Size-Dependent Interactions of Lipid-Coated Gold Nanoparticles: Developing a Better Mechanistic Understanding Through Model Cell Membranes and in vivo Toxicity

References

• Bobo D, Robinson KJ, Islam J, Thurecht KJ, Corrie SR. Nanoparticle-based medicines: a review of FDA-approved materials and clinical trials to date. Pharm Res. 2016;33(10):2373–2387. doi:10.1007/s11095-016-1958-527299311
   PubMed Web of Science ®Google Scholar
• Caster JM, Patel AN, Zhang T, Wang A. Investigational nanomedicines in 2016: a review of nanotherapeutics currently undergoing clinical trials. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2017;9(1):e1416.
   Web of Science ®Google Scholar
• Min Y, Caster JM, Eblan MJ, Wang AZ. Clinical translation of nanomedicine. Chem Rev. 2015;115(19):11147–11190. doi:10.1021/acs.chemrev.5b0011626088284
   PubMed Web of Science ®Google Scholar
• Adnan NN, Cheng Y, Ong NM, et al. Effect of gold nanoparticle shapes for phototherapy and drug delivery. Polym Chem. 2016;7(16):2888–2903. doi:10.1039/C6PY00465B
   Web of Science ®Google Scholar
• Von Maltzahn G, Park J-H, Agrawal A, et al. Computationally guided photothermal tumor therapy using long-circulating gold nanorod antennas. Cancer Res. 2009;69(9):3892–3900. doi:10.1158/0008-5472.CAN-08-424219366797
   PubMed Web of Science ®Google Scholar
• Huang X, Jain PK, El-Sayed IH, El-Sayed MA. Plasmonic photothermal therapy (PPTT) using gold nanoparticles. Lasers Med Sci. 2008;23(3):217. doi:10.1007/s10103-007-0470-x17674122
   PubMed Web of Science ®Google Scholar
• El-Sayed IH, Huang X, El-Sayed MA. Selective laser photo-thermal therapy of epithelial carcinoma using anti-EGFR antibody conjugated gold nanoparticles. Cancer Lett. 2006;239(1):129–135. doi:10.1016/j.canlet.2005.07.03516198049
   PubMed Web of Science ®Google Scholar
• Hainfeld JF, Slatkin DN, Smilowitz HM. The use of gold nanoparticles to enhance radiotherapy in mice. Phys Med Biol. 2004;49(18):N309. doi:10.1088/0031-9155/49/18/N0315509078
   PubMed Web of Science ®Google Scholar
• Park H, Lim D-J, Vines JB, Yoon J-H, Ryu N-E. Gold Nanoparticles for Photothermal Cancer Therapy. Front Chem. 2019;7:167. doi:10.3389/fchem.2019.0016731024882
   PubMed Web of Science ®Google Scholar
• Paciotti GF, Myer L, Weinreich D, et al. Colloidal gold: a novel nanoparticle vector for tumor directed drug delivery. Drug Deliv. 2004;11(3):169–183. doi:10.1080/1071754049043389515204636
   PubMed Web of Science ®Google Scholar
• Champion JA, Katare YK, Mitragotri S. Particle shape: a new design parameter for micro-and nanoscale drug delivery carriers. J Controlled Release. 2007;121(1–2):3–9.
