Insights into the regulatory role of bacterial sncRNA and its extracellular delivery via OMVs.

Publisher: Springer International Country of Publication: Germany NLM ID: 8406612 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1432-0614 (Electronic) Linking ISSN: 01757598 NLM ISO Abbreviation: Appl Microbiol Biotechnol Subsets: MEDLINE

Original Publication: Berlin ; New York : Springer International, c1984-

RNA, Small Untranslated*/genetics ; Extracellular Vesicles*/metabolism; Bacterial Outer Membrane Proteins/genetics ; Bacteria/metabolism ; Host-Pathogen Interactions/physiology ; Host Microbial Interactions

Small noncoding RNAs (sncRNAs) play important regulatory roles in bacterial physiological processes and host-pathogen interactions. Meanwhile, bacterial outer membrane vesicles (OMVs), as naturally secreted outer membrane structures, play a vital role in the interaction between bacteria and their living environment, including the host environment. However, most current studies focus on the biological functions of sncRNAs in bacteria or hosts, while neglecting the roles and regulatory mechanisms of the OMVs that encapsulate these sncRNAs. Therefore, this review aims to summarize the intracellular regulatory roles of bacterial sncRNAs in promoting pathogen survival by regulating virulence, modulating bacterial drug resistance, and regulating iron metabolism, and their extracellular regulatory function for influencing host immunity through host-pathogen interactions. Additionally, we introduce the key role played by OMVs, which serve as important cargoes in bacterial sncRNA-host interactions. We propose emerging pathways of sncRNA action to further discuss the mode of host-pathogen interactions, highlighting that the inhibition of sncRNA delivery by OMVs may prevent the occurrence of infection to some extent. Hence, this review lays the foundation for future prophylactic treatments against bacterial infections and strategies for addressing bacterial drug resistance. KEY POINTS: •sncRNAs have intracellular and extracellular regulatory functions in bacterial physiological processes and host-pathogen interactions. •OMVs are potential mediators between bacterial sncRNAs and host cells. •OMVs encapsulating sncRNAs have more potential biological functions.
(© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

Álvarez-Fraga L, Rumbo-Feal S, Pérez A, Gómez MJ, Gayoso C, Vallejo JA, Ohneck EJ, Valle J, Actis LA, Beceiro A, Bou G, Poza M (2017) Global assessment of small RNAs reveals a non-coding transcript involved in biofilm formation and attachment in Acinetobacter baumannii ATCC 17978. PLoS One 12:e0182084. (PMID: 28763494553864310.1371/journal.pone.0182084)
Bardill JP, Zhao X, Hammer BK (2011) The Vibrio cholerae quorum sensing response is mediated by Hfq-dependent sRNA/mRNA base pairing interactions. Mol Microbiol 80:1381–1394. (PMID: 2145344610.1111/j.1365-2958.2011.07655.x)
Barh D, Tiwari S, Kumavath RN, Ghosh P, Azevedo V (2018) Linking common non-coding RNAs of human lung cancer and M. tuberculosis. Bioinformation 14:337–345. (PMID: 30237679613756310.6026/97320630014337)
Bhardwaj S, Mehra P, Dhanjal DS, Sharma P, Sharma V, Singh R, Nepovimova E, Chopra C, Kuča K (2022) Antibiotics and antibiotic resistance- flipsides of the same coin. Curr Pharm Des 28:2312–2329. (PMID: 3567683910.2174/1381612828666220608120238)
Bitto NJ, Chapman R, Pidot S, Costin A, Lo C, Choi J, D'Cruze T, Reynolds EC, Dashper SG, Turnbull L, Whitchurch CB, Stinear TP, Stacey KJ, Ferrero RL (2017) Bacterial membrane vesicles transport their DNA cargo into host cells. Sci Rep 7:7072. (PMID: 28765539553919310.1038/s41598-017-07288-4)
Bitto NJ, Cheng L, Johnston EL, Pathirana R, Phan TK, Poon IKH, O'Brien-Simpson NM, Hill AF, Stinear TP, Kaparakis-Liaskos M (2021) Staphylococcus aureus membrane vesicles contain immunostimulatory DNA, RNA and peptidoglycan that activate innate immune receptors and induce autophagy. J Extracell Vesicles 10:e12080. (PMID: 33815695801588810.1002/jev2.12080)
Borgmann J, Schäkermann S, Bandow JE, Narberhaus F (2018) A small regulatory RNA controls cell wall biosynthesis and antibiotic resistance. mBio 9(6):e02100–18.
