Isolation and Characteristics of Extracellular Vesicles Produced by Probiotics: Yeast Saccharomyces boulardii CNCM I-745 and Bacterium Streptococcus salivarius K12.

Extracellular vesicles (EVs) Postbiotics Probiotics Proteins Proteomics THP-1 monocytes

Journal

Probiotics and antimicrobial proteins
ISSN: 1867-1314
Titre abrégé: Probiotics Antimicrob Proteins
Pays: United States
ID NLM: 101484100

Informations de publication

Date de publication:
20 May 2023
Historique:
accepted: 04 05 2023
medline: 20 5 2023
pubmed: 20 5 2023
entrez: 20 5 2023
Statut: aheadofprint

Résumé

Numerous probiotic microorganisms have repeatedly been shown to produce nanometer-sized structures named extracellular vesicles (EVs). Recently, it has been suggested that similarly to whole microbial cells, EVs produced by probiotics may also demonstrate health benefits to the host, while their application does not involve the risk of infection caused by live microorganisms. In this work, we isolated EVs from two probiotic species originating from different taxonomic domains - yeast Saccharomyces boulardii CNCM I-745 and bacterium Streptococcus salivarius K12. The diameters of S. boulardii EVs were about 142 nm and for S. salivarius EVs about 123 nm. For S. boulardii EVs, 1641 proteins and for S. salivarius EVs, 466 proteins were identified with a liquid chromatography-coupled tandem mass spectrometry and then functionally classified. In both microbial species, metabolic proteins significantly contributed to the cargo of EVs comprising 25% and 26% of all identified vesicular proteins for fungi and bacteria, respectively. Moreover, enzymes associated with cell wall rearrangement, including enzymatically active glucanases, were also identified in EVs. Furthermore, probiotic EVs were shown to influence host cells and stimulate the production of IL-1β and IL-8 by the human monocytic cell line THP-1, and, at the same time, did not cause any remarkable reduction in the survival rate of Galleria mellonella larvae in this invertebrate model commonly used to evaluate microbial EV toxicity. These observations suggest that the EVs produced by the investigated probiotic microorganisms may be promising structures for future use in pro-health applications.

Identifiants

pubmed: 37209320
doi: 10.1007/s12602-023-10085-3
pii: 10.1007/s12602-023-10085-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Narodowe Centrum Nauki
ID : 2021/43/D/NZ6/01464

Informations de copyright

© 2023. The Author(s).

