Liposomal drug delivery systems for targeted cancer therapy: is active targeting the best choice?

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1 Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J. Clin. 66(1), 7–30 (2016).
  MedlineGoogle Scholar
• 2 Harding MC, Sloan CD, Merrill RM, Harding TM, Thacker BJ, Thacker EL. Abstract MP67: transition from cardiovascular disease to cancer as the leading cause of death in US states, 1999–2013. Circulation 133(Suppl. 1), AMP67–AMP67 (2016).
  Google Scholar
• 3 Pérez-Herrero E, Fernández-Medarde A. Advanced targeted therapies in cancer: drug nanocarriers, the future of chemotherapy. Eur. J. Pharm. Biopharm. 93, 52–79 (2015).
  Medline CASGoogle Scholar
• 4 Bertrand N, Leroux J-C. The journey of a drug-carrier in the body: an anatomo-physiological perspective. J. Control. Release 161(2), 152–163 (2012).
  Medline CASGoogle Scholar
• 5 Jain RK, Stylianopoulos T. Delivering nanomedicine to solid tumors. Nat. Rev. Clin. Oncol. 7(11), 653–664 (2010).
  Medline CASGoogle Scholar
• 6 Hrkach J, Von Hoff D, Ali MM et al. Preclinical development and clinical translation of a PSMA-targeted docetaxel nanoparticle with a differentiated pharmacological profile. Sci. Transl. Med. 4(128), 128ra139–128ra139 (2012).
  Google Scholar
• 7 Allen TM, Cullis PR. Liposomal drug delivery systems: from concept to clinical applications. Adv. Drug Deliv. Rev. 65(1), 36–48 (2013).
  Medline CASGoogle Scholar
• 8 Patil YP, Jadhav S. Novel methods for liposome preparation. Chem. Phys. Lipids 177, 8–18 (2014).
  Medline CASGoogle Scholar
• 9 Chang H-I, Yeh M-K. Clinical development of liposome-based drugs: formulation, characterization, and therapeutic efficacy. Int. J. Nanomed. 7, 49 (2012).
  Medline CASGoogle Scholar
• 10 Pattni BS, Chupin VV, Torchilin VP. New developments in liposomal drug delivery. Chem. Rev. 115(19), 10938–10966 (2015).
  Medline CASGoogle Scholar
• 11 Alexis F, Pridgen E, Molnar LK, Farokhzad OC. Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol. Pharm. 5(4), 505–515 (2008).
  Medline CASGoogle Scholar
• 12 Lian T, Ho RJ. Trends and developments in liposome drug delivery systems. J. Pharm. Sci. 90(6), 667–680 (2001).
  Medline CASGoogle Scholar
• 13 Hamann PR, Hinman LM, Hollander I et al. Gemtuzumab ozogamicin, a potent and selective anti-CD33 antibody-calicheamicin conjugate for treatment of acute myeloid leukemia. Bioconjug. Chem. 13(1), 47–58 (2002).
  Medline CASGoogle Scholar
• 14 Marcucci F, Lefoulon F. Active targeting with particulate drug carriers in tumor therapy: fundamentals and recent progress. Drug Discov. Today 9(5), 219–228 (2004).
  Medline CASGoogle Scholar
• 15 Çağdaş M, Sezer AD, Bucak S. Liposomes as potential drug carrier systems for drug delivery. Application of Nanotechnology in Drug Delivery. In: Sezer AD (Ed.). Intech, Rijeka, Croatia (2014).
  Google Scholar
• 16 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. 46(12 Part 1), 6387–6392 (1986).
  Medline CASGoogle Scholar
• 17 Fang J, Nakamura H, Maeda H. 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(3), 136–151 (2011).
  Medline CASGoogle Scholar
• 18 Gabizon A, Goren D, Horowitz AT, Tzemach D, Lossos A, Siegal T. Long-circulating liposomes for drug delivery in cancer therapy: a review of biodistribution studies in tumor-bearing animals. Adv. Drug Deliv. Rev. 24(2), 337–344 (1997).
  CASGoogle Scholar
• 19 Torchilin V. Tumor delivery of macromolecular drugs based on the EPR effect. Adv. Drug Deliv. Rev. 63(3), 131–135 (2011).
  Medline CASGoogle Scholar
• 20 Nagamitsu A, Greish K, Maeda H. 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(11), 756–766 (2009).
  MedlineGoogle Scholar
• 21 Chattopadhyay N, Fonge H, Cai Z et al. Role of antibody-mediated tumor targeting and route of administration in nanoparticle tumor accumulation in vivo. Mol. Pharm. 9(8), 2168–2179 (2012).
  Medline CASGoogle Scholar
• 22 Noble GT, Stefanick JF, Ashley JD, Kiziltepe T, Bilgicer B. Ligand-targeted liposome design: challenges and fundamental considerations. Trends Biotechnol. 32(1), 32–45 (2014).
  Medline CASGoogle Scholar
• 23 Maruyama K. Intracellular targeting delivery of liposomal drugs to solid tumors based on EPR effects. Adv. Drug Deliv. Rev. 63(3), 161–169 (2011).
  Medline CASGoogle Scholar
• 24 Owens DE, Peppas NA. Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int. J. Pharm. 307(1), 93–102 (2006).
  Medline CASGoogle Scholar
• 25 Fan Y, Zhang Q. Development of liposomal formulations: from concept to clinical investigations. Asian J. Pharm. Sci. 8(2), 81–87 (2013).
  CASGoogle Scholar
• 26 Dawidczyk CM, Kim C, Park JH et al. State-of-the-art in design rules for drug delivery platforms: lessons learned from FDA-approved nanomedicines. J. Control. Release 187, 133–144 (2014).
