Advertisement

Investigating Interactions Between Nanoparticles and Cells: Internalization and Intracellular Trafficking

  • Hervé HillaireauEmail author
Chapter

Abstract

Nanoparticles used as drug nanocarriers offer unique possibilities to overcome cellular barriers in order to improve the delivery of various molecules, including biomacromolecules such as nucleic acids or proteins. Depending on nanoparticle characteristics and the type of cells considered, various mechanisms of internalization may occur, as well as subsequent intracellular trafficking pathways. Understanding these pathways may have important pharmacological implications. This chapter will review the main nanoparticle internalization and trafficking mechanisms and their experimental characterizations, allowing to understand how they are affected by nanoparticle physicochemical properties. The phagocytosis pathway will first be described, being increasingly well characterized and understood, which has allowed several successes in the treatment of some cancers and infectious diseases. In contrast, other non-phagocytic pathways encompass various complex mechanisms, such as clathrin-mediated endocytosis, caveolae-mediated endocytosis and macropinocytosis. Although more challenging to control for pharmaceutical drug delivery applications, they are actively investigated in order to tailor nanocarriers able to deliver anticancer agents, nucleic acids, proteins, and peptides for therapeutic applications.

Keywords

Caveolae Caveolae-mediated endocytosis Clathrin Clathrin-mediated endocytosis Endocytosis Endosome Internalization Intracellular trafficking Lysosome Macropinocytosis Opsonization Phagocytosis Pinocytosis Receptor-mediated endocytosis 

References

  1. Aderem A (2002) How to eat something bigger than your head. Cell 110:5–8PubMedCrossRefGoogle Scholar
  2. Aderem A, Underhill D (1999) Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17:593–623PubMedCrossRefGoogle Scholar
  3. Aktaş Y, Yemisci M, Andrieux K, Gürsoy RN, Alonso MJ, Fernandez-Megia E, Novoa-Carballal R, Quiñoá E, Riguera R, Sargon MF, Celik HH, Demir AS, Hincal AA, Dalkara T, Capan Y, Couvreur P (2005) Development and brain delivery of chitosan-PEG nanoparticles functionalized with the monoclonal antibody OX26. Bioconjug Chem 16:1503–1511PubMedCrossRefGoogle Scholar
  4. Al-Awqati Q (1986) Proton-translocating ATPases. Annu Rev Cell Biol 2:179–199PubMedCrossRefGoogle Scholar
  5. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Intracellular vesicular traffic. In: Alberts B (ed) Molecular biology of the cell, 4th edn. Garland Science, New YorkGoogle Scholar
  6. Alexis F, Pridgen E, Molnar LK, Farokhzad OC (2008) Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol Pharm 5:505–515PubMedPubMedCentralCrossRefGoogle Scholar
  7. Allen TM, Austin GA, Chonn A, Lin L, Lee KC (1991) Uptake of liposomes by cultured mouse bone marrow macrophages: influence of liposome composition and size. Biochim Biophys Acta Biomembranes 1061:56–64CrossRefGoogle Scholar
  8. Andresen TL, Jensen SS, Jørgensen K (2005) Advanced strategies in liposomal cancer therapy: problems and prospects of active and tumor specific drug release. Prog Lipid Res 44:68–97PubMedCrossRefGoogle Scholar
  9. Aub JC, Tieslaut C, Lankester A (1963) Reactions of normal and tumor cell surfaces to enzymes. I. Wheat-germ lipase and associated mucopolysaccharides. Proc Natl Acad Sci USA 50:613–619PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bae Y, Nishiyama N, Fukushima S, Koyama H, Yasuhiro M, Kataoka K (2005) Preparation and biological characterization of polymeric micelle drug carriers with intracellular pH-triggered drug release property: tumor permeability, controlled subcellular drug distribution, and enhanced in vivo antitumor efficacy. Bioconjug Chem 16:122–130PubMedCrossRefGoogle Scholar
  11. Bareford LM, Swaan PW (2007) Endocytic mechanisms for targeted drug delivery. Adv Drug Deliv Rev 59:748–758PubMedPubMedCentralCrossRefGoogle Scholar
  12. Barratt G, Tenu JP, Yapo A, Petit JF (1986) Preparation and characterisation of liposomes containing mannosylated phospholipids capable of targetting drugs to macrophages. Biochim Biophys Acta 862:153–164PubMedCrossRefGoogle Scholar
  13. Behr JP (1997) The proton sponge: a trick to enter cells the viruses did not exploit. Chimia 51:34–36Google Scholar
  14. Beningo KA, Wang Y (2002) Fc-receptor-mediated phagocytosis is regulated by mechanical properties of the target. J Cell Sci 115:849–856PubMedGoogle Scholar
  15. Bergstrand N, Arfvidsson MC, Kim J, Thompson DH, Edwards K (2003) Interactions between pH-sensitive liposomes and model membranes. Biophys Chem 104:361–379PubMedCrossRefGoogle Scholar
  16. Bertholon I, Vauthier C, Labarre D (2006) Complement activation by core-shell poly(isobutylcyanoacrylate)–polysaccharide nanoparticles: influences of surface morphology, length, and type of polysaccharide. Pharm Res 23:1313–1323PubMedCrossRefGoogle Scholar
  17. Betageri GV, Black CD, Szebeni J, Wahl LM, Weinstein JN (1993) Fc-receptor-mediated targeting of antibody-bearing liposomes containing dideoxycytidine triphosphate to human monocyte/macrophages. J Pharm Pharmacol 45:48–53PubMedCrossRefGoogle Scholar
  18. Bieber T, Meissner W, Kostin S, Niemann A, Elsasser H (2002) Intracellular route and transcriptional competence of polyethylenimine-DNA complexes. J Control Release 82:441–454PubMedCrossRefGoogle Scholar
  19. Black C, Gregoriadis G (1974) Intracellular fate and effect of liposome-entrapped actinomycin-d injected into rats. Biochem Soc Trans 2:869–871CrossRefGoogle Scholar
  20. Boussif O, Lezoualc’h F, Zanta MA, Mergny MD, Scherman D, Demeneix B, Behr JP (1995) A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci USA 92:7297–7301PubMedPubMedCentralCrossRefGoogle Scholar
