Remediation of Metal Oxide Nanotoxicity with a Functional Amyloid.

functional amyloid ion release metal oxide nanoparticle sequestration toxicity

Journal

Advanced science (Weinheim, Baden-Wurttemberg, Germany)
ISSN: 2198-3844
Titre abrégé: Adv Sci (Weinh)
Pays: Germany
ID NLM: 101664569

Informations de publication

Date de publication:
06 Apr 2024
Historique:
revised: 21 03 2024
received: 29 12 2023
medline: 7 4 2024
pubmed: 7 4 2024
entrez: 6 4 2024
Statut: aheadofprint

Résumé

Understanding the environmental health and safety of nanomaterials (NanoEHS) is essential for the sustained development of nanotechnology. Although extensive research over the past two decades has elucidated the phenomena, mechanisms, and implications of nanomaterials in cellular and organismal models, the active remediation of the adverse biological and environmental effects of nanomaterials remains largely unexplored. Inspired by recent developments in functional amyloids for biomedical and environmental engineering, this work shows their new utility as metallothionein mimics in the strategically important area of NanoEHS. Specifically, metal ions released from CuO and ZnO nanoparticles are sequestered through cysteine coordination and electrostatic interactions with beta-lactoglobulin (bLg) amyloid, as revealed by inductively coupled plasma mass spectrometry and molecular dynamics simulations. The toxicity of the metal oxide nanoparticles is subsequently mitigated by functional amyloids, as validated by cell viability and apoptosis assays in vitro and murine survival and biomarker assays in vivo. As bLg amyloid fibrils can be readily produced from whey in large quantities at a low cost, the study offers a crucial strategy for remediating the biological and environmental footprints of transition metal oxide nanomaterials.

Identifiants

pubmed: 38582521
doi: 10.1002/advs.202310314
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2310314

Subventions

Organisme : National Natural Science Foundation of China
ID : T2250710182
Organisme : National Natural Science Foundation of China
ID : 22306145
Organisme : Eesti Teadusagentuur
ID : PRG2188
Organisme : Fundamental Research Funds for the Central Universities
Organisme : Key Technologies Research and Development Program
ID : 2022YFC2409700
Organisme : Key Technologies Research and Development Program
ID : 2021YFA12009000

Informations de copyright

© 2024 The Authors. Advanced Science published by Wiley‐VCH GmbH.

