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Liposomes Conjugated with a Pilot Molecule

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Cancer Drug Delivery Systems Based on the Tumor Microenvironment

Abstract

The liposome is a lipid-based nanoparticle that is widely used as a drug encapsulation device and drug delivery system (DDS), because it enables the encapsulation of many drugs into it. Notably, the liposome is suitable as a targetable drug carrier, since it can be easily conjugated with functional pilot molecules such as antibody, peptide, sugar chain, etc., on its surface. These liposomes are referred to as active targeting liposomes, and they enable the encapsulated drugs or imaging agents to be delivered to specific sites for the treatment and diagnosis, respectively, of refractory diseases such as cancer. In this chapter, the advantages of the use of active-targeting liposomes as a tool of DDS and their application to cancer treatment are reviewed.

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Abbreviations

APRPG:

Ala-Pro-Arg-Pro-Gly

ASSHN:

Ala-Ser-Ser-His-Asn

BBB:

blood-brain barrier

BPA:

Bauhinia purprea agglutinin

BNCT:

boron neutron capture therapy

CT:

computed tomography

DDS:

drug delivery system

DCP:

dicetylphosphate

DOX:

doxorubicin

DSPE:

distearoylphosphatidylethanolamine

ECM:

extracellular matrix

EGF:

epidermal growth factor

EGFP:

enhanced green fluorescent protein

EPR:

enhanced permeability and retention

FR:

folate receptor

GPLPLR:

Gly-Pro-Leu-Pro-Leu-Arg

HB-EGF:

heparin-binding epidermal growth factor-like growth factor

HUVECs:

human umbilical vein endothelial cells

Mal:

maleimide

MRI:

magnetic resonance imaging

MT1-MMP:

membrane-type 1 matrix metalloproteinase

NGR:

Asn-Gly-Arg

NHS:

N-hydroxysuccinimide

OVA:

ovalbumin

PC:

phosphatidylcholine

PCL:

polycation liposome

PDT:

photodynamic therapy

PEG:

polyethylene glycol

PEI:

polyethylenimine

P-gp:

P-glycoprotein

PS:

phosphatidylserine

PTX:

paclitaxel

RES:

reticuloendothelial system

RGD:

Arg-Gly-Asp

siRNA:

small interfering RNA

sLeX:

sialyl LewisX

SM:

sphingomyelin

SWKLPPS:

Ser-Trp-Lys-Leu-Pro-Pro-Ser

TAMs:

tumor-associated macrophages

TEPA:

tetraethylenepentamine

Tf:

transferrin

VEGFR-1:

vascular endothelial growth factor receptor-1

WGA:

Wheat germ agglutinin

References

  1. Akita N, Maruta F, Seymour LW, Kerr DJ, Parker AL, Asai T, Oku N, Nakayama J, Miyagawa S (2006) Identification of oligopeptides binding to peritoneal tumors of gastric cancer. Cancer Sci 97:1075–1081

    Article  CAS  PubMed  Google Scholar 

  2. Alekseeva A, Kapkaeva M, Shcheglovitova O, Boldyrev I, Pazynina G, Bovin N, Vodovozova E (2015) Interactions of antitumour Sialyl Lewis X liposomes with vascular endothelial cells. Biochim Biophys Acta 1848:1099–1110

    Article  CAS  PubMed  Google Scholar 

  3. Allavena P, Mantovani A (2012) Immunology in the clinic review series; focus on cancer: tumour-associated macrophages: undisputed stars of the inflammatory tumour microenvironment. Clin Exp Immunol 167:195–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Allen TM, Cullis PR (2004) Drug delivery systems: entering the mainstream. Science 303:1818–1822

    Article  CAS  PubMed  Google Scholar 

  5. Allen TM, Cullis PR (2013) Liposomal drug delivery systems: from concept to clinical applications. Adv Drug Deliv Rev 65:36–48

    Article  CAS  PubMed  Google Scholar 

  6. Allen TM, Hansen C, Rutledge J (1989) Liposomes with prolonged circulation times: factors affecting uptake by reticuloendothelial and other tissues. Biochim Biophys Acta 981:27–35

    Article  CAS  PubMed  Google Scholar 

  7. Ando H, Okamoto A, Yokota M, Asai T, Dewa T, Oku N (2013) Polycation liposomes as a vector for potential intracellular delivery of microRNA. J Gene Med 15:375–383

    Article  CAS  PubMed  Google Scholar 

  8. Arap W, Pasqualini R, Ruoslahti E (1998) Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model. Science 279:377–380

    Article  CAS  PubMed  Google Scholar 

  9. Asai T, Kurohane K, Shuto S, Awano H, Matsuda A, Tsukada H, Namba Y, Okada S, Oku N (1998) Antitumor activity of 5′-O-dipalmitoylphosphatidyl 2′-C-cyano-2′-deoxy-1-beta-D-arabino-pentofuranosylcytosine is enhanced by long-circulating liposomalization. Biol Pharm Bull 21:766–771

    Article  CAS  PubMed  Google Scholar 

  10. Asai T, Shuto S, Matsuda A, Kakiuchi T, Ohba H, Tsukada H, Oku N (2001) Targeting and anti-tumor efficacy of liposomal 5′-O-dipalmitoylphosphatidyl 2′-C-cyano-2′-deoxy-1-beta-D-arabino-pentofuranosylcytosine in mice lung bearing B16BL6 melanoma. Cancer Lett 162:49–56

    Article  CAS  PubMed  Google Scholar 

  11. Asai T, Shimizu K, Kondo M, Kuromi K, Watanabe K, Ogino K, Taki T, Shuto S, Matsuda A, Oku N (2002) Anti-neovascular therapy by liposomal DPP-CNDAC targeted to angiogenic vessels. FEBS Lett 520:167–170

    Article  CAS  PubMed  Google Scholar 

  12. Asai T, Miyazawa S, Maeda N, Hatanaka K, Katanasaka Y, Shimizu K, Shuto S, Oku N (2008) Antineovascular therapy with angiogenic vessel-targeted polyethyleneglycol-shielded liposomal DPP-CNDAC. Cancer Sci 99:1029–1033

    Article  CAS  PubMed  Google Scholar 

  13. Asai T, Matsushita S, Kenjo E, Tsuzuku T, Yonenaga N, Koide H, Hatanaka K, Dewa T, Nango M, Maeda N, Kikuchi H, Oku N (2011) Dicetyl phosphate-tetraethylenepentamine-based liposomes for systemic siRNA delivery. Bioconjug Chem 22:429–435

    Article  CAS  PubMed  Google Scholar 

  14. Atobe K, Ishida T, Ishida E, Hashimoto K, Kobayashi H, Yasuda J, Aoki T, Obata K, Kikuchi H, Akita H, Asai T, Harashima H, Oku N, Kiwada H (2007) In vitro efficacy of a sterically stabilized immunoliposomes targeted to membrane type 1 matrix metalloproteinase (MT1-MMP). Biol Pharm Bull 30:972–978

    Article  CAS  PubMed  Google Scholar 

  15. Bocci G, Kerbel RS (2016) Pharmacokinetics of metronomic chemotherapy: a neglected but crucial aspect. Nat Rev Clin Oncol 13:659–673

    Article  CAS  PubMed  Google Scholar 

  16. Bogdanov AA Jr, Gordeeva LV, Torchilin VP, Margolis LB (1989) Lectin-bearing liposomes: differential binding to normal and to transformed mouse fibroblasts. Exp Cell Res 181:362–374

    Article  CAS  PubMed  Google Scholar 

  17. Bostic HE, Smith MD, Poloukhtine AA, Popik VV, Best MD (2012) Membrane labeling and immobilization via copper-free click chemistry. Chem Commun (Camb) 48:1431–1433

