Dynamic changes of protein corona compositions on the surface of zinc oxide nanoparticle in cell culture media

Vo-Van Giau, Yoon-Hee Park, Kyu-Hwan Shim, Sang-Wook Son, Seong-Soo A. An

PDF(1264 KB)
PDF(1264 KB)
Front. Chem. Sci. Eng. ›› 2019, Vol. 13 ›› Issue (1) : 90-97. DOI: 10.1007/s11705-018-1766-z
RESEARCH ARTICLE
RESEARCH ARTICLE

Dynamic changes of protein corona compositions on the surface of zinc oxide nanoparticle in cell culture media

Author information +
History +

Abstract

The potential applications of nanomaterials used in nanomedicine as ingredients in drug delivery systems and in other products continue to expand. When nanomaterials are introduced into physiological environments and driven by energetics, they readily associate proteins forming a protein corona (PC) on their surface. This PC could result in an alteration of the nanomaterial’s surface characteristics, affecting their interaction with cells due to conformational changes in adsorbed protein molecules. However, our current understanding of nanobiological interactions is still very limited. Utilizing a liquid chromatography–mass spectroscopy/mass spectroscopy technology and a Cytoscape plugin (ClueGO) approach, we examined the composition of the PC for a set of zinc oxide nanoparticles (ZnONP) from cell culture media typically and further analyzed the biological interaction of identified proteins, respectively. In total, 36 and 33 common proteins were investigated as being bound to ZnONP at 5 min and 60 min, respectively. These proteins were further analyzed with ClueGO, a Cytoscape plugin, which provided gene ontology and the biological interaction processes of identified proteins. Proteins bound to the surface of nanoparticles that may modify the structure, therefore the function of the adsorbed protein could be consequently affect the complicated biological processes.

Graphical abstract

Keywords

ZnONPs / nanoparticles / protein corona / ClueGO

Cite this article

Download citation ▾
Vo-Van Giau, Yoon-Hee Park, Kyu-Hwan Shim, Sang-Wook Son, Seong-Soo A. An. Dynamic changes of protein corona compositions on the surface of zinc oxide nanoparticle in cell culture media. Front. Chem. Sci. Eng., 2019, 13(1): 90‒97 https://doi.org/10.1007/s11705-018-1766-z

