Advances on function and mechanism of bacterial outer membrane vesicles in acute respiratory distress syndrome

doi:10.3877/cma.j.issn.2096-1537.2023.04.009

Abstract

Abstract:

Acute respiratory distress syndrome (ARDS), a fatal disease characterized by uncontrolled immune response and refractory hypoxemia, is most commonly induced by infection. Outer membrane vesicles (OMVs) are nanoparticles produced by gram-negative bacteria via the extrusion of the outer membrane and can deliver a range of bacterial molecules to host cells. Recently it was found that OMVs play vital roles in bacterial colonization, delivery of virulence factors, and disease pathogenesis. This article reviews the formation and biological functions of OMVs, and the inflammatory and pathological mechanisms of OMVs in ARDS.

Key words: Acute respiratory distress syndrome, Gram negative bacteria, Outer membrane vesicles, Immune response

Jing Chen, Wei Huang, Haibo Qiu. Advances on function and mechanism of bacterial outer membrane vesicles in acute respiratory distress syndrome[J]. Chinese Journal of Critical Care & Intensive Care Medicine(Electronic Edition), 2023, 09(04): 391-395.

/ / Recommend

Add to citation manager EndNote|Ris|BibTeX

URL: https://icu.cma-cmc.com.cn/EN/10.3877/cma.j.issn.2096-1537.2023.04.009

https://icu.cma-cmc.com.cn/EN/Y2023/V09/I04/391

References 46

1	Bellani G, Laffey JG, Pham T, et al. Epidemiology, patterns of care, and mortality for patients with acute respiratory distress syndrome in intensive care units in 50 countries [J]. JAMA, 2016, 315(8): 788-800.
2	Hendrix A, De Wever O. Systemically circulating bacterial extracellular vesicles: origin, fate, and function [J]. Trends Microbiol, 2022, 30(3): 213-216.
3	DeVoe IW, Gilchrist JE. Pili on meningococci from primary cultures of nasopharyngeal carriers and cerebrospinal fluid of patients with acute disease [J]. J Exp Med, 1975, 141(2): 297-305.
4	Stephens DS, Edwards KM, Morris F, et al. Pili and outer membrane appendages on Neisseria meningitidis in the cerebrospinal fluid of an infant [J]. J Infect Dis, 1982, 146(4): 568.
5	Ren D, Nelson KL, Uchakin PN, et al. Characterization of extended co-culture of non-typeable Haemophilus influenzae with primary human respiratory tissues [J]. Exp Biol Med (Maywood), 2012, 237(5): 540-547.
6	Schwechheimer C, Kuehn MJ. Outer-membrane vesicles from gram-negative bacteria: biogenesis and functions [J]. Nat Rev Microbiol, 2015, 13(10): 605-619.
7	Bernadac A, Gavioli M, Lazzaroni JC, et al. Escherichia coli tol-pal mutants form outer membrane vesicles [J]. J Bacteriol, 1998, 180(18): 4872-4878.
8	Park JS, Lee WC, Yeo KJ, et al. Mechanism of anchoring of OmpA protein to the cell wall peptidoglycan of the gram-negative bacterial outer membrane [J]. FASEB J, 2012, 26(1): 219-228.
9	Moon DC, Choi CH, Lee JH, et al. Acinetobacter baumannii outer membrane protein a modulates the biogenesis of outer membrane vesicles [J]. J Microbiol, 2012, 50(1): 155-160.
10	Bauwens A, Kunsmann L, Karch H, et al. Antibiotic-mediated modulations of outer membrane vesicles in enterohemorrhagic Escherichia coli O104: H4 and O157: H7 [J]. Antimicrob Agents Chemother, 2017, 61(9): e00937-17.
11	Cahill BK, Seeley KW, Gutel D, et al. Klebsiella pneumoniae O antigen loss alters the outer membrane protein composition and the selective packaging of proteins into secreted outer membrane vesicles [J]. Microbiol Res, 2015, 180: 1-10.
