Gene Therapy, Cancer, and Regenerative Medicine
5.1. Recombinant Adenovirus Vector Applied in Gene Therapy
5.2. Recombinant Adenovirus Vector Applied in Oncolytic Virotherapy
- Suicide genes: These genes make an enzyme that, when given a prodrug, triggers cell death. Suicide gene therapy approach is mostly used for solid tumors. After adenovirus is injected into the tumor (ITU), inactive prodrugs can be broken down into cytotoxic metabolites, leading to cell death. Adenovirus vectors have been designed to activate the p53 pathway, causing cell-cycle arrest and apoptosis in tumor cells, as many tumor types exhibit p53 dysfunction [62,63]. However, not all cancer cells lack p53. Various applications of adenoviruses in anticancer therapy have been explored beyond targeting p53 dysfunction. For example, herpes simplex virus thymidine kinase (HSV-TK) can convert prodrugs into cytotoxic compounds, such as converting fludarabine monophosphate (F-ara-AMP) into fluoroadenine or ganciclovir (GCV) into a cytotoxic nucleotide. It inhibits DNA polymerase and/or leads to incorporation into DNA and causes chain termination and tumoral cell death [64]. Additionally, the enzyme cytosine deaminase (CD) converts the prodrug 5-fluorocytosine (5-FC) into cytotoxic 5-fluorouridine (5-FU), causing DNA damage [65]. Other approaches include using varicella zoster virus-thymidine kinase (VZV-tk), purine nucleoside phosphorylase (PNP), and nitroreductase (NR). Modified adenovirus vectors delivering CD/HSV-TK chimeric enzymes, often in combination with other therapies such as radiotherapy, have shown effectiveness in clinical trials for various cancers, including prostate and pancreatic cancer [66,67]. Some vectors also carry additional genes, such as the human sodium iodide transporter (hNIS) for tumor imaging or pro-inflammatory cytokines such as IL-12 to trigger antitumor immune responses [68].
- Immunostimulatory genes: They introduce genes that regulate the immune system into the tumor cells, leading to a focused immune response. Adenovirus vectors can be equipped with immune-boosting genes to trigger the patient’s immune system against tumors. Delivering interferon (IFN)-β or IFN-α-2b using AdV vectors directly into the lungs has been shown to be a safe therapy for malignant pleural mesothelioma [69]. In Table 2, there are multiple active clinical trials ongoing using this strategy.
- Tumor suppressor drugs: These therapies reactivate the mutated tumor suppressor pathway. Tumor suppressor genes, such as p53, p16, RB, PTEN, and WWOX, are critical for controlling cell growth and differentiation under normal circumstances. Various strategies for tumor suppressor gene therapy exist. One such therapy, Gendicine, has been approved for clinical use. Combining p53 with treatments such as radiotherapy and chemotherapy has shown promise in treating cervical and liver cancers. Another approach involves inhibiting MDM2, a negative regulator of p53, with drugs such as RG7112, showing clinical activity in leukemia treatment [70]. Converting mutant p53 into a functional form using metallochaperones is another strategy, while vaccines targeting p53 mutant proteins have shown success in preclinical trials [71,72]. The adenovirus-mediated pRb94 has inhibited lung cancer cell growth, but wild-type Rb gene activation is challenging [73]. Additionally, introducing the PTEN gene can enhance the antitumor effect and reduce drug resistance in ovarian cancer cells. It has been evaluated with the rAdV approach as well [74].
