Abstract

Nanotechnology is paving the way for new carrier systems designed to overcome the greatest challenges of oncolytic virotherapy; systemic administration and subsequent implications of immune responses and specific cell binding and entry. Systemic administration of oncolytic agents is vital for disseminated neoplasms, however transition of nanoparticles (NP) to virotherapy has yielded modest results. Their success relies on how they navigate the merry-go-round of often-contradictory phases of NP delivery: circulatory longevity, tissue permeation and cellular interaction, with many studies postulating design features optimal for each phase. This review discusses the optimal design of NPs for the transport of oncolytic viruses within these phases, to determine whether improved virotherapeutic efficacy lies in the pharmacokinetic/pharmacodynamics characteristics of the NP–oncolytic viruses complexes rather than manipulation of the virus and targeting ligands.

Keywords:

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

1. Duffy MR, Fisher KD, Seymour LW. Making oncolytic virotherapy a clinical reality: the European contribution. Hum. Gene Ther. 28(11), 1033–1046 (2017).
Medline CASGoogle Scholar
2. Iwamoto T. Clinical application of drug delivery systems in cancer chemotherapy: review of the efficacy and side effects of approved drugs. Biol. Pharm. Bull. 36(5), 715–718 (2013).
Medline CASGoogle Scholar
3. Ernsting MJ, Murakami M, Roy A, Li SD. Factors controlling the pharmacokinetics, biodistribution and intratumoral penetration of nanoparticles. J. Control. Rel. 172(3), 782–794 (2013). • Comprehensive summary of how both nanoparticles (NP) and biological factors can influence NP delivery to tumors.
Medline CASGoogle Scholar
4. Setyawati MI, Tay CY, Docter D, Stauber RH, Leong DT. Understanding and exploiting nanoparticles’ intimacy with the blood vessel and blood. Chem. Soc. Rev. 44(22), 8174–8199 (2015).
Medline CASGoogle Scholar
5. Caldorera-Moore M, Guimard N, Shi L, Roy K. Designer nanoparticles: incorporating size, shape and triggered release into nanoscale drug carriers. Expert Opin. Drug Deliv. 7(4), 479–495 (2010).
Medline CASGoogle Scholar
6. Fang C, Shi B, Pei YY, Hong MH, Wu J, Chen HZ. In vivo tumor targeting of tumor necrosis factor-alpha-loaded stealth nanoparticles: effect of MePEG molecular weight and particle size. Eur. J. Pharm. Sci. 27(1), 27–36 (2006).
Medline CASGoogle Scholar
7. Decuzzi P, Lee S, Bhushan B, Ferrari M. A theoretical model for the margination of particles within blood vessels. Ann. Biomed. Eng. 33(2), 179–190 (2005).
Medline CASGoogle Scholar
8. Duan D, Liu H, Xu M et al. Size-controlled synthesis of drug-loaded zeolitic imidazolate framework in aqueous solution and size effect on their cancer theranostics in vivo. ACS Appl. Mater. Interfaces 10(49), 42165–42174 (2018).
Medline CASGoogle Scholar
9. Mohr K, Sommer M, Baier G et al. Aggregation behaviour of polystyrene-nanoparticles in human blood serum and its impact on the in vivo distribution in mice. J. Nanomed. Nanotechnol. 5(2), 1000193 (2014).
Google Scholar
10. Durantie E, Vanhecke D, Rodriguez-Lorenzo L et al. Biodistribution of single and aggregated gold nanoparticles exposed to the human lung epithelial tissue barrier at the air-liquid interface. Part. Fibre Toxicol. 14(1), 49 (2017).
MedlineGoogle Scholar
11. Tang L, Yang X, Yin Q et al. Investigating the optimal size of anticancer nanomedicine. Proc. Natl Acad. Sci. USA 111(43), 15344–15349 (2014).
Medline CASGoogle Scholar
12. Kang JH, Cho J, Ko YT. Investigation on the effect of nanoparticle size on the blood–brain tumour barrier permeability by in situ perfusion via internal carotid artery in mice. J. Drug Target. 27(1), 103–110 (2019).
Medline CASGoogle Scholar
13. Kettiger H, Schipanski A, Wick P, Huwyler J. Engineered nanomaterial uptake and tissue distribution: from cell to organism. Int. J. Nanomed. 8, 3255–3269 (2013).
MedlineGoogle Scholar
14. Shang L, Nienhaus K, Nienhaus GU. Engineered nanoparticles interacting with cells: size matters. J. Nanobiotechnol. 12, 5 (2014).
MedlineGoogle Scholar
15. Sykes EA, Dai Q, Sarsons CD et al. Tailoring nanoparticle designs to target cancer based on tumor pathophysiology. Proc. Natl Acad. Sci. USA 113(9), E1142–1151 (2016). • Tumor interaction with NPs influenced by the size of the NPs as well as tumor volume. Therefore, NP size should be personalized to a patient’s disease state to increase efficacy.
Medline CASGoogle Scholar
