Blood protein and blood cell interactions with gold nanoparticles: The need for in vivo studies

BioNanoMaterials

Volumn 14, Issue 1-2, 2013, Pages 65-79

  Shah, Neha B ^a   Bischof, John C ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

blood nanoparticle interactions; cell activation; coagulation; Gold Nanoparticles; phagocytosis; plasma protein; red blood cells; white blood cells

Indexed keywords

EID: 84924906324     PISSN: 21930651     EISSN: 2193066X     Source Type: Journal    
DOI: 10.1515/bnm-2012-0003     Document Type: Article

References (89)

1. Dykman L, Khlebtsov N. Gold nanoparticles in biomedical applications: recent advances and perspectives. Chem Soc Rev 2012;41:2256–2282.
2. Giljohann DA, Seferos DS, Daniel WL, Massich MD, Patel PC, Mirkin CA. Gold Nanoparticles for Biology and Medicine. Angew Chem Int Edit 2010;49:3280–3294.
3. Thakor AS, Jokerst J, Zavaleta C, Massoud TF, Gambhir SS. Gold nanoparticles: a revival in precious metal administration to patients. Nano Letters 2011;11:4029–4036.
4. Khlebtsov N, Dykman L. Biodistribution and toxicity of engineered gold nanoparticles: a review of in vitro and in vivo studies. Chem Soc Rev 2011;40:1647–1671.
5. Gunatilleke SS, Barrios AM. Tuning the Au(l)-mediated inhibition of cathepsin B through ligand substitutions. J Inorg Biochem 2008;102:555–563.
6. Paciotti GF, Myer L, Weinreich D, Goia D, Pavel N, McLaughlin RE, et al. Colloidal gold: a novel nanoparticle vector for tumor directed drug delivery. Drug Deliv 2004;11:169–183.
7. Hirsch LR, Stafford RJ, Bankson JA, Sershen SR, Rivera B, Price RE. Nanoshell-mediated near-infrared thermal therapy of tumors under magnetic resonance guidance. Proc Natl Acad Sci USA 2003;100:13549–13554.
8. Kim BY Rutka JT, Chan WC. Nanomedicine. N Engl J Med 2010;363:2434–2443.
9. Walkey CD, Chan WC. Understanding and controlling the interaction of nanomaterials with proteins in a physiological environment. Chem Soc Rev 2012;41:2780–2799.
10. Schaller J. Human blood plasma proteins: structure and function. Hoboken, NJ: John Wiley & Sons, Ltd. x, 2008: 526 p.
11. Putnam FW. The plasma proteins: structure, function, and genetic control, 2nd ed. New York: Academic Press, 1975:1–5.
12. Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Mol Cell Proteomics 2002;1:845–867.
13. Capriotti AL, Caracciolo G, Cavaliere C, Foglia P, Pozzi D, Samperi R, et al. Do plasma proteins distinguish between liposomes of varying charge density? J Proteomics 2012;75:1924–1932.
14. Moghimi SM, Hunter AC, Murray JC. Long-Circulating and Target Specific Nanoparticles: Theory to Practice. Pharmacol Rev 2001;53:283–318.
15. Gaucher G, Asahina K, Wang J, Leroux JC. Effect of poly(Nvinyl-pyrrolidone)-block-poly(D,L-lactide) as coating agent on the opsonization, phagocytosis, and pharmacokinetics of biodegradable nanoparticles. Biomacromolecules 2009;10:408–416.
16. Leroux JC, Gravel P, Balant L, Volet B, Anner BM, Allémann E, et al. 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 1994;28:471–481.
17. Gref R, Lück M, Quellec P, Marchand M, Dellacherie E, Harnisch S, et al. “Stealth” corona-core nanoparticles surface modified by polyethylene glycol (PEG): influences of the corona (PEG chain length and surface density) and of the core composition on phagocytic uptake and plasma protein adsorption. Colloid Surface B 2000;18:301–313.
