Species differences take shape at nanoparticles: Protein corona made of the native repertoire assists cellular interaction

Environmental Science and Technology

Volumn 47, Issue 24, 2013, Pages 14367-14375

  Hayashi, Yuya ^a   Miclaus, Teodora ^a   Scavenius, Carsten ^a   Kwiatkowska, Katarzyna ^b   Sobota, Andrzej ^b   Engelmann, Péter ^c   Scott Fordsmand, Janeck J ^a   Enghild, Jan J ^a   Sutherland, Duncan S ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^c UNIVERSITY OF PÉCS   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

BIO-MOLECULAR; CELLULAR INTERACTION; EARTHWORM EISENIA FETIDA; FETAL BOVINE SERUM; IN-VITRO TESTING; PROTEIN CORONAS; REFERENCE MATERIAL; SILVER NANOPARTICLES;

NANOPARTICLES; PROTEINS; RISK ASSESSMENT;

SILVER;

COELOMIC PROTEIN; PROTEIN; SILVER NANOPARTICLE; UNCLASSIFIED DRUG;

BIOTECHNOLOGY; EARTHWORM; NANOTECHNOLOGY; PROTEIN; RECOMBINATION; RISK ASSESSMENT; SERUM; SILVER;

ARTICLE; CELL INTERACTION; CONTROLLED STUDY; EISENIA FETIDA; GENETIC CONSERVATION; MICROENVIRONMENT; NONHUMAN; SPECIES DIFFERENTIATION;

ANIMALS; CATTLE; CELL COMMUNICATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLOW CYTOMETRY; HUMANS; MOLECULAR WEIGHT; NANOPARTICLES; OLIGOCHAETA; PROTEINS; SILVER; SPECIES SPECIFICITY; TOXINS, BIOLOGICAL;

EID: 84890680515     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es404132w     Document Type: Article

References (46)