    Article  CAS  Google Scholar 

  18. Bruck A, Abu-Dahab R, Borchard G, Schafer UF, Lehr CM (2001) Lectin-functionalized liposomes for pulmonary drug delivery: interaction with human alveolar epithelial cells. J Drug Target 9:241–251

    Article  CAS  PubMed  Google Scholar 

  19. Burks SR, Macedo LF, Barth ED, Tkaczuk KH, Martin SS, Rosen GM, Halpern HJ, Brodie AM, Kao JP (2010) Anti-HER2 immunoliposomes for selective delivery of electron paramagnetic resonance imaging probes to HER2-overexpressing breast tumor cells. Breast Cancer Res Treat 124:121–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Cardoso AL, Simoes S, de Almeida LP, Plesnila N, Pedroso de Lima MC, Wagner E, Culmsee C (2008) Tf-lipoplexes for neuronal siRNA delivery: a promising system to mediate gene silencing in the CNS. J Control Release 132:113–123

    Article  CAS  PubMed  Google Scholar 

  21. Cardoso AL, Costa P, de Almeida LP, Simoes S, Plesnila N, Culmsee C, Wagner E, de Lima MC (2010) Tf-lipoplex-mediated c-Jun silencing improves neuronal survival following excitotoxic damage in vivo. J Control Release 142:392–403

    Article  CAS  PubMed  Google Scholar 

  22. Chantarasrivong C, Ueki A, Ohyama R, Unga J, Nakamura S, Nakanishi I, Higuchi Y, Kawakami S, Ando H, Imamura A, Ishida H, Yamashita F, Kiso M, Hashida M (2017) Synthesis and functional characterization of novel Sialyl LewisX mimic-decorated liposomes for E-selectin-mediated targeting to inflamed endothelial cells. Mol Pharm 14:1528–1537

    Article  CAS  PubMed  Google Scholar 

  23. Chaudhury A, Das S (2015) Folate receptor targeted liposomes encapsulating anti-cancer drugs. Curr Pharm Biotechnol 16:333–343

    Article  CAS  PubMed  Google Scholar 

  24. Chen X, Plasencia C, Hou Y, Neamati N (2005) Synthesis and biological evaluation of dimeric RGD peptide-paclitaxel conjugate as a model for integrin-targeted drug delivery. J Med Chem 48:1098–1106

    Article  CAS  PubMed  Google Scholar 

  25. Curnis F, Sacchi A, Borgna L, Magni F, Gasparri A, Corti A (2000) Enhancement of tumor necrosis factor alpha antitumor immunotherapeutic properties by targeted delivery to aminopeptidase N (CD13). Nat Biotechnol 18:1185–1190

    Article  CAS  PubMed  Google Scholar 

  26. Curnis F, Arrigoni G, Sacchi A, Fischetti L, Arap W, Pasqualini R, Corti A (2002) Differential binding of drugs containing the NGR motif to CD13 isoforms in tumor vessels, epithelia, and myeloid cells. Cancer Res 62:867–874

    CAS  PubMed  Google Scholar 

  27. Daemen T, Regts J, Scherphof GL (1996) Liposomal phosphatidylserine inhibits tumor cytotoxicity of liver macrophages induced by muramyl dipeptide and lipopolysaccharide. Biochim Biophys Acta 1285:219–228

    Article  CAS  PubMed  Google Scholar 

  28. de Oliveira FE, Albuquerque da Cunha CR, Albuquerque PBS, de Paula RA, Aranda-Souza MA, Alves MS, Zagmignan A, Carneiro-da-Cunha MG, Nascimento da Silva LC, Dos Santos Correia MT (2017) Lectin-carbohydrate interactions: implications for the development of new anticancer agents. Curr Med Chem 24:3667–3680

    Google Scholar 

  29. Derycke AS, Kamuhabwa A, Gijsens A, Roskams T, De Vos D, Kasran A, Huwyler J, Missiaen L, de Witte PA (2004) Transferrin-conjugated liposome targeting of photosensitizer AlPcS4 to rat bladder carcinoma cells. J Natl Cancer Inst 96:1620–1630

    Article  CAS  PubMed  Google Scholar 

  30. Di Paolo D, Pastorino F, Zuccari G, Caffa I, Loi M, Marimpietri D, Brignole C, Perri P, Cilli M, Nico B, Ribatti D, Pistoia V, Ponzoni M, Pagnan G (2013) Enhanced anti-tumor and anti-angiogenic efficacy of a novel liposomal fenretinide on human neuroblastoma. J Control Release 170:445–451

    Article  PubMed  CAS  Google Scholar 

  31. DiCorleto PE, de la Motte CA (1989) Role of cell surface carbohydrate moieties in monocytic cell adhesion to endothelium in vitro. J Immunol 143:3666–3672

    CAS  PubMed  Google Scholar 

  32. Ding N, Lu Y, Lee RJ, Yang C, Huang L, Liu J, Xiang G (2011) Folate receptor-targeted fluorescent paramagnetic bimodal liposomes for tumor imaging. Int J Nanomedicine 6:2513–2520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Doi A, Kawabata S, Iida K, Yokoyama K, Kajimoto Y, Kuroiwa T, Shirakawa T, Kirihata M, Kasaoka S, Maruyama K, Kumada H, Sakurai Y, Masunaga S, Ono K, Miyatake S (2008) Tumor-specific targeting of sodium borocaptate (BSH) to malignant glioma by transferrin-PEG liposomes: a modality for boron neutron capture therapy. J Neuro-Oncol 87:287–294

    Article  CAS  Google Scholar 

  34. Dougherty TJ, Gomer CJ, Henderson BW, Jori G, Kessel D, Korbelik M, Moan J, Peng Q (1998) Photodynamic therapy. J Natl Cancer Inst 90:889–905

    Article  CAS  PubMed  Google Scholar 

  35. Du J, Lu WL, Ying X, Liu Y, Du P, Tian W, Men Y, Guo J, Zhang Y, Li RJ, Zhou J, Lou JN, Wang JC, Zhang X, Zhang Q (2009) Dual-targeting topotecan liposomes modified with tamoxifen and wheat germ agglutinin significantly improve drug transport across the blood-brain barrier and survival of brain tumor-bearing animals. Mol Pharm 6:905–917

    Article  CAS  PubMed  Google Scholar 

  36. Dubey PK, Mishra V, Jain S, Mahor S, Vyas SP (2004) Liposomes modified with cyclic RGD peptide for tumor targeting. J Drug Target 12:257–264

    Article  CAS  PubMed  Google Scholar 

  37. Fleiner M, Benzinger P, Fichert T, Massing U (2001) Studies on protein-liposome coupling using novel thiol-reactive coupling lipids: influence of spacer length and polarity. Bioconjug Chem 12:470–475

    Article  CAS  PubMed  Google Scholar 

  38. Frisch B, Hassane FS, Schuber F (2010) Conjugation of ligands to the surface of preformed liposomes by click chemistry. Methods Mol Biol 605:267–277

    Article  CAS  PubMed  Google Scholar 

  39. Fukuta T, Asai T, Kiyokawa Y, Nakada T, Bessyo-Hirashima K, Fukaya N, Hyodo K, Takase K, Kikuchi H, Oku N (2017) Targeted delivery of anticancer drugs to tumor vessels by use of liposomes modified with a peptide identified by phage biopanning with human endothelial progenitor cells. Int J Pharm 524:364–372

    Article  CAS  PubMed  Google Scholar 

  40. Gabizon A, Papahadjopoulos D (1988) Liposome formulations with prolonged circulation time in blood and enhanced uptake by tumors. Proc Natl Acad Sci U S A 85:6949–6953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Gabizon A, Shmeeda H, Horowitz AT, Zalipsky S (2004) Tumor cell targeting of liposome-entrapped drugs with phospholipid-anchored folic acid-PEG conjugates. Adv Drug Deliv Rev 56:1177–1192

