The DOI matches its Crossref record; 78 of the 78 references it cites were found in a registry or an index.
Photodynamic Therapy Mediated by Nontoxic Core–Shell Nanoparticles Synergizes with Immune Checkpoint Blockade To Elicit Antitumor Immunity and Antimetastatic Effect on Breast Cancer
Open accessAbstract
An effective, nontoxic, tumor-specific immunotherapy is the ultimate goal in the battle against cancer, especially the metastatic disease. Checkpoint blockade-based immunotherapies have been shown to be extraordinarily effective but benefit only the minority of patients whose tumors have been pre-infiltrated by T cells. Here, we show that Zn-pyrophosphate (ZnP) nanoparticles loaded with the photosensitizer pyrolipid (ZnP@pyro) can kill tumor cells upon irradiation with light directly by inducing apoptosis and/or necrosis and indirectly by disrupting tumor vasculature and increasing tumor immunogenicity. Furthermore, immunogenic ZnP@pyro photodynamic therapy (PDT) treatment sensitizes tumors to checkpoint inhibition mediated by a PD-L1 antibody, not only eradicating the primary 4T1 breast tumor but also significantly preventing metastasis to the lung. The abscopal effects on both 4T1 and TUBO bilateral syngeneic mouse models further demonstrate that ZnP@pyro PDT treatment combined with anti-PD-L1 results in the eradication of light-irradiated primary tumors and the complete inhibition of untreated distant tumors by generating a systemic tumor-specific cytotoxic T cell response. These findings indicate that nanoparticle-mediated PDT can potentiate the systemic efficacy of checkpoint blockade immunotherapies by activating the innate and adaptive immune systems in tumor microenvironment.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
PD-1 and PD-L1 Immune Checkpoint Blockade to Treat Breast Cancer
Hartkopf, A. D., Taran, F.-A., Wallwiener, M., Walter, C. B., Krämer, B., Grischke, E.-M., & Brucker, S. Y. (2016) · Breast Care · doi:10.1159/000453569 · Cited by 30,845
The blockade of immune checkpoints in cancer immunotherapy
Pardoll, D. M. (2012) · Nature Reviews Cancer · doi:10.1038/nrc3239 · Cited by 13,838
Mutational landscape determines sensitivity to PD-1 blockade in non–small cell lung cancer
Rizvi, N. A., Hellmann, M. D., Snyder, A., Kvistborg, P., Makarov, V., Havel, J. J., Lee, W., Yuan, J., Wong, P., Ho, T. S., et al. (2015) · Science · doi:10.1126/science.aaa1348 · Cited by 7,802
Photodynamic therapy for cancer
Dolmans, D. E. J. G. J., Fukumura, D., & Jain, R. K. (2003) · Nature Reviews Cancer · doi:10.1038/nrc1071 · Cited by 6,758
PD-1 blockade induces responses by inhibiting adaptive immune resistance
Tumeh, P. C., Harview, C. L., Yearley, J. H., Shintaku, I. P., Taylor, E. J. M., Robert, L., Chmielowski, B., Spasic, M., Henry, G., Ciobanu, V., et al. (2014) · Nature · doi:10.1038/nature13954 · Cited by 6,609
The future of immune checkpoint therapy
Sharma, P., & Allison, J. P. (2015) · Science · doi:10.1126/science.aaa8172 · Cited by 4,878
Neoantigens in cancer immunotherapy
Schumacher, T. N., & Schreiber, R. D. (2015) · Science · doi:10.1126/science.aaa4971 · Cited by 4,783
Immune Checkpoint Blockade: A Common Denominator Approach to Cancer Therapy
Topalian, S. L., Drake, C. G., & Pardoll, D. M. (2015) · Cancer Cell · doi:10.1016/j.ccell.2015.03.001 · Cited by 4,229
Innate and adaptive immune cells in the tumor microenvironment
Gajewski, T. F., Schreiber, H., & Fu, Y.-X. (2013) · Nature Immunology · doi:10.1038/ni.2703 · Cited by 4,148
Molecular and genetic properties of tumors associated with local immune cytolytic activity
Rooney, M. S., Shukla, S. A., Wu, C. J., Getz, G., & Hacohen, N. (2015) · Cell · doi:10.1016/j.cell.2014.12.033 · Cited by 3,825
Immunogenic Cell Death in Cancer Therapy