Bos J, Cisneros LH, Mazel D (2021) Real-time tracking of bacterial membrane vesicles reveals enhanced membrane traffic upon antibiotic exposure. Sci Adv 7(4):eabd1033.
Chareyre S, Mandin P (2018) Bacterial iron homeostasis regulation by sRNAs. Microbiol Spectr 6(2).
Chen F, Cui G, Wang S, Nair MKM, He L, Qi X, Han X, Zhang H, Zhang JR, Su J (2017) Outer membrane vesicle-associated lipase FtlA enhances cellular invasion and virulence in Francisella tularensis LVS. Emerg Microbes Infect 6:e66. (PMID: 28745311556716910.1038/emi.2017.53)
Chen G, Sun Q, Cai Q, Zhou H (2022a) Outer membrane vesicles from Fusobacterium nucleatum switch M0-like macrophages toward the M1 phenotype to destroy periodontal tissues in mice. Front Microbiol 13:815638. (PMID: 35391731898199110.3389/fmicb.2022.815638)
Chen Y, Jie K, Li B, Yu H, Ruan H, Wu J, Huang X, Liu Q (2020) Immunization with outer membrane vesicles derived from major outer membrane protein-deficient Salmonella typhimurium mutants for cross protection against Salmonella enteritidis and avian pathogenic Escherichia coli O78 infection in chickens. Front Microbiol 11:588952. (PMID: 33329465772050810.3389/fmicb.2020.588952)
Chen Z, Jiang W, Zhang M, Yu B, Li W, Liu J, Ai F (2022b) Mycobacterium tuberculosis sRNA MTS2823 regulates the growth of the multidrug-resistant strain in macrophages. FEMS Microbiol Lett 369(1):fnac106.
Choi HI, Kim M, Jeon J, Han JK, Kim KS (2017) Overexpression of MicA induces production of OmpC-enriched outer membrane vesicles that protect against Salmonella challenge. Biochem Biophys Res Commun 490:991–996. (PMID: 2866687310.1016/j.bbrc.2017.06.152)
Coleman SR, Bains M, Smith ML, Spicer V, Lao Y, Taylor PK, Mookherjee N, Hancock REW (2021) The small RNAs PA2952.1 and PrrH as regulators of virulence, motility, and iron metabolism in Pseudomonas aeruginosa. Appl Environ Microbiol 87(3):e02182–20.
Coronel-Tellez RH, Pospiech M, Barrault M, Liu W, Bordeau V, Vasnier C, Felden B, Sargueil B, Bouloc P (2022) sRNA-controlled iron sparing response in Staphylococci. Nucleic Acids Res 50:8529–8546. (PMID: 35904807941091710.1093/nar/gkac648)
Desgranges E, Barrientos L, Herrgott L, Marzi S, Toledo-Arana A, Moreau K, Vandenesch F, Romby P, Caldelari I (2022) The 3'UTR-derived sRNA RsaG coordinates redox homeostasis and metabolism adaptation in response to glucose-6-phosphate uptake in Staphylococcus aureus. Mol Microbiol 117:193–214. (PMID: 3478340010.1111/mmi.14845)
Desnoyers G, Morissette A, Prévost K, Massé E (2009) Small RNA-induced differential degradation of the polycistronic mRNA iscRSUA. EMBO J 28:1551–1561. (PMID: 19407815269315110.1038/emboj.2009.116)
Deusenbery C, Wang Y, Shukla A (2021) Recent innovations in bacterial infection detection and treatment. ACS Infect Dis 7:695–720. (PMID: 3373374710.1021/acsinfecdis.0c00890)
Eisenbart SK, Alzheimer M, Pernitzsch SR, Dietrich S, Stahl S, Sharma CM (2020) A Repeat-associated small RNA controls the major virulence factors of Helicobacter pylori. Mol Cell 80:210–226.e217. (PMID: 3300242410.1016/j.molcel.2020.09.009)
Ellis TN, Kuehn MJ (2010) Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev 74:81–94. (PMID: 20197500283235010.1128/MMBR.00031-09)
Eyraud A, Tattevin P, Chabelskaya S, Felden B (2014) A small RNA controls a protein regulator involved in antibiotic resistance in Staphylococcus aureus. Nucleic Acids Res 42:4892–4905. (PMID: 24557948400569010.1093/nar/gku149)
Felden B, Augagneur Y (2021) Diversity and versatility in small RNA-mediated regulation in bacterial pathogens. Front Microbiol 12:719977. (PMID: 34447363838307110.3389/fmicb.2021.719977)
Frantz R, Teubner L, Schultze T, La Pietra L, Müller C, Gwozdzinski K, Pillich H, Hain T, Weber-Gerlach M, Panagiotidis GD, Mostafa A, Weber F, Rohde M, Pleschka S, Chakraborty T, Abu Mraheil M (2019) The secRNome of Listeria monocytogenes harbors small noncoding RNAs that are potent inducers of beta interferon. mBio 10(5):e01223–19.
