Lactic acid from vaginal microbiota enhances cervicovaginal epithelial barrier integrity by promoting tight junction protein expression.

Epithelial cells Female reproductive tract HIV Lactic acid Lactobacilli Metabolites STIs Tight junctions Transcriptomics Vaginal microbiome

Journal

Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147

Informations de publication

Date de publication:
31 08 2022
Historique:
received: 12 02 2022
accepted: 30 07 2022
entrez: 31 8 2022
pubmed: 1 9 2022
medline: 9 9 2022
Statut: epublish

Résumé

Women with a cervicovaginal microbiota dominated by Lactobacillus spp. are at reduced risk of acquiring sexually transmitted infections including HIV, but the biological mechanisms involved remain poorly defined. Here, we performed metaproteomics on vaginal swab samples from young South African women (n = 113) and transcriptomics analysis of cervicovaginal epithelial cell cultures to examine the ability of lactic acid, a metabolite produced by cervicovaginal lactobacilli, to modulate genital epithelial barrier function. Compared to women with Lactobacillus-depleted microbiota, women dominated by vaginal lactobacilli exhibit higher abundance of bacterial lactate dehydrogenase, a key enzyme responsible for lactic acid production, which is independently associated with an increased abundance of epithelial barrier proteins. Physiological concentrations of lactic acid enhance epithelial cell culture barrier integrity and increase intercellular junctional molecule expression. These findings reveal a novel ability of vaginal lactic acid to enhance genital epithelial barrier integrity that may help prevent invasion by sexually transmitted pathogens. Video abstract.

Sections du résumé

BACKGROUND
Women with a cervicovaginal microbiota dominated by Lactobacillus spp. are at reduced risk of acquiring sexually transmitted infections including HIV, but the biological mechanisms involved remain poorly defined. Here, we performed metaproteomics on vaginal swab samples from young South African women (n = 113) and transcriptomics analysis of cervicovaginal epithelial cell cultures to examine the ability of lactic acid, a metabolite produced by cervicovaginal lactobacilli, to modulate genital epithelial barrier function.
RESULTS
Compared to women with Lactobacillus-depleted microbiota, women dominated by vaginal lactobacilli exhibit higher abundance of bacterial lactate dehydrogenase, a key enzyme responsible for lactic acid production, which is independently associated with an increased abundance of epithelial barrier proteins. Physiological concentrations of lactic acid enhance epithelial cell culture barrier integrity and increase intercellular junctional molecule expression.
CONCLUSIONS
These findings reveal a novel ability of vaginal lactic acid to enhance genital epithelial barrier integrity that may help prevent invasion by sexually transmitted pathogens. Video abstract.

Identifiants

pubmed: 36045402
doi: 10.1186/s40168-022-01337-5
pii: 10.1186/s40168-022-01337-5
pmc: PMC9429363
doi:

Substances chimiques

Tight Junction Proteins 0
Lactic Acid 33X04XA5AT

Types de publication

Journal Article Video-Audio Media Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

141

Subventions

Organisme : NIAID NIH HHS
ID : U01 AI070921
Pays : United States
Organisme : NIAID NIH HHS
ID : UH2 AI083264
Pays : United States
Organisme : NIAID NIH HHS
ID : U19 AI084044
Pays : United States

Informations de copyright

© 2022. The Author(s).

