Synergistic Transcutaneous Immunotherapy Enhances Antitumor Immune Responses through Delivery of Checkpoint Inhibitors

ACS Nano

Volumn 10, Issue 9, 2016, Pages 8956-8963

  Ye, Yanqi ^a,b   Wang, Jinqiang ^a,b   Hu, Quanyin ^a,b   Hochu, Gabrielle M ^a   Xin, Hongliang ^a   Wang, Chao ^a,b   Gu, Zhen ^a,b,c  

^a USA and North Carolina State University   (United States)

^b University of North Carolina   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

anti PD1; drug delivery; IDO; immunotherapy; microneedle

Indexed keywords

CELL DEATH; DERMATOLOGY; DRUG DELIVERY; HYALURONIC ACID; NEEDLES; ONCOLOGY; T-CELLS;

ANTI-PD1; COMBINATION STRATEGIES; IMMUNOTHERAPY; INDOLEAMINE 2 ,3-DIOXYGENASE; MICRONEEDLES; PROGRAMMED CELL DEATHS; TRANSCUTANEOUS DELIVERY; TUMOR MICROENVIRONMENT;

DRUG PRODUCTS;

INDOLEAMINE 2,3 DIOXYGENASE; PROGRAMMED DEATH 1 RECEPTOR;

ANIMAL; CELL CYCLE CHECKPOINT; DRUG DELIVERY SYSTEM; DRUG EFFECT; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; MELANOMA; PROCEDURES; SKIN TUMOR; TUMOR MICROENVIRONMENT;

ANIMALS; CELL CYCLE CHECKPOINTS; DRUG DELIVERY SYSTEMS; IMMUNOSUPPRESSION; IMMUNOTHERAPY; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; MELANOMA; PROGRAMMED CELL DEATH 1 RECEPTOR; SKIN NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84989172005     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.6b04989     Document Type: Article

References (43)