Gutierrez A, Laureti L, Crussard S, Abida H, Rodríguez-Rojas A, Blázquez J, Baharoglu Z, Mazel D, Darfeuille F, Vogel J, Matic I (2013) β-Lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity. Nat Commun 4:1610. (PMID: 2351147410.1038/ncomms2607)
Ha JY, Choi SY, Lee JH, Hong SH, Lee HJ (2020) Delivery of periodontopathogenic extracellular vesicles to brain monocytes and microglial IL-6 promotion by RNA cargo. Front Mol Biosci 7:596366. (PMID: 33330627773264410.3389/fmolb.2020.596366)
Han EC, Choi SY, Lee Y, Park JW, Hong SH, Lee HJ (2019) Extracellular RNAs in periodontopathogenic outer membrane vesicles promote TNF-α production in human macrophages and cross the blood-brain barrier in mice. FASEB J 33:13412–13422. (PMID: 31545910689404610.1096/fj.201901575R)
Jeon HJ, Lee Y, Monford Paul Abishek N, Wang X, Chattoraj DK, Lim HM (2021) sRNA-mediated regulation of gal mRNA in E. coli: Involvement of transcript cleavage by RNase E together with Rho-dependent transcription termination. PLoS Genet 17:e1009878. (PMID: 34710092857778410.1371/journal.pgen.1009878)
Jousselin A, Metzinger L, Felden B (2009) On the facultative requirement of the bacterial RNA chaperone, Hfq. Trends Microbiol 17:399–405. (PMID: 1973308010.1016/j.tim.2009.06.003)
Keegan C, Krutzik S, Schenk M, Scumpia PO, Lu J, Pang YLJ, Russell BS, Lim KS, Shell S, Prestwich E, Su D, Elashoff D, Hershberg RM, Bloom BR, Belisle JT, Fortune S, Dedon PC, Pellegrini M, Modlin RL (2018) Mycobacterium tuberculosis transfer RNA induces IL-12p70 via synergistic activation of pattern recognition receptors within a cell network. J Immunol 200:3244–3258. (PMID: 2961014010.4049/jimmunol.1701733)
Khan MA, Göpel Y, Milewski S, Görke B (2016) Two small RNAs conserved in enterobacteriaceae provide intrinsic resistance to antibiotics targeting the cell wall biosynthesis enzyme glucosamine-6-phosphate synthase. Front Microbiol 7:908. (PMID: 27379045490814310.3389/fmicb.2016.00908)
Koeppen K, Hampton TH, Jarek M, Scharfe M, Gerber SA, Mielcarz DW, Demers EG, Dolben EL, Hammond JH, Hogan DA, Stanton BA (2016) A novel mechanism of host-pathogen interaction through sRNA in bacterial outer membrane vesicles. PLoS Pathog 12:e1005672. (PMID: 27295279490563410.1371/journal.ppat.1005672)
Kuehn MJ, Kesty NC (2005) Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev 19:2645–2655. (PMID: 1629164310.1101/gad.1299905)
Kuscu C, Kumar P, Kiran M, Su Z, Malik A, Dutta A (2018) tRNA fragments (tRFs) guide Ago to regulate gene expression post-transcriptionally in a Dicer-independent manner. Rna 24:1093–1105. (PMID: 29844106604949910.1261/rna.066126.118)
Landa A, Navarro L, Ochoa-Sánchez A, Jiménez L (2019) Taenia solium and Taenia crassiceps: miRNomes of the larvae and effects of miR-10-5p and let-7-5p on murine peritoneal macrophages. Biosci Rep 39(11):BSR20190152.
