Seminal plasma inhibits Chlamydia trachomatis infection in vitro, and may have consequences on mucosal immunity.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
09 09 2024
Historique:
received: 12 10 2023
accepted: 28 08 2024
medline: 10 9 2024
pubmed: 10 9 2024
entrez: 9 9 2024
Statut: epublish

Résumé

Seminal plasma (SP) is the main vector of C. trachomatis (CT) during heterosexual transmission from male to female. It has immunomodulatory properties and impacts the susceptibility to HIV-1 infection, but its role has not been explored during CT infection. In the female reproductive tract (FRT), CT infection induces cytokine production and neutrophil recruitment. The role of neutrophils during CT infection is partially described, they could be at the origin of the pathology observed during CT infection. During this study, we developed an experimental in vitro model to characterize the impact of CT infection and SP on endocervical epithelial cell immune response in the FRT. We also studied the impact of the epithelial cell response on neutrophil phenotype and functions. We showed that the production by epithelial cells of pro-inflammatory cytokines increased during CT infection. Moreover, the pool of SP as well as individuals SP inhibited CT infection in a dose-dependent manner. The pool of SP inhibited cytokine production in a dose-dependent manner. The pool of SP altered gene expression profiles of infected cells. The culture supernatants of cells infected or not with CT, in presence or not of the pool of SP, had an impact on neutrophil phenotype and functions: they affected markers of neutrophil maturation, activation and adhesion capacity, as well as the survival, ROS production and phagocytosis ability. This study proposes a novel approach to study the impact of the environment on the phenotype and functions of neutrophils in the FRT. It highlights the impact of the factors of the FRT environment, in particular SP and CT infection, on the mucosal inflammation and the need to take into account the SP component while studying sexually transmitted infections during heterosexual transmission from male to female.

Identifiants

pubmed: 39251689
doi: 10.1038/s41598-024-71499-9
pii: 10.1038/s41598-024-71499-9
doi:

Substances chimiques

Cytokines 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

21050

Subventions

Organisme : Agence Nationale de Recherches sur le Sida et les Hépatites Virales
ID : AO 2020-1

Informations de copyright

© 2024. The Author(s).

