Email Alert RSS
Volume 14 Issue 5
Sep.  2023
Turn off MathJax
Article Contents
Abstract
References
LUO Xiaoxia, QIN Sihua, WANG Huidi, ZHOU Hongwei, HE Yan. Mechanism of Bacterial Extracellular Vesicles in Disease Development and Prospects for Application[J]. Medical Journal of Peking Union Medical College Hospital, 2023, 14(5): 915-924. DOI: 10.12290/xhyxzz.2023-0260
Citation: LUO Xiaoxia, QIN Sihua, WANG Huidi, ZHOU Hongwei, HE Yan. Mechanism of Bacterial Extracellular Vesicles in Disease Development and Prospects for Application[J]. Medical Journal of Peking Union Medical College Hospital, 2023, 14(5): 915-924. DOI: 10.12290/xhyxzz.2023-0260
shu

Mechanism of Bacterial Extracellular Vesicles in Disease Development and Prospects for Application

  • 1.

    Microbiome Medicine Center, Department of Laboratory Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou 510000, China

  • 2.

    State Key Laboratory of Organ Failure Research, Southern Medical University, Guangzhou 510000, China

  • 3.

    Guangdong Provincial Clinical Research Center for Laboratory Medicine, Guangzhou 510000, China

Funds: 

National Natural Science Foundation of China 82272391

National Natural Science Foundation of China 82022044

More Information
  • Corresponding author:

