Lysine-based surfactants in nanovesicle formulations: the role of cationic charge position and hydrophobicity in in vitro cytotoxicity and intracellular delivery

References

• Ahmad J, Ahamed M, Akhtar MJ, Alrokayan SA, Siddiqui M, Musarrat J, et al. 2012. Apoptosis induction by silica nanoparticles mediated through reactive oxygen species in human liver cell line HepG2. Toxicol Appl Pharmacol 259:160–168.
   PubMed Web of Science ®Google Scholar
• Arora S, Rajwade JM, Paknikar KM. 2012. Nanotoxicology and in vitro studies: the need of the hour. Toxicol Appl Pharmacol 258:151–165.
   PubMed Web of Science ®Google Scholar
• AshaRani PV, Mun GLK, Hande MP, Valiyaveettil S. 2009. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3:279–290.
   PubMed Web of Science ®Google Scholar
• Bai W, Zhang Z, Tian W, He X, Ma Y, Zhao Y, et al. 2009. Toxicity of zinc oxide nanoparticles to zebrafish embryo: a physicochemical study of toxicity mechanism. J Nanopart Res 12:1645–1654.
   Web of Science ®Google Scholar
• Bhattacharjee S, Ershov D, van der Gucht J, Alink GM, Rietjens IMCM, Zuilhof H, et al. 2013. Surface charge-specific cytotoxicity and cellular uptake of tri-block copolymer nanoparticles. Nanotoxicology 7:71–84.
   PubMed Web of Science ®Google Scholar
• Bombelli C, Caracciolo G, Di Profio P, Diociaiuti M, Luciani P, Mancini G, et al. 2005. Inclusion of a photosensitizer in liposomes formed by DMPC/Gemini Surfactant: Correlation between physicochemical and biological features of the complexes. J Med Chem 48:4882–4891.
   PubMed Web of Science ®Google Scholar
• Bradford MM. 1976. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254.
   PubMed Web of Science ®Google Scholar
• Cevc G. 2012. Rational design of new product candidates: the next generation of highly deformable bilayer vesicles for noninvasive, targeted therapy. J Control Release 160:135–146.
   PubMed Web of Science ®Google Scholar
• Chen R, Khormaee S, Eccleston ME, Slater NKH. 2009. The role of hydrophobic amino acid grafts in the enhancement of membrane-disruptive activity of pH-responsive pseudo-peptides. Biomaterials 30:1954–1961.
   PubMed Web of Science ®Google Scholar
• Chen T, McIntosh D, He Y, Kim J, Tirrell DA, Scherrer P, et al. 2004. Alkylated derivatives of poly(ethylacrylic acid) can be inserted into preformed liposomes and trigger pH-dependent intracellular delivery of liposomal contents. Mol Membr Biol 21:385–393.
   PubMed Web of Science ®Google Scholar
• Choi AO, Cho SJ, Desbarats J, Lovric J, Maysinger D. 2007. Quantum dot-induced cell death involves Fas upregulation and lipid peroxidation in human neuroblastoma cells. J Nanobiotechnol 5:1.
   PubMedGoogle Scholar
• Coldren B, van Zanten R, Mackel MJ, Zasadzinski JA. 2003. From vesicle size distributions to bilayer elasticity via cryo-transmission and freeze-fracture electron microscopy. Langmuir 19:5632–5639.
   Web of Science ®Google Scholar
• Collins TJ. 2007. ImageJ for microscopy. Biotechniques 43:S25–S30.
   PubMed Web of Science ®Google Scholar
• Colomer A, Pinazo A, Garcia T, Mitjans M, Vinardell P, Infante MR, et al. 2012. pH sensitive surfactants from lysine: assessment of their cytotoxicity and environmental behavior. Langmuir 28:5900–5912.
   PubMed Web of Science ®Google Scholar
• Dakwar GR, Hammad IA, Popov M, Linder C, Grinberg S, Heldman E, et al. 2012. Delivery of proteins to the brain by bolaamphiphilic nao-sized vesicles. J Control Release 160:315–321.
   PubMed Web of Science ®Google Scholar
• Di Guglielmo C, De Lapuente J, Porredon C, Ramos-López D, Sendra J, Borràs M. 2012. In vitro safety toxicology data for evaluation of gold nanoparticles–chronic cytotoxicity, genotoxicity and uptake. J Nanosci Nanotechnol 12:1–6.
   PubMed Web of Science ®Google Scholar
• Di Marzio L, Marianecci C, Petrone M, Rinaldi F, Carafa M. 2011. Novel pH-sensitive non-ionic surfactant vesicles: comparison between Tween 21 and Tween 20. Colloids Surf B Biointerfaces 82:18–24.
