Nanomedicines Targeting the Tumor Microenvironment

Cancer Journal (United States)

Volumn 21, Issue 4, 2015, Pages 314-321

  Tong, Rong ^a,b   Langer, Robert ^a  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cancer immunology; extracellular matrix; nanomedicine; nanoparticle; near infrared light; photothermal; stimulus responsive drug delivery; triggered drug delivery; tumor microenvironment; tumor penetration

Indexed keywords

NANOPARTICLE; ANTINEOPLASTIC AGENT; DRUG CARRIER; NANOMATERIAL;

ANTIANGIOGENIC THERAPY; CANCER IMMUNOTHERAPY; DRUG DELIVERY SYSTEM; EXTRACELLULAR MATRIX; GEOMETRY; HUMAN; MULTICENTER STUDY (TOPIC); NANOCHEMISTRY; NANOMEDICINE; PARTICLE SIZE; PHASE 2 CLINICAL TRIAL (TOPIC); PHOTOTHERMAL THERAPY; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; REVIEW; SURFACE PROPERTY; TUMOR MICROENVIRONMENT; VASCULARIZATION; IMMUNOTHERAPY; NEOPLASMS;

ANTINEOPLASTIC AGENTS; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; HUMANS; IMMUNOTHERAPY; NANOMEDICINE; NANOPARTICLES; NANOSTRUCTURES; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84938602340     PISSN: 15289117     EISSN: 1540336X     Source Type: Journal    
DOI: 10.1097/PPO.0000000000000123     Document Type: Review

References (130)

1. Moghimi SM, Hunter AC, Murray JC. Nanomedicine: current status and future prospects. FASEB J. 2005;19:311-330.
2. Matsumura Y,Maeda H. A new concept for macromolecular therapeutics in cancer-chemotherapy-mechanism of tumoritropic accumulation of proteins and the antitumor agent SMANCS. Cancer Res. 1986;46: 6387-6392.
3. Dvorak HF, Brown LF, Detmar M, et al. Vascular permeability factor/ vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Physiol. 1995;146:1029-1039.
4. Padera TP, Kadambi A, di Tomaso E, et al. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science. 2002;296:1883-1886.
5. Jain RK, Stylianopoulos T. Delivering nanomedicine to solid tumors. Nat Rev Clin Oncol. 2010;7:653-664.
6. Chow EK-H, Ho D. Cancer nanomedicine: from drug delivery to imaging. Sci Transl Med. 2013;5:216rv4.
7. Gref R, Minamitake Y, Peracchia MT, et al. Biodegradable longcirculating polymeric nanospheres. Science. 1994;263:1600-1603.
8. Langer R. Drug delivery and targeting. Nature. 1998;392:5-10.
9. Green MR, Manikhas GM, Orlov S, et al. Abraxane, a novel Cremophor-free, albumin-bound particle formof paclitaxel for the treatment of advanced non-small-cell lung cancer. Ann Oncol. 2006;17: 1263-1268.
10. Von Hoff DD, Ervin T, Arena FP, et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med. 2013;369: 1691-1703.
11. Hirsch LR, Stafford RJ, Bankson JA, et al. Nanoshell-mediated nearinfrared thermal therapy of tumors under magnetic resonance guidance. Proc Natl Acad Sci U S A. 2003;100:13549-13554.
12. Phillips E, Penate-Medina O, Zanzonico PB, et al. Clinical translation of an ultrasmall inorganic optical-PET imaging nanoparticle probe. Sci Transl Med. 2014;6:260ra149.
13. Prabhakar U, Blakey DC, Maeda H, et al. Challenges and key considerations of the enhanced permeability and retention effect (EPR) for nanomedicine drug delivery in oncology. Cancer Res. 2013;73:2412-2417.
14. Jain RK, Baxter LT. Mechanisms of heterogeneous distribution of monoclonal antibodies and other macromolecules in tumors: significance of elevated interstitial pressure. Cancer Res. 1988;48:7022-7032.
