دورية أكاديمية
أعرض في EDS

Biogenic Amines Increase the Odds of Bacterial Vaginosis and Affect the Growth of and Lactic Acid Production by Vaginal Lactobacillus spp.

التفاصيل البيبلوغرافية
العنوان: Biogenic Amines Increase the Odds of Bacterial Vaginosis and Affect the Growth of and Lactic Acid Production by Vaginal Lactobacillus spp.
المؤلفون: Borgogna JC; Department of Animal & Range Sciences, Montana State University, Bozeman, Montana, USA.; Department of Microbiology & Immunology, Montana State University, Bozeman, Montana, USA., Shardell MD; Department of Epidemiology and Public Health, University of Maryland School of Medicine, Baltimore, Maryland, USA.; Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, USA., Grace SG; Department of Animal & Range Sciences, Montana State University, Bozeman, Montana, USA., Santori EK; Department of Microbiology & Immunology, Montana State University, Bozeman, Montana, USA., Americus B; Department of Microbiology & Immunology, Montana State University, Bozeman, Montana, USA., Li Z; Roy J. Carver Biotechnology Center, University of Illinois, Urbana, Illinois, USA., Ulanov A; Roy J. Carver Biotechnology Center, University of Illinois, Urbana, Illinois, USA., Forney L; Institute for Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, Idaho, USA.; Department of Biological Sciences, University of Idaho, Moscow, Idaho, USA., Nelson TM; Department of Animal & Range Sciences, Montana State University, Bozeman, Montana, USA.; Department of Microbiology & Immunology, Montana State University, Bozeman, Montana, USA., Brotman RM; Department of Epidemiology and Public Health, University of Maryland School of Medicine, Baltimore, Maryland, USA.; Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, USA., Ravel J; Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, USA.; Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, USA., Yeoman CJ; Department of Animal & Range Sciences, Montana State University, Bozeman, Montana, USA carl.yeoman@montana.edu.; Department of Microbiology & Immunology, Montana State University, Bozeman, Montana, USA.
المصدر: Applied and environmental microbiology [Appl Environ Microbiol] 2021 Apr 27; Vol. 87 (10). Date of Electronic Publication: 2021 Apr 27 (Print Publication: 2021).
نوع المنشور: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: American Society for Microbiology Country of Publication: United States NLM ID: 7605801 Publication Model: Electronic-Print Cited Medium: Internet ISSN: 1098-5336 (Electronic) Linking ISSN: 00992240 NLM ISO Abbreviation: Appl Environ Microbiol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Washington, American Society for Microbiology.
مواضيع طبية MeSH: Biogenic Amines/*biosynthesis , Lactobacillus/*metabolism , Vaginosis, Bacterial/*microbiology, Female ; Humans ; Lactic Acid/biosynthesis ; Lactobacillus/growth & development ; Vagina/microbiology
مستخلص: Bacterial vaginosis (BV) is the most common vaginal disorder of reproductive-aged women, yet its etiology remains enigmatic. One clinical symptom of BV, malodor, is linked to the microbial production of biogenic amines (BA). Using targeted liquid chromatography mass spectrometry, we analyzed 149 longitudinally collected vaginal samples to determine the in vivo concentrations of the most common BAs and then assessed their relationship to BV and effect upon the growth kinetics of axenically cultured vaginal Lactobacillus species. Increases in cadaverine, putrescine, and tyramine were associated with greater odds of women transitioning from L. crispatus - dominated vaginal microbiota to microbiota that have a paucity of Lactobacillus spp. and from Nugent scores of 0 to 3 to Nugent scores of 7 to 10, consistent with BV. Exposure to putrescine lengthened the lag time and/or slowed the growth of all vaginal Lactobacillus spp. except L. jensenii 62G. L. iners AB107's lag time was lengthened by cadaverine but reduced in the presence of spermidine and spermine. The growth rate of L. crispatus VPI 3199 was slowed by cadaverine and tyramine, and strain-specific responses to spermine and spermidine were observed. BAs were associated with reduced production of d- and l-lactic acid by vaginal Lactobacillus spp., and this effect was independent of their effect upon Lactobacillus species growth. The exceptions were higher levels of d- and l-lactic acid by two strains of L. crispatus when grown in the presence of spermine. Results of this study provide evidence of a direct impact of common biogenic amines on vaginal Lactobacillus spp. IMPORTANCE Lactobacillus spp. are credited with providing the primary defense against gynecological conditions, including BV, most notably through the acidification of the vaginal microenvironment, which results from their production of lactic acid. The microbial production of BAs has been hypothesized to play a mechanistic role in diminishing Lactobacillus species-mediated protection, enabling the colonization and outgrowth of diverse anaerobic bacterial species associated with BV. Here, we demonstrate that in vivo increases in the most commonly observed BAs are associated with a loss of Lactobacillus spp. and the development of BV, measured by Nugent score. Further, we show that BAs formed by amino acid decarboxylase enzymes negatively affect the growth of type strains of the most common vaginal Lactobacillus spp. and separately alter their production of lactic acid. These results suggest that BAs destabilize vaginal Lactobacillus spp. and play an important and direct role in diminishing their protection of the vaginal microenvironment.