Références

Domínguez Rubio AP, D’Antoni CL, Piuri M, Pérez OE (2022) Probiotics, their extracellular vesicles and infectious diseases. Front Microbiol 13:864720. https://doi.org/10.3389/fmicb.2022.864720
doi: 10.3389/fmicb.2022.864720 pubmed: 35432276 pmcid: 9006447
Higuchi A, Morishita M, Nagata R, Maruoka K, Katsumi H, Yamamoto A (2023) Functional characterization of extracellular vesicles from baker’s yeast Saccharomyces cerevisiae as a novel vaccine material for immune cell maturation. J Pharm Sci 112(2):525–524. https://doi.org/10.1016/j.xphs.2022.08.032
doi: 10.1016/j.xphs.2022.08.032 pubmed: 36057319
Liu Y, Defourny KAY, Smid EJ, Abee T (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
doi: 10.3389/fmicb.2018.01502 pubmed: 30038605 pmcid: 6046439
Taverniti V, Guglielmetti S (2011) The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes Nutr 6:261–274. https://doi.org/10.1007/s12263-011-0218-x
doi: 10.1007/s12263-011-0218-x pubmed: 21499799 pmcid: 3145061
Sanders ME, Merenstein D, Merrifield CA, Hutkins R (2018) Probiotics for human use. Nutr Bull 43(3):212–225. https://doi.org/10.1111/nbu.12334
doi: 10.1111/nbu.12334
Wieërs G, Belkhir L, Enaud R, Leclercq S, Philippart de Foy JM, Dequenne I, de Timary P, Cani PD (2020) How probiotics affect the microbiota. Front Cell Infect Microbiol 9:454. https://doi.org/10.3389/fcimb.2019.00454
doi: 10.3389/fcimb.2019.00454 pubmed: 32010640 pmcid: 6974441
Binda S, Hill C, Johansen E, Obis D, Pot B, Sanders ME, Tremblay A, Ouwehand AC (2020) Criteria to qualify microorganisms as “probiotic” in foods and dietary supplements. Front Microbio 11:1662. https://doi.org/10.3389/fmicb.2020.01662
doi: 10.3389/fmicb.2020.01662
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):1038. https://doi.org/10.3390/nu11051038
doi: 10.3390/nu11051038 pubmed: 31075872 pmcid: 6567093
González-Lozano E, García-García J, Gálvez J, Hidalgo-García L, Rodríguez-Nogales A, Rodríguez-Cabezas ME, Sánchez M (2022) Novel horizons in postbiotics: Lactobacillaceae extracellular vesicles and their applications in health and disease. Nutrients 14(24):5296. https://doi.org/10.3390/nu14245296
doi: 10.3390/nu14245296 pubmed: 36558455 pmcid: 9782203
Wilcox CR, Stuart B, Leaver H, Lown M, Willcox M, Moore M, Little P (2019) Effectiveness of the probiotic Streptococcus salivarius K12 for the treatment and/or prevention of sore throat: a systematic review. Clin Microbiol Infect 25(6):673–680. https://doi.org/10.1016/j.cmi.2018.12.031
doi: 10.1016/j.cmi.2018.12.031 pubmed: 30616011
Kaźmierczak-Siedlecka K, Ruszkowski J, Fic M, Folwarski M, Makarewicz W (2020) Saccharomyces boulardii CNCM I-745: a non-bacterial microorganism used as probiotic agent in supporting treatment of selected diseases. Curr Microbiol 77(9):1987–1996. https://doi.org/10.1007/s00284-020-02053-9
doi: 10.1007/s00284-020-02053-9 pubmed: 32472262 pmcid: 7415030
Czerucka D, Rampal P (2019) Diversity of Saccharomyces boulardii CNCM I-745 mechanisms of action against intestinal infections. World J Gastroenterol 25(18):2188–2203. https://doi.org/10.3748/wjg.v25.i18.2188
doi: 10.3748/wjg.v25.i18.2188 pubmed: 31143070 pmcid: 6526157
Burton JP, Wescombe PA, Moore CJ, Chilcott CN, Tagg JR (2006) Safety assessment of the oral cavity probiotic Streptococcus salivarius K12. Appl Environ Microbiol 72(4):3050–3053. https://doi.org/10.1128/AEM.72.4.3050-3053.2006
doi: 10.1128/AEM.72.4.3050-3053.2006 pubmed: 16598017 pmcid: 1449041
