Tumour-associated macrophages act as a slow-release reservoir of nano-therapeutic Pt(IV) pro-drug

Nature Communications

Volumn 6, Issue , 2015, Pages

  Miller, Miles A ^a   Zheng, Yao Rong ^b   Gadde, Suresh ^c   Pfirschke, Christina ^a   Zope, Harshal ^c   Engblom, Camilla ^a   Kohler, Rainer H ^a   Iwamoto, Yoshiko ^a   Yang, Katherine S ^a   Askevold, Bjorn ^a   Kolishetti, Nagesh ^c   Pittet, Mikael ^a   Lippard, Stephen J ^b   Farokhzad, Omid C ^c,d   Weissleder, Ralph ^a,e,f  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^e HARVARD MEDICAL SCHOOL   (United States)

^f UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER; DRUG; GENE EXPRESSION; NANOPARTICLE; REACTION KINETICS; TUMOR;

ANTINEOPLASTIC AGENT; NANOPARTICLE; PLATINUM; PRODRUG;

ANIMAL; C57BL MOUSE; CHEMISTRY; DRUG DELIVERY SYSTEM; FEMALE; HUMAN; MACROPHAGE; METABOLISM; MOUSE; NEOPLASMS; NUDE MOUSE; PROCEDURES; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DRUG DELIVERY SYSTEMS; FEMALE; HUMANS; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, NUDE; NANOPARTICLES; NEOPLASMS; PLATINUM; PRODRUGS;

EID: 84945405311     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9692     Document Type: Article

References (70)

