Vaginal Microbiota and HPV Infection: Novel Mechanistic Insights and Therapeutic Strategies

References

• Small W Jr., Bacon MA, Bajaj A, et al. Cervical cancer: a global health crisis. Cancer. 2017;123(13):2404–2412. doi:10.1002/cncr.v123.1328464289
   PubMed Web of Science ®Google Scholar
• Bzhalava D, Muhr LS, Lagheden C, et al. Deep sequencing extends the diversity of human papillomaviruses in human skin. Sci Rep. 2014;4:5807. doi:10.1038/srep0580725055967
   PubMed Web of Science ®Google Scholar
• N M, Bosch FX, de Sanjosé S, et al. International agency for research on cancer multicenter cervical cancer study group.: epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003;348(6):10. doi:10.1056/NEJMicm020037
   Web of Science ®Google Scholar
• Zur Hausen H. Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer. 2002;2(5):342–350. doi:10.1038/nrc79812044010
   PubMed Web of Science ®Google Scholar
• Wilting SM, Steenbergen RDM. Molecular events leading to HPV-induced high grade neoplasia. Papillomavirus Res. 2016;2:85–88. doi:10.1016/j.pvr.2016.04.00329074190
   PubMed Web of Science ®Google Scholar
• Consortium TH. Project M. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–214.22699609
   PubMed Web of Science ®Google Scholar
• Mitra A, MacIntyre DA, Marchesi JR, Lee YS, Bennett PR, Kyrgiou M. The vaginal microbiota, human papillomavirus infection and cervical intraepithelial neoplasia: what do we know and where are we going next? Microbiome. 2016;4(1):58. doi:10.1186/s40168-016-0203-027802830
   PubMed Web of Science ®Google Scholar
• Seo SS, Oh HY, Lee JK, Kong JS, Lee DO, Kim MK. Combined effect of diet and cervical microbiome on the risk of cervical intraepithelial neoplasia. Clin Nutr. 2016;35(6):1434–1441. doi:10.1016/j.clnu.2016.03.01927075319
   PubMed Web of Science ®Google Scholar
• Audirac-Chalifour A, Torres-Poveda K, Bahena-Roman M, et al. Cervical microbiome and cytokine profile at various stages of cervical cancer: a pilot study. PLoS One. 2016;11(4):e0153274. doi:10.1371/journal.pone.015327427115350
   PubMed Web of Science ®Google Scholar
• Oh HY, Kim BS, Seo SS, et al. The association of uterine cervical microbiota with an increased risk for cervical intraepithelial neoplasia in Korea. Clin Microbiol Infect 2015;21(7):674e671–679. doi:10.1016/j.cmi.2015.02.026
   Google Scholar
• Mitra A, MacIntyre DA, Lee YS, et al. Cervical intraepithelial neoplasia disease progression is associated with increased vaginal microbiome diversity. Sci Rep. 2015;5:16865. doi:10.1038/srep1686526574055
   PubMed Web of Science ®Google Scholar
• Brotman RM, Shardell MD, Gajer P, et al. Interplay between the temporal dynamics of the vaginal microbiota and human papillomavirus detection. J Infect Dis. 2014;210(11):1723–1733. doi:10.1093/infdis/jiu33024943724
   PubMed Web of Science ®Google Scholar
• Nardis C, Mosca L, Mastromarino P. Vaginal microbiota and viral sexually transmitted diseases. Ann Ig. 2013;25(5):14.