15. Thomlinson RH, Gray LH. The histological structure of some human lung cancers and the possible implications for radiotherapy. Br J Cancer. 1955; 9:539-549.
16. Less JR, Skalak TC, Sevick EM, et al. Microvascular architecture in a mammary carcinoma: branching patterns and vessel dimensions. Cancer Res. 1991;51:265-273.
17. Netti PA, Berk DA, Swartz MA, et al. Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res. 2000;60: 2497-2503.
18. Sugahara KN, Teesalu T, Karmali PP, et al. Tissue-penetrating delivery of compounds and nanoparticles into tumors. Cancer Cell. 2009;16: 510-520.
19. Huang SK, Martin FJ, Jay G, et al. Extravasation and transcytosis of liposomes in Kaposi's sarcoma-like dermal lesions of transgenic mice bearing the HIV tat gene. Am J Physiol. 1993;143:10-14.
20. Dong H, Strome SE, Salomao DR, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med. 2002;8:793-800.
21. Schwartz RH. T Cell Anergy. Annu Rev Immunol. 2003;21:305-334.
22. Shimizu J, Yamazaki S, Sakaguchi S. Induction of tumor immunity by removing CD25(+)CD4(+) T cells: a common basis between tumor immunity and autoimmunity. J Immunol. 1999;163:5211-5218.
23. Brigl M, Brenner MB. CD1: antigen presentation and T cell function. Annu Rev Immunol. 2004;22:817-890.
24. Chauhan VP, Jain RK. Strategies for advancing cancer nanomedicine. Nat Mater. 2013;12:958-962.
25. Longmire M, Choyke PL, Kobayashi H. Clearance properties of nanosized particles and molecules as imaging agents: considerations and caveats. Nanomedicine. 2008;3:703-717.
26. Perrault SD, Walkey C, Jennings T, et al. Mediating tumor targeting efficiency of nanoparticles through design. Nano Lett. 2009;9:1909-1915.
27. Popovic Z, Liu WH, Chauhan VP, et al. A nanoparticle size series for in vivo fluorescence imaging. Angew Chem Int Ed. 2010;49:8649-8652.
28. Wong C, Stylianopoulos T, Cui JA, et al. Multistage nanoparticle delivery system for deep penetration into tumor tissue. Proc Natl Acad Sci U S A. 2011;108:2426-2431.
29. Chauhan VP, Stylianopoulos T,Martin JD, et al. Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner. Nat Nanotechnol. 2012;7:383-388.
30. Tang L, Yang X, Yin Q, et al. Investigating the optimal size of anticancer nanomedicine. Proc Natl Acad Sci U S A. 2014;111:15344-15349.
31. Cabral H, Matsumoto Y, Mizuno K, et al. Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size. Nat Nanotechnol. 2011;6:815-823.
32. Jensen SA, Day ES, Ko CH, et al. Spherical nucleic acid nanoparticle conjugates as an RNAi-based therapy for glioblastoma. Sci TranslMed. 2013; 5:209ra152.
33. Dellian M, Yuan F, Trubetskoy VS, et al. Vascular permeability in a human tumour xenograft: molecular charge dependence. Br J Cancer. 2000;82:1513-1518.
34. Krasnici S,Werner A, Eichhorn ME, et al. Effect of the surface charge of liposomes on their uptake by angiogenic tumor vessels. Int J Cancer. 2003;105:561-567.
35. Campbell RB, Fukumura D, Brown EB, et al. Cationic charge determines the distribution of liposomes between the vascular and extravascular compartments of tumors. Cancer Res. 2002;62:6831-6836.
36. Schmitt-Sody M, Strieth S, Krasnici S, et al. Neovascular targeting therapy: paclitaxel encapsulated in cationic liposomes improves antitumoral efficacy. Clin Cancer Res. 2003;9:2335-2341.
37. Thurston G,McLean JW, RizenM, et al. Cationic liposomes target angiogenic endothelial cells in tumors and chronic inflammation inmice. J Clin Invest. 1998;101:1401-1413.
