Advanced search
Publication Cover
Future Microbiology Volume 6, 2011 - Issue 5
Submit an article Journal homepage
333
Views
0
CrossRef citations to date
0
Altmetric
Review

Lactobacilli at the Front Line of Defense Against Vaginally Acquired Infections

Rachel R Spurbeck1 Genetics Program,Michigan State University,5192 Biomedical Physical Sciences, Michigan State University,East Lansing,MI 48824-1101,USA;2 Department of Microbiology & Immunology,5641 Medical Science II,University of Michigan,Ann Arbor,MI 48109-0620,USAView further author information
&
Cindy Grove Arvidson1 Genetics Program,Michigan State University,5192 Biomedical Physical Sciences, Michigan State University,East Lansing,MI 48824-1101,USA;3 Department of Microbiology & Molecular Genetics,5192 Biomedical Physical Sciences,Michigan State University,East Lansing,MI 48824-1101,USA.Correspondence[email protected]
View further author information
Pages 567-582 | Published online: 17 May 2011

Bibliography

  • Papaioannou S , BourdrezP, VarmaR, AfnanM, MolBW, CoomarasamyA: Tubal evaluation in the investigation of subfertility: a structured comparison of tests.BJOG111(12) , 1313–1321 (2004).
  • Westrom LV : Chlamydia and its effect on reproduction.J. Br. Fer. Soc.1(1) , 23–30 (1996).
  • Westrom L , EschenbachD: Pelvic Inflammatory Disease. In:Sexually Transmitted Diseases (3rd Edition). HolmesKK, SparlingPF, MardhPet al. (Eds). McGraw-Hill, NY, USA789–809 (1999).
  • R⊘ttingen J-A , CameronW, GarnettGP: A systematic review of the epidemiologic interactions between classic sexually transmitted diseases and HIV: how much really is known?Sex. Transm. Dis.28(10) , 579–597 (2001).
  • Johnson LF , LewisDA: The effect of genital tract infections on HIV-1 shedding in the genital tract: a systematic review and meta-analysis.Sex. Transm. Dis.35(11) , 946–959 (2008).
  • Laga M , ManokaA, KivuvuMet al. : Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: results from a cohort study.AIDS7(1) , 95–102 (1993).
  • Guenthner PC , SecorWE, DezzuttiCS: Trichomonas vaginalis-induced epithelial monolayer disruption and human immunodeficiency virus type 1 (HIV-1) replication: implications for the sexual transmission of HIV-1.Infect. Immun.73(7) , 4155–4160 (2005).
  • Eschenbach D : Bacterial vaginosis and anaerobes in obstetric-gynecologic infection.Clin. Infect. Dis.16(4) , S282–S287 (1993).
  • Dumonceaux TJ , SchellenbergJ, GoleskiVet al. : Multiplex detection of bacteria associated with normal microbiota and with bacterial vaginosis in vaginal swabs by use of oligonucleotide-coupled fluorescent microspheres.J. Clin. Microbiol.47(12) , 4067–4077 (2009).
  • Menard P-P , FenollarF, HenryM, BretelleF, RaoultD: Molecular quantification of Gardnerella vaginalis and Atopobium vaginae loads to predict bacterial vaginosis.Clin. Infect. Dis.47(1) , 33–43 (2008).
  • Pybus V , OnderdonkAB: Microbial interactions in the vaginal ecosystem, with emphasis on the pathogenesis of bacterial vaginosis.Microbes Infect.1(4) , 285–292 (1999).
  • Verhelst R , VerstraelenH, ClaeysGet al. : Cloning of 16S rRNA genes amplified from normal and disturbed vaginal microflora suggests a strong association between Atopobium vaginae, Gardnerella vaginalis and bacterial vaginosis.BMC Microbiol.4 , 16 (2004).
  • Ferris MJ , NororiJ, Zozaya-HinchliffeM, MartinDH: Cultivation-independent analysis of changes in bacterial vaginosis flora following metronidazole treatment.J. Clin. Microbiol.45(3) , 1016–1018 (2007).
  • Fredricks DN , FiedlerTL, ThomasKK, MitchellCM, MarrazzoJM: Changes in vaginal bacterial concentrations with intravaginal metronidazole therapy for bacterial vaginosis as assessed by quantitative PCR.J. Clin. Microbiol.47(3) , 721–726 (2009).
  • Koumans EH , SternbergM, BruceCet al. : The prevalence of bacterial vaginosis in the United States, 2001–2004; associations with symptoms, sexual behaviors, and reproductive health.Sex. Transm. Dis.34(11) , 864–869 (2007).
  • Martin HL , RichardsonBA, NyangePMet al. : Vaginal lactobacilli, microbial flora, and risk of human immunodeficiency virus type 1 and sexually transmitted disease acquisition.J. Infect. Dis.180(6) , 1863–1868 (1999).
  • Sweet RL : Gynecologic conditions and bacterial vaginosis: implications for the non-pregnant patient.Infect. Dis. Obstet. Gynecol.8(3–4) , 184–190 (2000).
  • Wiesenfeld HC , HillierSL, KrohnMA, LandersDV, SweetR: Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection.Clin. Infect. Dis.36(5) , 663–668 (2003).