Burton JP, Chilcott CN, Wescombe PA, Tagg JR (2010) Extended safety data for the oral cavity probiotic Streptococcus salivarius K12. Probiotics Antimicrob Proteins 2(3):135–144. https://doi.org/10.1007/s12602-010-9045-4
doi: 10.1007/s12602-010-9045-4 pubmed: 26781236
Hyink O, Wescombe PA, Upton M, Ragland N, Burton JP, Tagg JR (2007) Salivaricin A2 and the novel lantibiotic salivaricin B are encoded at adjacent loci on a 190-kilobase transmissible megaplasmid in the oral probiotic strain Streptococcus salivarius K12. Appl Environ Microbiol 73(4):1107–1113. https://doi.org/10.1128/AEM.02265-06
doi: 10.1128/AEM.02265-06 pubmed: 17194838
Gregori G, Righi O, Risso P, Boiardi G, Demuru G, Ferzetti A, Galli A, Ghisoni M, Lenzini S, Marenghi C, Mura C, Sacchetti R, Suzzani L (2016) Reduction of group A beta-hemolytic streptococcus pharyngo-tonsillar infections associated with use of the oral probiotic Streptococcus salivarius K12: a retrospective observational study. Ther Clin Risk Manag 12:87–92. https://doi.org/10.2147/TCRM.S96134
doi: 10.2147/TCRM.S96134 pubmed: 26855579 pmcid: 4725641
Ishijima SA, Hayama K, Burton JP, Reid G, Okada M, Matsushita Y, Abe S (2012) Effect of Streptococcus salivarius K12 on the in vitro growth of Candida albicans and its protective effect in an oral candidiasis model. Appl Environ Microbiol 78(7):2190–2199. https://doi.org/10.1128/AEM.07055-11
doi: 10.1128/AEM.07055-11 pubmed: 22267663 pmcid: 3302625
Wescombe PA, Hale JD, Heng NC, Tagg JR (2012) Developing oral probiotics from Streptococcus salivarius. Future Microbiol 7(12):1355–1371. https://doi.org/10.2217/fmb.12.113
doi: 10.2217/fmb.12.113 pubmed: 23231486
Stašková A, Sondorová M, Nemcová R, Kačírová J, Maďar M (2021) Antimicrobial and antibiofilm activity of the probiotic strain Streptococcus salivarius K12 against oral potential pathogens. Antibiotics (Basel) 10(7):793. https://doi.org/10.3390/antibiotics10070793
doi: 10.3390/antibiotics10070793 pubmed: 34209988
Bose S, Aggarwal S, Singh DV, Acharya N (2020) Extracellular vesicles: an emerging platform in gram-positive bacteria. Microb Cell 7(12):312–322. https://doi.org/10.15698/mic2020.12.737
Karkowska-Kuleta J, Kulig K, Karnas E, Zuba-Surma E, Woznicka O, Pyza E, Kuleta P, Osyczka A, Rapala-Kozik M, Kozik A (2020) characteristics of extracellular vesicles released by the pathogenic yeast-like fungi Candida glabrata, Candida parapsilosis and Candida tropicalis. Cells 9(7):1722. https://doi.org/10.3390/cells9071722
doi: 10.3390/cells9071722 pubmed: 32708393 pmcid: 7408413
Benson JR, Hare PE (1975) O-phthalaldehyde: fluorogenic detection of primary amines in the picomole range. Comparison with fluorescamine and ninhydrin. Proc Natl Acad Sci U S A 72(2):619–622. https://doi.org/10.1073/pnas.72.2.619
doi: 10.1073/pnas.72.2.619 pubmed: 1054843 pmcid: 432365
Takayama M, Itoh S, Nagasaki T, Tanimizu I (1977) A new enzymatic method for determination of serum choline-containing phospholipids. Clin Chim Acta 79(1):93–98. https://doi.org/10.1016/0009-8981(77)90465-x
doi: 10.1016/0009-8981(77)90465-x pubmed: 890967
Kulig K, Karnas E, Woznicka O, Kuleta P, Zuba-Surma E, Pyza E, Osyczka A, Kozik A, Rapala-Kozik M, Karkowska-Kuleta J (2022) Insight into the properties and immunoregulatory effect of extracellular vesicles produced by Candida glabrata, Candida parapsilosis, and Candida tropicalis biofilms. Front Cell Infect Microbiol 12:879237. https://doi.org/10.3389/fcimb.2022.879237
doi: 10.3389/fcimb.2022.879237 pubmed: 35734578 pmcid: 9207348
