Skip to main content

Membrane Vesicles from the Gut Microbiota and Their Interactions with the Host

  • Chapter
  • First Online:
Bacterial Membrane Vesicles

Abstract

Gut microbiota plays an essential role in maintaining intestinal homeostasis and human health. Microbiota establishes a complex network of dynamic and reciprocal interactions with the intestinal epithelium and immune system. The mucin layer that covers the epithelium prevents luminal bacteria from accessing host cells. Thus, microbiota–host communication mainly relies on secreted factors and membrane vesicles (MVs), which can cross the inner mucus layer and reach the epithelium. This chapter focuses on the role of microbiota-secreted MVs as key players in signaling processes in the intestinal mucosa. This is an emerging research topic, with the first reports dating from 2012. Microbiota-derived MVs are involved in interspecies communication in the gut, between bacteria and between microbiota and host. Here we present current knowledge on the mechanisms used by microbiota MVs to assist and control the gut microbial community and to modulate host immune and defense responses. Constant stimulation of immune receptors by microbiota MVs results in tightly controlled inflammation that contributes to tolerogenic responses essential to maintaining intestinal homeostasis. Moreover, gut microbiota MVs are emerging as physical vehicles for distribution and delivery of bacterial effectors to distal tissues in human health and disease.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

Abbreviations

BMCDs:

bone marrow-derived dendritic cells

CME:

clathrin-mediated endocytosis

DCs:

dendritic cells

DSS:

dextran sodium sulfate

Gadd45α:

growth arrest and DNA-damage-inducible protein,

GI:

gastrointestinal

HFD:

high-fat diet

IBD:

inflammatory bowel disease

IECs:

intestinal epithelial cells

iNOS:

inducible nitric oxide synthase

LPS:

lipopolysaccharide

MAMPs:

microbial-associated molecular patterns

miRNAs:

microRNAs

MMP:

matrix metalloprotease

MUC:

mucin

MVs:

membrane vesicles

ncRNAs:

non coding RNAs

NOD:

nucleotide-binding oligomerization domain protein

PGN:

peptidoglycan

PRRs:

pattern-recognition receptors

PSA:

polysaccharide A

RIP2:

receptor-interacting protein 2

TFF-3:

trefoil factor 3

Th:

T helper

TLRs:

tol-like receptors

TNBS:

2,4,6-trinitrobenzene sulfonic acid

Treg:

regulatory T cells

ZO:

zonula occludens

References

  • Aguilar C, Mano M, Eulalio A (2018) MicroRNAs at the host-bacteria interface: host defense or bacterial offense. Trends Microbiol 27:206–218

    Article  PubMed  CAS  Google Scholar 

  • Aguilera L, Toloza L, Giménez R et al (2014) Proteomic analysis of outer membrane vesicles from the probiotic strain Escherichia coli Nissle 1917. Proteomics 14(2–3):222–229

    Article  CAS  PubMed  Google Scholar 

  • Allison CC, Kufer TA, Kremmer et al (2009) Helicobacter pylori induces MAPK phosphorylation and AP-1 activation via a NOD1-dependent mechanism. J Immunol 183(12):8099–8109

    Article  CAS  PubMed  Google Scholar 

  • Al-Nedawi K, Main MF, Hossain N et al (2015) Gut commensal microvesicles reproduce parent bacterial signals to host immune and enteric nervous systems. FASEB J 29(2):684–695

    Article  CAS  PubMed  Google Scholar 

  • Alvarez CS, Badia J, Bosch M et al (2016) Outer membrane vesicles and soluble factors released by probiotic Escherichia coli Nissle 1917 and commensal EcoR63 enhance barrier function by regulating expression of tight junction proteins in intestinal epithelial cells. Front Microbiol 7:1981

    PubMed  PubMed Central  Google Scholar 

  • Apostolopoulos V, Stojanovska L, Gargosky SE (2015) MUC1 (CD227): a multi-tasked molecule. Cell Mol Life Sci 72:4475–4500

    Article  CAS  PubMed  Google Scholar 

  • Arentsen T, Qian Y, Gkotzis S et al (2017) The bacterial peptidoglycan-sensing molecule Pglyrp2 modulates brain development and behavior. Mol Psychiatry 22:257–266