  • Blondeau JM : Current issues in the management of urinary tract infections: extended-release ciprofloxacin as a novel treatment option.Drugs64(6) , 611–628 (2004).
  • Hooton TM : Recurrent urinary tract infection in women.Int. J. Antimicrob. Agents17(4) , 259–268 (2001).
  • Foxman B : Recurring urinary tract infection: incidence and risk factors.Am. J. Public Health.80(3) , 331–333 (1990).
  • Ikäheimo R , SiitonenA, HeiskanenTet al. : Recurrence of urinary tract infection in a primary care setting: analysis of a 1-year follow-up of 179 women.Clin. Infect. Dis.22(1) , 91–99 (1996).
  • Musser JM , SchlievertPM, ChowAWet al. : A single clone of Staphylococcus aureus causes the majority of cases of toxic shock syndrome.Proc. Natl Acad. Sci. USA87(1) , 225–229 (1990).
  • Shands KN , SchmidGP, DanBBet al. : Toxic-shock syndrome in menstruating women: association with tampon use and Staphylococcus aureus and clinical features in 52 cases.N. Engl. J. Med.303(25) , 1436–1442 (1980).
  • Parsonnet J , HansmannMA, DelaneyMLet al. : Prevalence of toxic shock syndrome toxin 1-producing Staphylococcus aureus and the presence of antibodies to this superantigen in menstruating women.J. Clin. Microbiol.43(9) , 4628–4634 (2005).
  • Nannini E , MurrayBE, AriasCA: Resistance or decreased susceptibility to glycopeptides, daptomycin, and linezolid in methicillin-resistant Staphylococcus aureus.Curr. Opin. Pharm.10(5) , 516–521 (2010).
  • Thomas CM , HothersallJ, WillisCL, SimpsonTJ: Resistance to and synthesis of the antibiotic mupirocin.Nat. Rev. Microbiol.8(4) , 281–289 (2010).
  • Hansen SM , UldbjergN, KilianM, SorensenUBS: Dynamics of Streptococcus agalactiae colonization in women during and after pregnancy and in their infants.J. Clin. Microbiol.42(1) , 83–89 (2004).
  • Puopolo KM , MadoffLC, EichenwaldEC: Early-onset group B streptococcal disease in the era of maternal screening.Pediatrics115(5) , 1240–1246 (2005).
  • Zhou X , BrownCJ, AbdoZet al. : Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women.ISME J.1(2) , 121–133 (2007).
  • Hyman RW , FukushimaM, DiamondL, KummJ, GiudiceLC, DavisRW: Microbes on the human vaginal epithelium.Proc. Natl Acad. Sci. USA102(22) , 7952–7957 (2005).
  • Zhou X , BentSJ, SchneiderMG, DavisCC, IslamMR, ForneyLJ: Characterization of vaginal microbial communities in adult healthy women using cultivation-independent methods.Microbiology150(8) , 2565–2573 (2004).
  • Burton JP , CadieuxPA, ReidG: Improved understanding of the bacterial vaginal microbiota of women before and after probiotic instillation.Appl. Env. Microbiol.69(1) , 97–101 (2003).
  • Ravel J , GajerP, AbdoZet al. : Vaginal microbiome of reproductive-age women.Proc. Natl Acad. Sci. USA108(Suppl. l) , 4680–4687 (2011).
  • Antonio MAD , HawesSE, HillierSL: The identification of vaginal Lactobacillus species and the demographic and microbiologic characteristics of women colonized by these species.J. Infect. Dis.180(6) , 1950–1956 (1999).
  • Eschenbach DA , DavickPR, WilliamsBLet al. : Prevalence of hydrogen peroxide-producing Lactobacillus species in normal women and women with bacterial vaginosis.J. Clin. Microbiol.27(2) , 251–256 (1989).
  • Giorgi A , TorrianiF, DellaglioF, BoG, StolaE, BernuzziL: Identification of vaginal lactobacilli from asymptomatic women.Microbiologica10(4) , 377–384 (1987).
  • Torok MR , MillerWC, HobbsMMet al. : The association between Trichomonas vaginalis infection and level of vaginal lactobacilli, in nonpregnant women.J. Infect. Dis.196(7) , 1102–1107 (2007).
  • Hawes SE , HillierSL, BenedettiJet al. : Hydrogen peroxide-producing lactobacilli and acquisition of vaginal infections.J. Infect. Dis.174(5) , 1058–1063 (1996).
  • Baeten JM , HassanWM, ChohanVet al. : Prospective study of correlates of vaginal Lactobacillus colonisation among high-risk HIV-1 seronegative women.Sex. Transm. Infect.85(5) , 348–353 (2009).
  • Andreu A , StapletonAE, FennellCL, HillierSL, StammWE: Hemagglutination, adherence, and surface properties of vaginal Lactobacillus species.J. Infect. Dis.171(15) , 1237–1243 (1995).
  • Spurbeck RR , ArvidsonCG: Inhibition of Neisseria gonorrhoeae epithelial cell interactions by vaginal Lactobacillus species.Infect. Immun.76(7) , 3124–3130 (2008).