Surman M, Hoja-Łukowicz D, Szwed S, Kędracka-Krok S, Jankowska U, Kurtyka M, Drożdż A, Lityńska A, Stępień E, Przybyło M (2019) An insight into the proteome of uveal melanoma-derived ectosomes reveals the presence of potentially useful biomarkers. Int J Mol Sci 20(15):3789. https://doi.org/10.3390/ijms20153789
doi: 10.3390/ijms20153789 pubmed: 31382537 pmcid: 6695883
Hughes CS, Foehr S, Garfield DA, Furlong EE, Steinmetz LM, Krijgsveld J (2014) Ultrasensitive proteome analysis using paramagnetic bead technology. Mol Syst Biol 10(10):757. https://doi.org/10.15252/msb.20145625
Perez-Riverol Y, Bai J, Bandla C, García-Seisdedos D, Hewapathirana S, Kamatchinathan S, Kundu DJ, Prakash A, Frericks-Zipper A, Eisenacher M, Walzer M, Wang S, Brazma A, Vizcaíno JA (2022) The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res 50(D1):D543–D552. https://doi.org/10.1093/nar/gkab1038
doi: 10.1093/nar/gkab1038 pubmed: 34723319
Miller GL (1959) Use of dinitrosalicylic acid reagent for the determination of reducing sugar. Anal Chem 31(3):426–428. https://doi.org/10.1021/ac60147a030
doi: 10.1021/ac60147a030
Ottaviano E, Borghi E, Giovati L, Falleni M, Tosi D, Magliani W, Morace G, Conti S, Ciociola T (2021) Therapeutic effect of an antibody-derived peptide in a Galleria mellonella model of systemic candidiasis. Int J Mol Sci 22(20):10904. https://doi.org/10.3390/ijms222010904
doi: 10.3390/ijms222010904 pubmed: 34681564 pmcid: 8536055
Mehanny M, Koch M, Lehr CM, Fuhrmann G (2020) Streptococcal extracellular membrane vesicles are rapidly internalized by immune cells and alter their cytokine release. Front Immunol 11:80. https://doi.org/10.3389/fimmu.2020.00080
doi: 10.3389/fimmu.2020.00080 pubmed: 32117243 pmcid: 7034238
Kurata A, Kiyohara S, Imai T, Yamasaki-Yashiki S, Zaima N, Moriyama T, Kishimoto N, Uegaki K (2022) Characterization of extracellular vesicles from Lactiplantibacillus plantarum. Sci Rep 12:13330. https://doi.org/10.1038/s41598-022-17629-7
doi: 10.1038/s41598-022-17629-7 pubmed: 35941134 pmcid: 9360025
UniProt Consortium (2022) UniProt: the universal protein knowledgebase in 2023. Nucleic Acids Res. https://doi.org/10.1093/nar/gkac1052
doi: 10.1093/nar/gkac1052
Paysan-Lafosse T, Blum M, Chuguransky S, Grego T, Pinto BL, Salazar GA, Bileschi ML, Bork P, Bridge A, Colwell L, Gough J, Haft DH, Letunić I, Marchler-Bauer A, Mi H, Natale DA, Orengo CA, Pandurangan AP, Rivoire C, Sigrist CJA, Sillitoe I, Thanki N, Thomas PD, Tosatto SCE, Wu CH, Bateman A (2022) InterPro in 2022. Nucleic Acids Res. https://doi.org/10.1093/nar/gkac993
doi: 10.1093/nar/gkac993 pmcid: 9825450
Cortat M, Matile P, Wiemken A (1972) Isolation of glucanase-containing vesicles from budding yeast. Archiv Mikrobiol 82:189–205. https://doi.org/10.1007/BF00412191
doi: 10.1007/BF00412191
Macia L, Nanan R, Hosseini-Beheshti E, Grau GE (2020) Host- and microbiota-derived extracellular vesicles, immune function, and disease development. Int J Mol Sci 21(1):107. https://doi.org/10.3390/ijms21010107
doi: 10.3390/ijms21010107
Doron S, Snydman DR (2015) Risk and safety of probiotics. Clin Infect Dis 60(Suppl2):S129–S134. https://doi.org/10.1093/cid/civ085
doi: 10.1093/cid/civ085 pubmed: 25922398 pmcid: 4490230
Imre A, Kovács R, Pázmándi K, Nemes D, Jakab Á, Fekete T, Rácz HV, Dóczi I, Bácskay I, Gácser A, Kovács K, Majoros L, Farkas Z, Pócsi I, Pfliegler WP (2021) Virulence factors and in-host selection on phenotypes in infectious probiotic yeast isolates (Saccharomyces ‘boulardii’). J Fungi (Basel) 7(9):746. https://doi.org/10.3390/jof7090746