Kroemer, G., Galluzzi, L., Kepp, O., & Zitvogel, L. (2013) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-100008 · Cited by 3,303
Calreticulin exposure dictates the immunogenicity of cancer cell death
Obeid, M., Tesniere, A., Ghiringhelli, F., Fimia, G. M., Apetoh, L., Perfettini, J.-L., Castedo, M., Mignot, G., Panaretakis, T., Casares, N., et al. (2007) · Nature Medicine · doi:10.1038/nm1523 · Cited by 3,216
Iwai, Y., Ishida, M., Tanaka, Y., Okazaki, T., Honjo, T., & Minato, N. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.192461099 · Cited by 3,203
Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy
Topalian, S. L., Taube, J. M., Anders, R. A., & Pardoll, D. M. (2016) · Nature Reviews Cancer · doi:10.1038/nrc.2016.36 · Cited by 2,733
Photodynamic therapy and anti-tumour immunity
Castano, A. P., Mroz, P., & Hamblin, M. R. (2006) · Nature Reviews Cancer · doi:10.1038/nrc1894 · Cited by 2,676
T cell exclusion, immune privilege, and the tumor microenvironment
Joyce, J. A., & Fearon, D. T. (2015) · Science · doi:10.1126/science.aaa6204 · Cited by 2,473
Maeda, H., Nakamura, H., & Fang, J. (2013) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2012.10.002 · Cited by 2,376
Imaging and Photodynamic Therapy: Mechanisms, Monitoring, and Optimization
Celli, J. P., Spring, B. Q., Rizvi, I., Evans, C. L., Samkoe, K. S., Verma, S., Pogue, B. W., & Hasan, T. (2010) · Chemical Reviews · doi:10.1021/cr900300p · Cited by 2,324
Breast cancer statistics, 2013
DeSantis, C., Ma, J., Bryan, L., & Jemal, A. (2014) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.21203 · Cited by 2,143
Couzin-Frankel, J. (2013) · Science · doi:10.1126/science.342.6165.1432 · Cited by 2,051
Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens
Gubin, M. M., Zhang, X., Schuster, H., Caron, E., Ward, J. P., Noguchi, T., Ivanova, Y., Hundal, J., Arthur, C. D., Krebber, W.-J., et al. (2014) · Nature · doi:10.1038/nature13988 · Cited by 1,974
Adoptive immunotherapy for cancer: harnessing the T cell response
Restifo, N. P., Dudley, M. E., & Rosenberg, S. A. (2012) · Nature Reviews Immunology · doi:10.1038/nri3191 · Cited by 1,688
Nanoshell-Enabled Photothermal Cancer Therapy: Impending Clinical Impact
Lal, S., Clare, S. E., & Halas, N. J. (2008) · Accounts of Chemical Research · doi:10.1021/ar800150g · Cited by 1,625
Combining immunotherapy and targeted therapies in cancer treatment
Vanneman, M., & Dranoff, G. (2012) · Nature Reviews Cancer · doi:10.1038/nrc3237 · Cited by 1,586
Nanoparticle Delivery of Cancer Drugs
Wang, A. Z., Langer, R., & Farokhzad, O. C. (2012) · Annual Review of Medicine · doi:10.1146/annurev-med-040210-162544 · Cited by 1,561
In vivo photodynamic therapy using upconversion nanoparticles as remote-controlled nanotransducers
Idris, N. M., Gnanasammandhan, M. K., Zhang, J., Ho, P. C., Mahendran, R., & Zhang, Y. (2012) · Nature Medicine · doi:10.1038/nm.2933 · Cited by 1,464
Lovell, J. F., Jin, C. S., Huynh, E., Jin, H., Kim, C., Rubinstein, J. L., Chan, W. C. W., Cao, W., Wang, L. V., & Zheng, G. (2011) · Nature Materials · doi:10.1038/nmat2986 · Cited by 1,362
Targeting the PD-1/B7-H1(PD-L1) pathway to activate anti-tumor immunity
Topalian, S. L., Drake, C. G., & Pardoll, D. M. (2012) · Current Opinion in Immunology · doi:10.1016/j.coi.2011.12.009 · Cited by 1,329
Nanoparticles in photodynamic therapy: An emerging paradigm
Chatterjee, D. K., Fong, L. S., & Zhang, Y. (2008) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2008.08.003 · Cited by 1,184
History of myeloid-derived suppressor cells
Talmadge, J. E., & Gabrilovich, D. I. (2013) · Nature Reviews Cancer · doi:10.1038/nrc3581 · Cited by 1,148
