Skip to main content
SpringerLink
Log in

Mesoscopic simulations of protein corona formation on zwitterionic peptide-grafted gold nanoparticles

  • Research paper
  • Published:
Journal of Nanoparticle Research Aims and scope Submit manuscript

Abstract

Understanding protein corona formation on nanoparticle surface is crucial to broad applications of nanomedicine and nanotechnologies. In this work, we performed mesoscopic coarse-grained molecular dynamics simulations to study the effect of nanoparticle surface’s charge distribution on protein corona formation. Short peptide chains consisting of alternating oppositely charged amino acid residues were grafted on a gold nanoparticle surface to generate surface zwitterionic charge distribution and the ovispirin-1 peptide of high positive charge density was adopted as a model system to examine the zwitterionic nanoparticle’s antibiofouling activities. Our mesoscopic simulations showed that the mixing of opposite charges on the nanoparticle’s surface can significantly reduce the nanoparticle’s electrostatic interactions with ovispirin-1 peptides in water. The formation of protein corona on the gold nanoparticle surface is effectively slowed down by 27% compared to a bare gold nanoparticle, thanks to the grafted zwitterionic peptide chains that introduce enhanced interfacial hydration, reduce hydrophobic interactions between the gold nanoparticle’s core and ovispirin-1 peptides, and minimize electrostatic interactions. However, the presence of the small double charge layers as a result of the slightly selective adsorption of different amino acid residues, the local heterogeneity of charge distribution on the nanoparticle surface, and the nanoparticle-ovispirin-1 peptides hydrophobic interactions still result in a monolayer adsorption of ovispirin-1 peptides. Compared to a bare gold nanoparticle, ovispirin-1 peptides are more tilted on the zwitterionic nanoparticle surface.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Zhu Y-X, Jia H-R, Pan G-Y, Ulrich NW, Chen Z, Wu F-G (2018) Development of a light-controlled nanoplatform for direct nuclear delivery of molecular and nanoscale materials. J Am Chem Soc 140:4062–4070

    CAS  Google Scholar 

  2. Jeun M, Lee S, Kyeong Kang J, Tomitaka A, Wook Kang K, Il Kim Y, Takemura Y, Chung K-W, Kwak J, Bae S (2012) Physical limits of pure superparamagnetic Fe3O4 nanoparticles for a local hyperthermia agent in nanomedicine. Appl Phys Lett 100:092406

    Google Scholar 

  3. Gioria S, Caputo F, Urbán P, Maguire CM, Bremer-Hoffmann S, Prina-Mello A, Calzolai L, Mehn D (2018) Are existing standard methods suitable for the evaluation of nanomedicines: some case studies. Nanomedicine 13:539–554

    CAS  Google Scholar 

  4. Santiago-Cordoba MA, Boriskina SV, Vollmer F, Demirel MC (2011) Nanoparticle-based protein detection by optical shift of a resonant microcavity. Appl Phys Lett 99:073701

    Google Scholar 

  5. Zhou H, Yang D, Ivleva NP, Mircescu NE, Niessner R, Haisch C (2014) SERS detection of bacteria in water by in situ coating with Ag nanoparticles. Anal Chem 86:1525–1533

    CAS  Google Scholar 

  6. Ximendes E, Benayas A, Jaque D, Marin R (2021) Quo vadis, nanoparticle-enabled in vivo fluorescence imaging? ACS Nano 15:1917–1941

    CAS  Google Scholar 

  7. Walsh TR, Knecht MR (2017) Biointerface structural effects on the properties and applications of bioinspired peptide-based nanomaterials. Chem Rev 117:12641–12704

    CAS  Google Scholar 

  8. Singh J, Dutta T, Kim K-H, Rawat M, Samddar P, Kumar P (2018) ‘Green’synthesis of metals and their oxide nanoparticles: applications for environmental remediation. J Nanobiotechnol 16:1–24