  Medline CASGoogle Scholar
• 27 Drummond DC, Meyer O, Hong K, Kirpotin DB, Papahadjopoulos D. Optimizing liposomes for delivery of chemotherapeutic agents to solid tumors. Pharmacol. Rev. 51(4), 691–744 (1999).
  Medline CASGoogle Scholar
• 28 Litzinger DC, Buiting AM, Van Rooijen N, Huang L. Effect of liposome size on the circulation time and intraorgan distribution of amphipathic poly (ethylene glycol)-containing liposomes. Biochim. Biophys. Acta 1190(1), 99–107 (1994).
  Medline CASGoogle Scholar
• 29 Akbarzadeh A, Rezaei-Sadabady R, Davaran S et al. Liposome: classification, preparation, and applications. Nanoscale Res. Lett. 8(1), 102 (2013).
  MedlineGoogle Scholar
• 30 Cuomo F, Mosca M, Murgia S, Ceglie A, Lopez F. Oligonucleotides and polynucleotides condensation onto liposome surface: effects of the base and of the nucleotide length. Colloids Surf. B Biointerfaces 104, 239–244 (2013).
  Medline CASGoogle Scholar
• 31 Miller CR, Bondurant B, Mclean SD, Mcgovern KA, O'brien DF. Liposome-cell interactions in vitro: effect of liposome surface charge on the binding and endocytosis of conventional and sterically stabilized liposomes. Biochemistry 37(37), 12875–12883 (1998).
  Medline CASGoogle Scholar
• 32 Levchenko TS, Rammohan R, Lukyanov AN, Whiteman KR, Torchilin VP. Liposome clearance in mice: the effect of a separate and combined presence of surface charge and polymer coating. Int. J. Pharm. 240(1), 95–102 (2002).
  Medline CASGoogle Scholar
• 33 Lasic D, Martin F, Gabizon A, Huang S, Papahadjopoulos D. Sterically stabilized liposomes: a hypothesis on the molecular origin of the extended circulation times. Biochim. Biophys. Acta 1070(1), 187–192 (1991).
  Medline CASGoogle Scholar
• 34 Tirosh O, Barenholz Y, Katzhendler J, Priev A. Hydration of polyethylene glycol-grafted liposomes. Biophys. J. 74(3), 1371–1379 (1998).
  Medline CASGoogle Scholar
• 35 Tan C, Zhang Y, Abbas S et al. Biopolymer-lipid bilayer interaction modulates the physical properties of liposomes: mechanism and structure. J. Agric. Food Chem. 63(32), 7277–7285 (2015).
  Medline CASGoogle Scholar
• 36 Sinico C, Manconi M, Peppi M, Lai F, Valenti D, Fadda AM. Liposomes as carriers for dermal delivery of tretinoin: in vitro evaluation of drug permeation and vesicle-skin interaction. J. Control. Release 103(1), 123–136 (2005).
  Medline CASGoogle Scholar
• 37 Coderch L, Fonollosa J, De Pera M, Estelrich J, De La Maza A, Parra J. Influence of cholesterol on liposome fluidity by EPR: relationship with percutaneous absorption. J. Control. Release 68(1), 85–95 (2000). • This is an interesting paper which quantified the relationship between liposome bilayer fluidity and tissue absorption.
  Medline CASGoogle Scholar
• 38 Alam MI, Paget T, Elkordy AA. Formulation and advantages of furazolidone in liposomal drug delivery systems. Eur. J. Pharm. Sci. 84, 139–145 (2016).
  Medline CASGoogle Scholar
• 39 Gabizon A, Price DC, Huberty J, Bresalier RS, Papahadjopoulos D. Effect of liposome composition and other factors on the targeting of liposomes to experimental tumors: biodistribution and imaging studies. Cancer Res. 50(19), 6371–6378 (1990).
  Medline CASGoogle Scholar
• 40 Lee C-M, Choi Y, Huh EJ et al. Polyethylene glycol (PEG) modified 99mTc-HMPAO-liposome for improving blood circulation and biodistribution: the effect of the extent of PEGylation. Cancer Biother. Radiopharm. 20(6), 620–628 (2005).
  Medline CASGoogle Scholar
• 41 Oussoren C, Zuidema J, Crommelin D, Storm G. Lymphatic uptake and biodistribution of liposomes after subcutaneous injection.: II. Influence of liposomal size, lipid composition and lipid dose. Biochim. Biophys. Acta 1328(2), 261–272 (1997).
  Medline CASGoogle Scholar
• 42 Allen T, Hansen C, Guo L. Subcutaneous administration of liposomes: a comparison with the intravenous and intraperitoneal routes of injection. Biochim. Biophys. Acta 1150(1), 9–16 (1993).
  Medline CASGoogle Scholar
• 43 Lu F, Wu SH, Hung Y, Mou CY. Size effect on cell uptake in well-suspended, uniform mesoporous silica nanoparticles. Small 5(12), 1408–1413 (2009).
  Medline CASGoogle Scholar
• 44 Lee KD, Nir S, Papahadjopoulos D. Quantitative analysis of liposome-cell interactions in vitro: rate constants of binding and endocytosis with suspension and adherent J774 cells and human monocytes. Biochemistry 32(3), 889–899 (1993).
  Medline CASGoogle Scholar
• 45 He C, Hu Y, Yin L, Tang C, Yin C. Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials 31(13), 3657–3666 (2010).
  Medline CASGoogle Scholar
• 46 Andresen TL, Jensen SS, Jørgensen K. Advanced strategies in liposomal cancer therapy: problems and prospects of active and tumor specific drug release. Prog. Lipid Res. 44(1), 68–97 (2005).