doi: 10.3390/jof7090746 pubmed: 34575784
Oliveira DL, Nakayasu ES, Joffe LS, Guimarães AJ, Sobreira TJ, Nosanchuk JD, Cordero RJ, Frases S, Casadevall A, Almeida IC, Nimrichter L, Rodrigues ML (2010) Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS ONE 5(6):e11113. https://doi.org/10.1371/journal.pone.0011113
doi: 10.1371/journal.pone.0011113 pubmed: 20559436 pmcid: 2885426
Mencher A, Morales P, Valero E, Tronchoni J, Patil KR, Gonzalez R (2020) Proteomic characterization of extracellular vesicles produced by several wine yeast species. Microb Biotechnol 13(5):1581–1596. https://doi.org/10.1111/1751-7915.13614
doi: 10.1111/1751-7915.13614 pubmed: 32578397 pmcid: 7415363
Lee H, Yun SH, Hyon JY, Lee SY, Yi YS, Choi CW, Jun S, Park EC, Kim SI (2021) Streptococcus equi-derived extracellular vesicles as a vaccine candidate against Streptococcus equi infection. Vet Microbiol 259:109165. https://doi.org/10.1016/j.vetmic.2021.109165
doi: 10.1016/j.vetmic.2021.109165 pubmed: 34225054
Croatti V, Parolin C, Giordani B, Foschi C, Fedi S, Vitali B (2022) Lactobacilli extracellular vesicles: potential postbiotics to support the vaginal microbiota homeostasis. Microb Cell Fact 21(1):237. https://doi.org/10.1186/s12934-022-01963-6
doi: 10.1186/s12934-022-01963-6 pubmed: 36376912 pmcid: 9664694
Morishita M, Sagayama R, Yamawaki Y, Yamaguchi M, Katsumi H, Yamamoto A (2022) Activation of host immune cells by probiotic-derived extracellular vesicles via TLR2-mediated signaling pathways. Biol Pharm Bull 45(3):354–359. https://doi.org/10.1248/bpb.b21-00924
doi: 10.1248/bpb.b21-00924 pubmed: 35228401
Zhao K, Bleackley M, Chisanga D, Gangoda L, Fonseka P, Liem M, Kalra H, Al Saffar H, Keerthikumar S, Ang CS, Adda CG, Jiang L, Yap K, Poon IK, Lock P, Bulone V, Anderson M, Mathivanan S (2019) Extracellular vesicles secreted by Saccharomyces cerevisiae are involved in cell wall remodelling. Commun Biol 2:305. https://doi.org/10.1038/s42003-019-0538-8
doi: 10.1038/s42003-019-0538-8 pubmed: 31428693 pmcid: 6688994
Sánchez N, Roncero C (2022) Chitin Synthesis in Yeast: A Matter of Trafficking. Int J Mol Sci 23(20):12251. https://doi.org/10.3390/ijms232012251
doi: 10.3390/ijms232012251 pubmed: 36293107 pmcid: 9603707
Brown L, Wolf JM, Prados-Rosales R, Casadevall A (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
doi: 10.1038/nrmicro3480 pubmed: 26324094 pmcid: 4860279
Brown GD, Taylor PR, Reid DM, Willment JA, Williams DL, Martinez-Pomares L, Wong SY, Gordon S (2002) Dectin-1 is a major beta-glucan receptor on macrophages. J Exp Med 196(3):407–412. https://doi.org/10.1084/jem.20020470
doi: 10.1084/jem.20020470 pubmed: 12163569 pmcid: 2193936
Nimrichter L, de Souza MM, Del Poeta M, Nosanchuk JD, Joffe L, Tavares Pde M, Rodrigues ML (2016) Extracellular vesicle-associated transitory cell wall components and their impact on the interaction of fungi with host cells. Front Microbiol 7:1034. https://doi.org/10.3389/fmicb.2016.01034
doi: 10.3389/fmicb.2016.01034 pubmed: 27458437 pmcid: 4937017
Oliveira DL, Rizzo J, Joffe LS, Godinho RM, Rodrigues ML (2013) Where do they come from and where do they go: candidates for regulating extracellular vesicle formation in fungi. Int J Mol Sci 14(5):9581–9603. https://doi.org/10.3390/ijms14059581
doi: 10.3390/ijms14059581 pubmed: 23644887 pmcid: 3676800
Douglas LM, Konopka JB (2014) Fungal membrane organization: the eisosome concept. Annu Rev Microbiol 68:377–393. https://doi.org/10.1146/annurev-micro-091313-103507
