Vaginal lactobacilli reduce Neisseria gonorrhoeae viability through multiple strategies: An in vitro study

Frontiers in Cellular and Infection Microbiology

Volumn 7, Issue DEC, 2017, Pages

  Foschi, Claudio ^a   Salvo, Melissa ^a   Cevenini, Roberto ^a   Parolin, Carola ^a   Vitali, Beatrice ^a   Marangoni, Antonella ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Gonococcus; Gonorrhea; Lactobacillus; Probiotics; STIs

Indexed keywords

HYDROCHLORIC ACID; LACTIC ACID; METHANOL; PROTEINASE K; SURFACTANT;

ARTICLE; CELL VIABILITY ASSAY; CONTROLLED STUDY; GONORRHEA; IN VITRO STUDY; LACTOBACILLUS; NEISSERIA GONORRHOEAE; NONHUMAN; STEREOMICROSCOPY; UROGENITAL TRACT INFECTION; ANTIBIOSIS; FEMALE; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PH; TIME FACTOR; VAGINA;

ANTIBIOSIS; FEMALE; HUMANS; HYDROGEN-ION CONCENTRATION; LACTIC ACID; LACTOBACILLUS; MICROBIAL VIABILITY; NEISSERIA GONORRHOEAE; SURFACE-ACTIVE AGENTS; TIME FACTORS; VAGINA;

EID: 85037050656     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2017.00502     Document Type: Article

References (52)