18. Gessner A, Waicz R, Lieske A, Paulke B, Mäder K, Müller RH. Nanoparticles with decreasing surface hydrophobicities: influence on plasma protein adsorption. Int J Pharm 2000;196:245–249.
19. Walkey CD, Olsen JB, Guo H, Emili A, Chan WC. Nanoparticle size and surface chemistry determine serum protein adsorption and macrophage uptake. J Am Chem Soc 2012;134:2139–2147.
20. Cedervall T, Lynch I, Foy M, Berggård T, Donnelly SC, Cagney G, et al. Detailed Identification of Plasma Proteins Adsorbed on Copolymer Nanoparticles. Angew Chem 2007;119:5856–5858.
21. Cedervall T, Lynch I, Lindman S, Berggård T, Thulin E, Nilsson H, et al. Understanding the nanoparticle-protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc Natl Acad Sci 2007;104:2050–2055.
22. Dobrovolskaia MA, Patri AK, Zheng J, Clogston JD, Ayub N, Aggarwal P, et al. Interaction of colloidal gold nanoparticles with human blood: effects on particle size and analysis of plasma protein binding profiles. Nanomed Nanotechnol Biol Med 2009;5:106–117.
23. Casals E, Pfaller T, Duschl A, Oostingh GJ, Puntes V. Time evolution of the nanoparticle protein corona. ACS Nano 2010;4:3623–3632.
24. Treuel L, Malissek M, Gebauer JS, Zellner R. The influence of surface composition of nanoparticles on their interactions with serum albumin. ChemPhysChem 2010;11:3093–3099.
25. Zhang D, Neumann O, Wang H, Yuwono VM, Barhoumi A, Perham M, et al. Gold nanoparticles can induce the formation of protein-based aggregates at physiological ph. Nano Letters 2009;9:666–671.
26. Moghimi SM, Andersen AJ, Hashemi SH, Lettiero B, Ahmadvand D, Hunter AC, et al. Complement activation cascade triggered by peg-pl engineered nanomedicines and carbon nanotubes: the challenges ahead. J Control Release 2010;146:175–181.
27. Lacerda SH, Park JJ, Meuse C, Pristinski D, Becker ML, Karim A, et al. Interaction of gold nanoparticles with common human blood proteins. ACS Nano 2010;4:365–379.
28. Lartigue L, Wilhelm C, Servais J, Factor C, Dencausse A, Bacri J-C, et al. Nanomagnetic sensing of blood plasma protein interactions with iron oxide nanoparticles: impact on macrophage uptake. ACS Nano 2012;6:2665–2678.
29. Schaller J, Gerber S, Kämpfer U, Lejon S, Trachsel C. Blood Components. In: Human Blood Plasma Proteins: Structure and Function. Homoken, NJ: Wiley, pp. 5–16.
30. White JG. Platelets are covercytes, not phagocytes: uptake of bacteria involves channels of the open canalicular system. Platelets 2005;16:121–131.
31. White JG, Clawson CC. The surface-connected canalicular system of blood platelets-a fenestrated membrane system. Am J Pathol 1980;101:353–364.
32. Munker R. Basic biology of hemopoieses. In: Modern Hematology: Biology and Clinical Management, 2nd edition. Munker, R., Hiller, E., Glass, J., Paquette, R, eds. Humana Press, 2007, 1–18.
33. Rhodin JA. Histology; a text and atlas. New York: Oxford University Press, 1974:viii, 803.
34. Rothen-Rutishauser BM, Schürch S, Haenni B, Kapp N, Gehr P. Interaction of fine particles and nanoparticles with red blood cells visualized with advanced microscopic techniques. Environ Sci Technol 2006;40:4353–4359.
35. Spiegelberg HL, Miescher PA, Benacerraf B. Studies on the role of complement in the immune clearance of Escherichia coli and rat erythrocytes by the reticuloendothelial system in mice. J Immunol 1963;90:751–759.
36. Chambers E, Mitragotri S. Prolonged circulation of large polymeric nanoparticles by non-covalent adsorption on erythrocytes. J Control Release 2004;100:111–119.
