The EPR effect for macromolecular drug delivery to solid tumors: Improvement of tumor uptake, lowering of systemic toxicity, and distinct tumor imaging in vivo

Advanced Drug Delivery Reviews - Tập 65 Số 1 - Trang 71-79 - 2013
Hiroshi Maeda1, Hideaki Nakamura1, Jun Fang1
1DDS Research Institute, Sojo University, 4-22-1 Ikeda, Kumamoto 860-0082, Japan

Tóm tắt

Từ khóa


Tài liệu tham khảo

Matsumoto, 1984, Pathogenesis of serratial infection: activation of the Hageman factor-prekallikrein cascade by serratial protease, J. Biochem., 96, 739, 10.1093/oxfordjournals.jbchem.a134892

Kamata, 1985, A serratial protease causes vascular permeability reaction by activation of the Hageman factor-dependent pathway in guinea pigs, Infect. Immun., 48, 747, 10.1128/IAI.48.3.747-753.1985

Molla, 1989, Activation of Hageman factor and prekallikrein and generation of kinin by various microbial proteinases, J. Biol. Chem., 264, 10589, 10.1016/S0021-9258(18)81661-1

Maruo, 1993, Effect of microbial and mite proteases on low and high molecular weight kininogens, J. Biol. Chem., 268, 17711, 10.1016/S0021-9258(17)46762-7

Maeda, 1996, Pathogenic mechanisms induced by microbial proteases in microbial infections, Biol. Chem., 377, 217

Maeda, 1988, Purification and identification of [hydroxyprolyl3]bradykinin in ascitic fluid from a patient with gastric cancer, J. Biol. Chem., 263, 16051, 10.1016/S0021-9258(18)37555-0

Matsumura, 1988, Involvement of the kinin-generating cascade and enhanced vascular permeability in tumor tissue, Jpn. J. Cancer Res., 79, 1327, 10.1111/j.1349-7006.1988.tb01563.x

Matsumura, 1991, Kinin-generating cascade in advanced cancer patients and in vitro study, Jpn. J. Cancer Res., 82, 732, 10.1111/j.1349-7006.1991.tb01910.x

Maeda, 1994, Enhanced vascular permeability in solid tumor is mediated by nitric oxide and inhibited by both new nitric oxide scavenger and nitric oxide synthase inhibitor, Jpn. J. Cancer Res., 85, 331, 10.1111/j.1349-7006.1994.tb02362.x

Doi, 1996, Excessive production of nitric oxide in rat solid tumor and its implication in rapid tumor growth, Cancer, 77, 1598, 10.1002/(SICI)1097-0142(19960415)77:8<1598::AID-CNCR27>3.0.CO;2-U

Maeda, 1996, Bradykinin and nitric oxide in infectious disease and cancer, Immunopharmacology, 33, 222, 10.1016/0162-3109(96)00063-X

Wu, 2001, Enhanced vascular permeability in solid tumor involving peroxynitrite and matrix metalloproteinase, Jpn. J. Cancer Res., 92, 439, 10.1111/j.1349-7006.2001.tb01114.x

Wu, 1998, Modulation of enhanced vascular permeability in tumors by a bradykinin antagonist, a cyclooxygenase inhibitor, and a nitric oxide scavenger, Cancer Res., 58, 159

Tanaka, 2003, Modulation of tumor-selective vascular blood flow and extravasation by the stable prostaglandin I2 analogue beraprost sodium, J. Drug Target., 11, 45, 10.1080/1061186031000086072

Maeda, 2003, Vascular permeability enhancement in solid tumor: various factors, mechanisms involved and its implications, Int. Immunopharmacol., 3, 319, 10.1016/S1567-5769(02)00271-0

Matsumura, 1986, A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent SMANCS, Cancer Res., 46, 6387

Maeda, 2001, The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumor-selective macromolecular drug targeting, 189

Maeda, 2010, Tumor-selective delivery of macromolecular drugs via the EPR effect: background and future prospects, Bioconjug. Chem., 21, 797, 10.1021/bc100070g

Fang, 2011, The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect, Adv. Drug Deliv. Rev., 63, 136, 10.1016/j.addr.2010.04.009