  Medline CASGoogle Scholar
• 47 Ishida T, Kirchmeier M, Moase E, Zalipsky S, Allen T. Targeted delivery and triggered release of liposomal doxorubicin enhances cytotoxicity against human B lymphoma cells. Biochim. Biophys. Acta 1515(2), 144–158 (2001). • Suggests that a combination of targeted delivery and triggered release can improve the therapeutic efficacy liposome encapsulated drugs.
  Medline CASGoogle Scholar
• 48 Connor J, Yatvin MB, Huang L. pH-sensitive liposomes: acid-induced liposome fusion. Proc. Natl Acad. Sci. USA 81(6), 1715–1718 (1984).
  Medline CASGoogle Scholar
• 49 Drummond DC, Zignani M, Leroux J-C. Current status of pH-sensitive liposomes in drug delivery. Prog. Lipid Res. 39(5), 409–460 (2000).
  Medline CASGoogle Scholar
• 50 Luo D, Carter KA, Razi A et al. Doxorubicin encapsulated in stealth liposomes conferred with light-triggered drug release. Biomaterials 75, 193–202 (2016).
  Medline CASGoogle Scholar
• 51 Morgan C, Yianni Y, Sandhu S, Mitchell A. Liposome fusion and lipid exchange on ultraviolet irradiation of liposomes containing a photochromic phospholipid. Photochem. Photobiol. 62(1), 24–29 (1995).
  Medline CASGoogle Scholar
• 52 Yatvin MB, Weinstein JN, Dennis WH, Blumenthal R. Design of liposomes for enhanced local release of drugs by hyperthermia. Science 202(4374), 1290–1293 (1978).
  Medline CASGoogle Scholar
• 53 Needham D, Dewhirst MW. The development and testing of a new temperature-sensitive drug delivery system for the treatment of solid tumors. Adv. Drug Deliv. Rev. 53(3), 285–305 (2001).
  Medline CASGoogle Scholar
• 54 Gaber MH, Hong K, Huang SK, Papahadjopoulos D. Thermosensitive sterically stabilized liposomes: formulation and in vitro studies on mechanism of doxorubicin release by bovine serum and human plasma. Pharm. Res. 12(10), 1407–1416 (1995).
  Medline CASGoogle Scholar
• 55 Lamparski H, Liman U, Barry JA et al. Photoinduced destabilization of liposomes. Biochemistry 31(3), 685–694 (1992).
  Medline CASGoogle Scholar
• 56 Kirpotin D, Hong K, Mullah N, Papahadjopoulos D, Zalipsky S. Liposomes with detachable polymer coating: destabilization and fusion of dioleoylphosphatidylethanolamine vesicles triggered by cleavage of surface-grafted poly (ethylene glycol). FEBS Lett. 388(2), 115–118 (1996).
  Medline CASGoogle Scholar
• 57 Saito G, Swanson JA, Lee K-D. Drug delivery strategy utilizing conjugation via reversible disulfide linkages: role and site of cellular reducing activities. Adv. Drug Deliv. Rev. 55(2), 199–215 (2003).
  Medline CASGoogle Scholar
• 58 Duzgunes N, Straubinger R, Baldwin P, Papahadjopoulos D, Wilschut J, Hoekstra D. pH-Sensitive Liposomes: Introduction of Foreign Substances into Cells. Marcel Dekker, NY, USA, 713–730 (1991).
  Google Scholar
• 59 Cullis PT, Kruijff BD. Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim. Biophys. Acta 559(4), 399–420 (1979).
  Medline CASGoogle Scholar
• 60 Simões S, Moreira JN, Fonseca C, Düzgüneş N, De Lima MCP. On the formulation of pH-sensitive liposomes with long circulation times. Adv. Drug Deliv. Rev. 56(7), 947–965 (2004).
  Medline CASGoogle Scholar
• 61 Sudimack JJ, Guo W, Tjarks W, Lee RJ. A novel pH-sensitive liposome formulation containing oleyl alcohol. Biochim. Biophys. Acta 1564(1), 31–37 (2002).
  Medline CASGoogle Scholar
• 62 Subbarao NK, Parente RA, Szoka FC Jr, Nadasdi L, Pongracz K. The pH-dependent bilayer destabilization by an amphipathic peptide. Biochemistry 26(11), 2964–2972 (1987).
  Medline CASGoogle Scholar
• 63 Legendre J-Y, Szoka FC Jr. Delivery of plasmid DNA into mammalian cell lines using pH-sensitive liposomes: comparison with cationic liposomes. Pharm. Res. 9(10), 1235–1242 (1992).
  Medline CASGoogle Scholar
• 64 Ohkuma S, Poole B. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc. Natl Acad. Sci. USA 75(7), 3327–3331 (1978).
  Medline CASGoogle Scholar
• 65 Fomina N, Sankaranarayanan J, Almutairi A. Photochemical mechanisms of light-triggered release from nanocarriers. Adv. Drug Deliv. Rev. 64(11), 1005–1020 (2012).
  Medline CASGoogle Scholar
• 66 Bisby RH, Mead C, Morgan CG. Active uptake of drugs into photosensitive liposomes and rapid release on UV photolysis. Photochem. Photobiol. 72(1), 57–61 (2000).
  Medline CASGoogle Scholar
• 67 Kano K, Tanaka Y, Ogawa T, Shimomura M, Okahata Y, Kunitake T. Photoresponsive membranes. Regulation of membrane properties by photoreversible cis-trans isomerization of azobenzenes. Chem. Lett. 9(4), 421–424 (1980).
  Google Scholar
• 68 Regen SL, Singh A, Oehme G, Singh M. Polymerized phosphatidyl choline vesicles. Stabilized and controllable time-release carriers. Biochem. Biophys. Res. Commun. 101(1), 131–136 (1981).