   PubMed Web of Science ®Google Scholar
• Men W, Zhu P, Dong S, et al. Fabrication of dual ph/redox-responsive lipid-polymer hybrid nanoparticles for anticancer drug delivery and controlled release. Int J Nanomedicine. 2019;14:8001. doi:10.2147/IJN.S22679831632014
   PubMed Web of Science ®Google Scholar
• Dreaden EC, Mackey MA, Huang X, Kang B, El-Sayed MA. Beating cancer in multiple ways using nanogold. Chem Soc Rev. 2011;40(7):3391–3404. doi:10.1039/c0cs00180e21629885
   PubMed Web of Science ®Google Scholar
• Conde J, Ambrosone A, Sanz V, et al. Design of multifunctional gold nanoparticles for in vitro and in vivo gene silencing. ACS Nano. 2012;6(9):8316–8324. doi:10.1021/nn303022322882598
   PubMed Web of Science ®Google Scholar
• Min Y, Mao CQ, Chen S, Ma G, Wang J, Liu Y. Combating the drug resistance of cisplatin using a platinum prodrug based delivery system. Angew Chem Int Ed. 2012;51(27):6742–6747. doi:10.1002/anie.201201562
   PubMed Web of Science ®Google Scholar
• Wang F, Wang Y-C, Dou S, Xiong M-H, Sun T-M, Wang J. Doxorubicin-tethered responsive gold nanoparticles facilitate intracellular drug delivery for overcoming multidrug resistance in cancer cells. ACS Nano. 2011;5(5):3679–3692. doi:10.1021/nn200007z21462992
   PubMed Web of Science ®Google Scholar
• Barenholz YC. Doxil®—the first FDA-approved nano-drug: lessons learned. J Controlled Release. 2012;160(2):117–134. doi:10.1016/j.jconrel.2012.03.020
   PubMed Web of Science ®Google Scholar
• Connor EE, Mwamuka J, Gole A, Murphy CJ, Wyatt MD. Gold nanoparticles are taken up by human cells but do not cause acute cytotoxicity. Small. 2005;1(3):325–327. doi:10.1002/smll.20040009317193451
   PubMed Web of Science ®Google Scholar
• Elci SG, Jiang Y, Yan B, et al. Surface charge controls the suborgan biodistributions of gold nanoparticles. ACS Nano. 2016;10(5):5536–5542. doi:10.1021/acsnano.6b0208627164169
   PubMed Web of Science ®Google Scholar
• Wang J-Y, Chen J, Yang J, et al. Effects of surface charges of gold nanoclusters on long-term in vivo biodistribution, toxicity, and cancer radiation therapy. Int J Nanomedicine. 2016;11:3475. doi:10.2147/IJN.S10607327555769
   PubMed Web of Science ®Google Scholar
• Harper B, Sinche F, Ho Wu R, et al. The impact of surface ligands and synthesis method on the toxicity of glutathione-coated gold nanoparticles. Nanomaterials. 2014;4(2):355–371. doi:10.3390/nano402035526213631
   PubMed Web of Science ®Google Scholar
• Patlolla AK, Kumari SA, Tchounwou PB. A comparison of poly-ethylene-glycol-coated and uncoated gold nanoparticle-mediated hepatotoxicity and oxidative stress in Sprague Dawley rats. Int J Nanomedicine. 2019;14:639. doi:10.2147/IJN.S18557430697047
   PubMed Web of Science ®Google Scholar
• Carnovale C, Bryant G, Shukla R, Bansal V. Identifying trends in gold nanoparticle toxicity and uptake: size, shape, capping ligand, and biological corona. ACS Omega. 2019;4(1):242–256. doi:10.1021/acsomega.8b03227
   Web of Science ®Google Scholar
• Pan Y, Neuss S, Leifert A, et al. Size‐dependent cytotoxicity of gold nanoparticles. Small. 2007;3(11):1941–1949. doi:10.1002/smll.20070037817963284
   PubMed Web of Science ®Google Scholar
• Coradeghini R, Gioria S, Garcia CP, et al. Size-dependent toxicity and cell interaction mechanisms of gold nanoparticles on mouse fibroblasts. Toxicol Lett. 2013;217(3):205–216. doi:10.1016/j.toxlet.2012.11.02223246733
   PubMed Web of Science ®Google Scholar
• Li X, Hu Z, Ma J, et al. The systematic evaluation of size-dependent toxicity and multi-time biodistribution of gold nanoparticles. Colloids Surf B Biointerfaces. 2018;167:260–266. doi:10.1016/j.colsurfb.2018.04.00529677597
   PubMed Web of Science ®Google Scholar
• Mironava T, Hadjiargyrou M, Simon M, Jurukovski V, Rafailovich MH. Gold nanoparticles cellular toxicity and recovery: effect of size, concentration and exposure time. Nanotoxicology. 2010;4(1):120–137. doi:10.3109/1743539090347146320795906