Law COK, Huang C, Pan Q, Lee J, Hao Q, Chan TF, Lo NWS, Ang IL, Koon A, Ip M, Chan E, Lau TCK (2019) A small RNA transforms the multidrug resistance of Pseudomonas aeruginosa to drug susceptibility. Mol Ther Nucleic Acids 16:218–228. (PMID: 30901580642955510.1016/j.omtn.2019.02.011)
Li B, Xu Y, Xu T, Guo Z, Xu Q, Li Y, Zeng L, Huang X, Liu Q (2022a) Disruption of sncRNA improves the protective efficacy of outer membrane vesicles against Helicobacter pylori infection in a mouse model. Infect Immun 90:e0026722. (PMID: 3586153210.1128/iai.00267-22)
Li C, Zhu L, Wang D, Wei Z, Hao X, Wang Z, Li T, Zhang L, Lu Z, Long M, Wang Y, Wei G, Shen X (2022b) T6SS secretes an LPS-binding effector to recruit OMVs for exploitative competition and horizontal gene transfer. Isme J 16:500–510. (PMID: 3443389810.1038/s41396-021-01093-8)
Li J, Li N, Ning C, Guo Y, Ji C, Zhu X, Zhang X, Meng Q, Shang Y, Xiao C, Xia X, Cai X, Qiao J (2021) sRNA STnc150 is involved in virulence regulation of Salmonella Typhimurium by targeting fimA mRNA. FEMS Microbiol Lett 368(18):fnab124.
Liu D, Liu S, Liu J, Miao L, Zhang S, Pan Y (2021) sRNA23392 packaged by Porphyromonas gingivalis outer membrane vesicles promotes oral squamous cell carcinomas migration and invasion by targeting desmocollin-2. Mol Oral Microbiol 36:182–191. (PMID: 3376400810.1111/omi.12334)
Liu Q, Li X, Zhang Y, Song Z, Li R, Ruan H, Huang X (2019) Orally-administered outer-membrane vesicles from Helicobacter pylori reduce H. pylori infection via Th2-biased immune responses in mice. Pathog Dis 77(5):ftz050.
Massé E, Gottesman S (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci USA 99:4620–4625. (PMID: 1191709812369710.1073/pnas.032066599)
Massé E, Vanderpool CK, Gottesman S (2005) Effect of RyhB small RNA on global iron use in Escherichia coli. J Bacteriol 187:6962–6971. (PMID: 16199566125160110.1128/JB.187.20.6962-6971.2005)
Mediati DG, Wu S, Wu W, Tree JJ (2021) Networks of resistance: small RNA control of antibiotic resistance. Trends Genet 37:35–45. (PMID: 3295194810.1016/j.tig.2020.08.016)
Meng X, He M, Chen B, Xia P, Wang J, Zhu C, Wang H, Zhu G (2023) RyhB paralogs downregulate the expressions of multiple survival-associated genes and attenuate the survival of Salmonella enteritidis in the chicken macrophage HD11. Microorganisms 11(1):214.