    Article  CAS  PubMed  Google Scholar 

  • Baothman OA, Zamzami MA, Taher I et al (2016) The role of gut microbiota in the development of obesity and diabetes. Lipids Health Dis 15:108

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Belkaid Y, Hand TW (2014) Role of the microbiota in immunity and inflammation. Cell 157(1):121–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behzadi E, Mahmoodzadeh Hosseini H, Imani Fooladi AA (2017) The inhibitory impacts of Lactobacillus rhamnosus GG-derived extracellular vesicles on the growth of hepatic cancer cells. Microb Pathog 110:1–6

    Article  CAS  PubMed  Google Scholar 

  • Bomberger JM, Maceachran DP, Coutermarsh BA et al (2009) Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog 5:e1000382. https://doi.org/10.1371/journal.ppat.1000382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brameyer S, Plener L, Muller A et al (2018) Outer membrane vesicles facilitate trafficking of the hydrophobic signaling molecules CAI-1 between Vibrio harveyi cells. J Bacteriol 200:e00740–e00717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bron PA, van Baarlen P, Kleerebezem M (2011) Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat Rev Microbiol 10(1):66–78

    Article  PubMed  CAS  Google Scholar 

  • Brown L, Wolf JM, Prados-Rosales R et al (2015) Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi. Nat Rev Microbiol 13(10):620–630. https://doi.org/10.1038/nrmicro3480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bryant WA, Stentz R, Le Gall G et al (2017) In silico analysis of the small molecule content of outer membrane vesicles produced by Bacteroides thetaiotaomicron indicates an extensive metabolic link between microbe and host. Front Microbiol 8:2440. https://doi.org/10.3389/fmicb.2017.02440

    Article  PubMed  PubMed Central  Google Scholar 

  • Caballero S, Pamer EG (2015) Microbiota-mediated inflammation and antimicrobial defense in the intestine. Annu Rev Immunol 33:227–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cani PD, Amar J, Iglesias MA et al (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56:1761–1772

    Article  CAS  PubMed  Google Scholar 

  • Cani PD (2018) Human gut microbiome: hopes, threats and promises. Gut 67(9):1716–1725

    Article  CAS  PubMed  Google Scholar 

  • Cañas MA, Giménez R, Fábrega MJ et al (2016) Outer membrane vesicles from the probiotic Escherichia coli Nissle 1917 and the commensal ECOR12 enter intestinal epithelial cells via clathrin-dependent endocytosis and elicit differential effects on DNA damage. PLoS One 11(8):e0160374

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cañas MA, Fábrega MJ, Giménez R et al (2018) Outer membrane vesicles from probiotic and commensal Escherichia coli activate Nod1-mediated immune responses in intestinal epithelial cells. Front Microbiol 9:98

    Article  Google Scholar 

  • Celluzzi A, Masotti A (2016) How our other genome controls our epi-genome. Trends Microbiol 24(10):777–787

    Article  CAS  PubMed  Google Scholar 

  • Chamaillard M, Hashimoto M, Horie Y et al (2003) An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol 4:702–707

    Article  CAS  PubMed  Google Scholar 

  • Chatzidaki-Livanis M, Coyne MJ, Comstock LE (2014) An antimicrobial protein of the gut symbiont Bacteroides fragilis with a MACPF domain of host immune proteins. Mol Microbiol 94(6):1361–1374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chelakkot C, Choi Y, Kim DK et al (2018) Akkermansia muciniphila-derived extracellular vesicles influence gut permeability through the regulation of tight junctions. Exp Mol Med 50(2):e450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi JW, Kim SC, Hong SH et al (2017) Secretable small RNAs via outer membrane vesicles in periodontal pathogens. J Dent Res 96(4):458–466

    Article  CAS  PubMed  Google Scholar 

  • Chu H (2017) Host gene–microbiome interactions: molecular mechanisms in inflammatory bowel disease. Genome Med 9:69