16. Arvizo RR, Rana S, Miranda OR, Bhattacharya R, Rotello VM, Mukherjee P. Mechanism of anti-angiogenic property of gold nanoparticles: role of nanoparticle size and surface charge. Nanomedicine 7(5), 580–587 (2011).
Medline CASGoogle Scholar
17. Truong NP, Whittaker MR, Mak CW, Davis TP. The importance of nanoparticle shape in cancer drug delivery. Expert Opin. Drug Deliv. 12(1), 129–142 (2015). •• Focuses on the role of nonspherical nanoparticles for cancer drug delivery.
Medline CASGoogle Scholar
18. Bruckman MA, Randolph LN, Vanmeter A et al. Biodistribution, pharmacokinetics, and blood compatibility of native and PEGylated tobacco mosaic virus nano-rods and -spheres in mice. Virology 449, 163–173 (2014).
Medline CASGoogle Scholar
19. Chariou PL, Lee KL, Pokorski JK, Saidel GM, Steinmetz NF. Diffusion and uptake of tobacco mosaic virus as therapeutic carrier in tumor tissue: effect of nanoparticle aspect ratio. J. Phys. Chem. B 120(26), 6120–6129 (2016).
Medline CASGoogle Scholar
20. Lee SY, Ferrari M, Decuzzi P. Shaping nano-/micro-particles for enhanced vascular interaction in laminar flows. Nanotechnology 20(49), 495101 (2009).
MedlineGoogle Scholar
21. Gratton SE, Ropp PA, Pohlhaus PD et al. The effect of particle design on cellular internalization pathways. Proc. Natl Acad. Sci. USA 105(33), 11613–11618 (2008).
Medline CASGoogle Scholar
22. Favi PM, Valencia MM, Elliott PR et al. Shape and surface chemistry effects on the cytotoxicity and cellular uptake of metallic nanorods and nanospheres. J. Biomed. Mater. Res. A 103(12), 3940–3955 (2015).
Medline CASGoogle Scholar
23. Favi PM, Gao M, Johana Sepulveda Arango L et al. Shape and surface effects on the cytotoxicity of nanoparticles: gold nanospheres versus gold nanostars. J. Biomed. Mater. Res. A 103(11), 3449–3462 (2015).
Medline CASGoogle Scholar
24. Armstrong JK, Hempel G, Koling S et al. Antibody against poly(ethylene glycol) adversely affects PEG-asparaginase therapy in acute lymphoblastic leukemia patients. Cancer 110(1), 103–111 (2007).
MedlineGoogle Scholar
25. Garay RP, El-Gewely R, Armstrong JK, Garratty G, Richette P. Antibodies against polyethylene glycol in healthy subjects and in patients treated with PEG-conjugated agents. Expert Opin. Drug Deliv. 9(11), 1319–1323 (2012).
Medline CASGoogle Scholar
26. Hsieh YC, Wang HE, Lin WW et al. Pre-existing anti-polyethylene glycol antibody reduces the therapeutic efficacy and pharmacokinetics of PEGylated liposomes. Theranostics 8(11), 3164–3175 (2018).
Medline CASGoogle Scholar
27. Fix SM, Nyankima AG, Mcsweeney MD, Tsuruta JK, Lai SK, Dayton PA. Accelerated clearance of ultrasound contrast agents containing polyethylene glycol is associated with the generation of anti-polyethylene glycol antibodies. Ultrasound Med. Biol. 44(6), 1266–1280 (2018).
MedlineGoogle Scholar
28. Zhang P, Sun F, Liu S, Jiang S. Anti-PEG antibodies in the clinic: current issues and beyond PEGylation. J. Control. Rel. 244(Pt B), 184–193 (2016).
Medline CASGoogle Scholar
29. Fu S, Liang M, Wang Y et al. Dual-modified novel biomimetic nanocarriers improve targeting and therapeutic efficacy in glioma. ACS Appl. Mater. Interfaces 11(2), 1841–1854 (2018).
Google Scholar
30. Hu CM, Zhang L, Aryal S, Cheung C, Fang RH, Zhang L. Erythrocyte membrane-camouflaged polymeric nanoparticles as a biomimetic delivery platform. Proc. Natl Acad. Sci. USA 108(27), 10980–10985 (2011).
Medline CASGoogle Scholar
31. Honary S, Zahir F. Effect of zeta potential on the proeprties of nano-drug delivery systems – a review (Part 2). Tropic. J. Pharm. Res. 12(2), 265–273 (2013).
Google Scholar
32. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 144(5), 646–674 (2011).
Medline CASGoogle Scholar
33. Russell SJ. RNA viruses as virotherapy agents. Cancer Gene Ther. 9(12), 961–966 (2002).
Medline CASGoogle Scholar
34. Haddad D. Genetically engineered vaccinia viruses as agents for cancer treatment, imaging, and transgene delivery. Front. Oncol. 7, 96 (2017).
MedlineGoogle Scholar
35. Sokolowski NA, Rizos H, Diefenbach RJ. Oncolytic virotherapy using herpes simplex virus: how far have we come? Oncolytic Virother. 4, 207–219 (2015).
Medline CASGoogle Scholar
36. Alemany R. Oncolytic adenoviruses in cancer treatment. Biomedicines 2(1), 36–49 (2014).
MedlineGoogle Scholar
37. Brown MC, Dobrikova EY, Dobrikov MI et al. Oncolytic polio virotherapy of cancer. Cancer 120(21), 3277–3286 (2014).
MedlineGoogle Scholar
38. Assessment of adenoviral vector safety and toxicity: report of the National Institutes of Health Recombinant DNA Advisory Committee. Hum. Gene Ther. 13(1), 3–13 (2002).
MedlineGoogle Scholar
