Advances in an active and passive targeting to tumor and adipose tissues

Expert Opinion on Drug Delivery

Volumn 12, Issue 1, 2015, Pages 41-52

  Sakurai, Yu ^a   Kajimoto, Kazuaki ^a   Hatakeyama, Hiroto ^b   Harashima, Hideyoshi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Active targeting; Anti obese effect; Antitumor; Enhanced permeability and retention effect; Passive targeting; Vascular targeting

Indexed keywords

ANTINEOPLASTIC AGENT; ARGINYLGLYCYLASPARTIC ACID; DOXORUBICIN; IMMUNOLIPOSOME; LIPOSOME; MACROGOL; MULTIFUNCTIONAL ENVELOPE TYPE NANODEVICE; NANOCARRIER; SMALL INTERFERING RNA; SMALL MOLECULE TRANSPORT AGENT; UNCLASSIFIED DRUG; LIGAND; MACROGOL DERIVATIVE; NANOPARTICLE; PEPTIDE;

ADIPOCYTE; ADIPOSE TISSUE; ADIPOSE TISSUE CELL; ANTIANGIOGENIC THERAPY; CANCER CHEMOTHERAPY; CANCER TISSUE; DRUG ACTIVE TARGETING; DRUG PASSIVE TARGETING; DRUG TARGETING; HUMAN; INTRAABDOMINAL FAT; LIPOSOMAL DELIVERY; MAXIMUM TOLERATED DOSE; MOLECULARLY TARGETED THERAPY; NONHUMAN; OBESITY; PARTICLE SIZE; PROTEIN TRANSPORT; RETICULOENDOTHELIAL SYSTEM; REVIEW; RNA INTERFERENCE; STROMA CELL; TUMOR VASCULARIZATION; ANIMAL; CHEMISTRY; DRUG DELIVERY SYSTEM; ENDOTHELIUM CELL; METABOLISM; MOUSE; NEOPLASMS; PATHOLOGY; PH; PROCEDURES; VASCULARIZATION;

ADIPOSE TISSUE; ANIMALS; DRUG DELIVERY SYSTEMS; ENDOTHELIAL CELLS; HYDROGEN-ION CONCENTRATION; LIGANDS; LIPOSOMES; MICE; NANOPARTICLES; NEOPLASMS; OBESITY; PEPTIDES; POLYETHYLENE GLYCOLS; RNA, SMALL INTERFERING;

EID: 84919430812     PISSN: 17425247     EISSN: 17447593     Source Type: Journal    
DOI: 10.1517/17425247.2015.955847     Document Type: Review

References (106)