   Google Scholar
• Lee JE, Lee S, Lee H, et al. Association of the vaginal microbiota with human papillomavirus infection in a Korean twin cohort. PLoS One. 2013;8(5):e63514. doi:10.1371/journal.pone.006351423717441
   PubMed Web of Science ®Google Scholar
• Brotman RM. Vaginal microbiome and sexually transmitted infections: an epidemiologic perspective. J Clin Invest. 2011;121(12):4610–4617. doi:10.1172/JCI5717222133886
   PubMed Web of Science ®Google Scholar
• Martin DH. The microbiota of the vagina and its influence on women’s health and disease. Am J Med Sci. 2012;343(1):2–9. doi:10.1097/MAJ.0b013e31823ea22822143133
   PubMed Web of Science ®Google Scholar
• Lamont RF, Sobel JD, Akins RA, et al. The vaginal microbiome: new information about genital tract flora using molecular based techniques. BJOG. 2011;118(5):533–549. doi:10.1111/j.1471-0528.2010.02840.x21251190
   PubMed Web of Science ®Google Scholar
• Ravel JGP, Abdo Z, Schneider GM, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):8. doi:10.1073/pnas.1002611107
   Web of Science ®Google Scholar
• Goldstein EJ, Tyrrell KL, Citron DM. Lactobacillus species: taxonomic complexity and controversial susceptibilities. Clin Infect Dis. 2015;60(Suppl 2):S98–107. doi:10.1093/cid/civ07225922408
   PubMed Web of Science ®Google Scholar
• Reid G, Younes JA, Van der Mei HC, Gloor GB, Knight R, Busscher HJ. Microbiota restoration: natural and supplemented recovery of human microbial communities. Nat Rev Microbiol. 2011;9(1):27–38. doi:10.1038/nrmicro247321113182
   PubMed Web of Science ®Google Scholar
• Swidsinski A, Mendling W, Loening-Baucke V, et al. Adherent biofilms in bacterial vaginosis. Obstet Gynecol. 2005;106:11. doi:10.1097/01.AOG.0000183594.45524.d2
   Web of Science ®Google Scholar
• Barbonetti A, Cinque B, Vassallo MR, et al. Effect of vaginal probiotic lactobacilli on in vitro-induced sperm lipid peroxidation and its impact on sperm motility and viability. Fertil Steril. 2011;95(8):2485–2488. doi:10.1016/j.fertnstert.2011.03.06621497805
   PubMed Web of Science ®Google Scholar
• Ramos AN, Sesto Cabral ME, Arena ME, Arrighi CF, Arroyo Aguilar AA, Valdez JC. Compounds from lactobacillus plantarum culture supernatants with potential pro-healing and anti-pathogenic properties in skin chronic wounds. Pharm Biol. 2015;53(3):350–358. doi:10.3109/13880209.2014.92003725347359
   PubMed Web of Science ®Google Scholar
• Aroutcheva A, Gariti D, Simon M, et al. Defense factors of vaginal lactobacilli. Am J Obstet Gynecol. 2001;185(2):375–379. doi:10.1067/mob.2001.11586711518895
   PubMed Web of Science ®Google Scholar
• Valenti P, Rosa L, Capobianco D, et al. Role of lactobacilli and lactoferrin in the mucosal cervicovaginal defense. Front Immunol. 2018;9:376. doi:10.3389/fimmu.2018.0037629545798
   PubMed Web of Science ®Google Scholar
• Gillet E, Meys JF, Verstraelen H, et al. Bacterial vaginosis is associated with uterine cervical human papillomavirus infection: a meta-analysis. BMC Infect Dis. 2011;11:10. doi:10.1186/1471-2334-11-1021223574
   PubMed Web of Science ®Google Scholar
• Gillet E, Meys JF, Verstraelen H, et al. Association between bacterial vaginosis and cervical intraepithelial neoplasia: systematic review and meta-analysis. PLoS One. 2012;7(10):e45201. doi:10.1371/journal.pone.004520123056195
   PubMed Web of Science ®Google Scholar