    Google Scholar 

  9. Pasinszki T, Krebsz M (2020) Synthesis and application of zero-valent iron nanoparticles in water treatment, environmental remediation, catalysis, and their biological effects. Nanomaterials 10:917

    CAS  Google Scholar 

  10. Zhu ZJ, Posati T, Moyano DF, Tang R, Yan B, Vachet RW, Rotello VM (2012) The interplay of monolayer structure and serum protein interactions on the cellular uptake of gold nanoparticles. Small 8:2659–2663

    CAS  Google Scholar 

  11. Shang L, Yang L, Seiter J, Heinle M, Brenner-Weiss G, Gerthsen D, Nienhaus GU (2014) Nanoparticles interacting with proteins and cells: a systematic study of protein surface charge effects. Adv Mater Interfaces 1:1300079

    Google Scholar 

  12. Lesniak A, Fenaroli F, Monopoli MP, Åberg C, Dawson KA, Salvati A (2012) Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano 6:5845–5857

    CAS  Google Scholar 

  13. Lynch I, Dawson KA (2020) Protein–nanoparticle interactions. Nano-Enabled Med Appl 231–250

  14. Huang H, Zhang C, Crisci R, Lu T, Hung H-C, Sajib MSJ, Sarker P, Ma J, Wei T, Jiang S (2021) Strong surface hydration and salt resistant mechanism of a new nonfouling zwitterionic polymer based on protein stabilizer TMAO. J Am Chem Soc 143:16786–16795

    CAS  Google Scholar 

  15. Lau KHA, Sileika TS, Park SH, Sousa AM, Burch P, Szleifer I, Messersmith PB (2015) Molecular design of antifouling polymer brushes using sequence-specific peptoids. Adv Mater Interfaces 2:1400225

    Google Scholar 

  16. Zhang L, Cao Z, Bai T, Carr L, Ella-Menye J-R, Irvin C, Ratner BD, Jiang S (2013) Zwitterionic hydrogels implanted in mice resist the foreign-body reaction. Nat Biotechnol 31:553–556

    CAS  Google Scholar 

  17. Schultz M, Bendick J, Holm E, Hertel W (2011) Economic impact of biofouling on a naval surface ship. Biofouling 27:87–98

    CAS  Google Scholar 

  18. Casals E, Pfaller T, Duschl A, Oostingh GJ, Puntes V (2010) Time evolution of the nanoparticle protein corona. ACS Nano 4:3623–3632

    CAS  Google Scholar 

  19. Hühn D, Kantner K, Geidel C, Brandholt S, De Cock I, Soenen SJ, Rivera Gil P, Montenegro J-M, Braeckmans K, Mullen K (2013) Polymer-coated nanoparticles interacting with proteins and cells: focusing on the sign of the net charge. ACS Nano 7:3253–3263

    Google Scholar 

  20. Izak-Nau E, Voetz M, Eiden S, Duschl A, Puntes VF (2013) Altered characteristics of silica nanoparticles in bovine and human serum: the importance of nanomaterial characterization prior to its toxicological evaluation. Part Fibre Toxicol 10:1–12

    Google Scholar 

  21. Mortensen NP, Hurst GB, Wang W, Foster CM, Nallathamby PD, Retterer ST (2013) Dynamic development of the protein corona on silica nanoparticles: composition and role in toxicity. Nanoscale 5:6372–6380

    CAS  Google Scholar 

  22. Röcker C, Pötzl M, Zhang F, Parak WJ, Nienhaus GU (2009) A quantitative fluorescence study of protein monolayer formation on colloidal nanoparticles. Nat Nanotechnol 4:577–580

    Google Scholar 

  23. Le TS, Takahashi M, Isozumi N, Miyazato A, Hiratsuka Y, Matsumura K, Taguchi T, Maenosono S (2022) Quick and mild isolation of intact lysosomes using magnetic–plasmonic hybrid nanoparticles. ACS Nano 16:885–896