  • Swidsinski A , MendlingW, Loening-BauckeVet al. : Adherent biofilms in bacterial vaginosis.Obstet. Gynecol.106(5) , 1013–1023 (2005).
  • Boris S , SuarezJE, VazquezF, Barbes C; Adherence of human vaginal lactobacilli to vaginal epithelial cells and interaction with uropathogens. Infect. Immun.66(5) , 1985–1989 (1998).
  • Mastromarino P , BrigidiP, MacchiaSet al. : Characterization and selection of vaginal Lactobacillus strains for the preparation of vaginal tablets.J. Appl. Microbiol.93(5) , 884–893 (2002).
  • Vallor AC , AntonioMA, HawesSE, HillierSL: Factors associated with acquisition of, or persistent colonization by, vaginal lactobacilli: role of hydrogen peroxide production.J. Infect. Dis.184(11) , 1431–1436 (2001).
  • Antonio MA , RabeLK, HillierSL: Colonization of the rectum by Lactobacillus species and decreased risk of bacterial vaginosis.J. Infect. Dis.192(3) , 394–398 (2005).
  • Kaufmann SH : Elie Metchnikoff‘s and Paul Ehrlich‘s impact on infection biology.Microbes Infect.10(14–15) , 1417–1419 (2008).
  • Bruce AW , ChadwickP, HassanA, VanCottGF: Recurrent urethritis in women.Can. Med. Assoc. J.108(8) , 973–976 (1973).
  • Bruce AW , ReidG: Intravaginal instillation of lactobacilli for prevention of recurrent urinary tract infections.Can. J. Microbiol.34(3) , 339–343 (1988).
  • Huffnagle GB , WernickS: The Probiotics Revolution. Bantam Dell, NY, USA (2007).
  • Redondo-Lopez V , CookRL, SobelJD: Emerging role of lactobacilli in the control and maintenance of the vaginal bacterial microflora.Rev. Infect. Dis.12(5) , 856–872 (1990).
  • Boskey ER , TelschKM, WhaleyKJ, MoenchTR, ConeRA: Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification.Infect. Immun.67(10) , 5170–5175 (1999).
  • Wilson M : The reproductive system and its indiginous microbiota. In:Microbial Inhabitants of Humans: Their Ecology and Role in Health and Disease. Cambridge University Press, NY, USA, 206–250 (2005).
  • Juarez Tomas MS , OcanaVS, WieseB, Nader-MaciasME: Growth and lactic acid production by vaginal Lactobacillus acidophilus CRL 1259, and inhibition of uropathogenic Escherichia coli.J. Med. Microbiol.52(12) , 1117–1124 (2003).
  • Cadieux PA , BurtonJ, DevillardE, ReidG. Lactobacillus by-products inhibit the growth and virulence of uropathogenic Escherichia coli.J. Physiol. Pharmacol.60(S6), 13–18 (2009).
  • Ocana VS , Pescede Ruiz Holgado AA, Nader-MaciasME: Selection of vaginal H2O2-generating Lactobacillus species for probiotic use.Curr. Microbiol.38(5) , 279–284 (1999).
  • McLean NW , RosensteinIJ: Characterization and selection of a Lactobacillus species to re-colonize the vagina of women with recurrent bacterial vaginosis.J. Med. Microbiol.49(6) , 543–552 (2000).
  • Smith H , YatesEA, ColeJA, ParsonsNJ: Lactate stimulation of gonococcal metabolism in media containing glucose: mechanism, impact on pathogenicity, and wider implications for other pathogens.Infect. Immun.69(11) , 6565–6572 (2001).
  • Strus M , KucharskaA, KuklaG, Brzychczy-WlochM, MareszK, HeczkoPB: The in vitro activity of vaginal Lactobacillus with probiotic properties against Candida.Infect. Dis. Obstet. Gynecol.13(2) , 69–75 (2005).
  • Zarate G , Nader-MaciasME: Influence of probiotic vaginal lactobacilli on in vitro adhesion of urogenital pathogens to vaginal epithelial cells.Lett. Appl. Microbiol.43(2) , 174–180 (2006).
  • Rabe LK , HillierSL: Optimization of media for detection of hydrogen peroxide production by Lactobacillus species.J. Clin. Microbiol.41(7) , 3260–3264 (2003).
  • Kim YH , KimCH, ChoMK, NaJH, SongTB, OhJS: Hydrogen peroxide-producing Lactobacilli in the vaginal flora of pregnant women with preterm labor with intact membranes.Int. J. Gynaecol. Obstet.93(1) , 22–27 (2006).
  • Wilks M , WigginsR, WhileyAet al. : Identification and H2O2 production of vaginal lactobacilli from pregnant women at high risk of preterm birth and relation with outcome.J. Clin. Microbiol.42(2) , 713–717 (2004).
  • Schwebke JR : Role of vaginal flora as a barrier to HIV acquisition.Curr. Infect. Dis. Rep.3(2) , 152–155 (2001).
  • Knezevic A , StepanovicS, CupicM, JevtovicD, RaninJ, JovanovicT: Reduced quantity and hydrogen-peroxide production of vaginal lactobacilli in HIV positive women.Biomed. Pharmacother.59(9) , 521–523 (2005).