1. Kelland, L. The resurgence of platinum-based cancer chemotherapy. Nat. Rev. Cancer 7, 573-584 (2007).
2. O'Shaughnessy, J. et al. Phase III study of iniparib plus gemcitabine and carboplatin versus gemcitabine and carboplatin in patients with metastatic triple-negative breast cancer. J. Clin. Oncol. 32, 3840-3847 (2014).
3. Cooke, S. L., Brenton, J. D. Evolution of platinum resistance in high-grade serous ovarian cancer. Lancet Oncol. 12, 1169-1174 (2011).
4. Bertrand, N., Wu, J., Xu, X., Kamaly, N., Farokhzad, O. C. Cancer nanotechnology: the impact of passive and active targeting in the era of modern cancer biology. Adv. Drug Deliv. Rev. 66, 2-25 (2014).
5. Hrkach, J. et al. Preclinical development and clinical translation of a PSMAtargeted docetaxel nanoparticle with a differentiated pharmacological profile. Sci. Transl. Med. 4, 128-39 (2012).
6. Dhar, S., Kolishetti, N., Lippard, S. J., Farokhzad, O. C. Targeted delivery of a cisplatin prodrug for safer and more effective prostate cancer therapy in vivo. Proc. Natl Acad. Sci. USA 108, 1850-1855 (2011).
7. Valencia, P. M. et al. Synergistic cytotoxicity of irinotecan and cisplatin in dualdrug targeted polymeric nanoparticles. Nanomedicine (Lond.) 8, 687-698 (2013).
8. Gadde, S. Multi-drug delivery nanocarriers for combination therapy. Med. Chem. Commun. doi: 10.1039/C5MD00365B (2015).
9. Xu, X. et al. Enhancing tumor cell response to chemotherapy through nanoparticle-mediated codelivery of siRNA and cisplatin prodrug. Proc. Natl Acad. Sci. USA 110, 18638-18643 (2013).
10. Johnstone, T. C. et al. Nanoparticle encapsulation of mitaplatin and the effect thereof on in vivo properties. ACS Nano 7, 5675-5683 (2013).
11. Prabhakar, U. et al. Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology. Cancer Res. 73, 2412-2417 (2013).
12. Maeda, H., Nakamura, H., Fang, J. The EPR effect for macromolecular drug delivery to solid tumors: Improvement of tumor uptake, lowering of systemic toxicity, and distinct tumor imaging in vivo. Adv. Drug Deliv. Rev. 65, 71-79 (2013).
13. Harrington, K. J. et al. Phase I-II study of pegylated liposomal cisplatin (SPI-077) in patients with inoperable head and neck cancer. Ann. Oncol. 12, 493-496 (2001).
14. Wright, J. Nanotechnology: deliver on a promise. Nature 509, S58-S59 (2014).
15. Caron, W. P., Song, G., Kumar, P., Rawal, S., Zamboni, W. C. Interpatient pharmacokinetic and pharmacodynamic variability of carrier-mediated anticancer agents. Clin. Pharmacol. Ther. 91, 802-812 (2012).
16. Thurber, G. M. et al. Single-cell and subcellular pharmacokinetic imaging allows insight into drug action in vivo. Nat. Commun. 4, 1504 (2013).
17. Yamamoto, N. et al. Cellular dynamics visualized in live cells in vitro and in vivo by differential dual-color nuclear-cytoplasmic fluorescent-protein expression. Cancer Res. 64, 4251-4256 (2004).
18. Hinkeldey, B., Schmitt, A., Jung, G. Comparative photostability studies of BODIPY and fluorescein dyes by using fluorescence correlation spectroscopy. ChemPhysChem 9, 2019-2027 (2008).
19. Karolin, J., Johansson, L. B.-A., Strandberg, L., Ny, T. Fluorescence and absorption spectroscopic properties of dipyrrometheneboron difluoride (BODIPY) derivatives in liquids, lipid membranes, and proteins. J. Am. Chem. Soc. 116, 7801-7806 (1994).
20. Ulrich, G., Ziessel, R., Harriman, A. The chemistry of fluorescent bodipy dyes: versatility unsurpassed. Angew Chem. Int. Ed. Engl. 47, 1184-1201 (2008).
21. Xiao, K. et al. The effect of surface charge on in vivo biodistribution of PEG-oligocholic acid based micellar nanoparticles. Biomaterials 32, 3435-3446 (2011).
22. He, C., Hu, Y., Yin, L., Tang, C., Yin, C. Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials 31, 3657-3666 (2010).
23. Yamamoto, Y., Nagasaki, Y., Kato, Y., Sugiyama, Y., Kataoka, K. Long-circulating poly(ethylene glycol)-poly(D,L-lactide) block copolymer micelles with modulated surface charge. J. Control Release 77, 27-38 (2001).
24. Kommareddy, S., Amiji, M. Biodistribution and pharmacokinetic analysis of long-circulating thiolated gelatin nanoparticles following systemic administration in breast cancer-bearing mice. J. Pharm. Sci. 96, 397-407 (2007).
25. Zheng, Y. R. et al. Pt(IV) prodrugs designed to bind non-covalently to human serum albumin for drug delivery. J. Am. Chem. Soc. 136, 8790-8798 (2014).
26. Orth, J. D. et al. Analysis of mitosis and antimitotic drug responses in tumors by in vivo microscopy and single-cell pharmacodynamics. Cancer Res. 71, 4608-4616 (2011).
27. Laughney, A. M. et al. Single-cell pharmacokinetic imaging reveals a therapeutic strategy to overcome drug resistance to the microtubule inhibitor eribulin. Sci. Transl. Med 6, 261-152 (2014).
28. Yang, M., Jiang, P., Hoffman, R. M. Whole-body subcellular multicolor imaging of tumor-host interaction and drug response in real time. Cancer Res. 67, 5195-5200 (2007).
29. Miller, M. A., Askevold, B., Yang, K. S., Kohler, R. H., Weissleder, R. Platinum compounds for high-resolution in vivo cancer imaging. ChemMedChem 9, 1131-1135 (2014).
30. Miwa, S. et al. Imaging UVC-induced DNA damage response in models of minimal cancer. J. Cell Biochem. 114, 2493-2499 (2013).
31. Beletsi, A., Panagi, Z., Avgoustakis, K. Biodistribution properties of nanoparticles based on mixtures of PLGA with PLGA-PEG diblock copolymers. Int. J. Pharm. 298, 233-241 (2005).
32. Doxil (package insert)Horsham, P. A. Janssen, Products, LP (2015).
33. Gabizon, A., Shmeeda, H., Barenholz, Y. Pharmacokinetics of pegylated liposomal doxorubicin: review of animal and human studies. Clin. Pharmacokinet. 42, 419-436 (2003).
34. Kolishetti, N. et al. Engineering of self-assembled nanoparticle platform for precisely controlled combination drug therapy. Proc. Natl Acad. Sci. USA 107, 17939-17944 (2010).
