Student or educator? Sign up with your school email and get 6 months of Pro free.
CoChat
Sign Up
Cited by 625

The DOI matches its Crossref record; 28 of the 28 references it cites were found in a registry or an index.

The protein corona from nanomedicine to environmental science

Open access
Mahmoudi, Morteza, Landry, Markita P., Moore, Anna, Coreas, Roxana·2023·Nature Reviews Materials
DOI 10.1038/s41578-023-00552-2
Open this paper in CoChat — free account

Abstract

The protein corona spontaneously develops and evolves on the surface of nanoscale materials when they are exposed to biological environments, altering their physiochemical properties and affecting their subsequent interactions with biosystems. In this Review, we provide an overview of the current state of protein corona research in nanomedicine. We next discuss remaining challenges in the research methodology and characterization of the protein corona that slow the development of nanoparticle therapeutics and diagnostics, and we address how artificial intelligence can advance protein corona research as a complement to experimental research efforts. We then review emerging opportunities provided by the protein corona to address major issues in healthcare and environmental sciences. This Review details how mechanistic insights into nanoparticle protein corona formation can broadly address unmet clinical and environmental needs, as well as enhance the safety and efficacy of nanobiotechnology products. Understanding the protein corona can advance nanomedicinal developments and elucidate how nanomaterials impact the environment. This Review discusses the evolution and challenges in characterizing the protein corona, explores how artificial intelligence can supplement experimental efforts and exposes emerging opportunities in nanomedicine and the environment.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41578-023-00552-2

Cites

28 of 28 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 28 references

Research works printed but not linked: 186

  1. Lima, T., Bernfur, K., Vilanova, M. & Cedervall, T. Understanding the lipid and protein corona formation on different sized polymeric nanoparticles. Sci. Rep. 10, 1129 (2020). · DOI
  2. Martel, J. et al. Fatty acids and small organic compounds bind to mineralo-organic nanoparticles derived from human body fluids as revealed by metabolomic analysis. Nanoscale 8, 5537–5545 (2016). · DOI
  3. Chetwynd, A. J., Zhang, W., Thorn, J. A., Lynch, I. & Ramautar, R. The nanomaterial metabolite corona determined using a quantitative metabolomics approach: a pilot study. Small 16, e2000295 (2020). · DOI
  4. Zhang, W., Chetwynd, A. J., Thorn, J. A., Lynch, I. & Ramautar, R. Understanding the significance of sample preparation in studies of the nanoparticle metabolite corona. ACS Meas. Au 2, 251–260 (2022). · DOI
  5. Lynch, I., Dawson, K. A. & Linse, S. Detecting cryptic epitopes created by nanoparticles. Sci. STKE 2006, pe14 (2006). · DOI · Paper page
  6. Monopoli, M. P., Åberg, C., Salvati, A. & Dawson, K. A. Biomolecular coronas provide the biological identity of nanosized materials. Nat. Nanotechnol. 7, 779–786 (2012). · DOI · Paper page
  7. Walczyk, D., Bombelli, F. B., Monopoli, M., Lynch, I. & Dawson, K. A. What the ‘cell’ sees in bionanoscience. J. Am. Chem. Soc. 132, 5761–5768 (2010). · DOI · Paper page
  8. Hadjidemetriou, M. & Kostarelos, K. Evolution of the nanoparticle corona. Nat. Nanotechnol. 12, 288–290 (2017). · DOI · Paper page
  9. Chetwynd, A. J. & Lynch, I. The rise of the nanomaterial metabolite corona, and emergence of the complete corona. Environ. Sci. Nano 7, 1041–1060 (2020). · DOI
  10. Cedervall, T. et al. Understanding the nanoparticle–protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc. Natl Acad. Sci. USA 104, 2050–2055 (2007). · DOI · Paper page
  11. Bangham, A. D., Pethica, B. A. & Seaman, G. V. The charged groups at the interface of some blood cells. Biochem. J. 69, 12–19 (1958). · DOI
  12. Vroman, L. Effect of adsorbed proteins on the wettability of hydrophilic and hydrophobic solids. Nature 196, 476–477 (1962). · DOI · Paper page
  13. Harley, J. D. & Margolis, J. Haemolytic activity of colloidal silica. Nature 189, 1010–1011 (1961). · DOI
  14. Zhang, X. et al. Intracellular activation of bioorthogonal nanozymes through endosomal proteolysis of the protein corona. ACS Nano 14, 4767–4773 (2020). · DOI
  15. Francia, V. et al. Corona composition can affect the mechanisms cells use to internalize nanoparticles. ACS Nano 13, 11107–11121 (2019). · DOI · Paper page
  16. Lesniak, A. et al. Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano 6, 5845–5857 (2012). · DOI · Paper page
  17. Salvati, A. et al. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat. Nanotechnol. 8, 137–143 (2013). · DOI · Paper page
  18. Ge, C. et al. Binding of blood proteins to carbon nanotubes reduces cytotoxicity. Proc. Natl Acad. Sci. USA 108, 16968–16973 (2011). · DOI · Paper page
