Abstract
The formation of protein coronas on nanomaterial will significantly alter the surface properties of nanomaterial in biological systems and subsequently impact biological responses including signaling, cellular uptake, transport, and toxicity etc. It is of critical importance to understand the formation of protein coronas on the surface of nanomaterial. Analytical techniques, especially mass spectrometry-based proteomics methods, are playing a key role for the qualitative and quantitative analyses of protein coronas on nanomaterial. In this review, the proteomic approaches developed for the characterization of protein coronas on various nanomaterials are introduced with the emphasis on the mass spectrometry-based proteomic strategies.
Similar content being viewed by others
References
Li Y, Wang F, Sun TM, Du JZ, Yang XZ, Wang J. Surfacemodulated and thermoresponsive polyphosphoester nanoparticles for enhanced intracellular drug delivery. Sci China Chem, 2014, 57: 579–585
Cao M, Liu X, Tang T, Sui M, Shen Y. Facile synthesis of sizetunable stable nanoparticles via click reaction for cancer drug delivery. Sci China Chem, 2014, 57: 633–644
Zhang Y, Xiao CS, Li MQ, Ding JX, Yang CG, Zhuang XL, Chen XS. Co-delivery of doxorubicin and paclitaxel with linear-dendritic block copolymer for enhanced anti-cancer efficacy. Sci China Chem, 2014, 57: 624–632
Ma HL, Liang XJ. Fullerenes as unique nanopharmaceuticals for disease treatment. Sci China Chem, 2010, 53: 2233–2240
Kenouche S, Larionova J, Bezzi N, Guari Y, Bertin N, Zanca M, Lartigue L, Cieslak M, Godin C, Morrot G, Goze-Bac C. NMR investigation of functionalized magnetic nanoparticles Fe3O4 as T-1-T- 2 contrast agents. Powder Technol, 2014, 255: 60–65
Naccache R, Chevallier P, Lagueux J, Gossuin Y, Laurent S, Vander Elst L, Chilian C, Capobianco JA, Fortin MA. High relaxivities and strong vascular signal enhancement for NaGdF4 nanoparticles designed for dual MR/optical imaging. Adv Healthc Mater, 2013, 2: 1478–1488
Atkins TM, Cassidy MC, Lee M, Ganguly S, Marcus CM, Kauzlarich SM. Synthesis of long T-1 silicon nanoparticles for hyperpolarized Si-29 magnetic resonance imaging. ACS Nano, 2013, 7: 1609–1617
Liu CY, Gao ZY, Zeng JF, Hou Y, Fang F, Li YL, Qiao RR, Shen L, Lei H, Yang WS, Gao MY. Magnetic/upconversion fluorescent NaGdF4:Yb,Er nanoparticle-based dual-modal molecular probes for imaging tiny tumors in vivo. ACS Nano, 2013, 7: 7227–7240
Wu S, Zhang LL, Qi L, Tao SY, Lan XQ, Liu ZG, Meng CG. Ultrasensitive biosensor based on mesocellular silica foam for organophosphorous pesticide detection. Biosens Bioelectron, 2011, 26: 2864–2869
Yen SK, Janczewski D, Lakshmi JL, Bin Dolmanan S, Tripathy S, Ho VHB, Vijayaragavan V, Hariharan A, Padmanabhan P, Bhakoo KK, Sudhaharan T, Ahmed S, Zhang Y, Selvan ST. Design and synthesis of polymer-functionalized nir fluorescent dyes-magnetic nanoparticles for bioimaging. ACS Nano, 2013, 7: 6796–6805
Nel AE, Mädler L, Velegol D, Xia T, Hoek EMV, Somasundaran P, Klaessig F, Castranova V, Thompson M. Understanding biophysicochemical interactions at the nano-bio interface. Nat Mater, 2009, 8: 543–557
Walkey CD, Chan WCW. Understanding and controlling the interaction of nanomaterials with proteins in a physiological environment. Chem Soc Rev, 2012, 41: 2780–2799