  • Atassi F , BrassartD, GrobP, GrafF, ServinAL: Lactobacillus strains isolated from the vaginal microbiota of healthy women inhibit Prevotella bivia and Gardnerella vaginalis in coculture and cell culture.FEMS Immunol. Med. Microbiol.48(3) , 424–432 (2006).
  • Ocaña VS , PesceDe Ruiz Holgado AA, Nader-MacíasME: Characterization of a bacteriocin-like substance produced by a vaginal Lactobacillus salivarius strain.Appl. Environ. Microbiol.65(12) , 5631–5635 (1999).
  • Saigh JH , SandersCC, SandersWEJ: Inhibition of Neisseria gonorrhoeae by aerobic and facultatively anaerobic components of the endocervical flora: evidence for a protective effect against infection.Infect. Immun.19(2) , 704–710 (1978).
  • St. Amant DC , Valentin-BonIE, JerseAE: Inhibition of Neisseria gonorrhoeae by Lactobacillus species that are commonly isolated from the female genital tract.Infect. Immun.70(12) , 7169–7171 (2002).
  • Zheng HY , AlcornTM, CohenMS: Effects of H2O2-producing lactobacilli on Neisseria gonorrhoeae growth and catalase activity.J. Infect. Dis.170(5) , 1209–1215 (1994).
  • Atassi F , ServinAL: Individual and co-operative roles of lactic acid and hydrogen peroxide in the killing activity of enteric strain Lactobacillus johnsonii NCC933 and vaginal strain Lactobacillus gasseri KS120.1 against enteric, uropathogenic and vaginosis-associated pathogens.FEMS Microbiol. Lett.304(1) , 29–38 (2010).
  • Martín R , SuárezJE: Biosynthesis and degradation of H2O2 by vaginal lactobacilli.Appl. Env. Microbiol.76(2) , 400–405 (2010).
  • Genco CA , DesaiPJ: Iron acquisition in the pathogenic Neisseria.Trends Microbiol.4(5) , 179–184 (1996).
  • Kawai Y , KempermanR, KokJ, SaitoT: The circular bacteriocins gassericin A and circularin A.Curr. Prot. Pept. Sci.5(5) , 393–398 (2004).
  • Majhenic AC , VenemaK, AllisonGE, MatijasiBB, RogeljI, KlaenhammerTR: DNA analysis of the genes encoding acidocin LF221 A and acidocin LF221 B, two bacteriocins produced by Lactobacillus gasseri LF221.Appl. Microbiol. Biotechnol.63(6) , 705–714 (2004).
  • Tahara T , YoshiokaS, UtsumiR, KanataniK. Isolation and partial characterization of bacteriocins produced by Lactobacillus gasseri JCM 2124. FEMS Microbiol. Lett.148(1) , 97–100 (1997).
  • Pascual LM , DanieleMB, GiordanoW, PajaroMC, BarberisIL: Purification and partial characterization of novel bacteriocin L23 produced by Lactobacillus fermentum L23.Curr. Microbiol.56(4) , 397–402 (2008).
  • Kaewsrichan J , PeeyananjarassriK, KongprasertkitJ: Selection and identification of anaerobic lactobacilli producing inhibitory compounds against vaginal pathogens.FEMS Immun. Med. Microbiol.48(1) , 75–83 (2006).
  • Kawai Y , KusnadiJ, KempermanRet al. : DNA sequencing and homologous expression of a small peptide conferring immunity to gassericin A, a circular bacteriocin produced by Lactobacillus gasseri LA39.Appl. Environ. Microbiol.75(5) , 1324–1330 (2009).
  • McGroarty JA , ReidG: Detection of a Lactobacillus substance that inhibits Escherichia coli.Can. J. Microbiol.34(8) , 974–978 (1988).
  • Turovskiy Y , LudescherRD, AroutchevaAA, FaroS, ChikindasML: Lactocin 160, a bacteriocin produced by vaginal Lactobacillus rhamnosus, targets cytoplasmic membranes of the vaginal pathogen, Gardnerella vaginalis.Probiotics Antimicrob. Proteins1(1) , 67–74 (2009).
  • Martin R , SoberonN, VaneechoutteM, FlorezAB, VazquezF, SuarezJE: Characterization of indigenous vaginal lactobacilli from healthy women as probiotic candidates.Int. Microbiol.11(4) , 261–266 (2008).
  • Corr SC , LiY, RiedelCU, O‘ToolePW, HillC, GahanCG: Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118.Proc. Natl Acad. Sci. USA104(18) , 7617–7621 (2007).
  • Reid G , McGroartyJA, AngottiR, CookRL: Lactobacillus inhibitor production against Escherichia coli and coaggregation ability with uropathogens.Can. J. Microbiol.34(3) , 344–351 (1988).
  • Ekmekci H , AslimB, OzturkS: Characterization of vaginal lactobacilli coaggregation ability with Escherichia coli.Microbiol. Immunol.53(2) , 59–65 (2009).
  • Kmet V , LucchiniF: Aggregation-promoting factor in human vaginal Lactobacillus strains.FEMS Immun. Med. Microbiol.19(2) , 111–114 (1997).