References

[1]
Blunk T, Hochstrasser D F, Sanchez J C, Muller B W, Muller R H. Colloidal carriers for intravenous drug targeting: Plasma protein adsorption patterns on surface-modified latex particles evaluated by two-dimensional polyacrylamide gel electrophoresis. Electrophoresis, 1993, 14(12): 1382–1387
CrossRef Google scholar
[2]
Ehrenberg M S, Friedman A E, Finkelstein J N, Oberdorster G, McGrath J L. The influence of protein adsorption on nanoparticle association with cultured endothelial cells. Biomaterials, 2009, 30(4): 603–610
CrossRef Google scholar
[3]
Lundqvist M, Augustsson C, Lilja M, Lundkvist K, Dahlbäck B, Linse S, Cedervall T. The nanoparticle protein corona formed in human blood or human blood fractions. PLoS One, 2017, 12(4): e0175871
CrossRef Google scholar
[4]
Beduneau A, Ma Z, Grotepas C B, Kabanov A, Rabinow B E, Gong N, Mosley R L, Dou H, Boska M D, Gendelman H E. Facilitated monocyte-macrophage uptake and tissue distribution of superparmagnetic iron-oxide nanoparticles. PLoS One, 2009, 4(2): e4343
CrossRef Google scholar
[5]
Clift M J, Bhattacharjee S, Brown D M, Stone V. The effects of serum on the toxicity of manufactured nanoparticles. Toxicology Letters, 2010, 198(3): 358–365
CrossRef Google scholar
[6]
Khanna P, Ong C, Bay B H, Baeg G H. Nanotoxicity: An interplay of oxidative stress, inflammation and cell death. Nanomaterials (Basel, Switzerland), 2015, 5(3): 1163–1180
CrossRef Google scholar
[7]
Lartigue L, Wilhelm C, Servais J, Factor C, Dencausse A, Bacri J C, Luciani N, Gazeau F. Nanomagnetic sensing of blood plasma protein interactions with iron oxide nanoparticles: Impact on macrophage uptake. ACS Nano, 2012, 6(3): 2665–2678
CrossRef Google scholar
[8]
Lunov O, Syrovets T, Loos C, Beil J, Delacher M, Tron K, Nienhaus G U, Musyanovych A, Mailänder V, Landfester K, et al. Differential uptake of functionalized polystyrene nanoparticles by human macrophages and a monocytic cell line. ACS Nano, 2011, 5(3): 1657–1669
CrossRef Google scholar
[9]
Walkey C D, Olsen J B, Song F, Liu R, Liu R, Guo H, Olsen D W, Cohen Y, Emili A, Chan W C. Protein corona fingerprinting predicts the cellular interaction of gold and silver nanoparticles. ACS Nano, 2014, 8(3): 2439–2455
CrossRef Google scholar
[10]
Gu Z, Yang Z, Chong Y, Ge C, Weber J K, Bell D R, Zhou R. Surface curvature relation to protein adsorption for carbon-based nanomaterials. Scientific Reports, 2015, 5(1): 10886
CrossRef Google scholar
[11]
Marucco A, Gazzano E, Ghigo D, Enrico E, Fenoglio I. Fibrinogen enhances the inflammatory response of alveolar macrophages to TiO2, SiO2 and carbon nanomaterials. Nanotoxicology, 2016, 10(1): 1–9
[12]
Ge C, Du J, Zhao L, Wang L, Liu Y, Li D, Yang Y, Zhou R, Zhao Y, Chai Z, Chen C. Binding of blood proteins to carbon nanotubes reduces cytotoxicity. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(41): 16968–16973
CrossRef Google scholar
[13]
Hajipour M J, Raheb J, Akhavan O, Arjmand S, Mashinchian O, Rahman M, Abdolahad M, Serpooshan V, Laurentj L, Mahmoudi M. Personalized disease-specific protein corona influences the therapeutic impact of graphene oxide. Nanoscale, 2015, 7(19): 8978–8994
CrossRef Google scholar
[14]
Salvati A, Pitek A S, Monopoli M P, Prapainop K, Bombelli F B, Hristov D R, Kelly P M, Åberg C, Mahon E, Dawson K A. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nature Nanotechnology, 2013, 8(2): 137–143
CrossRef Google scholar
[15]
Deng Z J, Liang M, Monteiro M, Toth I, Minchin R F. Nanoparticle-induced unfolding of fibrinogen promotes Mac-1 receptor activation and inflammation. Nature Nanotechnology, 2011, 6(1): 39–44