38. Wiig H, Gyenge CC, Tenstad O. The interstitial distribution of macromolecules in rat tumours is influenced by the negatively charged matrix components. J Physiol. 2005;567:557-567.
39. Stylianopoulos T, Poh M-Z, Insin N, et al. Diffusion of particles in the extracellular matrix: the effect of repulsive electrostatic interactions. Biophys J. 2010;99:1342-1349.
40. Lieleg O, Baumgärtel RM, Bausch AR. Selective filtering of particles by the extracellular matrix: an electrostatic bandpass. Biophys J. 2009;97: 1569-1577.
41. Choi HS, Liu W, Liu F, et al. Design considerations for tumour-targeted nanoparticles. Nat Nano. 2010;5:42-47.
42. AllenTM. Toxicity of drug carriers to the mononuclear phagocyte system. Adv Drug Deliv Rev. 1988;2:55-67.
43. Derfus AM, Chan WCW, Bhatia SN. Probing the cytotoxicity of semiconductor quantum dots. Nano Lett. 2004;4:11-18.
44. Hauck TS, Anderson RE, Fischer HC, et al. In vivo quantum-dot toxicity assessment. Small. 2010;6:138-144.
45. Balasubramanian SK, Jittiwat J, Manikandan J, et al. Biodistribution of gold nanoparticles and gene expression changes in the liver and spleen after intravenous administration in rats. Biomaterials. 2010;31:2034-2042.
46. Yang RH, Chang LW,Wu JP, et al. Persistent tissue kinetics and redistribution of nanoparticles, quantum dot 705, in mice: ICP-MS quantitative assessment. Environ Health Perspect. 2007;115:1339-1343.
47. Allen TM, Hansen C, Martin F, et al. Liposomes containing synthetic lipid derivatives of poly (ethylene glycol) show prolonged circulation half-lives in vivo. Biochim Biophys Acta. 1991;1066:29-36.
48. Allen TM. The use of glycolipids and hydrophilic polymers in avoiding rapid uptake of liposomes by the mononuclear phagocyte system. Adv Drug Deliv Rev. 1994;13:285-309.
49. Papahadjopoulos D, Allen TM, Gabizon A, et al. Sterically stabilized liposomes-improvements in pharmacokinetics and antitumor therapeutic efficacy. Proc Natl Acad Sci U S A. 1991;88:11460-11464.
50. Walkey CD, Olsen JB, Guo H, et al. Nanoparticle size and surface chemistry determine serum protein adsorption and macrophage uptake. J Am Chem Soc. 2012;134:2139-2147.
51. Oldenborg P-A, Zheleznyak A, Fang Y-F, et al. Role of CD47 as a marker of self on red blood cells. Science. 2000;288:2051-2054.
52. Rodriguez PL, Harada T, Christian DA, et al. Minimal "self " peptides that inhibit phagocytic clearance and enhance delivery of nanoparticles. Science. 2013;339:971-975.
53. Gratton SEA, Ropp PA, Pohlhaus PD, et al. The effect of particle design on cellular internalization pathways. Proc Natl Acad Sci U S A. 2008; 105:11613-11618.
54. Smith BR, Kempen P, Bouley D, et al. Shape matters: intravital microscopy reveals surprising geometrical dependence for nanoparticles in tumor models of extravasation. Nano Lett. 2012;12:3369-3377.
55. Chauhan VP, Popovic Z, Chen O, et al. Fluorescent nanorods and nanospheres for real-time in vivo probing of nanoparticle shape-dependent tumor penetration. Angew Chem Int Ed. 2011;50:11417-11420.
56. Geng Y, Dalhaimer P, Cai SS, et al. Shape effects of filaments versus spherical particles in flow and drug delivery. Nat Nanotechnol. 2007; 2:249-255.
57. Ruggiero A, Villa CH, Bander E, et al. Paradoxical glomerular filtration of carbon nanotubes. Proc Natl Acad Sci U S A. 2010;107:12369-12374.