  • Atassi F , BrassartD, GrobP, GrafF, ServinAL: In vitro antibacterial activity of Lactobacillus helveticus strain KS300 against diarrhoeagenic, uropathogenic and vaginosis-associated bacteria.J. Appl. Microbiol.101(3) , 647–654 (2006).
  • Atassi F , BrassartD, GrobP, GrafF, ServinAL: Vaginal Lactobacillus isolates inhibit uropathogenic Escherichia coli.FEMS Microbiol. Lett.257(1) , 132–138 (2006).
  • Osset J , BartolomeRM, GarciaE, AndreuA: Assessment of the capacity of Lactobacillus to inhibit the growth of uropathogens and block their adhesion to vaginal epithelial cells.J. Infect. Dis.183(3) , 485–491 (2001).
  • Saunders S , BockingA, ChallisJ, ReidG: Effect of Lactobacillus challenge on Gardnerella vaginalis biofilms.Colloids Surf. B. Biointerfaces.55(2) , 138–142 (2007).
  • Chan RCY , ReidG, IrvinRT, BruceAW, CostertonJW: Competitive exclusion of uropathogens from human uroepithelial cells by Lactobacillus whole cells and cell wall fragments.Infect. Immun.47(1) , 84–89 (1985).
  • Zarate G , SantosV, Nader-MaciasME: Protective effect of vaginal Lactobacillus paracasei CRL 1289 against urogenital infection produced by Staphylococcus aureus in a mouse animal model.Infect. Dis. Obstet. Gynecol.48358 (2009).
  • Greene JD , KlaenhammerTR: Factors involved in adherence of lactobacilli to human Caco-2 cells.Appl. Environ. Microbiol.60(12) , 4487–4494 (1994).
  • Henriksson A , SzewzykR, ConwayPL: Characteristics of the adhesive determinants of Lactobacillus fermentum 104.Appl. Environ. Microbiol.57(2) , 499–502 (1991).
  • Kankainen M , PaulinL, TynkkynenSet al. : Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein.Proc. Natl Acad. Sci. USA106(40) , 17193–17198 (2009).
  • Miyoshi Y , OkadaS, UchimuraT, SatohE: A mucus adhesion promoting protein, MapA, mediates the adhesion of Lactobacillus reuteri to Caco-2 human intestinal epithelial cells.Biosci. Biotechnol. Biochem.70(7) , 1622–1628 (2006).
  • Reid G , ServinAL, BruceAW, BusscherHJ: Adhesion of three Lactobacillus strains to human urinary and intestinal epithelial cells.Microbios.75(302) , 57–65 (1993).
  • Adlerberth I , AhrneS, JohanssonML, MolinG, HansonLA, WoldAE: A mannose-specific adherence mechanism in Lactobacillus plantarum conferring binding to the human colonic cell line HT-29.Appl. Environ. Microbiol.62(7) , 2244–2251 (1996).
  • Ahrne S , NobaekS, JeppssonB, AdlerberthI, WoldAE, MolinG: The normal Lactobacillus flora of healthy human rectal and oral mucosa.J. Appl. Microbiol.85(1) , 88–94 (1998).
  • Coconnier MH , KlaenhammerTR, KerneisS, BernetMF, ServinAL: Protein-mediated adhesion of Lactobacillus acidophilus BG2FO4 on human enterocyte and mucus-secreting cell lines in culture.Appl. Environ. Microbiol.58(6) , 2034–2039 (1992).
  • Granato D , PerottiF, MassereyIet al. : Cell surface-associated lipoteichoic acid acts as an adhesion factor for attachment of Lactobacillus johnsonii La1 to human enterocyte-like Caco-2 cells.Appl. Environ. Microbiol.65(3) , 1071–1077 (1999).
  • Neeser JR , GranatoD, RouvetM, ServinA, TenebergS, KarlssonKA: Lactobacillus johnsonii La1 shares carbohydrate-binding specificities with several enteropathogenic bacteria.Glycobiology10(11) , 1193–1199 (2000).
  • Aleljung P , ShenW, RozalskaB, HellmanU, LjunghA, WadstromT: Purification of collagen-binding proteins of Lactobacillus reuteri NCIB 11951.Curr. Microbiol.28(4) , 231–236 (1994).
  • Antikainen J , AntonL, SillanpaaJ, KorhonenTK: Domains in the S-layer protein CbsA of Lactobacillus crispatus involved in adherence to collagens, laminin and lipoteichoic acids and in self-assembly.Mol. Microbiol.46(2) , 381–394 (2002).
  • Antikainen J , KuparinenV, LähteenmäkiK, KorhonenTK: Enolases from Gram-positive bacterial pathogens and commensal lactobacilli share functional similarity in virulence-associated traits.FEMS Immun. Med. Microbiol.51(3) , 526–534 (2007).
  • Castaldo C , VastanoV, SicilianoRAet al. : Surface displaced alfa-enolase of Lactobacillus plantarum is a fibronectin binding protein.Microb. Cell Fact.8 , 14 (2009).