Références

Rowley, J. et al. Chlamydia, gonorrhoea, trichomoniasis and syphilis: global prevalence and incidence estimates, 2016. Bull. World Health Organ. 97, 32 (2019).
doi: 10.2471/BLT.18.228486
Chlamydia Infection. https://www.ecdc.europa.eu/en/chlamydia-infection .
Agrawal, T., Vats, V., Salhan, S. & Mittal, A. The mucosal immune response to Chlamydia trachomatis infection of the reproductive tract in women. J. Reprod. Immunol. 83, 173–178 (2009).
pubmed: 19896206 doi: 10.1016/j.jri.2009.07.013
Lu, H., Shen, C. & Brunham, R. C. Chlamydia trachomatis infection of epithelial cells induces the activation of caspase-1 and release of mature IL-18. J. Immunol. 165, 1463–1469 (2000).
pubmed: 10903751 doi: 10.4049/jimmunol.165.3.1463
Buckner, L. R., Lewis, M. E., Greene, S. J., Foster, T. P. & Quayle, A. J. Chlamydia trachomatis infection results in a modest pro-inflammatory cytokine response and a decrease in T cell chemokine secretion in human polarized endocervical epithelial cells. Cytokine 63, 151–165 (2013).
pubmed: 23673287 pmcid: 3703936 doi: 10.1016/j.cyto.2013.04.022
Darville, T. & Hiltke, T. J. Pathogenesis of genital tract disease due to Chlamydia trachomatis. J. Infect. Dis. 201, S114 (2010).
pubmed: 20524234 doi: 10.1086/652397
Poston, T. B. et al. Cervical cytokines associated with Chlamydia trachomatis susceptibility and protection. J. Infect. Dis. 220, 330–339 (2019).
pubmed: 30820577 pmcid: 6581900 doi: 10.1093/infdis/jiz087
Lijek, R. S., Helble, J. D., Olive, A. J., Seiger, K. W. & Starnbach, M. N. Pathology after Chlamydia trachomatis infection is driven by nonprotective immune cells that are distinct from protective populations. Proc. Natl. Acad. Sci. USA 115, 2216–2221 (2018).
pubmed: 29440378 pmcid: 5834673 doi: 10.1073/pnas.1711356115
Lehr, S., Vier, J., Häcker, G. & Kirschnek, S. Activation of neutrophils by Chlamydia trachomatis-infected epithelial cells is modulated by the chlamydial plasmid. Microbes Infect. 20, 284–292 (2018).
pubmed: 29499390 doi: 10.1016/j.micinf.2018.02.007
Rajeeve, K., Das, S., Prusty, B. K. & Rudel, T. Chlamydia trachomatis paralyses neutrophils to evade the host innate immune response. Nat. Microbiol. 3, 824–835 (2018).
pubmed: 29946164 doi: 10.1038/s41564-018-0182-y
Naglak, E. K., Morrison, S. G. & Morrison, R. P. Neutrophils are central to antibody-mediated protection against genital Chlamydia. Infect. Immun. 85, 11 (2017).
doi: 10.1128/IAI.00409-17
Schjenken, J. E. et al. Sperm modulate uterine immune parameters relevant to embryo implantation and reproductive success in mice. Commun. Biol. 4, 1–14 (2021).
doi: 10.1038/s42003-021-02038-9
Cavarelli, M. & le Grand, R. The Importance of Semen Leukocytes in HIV-1 Transmission and the Development of Prevention Strategies. 2018–2032. https://doi.org/10.1080/21645515.2020.1765622 (2020).
Owen, D. H. & Katz, D. F. A review of the physical and chemical properties of human semen and the formulation of a semen simulant. J. Androl. 26, 459–469 (2005).
pubmed: 15955884 doi: 10.2164/jandrol.04104
Song, Z. H. et al. Seminal plasma induces inflammation in the uterus through the γδ T/IL-17 pathway. Sci. Rep. 6, 1–8 (2016).
Katila, T. Post-mating inflammatory responses of the uterus. Reprod. Domest. Anim. 47(Suppl 5), 31–41 (2012).
pubmed: 22913558 doi: 10.1111/j.1439-0531.2012.02120.x
Adefuye, A., Katz, A. A. & Sales, K. J. The regulation of inflammatory pathways and infectious disease of the cervix by seminal fluid. Patholog. Res. Int. 2014, 45 (2014).
Abdulhaqq, S. A. et al. Repeated semen exposure decreases cervicovaginal SIVmac251 infection in rhesus macaques. Nat. Commun. 10, 1–10 (2019).
doi: 10.1038/s41467-019-11814-5
Edström, A. M. L. et al. The major bactericidal activity of human seminal plasma is zinc-dependent and derived from fragmentation of the semenogelins. J. Immunol. 181, 3413 (2008).
pubmed: 18714013 doi: 10.4049/jimmunol.181.5.3413
Rodriguez-Martinez, H., Martinez, E. A., Calvete, J. J., Peña Vega, F. J. & Roca, J. Seminal plasma: Relevant for fertility?. Int. J. Mol. Sci. 22, 13 (2021).
doi: 10.3390/ijms22094368