39. Matsuda T, Karube H, Aruga A. A comparative safety profile assessment of oncolytic virus therapy based on clinical trials. Ther. Innov. Regul. Sci. 52(4), 430–437 (2018).
MedlineGoogle Scholar
40. Global Oncolytic Virus Therapy Market Size, Status and Forecast 2018–2025. (2019). www.globenewswire.com/news-release/2019/01/29/1706861/0/en/Global-Oncolytic-Virus-Therapy-Market-to-Collect-More-than-US-13-5-Mn-by-2025-QY-Research-Inc.html
Google Scholar
41. Johnson DB, Puzanov I, Kelley MC. Talimogene laherparepvec (T-VEC) for the treatment of advanced melanoma. Immunotherapy 7(6), 611–619 (2015). •• First US FDA approved oncolytic virus for the treatment of melanoma.
CASGoogle Scholar
42. Killock D. Skin cancer: T-VEC oncolytic viral therapy shows promise in melanoma. Nat. Rev. Clin. Oncol. 12(8), 438 (2015).
MedlineGoogle Scholar
43. Kohlhapp FJ, Zloza A, Kaufman HL. Talimogene laherparepvec (T-VEC) as cancer immunotherapy. Drugs Today (Barc.) 51(9), 549–558 (2015).
Medline CASGoogle Scholar
44. Geletneky K, Hajda J, Angelova AL et al. Oncolytic H-1 parvovirus shows safety and signs of immunogenic activity in a first Phase I/IIa glioblastoma trial. Mol. Ther. 25(12), 2620–2634 (2017).
Medline CASGoogle Scholar
45. Donnelly OG, Errington-Mais F, Prestwich R et al. Recent clinical experience with oncolytic viruses. Curr. Pharm. Biotechnol. 13(9), 1834–1841 (2012).
Medline CASGoogle Scholar
46. Lawler SE, Speranza MC, Cho CF, Chiocca EA. Oncolytic viruses in cancer treatment: a review. JAMA Oncol. 3(6), 841–849 (2017).
MedlineGoogle Scholar
47. Motalleb G. Virotherapy in cancer. Iran. J. Cancer Prev. 6(2), 101–107 (2013).
Medline CASGoogle Scholar
48. Maroun J, Munoz-Alia M, Ammayappan A, Schulze A, Peng KW, Russell S. Designing and building oncolytic viruses. Future Virol. 12(4), 193–213 (2017).
CASGoogle Scholar
49. Ebert O, Harbaran S, Shinozaki K, Woo SL. Systemic therapy of experimental breast cancer metastases by mutant vesicular stomatitis virus in immune-competent mice. Cancer Gene Ther. 12(4), 350–358 (2005).
Medline CASGoogle Scholar
50. Naik S, Nace R, Barber GN, Russell SJ. Potent systemic therapy of multiple myeloma utilizing oncolytic vesicular stomatitis virus coding for interferon-beta. Cancer Gene Ther. 19(7), 443–450 (2012).
Medline CASGoogle Scholar
51. Ozduman K, Wollmann G, Piepmeier JM, van den Pol AN. Systemic vesicular stomatitis virus selectively destroys multifocal glioma and metastatic carcinoma in brain. J. Neurosci. 28(8), 1882–1893 (2008).
Medline CASGoogle Scholar
52. Rommelfanger DM, Wongthida P, Diaz RM et al. Systemic combination virotherapy for melanoma with tumor antigen-expressing vesicular stomatitis virus and adoptive T-cell transfer. Cancer Res. 72(18), 4753–4764 (2012).
Medline CASGoogle Scholar
53. Phuangsab A, Lorence RM, Reichard KW, Peeples ME, Walter RJ. Newcastle disease virus therapy of human tumor xenografts: antitumor effects of local or systemic administration. Cancer Lett. 172(1), 27–36 (2001).
Medline CASGoogle Scholar
54. Schirrmacher V, Griesbach A, Ahlert T. Antitumor effects of Newcastle disease virus in vivo: local versus systemic effects. Int. J. Oncol. 18(5), 945–952 (2001).
Medline CASGoogle Scholar
55. Kottke T, Thompson J, Diaz RM et al. Improved systemic delivery of oncolytic reovirus to established tumors using preconditioning with cyclophosphamide-mediated Treg modulation and interleukin-2. Clin. Cancer Res. 15(2), 561–569 (2009).
Medline CASGoogle Scholar
56. Ma JL, Han SX, Zhao J et al. Systemic delivery of lentivirus-mediated secretable TAT-apoptin eradicates hepatocellular carcinoma xenografts in nude mice. Int. J. Oncol. 41(3), 1013–1020 (2012).
Medline CASGoogle Scholar
57. Hodish I, Tal R, Shaish A et al. Systemic administration of radiation-potentiated anti-angiogenic gene therapy against primary and metastatic cancer based on transcriptionally controlled HSV-TK. Cancer Biol. Ther. 8(5), 424–432 (2009).
MedlineGoogle Scholar
58. Leoni V, Gatta V, Palladini A et al. Systemic delivery of HER2-retargeted oncolytic-HSV by mesenchymal stromal cells protects from lung and brain metastases. Oncotarget 6(33), 34774–34787 (2015).
MedlineGoogle Scholar
59. Auffinger B, Ahmed AU, Lesniak MS. Oncolytic virotherapy for malignant glioma: translating laboratory insights into clinical practice. Front. Oncol. 3, 32 (2013).
MedlineGoogle Scholar
60. Kaur B, Chiocca EA, Cripe TP. Oncolytic HSV-1 virotherapy: clinical experience and opportunities for progress. Curr. Pharm. Biotechnol. 13(9), 1842–1851 (2012).
Medline CASGoogle Scholar