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Clarke TB, Davis KM, Lysenko ES et al (2010) Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med 16(2):228–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Domínguez Rubio AP, Martínez JH, Martinez Casillas DC et al (2017) Lactobacillus casei BL23 produces microvesicles carrying proteins that have been associated with its probiotic effect. Front Microbiol 8:1783

    Article  PubMed  PubMed Central  Google Scholar 

  • Donaldson GP, Lee SM, Mazmanian SK (2016) Gut biogeography of the bacterial microbiota. Nat Rev Microbiol 14(1):20–32

    Article  CAS  PubMed  Google Scholar 

  • Emery DC, Shoemark DK, Batstone TE et al (2017) 16S rRNA next generation sequencing analysis shows bacteria in Alzheimer’s post-mortem brain. Front Aging Neurosci 9:195

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Elhenawy W, Debelyy MO, Feldman MF (2014) Preferential packing of acidic glycosidases and proteases into Bacteroides outer membrane vesicles. MBio 5(2):e00909–e00914

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ewaschuk JB, Diaz H, Meddings L et al (2008) Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am J Physiol Gastrointest Liver Physiol 295:G1025–G1034

    Article  CAS  PubMed  Google Scholar 

  • Fábrega MJ, Aguilera L, Giménez R et al (2016) Activation of immune and defense responses in the intestinal mucosa by outer membrane vesicles of commensal and probiotic Escherichia coli strains. Front Microbiol 7:705

    PubMed  PubMed Central  Google Scholar 

  • Fábrega MJ, Rodríguez-Nogales A, Garrido-Mesa J et al (2017) Intestinal anti-inflammatory effects of outer membrane vesicles from Escherichia coli Nissle 1917 in DSS-experimental colitis in mice. Front Microbiol 8:1274

    Article  PubMed  PubMed Central  Google Scholar 

  • Faderl M, Noti M, Corazza N et al (2015) Keeping bugs in check: the mucus layer as a critical component in maintaining intestinal homeostasis. IUBMB Life 67(4):275–285

    Article  CAS  PubMed  Google Scholar 

  • Feerick CL, McKernan DP (2016) Understanding the regulation of pattern recognition receptors in inflammatory diseases - a ‘Nod’ in the right direction. Immunology 150(3):237–247

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Feng Q, Chen WD, Wang YD (2018) Gut microbiota: an integral moderator in health and disease. Front Microbiol 9:151

    Article  PubMed  PubMed Central  Google Scholar 

  • Geuking MB, Cahenzli J, Lawson MA et al (2011) Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 34(5):794–806

    Article  CAS  PubMed  Google Scholar 

  • Girardin SE, Boneca IG, Carneiro LA et al (2003a) Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300:1584–1587

    Article  CAS  PubMed  Google Scholar 

  • Girardin SE, Boneca IG, Viala J et al (2003b) Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278:8869–8872

    Article  CAS  PubMed  Google Scholar 

  • Gopalakrishnan V, Helmink BA, Spencer CN et al (2018) The influence of the gut microbiome on cancer, immunity and cancer immunotherapy. Cancer Cell 33:570–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosal A, Upadhyaya BB, Fritz JV et al (2015) The extracellular RNA complement of Escherichia coli. Microbiology 4(2):252–266

    CAS  Google Scholar 

  • Guerrero-Mandujano A, Hernández-Cortez C, Ibarra JA (2017) The outer membrane vesicles: secretion system type zero. Traffic 18:425–432

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa M, Fujimoto Y, Lucas PC et al (2008) A critical role of RICK/RIP2 polyubiquitination in nod-induced NF-kappa B activation. EMBO J 27:373–383

    Article  CAS  PubMed  Google Scholar 

  • Hering NA, Richter JF, Fromm A et al (2014) TcpC protein from E. coli Nissle improves epithelial barrier function involving PKCƺ and ERK1/2 signaling in HT-29/B6 cells. Mucosal Immunol 7:369–378

    Article  CAS  PubMed  Google Scholar 

  • Hickey CA, Kuhn KA, Donermeyer DL et al (2015) Colitogenic Bacteroides thetaiotaomicron antigens access host immune cells in a sulfatase-dependent manner via outer membrane vesicles. Cell Host Microbe 17(5):672–680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inohara N, Koseki T, Lin J et al (2000) An induced proximity model for NF-kappa B activation in the Nod1/RICK and RIP signaling pathways. J Biol Chem 275(36):27823–27831