  19. Fadare, O. O. et al. Eco-corona vs protein corona: effects of humic substances on corona formation and nanoplastic particle toxicity in Daphnia magna. Environ. Sci. Technol. 54, 8001–8009 (2020). · DOI · Paper page
  20. Trinh, D. N. et al. Nanoparticle biomolecular corona-based enrichment of plasma glycoproteins for N-glycan profiling and application in biomarker discovery. ACS Nano 16, 5463–5475 (2022). · DOI
  21. Papafilippou, L., Claxton, A., Dark, P., Kostarelos, K. & Hadjidemetriou, M. Protein corona fingerprinting to differentiate sepsis from non-infectious systemic inflammation. Nanoscale 12, 10240–10253 (2020). · DOI
  22. Blume, J. E. et al. Rapid, deep and precise profiling of the plasma proteome with multi-nanoparticle protein corona. Nat. Commun. 11, 3662 (2020). · DOI · Paper page
  23. Hajipour, M. J., Laurent, S., Aghaie, A., Rezaee, F. & Mahmoudi, M. Personalized protein coronas: a ‘key’ factor at the nanobiointerface. Biomater. Sci. 2, 1210–1221 (2014). · DOI · Paper page
  24. Wang, X. et al. Chiral surface of nanoparticles determines the orientation of adsorbed transferrin and its interaction with receptors. ACS Nano 11, 4606–4616 (2017). · DOI
  25. Ritz, S. et al. Protein corona of nanoparticles: distinct proteins regulate the cellular uptake. Biomacromolecules 16, 1311–1321 (2015). · DOI · Paper page
  26. Mohr, K. et al. Aggregation behavior of polystyrene-nanoparticles in human blood serum and its impact on the in vivo distribution in mice. J. Nanomed. Nanotechnol. 5, 1000193 (2014). · DOI
  27. Dawson, K. A. & Yan, Y. Current understanding of biological identity at the nanoscale and future prospects. Nat. Nanotechnol. 16, 229–242 (2021). This article elaborates on how biological systems interact with nanomaterials and protein coronas and form bionanoscale synapses. The authors discuss future directions within protein corona research, such as the development of new technologies to study NP–biological interactions in cells. · DOI · Paper page
  28. Caracciolo, G. et al. Disease-specific protein corona sensor arrays may have disease detection capacity. Nanoscale Horiz. 4, 1063–1076 (2019). · DOI
  29. Hadjidemetriou, M., Al-ahmady, Z., Buggio, M., Swift, J. & Kostarelos, K. A novel scavenging tool for cancer biomarker discovery based on the blood-circulating nanoparticle protein corona. Biomaterials 188, 118–129 (2019). · DOI
  30. Wheeler, K. E. et al. Environmental dimensions of the protein corona. Nat. Nanotechnol. 16, 617–629 (2021). · DOI · Paper page
  31. Nasser, F., Constantinou, J. & Lynch, I. Nanomaterials in the environment acquire an “eco-corona” impacting their toxicity to Daphnia magna — a call for updating toxicity testing policies. Proteomics 20, e1800412 (2020). · DOI
  32. Lynch, I., Dawson, K. A., Lead, J. R. & Valsami-Jones, E. in Frontiers of Nanoscience Vol. 7 (eds Lead, J. R. & Valsami-Jones, E.) 127–156 (Elsevier, 2014). · DOI · Paper page
  33. Ramsperger, A. F. R. M. et al. Environmental exposure enhances the internalization of microplastic particles into cells. Sci. Adv. 6, eabd1211 (2020). · DOI · Paper page
  34. Deloid, G. M. et al. Incineration-generated polyethylene micro-nanoplastics increase triglyceride lipolysis and absorption in an in vitro small intestinal epithelium model. Environ. Sci. Technol. 56, 12288–12297 (2022). · DOI
  35. Ouassil, N., Pinals, R. L., Del Bonis-O’Donnell, J. T., Wang, J. W. & Landry, M. P. Supervised learning model predicts protein adsorption to carbon nanotubes. Sci. Adv. 8, eabm0898 (2022). This study utilizes machine learning algorithms to predict protein corona formation on CNTs by solely utilizing protein sequences from proteomic data sets. Moreover, AI identifies the most important protein features associated with high binding affinity to CNTs. · DOI
  36. Blunk, T., Hochstrasser, D. F., Sanchez, J. ‐C., Müller, B. W. & Müller, 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 14, 1382–1387 (1993). · DOI · Paper page
  37. Norman, M. E., Williams, P. & Illum, L. In vivo evaluation of protein adsorption to sterically stabilised colloidal carriers. J. Biomed. Mater. Res. 27, 8610866 (1993). · DOI
  38. Norman, M. E., Williams, P. & Illum, L. Influence of block copolymers on the adsorption of plasma proteins to microspheres. Biomaterials 14, 193–202 (1993). · DOI
  39. Gebauer, J. S. et al. Impact of the nanoparticle–protein corona on colloidal stability and protein structure. Langmuir 28, 9673–9679 (2012). · DOI · Paper page
  40. Pan, H., Qin, M., Meng, W., Cao, Y. & Wang, W. How do proteins unfold upon adsorption on nanoparticle surfaces? Langmuir 28, 12779–12787 (2012). · DOI
  41. Roach, P., Farrar, D. & Perry, C. C. Interpretation of protein adsorption: surface-induced conformational changes. J. Am. Chem. Soc. 127, 8168–8173 (2005). · DOI · Paper page
  42. Roach, P., Farrar, D. & Perry, C. C. Surface tailoring for controlled protein adsorption: effect of topography at the nanometer scale and chemistry. J. Am. Chem. Soc. 128, 3939–3945 (2006). · DOI · Paper page