  Medline CASGoogle Scholar
• 69 Yavlovich A, Singh A, Blumenthal R, Puri A. A novel class of photo-triggerable liposomes containing DPPC: DC 8, 9 PC as vehicles for delivery of doxorubcin to cells. Biochim. Biophys. Acta 1808(1), 117–126 (2011).
  Medline CASGoogle Scholar
• 70 Kadri R, Messaoud GB, Tamayol A et al. Preparation and characterization of nanofunctionalized alginate/methacrylated gelatin hybrid hydrogels. RSC Adv. 6(33), 27879–27884 (2016).
  CASGoogle Scholar
• 71 Anderson VC, Thompson DH. Triggered release of hydrophilic agents from plasmologen liposomes using visible light or acid. Biochim. Biophys. Acta 1109(1), 33–42 (1992).
  Medline CASGoogle Scholar
• 72 Thompson DH, Gerasimov OV, Wheeler JJ, Rui Y, Anderson VC. Triggerable plasmalogen liposomes: improvement of system efficiency. Biochim. Biophys. Acta 1279(1), 25–34 (1996).
  MedlineGoogle Scholar
• 73 Girotti AW. Photodynamic lipid peroxidation in biological systems. Photochem. Photobiol. 51(4), 497–509 (1990).
  Medline CASGoogle Scholar
• 74 Weissleder R. A clearer vision for in vivo imaging. Nat. Biotechnol. 19(4), 316–317 (2001).
  Medline CASGoogle Scholar
• 75 Prevo BG, Esakoff SA, Mikhailovsky A, Zasadzinski JA. Scalable routes to gold nanoshells with tunable sizes and response to near-infrared pulsed-laser irradiation. Small 4(8), 1183–1195 (2008).
  Medline CASGoogle Scholar
• 76 Pashkovskaya A, Kotova E, Zorlu Y et al. Light-triggered liposomal release: membrane permeabilization by photodynamic action. Langmuir 26(8), 5726–5733 (2009).
  Google Scholar
• 77 Wu G, Mikhailovsky A, Khant HA, Fu C, Chiu W, Zasadzinski JA. Remotely triggered liposome release by near-infrared light absorption via hollow gold nanoshells. J. Am. Chem. Soc. 130(26), 8175–8177 (2008).
  Medline CASGoogle Scholar
• 78 Dromi S, Frenkel V, Luk A et al. Pulsed-high intensity focused ultrasound and low temperature-sensitive liposomes for enhanced targeted drug delivery and antitumor effect. Clin. Cancer Res. 13(9), 2722–2727 (2007).
  Medline CASGoogle Scholar
• 79 Anyarambhatla GR, Needham D. Enhancement of the phase transition permeability of DPPC liposomes by incorporation of MPPC: a new temperature-sensitive liposome for use with mild hyperthermia. J. Liposome Res. 9(4), 491–506 (1999).
  CASGoogle Scholar
• 80 Li L, Ten Hagen TL, Schipper D et al. Triggered content release from optimized stealth thermosensitive liposomes using mild hyperthermia. J. Control. Release 143(2), 274–279 (2010).
  Medline CASGoogle Scholar
• 81 Nicholas AR, Scott MJ, Kennedy NI, Jones MN. Effect of grafted polyethylene glycol (PEG) on the size, encapsulation efficiency and permeability of vesicles. Biochim. Biophys. Acta 1463(1), 167–178 (2000). • An important manuscript which elucidates the effect of PEGylation on liposome cargo encapsulation efficiency.
  Medline CASGoogle Scholar
• 82 Koning GA, Eggermont AM, Lindner LH, Ten Hagen TL. Hyperthermia and thermosensitive liposomes for improved delivery of chemotherapeutic drugs to solid tumors. Pharm. Res. 27(8), 1750–1754 (2010).
  Medline CASGoogle Scholar
• 83 Gaber MH, Wu NZ, Hong K, Huang SK, Dewhirst MW, Papahadjopoulos D. Thermosensitive liposomes: extravasation and release of contents in tumor microvascular networks. Int. J. Radiat. Oncol. Biol. Phys. 36(5), 1177–1187 (1996).
  Medline CASGoogle Scholar
• 84 Kong G, Anyarambhatla G, Petros WP et al. Efficacy of liposomes and hyperthermia in a human tumor xenograft model: importance of triggered drug release. Cancer Res. 60(24), 6950–6957 (2000).
  Medline CASGoogle Scholar
• 85 Weinstein JN, Magin RL, Cysyk RL, Zaharko DS. Treatment of solid L1210 murine tumors with local hyperthermia and temperature-sensitive liposomes containing methotrexate. Cancer Res. 40(5), 1388–1395 (1980).
  Medline CASGoogle Scholar
• 86 Issels R, Lindner L, Wendtner C et al. 1LBA Impact of regional hyperthermia (RHT) on response to neo-adjuvant chemotherapy and survival of patients with high-risk soft-tissue sarcoma (HR-STS): results of the randomized EORTC-ESHO intergroup trial (NCI-00003052). Eur. J. Cancer Suppl. 7(3), 2 (2009).
  Google Scholar
• 87 Barenholz Y. Liposome application: problems and prospects. Curr. Opin. Colloid Interface Sci. 6(1), 66–77 (2001).
  CASGoogle Scholar
• 88 Malam Y, Loizidou M, Seifalian AM. Liposomes and nanoparticles: nanosized vehicles for drug delivery in cancer. Trends Pharmacol. Sci. 30(11), 592–599 (2009).
  Medline CASGoogle Scholar
• 89 Danhier F, Feron O, Préat V. To exploit the tumor microenvironment: passive and active tumor targeting of nanocarriers for anti-cancer drug delivery. J. Control. Release 148(2), 135–146 (2010).