    Article  CAS  PubMed  Google Scholar 

  42. Gabizon A, Tzemach D, Gorin J, Mak L, Amitay Y, Shmeeda H, Zalipsky S (2010) Improved therapeutic activity of folate-targeted liposomal doxorubicin in folate receptor-expressing tumor models. Cancer Chemother Pharmacol 66:43–52

    Article  CAS  PubMed  Google Scholar 

  43. Gao J, Liu W, Xia Y, Li W, Sun J, Chen H, Li B, Zhang D, Qian W, Meng Y, Deng L, Wang H, Chen J, Guo Y (2011) The promotion of siRNA delivery to breast cancer overexpressing epidermal growth factor receptor through anti-EGFR antibody conjugation by immunoliposomes. Biomaterials 32:3459–3470

    Article  CAS  PubMed  Google Scholar 

  44. Gao J, Yu Y, Zhang Y, Song J, Chen H, Li W, Qian W, Deng L, Kou G, Chen J, Guo Y (2012) EGFR-specific PEGylated immunoliposomes for active siRNA delivery in hepatocellular carcinoma. Biomaterials 33:270–282

    Article  CAS  PubMed  Google Scholar 

  45. Gao JQ, Lv Q, Li LM, Tang XJ, Li FZ, Hu YL, Han M (2013) Glioma targeting and blood-brain barrier penetration by dual-targeting doxorubincin liposomes. Biomaterials 34:5628–5639

    Article  CAS  PubMed  Google Scholar 

  46. Geng L, Osusky K, Konjeti S, Fu A, Hallahan D (2004) Radiation-guided drug delivery to tumor blood vessels results in improved tumor growth delay. J Control Release 99:369–381

    Article  CAS  PubMed  Google Scholar 

  47. Gijsens A, Derycke A, Missiaen L, De Vos D, Huwyler J, Eberle A, de Witte P (2002) Targeting of the photocytotoxic compound AlPcS4 to Hela cells by transferrin conjugated PEG-liposomes. Int J Cancer 101:78–85

    Article  CAS  PubMed  Google Scholar 

  48. Golkar N, Tamaddon AM, Samani SM (2016) Effect of lipid composition on incorporation of trastuzumab-PEG-lipid into nanoliposomes by post-insertion method: physicochemical and cellular characterization. J Liposome Res 26:113–125

    CAS  PubMed  Google Scholar 

  49. Greco E, Quintiliani G, Santucci MB, Serafino A, Ciccaglione AR, Marcantonio C, Papi M, Maulucci G, Delogu G, Martino A, Goletti D, Sarmati L, Andreoni M, Altieri A, Alma M, Caccamo N, Di Liberto D, De Spirito M, Savage ND, Nisini R, Dieli F, Ottenhoff TH, Fraziano M (2012) Janus-faced liposomes enhance antimicrobial innate immune response in Mycobacterium tuberculosis infection. Proc Natl Acad Sci U S A 109:E1360–E1368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Griffioen AW, van der Schaft DW, Barendsz-Janson AF, Cox A, Struijker Boudier HA, Hillen HF, Mayo KH (2001) Anginex, a designed peptide that inhibits angiogenesis. Biochem J 354:233–242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Guo B, Cheng Y, Li N, Li X, Jin M, Li T, Li J (2012) In vitro and in vivo studies of galactose-modified liver-targeting liposomes. J Drug Target 21(3):257–264

    Article  PubMed  CAS  Google Scholar 

  52. Hanasaki K, Varki A, Stamenkovic I, Bevilacqua MP (1994) Cytokine-induced beta-galactoside alpha-2,6-sialyltransferase in human endothelial cells mediates alpha 2,6-sialylation of adhesion molecules and CD22 ligands. J Biol Chem 269:10637–10643

    CAS  PubMed  Google Scholar 

  53. Harel-Adar T, Ben Mordechai T, Amsalem Y, Feinberg MS, Leor J, Cohen S (2011) Modulation of cardiac macrophages by phosphatidylserine-presenting liposomes improves infarct repair. Proc Natl Acad Sci U S A 108:1827–1832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Hatakeyama H, Akita H, Ishida E, Hashimoto K, Kobayashi H, Aoki T, Yasuda J, Obata K, Kikuchi H, Ishida T, Kiwada H, Harashima H (2007) Tumor targeting of doxorubicin by anti-MT1-MMP antibody-modified PEG liposomes. Int J Pharm 342:194–200

    Article  CAS  PubMed  Google Scholar 

  55. Hatakeyama H, Akita H, Harashima H (2011) 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 63:152–160

    Article  CAS  PubMed  Google Scholar 

  56. Hatakeyama H, Akita H, Harashima H (2013) The polyethyleneglycol dilemma: advantage and disadvantage of PEGylation of liposomes for systemic genes and nucleic acids delivery to tumors. Biol Pharm Bull 36:892–899

    Article  CAS  PubMed  Google Scholar 

  57. Hattori Y, Kawakami S, Yamashita F, Hashida M (2000) Controlled biodistribution of galactosylated liposomes and incorporated probucol in hepatocyte-selective drug targeting. J Control Release 69:369–377

    Article  CAS  PubMed  Google Scholar 

  58. Heger Z, Polanska H, Merlos Rodrigo MA, Guran R, Kulich P, Kopel P, Masarik M, Eckschlager T, Stiborova M, Kizek R, Adam V (2016) Prostate tumor attenuation in the nu/nu murine model due to anti-sarcosine antibodies in folate-targeted liposomes. Sci Rep 6:33379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Hilgenbrink AR, Low PS (2005) Folate receptor-mediated drug targeting: from therapeutics to diagnostics. J Pharm Sci 94:2135–2146

    Article  CAS  PubMed  Google Scholar 

  60. Hirai M, Minematsu H, Hiramatsu Y, Kitagawa H, Otani T, Iwashita S, Kudoh T, Chen L, Li Y, Okada M, Salomon DS, Igarashi K, Chikuma M, Seno M (2010) Novel and simple loading procedure of cisplatin into liposomes and targeting tumor endothelial cells. Int J Pharm 391:274–283

    Article  CAS  PubMed  Google Scholar 

  61. Huang P, Wu J, Li X, Liu X, Li Y, Cui G (2015) RGD peptide-pegylated PLLA nanoparticles containing epirubicin hydrochloride exhibit receptor-dependent tumor trafficking in vitro and in vivo. Pharm Res 32:2328–2343

    Article  CAS  PubMed  Google Scholar 

  62. Humphries MJ, Olden K, Yamada KM (1986) A synthetic peptide from fibronectin inhibits experimental metastasis of murine melanoma cells. Science 233:467–470

    Article  CAS  PubMed  Google Scholar 

  63. Ichikawa K, Urakami T, Yonezawa S, Miyauchi H, Shimizu K, Asai T, Oku N (2007) Enhanced desensitization efficacy by liposomal conjugation of a specific antigen. Int J Pharm 336:391–395

    Article  CAS  PubMed  Google Scholar 

  64. Ichikawa K, Asai T, Shimizu K, Yonezawa S, Urakami T, Miyauchi H, Kawashima H, Ishida T, Kiwada H, Oku N (2013) Suppression of immune response by antigen-modified liposomes encapsulating model agents: a novel strategy for the treatment of allergy. J Control Release 167:284–289