61. Davola ME, Mossman KL. Oncolytic viruses: how “lytic” must they be for therapeutic efficacy? Oncoimmunology 8(6), e1581528 (2019).
MedlineGoogle Scholar
62. Brestovitsky A, Sharf R, Mittelman K, Kleinberger T. The adenovirus E4orf4 protein targets PP2A to the ACF chromatin-remodeling factor and induces cell death through regulation of SNF2h-containing complexes. Nucleic Acids Res. 39(15), 6414–6427 (2011).
Medline CASGoogle Scholar
63. Ito N, Demarco RA, Mailliard RB et al. Cytolytic cells induce HMGB1 release from melanoma cell lines. J. Leukoc. Biol. 81(1), 75–83 (2007).
Medline CASGoogle Scholar
64. Haanen J. Converting cold into hot tumors by combining immunotherapies. Cell 170(6), 1055–1056 (2017).
Medline CASGoogle Scholar
65. Kohlhapp FJ, Kaufman HL. Molecular pathways: mechanism of action for Talimogene Laherparepvec, a new oncolytic virus immunotherapy. Clin. Cancer Res. 22(5), 1048–1054 (2016).
Medline CASGoogle Scholar
66. Chaurasiya S, Chen NG, Fong Y. Oncolytic viruses and immunity. Curr. Opin. Immunol. 51, 83–90 (2018).
Medline CASGoogle Scholar
67. Diaconu I, Cerullo V, Hirvinen ML et al. Immune response is an important aspect of the antitumor effect produced by a CD40L-encoding oncolytic adenovirus. Cancer Res. 72(9), 2327–2338 (2012).
Medline CASGoogle Scholar
68. Donnelly OG, Errington-Mais F, Steele L et al. Measles virus causes immunogenic cell death in human melanoma. Gene Ther. 20(1), 7–15 (2013).
Medline CASGoogle Scholar
69. Workenhe ST, Mossman KL. Oncolytic virotherapy and immunogenic cancer cell death: sharpening the sword for improved cancer treatment strategies. Mol. Ther. 22(2), 251–256 (2014).
Medline CASGoogle Scholar
70. Breitbach CJ, De Silva NS, Falls TJ et al. Targeting tumor vasculature with an oncolytic virus. Mol. Ther. 19(5), 886–894 (2011).
Medline CASGoogle Scholar
71. Hou W, Chen H, Rojas J, Sampath P, Thorne SH. Oncolytic vaccinia virus demonstrates antiangiogenic effects mediated by targeting of VEGF. Int. J. Cancer 135(5), 1238–1246 (2014).
Medline CASGoogle Scholar
72. Angarita FA, Acuna SA, Ottolino-Perry K, Zerhouni S, Mccart JA. Mounting a strategic offense: fighting tumor vasculature with oncolytic viruses. Trends Mol. Med. 19(6), 378–392 (2013).
Medline CASGoogle Scholar
73. Thorne SH, Tam BY, 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. 13(5), 938–946 (2006).
Medline CASGoogle Scholar
74. Chiocca EA, Rabkin SD. Oncolytic viruses and their application to cancer immunotherapy. Cancer Immunol. Res. 2(4), 295–300 (2014).
Medline CASGoogle Scholar
75. Zeng W, Hu P, Wu J et al. The oncolytic herpes simplex virus vector G47 effectively targets breast cancer stem cells. Oncol. Rep. 29(3), 1108–1114 (2013).
Medline CASGoogle Scholar
76. Simpson GR, Relph K, Harrington K, Melcher A, Pandha H. Cancer immunotherapy via combining oncolytic virotherapy with chemotherapy: recent advances. Oncolytic Virother. 5, 1–13 (2016).
Medline CASGoogle Scholar
77. Kasala D, Lee SH, Hong JW et al. Synergistic antitumor effect mediated by a paclitaxel-conjugated polymeric micelle-coated oncolytic adenovirus. Biomaterials 145, 207–222 (2017).
Medline CASGoogle Scholar
78. Tong JG, Valdes YR, Sivapragasam M et al. Spatial and temporal epithelial ovarian cancer cell heterogeneity impacts Maraba virus oncolytic potential. BMC Cancer 17(1), 594 (2017).
MedlineGoogle Scholar
79. Filley AC, Dey M. Immune system, friend or foe of oncolytic virotherapy? Front. Oncol. 7, 106 (2017).
MedlineGoogle Scholar
80. Gujar S, Pol JG, Kim Y, Lee PW, Kroemer G. Antitumor benefits of antiviral immunity: an underappreciated aspect of oncolytic virotherapies. Trends Immunol. 39(3), 209–221 (2018).
Medline CASGoogle Scholar
81. Dayton AI. Hitting HIV where it hides. Retrovirology 5, 15 (2008).
MedlineGoogle Scholar
82. Di Lorenzo C, Angus AG, Patel AH. Hepatitis C virus evasion mechanisms from neutralizing antibodies. Viruses 3(11), 2280–2300 (2011).
MedlineGoogle Scholar
83. Schiffner T, Sattentau QJ, Duncan CJ. Cell-to-cell spread of HIV-1 and evasion of neutralizing antibodies. Vaccine 31(49), 5789–5797 (2013).
Medline CASGoogle Scholar
84. Myers R, Coviello C, Erbs P et al. Polymeric cups for cavitation-mediated delivery of oncolytic vaccinia virus. Mol. Ther. 24(9), 1627–1633 (2016).
Medline CASGoogle Scholar
85. Nosaki K, Hamada K, Takashima Y et al. A novel, polymer-coated oncolytic measles virus overcomes immune suppression and induces robust antitumor activity. Mol. Ther. Oncolytics 3, 16022 (2016).
Medline CASGoogle Scholar
