In situ vaccination with cowpea mosaic virus nanoparticles suppresses metastatic cancer

Nature Nanotechnology

Volumn 11, Issue 3, 2016, Pages 295-303

  Lizotte, P H ^a   Wen, A M ^b   Sheen, M R ^a   Fields, J ^a   Rojanasopondist, P ^a   Steinmetz, N F ^b,c   Fiering, S ^a,d  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

^d NORRIS COTTON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DISEASES; NANOPARTICLES; TUMORS; VACCINES; VIRUSES;

ADAPTIVE IMMUNITY; CANCER IMMUNOTHERAPY; COWPEA MOSAIC VIRUS; IMMUNE RESPONSE; IMMUNOGENICITY; METASTATIC CANCERS; MICROENVIRONMENTS; SELF-ASSEMBLING;

DRUG DELIVERY;

GAMMA INTERFERON; INTERLEUKIN 12; NANOPARTICLE; TYROSINASE RELATED PROTEIN 1; VIRUS LIKE PARTICLE VACCINE; CANCER VACCINE; VIRUS VACCINE;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST TUMOR; CANCER IMMUNOTHERAPY; COLON TUMOR; CONTROLLED STUDY; COWPEA MOSAIC VIRUS; DRUG EFFICACY; IMMUNOGENICITY; MELANOMA; METASTASIS; MOUSE; NANOPHARMACEUTICS; NEUTROPHIL; NONHUMAN; OVARY TUMOR; PRIORITY JOURNAL; TUMOR MICROENVIRONMENT; VACCINATION; ANIMAL; C57BL MOUSE; CHEMISTRY; COMOVIRUS; FEMALE; NEOPLASMS, EXPERIMENTAL; PATHOLOGY; PROCEDURES; SECONDARY; TREATMENT OUTCOME; TUMOR CELL LINE;

ANIMALS; CANCER VACCINES; CELL LINE, TUMOR; COMOVIRUS; FEMALE; MICE; MICE, INBRED C57BL; NANOPARTICLES; NEOPLASMS, EXPERIMENTAL; TREATMENT OUTCOME; VACCINATION; VIRAL VACCINES;

EID: 84960114076     PISSN: 17483387     EISSN: 17483395     Source Type: Journal    
DOI: 10.1038/nnano.2015.292     Document Type: Article

References (49)