Milewski S (2002) Glucosamine-6-phosphate synthase--the multi-facets enzyme. Biochim Biophys Acta 1597:173–192. (PMID: 1204489810.1016/S0167-4838(02)00318-7)
Moriano-Gutierrez S, Bongrand C, Essock-Burns T, Wu L, McFall-Ngai MJ, Ruby EG (2020) The noncoding small RNA SsrA is released by Vibrio fischeri and modulates critical host responses. PLoS Biol 18:e3000934. (PMID: 33141816766574810.1371/journal.pbio.3000934)
Munhoz da Rocha IF, Amatuzzi RF, Lucena ACR, Faoro H, Alves LR (2020) Cross-kingdom extracellular vesicles EV-RNA communication as a mechanism for host-pathogen interaction. Front Cell Infect Microbiol 10:593160. (PMID: 33312966770832910.3389/fcimb.2020.593160)
Ñahui Palomino RA, Vanpouille C, Costantini PE, Margolis L (2021) Microbiota-host communications: bacterial extracellular vesicles as a common language. PLoS Pathog 17:e1009508. (PMID: 33984071811830510.1371/journal.ppat.1009508)
Nishino K, Yamasaki S, Hayashi-Nishino M, Yamaguchi A (2011) Effect of overexpression of small non-coding DsrA RNA on multidrug efflux in Escherichia coli. J Antimicrob Chemother 66:291–296. (PMID: 2108802010.1093/jac/dkq420)
Papenfort K, Förstner KU, Cong JP, Sharma CM, Bassler BL (2015) Differential RNA-seq of Vibrio cholerae identifies the VqmR small RNA as a regulator of biofilm formation. Proc Natl Acad Sci USA 112:E766–E775. (PMID: 25646441434308810.1073/pnas.1500203112)
Papenfort K, Silpe JE, Schramma KR, Cong JP, Seyedsayamdost MR, Bassler BL (2017) A Vibrio cholerae autoinducer-receptor pair that controls biofilm formation. Nat Chem Biol 13:551–557. (PMID: 28319101539128210.1038/nchembio.2336)
Parker A, Gottesman S (2016) Small RNA regulation of TolC, the outer membrane component of bacterial multidrug transporters. J Bacteriol 198:1101–1113. (PMID: 26811318480087110.1128/JB.00971-15)
Peschek N, Hoyos M, Herzog R, Förstner KU, Papenfort K (2019) A conserved RNA seed-pairing domain directs small RNA-mediated stress resistance in enterobacteria. EMBO J 38:e101650. (PMID: 31313835669421810.15252/embj.2019101650)
Prévost K, Salvail H, Desnoyers G, Jacques JF, Phaneuf E, Massé E (2007) The small RNA RyhB activates the translation of shiA mRNA encoding a permease of shikimate, a compound involved in siderophore synthesis. Mol Microbiol 64:1260–1273. (PMID: 1754291910.1111/j.1365-2958.2007.05733.x)
Raad N, Tandon D, Hapfelmeier S, Polacek N (2022) The stationary phase-specific sRNA FimR2 is a multifunctional regulator of bacterial motility, biofilm formation and virulence. Nucleic Acids Res 50:11858–11875. (PMID: 36354005972350210.1093/nar/gkac1025)
Rojano-Nisimura, A.M., Simmons, T.R., Leistra, A.N., Mihailovic, M.K., Buchser, R., Ekdahl, A.M., Joseph, I., Curtis, N.C., Contreras, L.M., (2023). CsrA shows selective regulation of sRNA-mRNA networks. bioRxiv.
Romilly C, Lays C, Tomasini A, Caldelari I, Benito Y, Hammann P, Geissmann T, Boisset S, Romby P, Vandenesch F (2014) A non-coding RNA promotes bacterial persistence and decreases virulence by regulating a regulator in Staphylococcus aureus. PLoS Pathog 10:e1003979. (PMID: 24651379396135010.1371/journal.ppat.1003979)
Salvail H, Caron MP, Bélanger J, Massé E (2013) Antagonistic functions between the RNA chaperone Hfq and an sRNA regulate sensitivity to the antibiotic colicin. EMBO J 32:2764–2778. (PMID: 24065131380143910.1038/emboj.2013.205)
Santiago-Frangos A, Woodson SA (2018) Hfq chaperone brings speed dating to bacterial sRNA. Wiley Interdiscip Rev RNA 9:e1475. (PMID: 29633565600292510.1002/wrna.1475)
Sarshar M, Scribano D, Palamara AT, Ambrosi C, Masotti A (2022) The Acinetobacter baumannii model can explain the role of small non-coding RNAs as potential mediators of host-pathogen interactions. Front Mol Biosci 9:1088783. (PMID: 36619166981063310.3389/fmolb.2022.1088783)
Sartorio MG, Pardue EJ, Feldman MF, Haurat MF (2021) Bacterial outer membrane vesicles: from discovery to applications. Annu Rev Microbiol 75:609–630. (PMID: 34351789850093910.1146/annurev-micro-052821-031444)