  43. Ashby, J., Duan, Y., Ligans, E., Tamsi, M. & Zhong, W. High-throughput profiling of nanoparticle–protein interactions by fluorescamine labeling. Anal. Chem. 87, 2213–2219 (2015). · DOI
  44. Castagnola, V. et al. Biological recognition of graphene nanoflakes. Nat. Commun. 9, 1577 (2018). · DOI
  45. Lara, S. et al. Identification of receptor binding to the biomolecular corona of nanoparticles. ACS Nano 11, 1884–1893 (2017). · DOI · Paper page
  46. Ren, J. et al. Precision nanomedicine development based on specific opsonization of human cancer patient-personalized protein coronas. Nano Lett. 19, 4692–4701 (2019). · DOI
  47. Corbo, C. et al. Analysis of the human plasma proteome using multi-nanoparticle protein corona for detection of Alzheimer’s disease. Adv. Healthc. Mater. 10, e2000948 (2021). · DOI
  48. Colapicchioni, V. et al. Personalized liposome–protein corona in the blood of breast, gastric and pancreatic cancer patients. Int. J. Biochem. Cell Biol. 75, 180–187 (2016). · DOI
  49. Pink, M., Verma, N., Kersch, C. & Schmitz-Spanke, S. Identification and characterization of small organic compounds within the corona formed around engineered nanoparticles. Environ. Sci. Nano 5, 1420–1427 (2018). · DOI
  50. Baig, N., Kammakakam, I., Falath, W. & Kammakakam, I. Nanomaterials: a review of synthesis methods, properties, recent progress, and challenges. Mater. Adv. 2, 1821–1871 (2021). · DOI · Paper page
  51. Lundqvist, M. et al. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc. Natl Acad. Sci. USA 105, 14265–14270 (2008). · DOI · Paper page
  52. 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 6, 15412–15419 (2014). · DOI
  53. García-Álvarez, R., Hadjidemetriou, M., Sánchez-Iglesias, A., Liz-Marzán, L. M. & Kostarelos, K. In vivo formation of protein corona on gold nanoparticles: the effect of their size and shape. Nanoscale 10, 1256–1264 (2018). · DOI · Paper page
  54. Gorshkov, V., Bubis, J. A., Solovyeva, E. M., Gorshkov, M. V. & Kjeldsen, F. Protein corona formed on silver nanoparticles in blood plasma is highly selective and resistant to physicochemical changes of the solution. Environ. Sci. Nano 6, 1089–1098 (2019). · DOI
  55. Maiorano, G. et al. Effects of cell culture media on the dynamic formation of protein–nanoparticle complexes and influence on the cellular response. ACS Nano 4, 7481–7491 (2010). · DOI · Paper page
  56. Mahmoudi, M. et al. Temperature: the ‘ignored’ at the NanoBio interface. ACS Nano 7, 6555–6562 (2013). · DOI · Paper page
  57. Abbina, S. et al. Blood circulation of soft nanomaterials is governed by dynamic remodeling of protein opsonins at nano–biointerface. Nat. Commun. 11, 3048 (2020). The in vivo protein corona is analysed over time to understand mechanisms that increase the blood residency time of NPs. This study confirmes that the evolution of the in vivo protein corona is highly dynamic and the corona, composed of several opsonins, fluctuates as NPs circulate in the blood. · DOI
  58. Dell’Orco, D., Lundqvist, M., Oslakovic, C., Cedervall, T. & Linse, S. Modeling the time evolution of the nanoparticle–protein corona in a body fluid. PLoS ONE 5, e10949 (2010). · DOI · Paper page
  59. Nel, A. E. et al. Understanding biophysicochemical interactions at the nano–bio interface. Nat. Mater. 8, 543–557 (2009). · DOI · Paper page
  60. Lesniak, A. et al. Nanoparticle adhesion to the cell membrane and its effect on nanoparticle uptake efficiency. J. Am. Chem. Soc. 135, 1438–1444 (2013). · DOI · Paper page
  61. Deng, Z. J., Liang, M., Monteiro, M., Toth, I. & Minchin, R. F. Nanoparticle-induced unfolding of fibrinogen promotes Mac-1 receptor activation and inflammation. Nat. Nanotechnol. 6, 39–44 (2011). · DOI · Paper page
  62. Li, M. et al. Nanoparticle elasticity affects systemic circulation lifetime by modulating adsorption of apolipoprotein A-I in corona formation. Nat. Commun. 13, 4137 (2022). The protein corona analysis of lipid-based core-shell NPs reveales that apolipoprotein A1 correlated with blood clearance lifetimes of elastic NPs. · DOI
  63. Tenzer, S. et al. Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology. Nat. Nanotechnol. 8, 772–781 (2013). · DOI · Paper page
  64. Carril, M. et al. In situ detection of the protein corona in complex environments. Nat. Commun. 8, 1542 (2017). · DOI
  65. Milani, S., Baldelli Bombelli, F., Pitek, A. S., Dawson, K. A. & Rädler, J. Reversible versus irreversible binding of transferrin to polystyrene nanoparticles: soft and hard corona. ACS Nano 6, 2532–2541 (2012). · DOI · Paper page
  66. Kokkinopoulou, M., Simon, J., Landfester, K., Mailänder, V. & Lieberwirth, I. Visualization of the protein corona: towards a biomolecular understanding of nanoparticle–cell interactions. Nanoscale 9, 8858–8870 (2017). · DOI · Paper page