  Medline CASGoogle Scholar
• 90 Rofstad EK, Galappathi K, Mathiesen BS. Tumor interstitial fluid pressure – a link between tumor hypoxia, microvascular density, and lymph node metastasis. Neoplasia 16(7), 586–594 (2014).
  MedlineGoogle Scholar
• 91 Lammers T, Hennink W, Storm G. Tumour-targeted nanomedicines: principles and practice. Br. J. Cancer 99(3), 392–397 (2008).
  Medline CASGoogle Scholar
• 92 Heldin C-H, Rubin K, Pietras K, Östman A. High interstitial fluid pressure – an obstacle in cancer therapy. Nat. Rev. Cancer 4(10), 806–813 (2004).
  Medline CASGoogle Scholar
• 93 Maeda H, Sawa T, Konno T. 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(1), 47–61 (2001).
  Medline CASGoogle Scholar
• 94 Jain RK. Transport of molecules in the tumor interstitium: a review. Cancer Res. 47(12), 3039–3051 (1987).
  Medline CASGoogle Scholar
• 95 Béduneau A, Saulnier P, Benoit J-P. Active targeting of brain tumors using nanocarriers. Biomaterials 28(33), 4947–4967 (2007).
  Medline CASGoogle Scholar
• 96 Weinstein JN, Blumenthal R, Sharrow SO, Henkart PA. Antibody-mediated targeting of liposomes. Binding to lymphocytes does not ensure incorporation of vesicle contents into the cells. Biochim. Biophys. Acta 509(2), 272–288 (1978).
  Medline CASGoogle Scholar
• 97 Chauhan VP, Stylianopoulos T, Boucher Y, Jain RK. Delivery of molecular and nanoscale medicine to tumors: transport barriers and strategies. Annu. Rev. Chem. Biomol. Eng. 2, 281–298 (2011).
  Medline CASGoogle Scholar
• 98 Byrne JD, Betancourt T, Brannon-Peppas L. Active targeting schemes for nanoparticle systems in cancer therapeutics. Adv. Drug Deliv. Rev. 60(15), 1615–1626 (2008).
  Medline CASGoogle Scholar
• 99 Cheng Z, Al Zaki A, Hui JZ, Muzykantov VR, Tsourkas A. Multifunctional nanoparticles: cost versus benefit of adding targeting and imaging capabilities. Science 338(6109), 903–910 (2012). • An excellent review which focuses on the analysis of the cost and benefit of incorporating additional functionalities, such as targeting ligands and imaging capabilities, into the design of nanoparticles.
  Medline CASGoogle Scholar
• 100 Kamaly N, Xiao Z, Valencia PM, Radovic-Moreno AF, Farokhzad OC. Targeted polymeric therapeutic nanoparticles: design, development and clinical translation. Chem. Soc. Rev. 41(7), 2971–3010 (2012).
  Medline CASGoogle Scholar
• 101 Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2(12), 751–760 (2007). • Explains passive and active targeting and describes types of targeting agents that can be used in liposomal active targeting.
  Medline CASGoogle Scholar
• 102 Shi J, Xiao Z, Kamaly N, Farokhzad OC. Self-assembled targeted nanoparticles: evolution of technologies and bench to bedside translation. Acc. Chem. Res. 44(10), 1123–1134 (2011).
  Medline CASGoogle Scholar
• 103 Kirpotin DB, Drummond DC, Shao Y et al. Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localization but does increase internalization in animal models. Cancer Res. 66(13), 6732–6740 (2006).
  Medline CASGoogle Scholar
• 104 Jeong Y, Xie Y, Xiao G et al. Nuclear receptor expression defines a set of prognostic biomarkers for lung cancer. PLoS Med. 7(12), e1000378 (2010).
  MedlineGoogle Scholar
• 105 Holbeck S, Chang J, Best AM, Bookout AL, Mangelsdorf DJ, Martinez ED. Expression profiling of nuclear receptors in the NCI60 cancer cell panel reveals receptor–drug and receptor–gene interactions. Mol. Endocrinol. 24(6), 1287–1296 (2010).
  Medline CASGoogle Scholar
• 106 Koshkaryev A, Sawant R, Deshpande M, Torchilin V. Immunoconjugates and long circulating systems: origins, current state of the art and future directions. Adv. Drug Deliv. Rev. 65(1), 24–35 (2013).
  Medline CASGoogle Scholar
• 107 Srinivasarao M, Galliford CV, Low PS. Principles in the design of ligand-targeted cancer therapeutics and imaging agents. Nat. Rev. Drug Discov. 14(3), 203–219 (2015).
  Medline CASGoogle Scholar
• 108 Duncan R, Vicent M, Greco F, Nicholson R. Polymer-drug conjugates: towards a novel approach for the treatment of endrocine-related cancer. Endocr. Relat. Cancer 12(Suppl. 1), S189–S199 (2005).
  Medline CASGoogle Scholar
• 109 Bertrand N, Wu J, Xu X, Kamaly N, Farokhzad OC. Cancer nanotechnology: the impact of passive and active targeting in the era of modern cancer biology. Adv. Drug Deliv. Rev. 66, 2–25 (2014).
  Medline CASGoogle Scholar
• 110 Monopoli MP, Åberg C, Salvati A, Dawson KA. Biomolecular coronas provide the biological identity of nanosized materials. Nat. Nanotechnol. 7(12), 779–786 (2012).
  Medline CASGoogle Scholar
• 111 Jiang W, Kim BY, Rutka JT, Chan WC. Nanoparticle-mediated cellular response is size-dependent. Nat. Nanotechnol. 3(3), 145–150 (2008).
  Medline CASGoogle Scholar
• 112 Yu B, Tai HC, Xue W, Lee LJ, Lee RJ. Receptor-targeted nanocarriers for therapeutic delivery to cancer. Mol. Membr. Biol. 27(7), 286–298 (2010).