Pozzi D, Caracciolo G, Capriotti AL, Cavaliere C, Piovesana S, Colapicchioni V, Palchetti S, Riccioli A, Laganà A. A proteomicsbased methodology to investigate the protein corona effect for targeted drug delivery. Mol BioSyst, 2014, 10: 2815–2819
Gessner A, Lieske A, Paulke BR, Muller RH. Functional groups on polystyrene model nanoparticles: influence on protein adsorption. J Biomed Mater Res A, 2003, 65: 319–326
Lee WA, Pernodet N, Li B, Lin CH, Hatchwell E, Rafailovich MH. Multicomponent polymer coating to block photocatalytic activity of TiO2 nanoparticles. Chem Commun (Camb), 2007: 4815–4817
Monopoli MP, Bombelli FB, Dawson KA. Nanobiotechnology: nanoparticle coronas take shape. Nat Nanotechnol, 2011, 6: 11–12
Mahmoudi M, Lynch I, Ejtehadi MR, Monopoli MP, Bombelli FB, Laurent S. Protein-nanoparticle interactions: opportunities and challenges. Chem Rev, 2011, 111: 5610–5637
Karmali PP, Simberg D. Interactions of nanoparticles with plasma proteins: implication on clearance and toxicity of drug delivery systems. Expert Opin Drug Deliv, 2011, 8: 343–357
Lundqvist M, Stigler J, Elia G, Lynch I, Cedervall T, Dawson KA. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. P Natl Acad Sci USA, 2008, 105: 14265–14270
Monopoli MP, Walczyk D, Campbell A, Elia G, Lynch I, Bombelli FB, Dawson KA. Physical-chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. J Am Chem Soc, 2011, 133: 2525–2534
Mortensen NP, Hurst GB, Wang W, Foster CM, Nallathamby PD, Retterer ST. Dynamic development of the protein corona on silica nanoparticles: composition and role in toxicity. Nanoscale, 2013, 5: 6372–6380
Miclaus T, Bochenkov VE, Ogaki R, Howard KA, Sutherland DS. Spatial mapping and quantification of soft and hard protein coronas at silver nanocubes. Nano Lett, 2014, 14: 2086–2093
Ashby J, Pan S, Zhong W. Size and surface functionalization of iron oxide nanoparticles influence the composition and dynamic nature of their protein corona. ACS Appl Mater Interfaces, 2014, 6: 15412–15419
Milani S, Bombelli FB, Pitek AS, Dawson KA, Radler J. Reversible versus irreversible binding of transferrin to polystyrene nanoparticles: soft and hard corona. ACS Nano, 2012, 6: 2532–2541
Shang W, Nuffer JH, Dordick JS, Siegel RW. Unfolding of ribonuclease A on silica nanoparticle surfaces. Nano Lett, 2007, 7: 1991–1995
Du X, Shi B, Tang Y, Dai S and Qiao SZ. Label-free dendrimer-like silica nanohybrids for traceable and controlled gene delivery. Biomaterials, 2014, 35: 5580–5590
Ge Y, Bruno M, Wallace K, Winnik W, Prasad RY. Proteome profiling reveals potential toxicity and detoxification pathways following exposure of BEAS-2B cells to engineered nanoparticle titanium dioxide. Proteomics, 2011, 11: 2406–2422
Walczyk D, Bombelli FB, Monopoli MP, Lynch I, Dawson KA. What the cell “sees” in bionanoscience. J Am Chem Soc, 2010, 132: 5761–5768
Monopoli MP, Aberg C, Salvati A, Dawson KA. Biomolecular coronas provide the biological identity of nanosized materials. Nat Nanotechnol, 2012, 7: 779–786
Lesniak A, Fenaroli F, Monopoli MR, Aberg C, Dawson KA, Salvati A. Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano, 2012, 6: 5845–5857