  67. De, M., You, C. C., Srivastava, S. & Rotello, V. M. Biomimetic interactions of proteins with functionalized nanoparticles: a thermodynamic study. J. Am. Chem. Soc. 129, 10747–10753 (2007). · DOI · Paper page
  68. Vilanova, O. et al. Understanding the kinetics of protein–nanoparticle corona formation. ACS Nano 10, 10842–10850 (2016). · DOI · Paper page
  69. Zhang, Y., Wu, J. L. Y., Lazarovits, J. & Chan, W. C. W. An analysis of the binding function and structural organization of the protein corona. J. Am. Chem. Soc. 142, 8827–8836 (2020). · DOI
  70. Mohammad-Beigi, H. et al. Mapping and identification of soft corona proteins at nanoparticles and their impact on cellular association. Nat. Commun. 11, 4535 (2020). By utilizing in situ click chemistry, the interactions between soft corona proteins and cellular interfaces are analysed. This study confirms that although soft corona proteins can also comprise the hard corona, soft corona proteins modulate NP–cell interactions owing to their dynamic nature. · DOI · Paper page
  71. Baimanov, D. et al. In situ analysis of nanoparticle soft corona and dynamic evolution. Nat. Commun. 13, 5389 (2022). In this study, chiral NPs differentiate soft and hard corona proteins and suggest that protein corona formation is stereo-specific. Chirality-dependent protein coronas are found to mediate different NP blood circulation lifetimes, suggesting that protein coronas evolve in vivo leading to rapid clearance from circulation. · DOI · Paper page
  72. Liu, J., Sonshine, D. A., Shervani, S. & Hurt, R. H. Controlled release of biologically active silver from nanosilver surfaces. ACS Nano 4, 6903–6913 (2010). · DOI · Paper page
  73. Levard, C. et al. Sulfidation of silver nanoparticles: natural antidote to their toxicity. Environ. Sci. Technol. 47, 13440–13448 (2013). · DOI · Paper page
  74. Miclāuş, T. et al. Dynamic protein coronas revealed as a modulator of silver nanoparticle sulphidation in vitro. Nat. Commun. 7, 11770 (2016). · DOI · Paper page
  75. Yin, H. et al. Reducing the cytotoxicity of ZnO nanoparticles by a pre-formed protein corona in a supplemented cell culture medium. RSC Adv. 5, 73963–73973 (2015). · DOI
  76. Duan, G. et al. Protein corona mitigates the cytotoxicity of graphene oxide by reducing its physical interaction with cell membrane. Nanoscale 7, 15214–15224 (2015). · DOI · Paper page
  77. Leibe, R. et al. The protein corona suppresses the cytotoxic and pro-inflammatory response in lung epithelial cells and macrophages upon exposure to nanosilica. Arch. Toxicol. 93, 871–885 (2019). · DOI
  78. Coreas, R. et al. Biological impacts of reduced graphene oxide affected by protein corona formation. Chem. Res. Toxicol. 35, 1244–1256 (2022). · doi:10.1021/acs.chemrestox.2c00042
  79. Barbalinardo, M., Caicci, F., Cavallini, M. & Gentili, D. Protein corona mediated uptake and cytotoxicity of silver nanoparticles in mouse embryonic fibroblast. Small 14, 1801219 (2018). · DOI
  80. Li, Y. et al. Protein corona of airborne nanoscale PM2.5 induces aberrant proliferation of human lung fibroblasts based on a 3D organotypic culture. Sci. Rep. 8, 1939 (2018). · DOI
  81. Liu, N., Tang, M. & Ding, J. The interaction between nanoparticles–protein corona complex and cells and its toxic effect on cells. Chemosphere 245, 125624 (2020). · DOI · Paper page
  82. De Paoli, S. H. et al. The effect of protein corona composition on the interaction of carbon nanotubes with human blood platelets. Biomaterials 35, 6182–6194 (2014). · DOI
  83. Yan, Y. et al. Differential roles of the protein corona in the cellular uptake of nanoporous polymer particles by monocyte and macrophage cell lines. ACS Nano 7, 10960–10970 (2013). · DOI · Paper page
  84. Park, J. Y. et al. Unfolded protein corona surrounding nanotubes influence the innate and adaptive immune system. Adv. Sci. 8, 2004979 (2021). · DOI
  85. Latreille, P. L. et al. Scratching the surface of the protein corona: challenging measurements and controversies. ACS Nano 16, 1689–1707 (2022). · DOI
  86. Moein Moghimi, S., Simberg, D., Skotland, T., Yaghmur, A. & Christy Hunter, A. The interplay between blood proteins, complement, and macrophages on nanomedicine performance and responses. J. Pharmacol. Exp. Ther. 370, 581–592 (2019). · DOI
  87. Moghimi, S. M., Simberg, D., Papini, E. & Farhangrazi, Z. S. Complement activation by drug carriers and particulate pharmaceuticals: principles, challenges and opportunities. Adv. Drug Deliv. Rev. 157, 83–95 (2020). · DOI
  88. Ashkarran, A. A., Dararatana, N., Crespy, D., Caracciolo, G. & Mahmoudi, M. Mapping the heterogeneity of protein corona by ex vivo magnetic levitation. Nanoscale 12, 2374–2383 (2020). · DOI
  89. Forest, V. & Pourchez, J. The nanoparticle protein corona: the myth of average. Nano Today 11, 700–703 (2016). · DOI
  90. Levsky, J. Gene expression and the myth of the average cell. Trends Cell Biol. 13, 4–6 (2003). · DOI · Paper page