  Medline CASGoogle Scholar
• 113 Saha RN, Vasanthakumar S, Bende G, Snehalatha M. Nanoparticulate drug delivery systems for cancer chemotherapy. Mol. Membr. Biol. 27(7), 215–231 (2010).
  Medline CASGoogle Scholar
• 114 Reubi JC, Schonbrunn A. Illuminating somatostatin analog action at neuroendocrine tumor receptors. Trends Pharmacol. Sci. 34(12), 676–688 (2013).
  Medline CASGoogle Scholar
• 115 Kularatne SA, Wang K, Santhapuram H-KR, Low PS. Prostate-specific membrane antigen targeted imaging and therapy of prostate cancer using a PSMA inhibitor as a homing ligand. Mol. Pharm. 6(3), 780–789 (2009).
  Medline CASGoogle Scholar
• 116 Lepenies B, Lee J, Sonkaria S. Targeting C-type lectin receptors with multivalent carbohydrate ligands. Adv. Drug Deliv. Rev. 65(9), 1271–1281 (2013).
  Medline CASGoogle Scholar
• 117 Yuan F, Dellian M, Fukumura D et al. Vascular permeability in a human tumor xenograft: molecular size dependence and cutoff size. Cancer Res. 55(17), 3752–3756 (1995).
  Medline CASGoogle Scholar
• 118 Florence AT. “Targeting” nanoparticles: the constraints of physical laws and physical barriers. J. Control. Release 164(2), 115–124 (2012).
  Medline CASGoogle Scholar
• 119 Pirollo KF, Chang EH. Does a targeting ligand influence nanoparticle tumor localization or uptake? Trends Biotechnol. 26(10), 552–558 (2008).
  Medline CASGoogle Scholar
• 120 Maruyama K, Ishida O, Takizawa T, Moribe K. Possibility of active targeting to tumor tissues with liposomes. Adv. Drug Deliv. Rev. 40(1), 89–102 (1999).
  Medline CASGoogle Scholar
• 121 Cedervall T, Lynch I, Foy M et al. Detailed identification of plasma proteins adsorbed on copolymer nanoparticles. Angew. Chem. Int. Ed. Engl. 46(30), 5754–5756 (2007). • One of the first studies to characterize plasma proteins adsorbed on nanoparticles and the dynamics of interaction of nanoparticles with distinct proteins within the protein corona on nanoparticle surface.
  Medline CASGoogle Scholar
• 122 Lundqvist M, Stigler J, Elia G, Lynch I, Cedervall T, Dawson KA. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc. Natl Acad. Sci. USA 105(38), 14265–14270 (2008).
  Medline CASGoogle Scholar
• 123 Lammers T, Kiessling F, Hennink WE, Storm G. Drug targeting to tumors: principles, pitfalls and (pre-) clinical progress. J. Control. Release 161(2), 175–187 (2012).
  Medline CASGoogle Scholar
• 124 Choi CHJ, Alabi CA, Webster P, Davis ME. Mechanism of active targeting in solid tumors with transferrin-containing gold nanoparticles. Proc. Natl Acad. Sci. USA 107(3), 1235–1240 (2010).
  Medline CASGoogle Scholar
• 125 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. 21(1), 221–232 (2005).
  Medline CASGoogle Scholar
• 126 Suzuki R, Takizawa T, Kuwata Y et al. Effective anti-tumor activity of oxaliplatin encapsulated in transferrin-PEG-liposome. Int. J. Pharm. 346(1), 143–150 (2008).
  Medline CASGoogle Scholar
• 127 Lu Y, Low PS. Folate-mediated delivery of macromolecular anticancer therapeutic agents. Adv. Drug Deliv. Rev. 64, 342–352 (2012).
  Google Scholar
• 128 Sudimack J, Lee RJ. Targeted drug delivery via the folate receptor. Adv. Drug Deliv. Rev. 41(2), 147–162 (2000).
  Medline CASGoogle Scholar
• 129 Antony AC. Folate receptors. Annu. Rev. Nutr. 16(1), 501–521 (1996).
  Medline CASGoogle Scholar
• 130 Reddy JA, Haneline LS, Srour EF, Antony AC, Clapp DW, Low PS. Expression and functional characterization of the β-isoform of the folate receptor on CD34⁺ cells. Blood 93(11), 3940–3948 (1999).
  Medline CASGoogle Scholar
• 131 Lee RJ, Low PS. Delivery of liposomes into cultured KB cells via folate receptor-mediated endocytosis. J. Biol. Chem. 269(5), 3198–3204 (1994).
  Medline CASGoogle Scholar
• 132 Lu Y, Low PS. Folate targeting of haptens to cancer cell surfaces mediates immunotherapy of syngeneic murine tumors. Cancer Immunol. Immunother. 51(3), 153–162 (2002).
  Medline CASGoogle Scholar
• 133 Siegel BA, Dehdashti F, Mutch DG et al. Evaluation of 111In-DTPA-folate as a receptor-targeted diagnostic agent for ovarian cancer: initial clinical results. J. Nucl. Med. 44(5), 700–707 (2003).
  Medline CASGoogle Scholar
• 134 Wang S, Luo J, Lantrip DA et al. Design and synthesis of [111In] DTPA-folate for use as a tumor-targeted radiopharmaceutical. Bioconjug. Chem. 8(5), 673–679 (1997).
  Medline CASGoogle Scholar
• 135 Werner ME, Karve S, Sukumar R et al. Folate-targeted nanoparticle delivery of chemo-and radiotherapeutics for the treatment of ovarian cancer peritoneal metastasis. Biomaterials 32(33), 8548–8554 (2011).
