Implications of silver nanoparticles for H. pylori infection: modulation of CagA function and signaling
Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
Grantová podpora
I 4360
Austrian Science Fund FWF - Austria
P 31507
Austrian Science Fund FWF - Austria
PubMed
38983115
PubMed Central
PMC11231068
DOI
10.3389/fcimb.2024.1419568
Knihovny.cz E-zdroje
- Klíčová slova
- AGS, CagA, H. pylori, IL-8, infection, minimum inhibitory concentration, silver nanoparticles,
- MeSH
- antibakteriální látky farmakologie MeSH
- antigeny bakteriální * metabolismus MeSH
- bakteriální proteiny * metabolismus MeSH
- buněčné linie MeSH
- epitelové buňky mikrobiologie MeSH
- faktory virulence metabolismus MeSH
- Helicobacter pylori * účinky léků MeSH
- infekce vyvolané Helicobacter pylori * mikrobiologie farmakoterapie MeSH
- interakce hostitele a patogenu MeSH
- kovové nanočástice * MeSH
- lidé MeSH
- nádorové buněčné linie MeSH
- signální transdukce * účinky léků MeSH
- stříbro * farmakologie metabolismus MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- antibakteriální látky MeSH
- antigeny bakteriální * MeSH
- bakteriální proteiny * MeSH
- cagA protein, Helicobacter pylori MeSH Prohlížeč
- faktory virulence MeSH
- stříbro * MeSH
BACKGROUND: Helicobacter pylori infection poses a significant health burden worldwide, and its virulence factor CagA plays a pivotal role in its pathogenesis. METHODS: In this study, the interaction between H. pylori-infected AGS cells and silver nanoparticles (AgNPs) was investigated, with a focus on the modulation of CagA-mediated responses, investigated by western blotting. Both, the dose-dependent efficacy against H. pylori (growth curves, CFU assay) and the impact of the nanoparticles on AGS cells (MTT assay) were elucidated. RESULTS: AGS cells infected with H. pylori displayed dramatic morphological changes, characterized by elongation and a migratory phenotype, attributed to CagA activity. Preincubation of H. pylori with AgNPs affected these morphological changes in a concentration-dependent manner, suggesting a correlation between AgNPs concentration and CagA function. CONCLUSION: Our study highlights the nuanced interplay between host-pathogen interactions and the therapeutic potential of AgNPs in combating H. pylori infection and offers valuable insights into the multifaceted dynamics of CagA mediated responses.
Cancer Cluster Salzburg Salzburg Austria
Center for Tumor Biology and Immunology Paris Lodron University of Salzburg Salzburg Austria
Department of Biosciences and Medical Biology Paris Lodron University of Salzburg Salzburg Austria
Department of Physical Chemistry Palacky University Olomouc Olomouc Czechia
Zobrazit více v PubMed
Alipour M. (2021). Molecular mechanism of helicobacter pylori-induced gastric cancer. J. Gastrointest Cancer 52, 23–30. doi: 10.1007/s12029-020-00518-5 PubMed DOI PMC
Amin M., Hameed S., Ali A., Anwar F., Shahid S. A., Shakir I., et al. . (2014). Green Synthesis of Silver Nanoparticles: Structural Features and in Vivo and in Vitro Therapeutic Effects against Helicobacter pylori Induced Gastritis. Bioinorg. Chem. Appl. 2014, 1–11. doi: 10.1155/2014/135824 PubMed DOI PMC
Asgari S., Nikkam N., Saniee P. (2022). Metallic Nanoparticles as promising tools to eradicate H. Pylori: A. Compr. Rev. Recent Advancements Talanta Open 6, 1–8. doi: 10.1016/j.talo.2022.100129 DOI