   PubMed Web of Science ®Google Scholar
• Hou W-C, Moghadam BY, Corredor C, Westerhoff P, Posner JD. Distribution of functionalized gold nanoparticles between water and lipid bilayers as model cell membranes. Environ Sci Technol. 2012;46(3):1869–1876. doi:10.1021/es203661k22242832
   PubMed Web of Science ®Google Scholar
• Simko M, Nosske D, Kreyling WG. Metrics, dose, and dose concept: the need for a proper dose concept in the risk assessment of nanoparticles. Int J Environ Res Public Health. 2014;11(4):4026–4048. doi:10.3390/ijerph11040402624736686
   PubMed Web of Science ®Google Scholar
• Rushton EK, Jiang J, Leonard SS, et al. Concept of assessing nanoparticle hazards considering nanoparticle dosemetric and chemical/biological response metrics. J Toxicol Environ Health A. 2010;73(5):445–461. doi:10.1080/1528739090348942220155585
   PubMed Web of Science ®Google Scholar
• Wittmaack K. In search of the most relevant parameter for quantifying lung inflammatory response to nanoparticle exposure: particle number, surface area, or what? Environ Health Perspect. 2007;115(2):187–194. doi:10.1289/ehp.925417384763
   PubMed Web of Science ®Google Scholar
• Brockman H. Lipid monolayers: why use half a membrane to characterize protein-membrane interactions? Curr Opin Struct Biol. 1999;9(4):438–443. doi:10.1016/S0959-440X(99)80061-X10449364
   PubMed Web of Science ®Google Scholar
• Franz J, Lelle M, Peneva K, Bonn M, Weidner T. SAP (E)–A cell-penetrating polyproline helix at lipid interfaces. Biochim Et Biophys Acta (BBA) Biomembr. 2016;1858(9):2028–2034. doi:10.1016/j.bbamem.2016.05.021
   PubMed Web of Science ®Google Scholar
• Franz J, van Zadel M-J, Weidner T. A trough for improved SFG spectroscopy of lipid monolayers. Rev Sci Instrum. 2017;88(5):053106. doi:10.1063/1.498205028571440
   PubMed Web of Science ®Google Scholar
• Golbek TW, Franz J, Elliott Fowler J, Schilke KF, Weidner T, Baio JE. Identifying the selectivity of antimicrobial peptides to cell membranes by sum frequency generation spectroscopy. Biointerphases. 2017;12(2):02D406. doi:10.1116/1.4982710
   PubMed Web of Science ®Google Scholar
• Liljeblad JF, Bulone V, Rutland MW, Johnson CM. Supported phospholipid monolayers. The molecular structure investigated by vibrational sum frequency spectroscopy. J Phys Chem C. 2011;115(21):10617–10629. doi:10.1021/jp111587e
   Web of Science ®Google Scholar
• Liljeblad JF, Bulone V, Tyrode E, Rutland MW, Johnson CM. Phospholipid monolayers probed by vibrational sum frequency spectroscopy: instability of unsaturated phospholipids. Biophys J. 2010;98(10):L50–L52. doi:10.1016/j.bpj.2010.02.00920483309
   PubMed Web of Science ®Google Scholar
• Ma G, Allen HC. DPPC Langmuir monolayer at the air− water interface: probing the tail and head groups by vibrational sum frequency generation spectroscopy. Langmuir. 2006;22(12):5341–5349. doi:10.1021/la053522716732662
   PubMed Web of Science ®Google Scholar
• Maget-Dana R. The monolayer technique: a potent tool for studying the interfacial properties of antimicrobial and membrane-lytic peptides and their interactions with lipid membranes. Biochim Et Biophys Acta (BBA) Biomembr. 1999;1462(1–2):109–140. doi:10.1016/S0005-2736(99)00203-5
   PubMed Web of Science ®Google Scholar
• Mauri S, Pandey R, Rzeznicka I, Lu H, Bonn M, Weidner T. Bovine and human insulin adsorption at lipid monolayers: a comparison. Front Physics. 2015;3:51. doi:10.3389/fphy.2015.00051
   Google Scholar
• Watry MR, Tarbuck TL, Richmond GL. Vibrational sum-frequency studies of a series of phospholipid monolayers and the associated water structure at the vapor/water interface. J Phys Chem B. 2003;107(2):512–518. doi:10.1021/jp0216878
   Web of Science ®Google Scholar
• Ahn D, Dhinojwala A. Sum frequency generation vibrational spectroscopy of silicone surfaces & interfaces In: Silicone Surface Science. Springer; 2012:23–58.