Références

S. Lin, M. Mortimer, R. Chen, A. Kakinen, J. E. Riviere, T. P. Davis, F. Ding, P. C. Ke, Environ. Sci.: Nano 2017, 4, 1433.
A. Nel, T. Xia, L. Mädler, N. Li, Science 2006, 311, 622.
A. Carboni, D. L. Slomberg, M. Nassar, C. Santaella, A. Masion, J. Rose, M. Auffan, Environ. Sci. Technol. 2021, 55, 16270.
C. Wang, B. Zhao, Q. Wang, S. Zhang, Q. Wu, X. Shi, J. Hazard. Mater. 2024, 465, 133050.
V. H. Grassian, A. J. Haes, I. A. Mudunkotuwa, P. Demokritou, A. B. Kane, C. J. Murphy, J. E. Hutchison, J. A. Isaacs, Y.‐S. Jun, B. Karn, S. I. Khondaker, S. C. Larsen, B. L. T. Lau, J. M. Pettibone, O. A. Sadik, N. B. Saleh, C. Teague, Environ. Sci.: Nano 2016, 3, 15.
S. Liu, T. Xia, Small 2020, 16, 2000603.
G. Ren, D. Hu, E. W. C. Cheng, M. A. Vargas‐Reus, P. Reip, R. P. Allaker, Int. J. Antimicrob. Agents 2009, 33, 587.
O. Bondarenko, K. Juganson, A. Ivask, K. Kasemets, M. Mortimer, A. Kahru, Arch. Toxicol. 2013, 87, 1181.
M. Mortimer, A. Kahru, Nanomaterials 2022, 12, 4265.
B. E. El Bialy, R. A. Hamouda, M. A. Abd Eldaim, S. S. El Ballal, H. S. Heikal, H. K. Khalifa, W. N. Hozzein, Int. J. Nanomed. 2020, 15, 3827.
L. I. Privalova, B. A. Katsnelson, N. V. Loginova, V. B. Gurvich, V. Y. Shur, I. E. Valamina, O. H. Makeyev, M. P. Sutunkova, I. A. Minigalieva, E. P. Kireyeva, V. O. Rusakov, A. E. Tyurnina, R. V. Kozin, E. Y. Meshtcheryakova, A. V. Korotkov, E. A. Shuman, A. E. Zvereva, S. V. Kostykova, Int. J. Mol. Sci. 2014, 15, 12379.
J. Meng, J. Yang, T. Pan, X. Qu, S. Cui, Environ Int 2022, 158, 106923.
J. Hou, H. Liu, L. Wang, L. Duan, S. Li, X. Wang, Environ. Sci. Technol. 2018, 52, 7996.
P. J. A. Borm, D. Robbins, S. Haubold, T. Kuhlbusch, H. Fissan, K. Donaldson, R. Schins, V. Stone, W. Kreyling, J. Lademann, J. Krutmann, D. Warheit, E. Oberdorster, Part. Fibre Toxicol. 2006, 3, 11.
P. Chen, B. A. Powell, M. Mortimer, P. C. Ke, Environ. Sci. Technol. 2012, 46, 12178.
A. Malysheva, A. Ivask, C. L. Doolette, N. H. Voelcker, E. Lombi, Nat. Nanotechnol. 2021, 16, 926.
P. Cronholm, H. L. Karlsson, J. Hedberg, T. A. Lowe, L. Winnberg, K. Elihn, I. O. Wallinder, L. Möller, Small 2013, 9, 970.
O. Bondarenko, A. Ivask, A. Käkinen, A. Kahru, Environ. Pollut. 2012, 169, 81.
M. Cuillel, M. Chevallet, P. Charbonnier, C. Fauquant, I. Pignot‐Paintrand, J. Arnaud, D. Cassio, I. Michaud‐Soret, E. Mintz, Nanoscale 2014, 6, 1707.
P. C. Ke, M.‐A. Sani, F. Ding, A. Kakinen, I. Javed, F. Separovic, T. P. Davis, R. Mezzenga, Chem. Soc. Rev. 2017, 46, 6492.
N. Andrikopoulos, H. Tang, Y. Wang, X. Liang, Y. Li, T. P. Davis, P. C. Ke, Angew. Chem., Int. Ed. 2024, 63, e202309958.
M. G. Iadanza, M. P. Jackson, E. W. Hewitt, N. A. Ranson, S. E. Radford, Nat. Rev. Mol. Cell Biol. 2018, 19, 755.
P. C. Ke, R. Zhou, L. C. Serpell, R. Riek, T. P. J. Knowles, H. A. Lashuel, E. Gazit, I. W. Hamley, T. P. Davis, M. Fändrich, D. E. Otzen, M. R. Chapman, C. M. Dobson, D. S. Eisenberg, R. Mezzenga, Chem. Soc. Rev. 2020, 49, 5473.
P. Tian, W. Boomsma, Y. Wang, D. E. Otzen, M. H. Jensen, K. Lindorff‐Larsen, J. Am. Chem. Soc. 2015, 137, 22.
D. Otzen, R. Riek, Cold Spring Harb. Perspect. Biol. 2019, 11, a033860.
V. Jayawarna, M. Ali, T. A. Jowitt, A. F. Miller, A. Saiani, J. E. Gough, R. V. Ulijn, Adv. Mater. 2006, 18, 611.
S. L. Gras, A. K. Tickler, A. M. Squires, G. L. Devlin, M. A. Horton, C. M. Dobson, C. E. MacPhee, Biomaterials 2008, 29, 1553.
M. Peydayesh, R. Mezzenga, Nat. Commun. 2021, 12, 3248.
D. Xu, J. Zhou, W. L. Soon, I. Kutzli, A. Molière, S. Diedrich, M. Radiom, S. Handschin, B. Li, L. Li, S. J. Sturla, C. Y. Ewald, R. Mezzenga, Nat. Commun. 2023, 14, 6806.
M. M. Rahman, R. S. Pires, A. Herneke, V. Gowda, M. Langton, H. Biverstal, C. Lendel, Sci. Rep. 2023, 13, 985.