  Medline CASGoogle Scholar
• 136 Low PS, Kularatne SA. Folate-targeted therapeutic and imaging agents for cancer. Curr. Opin. Chem. Biol. 13(3), 256–262 (2009).
  Medline CASGoogle Scholar
• 137 Zhao X, Li H, Lee RJ. Targeted drug delivery via folate receptors. Expert Opin. Drug Deliv. 5(3), 309–319 (2008).
  Medline CASGoogle Scholar
• 138 Salazar MDA, Ratnam M. The folate receptor: what does it promise in tissue-targeted therapeutics? Cancer Metastasis Rev. 26(1), 141–152 (2007).
  Medline CASGoogle Scholar
• 139 Weitman SD, Lark RH, Coney LR et al. Distribution of the folate receptor GP38 in normal and malignant cell lines and tissues. Cancer Res. 52(12), 3396–3401 (1992).
  Medline CASGoogle Scholar
• 140 Nakashima-Matsushita N, Homma T, Yu S et al. Selective expression of folate receptor and its possible role in methotrexate transport in synovial macrophages from patients with rheumatoid arthritis. Arthritis Rheum. 42, 1609–1616 (1999).
  Medline CASGoogle Scholar
• 141 Galluzzi L, Morselli E, Kepp O et al. Mitochondrial gateways to cancer. Mol. Aspects Med. 31(1), 1–20 (2010).
  Medline CASGoogle Scholar
• 142 Guzman-Villanueva D, Mendiola MR, Nguyen HX, Weissig V. Influence of triphenylphosphonium (TPP) cation hydrophobization with phospholipids on cellular toxicity and mitochondrial selectivity (2015). www.symbiosisonlinepublishing.com/pharmacy-pharmaceuticalsciences/pharmacy-pharmaceuticalsciences21.pdf.
  Google Scholar
• 143 Fulda S, Galluzzi L, Kroemer G. Targeting mitochondria for cancer therapy. Nat. Rev. Drug Discov. 9(6), 447–464 (2010).
  Medline CASGoogle Scholar
• 144 Smith RA, Porteous CM, Gane AM, Murphy MP. Delivery of bioactive molecules to mitochondria in vivo. Proc. Natl Acad. Sci. USA 100(9), 5407–5412 (2003).
  Medline CASGoogle Scholar
• 145 Marrache S, Dhar S. Engineering of blended nanoparticle platform for delivery of mitochondria-acting therapeutics. Proc. Natl Acad. Sci. USA 109(40), 16288–16293 (2012).
  Medline CASGoogle Scholar
• 146 Pathak RK, Kolishetti N, Dhar S. Targeted nanoparticles in mitochondrial medicine. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 7(3), 315–329 (2015).
  Medline CASGoogle Scholar
• 147 Stylianopoulos T, Jain RK. Design considerations for nanotherapeutics in oncology. Nanomedicine 11(8), 1893–1907 (2015).
  Medline CASGoogle Scholar
• 148 Hillier SM, Maresca KP, Femia FJ et al. Preclinical evaluation of novel glutamate-urea-lysine analogues that target prostate-specific membrane antigen as molecular imaging pharmaceuticals for prostate cancer. Cancer Res. 69(17), 6932–6940 (2009).
  Medline CASGoogle Scholar
• 149 Li X, Yang W, Zou Y, Meng F, Deng C, Zhong Z. Efficacious delivery of protein drugs to prostate cancer cells by PSMA-targeted pH-responsive chimaeric polymersomes. J. Control. Release 220, 704–714 (2015).
  Medline CASGoogle Scholar
• 150 Deng C, Jiang Y, Cheng R, Meng F, Zhong Z. Biodegradable polymeric micelles for targeted and controlled anticancer drug delivery: promises, progress and prospects. Nano Today 7(5), 467–480 (2012).
  CASGoogle Scholar
• 151 Maeda H. The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumor-selective macromolecular drug targeting. Adv. Enzyme Regul. 41(1), 189–207 (2001).
  Medline CASGoogle Scholar
• 152 Allen TM. Ligand-targeted therapeutics in anticancer therapy. Nat. Rev. Cancer 2(10), 750–763 (2002).
  Medline CASGoogle Scholar
• 153 Pinheiro VB, Taylor AI, Cozens C et al. Synthetic genetic polymers capable of heredity and evolution. Science 336(6079), 341–344 (2012).
  Medline CASGoogle Scholar
• 154 Farokhzad OC, Jon S, Khademhosseini A, Tran T-NT, Lavan DA, Langer R. Nanoparticle-aptamer bioconjugates a new approach for targeting prostate cancer cells. Cancer Res. 64(21), 7668–7672 (2004).
  Medline CASGoogle Scholar
• 155 Xiao Z, Farokhzad OC. Aptamer-functionalized nanoparticles for medical applications: challenges and opportunities. ACS Nano 6(5), 3670–3676 (2012).
  Medline CASGoogle Scholar
• 156 Dubey PK, Mishra V, Jain S, Mahor S, Vyas S. Liposomes modified with cyclic RGD peptide for tumor targeting. J. Drug Target. 12(5), 257–264 (2004).
  Medline CASGoogle Scholar
• 157 Colombo G, Curnis F, De Mori GM et al. Structure-activity relationships of linear and cyclic peptides containing the NGR tumor-homing motif. J. Biol. Chem. 277(49), 47891–47897 (2002).
  Medline CASGoogle Scholar
• 158 Negussie AH, Miller JL, Reddy G, Drake SK, Wood BJ, Dreher MR. Synthesis and in vitro evaluation of cyclic NGR peptide targeted thermally sensitive liposome. J. Control. Release 143(2), 265–273 (2010).