    CAS  PubMed  Google Scholar 

  • Irving AT, Mimuro H, Kufer TA et al (2014) The immune receptor NOD1 and kinase RIP2 interact with bacterial peptidoglycan on early endosomes to promote autophagy and inflammatory signalling. Cell Host Microbe 15(5):623–635

    Article  CAS  PubMed  Google Scholar 

  • Jager J, Keese S, Roessle M et al (2014) Fusion of Legionella pneumophila outer membrane vesicles with eukaryotic membrane systems is a mechanism to deliver pathogen factors to host cell membranes. Cell Microbiol 17:607–620. https://doi.org/10.1111/cmi.12392

    Article  CAS  PubMed  Google Scholar 

  • Jandhyala SM, Talukdar R, Subramanyam C et al (2015) Role of the normal gut microbiota. World J Gastroenterol 21(29):8787–8803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia L, Lu J, Zhou Y et al (2018) Tolerogenic dendritic cells induced the enrichment of CD4+Foxp3+ regulatory T cells via TGF-β in mesenteric lymph nodes of murine LPS-induced tolerance model. Clin Immunol 197:118–129

    Article  CAS  PubMed  Google Scholar 

  • Johansson MEV, Holmén Larsson JM, Hansson GC (2011) The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci U S A 108(3Suppl 1):4659–4665

    Article  CAS  PubMed  Google Scholar 

  • Kang CS, Ban M, Choi EJ et al (2013) Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis. PLoS One 8(10):e76520. https://doi.org/10.1371/journal.pone.0076520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaparakis-Liaskos M (2015) The intracellular location, mechanisms and outcomes of NOD1 signalling. Cytokine 74:207–212

    Article  CAS  PubMed  Google Scholar 

  • Kaparakis-Liaskos M, Ferrero RL (2015) Immune modulation by bacterial outer membrane vesicles. Nat Rev Immunol 15(6):375–387

    Article  CAS  PubMed  Google Scholar 

  • Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nat Immunol 11(5):373–384

    Article  CAS  PubMed  Google Scholar 

  • Kesty NC, Mason KM, Reedy M et al (2004) Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J 23:4538–4549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JH, Jeun EJ, Hong CP et al (2015) Extracellular vesicle-derived protein from Bifidobacterium longum alleviates food allergy through mast cell suppression. J Allergy Clin Immunol 137(2):507–516.e8

    Article  PubMed  CAS  Google Scholar 

  • Koeppen K, Hampton TH, Jarek M et al (2016) Novel mechanism of host-pathogen interaction through sRNA in bacterial outer membrane vesicles. PLoS Pathog 12(6):e1005672

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee E-Y, Bang JY, Park GW et al (2007) Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics 7:3143–3153

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Park JY, Lee EH et al (2017) Rapid assessment of microbiota changes in individuals with autism spectrum disorder using bacteria-derived membrane vesicles in urine. Exp Neurobiol 26(5):3017–3317

    Article  Google Scholar 

  • Li M, Lee K, Hsu M et al (2017) Lactobacillus-derived extracellular vesicles enhance host immune responses against vancomycin-resistant enterococci. BMC Microbiol 17(1):66. https://doi.org/10.1186/s12866-017-0977-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Yang G, Geng XR et al (2013) Microbial products induce claudin-2 to compromise gut epithelial barrier function. PloS ONE 8:e68547. https://doi.org/10.1371/journal.pone.0068547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Defourny KAY, Smid EJ et al (2018) Gram-positive bacterial extracellular vesicles and their impact on health and disease. Front Microbiol 9:1502. https://doi.org/10.3389/fmicb.2018.01502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Llewellyn A, Foey A (2017) Probiotic modulation of innate cell pathogen sensing and signaling events. Nutrients 9(10):E1156

    Article  PubMed  CAS  Google Scholar 

  • López P, Gueimonde M, Margolles A et al (2010) Distinct Bifidobacterium strains drive different immune responses in vitro. Int J Food Microbiol 138(1–2):157–165