1. Abbai, N. S., Reddy, T., and Ramjee, G. (2016). Prevalent bacterial vaginosis infection-a risk factor for incident sexually transmitted infections in women in Durban, South Africa. Int. J. STD AIDS 27, 1283-1288. doi: 10.1177/0956462415616038
2. Barrons, R., and Tassone, D. (2008). Use of Lactobacillus probiotics for bacterial genitourinary infections in women: a review. Clin. Ther. 30, 453-468. doi: 10.1016/j.clinthera.2008.03.013
3. Bergsson, G., Steingrímsson, O., and Thormar, H. (1999). In vitro susceptibilities of Neisseria gonorrhoeae to fatty acids and monoglycerides. Antimicrob. Agents Chemother. 43, 2790-2792
4. Bergström, S., Robbins, K., Koomey, J. M., and Swanson, J. (1986). Piliation control mechanisms in Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. U.S.A. 83, 3890-3894. doi: 10.1073/pnas.83.11.3890
5. Bolton, M., van der Straten, A., and Cohen, C. R. (2008). Probiotics: potential to prevent HIV and sexually transmitted infections in women. Sex. Transm. Dis. 35, 214-225. doi: 10.1097/OLQ.0b013e31815b017a
6. Borges, S., Silva, J., and Teixeira, P. (2014). The role of lactobacilli and probiotics in maintaining vaginal health. Arch. Gynecol. Obstet. 289, 479-489. doi: 10.1007/s00404-013-3064-9
7. Boris, S., Suárez, J. E., and Barbés, C. (1997). Characterization of the aggregation promoting factor from Lactobacillus gasseri, avaginal isolate. J. Appl. Microbiol. 83, 413-420. doi: 10.1046/j.1365-2672.1997.00250.x
8. Breshears, L. M., Edwards, V. L., Ravel, J., and Peterson, M. L. (2015). Lactobacillus crispatus inhibits growth of Gardnerella vaginalis and Neisseria gonorrhoeae on a porcine vaginal mucosa model. BMC Microbiol. 15:276. doi: 10.1186/s12866-015-0608-0
9. Calonghi, N., Parolin, C., Sartor, G., Verardi, L., Giordani, B., Frisco, G., et al. (2017). Interaction of vaginal Lactobacillus strains with HeLa cells plasma membrane. Benef. Microbes 8, 625-633. doi: 10.3920/BM2016.0212
10. Chun, H. M., Carpenter, R. J., Macalino, G. E., and CrumCianflone, N. F. (2013). The role of sexually transmitted infections in HIV-1 Progression: a comprehensive review of the literature. J. Sex. Transm. Dis. 2013:176459. doi: 10.1155/2013/176459
11. Detels, R., Green, A. M., Klausner, J. D., Katzenstein, D., Gaydos, C., Handsfield, H., et al. (2011). The incidence and correlates of symptomatic and asymptomatic Chlamydia trachomatis and Neisseria gonorrhoeae infections in selected populations in five countries. Sex. Transm. Dis. 38, 503-509. doi: 10.1097/OLQ.0b013e318206c288
12. European Centre for Disease Prevention Control (ECDC) (2016). Gonococcal Antimicrobial Susceptibility Surveillance in Europe, 2014. Stockholm: ECDC. Available online at: https://ecdc.europa.eu/sites/portal/files/media/en/publications/Publications/gonococcal-antimicrobial-susceptibility-surveillance-Europe-2014.pdf
13. European Centre for Disease Prevention Control (ECDC) (2015). Sexually Transmitted Infections in Europe, 2013. Stockholm: ECDC. Available online at: https://ecdc.europa.eu/sites/portal/files/media/en/publications/Publications/sexual-transmitted-infections-europe-surveillance-report-2013.pdf
14. Fifer, H., Natarajan, U., Jones, L., Alexander, S., Hughes, G., Golparian, D., et al. (2016). Failure of dual antimicrobial therapy in treatment of gonorrhea. N. Engl. J. Med. 374, 2504-2506. doi: 10.1056/NEJMc1512757
15. Foschi, C., Laghi, L., Parolin, C., Giordani, B., Compri, M., Cevenini, R., et al. (2017). Novel approaches for the taxonomic and metabolic characterization of lactobacilli: integration of 16S rRNA gene sequencing with MALDI-TOF MS and 1H-NMR. PLoS ONE 12:e0172483. doi: 10.1371/journal.pone.0172483
16. Graver, M. A., and Wade, J. J. (2011). The role of acidification in the inhibition of Neisseria gonorrhoeae by vaginal lactobacilli during anaerobic growth. Ann. Clin. Microbiol. Antimicrob. 10:8. doi: 10.1186/1476-0711-10-8
17. Johnson, L. F., and Lewis, D. A. (2008). The effect of genital tract infections on HIV-1 shedding in the genital tract: a systematic review and meta-analysis. Sex. Transm. Dis. 35, 946-959. doi: 10.1097/OLQ.0b013e3181812d15