• Guo YL, You K, Qiao J, Zhao YM, Geng L. Bacterial vaginosis is conducive to the persistence of HPV infection. Int J STD AIDS. 2012;23(8):581–584. doi:10.1258/ijsa.2012.01134222930296
   PubMed Web of Science ®Google Scholar
• Smith SB, Ravel J. The vaginal microbiota, host defence and reproductive physiology. J Physiol. 2017;595(2):451–463. doi:10.1113/tjp.2017.595.issue-227373840
   PubMed Web of Science ®Google Scholar
• Iwasaki A. Mucosal dendritic cells. Annu Rev Immunol. 2007;25:381–418. doi:10.1146/annurev.immunol.25.022106.14163417378762
   PubMed Web of Science ®Google Scholar
• Kumamoto Y, Iwasaki A. Unique features of antiviral immune system of the vaginal mucosa. Curr Opin Immunol. 2012;24(4):411–416. doi:10.1016/j.coi.2012.05.00622673876
   PubMed Web of Science ®Google Scholar
• Duluc D, Gannevat J, Anguiano E, et al. Functional diversity of human vaginal APC subsets in directing T-cell responses. Mucosal Immunol. 2013;6(3):626–638. doi:10.1038/mi.2012.10423131784
   PubMed Web of Science ®Google Scholar
• Duluc D, Banchereau R, Gannevat J, et al. Transcriptional fingerprints of antigen-presenting cell subsets in the human vaginal mucosa and skin reflect tissue-specific immune microenvironments. Genome Med. 2014;6(11):98. doi:10.1186/s13073-014-0098-y25520755
   PubMed Web of Science ®Google Scholar
• Kang JY, Lee JO. Structural biology of the toll-like receptor family. Annu Rev Biochem. 2011;80:917–941. doi:10.1146/annurev-biochem-052909-14150721548780
   PubMed Web of Science ®Google Scholar
• Neth O, Jack DL, Dodds AW, Holzel H, Klein NJ, Turner MW. Mannose-binding lectin binds to a range of clinically relevant microorganisms and promotes complement deposition. Infect Immun. 2000;68(2):688–693. doi:10.1128/IAI.68.2.688-693.200010639434
   PubMed Web of Science ®Google Scholar
• Wang YY, Kannan A, Nunn KL, et al. IgG in cervicovaginal mucus traps HSV and prevents vaginal herpes infections. Mucosal Immunol. 2014;7(5):1036–1044. doi:10.1038/mi.2013.12024496316
   PubMed Web of Science ®Google Scholar
• Wilson SS, Wiens ME, Smith JG. Antiviral mechanisms of human defensins. J Mol Biol. 2013;425(24):4965–4980. doi:10.1016/j.jmb.2013.09.03824095897
   PubMed Web of Science ®Google Scholar
• Reid G. Cervicovaginal microbiomes threats and possibilities. Trends Endocrinol Metab. 2016;27(7):9. doi:10.1016/j.tem.2016.04.004
   Web of Science ®Google Scholar
• Alvarez KLF, Beldi M, Sarmanho F, et al. Local and systemic immunomodulatory mechanisms triggered by human papillomavirus transformed cells: a potential role for G-CSF and neutrophils. Sci Rep. 2017;7(1). doi:10.1038/s41598-017-09079-3
   Web of Science ®Google Scholar
• Rose WA 2nd, McGowin CL, Spagnuolo RA, Eaves-Pyles TD, Popov VL, Pyles RB. Commensal bacteria modulate innate immune responses of vaginal epithelial cell multilayer cultures. PLoS One. 2012;7(3):e32728. doi:10.1371/journal.pone.003272822412914
   PubMed Web of Science ®Google Scholar
• Anahtar MN, Byrne EH, Doherty KE, et al. Cervicovaginal bacteria are a major modulator of host inflammatory responses in the female genital tract. Immunity. 2015;42(5):965–976. doi:10.1016/j.immuni.2015.04.01925992865
   PubMed Web of Science ®Google Scholar
• Ebner S, Smug LN, Kneifel W, Salminen SJ, Sanders ME. Probiotics in dietary guidelines and clinical recommendations outside the European Union. World J Gastroenterol. 2014;20(43):16095–16100. doi:10.3748/wjg.v20.i43.1609525473160