    Article  PubMed  CAS  Google Scholar 

  • López P, González-Rodríguez I, Sánchez B et al (2012) Treg-inducing membrane vesicles from Bifidobacterium bifidum LMG13195 as potential adjuvants in immunotherapy. Vaccine 30(5):825–829

    Article  PubMed  CAS  Google Scholar 

  • Losurdo G, Iannone A, Contaldo A et al (2015) Escherichia coli Nissle 1917 in ulcerative colitis treatment: systematic review and meta-analysis. J Gastrointestin Liver Dis 24(4):499–505

    Article  PubMed  Google Scholar 

  • Lu Z, Ding L, Lu Q et al (2013) Claudins in intestines: distribution and functional significance in health and diseases. Tissue Barriers 1(3):e24978

    Article  PubMed  PubMed Central  Google Scholar 

  • Luettig J, Rosenthal R, Barmeyer DC et al (2015) Claudin-2 as a mediator of leaky gut barrier during intestinal inflammation. Tissue Barriers 3(1–2):e977176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maguire M, Maguire G (2019) Gut dysbiosis, leaky gut, and intestinal epithelial proliferation in neurological disorders: towards the development of a new therapeutic using amino acids, prebiotics, probiotics, and postbiotics. Rev Neurosci 30(2):179–201

    Article  PubMed  Google Scholar 

  • Marin IA, Goertz JE, Ren T et al (2017) Microbiota alteration is associated with the development of stress-induced despair behavior. Sci Rep 7:43859

    Article  PubMed  PubMed Central  Google Scholar 

  • Masotti A (2012) Interplays between gut microbiota and gene expression regulation by miRNAs. Front Cell Infect Microbiol 2:137

    Article  PubMed  PubMed Central  Google Scholar 

  • Mazmanian SK, Round JL, Kasper DL (2008) A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453(7195):620–625

    Article  CAS  PubMed  Google Scholar 

  • Molina-Tijeras JA, Gálvez J, Rodríguez-Cabezas ME (2019) The immunomodulatory properties of extracellular vesicles derived from probiotics: a novel approach for the management of gastrointestinal diseases. Nutrients 11(5):E1038

    Article  PubMed  CAS  Google Scholar 

  • Nighot PK, Al-Sadi R, Rawat M et al (2015) Matrix metalloproteinase 9-induced increase in intestinal epithelial tight junction permeability contributes to the severity of experimental DSS colitis. Am J Physiol Gastrointest Liver Physiol 309(12):G988–G997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nikkari S, McLaughlin IJ, Bi W et al (2001) Does blood of healthy subjects contain bacterial ribosomal DNA? J Clin Microbiol 39:1956–1959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nikoopour E, Bellemore SM, Singh B (2015) IL-22, cell regeneration and autoimmunity. Cytokine 74:35–42

    Article  CAS  PubMed  Google Scholar 

  • Ochman H, Selander RK (1984) Standard reference strains of Escherichia coli from natural populations. J Bacteriol 157:690–693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Donoghue EJ, Krachler AM (2016) Mechanisms of outer membrane vesicle entry into host cells. Cell Microbiol 18(11):1508–1517

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • O’Donoghue EJ, Sirisaengtaksin N, Browning DF et al (2017) Lipopolysaccharide structure impacts the entry kinetics of bacterial outer membrane vesicles into host cells. PLoS Pathog 13(11):e1006760. https://doi.org/10.1371/journal.ppat.1006760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olier M, Marcq I, Salvador-Cartier C et al (2012) Genotoxicity of Escherichia coli Nissle 1917 strain cannot be dissociated from its probiòtic activity. Gut Microbes 3:501–509

    Article  PubMed  PubMed Central  Google Scholar 

  • Olofsson A, Nygard Skalman L, Obi I et al (2014) Uptake of Helicobacter pylori vesicles is facilitated by clathrin-dependent and clatrin-independent endocytic pathways. mBio 5(3):e00979-14. https://doi.org/10.1128/mBio.00979-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Païssé S, Valle C, Servant F et al (2016) Comprehensive description of blood microbiome from healthy donors assessed by 16S targeted metagenomic sequencing. Transfusion 56:1138–1147