1. Gabizon A, Shiota R, Papahadjopoulos D. Pharmacokinetics and tissue distribution of doxorubicin encapsulated in stable liposomes with long circulation times. J Natl Cancer Inst 1989;81:1484-8
2. Nakamura T, Akita H, Yamada Y, et al. A multifunctional envelope-type nanodevice for use in nanomedicine: concept and applications. Acc Chem Res 2012;45:1113-21
3. Kamiya H, Akita H, Harashima H. Pharmacokinetic and pharmacodynamic considerations in gene therapy. Drug Discov Today 2003;8:990-6
4. 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;46:6387-92.
5. Hatakeyama H, Akita H, Harashima H. A multifunctional envelope type nano device (MEND) for gene delivery to tumours based on the EPR effect: a strategy for overcoming the PEG dilemma. Adv Drug Deliv Rev 2011;63:152-60
6. Kerbel RS, Kamen BA. The antiangiogenic basis of metronomic chemotherapy. Nat Rev Cancer 2004;4:423-36
7. Takimoto CH. Maximum tolerated dose: clinical endpoint for a bygone era? Target Oncol 2009;4:143-7
8. Petrelli NJ, Winer EP, Brahmer J, et al. Clinical Cancer Advances 2009: major research advances in cancer treatment, prevention, and screening-a report from the American Society of Clinical Oncology. J Clin Oncol 2009;27:6052-69
9. Allen TM, Cullis PR. Liposomal drug delivery systems: from concept to clinical applications. Adv Drug Deliv Rev 2013;65:36-48.
10. 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 2013;65:71-9
11. Immordino ML, Dosio F, Cattel L. Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential. Int J Nanomedicine 2006;1:297-315
12. Davis ME, Chen ZG, Shin DM. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat Rev Drug Discov 2008;7:771-82
13. Prabhakar U, Maeda H, Jain RK, et al. Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology. Cancer Res 2013;73:2412-17
14. Suzuki R, Takizawa T, Kuwata Y, et al. Effective anti-tumor activity of oxaliplatin encapsulated in transferrin-PEG-liposome. Int J Pharm 2008;346:143-50
15. Nellis DF, Giardina SL, Janini GM, et al. Preclinical manufacture of anti-HER2 liposome-inserting, scFv-PEG-lipid conjugate. 2. Conjugate micelle identity, purity, stability, and potency analysis. Biotechnol Prog 2005;21:221-32
16. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971;285:1182-6
17. Kerbel RS. Inhibition of tumor angiogenesis as a strategy to circumvent acquired resistance to anti-cancer therapeutic agents. Bioessays 1991;13:31-6
18. Kerbel RS. Tumor angiogenesis: past, present and the near future. Carcinogenesis 2000;21:505-15
19. Hayman SR, Leung N, Grande JP, Garovic VD. VEGF inhibition, hypertension, and renal toxicity. Curr Oncol Rep 2012;14:285-94
20. Elice F, Rodeghiero F. Side effects of anti-angiogenic drugs. Thromb Res 2012;129(Suppl 1):S50-3
21. Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG. Cancer drug resistance: an evolving paradigm. Nat Rev Cancer 2013;13:714-26
22. Kibria G, Hatakeyama H, Harashima H. Cancer multidrug resistance: mechanismsinvolved and strategies for circumvention using a drug delivery system. Arch Pharm Res 2014;37:4-15
23. Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 2008;8:592-603
24. Nanda A, St Croix B. Tumor endothelial markers: new targets for cancer therapy. Curr Opin Oncol 2004;16:44-9
25. Arap W, Pasqualini R, Ruoslahti E. Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model. Science 1998;279:377-80
26. Barczyk M, Carracedo S, Gullberg D. Integrins. Cell Tissue Res 2010;339:269-80
27. Murphy EA, Majeti BK, Barnes LA, et al. Nanoparticle-mediated drug delivery to tumor vasculature suppresses metastasis. Proc Natl Acad Sci USA 2008;105:9343-8
28. Pasqualini R, Koivunen E, Kain R, et al. Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis. Cancer Res 2000;60:722-7
29. van Hensbergen Y, Broxterman HJ, Elderkamp YW, et al. A doxorubicin-CNGRC-peptide conjugate with prodrug properties. Biochem Pharmacol 2002;63:897-908
30. Pastorino F, Brignole C, Marimpietri D, et al. Vascular damage and antiangiogenic effects of tumor vesseltargeted liposomal chemotherapy. Cancer Res 2003;63:7400-9
31. Pastorino F, Brignole C, Di Paolo D, et al. Targeting liposomal chemotherapy via both tumor cell-specific and tumor vasculature-specific ligands potentiates therapeutic efficacy. Cancer Res 2006;66:10073-82