Lacerda SHD, Park JJ, Meuse C, Pristinski D, Becker ML, Karim A, Douglas JF. Interaction of gold nanoparticles with common human blood proteins. ACS Nano, 2010, 4: 365–379
Cedervall T, Lynch I, Lindman S, Berggard T, Thulin E, Nilsson H, Dawson KA, Linse S. Understanding the nanoparticle-protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. P Natl Acad Sci USA, 2007, 104: 2050–2055
Lindman S, Lynch I, Thulin E, Nilsson H, Dawson KA, Linse S. Systematic investigation of the thermodynamics of HSA adsorption to N-iso-propylacrylamide/N-tert-butylacrylamide copolymer nanoparticles. Effects of particle size and hydrophobicity. Nano Letters, 2007, 7: 914–920
Rocker C, Potzl M, Zhang F, Parak WJ, Nienhaus GU. A quantitative fluorescence study of protein monolayer formation on colloidal nanoparticles. Nat Nanotechnol, 2009, 4: 577–580
Xian F, Hendrickson CL, Marshall AG. High resolution mass spectrometry. Anal Chem, 2012, 84: 708–719
Angel TE, Aryal UK, Hengel SM, Baker ES, Kelly RT, Robinson EW, Smith RD. Mass spectrometry-based proteomics: existing capabilities and future directions. Chem Soc Rev, 2012, 41: 3912–3928
Sund J, Alenius H, Vippola M, Savolainen K, Puustinen A. Proteomic characterization of engineered nanomaterial-protein interactions in relation to surface reactivity. ACS Nano, 2011, 5: 4300–4309
Blunk T, Hochstrasser DF, Sanchez JC, Muller BW, Muller RH. 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: 1382–1387
Harnisch S, Muller RH. Plasma protein adsorption patterns on emulsions for parenteral administration: establishment of a protocol for two-dimensional polyacrylamide electrophoresis. Electrophoresis, 1998, 19: 349–354
Goppert TM, Muller RH. Alternative sample preparation prior to two-dimensional electrophoresis protein analysis on solid lipid nanoparticles. Electrophoresis, 2004, 25: 134–140
Thode K, Luck M, Semmler W, Muller RH, Kresse M. Determination of plasma protein adsorption on magnetic iron oxides: sample preparation. Pharmaceut Res, 1997, 14: 905–910
Jansch M, Stumpf P, Graf C, Ruhl E, Muller RH. Adsorption kinetics of plasma proteins on ultrasmall superparamagnetic iron oxide (USPIO) nanoparticles. Int J Pharmaceut, 2012, 428: 125–133
Kim MS, Pinto SM, Getnet D, Nirujogi RS, Manda SS, Chaerkady R, Madugundu AK, Kelkar DS, Isserlin R, Jain S, Thomas JK, Muthusamy B, Leal-Rojas P, Kumar P, Sahasrabuddhe NA, Balakrishnan L, Advani J, George B, Renuse S, Selvan LDN, Patil AH, Nanjappa V, Radhakrishnan A, Prasad S, Subbannayya T, Raju R, Kumar M, Sreenivasamurthy SK, Marimuthu A, Sathe GJ, Chavan S, Datta KK, Subbannayya Y, Sahu A, Yelamanchi SD, Jayaram S, Rajagopalan P, Sharma J, Murthy KR, Syed N, Goel R, Khan AA, Ahmad S, Dey G, Mudgal K, Chatterjee A, Huang TC, Zhong J, Wu XY, Shaw PG, Freed D, Zahari MS, Mukherjee KK, Shankar S, Mahadevan A, Lam H, Mitchell CJ, Shankar SK, Satishchandra P, Schroeder JT, Sirdeshmukh R, Maitra A, Leach SD, Drake CG, Halushka MK, Prasad TSK, Hruban RH, Kerr CL, Bader GD, Iacobuzio-Donahue CA, Gowda H, Pandey A. A draft map of the human proteome. Nature, 2014, 509: 575–581
Capriotti AL, Caracciolo G, Cavaliere C, Crescenzi C, Pozzi D, Lagana A. Shotgun proteomic analytical approach for studying proteins adsorbed onto liposome surface. Anal Bioanal Chem, 2011, 401: 1195–1202
