Single-site iron-anchored amyloid hydrogels as catalytic platforms for alcohol detoxification.
Journal
Nature nanotechnology
ISSN: 1748-3395
Titre abrégé: Nat Nanotechnol
Pays: England
ID NLM: 101283273
Informations de publication
Date de publication:
13 May 2024
13 May 2024
Historique:
received:
10
10
2023
accepted:
21
03
2024
medline:
14
5
2024
pubmed:
14
5
2024
entrez:
13
5
2024
Statut:
aheadofprint
Résumé
Constructing effective antidotes to reduce global health impacts induced by alcohol prevalence is a challenging topic. Despite the positive effects observed with intravenous applications of natural enzyme complexes, their insufficient activities and complicated usage often result in the accumulation of toxic acetaldehyde, which raises important clinical concerns, highlighting the pressing need for stable oral strategies. Here we present an effective solution for alcohol detoxification by employing a biomimetic-nanozyme amyloid hydrogel as an orally administered catalytic platform. We exploit amyloid fibrils derived from β-lactoglobulin, a readily accessible milk protein that is rich in coordinable nitrogen atoms, as a nanocarrier to stabilize atomically dispersed iron (ferrous-dominated). By emulating the coordination structure of the horseradish peroxidase enzyme, the single-site iron nanozyme demonstrates the capability to selectively catalyse alcohol oxidation into acetic acid, as opposed to the more toxic acetaldehyde. Administering the gelatinous nanozyme to mice suffering from alcohol intoxication significantly reduced their blood-alcohol levels (decreased by 55.8% 300 min post-alcohol intake) without causing additional acetaldehyde build-up. Our hydrogel further demonstrates a protective effect on the liver, while simultaneously mitigating intestinal damage and dysbiosis associated with chronic alcohol consumption, introducing a promising strategy in effective alcohol detoxification.
Identifiants
pubmed: 38740933
doi: 10.1038/s41565-024-01657-7
pii: 10.1038/s41565-024-01657-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
GBD 2016 Alcohol Collaborators. Alcohol use and burden for 195 countries and territories, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet 392, 1015–1035 (2018).
pmcid: 6148333
doi: 10.1016/S0140-6736(18)31310-2
Rehm, J. et al. Global burden of disease and injury and economic cost attributable to alcohol use and alcohol-use disorders. Lancet 373, 2223–2233 (2009).
pubmed: 19560604
doi: 10.1016/S0140-6736(09)60746-7
GBD 2019 Diseases and Injuries Collaborators. Global burden of 369 diseases and injuries in 204 countries and territories, 1990–2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet 396, 1204–1222 (2020).
GBD 2020 Alcohol Collaborators. Population-level risks of alcohol consumption by amount, geography, age, sex, and year: a systematic analysis for the Global Burden of Disease Study 2020. Lancet 400, 185–235 (2022).
Xie, L. et al. The protective effects and mechanisms of modified Lvdou Gancao decoction on acute alcohol intoxication in mice. J. Ethnopharmacol. 282, 114593 (2022).
pubmed: 34480998
doi: 10.1016/j.jep.2021.114593
Chen, X. et al. Protective effect of Flos puerariae extract following acute alcohol intoxication in mice. Alcohol. Clin. Exp. Res. 38, 1839–1846 (2014).
pubmed: 24931816
doi: 10.1111/acer.12437
Guo, J., Chen, Y., Yuan, F., Peng, L. & Qiu, C. Tangeretin protects mice from alcohol-induced fatty liver by activating mitophagy through the AMPK-ULK1 pathway. J. Agric. Food Chem. 70, 11236–11244 (2022).
pubmed: 36063077
doi: 10.1021/acs.jafc.2c02927
Liu, Y. et al. Biomimetic enzyme nanocomplexes and their use as antidotes and preventive measures for alcohol intoxication. Nat. Nanotechnol. 8, 187–192 (2013).
pubmed: 23416793
pmcid: 3670615
doi: 10.1038/nnano.2012.264
Xu, D. et al. A hepatocyte-mimicking antidote for alcohol intoxication. Adv. Mater. 30, e1707443 (2018).