   PubMed Web of Science ®Google Scholar
• Dutta D, Sundaram SK, Teeguarden JG, Riley BJ, Fifield LS, Jacobs JM. 2007. Adsorbed proteins influence the biological activity and molecular targeting of nanomaterials. Toxicol Sci 100:303–315.
   PubMed Web of Science ®Google Scholar
• Eliyahu H, Servel N, Domb AJ, Barenholz Y. 2002. Lipoplex-induced hemagglutination: potential involvement in intravenous gene delivery. Gene Ther 9:850–858.
   PubMed Web of Science ®Google Scholar
• Fisher D, Li Y, Ahlemeyer B, Krieglstein J, Kissel T. 2003. In vitro cytotoxicity testing of polycations: influence of polymer structure on cell viability and hemolysis. Biomaterials 24:1121–1131.
   PubMed Web of Science ®Google Scholar
• Fröhlich E, Meindl C, Roblegg E, Griesbacher A, Pieber TR. 2012. Cytotoxicity of nanoparticles is influenced by size, proliferation and embryogenic origin of the cells used for testing. Nanotoxicology 6:424–439.
   PubMed Web of Science ®Google Scholar
• Gao F, Cai Y, Zhou J, Xie X, Ouyang W, Zhang Y, et al. 2010. Pullulan acetate coated magnetic nanoparticles for hyperthermia: preparation, characterization and in vitro experiments. Nano Res 3:23–31.
   Web of Science ®Google Scholar
• Hartung T. 2010. Food and thought....on alternative methods for nanoparticle safety testing. ALTEX 27:87–95.
   PubMedGoogle Scholar
• He M, Zhao Z, Yin L, Tang C, Yin C. 2009. Hyaluronic acid coated poly(butyl cyano-acrylate) nanoparticles as anticancer drug carriers. Int J Pharm 373:165–173.
   PubMed Web of Science ®Google Scholar
• Horie M, Kato H, Fujita K, Endoh S, Iwahashi H. 2012. In vitro evaluation of cellular response induced by manufactured nanoparticles. Chem Res Toxicol 25:605–619.
   PubMed Web of Science ®Google Scholar
• Hsin YH, Chen CF, Huang S, Shih TS, Lai PS, Chueh PJ. 2008. The apoptotic effect of nanosilver is mediated by a ROS- and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells. Toxicol Lett 179:130–139.
   PubMed Web of Science ®Google Scholar
• Hu Y, Litwin T, Nagaraja AR, Kwong B, Katz J, Watson N, et al. 2007. Cytosolic delivery of membrane-impermeable molecules in dendritic cells using pH-responsive core-shell nanoparticles. Nano Lett 7:3056–3064.
   PubMed Web of Science ®Google Scholar
• Infante MR, Pérez L, Morán MC, Pons R, Mitjans M, Vinardell MP, et al. 2010. Biocompatible surfactants from renewable hydrophiles. Eur J Lipid Sci Technol 112:110–121.
   Web of Science ®Google Scholar
• Jones CF, Grainger DW. 2009. In vitro assessments of nanomaterial toxicity. Adv Drug Deliv Rev 61:438–456.
   PubMed Web of Science ®Google Scholar
• Jones RA, Cheung CY, Black FE, Zia JK, Stayton PS, Hoffman AS, et al. 2003. Poly(2-alkylacrylic acid) polymers deliver molecules to the cytosol by pH-sensitive disruption of endosomal vesicles. Biochem J 372:65–75.
   PubMed Web of Science ®Google Scholar
• Kelsch A, Tomcin S, Rausch K, Barz M, Mailänder V, Schmidt M, et al. 2012. HPMA copolymers as surfactants in the preparation of biocompatible nanoparticles for biomedical application. Biomacromolecules 13:4179–4187.
   PubMed Web of Science ®Google Scholar
• Liang C-H, Chou T-H. 2009. Effect of chain length on physicochemical properties and cytotoxicity of cationic vesicles composed of phosphatidylcholines and dialkyldimethylammonium bromides. Chem Phys Lip 158:81–90.
   PubMed Web of Science ®Google Scholar
• Lundberg D, Faneca H, Morán MC, Lima MCP, Miguel MG, Lindman B. 2011. Inclusion of a single-tail amino acid-based amphiphile in a lipoplex formulation: effects on transfection efficiency and physicochemical properties. Mol Membr Biol 28:42–53.
   PubMed Web of Science ®Google Scholar
• Mahto SK, Park C, Yoon TH, Rhee SW. 2010. Assessment of cytocompatibility of surface-modified CdSe/ZnSe quantum dots for BALB/3T3 fibroblast cells. Toxicol in vitro 24:1070–1077.
   PubMed Web of Science ®Google Scholar
• Marquis BJ, Love SA, Braun KL, Haynes CL. 2009. Analytical methods to assess nanoparticle toxicity. Analyst 134:425–439.