CrossRef Google scholar
[16]
Saikia J, Yazdimamaghani M, Hadipour M. S P, Ghandehari H. Differential protein adsorption and cellular uptake of silica nanoparticles based on size and porosity. ACS Applied Materials & Interfaces, 2016, 8(50): 34820–34832
CrossRef Google scholar
[17]
Anders C B, Eixenberger J E, Franco N A, Hermann R J, Rainey K D, Chess J J, Punnooseb A, Wingett D G. ZnO nanoparticle preparation route influences surface reactivity, dissolution and cytotoxicity. Environmental Science. Nano, 2018, 5(2): 572–588
CrossRef Google scholar
[18]
Rasmussen J W, Martinez E, Louka P, Denise G, Wingett D G. Zinc oxide nanoparticles for selective destruction of tumor cells and potential for drug delivery applications. Expert Opinion on Drug Delivery, 2010, 7(9): 1063–1077
CrossRef Google scholar
[19]
Scherzad A, Meyer T, Kleinsasser N, Hackenberg S. Molecular mechanisms of zinc oxide nanoparticle-induced genotoxicity short running title: Genotoxicity of ZnO NPs. Materials (Basel), 2017, 10(12): e1427
CrossRef Google scholar
[20]
Singh N, Manshian B, Jenkins G J, Griffiths S M, Williams P M, Maffeis T G, Wright C J, Doak S H. Nanogenotoxicology: The DNA damaging potential of engineered nanomaterials. Biomaterials, 2009, 30(23-24): 3891–3914
CrossRef Google scholar
[21]
Rajput V D, Minkina T M, Behal A, Sushkova S N, Mandzhieva S, Singh R, Gorovtsov A, Tsitsuashvili V S, Purvis W O, Ghazaryan K A, et al. Effects of zinc-oxide nanoparticles on soil, plants, animals and soil organisms: A review. Environmental Nanotechnology, Monitoring & Management, 2018, 9: 76–84
CrossRef Google scholar
[22]
Wahab R, Siddiqui M A, Saquib Q, Dwivedi S, Ahmad J, Musarrat J, Al-Khedhairy A A, Shin H S. ZnO nanoparticles induced oxidative stress and apoptosis in HepG2 and MCF-7 cancer cells and their antibacterial activity. Colloids and Surfaces. B, Biointerfaces, 2014, 117(1): 267–276
CrossRef Google scholar
[23]
Chevallet M, Gallet B, Fuchs A, Jouneau P H, Um K, Mintz E, Michaud-Soret I. Metal homeostasis disruption and mitochondrial dysfunction in hepatocytes exposed to sub-toxic doses of zinc oxide nanoparticles. Nanoscale, 2016, 8(43): 18495–18506
CrossRef Google scholar
[24]
Zhang W, Zhao Y, Li F, Li L, Feng Y, Min L, Ma D, Yu S, Liu J, Zhang H, et al. Zinc oxide nanoparticle caused plasma metabolomic perturbations correlate with hepatic steatosis. Frontiers in Pharmacology, 2018, 9: 57
CrossRef Google scholar
[25]
Leite-Silva V R, Liu D C, Sanchez W Y, Studier H, Mohammed Y H, Holmes A, Becker W, Grice J E, Benson H A, Roberts M S. Effect of flexing and massage on in vivo human skin penetration and toxicity of zinc oxide nanoparticles. Nanomedicine (London), 2016, 11(10): 1193–1205
CrossRef Google scholar
[26]
Sayes C M, Reed K L, Warheit D B. Assessing toxicity of fine and nanoparticles: Comparing in vitro measurements to in vivo pulmonary toxicity profiles. Toxicological Sciences: An Official Journal of the Society of Toxicology, 2007, 97(1): 163–180
CrossRef Google scholar
[27]
Xia T, Zhao Y, Sager T, George S, Pokhrel S, Li N, Schoenfeld D, Meng H, Lin S, Wang X, et al. Decreased dissolution of ZnO by iron doping yields nanoparticles with reduced toxicity in the rodent lung and zebrafish embryos. ACS Nano, 2011, 5(2): 1223–1235
CrossRef Google scholar
[28]
Warheit D B, Sayes C M, Reed K L. Nanoscale and fine zinc oxide particles: Can in vitro assays accurately forecast lung hazards following inhalation exposures? Environmental Science & Technology, 2009, 43(20): 7939–7945
CrossRef Google scholar
[29]
Giau V V, An S S. Emergence of exosomal miRNAs as a diagnostic biomarker for Alzheimer’s disease. Journal of the Neurological Sciences, 2016, 15(360): 141–152