  • Hynonen U , Westerlund-WikstromB, PalvaA, KorhonenTK: Identification by flagellum display of an epithelial cell- and fibronectin-binding function in the SlpA surface protein of Lactobacillus brevis.J. Bacteriol.184(12) , 3360–3367 (2002).
  • Kapczynski DR , MeinersmannRJ, LeeMD: Adherence of Lactobacillus to intestinal 407 cells in culture correlates with fibronectin binding.Curr. Microbiol.41(2) , 136–141 (2000).
  • Lindgren SE , SwaisgoodHE, JanolinoVGet al. : Binding of Lactobacillus reuteri to fibronectin immobilized on glass beads.Zentralbl. Bakteriol.277(4) , 519–528 (1992).
  • Roos S , AleljungP, RobertNet al. : A collagen binding protein from Lactobacillus reuteri is part of an ABC transporter system?FEMS Microbiol. Lett.144(1) , 33–38 (1996).
  • Sillanpaa J , MartinezB, AntikainenJet al. : Characterization of the collagen-binding S-layer protein CbsA of Lactobacillus crispatus.J. Bacteriol.182(22) , 6440–6450 (2000).
  • Heinemann C , vanHylckama Vlieg JE, JanssenDB, BusscherHJ, vander Mei HC, ReidG: Purification and characterization of a surface-binding protein from Lactobacillus fermentum RC-14 that inhibits adhesion of Enterococcus faecalis 1131.FEMS Microbiol. Lett.190(1) , 177–180 (2000).
  • Alander M , SatokariR, KorpelaRet al. : Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption.Appl. Env. Microbiol.65(1) , 351–354 (1999).
  • Antikainen J , KuparinenV, LähteenmäkiK, KorhonenTK: pH-dependent association of enolase and glyceraldehyde-3-phosphate dehydrogenase of Lactobacillus crispatus with the cell wall and lipoteichoic acids. Erratum in:J. Bacteriol.189(15) , 5788 (2007). J. Bacteriol.189(12) , 4539–4543 (2007).
  • Sánchez B , SchmitterJM, UrdaciMC: Identification of novel proteins secreted by Lactobacillus plantarum that bind to mucin and fibronectin.J. Mol. Microbiol. Biotechnol.17(3) , 158–162 (2009).
  • Spurbeck RR , ArvidsonCG: Lactobacillus jensenii surface associated proteins Inhibit Neisseria gonorrhoeae adherence to epithelial cells.Infect. Immun.78(7) , 3103–3111 (2010).
  • Johnson-Henry KC , HagenKE, GordonpourM, TompkinsTA, ShermanPM: Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells.Cell. Microbiol.9(2) , 356–367 (2007).
  • Toba T , VirkolaR, WesterlundBet al. : A collagen-binding S-layer protein in Lactobacillus crispatus.Appl. Environ. Microbiol.61(7) , 2467–2471 (1995).
  • Ventura M , JankovicI, WalkerDC, PridmoreRD, ZinkR: Identification and characterization of novel surface proteins in Lactobacillus johnsonii and Lactobacillus gasseri.Appl. Environ. Microbiol.68(12) , 6172–6181 (2002).
  • Boot HJ , KolenCP, PotB, KerstersK, PouwelsPH: The presence of two S-layer-protein-encoding genes is conserved among species related to Lactobacillus acidophilus.Microbiology142(9) , 2375–2384 (1996).
  • Pavlova SI , KilicAO, KilicSSet al. : Genetic diversity of vaginal lactobacilli from women in different countries based on 16S rRNA gene sequences.J. Appl. Microbiol.92(3) , 451–459 (2002).
  • Rodrigues LR , BanatIM, TeixeiraJA, OliveiraR: Biosurfactants: potential applications in medicine.J. Antimicrob. Chemother.57(4) , 609–618 (2006).
  • Singh P , CameotraSS: Potential applications of microbial surfactants in biomedical sciences.Trends Biotechnol.22(3) , 142–146 (2004).
  • Ron EZ , RosenbergE: Natural roles of biosurfactants.Environ. Microbiol.3(4) , 229–236 (2001).
  • Reid G , HeinemannC, VelraedsM, van der Mei HC, Busscher HJ: Biosurfactants produced by Lactobacillus.Meth. Enzymol.310 , 426–433 (1999).
  • Velraeds MM , vander Mei HC, ReidG, BusscherHJ: Inhibition of initial adhesion of uropathogenic Enterococcus faecalis by biosurfactants from Lactobacillus isolates.Appl. Environ. Microbiol.62(6) , 1958–1963 (1996).
  • Velraeds MM , vander Mei HC, ReidG, BusscherHJ: Inhibition of initial adhesion of uropathogenic Enterococcus faecalis to solid substrata by an adsorbed biosurfactant layer from Lactobacillus acidophilus.Urology49(5) , 790–794 (1997).
  • Velraeds MM , vande Belt-Gritter B, BusscherHJ, ReidG, vander Mei HC: Inhibition of uropathogenic biofilm growth on silicone rubber in human urine by lactobacilli – a teleologic approach.World J. Urol.18(6) , 422–426 (2000).