    CAS  Google Scholar 

  24. Palchetti S, Pozzi D, Capriotti AL, La Barbera G, Chiozzi RZ, Digiacomo L, Peruzzi G, Caracciolo G, Laganà A (2017) Influence of dynamic flow environment on nanoparticle-protein corona: from protein patterns to uptake in cancer cells. Colloids Surf B: Biointerfaces 153:263–271

    CAS  Google Scholar 

  25. Caracciolo G, Farokhzad OC, Mahmoudi M (2017) Biological identity of nanoparticles in vivo: clinical implications of the protein corona. Trends Biotechnol 35:257–264

    CAS  Google Scholar 

  26. Forest V, Cottier M, Pourchez J (2015) Electrostatic interactions favor the binding of positive nanoparticles on cells: A reductive theory. Nano Today 10:677–680

    CAS  Google Scholar 

  27. Zhdanov VP (2019) Formation of a protein corona around nanoparticles. Curr Opin Colloid Interface Sci 41:95–103

    CAS  Google Scholar 

  28. Jahan Sajib MS, Sarker P, Wei Y, Tao X, Wei T (2020) Protein corona on gold nanoparticles studied with coarse-grained simulations. Langmuir 36:13356–13363

    CAS  Google Scholar 

  29. Sarker P, Sajib MSJ, Tao X, Wei T (2022) Multiscale simulation of protein corona formation on silver nanoparticles: study of ovispirin-1 peptide adsorption. J Phys Chem B 126:601–608

    CAS  Google Scholar 

  30. Wei T, Carignano MA, Szleifer I (2012) Molecular dynamics simulation of lysozyme adsorption/desorption on hydrophobic surfaces. J Phys Chem B 116:10189–10194

    CAS  Google Scholar 

  31. Ramezani F, Rafii-Tabar H (2015) An in-depth view of human serum albumin corona on gold nanoparticles. Mol BioSyst 11:454–462

    CAS  Google Scholar 

  32. Jahan Sajib MS, Wei Y, Mishra A, Zhang L, Nomura K-I, Kalia RK, Vashishta P, Nakano A, Murad S, Wei T (2020) Atomistic simulations of biofouling and molecular transfer of a cross-linked aromatic polyamide membrane for desalination. Langmuir 36:7658–7668

    CAS  Google Scholar 

  33. Zhang T, Wei T, Han Y, Ma H, Samieegohar M, Chen P-W, Lian I, Lo Y-H (2016) Protein–ligand interaction detection with a novel method of transient induced molecular electronic spectroscopy (TIMES): experimental and theoretical studies. ACS Cent Sci 2:834–842

    CAS  Google Scholar 

  34. Wei T, Zhang L, Zhao H, Ma H, Sajib MSJ, Jiang H, Murad S (2016) Aromatic polyamide reverse-osmosis membrane: an atomistic molecular dynamics simulation. J Phys Chem B 120:10311–10318

    CAS  Google Scholar 

  35. Nakano CM, Ma H, Wei T (2015) Study of lysozyme mobility and binding free energy during adsorption on a graphene surface. Appl Phys Lett 106:153701

    Google Scholar 

  36. Wei T, Sajib MSJ, Samieegohar M, Ma H, Shing K (2015) Self-assembled monolayers of an azobenzene derivative on silica and their interactions with lysozyme. Langmuir 31:13543–13552

    CAS  Google Scholar 

  37. Yu G, Zhou J (2016) Understanding the curvature effect of silica nanoparticles on lysozyme adsorption orientation and conformation: a mesoscopic coarse-grained simulation study. Phys Chem Chem Phys 18:23500–23507

    CAS  Google Scholar 

  38. Quan X, Peng C, Zhao D, Li L, Fan J, Zhou J (2017) Molecular understanding of the penetration of functionalized gold nanoparticles into asymmetric membranes. Langmuir 33:361–371

    CAS  Google Scholar 

  39. Sarker P, Chen GT, Sajib MSJ, Jones NW, Wei T (2022) Hydration and antibiofouling of TMAO-derived zwitterionic polymers surfaces studied with atomistic molecular dynamics simulations. Colloids Surf A Physicochem Eng Asp 653:129943