18. Kaewsrichan, J., Peeyananjarassri, K., and Kongprasertkit, J. (2006). Selection and identification of anaerobic lactobacilli producing inhibitory compounds against vaginal pathogens. FEMS Immunol. Med. Microbiol. 48, 75-83. doi: 10.1111/j.1574-695X.2006.00124.x
19. Macklaim, J. M., Fernandes, A. D., Di Bella, J. M., Hammond, J. A., Reid, G., and Gloor, G. B. (2013). Comparative meta-RNAseq of the vaginal microbiota and differential expression by Lactobacillus iners in health and dysbiosis. Microbiome 1:12. doi: 10.1186/2049-2618-1-12
20. Merghni, A., Dallel, I., Noumi, E., Kadmi, Y., Hentati, H., Tobji, S., et al. (2017). Antioxidant and antiproliferative potential of biosurfactants isolated from Lactobacillus casei and their anti-biofilm effect in oral Staphylococcus aureus strains. Microb. Pathog. 104, 84-89. doi: 10.1016/j.micpath.2017.01.017
21. Morgan, M. K., and Decker, C. F. (2016). Gonorrhea. Dis. Mon. 62, 260-268. doi: 10.1016/j.disamonth.2016.03.009
22. Morin, A., Saheb, S. A., Bisaillon, J. G., Beaudet, R., and Sylvestre, M. (1980). In vitro inhibition of Neisseria gonorrhoeae growth by strict anaerobes. Infect. Immun. 28, 766-770
23. Morse, S. A., and Hebeler, B. H. (1978). Effect of pH on the growth and glucose metabolism of Neisseria gonorrhoeae. Infect. Immun. 21, 87-95
24. Nardini, P., ñahui Palomino, R. A., Parolin, C., Laghi, L., Foschi, C., Cevenini, R., et al. (2016). Lactobacillus crispatus inhibits the infectivity of Chlamydia trachomatis elementary bodies, in vitro study. Sci. Rep. 6:29024. doi: 10.1038/srep29024
25. Nunn, K. L., Wang, Y. Y., Harit, D., Humphrys, M. S., Ma, B., Cone, R., et al. (2015). Enhanced Trapping of HIV-1 by human cervicovaginal mucus is associated with Lactobacillus crispatus-dominant microbiota. mBio 6:e01084-15. doi: 10.1128/mBio.01084-15
26. Ohnishi, M., Golparian, D., Shimuta, K., Saika, T., Hoshina, S., Iwasaku, K., et al. (2011). Is Neisseria gonorrhoeae initiating a future era of untreatable gonorrhea?: detailed characterization of the first strain with high-level resistance to ceftriaxone. Antimicrob. Agents Chemother. 55, 3538-3545. doi: 10.1128/AAC.00325-11
27. ñahui Palomino, R. A., Zicari, S., Vanpouille, C., Vitali, B., and Margolis, L. (2017). Vaginal Lactobacillus Inhibits HIV-1 replication in human tissues Ex Vivo. Front. Microbiol. 8:906. doi: 10.3389/fmicb.2017.00906
28. Parolin, C., Marangoni, A., Laghi, L., Foschi, C., ñahui Palomino, R. A., Calonghi, N., et al. (2015). Isolation of vaginal lactobacilli and characterization of anti-Candida activity. PLoS ONE 10:e0131220. doi: 10.1371/journal.pone.0131220
29. Ravel, J., Gajer, P., Abdo, Z., Schneider, G. M., Koenig, S. S., McCulle, S. L., et al. (2011). Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. U.S.A. 108(Suppl. 1), 4680-4687. doi: 10.1073/pnas.1002611107
30. Ruíz, F. O., Pascual, L., Giordano, W., and Barberis, L. (2015). Bacteriocins and other bioactive substances of probiotic lactobacilli as biological weapons against Neisseria gonorrhoeae. Pathog. Dis. 73:ftv013. doi: 10.1093/femspd/ftv013
31. Sambanthamoorthy, K., Feng, X., Patel, R., Patel, S., and Paranavitana, C. (2014). Antimicrobial and antibiofilm potential of biosurfactants isolated from lactobacilli against multi-drug-resistant pathogens. BMC Microbiol. 14:197. doi: 10.1186/1471-2180-14-197
32. Satpute, S. K., Kulkarni, G. R., Banpurkar, A. G., Banat, I. M., Mone, N. S., Patil, R. H., et al. (2016). Biosurfactant/s from lactobacilli species: properties, challenges and potential biomedical applications. J. Basic Microbiol. 56, 1140-1158. doi: 10.1002/jobm.201600143
33. Schoolnik, G. K., Fernandez, R., Tai, J. Y., Rothbard, J., and Gotschlich, E. C. (1984). Gonococcal pili. Primary structure and receptor binding domain. J. Exp. Med. 159, 1351-1370. doi: 10.1084/jem.159.5.1351
34. Sheung, A., Rebbapragada, A., Shin, L. Y., Dobson-Belaire, W., Kimani, J., Ngugi, E., et al. (2008). Mucosal Neisseria gonorrhoeae coinfection during HIV acquisition is associated with enhanced systemic HIV-specific CD8 T-cell responses. AIDS 22, 1729-1737. doi: 10.1097/QAD.0b013e32830baf5e
35. Siroli, L., Patrignani, F., Serrazanetti, D. I., Parolin, C., ñahui Palomino, R. A., Vitali, B., et al. (2017). Determination of antibacterial and technological properties of vaginal lactobacilli for their potential application in dairy products. Front. Microbiol. 8:166. doi: 10.3389/fmicb.2017.00166