    HE Yan, E-mail: bioyanhe@gmail.com

  • Received Date: May 30, 2023
  • Accepted Date: June 26, 2023
  • Available Online: July 11, 2023
  • Issue Publish Date: September 29, 2023
    Graphical Abstract
    • Abstract
  • Bacterial extracellular vesicles (BEVs), bacteria-derived extracellular vesicles, are key intermediates of bacteria-bacteria and bacteria-host interactions. They are a "double-edged sword". On one hand, they play a negative role in the onset and progression of various diseases, including intestinal inflammatory disease, neurological disease, liver disease, metabolic disease, autoimmune disease and cancer. On the other hand, they play a positive role as potential biomarkers, vaccines, antitumor agents. The application of BEVs may provide novel strategies for the diagnosis and treatment of diseases. However, research on BEVs is still in its infancy, and challenges remain in vesicle isolation techniques, disease diagnostic specificity, optimization of vesicle storage and transport. Thus rigorously designed clinical studies are required to verify their diagnostic and therapeutic value.
    • FullText(HTML)
    • References (75)
  • [1]
    Toyofuku M, Nomura N, Eberl L. Types and origins of bacterial membrane vesicles[J]. Nat Rev Microbiol, 2019, 17: 13-24. DOI: 10.1038/s41579-018-0112-2
    [2]
    Díaz-Garrido N, Badia J, Baldomà L. Microbiota-derived extracellular vesicles in interkingdom communication in the gut[J]. J Extracell Vesicles, 2021, 10: e12161. DOI: 10.1002/jev2.12161
    [3]
    Toyofuku M, Schild S, Kaparakis-Liaskos M, et al. Composition and functions of bacterial membrane vesicles[J]. Nat Rev Microbiol, 2023, 21: 415-430. DOI: 10.1038/s41579-023-00875-5
    [4]
    Hendrix A, De Wever O. Systemically circulating bacterial extracellular vesicles: origin, fate, and function[J]. Trends Microbiol, 2022, 30: 213-216. DOI: 10.1016/j.tim.2021.12.012
    [5]
    Toyofuku M, Cárcamo-Oyarce G, Yamamoto T, et al. Prophage-triggered membrane vesicle formation through peptidoglycan damage in Bacillus subtilis[J]. Nat Commun, 2017, 8: 481. DOI: 10.1038/s41467-017-00492-w
    [6]
    Xie J, Li Q, Haesebrouck F, et al. The tremendous biomedical potential of bacterial extracellular vesicles[J]. Trends Biotechnol, 2022, 40: 1173-1194. DOI: 10.1016/j.tibtech.2022.03.005
    [7]
    Devos S, Van Putte W, Vitse J, et al. Membrane vesicle secretion and prophage induction in multidrug-resistant Stenotrophomonas maltophilia in response to ciprofloxacin stress[J]. Environ Microbiol, 2017, 19: 3930-3937. DOI: 10.1111/1462-2920.13793
    [8]
    Brown L, Wolf JM, Prados-Rosales R, et al. Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi[J]. Nat Rev Microbiol, 2015, 13: 620-630. DOI: 10.1038/nrmicro3480
    [9]
    Lee EY, Choi DS, Kim KP, et al. Proteomics in gram-negative bacterial outer membrane vesicles[J]. Mass Spectrom Rev, 2008, 27: 535-555. DOI: 10.1002/mas.20175
    [10]
    Zakharzhevskaya NB, Vanyushkina AA, Altukhov IA, et al. Outer membrane vesicles secreted by pathogenic and nonpathogenic Bacteroides fragilis represent different metabolic activities[J]. Sci Rep, 2017, 7: 5008. DOI: 10.1038/s41598-017-05264-6
    [11]
    Kaplan GG. The global burden of IBD: from 2015 to 2025[J]. Nat Rev Gastroenterol Hepatol, 2015, 12: 720-727. DOI: 10.1038/nrgastro.2015.150
    [12]
    Jones E, Stentz R, Telatin A, et al. The Origin of Plasma-Derived Bacterial Extracellular Vesicles in Healthy Individuals and Patients with Inflammatory Bowel Disease: A Pilot Study[J]. Genes (Basel), 2021, 12: 1636. DOI: 10.3390/genes12101636
    [13]
    Liu L, Liang L, Yang C, et al. Extracellular vesicles of Fusobacterium nucleatum compromise intestinal barrier through targeting RIPK1-mediated cell death pathway[J]. Gut Microbes, 2021, 13: 1-20.