Axson J. L., Stark D. I., Bondy A. L., Capracotta S. S., Maynard A. D., Philbert M. A., et al. . (2015). Rapid kinetics of size and pH-dependent dissolution and aggregation of silver nanoparticles in simulated gastric fluid. J. Phys. Chem. C. 119, 20632–20641. doi: 10.1021/acs.jpcc.5b03634 PubMed DOI PMC
Bauer M., Nascakova Z., Mihai A. I., Cheng P. F., Levesque M. P., Lampart S., et al. . (2020). ALPK1/TIFA/NF-κB axis links a bacterial carcinogen to R-loop-induced replication stress. Nat. Commun. 11, 1–16. doi: 10.1038/s41467-020-18857-z PubMed DOI PMC
Boyanova L., Hadzhiyski P., Gergova R., Markovska R. (2023). Evolution of helicobacter pylori resistance to antibiotics: A topic of increasing concern. Antibiotics 12, 1–19. doi: 10.3390/antibiotics12020332 PubMed DOI PMC
Brandt S., Kwok T., Hartig R., Kö W., Backert S. (2005). NF-B activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. PNAS 102, 9300–9305. doi: 10.1073/pnas.0409873102 PubMed DOI PMC
De Matteis V. (2017). Exposure to inorganic nanoparticles: Routes of entry, immune response, biodistribution and in vitro/In vivo toxicity evaluation. Toxics 5, 1–21. doi: 10.3390/toxics5040029 PubMed DOI PMC
Ding Y. M., Li Y. Y., Liu J., Wang J., Wan M., Lin M. J., et al. . (2023). The cure rate of 10-day bismuth-containing quadruple therapy for Helicobacter pylori eradication is equivalent to 14-day: a systematic review and meta-analysis. Clin. Exp. Med. 23, 1033–1043. doi: 10.1007/s10238-022-00953-7 PubMed DOI
El Filaly H., Desterke C., Outlioua A., Badre W., Rabhi M., Karkouri M., et al. . (2023). CXCL-8 as a signature of severe Helicobacter pylori infection and a stimulator of stomach region-dependent immune response. Clin. Immunol. 252, 1–14. doi: 10.1016/j.clim.2023.109648 PubMed DOI
Faass L., Stein S. C., Hauke M., Gapp M., Albanese M., Josenhans C. (2021). Contribution of Heptose Metabolites and the cag Pathogenicity Island to the Activation of Monocytes/Macrophages by Helicobacter pylori. Front. Immunol. 12. doi: 10.3389/fimmu.2021.632154 PubMed DOI PMC
Fernando I., Lu D., Zhou Y. (2020). Interactive influence of extracellular polymeric substances (EPS) and electrolytes on the colloidal stability of silver nanoparticles. Environ. Sci. Nano 7, 186–197. doi: 10.1039/C9EN00861F DOI
Grande R., Sisto F., Puca V., Carradori S., Ronci M., Aceto A., et al. . (2020). Antimicrobial and antibiofilm activities of new synthesized silver ultra-nanoClusters (SUNCs) against helicobacter pylori. Front. Microbiol. 11. doi: 10.3389/fmicb.2020.01705 PubMed DOI PMC
Gurunathan S., Jeong J. K., Han J. W., Zhang X. F., Park J. H., Kim J. H. (2015). Multidimensional effects of biologically synthesized silver nanoparticles in Helicobacter pylori, Helicobacter felis, and human lung (L132) and lung carcinoma A549 cells. Nanoscale Res. Lett. 10, 1–17. doi: 10.1186/s11671-015-0747-0 PubMed DOI PMC
Gurunathan S., Qasim M., Park C., Yoo H., Kim J. H., Hong K. (2018). Cytotoxic potential and molecular pathway analysis of silver nanoparticles in human colon cancer cells HCT116. Int. J. Mol. Sci. 19, 1–19. doi: 10.3390/ijms19082269 PubMed DOI PMC
Hamida R. S., Ali M. A., Goda D. A., Khalil M. I., Redhwan A. (2020). Cytotoxic effect of green silver nanoparticles against ampicillin-resistantKlebsiella pneumoniae. RSC Adv. 10, 21136–21146. doi: 10.1039/D0RA03580G PubMed DOI PMC
Hochvaldová L., Večeřová R., Kolář M., Prucek R., Kvítek L., Lapčík L., et al. . (2022). Antibacterial nanomaterials: Upcoming hope to overcome antibiotic resistance crisis. Nanotechnol. Rev. 11, 1115–1142. doi: 10.1515/ntrev-2022-0059 DOI