Chen, J., Wang, D., Xi, J., Au, L., Siekkinen, A., Warsen, A., Li, Z.-Y., Zhang, H., Xia, Y., & Li, X. (2007) · Nano Letters · doi:10.1021/nl070345g · Cited by 1,025
Immunogenic Chemotherapy Sensitizes Tumors to Checkpoint Blockade Therapy
Pfirschke, C., Engblom, C., Rickelt, S., Cortez-Retamozo, V., Garris, C., Pucci, F., Yamazaki, T., Poirier-Colame, V., Newton, A., Redouane, Y., et al. (2016) · Immunity · doi:10.1016/j.immuni.2015.11.024 · Cited by 952
Duan, X., & Li, Y. (2013) · Small · doi:10.1002/smll.201201390 · Cited by 926
Self-citationPulaski, B. A., & Ostrand‐Rosenberg, S. (2000) · Current Protocols in Immunology · doi:10.1002/0471142735.im2002s39 · Cited by 912
Zitvogel, L., Galluzzi, L., Smyth, M. J., & Kroemer, G. (2013) · Immunity · doi:10.1016/j.immuni.2013.06.014 · Cited by 870
Semiconductor Quantum Dots for Photodynamic Therapy
Samia, A. C. S., Chen, X., & Burda, C. (2003) · Journal of the American Chemical Society · doi:10.1021/ja0386905 · Cited by 813
A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death
Garg, A. D., Krysko, D. V., Verfaillie, T., Kaczmarek, A., Ferreira, G. B., Marysael, T., Rubio, N., Firczuk, M., Mathieu, C., Roebroek, A. J. M., et al. (2012) · The EMBO Journal · doi:10.1038/emboj.2011.497 · Cited by 800
Kulkarni, S. A., & Feng, S.-S. (2013) · Pharmaceutical Research · doi:10.1007/s11095-012-0958-3 · Cited by 768
He, C., Duan, X., Guo, N., Chan, C., Poon, C., Weichselbaum, R. R., & Lin, W. (2016) · Nature Communications · doi:10.1038/ncomms12499 · Cited by 754
Self-citationRegulatory T cells in cancer immunotherapy
Nishikawa, H., & Sakaguchi, S. (2014) · Current Opinion in Immunology · doi:10.1016/j.coi.2013.12.005 · Cited by 705
Ma, Y., Adjemian, S., Mattarollo, S. R., Yamazaki, T., Aymeric, L., Yang, H., Portela Catani, J. P., Hannani, D., Duret, H., Steegh, K., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.03.003 · Cited by 699
Blank, C., Gajewski, T. F., & Mackensen, A. (2005) · Cancer Immunology, Immunotherapy · doi:10.1007/s00262-004-0593-x · Cited by 637
Latchman, Y. E., Liang, S. C., Wu, Y., Chernova, T., Sobel, R. A., Klemm, M., Kuchroo, V. K., Freeman, G. J., & Sharpe, A. H. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307252101 · Cited by 636
The therapeutic effect of anti-HER2/neu antibody depends on both innate and adaptive immunity
Park, S., Jiang, Z., Mortenson, E. D., Deng, L., Radkevich-Brown, O., Yang, X., Sattar, H., Wang, Y., Brown, N. K., Greene, M., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2010.06.014 · Cited by 577
Imagable 4T1 model for the study of late stage breast cancer
Tao, K., Fang, M., Alroy, J., & Sahagian, G. G. (2008) · BMC Cancer · doi:10.1186/1471-2407-8-228 · Cited by 525
Lu, K., He, C., Guo, N., Chan, C., Ni, K., Weichselbaum, R. R., & Lin, W. (2016) · Journal of the American Chemical Society · doi:10.1021/jacs.6b06663 · Cited by 505
Self-citationSagiv-Barfi, I., Kohrt, H. E. K., Czerwinski, D. K., Ng, P. P., Chang, B. Y., & Levy, R. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1500712112 · Cited by 444
Chemophototherapy: An Emerging Treatment Option for Solid Tumors
Luo, D., Carter, K. A., Miranda, D., & Lovell, J. F. (2017) · Advanced Science · doi:10.1002/advs.201600106 · Cited by 436
Cancer immunotherapy strategies based on overcoming barriers within the tumor microenvironment
Gajewski, T. F., Woo, S.-R., Zha, Y., Spaapen, R., Zheng, Y., Corrales, L., & Spranger, S. (2013) · Current Opinion in Immunology · doi:10.1016/j.coi.2013.02.009 · Cited by 422
Tian, J., Ding, L., Xu, H.-J., Shen, Z., Ju, H., Jia, L., Bao, L., & Yu, J.-S. (2013) · Journal of the American Chemical Society · doi:10.1021/ja408286k · Cited by 416
Predictive biomarkers in PD-1/PD-L1 checkpoint blockade immunotherapy