12	Deo P, Chow SH, Hay ID, et al. Outer membrane vesicles from Neisseria gonorrhoeae target PorB to mitochondria and induce apoptosis [J]. PLoS Pathog, 2018, 14(3): e1006945.
13	Schwechheimer C, Kuehn MJ. Outer-membrane vesicles from gram-negative bacteria: biogenesis and functions [J]. Nat Rev Microbiol, 2015, 13(10): 605-619.
14	Kaparakis M, Turnbull L, Carneiro L, et al. Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells [J]. Cell Microbiol, 2010, 12(3): 372-385.
15	Dhital S, Deo P, Stuart I, et al. Bacterial outer membrane vesicles and host cell death signaling [J]. Trends Microbiol, 2021, 29(12): 1106-1116.
16	Turner L, Bitto NJ, Steer DL, et al. Helicobacter pylori outer membrane vesicle size determines their mechanisms of host cell entry and protein content [J]. Front Immunol, 2018, 9: 1466.
17	Zingl FG, Thapa HB, Scharf M, et al. Outer membrane vesicles of vibrio cholerae protect and deliver active cholera toxin to host cells via porin-dependent uptake [J]. mBio, 2021, 12(3): e0053421.
18	Tulkens J, Vergauwen G, Van Deun J, et al. Increased levels of systemic LPS-positive bacterial extracellular vesicles in patients with intestinal barrier dysfunction [J]. Gut, 2020, 69(1): 191-193.
19	Jang SC, Kim SR, Yoon YJ, et al. In vivo kinetic biodistribution of nano-sized outer membrane vesicles derived from bacteria [J]. Small, 2015, 11(4): 456-461.
20	Jones EJ, Booth C, Fonseca S, et al. The uptake, trafficking, and biodistribution of bacteroides thetaiotaomicron generated outer membrane vesicles [J]. Front Microbiol, 2020, 11: 57.
21	He Y, Shiotsu N, Uchida-Fukuhara Y, et al. Outer membrane vesicles derived from Porphyromonas gingivalis induced cell death with disruption of tight junctions in human lung epithelial cells [J]. Arch Oral Biol, 2020, 118: 104841.
22	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(9-10): 2400-2408.
23	Galka F, Wai SN, Kusch H, et al. Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles [J]. Infect Immun 2008, 76(5): 1825-1836.
24	Bielaszewska M, Marejkova M, Bauwens A, et al. Enterohemorrhagic Escherichia coli O157 outer membrane vesicles induce interleukin 8 production in human intestinal epithelial cells by signaling via Toll-like receptors TLR4 and TLR5 and activation of the nuclear factor NF-κB [J]. Int J Med Microbiol, 2018, 308(7): 882-889.
25	Soult MC, Lonergan NE, Shah B, et al. Outer membrane vesicles from pathogenic bacteria initiate an inflammatory response in human endothelial cells [J]. J Surg Res, 2013, 184(1): 458-466.
26	Lee J, Yoon YJ, Kim JH, et al. Outer membrane vesicles derived from Escherichia coli regulate neutrophil migration by induction of endothelial IL-8 [J]. Front Microbiol, 2018, 9: 2268.
27	Soult MC, Dobrydneva Y, Wahab KH, et al. Outer membrane vesicles alter inflammation and coagulation mediators [J]. J Surg Res, 2014, 192(1): 134-142.
28	Park KS, Lee J, Jang SC, et al. Pulmonary inflammation induced by bacteria-free outer membrane vesicles from Pseudomonas aeruginosa [J]. Am J Respir Cell Mol Biol, 2013, 49(4): 637-645.
29	Lapinet JA, Scapini P, Calzetti F, et al. Gene expression and production of tumor necrosis factor alpha, interleukin-1 beta (IL-1 beta), IL-8, macrophage inflammatory protein 1 alpha (MIP-1 alpha), MIP-1 beta, and gamma interferon-inducible protein 10 by human neutrophils stimulated with group B meningococcal outer membrane vesicles [J]. Infect Immun, 2000, 68(12): 6917-6923.