58. Black KCL, Wang Y, Luehmann HP, et al. Radioactive 198Au-doped nanostructures with different shapes for in vivo analyses of their biodistribution, tumor uptake, and intratumoral distribution. ACS Nano. 2014;8:4385-4394.
59. BlumAP, Kammeyer JK, Rush AM, et al. Stimuli-responsive nanomaterials for biomedical applications. J Am Chem Soc. 2015;137:2140-2154.
60. Tong R, Tang L,Ma L, et al. Smart chemistry in polymeric nanomedicine. Chem Soc Rev. 2014;43:6982-7012.
61. HelmlingerG,Yuan F,Dellian M, et al. Interstitial pHand PO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat Med. 1997;3:177-182.
62. Höckel M, Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst. 2001;93:266-276.
63. Schumacker PT. Reactive oxygen species in cancer cells: live by the sword, die by the sword. Cancer Cell. 2006;10:175-176.
64. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell;141:52-67.
65. Timko BP, Dvir T, Kohane DS. Remotely triggerable drug delivery systems. Adv Mater. 2010;22:4925-4943.
66. Tong R, Kohane DS. Shedding light on nanomedicine. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2012;4:638-662.
67. NtziachristosV, Ripoll J,Wang LV, et al. Looking and listening to light: the evolution of whole-body photonic imaging. Nat Biotechnol. 2005;23: 313-320.
68. Hong G, Lee JC, Robinson JT, et al. Multifunctional in vivo vascular imaging using near-infrared II fluorescence. Nat Med. 2012;18:1841-1846.
69. Song CW. Effect of local hyperthermia on blood flow and microenvironment: a review. Cancer Res. 1984;44:4721s-4730s.
70. Manzoor AA, Lindner LH, Landon CD, et al. Overcoming limitations in nanoparticle drug delivery: triggered, intravascular release to improve drug penetration into tumors. Cancer Res. 2012;72:5566-5575.
71. Zagar TM, Vujaskovic Z, Formenti S, et al. Two phase I dose-escalation/ pharmacokinetics studies of low temperature liposomal doxorubicin (LTLD) andmild local hyperthermia in heavily pretreated patientswith local regionally recurrent breast cancer. Int J Hyperthermia. 2014;30:285-294.
72. Huang X, Jain P, El-Sayed I, et al. Plasmonic photothermal therapy (PPTT) using gold nanoparticles. Lasers Med Sci. 2008;23:217-228.
73. MelanconMP, ZhouM, Li C. Cancer Theranostics with near-infrared lightactivatable multimodal nanoparticles. Acc Chem Res. 2011;44:947-956.
74. von Maltzahn G, Park J-H, Lin KY, et al. Nanoparticles that communicate in vivo to amplify tumour targeting. Nat Mater. 2011;10:545-552.
75. Buckway B, Frazier N, Gormley AJ, et al. Gold nanorod-mediated hyperthermia enhances the efficacy of HPMA copolymer-90Y conjugates in treatment of prostate tumors. Nucl Med Biol. 2014;41:282-289.
76. Lovell JF, Jin CS, Huynh E, et al. Porphysome nanovesicles generated by porphyrin bilayers for use as multimodal biophotonic contrast agents. Nat Mater. 2011;10:324-332.
77. Carter KA, Shao S, Hoopes MI, et al. Porphyrin-phospholipid liposomes permeabilized by near-infrared light. Nat Commun. 2014;5:3546.
78. YavuzMS,ChengY, Chen J, et al.Gold nanocages covered by smart polymers for controlled release with near-infrared light. Nat Mater. 2009;8:935-939.
79. Wang LV. Multiscale photoacoustic microscopy and computed tomography. Nat Photon. 2009;3:503-509.
80. Li M-L, Wang JC, Schwartz JA, et al. In-vivo photoacoustic microscopy of nanoshell extravasation from solid tumor vasculature. J Biomed Opt. 2009;14:010507.