Meng, X., Huang, Z., Teng, F., Xing, L., & Yu, J. (2015) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2015.11.001 · Cited by 401
The Smart Targeting of Nanoparticles
Friedman, A., Claypool, S., & Liu, R. (2013) · Current Pharmaceutical Design · doi:10.2174/13816128113199990375 · Cited by 364
Nanodrug applications in photodynamic therapy
Paszko, E., Ehrhardt, C., Senge, M. O., Kelleher, D. P., & Reynolds, J. V. (2011) · Photodiagnosis and Photodynamic Therapy · doi:10.1016/j.pdpdt.2010.12.001 · Cited by 356
Role of cytokines in photodynamic therapy-induced local and systemic inflammation
Gollnick, S. O., Evans, S. S., Baumann, H., Owczarczak, B., Maier, P., Vaughan, L., Wang, W. C., Unger, E., & Henderson, B. W. (2003) · British Journal of Cancer · doi:10.1038/sj.bjc.6600864 · Cited by 348
Stuchinskaya, T., Moreno, M., Cook, M. J., Edwards, D. R., & Russell, D. A. (2011) · Photochemical & Photobiological Sciences · doi:10.1039/c1pp05014a · Cited by 329
Photodynamic therapy: illuminating the road from cell death towards anti-tumour immunity
Garg, A. D., Nowis, D., Golab, J., & Agostinis, P. (2010) · Apoptosis · doi:10.1007/s10495-010-0479-7 · Cited by 297
Garg, A. D., & Agostinis, P. (2014) · Photochemical & Photobiological Sciences · doi:10.1039/c3pp50333j · Cited by 276
Stimulation of anti-tumor immunity by photodynamic therapy
Mroz, P., Hashmi, J. T., Huang, Y.-Y., Lange, N., & Hamblin, M. R. (2011) · Expert Review of Clinical Immunology · doi:10.1586/eci.10.81 · Cited by 261
EPR-effect: Utilizing size-dependent Nanoparticle Delivery to Solid Tumors
Stylianopoulos, T. (2013) · Therapeutic Delivery · doi:10.4155/tde.13.8 · Cited by 197
Bio-nanotechnology and photodynamic therapy—State of the art review
Allison, R. R., Mota, H. C., Bagnato, V. S., & Sibata, C. H. (2008) · Photodiagnosis and Photodynamic Therapy · doi:10.1016/j.pdpdt.2008.02.001 · Cited by 181
“Targeting” nanoparticles: The constraints of physical laws and physical barriers
Florence, A. T. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2012.03.022 · Cited by 179
Triple-Negative Breast Carcinoma
Schmadeka, R., Harmon, B. E., & Singh, M. (2014) · American Journal of Clinical Pathology · doi:10.1309/ajcpqn8gz8silkgn · Cited by 167
Enhancement of anti-tumor immunity by photodynamic therapy
Gollnick, S. O., & Brackett, C. M. (2010) · Immunologic Research · doi:10.1007/s12026-009-8119-4 · Cited by 163
Synthetic analogues of migrastatin that inhibit mammary tumor metastasis in mice
Shan, D., Chen, L., Njardarson, J. T., Gaul, C., Ma, X., Danishefsky, S. J., & Huang, X.-Y. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500658102 · Cited by 163
Vascular calcification is dependent on plasma levels of pyrophosphate
Lomashvili, K. A., Narisawa, S., Millán, J. L., & O'Neill, W. C. (2014) · Kidney International · doi:10.1038/ki.2013.521 · Cited by 162
Pyropheophorbide 2-Deoxyglucosamide: A New Photosensitizer Targeting Glucose Transporters
Zhang, M., Zhang, Z., Blessington, D. M., Li, H., Busch, T. M., Madrak, V., Miles, J. D., Chance, B., Glickson, J. D., & Zheng, G. (2003) · Bioconjugate Chemistry · doi:10.1021/bc034038n · Cited by 154
Targeting‐Triggered Porphysome Nanostructure Disruption for Activatable Photodynamic Therapy
Jin, C. S., Cui, L., Wang, F., Chen, J., & Zheng, G. (2014) · Advanced Healthcare Materials · doi:10.1002/adhm.201300651 · Cited by 153
Molecularly targeted therapies for metastatic triple-negative breast cancer
Bayraktar, S., & Glück, S. (2013) · Breast Cancer Research and Treatment · doi:10.1007/s10549-013-2421-5 · Cited by 147
Enlightening the impact of immunogenic cell death in photodynamic cancer therapy
Galluzzi, L., Kepp, O., & Kroemer, G. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.2 · Cited by 142
The immune checkpoint inhibitors: where are we now?