86. Oh E, Oh JE, Hong J et al. Optimized biodegradable polymeric reservoir-mediated local and sustained co-delivery of dendritic cells and oncolytic adenovirus co-expressing IL-12 and GM-CSF for cancer immunotherapy. J. Control. Rel. 259, 115–127 (2017).
Medline CASGoogle Scholar
87. Price DL, Li P, Chen CH et al. Silk-elastin-like protein polymer matrix for intraoperative delivery of an oncolytic vaccinia virus. Head Neck 38(2), 237–246 (2016).
MedlineGoogle Scholar
88. Na Y, Choi JW, Kasala D et al. Potent antitumor effect of neurotensin receptor-targeted oncolytic adenovirus co-expressing decorin and Wnt antagonist in an orthotopic pancreatic tumor model. J. Control. Rel. 220(Pt B), 766–782 (2015).
Medline CASGoogle Scholar
89. Yoon AR, Kasala D, Li Y et al. Antitumor effect and safety profile of systemically delivered oncolytic adenovirus complexed with EGFR-targeted PAMAM-based dendrimer in orthotopic lung tumor model. J. Control. Rel. 231, 2–16 (2016).
Medline CASGoogle Scholar
90. Grunwald GK, Vetter A, Klutz K et al. Systemic image-guided liver cancer radiovirotherapy using dendrimer-coated adenovirus encoding the sodium iodide symporter as theranostic gene. J. Nucl. Med. 54(8), 1450–1457 (2013).
MedlineGoogle Scholar
91. Sakurai F, Inoue S, Kaminade T et al. Cationic liposome-mediated delivery of reovirus enhances the tumor cell-killing efficiencies of reovirus in reovirus-resistant tumor cells. Int. J. Pharm. 524(1-2), 238–247 (2017).
Medline CASGoogle Scholar
92. Shikano T, Kasuya H, Sahin TT et al. High therapeutic potential for systemic delivery of a liposome-conjugated herpes simplex virus. Curr. Cancer Drug Targets 11(1), 111–122 (2011).
Medline CASGoogle Scholar
93. Yang L, Wang L, Su XQ et al. Suppression of ovarian cancer growth via systemic administration with liposome-encapsulated adenovirus-encoding endostatin. Cancer Gene Ther. 17(1), 49–57 (2010).
MedlineGoogle Scholar
94. Yoshida T, Mizuno M, Taniguchi K, Nakayashiki N, Wakabayashi T, Yoshida J. Rat glioma cell death induced by cationic liposome-mediated transfer of the herpes simplex virus thymidine kinase gene followed by ganciclovir treatment. J. Surg. Oncol. 76(1), 19–25 (2001).
Medline CASGoogle Scholar
95. Balvers RK, Belcaid Z, van den Hengel SK et al. Locally-delivered T-cell-derived cellular vehicles efficiently track and deliver adenovirus delta24-RGD to infiltrating glioma. Viruses 6(8), 3080–3096 (2014).
MedlineGoogle Scholar
96. Muthana M, Giannoudis A, Scott SD et al. Use of macrophages to target therapeutic adenovirus to human prostate tumors. Cancer Res. 71(5), 1805–1815 (2011). •• Oncolytic adenovirus hidden inside macrophages were activated by hypoxic tumor microenvironment. Selective replication of adenovirus inside prostate tumor cells only resulted in inhibition of tumor growth and pulmonary metastases.
Medline CASGoogle Scholar
97. Evgin L, Acuna SA, Tanese de Souza C et al. Complement inhibition prevents oncolytic vaccinia virus neutralization in immune humans and cynomolgus macaques. Mol. Ther. 23(6), 1066–1076 (2015).
Medline CASGoogle Scholar
98. Fulci G, Breymann L, Gianni D et al. Cyclophosphamide enhances glioma virotherapy by inhibiting innate immune responses. Proc. Natl Acad. Sci. USA 103(34), 12873–12878 (2006).
Medline CASGoogle Scholar
99. Lun XQ, Jang JH, Tang N et al. Efficacy of systemically administered oncolytic vaccinia virotherapy for malignant gliomas is enhanced by combination therapy with rapamycin or cyclophosphamide. Clin. Cancer Res. 15(8), 2777–2788 (2009).
Medline CASGoogle Scholar
100. Haisma HJ, Kamps JA, Kamps GK, Plantinga JA, Rots MG, Bellu AR. Polyinosinic acid enhances delivery of adenovirus vectors in vivo by preventing sequestration in liver macrophages. J. Gen. Virol. 89(Pt 5), 1097–1105 (2008).
Medline CASGoogle Scholar
101. Liu YP, Tong C, Dispenzieri A, Federspiel MJ, Russell SJ, Peng KW. Polyinosinic acid decreases sequestration and improves systemic therapy of measles virus. Cancer Gene Ther. 19(3), 202–211 (2012).
Medline CASGoogle Scholar
102. Fulci G, Dmitrieva N, Gianni D et al. Depletion of peripheral macrophages and brain microglia increases brain tumor titers of oncolytic viruses. Cancer Res. 67(19), 9398–9406 (2007).
Medline CASGoogle Scholar
103. Denton NL, Chen CY, Hutzen B et al. Myelolytic treatments enhance oncolytic herpes virotherapy in models of Ewing sarcoma by modulating the immune microenvironment. Mol. Ther. Oncolytics 11, 62–74 (2018).
Medline CASGoogle Scholar