Jahan I., Matpan Bekler F., Tunç A., Güven K. (2024). The effects of silver nanoparticles (AgNPs) on thermophilic bacteria: antibacterial, morphological, physiological and biochemical investigations. Microorganisms 12, 1–20. doi: 10.3390/microorganisms12020402 PubMed DOI PMC
Jang Y., Zhang X., Zhu R., Li S., Sun S., Li W., et al. . (2022). Viola betonicifolia-mediated biosynthesis of silver nanoparticles for improved biomedical applications. Front. Microbiol. 13. doi: 10.3389/fmicb.2022.891144 PubMed DOI PMC
Khan M. H., Unnikrishnan S., Ramalingam K. (2023). Antipathogenic efficacy of biogenic silver nanoparticles and antibiofilm activities against multi-drug-resistant ESKAPE pathogens. Appl. Biochem. Biotechnol. 196, 2031–2052. doi: 10.1007/s12010-023-04630-7 PubMed DOI
Krisch L. M., Posselt G., Hammerl P., Wesslera S. (2016). CagA phosphorylation in helicobacter pylori-infected B cells is mediated by the nonreceptor tyrosine kinases of the src and Abl families. Infect. Immun. 84, 2671–2680. doi: 10.1128/IAI.00349-16 PubMed DOI PMC
Kuo C. H., Lu C. Y., Yang Y. C., Chin C., Weng B. C., Liu C. J., et al. . (2014). Does long-term Use of silver nanoparticles have persistent inhibitory effect on H. pylori based on Mongolian gerbil’s model? BioMed. Res. Int. 2014, 1–7. doi: 10.1155/2014/461034 PubMed DOI PMC
Lopez-Carrizales M., Velasco K. I., Castillo C., Flores A., Magaña M., Martinez-Castanon G. A., et al. . (2018). In vitro synergism of silver nanoparticles with antibiotics as an alternative treatment in multiresistant uropathogens. Antibiotics 7, 1–13. doi: 10.3390/antibiotics7020050 PubMed DOI PMC
Malfertheiner P., Camargo M. C., El-Omar E., Liou J. M., Peek R., Schulz C., et al. . (2023). Helicobacter pylori infection. Nat. Rev. Dis. Primers 9, 1–24. doi: 10.1038/s41572-023-00431-8 PubMed DOI
Mansouri F., Saffari M., Moniri R., Abbas Moosavi G., Molaghanbari M., Razavizade M. (2022). Investigation of the effect of silver nanoparticles alone and their combination with clarithromycin on H. pylori isolates. Res. Quare. doi: 10.21203/rs.3.rs-1631922/v1 DOI
Mateo E. M., Jiménez M. (2022). Silver nanoparticle-based therapy: can it be useful to combat multi-drug resistant bacteria? Antibiotics 11, 1–13. doi: 10.3390/antibiotics11091205 PubMed DOI PMC
Moese S., Selbach M., Kwok T., Brinkmann V., König W., Meyer T. F., et al. . (2004). Helicobacter pylori induces AGS cell motility and elongation via independent signaling pathways. Infect. Immun. 72, 3646–3649. doi: 10.1128/IAI.72.6.3646-3649.2004 PubMed DOI PMC
Noga M., Milan J., Frydrych A., Jurowski K. (2023). Toxicological aspects, safety assessment, and green toxicology of silver nanoparticles (AgNPs)—Critical review: state of the art. Int. J. Mol. Sci. 24, 1–27. doi: 10.3390/ijms24065133 PubMed DOI PMC
Panáček A., Kvítek L., Prucek R., Kolář M., Večeřová R., Pizúrová N., et al. . (2006). Silver colloid nanoparticles: Synthesis, characterization, and their antibacterial activity. J. Phys. Chem. B. 110, 16248–16253. doi: 10.1021/jp063826h PubMed DOI
Pfannkuch L., Hurwitz R., Trauisen J., Sigulla J., Poeschke M., Matzner L., et al. . (2019). ADP heptose, a novel pathogen-associated molecular pattern identified in Helicobacter pylori. FASEB J. 33, 9087–9099. doi: 10.1096/fj.201802555R PubMed DOI PMC