    CAS  Google Scholar 

  40. Lopez H, Lobaskin V (2015) Coarse-grained model of adsorption of blood plasma proteins onto nanoparticles. J Chem Phys 143:12B620_621

    Google Scholar 

  41. Samieegohar M, Ma H, Sha F, Jahan Sajib MS, Guerrero-García GI, Wei T (2017) Understanding the interfacial behavior of lysozyme on Au (111) surfaces with multiscale simulations. Appl Phys Lett 110:073703

    Google Scholar 

  42. Zheng S, Sajib MSJ, Wei Y, Wei T (2021) Discontinuous molecular dynamics simulations of biomolecule interfacial behavior: study of ovispirin-1 adsorption on a graphene surface. J Chem Theory Comput 17:1874–1882

    CAS  Google Scholar 

  43. Wei T, Kaewtathip S, Shing K (2009) Buffer effect on protein adsorption at liquid/solid interface. J Phys Chem C 113:2053–2062

    CAS  Google Scholar 

  44. Chen J, Xu E, Wei Y, Chen M, Wei T, Zheng S (2022) Graph clustering analyses of discontinuous molecular dynamics simulations: study of lysozyme adsorption on a graphene surface. Langmuir 38:10817–10825

    CAS  Google Scholar 

  45. Giri K, Shameer K, Zimmermann MT, Saha S, Chakraborty PK, Sharma A, Arvizo RR, Madden BJ, Mccormick DJ, Kocher J-PA (2014) Understanding protein–nanoparticle interaction: a new gateway to disease therapeutics. Bioconjug Chem 25:1078–1090

    CAS  Google Scholar 

  46. Tavanti F, Pedone A, Menziani MC (2015) A closer look into the ubiquitin corona on gold nanoparticles by computational studies. New J Chem 39:2474–2482

    CAS  Google Scholar 

  47. Molino PJ, Yang D, Penna M, Miyazawa K, Knowles BR, MacLaughlin S, Fukuma T, Yarovsky I, Higgins MJ (2018) Hydration layer structure of biofouling-resistant nanoparticles. ACS Nano 12:11610–11624

    CAS  Google Scholar 

  48. Erfani A, Seaberg J, Aichele CP, Ramsey JD (2020) Interactions between biomolecules and zwitterionic moieties: a review. Biomacromolecules 21:2557–2573

    CAS  Google Scholar 

  49. Li Q, Wen C, Yang J, Zhou X, Zhu Y, Zheng J, Cheng G, Bai J, Xu T, Ji J (2022) Zwitterionic biomaterials. Chem Rev 122:17073–17154

    CAS  Google Scholar 

  50. Yuan Z, McMullen P, Luozhong S, Sarker P, Tang C, Wei T, Jiang S (2023) Hidden hydrophobicity impacts polymer immunogenicity. Chem Sci 14:2033–2039

    CAS  Google Scholar 

  51. Aramesh M, Shimoni O, Ostrikov K, Prawer S, Cervenka J (2015) Surface charge effects in protein adsorption on nanodiamonds. Nanoscale 7:5726–5736

    CAS  Google Scholar 

  52. Lima AC, Reis RL, Ferreira H, Neves NM (2021) Cellular uptake of three different nanoparticles in an inflammatory arthritis scenario versus normal conditions. Mol Pharm 18:3235–3246

    CAS  Google Scholar 

  53. Wang Q, Chen W-Q, Liu X-Y, Liu Y, Jiang F-L (2021) Thermodynamic implications and time evolution of the interactions of near-infrared PbS quantum dots with human serum albumin. ACS omega 6:5569–5581

    CAS  Google Scholar 

  54. Mousseau F, Puisney C, Mornet S, Le Borgne R, Vacher A, Airiau M, Baeza-Squiban A, Berret J-F (2017) Supported pulmonary surfactant bilayers on silica nanoparticles: formulation, stability and impact on lung epithelial cells. Nanoscale 9:14967–14978