    [14]
    Engevik MA, Danhof HA, Ruan W, et al. Fusobacterium nucleatum Secretes Outer Membrane Vesicles and Promotes Intestinal Inflammation[J]. mBio, 2021, 12: e02706-20.
    [15]
    Kaparakis M, Turnbull L, Carneiro L, et al. Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells[J]. Cell Microbiol, 2010, 12: 372-385. DOI: 10.1111/j.1462-5822.2009.01404.x
    [16]
    Patten DA, Hussein E, Davies SP, et al. Commensal-derived OMVs elicit a mild proinflammatory response in intestinal epithelial cells[J]. Microbiology (Reading), 2017, 163: 702-711. DOI: 10.1099/mic.0.000468
    [17]
    Pritchard AB, Fabian Z, Lawrence CL, et al. An Investigation into the Effects of Outer Membrane Vesicles and Lipopolysaccharide of Porphyromonas gingivalis on Blood-Brain Barrier Integrity, Permeability, and Disruption of Scaffolding Proteins in a Human in vitro Model[J]. J Alzheimers Dis, 2022, 86: 343-364. DOI: 10.3233/JAD-215054
    [18]
    Muraca M, Putignani L, Fierabracci A, et al. Gut microbiota-derived outer membrane vesicles: under-recognized major players in health and disease?[J]. Discov Med, 2015, 19: 343-348.
    [19]
    Choi HI, Choi JP, Seo J, et al. Helicobacter pylori-derived extracellular vesicles increased in the gastric juices of gastric adenocarcinoma patients and induced inflammation mainly via specific targeting of gastric epithelial cells[J]. Exp Mol Med, 2017, 49: e330. DOI: 10.1038/emm.2017.47
    [20]
    Lee KE, Kim JK, Han SK, et al. The extracellular vesicle of gut microbial Paenalcaligenes hominis is a risk factor for vagus nerve-mediated cognitive impairment[J]. Microbiome, 2020, 8: 107. DOI: 10.1186/s40168-020-00881-2
    [21]
    Ma X, Shin YJ, Yoo JW, et al. Extracellular vesicles derived from Porphyromonas gingivalis induce vagus nerve-mediated cognitive impairment[J]. J Adv Res, 2023. doi: 10.1016/j.jare.2023.02.006.
    [22]
    Park AM, Tsunoda I. Helicobacter pylori infection in the stomach induces neuroinflammation: the potential roles of bacterial outer membrane vesicles in an animal model of Alzheimer's disease[J]. Inflamm Regen, 2022, 42: 39. DOI: 10.1186/s41232-022-00224-8
    [23]
    Yoshida K, Yoshida K, Seyama M, et al. Porphyromonas gingivalis outer membrane vesicles in cerebral ventricles activate microglia in mice[J]. Oral Dis, 2022. doi: 10.1111/odi.14413.
    [24]
    Wei S, Peng W, Mai Y, et al. Outer membrane vesicles enhance tau phosphorylation and contribute to cognitive impairment[J]. J Cell Physiol, 2019, 235: 4843-4855.
    [25]
    Gong T, Chen Q, Mao H, et al. Outer membrane vesicles of Porphyromonas gingivalis trigger NLRP3 inflammasome and induce neuroinflammation, tau phosphorylation, and memory dysfunction in mice[J]. Front Cell Infect Microbiol, 2022, 12: 925435. DOI: 10.3389/fcimb.2022.925435
    [26]
    Younossi ZM, Golabi P, de Avila L, et al. The global epidemiology of NAFLD and NASH in patients with type 2 diabetes: A systematic review and meta-analysis[J]. J Hepatol, 2019, 71: 793-801. DOI: 10.1016/j.jhep.2019.06.021
    [27]
    Villard A, Boursier J, Andriantsitohaina R. Bacterial and eukaryotic extracellular vesicles and nonalcoholic fatty liver disease: new players in the gut-liver axis? [J]. Am J Physiol Gastrointest Liver Physiol, 2021, 320: G485-G495. DOI: 10.1152/ajpgi.00362.2020
    [28]
    Fizanne L, Villard A, Benabbou N, et al. Faeces-derived extracellular vesicles participate in the onset of barrier dysfunction leading to liver diseases[J]. J Extracell Vesicles, 2023, 12: e12303. DOI: 10.1002/jev2.12303
    [29]