  21. Brigger I, Morizet J, Aubert G, Chacun H, Terrier-Lacombe M, Couvreur P, Vassal G (2002) Poly(ethylene glycol)-coated hexadecylcyanoacrylate nanospheres display a combined effect for brain tumor targeting. J Pharmacol Exp Ther 303:928–936PubMedCrossRefGoogle Scholar
  22. Calvo P, Alonso MJ, Vila-Jato JL, Robinson JR (1996) Improved ocular bioavailability of indomethacin by novel ocular drug carriers. J Pharm Pharmacol 48:1147–1152PubMedCrossRefGoogle Scholar
  23. Calvo P, Gouritin B, Brigger I, Lasmezas C, Deslys J, Williams A, Andreux JP, Dormont D, Couvreur P (2001a) PEGylated polycyanoacrylate nanoparticles as vector for drug delivery in prion diseases. J Neurosci Methods 111:151–155PubMedCrossRefGoogle Scholar
  24. Calvo P, Gouritin B, Chacun H, Desmaële D, D’Angelo J, Noel JP, Georgin D, Fattal E, Andreux JP, Couvreur P (2001b) Long-circulating PEGylated polycyanoacrylate nanoparticles as new drug carrier for brain delivery. Pharm Res 18:1157–1166PubMedCrossRefGoogle Scholar
  25. Calvo P, Gouritin B, Villarroya H, Eclancher F, Giannavola C, Klein C, Andreux JP, Couvreur P (2002) Quantification and localization of PEGylated polycyanoacrylate nanoparticles in brain and spinal cord during experimental allergic encephalomyelitis in the rat. Eur J Neurosci 15:1317–1326PubMedCrossRefGoogle Scholar
  26. Carmona-Ribeiro AM (2006) Lipid bilayer fragments and disks in drug delivery. Curr Med Chem 13:1359–1370PubMedCrossRefGoogle Scholar
  27. Caron E, Hall A (1998) Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282:1717–1721PubMedCrossRefGoogle Scholar
  28. Cerletti A, Drewe J, Fricker G, Eberle AN, Huwyler J (2000) Endocytosis and transcytosis of an immunoliposome-based brain drug delivery system. J Drug Target 8:435–446PubMedCrossRefGoogle Scholar
  29. Champion JA, Mitragotri S (2006) Role of target geometry in phagocytosis. Proc Natl Acad Sci USA 103:4930–4934PubMedPubMedCentralCrossRefGoogle Scholar
  30. Champion JA, Katare YK, Mitragotri S (2007a) Making polymeric micro- and nanoparticles of complex shapes. Proc Natl Acad Sci USA 104:11901–11904PubMedPubMedCentralCrossRefGoogle Scholar
  31. Champion JA, Katare YK, Mitragotri S (2007b) Particle shape: a new design parameter for micro- and nanoscale drug delivery carriers. J Control Release 121:3–9PubMedPubMedCentralCrossRefGoogle Scholar
  32. Chang WJ, Rothberg KG, Kamen BA, Anderson RG (1992) Lowering the cholesterol content of MA104 cells inhibits receptor-mediated transport of folate. J Cell Biol 118:63–69PubMedCrossRefGoogle Scholar
  33. Chavanpatil MD, Khdair A, Panyam J (2006) Nanoparticles for cellular drug delivery: mechanisms and factors influencing delivery. J Nanosci Nanotechnol 6:2651–2663PubMedCrossRefGoogle Scholar
  34. Chawla JS, Amiji MM (2002) Biodegradable poly([var epsilon]-caprolactone) nanoparticles for tumor-targeted delivery of tamoxifen. Int J Pharm 249:127–138PubMedCrossRefGoogle Scholar
  35. Chen H, Langer R, Edwards DA (1997) A film tension theory of phagocytosis. J Colloid Interface Sci 190:118–133PubMedCrossRefGoogle Scholar
  36. Cheng Z, Singh RD, Marks DL, Pagano RE (2006) Membrane microdomains, caveolae, and caveolar endocytosis of sphingolipids. Mol Membr Biol 23:101–110PubMedCrossRefGoogle Scholar
  37. Chonn A, Cullis PR, Devine DV (1991) The role of surface charge in the activation of the classical and alternative pathways of complement by liposomes. J Immunol 146:4234–4241PubMedGoogle Scholar
  38. Christofidou-Solomidou M, Pietra GG, Solomides CC, Arguiris E, Harshaw D, Fitzgerald GA, Albelda SM, Muzykantov VR (2000) Immunotargeting of glucose oxidase to endothelium in vivo causes oxidative vascular injury in the lungs. Am J Physiol Lung Cell Mol Physiol 278:L794–L805PubMedGoogle Scholar
  39. Chung T, Wu S, Yao M, Lu C, Lin Y, Hung Y, Mou C, Chen Y, Huang D (2007) The effect of surface charge on the uptake and biological function of mesoporous silica nanoparticles in 3T3-L1 cells and human mesenchymal stem cells. Biomaterials 28:2959–2966PubMedCrossRefGoogle Scholar
  40. Claesson PM, Blomberg E, Fröberg JC, Nylander T, Arnebrant T (1995) Protein interactions at solid surfaces. Adv Colloid Interface Sci 57:161–227CrossRefGoogle Scholar
  41. Claus V, Jahraus A, Tjelle T, Berg T, Kirschke H, Faulstich H, Griffiths G (1998) Lysosomal enzyme trafficking between phagosomes, endosomes, and lysosomes in J774 macrophages. Enrichment of cathepsin H in early endosomes. J Biol Chem 273:9842–9851PubMedCrossRefGoogle Scholar
  42. Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422:37–44PubMedCrossRefGoogle Scholar
  43. Connor J, Norley N, Huang L (1986) Biodistribution of pH-sensitive immunoliposomes. Biochim Biophys Acta 884:474–481PubMedCrossRefGoogle Scholar
  44. Couvreur P, Tulkenst P, Roland M, Trouet A, Speiser P (1977) Nanocapsules: a new type of lysosomotropic carrier. FEBS Lett 84:323–326PubMedCrossRefGoogle Scholar
  45. Cullis PR, Chonn A, Semple SC (1998) Interactions of liposomes and lipid-based carrier systems with blood proteins: relation to clearance behaviour in vivo. Adv Drug Deliv Rev 32:3–17PubMedCrossRefGoogle Scholar
  46. Dauty E, Remy J, Zuber G, Behr J (2002) Intracellular delivery of nanometric DNA particles via the folate receptor. Bioconjug Chem 13:831–839PubMedCrossRefGoogle Scholar
  47. de la Fuente JM, Berry CC (2005) Tat peptide as an efficient molecule to translocate gold nanoparticles into the cell nucleus. Bioconjug Chem 16:1176–1180PubMedCrossRefGoogle Scholar
  48. de Rieux A, Fievez V, Théate I, Mast J, Préat V, Schneider Y (2007) An improved in vitro model of human intestinal follicle-associated epithelium to study nanoparticle transport by M cells. Eur J Pharm Biopharm 30:380–391Google Scholar
  49. Decuzzi P, Ferrari M (2007) The role of specific and non-specific interactions in receptor-mediated endocytosis of nanoparticles. Biomaterials 28:2915–2922PubMedCrossRefGoogle Scholar
  50. Demeneix B, Hassani Z, Behr J (2004) Towards multifunctional synthetic vectors. Curr Gene Ther 4:445–455PubMedCrossRefGoogle Scholar