   PubMed Web of Science ®Google Scholar
• Pan W, Kang Y. Gut microbiota and chronic kidney disease: implications for novel mechanistic insights and therapeutic strategies. Int Urol Nephrol. 2018;50(2):289–299. doi:10.1007/s11255-017-1689-528849345
   PubMed Web of Science ®Google Scholar
• Behnsen J, Deriu E, Sassone-Corsi M, Raffatellu M. Probiotics: properties, examples, and specific applications. Cold Spring Harb Perspect Med. 2013;3(3):a010074. doi:10.1101/cshperspect.a01007423457295
   PubMed Web of Science ®Google Scholar
• Verhoeven V, Renard N, Makar A, et al. Probiotics enhance the clearance of human papillomavirus-related cervical lesions: a prospective controlled pilot study. Eur J Cancer. 2013;22(1):46–51. doi:10.1097/CEJ.0b013e328355ed23
   Web of Science ®Google Scholar
• Ceccarelli G, Cavallari EN, Savinelli S, et al. Clearance of human papillomavirus related anal condylomas after oral and endorectal multistrain probiotic supplementation in an HIV positive male: a case report. Medicine. 2018;97(16):e0329. doi:10.1097/MD.000000000001032929668581
   PubMed Web of Science ®Google Scholar
• Burton JP, Reid G. Evaluation of the bacterial vaginal flora of 20 postmenopausal women by direct (Nugent score) and molecular (polymerase chain reaction and denaturing gradient gel electrophoresis) techniques. J Infect Dis. 2002;186(12):1770–1780. doi:10.1086/jid.2002.186.issue-1212447763
   PubMed Web of Science ®Google Scholar
• Zhou X, Hansmann MA, Davis CC, et al. The vaginal bacterial communities of Japanese women resemble those of women in other racial groups. FEMS Immunol Med Microbiol. 2010;58(2):169–181. doi:10.1111/j.1574-695X.2009.00618.x19912342
   PubMedGoogle Scholar
• Gajer P, Brotman RM, Bai G, et al. Temporal dynamics of the human vaginal microbiota. Sci Transl Med. 2012;4(132):132ra152. doi:10.1126/scitranslmed.3003605
   Web of Science ®Google Scholar
• Macklaim JM, Clemente JC, Knight R, Gloor GB, Reid G. Changes in vaginal microbiota following antimicrobial and probiotic therapy. Microb Ecol Health Dis. 2015;26:27799. doi:10.3402/mehd.v26.2779926282697
   PubMedGoogle Scholar
• Reid G, Beuerman D, Heinemann C, Bruce AW. Probiotic lactobacillus dose required to restore and maintain a normal vaginal flora. FEMS Immunol Med Microbiol. 2001;32(1):37–41. doi:10.1111/fim.2001.32.issue-111750220
   PubMedGoogle Scholar
• Reid G, Bruce AW, Fraser N, Heinemann C, Owen J, Henning B. Oral probiotics can resolve urogenital infections. FEMS Immunol Med Microbiol. 2001;30(1):49–52. doi:10.1111/fim.2001.30.issue-111172991
   PubMedGoogle Scholar
• Reid G, Charbonneau D, Erb J, et 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. 2003;35(2):131–134. doi:10.1016/S0928-8244(02)00465-012628548
   PubMedGoogle Scholar
• Morelli L, Zonenenschain D, Del Piano M, Cognein P. Utilization of the intestinal tract as a delivery system for urogenital probiotics. J Clin Gastroenterol. 2004;38(6 Suppl):S107–110. doi:10.1097/01.mcg.0000128938.32835.9815220672
   PubMed Web of Science ®Google Scholar
• Hanson L, VandeVusse L, Jerme M, Abad CL, Safdar N. Probiotics for treatment and prevention of urogenital infections in women: a systematic review. J. Midwifery Women’s Health. 2016;61(3):339–355. doi:10.1111/jmwh.2016.61.issue-327218592
   PubMed Web of Science ®Google Scholar