30	Davis JM, Carvalho HM, Rasmussen SB, et al. Cytotoxic necrotizing factor type 1 delivered by outer membrane vesicles of uropathogenic Escherichia coli attenuates polymorphonuclear leukocyte antimicrobial activity and chemotaxis [J]. Infect Immun, 2006, 74(8): 4401-4408.
31	Lappann M, Danhof S, Guenther F, et al. In vitro resistance mechanisms of Neisseria meningitidis against neutrophil extracellular traps [J]. Mol Microbiol, 2013, 89(3): 433-449.
32	Jung AL, Stoiber C, Herkt CE, et al. Legionella pneumophila-derived outer membrane vesicles promote bacterial replication in macrophages [J]. PLoS Pathog, 2016, 12(4): e1005592.
33	Winter J, Letley D, Rhead J, et al. Helicobacter pylori membrane vesicles stimulate innate pro-and anti-inflammatory responses and induce apoptosis in Jurkat T cells [J]. Infect Immun, 2014, 82(4): 1372-1381.
34	Tavano R, Franzoso S, Cecchini P, et al. The membrane expression of Neisseria meningitidis adhesin A (NadA) increases the proimmune effects of MenB OMVs on human macrophages, compared with NadA-OMVs, without further stimulating their proinflammatory activity on circulating monocytes [J]. J Leukoc Biol, 2009, 86(1): 143-153.
35	Mirlashari MR, Hoiby EA, Holst J, et al. Outer membrane vesicles from Neisseria meningitidis: effects on tissue factor and plasminogen activator inhibitor-2 production in human monocytes [J]. Thromb Res, 2001, 102(4): 375-380.
36	Vanaja SK, Russo AJ, Behl B, et al. Bacterial outer membrane vesicles mediate cytosolic localization of LPS and caspase-11 activation [J]. Cell, 2016, 165(5): 1106-1119.
37	Bitto NJ, Baker PJ, Dowling JK, et al. Membrane vesicles from Pseudomonas aeruginosa activate the noncanonical inflammasome through caspase-5 in human monocytes [J]. Immunol Cell Biol, 2018, 96(10): 1120-1130.
38	Durand V, MacKenzie J, de Leon J, et al. Role of lipopolysaccharide in the induction of type Ⅰ interferon-dependent cross-priming and IL-10 production in mice by meningococcal outer membrane vesicles. Vaccine, 2009, 27(13): 1912–1922.
39	Alaniz RC, Deatherage BL, Lara JC, et al. Membrane vesicles are immunogenic facsimiles of Salmonella typhimurium that potently activate dendritic cells, prime B and T cell responses, and stimulate protective immunity in vivo [J]. J Immunol, 2007, 179(11): 7692-7701.
40	Shen Y, Giardino Torchia ML, Lawson GW, et al. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection [J]. Cell Host Microbe, 2012, 12(4): 509-520.
41	Perl M, Lomas-Neira J, Venet F, et al. Pathogenesis of indirect (secondary) acute lung injury [J]. Expert Rev Respir Med, 2011, 5(1): 115-126.
42	Yu ZX, Ji MS, Yan J, et al. The ratio of Th17/Treg cells as a risk indicator in early acute respiratory distress syndrome [J]. Crit Care, 2015, 19: 82.
43	Yang D, Chen X, Wang J, et al. Dysregulated lung commensal bacteria drive interleukin-17B production to promote pulmonary fibrosis through their outer membrane vesicles [J]. Immunity, 2019, 50(3): 692-706.
44	Namork E, Brandtzaeg P. Fatal meningococcal septicaemia with "blebbing" meningococcus [J]. Lancet, 2002, 360(9347): 1741.
45	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.
46	Park JY, Choi J, Lee Y, et al. Metagenome analysis of bodily microbiota in a mouse model of Alzheimer disease using bacteria-derived membrane vesicles in blood [J]. Exp Neurobiol, 2017, 26(6): 369-379.