Noguchi, 1998, Early phase tumor accumulation of macromolecules: a great difference in clearance rate between tumor and normal tissues, Jpn. J. Cancer Res., 89, 307, 10.1111/j.1349-7006.1998.tb00563.x

Seymour, 1995, Influence of molecular weight on passive tumour accumulation of a soluble macromolecular drug carrier, Eur. J. Cancer, 31, 766, 10.1016/0959-8049(94)00514-6

Maeda, 2000, Tumor vascular permeability and the EPR effect in macromolecular therapeutics, J. Control. Release, 65, 271, 10.1016/S0168-3659(99)00248-5

Maeda, 2001, Mechanism of tumor-targeted delivery of macromolecular drugs, including the EPR effect in solid tumor and clinical overview of the prototype polymeric drug SMANCS, J. Control. Release, 74, 47, 10.1016/S0168-3659(01)00309-1

Allen, 2004, Drug delivery systems: entering the mainstream, Science, 303, 1818, 10.1126/science.1095833

Nam, 2010, Tumor targeting chitosan nanoparticles for dual-modality optical/MR cancer imaging, Bioconjug. Chem., 21, 578, 10.1021/bc900408z

Silindir, 2012, Liposomes and their applications in molecular imaging, J. Drug Target., 20, 401, 10.3109/1061186X.2012.685477

Mahmud, 2007, Polymeric micelles for drug targeting, J. Drug Target., 15, 553, 10.1080/10611860701538586

Jakobsohn, 2012, Towards real-time detection of tumor margins using photothermal imaging of immune-targeted gold nanoparticles, Int. J. Nanomedicine, 7, 4707

Pellegrin, 2002, Macromolecular uptake is a spontaneous event during mitosis in cultured fibroblasts: implications for vector-dependent plasmid transfection, Mol. Biol. Cell, 13, 570, 10.1091/mbc.01-06-0280

Li, 2008, Pharmacokinetics and biodistribution of nanoparticles, Mol. Pharm., 5, 496, 10.1021/mp800049w

Duncan, 2011, Nanomedicine(s) under the microscope, Mol. Pharm., 8, 2101, 10.1021/mp200394t

Moghimi, 2005, Nanomedicine: current status and future prospects, FASEB J., 19, 311, 10.1096/fj.04-2747rev

Ogawa, 2009, Dual-modality molecular imaging using antibodies labeled with activatable fluorescence and a radionuclide for specific and quantitative targeted cancer detection, Bioconjug. Chem., 20, 2177, 10.1021/bc900362k

Keereweer, 2012, Targeting integrins and enhanced permeability and retention (EPR) effect for optical imaging of oral cancer, J. Surg. Oncol., 105, 714, 10.1002/jso.22102

Yu, 2010, The magnetophoretic mobility and superparamagnetism of core-shell iron oxide nanoparticles with dual targeting and imaging functionality, Biomaterials, 31, 5842, 10.1016/j.biomaterials.2010.03.072

Gormley, 2012, Guided delivery of polymer therapeutics using plasmonic photothermal therapy, Nano Today, 7, 158, 10.1016/j.nantod.2012.04.002

2011, vol. 1–3, 1

Senger, 1983, Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid, Science, 219, 983, 10.1126/science.6823562

Dvorak, 1988, Identification and characterization of the blood vessels of solid tumors that are leaky to circulating macromolecules, Am. J. Pathol., 133, 95

Folkman, 1971, Tumor angiogenesis: therapeutic implications, N. Engl. J. Med., 285, 1182, 10.1056/NEJM197111182852108

Folkman, 1990, What is the evidence that tumors are angiogenesis dependent?, J. Natl. Cancer Inst., 82, 4, 10.1093/jnci/82.1.4

Maeda, 2012, Vascular permeability in cancer and infection as related to macromolecular drug delivery, with emphasis on the EPR effect for tumor-selective drug targeting, Proc. Jpn Acad. B Phys. Biol. Sci., 88, 53, 10.2183/pjab.88.53

Akaike, 1996, Pathogenesis of influenza virus-induced pneumonia: involvement of both nitric oxide and oxygen radicals, Proc. Natl. Acad. Sci. U. S. A., 93, 2448, 10.1073/pnas.93.6.2448