pubmed: 29638019
pmcid: 6386471
doi: 10.1002/adma.201707443
Wang, H., Wan, K. & Shi, X. Recent advances in nanozyme research. Adv. Mater. 31, e1805368 (2019).
pubmed: 30589120
doi: 10.1002/adma.201805368
Jiang, D. et al. Nanozyme: new horizons for responsive biomedical applications. Chem. Soc. Rev. 48, 3683–3704 (2019).
pubmed: 31119258
pmcid: 6696937
doi: 10.1039/C8CS00718G
Yu, Z., Lou, R., Pan, W., Li, N. & Tang, B. Nanoenzymes in disease diagnosis and therapy. Chem. Commun. 56, 15513–15524 (2020).
doi: 10.1039/D0CC05427E
Cao, C. et al. Biomedicine meets nanozyme catalytic chemistry. Coord. Chem. Rev. 491, 215–245 (2023).
doi: 10.1016/j.ccr.2023.215245
Peng, C., Pang, R., Li, J. & Wang, E. Current advances on the single-atom nanozyme and its bio-applications. Adv. Mater. 36, e2211724 (2023).
pubmed: 36773312
doi: 10.1002/adma.202211724
Jiao, L. et al. When nanozymes meet single-atom catalysis. Angew. Chem. Int. Ed. 59, 2565–2576 (2020).
doi: 10.1002/anie.201905645
Zhang, S. et al. Single-atom nanozymes catalytically surpassing naturally occurring enzymes as sustained stitching for brain trauma. Nat. Commun. 13, 4744 (2022).
pubmed: 35961961
pmcid: 9374753
doi: 10.1038/s41467-022-32411-z
Sun, A., Mu, L. & Hu, X. Graphene oxide quantum dots as novel nanozymes for alcohol intoxication. ACS Appl. Mater. Interfaces 9, 12241–12252 (2017).
pubmed: 28322544
doi: 10.1021/acsami.7b00306
Geng, X. et al. Confined cascade metabolic reprogramming nanoreactor for targeted alcohol detoxification and alcoholic liver injury management. ACS Nano 17, 7443–7455 (2023).
pubmed: 37057958
doi: 10.1021/acsnano.2c12075
Bolisetty, S. & Mezzenga, R. Amyloid–carbon hybrid membranes for universal water purification. Nat. Nanotechnol. 11, 365–371 (2016).
pubmed: 26809058
doi: 10.1038/nnano.2015.310
Xu, D. et al. Food amyloid fibrils are safe nutrition ingredients based on in-vitro and in-vivo assessment. Nat. Commun. 14, 6806 (2023).
pubmed: 37884488
pmcid: 10603083
doi: 10.1038/s41467-023-42486-x
Shen, Y. et al. Amyloid fibril systems reduce, stabilize and deliver bioavailable nanosized iron. Nat. Nanotechnol. 12, 642–647 (2017).
pubmed: 28436960
doi: 10.1038/nnano.2017.58
Cao, Y. & Mezzenga, R. Design principles of food gels. Nat. Food 1, 106–118 (2020).
pubmed: 37127997
doi: 10.1038/s43016-019-0009-x
Hu, B. et al. Amyloid–polyphenol hybrid nanofilaments mitigate colitis and regulate gut microbial dysbiosis. ACS Nano 14, 2760–2776 (2020).
pubmed: 31961657
doi: 10.1021/acsnano.9b09125
Peydayesh, M. et al. Amyloid–polysaccharide interfacial coacervates as therapeutic materials. Nat. Commun. 14, 1848 (2023).
pubmed: 37012278
pmcid: 10070338
doi: 10.1038/s41467-023-37629-z
Scheffen, M. et al. A new-to-nature carboxylation module to improve natural and synthetic CO
doi: 10.1038/s41929-020-00557-y
Wang, C. et al. Atomic Fe hetero-layered coordination between g-C
doi: 10.1039/C8TA09722D
Kim, S. et al. In situ XANES of an iron porphyrin irreversibly adsorbed on an electrode surface. J. Am. Chem. Soc. 113, 9063–9066 (1991).
