Group B Streptococcus serotypes Ia and V induce differential vaginal immune responses that may contribute to long term colonization of the female reproductive tract.


Journal

American journal of reproductive immunology (New York, N.Y. : 1989)
ISSN: 1600-0897
Titre abrégé: Am J Reprod Immunol
Pays: Denmark
ID NLM: 8912860

Informations de publication

Date de publication:
01 2020
Historique:
received: 14 08 2019
revised: 30 09 2019
accepted: 07 10 2019
pubmed: 19 10 2019
medline: 1 12 2020
entrez: 19 10 2019
Statut: ppublish

Résumé

Group B Streptococcus (GBS) is a common colonizer of the female genital tract at the time of pregnancy and has been associated with severe neonatal infections. Despite trials for GBS vaccines already being underway, the factors influencing vaginal GBS colonization and clearance are currently poorly understood. Within this study, we investigated the host immune responses to GBS infections in mice that affect GBS vaginal colonization and clearance. Cervicovaginal swabs were used to measure vaginal GBS persistence, and vaginal cytokine responses were measured using the BioPlex We observed significant differences in the ability of GBS serotype V infections to persist, compared with GBS serotype Ia vaginal infections. Vaginal cytokine response examination identified temporal changes in cytokine production (IL10, IFNγ, IL6, IL1β, and TNFα) in relation to GBS serotype and clearance or colonization. Lymphocyte proliferation assays also revealed robust cellular immune responses to GBS vaginal infections irrespective of clearance or colonization. In vitro human cellular analyses also identified that vaginal epithelial cell line cytokine production was suppressed in the presence of hormones despite no alteration in adhesion/invasion. Here, we establish previously unknown, serotype specific, temporal immune responses which may be associated with vaginal GBS colonization or clearance in the female genital tract.

Identifiants

pubmed: 31626718
doi: 10.1111/aji.13199
doi:

Substances chimiques

Cytokines 0
Estrogens 0
Progesterone 4G7DS2Q64Y

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13199

Subventions

Organisme : National Health & Medical Research Early Career Fellowship
ID : APP1052464
Pays : International
Organisme : Institute of Health & Biomedical Innovation Early Career Researcher Grant
Pays : International

Informations de copyright

© 2019 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.