Schulthess B, Bloes DA, François P, Girard M, Schrenzel J, Bischoff M, Berger-Bächi B (2011) The σB-dependent yabJ-spoVG operon is involved in the regulation of extracellular nuclease, lipase, and protease expression in Staphylococcus aureus. J Bacteriol 193:4954–4962. (PMID: 21725011316568310.1128/JB.05362-11)
Schulthess B, Meier S, Homerova D, Goerke C, Wolz C, Kormanec J, Berger-Bächi B, Bischoff M (2009) Functional characterization of the sigmaB-dependent yabJ-spoVG operon in Staphylococcus aureus: role in methicillin and glycopeptide resistance. Antimicrob Agents Chemother 53:1832–1839. (PMID: 19223635268152510.1128/AAC.01255-08)
Sharma A, Dubey V, Sharma R, Devnath K, Gupta VK, Akhter J, Bhando T, Verma A, Ambatipudi K, Sarkar M, Pathania R (2018) The unusual glycine-rich C terminus of the Acinetobacter baumannii RNA chaperone Hfq plays an important role in bacterial physiology. J Biol Chem 293:13377–13388. (PMID: 30002121612021010.1074/jbc.RA118.002921)
Sharma A, Sharma R, Bhattacharyya T, Bhando T, Pathania R (2017) Fosfomycin resistance in Acinetobacter baumannii is mediated by efflux through a major facilitator superfamily (MFS) transporter-AbaF. J Antimicrob Chemother 72:68–74. (PMID: 2765018510.1093/jac/dkw382)
Shi J, Zhou T, Chen Q (2022) Exploring the expanding universe of small RNAs. Nat Cell Biol 24:415–423. (PMID: 35414016903512910.1038/s41556-022-00880-5)
Stanton BA (2021) Extracellular vesicles and host-pathogen interactions: a review of inter-kingdom signaling by small noncoding RNA. Genes (Basel) 12(7):1010.
Stubben CJ, Micheva-Viteva SN, Shou Y, Buddenborg SK, Dunbar JM, Hong-Geller E (2014) Differential expression of small RNAs from Burkholderia thailandensis in response to varying environmental and stress conditions. BMC Genomics 15:385. (PMID: 24884623403508810.1186/1471-2164-15-385)
Su Z, Wilson B, Kumar P, Dutta A (2020) Noncanonical roles of tRNAs: tRNA fragments and beyond. Annu Rev Genet 54:47–69. (PMID: 32841070768612610.1146/annurev-genet-022620-101840)
Trouillon J, Han K, Attrée I, Lory S (2022) The core and accessory Hfq interactomes across Pseudomonas aeruginosa lineages. Nat Commun 13:1258. (PMID: 35273147891370510.1038/s41467-022-28849-w)
van der Ley PA, Zariri A, van Riet E, Oosterhoff D, Kruiswijk CP (2021) An intranasal OMV-based vaccine induces high mucosal and systemic protecting immunity against a SARS-CoV-2 infection. Front Immunol 12:781280. (PMID: 34987509872166310.3389/fimmu.2021.781280)
Vickers KC, Michell DL (2021) HDL-small RNA export, transport, and functional delivery in atherosclerosis. Curr Atheroscler Rep 23:38. (PMID: 33983531845507010.1007/s11883-021-00930-7)
Vroom MM, Rodriguez-Ocasio Y, Lynch JB, Ruby EG, Foster JS (2021) Modeled microgravity alters lipopolysaccharide and outer membrane vesicle production of the beneficial symbiont Vibrio fischeri. NPJ Microgravity 7:8. (PMID: 33686090794039310.1038/s41526-021-00138-8)
Wang L, Ji C, Xia X, Cai X, Meng Q, Qiao J (2022) A regulatory SRNA Rli43 is involved in the modulation of biofilm formation and virulence in Listeria monocytogenes. Pathogens 11(10):1137.
Wang Y, Hoffmann JP, Baker SM, Bentrup KHZ, Wimley WC, Fuselier JA, Bitoun JP, Morici LA (2021) Inhibition of Streptococcus mutans biofilms with bacterial-derived outer membrane vesicles. BMC Microbiol 21:234. (PMID: 34429066838604710.1186/s12866-021-02296-x)
Wang Y, Ke Y, Duan C, Ma X, Hao Q, Song L, Guo X, Sun T, Zhang W, Zhang J, Zhao Y, Zhong Z, Yang X, Chen Z (2019) A small non-coding RNA facilitates Brucella melitensis intracellular survival by regulating the expression of virulence factor. Int J Med Microbiol 309:225–231. (PMID: 3105480810.1016/j.ijmm.2019.04.002)
Westermann AJ (2018) Regulatory RNAs in virulence and host-microbe interactions. Microbiol Spectr 6(4).