  51. Derksen JT, Morselt HW, Scherphof GL (1988) Uptake and processing of immunoglobulin-coated liposomes by subpopulations of rat liver macrophages. Biochim Biophys Acta 971:127–136PubMedCrossRefGoogle Scholar
  52. Desai MP, Labhasetwar V, Amidon GL, Levy RJ (1996) Gastrointestinal uptake of biodegradable microparticles: effect of particle size. Pharm Res 13:1838–1845PubMedCrossRefGoogle Scholar
  53. Desai MP, Labhasetwar V, Walter E, Levy RJ, Amidon GL (1997) The mechanism of uptake of biodegradable microparticles in Caco-2 cells is size dependent. Pharm Res 14:1568–1573PubMedCrossRefGoogle Scholar
  54. Desjardins M, Griffiths G (2003) Phagocytosis: latex leads the way. Curr Opin Cell Biol 15:498–503PubMedCrossRefGoogle Scholar
  55. Devika Chithrani B, Ghazani A, Chan W (2006) Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett 6:662–668PubMedCrossRefGoogle Scholar
  56. Devine DV, Wong K, Serrano K, Chonn A, Cullis PR (1994) Liposome-complement interactions in rat serum: implications for liposome survival studies. Biochim Biophys Acta 1191:43–51PubMedCrossRefGoogle Scholar
  57. Di Fiore PP, De Camilli P (2001) Endocytosis and signaling. an inseparable partnership. Cell 106:1–4PubMedCrossRefGoogle Scholar
  58. Ding B, Dziubla T, Shuvaev VV, Muro S, Muzykantov VR (2006) Advanced drug delivery systems that target the vascular endothelium. Mol Interv 6:98–112PubMedCrossRefGoogle Scholar
  59. Drummond CJ, Fong C (1999) Surfactant self-assembly objects as novel drug delivery vehicles. Curr Opin Colloid Interface Sci 4:449–456CrossRefGoogle Scholar
  60. Drummond DC, Zignani M, Leroux J (2000) Current status of pH-sensitive liposomes in drug delivery. Prog Lipid Res 39:409–460PubMedCrossRefGoogle Scholar
  61. Dunehoo AL, Anderson M, Majumdar S, Kobayashi N, Berkland C, Siahaan TJ (2006) Cell adhesion molecules for targeted drug delivery. J Pharm Sci 95:1856–1872PubMedCrossRefGoogle Scholar
  62. Düzgünes N, Simões S, Slepushkin V, Pretzer E, Rossi JJ, De Clercq E, Antao VP, Collins ML, de Lima MC (2001) Enhanced inhibition of HIV-1 replication in macrophages by antisense oligonucleotides, ribozymes and acyclic nucleoside phosphonate analogs delivered in pH-sensitive liposomes. Nucleosides, Nucleotides Nucleic Acids 20:515–523PubMedCrossRefGoogle Scholar
  63. Eboue D, Auger R, Angiari C, Le Doan T, Tenu JP (2003) Use of a simple fractionation method to evaluate binding, internalization and intracellular distribution of oligonucleotides in vascular smooth muscle cells. Arch Physiol Biochem 111:265–272PubMedCrossRefGoogle Scholar
  64. Ellens H, Bentz J, Szoka FC (1984) pH-induced destabilization of phosphatidylethanolamine-containing liposomes: role of bilayer contact. Biochemistry 23:1532–1538PubMedCrossRefGoogle Scholar
  65. Esmaeili F, Ghahremani MH, Esmaeili B, Khoshayand MR, Atyabi F, Dinarvand R (2008) PLGA nanoparticles of different surface properties: preparation and evaluation of their body distribution. Int J Pharm 349:249–255PubMedCrossRefGoogle Scholar
  66. Fattal E, Couvreur P, Dubernet C (2004) “Smart” delivery of antisense oligonucleotides by anionic pH-sensitive liposomes. Adv Drug Deliv Rev 56:931–946PubMedCrossRefGoogle Scholar
  67. Felgner JH, Kumar R, Sridhar CN, Wheeler CJ, Tsai YJ, Border R, Ramsey P, Martin M, Felgner PL (1994) Enhanced gene delivery and mechanism studies with a novel series of cationic lipid formulations. J Biol Chem 269:2550–2561PubMedGoogle Scholar
  68. Florence AT, Hillery AM, Hussain N, Jani PU (1995) Nanoparticles as carriers for oral peptide absorption: studies on particle uptake and fate. J Control Release 36:39–46CrossRefGoogle Scholar
  69. Frank M, Fries L (1991) The role of complement in inflammation and phagocytosis. Immunol Today 12:322–326PubMedCrossRefGoogle Scholar
  70. Gabizon A, Papahadjopoulos D (1992) The role of surface charge and hydrophilic groups on liposome clearance in vivo. Biochim Biophys Acta Biomembranes 1103:94–100CrossRefGoogle Scholar
  71. 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 56:1177–1192PubMedCrossRefGoogle Scholar
  72. Gao H, Shi W, Freund LB (2005) Mechanics of receptor-mediated endocytosis. Proc Natl Acad Sci USA 102:9469–9474PubMedPubMedCentralCrossRefGoogle Scholar
  73. Garcia-Garcia E, Gil S, Andrieux K, Desmaële D, Nicolas V, Taran F, Georgin D, Andreux JP, Roux F, Couvreur P (2005a) A relevant in vitro rat model for the evaluation of blood-brain barrier translocation of nanoparticles. Cell Mol Life Sci 62:1400–1408PubMedPubMedCentralCrossRefGoogle Scholar
  74. Garcia-Garcia E, Andrieux K, Gil S, Kim HR, Le Doan T, Desmaële D, d’Angelo J, Taran F, Georgin D, Couvreur P (2005b) A methodology to study intracellular distribution of nanoparticles in brain endothelial cells. Int J Pharm 298(2):310–314PubMedCrossRefGoogle Scholar
  75. Gillies ER, Fréchet JMJ (2005) pH-responsive copolymer assemblies for controlled release of doxorubicin. Bioconjug Chem 16:361–368PubMedCrossRefGoogle Scholar
  76. Gillies ER, Goodwin AP, Fréchet JMJ (2004) Acetals as pH-sensitive linkages for drug delivery. Bioconjug Chem 15:1254–1263PubMedCrossRefGoogle Scholar
  77. Göppert TM, Müller RH (2003) Plasma protein adsorption of Tween 80- and poloxamer 188-stabilized solid lipid nanoparticles. J Drug Target 11:225–231PubMedCrossRefGoogle Scholar
  78. Göppert TM, Müller RH (2005) Polysorbate-stabilized solid lipid nanoparticles as colloidal carriers for intravenous targeting of drugs to the brain: comparison of plasma protein adsorption patterns. J Drug Target 13:179–187PubMedCrossRefGoogle Scholar
  79. Grabowski N, Hillaireau H, Vergnaud-Gauduchon J, Nicolas V, Tsapis N, Kerdine-Romer S, Fattal E (2016) Surface-modified biodegradable nanoparticles’ impact on cytotoxicity and inflammation response on a co-culture of lung epithelial cells and human-like macrophages. J Biomed Nanotechnol 12(1):135–146PubMedCrossRefGoogle Scholar