   Google Scholar
• Shen Y-R. The principles of nonlinear optics. N Y Wiley Intersci. 1984;575(p):1984.
   Google Scholar
• Wang H-F, Velarde L, Gan W, Fu L. Quantitative sum-frequency generation vibrational spectroscopy of molecular surfaces and interfaces: lineshape, polarization, and orientation. Annu Rev Phys Chem. 2015;66(1):189–216. doi:10.1146/annurev-physchem-040214-12132225493712
   PubMedGoogle Scholar
• Wang H-F, Gan W, Lu R, Rao Y, Wu B-H. Quantitative spectral and orientational analysis in surface sum frequency generation vibrational spectroscopy (SFG-VS). Int Rev Phys Chem. 2005;24(2):191–256. doi:10.1080/01442350500225894
   Web of Science ®Google Scholar
• Zhuang X, Miranda P, Kim D, Shen Y. Mapping molecular orientation and conformation at interfaces by surface nonlinear optics. Phys Rev B. 1999;59(19):12632. doi:10.1103/PhysRevB.59.12632
   Web of Science ®Google Scholar
• Ding B, Chen Z. Molecular interactions between cell penetrating peptide Pep-1 and model cell membranes. J Phys Chem B. 2012;116(8):2545–2552. doi:10.1021/jp209604m22292835
   PubMed Web of Science ®Google Scholar
• Liu Y, Jasensky J, Chen Z. Molecular interactions of proteins and peptides at interfaces studied by sum frequency generation vibrational spectroscopy. Langmuir. 2011;28(4):2113–2121. doi:10.1021/la203823t22171656
   PubMed Web of Science ®Google Scholar
• Rzeznicka I, Pandey R, Schleeger M, Bonn M, Weidner T. Formation of lysozyme oligomers at model cell membranes monitored with sum frequency generation spectroscopy. Langmuir. 2014;30(26):7736–7744. doi:10.1021/la501022724941083
   PubMed Web of Science ®Google Scholar
• Schach DK, Rock W, Franz J, Bonn M, Parekh SH, Weidner T. Reversible activation of a cell-penetrating peptide in a membrane environment. J Am Chem Soc. 2015;137(38):12199–12202. doi:10.1021/jacs.5b0672026335659
   PubMed Web of Science ®Google Scholar
• Thennarasu S, Huang R, Lee D-K, et al. Limiting an antimicrobial peptide to the lipid− water interface enhances its bacterial membrane selectivity: a case study of MSI-367. Biochemistry. 2010;49(50):10595–10605. doi:10.1021/bi101394r21062093
   PubMed Web of Science ®Google Scholar
• Wang J, Buck SM, Chen Z. Sum frequency generation vibrational spectroscopy studies on protein adsorption. J Phys Chem B. 2002;106(44):11666–11672. doi:10.1021/jp021363j
   Web of Science ®Google Scholar
• Ye S, Nguyen KT, Le Clair SV, Chen Z. In situ molecular level studies on membrane related peptides and proteins in real time using sum frequency generation vibrational spectroscopy. J Struct Biol. 2009;168(1):61–77. doi:10.1016/j.jsb.2009.03.00619306928
   PubMed Web of Science ®Google Scholar
• Hu P, Qian W, Liu B, Pichan C, Chen Z. Molecular interactions between gold nanoparticles and model cell membranes: a study of nanoparticle surface charge effect. J Phys Chem C. 2016;120(39):22718–22729. doi:10.1021/acs.jpcc.6b07565
   Web of Science ®Google Scholar
• Toledo-Fuentes X, Lis D, Cecchet F. Structural changes to lipid bilayers and their surrounding water upon interaction with functionalized gold nanoparticles. J Phys Chem C. 2016;120(38):21399–21409. doi:10.1021/acs.jpcc.6b05460
   Web of Science ®Google Scholar