    CAS  Google Scholar 

  55. Rezwan K, Studart AR, Vörös J, Gauckler LJ (2005) Change of ζ potential of biocompatible colloidal oxide particles upon adsorption of bovine serum albumin and lysozyme. J Phys Chem B 109:14469–14474

    CAS  Google Scholar 

  56. Abraham MJ, Murtola T, Schulz R, Páll S, Smith JC, Hess B, Lindahl E (2015) GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1:19–25

    Google Scholar 

  57. Monticelli L, Kandasamy SK, Periole X, Larson RG, Tieleman DP, Marrink S-J (2008) The MARTINI coarse-grained force field: extension to proteins. J Chem Theory Comput 4:819–834

    CAS  Google Scholar 

  58. Song B, Yuan H, Jameson CJ, Murad S (2012) Role of surface ligands in nanoparticle permeation through a model membrane: a coarse-grained molecular dynamics simulations study. Mol Phys 110:2181–2195

    CAS  Google Scholar 

  59. Lin J, Zhang H, Chen Z, Zheng Y (2010) Penetration of lipid membranes by gold nanoparticles: insights into cellular uptake, cytotoxicity, and their relationship. ACS Nano 4:5421–5429

    CAS  Google Scholar 

  60. Hossain SI, Gandhi NS, Hughes ZE, Saha SC (2020) The role of SP-B 1–25 peptides in lung surfactant monolayers exposed to gold nanoparticles. Phys Chem Chem Phys 22:15231–15241

    CAS  Google Scholar 

  61. de Jong DH, Singh G, Bennett WD, Arnarez C, Wassenaar TA, Schafer LV, Periole X, Tieleman DP, Marrink SJ (2013) Improved parameters for the martini coarse-grained protein force field. J Chem Theory Comput 9:687–697

    Google Scholar 

  62. Satulovsky J, Carignano M, Szleifer I (2000) Kinetic and thermodynamic control of protein adsorption. Proc Natl Acad Sci USA 97:9037–9041

    CAS  Google Scholar 

Download references

Funding

T. Wei thank the grant support from National Science Foundation (NSF 1831559). T. Wei is indebted to computational resources from the program of Extreme Science and Engineering Discovery Environment (XSEDE) and the Texas Advanced Computing Center (TACC).

Author information

Authors and Affiliations

  1. Adlai E. Stevenson High School, Lincolnshire, IL, 60069, USA

    Grace Tang Chen

  2. Department of Chemical Engineering, Howard University, Washington, DC, 20059, USA

    Pranab Sarker & Tao Wei

  3. Department of Natural Sciences, Baruch College, City University of New York, NY, 10010, USA

    Baofu Qiao

Authors
  1. Grace Tang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pranab Sarker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Baofu Qiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tao Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: Grace Tang Chen, Pranab Sarker, Baofu Qiao Tao Wei; methodology: Grace Tang Chen, Pranab Sarker, Baofu Qiao, Tao Wei; formal analysis and investigation: Grace Tang Chen, Pranab Sarker, Baofu Qiao, Tao Wei; writing—original draft preparation: Grace Tang Chen, Pranab Sarker, Baofu Qiao, Tao Wei; writing—review and editing: Baofu Qiao, Pranab Sarker, Tao Wei; funding acquisition: Tao Wei; resources: Tao Wei, Baofu Qiao; supervision: Pranab Sarker, Baofu Qiao, Tao Wei.

Corresponding authors

Correspondence to Pranab Sarker, Baofu Qiao or Tao Wei.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(DOCX 3.93 MB)

(MPG 6646 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, G.T., Sarker, P., Qiao, B. et al. Mesoscopic simulations of protein corona formation on zwitterionic peptide-grafted gold nanoparticles. J Nanopart Res 25, 108 (2023). https://doi.org/10.1007/s11051-023-05761-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11051-023-05761-y

Keywords

Search

Navigation