Références

Hum Reprod. 2001 Sep;16(9):1809-13
pubmed: 11527880
Anaerobe. 2013 Dec;24:43-8
pubmed: 24036421
N Engl J Med. 2020 May 14;382(20):1906-1915
pubmed: 32402161
Am J Reprod Immunol. 2018 Sep;80(3):e13027
pubmed: 30144195
Nat Genet. 2000 May;25(1):25-9
pubmed: 10802651
Int J STD AIDS. 2003 Apr;14(4):270-3
pubmed: 12716498
Biol Reprod. 2011 Jul;85(1):97-104
pubmed: 21471299
Nat Commun. 2019 Mar 21;10(1):1305
pubmed: 30899005
J Immunol. 2013 Oct 15;191(8):4246-58
pubmed: 24043886
EBioMedicine. 2019 Jun;44:675-690
pubmed: 31027917
Front Physiol. 2015 Jun 02;6:164
pubmed: 26082720
Biol Reprod. 2005 Dec;73(6):1253-63
pubmed: 16093359
J Infect Dis. 2021 Jun 16;223(12 Suppl 2):S222-S235
pubmed: 33576776
PLoS Med. 2011 Feb 15;8(2):e1000416
pubmed: 21358808
Sci Transl Med. 2012 May 2;4(132):132ra52
pubmed: 22553250
J Infect Dis. 2010 Dec 15;202(12):1907-15
pubmed: 21067371
Front Microbiol. 2018 Oct 08;9:2181
pubmed: 30349508
Nat Med. 2019 Jun;25(6):1012-1021
pubmed: 31142849
Nat Rev Microbiol. 2003 Oct;1(1):25-34
pubmed: 15040177
Cells. 2019 Sep 21;8(10):
pubmed: 31546582
J Virol. 2011 Feb;85(4):1757-64
pubmed: 21123374
PLoS Pathog. 2014 Oct 09;10(10):e1004440
pubmed: 25299616
Res Microbiol. 2017 Nov - Dec;168(9-10):782-792
pubmed: 28435139
J Clin Microbiol. 1991 Feb;29(2):297-301
pubmed: 1706728
Nucleic Acids Res. 2015 Apr 20;43(7):e47
pubmed: 25605792
BMC Infect Dis. 2011 Jul 19;11:200
pubmed: 21771337
Immunity. 2017 Jan 17;46(1):29-37
pubmed: 28087240
Am J Reprod Immunol. 2011 Mar;65(3):253-60
pubmed: 21223427
mBio. 2019 Aug 13;10(4):
pubmed: 31409678
Front Microbiol. 2017 May 19;8:906
pubmed: 28579980
PLoS Pathog. 2010 Apr 08;6(4):e1000852
pubmed: 20386714
mSphere. 2018 Jul 5;3(4):
pubmed: 29976641
PLoS Pathog. 2016 Sep 22;12(9):e1005885
pubmed: 27658293
Curr Immunol Rev. 2019;15(1):4-13
pubmed: 31853241
AIDS. 2008 Jul 31;22(12):1493-501
pubmed: 18614873
Genome Res. 2003 Nov;13(11):2498-504
pubmed: 14597658
Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1:4680-7
pubmed: 20534435
Antimicrob Agents Chemother. 2013 Aug;57(8):3806-14
pubmed: 23716050
PLoS One. 2012;7(3):e32728
pubmed: 22412914
Sci Rep. 2019 Feb 13;9(1):1917
pubmed: 30760770
Infect Immun. 2020 Mar 23;88(4):
pubmed: 32094253
J Antimicrob Chemother. 2013 Sep;68(9):2015-25
pubmed: 23657804
mBio. 2015 Oct 06;6(5):e01084-15
pubmed: 26443453
Sci Rep. 2018 Jul 18;8(1):10868
pubmed: 30022083
Genome Biol. 2014 Feb 03;15(2):R29
pubmed: 24485249
Microbiome. 2020 Nov 21;8(1):165
pubmed: 33220709
Ann Clin Microbiol Antimicrob. 2011 Feb 17;10:8
pubmed: 21329492
AIDS Res Hum Retroviruses. 2019 Mar;35(3):219-228
pubmed: 30638028
Bioinformatics. 2005 Aug 15;21(16):3448-9
pubmed: 15972284
Gut. 1987 Oct;28(10):1221-7
pubmed: 3678950
ISME J. 2014 Sep;8(9):1781-93
pubmed: 24599071
Am J Reprod Immunol. 2018 Aug;80(2):e12977
pubmed: 29790240
Sci Rep. 2020 Apr 10;10(1):6196
pubmed: 32277092
Infect Immun. 1999 Oct;67(10):5170-5
pubmed: 10496892
PLoS Med. 2012;9(6):e1001251
pubmed: 22745608
Am J Obstet Gynecol. 2021 Jun;224(6):635-636
pubmed: 33561441
J Virol. 2013 Nov;87(21):11388-400
pubmed: 23966398
Methods. 2001 Dec;25(4):402-8
pubmed: 11846609
PLoS Pathog. 2017 Feb 27;13(2):e1006247
pubmed: 28241053
Int J STD AIDS. 2018 May;29(6):531-539
pubmed: 29198180
N Engl J Med. 1995 Dec 28;333(26):1737-42
pubmed: 7491137
Infect Immun. 2017 Dec 19;86(1):
pubmed: 29038128
PLoS One. 2021 Feb 11;16(2):e0246953
pubmed: 33571286
PLoS Pathog. 2016 Sep 22;12(9):e1005889
pubmed: 27656899
Microbiology (Reading). 2014 Oct;160(Pt 10):2272-2282
pubmed: 25073854
PLoS One. 2013 Nov 06;8(11):e80074
pubmed: 24223212
Front Cell Infect Microbiol. 2020 Jan 10;9:446
pubmed: 31998660
PLoS One. 2019 Nov 15;14(11):e0224964
pubmed: 31730666
Mucosal Immunol. 2017 Nov;10(6):1480-1490
pubmed: 28401934
mBio. 2013 Aug 06;4(4):
pubmed: 23919998

Auteurs

David Jose Delgado-Diaz (DJ)

Life Sciences Discipline, Burnet Institute, 85 Commercial Road, Melbourne, VIC, 3004, Australia.
Department of Microbiology, Monash University, Clayton, VIC, 3168, Australia.

Brianna Jesaveluk (B)

Life Sciences Discipline, Burnet Institute, 85 Commercial Road, Melbourne, VIC, 3004, Australia.
Department of Microbiology, Monash University, Clayton, VIC, 3168, Australia.