    Natsui K, Tsuchiya A, Imamiya R, et al. Escherichia coli-derived outer-membrane vesicles induce immune activation and progression of cirrhosis in mice and humans[J]. Liver Int, 2023, 43: 1126-1140. DOI: 10.1111/liv.15539
    [30]
    Choi Y, Kwon Y, Kim DK, et al. Gut microbe-derived extracellular vesicles induce insulin resistance, thereby impairing glucose metabolism in skeletal muscle[J]. Sci Rep, 2015, 5: 15878. DOI: 10.1038/srep15878
    [31]
    Chelakkot C, Choi Y, Kim D, et al. Akkermansia muciniphila-derived extracellular vesicles influence gut permea-bility through the regulation of tight junctions[J]. Exp Mol Mede, 2018, 50: e450. DOI: 10.1038/emm.2017.282
    [32]
    Luo Z, Ji Y, Gao H, et al. CRIg+ Macrophages Prevent Gut Microbial DNA-Containing Extracellular Vesicle-Induced Tissue Inflammation and Insulin Resistance[J]. Gastroenterology, 2021, 160: 863-874. DOI: 10.1053/j.gastro.2020.10.042
    [33]
    Mcinnes IB, Schett G. The pathogenesis of rheumatoid arthritis[J]. N Engl J Med, 2011, 365: 2205-2219. DOI: 10.1056/NEJMra1004965
    [34]
    Hong M, Li Z, Liu H, et al. Fusobacterium nucleatum aggravates rheumatoid arthritis through FadA-containing outer membrane vesicles[J]. Cell Host Microbe, 2023, 31: 798-810. e7. DOI: 10.1016/j.chom.2023.03.018
    [35]
    Quirke AM, Lugli EB, Wegner N, et al. Heightened immune response to autocitrullinated Porphyromonas gin-givalis peptidylarginine deiminase: a potential mechanism for breaching immunologic tolerance in rheumatoid arthritis[J]. Ann Rheum Dis, 2014, 73: 263-269.
    [36]
    Gabarrini G, Palma Medina LM, Stobernack T, et al. There's no place like OM: Vesicular sorting and secretion of the peptidylarginine deiminase of Porphyromonas gingivalis[J]. Virulence, 2018, 9: 456-464.
    [37]
    Sepich-Poore GD, Zitvogel L, Straussman R, et al. The microbiome and human cancer[J]. Science, 2021, 371: eabc4552. DOI: 10.1126/science.abc4552
    [38]
    Chronopoulos A, Kalluri R. Emerging role of bacterial extracellular vesicles in cancer[J]. Oncogene, 2020, 39: 6951-6960. DOI: 10.1038/s41388-020-01509-3
    [39]
    Chen G, Gao C, Jiang S, et al. Fusobacterium nucleatum outer membrane vesicles activate autophagy to promote oral cancer metastasis[J]. J Adv Res, 2023. doi: 10.1016/j.jare.2023.04.002.
    [40]
    Schaack B, Hindré T, Quansah N, et al. Microbiota-Derived Extracellular Vesicles Detected in Human Blood from Healthy Donors[J]. Int J Mol Sci, 2022, 23: 13787. DOI: 10.3390/ijms232213787
    [41]
    Yoo JY, Rho M, You YA, et al. 16S rRNA gene-based metagenomic analysis reveals differences in bacteria-derived extracellular vesicles in the urine of pregnant and non-pregnant women[J]. Exp Mol Med, 2016, 48: e208. DOI: 10.1038/emm.2015.110
    [42]
    Vandendriessche C, Kapogiannis D, Vandenbroucke RE. Biomarker and therapeutic potential of peripheral extracel-lular vesicles in Alzheimer's disease[J]. Adv Drug Deliv Rev, 2022, 190: 114486. DOI: 10.1016/j.addr.2022.114486
    [43]
    Dey S, Gudipati S, Giuliano C, et al. Reduced Production of Bacterial Membrane Vesicles Predicts Mortality in ST45/USA600 Methicillin-Resistant Staphylococcus aureus Bacteremia[J]. Antibiotics (Basel), 2019, 9: 2. DOI: 10.3390/antibiotics9010002
    [44]
    Wei SC, Wei W, Peng WJ, et al. Metabolic Alterations in the Outer Membrane Vesicles of Patients with Alzheimer's Disease: An LC-MS/MS-based Metabolomics Analysis[J]. Curr Alzheimer Res, 2019, 16: 1183-1195.
    [45]
    Yang J, Moon HE, Park HW, et al. Brain tumor diagnostic model and dietary effect based on extracellular vesicle microbiome data in serum[J]. Exp Mol Med, 2020, 52: 1602-1613. DOI: 10.1038/s12276-020-00501-x
    [46]
    Kim SI, Kang N, Leem S, et al. Metagenomic Analysis of Serum Microbe-Derived Extracellular Vesicles and Diagnostic Models to Differentiate Ovarian Cancer and Benign Ovarian Tumor[J]. Cancers (Basel), 2020, 12: 1309. DOI: 10.3390/cancers12051309
    [47]
    Kim DJ, Yang J, Seo H, et al. Colorectal cancer diagnostic model utilizing metagenomic and metabolomic data of stool microbial extracellular vesicles[J]. Sci Rep, 2020, 10: 2860. DOI: 10.1038/s41598-020-59529-8
    [48]
    Yang J, McdowelL A, Seo H, et al. Diagnostic Models for Atopic Dermatitis Based on Serum Microbial Extracellular Vesicle Metagenomic Analysis: A Pilot Study[J]. Allergy Asthma Immunol Res, 2020, 12: 792-805. DOI: 10.4168/aair.2020.12.5.792
    [49]
    Yang J, Hong G, Kim YS, et al. Lung Disease Diagnostic Model Through IgG Sensitization to Microbial Extracellular Vesicles[J]. Allergy Asthma Immunol Res, 2020, 12: 669-683. DOI: 10.4168/aair.2020.12.4.669
    [50]
    Han P, Bartold PM, Salomon C, et al. Salivary Outer Membrane Vesicles and DNA Methylation of Small Extracellular Vesicles as Biomarkers for Periodontal Status: A Pilot Study[J]. Int J Mol Sci, 2021, 22: 2423. DOI: 10.3390/ijms22052423
    [51]
    Yoon H, Kim NE, Park J, et al. Analysis of the gut microbiome using extracellular vesicles in the urine of patients with colorectal cancer[J]. Korean J Intern Med, 2023, 38: 27-38. DOI: 10.3904/kjim.2022.112
    [52]
    VesikarI T, Esposito S, Prymula R, et al. Immunogenicity and safety of an investigational multicomponent, recombin-ant, meningococcal serogroup B vaccine (4CMenB) administered concomitantly with routine infant and child vaccinations: results of two randomised trials[J]. Lancet, 2013, 381: 825-835. DOI: 10.1016/S0140-6736(12)61961-8
    [53]
    Kaparakis-Liaskos M, Ferrero RL. Immune modulation by bacterial outer membrane vesicles[J]. Nat Rev Immunol, 2015, 15: 375-387. DOI: 10.1038/nri3837
    [54]
    Wo J, Lv ZY, Sun JN, et al. Engineering probiotic-derived outer membrane vesicles as functional vaccine carriers to enhance immunity against SARS-CoV-2[J]. iScience, 2023, 26: 105772. DOI: 10.1016/j.isci.2022.105772
    [55]
    Chen L, Valentine JL, Huang CJ, et al. Outer membrane vesicles displaying engineered glycotopes elicit protective antibodies[J]. Proc Natl Acad Sci U S A, 2016, 113: E3609-E3618. DOI: 10.1073/pnas.1523686113
    [56]
    Ñahui Palomino RA, Vanpouille C, Laghi L, et al. Extracellular vesicles from symbiotic vaginal lactobacilli inhibit HIV-1 infection of human tissues[J]. Nat Commun, 2019, 10: 5656. DOI: 10.1038/s41467-019-13468-9
    [57]
    Kim MH, Choi S J, Choi HI, et al. Lactobacillus plantarum-derived Extracellular Vesicles Protect Atopic Dermatitis Induced by Staphylococcus aureus-derived Extracellular Vesicles[J]. Allergy Asthma Immunol Res, 2018, 10: 516-532. DOI: 10.4168/aair.2018.10.5.516
    [58]
    Tong L, Zhang X, Hao H, et al. Lactobacillus rhamnosus GG Derived Extracellular Vesicles Modulate Gut Microbiota and Attenuate Inflammatory in DSS-Induced Colitis Mice[J]. Nutrients, 2021, 13: 3319. DOI: 10.3390/nu13103319
    [59]
    Hu R, Lin H, Wang M, et al. Lactobacillus reuteri-derived extracellular vesicles maintain intestinal immune homeostasis against lipopolysaccharide-induced inflammatory responses in broilers[J]. J Anim Sci Biotechnol, 2021, 12: 25. DOI: 10.1186/s40104-020-00532-4
    [60]
    Lee DH, Park HK, Lee HR, et al. Immunoregulatory effects of Lactococcus lactis-derived extracellular vesicles in allergic asthma[J]. Clin Transl Allergy, 2022, 12: e12138. DOI: 10.1002/clt2.12138
    [61]
    Croatti V, Parolin C, Giordani B, et al. Lactobacilli extracellular vesicles: potential postbiotics to support the vaginal microbiota homeostasis[J]. Microb Cell Fact, 2022, 21: 237. DOI: 10.1186/s12934-022-01963-6