    Article  CAS  PubMed  Google Scholar 

  65. Iinuma H, Maruyama K, Okinaga K, Sasaki K, Sekine T, Ishida O, Ogiwara N, Johkura K, Yonemura Y (2002) Intracellular targeting therapy of cisplatin-encapsulated transferrin-polyethylene glycol liposome on peritoneal dissemination of gastric cancer. Int J Cancer 99:130–137

    Article  CAS  PubMed  Google Scholar 

  66. Ikemoto K, Shimizu K, Ohashi K, Takeuchi Y, Shimizu M, Oku N (2016) Bauhinia purprea agglutinin-modified liposomes for human prostate cancer treatment. Cancer Sci 107:53–59

    Article  CAS  PubMed  Google Scholar 

  67. Ishida O, Maruyama K, Tanahashi H, Iwatsuru M, Sasaki K, Eriguchi M, Yanagie H (2001) Liposomes bearing polyethyleneglycol-coupled transferrin with intracellular targeting property to the solid tumors in vivo. Pharm Res 18:1042–1048

    Article  CAS  PubMed  Google Scholar 

  68. Ito H, Kamachi T, Yashima E (2012) Specific surface modification of the acetylene-linked glycolipid vesicle by click chemistry. Chem Commun (Camb) 48:5650–5652

    Article  CAS  Google Scholar 

  69. Janssen AP, Schiffelers RM, ten Hagen TL, Koning GA, Schraa AJ, Kok RJ, Storm G, Molema G (2003) Peptide-targeted PEG-liposomes in anti-angiogenic therapy. Int J Pharm 254:55–58

    Article  CAS  PubMed  Google Scholar 

  70. Kamaly N, Kalber T, Thanou M, Bell JD, Miller AD (2009) Folate receptor targeted bimodal liposomes for tumor magnetic resonance imaging. Bioconjug Chem 20:648–655

    Article  CAS  PubMed  Google Scholar 

  71. Kamps JA, Morselt HW, Scherphof GL (1999) Uptake of liposomes containing phosphatidylserine by liver cells in vivo and by sinusoidal liver cells in primary culture: in vivo-in vitro differences. Biochem Biophys Res Commun 256:57–62

    Article  CAS  PubMed  Google Scholar 

  72. Kang MH, Yoo HJ, Kwon YH, Yoon HY, Lee SG, Kim SR, Yeom DW, Kang MJ, Choi YW (2015) Design of multifunctional liposomal nanocarriers for folate receptor-specific intracellular drug delivery. Mol Pharm 12:4200–4213

    Article  CAS  PubMed  Google Scholar 

  73. Kawakami S, Yamashita F, Nishikawa M, Takakura Y, Hashida M (1998) Asialoglycoprotein receptor-mediated gene transfer using novel galactosylated cationic liposomes. Biochem Biophys Res Commun 252:78–83

    Article  CAS  PubMed  Google Scholar 

  74. Kawakami S, Wong J, Sato A, Hattori Y, Yamashita F, Hashida M (2000) Biodistribution characteristics of mannosylated, fucosylated, and galactosylated liposomes in mice. Biochim Biophys Acta 1524:258–265

    Article  CAS  PubMed  Google Scholar 

  75. Kenjo E, Asai T, Yonenaga N, Ando H, Ishii T, Hatanaka K, Shimizu K, Urita Y, Dewa T, Nango M, Tsukada H, Oku N (2013) Systemic delivery of small interfering RNA by use of targeted polycation liposomes for cancer therapy. Biol Pharm Bull 36:287–291

    Article  CAS  PubMed  Google Scholar 

  76. Kerbel RS, Kamen BA (2004) The anti-angiogenic basis of metronomic chemotherapy. Nat Rev Cancer 4:423–436

    Article  CAS  PubMed  Google Scholar 

  77. Kibria G, Hatakeyama H, Ohga N, Hida K, Harashima H (2013) The effect of liposomal size on the targeted delivery of doxorubicin to integrin alphavbeta3-expressing tumor endothelial cells. Biomaterials 34:5617–5627

    Article  CAS  PubMed  Google Scholar 

  78. Kim IY, Kang YS, Lee DS, Park HJ, Choi EK, Oh YK, Son HJ, Kim JS (2009) Antitumor activity of EGFR targeted pH-sensitive immunoliposomes encapsulating gemcitabine in A549 xenograft nude mice. J Control Release 140:55–60

    Article  CAS  PubMed  Google Scholar 

  79. Kluza E, Jacobs I, Hectors SJ, Mayo KH, Griffioen AW, Strijkers GJ, Nicolay K (2012) Dual-targeting of alphavbeta3 and galectin-1 improves the specificity of paramagnetic/fluorescent liposomes to tumor endothelium in vivo. J Control Release 158:207–214

    Article  CAS  PubMed  Google Scholar 

  80. Kobayashi T, Ishida T, Okada Y, Ise S, Harashima H, Kiwada H (2007) Effect of transferrin receptor-targeted liposomal doxorubicin in P-glycoprotein-mediated drug resistant tumor cells. Int J Pharm 329:94–102

    Article  CAS  PubMed  Google Scholar 

  81. Koide H, Asai T, Furuya K, Tsuzuku T, Kato H, Dewa T, Nango M, Maeda N, Oku N (2011) Inhibition of Akt (ser473) phosphorylation and rapamycin-resistant cell growth by knockdown of mammalian target of rapamycin with small interfering RNA in vascular endothelial growth factor receptor-1-targeting vector. Biol Pharm Bull 34:602–608

    Article  CAS  PubMed  Google Scholar 

  82. Kolb HC, Finn MG, Sharpless KB (2001) Click chemistry: diverse chemical function from a few good reactions. Angew Chem Int Ed Eng 40:2004–2021

    Article  CAS  Google Scholar 

  83. Kondo M, Asai T, Katanasaka Y, Sadzuka Y, Tsukada H, Ogino K, Taki T, Baba K, Oku N (2004) Anti-neovascular therapy by liposomal drug targeted to membrane type-1 matrix metalloproteinase. Int J Cancer 108:301–306

    Article  CAS  PubMed  Google Scholar 

  84. Kono Y, Kawakami S, Higuchi Y, Maruyama K, Yamashita F, Hashida M (2014) Tumour-associated macrophages targeted transfection with NF-kappaB decoy/mannose-modified bubble lipoplexes inhibits tumour growth in tumour-bearing mice. J Drug Target 22:439–449

    Article  CAS  PubMed  Google Scholar 

  85. Kono K, Takashima M, Yuba E, Harada A, Hiramatsu Y, Kitagawa H, Otani T, Maruyama K, Aoshima S (2015) Multifunctional liposomes having target specificity, temperature-triggered release, and near-infrared fluorescence imaging for tumor-specific chemotherapy. J Control Release 216:69–77

    Article  CAS  PubMed  Google Scholar 

  86. Koo H, Lee S, Na JH, Kim SH, Hahn SK, Choi K, Kwon IC, Jeong SY, Kim K (2012) Bioorthogonal copper-free click chemistry in vivo for tumor-targeted delivery of nanoparticles. Angew Chem Int Ed Eng 51:11836–11840

    Article  CAS  Google Scholar 

  87. Koshkaryev A, Piroyan A, Torchilin VP (2012) Increased apoptosis in cancer cells in vitro and in vivo by ceramides in transferrin-modified liposomes. Cancer Biol Ther 13:50–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Krug S, Abbassi R, Griesmann H, Sipos B, Wiese D, Rexin P, Blank A, Perren A, Haybaeck J, Huttelmaier S, Rinke A, Gress TM, Michl P (2018) Therapeutic targeting of tumor-associated macrophages in pancreatic neuroendocrine tumors. Int J Cancer 143(7):1806–1816