doi: 10.1021/ja00024a006
Shui, J. L., Karan, N. K., Balasubramanian, M., Li, S. Y. & Liu, D. J. Fe/N/C composite in Li–O
pubmed: 22998563
doi: 10.1021/ja3042993
Bagus, P. S. et al. Combined multiplet theory and experiment for the Fe 2p and 3p XPS of FeO and Fe
pubmed: 33685168
doi: 10.1063/5.0039765
Nelson, G. W., Perry, M., He, S. M., Zechel, D. L. & Horton, J. H. Characterization of covalently bonded proteins on poly(methyl methacrylate) by X-ray photoelectron spectroscopy. Colloids Surf. B 78, 61–68 (2010).
doi: 10.1016/j.colsurfb.2010.02.012
Vanea, E. & Simon, V. XPS study of protein adsorption onto nanocrystalline aluminosilicate microparticles. Appl. Surf. Sci. 257, 2346–2352 (2011).
doi: 10.1016/j.apsusc.2010.09.101
Ji, S. et al. Matching the kinetics of natural enzymes with a single-atom iron nanozyme. Nat. Catal. 4, 407–417 (2021).
doi: 10.1038/s41929-021-00609-x
Chamarro, E., Marco, A. & Esplugas, S. Use of Fenton reagent to improve organic chemical biodegradability. Water Res. 35, 1047–1051 (2001).
pubmed: 11235870
doi: 10.1016/S0043-1354(00)00342-0
Meyerstein, D. Re-examining Fenton and Fenton-like reactions. Nat. Rev. Chem. 5, 595–597 (2021).
pubmed: 37118415
doi: 10.1038/s41570-021-00310-4
Vonghia, L. et al. Acute alcohol intoxication. Eur. J. Intern. Med. 19, 561–567 (2008).
pubmed: 19046719
doi: 10.1016/j.ejim.2007.06.033
Schweizer, T. A. et al. Neuropsychological profile of acute alcohol intoxication during ascending and descending blood alcohol concentrations. Neuropsychopharmacology 31, 1301–1309 (2006).
pubmed: 16251993
doi: 10.1038/sj.npp.1300941
Chen, J. et al. Glucose-oxidase like catalytic mechanism of noble metal nanozymes. Nat. Commun. 12, 3375 (2021).
pubmed: 34099730
pmcid: 8184917
doi: 10.1038/s41467-021-23737-1
Comotti, M., Della|Pina, C., Falletta, E. & Rossi, M. Aerobic oxidation of glucose with gold catalyst: hydrogen peroxide as intermediate and reagent. Adv. Synth. Catal. 348, 313–316 (2006).
doi: 10.1002/adsc.200505389
Ishida, T. et al. Influence of the support and the size of gold clusters on catalytic activity for glucose oxidation. Angew. Chem. Int. Ed. 47, 9265–9268 (2008).
doi: 10.1002/anie.200802845
Usuelli, M. et al. Polysaccharide-reinforced amyloid fibril hydrogels and aerogels. Nanoscale 13, 12534–12545 (2021).
pubmed: 34263899
doi: 10.1039/D1NR03133C
Dolganiuc, A. & Szabo, G. In vitro and in vivo models of acute alcohol exposure. World J. Gastroenterol. 15, 1168–1177 (2009).
pubmed: 19291816
pmcid: 2658858
doi: 10.3748/wjg.15.1168
Zakhari, S. Overview: how is alcohol metabolized by the body? Alcohol Res. Health 29, 245–254 (2006).
pubmed: 17718403
pmcid: 6527027
Bertola, A., Mathews, S., Ki, S. H., Wang, H. & Gao, B. Mouse model of chronic and binge ethanol feeding (the NIAAA model). Nat. Protoc. 8, 627–637 (2013).
pubmed: 23449255
pmcid: 3788579
doi: 10.1038/nprot.2013.032
Mutlu, E. A. et al. Colonic microbiome is altered in alcoholism. Am. J. Physiol. Gastrointest. 302, G966–G978 (2012).
doi: 10.1152/ajpgi.00380.2011
Canesso MCC et al. Comparing the effects of acute alcohol consumption in germ-free and conventional mice: the role of the gut microbiota. BMC Microbiol. 14, 1–10 (2014).