  • Gan BS , KimJ, ReidG, CadieuxP, HowardJC: Lactobacillus fermentum RC-14 inhibits Staphylococcus aureus infection of surgical implants in rats.J. Infect. Dis.185(9) , 1369–1372 (2002).
  • Walencka E , RózalskaS, SadowskaB, RózalskaB: The influence of Lactobacillus acidophilus-derived surfactants on staphylococcal adhesion and biofilm formation.Folia Microbiol.53(1) , 61–66 (2008).
  • Rose MC : Mucins: structure, function, and role in pulmonary diseases.Am. J. Physiol.263(4) , L413–L429 (1992).
  • Amit-Romach E , UniZ, ReifenR: Multistep mechanism of probiotic bacterium, the effect on innate immune system.Mol. Nutr. Food Res.54(2) , 277–284 (2009).
  • Kim Y , KimS-H, WhangK-Y, KimY-J, OhS: Inhibition of Escherichia coli O157:H7 attachment by interactions between lactic acid bacteria and intestinal epithelial cells.J. Microbiol. Biotechnol.18(7) , 1278–1285 (2008).
  • Mack DR , MichailS, WeiS, McDougallL, HollingsworthMA: Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression.Am. J. Physiol.276(4) , G941–G950 (1999).
  • Mack DR , AhrneS, HydeL, WeiS, HollingsworthMA: Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro.Gut52(6) , 827–833 (2003).
  • Mattar AF , TeitelbaumDH, DrongowskiRA, YongyiF, HarmonCM, CoranAG: Probiotics up-regulate MUC-2 mucin gene expression in a Caco-2 cell-culture model.Pediatr. Surg. Int.18(7) , 586–590 (2002).
  • Domino SE , HurdEA, ThomssonKAet al. : Cervical mucins carry α(1,2)fucosylated glycans that partly protect from experimental vaginal candidiasis.Glycoconj. J.26(9) , 1125–1134 (2009).
  • McGee ZA , JohnsonAP, Taylor-RobinsonD: Pathogenic mechanisms of Neisseria gonorrhoeae: observations on damage to human Fallopian tubes in organ culture by gonococci of colony type 1 or type 4.J. Infect. Dis.143(3) , 413–422 (1981).
  • Merz AJ , SoM. Interactions of pathogenic Neisseriae with epithelial cell membranes.Annu. Rev. Cell Dev. Biol.16 , 423–457 (2000).
  • Johnson-Henry KC , DonatoKA, Shen-TuG, GordanpourM, ShermanPM: Lactobacillus rhamnosus strain GG prevents enterohemorrhagic Escherichia coli O157:H7-induced changes in epithelial barrier function.Infect. Immun.76(4) , 1340–1348 (2008).
  • Qin H , ZhangZ, HangX, JiangY: L. plantarum prevents enteroinvasive Escherichia coli-induced tight junction proteins changes in intestinal epithelial cells.BMC Microbiol.9 , 63 (2009).
  • Moorthy G , MuraliMR, DevarajSN: Lactobacilli facilitate maintenance of intestinal membrane integrity during Shigella dysenteriae 1 infection in rats.Nutrition25(3) , 350–358 (2009).
  • Putaala H , SalusjarviT, NordstromMet al. : Effect of four probiotic strains and Escherichia coli O157:H7 on tight junction integrity and cyclo-oxygenase expression.Res. Microbiol.159(9–10) , 692–698 (2008).
  • Du Y , LenzJ, ArvidsonCG: Global gene expression and the role of sigma factors in Neisseria gonorrhoeae in interactions with epithelial cells.Infect. Immun.73(8) , 4834–4845 (2005).
  • Kohler T , BucklingA, vanDelden C: Cooperation and virulence of clinical Pseudomonas aeruginosa populations.Proc. Natl Acad. Sci. USA.106(15) , 6339–6344 (2009).
  • Medellin-Pena MJ , WangH, JohnsonR, AnandS, GriffithsMW: Probiotics affect virulence-related gene expression in Escherichia coli O157:H7.Appl. Environ. Microbiol.73(13) , 4259–4267 (2007).
  • Bronner S , MonteilH, PrevostG: Regulation of virulence determinants in Staphylococcus aureus: complexity and applications.FEMS Microbiol. Rev.28(2) , 183–200 (2004).
  • Laughton JM , DevillardE, HeinrichsDE, ReidG, McCormickJK: Inhibition of expression of a staphylococcal superantigen-like protein by a soluble factor from Lactobacillus reuteri.Microbiology152(4) , 1155–1167 (2006).
  • Lyons JM , MorréSA, Airo-BrownLP, PeñaAS, ItoJI: Comparison of multiple genital tract infections with Chlamydia trachomatis in different strains of female mice.J. Microbiol. Immunol. Infect.38(6) , 383–393 (2005).
  • Nader de Macías ME , deRuiz CS, Lópezde Bocanera ME, Pescede Ruiz Holgado AA: Preventive and therapeutic effects of lactobacilli on urinary tract infections in mice: clinical microbiology.Anaerobe2(2) , 85–93 (1996).
  • Pascual L , RuizF, GiordanoW, BarberisIL: Vaginal colonization and activity of the probiotic bacterium Lactobacillus fermentum L23 in a murine model of vaginal tract infection.J. Med. Microbiol.59(3) , 360–364 (2010).
