journal article Jan 01, 2024

Copper-Bearing Metal-Organic Framework with Mucus-Penetrating Function for the Multi-Effective Clearance of Mucosal Colonized Helicobacter pylori

View at Publisher Save 10.34133/research.0358
Abstract
Helicobacter pylori
colonizes over 50% of people worldwide. Biofilm formation through penetrating gastric mucus and resistance acquired by
H. pylori
markedly reduces the efficacy of traditional antibiotics. The present triple therapy and bismuth-based quadruple therapy inevitably causes intestinal flora disturbance and fails to address the excessive
H. pylori
-triggered inflammatory response. Herein, a mucus-permeable therapeutic platform (Cu-MOF@NF) that consists of copper-bearing metal-organic framework (Cu-MOF) loaded with nitrogen-doped carbon dots and naturally active polysaccharide fucoidan is developed. The experimental results demonstrate that Cu-MOF@NF can penetrate the mucus layer and hinder
H. pylori
from adhering on gastric epithelial cells of the stomach. Notably, released Cu
2+
can degrade the polysaccharides in the biofilm and interfere with the cyclic growing mode of “bacterioplankton ↔ biofilm”, thereby preventing recurrent and persistent infection. Compared with traditional triple therapy, the Cu-MOF@NF not only possesses impressive antibacterial effect (even include multidrug-resistant strains), but also improves the inflammatory microenvironment without disrupting the balance of intestinal flora, providing a more efficient, safe, and antibiotic-free new approach to eradicating
H. pylori
.
Topics

No keywords indexed for this article. Browse by subject →

References
60
[1]
Helicobacter pylori Resists the Antimicrobial Activity of Calprotectin via Lipid A Modification and Associated Biofilm Formation

Jennifer A. Gaddy, Jana N. Radin, Thomas W. Cullen et al.