    [62]
    Choi J, Kwon H, Kim YK, et al. Extracellular Vesicles from Gram-positive and Gram-negative Probiotics Remediate Stress-Induced Depressive Behavior in Mice[J]. Mol Neurobiol, 2022, 59: 2715-2728. DOI: 10.1007/s12035-021-02655-9
    [63]
    Ye W, Chen Z, He Z, et al. Lactobacillus plantarum-Derived Postbiotics Ameliorate Acute Alcohol-Induced Liver Injury by Protecting Cells from Oxidative Damage, Improving Lipid Metabolism, and Regulating Intestinal Microbiota[J]. Nutrients, 2023, 15: 845. DOI: 10.3390/nu15040845
    [64]
    Wang X, Lin S, Wang L, et al. Versatility of bacterial outer membrane vesicles in regulating intestinal homeostasis[J]. Sci Adv, 2023, 9: eade5079.
    [65]
    Starnes CO. Coley's toxins[J]. Nature, 1992, 360: 23.
    [66]
    Kim OY, ParK HT, Dinh NTH, et al. Bacterial outer membrane vesicles suppress tumor by interferon-γ-mediated antitumor response[J]. Nat Commun, 2017, 8: 626. DOI: 10.1038/s41467-017-00729-8
    [67]
    Qing S, Lyu C, Zhu L, et al. Biomineralized Bacterial Outer Membrane Vesicles Potentiate Safe and Efficient Tumor Microenvironment Reprogramming for Anticancer Therapy[J]. Adv Mater, 2020, 32: e2002085. DOI: 10.1002/adma.202002085
    [68]
    Li Y, Ma X, Yue Y, et al. Rapid Surface Display of mRNA Antigens by Bacteria-Derived Outer Membrane Vesicles for a Personalized Tumor Vaccine [J]. Adv Mater, 2022, 34: e2109984. DOI: 10.1002/adma.202109984
    [69]
    Meng F, Li L, Zhang Z, et al. Biosynthetic neoantigen displayed on bacteria derived vesicles elicit systemic antitumour immunity[J]. J Extracell Vesicles, 2022, 11: e12289. DOI: 10.1002/jev2.12289
    [70]
    Kuerban K, Gao X, Zhang H, et al. Doxorubicin-loaded bacterial outer-membrane vesicles exert enhanced anti-tumor efficacy in non-small-cell lung cancer[J]. Acta Pharm Sin B, 2020, 10: 1534-1548.
    [71]
    Liu XZ, Wen ZJ, Li YM, et al. Bioengineered Bacterial Membrane Vesicles with Multifunctional Nanoparticles as a Versatile Platform for Cancer Immunotherapy[J]. ACS Appl Mater Interfaces, 2023, 15: 3744-3759. DOI: 10.1021/acsami.2c18244
    [72]
    Bauman SJ, Kuehn MJ. Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response[J]. Microbes Infect, 2006, 8: 2400-2408. DOI: 10.1016/j.micinf.2006.05.001
    [73]
    Northrop-Albrecht EJ, Taylor WR, Huang BQ, et al. Assessment of extracellular vesicle isolation methods from human stool supernatant[J]. J Extracell Vesicles, 2022, 11: e12208. DOI: 10.1002/jev2.12208
    [74]
    Hong J, Dauros-Singorenko P, Whitcombe A, et al. Analysis of the Escherichia coli extracellular vesicle proteome identifies markers of purity and culture conditions[J]. J Extracell Vesicles, 2019, 8: 1632099.
    [75]
    Gelibter S, Marostica G, Mandelli A, et al. The impact of storage on extracellular vesicles: A systematic study[J]. J Extracell Vesicles, 2022, 11: e12162. DOI: 10.1002/jev2.12162
    • Related Articles

Catalog

    Get Citation
    PDF
    XML

    Article Metrics

    Article views (2153) PDF downloads (217) Cited by()
    Related
    Links: National Health Commission of the People's Republic of China Chinese Academy of Medical Sciences(CAMS) AMLC Check CNKI Database CNKI Term Online Chinese General Practice
    Address：Room 302,Third Floor,Building 7, No. 1 Shuaifuyuan, Wangfujing, Dongcheng District, Beijing 100730, China
    Tel：010-69154261/4262
    E - mail：medj@pumch.cn mjpumch@126.com
    Copyright of website：Editorial Office of Medical Journal of Peking Union Medical College Hospital

    Supported by: Beijing Renhe Information Technology Co., Ltd.  Baidu Analytics

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return
    x Close Forever Close