doi: 10.1146/annurev-micro-091313-103507 pubmed: 25002088
Dawson CS, Garcia-Ceron D, Rajapaksha H, Faou P, Bleackley MR, Anderson MA (2020) Protein markers for Candida albicans EVs include claudin-like Sur7 family proteins. J Extracell Vesicles 9(1):1750810. https://doi.org/10.1080/20013078.2020.1750810
doi: 10.1080/20013078.2020.1750810 pubmed: 32363014 pmcid: 7178836
Moré MI, Vandenplas Y (2018) Saccharomyces boulardii CNCM I-745 improves intestinal enzyme function: a trophic effects Review. Clin Med Insights Gastroenterol 11:1179552217752679. https://doi.org/10.1177/1179552217752679
doi: 10.1177/1179552217752679 pubmed: 29449779 pmcid: 5808955
Nakamura A, Kurihara S, Takahashi D, Ohashi W, Nakamura Y, Kimura S, Onuki M, Kume A, Sasazawa Y, Furusawa Y, Obata Y, Fukuda S, Saiki S, Matsumoto M, Hase K (2021) Symbiotic polyamine metabolism regulates epithelial proliferation and macrophage differentiation in the colon. Nat Commun 12(1):2105. https://doi.org/10.1038/s41467-021-22212-1
doi: 10.1038/s41467-021-22212-1 pubmed: 33833232 pmcid: 8032791
Buts JP, De Keyser N, Stilmant C, Sokal E, Marandi S (2002) Saccharomyces boulardii enhances N-terminal peptide hydrolysis in suckling rat small intestine by endoluminal release of a zinc-binding metalloprotease. Pediatr Res 51(4):528–534. https://doi.org/10.1203/00006450-200204000-00021
doi: 10.1203/00006450-200204000-00021 pubmed: 11919341
Buts JP, Dekeyser N, Stilmant C, Delem E, Smets F, Sokal E (2006) Saccharomyces boulardii produces in rat small intestine a novel protein phosphatase that inhibits Escherichia coli endotoxin by dephosphorylation. Pediatr Res 60(1):24–29. https://doi.org/10.1203/01.pdr.0000220322.31940.29
doi: 10.1203/01.pdr.0000220322.31940.29 pubmed: 16690953
Dassa E, Bouige P (2001) The ABC of ABCS: a phylogenetic and functional classification of ABC systems in living organisms. Res Microbiol 152(3–4):211–229. https://doi.org/10.1016/s0923-2508(01)01194-9
doi: 10.1016/s0923-2508(01)01194-9 pubmed: 11421270
Lewis VG, Ween MP, McDevitt CA (2012) The role of ATP-binding cassette transporters in bacterial pathogenicity. Protoplasma 249(4):919–942. https://doi.org/10.1007/s00709-011-0360-8
doi: 10.1007/s00709-011-0360-8 pubmed: 22246051
Chaffanel F, Charron-Bourgoin F, Soligot C, Kebouchi M, Bertin S, Payot S, Le Roux Y, Leblond-Bourget N (2018) Surface proteins involved in the adhesion of Streptococcus salivarius to human intestinal epithelial cells. Appl Microbiol Biotechnol 102(6):2851–2865. https://doi.org/10.1007/s00253-018-8794-y
doi: 10.1007/s00253-018-8794-y pubmed: 29442170 pmcid: 5847202
Cao Y, Zhou Y, Chen D, Wu R, Guo L, Lin H (2020) Proteomic and metabolic characterization of membrane vesicles derived from Streptococcus mutans at different pH values. Appl Microbiol Biotechnol 104(22):9733–9748. https://doi.org/10.1007/s00253-020-10563-6
doi: 10.1007/s00253-020-10563-6 pubmed: 33064184
Miyachiro MM, Contreras-Martel C, Dessen A (2019) Penicillin-binding proteins (PBPs) and bacterial cell wall elongation complexes. Subcell Biochem 93:273–289. https://doi.org/10.1007/978-3-030-28151-9_8
doi: 10.1007/978-3-030-28151-9_8 pubmed: 31939154
Mora D, Arioli S (2014) Microbial urease in health and disease. PLoS Pathog 10(12):e1004472. https://doi.org/10.1371/journal.ppat.1004472
doi: 10.1371/journal.ppat.1004472 pubmed: 25501953 pmcid: 4263730
Wescombe PA, Heng NC, Burton JP, Tagg JR (2010) Something old and something new: an update on the amazing repertoire of bacteriocins produced by Streptococcus salivarius. Probiotics Antimicrob Proteins 2(1):37–45. https://doi.org/10.1007/s12602-009-9026-7