  • Silva de Ruiz C , Lópezde Bocanera ME, Naderde Macías ME, Pescede Ruiz Holgado AA: Effect of lactobacilli and antibiotics on E. coli urinary infections in mice.Biol. Pharm. Bull.19(1) , 88–93 (1996).
  • Silva de Ruiz C , ReyM, Pescede Ruiz Holgado AA, Naderde Macías ME: Experimental administration of estradiol on the colonization of Lactobacillus fermentum and Escherichia coli in the urogenital tract of mice.Biol. Pharm. Bull.24(2) , 127–134 (2001).
  • Taylor-Robinson D , FurrPM: Further observations on the murine model of Mycoplasma hominis infection.J. Med. Microbiol.59(8) , 970–975 (2010).
  • Hamad M , Muta‘ebE, Abu-ShaqraQ, FraijA, Abu-ElteenK, YasinSR: Utility of the oestrogen-dependent vaginal candidosis murine model in evaluating the efficacy of various therapies against vaginal Candida albicans infection.Mycoses49(2) , 104–108 (2006).
  • Jerse AE : Experimental gonococcal genital tract infection and opacity protein expression in estradiol-treated mice.Infect. Immun.67(11) , 5699–5708 (1999).
  • Jerse AE , CrowET, BordnerANet al. : Growth of Neisseria gonorrhoeae in the female mouse genital tract does not require the gonococcal transferrin or hemoglobin receptors and may be enhanced by commensal Lactobacilli.Infect. Immun.70(5) , 2549–2558 (2002).
  • Muench DF , KuchDJ, WuHet al. : Hydrogen peroxide–producing lactobacilli Inhibit gonococci in vitro but not during experimental genital tract infection.J. Inf. Dis.199(9) , 1369–1378 (2009).
  • Hedrich HJ , BullockG: The Laboratory Mouse. Elsevier, MO, USA (2004).
  • Patton DL , Cosgrove-SweeneyYT, RabeLK, HillierSL: The pig-tailed macaque rectal model: microflora and chlamydial infection.Sex. Transm. Dis.28(7) , 363–366 (2001).
  • Patton DL , SweeneyYC, BohannonNJet al. : Effects of doxycycline and anti-inflammatory agents on experimentally induced chlamydial upper genital tract infection in female macaques.J. Infect. Dis.175 , 648–654 (1997).
  • Patton DL , SweeneyYC, RabeLK, HillierSL: The vaginal microflora of pig-tailed macaques and the effects of chlorhexidine and benzalkonium on this ecosystem. Erratum in:Sex. Transm. Dis.24(3) , 180 (1997). Sex. Transm. Dis.23(6) , 489–493 (1996).
  • Patton DL , SweeneyYTC, ClarkAM, StammWE: Antibiotic/antiinflammatory treatment of acute chlamydial upper genital tract infection in female macaques. Presented at: Third Meeting of the European Society for Chlamydial Research. Vienna, Austria, 11–14 September 1996.
  • Patton DL , KuoC, WangSP, HalbertSA: Distal tubal obstruction induced by repeated Chlamydia trachomatis salpingeal infections in pig-tailed macaques.J. Infect. Dis.155(5) , 1292–1299 (1987).
  • Patton DL , CosgroveSweeney YT, AntonioMA, RabeLK, HillierSL: Lactobacillus crispatus capsules: single-use safety study in the Macaca nemestrina model.Sex. Transm. Dis.30(7) , 568–570 (2003).
  • Chandler FWJ , KrausSJ: Animal model of human disease. Gonorrhea.Am. J. Path.82(2) , 437–440 (1976).
  • Herthelius M , GorbachSL, MöllbyR, NordCE, PetterssonL, WinbergJ: Elimination of vaginal colonization with Escherichia coli by administration of indigenous flora.Infect. Immun.57(8) , 2447–2451 (1989).
  • Ozkinay E , TerekMC, YayciM, KaiserR, GrobP, TuncayG: The effectiveness of live lactobacilli in combination with low dose oestriol (Gynoflor) to restore the vaginal flora after treatment of vaginal infections.BJOG112(2) , 234–240 (2005).
  • Anukam K , OsazuwaE, AhonkhaiIet al. : Augmentation of antimicrobial metronidazole therapy of bacterial vaginosis with oral probiotic Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14: randomized, double-blind, placebo controlled trial.Microbes Infect.8(6) , 1450–1454 (2006).
  • Anukam KC , OsazuwaE, OsemeneGI, EhigiagbeF, BruceAW, ReidG: Clinical study comparing probiotic Lactobacillus GR-1 and RC-14 with metronidazole vaginal gel to treat symptomatic bacterial vaginosis.Microbes Infect.8(12–13) , 2772–2776 (2006).
  • Reid G , CharbonneauD, ErbJet al. : Oral use of Lactobacillus rhamnosus GR-1 and L. fermentum RC-14 significantly alters vaginal flora: randomized, placebo-controlled trial in 64 healthy women.FEMS Immunol. Med. Microbiol.35(2) , 131–134 (2003).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.