1. Topalian, S. L.; Drake, C. G.; Pardoll, D. M. Immune Checkpoint Blockade: A Common Denominator Approach to Cancer Therapy Cancer Cell 2015, 27, 450-461 10.1016/j.ccell.2015.03.001
2. Cheung, A. S.; Mooney, D. J. Engineered Materials for Cancer Immunotherapy Nano Today 2015, 10, 511-531 10.1016/j.nantod.2015.06.007
3. Jeanbart, L.; Swartz, M. A. Engineering Opportunities in Cancer Immunotherapy Proc. Natl. Acad. Sci. U. S. A. 2015, 112, 14467-14472 10.1073/pnas.1508516112
4. Koshy, S. T.; Mooney, D. J. Biomaterials for Enhancing Anti-Cancer Immunity Curr. Opin. Biotechnol. 2016, 40, 1-8 10.1016/j.copbio.2016.02.001
5. Sharma, P.; Allison, J. P. The Future of Immune Checkpoint Therapy Science 2015, 348, 56-61 10.1126/science.aaa8172
6. Sharma, P.; Allison; James, P. Immune Checkpoint Targeting in Cancer Therapy: Toward Combination Strategies with Curative Potential Cell 2015, 161, 205-214 10.1016/j.cell.2015.03.030
7. Zou, W.; Wolchok, J. D.; Chen, L. PD-L1 (B7-H1) and PD-1 Pathway Blockade for Cancer Therapy: Mechanisms, Response Biomarkers, and Combinations Sci. Transl. Med. 2016, 8, 328-328 10.1126/scitranslmed.aad7118
8. Buchbinder, E. I.; Hodi, F. S. Melanoma in 2015: Immune-Checkpoint Blockade-Durable Cancer Control Nat. Rev. Clin. Oncol. 2016, 13, 77-78 10.1038/nrclinonc.2015.237
9. Larkin, J.; Chiarion-Sileni, V.; Gonzalez, R.; Grob, J. J.; Cowey, C. L.; Lao, C. D.; Schadendorf, D.; Dummer, R.; Smylie, M.; Rutkowski, P.; Ferrucci, P. F.; Hill, A.; Wagstaff, J.; Carlino, M. S.; Haanen, J. B.; Maio, M.; Marquez-Rodas, I.; McArthur, G. A.; Ascierto, P. A.; Long, G. V. et al. Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma N. Engl. J. Med. 2015, 373, 23-34 10.1056/NEJMoa1504030
10. Sullivan, R. J.; Flaherty, K. T. Immunotherapy: Anti-PD-1 Therapies-a New First-Line Option in Advanced Melanoma Nat. Rev. Clin. Oncol. 2015, 12, 625-626 10.1038/nrclinonc.2015.170
11. Rosenberg, J. E.; Hoffman-Censits, J.; Powles, T.; van der Heijden, M. S.; Balar, A. V.; Necchi, A.; Dawson, N.; O'Donnell, P. H.; Balmanoukian, A.; Loriot, Y.; Srinivas, S.; Retz, M. M.; Grivas, P.; Joseph, R. W.; Galsky, M. D.; Fleming, M. T.; Petrylak, D. P.; Perez-Gracia, J. L.; Burris, H. A.; Castellano, D. et al. Atezolizumab in Patients with Locally Advanced and Metastatic Urothelial Carcinoma Who Have Progressed Following Treatment with Platinum-Based Chemotherapy: a Single-Arm, Multicentre, Phase 2 Trial Lancet 2016, 387, 1909-1920 10.1016/S0140-6736(16)00561-4
12. Postow, M. A.; Chesney, J.; Pavlick, A. C.; Robert, C.; Grossmann, K.; McDermott, D.; Linette, G. P.; Meyer, N.; Giguere, J. K.; Agarwala, S. S.; Shaheen, M.; Ernstoff, M. S.; Minor, D.; Salama, A. K.; Taylor, M.; Ott, P. A.; Rollin, L. M.; Horak, C.; Gagnier, P.; Wolchok, J. D. et al. Nivolumab and Ipilimumab versus Ipilimumab in Untreated Melanoma N. Engl. J. Med. 2015, 372, 2006-2017 10.1056/NEJMoa1414428
13. Robert, C.; Schachter, J.; Long, G. V.; Arance, A.; Grob, J. J.; Mortier, L.; Daud, A.; Carlino, M. S.; McNeil, C.; Lotem, M.; Larkin, J.; Lorigan, P.; Neyns, B.; Blank, C. U.; Hamid, O.; Mateus, C.; Shapira-Frommer, R.; Kosh, M.; Zhou, H.; Ibrahim, N. et al. Pembrolizumab versus Ipilimumab in Advanced Melanoma N. Engl. J. Med. 2015, 372, 2521-2532 10.1056/NEJMoa1503093
14. Le, D. T.; Uram, J. N.; Wang, H.; Bartlett, B. R.; Kemberling, H.; Eyring, A. D.; Skora, A. D.; Luber, B. S.; Azad, N. S.; Laheru, D.; Biedrzycki, B.; Donehower, R. C.; Zaheer, A.; Fisher, G. A.; Crocenzi, T. S.; Lee, J. J.; Duffy, S. M.; Goldberg, R. M.; de la Chapelle, A.; Koshiji, M. et al. PD-1 Blockade in Tumors with Mismatch-Repair Deficiency N. Engl. J. Med. 2015, 372, 2509-2520 10.1056/NEJMoa1500596