CrossRef Google scholar
[30]
Mana M N, Fougères P A, Leung Y H, Liu F, Djurišić A B, Giesy J P, Leung K M Y. Physicochemical characteristics and toxicity of surface-modified zinc oxide nanoparticles to freshwater and marine microalgae. Scientific Reports, 2017, 7(1): 15909
CrossRef Google scholar
[31]
Milani S, Bombelli F B, Pitek A S, Dawson K A, Rädler J. Reversible versus irreversible binding of transferrin to polystyrene nanoparticles: Soft and hard corona. ACS Nano, 2012, 6(3): 2532–2541
CrossRef Google scholar
[32]
Pederzoli F, Tosi G, Vandelli M A, Belletti D, Forni F, Ruozi B. Protein corona and nanoparticles: How can we investigate on? Wiley Interdisciplinary Reviews. Nanomedicine and Nanobiotechnology, 2017, 9(6): e1467
CrossRef Google scholar
[33]
Rao A, Long H, Harley-Trochimczyk A, Pham T, Zettl A, Carraro C, Maboudian R. In situ localized growth of ordered metal oxide hollow sphere array on microheater platform for sensitive, ultra-fast gas sensing. ACS Applied Materials & Interfaces, 2017, 9(3): 2634–2641
CrossRef Google scholar
[34]
Schöttler S, Landfester K, Mailänder V. Controlling the stealth effect of nanocarriers through understanding the protein corona. Angewandte Chemie International Edition in English, 2016, 55(31): 8806–8815
CrossRef Google scholar
[35]
Tenzer S, Docter D, Kuharev J, Musyanovych A, Fetz V, Hecht R, Schlenk F, Fischer D, Kiouptsi K, Reinhardt C, et al. Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology. Nature Nanotechnology, 2013, 8(10): 772–781
CrossRef Google scholar
[36]
Saha K, Rahimi M, Yazdani M, Kim S T, Moyano D F, Hou S, Das R, Mout R, Rezaee F, Mahmoudi M, et al. Regulation of macrophage recognition through the interplay of nanoparticle surface functionality and protein corona. ACS Nano, 2016, 10(4): 4421–4430
CrossRef Google scholar
[37]
Shannahan J H, Brown J M, Chen R, Ke P C, Lai X, Mitra S, Witzmann F A. Comparison of nanotube-protein corona composition in cell culture media. Small, 2013, 9(12): 2171–2181
CrossRef Google scholar
[38]
Shannahan J H, Lai X, Ke P C, Podila R, Brown J M, Witzmann F A. Silver nanoparticle protein corona composition in cell culture media. PLoS One, 2013, 8(9): e74001
CrossRef Google scholar
[39]
Kim K M, Choi M H, Lee J K, Jeong J, Kim Y R, Kim M K, Paek S M, Oh J M. Physicochemical properties of surface charge-modified ZnO nanoparticles with different particle sizes. International Journal of Nanomedicine, 2014, 9(Suppl 2): 41–56
[40]
Shim K H, Hulme J, Maeng E H, Kim M K. An S S A. Analysis of zinc oxide nanoparticles binding proteins in rat blood and brain homogenate. International Journal of Nanomedicine, 2014, 9(Suppl 2): 217–224
[41]
Cedervall T, Lynch I, Foy M, Berggård T, Donnelly S C, Cagney G, Linse S, Dawson K A. Detailed identification of plasma proteins adsorbed on copolymer nanoparticles. Angewandte Chemie International Edition in English, 2007, 46(30): 5754–5756
CrossRef Google scholar
[42]
Lara S, Alnasser F, Polo E, Garry D, Giudice M C L, Hristov D R, Rocks L, Salvati A, Yan Y, Dawso N K A. Identification of receptor binding to the biomolecular corona of nanoparticles. ACS Nano, 2017, 11(2): 1884–1893
CrossRef Google scholar
[43]
Kreuter J, Shamenkov D, Petrov V, Ramge P, Cychutek K, Koch-Brandt C, Alyautdin R. Apolipoprotein-mediated transport of nanoparticle-bond drugs across the blood-brain barrier. Journal of Drug Targeting, 2002, 10(4): 317–325
CrossRef Google scholar
[44]
Palchetti S, Colapicchioni V, Digiacomo L, Caracciolo G, Pozzi D, Capriotti A L, La Barbera G, Laganà A. The protein corona of circulating PEGylated liposomes. Biochimica et Biophysica Acta, 2016, 1858(2): 189–196