Polet M., Laloux L., Cambier S., Ziebel J., Gutleb A. C., Schneider Y. J. (2020). Soluble silver ions from silver nanoparticles induce a polarised secretion of interleukin-8 in differentiated Caco-2 cells. Toxicol. Lett. 325, 14–24. doi: 10.1016/j.toxlet.2020.02.004 PubMed DOI
Poppe M., Feller S. M., Römer G., Wessler S. (2007). Phosphorylation of Helicobacter pylori CagA by c-Abl leads to cell motility. Oncogene 26, 3462–3472. doi: 10.1038/sj.onc.1210139 PubMed DOI
Pormohammad A., Mohtavinejad N., Gholizadeh P., Dabiri H., Salimi Chirani A., Hashemi A., et al. . (2019). Global estimate of gastric cancer in Helicobacter pylori–infected population: A systematic review and meta-analysis. J. Cell Physiol. 234, 1208–1218. doi: 10.1002/jcp.27114 PubMed DOI
Reyes V. E. (2023). Helicobacter pylori and its role in gastric cancer. Microorganisms 11, 1–21. doi: 10.3390/microorganisms11051312 PubMed DOI PMC
Rizzato C., Torres J., Obazee O., Camorlinga-Ponce M., Trujillo E., Stein A., et al. . (2020). Variations in cag pathogenicity island genes of Helicobacter pylori from Latin American groups may influence neoplastic progression to gastric cancer. Sci. Rep. 10, 1–9. doi: 10.1038/s41598-020-63463-0 PubMed DOI PMC
Sah D. K., Arjunan A., Lee B., Jung Y. D. (2023). Reactive oxygen species and H. pylori infection: A comprehensive review of their roles in gastric cancer development. Antioxidants 12, 1–27. doi: 10.3390/antiox12091712 PubMed DOI PMC
Sansonetti P. J., Arondel J., Huerre M., Harada A., Matsushima A. K. (1999). Interleukin-8 controls bacterial transepithelial translocation at the cost of epithelial destruction in experimental shigellosis. Infect Immun 67, 1471–1480. doi: 10.1128/IAI.67.3.1471-1480.1999 PubMed DOI PMC
Saravanakumar K., Chelliah R., MubarakAli D., Oh D. H., Kathiresan K., Wang M. H. (2019). Unveiling the potentials of biocompatible silver nanoparticles on human lung carcinoma A549 cells and Helicobacter pylori. Sci. Rep. 9, 1–8. doi: 10.1038/s41598-019-42112-1 PubMed DOI PMC
Sivera M., Kvitek L., Prucek R., Panacek A., Soukupova J. (2012). Study of silver nanoparticles stabilization performed by gelatin. Adv. Sci. Eng. Med. 3, 155–159. doi: 10.1166/asem.2011.1092 DOI
Slavin Y. N., Asnis J., Häfeli U. O., Bach H. (2017). Metal nanoparticles: Understanding the mechanisms behind antibacterial activity. J. Nanobiotechnol. 15, 1–20. doi: 10.1186/s12951-017-0308-z PubMed DOI PMC
Takahashi-Kanemitsu A., Knight C. T., Hatakeyama M. (2020). Molecular anatomy and pathogenic actions of Helicobacter pylori CagA that underpin gastric carcinogenesis. Cell Mol. Immunol. 17, 50–63. doi: 10.1038/s41423-019-0339-5 PubMed DOI PMC
Wahab S., Khan T., Adil M., Khan A. (2021). Mechanistic aspects of plant-based silver nanoparticles against multi-drug resistant bacteria. Heliyon 7, 1–11. doi: 10.1016/j.heliyon.2021.e07448 PubMed DOI PMC
Wang L., Hu C., Shao L. (2017). The antimicrobial activity of nanoparticles: Present situation and prospects for the future. Int. J. Nanomed. 12, 1227–1249. doi: 10.2147/IJN.S121956 PubMed DOI PMC
Yin X., Lai Y., Du Y., Zhang T., Gao J., Li Z. (2023). Metal-based nanoparticles: A prospective strategy for helicobacter pylori treatment. Int. J. Nanomed. 18, 2413–2429. doi: 10.2147/IJN.S405052 PubMed DOI PMC
Zhang J., Wang F., Yalamarty S. S. K., Filipczak N., Jin Y., Li X. (2022). Nano silver-induced toxicity and associated mechanisms. Int. J. Nanomed. 17, 1851–1864. doi: 10.2147/IJN.S355131 PubMed DOI PMC