    Article  PubMed  CAS  Google Scholar 

  • Palatka K, Serfozo Z, Veréb Z et al (2005) Changes in the expression and distribution of the inducible and endothelial nitric oxide synthase in mucosal biopsy specimens of inflammatory bowel disease. Scand J Gastroenterol 40(6):670–680

    Article  CAS  PubMed  Google Scholar 

  • Park JY, Choi J, Lee Y et al (2017) Metagenome analysis of bodily microbiota in a mouse model of Alzheimer disease using bacteria-derived membrane vesicles in blood. Exp Neurobiol 26:369–379

    Article  PubMed  PubMed Central  Google Scholar 

  • Pérez-Cruz C, Cañas MA, Giménez R et al (2016) Membrane vesicles released by a hypervesiculating Escherichia coli Nissle 1917 tolR mutant are highly heterogeneous and show reduced capacity for epithelial cell interaction and Entry. PLoS One 11(12):e0169186. https://doi.org/10.1371/journal.pone.0169186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peterson LW, Artis D (2014) Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 14(3):141–153

    Article  CAS  PubMed  Google Scholar 

  • Philpott DJ, Sorbara MT, Robertson SJ et al (2014) NOD proteins: regulators of inflammation in health and disease. Nat Rev Immunol 14(1):9–23

    Article  CAS  PubMed  Google Scholar 

  • Qin J, Li R, Raes J et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464(7285):59–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rakoff-Nahoum S, Coyne MJ, Comstock LE (2014) An ecological network of polysaccharide utilization among human intestinal symbionts. Curr Biol 24(1):40–49

    Article  CAS  PubMed  Google Scholar 

  • Round JL, Lee SM, Li J et al (2011) The toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332(6032):974–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Runtsch MC, Round JL, O’Connell RM (2014) MicroRNAs and the regulation of intestinal homeostasis. Front Genet 5:347

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanjabi S, Zenewicz LA, Kamanaka M et al (2009) Anti-inflammatory and pro-inflammatory roles of TGF-beta, IL-10 and IL-22 in immunity and autoimmunity. Curr Opin Pharmacol 9:447–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwechheimer C, Kuehn MJ (2015) Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat Rev Microbiol 13(10):605–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Severi E, Hood DW, Thomas GH (2007) Sialic acid utilization by bacterial pathogens. Microbiology 153:2817–2822

    Article  CAS  PubMed  Google Scholar 

  • Shanahan F (2011) The gut microbiota in 2011: translating the microbiota to medicine. Nat Rev Gastroenterol Hepatol 9(2):72–74

    Article  PubMed  Google Scholar 

  • Shen Y, Giordano Torchia ML, Lawson GW et al (2012) Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe 12(4):509–520. https://doi.org/10.1016/j.chom.2012.08.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stentz R, Osborne S, Horn N et al (2014) A bacterial homolog of a eukaryotic inositol phosphate signaling enzyme mediates cross-kingdom dialog in the mammalian gut. Cell Rep 6(4):646–656. https://doi.org/10.1016/j.celrep.2014.01.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stentz R, Horn N, Cross K et al (2015) Cephalosporinases associated with outer membrane vesicles released by Bacteroides spp. protect gut pathogens and commensals against β-lactam antibiotics. J Antimicrob Chemother 70(3):701–709. https://doi.org/10.1093/jac/dku466

    Article  CAS  PubMed  Google Scholar 

  • Stentz R, Carvalho AL, Jones EJ et al (2018) Fantastic voyage: the journey of intestinal microbiota-derived microvesicles through the body. Biochem Soc Trans 46(5):1021–1027. https://doi.org/10.1042/BST20180114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swaan PW, Bensman T, Bahadduri PM et al (2008) Bacterial peptide recognition and immune activation facilitated by human peptide transporter PEPT2. Am J Respir Cell Mol Biol 39(5):536–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki T (2013) Regulation of intestinal epithelial permeability by tight junctions. Cell Mol Life Sci 70(4):631–659