15. Spranger, S.; Spaapen, R. M.; Zha, Y.; Williams, J.; Meng, Y.; Ha, T. T.; Gajewski, T. F. Up-Regulation of PD-L1, IDO, and Tregs in the Melanoma Tumor Microenvironment Is Driven by CD8+ T Cells Sci. Transl. Med. 2013, 5, 200ra116-200ra116 10.1126/scitranslmed.3006504
16. Mellor, A. L.; Munn, D. H. Ido Expression by Dendritic Cells: Tolerance and Tryptophan Catabolism Nat. Rev. Immunol. 2004, 4, 762-774 10.1038/nri1457
17. Moon, Y. W.; Hajjar, J.; Hwu, P.; Naing, A. Targeting the Indoleamine 2,3-Dioxygenase Pathway in Cancer J. Immunother. Cancer. 2015, 3, 51 10.1186/s40425-015-0094-9
18. Muller, A. J.; DuHadaway, J. B.; Donover, P. S.; Sutanto-Ward, E.; Prendergast, G. C. Inhibition of Indoleamine 2,3-Dioxygenase, an Immunoregulatory Target of The Cancer Suppression Gene Bin1, Potentiates Cancer Chemotherapy Nat. Med. 2005, 11, 312-319 10.1038/nm1196
19. Topalian, S. L.; Hodi, F. S.; Brahmer, J. R.; Gettinger, S. N.; Smith, D. C.; McDermott, D. F.; Powderly, J. D.; Carvajal, R. D.; Sosman, J. A.; Atkins, M. B.; Leming, P. D.; Spigel, D. R.; Antonia, S. J.; Horn, L.; Drake, C. G.; Pardoll, D. M.; Chen, L.; Sharfman, W. H.; Anders, R. A.; Taube, J. M. et al. Safety, Activity, and Immune Correlates of Anti-PD-1 Antibody in Cancer N. Engl. J. Med. 2012, 366, 2443-2454 10.1056/NEJMoa1200690
20. DeMuth, P. C.; Min, Y.; Irvine, D. J.; Hammond, P. T. Implantable Silk Composite Microneedles for Programmable Vaccine Release Kinetics and Enhanced Immunogenicity in Transcutaneous Immunization Adv. Healthcare Mater. 2014, 3, 47-58 10.1002/adhm.201300139
21. DeMuth, P. C.; Moon, J. J.; Suh, H.; Hammond, P. T.; Irvine, D. J. Releasable Layer-by-Layer Assembly of Stabilized Lipid Nanocapsules on Microneedles for Enhanced Transcutaneous Vaccine Delivery ACS Nano 2012, 6, 8041-8051 10.1021/nn302639r
22. Sullivan, S. P.; Koutsonanos, D. G.; del Pilar Martin, M.; Lee, J. W.; Zarnitsyn, V.; Choi, S.-O.; Murthy, N.; Compans, R. W.; Skountzou, I.; Prausnitz, M. R. Dissolving Polymer Microneedle Patches for Influenza Vaccination Nat. Med. 2010, 16, 915-920 10.1038/nm.2182
23. Kim, Y.-C.; Park, J.-H.; Prausnitz, M. R. Microneedles for Drug and Vaccine Delivery Adv. Drug Delivery Rev. 2012, 64, 1547-1568 10.1016/j.addr.2012.04.005
24. Prausnitz, M. R.; Langer, R. Transdermal Drug Delivery Nat. Biotechnol. 2008, 26, 1261-1268 10.1038/nbt.1504
25. DeMuth, P. C.; Su, X.; Samuel, R. E.; Hammond, P. T.; Irvine, D. J. Nano-Layered Microneedles for Transcutaneous Delivery of Polymer Nanoparticles and Plasmid DNA Adv. Mater. 2010, 22, 4851-4856 10.1002/adma.201001525
26. Uyttenhove, C.; Pilotte, L.; Théate, I.; Stroobant, V.; Colau, D.; Parmentier, N.; Boon, T.; Van den Eynde, B. J. Evidence for a Tumoral Immune Resistance Mechanism Based on Tryptophan Degradation by Indoleamine 2,3-Dioxygenase Nat. Med. 2003, 9, 1269-1274 10.1038/nm934
27. Pilotte, L.; Larrieu, P.; Stroobant, V.; Colau, D.; Dolusic, E.; Frederick, R.; De Plaen, E.; Uyttenhove, C.; Wouters, J.; Masereel, B.; Van den Eynde, B. J. Reversal of Tumoral Immune Resistance by Inhibition of Tryptophan 2,3-Dioxygenase Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 2497-2502 10.1073/pnas.1113873109