Tenzer S, Docter D, Rosfa S, Wlodarski A, Kuharev J, Rekik A, Knauer SK, Bantz C, Nawroth T, Bier C, Sirirattanapan J, Mann W, Treuel L, Zellner R, Maskos M, Schild H, Stauber RH. Nanoparticle size is a critical physicochemical determinant of the human blood plasma corona: a comprehensive quantitative proteomic analysis. ACS Nano, 2011, 5: 7155–7167
Walkey CD, Olsen JB, Guo H, Emili A, Chan WCW. Nanoparticle size and surface chemistry determine serum protein adsorption and macrophage uptake. J Am Chem Soc, 2012, 134: 2139–2147
Zhang HZ, Burnum KE, Luna ML, Petritis BO, Kim JS, Qian WJ, Moore RJ, Heredia-Langner A, Webb-Robertson BJM, Thrall BD, Camp DG, Smith RD, Pounds JG, Liu T. Quantitative proteomics analysis of adsorbed plasma proteins classifies nanoparticles with different surface properties and size. Proteomics, 2011, 11: 4569–4577
Turriziani B, Garcia-Munoz A, Pilkington R, Raso C, Kolch W, von Kriegsheim A. On-beads digestion in conjunction with datadependent mass spectrometry: a shortcut to quantitative and dynamic interaction proteomics. Biology (Basel), 2014, 3: 320–332
Lin S, Yao G, Qi D, Li Y, Deng C, Yang P, Zhang X. Fast and efficient proteolysis by microwave-assisted protein digestion using trypsin-immobilized magnetic silica microspheres. Anal Chem, 2008, 80: 3655–3665
Sun LL, Li YH, Yang P, Zhu GJ, Dovichi NJ. High efficiency and quantitatively reproducible protein digestion by trypsin-immobilized magnetic microspheres. J Chromatogr A, 2012, 1220: 68–74
Hu ZY, Zhao L, Zhang HY, Zhang Y, Wu RA, Zou HF. The on-bead digestion of protein corona on nanoparticles by trypsin immobilized on the magnetic nanoparticle. J Chromatogr A, 2014, 1334: 55–63
Hu Z, Zhang H, Zhang Y, Wu R, Zou H. Nanoparticle size matters in the formation of plasma protein coronas on Fe3O4 nanoparticles. Colloids Surf B Biointerfaces, 2014, 121: 354–361
Tate S, Larsen B, Bonner R, Gingras AC. Label-free quantitative proteomics trends for protein-protein interactions. J Proteomics, 2013, 81: 91–101
Hsu JL, Huang SY, Chow NH, Chen SH. Stable-isotope dimethyl labeling for quantitative proteomics. Anal Chem, 2003, 75: 6843–6852
Righetti PG, Campostrini N, Pascali J, Hamdan M, Astner H. Quantitative proteomics: a review of different methodologies. Eur J Mass Spectrom, 2004, 10: 335–348
Miyagi M, Rao KC. Proteolytic 18O-labeling strategies for quantitative proteomics. Mass Spectrom Rev, 2007, 26: 121–136
Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJR. Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc, 2009, 4: 484–494
Liu Z, Cao J, He Y, Qiao L, Xu C, Lu H, Yang P. Tandem 18O stable isotope labeling for quantification of N-glycoproteome. J Proteome Res, 2010, 9: 227–236
Lundgren DH, Hwang SI, Wu LF, Han DK. Role of spectral counting in quantitative proteomics. Expert Rev Proteomic, 2010, 7: 39–53
Cai X, Ramalingam R, Wong HS, Cheng J, Ajuh P, Cheng SH, Lam YW. Characterization of carbon nanotube protein corona by using quantitative proteomics. Nanomedicine, 2013, 9: 583–593
Hu ZY, Sun Z, Zhang Y, Wu RA, Zou HF. Glycoproteome quantification of human lung cancer cells exposed to amorphous silica nanoparticles. Acta Chim Sinica, 2012, 70: 2059–2065
Zhu W, Smith JW, Huang CM. Mass spectrometry-based label-free quantitative proteomics. J Biomed Biotechnol, 2010, 2010: 840518