37. Hall SS, Mitragotri S, Daugherty PS. Identification of peptide ligands facilitating nanoparticle attachment to erythrocytes. Biotechnol Progr 2007;23:749–754.
38. Dobrovolskaia MA, Clogston JD, Neun BW, Hall JB, Patri AK, McNeil SE. Method for analysis of nanoparticle hemolytic properties in vitro. Nano Letters 2008;8:2180–2187.
39. Mayer A, Vadon M, Rinner B, Novak A, Wintersteiger R, Fröhlich E. The role of nanoparticle size in hemocompatibility. Toxicology 2009;258:139–147.
40. Zhao Y, Sun X, Zhang G, Trewyn BG, Slowing II, Lin VS. Interaction of mesoporous silica nanoparticles with human red blood cell membranes: size and surface effects. ACS Nano 2011;5:1366–1375.
41. Dash BC, Réthoré G, Monaghan M, Fitzgerald K, Gallagher W, Pandit A. The influence of size and charge of chitosan/ polyglutamic acid hollow spheres on cellular internalization, viability and blood compatibility. Biomaterials 2010;31:8188–8197.
42. Ziemba B, Matuszko G, Bryszewska M, Klajnert B. Influence of dendrimers on red blood cells. Cell Mol Biol Lett 2012;17:21–35.
43. Goodman CM, McCusker CD, Yilmaz T, Rotello VM. Toxicity of gold nanoparticles functionalized with cationic and anionic side chains. Bioconjugate Chem 2004;15:897–900.
44. Kim D, El-Shall H, Dennis D, Morey T. Interaction of PLGA nanoparticles with human blood constituents. Colloid and Surface B Biointerfaces 2005;40:83–91.
45. McGuinnes C, Duffin R, Brown S. L., Mills N, Megson IL, Macnee W, et al. Surface derivatization state of polystyrene latex nanoparticles determines both their potency and their mechanism of causing human platelet aggregation in vitro. Toxicol Sci 2011;119:359–368.
46. Bosi S, Feruglio L, Da Ros T, Spalluto G, Gregoretti B, Terdoslavich M, et al. Hemolytic effects of water-soluble fullerene derivatives. J Med Chem 2004;47:6711–6715.
47. Han MH, Chen J, Wang J, Chen SL, Wang XT. Blood compatibility of polyamidoamine dendrimers and erythrocyte protection. J Biomed Nanotechnol 2010;6:82–92.
48. Wang W, Xiong W, Zhu Y, Xu H, Yang X. Protective effect of PEGylation against poly(amidoamine) dendrimer-induced hemolysis of human red blood cells. J Biomed Mater Res B 2010;93B:59–64.
49. Lin Y-S, Haynes CL. Impacts of mesoporous silica nanoparticle size, pore ordering, and pore integrity on hemolytic activity. J Am Chem Soc 2010;132:4834–4842.
50. Gulati N, Rastogi R, Dinda AK, Saxena R, Koul V. Characterization and cell material interactions of PEGylated PNIPAAM nanoparticles. Colloid Surface B 2010;79:164–173.
51. Koziara JM, Oh JJ, Akers WS, Ferraris SP, Mumper RJ. Blood compatibility of cetyl alcohol/polysorbate-based nanoparticles. Pharmaceut Res 2005;22:1821–1828.
52. Li SQ, Zhu RR, Zhu H, Xue M, Sun XY, Yao SD, et al. Nanotoxicity of TiO2 nanoparticles to erythrocyte in vitro. Food Chem Toxicol 2008;46:3626–3631.
53. Trpkovic A, Todorovic-Markovic B, Kleut D, Misirkic M, Janjetovic K, Vucicevic L, et al. Oxidative stress-mediated hemolytic activity of solvent exchange-prepared fullerene (C 60) nanoparticles. Nanotechnology 2010;21:375102.