    Article  CAS  PubMed  Google Scholar 

  89. Kularatne SA, Low PS (2010) Targeting of nanoparticles: folate receptor. Methods Mol Biol 624:249–265

    Article  CAS  PubMed  Google Scholar 

  90. Kurohane K, Namba Y, Oku N (2000) Liposomes modified with a synthetic Arg-Gly-Asp mimetic inhibit lung metastasis of B16BL6 melanoma cells. Life Sci 68:273–281

    Article  CAS  PubMed  Google Scholar 

  91. Kuznetsova NR, Stepanova EV, Peretolchina NM, Khochenkov DA, Boldyrev IA, Bovin NV, Vodovozova EL (2013) Targeting liposomes loaded with melphalan prodrug to tumour vasculature via the Sialyl Lewis X selectin ligand. J Drug Target 22(3):242–250

    Article  PubMed  CAS  Google Scholar 

  92. Kwon S, Ke S, Houston JP, Wang W, Wu Q, Li C, Sevick-Muraca EM (2005) Imaging dose-dependent pharmacokinetics of an RGD-fluorescent dye conjugate targeted to alpha v beta 3 receptor expressed in Kaposi’s sarcoma. Mol Imaging 4:75–87

    Article  PubMed  Google Scholar 

  93. Lallana E, Sousa-Herves A, Fernandez-Trillo F, Riguera R, Fernandez-Megia E (2012) Click chemistry for drug delivery nanosystems. Pharm Res 29:1–34

    Article  CAS  PubMed  Google Scholar 

  94. Latif N, Bachhawat BK (1984) The effect of surface sugars on liposomes in immunopotentiation. Immunol Lett 8:75–78

    Article  CAS  PubMed  Google Scholar 

  95. Lee MH, Kim JY, Han JH, Bhuniya S, Sessler JL, Kang C, Kim JS (2012) Direct fluorescence monitoring of the delivery and cellular uptake of a cancer-targeted RGD peptide-appended naphthalimide theragnostic prodrug. J Am Chem Soc 134:12668–12674

    Article  CAS  PubMed  Google Scholar 

  96. Leung SL, Zha Z, Cohn C, Dai Z, Wu X (2014) Anti-EGFR antibody conjugated organic-inorganic hybrid lipid nanovesicles selectively target tumor cells. Colloids Surf B: Biointerfaces 121:141–149

    Article  CAS  PubMed  Google Scholar 

  97. Li XT, He ML, Zhou ZY, Jiang Y, Cheng L (2015) The antitumor activity of PNA modified vinblastine cationic liposomes on Lewis lung tumor cells: in vitro and in vivo evaluation. Int J Pharm 487:223–233

    Article  CAS  PubMed  Google Scholar 

  98. Limasale YD, Tezcaner A, Ozen C, Keskin D, Banerjee S (2015) Epidermal growth factor receptor-targeted immunoliposomes for delivery of celecoxib to cancer cells. Int J Pharm 479:364–373

    Article  CAS  PubMed  Google Scholar 

  99. Liu XQ, Song WJ, Sun TM, Zhang PZ, Wang J (2011) Targeted delivery of antisense inhibitor of miRNA for antiangiogenesis therapy using cRGD-functionalized nanoparticles. Mol Pharm 8:250–259

    Article  CAS  PubMed  Google Scholar 

  100. Liu S, Song XL, Wang YH, Wang XM, Xiao Y, Wang X, Cheng L, Li XT (2017) The efficacy of WGA modified daunorubicin anti-resistant liposomes in treatment of drug-resistant MCF-7 breast cancer. J Drug Target 25:541–553

    Article  CAS  PubMed  Google Scholar 

  101. Luo LM, Huang Y, Zhao BX, Zhao X, Duan Y, Du R, Yu KF, Song P, Zhao Y, Zhang X, Zhang Q (2013) Anti-tumor and anti-angiogenic effect of metronomic cyclic NGR-modified liposomes containing paclitaxel. Biomaterials 34:1102–1114

    Article  CAS  PubMed  Google Scholar 

  102. Maeda N, Takeuchi Y, Takada M, Namba Y, Oku N (2004a) Synthesis of angiogenesis-targeted peptide and hydrophobized polyethylene glycol conjugate. Bioorg Med Chem Lett 14:1015–1017

    Article  CAS  PubMed  Google Scholar 

  103. Maeda N, Takeuchi Y, Takada M, Sadzuka Y, Namba Y, Oku N (2004b) Anti-neovascular therapy by use of tumor neovasculature-targeted long-circulating liposome. J Control Release 100:41–52

    Article  CAS  PubMed  Google Scholar 

  104. Mamot C, Drummond DC, Greiser U, Hong K, Kirpotin DB, Marks JD, Park JW (2003) Epidermal growth factor receptor (EGFR)-targeted immunoliposomes mediate specific and efficient drug delivery to EGFR- and EGFRvIII-overexpressing tumor cells. Cancer Res 63:3154–3161

    CAS  PubMed  Google Scholar 

  105. Mamot C, Drummond DC, Noble CO, Kallab V, Guo Z, Hong K, Kirpotin DB, Park JW (2005) Epidermal growth factor receptor-targeted immunoliposomes significantly enhance the efficacy of multiple anticancer drugs in vivo. Cancer Res 65:11631–11638

    Article  CAS  PubMed  Google Scholar 

  106. Managit C, Kawakami S, Yamashita F, Hashida M (2005) Effect of galactose density on asialoglycoprotein receptor-mediated uptake of galactosylated liposomes. J Pharm Sci 94:2266–2275

    Article  CAS  PubMed  Google Scholar 

  107. Maruyama K, Takahashi N, Tagawa T, Nagaike K, Iwatsuru M (1997) Immunoliposomes bearing polyethyleneglycol-coupled Fab’ fragment show prolonged circulation time and high extravasation into targeted solid tumors in vivo. FEBS Lett 413:177–180

    Article  CAS  PubMed  Google Scholar 

  108. Maruyama K, Ishida O, Kasaoka S, Takizawa T, Utoguchi N, Shinohara A, Chiba M, Kobayashi H, Eriguchi M, Yanagie H (2004) Intracellular targeting of sodium mercaptoundecahydrododecaborate (BSH) to solid tumors by transferrin-PEG liposomes, for boron neutron-capture therapy (BNCT). J Control Release 98:195–207

    Article  CAS  PubMed  Google Scholar 

  109. Matsumura Y, Maeda H (1986) A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res 46:6387–6392

    CAS  PubMed  Google Scholar 

  110. Mendonca LS, Firmino F, Moreira JN, Pedroso de Lima MC, Simoes S (2010) Transferrin receptor-targeted liposomes encapsulating anti-BCR-ABL siRNA or asODN for chronic myeloid leukemia treatment. Bioconjug Chem 21:157–168

    Article  CAS  PubMed  Google Scholar 

  111. Minami A, Otsubo T, Ieno D, Ikeda K, Kanazawa H, Shimizu K, Ohata K, Yokochi T, Horii Y, Fukumoto H, Taguchi R, Takahashi T, Oku N, Suzuki T (2014) Visualization of sialidase activity in mammalian tissues and cancer detection with a novel fluorescent sialidase substrate. PLoS One 9:e81941

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Miselis NR, Wu ZJ, Van Rooijen N, Kane AB (2008) Targeting tumor-associated macrophages in an orthotopic murine model of diffuse malignant mesothelioma. Mol Cancer Ther 7:788–799

    Article  CAS  PubMed  Google Scholar 

  113. Miyamoto S, Yagi H, Yotsumoto F, Kawarabayashi T, Mekada E (2006) Heparin-binding epidermal growth factor-like growth factor as a novel targeting molecule for cancer therapy. Cancer Sci 97:341–347

    Article  CAS  PubMed  Google Scholar 

  114. Miyata S, Kawabata S, Hiramatsu R, Doi A, Ikeda N, Yamashita T, Kuroiwa T, Kasaoka S, Maruyama K, Miyatake S (2011) Computed tomography imaging of transferrin targeting liposomes encapsulating both boron and iodine contrast agents by convection-enhanced delivery to F98 rat glioma for boron neutron capture therapy. Neurosurgery 68:1380–1387. discussion 1387

    Article  PubMed  Google Scholar 

  115. Murase Y, Asai T, Katanasaka Y, Sugiyama T, Shimizu K, Maeda N, Oku N (2010) A novel DDS strategy, “dual-targeting”, and its application for antineovascular therapy. Cancer Lett 287:165–171

    Article  CAS  PubMed  Google Scholar 

  116. Nag A, Ghosh PC (1999) Assessment of targeting potential of galactosylated and mannosylated sterically stabilized liposomes to different cell types of mouse liver. J Drug Target 6:427–438

    Article  CAS  PubMed  Google Scholar 

  117. Nakamura H (2009) Liposomal boron delivery for neutron capture therapy. Methods Enzymol 465:179–208

    Article  CAS  PubMed  Google Scholar 

  118. Namba Y, Sakakibara T, Masada M, Ito F, Oku N (1990) Glucuronate-modified liposomes with prolonged circulation time. Chem Pharm Bull (Tokyo) 38:1663–1666

    Article  CAS  Google Scholar 

  119. Negussie AH, Miller JL, Reddy G, Drake SK, Wood BJ, Dreher MR (2010) Synthesis and in vitro evaluation of cyclic NGR peptide targeted thermally sensitive liposome. J Control Release 143:265–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Ng KK, Weis WI (1997) Structure of a selectin-like mutant of mannose-binding protein complexed with sialylated and sulfated Lewis(x) oligosaccharides. Biochemistry 36:979–988

    Article  CAS  PubMed  Google Scholar 

  121. Ni S, Stephenson SM, Lee RJ (2002) Folate receptor targeted delivery of liposomal daunorubicin into tumor cells. Anticancer Res 22:2131–2135

    CAS  PubMed  Google Scholar 

  122. Ogawa M, Umeda IO, Kosugi M, Kawai A, Hamaya Y, Takashima M, Yin H, Kudoh T, Seno M, Magata Y (2014) Development of 111In-labeled liposomes for vulnerable atherosclerotic plaque imaging. J Nucl Med 55:115–120

    Article  CAS  PubMed  Google Scholar 

  123. Okamoto A, Asai T, Kato H, Ando H, Minamino T, Mekada E, Oku N (2014) Antibody-modified lipid nanoparticles for selective delivery of siRNA to tumors expressing membrane-anchored form of HB-EGF. Biochem Biophys Res Commun 449:460–465

    Article  CAS  PubMed  Google Scholar 

  124. Okamoto A, Asai T, Hirai Y, Shimizu K, Koide H, Minamino T, Oku N (2018) Systemic administration of siRNA with Anti-HB-EGF antibody-modified lipid nanoparticles for the treatment of triple-negative breast cancer. Mol Pharm 15:1495–1504

    Article  CAS  PubMed  Google Scholar 

  125. Okazaki F, Matsunaga N, Okazaki H, Utoguchi N, Suzuki R, Maruyama K, Koyanagi S, Ohdo S (2010) Circadian rhythm of transferrin receptor 1 gene expression controlled by c-Myc in colon cancer-bearing mice. Cancer Res 70:6238–6246

    Article  CAS  PubMed  Google Scholar 

  126. Oku N (1999) Anticancer therapy using glucuronate modified long-circulating liposomes. Adv Drug Deliv Rev 40:63–73

    Article  CAS  PubMed  Google Scholar 

  127. Oku N, Asai T, Watanabe K, Kuromi K, Nagatsuka M, Kurohane K, Kikkawa H, Ogino K, Tanaka M, Ishikawa D, Tsukada H, Momose M, Nakayama J, Taki T (2002) Anti-neovascular therapy using novel peptides homing to angiogenic vessels. Oncogene 21:2662–2669

    Article  CAS  PubMed  Google Scholar 

  128. Omata D, Negishi Y, Hagiwara S, Yamamura S, Endo-Takahashi Y, Suzuki R, Maruyama K, Aramaki Y (2012) Enhanced gene delivery using bubble liposomes and ultrasound for folate-PEG liposomes. J Drug Target 20:355–363

    Article  CAS  PubMed  Google Scholar 

  129. Ongusaha PP, Kwak JC, Zwible AJ, Macip S, Higashiyama S, Taniguchi N, Fang L, Lee SW (2004) HB-EGF is a potent inducer of tumor growth and angiogenesis. Cancer Res 64:5283–5290

    Article  CAS  PubMed  Google Scholar 

  130. Pacis R, Pilat M, Yamazaki K, Pienta K (1995) Differential carbohydrate expression in tumorigenic vs nontumorigenic prostate cell-lines. Int J Oncol 7:1349–1354

    CAS  PubMed  Google Scholar 

  131. Pan XQ, Wang H, Lee RJ (2003) Antitumor activity of folate receptor-targeted liposomal doxorubicin in a KB oral carcinoma murine xenograft model. Pharm Res 20:417–422

    Article  CAS  PubMed  Google Scholar 

  132. Pasqualini R, Koivunen E, Kain R, Lahdenranta J, Sakamoto M, Stryhn A, Ashmun RA, Shapiro LH, Arap W, Ruoslahti E (2000) Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis. Cancer Res 60:722–727

    CAS  PubMed  PubMed Central  Google Scholar 

  133. Pastorino F, Brignole C, Marimpietri D, Cilli M, Gambini C, Ribatti D, Longhi R, Allen TM, Corti A, Ponzoni M (2003) Vascular damage and anti-angiogenic effects of tumor vessel-targeted liposomal chemotherapy. Cancer Res 63:7400–7409

    CAS  PubMed  Google Scholar 

  134. Pastorino F, Brignole C, Di Paolo D, Nico B, Pezzolo A, Marimpietri D, Pagnan G, Piccardi F, Cilli M, Longhi R, Ribatti D, Corti A, Allen TM, Ponzoni M (2006) Targeting liposomal chemotherapy via both tumor cell-specific and tumor vasculature-specific ligands potentiates therapeutic efficacy. Cancer Res 66:10073–10082

    Article  CAS  PubMed  Google Scholar 

  135. Paszko E, Vaz GM, Ehrhardt C, Senge MO (2013) Transferrin conjugation does not increase the efficiency of liposomal Foscan during in vitro photodynamic therapy of oesophageal cancer. Eur J Pharm Sci 48:202–210

    Article  CAS  PubMed  Google Scholar 

  136. Patil Y, Amitay Y, Ohana P, Shmeeda H, Gabizon A (2016) Targeting of pegylated liposomal mitomycin-C prodrug to the folate receptor of cancer cells: intracellular activation and enhanced cytotoxicity. J Control Release 225:87–95

    Article  CAS  PubMed  Google Scholar 

  137. Petrilli R, Eloy JO, Lee RJ, Lopez RFV (2018) Preparation of immunoliposomes by direct coupling of antibodies based on a thioether bond. Methods Mol Biol 1674:229–237

    Article  CAS  PubMed  Google Scholar 

  138. Qin L, Wang CZ, Fan HJ, Zhang CJ, Zhang HW, Lv MH, Cui SD (2014) A dual-targeting liposome conjugated with transferrin and arginine-glycine-aspartic acid peptide for glioma-targeting therapy. Oncol Lett 8:2000–2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Riviere K, Huang Z, Jerger K, Macaraeg N, Szoka FC Jr (2011) Antitumor effect of folate-targeted liposomal doxorubicin in KB tumor-bearing mice after intravenous administration. J Drug Target 19:14–24