(Copyright © 2021 American Society for Microbiology.)
References: FEMS Immunol Med Microbiol. 2006 Oct;48(1):75-83. (PMID: 16965354)
Sci Transl Med. 2012 May 2;4(132):132ra52. (PMID: 22553250)
Appl Environ Microbiol. 2009 Jan;75(2):345-52. (PMID: 19011061)
Hum Reprod. 2013 Jul;28(7):1809-15. (PMID: 23543384)
Annu Rev Microbiol. 2013;67:65-81. (PMID: 23701194)
Front Physiol. 2015 Sep 29;6:253. (PMID: 26483694)
PLoS One. 2016 Mar 10;11(3):e0150767. (PMID: 26963809)
Clin Infect Dis. 2003 Mar 1;36(5):663-8. (PMID: 12594649)
Sci Transl Med. 2012 May 2;4(132):132fs11. (PMID: 22553249)
Mol Biol Evol. 2014 Jan;31(1):232-8. (PMID: 24170494)
Microbiome. 2020 Nov 23;8(1):166. (PMID: 33228810)
Am J Med. 1983 Jan;74(1):14-22. (PMID: 6600371)
J Infect Dis. 2014 Dec 1;210(11):1723-33. (PMID: 24943724)
Hum Reprod. 2001 Sep;16(9):1809-13. (PMID: 11527880)
Sci Rep. 2018 Jan 16;8(1):852. (PMID: 29339821)
Mol Microbiol. 2008 Apr;68(1):4-16. (PMID: 18405343)
Epidemiol Infect. 2016 Jan;144(1):123-37. (PMID: 26062721)
PLoS One. 2015 May 20;10(5):e0127021. (PMID: 25993513)
J Biol Chem. 1978 May 25;253(10):3671-6. (PMID: 348695)
Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2261-5. (PMID: 12591940)
Anal Chem. 2005 Oct 15;77(20):6729-36. (PMID: 16223263)
PLoS One. 2013 May 22;8(5):e63514. (PMID: 23717441)
Am J Obstet Gynecol. 2001 Aug;185(2):375-9. (PMID: 11518895)
Nat Methods. 2016 Jul;13(7):581-3. (PMID: 27214047)
J Infect Dis. 2010 Dec 15;202(12):1907-15. (PMID: 21067371)
J Clin Invest. 1979 May;63(5):828-35. (PMID: 447831)
Reprod Sci. 2013 Jul;20(7):791-6. (PMID: 23202727)
J Bacteriol. 1975 Nov;124(2):791-9. (PMID: 1102531)
Eur J Obstet Gynecol Reprod Biol. 2012 Jul;163(1):81-4. (PMID: 22520996)
J Clin Microbiol. 1991 Feb;29(2):297-301. (PMID: 1706728)
Sex Transm Dis. 2010 Dec;37(12):732-44. (PMID: 21068695)
Nat Protoc. 2011 Jun;6(6):743-60. (PMID: 21637195)
Eur J Clin Microbiol Infect Dis. 2015 Dec;34(12):2367-76. (PMID: 26385347)
BMC Infect Dis. 2011 Jul 19;11:200. (PMID: 21771337)
Am J Obstet Gynecol. 2003 Jul;189(1):139-47. (PMID: 12861153)
J Infect Dis. 1982 Mar;145(3):337-45. (PMID: 7061879)
BJOG. 2020 Jan;127(2):264-274. (PMID: 31573753)
mBio. 2019 Aug 13;10(4):. (PMID: 31409678)
Am J Med Sci. 2012 Jan;343(1):2-9. (PMID: 22143133)
Antimicrob Agents Chemother. 2006 May;50(5):1615-22. (PMID: 16641426)
BJOG. 2020 Jan;127(2):182-192. (PMID: 31749298)