5.3. Recombinant Adenovirus Vector Applied in Regenerative Medicine and Stem Cell Related Research
6. Vaccine Related Recombinant Adenovirus Development
7. Addressing Key Challenges for Enhanced Adenovirus Vector Performance
7.1. Pre-Existing Humoral and Cellular Immunity
7.2. Manufacturing Bottlenecks
7.3. Viral Vector Characterization Dilemma
7.4. Seroepidemiological Data
8. Recent Progress in the Field
9. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Adenovirus Related Genes | Functions |
---|---|
Capsid proteins II, III, IIIa, IV, VI, VIII, and IX | Structural proteins for capsid |
Core proteins V, VII, X | Structural proteins for capsid |
CR1β | Membrane glycoprotein, helps modulate the host immune response |
E1A | Most important early gene, activates transcription of a number of viral genes as well as genes of the host cells |
E1B55K | Binds to and inactivates p53, to block p53-mediated functions in the cell |
E2A and E2B | Participates in replication of viral DNA |
E3 RIDα and E3 RIDβ | Membrane proteins, plays role to prevent apoptosis |
E3 gp19K | Membrane glycoprotein, blocks class I MHC protein insertion in the host cell membrane to prevent T cell recognition of viral infection |
E3 14.7K | Defends the virus from host antiviral responses |
E4 transcription unit | Multifunctional viral proteins regulate viral and host-cell gene expressions |
IVa2, 52K, L1, and 100K | Encapsidation proteins, helps in proper assembly of viral capsids |
L3 protease | Cleave precursor polypeptides of pTP, pVI, pVII, pVIII, and IIIa to produce the mature viral proteins |
Terminal protein TP | Covalently attached to 5′ ends of the DNA, plays critical role in replication and long-term infectivity |
SN | NCT Identifier | Trial Stage | Conditions | Transgene/Strategy | Route | Enrol. |
---|---|---|---|---|---|---|
1 | NCT05124002 | Phase IV | Intrahepatic Cholangiocarcinoma | rHAdV 5 (H101) + HAIC | ITU | 66 |
2 | NCT04452591 | Phase III | Non-Muscle Invasive Bladder Cancer (NMIBC) | DDM in engineered oncolytic rAdV (CG0070) + n-dodecyl-B-D-maltoside | IVE | 110 |
3 | NCT03780049 | Phase III | Hepatocellular carcinoma | Hepatic artery infusion chemotherapy ± H101 | IV | 304 |
4 | NCT02928094 | Phase III | Refractory Angina Due to Myocardial Ischemia | HAdV 5 + FGF-4 | ICOI | 160 |
5 | NCT05664139 | Phase II | Liver Metastases from Malignant Melanoma | HAdV 5 + PD-1 mAb + Nab-paclitaxel | ITU/IV | 30 |
6 | NCT04111172 | Phase II | Gastrointestinal Adenocarcinoma | HAdV 5 + F35-hGCC-PADRE | IM | 81 |
7 | NCT03947190 | Phase II | Malaria Vaccine | ChAdV 63/MVA ME-TRAP + R21/Matrix-M | ID/DVI | 64 |
8 | NCT05419011 | Phase II | Lynch Syndrome | CEA/MUC1/Brachyury (TRI-AdV 5)+ IL-15 Superagonist N-803 | ITU | 186 |
9 | NCT05872841 | Phase II | Primary Hepatocellular Carcinoma | H101 Combined + TACE | ITU | 38 |
10 | NCT05564897 | Phase II | Bladder Cancer | Oncolytic AdV + PD-1 inhibitor (Camrelizumab) | IVE | 25 |
11 | NCT05419011 | Phase II | Lynch Syndrome | Tri-AdV 5 + IL-15 superagonist nogapendekin alfa inbakicept (N-803) | SC | 186 |
12 | NCT05234905 | Phase II | Cervical Cancer | H101 + Camrelizumab | ITU | 55 |
13 | NCT01913106 | Phase II | Prostate Cancer | AdV/RSC-TK + Brachytherapy | ITU | 25 |
14 | NCT03039751 | Phase II | Refractory Angina Pectoris | AdV + VEGF-D | IMCD | 180 |
15 | NCT04095689 | Phase II | Triple Negative Breast Cancer | Docetaxel + Pembrolizumab + AdV/IL-12 | ITU | 30 |
16 | NCT04495153 | Phase II | Non-Small Cell Lung Cancer | Aglatimagene besadenovec (CAN-2409 + prodrug) | ITU | 86 |
17 | NCT04416516 | Phase II | Basal Cell Carcinomas/Basal Cell Nevus Syndrome | ASN-002 + Hh inhibitor vismodegib | ITU | 18 |
18 | NCT04739046 | Phase II | Pancreatic cancer | HAdV 5-yCD/mutTKSR39rep-ADP (Theragene) | ITU | 12 |
19 | NCT05441410 | Phase I/II | Malaria | ME-TRAP + ChAdV 63 | IM | 30 |
20 | NCT04097002 | Phase I/IIa | Prostate Cancer | Improved AdV 5 (ORCA-010) | ITU | 24 |
21 | NCT05078866 | Phase Ib/II | Lynch Syndrome | AdV neoantigen priming vaccine GAdV-209-FSP + MVA tumor-specific neoantigen-boosting vaccine MVA-209-FSP | IM | 45 |
22 | NCT04673942 | Phase I/II | Refractory Solid Tumors | Replicative AdV 5 + TGF-β receptor-immunoglobulin Fc fusion trap (AdAPT-001) | ITU | 79 |
23 | NCT03754933 | Phase I/II | Head/Neck Cancer | rAdV expressing E. coli Purine nucleoside phosphorylase + fludarabine phosphate (Ad/PNP) | ITU | 10 |
24 | NCT02749331 | Phase I/II | Neuroendocrine Tumors | rAdV AdVince (CgA-E1AmiR122) | HAI | 35 |
25 | NCT02705196 | Phase I/II | Pancreatic Cancer | rAdV + TMZ-CD40L + 4-1BBL (LOAd703) | ITU | 55 |
26 | NCT05617040 | Phase I/II | Prostate Cancer | ChAdOx1-PCAQ + MVA-PCAQ + PSA + PAP + STEAP1+ 5T4 | IM/IV | 137 |
27 | NCT05914935 | Phase I | Malignant Tumors; Glioblastoma | AdV + rL-IFN | ITU | 6 |
28 | NCT04695327 | Phase I | Solid Tumors | TNFα + IL-2 + rAdV (TILT-123) | ITU | 18 |
29 | NCT05180851 | Phase I | Head and Neck Cancer; Melanoma; Ovarian/Cervical Carcinoma; Lung Cancer | rAdV L-IFN (YSCH-01) | ITU | 19-28 |
30 | NCT04053283 | Phase I | Metastatic or Advanced Epithelial Tumors | Tumor-selective transgene expressing AdV (NG-641) | IV | 186 |
31 | NCT05271318 | Phase I | Ovarian Cancer | rAdV TILT-123 + pembrolizumab [AdV 5/3-E2F-d24-hTNFa-IRES-hIL2] | ITU | 29 |
32 | NCT05222932 | Phase I | Melanoma; Head and Neck Squamous Cell Carcinoma | rAdV (TILT-123) + avelumab + anti-PD1 (L) (AVENTIL) [AdV 5/3-E2F-d24-hTNFa-IRES-hIL2] | ITU | 15 |
33 | NCT05165433 | Phase I | Metastatic or Advanced Epithelial Tumors | NG-350A vector + pembrolizumab (tumor-selective anti-CD40) | IV | 198 |
34 | NCT05686798 | Phase I | Progressive Astrocytoma; GBM; Brain Tumor | AdV 5-yCD/ mutTKSR39rep-ADP | ITU | 18 |
35 | NCT05043714 | Phase I | Metastatic or Advanced Epithelial Tumors (NEBULA) | NG-641 vector + nivolumab (NG-641) | IV | 30 |
36 | NCT04217473 | Phase I | Advanced Melanoma | TNFalpha + IL 2 coding rAdV TILT-123 (TUNINTIL) | ITU | 15 |
37 | NCT03896568 | Phase I | High-Grade Glioma | MSC-DNX-2401 (AdV 5-DNX-2401) | IA | 36 |
38 | NCT03740256 | Phase I | Advanced HER2 Positive Solid Tumors | HER2-specific CAR-T + ChAdVEC | ITU | 45 |
39 | NCT03896568 | Phase I | Recurrent High-Grade Glioma | BM-hMSCs + DNX-2401 (MSC-DNX-2401) | IA | 36 |
40 | NCT04053283 | Phase I | Metastatic Cancer, Epithelial Tumor | rAdV + FAP-TAc antibody/ CXCL9/CXCL10/IFN-α (NG-641) | IV | 186 |
41 | NCT03284268 | Phase I | Refractory Retinoblastoma (RTB) | rAdV (VCN-01) | IVE | 13 |
42 | NCT02455479 | Phase I | Cocaine-Dependent Individuals | Disruptive dAd5GNE | IV | 15 |
43 | NCT05076760 | Phase I | Non-Small Cell Lung Cancer | rAdV (MEM-288) + IFNβ + rCD40-ligand | ITU | 18 |
44 | NCT03878121 | Phase I | HIV | ADV 4-HIV envelope vaccine vectors [AdV 4-Env145NFL + AdV 4-Env150KN + VRC-HIVRGP096-00-VP (Trimer 4571)] | IN/IM | 300 |
45 | NCT04839042 | Phase I | COVID-19 Vaccine | AdV 6 vector (SC-AdV 6-1) | IM/IN/ IH | 190 |
46 | NCT05526183 | Phase I | COVID-19 Vaccine | AdV 5 CoVacHGMix (with equal amounts of CoVacHGA1320, CoVacHGB420, CoVacHGC720 and CoVacHGD1480 | IM | 36 |
47 | NCT05717699 | Phase I | Intrinsic Pontine Glioma | AdV 5-TD-nsIL12 + human non-secretory interleukin-12 | ITU | 18 |
48 | NCT05717712 | Phase I | Intrinsic Pontine Glioma | AdV 5-TD-nsIL12 + human non-secretory interleukin-12 | ITU | 18 |
49 | NCT03546361 | Phase I | Non-Small Cell Lung Cancer | CCL21-Gene modified dendritic cell (rAdV -CCL21-DC) + pembrolizumab | ITU + IV | 24 |
50 | NCT05991427 | Phase I | Zoster Disease | ChAdOx1-VZV | IM | 65 |
SN | Name | Sponsor | AdV Type | Payload/ Antigen | Application |
---|---|---|---|---|---|
1 | Jcovden | Johnson & Johnson (Solothurn, Switzerland) | AdV 26 | CoV2-S spike protein | COVID-19 vaccine |
2 | Convidecia | CanSino Biologics Inc. (Tianjin, China) | AdV 5 | SARS-CoV-2 spike protein | COVID-19 vaccine |
3 | Vaxzevria / Covishield | AstraZeneca/ University of Oxford (Oxford, UK) | ChAdV | ChAdOx1-S spike protein antigen | COVID-19 vaccine |
4 | Sputnik V | Gamaleya Research Institute (Moscow, Russia) | AdV 26 (prime) + AdV 5 (boost) | Spike protein (S) antigen | COVID-19 vaccine |
5 | Zabdeno | Johnson and Johnson (Solothurn, Switzerland) | AdV 26 | Ad26.ZEBOV | Ebola Vaccine |
6 | Adstiladrin | Ferring Pharmaceuticals (Parsippany-Troy Hills, NJ, USA) | AdV 5 | Nadofaragene firadenovec-vncg with IFNα2b | Gene Therapy for Bladder Cancer |
7 | H101/Oncorine | Shanghai Sunway Biotech (Shanghai, China) | AdV 5 | Tumor-specific | Cancer Therapy for Nasopharyngeal cancer |
8 | Gendicine | Shenzhen SiBiono GeneTech (Shenzhen, China) | AdV 5 | Anti-p53 | Cancer Therapy for Head and neck cancer |
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Trivedi, P.D.; Byrne, B.J.; Corti, M. Evolving Horizons: Adenovirus Vectors’ Timeless Influence on Cancer, Gene Therapy and Vaccines. Viruses 2023, 15, 2378. https://doi.org/10.3390/v15122378
Trivedi PD, Byrne BJ, Corti M. Evolving Horizons: Adenovirus Vectors’ Timeless Influence on Cancer, Gene Therapy and Vaccines. Viruses. 2023; 15(12):2378. https://doi.org/10.3390/v15122378
Chicago/Turabian StyleTrivedi, Prasad D., Barry J. Byrne, and Manuela Corti. 2023. "Evolving Horizons: Adenovirus Vectors’ Timeless Influence on Cancer, Gene Therapy and Vaccines" Viruses 15, no. 12: 2378. https://doi.org/10.3390/v15122378