104. Tresilwised N, Pithayanukul P, Mykhaylyk O et al. Boosting oncolytic adenovirus potency with magnetic nanoparticles and magnetic force. Mol. Pharm. 7(4), 1069–1089 (2010). •• Magnetic oncolytic virus complexes exhibited stronger oncolytic activity than adenovirus alone when administered intra-tumorally.
Medline CASGoogle Scholar
105. Choi JW, Park JW, Na Y et al. Using a magnetic field to redirect an oncolytic adenovirus complexed with iron oxide augments gene therapy efficacy. Biomaterials 65, 163–174 (2015).
Medline CASGoogle Scholar
106. Almstatter I, Mykhaylyk O, Settles M et al. Characterization of magnetic viral complexes for targeted delivery in oncology. Theranostics 5(7), 667–685 (2015).
MedlineGoogle Scholar
107. Wojcik M, Lewandowski W, Krol M et al. Enhancing anti-tumor efficacy of Doxorubicin by non-covalent conjugation to gold nanoparticles – in vitro studies on feline fibrosarcoma cell lines. PLoS ONE 10(4), e0124955 (2015).
MedlineGoogle Scholar
108. Lim EK, Sajomsang W, Choi Y et al. Chitosan-based intelligent theragnosis nanocomposites enable pH-sensitive drug release with MR-guided imaging for cancer therapy. Nanoscale Res. Lett. 8(1), 467 (2013).
MedlineGoogle Scholar
109. Korin E, Froumin N, Cohen S. Surface analysis of nanocomplexes by x-ray photoelectron spectroscopy (XPS). ACS Biomater. Sci. Eng. 3, 882–889 (2017).
Medline CASGoogle Scholar
110. Soldemo M, Adori M, Stark JM et al. Glutaraldehyde cross-linking of HIV-1 env trimers skews the antibody subclass response in mice. Front. Immunol. 8, 1654 (2017).
MedlineGoogle Scholar
111. Fang J, Nakamura H, Maeda H. The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv. Drug Deliv. Rev. 63(3), 136–151 (2011).
Medline CASGoogle Scholar
112. Hoyos V, Del Bufalo F, Yagyu S et al. Mesenchymal stromal cells for linked delivery of oncolytic and apoptotic adenoviruses to non-small-cell lung cancers. Mol. Ther. 23(9), 1497–1506 (2015).
Medline CASGoogle Scholar
113. Parker Kerrigan BC, Shimizu Y, Andreeff M, Lang FF. Mesenchymal stromal cells for the delivery of oncolytic viruses in gliomas. Cytotherapy 19(4), 445–457 (2017).
MedlineGoogle Scholar
114. Uldry E, Faes S, Demartines N, Dormond O. Fine-tuning tumor endothelial cells to selectively kill cancer. Int. J. Mol. Sci. 18(7), 1401 (2017).
Google Scholar
115. McFadden G, Mohamed MR, Rahman MM, Bartee E. Cytokine determinants of viral tropism. Nat. Rev. Immunol. 9(9), 645–655 (2009).
Medline CASGoogle Scholar
116. Jhawar SR, Thandoni A, Bommareddy PK et al. Oncolytic viruses-natural and genetically engineered cancer immunotherapies. Front. Oncol. 7, 202 (2017).
MedlineGoogle Scholar
117. Zhou J, Leuschner C, Kumar C, Hormes JF, Soboyejo WO. Sub-cellular accumulation of magnetic nanoparticles in breast tumors and metastases. Biomaterials 27(9), 2001–2008 (2006).
Medline CASGoogle Scholar
118. Trabulo S, Aires A, Aicher A, Heeschen C, Cortajarena AL. Multifunctionalized iron oxide nanoparticles for selective targeting of pancreatic cancer cells. Biochim. Biophys. Acta 1861(6), 1597–1605 (2017).
CASGoogle Scholar
119. Tan PH, Xue SA, Wei B, Holler A, Voss RH, George AJ. Changing viral tropism using immunoliposomes alters the stability of gene expression: implications for viral vector design. Mol. Med. 13(3–4), 216–226 (2007).
Medline CASGoogle Scholar
120. Maeda H. Vascular permeability in cancer and infection as related to macromolecular drug delivery, with emphasis on the EPR effect for tumor-selective drug targeting. Proc. Jpn Acad. Ser. B Phys. Biol. Sci. 88(3), 53–71 (2012).
Medline CASGoogle Scholar
121. Nakamura Y, Mochida A, Choyke PL, Kobayashi H. Nanodrug delivery: is the enhanced permeability and retention effect sufficient for curing cancer? Bioconjug. Chem. 27(10), 2225–2238 (2016).
Medline CASGoogle Scholar
122. McDonald D, Stockwin L, Matzow T, Blair Zajdel ME, Blair GE. Coxsackie and adenovirus receptor (CAR)-dependent and major histocompatibility complex (MHC) class I-independent uptake of recombinant adenoviruses into human tumour cells. Gene Ther. 6(9), 1512–1519 (1999).
Medline CASGoogle Scholar
123. Campadelli-Fiume G, Petrovic B, Leoni V et al. Retargeting strategies for oncolytic herpes simplex viruses. Viruses 8(3), 63 (2016).
MedlineGoogle Scholar
124. Pereyra AS, Mykhaylyk O, Lockhart EF et al. Magnetofection enhances adenoviral vector-based gene delivery in skeletal muscle cells. J. Nanomed. Nanotechnol. 7(2), 364 (2016).
MedlineGoogle Scholar
125. Muthana M, Scott SD, Farrow N et al. A novel magnetic approach to enhance the efficacy of cell-based gene therapies. Gene Ther. 15(12), 902–910 (2008).
Medline CASGoogle Scholar