36. Smith, H., Tang, C. M., and Exley, R. M. (2007). Effect of host lactate on gonococci and meningococci: new concepts on the role of metabolites in pathogenicity. Infect. Immun. 75, 4190-4198. doi: 10.1128/IAI.00117-07
37. Smith, H., Yates, E. A., Cole, J. A., and Parsons, N. J. (2001). Lactate stimulation of gonococcal metabolism in media containing glucose: mechanism, impact on pathogenicity, and wider implications for other pathogens. Infect. Immun. 69, 6565-6572. doi: 10.1128/IAI.69.11.6565-6572.2001
38. Spurbeck, R. R., and Arvidson, C. G. (2008). Inhibition of Neisseria gonorrhoeae epithelial cell interactions by vaginal Lactobacillus species. Infect. Immun. 76, 3124-3130. doi: 10.1128/IAI.00101-08
39. Spurbeck, R. R., and Arvidson, C. G. (2010). Lactobacillus jensenii surface-associated proteins inhibit Neisseria gonorrhoeae adherence to epithelial cells. Infect. Immun. 78, 3103-3111. doi: 10.1128/IAI.01200-09
40. Spurbeck, R. R., and Arvidson, C. G. (2011). Lactobacilli at the front line of defense against vaginally acquired infections. Future Microbiol. 6, 567-582. doi: 10.2217/fmb.11.36
41. St Amant, D. C., Valentin-Bon, I. E., and Jerse, A. E. (2002). Inhibition of Neisseria gonorrhoeae by Lactobacillus species that are commonly isolated from the female genital tract. Infect. Immun. 70, 7169-7171. doi: 10.1128/IAI.70.12.7169-7171.2002
42. Swanson, J. (1978). Studies on gonococcus infection. XIV. Cell wall protein differences among color/opacity colony variants of Neisseria gonorrhoeae. Infect. Immun. 21, 292-302
43. Swanson, J., Kraus, S. J., and Gotschlich, E. C. (1971). Studies on gonococcus infection. I. Pili and zones of adhesion: their relation to gonococcal growth patterns. J. Exp. Med. 134, 886-906. doi: 10.1084/jem.134.4.886
44. Unemo, M. (2015). Current and future antimicrobial treatment of gonorrhoea-the rapidly evolving Neisseria gonorrhoeae continues to challenge. BMC Infect. Dis. 15:364. doi: 10.1186/s12879-015-1029-2
45. Unemo, M., Golparian, D., Nicholas, R., Ohnishi, M., Gallay, A., and Sednaoui, P. (2012). High-level cefixime-and ceftriaxone-resistant Neisseria gonorrhoeae in France: novel penA mosaic allele in a successful international clone causes treatment failure. Antimicrob. Agents Chemother. 56, 1273-1280. doi: 10.1128/AAC.05760-11
46. Vielfort, K., Sjölinder, H., Roos, S., Jonsson, H., and Aro, H. (2008). Adherence of clinically isolated lactobacilli to human cervical cells in competition with Neisseria gonorrhoeae. Microbes Infect. 10, 1325-1334. doi: 10.1016/j.micinf.2008.07.032
47. Vitali, B., Abruzzo, A., Parolin, C., Palomino, R. A., Dalena, F., Bigucci, F., et al. (2016). Association of Lactobacillus crispatus with fructo-oligosaccharides and ascorbic acid in hydroxypropyl methylcellulose vaginal insert. Carbohydr. Polym. 136, 1161-1169. doi: 10.1016/j.carbpol.2015.10.035
48. World Health Organization (WHO) (2012). Global Incidence and Prevalence of Selected Curable Sexually Transmitted Infections-2008. Geneva: World Health Organization. Available online at: http://www.who.int/reproductivehealth/publications/rtis/stisestimates/en/
49. Wiesenfeld, H. C., Hillier, S. L., Krohn, M. A., Landers, D. V., and Sweet, R. L. (2003). Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clin. Infect. Dis. 36, 663-668. doi: 10.1086/367658
50. Workowski, K. A., and Bolan, G. A. (2015). Centers for disease control and prevention, sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm. Rep. 64, 1-137
51. Yates, E., Gao, L., Woodcock, N., Parsons, N., Cole, J., and Smith, H. (2000). In a medium containing glucose, lactate carbon is incorporated by gonococci predominantly into fatty acids and glucose carbon incorporation is increased: implications regarding lactate stimulation of metabolism. Int. J. Med. Microbiol. 290, 627-639. doi: 10.1016/S1438-4221(00)80012-0
52. Zheng, H. Y., Alcorn, T. M., and Cohen, M. D. (1994). Effects of H2O2 producing lactobacilli on Neisseria gonorrhoeae growth and catalase activity. J. Infect. Dis. 170, 1209-1215. doi: 10.1093/infdis/170.5.1209