1. Pardoll, D. M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 12, 252-264 (2012
2. Kershaw, M. H., Westwood, J. A., & Darcy, P. K. Gene-engineered T cells for cancer therapy. Nat. Rev. Cancer 13, 525-541 (2013
3. Ali, O. A., et al. Identification of immune factors regulating antitumor immunity using polymeric vaccines with multiple adjuvants. Cancer Res. 74, 1670-1681 (2014
4. Callahan, M. K., Postow, M. A., & Wolchok, J. D. CTLA-4 and PD-1 pathway blockade: combinations in the clinic. Front. Oncol. 4, (2015
5. Winograd, R., et al. Induction of T cell immunity overcomes complete resistance to PD-1 and CTLA-4 blockade and improves survival in pancreatic carcinoma. Cancer Immunol. Res. 3, 399-411 (2015
6. Robert, C., et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N. Engl. J. Med. 364, 2517-2526 (2011
7. Andtbacka, R. H. I., et al. Talimogene laherparepvec improves durable response rate in patients with advanced melanoma. J. Clin. Oncol. 33, 2780-2788 (2015
8. Corrales, L., et al. Direct activation of STING in the tumor microenvironment leads to potent and systemic tumor regression and immunity. Cell Rep. 11, 1018-1030 (2015
9. Sheen, M. R., Lizotte, P. H., Toraya-Brown, S., & Fiering, S. Stimulating antitumor immunity with nanoparticles. WIREs Nanomed. Nanobiotechnol. 6, 496-505 (2014
10. Halperin, S. A., et al. Comparison of safety and immunogenicity of two doses of investigational hepatitis B virus surface antigen co-Administered with an immunostimulatory phosphorothioate oligodeoxyribonucleotide and three doses of a licensed hepatitis B vaccine in healthy adults 18-55 years of age. Vaccine 30, 2556-2563 (2012
11. Huber, B., et al. A chimeric 18L1-45RG1 virus-like particle vaccine cross-protects against oncogenic alpha-7 human papillomavirus types. PLoS ONE 10, e0120152 (2015
12. Rynda-Apple, A., Patterson, D. P., & Douglas, T. Virus-like particles as antigenic nanomaterials for inducing protective immune responses in the lung. Nanomed. 9, 1857-1868 (2014
13. Rynda-Apple, A., et al. Virus-like particle-induced protection against MRSA pneumonia is dependent on IL-13 and enhancement of phagocyte function. Am. J. Pathol. 181, 196-210 (2012
14. Wiley, J. A., et al. Inducible bronchus-Associated lymphoid tissue elicited by a protein cage nanoparticle enhances protection in mice against diverse respiratory viruses. PLoS ONE 4, e7142 (2009
15. Patterson, D. P., Rynda-Apple, A., Harmsen, A. L., Harmsen, A. G., & Douglas, T. Biomimetic antigenic nanoparticles elicit controlled protective immune response to influenza. ACS Nano 7, 3036-3044 (2013
16. Richert, L. E., et al. CD11c+ cells primed with unrelated antigens facilitate an accelerated immune response to influenza virus in mice. Eur. J. Immunol. 44, 397-408 (2014
17. Saunders, K., Sainsbury, F., & Lomonossoff, G. P. Efficient generation of cowpea mosaicvirus empty virus-like particles by the proteolytic processing of precursors in insect cells and plants. Virology 393, 329-337 (2009
18. Aljabali, A. A. A., Shukla, S., Lomonossoff, G. P., Steinmetz, N. F., & Evans, D. J. CPMV-DOX delivers. Mol. Pharm. 10, 3-10 (2013
19. Yildiz, I., Lee, K. L., Chen, K., Shukla, S., & Steinmetz, N. F. Infusion of imaging and therapeutic molecules into the plant virus-based carrier cowpea mosaic virus: Cargo-loading and delivery. J. Controlled Release 172, 568-578 (2013
20. Costantini, C., et al. Neutrophil activation and survival are modulated by interaction with NK cells. Int. Immunol. 22, 827-838 (2010
21. Gabrilovich, D. I., Ostrand-Rosenberg, S., & Bronte, V. Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 12, 253-268 (2012
22. Fridlender, Z. G., et al. Polarization of tumor-Associated neutrophil (TAN) phenotype by TGF-β: N1 versus N2 TAN. Cancer Cell 16, 183-194 (2009
23. Mantovani, A., Cassatella, M. A., Costantini, C., & Jaillon, S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11, 519-531 (2011
24. Zhu, M.-L., Nagavalli, A., & Su, M. A. Aire deficiency promotes TRP-1-specific immune rejection of melanoma. Cancer Res. 73, 2104-2116 (2013
25. Conejo-Garcia, J R., et al. Tumor-infiltrating dendritic cell precursors recruited by a β-defensin contribute to vasculogenesis under the influence of Vegf-A. Nature Med. 10, 950-958 (2004