  Medline CASGoogle Scholar
• 159 Sakaguchi N, Kojima C, Harada A, Koiwai K, Emi N, Kono K. Effect of transferrin as a ligand of pH-sensitive fusogenic liposome−lipoplex hybrid complexes. Bioconjug. Chem. 19(8), 1588–1595 (2008).
  Medline CASGoogle Scholar
• 160 Szwed M, Matusiak A, Laroche-Clary A, Robert J, Marszalek I, Jozwiak Z. Transferrin as a drug carrier: cytotoxicity, cellular uptake and transport kinetics of doxorubicin transferrin conjugate in the human leukemia cells. Toxicol. In Vitro 28(2), 187–197 (2014).
  Medline CASGoogle Scholar
• 161 Joshee N, Bastola DR, Cheng P-W. Transferrin-facilitated lipofection gene delivery strategy: characterization of the transfection complexes and intracellular trafficking. Hum. Gene Ther. 13(16), 1991–2004 (2002).
  Medline CASGoogle Scholar
• 162 Alexis F, Basto P, Levy-Nissenbaum E et al. HER-2-targeted nanoparticle-affibody bioconjugates for cancer therapy. ChemMedChem 3(12), 1839–1843 (2008).
  Medline CASGoogle Scholar
• 163 Sandström M, Lindskog K, Velikyan I et al. Biodistribution and radiation dosimetry of the anti-HER2 affibody molecule 68Ga-ABY-025 in breast cancer patients. J. Nucl. Med. 57(6), 867–871 (2016).
  MedlineGoogle Scholar
• 164 Winkler J, Martin-Killias P, Plückthun A, Zangemeister-Wittke U. EpCAM-targeted delivery of nanocomplexed siRNA to tumor cells with designed ankyrin repeat proteins. Mol. Cancer Ther. 8(9), 2674–2683 (2009).
  Medline CASGoogle Scholar
• 165 Trzpis M, Mclaughlin PM, De Leij LM, Harmsen MC. Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule. Am. J. Pathol. 171(2), 386–395 (2007).
  Medline CASGoogle Scholar
• 166 Chari RV. Targeted delivery of chemotherapeutics: tumor-activated prodrug therapy. Adv. Drug Deliv. Rev. 31(1), 89–104 (1998).
  Medline CASGoogle Scholar
• 167 Glennie MJ, Van De Winkel JG. Renaissance of cancer therapeutic antibodies. Drug Discov. Today 8(11), 503–510 (2003).
  Medline CASGoogle Scholar
• 168 Abou-Jawde R, Choueiri T, Alemany C, Mekhail T. An overview of targeted treatments in cancer. Clin. Ther. 25(8), 2121–2137 (2003).
  Medline CASGoogle Scholar
• 169 Brannon-Peppas L, Blanchette JO. Nanoparticle and targeted systems for cancer therapy. Adv. Drug Deliv. Rev. 64, 206–212 (2012).
  Google Scholar
• 170 Leserman LD, Barbet J, Kourilsky F, Weinstein JN. Targeting to cells of fluorescent liposomes covalently coupled with monoclonal antibody or protein A. Nature 288(5791), 602–604 (1980).
  Medline CASGoogle Scholar
• 171 Bartlett DW, Su H, Hildebrandt IJ, Weber WA, Davis ME. Impact of tumor-specific targeting on the biodistribution and efficacy of siRNA nanoparticles measured by multimodality in vivo imaging. Proc. Natl Acad. Sci. USA 104(39), 15549–15554 (2007).
  Medline CASGoogle Scholar
• 172 Simard P, Leroux J-C. In vivo evaluation of pH-sensitive polymer-based immunoliposomes targeting the CD33 antigen. Mol. Pharm. 7(4), 1098–1107 (2010).
  Medline CASGoogle Scholar
• 173 Anselmo AC, Mitragotri S. Nanoparticles in the clinic. Bioeng. Transl. Med. 1(1), 10–29 (2016).
  MedlineGoogle Scholar
• 174 Munster PN, Miller K, Krop IE et al. A Phase I study of MM-302, a HER2-targeted liposomal doxorubicin, in patients with advanced, HER2-positive (HER2+) breast cancer. Presented at: ASCO Annual Meeting. 1–5 June, Chicago, IL, USA (2012).
  Google Scholar
• 175 Matsumura Y, Gotoh M, Muro K et al. Phase I and pharmacokinetic study of MCC-465, a doxorubicin (DXR) encapsulated in PEG immunoliposome, in patients with metastatic stomach cancer. Ann. Oncol. 15(3), 517–525 (2004).
  Medline CASGoogle Scholar
• 176 Albanese A, Tang PS, Chan WC. The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu. Rev. Biomed. Eng. 14, 1–16 (2012).
  Medline CASGoogle Scholar
• 177 Rodriguez PL, Harada T, Christian DA, Pantano DA, Tsai RK, Discher DE. Minimal “self” peptides that inhibit phagocytic clearance and enhance delivery of nanoparticles. Science 339, 971–975 (2013). • Describes an innovative approach to attenuate nanoparticle clearance by phagocytes based on the engrafment of CD47-derived ‘self peptides’ on to nanoparticles surface.
  Medline CASGoogle Scholar
• 178 Blanco E, Shen H, Ferrari M. Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat. Biotech. 33, 941–951 (2015).
  Medline CASGoogle Scholar
• 179 Ritz S, Schöttler S, Kotman N et al. Protein corona of nanoparticles: distinct proteins regulate the cellular uptake. Biomacromolecules 16(4), 1311–1321 (2015). • One of the first studies to show that distinct proteins found within coronas have different effects on nanoparticles cell uptake.
  Medline CASGoogle Scholar
• 180 Nie S. Understanding and overcoming major barriers in cancer nanomedicine. Nanomedicine 5(4), 523–528 (2010).
  MedlineGoogle Scholar