126. Kim J, Hall RR, Lesniak MS, Ahmed AU. Stem cell-based cell carrier for targeted oncolytic virotherapy: translational opportunity and open questions. Viruses 7(12), 6200–6217 (2015).
Medline CASGoogle Scholar
127. Komarova S, Kawakami Y, Stoff-Khalili MA, Curiel DT, Pereboeva L. Mesenchymal progenitor cells as cellular vehicles for delivery of oncolytic adenoviruses. Mol. Cancer Ther. 5(3), 755–766 (2006).
Medline CASGoogle Scholar
128. Ahmed AU, Tyler MA, Thaci B et al. A comparative study of neural and mesenchymal stem cell-based carriers for oncolytic adenovirus in a model of malignant glioma. Mol. Pharm. 8(5), 1559–1572 (2011).
Medline CASGoogle Scholar
129. Mooney R, Majid AA, Batalla-Covello J et al. Enhanced delivery of oncolytic adenovirus by neural stem cells for treatment of metastatic ovarian cancer. Mol. Ther. Oncolytics 12, 79–92 (2019).
Medline CASGoogle Scholar
130. Batist G, Ramakrishnan G, Rao CS et al. Reduced cardiotoxicity and preserved antitumor efficacy of liposome-encapsulated doxorubicin and cyclophosphamide compared with conventional doxorubicin and cyclophosphamide in a randomized, multicenter trial of metastatic breast cancer. J. Clin. Oncol. 19(5), 1444–1454 (2001).
Medline CASGoogle Scholar
131. Gill PS, Wernz J, Scadden DT et al. Randomized Phase III trial of liposomal daunorubicin versus doxorubicin, bleomycin, and vincristine in AIDS-related Kaposi’s sarcoma. J. Clin. Oncol. 14(8), 2353–2364 (1996).
Medline CASGoogle Scholar
132. Koudelka S, Turanek J. Liposomal paclitaxel formulations. J. Control. Rel. 163(3), 322–334 (2012).
Medline CASGoogle Scholar
133. Frenkel V, Etherington A, Greene M et al. Delivery of liposomal doxorubicin (Doxil) in a breast cancer tumor model: investigation of potential enhancement by pulsed-high intensity focused ultrasound exposure. Acad. Radiol. 13(4), 469–479 (2006).
MedlineGoogle Scholar
134. Williams G, Cortazar P, Pazdur R. Developing drugs to decrease the toxicity of chemotherapy. J. Clin. Oncol. 19(14), 3439–3441 (2001).
Medline CASGoogle Scholar
135. Cosse JP, Michiels C. Tumour hypoxia affects the responsiveness of cancer cells to chemotherapy and promotes cancer progression. Anticancer Agents Med. Chem. 8(7), 790–797 (2008).
Medline CASGoogle Scholar
136. Baran N, Konopleva M. Molecular pathways: hypoxia-activated prodrugs in cancer therapy. Clin Cancer Res. 23(10), 2382–2390 (2017).
Medline CASGoogle Scholar
137. Hay JG. The potential impact of hypoxia on the success of oncolytic virotherapy. Curr. Opin. Mol. Ther. 7(4), 353–358 (2005).
Medline CASGoogle Scholar
138. Pin RH, Reinblatt M, Fong Y. Employing tumor hypoxia to enhance oncolytic viral therapy in breast cancer. Surgery 136(2), 199–204 (2004).
MedlineGoogle Scholar
139. Aghi MK, Liu TC, Rabkin S, Martuza RL. Hypoxia enhances the replication of oncolytic herpes simplex virus. Mol. Ther. 17(1), 51–56 (2009).
Medline CASGoogle Scholar
140. Saint-Cricq P, Deshayes S, Zink JI, Kasko AM. Magnetic field activated drug delivery using thermodegradable azo-functionalised PEG-coated core-shell mesoporous silica nanoparticles. Nanoscale 7(31), 13168–13172 (2015).
Medline CASGoogle Scholar
141. Chen P-J, Hu S-H, Hsiao C-S, Chen Y-Y, Liu D-M, Chen S-Y. Multifunctional magnetically removable nanogated lids of Fe₃O₄-capped mesoporous silica nanoparticles for intracellular controlled release and MR imaging. J. Mater. Chem. 21(8), 2535–2543 (2011). • The design of multifunctional nanodevices for tunable drug release.
CASGoogle Scholar
142. Lu YJ, Lin PY, Huang PH et al. Magnetic graphene oxide for dual targeted delivery of doxorubicin and photothermal therapy. Nanomaterials (Basel) 8(4), (2018).
Google Scholar
143. Lu Q, Dai X, Zhang P et al. Fe₃O₄@Au composite magnetic nanoparticles modified with cetuximab for targeted magneto-photothermal therapy of glioma cells. Int. J. Nanomed. 13, 2491–2505 (2018).
Medline CASGoogle Scholar
144. Zhang L, Sheng D, Wang D et al. Bioinspired multifunctional melanin-based nanoliposome for photoacoustic/magnetic resonance imaging-guided efficient photothermal ablation of cancer. Theranostics 8(6), 1591–1606 (2018).
Medline CASGoogle Scholar
145. Lu YJ, Wei KC, Ma CC, Yang SY, Chen JP. Dual targeted delivery of doxorubicin to cancer cells using folate-conjugated magnetic multi-walled carbon nanotubes. Colloids Surf. B Biointerfaces 89, 1–9 (2012).
Medline CASGoogle Scholar
146. Felfoul O, Mohammadi M, Taherkhani S et al. Magneto-aerotactic bacteria deliver drug-containing nanoliposomes to tumour hypoxic regions. Nat. Nanotechnol. 11(11), 941–947 (2016).
Medline CASGoogle Scholar