doi: 10.1007/s12602-009-9026-7 pubmed: 26780899
Dean SN, Leary DH, Sullivan CJ, Oh E, Walper SA (2019) Isolation and characterization of Lactobacillus-derived membrane vesicles. Sci Rep 9:877. https://doi.org/10.1038/s41598-018-37120-6
doi: 10.1038/s41598-018-37120-6 pubmed: 30696852 pmcid: 6351534
Wang Y, Wu J, Lv M, Shao Z, Hungwe M, Wang J, Bai X, Xie J, Wang Y, Geng W (2021) Metabolism characteristics of lactic acid bacteria and the expanding applications in food industry. Front Bioeng Biotechnol 9:612285. https://doi.org/10.3389/fbioe.2021.612285
doi: 10.3389/fbioe.2021.612285 pubmed: 34055755 pmcid: 8149962
Couvigny B, Kulakauskas S, Pons N, Quinquis B, Abraham AL, Meylheuc T, Delorme C, Renault P, Briandet R, Lapaque N, Guedon E (2018) Identification of new factors modulating adhesion abilities of the pioneer commensal bacterium Streptococcus salivarius. Front Microbiol 9:273. https://doi.org/10.3389/fmicb.2018.00273
doi: 10.3389/fmicb.2018.00273 pubmed: 29515553 pmcid: 5826255
Xu RR, Yang WD, Niu KX, Wang B, Wang WM (2018) An uptake on the evolution of glucosyltransferase (Gtf) genes in Streptococcus. Front Microbiol 9:2979. https://doi.org/10.3389/fmicb.2018.02979
doi: 10.3389/fmicb.2018.02979 pubmed: 30568640 pmcid: 6290343
Domínguez Rubio AP, Martinez JH, Martinez Casillas DC, Coluccio Leskow F, Piuri M, Pérez OE (2017) Lactobacillus casei BL23 produces microvesicles carrying proteins that have been associated with its probiotic effect. Front Microbiol 8:1783. https://doi.org/10.3389/fmicb.2017.01783
doi: 10.3389/fmicb.2017.01783 pubmed: 28979244 pmcid: 5611436
Smith IM, Christensen JE, Arneborg N, Jespersen L (2014) Yeast modulation of human dendritic cell cytokine secretion: an in vitro study. PLoS ONE 9(5):e96595. https://doi.org/10.1371/journal.pone.0096595
doi: 10.1371/journal.pone.0096595 pubmed: 24816850 pmcid: 4015989
van Baarlen P, Troost F, van der Meer C, Hooiveld G, Boekschoten M, Brummer RJ, Kleerebezem M (2011) Human mucosal in vivo transcriptome responses to three lactobacilli indicate how probiotics may modulate human cellular pathways. Proc Natl Acad Sci U S A 108(Suppl 1):4562–4569. https://doi.org/10.1073/pnas.1000079107
doi: 10.1073/pnas.1000079107 pubmed: 20823239
Meijerink M, Wells JM, Taverne N, de Zeeuw Brouwer ML, Hilhorst B, Venema K, van Bilsen J (2012) Immunomodulatory effects of potential probiotics in a mouse peanut sensitization model. FEMS Immunol Med Microbiol 65:488–496. https://doi.org/10.1111/j.1574-695X.2012.00981.x
doi: 10.1111/j.1574-695X.2012.00981.x pubmed: 22540665
Cosseau C, Devine DA, Dullaghan E, Gardy JL, Chikatamarla A, Gellatly S, Yu LL, Pistolic J, Falsafi R, Tagg J, Hancock REW (2008) The commensal Streptococcus salivarius K12 Downregulates the innate immune responses of human epithelial cells and promotes host-microbe homeostasis. Infect Immun 76(9):4163–4175. https://doi.org/10.1128/IAI.00188-08
doi: 10.1128/IAI.00188-08 pubmed: 18625732 pmcid: 2519405
van den Bogert B, Meijerink M, Zoetendal EG, Wells JM, Kleerebezem M (2014) Immunomodulatory properties of Streptococcus and Veillonella isolates from the human small intestine microbiota. PLoS ONE 9(12):e114277. https://doi.org/10.1371/journal.pone.0114277
doi: 10.1371/journal.pone.0114277 pubmed: 25479553 pmcid: 4257559