54. Movat HZ, Weiser WJ, Glynn MF, Mustard JF. Platelet phagocytosis and aggregation. J Cell Biol 1965;27:531–543.
55. White JG. Uptake of latex particles by blood platelets: phagocytosis or sequestration? Am J Pathol 1972;69:439–458.
56. Xu N, Zhou L, Odselius R, Nilsson A. Uptake of radiolabeled and colloidal gold-labeled chyle chylomicrons and chylomicron remnants by rat platelets in vitro. Arterioscler Thromb Vasc Biol 1995;15:972–981.
57. Weiss D, Wardrop KJ. Schalm's veterinary hematology, 6th edition. Aimes Iowa: Wiley Blackwell, 2010.
58. Radomski A, Jurasz P, Alonso-Escolano D, Drews M, Morandi M, Malinski T, et al. Nanoparticle-induced platelet aggregation and vascular thrombosis. Br J Pharmacol 2005;146:882–893.
59. Miller VM, Hunter LW, Chu K, Kaul V, Squillace PD, Lieske JC, et al. Biologic nanoparticles and platelet reactivity. Nanomedicine (Lond) 2009;4:725–733.
60. Stefanou E, Evangelou A, Falaras P. Effects of UV-irradiated titania nanoparticles on cell proliferation, cancer metastasis and promotion. Catal Today 2010;151:58–63.
61. Ramtoola Z, Lyons P, Keohane K, Kerrigan SW, Kirby BP, Kelly JG. Investigation of the interaction of biodegradable micro-and nanoparticulate drug delivery systems with platelets. J Pharm Pharmacol 2010;63:26–32.
62. Li X, Radomski A, Corrigan OI, Tajber L, De Sousa Menezes F, Endter S, et al. Platelet compatibility of PLGA, chitosan and PLGA chitosan nanoparticles. Nanomedicine 2009;4:735–746.
63. Cejas MA, Chen C, Kinney WA, Maryanoff BE. Nanoparticles that display short collagen-related peptides. Potent stimulation of human platelet aggregation by triple helical motifs. Bioconjugate Chem 2007;18:1025–1027.
64. Akchurin GG, Akchurin GG, Ivanov AN, Kirichuk VF, Terentyuk GS, Khlebtsov BN, et al. Influence of gold nanoparticles on platelets functional activity in vitro. Proc. SPIE 6869, Plasmonics in Biology and Medicine V, 68690V (February 13, 2008); doi:10.1117/12.765076.
65. Bihari P, Holzer M, Praetner M, Fent J, Lerchenberger M, Reichel CA, et al. Single-walled carbon nanotubes activate platelets and accelerate thrombus formation in the microcirculation. Toxicology 2010;269:148–154.
66. Shah NB, Vercellotti GM, White JG, Fegan A, Wagner CR, Bischof JC. Blood-Nanoparticle Interactions and in vivo biodistribution: impact of surface PEG and ligand properties. Mol Pharm 2012;9:2146–2155.
67. Santos-Martinez MJ, Inkielewicz-Stepniak I, Medina C, Rahme K, D'Arcy DM, Fox D, et al. The use of quartz crystal microbalance with dissipation (QCM-D) for studying nanoparticle-induced platelet aggregation. Int J Nanomed 2012;7:243–255.
68. Lunov O, Landfester K, Simmet T. Differential uptake of functionalized polystyrene nanoparticles by human macrophages and a monocytic cell line. ACS Nano 2011;5:1657–1659.
69. Zahr AS, Davis CA, Pishko MV. Macrophage uptake of core-shell nanoparticles surface modified with poly(ethylene glycol). Langmuir 2006;22:8178–8185.
70. Rehor A, Schmoekela H, Tirellib N, Hubbella JA. Functionalization of polysulfide nanoparticles and their performance as circulating carriers. Biomaterials 2008;29:1958–1966.
71. Díaz B, Sánchez-Espinel C, Arruebo M, Faro J, de Miguel E, Magad á n S, et al. Assessing methods for blood cell cytotoxic responses to inorganic nanoparticles and nanoparticle ggregates. Small 2008;4:2025–2034.