  80. Gratton SEA, Ropp PA, Pohlhaus PD, Luft JC, Madden VJ, Napier ME, DeSimone JM (2008a) The effect of particle design on cellular internalization pathways. Proc Natl Acad Sci USA 105:11613–11618PubMedPubMedCentralCrossRefGoogle Scholar
  81. Gratton SEA, Napier ME, Ropp PA, Tian S, Desimone JM (2008b) Microfabricated particles for engineered drug therapies: elucidation into the mechanisms of cellular internalization of PRINT particles. Pharm Res 25:2845–2852PubMedPubMedCentralCrossRefGoogle Scholar
  82. Gregoriadis G (1978) Liposomes in the therapy of lysosomal storage diseases. Nature 275:695–696PubMedCrossRefGoogle Scholar
  83. Grislain L, Couvreur P, Lenaerts V, Roland M, Deprezdecampeneere D, Speiser P (1983) Pharmacokinetics and distribution of a biodegradable drug-carrier. Int J Pharm 15:335–345CrossRefGoogle Scholar
  84. Groves E, Dart A, Covarelli V, Caron E (2008) Molecular mechanisms of phagocytic uptake in mammalian cells. Cell Mol Life Sci 65:1957–1976PubMedCrossRefGoogle Scholar
  85. Guo LSS (2001) Amphotericin B colloidal dispersion: an improved antifungal therapy. Adv Drug Deliv Rev 47:149–163PubMedCrossRefGoogle Scholar
  86. Haag R, Kratz F (2006) Polymer therapeutics: concepts and applications. Angew Chem Int Ed Engl 45:1198–1215PubMedCrossRefGoogle Scholar
  87. Harashima H, Sakata K, Funato K, Kiwada H (1994) Enhanced hepatic uptake of liposomes through complement activation depending on the size of liposomes. Pharm Res 11:402–406PubMedCrossRefGoogle Scholar
  88. Harashima H, Hiraiwa T, Ochi Y, Kiwada H (1995) Size dependent liposome degradation in blood: in vivo/in vitro correlation by kinetic modeling. J Drug Target 3:253–261PubMedCrossRefGoogle Scholar
  89. Harding JA, Engbers CM, Newman MS, Goldstein NI, Zalipsky S (1997) Immunogenicity and pharmacokinetic attributes of poly(ethylene glycol)-grafted immunoliposomes. Biochim Biophys Acta 1327:181–192PubMedCrossRefGoogle Scholar
  90. Harush-Frenkel O, Debotton N, Benita S, Altschuler Y (2007) Targeting of nanoparticles to the clathrin-mediated endocytic pathway. Biochem Biophys Res Commun 353:26–32PubMedCrossRefGoogle Scholar
  91. Harush-Frenkel O, Rozentur E, Benita S, Altschuler Y (2008) Surface charge of nanoparticles determines their endocytic and transcytotic pathway in polarized MDCK cells. Biomacromolecules 9:435–443PubMedCrossRefGoogle Scholar
  92. Heath TD, Lopez NG, Papahadjopoulos D (1985) The effects of liposome size and surface charge on liposome-mediated delivery of methotrexate-gamma-aspartate to cells in vitro. Biochim Biophys Acta 820:74–84PubMedCrossRefGoogle Scholar
  93. Hilgenbrink AR, Low PS (2005) Folate receptor-mediated drug targeting: from therapeutics to diagnostics. J Pharm Sci 94:2135–2146PubMedCrossRefGoogle Scholar
  94. Hoffmann PR, deCathelineau AM, Ogden CA, Leverrier Y, Bratton DL, Daleke DL, Ridley AJ, Fadok VA, Henson PM (2001) Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J Cell Biol 155:649–660PubMedPubMedCentralCrossRefGoogle Scholar
  95. Hoshino A, Fujioka K, Oku T, Nakamura S, Suga M, Yamaguchi Y, Suzuki K, Yasuhara M, Yamamoto K (2004) Quantum dots targeted to the assigned organelle in living cells. Microbiol Immunol 48:985–994PubMedCrossRefGoogle Scholar
  96. Hsu MJ, Juliano RL (1982) Interactions of liposomes with the reticuloendothelial system. II: nonspecific and receptor-mediated uptake of liposomes by mouse peritoneal macrophages. Biochim Biophys Acta 720:411–419PubMedCrossRefGoogle Scholar
  97. Huang M, Ma Z, Khor E, Lim L (2002) Uptake of FITC-chitosan nanoparticles by A549 cells. Pharm Res 19:1488–1494PubMedCrossRefGoogle Scholar
  98. Huang M, Khor E, Lim L (2004) Uptake and cytotoxicity of chitosan molecules and nanoparticles: effects of molecular weight and degree of deacetylation. Pharm Res 21:344–353PubMedCrossRefGoogle Scholar
  99. Huwyler J, Wu D, Pardridge WM (1996) Brain drug delivery of small molecules using immunoliposomes. Proc Natl Acad Sci USA 93:14164–14169PubMedPubMedCentralCrossRefGoogle Scholar
  100. Huwyler J, Yang J, Pardridge WM (1997) Receptor mediated delivery of daunomycin using immunoliposomes: pharmacokinetics and tissue distribution in the rat. J Pharmacol Exp Ther 282:1541–1546PubMedGoogle Scholar
  101. Ilium L, Hunneyball I, Davis S (1986) The effect of hydrophilic coatings on the uptake of colloidal particles by the liver and by peritoneal macrophages. Int J Pharm 29:53–65CrossRefGoogle Scholar
  102. Jeon S, Lee J, Andrade J, De Gennes P (1991) Protein–surface interactions in the presence of polyethylene oxide: I. Simplified theory. J Colloid Interface Sci 142:149–158CrossRefGoogle Scholar
  103. Jiang W, Kim BYS, Rutka JT, Chan WCW (2008) Nanoparticle-mediated cellular response is size-dependent. Nat Nanotechnol 3:145–150PubMedCrossRefGoogle Scholar
  104. Jones A, Shusta E (2007) Blood–brain barrier transport of therapeutics via receptor-mediation. Pharm Res 24:1759–1771PubMedPubMedCentralCrossRefGoogle Scholar
  105. Juliano RL, Lin G (1980) The binding of human plasma proteins to cholesterol containing liposomes. In: Baldwin H (ed) Liposomes and immunobiology. Elsevier, New York, pp 49–66Google Scholar
  106. Juliano RL, Stamp D (1975) The effect of particle size and charge on the clearance rates of liposomes and liposome encapsulated drugs. Biochem Biophys Res Commun 63:651–658PubMedCrossRefGoogle Scholar
  107. Kanaseki T, Kadota K (1969) The “vesicle in a basket”. A morphological study of the coated vesicle isolated from the nerve endings of the guinea pig brain, with special reference to the mechanism of membrane movements. J Cell Biol 42:202–220PubMedPubMedCentralCrossRefGoogle Scholar
  108. Kichler A, Leborgne C, Coeytaux E, Danos O (2001) Polyethylenimine-mediated gene delivery: a mechanistic study. J Gene Med 3:135–144PubMedCrossRefGoogle Scholar