Keshavarzian, A. et al. Evidence that chronic alcohol exposure promotes intestinal oxidative stress, intestinal hyperpermeability and endotoxemia prior to development of alcoholic steatohepatitis in rats. J. Hepatol. 50, 538–547 (2009).
pubmed: 19155080
doi: 10.1016/j.jhep.2008.10.028
Horowitz, A., Chanez-Paredes, S. D., Haest, X. & Turner, J. R. Paracellular permeability and tight junction regulation in gut health and disease. Nat. Rev. Gastroenterol. Hepatol. 20, 417–432 (2023).
pubmed: 37186118
doi: 10.1038/s41575-023-00766-3
Martino, C. et al. Acetate reprograms gut microbiota during alcohol consumption. Nat. Commun. 13, 4630 (2022).
pubmed: 35941112
pmcid: 9359997
doi: 10.1038/s41467-022-31973-2
Han, Y. H. et al. Enterically derived high-density lipoprotein restrains liver injury through the portal vein. Science 373, eabe6729 (2021).
pubmed: 34437091
pmcid: 8478306
doi: 10.1126/science.abe6729
Jung, J.-M., Savin, G., Pouzot, M., Schmit, C. & Mezzenga, R. Structure of heat-induced β-lactoglobulin aggregates and their complexes with sodium-dodecyl sulfate. Biomacromolecules 9, 2477–2486 (2008).
pubmed: 18698816
doi: 10.1021/bm800502j
Jung, J.-M. & Mezzenga, R. Liquid crystalline phase behavior of protein fibers in water: experiments versus theory. Langmuir: ACS J. Surf. Colloids 26, 504–514 (2010).
doi: 10.1021/la9021432
Kutzner, C. et al. Best bang for your buck: GPU nodes for GROMACS biomolecular simulations. J. Comput. Chem. 36, 1990–2008 (2015).
pubmed: 26238484
pmcid: 5042102
doi: 10.1002/jcc.24030
Wennberg, C. L. et al. Direct-space corrections enable fast and accurate Lorentz–Berthelot combination rule Lennard–Jones lattice summation. J. Chem. Theory Comput. 11, 5737–5746 (2015).
pubmed: 26587968
doi: 10.1021/acs.jctc.5b00726
Humphrey, W., Dalke, A. & Schulten, K. VMD—Visual Molecular Dynamics. J. Mol. Graph. 14, 33–38 (1996).
pubmed: 8744570
doi: 10.1016/0263-7855(96)00018-5
Kuhne, T. D. et al. CP2K: An electronic structure and molecular dynamics software package—Quickstep: efficient and accurate electronic structure calculations. J. Chem. Phys. 152, 194103 (2020).
pubmed: 33687235
doi: 10.1063/5.0007045
Grimme, S., Antony, J., Ehrlich, S. & Krieg, H. A consistent and accurate ab initio parametrization of density functional dispersion correction (DFT-D) for the 94 elements H–Pu. J. Chem. Phys. 132, 154104 (2010).
pubmed: 20423165
doi: 10.1063/1.3382344
Lu, T. & Chen, F. Multiwfn: a multifunctional wavefunction analyzer. J. Comput. Chem. 33, 580–592 (2012).
pubmed: 22162017
doi: 10.1002/jcc.22885
Brodkorb, A. et al. INFOGEST static in vitro simulation of gastrointestinal food digestion. Nat. Protoc. 14, 991–1014 (2019).
pubmed: 30886367
doi: 10.1038/s41596-018-0119-1
Vorhees, C. V. & Williams, M. T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat. Protoc. 1, 848–858 (2006).
pubmed: 17406317
pmcid: 2895266
doi: 10.1038/nprot.2006.116
Folch, J., Lees, M. & Sloane Stanley, G. H. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497–509 (1957).
pubmed: 13428781
doi: 10.1016/S0021-9258(18)64849-5
Su, J. Code for MD and DFT. Zenodo https://doi.org/10.5281/zenodo.10819612 (2024).