CrossRef Google scholar
[45]
Ritz S, Schöttler S, Kotman N, Baier G, Musyanovych A, Kuharev J, Landfester K, Schild H, Jahn O, Tenzer S, et al. Protein corona of nanoparticles: Distinct proteins regulate the cellular uptake. Biomacromolecules, 2015, 16(4): 1311–1321
CrossRef Google scholar
[46]
Lundqvist M, Stigler J, Elia G, Lynch I, Cedervall T, Dawson K A. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(38): 14265–14270
CrossRef Google scholar
[47]
Townson J L, Lin Y S, Agola J O, Carnes E C, Leong H S, Lewis J D, Haynes C L, Brinker C J. Differing in vivo characteristics of size- and charge-matched mesoporous silica nanoparticles. Journal of the American Chemical Society, 2013, 135(43): 16030–16033
CrossRef Google scholar
[48]
Röcker C, Pötzl M, Zhang F, Parak W J, Nienhaus G U. A quantitative fluorescence study of protein monolayer formation on colloidal nanoparticles. Nature Nanotechnology, 2009, 4(9): 577–580
CrossRef Google scholar
[49]
Deng Z J, Mortimer G, Schiller T, Musumeci A, Martin D, Minchin R F. Differential plasma protein binding to metal oxide nanoparticles. Nanotechnology, 2009, 20(45): 455101
CrossRef Google scholar
[50]
Lesniak A, Campbell A, Monopoli M P, Lynch I, Salvati A, Dawson K A. Serum heat inactivation affects protein corona composition and nanoparticle uptake. Biomaterials, 2010, 31(36): 9511–5918
CrossRef Google scholar
[51]
Lesniak A, Fenaroli F, Monopoli M P, Åberg C, Dawson K A, Salvati A. Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano, 2012, 6(7): 5845–5857
CrossRef Google scholar
[52]
Lesniak A, Salvati A, Santos-Martinez M J, Radomski M W, Dawson K A, Åberg C. Nanoparticle adhesion to the cell membrane and its effect on nanoparticle uptake efficiency. Journal of the American Chemical Society, 2013, 135(4): 1438–1444
CrossRef Google scholar
[53]
Murdock R C, Braydich-Stolle L, Schrand A M, Schlager J J, Hussain S M. Characterization of nanomaterial dispersion in solution prior to in vitro exposure using dynamic light scattering technique. Toxicological Sciences: An Official Journal of the Society of Toxicology, 2008, 101(2): 239–253
CrossRef Google scholar
[54]
Maiorano G, Sabella S, Sorce B, Brunetti V, Malvindi M A, Cingolani R, Pompa P P. Effects of cell culture media on the dynamic formation of protein-nanoparticle complexes and influence on the cellular response. ACS Nano, 2010, 4(12): 7481–7491
CrossRef Google scholar
[55]
Wang J, Jensen U B, Jensen G V, Shipovskov S, Balakrishnan V S, Otzen D, Pedersen J S, Besenbacher F, Sutherland D S. Soft interactions at nanoparticles alter protein function and conformation in a size dependent manner. Nano Letters, 2011, 11(11): 4985–4991
CrossRef Google scholar
[56]
Zhou Y, Fang X, Gong Y, Xiao A, Xie Y, Liu L, Cao Y. The interactions between ZnO nanoparticles (NPs) and α-linolenic acid (LNA) complexed to BSA did not influence the toxicity of ZnO NPs on HepG2 cells. Journal of the American Chemical Society, 2017, 135(4): 1438–1444
[57]
Go M R, Yu J, Bae S H, Kim H J, Choi S J. Effects of interactions between ZnO nanoparticles and saccharides on biological responses. International Journal of Molecular Sciences, 2018, 19(2): 486
CrossRef Google scholar

Acknowledgement

This research was supported by a National Research Foundation of Korea (NRF) awarded by the Korean government (NRF-2017R1A2B4012636).

RIGHTS & PERMISSIONS

2019 Higher Education Press and Springer-Verlag GmbH Germany, part of Springer Nature
AI Summary AI Mindmap
PDF(1264 KB)

Accesses

Citations

Detail

Sections
Recommended

/