Taverniti V, Minuzzo M, Arioli S, Junttila I, Hämäläinen S, Turpeinen H, Mora D, Karp M, Pesu M, Guglielmetti S (2012) In vitro functional and immunomodulatory properties of the Lactobacillus helveticus MIMLh5-Streptococcus salivarius st3 association that are relevant to the development of a pharyngeal probiotic product. Appl Environ Microbiol 78(12):4209–4216. https://doi.org/10.1128/AEM.00325-12
doi: 10.1128/AEM.00325-12 pubmed: 22504812 pmcid: 3370528
Kaci G, Lakhdari O, Dore J, Ehrlich SD, Renault P, Blottiere HM, Delorme C (2011) Inhibition of the NF-kB pathway in human intestinal epithelial cells by commensal Streptococcus salivarius. Appl Environ Microbiol 77(13):4681–4684. https://doi.org/10.1128/AEM.03021-10
doi: 10.1128/AEM.03021-10 pubmed: 21602373 pmcid: 3127691
Kim W, Lee EJ, Bae IH, Myoung K, Kim ST, Park PJ, Lee KH, Pham AVQ, Ko J, Oh SH, Cho EG (2020) Lactobacillus plantarum-derived extracellular vesicles induce anti-inflammatory M2 macrophage polarization in vitro. J Extracell Vesicles 9(1):1793514. https://doi.org/10.1080/20013078.2020.1793514
doi: 10.1080/20013078.2020.1793514 pubmed: 32944181 pmcid: 7480564
Gu Z, Li F, Liu Y, Jiang M, Zhang L, He L, Wilkey DW, Merchant M, Zhang X, Deng Z-B, Chen S-Y, Barve S, McClain CJ, Feng W (2021) Exosome-like nanoparticles from Lactobacillus rhamnosus GG protect against alcohol-associated liver disease through intestinal aryl hydrocarbon receptor in mice. Hepatol Commun 5:846–864. https://doi.org/10.1002/hep4.1679
doi: 10.1002/hep4.1679 pubmed: 34027273 pmcid: 8122379
Morishita M, Horita M, Higuchi A, Marui M, Katsumi H, Yamamoto A (2021) Characterizing different probiotic-derived extracellular vesicles as a novel adjuvant for immunotherapy. Mol Pharm 18(3):1080–1092. https://doi.org/10.1021/acs.molpharmaceut.0c01011
doi: 10.1021/acs.molpharmaceut.0c01011 pubmed: 33554596
Moman R, O’Neill CA, Ledder RG, Cheesapcharoen T, McBain AJ (2020) Mitigation of the toxic effects of periodontal pathogens by candidate probiotics in oral keratinocytes, and in an invertebrate model. Front Microbiol 11:999. https://doi.org/10.3389/fmicb.2020.00999
doi: 10.3389/fmicb.2020.00999 pubmed: 32612578 pmcid: 7308727

Auteurs

Kamila Kulig (K)

Department of Comparative Biochemistry and Bioanalytics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland.

Katarzyna Kowalik (K)

Department of Comparative Biochemistry and Bioanalytics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland.

Magdalena Surowiec (M)

Department of Comparative Biochemistry and Bioanalytics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland.
Doctoral School of Exact and Natural Sciences, Jagiellonian University, Kraków, Poland.

Elzbieta Karnas (E)

Department of Cell Biology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland.

Olga Barczyk-Woznicka (O)

Department of Cell Biology and Imaging, Institute of Zoology and Biomedical Research, Jagiellonian University, Kraków, Poland.

Ewa Zuba-Surma (E)

Department of Cell Biology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland.

Elzbieta Pyza (E)

Department of Cell Biology and Imaging, Institute of Zoology and Biomedical Research, Jagiellonian University, Kraków, Poland.

Andrzej Kozik (A)

Department of Analytical Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland.

Maria Rapala-Kozik (M)

Department of Comparative Biochemistry and Bioanalytics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland.

Justyna Karkowska-Kuleta (J)

Department of Comparative Biochemistry and Bioanalytics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland. justyna.karkowska@uj.edu.pl.

Classifications MeSH