    Article  CAS  PubMed  Google Scholar 

  140. Ruoslahti E (1996) RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 12:697–715

    Article  CAS  PubMed  Google Scholar 

  141. Said Hassane F, Frisch B, Schuber F (2006) Targeted liposomes: convenient coupling of ligands to preformed vesicles using “click chemistry”. Bioconjug Chem 17:849–854

    Article  PubMed  CAS  Google Scholar 

  142. Saiki I, Koike C, Obata A, Fujii H, Murata J, Kiso M, Hasegawa A, Komazawa H, Tsukada H, Azuma I, Okada S, Oku N (1996) Functional role of sialyl Lewis X and fibronectin-derived RGDS peptide analogue on tumor-cell arrest in lungs followed by extravasation. Int J Cancer 65:833–839

    Article  CAS  PubMed  Google Scholar 

  143. Sakurai Y, Hatakeyama H, Sato Y, Hyodo M, Akita H, Ohga N, Hida K, Harashima H (2014) RNAi-mediated gene knockdown and anti-angiogenic therapy of RCCs using a cyclic RGD-modified liposomal-siRNA system. J Control Release 173:110–118

    Article  CAS  PubMed  Google Scholar 

  144. Saul JM, Annapragada AV, Bellamkonda RV (2006) A dual-ligand approach for enhancing targeting selectivity of therapeutic nanocarriers. J Control Release 114:277–287

    Article  CAS  PubMed  Google Scholar 

  145. Schiffelers RM, Koning GA, ten Hagen TL, Fens MH, Schraa AJ, Janssen AP, Kok RJ, Molema G, Storm G (2003) Anti-tumor efficacy of tumor vasculature-targeted liposomal doxorubicin. J Control Release 91:115–122

    Article  CAS  PubMed  Google Scholar 

  146. Scomparin A, Salmaso S, Eldar-Boock A, Ben-Shushan D, Ferber S, Tiram G, Shmeeda H, Landa-Rouben N, Leor J, Caliceti P, Gabizon A, Satchi-Fainaro R (2015) A comparative study of folate receptor-targeted doxorubicin delivery systems: dosing regimens and therapeutic index. J Control Release 208:106–120

    Article  CAS  PubMed  Google Scholar 

  147. Shahinian S, Silvius JR (2004) High-yield coupling of antibody Fab’ fragments to liposomes containing maleimide-functionalized lipids. Methods Enzymol 387:3–15

    Article  CAS  PubMed  Google Scholar 

  148. Shan L, Wang S, Sridhar R, Bhujwalla ZM, Wang PC (2007) Dual probe with fluorescent and magnetic properties for imaging solid tumor xenografts. Mol Imaging 6:85–95

    Article  CAS  PubMed  Google Scholar 

  149. Shimizu K, Oku N (2004) Cancer anti-angiogenic therapy. Biol Pharm Bull 27:599–605

    Article  CAS  PubMed  Google Scholar 

  150. Shimizu K, Asai T, Oku N (2005) Antineovascular therapy, a novel antiangiogenic approach. Expert Opin Ther Targets 9:63–76

    Article  CAS  PubMed  Google Scholar 

  151. Shimizu K, Miyauchi H, Urakami T, Yamamura-Ichikawa K, Yonezawa S, Asai T, Oku N (2016) Specific delivery of an immunosuppressive drug to splenic B cells by antigen-modified liposomes and its antiallergic effect. J Drug Target 24:890–895

    Article  CAS  PubMed  Google Scholar 

  152. Shmeeda H, Amitay Y, Gorin J, Tzemach D, Mak L, Ogorka J, Kumar S, Zhang JA, Gabizon A (2010) Delivery of zoledronic acid encapsulated in folate-targeted liposome results in potent in vitro cytotoxic activity on tumor cells. J Control Release 146:76–83

    Article  CAS  PubMed  Google Scholar 

  153. Shmeeda H, Amitay Y, Tzemach D, Gorin J, Gabizon A (2013) Liposome encapsulation of zoledronic acid results in major changes in tissue distribution and increase in toxicity. J Control Release 167:265–275

    Article  CAS  PubMed  Google Scholar 

  154. Silverman JA, Deitcher SR (2013) Marqibo(R) (vincristine sulfate liposome injection) improves the pharmacokinetics and pharmacodynamics of vincristine. Cancer Chemother Pharmacol 71:555–564

    Article  CAS  PubMed  Google Scholar 

  155. Singh M (1999) Transferrin as a targeting ligand for liposomes and anticancer drugs. Curr Pharm Des 5:443–451

    CAS  PubMed  Google Scholar 

  156. Smyth T, Petrova K, Payton NM, Persaud I, Redzic JS, Graner MW, Smith-Jones P, Anchordoquy TJ (2014) Surface functionalization of exosomes using click chemistry. Bioconjug Chem 25:1777–1784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Sonali SRP, Singh N, Sharma G, Vijayakumar MR, Koch B, Singh S, Singh U, Dash D, Pandey BL, Muthu MS (2016) Transferrin liposomes of docetaxel for brain-targeted cancer applications: formulation and brain theranostics. Drug Deliv 23:1261–1271

    Article  CAS  PubMed  Google Scholar 

  158. Spanedda MV, De Giorgi M, Hassane FS, Schuber F, Bourel-Bonnet L, Frisch B (2017) Coupling of ligands to the liposome surface by click chemistry. Methods Mol Biol 1522:93–106

    Article  CAS  PubMed  Google Scholar 

  159. Springer TA, Lasky LA (1991) Cell adhesion. Sticky sugars for selectins. Nature 349:196–197

    Article  CAS  PubMed  Google Scholar 

  160. Stahn R, Schafer H, Kernchen F, Schreiber J (1998) Multivalent sialyl Lewis x ligands of definite structures as inhibitors of E-selectin mediated cell adhesion. Glycobiology 8:311–319

    Article  CAS  PubMed  Google Scholar 

  161. Storm G, Roerdink FH, Steerenberg PA, de Jong WH, Crommelin DJ (1987) Influence of lipid composition on the antitumor activity exerted by doxorubicin-containing liposomes in a rat solid tumor model. Cancer Res 47:3366–3372

    CAS  PubMed  Google Scholar 

  162. Sugiyama M, Matsuura M, Takeuchi Y, Kosaka J, Nango M, Oku N (2004) Possible mechanism of polycation liposome (PCL)-mediated gene transfer. Biochim Biophys Acta 1660:24–30

    Article  CAS  PubMed  Google Scholar 

  163. Sugiyama T, Asai T, Nedachi YM, Katanasaka Y, Shimizu K, Maeda N, Oku N (2013) Enhanced active targeting via cooperative binding of ligands on liposomes to target receptors. PLoS One 8:e67550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Sundaram S, Trivedi R, Durairaj C, Ramesh R, Ambati BK, Kompella UB (2009) Targeted drug and gene delivery systems for lung cancer therapy. Clin Cancer Res 15:7299–7308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Suzuki R, Takizawa T, Kuwata Y, Mutoh M, Ishiguro N, Utoguchi N, Shinohara A, Eriguchi M, Yanagie H, Maruyama K (2008) Effective anti-tumor activity of oxaliplatin encapsulated in transferrin-PEG-liposome. Int J Pharm 346:143–150

    Article  CAS  PubMed  Google Scholar 

  166. Tang Y, Soroush F, Tong Z, Kiani MF, Wang B (2017) Targeted multidrug delivery system to overcome chemoresistance in breast cancer. Int J Nanomedicine 12:671–681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Tardi P, Choice E, Masin D, Redelmeier T, Bally M, Madden TD (2000) Liposomal encapsulation of topotecan enhances anticancer efficacy in murine and human xenograft models. Cancer Res 60:3389–3393