32. Pastorino F, Di Paolo D, Piccardi F, et al. Enhanced antitumor efficacy of clinical-grade vasculature-targeted liposomal doxorubicin. Clin Cancer Res 2008;14:7320-9
33. Loi M, Marchio S, Becherini P, et al. Combined targeting of perivascular and endothelial tumor cells enhances antitumor efficacy of liposomal chemotherapy in neuroblastoma. J Control Release 2010;145:66-73
34. Asai T, Miyazawa S, Maeda N, et al. Antineovascular therapy with angiogenic vessel-targeted polyethyleneglycol-shielded liposomal DPP-CNDAC. Cancer Sci 2008;99:1029-33
35. Gosk S, Moos T, Gottstein C, Bendas G. VCAM-1 directed immunoliposomes selectively target tumor vasculature in vivo. Biochim Biophys Acta 2008;1778:854-63
36. Wicki A, Rochlitz C, Orleth A, et al. Targeting tumor-associated endothelial cells: anti-VEGFR2 immunoliposomes mediate tumor vessel disruption and inhibit tumor growth. Clin Cancer Res 2012;18:454-64
37. Mann AP, Bhavane RC, Somasunderam A, et al. Thioaptamer conjugated liposomes for tumor vasculature targeting. Oncotarget 2011;2:298-304
38. Takara K, Hatakeyama H, Ohga N, et al. Design of a dual-ligand system using a specific ligand and cell penetrating peptide, resulting in a synergistic effect on selectivity and cellular uptake. Int J Pharm 2010;396:143-8
39. Takara K, Hatakeyama H, Kibria G, et al. Size-controlled, dual-ligand modified liposomes that target the tumor vasculature show promise for use in drug-resistant cancer therapy. J Control Release 2012;162:225-32
40. Kibria G, Hatakeyama H, Ohga N, et al. Dual-ligand modification of PEGylated liposomes shows better cell selectivity and efficient gene delivery. J Control Release 2011;153:141-8
41. Gentile F, Curcio A, Indolfi C, et al. The margination propensity of spherical particles for vascular targeting in the microcirculation. J Nanobiotechnology 2008;6:9
42. Kibria G, Hatakeyama H, Ohga N, et al. The effect of liposomal size on the targeted delivery of doxorubicin to Integrin alphavbeta3-expressing tumor endothelial cells. Biomaterials 2013;34:5617-27
43. Kanasty R, Dorkin JR, Vegas A, Anderson D. Delivery materials for siRNA therapeutics. Nat Mater 2013;12:967-77
44. Whitehead KA, Langer R, Anderson DG. Knocking down barriers: advances in siRNA delivery. Nat Rev Drug Discov 2009;8:129-38
45. Hatakeyama H, Akita H, Harashima H. The polyethyleneglycol dilemma: advantage and disadvantage of PEGylation of liposomes for systemic genes and nucleic acids delivery to tumors. Biol Pharm Bull 2013;36:892-9
46. Sato Y, Hatakeyama H, Sakurai Y, et al. A pH-sensitive cationic lipid facilitates the delivery of liposomal siRNA and gene silencing activity in vitro and in vivo. J Control Release 2012;163:267-76
47. Hatakeyama H, Murata M, Sato Y, et al. The systemic administration of an antimiRNA oligonucleotide encapsulated pH-sensitive liposome results in reduced level of hepatic microRNA-122 in mice. J Control Release 2013;173:45-50
48. Sakurai Y, Hatakeyama H, Sato Y, et al. Gene silencing via RNAi and siRNA quantification in tumor tissue using MEND, a liposomal siRNA delivery system. Mol Ther 2013;21:1195-203
49. Hayashi Y, Suemitsu E, Kajimoto K, et al. Hepatic monoacylglycerol o-acyltransferase 1 as a promising therapeutic target for steatosis, obesity and type2 diabetes. Mol Ther Nucleic Acids 2014;3:e154
50. Sakurai Y, Hatakeyama H, Sato Y, et al. RNAi-mediated gene knockdown and anti-angiogenic therapy of RCCs using a cyclic RGD-modified liposomalsiRNA system. J Control Release 2014;173:110-18.
51. Kagaya H, Oba M, Miura Y, et al. Impact of polyplex micelles installed with cyclic RGD peptide as ligand on gene delivery to vascular lesions. Gene Ther 2012;19:61-9
52. Alam MR, Ming X, Fisher M, et al. Multivalent cyclic RGD conjugates for targeted delivery of small interfering RNA. Bioconjug Chem 2011;22:1673-81
53. Kiss AL, Botos E. Endocytosis via caveolae: alternative pathway with distinct cellular compartments to avoid lysosomal degradation? J Cell Mol Med 2009;13:1228-37
54. Kolonin MG, Saha PK, Chan L, et al. Reversal of obesity by targeted ablationof adipose tissue. Nat Med 2004;10:625-32.