• Harper B, Thomas D, Chikkagoudar S, et al. Comparative hazard analysis and toxicological modeling of diverse nanomaterials using the embryonic zebrafish (EZ) metric of toxicity. J Nanopart Res. 2015;17(6):250. doi:10.1007/s11051-015-3051-026069453
   PubMed Web of Science ®Google Scholar
• Harper S, Usenko C, Hutchison J, Maddux B, Tanguay R. In vivo biodistribution and toxicity depends on nanomaterial composition, size, surface functionalisation and route of exposure. J Exp Nanosci. 2008;3(3):195–206. doi:10.1080/17458080802378953
   Web of Science ®Google Scholar
• Harper SL, Carriere JL, Miller JM, Hutchison JE, Maddux BLS, Tanguay RL. Systematic evaluation of nanomaterial toxicity: utility of standardized materials and rapid assays. ACS Nano. 2011;5(6):4688–4697. doi:10.1021/nn200546k21609003
   PubMed Web of Science ®Google Scholar
• Harper SL, Dahl JA, Maddux BL, Tanguay RL, Hutchison JE. Proactively designing nanomaterials to enhance performance and minimise hazard. Int J Nanotechnol. 2008;5(1):124–142. doi:10.1504/IJNT.2008.016552
   Web of Science ®Google Scholar
• Lin S, Zhao Y, Ji Z, et al. Zebrafish high throughput screening to study the impact of dissolvable metal oxide nanoparticles on the hatching enzyme, ZHE1. Small. 2013;9(9–10):1776–1785. doi:10.1002/smll.20120212823180726
   PubMed Web of Science ®Google Scholar
• Lin S, Zhao Y, Nel AE, Lin S. Zebrafish: an in vivo model for nano EHS studies. Small. 2013;9(9–10):1608–1618. doi:10.1002/smll.20120211523208995
   PubMed Web of Science ®Google Scholar
• Hill AJ, Teraoka H, Heideman W, Peterson RE. Zebrafish as a Model vertebrate for investigating chemical toxicity. Toxicol Sci. 2005;86(1):6–19. doi:10.1093/toxsci/kfi11015703261
   PubMed Web of Science ®Google Scholar
• Howe K, Clark MD, Torroja CF, et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature. 2013;496(7446):498–503. doi:10.1038/nature1211123594743
   PubMed Web of Science ®Google Scholar
• Tropepe V, Sive HL. Can zebrafish be used as a model to study the neurodevelopmental causes of autism? Genes Brain Behav. 2003;2(5):268–281. doi:10.1034/j.1601-183X.2003.00038.x14606692
   PubMed Web of Science ®Google Scholar
• Zon LI, Peterson RT. In vivo drug discovery in the zebrafish. Nat Rev Drug Discov. 2005;4(1):35–44. doi:10.1038/nrd160615688071
   PubMed Web of Science ®Google Scholar
• Holman J, Davies PB, Nishida T, Ye S, Neivandt DJ. Sum Frequency Generation from Langmuir− Blodgett Multilayer Films on Metal and Dielectric Substrates. ACS Publications; 2005.
   Google Scholar
• Weidner T, Apte JS, Gamble LJ, Castner DG. Probing the orientation and conformation of α-helix and β-strand model peptides on self-assembled monolayers using sum frequency generation and NEXAFS spectroscopy. Langmuir. 2009;26(5):3433–3440. doi:10.1021/la903267x
   Web of Science ®Google Scholar
• Ingólfsson HI, Melo MN, Van Eerden FJ, et al. Lipid organization of the plasma membrane. J Am Chem Soc. 2014;136(41):14554–14559. doi:10.1021/ja507832e25229711
   PubMed Web of Science ®Google Scholar
• Roke S, Schins J, Müller M, Bonn M. Vibrational spectroscopic investigation of the phase diagram of a biomimetic lipid monolayer. Phys Rev Lett. 2003;90(12):128101. doi:10.1103/PhysRevLett.90.12810112688904
   PubMed Web of Science ®Google Scholar
• Westerfield M, The zebrafish book: a guide for the laboratory use of zebrafish. http://zfin.org/zf_info/zfbook/zfbk.html Accessed 527, 2020 2000.