35. Dhar, S., Gu, F. X., Langer, R., Farokhzad, O. C., Lippard, S. J. Targeted delivery of cisplatin to prostate cancer cells by aptamer functionalized Pt(IV) prodrug-PLGA-PEG nanoparticles. Proc. Natl Acad. Sci. USA 105, 17356-17361 (2008).
36. Karanam, K., Kafri, R., Loewer, A., Lahav, G. Quantitative live cell imaging reveals a gradual shift between DNA repair mechanisms and a maximal use of HR in mid S phase. Mol. Cell 47, 320-329 (2012).
37. Shaw, T. J., Senterman, M. K., Dawson, K., Crane, C. A., Vanderhyden, B. C. Characterization of intraperitoneal, orthotopic, and metastatic xenograft models of human ovarian cancer. Mol. Ther. 10, 1032-1042 (2004).
38. Ginhoux, F. et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330, 841-845 (2010).
39. DuPage, M., Dooley, A. L., Jacks, T. Conditional mouse lung cancer models using adenoviral or lentiviral delivery of Cre recombinase. Nat. Protoc. 4, 1064-1072 (2009).
40. Zeisberger, S. M. et al. Clodronate-liposome-mediated depletion of tumourassociated macrophages: a new and highly effective antiangiogenic therapy approach. Br. J. Cancer 95, 272-281 (2006).
41. Denis, M. C., Mahmood, U., Benoist, C., Mathis, D., Weissleder, R. Imaging inflammation of the pancreatic islets in type 1 diabetes. Proc. Natl Acad. Sci. USA 101, 12634-12639 (2004).
42. McInnes, I. B., Schett, G. The pathogenesis of rheumatoid arthritis. N. Engl. J. Med. 365, 2205-2219 (2011).
43. Beste, M. T. et al. Molecular network analysis of endometriosis reveals a role for c-Jun-regulated macrophage activation. Sci. Transl. Med. 6, 222-16 (2014).
44. Moore, K. J., Tabas, I. Macrophages in the pathogenesis of atherosclerosis. Cell 145, 341-355 (2011).
45. Frantz, S., Nahrendorf, M. Cardiac macrophages and their role in ischaemic heart disease. Cardiovasc. Res. 102, 240-248 (2014).
46. Weissleder, R., Nahrendorf, M., Pittet, M. J. Imaging macrophages with nanoparticles. Nature Mater. 13, 125-138 (2014).
47. Aouadi, M. et al. Orally delivered siRNA targeting macrophage Map4k4 suppresses systemic inflammation. Nature 458, 1180-1184 (2009).
48. De Palma, M., Lewis, C. E. Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell 23, 277-286 (2013).
49. Cortez-Retamozo, V. et al. Origins of tumor-associated macrophages and neutrophils. Proc. Natl Acad. Sci. USA 109, 2491-2496 (2012).
50. Steidl, C. et al. Tumor-associated macrophages and survival in classic Hodgkin's lymphoma. N. Engl. J. Med. 362, 875-885 (2010).
51. Zhang, Q. W. et al. Prognostic significance of tumor-associated macrophages in solid tumor: a meta-analysis of the literature. PLoS ONE 7, e50946 (2012).
52. Nakasone, E. S. et al. Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance. Cancer Cell 21, 488-503 (2012).
53. Zhang, W. et al. Depletion of tumor-associated macrophages enhances the effect of sorafenib in metastatic liver cancer models by antimetastatic and antiangiogenic effects. Clin. Cancer Res. 16, 3420-3430 (2010).
54. Pyonteck, S. M. et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nature Med. 19, 1264-1272 (2013).
55. Zhu, Y. et al. CSF1/CSF1R blockade reprograms tumor-infiltrating macrophages and improves response to T-cell checkpoint immunotherapy in pancreatic cancer models. Cancer Res. 74, 5057-5069 (2014).
56. Ries, C. H. et al. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell 25, 846-859 (2014).
57. Mayer, L. D., Dougherty, G., Harasym, T. O., Bally, M. B. The role of tumor-associated macrophages in the delivery of liposomal doxorubicin to solid murine fibrosarcoma tumors. J. Pharmacol. Exp. Ther. 280, 1406-1414 (1997).
58. Hirota, K. et al. Optimum conditions for efficient phagocytosis of rifampicinloaded PLGA microspheres by alveolar macrophages. J. Control. Release 119, 69-76 (2007).
59. Liu, H. et al. Structure-based programming of lymph-node targeting in molecular vaccines. Nature 507, 519-522 (2014).
60. Kirpotin, D. B. et al. Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localization but does increase internalization in animal models. Cancer Res. 66, 6732-6740 (2006).
61. Venkatraman, S. S., Ma, L. L., Natarajan, J. V., Chattopadhyay, S. Polymer-and liposome-based nanoparticles in targeted drug delivery. Front. Biosci. (Schol. Ed) 2, 801-814 (2010).
62. She, W. et al. The potential of self-assembled, pH-responsive nanoparticles of mPEGylated peptide dendron-doxorubicin conjugates for cancer therapy. Biomaterials 34, 1613-1623 (2013).
63. Harisinghani, M., Ross, R. W., Guimaraes, A. R., Weissleder, R. Utility of a new bolus-injectable nanoparticle for clinical cancer staging. Neoplasia 9, 1160-1165 (2007).
64. Ansari, C. et al. Development of novel tumor-targeted theranostic nanoparticles activated by membrane-type matrix metalloproteinases for combined cancer magnetic resonance imaging and therapy. Small 10, 417 (2014).
65. Kaittanis, C. et al. Environment-responsive nanophores for therapy and treatment monitoring via molecular MRI quenching. Nat. Commun. 5, 3384 (2014).
66. Beatty, G. L. et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 331, 1612-1616 (2011).
67. Germano, G. et al. Role of macrophage targeting in the antitumor activity of trabectedin. Cancer Cell 23, 249-262 (2013).
68. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L., Luo, L. A global doublefluorescent Cre reporter mouse. Genesis 45, 593-605 (2007).
69. Alieva, M., Ritsma, L., Giedt, R. J., Weissleder, R., van Rheenen, J. Imaging windows for long-term intravital imaging. IntraVital 3, e29917 (2014).
70. Turetsky, A., Kim, E., Kohler, R. H., Miller, M. A., Weissleder, R. Single cell imaging of Bruton's tyrosine kinase using an irreversible inhibitor. Sci. Rep. 4, 4782 (2014).