  91. Leong, H. S. et al. On the issue of transparency and reproducibility in nanomedicine. Nat. Nanotechnol. 14, 629–635 (2019). · DOI · Paper page
  92. Moyano, D. F. et al. Fabrication of corona-free nanoparticles with tunable hydrophobicity. ACS Nano 8, 6748–6755 (2014). · DOI · Paper page
  93. Safavi-Sohi, R. et al. Bypassing protein corona issue on active targeting: zwitterionic coatings dictate specific interactions of targeting moieties and cell receptors. ACS Appl. Mater. Interfaces 8, 22808–22818 (2016). · DOI
  94. Pattipeiluhu, R. et al. Unbiased identification of the liposome protein corona using photoaffinity-based chemoproteomics. ACS Cent. Sci. 6, 535–545 (2020). · DOI
  95. Schöttler, S. et al. Protein adsorption is required for stealth effect of poly(ethylene glycol)- and poly(phosphoester)-coated nanocarriers. Nat. Nanotechnol. 11, 372–377 (2016). · DOI · Paper page
  96. Torchilin, V. P., Berdichevsky, V. R., Barsukov, A. A. & Smirnov, V. N. Coating liposomes with protein decreases their capture by macrophages. FEBS Lett. 111, 184–1888 (1980). · DOI
  97. Tonigold, M. et al. Pre-adsorption of antibodies enables targeting of nanocarriers despite a biomolecular corona. Nat. Nanotechnol. 13, 862–869 (2018). · DOI · Paper page
  98. Stordy, B. et al. Conjugating ligands to an equilibrated nanoparticle protein corona enables cell targeting in serum. Chem. Mater. 34, 6868–6882 (2022). · DOI
  99. Mahmoudi, M. The need for improved methodology in protein corona analysis. Nat. Commun. 13, 49 (2022). This comment remarks on the need to improve methodologies for protein corona characterization that enhance reproducibility and transparency in nanomedicine, outlines common sources of errors within methodology and data analysis and elaborates on how methodological errors can be reduced. · DOI
  100. Cabaleiro-Lago, C. et al. Inhibition of amyloid β protein fibrillation by polymeric nanoparticles. J. Am. Chem. Soc. 130, 15437–15443 (2008). · DOI · Paper page
  101. Linse, S. et al. Nucleation of protein fibrillation by nanoparticles. Proc. Natl Acad. Sci. USA 104, 8691–8696 (2007). · DOI · Paper page
  102. McClain, S. M., Ojoawo, A. M., Lin, W., Rienstra, C. M. & Murphy, C. J. Interaction of alpha-synuclein and its mutants with rigid lipid vesicle mimics of varying surface curvature. ACS Nano 14, 10153–10167 (2020). · DOI
  103. Mahmoudi, M. et al. The protein corona mediates the impact of nanomaterials and slows amyloid beta fibrillation. ChemBioChem 14, 568–572 (2013). · DOI
  104. Sharifi, S., Caracciolo, G. & Mahmoudi, M. Biomolecular corona affects controlled release of drug payloads from nanocarriers. Trends Pharmacol. Sci. 41, 641–652 (2020). · DOI
  105. Mahmoudi, M. The need for robust characterization of nanomaterials for nanomedicine applications. Nat. Commun. 12, 526 (2021). This comment emphasizes the necessity of standardization in protein corona research to develop more efficient nanomedicines. Checklists, such as MIRIBEL (Minimum Information Reporting in Bio–Nano Experimental Literature), can improve the reliability and robustness of nanomedicine research. · DOI
  106. Zimmerman, L. J., Li, M., Yarbrough, W. G., Slebos, R. J. C. & Liebler, D. C. Global stability of plasma proteomes for mass spectrometry-based analyses. Mol. Cell. Proteom. 11, M111.014340 (2012). · DOI
  107. Ostroff, R. et al. The stability of the circulating human proteome to variations in sample collection and handling procedures measured with an aptamer-based proteomics array. J. Proteom. 73, 649–666 (2010). · DOI
  108. Gibb, B. C. Reproducibility. Nat. Chem. 6, 653–654 (2014). · doi:10.1038/nchem.2017
  109. Ashkarran, A. et al. Measurements of heterogeneity in proteomics analysis of nanoparticle protein corona across core facilities. Nat. Commun. 13, 6610 (2022). Variations in the protein corona analysis are investigated by sending identical corona samples to several proteomics core facilities and analysing resultant LC–MS/MS data. Although data correlated well between core facilities, the authors observed considerable heterogeneity. This study supports the need to develop protocols that improve protein corona characterization. · DOI
  110. Bondarenko, O. et al. Nanotoxicology and nanomedicine: the Yin and Yang of nano–bio interactions for the new decade. Nano Today 39, 101184 (2021). · DOI
  111. Westmeier, D., Stauber, R. H. & Docter, D. The concept of bio-corona in modulating the toxicity of engineered nanomaterials (ENM). Toxicol. Appl. Pharmacol. 299, 53–57 (2016). · DOI
  112. Sharifi, S., Mahmoud, N. N., Voke, E., Landry, M. P. & Mahmoudi, M. Importance of standardizing analytical characterization methodology for improved reliability of the nanomedicine literature. Nano Micro Lett. 14, 172 (2022). This perspective highlights how standardized protocols for protein corona analysis can improve NP–biological interface data reproducibility and clinical translation of nanotechnologies. Implementation of standardized protocols for protein corona research involves several stakeholders including research institutions, trainees and funding agencies. · DOI