Webster, R. M. (2014) · Nature Reviews Drug Discovery · doi:10.1038/nrd4476 · Cited by 140
Sian, L., Mingyan, X., Miller, L. V., Tong, L., Krebs, N., & Hambidge, K. M. (1996) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/63.3.348 · Cited by 137
Sanabria, L. M., Rodríguez, M. E., Cogno, I. S., Vittar, N. B. R., Pansa, M. F., Lamberti, M. J., & Rivarola, V. A. (2012) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2012.10.001 · Cited by 123
Shams, M., Owczarczak, B., Manderscheid, P. A., Bellnier, D. A., & Gollnick, S. O. (2014) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-014-1633-9 · Cited by 114
Shahabi, V., Postow, M. A., Tuck, D. P., & Wolchok, J. D. (2013) · American Journal of Clinical Oncology · doi:10.1097/coc.0b013e3182868ec8 · Cited by 86
Hirsjärvi, S., Dufort, S., Gravier, J., Texier, I., Yan, Q., Bibette, J., Sancey, L., Josserand, V., Passirani, C., Benoît, J., et al. (2012) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2012.08.005 · Cited by 77
Yom, S. S., Busch, T. M., Friedberg, J. S., Wileyto, E. P., Smith, D., GLATSTEIN, E. J., & Hahn, S. M. (2003) · Photochemistry and Photobiology · doi:10.1562/0031-8655(2003)0780075esclim2.0.co2 · Cited by 55
Immunotherapy: a way to improve the therapeutic outcome of photodynamic therapy?
Kwitniewski, M., Juzeniene, A., Głośnicka, R., & Moan, J. E. (2008) · Photochemical & Photobiological Sciences · doi:10.1039/b806710d · Cited by 51
Leventakos, K., & Mansfield, A. S. (2016) · BioDrugs · doi:10.1007/s40259-016-0187-0 · Cited by 43
Cited by
Metal–Organic Framework (MOF)‐Based Drug/Cargo Delivery and Cancer Therapy
Wu, M., & Yang, Y. (2017) · Advanced Materials · doi:10.1002/adma.201606134 · Cited by 2,285
Tumor targeting via EPR: Strategies to enhance patient responses
Golombek, S. K., May, J.-N., Theek, B., Appold, L., Drude, N., Kiessling, F., & Lammers, T. (2018) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2018.07.007 · Cited by 1,262
Cancer nanomedicine for combination cancer immunotherapy
Nam, J., Son, S., Park, K. S., Zou, W., Shea, L. D., & Moon, J. J. (2019) · Nature Reviews Materials · doi:10.1038/s41578-019-0108-1 · Cited by 940
Recent Advances in Tumor Targeting via EPR Effect for Cancer Treatment
Subhan, M. A., Yalamarty, S. S. K., Filipczak, N., Parveen, F., & Torchilin, V. P. (2021) · Journal of Personalized Medicine · doi:10.3390/jpm11060571 · Cited by 623
Yue, W., Chen, L., Yu, L., Zhou, B., Yin, H., Ren, W., Liu, C., Guo, L., Zhang, Y., Sun, L., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09760-3 · Cited by 590
Metadata
- Authors
- Duan, X., Chan, C., Guo, N., Han, W., Weichselbaum, R. R., & Lin, W.
- Venue
- Journal of the American Chemical Society
- Publisher
- American Chemical Society (ACS)
- Published
- 2016-12-15
- Volume
- 138
- Issue
- 51
- Pages
- 16686-16695
- ISSN
- 0002-7863 (ISSN-L)
- 1520-5126
- OpenAlex
- W2558284519
- Cited by
- 458
- References
- 78
- FWCI
- 19.00
- Type
- journal article
- Language
- en
- Open access
- green
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.