81. Kim C, Cho EC, Chen J, et al. In vivo molecular photoacoustic tomography of melanomas targeted by bioconjugated gold nanocages. ACS Nano. 2010;4:4559-4564.
82. Lu W, Melancon MP, Xiong C, et al. Effects of photoacoustic imaging and photothermal ablation therapy mediated by targeted hollow gold nanospheres in an orthotopic mouse xenograft model of glioma. Cancer Res. 2011;71:6116-6121.
83. Kim J-W, Galanzha EI, Shashkov EV, et al. Golden carbon nanotubes as multimodal photoacoustic and photothermal high-contrast molecular agents. Nat Nanotechnol. 2009;4:688-694.
84. Kircher MF, de la Zerda A, Jokerst JV, et al. A brain tumor molecular imaging strategy using a new triple-modality MRI-photoacoustic-Raman nanoparticle. Nat Med. 2012;18:829-834.
85. Tong R, Hemmati HD, Langer R, et al. Photoswitchable nanoparticles for triggered tissue penetration and drug delivery. J AmChemSoc. 2012;134: 8848-8855.
86. Tong R, Chiang HH, Kohane DS. Photoswitchable nanoparticles for in vivo cancer chemotherapy. Proc Natl Acad Sci U S A. 2013;110:19048-19053.
87. Jain RK. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat Med. 2001;7:987-989.
88. McKee TD, Grandi P, Mok W, et al. Degradation of fibrillar collagen in a human melanoma xenograft improves the efficacy of an oncolytic herpes simplex virus vector. Cancer Res. 2006;66:2509-2513.
89. MokW, Boucher Y, Jain RK. Matrix metalloproteinases-1 and-8 improve the distribution and efficacy of an oncolytic virus. Cancer Res. 2007;67: 10664-10668.
90. Provenzano PP, Cuevas C, Chang AE, et al. Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell. 2012;21:418-429.
91. Feng S, Agoulnik IU, Bogatcheva NV, et al. Relaxin promotes prostate cancer progression. Clin Cancer Res. 2007;13:1695-1702.
92. Diop-Frimpong B, Chauhan VP, Krane S, et al. Losartan inhibits collagen I synthesis and improves the distribution and efficacy of nanotherapeutics in tumors. Proc Natl Acad Sci U S A. 2011;108:2909-2914.
93. Chauhan VP, Martin JD, Liu H, et al. Angiotensin inhibition enhances drug delivery and potentiates chemotherapy by decompressing tumour blood vessels. Nat Commun. 2013;4.
94. Nakai Y, Isayama H, Ijichi H, et al. A multicenter phase II trial of gemcitabine and candesartan combination therapy in patientswith advanced pancreatic cancer: GECA2. Invest New Drugs. 2013;31:1294-1299.
95. Whatcott CJ, Han H, Posner RG, et al. Targeting the tumor microenvironment in cancer: why hyaluronidase deserves a second look. Cancer Discov. 2011;1:291-296.
96. Sugahara KN, Teesalu T, Karmali PP, et al. Coadministration of a tumorpenetrating peptide enhances the efficacy of cancer drugs. Science. 2010; 328:1031-1035.
97. Teesalu T, Sugahara KN, Kotamraju VR, et al. C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc Natl Acad Sci U S A. 2009;106:16157-16162.
98. Pang HB, Braun GB, Friman T, et al. An endocytosis pathway initiated through neuropilin-1 and regulated by nutrient availability. Nat Commun. 2014;5:4904.
99. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer. 2004;4:891-899.
100. Som P, Atkins HL, Bandoypadhyay D, et al. A fluorinated glucose analog, 2-fluoro-2-deoxy-D-glucose (F-18): nontoxic tracer for rapid tumor detection. J NuclMed. 1980;21:670-675.
101. Kelloff GJ, Hoffman JM, Johnson B, et al. Progress and promise of FDGPET imaging for cancer patient management and oncologic drug development. Clin Cancer Res. 2005;11:2785-2808.