  113. Findlay, M. R., Freitas, D. N., Mobed-Miremadi, M. & Wheeler, K. E. Machine learning provides predictive analysis into silver nanoparticle protein corona formation from physicochemical properties. Environ. Sci. Nano 5, 64–71 (2018). Machine learning is used to predict protein corona formation using few NP physicochemical properties and several protein characteristics as features. This study finds that protein features, and not NP physicochemical features, are more influential in predicting protein corona formation. · DOI
  114. Duan, Y. et al. Prediction of protein corona on nanomaterials by machine learning using novel descriptors. NanoImpact 17, 100207 (2020). Fluorescamine-labelled protein coronas are utilized as unique NP features to build random forest classifiers that could predict protein corona formation. These unique NP features are able to predict protein corona formation on 2D heterogeneous nanomaterials. · DOI
  115. Ban, Z. et al. Machine learning predicts the functional composition of the protein corona and the cellular recognition of nanoparticles. Proc. Natl Acad. Sci. USA 117, 10492–10499 (2020). In this study, machine learning is used to predict functional proteins on NP protein coronas that are correlated with cellular associations. Protein corona composition is also predicted, and NP surface functionalization is found to be the most important factor that influenced the predictive power of the model. · DOI · Paper page
  116. Walkey, C. D. et al. Protein corona fingerprinting predicts the cellular interaction of gold and silver nanoparticles. ACS Nano 8, 2439–2455 (2014). · DOI · Paper page
  117. Liu, R., Jiang, W., Walkey, C. D., Chan, W. C. W. & Cohen, Y. Prediction of nanoparticles–cell association based on corona proteins and physicochemical properties. Nanoscale 7, 9664–9675 (2015). · DOI
  118. Lazarovits, J. et al. Supervised learning and mass spectrometry predicts the in vivo fate of nanomaterials. ACS Nano 13, 8023–8034 (2019). · DOI · Paper page
  119. Fourches, D. et al. Quantitative nanostructure–activity relationship modeling. ACS Nano 4, 5703–5712 (2010). · DOI · Paper page
  120. Yamankurt, G. et al. Exploration of the nanomedicine-design space with high-throughput screening and machine learning. Nat. Biomed. Eng. 3, 318–327 (2019). · DOI · Paper page
  121. Li, G. et al. Coronavirus infections and immune responses. J. Med. Virol. 92, 424–432 (2020). · DOI · Paper page
  122. Igakura, T. et al. Spread of HTLV-I between lymphocytes by virus-induced polarization of the cytoskeleton. Science 299, 1713–1716 (2003). · DOI · Paper page
  123. Merad, M., Blish, C. A., Sallusto, F. & Iwasaki, A. The immunology and immunopathology of COVID-19. Science 375, 1122–1127 (2022). · DOI · Paper page
  124. Akinc, A. et al. The Onpattro story and the clinical translation of nanomedicines containing nucleic acid-based drugs. Nat. Nanotechnol. 14, 1084–1087 (2019). · DOI · Paper page
  125. Joshi, A. S., Zhang, H. & Prinz, W. A. Organelle biogenesis in the endoplasmic reticulum. Nat. Cell Biol. 19, 876–882 (2017). · DOI
  126. Shpilka, T. & Haynes, C. M. The mitochondrial UPR: mechanisms, physiological functions and implications in ageing. Nat. Rev. Mol. Cell Biol. 19, 109–120 (2018). · DOI · Paper page
  127. Hajipour, M. J. et al. Sex as an important factor in nanomedicine. Nat. Commun. 12, 2984 (2021). · DOI
  128. Bartleson, J. M. et al. SARS-CoV-2, COVID-19 and the aging immune system. Nat. Aging 1, 769–782 (2021). · DOI · Paper page
  129. Takahashi, T. et al. Sex differences in immune responses that underlie COVID-19 disease outcomes. Nature 588, 315–320 (2020). · DOI · Paper page
  130. Lundqvist, M. et al. The evolution of the protein corona around nanoparticles: a test study. ACS Nano 5, 7503–7509 (2011). · DOI · Paper page
  131. Schleh, C. et al. Size and surface charge of gold nanoparticles determine absorption across intestinal barriers and accumulation in secondary target organs after oral administration. Nanotoxicology 6, 36–46 (2012). · DOI · Paper page
  132. Papafilippou, L., Claxton, A., Dark, P., Kostarelos, K. & Hadjidemetriou, M. Nanotools for sepsis diagnosis and treatment. Adv. Healthc. Mater. 10, e2001378 (2021). · DOI · Paper page
  133. Digiacomo, L. et al. Efficient pancreatic cancer detection through personalized protein corona of gold nanoparticles. Biointerphases 16, 011010 (2021). · DOI
  134. Barui, A. K., Oh, J. Y., Jana, B., Kim, C. & Ryu, J. Cancer‐targeted nanomedicine: overcoming the barrier of the protein corona. Adv. Ther. 3, 1900124 (2020). · DOI
  135. Ju, Y. et al. Person-specific biomolecular coronas modulate nanoparticle interactions with immune cells in human blood. ACS Nano 14, 15723–15737 (2020). · DOI
  136. Aguado, B. A., Grim, J. C., Rosales, A. M., Watson-Capps, J. J. & Anseth, K. S. Engineering precision biomaterials for personalized medicine. Sci. Transl Med. 10, eaam8645 (2018). · DOI · Paper page