72. Shi B, Fang C, You MX, Hong MH, Pei YY. Stealth PEG-PHDCA niosomes: effects of chain length of PEG on niosomes in vitro complement consumption and phagocytic uptake. J Pharm Sci 2005;40:976–981.
73. Pan Y, Neuss S, Leifert A, Fischler M, Wen F, Simon U, et al. Size-dependent cytotoxicity of gold nanoparticles. Small 2007;3:1941–1949.
74. Arnida, Janát-Amsbury MM, Ray A, Peterson CM, Ghandehari H. Geometry and surface characteristics of gold nanoparticles influence their biodistribution and uptake by macrophages. Eur Pharm Biopharm 2011;77:417–423.
75. Zhang Q, Hitchins VM, Schrand AM, Hussain SM, Goering PL. Uptake of gold nanoparticles in murine macrophage cells without cytotoxicity or production of pro-inflammatory mediators. Nanotoxicology 2011;5:284–295.
76. Kah JC, Wong KY, Neoh KG, Song JH, Fu JW, Mhaisalkar S, et al. Critical parameters in the pegylation of gold nanoshells for biomedical applications: an in vitro macrophage study. J Drug Target 2009;17:181–193.
77. Shukla R, Bansal V, Chaudhary M, Basu A, Bhonde RR, Sastry M. Biocompatibility of gold nanoparticles and their endocytotic fate inside the cellular compartment: a microscopic overview. Langmuir 2005;21:10644–10654.
78. Vallhov H, Gabrielsson S, Strømme M, Scheynius A, Garcia Bennett AE. Mesoporous silica particles induce size dependent effects on human dendritic cells. Nano Letters 2007;7:3576–3582.
79. Krpetić $ Porta F, Caneva E, Dal Santo V, Scari G. Phagocytosis of biocompatible gold nanoparticles. Langmuir 2010;26:14799–14805.
80. Bastús NG, Sanchez-Tillo E, Pujals S, Farrera C, Kogan MJ, Giralt E, et al. Peptides conjugated to gold nanoparticles induce macrophage activation. Mol Immunol 2009;46:743–748.
81. Bartneck M, Keul HA, Zwadlo-Klarwasser G, Groll J. Phagocytosis independent extracellular nanoparticle clearance by human immune cells. Nano Letters 2009;10:59–63.
82. Bartneck M, Keul HA, Singh S, Czaja K, Bornemann J, Bockstaller M, et al. Rapid uptake of gold nanorods by primary human blood phagocytes and immunomodulatory effects of surface chemistry. ACS Nano 2010;4:3073–3086.
83. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, et al. Neutrophil extracellular traps kill bacteria. Science 2004;303:1532–1535.
84. Dufort S, Sancey L, Coll JL. Physico-chemical parameters that govern nanoparticles fate also dictate rules for their molecular evolution. Adv Drug Deliv Rev 2012;64:179–189.
85. Aggarwal P, Hall JB, McLeland CB, Dobrovolskaia MA, McNeil SE. Nanoparticle interaction with plasma proteins as it relates to particle biodistribution, biocompatibility and therapeutic efficacy. Adv Drug Deliv Rev 2009;61:428–437.
86. Dobrovolskaia MA, Aggarwal P, Hall JB, McNeil SE. Preclinical studies to understand nanoparticle interaction with the immune system and its potential effects on nanoparticle biodistribution. Mol Pharm 2008;5:487–495.
87. Deng ZJ, Liang M, Monteiro M, Toth I, Minchin RF. Nanoparticleinduced unfolding of fibrinogen promotes Mac-1 receptor activation and inflammation. Nat Nano 2010;6:39–44.
88. Dutta D, Sundaram SK, Teeguarden JG, Riley BJ, Fifield LS, Jacobs JM, et al. Adsorbed proteins influence the biological activity and molecular targeting of nanomaterials. Toxicol Sci 2007;100:303–315.
89. Lynch I, Salvati A, Dawson KA. Protein-nanoparticle interactions: what does the cell see? Nat Nano 2009;4:546–547.