    Article  CAS  PubMed  Google Scholar 

  • Thaiss CA, Levy M, Suez J et al (2014) The interplay between the innate immune system and the microbiota. Curr Opin Immunol 26:41–48

    Article  CAS  PubMed  Google Scholar 

  • Thursby E, Juge N (2017) Introduction to the human gut microbiota. Biochem J 474(11):1823–1836

    Article  CAS  PubMed  Google Scholar 

  • Toloza L, Gimenez R, Fabrega MJ et al (2015) The secreted autotransporter toxin (Sat) does not act as a virulence factor in the probiotic Escherichia coli strain Nissle 1917. BMC Microbiol 15:250

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Turner JR (2009) Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9(11):799–809

    Article  CAS  PubMed  Google Scholar 

  • Turner L, Bitto NJ, Steer DL et al (2018) Helicobacter pylori outer membrane vesicle size determines their mechanisms of host cell entry and protein content. Front Immunol 9:1466. https://doi.org/10.3389/fimmu.2018.01466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ukena SN, Singh A, Dringenberg U et al (2007) Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity. PLoS One 2:e1308. https://doi.org/10.1371/journal.pone.0001308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaishnava S, Yamamoto M, Severson KM et al (2011) The antibacterial lectin RegIII-gamma promotes the spatial segregation of microbiota and host in the intestine. Science 334(6053):255–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Den Elsen LW, Poyntz HC, Weyrich LS et al (2017) Embrancing the gut microbiota: the new frontier for inflammatory and infectious diseases. Clin Transl Immunol 10:18–26

    Google Scholar 

  • Vejborg RM, Friis C, Hancock V et al (2010) A virulent parent with probiotic progeny: comparative genomics of Escherichia coli strains CFT073, Nissle 1917 and ABU 83972. Mol Gen Genomics 283(5):469–484

    Article  CAS  Google Scholar 

  • Vercauteren D, Vandenbroucke RE, Jones AT et al (2010) The use of inhibitors to study endocytic pathways of gene carriers: optimization and pitfalls. Mol Ther 18:561–569

    Article  CAS  PubMed  Google Scholar 

  • Vétizou M, Pitt JM, Daillère R et al (2015) Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350:1079–1084

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vimr ER, Kalivoda KA, Deszo EL et al (2004) Diversity of microbial sialic acid metabolism. Microbiol Mol Biol Rev 68(1):132–153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vindigni SM, Zisman TL, Suskind DL et al (2016) The intestinal microbiome, barrier function, and immune system in inflammatory bowel disease: a tripartite pathophysiological circuit with implications for new therapeutic directions. Ther Adv Gastroenterol 9(4):606–625

    Article  CAS  Google Scholar 

  • Wells JM, Rossi O, Meijerink M et al (2011) Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci U S A 108(Suppl 1):4607–4614

    Article  CAS  PubMed  Google Scholar 

  • Zakharzhevskaya NB, Vanyushkina AA, Altukhov IA et al (2017) Outer membrane vesicles secreted by pathogenic and nonpathogenic Bacteroides fragilis represent different metabolic activities. Sci Rep 7(1):5008

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhan X, Stamova B, Jin LW et al (2016) Gram-negative bacterial molecules associate with Alzheimer disease pathology. Neurology 87:2324–2332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YG, Wu S, Xia Y et al (2013) Salmonella infection upregulates the leaky protein claudin-2 in intestinal epithelial cells. PLoS One 8:e58606. https://doi.org/10.1371/journal.pone.0058606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YZ, Li YY (2014) Inflammatory bowel disease: pathogenesis. World J Gastroenterol 20:91–99. https://doi.org/10.3748/wjg.v20.i1.91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zyrek AA, Cichon C, Helms S et al (2007) Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKCzeta redistribution resulting in tight junction and epithelial barrier repair. Cell Microbiol 9:804–816

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laura Baldomà .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Badia, J., Baldomà, L. (2020). Membrane Vesicles from the Gut Microbiota and Their Interactions with the Host. In: Kaparakis-Liaskos, M., Kufer, T. (eds) Bacterial Membrane Vesicles. Springer, Cham. https://doi.org/10.1007/978-3-030-36331-4_9

Download citation

Publish with us

Policies and ethics