Oda, 1989, Oxygen radicals in influenza-induced pathogenesis and treatment with pyran polymer-conjugated SOD, Science, 244, 974, 10.1126/science.2543070

Maeda, 1991, Oxygen free radicals as pathogenic molecules in viral diseases, Proc. Soc. Exp. Biol. Med., 198, 721, 10.3181/00379727-198-43309C

Seki, 2009, Enhanced delivery of macromolecular antitumor drugs to tumors by nitroglycerin application, Cancer Sci., 100, 2426, 10.1111/j.1349-7006.2009.01323.x

Maeda, 2010, Nitroglycerin enhances vascular blood flow and drug delivery in hypoxic tumor tissues: analogy between angina pectoris and solid tumors and enhancement of the EPR effect, J. Control. Release, 142, 296, 10.1016/j.jconrel.2010.01.002

Matsuzawa, 2008, Redox control of cell fate by MAP kinase: physiological roles of ASK1-MAP kinase pathway in stress signaling, Biochim. Biophys. Acta, 1780, 1325, 10.1016/j.bbagen.2007.12.011

Shiratori, 2006, Suppressive effects of astaxanthin against rat endotoxin-induced uveitis by inhibiting the NF-κB signaling pathway, Exp. Eye Res., 82, 275, 10.1016/j.exer.2005.06.023

Wlaschek, 1994, UVA-induced autocrine stimulation of fibroblast-derived collagenase/MMP-1 by interrelated loops of interleukin-1 and interleukin-6, Photochem. Photobiol., 59, 550, 10.1111/j.1751-1097.1994.tb02982.x

Kramarenko, 2012, The bradykinin B2 receptor induces multiple cellular responses leading to the proliferation of human renal carcinoma cell lines, Cancer Treat. Res., 4, 195

Cao, 2008, 4-Vinyl-2,6-dimethoxyphenol (canolol) suppresses oxidative stress and gastric carcinogenesis in Helicobacter pylori-infected carcinogen-treated Mongolian gerbils, Int. J. Cancer, 122, 1445, 10.1002/ijc.23245

Maeda, 1986, Cancer selective macromolecular therapeutics: tailoring of an antitumor protein drug, 353

Maeda, 1984, Tailor-making of protein drugs by polymer conjugation for tumor targeting: a brief review on smancs, J. Protein Chem., 3, 181, 10.1007/BF01040499

Maeda, 1994, Polymer conjugated macromolecular drugs for tumor-specific targeting, 95

He, 2010, Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles, Biomaterials, 31, 3657, 10.1016/j.biomaterials.2010.01.065

Lee, 2011, Circulation kinetics and biodistribution of dual-labeled polymersomes with modulated surface charge in tumor-bearing mice: comparison with stealth liposomes, J. Control. Release, 155, 282, 10.1016/j.jconrel.2011.07.028

Oda, 1986, Stimulation of macrophage by polyanions and its conjugated proteins and effect on cell membrane, Proc. Soc. Exp. Biol. Med., 181, 9, 10.3181/00379727-181-42218

Oda, 1987, Binding to and internalization by cultured cells of neocarzinostatin and enhancement of its actions by conjugation with lipophilic styrene-maleic acid copolymer, Cancer Res., 47, 3206

Oda, 1987, Facilitated internalization of neocarzinostatin and its lipophilic polymer conjugate, SMANCS, into cytosol in acidic pH, J. Nat. Cancer Inst., 9, 1205

Nakamura, 2011, Intracellular uptake and behavior of two types zinc protoporphyrin (ZnPP) micelles, SMA-ZnPP and PEG-ZnPP as anticancer agents; Unique intracellular disintegration of SMA micelles, J. Control. Release, 155, 367, 10.1016/j.jconrel.2011.04.025

Oda, 1990, Inactivation of chemotactic activity of C5a by the serratial 56-kilodalton protease, Infect. Immun., 58, 1269, 10.1128/IAI.58.5.1269-1272.1990

Maeda, 1985, Conjugation of poly (styrene-co-maleic acid) derivatives to the antitumor protein neocarzinostatin: pronounced improvements in pharmacological properties, J. Med. Chem., 28, 455, 10.1021/jm00382a012