   Google Scholar
• Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn. 1995;203(3):253–310. doi:10.1002/aja.10020303028589427
   PubMed Web of Science ®Google Scholar
• Usenko CY, Harper SL, Tanguay RL. Fullerene C60 exposure elicits an oxidative stress response in embryonic zebrafish. Toxicol Appl Pharmacol. 2008;229(1):44–55. doi:10.1016/j.taap.2007.12.03018299140
   PubMed Web of Science ®Google Scholar
• Henn K, Braunbeck T. Dechorionation as a tool to improve the fish embryo toxicity test (FET) with the zebrafish (Danio rerio). Comp Biochem Physiol Part C. 2011;153(1):91–98.
   PubMed Web of Science ®Google Scholar
• Kim K-T, Tanguay RL. The role of chorion on toxicity of silver nanoparticles in the embryonic zebrafish assay. Environ Health Toxicol. 2014;29:e2014021. doi:10.5620/eht.e201402125518841
   PubMedGoogle Scholar
• Mackiewicz MR, Hodges HL, Reed SM. C-reactive protein induced rearrangement of phosphatidylcholine on nanoparticle mimics of lipoprotein particles. J Phys Chem B. 2010;114(16):5556–5562. doi:10.1021/jp911617q20364851
   PubMed Web of Science ®Google Scholar
• Sitaula S, Mackiewicz MR, Reed SM, Gold nanoparticles become stable to cyanide etch when coated with hybrid lipid bilayers. Chem Commun. 2008;26:3013–3015. doi:10.1039/b801525b
   PubMed Web of Science ®Google Scholar
• Yang JA, Murphy CJ. Evidence for patchy lipid layers on gold nanoparticle surfaces. Langmuir. 2012;28(12):5404–5416. doi:10.1021/la300325p22352432
   PubMed Web of Science ®Google Scholar
• Templeton AC, Hostetler MJ, Kraft CT, Murray RW. Reactivity of monolayer-protected gold cluster molecules: steric effects. J Am Chem Soc. 1998;120(8):1906–1911.
   Web of Science ®Google Scholar
• Kreibig U, Genzel L. Optical absorption of small metallic particles. Surf Sci. 1985;156:678–700. doi:10.1016/0039-6028(85)90239-0
   Web of Science ®Google Scholar
• Storhoff JJ, Lazarides AA, Mucic RC, Mirkin CA, Letsinger RL, Schatz GC. What controls the optical properties of DNA-linked gold nanoparticle assemblies? J Am Chem Soc. 2000;122(19):4640–4650. doi:10.1021/ja993825l
   Web of Science ®Google Scholar
• Engstrom AM, Wu H, Mackiewicz MR, Harper SL. Hybrid lipid-coated silver nanoparticles with long-chain hydrophobic thiol surface coatings show decreased toxicity compared to those without robust surface coatings. Int J Eng Res Appl. 2020;10:15677–15693.
   Google Scholar
• Manshian BB, Pokhrel S, Mädler L, Soenen SJ. The impact of nanoparticle-driven lysosomal alkalinization on cellular functionality. J Nanobiotechnology. 2018;16(1):85. doi:10.1186/s12951-018-0413-730382919
   PubMedGoogle Scholar
• Schutz I, Lopez-Hernandez T, Gao Q, et al. Lysosomal dysfunction caused by cellular accumulation of silica nanoparticles. J Biol Chem. 2016;291(27):14170–14184. doi:10.1074/jbc.M115.71094727226546
   PubMed Web of Science ®Google Scholar
• Martinez Legaspi S, Segatori L. Aggregation behavior of nanoparticle-peptide systems affects autophagy. Bioconjug Chem. 2019;30(7):1986–1997. doi:10.1021/acs.bioconjchem.9b0026631268689
   PubMed Web of Science ®Google Scholar
• Rathore B, Sunwoo K, Jangili P, et al. Nanomaterial designing strategies related to cell lysosome and their biomedical applications: A review. Biomaterials. 2019;211:25–47. doi:10.1016/j.biomaterials.2019.05.00231078050
   PubMed Web of Science ®Google Scholar
• Sovago M, Wurpel GW, Smits M, Müller M, Bonn M. Calcium-induced phospholipid ordering depends on surface pressure. J Am Chem Soc. 2007;129(36):11079–11084. doi:10.1021/ja071189i17696532