102. Laughlin ST, Baskin JM, Amacher SL, et al. In vivo imaging of membraneassociated glycans in developing zebrafish. Science. 2008;320:664-667.
103. Bertozzi CR. A decade of bioorthogonal chemistry. Acc Chem Res. 2011; 44:651-653.
104. Jewett JC, Bertozzi CR. Cu-free click cycloaddition reactions in chemical biology. Chem Soc Rev. 2010;39:1272-1279.
105. Devaraj NK, Weissleder R. Biomedical applications of tetrazine cycloadditions. Acc Chem Res. 2011;44:816-827.
106. Koo H, Lee S, Na JH, et al. Bioorthogonal copper-free click chemistry in vivo for tumor-targeted delivery of nanoparticles. Angew Chem Int Ed. 2012;51:11836-11840.
107. Zlitni A, JanzenN, Foster FS, et al. Catching bubbles: targeting ultrasound microbubbles using bioorthogonal inverse-electron-demand diels-alder reactions. Angew Chem Int Ed. 2014;53:6459-6463.
108. Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol. 2007; 25:267-296.
109. Boon T, Coulie PG, Van den Eynde BJ, et al. Human T cell responses against melanoma. Annu Rev Immunol. 2006;24:175-208.
110. Zhang L, Conejo-Garcia JR, Katsaros D, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med. 2003;348: 203-213.
111. Galon J, Costes A, Sanchez-Cabo F, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006;313:1960-1964.
112. ZouW, Chen L. Inhibitory B7-family molecules in the tumour microenvironment. Nat Rev Immunol. 2008;8:467-477.
113. PardollDM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252-264.
114. Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature. 2011;480:480-489.
115. Hodi FS, O'Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010; 363:711-723.
116. Hamid O, Robert C, Daud A, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med. 2013;369: 134-144.
117. Robert C, Long GV, Brady B, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 2015;372:320-330.
118. Reddy ST, van der Vlies AJ, Simeoni E, et al. Exploiting lymphatic transport and complement activation in nanoparticle vaccines. Nat Biotechnol. 2007;25:1159-1164.
119. Manolova V, Flace A, Bauer M, et al. Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol. 2008;38: 1404-1413.
120. Cho NH, Cheong T-C, Min JH, et al. A multifunctional core-shell nanoparticle for dendritic cell-based cancer immunotherapy. Nat Nano. 2011; 6:675-682.
121. de Titta A, Ballester M, Julier Z, et al. Nanoparticle conjugation of CpG enhances adjuvancy for cellular immunity and memory recall at low dose. Proc Natl Acad Sci U S A. 2013;110:19902-19907.
122. Nembrini C, Stano A,DaneKY, et al. Nanoparticle conjugation of antigen enhances cytotoxic T-cell responses in pulmonary vaccination. Proc Natl Acad Sci U S A. 2011;108:E989-E997.
123. LiAV,Moon JJ, AbrahamW, et al. Generation of effector memory T cell-based mucosal and systemic immunity with pulmonary nanoparticle vaccination. Sci Transl Med. 2013;5:204ra130.
124. Rosenberg SA, Restifo NP, Yang JC, et al. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer. 2008;8: 299-308.
125. Stephan MT, Moon JJ, Um SH, et al. Therapeutic cell engineering with surface-conjugated synthetic nanoparticles. Nat Med. 2010;16: 1035-1041.
126. Wang C, Xu L, Liang C, et al. Immunological responses triggered by photothermal therapy with carbon nanotubes in combination with anti-CTLA-4 therapy to inhibit cancer metastasis. Adv Mater. 2014;26: 8154-8162.
127. Weldon C, Tian B, Kohane DS. Nanotechnology for surgeons. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2011;3:223-228.
128. Langer R. Perspectives: drug delivery-drugs on target. Science. 2001; 293:58-59.
129. Mehlen P, Puisieux A. Metastasis: a question of life or death. Nat Rev Cancer. 2006;6:449-458.
130. Kohane DS, Langer R. Biocompatibility and drug delivery systems. Chem Sci. 2010;1:441-446.