  137. Lazarovits, J. et al. Synthesis of patient-specific nanomaterials. Nano Lett. 19, 116–123 (2019). · DOI
  138. Atkinson, S. P., Andreu, Z. & Vicent, M. J. Polymer therapeutics: biomarkers and new approaches for personalized cancer treatment. J. Pers. Med. 8, 6 (2018). · DOI
  139. Askim, J. R., Mahmoudi, M. & Suslick, K. S. Optical sensor arrays for chemical sensing: the optoelectronic nose. Chem. Soc. Rev. 42, 8649–8682 (2013). · DOI · Paper page
  140. Mahmoudi, M., Lohse, S. E., Murphy, C. J. & Suslick, K. S. Identification of nanoparticles with a colorimetric sensor array. ACS Sens. 1, 17–21 (2016). · DOI
  141. Lin, Y. T. et al. Global plasma metabolomics to identify potential biomarkers of blood pressure progression. Arterioscler. Thromb. Vasc. Biol. 40, E227–E237 (2020). · DOI
  142. Tavakol, M. et al. Disease-related metabolites affect protein–nanoparticle interactions. Nanoscale 10, 7108–7115 (2018). · DOI
  143. Palchetti, S. et al. Effect of glucose on liposome–plasma protein interactions: relevance for the physiological response of clinically approved liposomal formulations. Adv. Biosyst. 3, e1800221 (2019). · DOI
  144. Maurer-Jones, M. A., Gunsolus, I. L., Murphy, C. J. & Haynes, C. L. Toxicity of engineered nanoparticles in the environment. Anal. Chem. 85, 3036–3049 (2013). · DOI · Paper page
  145. Mueller, N. C. & Nowack, B. Exposure modeling of engineered nanoparticles in the environment. Environ. Sci. Technol. 42, 4447–4453 (2008). · DOI · Paper page
  146. Shahul Hamid, F. et al. Worldwide distribution and abundance of microplastic: how dire is the situation? Waste Manag. Res. 36, 873–897 (2018). · DOI · Paper page
  147. Demirer, G. S. et al. High aspect ratio nanomaterials enable delivery of functional genetic material without DNA integration in mature plants. Nat. Nanotechnol. 14, 456–464 (2019). · DOI · Paper page
  148. Zhang, H. et al. Nanoparticle cellular internalization is not required for RNA delivery to mature plant leaves. Nat. Nanotechnol. 17, 197–205 (2022). · doi:10.1038/s41565-021-01018-8
  149. Thabet, A. F. et al. Silica nanoparticles as pesticide against insects of different feeding types and their non-target attraction of predators. Sci. Rep. 11, 14484 (2021). · doi:10.1038/s41598-021-93518-9
  150. Nasser, F. & Lynch, I. Secreted protein eco-corona mediates uptake and impacts of polystyrene nanoparticles on Daphnia magna. J. Proteom. 137, 45–51 (2016). · DOI · Paper page
  151. Ong, K. J. et al. Humic acid ameliorates nanoparticle-induced developmental toxicity in zebrafish. Environ. Sci. Nano 4, 127–137 (2017). · doi:10.1039/c6en00408c
  152. Fadare, O. O. et al. Humic acid alleviates the toxicity of polystyrene nanoplastic particles to: Daphnia magna. Environ. Sci. Nano 6, 1466–1477 (2019). · DOI
  153. Lipczynska-Kochany, E. Humic substances, their microbial interactions and effects on biological transformations of organic pollutants in water and soil: a review. Chemosphere 202, 420–437 (2018). · DOI · Paper page
  154. Liu, F. et al. Modulation of cell uptake and cytotoxicity by nanoparticles with various physicochemical properties after humic acid adsorption. Environ. Sci. Nano 8, 3746–3761 (2021). · DOI
  155. Markiewicz, M. et al. Changing environments and biomolecule coronas: consequences and challenges for the design of environmentally acceptable engineered nanoparticles. Green. Chem. 20, 4133–4168 (2018). · DOI
  156. Radic, S. et al. Competitive binding of natural amphiphiles with graphene derivatives. Sci. Rep. 3, 2273 (2013). · DOI
  157. Xu, L. et al. The crucial role of environmental coronas in determining the biological effects of engineered nanomaterials. Small 16, e2003691 (2020). · DOI
  158. Wang, Z., Zhang, L., Zhao, J. & Xing, B. Environmental processes and toxicity of metallic nanoparticles in aquatic systems as affected by natural organic matter. Environ. Sci. Nano 3, 240–255 (2016). · DOI · Paper page
  159. Ekvall, M. T. et al. Adsorption of bio-organic eco-corona molecules reduces the toxic response to metallic nanoparticles in Daphnia magna. Sci. Rep. 11, 10784 (2021). · DOI
  160. Gunsolus, I. L., Mousavi, M. P. S., Hussein, K., Bühlmann, P. & Haynes, C. L. Effects of humic and fulvic acids on silver nanoparticle stability, dissolution, and toxicity. Environ. Sci. Technol. 49, 8078–8086 (2015). · DOI
  161. Voke, E., Pinals, R. L., Goh, N. S. & Landry, M. P. In planta nanosensors: understanding biocorona formation for functional design. ACS Sens. 6, 2802–2814 (2021). · DOI
  162. Buchman, J. T., Hudson-Smith, N. V., Landy, K. M. & Haynes, C. L. Understanding nanoparticle toxicity mechanisms to inform redesign strategies to reduce environmental impact. Acc. Chem. Res. 52, 1632–1642 (2019). · DOI · Paper page
  163. Priester, J. H. et al. Soybean susceptibility to manufactured nanomaterials with evidence for food quality and soil fertility interruption. Proc. Natl Acad. Sci. USA 109, 2451–2456 (2012). · DOI · Paper page