1. Lowry, G. V.; Gregory, K. B.; Apte, S. C.; Lead, J. R. Transformations of Nanomaterials in the Environment Environ. Sci. Technol. 2012, 46 (13) 6893-6899
2. Monopoli, M. P.; Aberg, C.; Salvati, A.; Dawson, K. A. Biomolecular coronas provide the biological identity of nanosized materials Nat. Nano 2012, 7 (12) 779-786
3. Shemetov, A. A.; Nabiev, I.; Sukhanova, A. Molecular Interaction of Proteins and Peptides with Nanoparticles ACS Nano 2012, 6 (6) 4585-4602
4. Chothia, C.; Gough, J.; Vogel, C.; Teichmann, S. A. Evolution of the Protein Repertoire Science 2003, 300 (5626) 1701-1703
5. Gebauer, J. S.; Malissek, M.; Simon, S.; Knauer, S. K.; Maskos, M.; Stauber, R. H.; Peukert, W.; Treuel, L. Impact of the Nanoparticle-Protein Corona on Colloidal Stability and Protein Structure Langmuir 2012, 28 (25) 9673-9679
6. Ding, F.; Radic, S.; Chen, R.; Chen, P.; Geitner, N. K.; Brown, J. M.; Ke, P. C. Direct observation of a single nanoparticle-ubiquitin corona formation Nanoscale 2013, 5, 9162-9169
7. 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 Lett. 2011, 11 (11) 4985-4991
8. Brown, D. M.; Dickson, C.; Duncan, P.; Al-Attili, F.; Stone, V. Interaction between nanoparticles and cytokine proteins: impact on protein and particle functionality Nanotechnology 2010, 21 (21) 215104
9. 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. Nano 2011, 6 (1) 39-44
10. 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) 9511-9518
11. 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
12. Hayashi, Y.; Engelmann, P.; Foldbjerg, R.; Szabó, M.; Somogyi, I.; Pollák, E.; Molnár, L.; Autrup, H.; Sutherland, D. S.; Scott-Fordsmand, J.; Heckmann, L.-H. Earthworms and Humans in Vitro: Characterizing Evolutionarily Conserved Stress and Immune Responses to Silver Nanoparticles Environ. Sci. Technol. 2012, 46 (7) 4166-4173
13. van der Ploeg, M. J.; van den Berg, J. H.; Bhattacharjee, S.; de Haan, L. H.; Ershov, D. S.; Fokkink, R. G.; Zuilhof, H.; Rietjens, I. M.; van den Brink, N. W. In vitro nanoparticle toxicity to rat alveolar cells and coelomocytes from the earthworm Lumbricus rubellus Nanotoxicology 2012, 10.3109/17435390. 2012.744857
14. 2) on Mytilus hemocytes Aquat. Toxicol. 2010, 96 (2) 151-158
15. Hayashi, Y.; Heckmann, L.-H.; Simonsen, V.; Scott-Fordsmand, J. J. Time-course profiling of molecular stress responses to silver nanoparticles in the earthworm Eisenia fetida Ecotoxicol. Environ. Saf. 2013, 98, 219-226
16. 60 exposure induced tissue damage and gene expression alterations in the earthworm Lumbricus rubellus Nanotoxicology 2013, 7 (4) 432-440
17. 60 nanoparticle exposure on earthworms (Lumbricus rubellus) and implications for population dynamics Environ. Pollut. 2011, 159 (1) 198-203
18. 2) Aquat. Toxicol. 2010, 100 (2) 168-177
19. Kasschau, M. R.; Ngo, T. D.; Sperber, L. M.; Tran, K. L. Formation of filopodia in earthworm (Lumbricus terrestris) coelomocytes in response to osmotic stress Zoology 2007, 110 (1) 66-76
20. 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
21. Lundqvist, M.; Stigler, J.; Cedervall, T.; BerggaÌŠrd, T.; Flanagan, M. B.; Lynch, I.; Elia, G.; Dawson, K. The Evolution of the Protein Corona around Nanoparticles: A Test Study ACS Nano 2011, 5 (9) 7503-7509
22. Monopoli, M. P.; Walczyk, D.; Campbell, A.; Elia, G.; Lynch, I.; Baldelli Bombelli, F.; Dawson, K. A. Physical-Chemical Aspects of Protein Corona: Relevance to in Vitro and in Vivo Biological Impacts of Nanoparticles J. Am. Chem. Soc. 2011, 133 (8) 2525-2534
23. Shevchenko, A.; Tomas, H.; Havlis, J.; Olsen, J. V.; Mann, M. In-gel digestion for mass spectrometric characterization of proteins and proteomes Nat. Protocols 2007, 1 (6) 2856-2860
24. Opper, B.; Bognár, A.; Heidt, D.; Németh, P.; Engelmann, P. Revising lysenin expression of earthworm coelomocytes Dev. Comp. Immunol. 2013, 39 (3) 214-218
25. Płytycz, B.; Homa, J.; Kozioł, B.; Rózanowska, M.; Morgan, A. J. Riboflavin content in autofluorescent earthworm coelomocytes is species-specific Folia Histochem. Cytobiol. 2006, 44 (4) 275-80
26. Kulma, M.; Hereć, M.; Grudziński, W.; Anderluh, G.; Gruszecki, W. I.; Kwiatkowska, K.; Sobota, A. Sphingomyelin-rich domains are sites of lysenin oligomerization: Implications for raft studies Biochim. Biophys. Acta 2010, 1798 (3) 471-481
27. Kauschke, E.; Mohrig, W.; Cooper, E. L. Coelomic fluid proteins as basic components of innate immunity in earthworms Eur. J. Soil Biol. 2007, 43, S110-S115
28. Casals, E.; Pfaller, T.; Duschl, A.; Oostingh, G. J.; Puntes, V. Time Evolution of the Nanoparticle Protein Corona ACS Nano 2010, 4 (7) 3623-3632
29. 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 Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (38) 14265-14270
30. Ashkarran, A. A.; Ghavami, M.; Aghaverdi, H.; Stroeve, P.; Mahmoudi, M. Bacterial Effects and Protein Corona Evaluations: Crucial Ignored Factors in the Prediction of Bio-Efficacy of Various Forms of Silver Nanoparticles Chem. Res. Toxicol. 2012, 25 (6) 1231-1242
31. Hirsh, S. L.; McKenzie, D. R.; Nosworthy, N. J.; Denman, J. A.; Sezerman, O. U.; Bilek, M. M. M. The Vroman effect: Competitive protein exchange with dynamic multilayer protein aggregates Colloids Surf., B 2013, 103, 395-404
32. De Colibus, L.; Sonnen, A. F. P.; Morris, K. J.; Siebert, C. A.; Abrusci, P.; Plitzko, J.; Hodnik, V.; Leippe, M.; Volpi, E.; Anderluh, G.; Gilbert, R. J. C. Structures of Lysenin Reveal a Shared Evolutionary Origin for Pore-Forming Proteins And Its Mode of Sphingomyelin Recognition Structure 2012, 20 (9) 1498-1507
33. Cooper, E. L.; Kvell, K.; Engelmann, P.; Nemeth, P. Still waiting for the toll? Immunol. Lett. 2006, 104 (1-2) 18-28
34. Hayashi, Y.; Engelmann, P. Earthworm's immunity in the nanomaterial world: new room, future challenges Invert. Surv. J. 2013, 10, 69-76
35. Beer, C.; Foldbjerg, R.; Hayashi, Y.; Sutherland, D. S.; Autrup, H. Toxicity of silver nanoparticles-Nanoparticle or silver ion? Toxicol. Lett. 2012, 208 (3) 286-292
36. Yang, X.; Gondikas, A. P.; Marinakos, S. M.; Auffan, M.; Liu, J.; Hsu-Kim, H.; Meyer, J. N. Mechanism of Silver Nanoparticle Toxicity Is Dependent on Dissolved Silver and Surface Coating in Caenorhabditis elegans Environ. Sci. Technol. 2011, 46 (2) 1119-1127
37. Suzuki, H.; Toyooka, T.; Ibuki, Y. Simple and easy method to evaluate uptake potential of nanoparticles in mammalian cells using a flow cytometric light scatter analysis Environ. Sci. Technol. 2007, 41 (8) 3018-3024
38. Toduka, Y.; Toyooka, T.; Ibuki, Y. Flow Cytometric Evaluation of Nanoparticles Using Side-Scattered Light and Reactive Oxygen Species-Mediated Fluorescence-Correlation with Genotoxicity Environ. Sci. Technol. 2012, 46 (14) 7629-7636
39. Lunov, O.; Syrovets, T.; Loos, C.; Beil, J.; Delacher, M.; Tron, K.; Nienhaus, G. U.; Musyanovych, A.; Mailänder, V.; Landfester, K.; Simmet, T. Differential Uptake of Functionalized Polystyrene Nanoparticles by Human Macrophages and a Monocytic Cell Line ACS Nano 2011, 5 (3) 1657-1669
40. dos Santos, T.; Varela, J.; Lynch, I.; Salvati, A.; Dawson, K. A. Effects of Transport Inhibitors on the Cellular Uptake of Carboxylated Polystyrene Nanoparticles in Different Cell Lines PLoS One 2011, 6 (9) e24438
41. Procházková, P.; Šilerová, M.; Felsberg, J.; Josková, R.; Beschin, A.; De Baetselier, P.; Bilej, M. Relationship between hemolytic molecules in Eisenia fetida earthworms Dev. Comp. Immunol. 2006, 30 (4) 381-392
42. Bruhn, H.; Winkelmann, J.; Andersen, C.; Andrä, J.; Leippe, M. Dissection of the mechanisms of cytolytic and antibacterial activity of lysenin, a defence protein of the annelid Eisenia fetida Dev. Comp. Immunol. 2006, 30 (7) 597-606
43. Bilej, M.; Procházková, P.; Šilerová, M.; Josková, R. Earthworm Immunity. In Invertebrate Immunity; Söderhäll, K., Ed.; Springer: New York, 2010; Vol. 708, pp 66-79.
44. 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 J. Am. Chem. Soc. 2013, 135 (4) 1438-1444
45. Engelmann, P.; Pálinkás, L.; Cooper, E. L.; Németh, P. Monoclonal antibodies identify four distinct annelid leukocyte markers Dev. Comp. Immunol. 2005, 29 (7) 599-614
46. Humphrey, W.; Dalke, A.; Schulten, K. VMD-Visual Molecular Dynamics J. Mol. Graph. Model. 1996, 14, 33-38