  109. Kim SH, Jeong JH, Chun KW, Park TG (2005) Target-specific cellular uptake of PLGA nanoparticles coated with poly(L-lysine)-poly(ethylene glycol)-folate conjugate. Langmuir 21:8852–8857PubMedCrossRefGoogle Scholar
  110. Kim HR, Gil S, Andrieux K, Nicolas V, Appel M, Chacun H, Desmaële D, Taran F, Georgin D, Couvreur P (2007a) Low-density lipoprotein receptor-mediated endocytosis of PEGylated nanoparticles in rat brain endothelial cells. Cell Mol Life Sci 64:356–364PubMedCrossRefGoogle Scholar
  111. Kim HR, Andrieux K, Gil S, Taverna M, Chacun H, Desmaële D, Taran F, Georgin D, Couvreur P (2007b) Translocation of poly(ethylene glycol-co-hexadecyl)cyanoacrylate nanoparticles into rat brain endothelial cells: role of apolipoproteins in receptor-mediated endocytosis. Biomacromolecules 8:793–799PubMedCrossRefGoogle Scholar
  112. Kim HR, Andrieux K, Delomenie C, Chacun H, Appel M, Desmaële D, Taran F, Georgin D, Couvreur P, Taverna M (2007c) Analysis of plasma protein adsorption onto PEGylated nanoparticles by complementary methods: 2-DE, CE and protein lab-on-chip system. Electrophoresis 28:2252–2261PubMedCrossRefGoogle Scholar
  113. Kleemann E, Neu M, Jekel N, Fink L, Schmehl T, Gessler T, Seeger W, Kissel T (2005) Nano-carriers for DNA delivery to the lung based upon a TAT-derived peptide covalently coupled to PEG-PEI. J Control Release 109:299–316PubMedCrossRefGoogle Scholar
  114. Kole L, Sarkar K, Mahato SB, Das PK (1994) Neoglycoprotein conjugated liposomes as macrophage specific drug carrier in the therapy of leishmaniasis. Biochem Biophys Res Commun 200:351–358PubMedCrossRefGoogle Scholar
  115. Korn ED, Weisman RA (1967) Phagocytosis of latex beads by Acanthamoeba. II. Electron microscopic study of the initial events. J Cell Biol 34:219–227PubMedPubMedCentralCrossRefGoogle Scholar
  116. Koval M, Preiter K, Adles C, Stahl PD, Steinberg TH (1998) Size of IgG-opsonized particles determines macrophage response during internalization. Exp Cell Res 242:265–273PubMedCrossRefGoogle Scholar
  117. Kreuter J (2001) Nanoparticulate systems for brain delivery of drugs. Adv Drug Deliv Rev 47:65–81PubMedCrossRefGoogle Scholar
  118. Kreuter J (2002) Transport of drugs accross the blood-brain barrier by nanoparticles. Curr Med Chem: Cent Nerv Syst Agents 2:241–249Google Scholar
  119. Kreuter J, Täuber U, Illi V (1979) Distribution and elimination of poly(methyl-2-14C-methacrylate) nanoparticle radioactivity after injection in rats and mice. J Pharm Sci 68:1443–1447PubMedCrossRefGoogle Scholar
  120. Kreuter J, Ramge P, Petrov V, Hamm S, Gelperina SE, Engelhardt B, Alyautdin R, von Briesen H, Begley DJ (2003) Direct evidence that polysorbate-80-coated poly(butylcyanoacrylate) nanoparticles deliver drugs to the CNS via specific mechanisms requiring prior binding of drug to the nanoparticles. Pharm Res 20:409–416PubMedCrossRefGoogle Scholar
  121. Labarre D (2012) The interactions between blood and polymeric nanoparticles depend on the nature and structure of the hydrogel covering the surface. Polymers 4:986–996CrossRefGoogle Scholar
  122. Labarre D, Montdargent B, Carreno M, Maillet F (1993) Strategy for in vitro evaluation of the interactions between biomaterials and complement system. J Appl Biomater 4:231–240CrossRefGoogle Scholar
  123. Lai SK, Hida K, Man ST, Chen C, Machamer C, Schroer TA, Hanes J (2007) Privileged delivery of polymer nanoparticles to the perinuclear region of live cells via a non-clathrin, non-degradative pathway. Biomaterials 28:2876–2884PubMedCrossRefGoogle Scholar
  124. Larabi M, Yardley V, Loiseau PM, Appel M, Legrand P, Gulik A, Bories C, Croft SL, Barratt G (2003) Toxicity and antileishmanial activity of a new stable lipid suspension of amphotericin B. Antimicrob Agents Chemother 47:3774–3779PubMedPubMedCentralCrossRefGoogle Scholar
  125. Lee RJ, Low PS (1995) Folate-mediated tumor cell targeting of liposome-entrapped doxorubicin in vitro. Biochim Biophys Acta 1233:134–144PubMedCrossRefGoogle Scholar
  126. Lee K, Hong K, Papahadjopoulos D (1992a) Recognition of liposomes by cells: In vitro binding and endocytosis mediated by specific lipid headgroups and surface charge density. Biochim Biophys Acta Biomembranes 1103:185–197CrossRefGoogle Scholar
  127. Lee K, Pitas RE, Papahadjopoulos D (1992b) Evidence that the scavenger receptor is not involved in the uptake of negatively charged liposomes by cells. Biochim Biophys Acta Biomembranes 1111:1–6CrossRefGoogle Scholar
  128. Lee KD, Nir S, Papahadjopoulos D (1993) Quantitative analysis of liposome-cell interactions in vitro: rate constants of binding and endocytosis with suspension and adherent J774 cells and human monocytes. Biochemistry 32:889–899PubMedCrossRefGoogle Scholar
  129. Lee HJ, Engelhardt B, Lesley J, Bickel U, Pardridge WM (2000) Targeting rat anti-mouse transferrin receptor monoclonal antibodies through blood-brain barrier in mouse. J Pharmacol Exp Ther 292:1048–1052PubMedGoogle Scholar
  130. Lee ES, Na K, Bae YH (2005) Doxorubicin loaded pH-sensitive polymeric micelles for reversal of resistant MCF-7 tumor. J Control Release 103:405–418PubMedCrossRefGoogle Scholar
  131. Lehr CM, Bouwstra J, Schacht E, Junginger H (1992) In vitro evaluation of mucoadhesive properties of chitosan and some other natural polymers. Int J Pharm 78:43–48CrossRefGoogle Scholar
  132. Lenaerts V, Nagelkerke JF, Van Berkel TJ, Couvreur P, Grislain L, Roland M, Speiser P (1984) In vivo uptake of polyisobutyl cyanoacrylate nanoparticles by rat liver Kupffer, endothelial, and parenchymal cells. J Pharm Sci 73:980–982PubMedCrossRefGoogle Scholar
  133. Leroux JC, Gravel P, Balant L, Volet B, Anner BM, Allémann E, Doelker E, Gurny R (1994) Internalization of poly(D, L-lactic acid) nanoparticles by isolated human leukocytes and analysis of plasma proteins adsorbed onto the particles. J Biomed Mater Res 28:471–481PubMedCrossRefGoogle Scholar