Références

Russell NJ, Seale AC, O'Driscoll M, et al. Maternal colonization with Group B Streptococcus and serotype distribution worldwide: systematic review and meta-analyses. Clin Infect Dis. 2017;65(suppl_2):S100-S111.
Bianchi-Jassir F, Seale AC, Kohli-Lynch M, et al. Preterm birth associated with Group B Streptococcus maternal colonization worldwide: systematic review and meta-analyses. Clin Infect Dis. 2017;65(suppl_2):S133-S142.
Stoll BJ, Hansen NI, Sanchez PJ, et al. Early onset neonatal sepsis: the burden of Group B Streptococcal and E. coli disease continues. Pediatrics. 2011;127(5):817-826.
Seale AC, Bianchi-Jassir F, Russell NJ, et al. Estimates of the burden of Group B streptococcal disease worldwide for pregnant women, stillbirths, and children. Clin Infect Dis. 2017;65(suppl_2):S200-S219.
Madrid L, Seale AC, Kohli-Lynch M, et al. Infant Group B streptococcal disease incidence and serotypes worldwide: systematic review and meta-analyses. Clin Infect Dis. 2017;65(suppl_2):S160-S172.
Joubrel C, Tazi A, Six A, et al. Group B Streptococcus neonatal invasive infections, France 2007-2012. Clin Microbiol Infect. 2015;21(10):910-916.
Sinha A, Russell LB, Tomczyk S, et al. Disease burden of Group B Streptococcus among infants in sub-Saharan Africa: a systematic literature review and meta-analysis. Pediatr Infect Dis J. 2016;35(9):933-942.
Pinto AM, Pereira TA, Alves V, Araujo A, Lage OM. Incidence and serotype characterisation of Streptococcus agalactiae in a Portuguese hospital. J Clin Pathol. 2018;71(6):508-513.
Lopez Y, Parra E, Cepas V, et al. Serotype, virulence profile, antimicrobial resistance and macrolide-resistance determinants in Streptococcus agalactiae isolates in pregnant women and neonates in Catalonia, Spain. Enferm Infecc Microbiol Clin. 2018;36(8):472-477.
Seoud M, Nassar AH, Zalloua P, et al. Prenatal and neonatal Group B Streptococcus screening and serotyping in Lebanon: incidence and implications. Acta Obstet Gynecol Scand. 2010;89(3):399-403.
Patras KA, Doran KS. A murine model of Group B Streptococcus vaginal colonization. J Vis Exp. 2016;18(1):197.
Carey AJ, Tan CK, Mirza S, et al. Infection and cellular defense dynamics in a novel 17beta-estradiol murine model of chronic human Group B Streptococcus genital tract colonization reveal a role for hemolysin in persistence and neutrophil accumulation. J Immunol. 2014;192(4):1718-1731.
Sullivan MJ, Leclercq SY, Ipe DS, et al. Effect of the Streptococcus agalactiae virulence regulator CovR on the pathogenesis of urinary tract infection. J Infect Dis. 2017;215(3):475-483.
Nikolaitchouk N, Andersch B, Falsen E, Strombeck L, Mattsby-Baltzer I. The lower genital tract microbiota in relation to cytokine-, SLPI- and endotoxin levels: application of checkerboard DNA-DNA hybridization (CDH). APMIS. 2008;116(4):263-277.
Patras KA, Wang NY, Fletcher EM, et al. Group B Streptococcus CovR regulation modulates host immune signalling pathways to promote vaginal colonization. Cell Microbiol. 2013;15(7):1154-1167.
O'Meara CP, Armitage CW, Kollipara A, et al. Induction of partial immunity in both males and females is sufficient to protect females against sexual transmission of Chlamydia. Mucosal Immunol. 2016;9(4):1076-1088.
Arslan SY, Yu Y, Burdette JE, et al. Novel three dimensional human endocervix cultures respond to 28-day hormone treatment. Endocrinology. 2015;156(4):1602-1609.
Hardie L, Trayhurn P, Abramovich D, Fowler P. Circulating leptin in women: a longitudinal study in the menstrual cycle and during pregnancy. Clin Endocrinol (Oxf). 1997;47(1):101-106.
Armistead B, Oler E, Adams Waldorf K, Rajagopal L. The double life of Group B Streptococcus: asymptomatic colonizer and potent pathogen. J Mol Biol. 2019;431(16):2914-2931.
Patras KA, Nizet V. Group B Streptococcal maternal colonization and neonatal disease: molecular mechanisms and preventative approaches. Front Pediatr. 2018;6:27.
Patras KA, Rosler B, Thoman ML, Doran KS. Characterization of host immunity during persistent vaginal colonization by Group B Streptococcus. Mucosal Immunol. 2015;8(6):1339-1348.
Williams PA, Bohnsack JF, Augustine NH, Drummond WK, Rubens CE, Hill HR. Production of tumor necrosis factor by human cells in vitro and in vivo, induced by Group B Streptococci. J Pediatr. 1993;123(2):292-300.
Dauby N, Chamekh M, Melin P, Slogrove AL, Goetghebuer T. Increased risk of Group B Streptococcus invasive infection in HIV-exposed but uninfected infants: a review of the evidence and possible mechanisms. Front Immunol. 2016;7:505.
Levy O, Jean-Jacques RM, Cywes C, et al. Critical role of the complement system in Group B Streptococcus-induced tumor necrosis factor alpha release. Infect Immun. 2003;71(11):6344-6353.
Madureira P, Andrade EB, Gama B, et al. Inhibition of IL-10 production by maternal antibodies against Group B Streptococcus GAPDH confers immunity to offspring by favoring neutrophil recruitment. PLoS Pathog. 2011;7(11):e1002363.
Friedman CA, Robbins KK, Temple DM, Miller CJ, Rawson JE. Survival and neutrophil kinetics in infants with severe Group B Streptococcal disease treated with gamma globulin. J Perinatol. 1996;16(6):439-442.
Andrade EB, Alves J, Madureira P, et al. TLR2-induced IL-10 production impairs neutrophil recruitment to infected tissues during neonatal bacterial sepsis. J Immunol. 2013;191(9):4759-4768.
Clarke D, Letendre C, Lecours MP, et al. Group B Streptococcus induces a robust IFN-gamma response by CD4(+) T cells in an in vitro and in vivo model. J Immunol Res. 2016;2016:5290604.
Gray KJ, Kafulafula G, Matemba M, Kamdolozi M, Membe G, French N. Group B Streptococcus and HIV infection in pregnant women, Malawi, 2008-2010. Emerg Infect Dis. 2011;17(10):1932-1935.
Dzanibe S, Madhi SA. Systematic review of the clinical development of Group B Streptococcus serotype-specific capsular polysaccharide-based vaccines. Expert Rev Vaccines. 2018;17(7):635-651.
Lewis AL, Nizet V, Varki A. Discovery and characterization of sialic acid O-acetylation in Group B Streptococcus. Proc Natl Acad Sci USA. 2004;101(30):11123-11128.
Weiman S, Uchiyama S, Lin FY, et al. O-Acetylation of sialic acid on Group B Streptococcus inhibits neutrophil suppression and virulence. Biochem J. 2010;428(2):163-168.
Lewis AL, Hensler ME, Varki A, Nizet V. The Group B Streptococcal sialic acid O-acetyltransferase is encoded by neuD, a conserved component of bacterial sialic acid biosynthetic gene clusters. J Biol Chem. 2006;281(16):11186-11192.
Mei J, Liu Y, Dai N, et al. Cxcr2 and Cxcl5 regulate the IL-17/G-CSF axis and neutrophil homeostasis in mice. J Clin Invest. 2012;122(3):974-986.
Iwakura Y, Ishigame H. The IL-23/IL-17 axis in inflammation. J Clin Invest. 2006;116(5):1218-1222.
Shivers KY, Amador N, Abrams L, Hunter D, Jenab S, Quinones-Jenab V. Estrogen alters baseline and inflammatory-induced cytokine levels independent from hypothalamic-pituitary-adrenal axis activity. Cytokine. 2015;72(2):121-129.
Stein B, Yang MX. Repression of the interleukin-6 promoter by estrogen receptor is mediated by NF-kappa B and C/EBP beta. Mol Cell Biol. 1995;15(9):4971-4979.
Wira CR, Rodriguez-Garcia M, Patel MV. The role of sex hormones in immune protection of the female reproductive tract. Nat Rev Immunol. 2015;15(4):217-230.

Auteurs

Emma L Sweeney (EL)

Institute of Health & Biomedical Innovation, School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Brisbane, QLD, Australia.

Stephanie Gardiner (S)

Institute of Health & Biomedical Innovation, School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Brisbane, QLD, Australia.

Jacob Tickner (J)

Institute of Health & Biomedical Innovation, School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Brisbane, QLD, Australia.

Logan Trim (L)

Institute of Health & Biomedical Innovation, School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Brisbane, QLD, Australia.

Kenneth W Beagley (KW)

Institute of Health & Biomedical Innovation, School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Brisbane, QLD, Australia.

Alison J Carey (AJ)

Institute of Health & Biomedical Innovation, School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Brisbane, QLD, Australia.

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