   PubMed Web of Science ®Google Scholar
• Hu P, Zhang X, Zhang C, Chen Z. Molecular interactions between gold nanoparticles and model cell membranes. Phys Chem Chem Phys. 2015;17(15):9873–9884. doi:10.1039/C5CP00477B25776800
   PubMed Web of Science ®Google Scholar
• Liu J, Conboy JC. 1, 2-diacyl-phosphatidylcholine flip-flop measured directly by sum-frequency vibrational spectroscopy. Biophys J. 2005;89(4):2522–2532. doi:10.1529/biophysj.105.06567216085770
   PubMed Web of Science ®Google Scholar
• Yi X, Shi X, Gao H. Cellular uptake of elastic nanoparticles. Phys Rev Lett. 2011;107(9):098101. doi:10.1103/PhysRevLett.107.09810121929271
   PubMed Web of Science ®Google Scholar
• Bahrami AH, Raatz M, Agudo-Canalejo J, et al. Wrapping of nanoparticles by membranes. Adv Colloid Interface Sci. 2014;208:214–224. doi:10.1016/j.cis.2014.02.01224703299
   PubMed Web of Science ®Google Scholar
• Hu P, Zhang X, Li Y, Pichan C, Chen Z. Molecular interactions between silver nanoparticles and model cell membranes. Top Catal. 2018;61(9–11):1148–1162. doi:10.1007/s11244-018-0926-1
   Web of Science ®Google Scholar
• Harper KL, Allen HC. Competition between DPPC and SDS at the Air− Aqueous Interface. Langmuir. 2007;23(17):8925–8931. doi:10.1021/la700697417629307
   PubMed Web of Science ®Google Scholar
• Tyrode E, Hedberg J. A comparative study of the CD and CH stretching spectral regions of typical surfactants systems using VSFS: orientation analysis of the terminal CH3 and CD3 groups. J Phys Chem C. 2011;116(1):1080–1091. doi:10.1021/jp210013g
   Web of Science ®Google Scholar
• Van Lehn RC, Atukorale PU, Carney RP, et al. Effect of particle diameter and surface composition on the spontaneous fusion of monolayer-protected gold nanoparticles with lipid bilayers. Nano Lett. 2013;13(9):4060–4067. doi:10.1021/nl401365n23915118
   PubMed Web of Science ®Google Scholar
• Baio J, Weidner T, Brison J, Graham D, Gamble LJ, Castner DG. Amine terminated SAMs: investigating why oxygen is present in these films. J Electron Spectros Relat Phenomena. 2009;172(1–3):2–8. doi:10.1016/j.elspec.2009.02.00820161353
   PubMed Web of Science ®Google Scholar
• Fowler JE, Kleinteich T, Franz J, et al. Surface chemistry of the frog sticky-tongue mechanism. Biointerphases. 2018;13(6):06E408. doi:10.1116/1.5052651
   PubMed Web of Science ®Google Scholar
• Dominguez H, Smondyrev A, Berkowitz M. Computer simulations of phosphatidylcholine monolayers at air/water and CCl4/water interfaces. J Phys Chem B. 1999;103(44):9582–9588. doi:10.1021/jp991352z
   Web of Science ®Google Scholar
• Mohwald H. Phospholipid and phospholipid-protein monolayers at the air/water interface. Annu Rev Phys Chem. 1990;41(1):441–476. doi:10.1146/annurev.pc.41.100190.0023012257038
   PubMedGoogle Scholar
• Li Y, Gu N. Thermodynamics of charged nanoparticle adsorption on charge-neutral membranes: a simulation study. J Phys Chem B. 2010;114(8):2749–2754. doi:10.1021/jp904550b20146444
   PubMed Web of Science ®Google Scholar
• Reif DM, Truong L, Mandrell D, Marvel S, Zhang G, Tanguay RL. High-throughput characterization of chemical-associated embryonic behavioral changes predicts teratogenic outcomes. Arch Toxicol. 2016;90(6):1459–1470. doi:10.1007/s00204-015-1554-126126630
   PubMed Web of Science ®Google Scholar
• Roiter Y, Ornatska M, Rammohan AR, Balakrishnan J, Heine DR, Minko S. Interaction of nanoparticles with lipid membrane. Nano Lett. 2008;8(3):941–944. doi:10.1021/nl080080l18254602
   PubMed Web of Science ®Google Scholar