  134. Leroux J, De Jaeghere F, Anner B, Doelker E, Gurny R (1995) An investigation on the role of plasma and serum opsonins on the evternalization of biodegradable poly(D, L-lactic acid) nanoparticles by human monocytes. Life Sci 57:695–703PubMedCrossRefGoogle Scholar
  135. Lewin M, Carlesso N, Tung CH, Tang XW, Cory D, Scadden DT, Weissleder R (2000) Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat Biotechnol 18:410–414PubMedCrossRefGoogle Scholar
  136. Ma Z, Lim L (2003) Uptake of chitosan and associated insulin in Caco-2 cell monolayers: a comparison between chitosan molecules and chitosan nanoparticles. Pharm Res 20:1812–1819PubMedCrossRefGoogle Scholar
  137. Mao S, Germershaus O, Fischer D, Linn T, Schnepf R, Kissel T (2005) Uptake and transport of PEG-graft-trimethyl-chitosan copolymer-insulin nanocomplexes by epithelial cells. Pharm Res 22:2058–2068PubMedCrossRefGoogle Scholar
  138. Marsh M, Helenius A (2006) Virus entry: open sesame. Cell 124:729–740PubMedCrossRefGoogle Scholar
  139. Martina M, Nicolas V, Wilhelm C, Ménager C, Barratt G, Lesieur S (2007) The in vitro kinetics of the interactions between PEG-ylated magnetic-fluid-loaded liposomes and macrophages. Biomaterials 28:4143–4153PubMedCrossRefGoogle Scholar
  140. Maruyama K, Takizawa T, Yuda T, Kennel SJ, Huang L, Iwatsuru M (1995) Targetability of novel immunoliposomes modified with amphipathic poly(ethylene glycol)s conjugated at their distal terminals to monoclonal antibodies. Biochim Biophys Acta 1234:74–80PubMedCrossRefGoogle Scholar
  141. 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 413:177–180PubMedCrossRefGoogle Scholar
  142. Maruyama K, Ishida O, Takizawa T, Moribe K (1999) Possibility of active targeting to tumor tissues with liposomes. Adv Drug Deliv Rev 40:89–102PubMedCrossRefGoogle Scholar
  143. Matter K, Mellman I (1994) Mechanisms of cell polarity: sorting and transport in epithelial cells. Curr Opin Cell Biol 6:545–554PubMedCrossRefGoogle Scholar
  144. Mayor S, Pagano RE (2007) Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8:603–612PubMedCrossRefGoogle Scholar
  145. Merdan T, Kunath K, Fischer D, Kopecek J, Kissel T (2002) Intracellular processing of poly(ethylene imine)/ribozyme complexes can be observed in living cells by using confocal laser scanning microscopy and inhibitor experiments. Pharm Res 19:140–146PubMedCrossRefGoogle Scholar
  146. Mishra V, Mahor S, Rawat A, Gupta PN, Dubey P, Khatri K, Vyas SP (2006) Targeted brain delivery of AZT via transferrin anchored pegylated albumin nanoparticles. J Drug Target 14:45–53PubMedCrossRefGoogle Scholar
  147. Mo Y, Lim L (2005a) Preparation and in vitro anticancer activity of wheat germ agglutinin (WGA)-conjugated PLGA nanoparticles loaded with paclitaxel and isopropyl myristate. J Control Release 107:30–42PubMedCrossRefGoogle Scholar
  148. Mo Y, Lim L (2005b) Paclitaxel-loaded PLGA nanoparticles: potentiation of anticancer activity by surface conjugation with wheat germ agglutinin. J Control Release 108:244–262PubMedCrossRefGoogle Scholar
  149. Moghimi SM, Szebeni J (2003) Stealth liposomes and long circulating nanoparticles: critical issues in pharmacokinetics, opsonization and protein-binding properties. Prog Lipid Res 42:463–478PubMedCrossRefGoogle Scholar
  150. Moghimi SM, Muir IS, Illum L, Davis SS, Kolb-Bachofen V (1993) Coating particles with a block co-polymer (poloxamine-908) suppresses opsonization but permits the activity of dysopsonins in the serum. Biochim Biophys Acta 1179:157–165PubMedCrossRefGoogle Scholar
  151. Mosqueira VC, Legrand P, Gref R, Heurtault B, Appel M, Barratt G (1999) Interactions between a macrophage cell line (J774A1) and surface-modified poly (D, L-lactide) nanocapsules bearing poly(ethylene glycol). J Drug Target 7:65–78PubMedCrossRefGoogle Scholar
  152. Mukherjee S, Ghosh RN, Maxfield FR (1997) Endocytosis. Physiol Rev 77:759–803PubMedGoogle Scholar
  153. Muller CD, Schuber F (1989) Neo-mannosylated liposomes: synthesis and interaction with mouse Kupffer cells and resident peritoneal macrophages. Biochim Biophys Acta 986:97–105PubMedCrossRefGoogle Scholar
  154. Müller RH, Wallis KH, Tröster SD, Kreuter J (1992) In vitro characterization of poly(methyl-methaerylate) nanoparticles and correlation to their in vivo fate. J Control Release 20:237–246CrossRefGoogle Scholar
  155. Muro S, Wiewrodt R, Thomas A, Koniaris L, Albelda SM, Muzykantov VR, Koval M (2003) A novel endocytic pathway induced by clustering endothelial ICAM-1 or PECAM-1. J Cell Sci 116:1599–1609PubMedCrossRefGoogle Scholar
  156. Muro S, Dziubla T, Qiu W, Leferovich J, Cui X, Berk E, Muzykantov VR (2006a) Endothelial targeting of high-affinity multivalent polymer nanocarriers directed to intercellular adhesion molecule 1. J Pharmacol Exp Ther 317:1161–1169PubMedCrossRefGoogle Scholar
  157. Muro S, Schuchman EH, Muzykantov VR (2006b) Lysosomal enzyme delivery by ICAM-1-targeted nanocarriers bypassing glycosylation- and clathrin-dependent endocytosis. Mol Ther 13:135–141PubMedCrossRefGoogle Scholar
  158. Muro S, Garnacho C, Champion JA, Leferovich J, Gajewski C, Schuchman EH, Mitragotri S, Muzykantov VR (2008) Control of endothelial targeting and intracellular delivery of therapeutic enzymes by modulating the size and shape of ICAM-1-targeted carriers. Mol Ther 16:1450–1458PubMedPubMedCentralCrossRefGoogle Scholar
  159. Neu M, Fischer D, Kissel T (2005) Recent advances in rational gene transfer vector design based on poly(ethylene imine) and its derivatives. J Gene Med 7:992–1009PubMedCrossRefGoogle Scholar
  160. Norman ME, Williams P, Illum L (1992) Human serum albumin as a probe for surface conditioning (opsonization) of block copolymer-coated microspheres. Biomaterials 13:841–849PubMedCrossRefGoogle Scholar
  161. Oh P, McIntosh DP, Schnitzer JE (1998) Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J Cell Biol 141:101–114PubMedPubMedCentralCrossRefGoogle Scholar