• Andreyev J. Gastrointestinal complications of pelvic radiotherapy: are they of any importance? Gut. 2005;54(8):1051–1054. doi:10.1136/gut.2004.06259616009675
   PubMed Web of Science ®Google Scholar
• Chase D, Goulder A, Zenhausern F, Monk B, Herbst-Kralovetz M. The vaginal and gastrointestinal microbiomes in gynecologic cancers: a review of applications in etiology, symptoms and treatment. Gynecol Oncol. 2015;138(1):190–200. doi:10.1016/j.ygyno.2015.04.03625957158
   PubMed Web of Science ®Google Scholar
• Griffin C. Probiotics in obstetrics and gynaecology. Aust N Z J Obstet Gynaecol. 2015;55(3):201–209. doi:10.1111/ajo.2015.55.issue-326052924
   PubMed Web of Science ®Google Scholar
• Bayerdorffer E, Neubauer A, Rudolph B, et al. Regression of primary gastric lymphoma of mucosa-associated lymphoid tissue type after cure of helicobacter pylori infection. Lancet. 1995;345(8965):1591–1594.7783535
   PubMed Web of Science ®Google Scholar
• Rauch M, Lynch SV. The potential for probiotic manipulation of the gastrointestinal microbiome. Curr Opin Biotechnol. 2012;23(2):192–201. doi:10.1016/j.copbio.2011.11.00422137452
   PubMed Web of Science ®Google Scholar
• Viaud S, Saccheri F, Mignot G, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science. 2013;342(6161):971–976. doi:10.1126/science.124053724264990
   PubMed Web of Science ®Google Scholar
• Iida N, Dzutsev A, Stewart CA, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 2013;342(6161):967–970. doi:10.1126/science.124052724264989
   PubMed Web of Science ®Google Scholar
• Vetizou M, Pitt JM, Daillere R, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015;350(6264):1079–1084. doi:10.1126/science.aad132926541610
   PubMed Web of Science ®Google Scholar
• Zamarin D, Jazaeri AA. Leveraging immunotherapy for the treatment of gynecologic cancers in the era of precision medicine. Gynecol Oncol. 2016;141(1):86–94. doi:10.1016/j.ygyno.2015.12.03027016233
   PubMed Web of Science ®Google Scholar
• Li J, Sung CY, Lee N, et al. Probiotics modulated gut microbiota suppresses hepatocellular carcinoma growth in mice. Proc Natl Acad Sci U S A. 2016;113(9):E1306–E1315. doi:10.1073/pnas.151818911326884164
   PubMed Web of Science ®Google Scholar
• Nami Y, Abdullah N, Haghshenas B, Radiah D, Rosli R, Khosroushahi AY. Assessment of probiotic potential and anticancer activity of newly isolated vaginal bacterium lactobacillus plantarum 5BL. Microbiol Immunol. 2014;58(9):492–502. doi:10.1111/mim.v58.925039934
   PubMed Web of Science ®Google Scholar
• Nami Y, Abdullah N, Haghshenas B, Radiah D, Rosli R, Yari Khosroushahi A. A newly isolated probiotic enterococcus faecalis strain from vagina microbiota enhances apoptosis of human cancer cells. J Appl Microbiol. 2014;117(2):498–508. doi:10.1111/jam.2014.117.issue-224775273
   PubMed Web of Science ®Google Scholar
• Wang KD, Xu DJ, Wang BY, Yan DH, Lv Z, Su JR. Inhibitory effect of vaginal lactobacillus supernatants on cervical cancer cells. Probiotics Antimicrob Proteins. 2017;10(2):236–242.
   Web of Science ®Google Scholar
• Eslami S, Hadjati J, Motevaseli E, et al. Lactobacillus crispatus strain SJ-3C-US induces human dendritic cells (DCs) maturation and confers an anti-inflammatory phenotype to DCs. APMIS. 2016;124(8):697–710. doi:10.1111/apm.2016.124.issue-827245496
   PubMed Web of Science ®Google Scholar