   PubMed Web of Science ®Google Scholar
• Mehrotra A, Nagarwal RC, Pandit JK. 2011. Lomustine loaded chitosan nanoparticles: characterization and in-vitro cytotoxicity on human luna cancer cell line L132. Chem Pharm Bull 59:315–320.
   PubMed Web of Science ®Google Scholar
• Mei L, Zhang Y, Zheng Y, Tian G, Song C, Yang D, et al. 2009. A novel docetaxel-loaded poly (ε-caprolactone)/pluronic F68 nanoparticle overcoming multidrug resistance for breast cancer treatment. Nanoscale Res Lett 4:1530–1539.
   PubMed Web of Science ®Google Scholar
• Monteiro-Riviere NA, Inman AO, Zhang LW. 2009. Limitations and relative utility of screening assays to assess engineered nanoparticle toxicity in a human cell line. Toxicol Appl Pharmacol 234:222–235.
   PubMed Web of Science ®Google Scholar
• Monteiro-Riviere NA, Oldenburg SJ, Inman AO. 2010. Interactions of aluminum nanoparticles with human epidermal keratinocytes. J Appl Toxicol 30:276–285.
   PubMed Web of Science ®Google Scholar
• Morán MC, Infante MR, Miguel MG, Lindman B, Pons R. 2010. Novel Biocompatible DNA Gel Particles. Langmuir 26:10606–10613.
   PubMed Web of Science ®Google Scholar
• Müller RH, Jacobs C, Kayser O. 2011. Nanosuspensions as particulate drug formulations in therapy. Rationale for development and what we can expect for the future. Adv Drug Deliv Rev 23:3–19.
   Google Scholar
• Müller RH, Rühl D, Runge SA, Schulze-Forster K, Mehnert W. 1997. Cytotoxicity of solid lipid nanoparticles as a function of the lipid matrix and the surfactant. Pharm Res 14:458–462.
   PubMed Web of Science ®Google Scholar
• National Research Council. 2007. Toxicity testing in the twenty-first century: a vision and strategy. Washington, DC: National Academy Press.
   Google Scholar
• Nogueira DR, Mitjans M, Busquets MA, Pérez L, Vinardell MP. 2012b. Phospholipid bilayer perturbing-properties underlying lysis induced by pH-sensitive cationic lysine-based surfactants in biomembranes. Langmuir 28:11687–11698.
   PubMed Web of Science ®Google Scholar
• Nogueira DR, Mitjans M, Infante MR, Vinardell MP. 2011a. The role of counterions in the membrane-disruptive properties of pH-sensitive lysine-based surfactants. Acta Biomater 7:2846–2856.
   PubMed Web of Science ®Google Scholar
• Nogueira DR, Mitjans M, Infante MR, Vinardell MP. 2011b. Comparative sensitivity of tumor and non-tumor cell lines as a reliable approach for in vitro cytotoxicity screening of lysine-based surfactants with potential pharmaceutical applications. Int J Pharm 420:51–58.
   PubMedGoogle Scholar
• Nogueira DR, Mitjans M, Morán MC, Pérez L, Vinardell MP. 2012a. Membrane-destabilizing activity of pH-responsive cationic lysine-based surfactants: role of charge position and alkyl chain length. Amino Acids 43:1203–1215.
   PubMed Web of Science ®Google Scholar
• Nogueira DR, Morán MC, Mitjans M, Martínez V, Pérez L, Vinardell MP. 2013. New cationic nanovesicular systems containing lysine-based surfactants for topical administration: toxicity assessment using representative skin cell lines. Eur J Pharm Biopharm 83:33–43.
   PubMed Web of Science ®Google Scholar
• Ojogun VA, Lehmler H-J, Knutson BL. 2009. Cationic-anionic vesicle templating from fluorocarbon/fluorocarbon and hydrocarbon/fluorocarbon surfactants. J Colloid Interface Sci 338:82–91.
   PubMed Web of Science ®Google Scholar
• Paillard A, Hindré F, Vignes-Colombeix C, Benoit J-P, Garcion E. 2010. The importance of endo-lysosomal escape with lipid nanocapsules for drug subcellular bioavailability. Biomaterials 31:7542–7554.
   PubMed Web of Science ®Google Scholar
• Pan Y, Neuss S, Leifert A, Fischler M, Wen F, Simon U, et al. 2007. Size-dependent cytotoxicity of gold nanoparticles. Small 3:1941–1949.
   PubMed Web of Science ®Google Scholar
• Park JS, Han TH, Lee KY, Han SS, Hwang JJ, Moon DH, et al. 2006. N-acetyl histidine-conjugated glycol chitosan self-assembled nanoparticles for intracytoplasmic delivery of drugs: endocytosis, exocytosis and drug release. J Control Release 115:37–45.