mBio 2015 10.1128/mbio.01349-15
[2]
Choi IJ, Kim CG, Lee JY, Kim Y-I, Kook M-C, Park B, Joo J. Family history of gastric cancer and Helicobacter pylori treatment. N Engl J Med. 2020;382:427–436. 10.1056/nejmoa1909666
[3]
Czinn SJ, Blanchard T. Vaccinating against Helicobacter pylori infection. Nat Rev Gastroenterol Hepatol. 2011;8:133–140. 10.1038/nrgastro.2011.1
[4]
Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87–108. 10.3322/caac.21262
[5]
Wang L, Lin Z, Chen S, Li J, Chen C, Huang Z, Ye B, Ding J, Li W, Wu L, et al. Ten-day bismuth-containing quadruple therapy is effective as first-line therapy for Helicobacter pylori-related chronic gastritis: A prospective randomized study in China. Clin Microbiol Infect. 2017;23:391–395. 10.1016/j.cmi.2016.12.032
[6]
Sijmons D, Guy AJ, Walduck AK, Ramsland PA. Helicobacter pylori and the role of lipopolysaccharide variation in innate immune evasion. Front Immunol. 2022;13: Article 868225. 10.3389/fimmu.2022.868225
[7]
Gong Y, Yuan Y. Resistance mechanisms of Helicobacter pylori and its dual target precise therapy. Crit Rev Microbiol. 2018;44:371–392. 10.1080/1040841x.2017.1418285
[8]
Sierra JC, Piazuelo MB, Luis PB, Barry DP, Allaman MM, Asim M, Sebrell TA, Finley JL, Rose KL, Hill S, et al. Spermine oxidase mediates Helicobacter pylori-induced gastric inflammation, DNA damage, and carcinogenic signaling. Oncogene. 2020;39:4465–4474. 10.1038/s41388-020-1304-6
[9]
Mommersteeg MC, Simovic I, Yu B, van Nieuwenburg SAV, Bruno IMJ, Doukas M, Kuipers EJ, Spaander MCW, Peppelenbosch MP, Castaño-Rodríguez N, et al. Autophagy mediates ER stress and inflammation in Helicobacter pylori-related gastric cancer. Gut Microbes. 2022;14(1):2015238. 10.1080/19490976.2021.2015238
[10]
Yu J, Guo Z, Yan J, Bu C, Peng C, Li C, Mao R, Zhang J, Wang Z, Chen S, et al. Gastric acid-responsive ROS nanogenerators for effective treatment of Helicobacter pylori infection without disrupting homeostasis of intestinal flora. Adv Sci. 2023;10(20):e2206957. 10.1002/advs.202206957
[11]
Cheng X, Geng J, Wang L, Ma X, Su Y, Arif M, Liu C. Berberine-loaded mannosylerythritol lipid-B nanomicelles as drug delivery carriers for the treatment of Helicobacter pylori biofilms in vivo. Eur J Pharm Biopharm. 2023;193:105–118. 10.1016/j.ejpb.2023.10.021
[12]
Hathroubi S, Servetas SL, Windham I, Merrell DS, Ottemann KM. Helicobacter pylori biofilm formation and its potential role in pathogenesis. Microbiol Mol Biol Rev. 2018;82(2):e00001–e00018. 10.1128/mmbr.00001-18
[13]
Yonezawa H, Osaki T, Kurata S, Zaman C, Hanawa T, Kamiya S. Assessment of in vitro biofilm formation by Helicobacter pylori. J Gastroenterol Hepatol. 2010;25(Suppl. 1):S90–S94.
[14]
Krzyzek P, Gosciniak G. A proposed role for diffusible signal factors in the biofilm formation and morphological transformation of Helicobacter pylori. Turk J Gastroenterol. 2018;29:7–13. 10.5152/tjg.2017.17349
[15]
Chang Y, Hu Y, McClements DJ. Competitive adsorption and displacement of anionic polysaccharides (fucoidan and gum arabic) on the surface of protein-coated lipid droplets. Food Hydrocoll. 2016;52:820–826. 10.1016/j.foodhyd.2015.08.023
[16]
Wang M, Veeraperumal S, Zhong S, Cheong K-L. Fucoidan-derived functional oligosaccharides: Recent developments, preparation, and potential applications. Foods. 2023;12(4):878. 10.3390/foods12040878
[17]
Lutay N, Nilsson I, Wadström T, Ljungh A. Effect of heparin, fucoidan and other polysaccharides on adhesion of enterohepatic Helicobacter species to murine macrophages. Appl Biochem Biotechnol. 2011;164(1):1–9. 10.1007/s12010-010-9109-7
[18]
Murru C, Badía-Laíño R, Díaz-García ME. Synthesis and characterization of green carbon dots for scavenging radical oxygen species in aqueous and oil samples. Antioxidants. 2020;9(11):1147. 10.3390/antiox9111147
[19]
Hu J, Luo J, Zhang ML, Wu JS, Zhang Y, Kong H, Qu HH, Cheng GL, Zhao Y. Protective effects of Radix Sophorae Flavescentis carbonisata-based carbon dots against ethanol-induced acute gastric ulcer in rats: Anti-inflammatory and antioxidant activities. Int J Nanomedicine. 2021;16:2461–2475. 10.2147/ijn.s289515
[20]
He Q, Zhang LY. Design of carbon dots as nanozymes to mediate redox biological processes. J Mater Chem B. 2023;11:5071–5082. 10.1039/d2tb02259a
[21]
Ezati P, Rhim JW, Molaei R, Priyadarshi R, Roy S, Min S, Kim YH, Lee SG, Han S. Preparation and characterization of B, S, and N-doped glucose carbon dots: Antibacterial, antifungal, and antioxidant activity. Sustain Mater Technol. 2022;32: Article e00397.
[22]
Yan H, Wang L, Chen Y, Jiao L, Wu Y, Xu W, Gu W, Song W, Du D, Zhu C. Fine-tuning pyridinic nitrogen in nitrogen-doped porous carbon nanostructures for boosted peroxidase-like activity and sensitive biosensing. Research. 2020;2020: Article 8202584.
[23]
Dong C, Ma X, Huang Y, Zhang Y, Gao X. Carbon dots nanozyme for anti-inflammatory therapy via scavenging intracellular reactive oxygen species. Front Bioeng Biotechnol. 2022;10: Article 943399. 10.3389/fbioe.2022.943399
[24]
Dollwet HHA, Sorenson JRJ. Historic uses of copper compounds in medicine. Trace Elem Med. 1985;2(2):80–87.
[25]
Casey AL, Adams D, Karpanen TJ, Lambert PA, Cookson BD, Nightingale P, Miruszenko L, Shillam R, Christian P, Elliott TSJ. Role of copper in reducing hospital environment contamination. J Hosp Infect. 2010;74(1):72–77. 10.1016/j.jhin.2009.08.018
[26]
Lai W-F, Wong W-T, Rogach AL. Development of copper nanoclusters for in vitro and in vivo theranostic applications. Adv Mater. 2020;32(9): Article 1906872. 10.1002/adma.201906872
[27]
Lin H, Ding L, Zhang B, Huang J. Detection of nitrite based on fluorescent carbon dots by the hydrothermal method with folic acid. R Soc Open Sci. 2018;5(5): Article 172149. 10.1098/rsos.172149
[28]
Luo H, Liu Y, Lu H, Fang Q, Rong H. Efficient adsorption of tetracycline from aqueous solutions by modified alginate beads after the removal of cu(II) ions. ACS Omega. 2021;6(9):6240–6251. 10.1021/acsomega.0c05807
[29]
Bosica G, Zammit R. One-pot multicomponent nitro-Mannich reaction using a heterogeneous catalyst under solvent-free conditions. PeerJ. 2018;6: Article e5065. 10.7717/peerj.5065
[30]
Gao Y-L, Inoue K. Crystal structures and magnetic properties of nitroxide radical-coordinated copper(II) and cobalt(II) complexes. Transit Met Chem. 2019;44:283–292. 10.1007/s11243-018-00297-w
[31]
Deng Z, Huang Z, Liu J, Huang Y, Lu P. Efficient activation of peroxymonosulfate by V-doped graphitic carbon nitride for organic contamination remediation. Materials. 2022;15(24): Article 8936. 10.3390/ma15248936
[32]
Al Monla R, Dassouki Z, Sari-Chmayssem N, Mawlawi H, Gali-Muhtasib H. Fucoidan and alginate from the Brown algae Colpomenia sinuosa and their combination with vitamin C trigger apoptosis in colon cancer. Molecules. 2022;27(2): Article 358. 10.3390/molecules27020358
[34]
Liu M, Wu L, Zhu X, Shan W, Li L, Cui Y, Huang Y. Core-shell stability of nanoparticles plays an important role for overcoming the intestinal mucus and epithelium barrier. J Mater Chem B. 2016;4(35):5831–5841. 10.1039/c6tb01199c
[37]
Khutoryanskiy VV. Beyond PEGylation: Alternative surface-modification of nanoparticles with mucus-inert biomaterials. Adv Drug Deliv Rev. 2018;124:140–149. 10.1016/j.addr.2017.07.015
[38]
Linden S, Nordman H, Hedenbro J, Hurtig M, Boren T, Carlstedt I. Strain and blood group-dependent binding of Helicobacter pylori to human gastric MUC5AC glycoforms. Gastroenterology. 2003;124:588–588.
[39]
Walz A, Odenbreit S, Mahdavi J, Borén T, Ruhl S. Identification and characterization of binding properties of Helicobacter pylori by glycoconjugate arrays. Glycobiology. 2005;15(7):700–708. 10.1093/glycob/cwi049
[40]
Song W, Wang Y, Zhang L, Fu S, Zeng Y, Hu H. Preparation and evaluation of polysaccharide sulfates for inhibiting Helicobacter pylori adhesion. Carbohydr Polym. 2014;103:398–404. 10.1016/j.carbpol.2013.12.063
[41]
Nicotera P, Leist M, Ferrando-May E. Intracellular ATP, a switch in the decision between apoptosis and necrosis. Toxicol Lett. 1998;102–103:139–142. 10.1016/s0378-4274(98)00298-7
[42]
Gupta N, Kumar A, Verma VK. Strategies adopted by gastric pathogen Helicobacter pylori for a mature biofilm formation: Antimicrobial peptides as a visionary treatment. Microbiol Res. 2023;273: Article 127417. 10.1016/j.micres.2023.127417
[43]
Yang FL, Hassanbhai AM, Chen H-Y, Huang Z-Y, Lin T-L, Wu S-H, Ho B. Proteomannans in biofilm of Helicobacter pylori ATCC 43504. Helicobacter. 2011;16(2):89–98. 10.1111/j.1523-5378.2010.00815.x
[44]
The biofilm matrix: multitasking in a shared space