26. Lebel, M.-È., et al. Nanoparticle adjuvant sensing by TLR7 enhances CD8+ T cell-mediated protection from listeria monocytogenes infection. J. Immunol. 192, 1071-1078 (2014
27. Link, A., et al. Innate immunity mediates follicular transport of particulate but not soluble protein antigen. J. Immunol. 188, 3724-3733 (2012
28. Wu, G. J., & Bruening, G. Two proteins from cowpea mosaic virus. Virology 46, 596-612 (1971
29. Steinmetz, N. F., Cho, C.-F., Ablack, A., Lewis, J. D., & Manchester, M. Cowpea mosaic virus nanoparticles target surface vimentin on cancer cells. Nanomed. 6, 351-364 (2011
30. Satelli, A., & Li, S. Vimentin in cancer and its potential as a molecular target for cancer therapy. Cell. Mol. Life Sci. 68, 3033-3046 (2011
31. Gonzalez, M. J., Plummer, E. M., Rae, C. S., & Manchester, M. Interaction of cowpea mosaic virus (CPMV) nanoparticles with antigen presenting cells in vitro and in vivo. PLoS ONE 4, e7981 (2009
32. Jablonska, J., Leschner, S., Westphal, K., Lienenklaus, S., & Weiss, S. Neutrophils responsive to endogenous IFN-β regulate tumor angiogenesis and growth in a mouse tumor model. J. Clin. Invest. 120, 1151-1164 (2010
33. Kuang, D.-M., et al. Peritumoral neutrophils link inflammatory response to disease progression by fostering angiogenesis in hepatocellular carcinoma. J. Hepatol. 54, 948-955 (2011
34. Pekarek, L. A., Starr, B. A., Toledano, A. Y., & Schreiber, H. Inhibition of tumor growth by elimination of granulocytes. J. Exp. Med. 181, 435-440 (1995
35. Wislez, M., et al. Hepatocyte growth factor production by neutrophils infiltrating bronchioloalveolar subtype pulmonary adenocarcinoma role in tumor progression and death. Cancer Res. 63, 1405-1412 (2003
36. Abdallah, D. S. A., Egan, C. E., Butcher, B. A., & Denkers, E. Y. Mouse neutrophils are professional antigen-presenting cells programmed to instruct Th1 and Th17 T-cell differentiation. Int. Immunol. 23, 317-326 (2011
37. van Gisbergen, K. P. J. M., Sanchez-Hernandez, M., Geijtenbeek, T. B. H., & van Kooyk, Y. Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J. Exp. Med. 201, 1281-1292 (2005
38. Beauvillain, C., et al. Neutrophils efficiently cross-prime naive T cells in vivo. Blood 110, 2965-2973 (2007
39. Pelletier, M., et al. Evidence for a cross-Talk between human neutrophils and Th17 cells. Blood 115, 335-343 (2010
40. Clancy-Thompson, E., et al. Peptide vaccination in montanide adjuvant induces and GM-CSF increases CXCR3 and cutaneous lymphocyte antigen expression by tumor antigen-specific CD8 T cells. Cancer Immunol. Res. 1, 332-339 (2013
41. Baird, J. R., et al. Immune-mediated regression of established B16F10 melanoma by intratumoral injection of attenuated toxoplasma gondii protects against rechallenge. J. Immunol. 190, 469-478 (2013
42. Caramori, G., Adcock, I. M., Di Stefano, A., & Chung, K. F. Cytokine inhibition in the treatment of COPD. Int. J. Chron. Obstruct. Pulmon. Dis. 9, 397-412 (2014
43. Lizotte, P. H., et al. Attenuated Listeria monocytogenes reprograms M2-polarized tumor-Associated macrophages in ovarian cancer leading to iNOS-mediated tumor cell lysis. Oncoimmunology 3, (2014
44. Baird, J. R., et al. Avirulent toxoplasma gondii generates therapeutic antitumor immunity by reversing immunosuppression in the ovarian cancer microenvironment. Cancer Res. 73, 3842-3851 (2013
45. Scarlett, U. K., et al. In situ stimulation of CD40 and toll-like receptor 3 transforms ovarian cancer-infiltrating dendritic cells from immunosuppressive to immunostimulatory cells. Cancer Res. 69, 7329-7337 (2009
46. Hart, K., Byrne, K., Molloy, M., Usherwood, E., & Berwin, B. IL-10 immunomodulation of myeloid cells regulates a murine model of ovarian cancer. T Cell Biol. 2, 29 (2011
47. Sainsbury, F., et al. Genetic engineering and characterisation of Cowpea mosaic virus empty virus-like particles. Methods Mol Biol Clifton NJ. 1108, 139-153 (2014
48. Lizotte, P. H., et al. Attenuated Listeria monocytogenes reprograms M2-polarized tumour-Associated macrophages in ovarian cancer leading to iNOSmediated tumour cell lysis. Oncoimmunology 3, e28926 (2014)
49. Pulaski, B. A., & Ostrand-Rosenberg, S. in Current Protocols in Immunology (eds Cooligan, J. E., et al.) 39: 20.2: 20.2.1-20.2.16 (John Wiley & Sons, 2001); http://onlinelibrary.wiley.com/doi/10.1002/0471142735.im2002s39/abstract