Y. Shen, L. Posavec, S. Bolisetty, F. M. Hilty, G. Nyström, J. Kohlbrecher, M. Hilbe, A. Rossi, J. Baumgartner, M. B. Zimmermann, R. Mezzenga, Nat. Nanotechnol. 2017, 12, 642.
M. Peydayesh, S. Kistler, J. Zhou, V. Lutz‐Bueno, F. D. Victorelli, A. B. Meneguin, L. Spósito, T. M. Bauab, M. Chorilli, R. Mezzenga, Nat. Commun. 2023, 14, 1848.
J. Wu, N. Österlund, H. Wang, R. Sternke‐Hoffmann, H. Pupart, L. L. Ilag, A. Gräslund, J. Luo, Cell Rep. Phys. Sci. 2022, 3, 101028.
I. Javed, Y. Sun, J. Adamcik, B. Wang, A. Kakinen, E. H. Pilkington, F. Ding, R. Mezzenga, T. P. Davis, P. C. Ke, Biomacromolecules 2017, 18, 4316.
S. Bolisetty, R. Mezzenga, Nat. Nanotechnol. 2016, 11, 365.
A. I. P. Taylor, R. A. Staniforth, Front. Neurosci. 2022, 16, 878869.
J. T. Rubino, M. P. Chenkin, M. Keller, P. Riggs‐Gelasco, K. J. Franz, Metallomics 2011, 3, 61.
A. Ivask, T. Titma, M. Visnapuu, H. Vija, A. Kakinen, M. Sihtmae, S. Pokhrel, L. Madler, M. Heinlaan, V. Kisand, R. Shimmo, A. Kahru, Curr. Top. Med. Chem. 2015, 15, 1914.
S. Jordens, J. Adamcik, I. Amar‐Yuli, R. Mezzenga, Biomacromolecules 2011, 12, 187.
L. J. G. Hoppenreijs, A. Overbeck, S. E. Brune, R. Biedendieck, A. Kwade, R. Krull, R. M. Boom, J. K. Keppler, Int. J. Biol. Macromol. 2023, 242, 124855.
C. Akkermans, P. Venema, A. J. van der Goot, H. Gruppen, E. J. Bakx, R. M. Boom, E. van der Linden, Biomacromolecules 2008, 9, 1474.
X. Ye, M. S. Hedenqvist, M. Langton, C. Lendel, RSC Adv. 2018, 8, 6915.
J.‐M. Jung, G. Savin, M. Pouzot, C. Schmitt, R. Mezzenga, Biomacromolecules 2008, 9, 2477.
J. Adamcik, J.‐M. Jung, J. Flakowski, P. De Los Rios, G. Dietler, R. Mezzenga, Nat. Nanotechnol. 2010, 5, 423.
R. Sarroukh, E. Goormaghtigh, J.‐M. Ruysschaert, V. Raussens, Biochim. Biophys. Acta Biomembr. 2013, 1828, 2328.
C. C. van den Akker, M. Schleeger, M. Bonn, G. H. Koenderink, in Bio‐Nanoimaging (Eds.: V. N. Uversky, Y. L. Lyubchenko), Academic Press, Boston, 2014.
D. Chen, L. S. Pinho, E. Federici, X. Zuo, J. Ilavsky, I. Kuzmenko, Z. Yang, O. G. Jones, O. Campanella, Food Hydrocoll. 2022, 124, 107291.
A. Kahru, M. Mortimer, Nanomaterials 2021, 11, 919.
G. Peng, Y. He, X. Wang, Y. Cheng, H. Zhang, K. Savolainen, L. Mädler, S. Pokhrel, S. Lin, ACS Nano 2020, 14, 4166.
M. Mortimer, K. Kasemets, M. Vodovnik, R. Marinšek‐Logar, A. Kahru, Environ. Sci. Technol. 2011, 45, 6617.
M.‐L. Avramescu, M. Chénier, S. Palaniyandi, P. E. Rasmussen, J. Nanopart. Res. 2020, 22, 222.
M. Peydayesh, S. Bolisetty, T. Mohammadi, R. Mezzenga, Langmuir 2019, 35, 4161.
F. Yang, F. Tao, C. Li, L. Gao, P. Yang, Nat. Commun. 2018, 9, 5443.
A. Palika, A. Armanious, A. Rahimi, C. Medaglia, M. Gasbarri, S. Handschin, A. Rossi, M. O. Pohl, I. Busnadiego, C. Gübeli, R. B. Anjanappa, S. Bolisetty, M. Peydayesh, S. Stertz, B. G. Hale, C. Tapparel, F. Stellacci, R. Mezzenga, Nat. Nanotechnol. 2021, 16, 918.
G. Kontopidis, C. Holt, L. Sawyer, J. Dairy Sci. 2004, 87, 785.
W. L. Soon, M. Peydayesh, R. Mezzenga, A. Miserez, Chem. Eng. J. 2022, 445, 136513.
X. Wu, X. Han, L. Lv, M. Li, J. You, C. Li, J. Coll. Interface Sci. 2018, 527, 117.
M. Heinlaan, A. Ivask, I. Blinova, H.‐C. Dubourguier, A. Kahru, Chemosphere 2008, 71, 1308.
J. Li, C. Chen, T. Xia, Adv. Mater. 2022, 34, 2106456.
Z. Wu, P. Shi, H. K. Lim, Y. Ma, M. I. Setyawati, D. Bitounis, P. Demokritou, K. W. Ng, C. Y. Tay, Small 2020, 16, 2000963.
Z. Wang, M. Tang, J. Appl. Toxicol. 2021, 41, 683.
G. Oberdorster, A. Maynard, K. Donaldson, V. Castranova, J. Fitzpatrick, K. Ausman, J. Carter, B. Karn, W. Kreyling, D. Lai, S. Olin, N. Monteiro‐Riviere, D. Warheit, H. Yang, A report from the ILSI Research Foundation/Risk Science Institute Nanomaterial Toxicity Screening Working Group, Part. Fibre Toxicol. 2005, 2, 8.