    CAS  PubMed  Google Scholar 

  168. Toita R, Kawano T, Murata M, Kang JH (2016) Anti-obesity and anti-inflammatory effects of macrophage-targeted interleukin-10-conjugated liposomes in obese mice. Biomaterials 110:81–88

    Article  CAS  PubMed  Google Scholar 

  169. Torchilin V (2008) Antibody-modified liposomes for cancer chemotherapy. Expert Opin Drug Deliv 5:1003–1025

    Article  CAS  PubMed  Google Scholar 

  170. Tros de Ilarduya C, Arangoa MA, Moreno-Aliaga MJ, Duzgunes N (2002) Enhanced gene delivery in vitro and in vivo by improved transferrin-lipoplexes. Biochim Biophys Acta 1561:209–221

    Article  CAS  PubMed  Google Scholar 

  171. Vader P, Crielaard BJ, van Dommelen SM, van der Meel R, Storm G, Schiffelers RM (2012) Targeted delivery of small interfering RNA to angiogenic endothelial cells with liposome-polycation-DNA particles. J Control Release 160:211–216

    Article  CAS  PubMed  Google Scholar 

  172. Wang HW, Jiang PL, Lin SF, Lin HJ, Ou KL, Deng WP, Lee LW, Huang YY, Liang PH, Liu DZ (2013) Application of galactose-modified liposomes as a potent antigen presenting cell targeted carrier for intranasal immunization. Acta Biomater 9:5681–5688

    Article  CAS  PubMed  Google Scholar 

  173. Wang F, Chen L, Zhang R, Chen Z, Zhu L (2014) RGD peptide conjugated liposomal drug delivery system for enhance therapeutic efficacy in treating bone metastasis from prostate cancer. J Control Release 196:222–233

    Article  CAS  PubMed  Google Scholar 

  174. Xiong S, Yu B, Wu J, Li H, Lee RJ (2011) Preparation, therapeutic efficacy and intratumoral localization of targeted daunorubicin liposomes conjugating folate-PEG-CHEMS. Biomed Pharmacother 65:2–8

    Article  CAS  PubMed  Google Scholar 

  175. Xu L, Pirollo KF, Chang EH (2001) Tumor-targeted p53-gene therapy enhances the efficacy of conventional chemo/radiotherapy. J Control Release 74:115–128

    Article  CAS  PubMed  Google Scholar 

  176. Yamada A, Taniguchi Y, Kawano K, Honda T, Hattori Y, Maitani Y (2008) Design of folate-linked liposomal doxorubicin to its antitumor effect in mice. Clin Cancer Res 14:8161–8168

    Article  CAS  PubMed  Google Scholar 

  177. Yang T, Choi MK, Cui FD, Kim JS, Chung SJ, Shim CK, Kim DD (2007) Preparation and evaluation of paclitaxel-loaded PEGylated immunoliposome. J Control Release 120:169–177

    Article  CAS  PubMed  Google Scholar 

  178. Ye P, Zhang W, Yang T, Lu Y, Lu M, Gai Y, Ma X, Xiang G (2014) Folate receptor-targeted liposomes enhanced the antitumor potency of imatinib through the combination of active targeting and molecular targeting. Int J Nanomedicine 9:2167–2178

    Article  PubMed  PubMed Central  Google Scholar 

  179. Yonenaga N, Kenjo E, Asai T, Tsuruta A, Shimizu K, Dewa T, Nango M, Oku N (2012) RGD-based active targeting of novel polycation liposomes bearing siRNA for cancer treatment. J Control Release 160:177–181

    Article  CAS  PubMed  Google Scholar 

  180. Yu LG (2007) The oncofetal Thomsen-Friedenreich carbohydrate antigen in cancer progression. Glycoconj J 24:411–420

    Article  CAS  PubMed  Google Scholar 

  181. Zalba S, Contreras AM, Haeri A, Ten Hagen TL, Navarro I, Koning G, Garrido MJ (2015) Cetuximab-oxaliplatin-liposomes for epidermal growth factor receptor targeted chemotherapy of colorectal cancer. J Control Release 210:26–38

    Article  CAS  PubMed  Google Scholar 

  182. Zeisig R, Stahn R, Wenzel K, Behrens D, Fichtner I (2004) Effect of sialyl Lewis X-glycoliposomes on the inhibition of E-selectin-mediated tumour cell adhesion in vitro. Biochim Biophys Acta 1660:31–40

    Article  CAS  PubMed  Google Scholar 

  183. Zembruski NC, Nguyen CD, Theile D, Ali RM, Herzog M, Hofhaus G, Heintz U, Burhenne J, Haefeli WE, Weiss J (2013) Liposomal sphingomyelin influences the cellular lipid profile of human lymphoblastic leukemia cells without effect on P-glycoprotein activity. Mol Pharm 10:1020–1034

    Article  CAS  PubMed  Google Scholar 

  184. Zhai G, Wu J, Yu B, Guo C, Yang X, Lee RJ (2010) A transferrin receptor-targeted liposomal formulation for docetaxel. J Nanosci Nanotechnol 10:5129–5136

    Article  CAS  PubMed  Google Scholar 

  185. Zhao C, Feng Q, Dou Z, Yuan W, Sui C, Zhang X, Xia G, Sun H, Ma J (2013) Local targeted therapy of liver metastasis from colon cancer by galactosylated liposome encapsulated with doxorubicin. PLoS One 8:e73860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Zhu Y, Cheng L, Cheng L, Huang F, Hu Q, Li L, Tian C, Wei L, Chen D (2014) Folate and TAT peptide co-modified liposomes exhibit receptor-dependent highly efficient intracellular transport of payload in vitro and in vivo. Pharm Res 31:3289–3303

    Article  CAS  PubMed  Google Scholar 

  187. Zhuo H, Peng Y, Yao Q, Zhou N, Zhou S, He J, Fang Y, Li X, Jin H, Lu X, Zhao Y (2013) Tumor imaging and interferon-gamma-inducible protein-10 gene transfer using a highly efficient transferrin-conjugated liposome system in mice. Clin Cancer Res 19:4206–4217

    Article  CAS  PubMed  Google Scholar 

  188. Zou M, Zhang L, Xie Y, Xu W (2012) NGR-based strategies for targeting delivery of chemotherapeutics to tumor vasculature. Anti Cancer Agents Med Chem 12:239–246

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Molecular Imaging, Institute for Medical Photonics Research, Preeminent Medical Photonics Education & Research Center, Hamamatsu University School of Medicine, Hamamatsu, Shizuoka, Japan

    Kosuke Shimizu

  2. Department of Medical Biochemistry, School of Pharmaceutical Sciences, University of Shizuoka, Shizuoka, Shizuoka, Japan

    Kosuke Shimizu & Naoto Oku

  3. Laboratory of Bioanalytical Chemistry, Faculty of Pharma-Science, Teikyo University, Tokyo, Japan

    Naoto Oku

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  1. Kosuke Shimizu
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  2. Naoto Oku
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Correspondence to Kosuke Shimizu .

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  1. Division of Developmental Therapeutics, Exploratory Oncology Research & Clinical Trial Center, National Cancer Center, Kashiwa, Japan

    Yasuhiro Matsumura

  2. Moores UCSD Cancer Center and Department of Pathology, University of California San Diego, La Jolla, CA, USA

    David Tarin

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Shimizu, K., Oku, N. (2019). Liposomes Conjugated with a Pilot Molecule. In: Matsumura, Y., Tarin, D. (eds) Cancer Drug Delivery Systems Based on the Tumor Microenvironment. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56880-3_9

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