   PubMed Web of Science ®Google Scholar
• Pérez L, Pinazo A, García MT, Lozano M, Manresa A, Angelet M, et al. 2009. Cationic surfactants from lysine: Synthesis, micellization and biological evaluation. Eur J Med Chem 44:1884–1892.
   PubMed Web of Science ®Google Scholar
• Pollock S, Antrobus R, Newton L, Kampa B, Rossa J, Latham S, et al. 2010. Uptake and trafficking of liposomes to the endoplasmic reticulum. FASEB J 24:1866–1878.
   PubMed Web of Science ®Google Scholar
• Ramezani M, Khoshhamdam M, Dehshahri A, Malaekeh-Nikouei B. 2009. The influence of size, lipid composition and bilayer fluidity of cationic liposomes on the transfection efficiency of nanolipoplexes. Colloids Surf B Biointerfaces 72:1–5.
   PubMed Web of Science ®Google Scholar
• Rasband W. 1997. ImageJ. National Institutes of Health, Bethesda, MD, USA. http://rsbweb.nih.gov/ij/index.html. Accessed on 9 January 2013.
   Google Scholar
• Robbens J, Vanparys C, Nobels I, Blust R, Hoecke KV, Janssen C, et al. 2010. Eco-, geno-, and human toxicology of bio-active nanoparticles for biomedical applications. Toxicology 269:170–181.
   PubMed Web of Science ®Google Scholar
• Salado J, Insausti M, Lezama L, Gil de Muro I, Moros M, Pelaz B, et al. 2012. Functionalized Fe3O4@Au superparamagnetic nanoparticles: in vitro bioactivity. Nanotechnology 23:315102.
   PubMed Web of Science ®Google Scholar
• Schöler N, Olbrich C, Tabatt K, Müller RH, Hahn H, Liesenfeld O. 2001. Surfactant, but not the size of solid lipid nanoparticles (SLN) influences viability and cytokine production of macrophages. Int J Pharm 221:57–67.
   PubMed Web of Science ®Google Scholar
• Simões S, Moreira JN, Fonseca C, Düzgünes N, Lima MC. 2004. On the formulation of pH-sensitive liposomes with long circulation times. Adv Drug Deliv Rev 56:947–965.
   PubMed Web of Science ®Google Scholar
• Singh NP, McCoy MT, Tice EL, Schneider EL. 1988. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191.
   PubMed Web of Science ®Google Scholar
• Sohaebuddin SK, Thevenot PT, Baker D, Eaton JW, Tang L. 2010. Nanomaterial cytotoxicity is composition, size, and cell type dependent. Part Fibre Toxicol 7:22.
   PubMed Web of Science ®Google Scholar
• Squier MKT, Cohen JJ. 2001. Standard quantitative assays for apoptosis. Mol Biotechnol 19:305–312.
   PubMed Web of Science ®Google Scholar
• Torchilin VP, Zhou F, Huang L. 1993. pH-sensitive liposomes. J Liposome Res 3:201–255.
   Google Scholar
• Uboldi C, Giudetti G, Broggi F, Gilliland D, Ponti J, Rossi F. 2012. Amorphous silica nanoparticles do not induce cytotoxicity, cell transformation or genotoxicity in Balb/3T3 mouse fibroblasts. Mutat Res 745:11–20.
   PubMed Web of Science ®Google Scholar
• Venkatesan P, Puvvada N, Dash R, Kumar BNP, Sarkar D, Azab B, et al. 2011. The potential of celecoxib-loaded hydroxyapatite-chitosan nanocomposite for the treatment of colon cancer. Biomaterials 32:3794–3806.
   PubMed Web of Science ®Google Scholar
• Xia T, Kovochich M, Liong M, Zink JI, Nel AE. 2008. Cationic polystyrene nanosphere toxicity depends on cell-specific endocytic and mitochondrial injury pathways. ACSNano 2:85–96.
   PubMed Web of Science ®Google Scholar
• Yang H, Liu C, Yang D, Zhang H, Xi Z. 2009. Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by four typical nanomaterilas: the role of particle size, shape and composition. J Appl Toxicol 29:69–78.
   PubMed Web of Science ®Google Scholar
• Yessine MA, Lafleur M, Meier C, Petereit HU, Leroux JC. 2003. Characterization of the membrane-destabilization properties of different pH-sensitive methacrylic acid copolymers. Biochim Biophys Acta 1613:28–38.
   PubMed Web of Science ®Google Scholar
• Zhang SB, Xu YM, Wang B, Qiao WH, Liu DL, Li ZS. 2004. Cationic compounds used in lipoplexes and polyplexes for gene delivery. J Control Release 100:165–180.
   PubMed Web of Science ®Google Scholar