  162. Olivier J, Fenart L, Chauvet R, Pariat C, Cecchelli R, Couet W (1999) Indirect evidence that drug brain targeting using polysorbate 80-coated polybutylcyanoacrylate nanoparticles is related to toxicity. Pharm Res 16:1836–1842PubMedCrossRefGoogle Scholar
  163. Owens D, Peppas N (2006) Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int J Pharm 307:93–102PubMedCrossRefGoogle Scholar
  164. Parton RG, Simons K (2007) The multiple faces of caveolae. Nat Rev Mol Cell Biol 8:185–194PubMedCrossRefGoogle Scholar
  165. Patel LN, Zaro JL, Shen W (2007) Cell penetrating peptides: intracellular pathways and pharmaceutical perspectives. Pharm Res 24:1977–1992PubMedCrossRefGoogle Scholar
  166. Pelkmans L, Helenius A (2002) Endocytosis via caveolae. Traffic 3:311–320PubMedCrossRefGoogle Scholar
  167. Ponchel G, Irache JM (1998) Specific and non-specific bioadhesive particulate systems for oral delivery to the gastrointestinal tract. Adv Drug Deliv Rev 34:191–219PubMedCrossRefGoogle Scholar
  168. Prabha S, Zhou W, Panyam J, Labhasetwar V (2002) Size-dependency of nanoparticle-mediated gene transfection: studies with fractionated nanoparticles. Int J Pharm 244:105–115PubMedCrossRefGoogle Scholar
  169. Qaddoumi M, Ueda H, Yang J, Davda J, Labhasetwar V, Lee V (2004) The characteristics and mechanisms of uptake of PLGA nanoparticles in rabbit conjunctival epithelial cell layers. Pharm Res 21:641–648PubMedCrossRefGoogle Scholar
  170. Qian ZM, Li H, Sun H, Ho K (2002) Targeted drug delivery via the transferrin receptor-mediated endocytosis pathway. Pharmacol Rev 54:561–587PubMedCrossRefGoogle Scholar
  171. Racoosin EL, Swanson JA (1992) M-CSF-induced macropinocytosis increases solute endocytosis but not receptor-mediated endocytosis in mouse macrophages. J Cell Sci 102(Pt 4):867–880PubMedGoogle Scholar
  172. Rahman YE, Cerny EA, Patel KR, Lau EH, Wright BJ (1982) Differential uptake of liposomes varying in size and lipid composition by parenchymal and kupffer cells of mouse liver. Life Sci 31:2061–2071PubMedCrossRefGoogle Scholar
  173. Raz A, Bucana C, Fogler WE, Poste G, Fidler IJ (1981) Biochemical, morphological, and ultrastructural studies on the uptake of liposomes by murine macrophages. Cancer Res 41:487–494PubMedGoogle Scholar
  174. Rejman J, Oberle V, Zuhorn IS, Hoekstra D (2004) Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J 377:159–169PubMedPubMedCentralCrossRefGoogle Scholar
  175. Rejman J, Bragonzi A, Conese M (2005) Role of clathrin- and caveolae-mediated endocytosis in gene transfer mediated by lipo- and polyplexes. Mol Ther 12:468–474PubMedCrossRefGoogle Scholar
  176. Rigotti A, Acton SL, Krieger M (1995) The class B scavenger receptors SR-BI and CD36 are receptors for anionic phospholipids. J Biol Chem 270:16221–16224PubMedCrossRefGoogle Scholar
  177. Roberts J, Quastel JH (1963) Particle uptake by polymorphonuclear leucocytes and ehrlich ascites-carcinoma cells. Biochem J 89:150–156PubMedPubMedCentralCrossRefGoogle Scholar
  178. Ropert C, Lavignon M, Dubernet C, Couvreur P, Malvy C (1992) Oligonucleotides encapsulated in pH sensitive liposomes are efficient toward Friend retrovirus. Biochem Biophys Res Commun 183:879–885PubMedCrossRefGoogle Scholar
  179. Roser M, Fischer D, Kissel T (1998) Surface-modified biodegradable albumin nano- and microspheres. II: effect of surface charges on in vitro phagocytosis and biodistribution in rats. Eur J Pharm Biopharm 46:255–263PubMedCrossRefGoogle Scholar
  180. Rothberg K, Ying Y, Kolhouse J, Kamen B, Anderson R (1990) The glycophospholipid-linked folate receptor internalizes folate without entering the clathrin-coated pit endocytic pathway. J Cell Biol 110:637–649PubMedCrossRefGoogle Scholar
  181. Rudt S, Muller R (1993) In-vitro phagocytosis assay of nanoparticles and microparticles by chemiluminescence.3. Uptake of differently sized surface-modified particles, and its correlation to particle properties and in-vivo distribution. Eur J Pharm Sci 1:31–39CrossRefGoogle Scholar
  182. Sabharanjak S, Mayor S (2004) Folate receptor endocytosis and trafficking. Adv Drug Deliv Rev 56:1099–1109PubMedCrossRefGoogle Scholar
  183. Sahoo SK, Labhasetwar V (2005) Enhanced antiproliferative activity of transferrin-conjugated paclitaxel-loaded nanoparticles is mediated via sustained intracellular drug retention. Mol Pharm 2:373–383PubMedCrossRefGoogle Scholar
  184. Schäfer V, von Briesen H, Andreesen R, Steffan A, Royer C, Tröster S, Kreuter J, Rübsamen-Waigmann H (1992) Phagocytosis of nanoparticles by human immunodeficiency virus (HlV)-infected macrophages: a possibility for antiviral drug targeting. Pharm Res 9:541–546PubMedCrossRefGoogle Scholar
  185. Scherphof G, Kamps J (1998) Receptor versus non-receptor mediated clearance of liposomes. Adv Drug Deliv Rev 32:81–97PubMedCrossRefGoogle Scholar
  186. Schiffelers RM, Koning GA, ten Hagen TLM, Fens MHAM, Schraa AJ, Janssen APCA, Kok RJ, Molema G, Storm G (2003) Anti-tumor efficacy of tumor vasculature-targeted liposomal doxorubicin. J Control Release 91:115–122PubMedCrossRefGoogle Scholar
  187. Schmid SL (1997) Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu Rev Biochem 66:511–548PubMedCrossRefGoogle Scholar
  188. Schnitzer JE (2001) Caveolae: from basic trafficking mechanisms to targeting transcytosis for tissue-specific drug and gene delivery in vivo. Adv Drug Deliv Rev 49:265–280PubMedCrossRefGoogle Scholar
  189. Schnitzer JE, Oh P, Pinney E, Allard J (1994) Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J Cell Biol 127:1217–1232PubMedCrossRefGoogle Scholar
  190. Schwendener R, Lagocki P, Rahman Y (1984) The effects of charge and size on the interaction of unilamellar liposomes with macrophages. Biochim Biophys Acta Biomembranes 772:93–101CrossRefGoogle Scholar
  191. Simberg D, Weisman S, Talmon Y, Barenholz Y (2004) DOTAP (and other cationic lipids): chemistry, biophysics, and transfection. Crit Rev Ther Drug Carrier Syst 21:257–317PubMedCrossRefGoogle Scholar