mBio. 2015 Apr 14;6(2):. (PMID: 25873373)
Antimicrob Agents Chemother. 2007 Jun;51(6):2070-7. (PMID: 17438056)
Sex Transm Dis. 2007 Nov;34(11):864-9. (PMID: 17621244)
Sex Transm Infect. 2018 Mar;94(2):117-123. (PMID: 28947665)
mSystems. 2019 Feb 19;4(1):. (PMID: 30801027)
APMIS. 2002 Nov;110(11):819-24. (PMID: 12588422)
Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1:4680-7. (PMID: 20534435)
Trans Am Clin Climatol Assoc. 2012;123:242-56. (PMID: 23303991)
FEMS Microbiol Lett. 2013 Jun;343(1):64-9. (PMID: 23506248)
Sci Rep. 2018 Jan 12;8(1):663. (PMID: 29330539)
Am J Obstet Gynecol. 1992 Mar;166(3):938-44. (PMID: 1372474)
AIDS Res Hum Retroviruses. 2019 Mar;35(3):219-228. (PMID: 30638028)
Front Mol Biosci. 2015 Feb 02;2:4. (PMID: 25988172)
Acta Obstet Gynecol Scand. 1989;68(3):217-20. (PMID: 2618604)
Appl Environ Microbiol. 1999 Dec;65(12):5631-5. (PMID: 10584033)
J Infect Dis. 1999 Dec;180(6):1863-8. (PMID: 10558942)
J Stat Softw. 2017;76:. (PMID: 36568334)
Sci Rep. 2020 Feb 25;10(1):3420. (PMID: 32098988)
Microbes Infect. 2000 Apr;2(5):543-6. (PMID: 10865199)
Nat Commun. 2019 Mar 21;10(1):1305. (PMID: 30899005)
PLoS One. 2013;8(2):e56111. (PMID: 23405259)
J Bacteriol. 1964 Jul;88:72-80. (PMID: 14197908)
J Clin Microbiol. 2007 Oct;45(10):3270-6. (PMID: 17687006)
Sex Transm Dis. 2019 May;46(5):304-311. (PMID: 30624309)
IUBMB Life. 2009 Sep;61(9):880-94. (PMID: 19603518)
J Glob Infect Dis. 2009 Jul;1(2):151-2. (PMID: 20300409)
Proc Natl Acad Sci U S A. 2015 Sep 1;112(35):11060-5. (PMID: 26283357)
Methods Enzymol. 1999;310:426-33. (PMID: 10547809)
Microbiome. 2013 Dec 02;1(1):29. (PMID: 24451163)
mBio. 2013 Aug 06;4(4):. (PMID: 23919998)
معلومات مُعتمدة: UH2 AI083264 United States AI NIAID NIH HHS; R01 NR015495 United States NR NINR NIH HHS; R21 AI111145 United States AI NIAID NIH HHS; U54 GM115371 United States GM NIGMS NIH HHS; R01 AI116799 United States AI NIAID NIH HHS; P20 GM103474 United States GM NIGMS NIH HHS
فهرسة مساهمة: Keywords: Lactobacillus; bacterial vaginosis; biogenic amines; growth response; vaginal microbiome
المشرفين على المادة: 0 (Biogenic Amines)
33X04XA5AT (Lactic Acid)
تواريخ الأحداث: Date Created: 20210306 Date Completed: 20210528 Latest Revision: 20240402
رمز التحديث: 20240402
مُعرف محوري في PubMed: PMC8117770
DOI: 10.1128/AEM.03068-20
PMID: 33674429
قاعدة البيانات: MEDLINE
الوصف
تدمد:1098-5336
DOI:10.1128/AEM.03068-20