Hans-Curt Flemming, Eric D. Van Hullebusch, Thomas R. Neu et al.

Nature Reviews Microbiology 10.1038/s41579-022-00791-0
[45]
Xiu W, Gan S, Wen Q, Qiu Q, Dai S, Dong H, Li Q, Yuwen L, Weng L, Teng Z, et al. Biofilm microenvironment-responsive nanotheranostics for dual-mode imaging and hypoxia-relief-enhanced photodynamic therapy of bacterial infections. Research. 2020;2020: Article 9426453.
[46]
Li W, Xiao X, Qi Y, Lin X, Hu H, Shi M, Zhou M, Jiang W, Liu L, Chen K, et al. Host-defense-peptide-mimicking β-peptide polymer acting as a dual-modal antibacterial agent by interfering quorum sensing and killing individual bacteria simultaneously. Research. 2023;6: Article 0051.
[47]
Han L, Shu X, Wang J. Helicobacter pylori-mediated oxidative stress and gastric diseases: A review. Front Microbiol. 2022;13: Article 811258. 10.3389/fmicb.2022.811258
[48]
Jain U, Saxena K, Chauhan N. Helicobacter pylori induced reactive oxygen species: A new and developing platform for detection. Helicobacter. 2021;26(3): Article e12796. 10.1111/hel.12796
[50]
Handa O, Naito Y, Yoshikawa T. Helicobacter pylori: A ROS-inducing bacterial species in the stomach. Inflamm Res. 2010;59(12):997–1003. 10.1007/s00011-010-0245-x

Showing 50 of 60 references

Metrics
21
Citations
60
References
Details
Published
Jan 01, 2024
Vol/Issue
7
Authors
Funding
National Natural Science Foundation of China Award: No.82170580
the First Affiliated Hospital of Nanchang University Clinical Research and Cultivation Project Award: YFYLCYJPY202002
The Key Research and Development Program of Jiangxi Province Award: 20212BBG73004
the Postdoctoral Fellowship Program Award: GZB20230283
Cite This Article
Chunxi Shu, Wei Zhang, Yiwei Zhang, et al. (2024). Copper-Bearing Metal-Organic Framework with Mucus-Penetrating Function for the Multi-Effective Clearance of Mucosal Colonized Helicobacter pylori. Research, 7. https://doi.org/10.34133/research.0358
Related

You May Also Like