Skinner, 1990, Microvascular architecture of experimental colon tumors in the rat, Cancer Res., 50, 2411

Konerding, 1995, Microvascular corrosion casting in the study of tumor vascularity: a review, Scanning Microsc., 9, 1233

Hashizume, 2000, Openings between defective endothelial cells explain tumor vessel leakiness, Am. J. Pathol., 1561, 1363, 10.1016/S0002-9440(10)65006-7

Suzuki, 1981, A new approach to cancer chemotherapy: selective enhancement of tumor blood flow with angiotensin II, J. Natl. Cancer Inst., 67, 663

Hori, 2000, blood flow decrease induced by an angiotensin converting enzyme inhibitor, temocapril hydrochloride, Jpn. J. Cancer Res., 91, 261, 10.1111/j.1349-7006.2000.tb00940.x

Iwai, 1984, Use of oily contrast medium for selective drug targeting to tumor: enhanced therapeutic effect and X-ray image, Cancer Res., 44, 2115

Konno, 1984, Selective targeting of anticancer drug and simultaneous image enhancement in solid tumors by arterially administered lipid contrast medium, Cancer, 54, 2367, 10.1002/1097-0142(19841201)54:11<2367::AID-CNCR2820541111>3.0.CO;2-F

Maki, 1985, Image enhancement in computerized tomography for sensitive diagnosis of liver cancer and semiquantitation of tumor selective drug targeting with oily contrast medium, Cancer, 56, 751, 10.1002/1097-0142(19850815)56:4<751::AID-CNCR2820560409>3.0.CO;2-Y

Konno, 1983, Effect of arterial administration of high-molecular-weight anticancer agent SMANCS with lipid lymphographic agent on hepatoma: a preliminary report, Eur. J. Cancer Clin. Oncol., 19, 1053, 10.1016/0277-5379(83)90028-7

Nagamitsu, 2009, Elevating blood pressure as a strategy to increase tumor targeted delivery of macromolecular drug SMANCS: cases of advanced solid tumors, Jpn. J. Clin. Oncol., 39, 756, 10.1093/jjco/hyp074

Yasuda, 2006, Randomized phase II trial comparing nitroglycerin plus vinorelbine and cisplatin with vinorelbine and cisplatin alone in previously untreated stage IIIB/IV non-small cell lung cancer, J. Clin. Oncol., 24, 688, 10.1200/JCO.2005.04.0436

Yasuda, 2006, Nitroglycerin treatment may increase response to docetaxel and carboplatin regimen via inhibitions of hypoxia-inducible factor-1 pathway and P-glycoprotein in patients with lung adenocarcinoma, Clin. Cancer Res., 12, 6748, 10.1158/1078-0432.CCR-06-1124

Yasuda, 2010, Therapeutic applications of nitric oxide for malignant tumor in animal models and human studies, 419

Siemens, 2009, Phase II study of nitric oxide donor for men with increasing prostate-specific antigen level after surgery or radiotherapy for prostate cancer, Urology, 74, 878, 10.1016/j.urology.2009.03.004

Noguchi, 1992, Enhanced tumor localization of monoclonal antibody by treatment with kininase II inhibitor and angiotensin II, Jpn. J. Cancer Res., 83, 240, 10.1111/j.1349-7006.1992.tb00093.x

Li, 1993, Augmentation of tumour delivery of macromolecular drugs with reduced bone marrow delivery by elevating blood pressure, Br. J. Cancer, 67, 975, 10.1038/bjc.1993.179

Fang, 2012, Carbon monoxide, generated by heme oxygenase-1, mediates the enhanced permeability and retention (EPR) effect of solid tumor, Cancer Sci., 102, 535, 10.1111/j.1349-7006.2011.02178.x

Kano, 2007, Improvement of cancer-targeting therapy, using nanocarriers for intractable solid tumors by inhibition of TGF-β signaling, Proc. Natl. Acad. Sci. U. S. A., 104, 3460, 10.1073/pnas.0611660104

Seki, 2011, Tumour necrosis factor-alpha increases extravasation of virus particles into tumour tissue by activating the Rho A/Rho kinase pathway, J. Control. Release, 156, 381, 10.1016/j.jconrel.2011.08.022