  164. Zhu, H., Han, J., Xiao, J. Q. & Jin, Y. Uptake, translocation, and accumulation of manufactured iron oxide nanoparticles by pumpkin plants. J. Environ. Monit. 10, 713–717 (2008). · DOI · Paper page
  165. Lin, D. & Xing, B. Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environ. Pollut. 150, 243–250 (2007). · DOI · Paper page
  166. Thiele, C. J., Hudson, M. D., Russell, A. E., Saluveer, M. & Sidaoui-Haddad, G. Microplastics in fish and fishmeal: an emerging environmental challenge? Sci. Rep. 11, 2045 (2021). · DOI · Paper page
  167. Zhang, N., Li, Y. B., He, H. R., Zhang, J. F. & Ma, G. S. You are what you eat: microplastics in the feces of young men living in Beijing. Sci. Total Environ. 767, 144345 (2021). · DOI · Paper page
  168. Farvardin, A. et al. The apoplast: a key player in plant survival. Antioxidants 9, 604 (2020). · DOI
  169. Faria, M., Björnmalm, M., Crampin, E. J. & Caruso, F. A few clarifications on MIRIBEL. Nat. Nanotechnol. 15, 2–3 (2020). · DOI
  170. Faria, M. et al. Minimum information reporting in bio–nano experimental literature. Nat. Nanotechnol. 13, 777–785 (2018). · DOI · Paper page
  171. Lammers, T. & Storm, G. Setting standards to promote progress in bio–nano science. Nat. Nanotechnol. 14, 626 (2019). · DOI
  172. Nance, E., Pun, S. H., Saigal, R. & Sellers, D. L. Drug delivery to the central nervous system. Nat. Rev. Mater. 7, 314–331 (2022). · DOI · Paper page
  173. Liu, R. & Lal, R. Potentials of engineered nanoparticles as fertilizers for increasing agronomic productions. Sci. Total Environ. 514, 131–139 (2015). · DOI · Paper page
  174. Wang, L. et al. Silica nanoparticles activate defense responses by reducing reactive oxygen species under Ralstonia solanacearum infection in tomato plants. NanoImpact 28, 100418 (2022). · doi:10.1016/j.impact.2022.100418
  175. Keshishian, H. et al. Quantitative, multiplexed workflow for deep analysis of human blood plasma and biomarker discovery by mass spectrometry. Nat. Protoc. 12, 1683–1701 (2017). · DOI · Paper page
  176. Etzioni, R. et al. The case for early detection. Nat. Rev. Cancer 3, 243–252 (2003). · DOI · Paper page
  177. Cuzick, J. et al. Prevention and early detection of prostate cancer. Lancet Oncol. 15, e484–e492 (2014). · DOI · Paper page
  178. Geyer, P. E., Holdt, L. M., Teupser, D. & Mann, M. Revisiting biomarker discovery by plasma proteomics. Mol. Syst. Biol. 13, 942 (2017). · DOI · Paper page
  179. Jacobs, J. M. et al. Utilizing human blood plasma for proteomic biomarker discovery. J. Proteome Res. 4, 1073–1085 (2005). · DOI · Paper page
  180. Stastna, M. & Van Eyk, J. E. Secreted proteins as a fundamental source for biomarker discovery. Proteomics 12, 722–735 (2012). · DOI · Paper page
  181. Baalousha, M., Manciulea, A., Cumberland, S., Kendall, K. & Lead, J. R. Aggregation and surface properties of iron oxide nanoparticles: influence of pH and natural organic matter. Environ. Toxicol. Chem. 27, 1875–1882 (2008). · DOI · Paper page
  182. Partikel, K., Korte, R., Mulac, D., Humpf, H. U. & Langer, K. Serum type and concentration both affect the protein-corona composition of PLGA nanoparticles. Beilstein J. Nanotechnol. 10, 1002–1015 (2019). · DOI
  183. Cai, R. et al. Dynamic intracellular exchange of nanomaterials’ protein corona perturbs proteostasis and remodels cell metabolism. Proc. Natl Acad. Sci. USA 119, e2200363119 (2022). · DOI
  184. Albanese, A. et al. Secreted biomolecules alter the biological identity and cellular interactions of nanoparticles. ACS Nano 8, 5515–5526 (2014). · DOI · Paper page
  185. Briffa, S. M., Nasser, F., Valsami-Jones, E. & Lynch, I. Uptake and impacts of polyvinylpyrrolidone (PVP) capped metal oxide nanoparticles on Daphnia magna: role of core composition and acquired corona. Environ. Sci. Nano 5, 1745–1756 (2018). · DOI
  186. Grintzalis, K., Lawson, T. N., Nasser, F., Lynch, I. & Viant, M. R. Metabolomic method to detect a metabolite corona on amino-functionalized polystyrene nanoparticles. Nanotoxicology 13, 783–794 (2019). · DOI

Cited by

See all 625

Metadata

Authors
Mahmoudi, M., Landry, M. P., Moore, A., & Coreas, R.
Venue
Nature Reviews Materials
Publisher
Springer Science and Business Media LLC
Published
2023-03-24
Volume
8
Issue
7
Pages
422-438
ISSN
2058-8437 (ISSN-L)
DOI
10.1038/s41578-023-00552-2
OpenAlex
W4360849792
Cited by
625
References
28
FWCI
8.84
Type
journal article
Language
en
Open access
bronze
Licence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: The protein corona from nanomedicine to environmental science. https://app.cochat.ai/papers/10.1038/s41578-023-00552-2
The paper
Mahmoudi, M., Landry, M. P., Moore, A., & Coreas, R. (2023). The protein corona from nanomedicine to environmental science. Nature Reviews Materials. https://doi.org/10.1038/s41578-023-00552-2

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.