  192. Stella B, Arpicco S, Peracchia MT, Desmaële D, Hoebeke J, Renoir M, D’Angelo J, Cattel L, Couvreur P (2000) Design of folic acid-conjugated nanoparticles for drug targeting. J Pharm Sci 89:1452–1464PubMedCrossRefGoogle Scholar
  193. Straubinger RM, Düzgünes N, Papahadjopoulos D (1985) pH-sensitive liposomes mediate cytoplasmic delivery of encapsulated macromolecules. FEBS Lett 179:148–154PubMedCrossRefGoogle Scholar
  194. Strømhaug PE, Berg TO, Gjøen T, Seglen PO (1997) Differences between fluid-phase endocytosis (pinocytosis) and receptor-mediated endocytosis in isolated rat hepatocytes. Eur J Cell Biol 73:28–39PubMedGoogle Scholar
  195. Sun SX, Wirtz D (2006) Mechanics of enveloped virus entry into host cells. Biophys J 90:L10–L12PubMedCrossRefGoogle Scholar
  196. Sun W, Xie C, Wang H, Hu Y (2004) Specific role of polysorbate 80 coating on the targeting of nanoparticles to the brain. Biomaterials 25:3065–3071PubMedCrossRefGoogle Scholar
  197. Sun X, Rossin R, Turner JL, Becker ML, Joralemon MJ, Welch MJ, Wooley KL (2005) An assessment of the effects of shell cross-linked nanoparticle size, core composition, and surface PEGylation on in vivo biodistribution. Biomacromolecules 6:2541–2554PubMedPubMedCentralCrossRefGoogle Scholar
  198. Swanson J (1989) Phorbol esters stimulate macropinocytosis and solute flow through macrophages. J Cell Sci 94:135–142PubMedGoogle Scholar
  199. Swanson JA, Baer SC (1995) Phagocytosis by zippers and triggers. Trends Cell Biol 5:89–93PubMedCrossRefGoogle Scholar
  200. Swanson JA, Watts C (1995) Macropinocytosis. Trends Cell Biol 5:424–428PubMedCrossRefGoogle Scholar
  201. Tabata Y, Ikada Y (1988) Effect of the size and surface-charge of polymer microspheres on their phagocytosis by macrophage. Biomaterials 9:356–362PubMedCrossRefGoogle Scholar
  202. Tabata Y, Ikada Y (1990) Phagocytosis of polymer microspheres by macrophages. In: Boutevin B (ed) New polymer materials. Springer, Berlin, pp 107–141CrossRefGoogle Scholar
  203. Tkachenko AG, Xie H, Coleman D, Glomm W, Ryan J, Anderson MF, Franzen S, Feldheim DL (2003) Multifunctional gold nanoparticle-peptide complexes for nuclear targeting. J Am Chem Soc 125:4700–4701PubMedCrossRefGoogle Scholar
  204. Torchilin VP (2008) Tat peptide-mediated intracellular delivery of pharmaceutical nanocarriers. Adv Drug Deliv Rev 60:548–558PubMedCrossRefGoogle Scholar
  205. Torchilin VP, Berdichevsky VR, Barsukov AA, Smirnov VN (1980) Coating liposomes with protein decreases their capture by macrophages. FEBS Lett 111:184–188PubMedCrossRefGoogle Scholar
  206. van Oss CJ (1978) Phagocytosis as a surface phenomenon. Annu Rev Microbiol 32:19–39PubMedCrossRefGoogle Scholar
  207. Vasir JK, Labhasetwar V (2007) Biodegradable nanoparticles for cytosolic delivery of therapeutics. Adv Drug Deliv Rev 59:718–728PubMedPubMedCentralCrossRefGoogle Scholar
  208. Vasir JK, Labhasetwar V (2008) Quantification of the force of nanoparticle-cell membrane interactions and its influence on intracellular trafficking of nanoparticles. Biomaterials 29:4244–4252PubMedPubMedCentralCrossRefGoogle Scholar
  209. Verrecchia T, Huve P, Bazile D, Veillard M, Spenlehauer G, Couvreur P (1993) Adsorption/desorption of human serum albumin at the surface of poly(lactic acid) nanoparticles prepared by a solvent evaporation process. J Biomed Mater Res 27:1019–1028PubMedCrossRefGoogle Scholar
  210. Vĕtvicka V, Fornůsek L (1987) Polymer microbeads in immunology. Biomaterials 8:341–345PubMedCrossRefGoogle Scholar
  211. von Bonsdorff CH, Fuller SD, Simons K (1985) Apical and basolateral endocytosis in Madin-Darby canine kidney (MDCK) cells grown on nitrocellulose filters. EMBO J 4:2781–2792Google Scholar
  212. Vonarbourg A, Passirani C, Saulnier P, Benoit J (2006a) Parameters influencing the stealthiness of colloidal drug delivery systems. Biomaterials 27:4356–4373PubMedCrossRefGoogle Scholar
  213. Vonarbourg A, Passirani C, Saulnier P, Simard P, Leroux JC, Benoit JP (2006b) Evaluation of pegylated lipid nanocapsules versus complement system activation and macrophage uptake. J Biomed Mater Res A 78:620–628PubMedCrossRefGoogle Scholar
  214. Wang LH, Rothberg KG, Anderson RG (1993) Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 123:1107–1117PubMedCrossRefGoogle Scholar
  215. Weitman SD, Lark RH, Coney LR, Fort DW, Frasca V, Zurawski VR, Kamen BA (1992) Distribution of the folate receptor GP38 in normal and malignant cell lines and tissues. Cancer Res 52:3396–3401PubMedGoogle Scholar
  216. Xu Z, Gu W, Huang J, Sui H, Zhou Z, Yang Y, Yan Z, Li Y (2005) In vitro and in vivo evaluation of actively targetable nanoparticles for paclitaxel delivery. Int J Pharm 288:361–368PubMedCrossRefGoogle Scholar
  217. Yagi N, Yano Y, Hatanaka K, Yokoyama Y, Okuno H (2007) Synthesis and evaluation of a novel lipid-peptide conjugate for functionalized liposome. Bioorg Med Chem Lett 17:2590–2593PubMedCrossRefGoogle Scholar
  218. Yu B, Hailman E, Wright SD (1997) Lipopolysaccharide binding protein and soluble CD14 catalyze exchange of phospholipids. J Clin Investig 99:315–324PubMedPubMedCentralCrossRefGoogle Scholar
  219. Zauner W, Farrow NA, Haines AMR (2001) In vitro uptake of polystyrene microspheres: effect of particle size, cell line and cell density. J Control Release 71:39–51PubMedCrossRefGoogle Scholar
  220. Zhang K, Fang H, Chen Z, Taylor JA, Wooley KL (2008) Shape effects of nanoparticles conjugated with cell-penetrating peptides (HIV Tat PTD) on CHO cell uptake. Bioconjug Chem 19:1880–1887PubMedPubMedCentralCrossRefGoogle Scholar
  221. Zuhorn IS, Engberts JBFN, Hoekstra D (2007) Gene delivery by cationic lipid vectors: overcoming cellular barriers. Eur Biophys J 36:349–362PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Institut Galien Paris Sud, Faculty of PharmacyUMR CNRS 8612, Univ. Paris-Sud, Université Paris SaclayChâtenay-MalabryFrance

Personalised recommendations