Wu C, Liu D, Zhang L, Wang J, Ding Y, Sun Z, Wang W (2023) 5’-tiRNA-Gln inhibits hepatocellular carcinoma progression by repressing translation through the interaction with eukaryotic initiation factor 4A-I. Front Med 17(3):476–492.
Xiong X, Li B, Zhou Z, Gu G, Li M, Liu J, Jiao H (2021) The VirB system plays a crucial role in brucella intracellular infection. Int J Mol Sci 22(24):13637.
Xu Z, Chen Y, Ma L, Chen Y, Liu J, Guo Y, Yu T, Zhang L, Zhu L, Shu Y (2022) Role of exosomal non-coding RNAs from tumor cells and tumor-associated macrophages in the tumor microenvironment. Mol Ther 30:3133–3154. (PMID: 35405312955291510.1016/j.ymthe.2022.01.046)
Yan H, Bu P (2021) Non-coding RNA in cancer. Essays Biochem 65:625–639. (PMID: 33860799856473810.1042/EBC20200032)
Yi L, Li J, Liu B, Wang Y (2019) Advances in research on signal molecules regulating biofilms. World J Microbiol Biotechnol 35:130. (PMID: 3138504310.1007/s11274-019-2706-x)
Zacharia A, Pal RR, Katsowich N, Mannully CT, Ibrahim A, Alfandary S, Serruya R, Baidya AK, Ben-Yehuda S, Rosenshine I, Moussaieff A (2022) Activation of the type III secretion system of enteropathogenic Escherichia coli leads to remodeling of its membrane composition and function. mSystems 7:e0020222. (PMID: 3547730410.1128/msystems.00202-22)
Zariri A, Beskers J, van de Waterbeemd B, Hamstra HJ, Bindels TH, van Riet E, van Putten JP, van der Ley P (2016) Meningococcal outer membrane vesicle composition-dependent activation of the innate immune response. Infect Immun 84:3024–3033. (PMID: 27481244503807310.1128/IAI.00635-16)
Zhang H, Zhang Y, Song Z, Li R, Ruan H, Liu Q, Huang X (2020) sncRNAs packaged by Helicobacter pylori outer membrane vesicles attenuate IL-8 secretion in human cells. Int J Med Microbiol 310:151356. (PMID: 3158571510.1016/j.ijmm.2019.151356)
Zhang W, Li S, Deng B, Wu P, Shui Y, Zhang J, Li Z (2022) Transcriptome analysis of sRNA responses to four different antibiotics in Pseudomonas aeruginosa PAO1. Microb Pathog 173:105865. (PMID: 3633279010.1016/j.micpath.2022.105865)
Zheng M, Lin R, Dong Q, Chen J, Jiang P, Zhang H, Liu J, Chen Z, Zhu J (2023) Effector Proteins of type IV secretion system: weapons of brucella used to fight against host immunity. Curr Stem Cell Res Ther 19(2):145–153.
Zingl FG, Kohl P, Cakar F, Leitner DR, Mitterer F, Bonnington KE, Rechberger GN, Kuehn MJ, Guan Z, Reidl J, Schild S (2020) Outer membrane vesiculation facilitates surface exchange and in vivo adaptation of Vibrio cholerae. Cell Host Microbe 27:225–237.e228. (PMID: 3190151910.1016/j.chom.2019.12.002)

82203032 National Natural Science Foundation of China; 32260193 National Natural Science Foundation of China; 20212BCJ23036 Training Plan for Academic and Technical Leaders of Major Disciplines in Jiangxi Province-Youth Talent Project; jxsq2023301110 Project for high and talent of Science and Technology Innovation in Jiangxi "double thousand plan"; 20220001 the start-up fund from the First Affiliated Hospital of Nanchang University

Keywords: Host-pathogen interaction; Outer membrane vesicles (OMVs); Small non-coding RNA (sncRNA); Virulence

0 (RNA, Small Untranslated)
0 (Bacterial Outer Membrane Proteins)

Date Created: 20231230 Date Completed: 20240103 Latest Revision: 20240117

20250114

10.1007/s00253-023-12855-z

38159117