[1]	Meicen Zhou, Hua Wang, Dezhi Mu. Vaccination timeliness in preterm infants: a review of literature [J]. Chinese Journal of Obstetrics & Gynecology and Pediatrics(Electronic Edition), 2023, 19(03): 261-266.
[2]	Caiying Wang, Ming He, Shuxin He, Yuhuan Liu, Hongling Yang, Lin Pang. Influencing factors of non- or low-response to hepatitis B vaccine immunity in infants of mothers with hepatitis B virus surface antigen positive [J]. Chinese Journal of Experimental and Clinical Infectious Diseases(Electronic Edition), 2022, 16(06): 377-384.
[3]	Lu Shi, Yuming Huang, Cheng Kou, Kaiyu Qin, Yali Wu, Xiaoyang Ma, Dongmei Xu. Differences of clinical phenotypes and laboratory indexes for couples co-infected with treponema pallidum [J]. Chinese Journal of Experimental and Clinical Infectious Diseases(Electronic Edition), 2022, 16(05): 328-336.
[4]	Lung Transplantation Study Group, Branch of Organ Transplantation of Chinese Medical Association;, National Lung Transplantation Quality Control Center. Selection of lung transplant candidates with COVID-19: Advises from China lung transplant expert group [J]. Chinese Journal of Transplantation(Electronic Edition), 2023, 17(01): 13-16.
[5]	Ting Luo, Shi Zhang. Prognostic analysis of 5 biomarkers for acute respiratory distress syndrome [J]. Chinese Journal of Lung Diseases(Electronic Edition), 2023, 16(04): 471-475.
[6]	Zongjun Hu, Xi Yue, Xia Huang. Effect of bronchopulmonary segments recruitment on the survival of patients with severe acute respiratory distress syndrome [J]. Chinese Journal of Lung Diseases(Electronic Edition), 2022, 15(06): 796-800.
[7]	Jianpeng Wang, Yongshi Liao, Wencong Ding, Chong Li, Rui Chen. Research progress of lncRNA in traumatic brain injury [J]. Chinese Journal of Neurotraumatic Surgery(Electronic Edition), 2022, 08(06): 365-370.
[8]	Rui Chen, Hongna Yang, Wei Fang, Xinxin Li, Tiantian Li, Xiaoyi Yu, Yanxue Wang, Wenyu Li. Correlation between the cytokine levels in serum and BALF and intrapulmonary and extrapulmonary ARDS [J]. Chinese Journal of Critical Care & Intensive Care Medicine(Electronic Edition), 2023, 09(03): 251-258.
[9]	Meiqing Wu, Jin Lin, Meili Duan, Xiaoyan Xue. Effect of high density lipoprotein level on the occurrence of sepsis-related acute respiratory distress syndrome [J]. Chinese Journal of Critical Care & Intensive Care Medicine(Electronic Edition), 2023, 09(02): 191-197.
[10]	Dongyu Chen, Chun Pan, Yi Yang. Techniques to monitor respiratory effort in acute respiratory distress syndrome [J]. Chinese Journal of Critical Care & Intensive Care Medicine(Electronic Edition), 2023, 09(01): 84-88.
[11]	Jieqiong Wang, Huixia Wang, Huiying Zhao, Youzhong An. Regulation of angiotensin converting enzyme 2 on inflammatory injury of human pulmonary microvascular endothelial cells [J]. Chinese Journal of Critical Care & Intensive Care Medicine(Electronic Edition), 2023, 09(01): 78-83.
[12]	Jingen Xia, Shiyu Hu. Application scenario of extracorporeal carbon dioxide removal technology in Intensive Care Unit [J]. Chinese Journal of Critical Care & Intensive Care Medicine(Electronic Edition), 2023, 09(01): 40-45.
[13]	Chengfen Yin, Lei Xu. Talk about the timing of prone position ventilation again [J]. Chinese Journal of Critical Care & Intensive Care Medicine(Electronic Edition), 2023, 09(01): 9-13.
[14]	Yumei Wang, Yan Wang, Yimin Zhou, Mingyue Miao, Yanlin Yang, Linlin Zhang, Ming Xu, Jianxin Zhou. Application of regional recruitment-to-inflation ratio monitored by electrical impedance tomography in the models of acute respiratory distress syndrome [J]. Chinese Journal of Critical Care & Intensive Care Medicine(Electronic Edition), 2022, 08(04): 360-366.
[15]	Chengfen Yin, Lei Xu. Settings of mechanical ventilation during V-V ECMO support in ARDS patients [J]. Chinese Journal of Critical Care & Intensive Care Medicine(Electronic Edition), 2022, 08(04): 378-383.

Please choose a citation manager

Content to export