I. M. Kennedy, D. Wilson, A. I. Barakat, H. E. I. H. R. Committee, Res. Rep. Health Eff. Inst. 2009, 136, 3.
R. Gupta, H. Xie, J. Environ. Pathol. Toxicol. Oncol. 2018, 37, 209.
A. Krȩżel, W. Maret, J. Am. Chem. Soc. 2007, 129, 10911.
Ò. Palacios, S. Atrian, M. Capdevila, J. Biol. Inorg. Chem. 2011, 16, 991.
I. A. Schulkens, K. C. M. Castricum, E. M. Weijers, P. Koolwijk, A. W. Griffioen, V. L. Thijssen, J. Vasc. Res. 2014, 51, 231.
P. Tsvetkov, S. Coy, B. Petrova, M. Dreishpoon, A. Verma, M. Abdusamad, J. Rossen, L. Joesch‐Cohen, R. Humeidi, R. D. Spangler, J. K. Eaton, E. Frenkel, M. Kocak, S. M. Corsello, S. Lutsenko, N. Kanarek, S. Santagata, T. R. Golub, Science 2022, 375, 1254.
M. A. Kahlson, S. J. Dixon, Science 2022, 375, 1231.
F. Collin, Int. J. Mol. Sci. 2019, 20, 2407.
S. Le Maux, L. Giblin, T. Croguennec, S. Bouhallab, A. Brodkorb, J. Agric. Food Chem. 2012, 60, 9476.
T. Wang, X. Chen, X. Long, Z. Liu, S. Yan, PLoS One 2016, 11, e0149484.
X. Wang, C. H. Chang, J. Jiang, X. Liu, J. Li, Q. Liu, Y.‐P. Liao, L. Li, A. E. Nel, T. Xia, Small 2020, 16, 2000528.
H. Liu, W. Lai, X. Liu, H. Yang, Y. Fang, L. Tian, K. Li, H. Nie, W. Zhang, Y. Shi, L. Bian, S. Ding, J. Yan, B. Lin, Z. Xi, J. Hazard. Mater. 2021, 401, 123349.
N. M. Franklin, N. J. Rogers, S. C. Apte, G. E. Batley, G. E. Gadd, P. S. Casey, Environ. Sci. Technol. 2007, 41, 8484.
M. Li, L. Zhu, D. Lin, Environ. Sci. Technol. 2011, 45, 1977.
T. Graf, V. Koch, J. Koser, J. Fischer, C. Tessarek, J. Filser, Environ. Sci. Technol. 2023, 57, 12376.
X. Zhang, G. Ma, W. Wei, NPG Asia Mater. 2021, 13, 52.
S. Sabella, R. P. Carney, V. Brunetti, M. A. Malvindi, N. Al‐Juffali, G. Vecchio, S. M. Janes, O. M. Bakr, R. Cingolani, F. Stellacci, P. P. Pompa, Nanoscale 2014, 6, 7052.
E.‐J. Park, J. Yi, Y. Kim, K. Choi, K. Park, In Vitro Toxicol. 2010, 24, 872.
D. A. Kuhn, D. Vanhecke, B. Michen, F. Blank, P. Gehr, A. Petri‐Fink, B. Rothen‐Rutishauser, Beilstein J. Nanotechnol. 2014, 5, 1625.
E. Hove, C. A. Elvehjem, E. B. Hart, Am. J. Physiol. 1937, 119, 768.
J. W. Pyatskowit, J. R. Prohaska, Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol. 2008, 147, 316.
A. Waris, S. Sharif, S. Naz, F. Manzoor, F. Jamil, M. Hussain, Y. J. Choi, Y.‐K. Park, Environ. Eng. Res. 2023, 28, 220625.
F. Huang, C. M. Pariante, A. Borsini, Psychoneuroendocrinology 2021, 131, 105483.
C. Wang, X. Yang, Q. Zheng, B. Moe, X.‐F. Li, Environ. Sci. Technol. 2018, 52, 10590.
S. Lin, Y. Zhao, Z. Ji, J. Ear, C. H. Chang, H. Zhang, C. Low‐Kam, K. Yamada, H. Meng, X. Wang, R. Liu, S. Pokhrel, L. Mädler, R. Damoiseaux, T. Xia, H. A. Godwin, S. Lin, A. E. Nel, Small 2013, 9, 1776.
S. Lin, Y. Zhao, T. Xia, H. Meng, Z. Ji, R. Liu, S. George, S. Xiong, X. Wang, H. Zhang, S. Pokhrel, L. Mädler, R. Damoiseaux, S. Lin, A. E. Nel, ACS Nano 2011, 5, 7284.
N. Andrikopoulos, Y. Li, A. Nandakumar, J. F. Quinn, T. P. Davis, F. Ding, N. Saikia, P. C. Ke, ACS Appl. Mater. Interfaces 2023, 15, 7777.
F. Ding, D. Tsao, H. Nie, N. V. Dokholyan, Structure 2008, 16, 1010.
F. Ding, N. V. Dokholyan, in Computational Modeling of Biological Systems: From Molecules to Pathways (Ed.: N. V. Dokholyan), Springer US, Boston, MA, 2012.
A. C. Dave, S. M. Loveday, S. G. Anema, T. S. Loo, G. E. Norris, G. B. Jameson, H. Singh, J. Agric. Food Chem. 2013, 61, 7817.
H. Tabatabaei Ghomi, E. M. Topp, M. A. Lill, J. Mol. Model. 2016, 22, 206.
X. Ge, A. Kakinen, E. N. Gurzov, W. Yang, L. Pang, E. H. Pilkington, P. Govindan‐Nedumpully, P. Chen, F. Separovic, T. P. Davis, P. C. Ke, F. Ding, Chem. Commun. 2017, 53, 9394.