28. Awuah, S. G.; Zheng, Y.-R.; Bruno, P. M.; Hemann, M. T.; Lippard, S. J. A Pt(IV) Pro-Drug Preferentially Targets Indoleamine-2,3-Dioxygenase, Providing Enhanced Ovarian Cancer Immuno-Chemotherapy J. Am. Chem. Soc. 2015, 137, 14854-14857 10.1021/jacs.5b10182
29. Yu, J.; Zhang, Y.; Ye, Y.; DiSanto, R.; Sun, W.; Ranson, D.; Ligler, F. S.; Buse, J. B.; Gu, Z. Microneedle-Array Patches Loaded with Hypoxia-Sensitive Vesicles Provide Fast Glucose-Responsive Insulin Delivery Proc. Natl. Acad. Sci. U. S. A. 2015, 112, 8260-8265 10.1073/pnas.1505405112
30. Lu, Y.; Sun, W.; Gu, Z. Stimuli-Responsive Nanomaterials for Therapeutic Protein Delivery J. Controlled Release 2014, 194, 1-19 10.1016/j.jconrel.2014.08.015
31. Moon, J. J.; Huang, B.; Irvine, D. J. Engineering Nano- and Microparticles to Tune Immunity Adv. Mater. 2012, 24, 3724-3746 10.1002/adma.201200446
32. Wang, C.; Sun, W.; Wright, G.; Wang, A.; Gu, Z. Inflammation-Triggered Cancer Immunotherapy by Programmed Delivery of CpG and Anti-PD1 Antibody Adv. Mater. 2016, 10.1002/adma.201506312
33. Tai, W.; Mo, R.; Di, J.; Subramanian, V.; Gu, X.; Buse, J. B.; Gu, Z. Bio-Inspired Synthetic Nanovesicles for Glucose-Responsive Release of Insulin Biomacromolecules 2014, 15, 3495-3502 10.1021/bm500364a
34. Lu, Y.; Hu, Q.; Lin, Y.; Pacardo, D. B.; Wang, C.; Sun, W.; Ligler, F. S.; Dickey, M. D.; Gu, Z. Transformable Liquid-Metal Nanomedicine Nat. Commun. 2015, 6, 10066 10.1038/ncomms10066
35. Wang, C.; Ye, Y.; Hochu, G. M.; Sadeghifar, H.; Gu, Z. Enhanced Cancer Immunotherapy by Microneedle Patch-Assisted Delivery of Anti-PD1 Antibody Nano Lett. 2016, 16, 2334-2340 10.1021/acs.nanolett.5b05030
36. Mitragotri, S.; Anderson, D. G.; Chen, X.; Chow, E. K.; Ho, D.; Kabanov, A. V.; Karp, J. M.; Kataoka, K.; Mirkin, C. A.; Petrosko, S. H.; Shi, J.; Stevens, M. M.; Sun, S.; Teoh, S.; Venkatraman, S. S.; Xia, Y.; Wang, S.; Gu, Z.; Xu, C. Accelerating the Translation of Nanomaterials in Biomedicine ACS Nano 2015, 9, 6644-6654 10.1021/acsnano.5b03569
37. Peer, D.; Karp, J. M.; Hong, S.; Farokhzad, O. C.; Margalit, R.; Langer, R. Nanocarriers as an Emerging Platform for Cancer Therapy Nat. Nanotechnol. 2007, 2, 751-760 10.1038/nnano.2007.387
38. DeMuth, P. C.; Li, A. V.; Abbink, P.; Liu, J.; Li, H.; Stanley, K. A.; Smith, K. M.; Lavine, C. L.; Seaman, M. S.; Kramer, J. A.; Miller, A. D.; Abraham, W.; Suh, H.; Elkhader, J.; Hammond, P. T.; Barouch, D. H.; Irvine, D. J. Vaccine Delivery with Microneedle Skin Patches in Nonhuman Primates Nat. Biotechnol. 2013, 31, 1082-1085 10.1038/nbt.2759
39. Li, W. A.; Mooney, D. J. Materials Based Tumor Immunotherapy Vaccines Curr. Opin. Immunol. 2013, 25, 238-245 10.1016/j.coi.2012.12.008
40. Hu, Q.; Sun, W.; Lu, Y.; Bomba, H. N.; Ye, Y.; Jiang, T.; Isaacson, A. J.; Gu, Z. Tumor Microenvironment-Mediated Construction and Deconstruction of Extracellular Drug-Delivery Depots Nano Lett. 2016, 16, 1118-1126 10.1021/acs.nanolett.5b04343
41. Mai, Y.; Eisenberg, A. Self-Assembly of Block Copolymers Chem. Soc. Rev. 2012, 41, 5969-5985 10.1039/c2cs35115c
42. Hervé, C.; Beyne, P.; Jamault, H.; Delacoux, E. Determination of Tryptophan and Its Kynurenine Pathway Metabolites in Human Serum by High-Performance Liquid Chromatography with Simultaneous Ultraviolet and Fluorimetric Detection J. Chromatogr., Biomed. Appl. 1996, 675, 157-161 10.1016/0378-4347(95)00341-X
43. Hwang, S. L.; Chung, N. P.-Y.; Chan, J. K.-Y.; Lin, C.-L. S. Indoleamine 2, 3-Dioxygenase (IDO) Is Essential for Dendritic Cell Activation and Chemotactic Responsiveness to Chemokines Cell Res. 2005, 15, 167-175 10.1038/sj.cr.7290282