Nanoengineering-armed oncolytic viruses drive antitumor response: progress and challenges

Abstract

Oncolytic viruses (OVs) have emerged as a powerful tool in cancer therapy. Characterized with the unique abilities to selectively target and lyse tumor cells, OVs can expedite the induction of cell death, thereby facilitating effective tumor eradication. Nanoengineering-derived OVs overcome traditional OV therapy limitations by enhancing the stability of viral circulation, and tumor targeting, promising improved clinical safety and efficacy and so on. This review provides a comprehensive analysis of the multifaceted mechanisms through which engineered OVs can suppress tumor progression. It initiates with a concise delineation on the fundamental attributes of existing OVs, followed by the exploration of their mechanisms of the antitumor response. Amid rapid advancements in nanomedicine, this review presents an extensive overview of the latest developments in the synergy between nanomaterials, nanotechnologies, and OVs, highlighting the unique characteristics and properties of the nanomaterials employed and their potential to spur innovation in novel virus design. Additionally, it delves into the current challenges in this emerging field and proposes strategies to overcome these obstacles, aiming to spur innovation in the design and application of next-generation OVs.

Keywords

nanomaterials / nanotechnology / oncolytic viruses / tumor microenvironment

References

[1] Lawler SE, Speranza M-C, Cho C-F, Chiocca EA. Oncolytic viruses in cancer treatment: a review. JAMA Oncol. 2017; 3(6): 841-849.

[2] Chaurasiya S, Chen NG, Fong Y. Oncolytic viruses and immunity. Curr Opin Immunol. 2018; 51: 83-90.

[3] Martuza R, Malick A, Markert J, Ruffner K, Coen D. Experimental-therapy of human glioma by means of a genetically engineered virus mutant. Science. 1991; 252(5007): 854-856.

[4] Melcher A, Harrington K, Vile R. Oncolytic virotherapy as immunotherapy. Science. 2021; 374(6573): 1325-1326.

[5] Lin D, Shen Y, Liang T. Oncolytic virotherapy: basic principles, recent advances and future directions. Signal Transd Target Ther. 2023; 8(1): 1-29.

[6] Twumasi-Boateng K, Pettigrew JL, Kwok YYE, Bell JC, Nelson BH. Oncolytic viruses as engineering platforms for combination immunotherapy. Nat Rev Cancer. 2018; 18(7): 419-432.

[7] Russell SJ, Peng KW, Bell JC. Oncolytic virotherapy. Nat Biotechnol. 2012; 30(7): 658-670.

[8] Gao Y, Wang K, Zhang J, Duan X, Sun Q, Men K. Multifunctional nanoparticle for cancer therapy. MedComm. 2023; 4(1): e187.

[9] Shukla A, Maiti P. Nanomedicine and versatile therapies for cancer treatment. MedComm. 2022; 3(3): e163.

[10] Tseng S-J, Kempson IM, Liao Z-X, Ho Y-C, Yang P-C. An acid degradable, lactate oxidizing nanoparticle formulation for non-small cell lung cancer virotherapy. Nano Today. 2022; 46: 101582.

[11] Xia M, Luo D, Dong J, et al. Graphene oxide arms oncolytic measles virus for improved effectiveness of cancer therapy. J Exp Clin Cancer Res. 2019; 38(1): 408.

[12] Cong Z, Tang S, Xie L, et al. Magnetic-powered Janus cell robots loaded with oncolytic Adenovirus for active and targeted virotherapy of bladder cancer. Adv Mater. 2022; 34(26): e2201042.

[13] Hassan HAFM, Diebold SS, Smyth LA, Walters AA, Lombardi G, Al-Jamal KT. Application of carbon nanotubes in cancer vaccines: achievements, challenges and chances. J Control Release. 2019; 297: 79-90.

[14] Huang H, Sun M, Liu M, et al. Full encapsulation of oncolytic virus using hybrid erythroctye-liposome membranes for augmented anti-refractory tumor effectiveness. Nano Today. 2022; 47: 101671.

[15] Tresilwised N, Pithayanukul P, Holm PS, Schillinger U, Plank C, Mykhaylyk O. Effects of nanoparticle coatings on the activity of oncolytic adenovirus–magnetic nanoparticle complexes. Biomaterials. 2012; 33(1): 256-269.

[16] Tresilwised N, Pithayanukul P, Mykhaylyk O, et al. Boosting oncolytic Adenovirus potency with magnetic nanoparticles and magnetic force. Mol Pharm. 2010; 7(4): 1069-1089.

[17] Choi J-W, Park JW, Na Y, et al. Using a magnetic field to redirect an oncolytic adenovirus complexed with iron oxide augments gene therapy efficacy. Biomaterials. 2015; 65: 163-174.

[18] Niemann J, Woller N, Brooks J, et al. Molecular retargeting of antibodies converts immune defense against oncolytic viruses into cancer immunotherapy. Nat Commun. 2019; 10: 3236.

[19] Le TMD, Jung B-K, Li Y, et al. Physically crosslinked injectable hydrogels for long-term delivery of oncolytic adenoviruses for cancer treatment. Biomater Sci. 2019; 7(10): 4195-4207.

[20] Bourgeois-Daigneault M-C, Roy DG, Aitken AS, et al. Neoadjuvant oncolytic virotherapy before surgery sensitizes triple-negative breast cancer to immune checkpoint therapy. Sci Transl Med. 2018; 10(422): eaao1641.

[21] Lan Q, Xia S, Wang Q, et al. Development of oncolytic virotherapy: from genetic modification to combination therapy. Front Med. 2020; 14(2): 160-184.

[22] Ren Y, Miao J-M, Wang Y-Y, et al. Oncolytic viruses combined with immune checkpoint therapy for colorectal cancer is a promising treatment option. Front Immunol. 2022; 13: 961796.

[23] Yin H, Sun L, Pu Y, et al. Ultrasound-controlled CRISPR/Cas9 system augments sonodynamic therapy of hepatocellular carcinoma. ACS Cent Sci. 2021; 7(12): 2049-2062.

[24] Tomko RP, Xu R, Philipson L. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc Natl Acad Sci USA. 1997; 94(7): 3352-3356.

[25] Bailer SM, Funk C, Riedl A, Ruzsics Z. Herpesviral vectors and their application in oncolytic therapy, vaccination, and gene transfer. Virus Genes. 2017; 53(5): 741-748.

[26] Navaratnarajah CK, Leonard VH, Cattaneo R. Measles virus glycoprotein complex assembly, receptor attachment, and cell entry. Curr Top Microbiol Immunol. 2009; 329: 59-76.

[27] Watanabe M, Nishikawaji Y, Kawakami H, Kosai K-i. Adenovirus biology, recombinant adenovirus, and adenovirus usage in gene therapy. Viruses. 2021; 13(12): 2502.

[28] Mercer J, Helenius A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science. 2008; 320(5875): 531-535.

[29] Msaouel P, Opyrchal M, Domingo Musibay E, Galanis E. Oncolytic measles virus strains as novel anticancer agents. Expert Opin Biol Ther. 2013; 13(4): 483-502.

[30] Danthi P, Guglielmi KM, Kirchner E, Mainou B, Stehle T, Dermody TS. From touchdown to transcription: the reovirus cell entry pathway. Curr Top Microbiol Immunol. 2010; 343: 91-119.

[31] Kirn DH, Thorne SH. Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer. Nat Rev Cancer. 2009; 9(1): 64-71.

[32] Kemball CC, Alirezaei M, Whitton JL. Type B coxsackieviruses and their interactions with the innate and adaptive immune systems. Future Microbiol. 2010; 5(9): 1329-1347.

[33] Errington F, Steele L, Prestwich R, et al. Reovirus activates human dendritic cells to promote innate antitumor immunity. J Immunol. 2008; 180(9): 6018-6026.

[34] Gromeier M, Nair SK. Recombinant poliovirus for cancer immunotherapy. Annu Rev Med. 2018; 69(1): 289-299.

[35] Au GG, Beagley LG, Haley ES, Barry RD, Shafren DR. Oncolysis of malignant human melanoma tumors by Coxsackieviruses A13, A15 and A18. Virol J. 2011; 8: 22.

[36] Goetz C, Gromeier M. Preparing an oncolytic poliovirus recombinant for clinical application against glioblastoma multiforme. Cytokine Growth Factor Rev. 2010; 21(2): 197-203.

[37] Zamarin D, Palese P. Oncolytic Newcastle disease virus for cancer therapy: old challenges and new directions. Future Microbiol. 2012; 7(3): 347-367.

[38] Cassel WA, Garrett RE. Newcastle disease virus as an antineoplastic agent. Cancer. 1965; 18: 863-868.

[39] Liang M. Oncorine, the world first oncolytic virus medicine and its update in China. Curr Cancer Drug Targets. 2018; 18(2): 171-176.

[40] Coffin R. Interview with Robert Coffin, inventor of T-VEC: the first oncolytic immunotherapy approved for the treatment of cancer. Immunotherapy. 2016; 8(2): 103-106.

[41] Fukuhara H, Ino Y, Todo T. Oncolytic virus therapy: a new era of cancer treatment at dawn. Cancer Sci. 2016; 107(10): 1373-1379.

[42] Lee A. Nadofaragene firadenovec: first approval. Drugs. 2023; 83(4): 353-357.

[43] Zamarin D, Ricca JM, Sadekova S, et al. PD-L1 in tumor microenvironment mediates resistance to oncolytic immunotherapy. J Clin Invest. 2018; 128(4): 1413-1428.

[44] Lopes A, Feola S, Ligot S, et al. Oncolytic adenovirus drives specific immune response generated by a poly-epitope pDNA vaccine encoding melanoma neoantigens into the tumor site. J ImmunoTher Cancer. 2019; 7(1): 174.

[45] Jung M-Y, Offord CP, Ennis MK, Kemler I, Neuhauser C, Dingli D. In vivo estimation of oncolytic virus populations within tumors. Cancer Res. 2018; 78(20): 5992-6000.

[46] Pascual-Pasto G, Bazan-Peregrino M, Olaciregui NG, et al. Therapeutic targeting of the RB1 pathway in retinoblastoma with the oncolytic adenovirus VCN-01. Sci Transl Med. 2019; 11(476): eaat9321.

[47] Samson A, Scott KJ, Taggart D, et al. Intravenous delivery of oncolytic reovirus to brain tumor patients immunologically primes for subsequent checkpoint blockade. Sci Transl Med. 2018; 10(422): aam7577.

[48] O’Leary MP, Choi AH, Kim S-I, et al. Novel oncolytic chimeric orthopoxvirus causes regression of pancreatic cancer xenografts and exhibits abscopal effect at a single low dose. J Transl Med. 2018; 16(1): 110.

[49] Friedman GK, Johnston JM, Bag AK, et al. Oncolytic HSV-1 G207 immunovirotherapy for pediatric high-grade gliomas. N Engl J Med. 2021; 384(17): 1613-1622.

[50] Yang M, Yang CS, Guo W, et al. A novel fiber chimeric conditionally replicative adenovirus-Ad5/F35 for tumor therapy. Cancer Biol Ther. 2017; 18(11): 833-840.

[51] Howells A, Marelli G, Lemoine NR, Wang Y. Oncolytic viruses—interaction of virus and tumor cells in the battle to eliminate cancer. Front Oncol. 2017; 7: 195.

[52] Gao J, Zheng Q, Xin N, Wang W, Zhao C. CD155, an onco-immunologic molecule in human tumors. Cancer Sci. 2017; 108(10): 1934-1938.

[53] Nandi SS, Gohil T, Sawant AS, Lambe PU, Ghosh S, Jana S. CD155: a key receptor playing diversified roles. Curr Mol Med. 2022; 22(7): 594-607.

[54] Ying C, Xiao B-d, Qin Y, et al. GOLPH2-regulated oncolytic adenovirus, GD55, exerts strong killing effect on human prostate cancer stem-like cells in vitro and in vivo. Acta Pharmacol Sin. 2018; 39(3): 405-414.

[55] Kulkarni A, Ferreira T, Bretscher C, et al. Oncolytic H-1 parvovirus binds to sialic acid on laminins for cell attachment and entry. Nat Commun. 2021; 12(1): 3834.

[56] Wienen F, Nilson R, Allmendinger E, et al. Affilin-based retargeting of adenoviral vectors to the epidermal growth factor receptor. Biomater Adv. 2023; 144: 213208.

[57] Gong J, Sachdev E, Mita AC, Mita MM. Clinical development of reovirus for cancer therapy: an oncolytic virus with immune-mediated antitumor activity. World J Methodol. 2016; 6(1): 25-42.

[58] Pan W, Bodempudi V, Esfandyari T, Farassati F. Utilizing Ras signaling pathway to direct selective replication of Herpes Simplex virus-1. PLoS One. 2009; 4(8): e6514.

[59] Brown MC, Holl EK, Boczkowski D, et al. Cancer immunotherapy with recombinant poliovirus induces IFN-dominant activation of dendritic cells and tumor antigen-specific CTLs. Sci Transl Med. 2017; 9(408): eaan4220.

[60] Ma J, Ramachandran M, Jin C, et al. Characterization of virus-mediated immunogenic cancer cell death and the consequences for oncolytic virus-based immunotherapy of cancer. Cell Death Dis. 2020; 11(1): 1-15.

[61] Zhang S, Wang J, Kong Z, et al. Emerging photodynamic nanotherapeutics for inducing immunogenic cell death and potentiating cancer immunotherapy. Biomaterials. 2022; 282: 121433.

[62] Taverner WK, Jacobus EJ, Christianson J, et al. Calcium influx caused by ER stress inducers enhances oncolytic adenovirus enadenotucirev replication and killing through PKCα activation. Mol Ther Oncol. 2019; 15: 117-130.

[63] Obaid QA, Al-Shammari AM, Khudair KK. Glucose deprivation induced by acarbose and oncolytic newcastle disease virus promote metabolic oxidative stress and cell death in a breast cancer model. Front Mol Biosci. 2022; 9: 816510.

[64] Howard FHN, Al-Janabi H, Patel P, et al. Nanobugs as drugs: bacterial derived nanomagnets enhance tumor targeting and oncolytic activity of HSV-1 virus. Small. 2022; 18(13): 2104763.

[65] Nakao S, Arai Y, Tasaki M, et al. Intratumoral expression of IL-7 and IL-12 using an oncolytic virus increases systemic sensitivity to immune checkpoint blockade. Sci Transl Med. 2020; 12(526): eaax7992.

[66] Alvarez-Breckenridge CA, Yu J, Price R, et al. NK cells impede glioblastoma virotherapy through NKp30 and NKp46 natural cytotoxicity receptors. Nat Med. 2012; 18(12): 1827-1834.

[67] Helmink BA, Reddy SM, Gao J, et al. B cells and tertiary lymphoid structures promote immunotherapy response. Nature. 2020; 577(7791): 549-555.

[68] Petitprez F, de Reyniès A, Keung EZ, et al. B cells are associated with survival and immunotherapy response in sarcoma. Nature. 2020; 577(7791): 556-560.

[69] DePeaux K, Rivadeneira DB, Lontos K, et al. An oncolytic virus-delivered TGFβ inhibitor overcomes the immunosuppressive tumor microenvironment. J Exp Med. 2023; 220(10): e20230053.

[70] Bommareddy PK, Aspromonte S, Zloza A, Rabkin SD, Kaufman HL. MEK inhibition enhances oncolytic virus immunotherapy through increased tumor cell killing and T cell activation. Sci Transl Med. 2018; 10(471).

[71] Zhang Y, Li Y, Chen K, Qian L, Wang P. Oncolytic virotherapy reverses the immunosuppressive tumor microenvironment and its potential in combination with immunotherapy. Cancer Cell Int. 2021; 21(1): 262.

[72] DePeaux K, Delgoffe GM. Integrating innate and adaptive immunity in oncolytic virus therapy. Trends Cancer. 2024; 10(2): 135-146.

[73] Chen L, Flies DB. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat Rev Immunol. 2013; 13(4): 227-242.

[74] Lin C, Ren W, Luo Y, et al. Intratumoral delivery of a PD-1–blocking scFv encoded in oncolytic HSV-1 promotes antitumor immunity and synergizes with TIGIT blockade. Cancer Immunol Res. 2020; 8(5): 632-647.

[75] Veinalde R, Pidelaserra-Martí G, Moulin C, et al. Oncolytic measles vaccines encoding PD-1 and PD-L1 checkpoint blocking antibodies to increase tumor-specific T cell memory. Mol Ther Oncol. 2022; 24: 43-58.

[76] Ju F, Luo Y, Lin C, et al. Oncolytic virus expressing PD-1 inhibitors activates a collaborative intratumoral immune response to control tumor and synergizes with CTLA-4 or TIM-3 blockade. J ImmunoTher Cancer. 2022; 10(6): e004762.

[77] Ren B, Cui M, Yang G, et al. Tumor microenvironment participates in metastasis of pancreatic cancer. Mol Cancer. 2018; 17(1): 108.

[78] Santry LA, van Vloten JP, Knapp JP, et al. Tumour vasculature: friend or foe of oncolytic viruses?. Cytokine Growth Factor Rev. 2020; 56: 69-82.

[79] Hack SP, Zhu AX, Wang YL. Augmenting anticancer immunity through combined targeting of angiogenic and PD-1/PD-L1 pathways: challenges and opportunities. Front Immunol. 2020; 11: 598877.

[80] Saito Y, Sunamura M, Motoi F, et al. Oncolytic replication-competent adenovirus suppresses tumor angiogenesis through preserved E1A region. Cancer Gene Ther. 2006; 13(3): 242-252.

[81] Hou W, Chen H, Rojas J, Sampath P, Thorne S. Oncolytic vaccinia virus demonstrates antiangiogenic effects mediated by targeting of VEGF. Int J Cancer. 2014; 135(5): 1238-1246.

[82] Breitbach CJ, De Silva NS, Falls TJ, et al. Targeting tumor vasculature with an oncolytic virus. Mol Ther. 2011; 19(5): 886-894.

[83] Benencia F, Courreges MC, Conejo-García JR, et al. Oncolytic HSV exerts direct antiangiogenic activity in ovarian carcinoma. Hum Gene Ther. 2005; 16(6): 765-778.

[84] Choi I-K, Shin H, Oh E, et al. Potent and long-term antiangiogenic efficacy mediated by FP3-expressing oncolytic adenovirus. Int J Cancer. 2015; 137(9): 2253-2269.

[85] Thorne SH, Tam BYY, Kirn DH, Contag CH, Kuo CJ. Selective intratumoral amplification of an antiangiogenic vector by an oncolytic virus produces enhanced antivascular and anti-tumor efficacy. Mol Ther. 2006; 13(5): 938-946.

[86] Yamauchi M, Gibbons DL, Zong C, Fradette JJ, Bota-Rabassedas N, Kurie JM. Fibroblast heterogeneity and its impact on extracellular matrix and immune landscape remodeling in cancer. Matrix Biol. 2020: 91-92.

[87] Tedcastle A, Illingworth S, Brown A, Seymour LW, Fisher KD. Actin-resistant DNAse I expression from oncolytic adenovirus enadenotucirev enhances its intratumoral spread and reduces tumor growth. Mol Ther. 2016; 24(4): 796-804.

[88] Guedan S, Rojas JJ, Gros A, Mercade E, Cascallo M, Alemany R. Hyaluronidase expression by an oncolytic adenovirus enhances its intratumoral spread and suppresses tumor growth. Mol Ther. 2010; 18(7): 1275-1283.

[89] Eriksson E, Milenova I, Wenthe J, Moreno R, Alemany R, Loskog A. IL-6 signaling blockade during CD40-mediated immune activation favors antitumor factors by reducing TGF-β collagen type I, and PD-L1/PD-1. J Immunol. 2019; 202(3): 787-798.

[90] Rivadeneira DB, DePeaux K, Wang Y, et al. Oncolytic viruses engineered to enforce Leptin expression reprogram tumor-infiltrating T cell metabolism and promote tumor clearance. Immunity. 2019; 51(3): 548-560. e544.

[91] Meng G, Li B, Chen A, et al. Targeting aerobic glycolysis by dichloroacetate improves Newcastle disease virus-mediated viro-immunotherapy in hepatocellular carcinoma. Br J Cancer. 2020; 122(1): 111-120.

[92] Faria SS, Fernando AJ, de Lima VCC, Rossi AG, de Carvalho JMA, Magalhães KG. Induction of pyroptotic cell death as a potential tool for cancer treatment. J Inflamm. 2022; 19(1): 19.

[93] Lin J, Sun S, Zhao K, et al. Oncolytic Parapoxvirus induces Gasdermin E-mediated pyroptosis and activates antitumor immunity. Nat Commun. 2023; 14(1): 224.

[94] Zhang Y, Xu T, Tian H, et al. Coxsackievirus group B3 has oncolytic activity against colon cancer through gasdermin E-mediated pyroptosis. Cancers. 2022; 14(24): 6206.

[95] Su W, Qiu W, Li S-J, et al. A dual-responsive STAT3 inhibitor nanoprodrug combined with oncolytic virus elicits synergistic antitumor immune responses by igniting pyroptosis. Adv Mater. 2023; 35(11): 2209379.

[96] Wang YY, Wang J, Wang S, et al. Dual-responsive epigenetic inhibitor nanoprodrug combined with oncolytic virus synergistically boost cancer immunotherapy by igniting Gasdermin E-mediated pyroptosis. ACS Nano. 2024.

[97] Alizadeh R, Ghanei M, Arashkia A, Dorostkar R, Azadmanesh K. Generation of recombinant measles virus containing the wild-type P gene to improve its oncolytic efficiency. Microb Pathogen. 2019; 135: 103631.

[98] Cai J, Lin Y, Zhang H, et al. Selective replication of oncolytic virus M1 results in a bystander killing effect that is potentiated by Smac mimetics. Proc Natl Acad Sci USA. 2017; 114(26): 6812-6817.

[99] Ghonime MG, Cassady KA. Combination therapy using Ruxolitinib and oncolytic HSV renders resistant MPNSTs susceptible to virotherapy. Cancer Immunol Res. 2018; 6(12): 1499-1510.

[100] Tseng S-J, Kempson IM, Huang K-Y, et al. Targeting tumor microenvironment by bioreduction-activated nanoparticles for light-triggered virotherapy. ACS Nano. 2018; 12(10): 9894-9902.

[101] Rommasi F, Esfandiari N. Liposomal nanomedicine: applications for drug delivery in cancer therapy. Nanoscale Res Lett. 2021; 16(1): 95.

[102] Deng S, Iscaro A, Zambito G, et al. Development of a new hyaluronic acid based redox-responsive nanohydrogel for the encapsulation of oncolytic viruses for cancer immunotherapy. Nanomaterials (Basel). 2021; 11(1): 144.

[103] Sun M, Yang S, Huang H, et al. Boarding oncolytic viruses onto tumor-homing bacterium-vessels for augmented cancer immunotherapy. Nano Lett. 2022; 22(12): 5055-5064.

[104] Wedge M-E, Jennings VA, Crupi MJF, et al. Virally programmed extracellular vesicles sensitize cancer cells to oncolytic virus and small molecule therapy. Nat Commun. 2022; 13(1): 1898.

[105] Riley RS, June CH, Langer R, Mitchell MJ. Delivery technologies for cancer immunotherapy. Nat Rev Drug Discov. 2019; 18(3): 175-196.

[106] Hall AR, Dix BR, O’Carroll SJ, Braithwaite AW. p53-dependent cell death/apoptosis is required for a productive adenovirus infection. Nat Med. 1998; 4(9): 1068-1072.

[107] Ridgway PJ, Hall AR, Myers CJ, Braithwaite AW. p53/E1b58kDa complex regulates adenovirus replication. Virology. 1997; 237(2): 404-413.

[108] Lin Y, Zhang H, Liang J, et al. Identification and characterization of alphavirus M1 as a selective oncolytic virus targeting ZAP-defective human cancers. Proc Natl Acad Sci USA. 2014; 111(42): E4504-E4512.

[109] Peng KW, Donovan KA, Schneider U, Cattaneo R, Lust JA, Russell SJ. Oncolytic measles viruses displaying a single-chain antibody against CD38, a myeloma cell marker. Blood. 2003; 101(7): 2557-2562.

[110] Nakamura T, Peng K-W, Harvey M, et al. Rescue and propagation of fully retargeted oncolytic measles viruses. Nat Biotechnol. 2005; 23(2): 209-214.

[111] Sinha A, Cha BG, Choi Y, et al. Carbohydrate-functionalized rGO as an effective cancer vaccine for stimulating antigen-specific cytotoxic T Cells and inhibiting tumor growth. Chem Mater. 2017; 29(16): 6883-6892.

[112] Jia X, Wang L, Feng X, et al. Cell membrane-coated oncolytic adenovirus for targeted treatment of glioblastoma. Nano Lett. 2023; 23(23): 11120-11128.

[113] Lammers T. Nanomedicine tumor targeting. Adv Mater. 2024; 36(26): 2312169.

[114] Xie L, Cong Z, Tang S, et al. Oncolytic adenovirus-loaded magnetic-driven Janus tumor cell robots for active and targeted virotherapy of homologous carcinoma. Mater Today Chem. 2023; 30: 101560.

[115] Koch J, Schober SJ, Hindupur SV, et al. Targeting the Retinoblastoma/E2F repressive complex by CDK4/6 inhibitors amplifies oncolytic potency of an oncolytic adenovirus. Nat Commun. 2022; 13(1): 4689.

[116] Garza-Morales R, Yaddanapudi K, Perez-Hernandez R, et al. Temozolomide renders murine cancer cells susceptible to oncolytic adenovirus replication and oncolysis. Cancer Biol Ther. 2018; 19(3): 188-197.

[117] Yang Y, Wang P, Shi R, et al. Design of the tumor microenvironment-multiresponsive nanoplatform for dual-targeting and photothermal imaging guided photothermal/photodynamic/chemodynamic cancer therapies with hypoxia improvement and GSH depletion. Chem Eng J. 2022; 441: 136042.

[118] Yang Y, Wang C, Tian C, Guo H, Shen Y, Zhu M. Fe3O4@MnO2@PPy nanocomposites overcome hypoxia: magnetic-targeting-assisted controlled chemotherapy and enhanced photodynamic/photothermal therapy. J Mater Chem B. 2018; 6(42): 6848-6857.

[119] Huang L-L, Li X, Zhang J, et al. MnCaCs-biomineralized oncolytic virus for bimodal imaging-guided and synergistically enhanced anticancer therapy. Nano Lett. 2019; 19(11): 8002-8009.

[120] Lagos KJ, Buzzá HH, Bagnato VS, Romero MP. Carbon-based materials in photodynamic and photothermal therapies applied to tumor destruction. Int J Mol Sci. 2022; 23(1): 22.

[121] Ding Y, Li Z, Jaklenec A, Hu Q. Vaccine delivery systems toward lymph nodes. Adv Drug Deliv Rev. 2021; 179: 113914.

[122] Naseer F, Ahmad T, Kousar K, et al. Formulation for the targeted delivery of a vaccine strain of oncolytic Measles virus (OMV) in hyaluronic acid coated thiolated chitosan as a green nanoformulation for the treatment of prostate cancer: a viro-immunotherapeutic approach. Int J Nanomed. 2023; 18: 185-205.

[123] Garofalo M, Villa A, Rizzi N, et al. Extracellular vesicles enhance the targeted delivery of immunogenic oncolytic adenovirus and paclitaxel in immunocompetent mice. J Control Release. 2019; 294: 165-175.

[124] Bah ES, Nace RA, Peng KW, Muñoz-Alía M, Russell SJ. Retargeted and stealth-modified oncolytic measles viruses for systemic cancer therapy in measles immune patients. Mol Cancer Ther. 2020; 19(10): 2057-2067.

[125] Chen G, Yuan Y, Li Y, et al. Enhancing oncolytic virus efficiency with methionine and N-(3-aminoprolil)methacrylamide modified acrylamide cationic block polymer. J Mater Chem B. 2024; 12(15): 3741-3750.

[126] Wang Y, Huang H, Zou H, et al. Liposome encapsulation of oncolytic virus M1 To reduce immunogenicity and immune clearance in vivo. Mol Pharm. 2019; 16(2): 779-785.

[127] Mendez N, Herrera V, Zhang L, et al. Encapsulation of adenovirus serotype 5 in anionic lecithin liposomes using a bead-based immunoprecipitation technique enhances transfection efficiency. Biomaterials. 2014; 35(35): 9554-9561.

[128] Record M, Silvente-Poirot S, Poirot M, Wakelam MJO. Extracellular vesicles: lipids as key components of their biogenesis and functions. J Lipid Res. 2018; 59(8): 1316-1324.

[129] Fang C, Xiao G, Wang T, et al. Emerging nano-/biotechnology drives oncolytic virus-activated and combined cancer immunotherapy. Research. 2023; 6: 0108.

[130] Packiam VT, Lamm DL, Barocas DA, et al. An open label, single-arm, phase II multicenter study of the safety and efficacy of CG0070 oncolytic vector regimen in patients with BCG-unresponsive non–muscle-invasive bladder cancer: interim results. Urol Oncol Semin Orig Invest. 2018; 36(10): 440-447.

[131] Thorne SH. Strategies to achieve systemic delivery of therapeutic cells and microbes to tumors. Expert Opin Biol Ther. 2007; 7(1): 41-51.

[132] Pelin A, Foloppe J, Petryk J, et al. Deletion of apoptosis inhibitor F1L in vaccinia virus increases safety and oncolysis for cancer therapy. Mol Ther Oncol. 2019; 14: 246-252.

[133] Mitchell MJ, Billingsley MM, Haley RM, Wechsler ME, Peppas NA, Langer R. Engineering precision nanoparticles for drug delivery. Nat Rev Drug Discov. 2021; 20(2): 101-124.

[134] Teja AS, Koh P-Y. Synthesis, properties, and applications of magnetic iron oxide nanoparticles. Prog Cryst Growth Charact Mater. 2009; 55(1-2): 22-45.

[135] Muthana M, Kennerley AJ, Hughes R, et al. Directing cell therapy to anatomic target sites in vivo with magnetic resonance targeting. Nat Commun. 2015; 6(1): 8009.

[136] Shen Z, Wu A, Chen X. Iron oxide nanoparticle based contrast agents for magnetic resonance imaging. Mol Pharm. 2017; 14(5): 1352-1364.

[137] Li W-P, Su C-H, Chang Y-C, Lin Y-J, Yeh C-S. Ultrasound-induced reactive oxygen species mediated therapy and imaging using a Fenton reaction activable polymersome. ACS Nano. 2016; 10(2): 2017-2027.

[138] Prasad C, Tang H, Liu W. Magnetic Fe3O4 based layered double hydroxides (LDHs) nanocomposites (Fe3O4/LDHs): recent review of progress in synthesis, properties and applications. J Nanostruct Chem. 2018; 8(4): 393-412.

[139] Zhang K, Qi C, Cai K. Manganese-based tumor immunotherapy. Adv Mater. 2023; 35(19): 2205409.

[140] Cai A-Y, Zhu Y-J, Qi C. Biodegradable inorganic nanostructured biomaterials for drug delivery. Adv Mater Interfaces. 2020; 7(20): 2000819.

[141] Wen Y, Liu Y, Chen C, et al. Metformin loaded porous particles with bio-microenvironment responsiveness for promoting tumor immunotherapy. Biomater Sci. 2021; 9(6): 2082-2089.

[142] Feng Y, Liu Y, Ma X, et al. Intracellular marriage of bicarbonate and Mn ions as “immune ion reactors” to regulate redox homeostasis and enhanced antitumor immune responses. J Nanobiotechnol. 2022; 20(1): 193.

[143] Lv M, Chen M, Zhang R, et al. Manganese is critical for antitumor immune responses via cGAS-STING and improves the efficacy of clinical immunotherapy. Cell Res. 2020; 30(11): 966-979.

[144] Feng L, Dong Z, Tao D, Zhang Y, Liu Z. The acidic tumor microenvironment: a target for smart cancer nano-theranostics. Natl Sci Rev. 2017; 5(2): 269-286.

[145] Wei R, Gong X, Lin H, et al. Versatile octapod-shaped hollow porous manganese(II) oxide nanoplatform for real-time visualization of cargo delivery. Nano Lett. 2019; 19(8): 5394-5402.

[146] Li Y-S, Ye L-Y, Luo Y-X, et al. Tumor-targeted delivery of copper-manganese biomineralized oncolytic adenovirus for colorectal cancer immunotherapy. Acta Biomater. 2024; 179: 243-255.

[147] Zhao Y, Pan Y, Zou K, et al. Biomimetic manganese-based theranostic nanoplatform for cancer multimodal imaging and twofold immunotherapy. Bioact Mater. 2023; 19: 237-250.

[148] Zou R, Li J, Yang T, et al. Biodegradable manganese engineered nanocapsules for tumor-sensitive near-infrared persistent luminescence/magnetic resonance imaging and simultaneous chemotherapy. Theranostics. 2021; 11(17): 8448-8463.

[149] Sun Z, Wang Z, Wang T, et al. Biodegradable MnO-based nanoparticles with engineering surface for tumor therapy: simultaneous Fenton-like ion delivery and immune activation. ACS Nano. 2022; 16(8): 11862-11875.

[150] Lin J, Chen X, Huang P. Graphene-based nanomaterials for bioimaging. Adv Drug Deliv Rev. 2016; 105: 242-254.

[151] Yang K, Feng L, Shi X, Liu Z. Nano-graphene in biomedicine: theranostic applications. Chem Soc Rev. 2012; 42(2): 530-547.

[152] Chen Y-W, Su Y-L, Hu S-H, Chen S-Y. Functionalized graphene nanocomposites for enhancing photothermal therapy in tumor treatment. Adv Drug Deliv Rev. 2016; 105: 190-204.

[153] Sun X, Liu Z, Welsher K, et al. Nano-graphene oxide for cellular imaging and drug delivery. Nano Res. 2008; 1(3): 203-212.

[154] Yue H, Wei W, Gu Z, et al. Exploration of graphene oxide as an intelligent platform for cancer vaccines. Nanoscale. 2015; 7(47): 19949-19957.

[155] Wang K, Hao Y, Wang Y, et al. Functional hydrogels and their application in drug delivery, biosensors, and tissue engineering. Int J Polym Sci. 2019; 2019: 3160732.

[156] Qu J, Zhao X, Ma PX, Guo B. pH-responsive self-healing injectable hydrogel based on N-carboxyethyl chitosan for hepatocellular carcinoma therapy. Acta Biomater. 2017; 58: 168-180.

[157] Emam HE, Shaheen T. Design of a dual pH and temperature responsive hydrogel based on esterified cellulose nanocrystals for potential drug release. Carbohydr Polym. 2022; 278: 118925.

[158] Lima-Tenorio MK, Tenorio-Neto ET, Garcia FP, et al. Hydrogel nanocomposite based on starch and Co-doped zinc ferrite nanoparticles that shows magnetic field-responsive drug release changes. J Mol Liq. 2015; 210: 100-105.

[159] Li L, Scheiger JM, Levkin PA. Design and applications of photoresponsive hydrogels. Adv Mater. 2019; 31(26): 1807333.

[160] Lim JYC, Goh SS, Loh XJ. Bottom-up engineering of responsive hydrogel materials for molecular detection and biosensing. ACS Mater Lett. 2020; 2(8): 918-950.

[161] Bordbar-Khiabani A, Gasik M. Smart hydrogels for advanced drug delivery systems. Int J Mol Sci. 2022; 23(7): 3665.

[162] Jung B-K, Oh E, Hong J, Lee Y, Park KD, Yun C-O. A hydrogel matrix prolongs persistence and promotes specific localization of an oncolytic adenovirus in a tumor by restricting nonspecific shedding and an antiviral immune response. Biomaterials. 2017; 147: 26-38.

[163] Du Y-n, Wei Q, Zhao L-j, et al. Hydrogel-based co-delivery of CIK cells and oncolytic adenovirus armed with IL12 and IL15 for cancer immunotherapy. Biomed Pharmacother. 2022; 151: 113110.

[164] van Schaik TA, Moreno-Lama L, Aligholipour Farzani T, et al. Engineered cell-based therapies in ex vivo ready-made CellDex capsules have therapeutic efficacy in solid tumors. Biomed Pharmacother. 2023; 162: 114665.

[165] Lv P, Chen H, Cheng H, et al. A calcium alginate hydrogel microsphere-based transcatheter arterial viroembolization strategy for hepatocellular carcinoma. Adv Ther. 2023; 6(4): 2200174.

[166] O’Riordan CR, Lachapelle A, Delgado C, et al. PEGylation of adenovirus with retention of infectivity and protection from neutralizing antibody in vitro and in vivo. Hum Gene Ther. 1999; 10(8): 1349-1358.

[167] Wortmann A, Vöhringer S, Engler T, et al. Fully detargeted polyethylene glycol-coated adenovirus vectors are potent genetic vaccines and escape from pre-existing anti-adenovirus antibodies. Mol Ther. 2008; 16(1): 154-162.

[168] Brugada-Vila P, Cascante A, Angel Lazaro M, et al. Oligopeptide-modified poly(beta-amino ester)s-coated AdNuPARmE1A: boosting the efficacy of intravenously administered therapeutic adenoviruses. Theranostics. 2020; 10(6): 2744-2758.

[169] Xu C, Cheng K, Wang X, et al. Antigen-capturing oncolytic adenoviruses along with IDO blockade for improved tumor immunotherapy. Nano Today. 2023; 51: 101922.

[170] Mattheolabakis G, Milane L, Singh A, Amiji MM. Hyaluronic acid targeting of CD44 for cancer therapy: from receptor biology to nanomedicine. J Drug Target. 2015; 23(7-8): 605-618.

[171] Kousar K, Naseer F, Abduh MS, Anjum S, Ahmad T. CD44 targeted delivery of oncolytic Newcastle disease virus encapsulated in thiolated chitosan for sustained release in cervical cancer: a targeted immunotherapy approach. Front Immunol. 2023; 14: 1175535.

[172] Erfani A, Diaz AE, Doyle PS. Hydrogel-enabled, local administration and combinatorial delivery of immunotherapies for cancer treatment. Mater Today. 2023; 65: 227-243.

[173] Namgung R, Mi Lee Y, Kim J, et al. Poly-cyclodextrin and poly-paclitaxel nano-assembly for anticancer therapy. Nat Commun. 2014; 5(1): 3702.

[174] Kim J, Sestito LF, Im S, Kim WJ, Thomas SN. Poly(cyclodextrin)-polydrug nanocomplexes as synthetic oncolytic virus for locoregional melanoma chemoimmunotherapy. Adv Funct Mater. 2020; 30(16): 1908788.

[175] Huang J, Ji L, Si J, et al. Platelet membrane-coated oncolytic vaccinia virus with indocyanine green for the second near-infrared imaging guided multi-modal therapy of colorectal cancer. J Colloid Interface Sci. 2024; 671: 216-231.

[176] Wu Q, Huang H, Sun M, et al. Inhibition of tumor metastasis by liquid-nitrogen-shocked tumor cells with oncolytic viruses infection. Adv Mater. 2023; 35(28): 2212210.

[177] Fusciello M, Fontana F, Tähtinen S, et al. Artificially cloaked viral nanovaccine for cancer immunotherapy. Nat Commun. 2019; 10(1): 5747.

[178] Chen Y, Chen X, Bao W, Liu G, Wei W, Ping Y. An oncolytic virus–T cell chimera for cancer immunotherapy. Nat Biotechnol. 2024: 1-12.

[179] Wang S, Song A, Xie J, et al. Fn-OMV potentiates ZBP1-mediated PANoptosis triggered by oncolytic HSV-1 to fuel antitumor immunity. Nat Commun. 2024; 15(1): 3669.

[180] Ban W, Sun M, Huang H, et al. Engineered bacterial outer membrane vesicles encapsulating oncolytic adenoviruses enhance the efficacy of cancer virotherapy by augmenting tumor cell autophagy. Nat Commun. 2023; 14(1): 2933.

[181] Kon E, Ad-El N, Hazan-Halevy I, Stotsky-Oterin L, Peer D. Targeting cancer with mRNA–lipid nanoparticles: key considerations and future prospects. Nat Rev Clin Oncol. 2023; 20(11): 739-754.

[182] Ulrich AS. Biophysical aspects of using liposomes as delivery vehicles. Biosci Rep. 2002; 22(2): 129-150.

[183] Lee SG, Yoon SJ, Kim CD, et al. Enhancement of adenoviral transduction with polycationic liposomes in vivo. Cancer Gene Ther. 2000; 7(10): 1329-1335.

[184] Jia J-X, Peng S-L, Kalisa NY, et al. A liposomal carbohydrate vaccine, adjuvanted with an NKT cell agonist, induces rapid and enhanced immune responses and antibody class switching. J Nanobiotechnol. 2023; 21(1): 175.

[185] Eguchi M, Hirata S, Ishigami I, et al. Pre-treatment of oncolytic reovirus improves tumor accumulation and intratumoral distribution of PEG-liposomes. J Control Release. 2023; 354: 35-44.

[186] Wang J-Y, Chen H, Dai S-Z, et al. Immunotherapy combining tumor and endothelium cell lysis with immune enforcement by recombinant MIP-3 alpha Newcastle disease virus in a vessel-targeting liposome enhances antitumor immunity. J ImmunoTher Cancer. 2022; 10(3): e003950.

[187] Zhang G, Wang Y, Zhou W, et al. A magnetically driven Tandem chip enables rapid isolation and multiplexed profiling of extracellular vesicles. Angew Chem Int Ed. 2023; 62(51): 202315113.

[188] Garofalo M, Villa A, Crescenti D, et al. Heterologous and cross-species tropism of cancer-derived extracellular vesicles. Theranostics. 2019; 9(19): 5681-5693.

[189] Brücher BLDM, Jamall IS. Cell-cell communication in the tumor microenvironment, carcinogenesis, and anticancer treatment. Cell Physiol Biochem. 2014; 34(2): 213-243.

[190] Schwab A, Meyering SS, Lepene B, et al. Extracellular vesicles from infected cells: potential for direct pathogenesis. Front Microbiol. 2015; 6: 1132.

[191] Kakiuchi Y, Kuroda S, Kanaya N, et al. Local oncolytic adenovirotherapy produces an abscopal effect via tumor-derived extracellular vesicles. Mol Ther. 2021; 29(10): 2920-2930.

[192] Saari H, Turunen T, Lohmus A, et al. Extracellular vesicles provide a capsid-free vector for oncolytic adenoviral DNA delivery. J Extracell Vesicles. 2020; 9(1): 1747206.

[193] Hong B, Chapa V, Saini U, et al. Oncolytic HSV therapy modulates vesicular trafficking inducing Cisplatin sensitivity and antitumor immunity. Clin Cancer Res. 2021; 27(2): 542-553.

[194] Garofalo M, Saari H, Somersalo P, et al. Antitumor effect of oncolytic virus and paclitaxel encapsulated in extracellular vesicles for lung cancer treatment. J Control Release. 2018; 283: 223-234.

[195] Lv P, Liu X, Chen X, et al. Genetically engineered cell membrane nanovesicles for oncolytic Adenovirus delivery: a versatile platform for cancer virotherapy. Nano Lett. 2019; 19(5): 2993-3001.

[196] Yu Q, Li X, Wang J, et al. Recent advances in reprogramming strategy of tumor microenvironment for rejuvenating photosensitizers-mediated photodynamic therapy. Small. 2024; 20(16): 2305708.

[197] Guo Y, Song M, Liu X, et al. Photodynamic therapy-improved oncolytic bacterial immunotherapy with FAP-encoding S. typhimurium. J Control Release. 2022; 351: 860-871.

[198] Zhang Y, Zhu J, Sun H, Li J. Modulation of tumor hypoxia and redox microenvironment using nanomedicines for enhanced cancer photodynamic therapy. Appl Mater Today. 2022; 29: 101687.

[199] Zhang Y, Fang C, Zhang W, Zhang K. Emerging pyroptosis-engineered nanobiotechnologies regulate cancers and inflammatory diseases: a double-edged sword. Matter. 2022; 5(11): 3740-3774.

[200] Kottke T, Hall G, Pulido J, et al. Antiangiogenic cancer therapy combined with oncolytic virotherapy leads to regression of established tumors in mice. J Clin Invest. 2010; 120(5): 1551-1560.

[201] Gil M, Bieniasz M, Seshadri M, et al. Photodynamic therapy augments the efficacy of oncolytic vaccinia virus against primary and metastatic tumours in mice. Br J Cancer. 2011; 105(10): 1512-1521.

[202] Shimizu K, Kahramanian A, Jabbar MADA, et al. Photodynamic augmentation of oncolytic virus therapy for central nervous system malignancies. Cancer Lett. 2023; 572: 216363.

[203] Tseng S-J, Huang K-Y, Kempson IM, et al. Remote control of light-triggered virotherapy. ACS Nano. 2016; 10(11): 10339-10346.

[204] Ni J, Sun Y, Song J, Zhao Y, Gao Q, Li X. Artificial cell-mediated photodynamic therapy enhanced anticancer efficacy through combination of tumor disruption and immune response stimulation. ACS Omega. 2019; 4(7): 12727-12735.

[205] Ghonime MG, Saini U, Kelly MC, et al. Eliciting an immune-mediated antitumor response through oncolytic herpes simplex virus-based shared antigen expression in tumors resistant to viroimmunotherapy. J ImmunoTher Cancer. 2021; 9(10): e002939.

[206] Wang Z, Liu W, Wang L, et al. Enhancing the antitumor activity of an engineered TRAIL-coated oncolytic adenovirus for treating acute myeloid leukemia. Signal Transd Target Ther. 2020; 5(1): 40.

[207] Wang Z, Yu B, Wang B, et al. A novel capsid-modified oncolytic recombinant adenovirus type 5 for tumor-targeting gene therapy by intravenous route. Oncotarget. 2016; 7(30): 47287-47301.

[208] Huang F-Y, Wang J-Y, Dai S-Z, et al. A recombinant oncolytic Newcastle virus expressing MIP-3 alpha promotes systemic antitumor immunity. J ImmunoTher Cancer. 2020; 8(2): e000330.

[209] Clubb JHA, Kudling TV, Heinioe C, et al. Adenovirus encoding tumor necrosis factor alpha and interleukin 2 Induces a tertiary lymphoid structure signature in immune checkpoint inhibitor refractory head and neck cancer. Front Immunol. 2022; 13: 794251.

[210] Zheng M, Huang J, Tong A, Yang H. Oncolytic viruses for cancer therapy: barriers and recent advances. Mol Ther Oncol. 2019; 15: 234-247.

[211] Hamilton JR, Vijayakumar G, Palese P. A RECOMBINANT antibody-expressing influenza virus delays tumor growth in a mouse model. Cell Rep. 2018; 22(1): 1-7.

[212] Zuo S, Wei M, Xu T, et al. An engineered oncolytic vaccinia virus encoding a single-chain variable fragment against TIGIT induces effective antitumor immunity and synergizes with PD-1 or LAG-3 blockade. J ImmunoTher Cancer. 2021; 9(12): e002843.

[213] Comfort N, Cai K, Bloomquist TR, Strait MD, Ferrante AW Jr, Baccarelli AA. Nanoparticle tracking analysis for the quantification and size determination of extracellular vesicles. J Vis Exp. 2021(169). 10.3791/62447

[214] Gast M, Sobek H, Mizaikoff B. Nanoparticle tracking of adenovirus by light scattering and fluorescence detection. Hum Gene Ther. 2019; 30(6): 235-244.

[215] Wirtz T, De Castro O, Audinot J-N, Philipp P. Imaging and analytics on the helium ion microscope. Annu Rev Anal Chem. 2019; 12(1): 523-543.

[216] Guerreiro MR, Freitas DF, Alves PM, Coroadinha AS. Detection and quantification of label-free infectious adenovirus using a switch-on cell-based fluorescent biosensor. ACS Sens. 2019; 4(6): 1654-1661.

[217] Nagano S, Perentes JY, Jain RK, Boucher Y. Cancer cell death enhances the penetration and efficacy of oncolytic herpes simplex virus in tumors. Cancer Res. 2008; 68(10): 3795-3802.

[218] Bernstock JD, Vicario N, Rong L, et al. A novel in situ multiplex immunofluorescence panel for the assessment of tumor immunopathology and response to virotherapy in pediatric glioblastoma reveals a role for checkpoint protein inhibition. Oncoimmunology. 2019; 8(12): e1678921.

[219] Sun S, Liu Y, He C, et al. Combining NanoKnife with M1 oncolytic virus enhances anticancer activity in pancreatic cancer. Cancer Lett. 2021; 502: 9-24.

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