Auteurs

Yue Wang (Y)

School of Biomedical Sciences and Engineering, Guangzhou International Campus, South China University of Technology, Guangzhou, 510006, China.
Nanomedicine Center, Great Bay Area National Institute for Nanotechnology Innovation, 136 Kaiyuan Avenue, Guangzhou, 510700, China.

Xiufang Liang (X)

School of Biomedical Sciences and Engineering, Guangzhou International Campus, South China University of Technology, Guangzhou, 510006, China.
Nanomedicine Center, Great Bay Area National Institute for Nanotechnology Innovation, 136 Kaiyuan Avenue, Guangzhou, 510700, China.

Nicholas Andrikopoulos (N)

Nanomedicine Center, Great Bay Area National Institute for Nanotechnology Innovation, 136 Kaiyuan Avenue, Guangzhou, 510700, China.
Drug Delivery, Disposition and Dynamics, Monash Institute of Pharmaceutical Sciences, Monash University, 381 Royal Parade, Parkville, VIC, 3052, Australia.

Huayuan Tang (H)

Department of Engineering Mechanics, Hohai University, Nanjing, 211100, China.
Department of Physics and Astronomy, Clemson University, Clemson, SC, 29634, USA.

Fei He (F)

College of Environmental Science and Engineering, Key Laboratory of Yangtze River Water Environment, Tongji University, 1239 Siping Road, Shanghai, 200092, China.

Xiang Yin (X)

College of Environmental Science and Engineering, Key Laboratory of Yangtze River Water Environment, Tongji University, 1239 Siping Road, Shanghai, 200092, China.

Yuhuan Li (Y)

Drug Delivery, Disposition and Dynamics, Monash Institute of Pharmaceutical Sciences, Monash University, 381 Royal Parade, Parkville, VIC, 3052, Australia.
Liver Cancer Institute, Zhongshan Hospital, Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Fudan University, Shanghai, 200032, China.

Feng Ding (F)

Department of Physics and Astronomy, Clemson University, Clemson, SC, 29634, USA.

Guotao Peng (G)

College of Environmental Science and Engineering, Key Laboratory of Yangtze River Water Environment, Tongji University, 1239 Siping Road, Shanghai, 200092, China.

Monika Mortimer (M)

Laboratory of Environmental Toxicology, National Institute of Chemical Physics and Biophysics, Akadeemia tee 23, Tallinn, 12618, Estonia.

Pu Chun Ke (PC)

Nanomedicine Center, Great Bay Area National Institute for Nanotechnology Innovation, 136 Kaiyuan Avenue, Guangzhou, 510700, China.
Drug Delivery, Disposition and Dynamics, Monash Institute of Pharmaceutical Sciences, Monash University, 381 Royal Parade, Parkville, VIC, 3052, Australia.

Classifications MeSH