55. Liu X, Ren Z, Zhan R, et al. Prohibitin protects against oxidative stress-induced cell injury in cultured neonatal cardiomyocyte. Cell Stress Chaperones 2009;14:311-19
56. Thuaud F, Ribeiro N, Nebigil CG, Desaubry L. Prohibitin ligands in cell death and survival: mode of action and therapeutic potential. Chem Biol 2013;20:316-31
57. Kolonin MG, Evans KW, Mani SA, Gomer RH. Alternative origins of stroma in normal organs and disease. Stem Cell Res 2012;8:312-23
58. Yurugi H, Tanida S, Ishida A, et al. Expression of prohibitins on the surface of activated T cells. Biochem Biophys Res Commun 2012;420:275-80
59. Sharma A, Qadri A. Vi polysaccharide of Salmonella typhi targets the prohibitin family of molecules in intestinal epithelial cells and suppresses early inflammatory responses. Proc Natl Acad Sci USA 2004;101:17492-7
60. Azhdarinia A, Daquinag AC, Tseng C, et al. A peptide probe for targeted brown adipose tissue imaging. Nat Commun 2013;4:2472
61. Daquinag AC, Zhang Y, Amaya-Manzanares F, et al. An isoform of decorin is a resistin receptor on the surface of adipose progenitor cells. Cell Stem Cell 2011;9:74-86
62. Lee NK, Kim HS, Kim KH, et al. Identification of a novel peptide ligand targeting visceral adipose tissue via transdermal route by in vivo phage display. J Drug Target 2011;19:805-13
63. Liu J, Liu H, Sefah K, et al. Selection of aptamers specific for adipose tissue. PLoS One 2012;7:e37789
64. Hobson B, Denekamp J. Endothelial proliferation in tumours and normal tissues: continuous labelling studies. Br J Cancer 1984;49:405-13
65. Lijnen HR, Christiaens V, Scroyen I, et al. Impaired adipose tissue development in mice with inactivation of placental growth factor function. Diabetes 2006;55:2698-704
66. Lijnen HR, Frederix L, Van Hoef B. Fumagillin reduces adipose tissue formation in murine models of nutritionally induced obesity. Obesity (Silver Spring) 2010;18:2241-6
67. Varzaneh FE, Shillabeer G, Wong KL, Lau DC. Extracellular matrix components secreted by microvascular endothelial cells stimulate preadipocyte differentiation in vitro. Metabolism 1994;43:906-12
68. Cao Y. Angiogenesis modulates adipogenesis and obesity. J Clin Invest 2007;117:2362-8
69. Tran KV, Gealekman O, Frontini A, et al. The vascular endothelium of the adipose tissue gives rise to both white and brown fat cells. Cell Metab 2012;15:222-9
70. Hausman GJ, Richardson RL. Adipose tissue angiogenesis. J Anim Sci 2004;82:925-34
71. Christiaens V, Lijnen HR. Angiogenesis and development of adipose tissue. Mol Cell Endocrinol 2010;318:2-9
72. Rutkowski JM, Davis KE, Scherer PE. Mechanisms of obesity and related pathologies: the macro- and microcirculation of adipose tissue. FEBS J 2009;276:5738-46
73. Elias I, Franckhauser S, Ferre T, et al. Adipose tissue overexpression of vascular endothelial growth factor protects against diet-induced obesity and insulin resistance. Diabetes 2012;61:1801-13
74. Rupnick MA, Panigrahy D, Zhang CY, et al. Adipose tissue mass can be regulated through the vasculature. Proc Natl Acad Sci USA 2002;99:10730-5.
75. Brakenhielm E, Cao R, Gao B, et al. Angiogenesis inhibitor, TNP-470, prevents diet-induced and genetic obesity in mice. Circ Res 2004;94:1579-88
76. Ellerby HM, Arap W, Ellerby LM, et al. Anti-cancer activity of targeted pro-apoptotic peptides. Nat Med 1999;5:1032-8
77. Kim DH, Woods SC, Seeley RJ. Peptide designed to elicit apoptosis in adipose tissue endothelium reduces food intake and body weight. Diabetes 2010;59:907-15
78. Barnhart KF, Christianson DR, Hanley PW, et al. A peptidomimetic targeting white fat causes weight loss and improved insulin resistance in obese monkeys. Sci Transl Med 2011;3:108ra12
79. Staquicini FI, Cardo-Vila M, Kolonin MG, et al. Vascular ligandreceptor mapping by direct combinatorial selection in cancer patients. Proc Natl Acad Sci USA 2011;108:18637-42
80. Karjalainen K, Jaalouk DE, Bueso-Ramos CE, et al. Targeting neuropilin-1 in human leukemia and lymphoma. Blood 2011;117:920-7
81. Agemy L, Friedmann-Morvinski D, Kotamraju VR, et al. Targeted nanoparticle enhanced proapoptotic peptide as potential therapy for glioblastoma. Proc Natl Acad Sci USA 2011;108:17450-5
82. Hossen MN, Kajimoto K, Akita H, et al. Ligand-based targeted delivery of a peptide modified nanocarrier to endothelial cells in adipose tissue. J Control Release 2010;147:261-8