Joshua A Hayward (JA)

Life Sciences Discipline, Burnet Institute, 85 Commercial Road, Melbourne, VIC, 3004, Australia.
Department of Microbiology, Monash University, Clayton, VIC, 3168, Australia.

David Tyssen (D)

Life Sciences Discipline, Burnet Institute, 85 Commercial Road, Melbourne, VIC, 3004, Australia.

Arghavan Alisoltani (A)

Division of Medical Virology, Department of Pathology, University of Cape Town, Cape Town, 7925, South Africa.
Division of Biomedical Sciences, University of California Riverside School of Medicine, Riverside, CA, 92521, USA.

Matthys Potgieter (M)

Computational Biology Division, Department of Integrative Biomedical Sciences, University of Cape Town, Cape Town, 7925, South Africa.
Division of Chemical and Systems Biology, Department of Integrative Biomedical Sciences, University of Cape Town, Cape Town, 7925, South Africa.

Liam Bell (L)

Centre for Proteomic and Genomic Research, Cape Town, 7925, South Africa.

Elizabeth Ross (E)

Centre for Proteomic and Genomic Research, Cape Town, 7925, South Africa.

Arash Iranzadeh (A)

Computational Biology Division, Department of Integrative Biomedical Sciences, University of Cape Town, Cape Town, 7925, South Africa.

Imane Allali (I)

Laboratory of Human Pathologies Biology, Department of Biology, Faculty of Sciences, Mohammed V University in Rabat, 1014, Rabat, Morocco.

Smritee Dabee (S)

Center for Global Infectious Disease Research, Seattle Children's Research Institute, Seattle, WA, 98101, USA.

Shaun Barnabas (S)

Family Centre for Research with Ubuntu, Stellenbosch University, Cape Town, 7505, South Africa.

Hoyam Gamieldien (H)

Division of Medical Virology, Department of Pathology, University of Cape Town, Cape Town, 7925, South Africa.

Jonathan M Blackburn (JM)

Division of Chemical and Systems Biology, Department of Integrative Biomedical Sciences, University of Cape Town, Cape Town, 7925, South Africa.
Institute of Infectious Disease and Molecular Medicine (IDM), University of Cape Town, Cape Town, 7925, South Africa.

Nicola Mulder (N)

Computational Biology Division, Department of Integrative Biomedical Sciences, University of Cape Town, Cape Town, 7925, South Africa.
Institute of Infectious Disease and Molecular Medicine (IDM), University of Cape Town, Cape Town, 7925, South Africa.
Centre for Infectious Diseases Research (CIDRI) in Africa Wellcome Trust Centre, University of Cape Town, Cape Town, 7925, South Africa.

Steven B Smith (SB)

Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.

Vonetta L Edwards (VL)

Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.

Adam D Burgener (AD)

Center for Global Health and Diseases, Case Western Reserve University, Cleveland, OH, 44106, USA.
Department of Obstetrics and Gynecology, University of Manitoba, Winnipeg, Canada.
Department of Medicine Solna, Karolinska Institutet, Stockholm, Sweden.

Linda-Gail Bekker (LG)

Institute of Infectious Disease and Molecular Medicine (IDM), University of Cape Town, Cape Town, 7925, South Africa.
Desmond Tutu HIV Centre, University of Cape Town, Cape Town, 7925, South Africa.

Jacques Ravel (J)

Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.

Jo-Ann S Passmore (JS)

Division of Medical Virology, Department of Pathology, University of Cape Town, Cape Town, 7925, South Africa.
Institute of Infectious Disease and Molecular Medicine (IDM), University of Cape Town, Cape Town, 7925, South Africa.
Centre for the AIDS Programme of Research in South Africa, Durban, 4013, South Africa.
National Health Laboratory Service, Cape Town, 7925, South Africa.

Lindi Masson (L)

Life Sciences Discipline, Burnet Institute, 85 Commercial Road, Melbourne, VIC, 3004, Australia.
Division of Medical Virology, Department of Pathology, University of Cape Town, Cape Town, 7925, South Africa.
Institute of Infectious Disease and Molecular Medicine (IDM), University of Cape Town, Cape Town, 7925, South Africa.
Centre for the AIDS Programme of Research in South Africa, Durban, 4013, South Africa.
Central Clinical School, Monash University, Melbourne, 3004, Australia.

Anna C Hearps (AC)

Life Sciences Discipline, Burnet Institute, 85 Commercial Road, Melbourne, VIC, 3004, Australia.
Central Clinical School, Monash University, Melbourne, 3004, Australia.

Gilda Tachedjian (G)

Life Sciences Discipline, Burnet Institute, 85 Commercial Road, Melbourne, VIC, 3004, Australia. gilda.tachedjian@burnet.edu.au.
Department of Microbiology, Monash University, Clayton, VIC, 3168, Australia. gilda.tachedjian@burnet.edu.au.
Department of Microbiology and Immunology at the Peter Doherty Institute for Infection and Immunity, University of Melbourne, Melbourne, VIC, 3010, Australia. gilda.tachedjian@burnet.edu.au.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH