A photoactivable multi-inhibitor nanoliposome for tumour control and simultaneous inhibition of treatment escape pathways

Nature Nanotechnology

Volumn 11, Issue 4, 2016, Pages 378-387

  Spring, Bryan Q ^a,b   Bryan Sears, R ^a,c   Zheng, Lei Zak ^a   Mai, Zhiming ^a   Watanabe, Reika ^d   Sherwood, Margaret E ^a   Schoenfeld, David A ^e   Pogue, Brian W ^f   Pereira, Stephen P ^g   Villa, Elizabeth ^d   Hasan, Tayyaba ^a,e  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b NORTHEASTERN UNIVERSITY   (United States)

^c EMMANUEL COLLEGE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e HARVARD UNIVERSITY   (United States)

^f DARTMOUTH COLLEGE   (United States)

^g UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOPHORES; DISEASES; DRUG PRODUCTS; INFRARED DEVICES; LIPID BILAYERS; TARGETED DRUG DELIVERY; TUMORS;

CANCER THERAPY; DRUG DELIVERY VEHICLES; DRUG RELEASE; LIGHT-INDUCED; NEAR INFRARED; SIGNALLING PATHWAYS; SPATIOTEMPORAL CONTROL; SUSTAINED RELEASE;

CONTROLLED DRUG DELIVERY;

ANTIMETASTATIC AGENT; BENZOPORPHYRIN DERIVATIVE; CABOZANTINIB; LIPOSOME; MULTI INHIBITOR NANOLIPOSOME; NANOPARTICLE; UNCLASSIFIED DRUG; ANILIDE; ANTINEOPLASTIC AGENT; BENZOPORPHYRIN D; PHOTOSENSITIZING AGENT; PORPHYRIN; PYRIDINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIANGIOGENIC THERAPY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CONTROL; CANCER RADIOTHERAPY; CHROMATOPHORE; CONTROLLED STUDY; CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG SYNTHESIS; ENDOTHELIUM CELL; INFRARED RADIATION; LIPID BILAYER; MALE; METASTASIS; METASTASIS INHIBITION; MICROVASCULATURE; MOUSE; NONHUMAN; PANCREAS CANCER; PHOTOACTIVATION; PRIORITY JOURNAL; STEM CELL; SUSTAINED DRUG RELEASE; ANIMAL; CHEMISTRY; DRUG SCREENING; HUMAN; TUMOR CELL LINE;

ANILIDES; ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; HUMANS; LIPOSOMES; MALE; MICE; PHOTOSENSITIZING AGENTS; PORPHYRINS; PYRIDINES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84954546545     PISSN: 17483387     EISSN: 17483395     Source Type: Journal    
DOI: 10.1038/nnano.2015.311     Document Type: Article

References (50)

1. Cheng, Z., Al Zaki, A., Hui, J. Z., Muzykantov, V. R. & Tsourkas, A. Multifunctional nanoparticles: cost versus benefit of adding targeting and imaging capabilities. Science 338, 903-910 (2012).
2. Lovell, J. F. et al. Porphysome nanovesicles generated by porphyrin bilayers for use as multimodal biophotonic contrast agents. Nature Mater. 10, 324-332 (2011).
3. Cui, S. et al. In vivo targeted deep-tissue photodynamic therapy based on near-infrared light triggered upconversion nanoconstruct. ACS Nano 7, 676-688 (2013).
4. Carter, K. A. et al. Porphyrin-phospholipid liposomes permeabilized by near-infrared light. Nature Commun. 5, 3546 (2014).
5. Sennino, B. & McDonald, D. M. Controlling escape from angiogenesis inhibitors. Nat. Rev. Cancer 12, 699-709 (2012).
6. Holohan, C., Van Schaeybroeck, S., Longley, D. B. & Johnston, P. G. Cancer drug resistance: an evolving paradigm. Nat. Rev. Cancer 13, 714-726 (2013).
7. Pennacchietti, S. et al. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell 3, 347-361 (2003).
8. Pàez-Ribes, M. et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15, 220-231 (2009).
9. Gorski, D. H. et al. Blockade of the vascular endothelial growth factor stress response increases the antitumor effects of ionizing radiation. Cancer Res. 59, 3374-3378 (1999).
10. Tran, J. et al. A role for survivin in chemoresistance of endothelial cells mediated by VEGF. Proc. Natl Acad. Sci. USA 99, 4349-4354 (2002).
11. Justinger, C. et al. Increased growth factor expression after hepatic and pancreatic resection. Oncol. Rep. 20, 1527-1531 (2008).
12. Ferrario, A. et al. Antiangiogenic treatment enhances photodynamic therapy responsiveness in a mouse mammary carcinoma. Cancer Res. 60, 4066-4069 (2000).
13. Solban, N. et al. Mechanistic investigation and implications of photodynamic therapy induction of vascular endothelial growth factor in prostate cancer. Cancer Res. 66, 5633-5640 (2006).
14. Hage, C. et al. The novel c-Met inhibitor cabozantinib overcomes gemcitabine resistance and stem cell signaling in pancreatic cancer. Cell Death Dis. 4, e627 (2013).
15. Gherardi, E., Birchmeier, W., Birchmeier, C. & Vande Woude, G. Targeting MET in cancer: rationale and progress. Nat. Rev. Cancer 12, 89-103 (2012).
16. Sennino, B. et al. Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors. Cancer Discov. 2, 270-287 (2012).
17. Sennino, B., Ishiguro-Oonuma, T., Schriver, B. J., Christensen, J. G. & McDonald, D. M. Inhibition of c-Met reduces lymphatic metastasis in RIP-Tag2 transgenic mice. Cancer Res. 73, 3692-3703 (2013).
18. Drummond, D. C., Meyer, O., Hong, K., Kirpotin, D. B. & Papahadjopoulos, D. Optimizing liposomes for delivery of chemotherapeutic agents to solid tumors. Pharmacol. Rev. 51, 691-743 (1999).
19. Davis, M. E., Chen, Z. G. & Shin, D. M. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat. Rev. Drug Discov. 7, 771-782 (2008).
20. Makadia, H. K. & Siegel, S. J. Poly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers 3, 1377-1397 (2011).
21. Hines, D. J. & Kaplan, D. L. Poly(lactic-co-glycolic) acid-controlled-release systems: experimental and modeling insights. Crit. Rev. Ther. Drug Carrier Syst. 30, 257-276 (2013).
22. Thompson, D. H., Gerasimov, O. V., Wheeler, J. J., Rui, Y. & Anderson, V. C. Triggerable plasmalogen liposomes: improvement of system efficiency. Biochim. Biophys. Acta 1279, 25-34 (1996).
23. Elisei, R. et al. Cabozantinib in progressive medullary thyroid cancer. J. Clin. Oncol. 31, 3639-3646 (2013).
24. Li, C. et al. c-Met is a marker of pancreatic cancer stem cells and therapeutic target. Gastroenterology 141, 2218-2227.e5 (2011).
25. Kindler, H. L. et al. Gemcitabine plus bevacizumab compared with gemcitabine plus placebo in patients with advanced pancreatic cancer: phase III trial of the Cancer and Leukemia Group B (CALGB 80303). J. Clin. Oncol. 28, 3617-3622 (2010).
26. Chen, B., Pogue, B. W., Hoopes, P. J. & Hasan, T. Combining vascular and cellular targeting regimens enhances the efficacy of photodynamic therapy. Int. J. Radiat. Oncol. Biol. Phys. 61, 1216-1226 (2005).
27. Fingar, V. H. et al. Analysis of acute vascular damage after photodynamic therapy using benzoporphyrin derivative (BPD). Br. J. Cancer 79, 1702-1708 (1999).
28. Kurohane, K. et al. Photodynamic therapy targeted to tumor-induced angiogenic vessels. Cancer Lett. 167, 49-56 (2001).
29. Schmidt-Erfurth, U. & Hasan, T. Mechanisms of action of photodynamic therapy with verteporfin for the treatment of age-related macular degeneration. Surv. Ophthalmol. 45, 195-214 (2000).
30. Huggett, M. T. et al. Phase I/II study of verteporfin photodynamic therapy in locally advanced pancreatic cancer. Br. J. Cancer 110, 1698-1704 (2014).
31. Kessel, D. & Luo, Y. Photodynamic therapy: a mitochondrial inducer of apoptosis. Cell. Death Differ. 6, 28-35 (1999).
32. Kessel, D. Death pathways associated with photodynamic therapy. Med. Laser Appl. 21, 219-224 (2006).
33. Duska, L. R., Hamblin, M. R., Miller, J. L. & Hasan, T. Combination photoimmunotherapy and cisplatin: effects on human ovarian cancer ex vivo. J. Natl Cancer Inst. 91, 1557-1563 (1999).
34. Rizvi, I. et al. Synergistic enhancement of carboplatin efficacy with photodynamic therapy in a three-dimensional model for micrometastatic ovarian cancer. Cancer Res. 70, 9319-9328 (2010).
35. Celli, J. P., Solban, N., Liang, A., Pereira, S. P. & Hasan, T. Verteporfin-based photodynamic therapy overcomes gemcitabine insensitivity in a panel of pancreatic cancer cell lines. Lasers Surg. Med. 43, 565-574 (2011).
36. del Carmen, M. G. et al. Synergism of epidermal growth factor receptor-targeted immunotherapy with photodynamic treatment of ovarian cancer in vivo. J. Natl Cancer Inst. 97, 1516-1524 (2005).
37. Hlatky, L., Hahnfeldt, P. & Folkman, J. Clinical application of antiangiogenic therapy: microvessel density, what it does and doesn't tell us. J. Natl Cancer Inst. 94, 883-893 (2002).
38. Spring, B. Q. et al. Efficient measurement of total tumor microvascularity ex vivo using a mathematical model to optimize volume subsampling. J. Biomed. Opt. 18, 096015 (2013).
39. Yakes, F. M. et al. Cabozantinib (XL184), a novel MET and VEGFR2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth. Mol. Cancer Ther. 10, 2298-2308 (2011).
40. Chang, S. K., Rizvi, I. & Solban, N. In vivo optical molecular imaging of vascular endothelial growth factor for monitoring cancer treatment. Clin. Cancer Res. 14, 4146-4153 (2008).
41. Tardi, P. et al. In vivo maintenance of synergistic cytarabine:daunorubicin ratios greatly enhances therapeutic efficacy. Leuk. Res. 33, 129-139 (2009).
42. Dromi, S. et al. Pulsed-high intensity focused ultrasound and low temperature-sensitive liposomes for enhanced targeted drug delivery and antitumor effect. Clin. Cancer Res. 13, 2722-2727 (2007).
43. Sengupta, S. et al. Temporal targeting of tumour cells and neovasculature with a nanoscale delivery system. Nature 436, 568-572 (2005).
44. Spring, B. Q. et al. Selective treatment and monitoring of disseminated cancer micrometastases in vivo using dual-function, activatable immunoconjugates. Proc. Natl Acad. Sci. USA 111, E933-E942 (2014).
45. Cheng, J. et al. Formulation of functionalized PLGA-PEG nanoparticles for in vivo targeted drug delivery. Biomaterials 28, 869-876 (2007).
46. Nel, A. E. et al. Understanding biophysicochemical interactions at the nano-bio interface. Nature Mater. 8, 543-557 (2009).
47. Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36-51 (2005).
48. Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76 (1996).
49. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graphics 14, 33-38 (1996).
50. Larson, M. G. Analysis of variance. Circulation 117, 115-121 (2008).