83. Kajimoto K, Hossen MN, Hida K, et al. Isolation and culture of microvascular endothelial cells from murine inguinal and epididymal adipose tissues. J Immunol Methods 2010;357:43-50
84. Hossen MN, Kajimoto K, Akita H, et al. Therapeutic assessment of cytochrome C for the prevention of obesity through endothelial cell-targeted nanoparticulate system. Mol Ther 2013;21:533-41
85. Willis M, Forssen E. Ligand-targeted liposomes. Adv Drug Deliv Rev 1998;29:249-71
86. Hua S, Wu SY. The use of lipid-based nanocarriers for targeted pain therapies. Front Pharmacol 2013;4:143
87. Hossen MN, Kajimoto K, Akita H, et al. Vascular-targeted nanotherapy for obesity: unexpected passive targeting mechanism to obese fat for the enhancement of active drug delivery. J Control Release 2012;163:101-10.
88. Emanuel N, Kedar E, Bolotin EM, et al. Targeted delivery of doxorubicin via sterically stabilized immunoliposomes: pharmacokinetics and biodistribution intumor-bearing mice. Pharm Res 1996;13:861-8
89. Iinuma H, Maruyama K, Okinaga K, et al. Intracellular targeting therapy of cisplatin-encapsulated transferrinpolyethylene glycol liposome on peritoneal dissemination of gastric cancer. Int J Cancer 2002;99:130-7
90. Turk MJ, Waters DJ, Low PS. Folate-conjugated liposomes preferentially target macrophages associated with ovarian carcinoma. Cancer Lett 2004;213:165-72
91. Chen Z, Deng J, Zhao Y, Tao T. Cyclic RGD peptide-modified liposomal drug delivery system: enhanced cellular uptake in vitro and improved pharmacokinetics in rats. Int J Nanomedicine 2012;7:3803-11
92. van Vlerken LE, Vyas TK, Amiji MM. Poly(ethylene glycol)-modified nanocarriers for tumor-targeted and intracellular delivery. Pharm Res 2007;24:1405-14
93. Sadzuka Y, Nakade A, Hirama R, et al. Effects of mixed polyethyleneglycol modification on fixed aqueous layer thickness and antitumor activity of doxorubicin containing liposome. Int J Pharm 2002;238:171-80
94. Gabizon A, Horowitz AT, Goren D, et al. Targeting folate receptor with folate linked to extremities of poly(ethylene glycol)-grafted liposomes: in vitro studies. Bioconjug Chem 1999;10:289-98
95. Danhier F, Feron O, Preat V. To exploit the tumor microenvironment: passive and active tumor targeting of nanocarriers for anti-cancer drug delivery. J Control Release 2010;148:135-46
96. Crielaard BJ, Lammers T, Schiffelers RM, Storm G. Drug targeting systems for inflammatory disease: one for all, all for one. J Control Release 2012;161:225-34
97. Hossen MN, Kajimoto K, Akita H, et al. A comparative study between nanoparticle-targeted therapeutics and bioconjugates as obesity medication. J Control Release 2013;171:104-12
98. Kajimoto K, Hossen MN, Harashima H. Antiangiogenic nanotherapy for the control of obesity. Nanomedicine 2013;8:671-3
99. Zalba S, Navarro I, Troconiz IF, et al. Application of different methods to formulate PEG-liposomes of oxaliplatin: evaluation in vitro and in vivo. Eur J Pharm Biopharm 2012;81:273-80
100. Szoka F Jr, Papahadjopoulos D. Procedure for preparation of liposomes with large internal aqueous space and high capture by reverse-phase evaporation. Proc Natl Acad Sci USA 1978;75:4194-8
101. Bangham AD, Standish MM, Watkins JC. Diffusion of univalent ions across the lamellae of swollen phospholipids. J Mol Biol 1965;13:238-52
102. Hossen MN, Kajimoto K, Tatsumi R, et al. Comparative assessments of crucial factors for a functional ligand-targeted nanocarrier. J Drug Target 2014;22:600-9
103. Gilleron J, Querbes W, Zeigerer A, et al. Image-based analysis of lipid nanoparticle-mediated siRNA delivery, intracellular trafficking and endosomal escape. Nat Biotechnol 2013;31:638-46
104. Khalil IA, Kogure K, Futaki S, Harashima H. High density of octaarginine stimulates macropinocytosis leading to efficient intracellular trafficking for gene expression. J Biol Chem 2006;281:3544-51
105. Sahay G, Querbes W, Alabi C, et al. Efficiency of siRNA delivery by lipid nanoparticles is limited by endocytic recycling. Nat Biotechnol 2013;31:653-8
106. Davis ME, Zuckerman JE, Choi CH, et al. Evidence of RNAi in humans from systemically administered siRNA via targeted nanoparticles. Nature 2010;464:1067-70