147. Yun WS, Choi JS, Ju HM et al. Enhanced homing technique of mesenchymal stem cells using iron oxide nanoparticles by magnetic attraction in olfactory-injured mouse models. Int. J. Mol. Sci. 19(5), (2018).
Google Scholar
148. Chen J, Huang N, Ma B et al. Guidance of stem cells to a target destination in vivo by magnetic nanoparticles in a magnetic field. ACS Appl. Mater. Interfaces 5(13), 5976–5985 (2013).
Medline CASGoogle Scholar
149. Toro-Cordova A, Flores-Cruz M, Santoyo-Salazar J et al. Liposomes loaded with cisplatin and magnetic nanoparticles: physicochemical characterization, pharmacokinetics, and in-vitro efficacy. Molecules 23(9), (2018).
MedlineGoogle Scholar
150. Li L, Jiang W, Luo K et al. Superparamagnetic iron oxide nanoparticles as MRI contrast agents for non-invasive stem cell labeling and tracking. Theranostics 3(8), 595–615 (2013).
MedlineGoogle Scholar
151. Hauser AK, Mitov MI, Daley EF, McGarry RC, Anderson KW, Hilt JZ. Targeted iron oxide nanoparticles for the enhancement of radiation therapy. Biomaterials 105, 127–135 (2016).
Medline CASGoogle Scholar
152. Alphandery E, Faure S, Seksek O, Guyot F, Chebbi I. Chains of magnetosomes extracted from AMB-1 magnetotactic bacteria for application in alternative magnetic field cancer therapy. ACS Nano 5(8), 6279–6296 (2011).
Medline CASGoogle Scholar
153. Alphandery E, Idbaih A, Adam C et al. Chains of magnetosomes with controlled endotoxin release and partial tumor occupation induce full destruction of intracranial U87-Luc glioma in mice under the application of an alternating magnetic field. J. Control. Rel. 262, 259–272 (2017).
Medline CASGoogle Scholar
154. Le Fevre R, Durand-Dubief M, Chebbi I et al. Enhanced antitumor efficacy of biocompatible magnetosomes for the magnetic hyperthermia treatment of glioblastoma. Theranostics 7(18), 4618–4631 (2017).
MedlineGoogle Scholar
155. Du X, Zhou J, Xu B. Ectoenzyme switches the surface of magnetic nanoparticles for selective binding of cancer cells. J. Colloid Interface Sci. 447, 273–277 (2015).
Medline CASGoogle Scholar
156. Muthana M, Kennerley AJ, Hughes R et al. Directing cell therapy to anatomic target sites in vivo with magnetic resonance targeting. Nat. Commun. 6, 8009 (2015). •• MRI scanners tracked and guided magnetically labeled macrophages from the bloodstream to tumors. Increased tumor macrophage number resulting in reduction in tumor burden.
Medline CASGoogle Scholar
157. Zablotskii V, Polyakova T, Lunov O, Dejneka A. How a high-gradient magnetic field could affect cell life. Sci. Rep. 6, 37407 (2016).
Medline CASGoogle Scholar
158. Erdal E, Demirbilek M, Yeh Y et al. A comparative study of receptor-targeted magnetosome and HSA-coated iron oxide nanoparticles as MRI contrast-enhancing agent in animal cancer model. Appl. Biochem. Biotechnol. 185(1), 91–113 (2018).
Medline CASGoogle Scholar
159. Sun JB, Duan JH, Dai SL et al. In vitro and in vivo antitumor effects of doxorubicin loaded with bacterial magnetosomes (DBMs) on H22 cells: the magnetic bio-nanoparticles as drug carriers. Cancer Lett. 258(1), 109–117 (2007).
Medline CASGoogle Scholar
160. Deng Q, Liu Y, Wang S et al. Construction of a novel magnetic targeting anti-tumor drug delivery system: cytosine arabinoside-loaded bacterial magnetosome. Materials (Basel) 6(9), 3755–3763 (2013).
Medline CASGoogle Scholar
161. Liu YG, Dai QL, Wang SB, Deng QJ, Wu WG, Chen AZ. Preparation and in vitro antitumor effects of cytosine arabinoside-loaded genipin-poly-l-glutamic acid-modified bacterial magnetosomes. Int. J. Nanomed. 10, 1387–1397 (2015).
Medline CASGoogle Scholar
162. Long RM, Dai QL, Zhou X et al. Bacterial magnetosomes-based nanocarriers for co-delivery of cancer therapeutics in vitro. Int. J. Nanomed. 13, 8269–8279 (2018).
Medline CASGoogle Scholar
163. Tang YS, Wang D, Zhou C et al. Bacterial magnetic particles as a novel and efficient gene vaccine delivery system. Gene Ther. 19(12), 1187–1195 (2012).
Medline CASGoogle Scholar

Vol. 15, No. 1

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Received 30 August 2019

Accepted 4 November 2019

Published online 23 December 2019

Published in print January 2020

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Financial & competing interests disclosure

Funding was received from Cancer Research UK (R/150024-11-1). The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed.

No writing assistance was utilized in the production of this manuscript.

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Designer nanocarriers for navigating the systemic delivery of oncolytic viruses

Abstract

References