Liu HB, Sadygov RG, Yates JR. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem, 2004, 76: 4193–4201
Capriotti AL, Caracciolo G, Caruso G, Cavaliere C, Pozzi D, Samperi R, Lagana A. Label-free quantitative analysis for studying the interactions between nanoparticles and plasma proteins. Anal Bioanal Chem, 2013, 405: 635–645
Capriotti AL, Caracciolo G, Caruso G, Foglia P, Pozzi D, Samperi R, Lagana A. DNA affects the composition of lipoplex protein corona: a proteomics approach. Proteomics, 2011, 11: 3349–3358
Docter D, Distler U, Storck W, Kuharev J, Wunsch D, Hahlbrock A, Knauer SK, Tenzer S, Stauber RH. Quantitative profiling of the protein coronas that form around nanoparticles. Nat Protoc, 2014, 9: 2030–2044
Shannahan JH, Lai X, Ke PC, Podila R, Brown JM, Witzmann FA. Silver nanoparticle protein corona composition in cell culture media. Plos One, 2013, 8: e74001
Wu Y, Wang F, Liu Z, Qin H, Song C, Huang J, Bian Y, Wei X, Dong J, Zou H Five-plex isotope dimethyl labeling for quantitative proteomics. Chem Commun, 2014, 50: 1708–1710
Gevaert K, Impens F, Ghesquiere B, Van Damme P, Lambrechts A, Vandekerckhove J. Stable isotopic labeling in proteomics. Proteomics, 2008, 8: 4873–4885
Yao XD, Freas A, Ramirez J, Demirev PA, Fenselau C. Proteolytic 18O labeling for comparative proteomics: model studies with two serotypes of adenovirus. Anal Chem, 2001, 73: 2836–2842
Petritis BO, Qian WJ, Camp DG, Smith RD. A simple procedure for effective quenching of trypsin activity and prevention of 18O-labeling back-exchange. J Proteome Res, 2009, 8: 2157–2163
Pan Y, Ye M, Zhao L, Cheng K, Dong M, Song C, Qin H, Wang F, Zou H. N-terminal labeling of peptides by trypsin-catalyzed ligation for quantitative proteomics. Angew Chem, 2013, 52: 9205–9209
Bordusa F. Proteases in organic synthesis. Chem Rev, 2002, 102: 4817–4868
Koeller KM, Wong CH. Enzymes for chemical synthesis. Nature, 2001, 409: 232–240
Oda Y, Huang K, Cross FR, Cowburn D, Chait BT. Accurate quantitation of protein expression and site-specific phosphorylation. P Natl Acad Sci USA, 1999, 96: 6591–6596
Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics, 2002, 1: 376–386
Ong SE. The expanding field of SILAC. Anal Bioanal Chem, 2012, 404: 967–976
Wasdo SC, Barber DS, Denslow ND, Powers KW, Palazuelos M, Stevens SM, Moudgil BM, Roberts SM. Differential binding of serum proteins to nanoparticles. Int J Nanotechnol, 2008, 5: 92–115
Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R. Quantitative analysis of complex protein mixtures using isotopecoded affinity tags. Nat Biotechnol, 1999, 17: 994–999
Zieske LR. A perspective on the use of iTRAQ reagent technology for protein complex and profiling studies. J Exp Bot, 2006, 57: 1501–1508
Wiese S, Reidegeld KA, Meyer HE, Warscheid B. Protein labeling by iTRAQ: a new tool for quantitative mass spectrometry in proteome research. Proteomics, 2007, 7: 340–350
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zhang, H., Wu, R. Proteomic profiling of protein corona formed on the surface of nanomaterial. Sci. China Chem. 58, 780–792 (2015). https://doi.org/10.1007/s11426-015-5395-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11426-015-5395-9