Herbst-Kralovetz, M. M. et al. Quantification and comparison of toll-like receptor expression and responsiveness in primary and immortalized human female lower genital tract epithelia. Am. J. Reprod. Immunol. 59, 212–224 (2008).
pubmed: 18201283 doi: 10.1111/j.1600-0897.2007.00566.x
Li, H. New strategies to improve minimap2 alignment accuracy. Bioinformatics 37, 4572–4574 (2021).
pubmed: 34623391 pmcid: 8652018 doi: 10.1093/bioinformatics/btab705
Li, H. Minimap2: Pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).
pubmed: 29750242 pmcid: 6137996 doi: 10.1093/bioinformatics/bty191
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).
pubmed: 28263959 pmcid: 5600148 doi: 10.1038/nmeth.4197
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 1–21 (2014).
doi: 10.1186/s13059-014-0550-8
Chen, E. Y. et al. Enrichr: Interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinform. 14, 1–14 (2013).
doi: 10.1186/1471-2105-14-S18-S1
Xie, Z. et al. Gene set knowledge discovery with enrichr. Curr. Protoc. 1, 23 (2021).
doi: 10.1002/cpz1.90
Huang, R. et al. The NCATS BioPlanet—An integrated platform for exploring the universe of cellular signaling pathways for toxicology, systems biology, and chemical genomics. Front. Pharmacol. 10, 56 (2019).
doi: 10.3389/fphar.2019.00445
Sharkey, D. J., Tremellen, K. P., Briggs, N. E., Dekker, G. A. & Robertson, S. A. Seminal plasma transforming growth factor-β, activin A and follistatin fluctuate within men over time. Hum. Reprod. 31, 2183–2191 (2016).
pubmed: 27609985 doi: 10.1093/humrep/dew185
Sharkey, D. J., Macpherson, A. M., Tremellen, K. P. & Robertson, S. A. Seminal plasma differentially regulates inflammatory cytokine gene expression in human cervical and vaginal epithelial cells. Mol. Hum. Reprod. 13, 491–501 (2007).
pubmed: 17483528 doi: 10.1093/molehr/gam028
Kolaczkowska, E. & Kubes, P. Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13, 159–175 (2013).
pubmed: 23435331 doi: 10.1038/nri3399
Passmore, J. A. S., Jaspan, H. B. & Masson, L. Genital inflammation, immune activation and risk of sexual HIV acquisition. Curr. Opin. HIV AIDS 11, 156 (2016).
pubmed: 26628324 pmcid: 6194860 doi: 10.1097/COH.0000000000000232
Anderson, D. J. & Politch, J. A. Role of seminal plasma in human female reproductive failure: Immunomodulation, inflammation, and infections. Adv. Exp. Med. Biol. 868, 159–169 (2015).
pubmed: 26178849 doi: 10.1007/978-3-319-18881-2_7
Belland, R. J. et al. From the cover: Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc. Natl. Acad. Sci. USA 100, 8478 (2003).
pubmed: 12815105 pmcid: 166254 doi: 10.1073/pnas.1331135100
Elwell, C., Mirrashidi, K. & Engel, J. Chlamydia cell biology and pathogenesis. Nat. Rev. Microbiol. 14, 385–400 (2016).
pubmed: 27108705 pmcid: 4886739 doi: 10.1038/nrmicro.2016.30
Zupin, L. et al. Human β-defensin 1 in follicular fluid and semen: impact on fertility. J. Assist. Reprod. Genet. 36, 787 (2019).
pubmed: 30712073 pmcid: 6504998 doi: 10.1007/s10815-019-01409-w
Buckner, L. R. et al. Innate immune mediator profiles and their regulation in a novel polarized immortalized epithelial cell model derived from human endocervix. J. Reprod. Immunol. 92, 8–20 (2011).
pubmed: 21943934 pmcid: 3894833 doi: 10.1016/j.jri.2011.08.002
Sharkey, D. J. et al. TGF-β mediates proinflammatory seminal fluid signaling in human cervical epithelial cells. J. Immunol. 189, 1024–1035 (2012).
pubmed: 22706080 doi: 10.4049/jimmunol.1200005
Schjenken, J. E. & Robertson, S. A. The female response to seminal fluid. Physiol. Rev. 100, 1077–1117 (2020).
pubmed: 31999507 doi: 10.1152/physrev.00013.2018
Ng, L. G., Ostuni, R. & Hidalgo, A. Heterogeneity of neutrophils. Nat. Rev. Immunol. 19, 255–265 (2019).
pubmed: 30816340 doi: 10.1038/s41577-019-0141-8
Gasson, J. C. Molecular physiology of granulocyte-macrophage colony-stimulating factor. Blood 77, 1131–1145 (1991).
pubmed: 2001448 doi: 10.1182/blood.V77.6.1131.1131
Kamp, V. M. et al. Modulation of granulocyte kinetics by GM-CSF/IFN-γ in a human LPS rechallenge model. J. Leukoc. Biol. 94, 513–520 (2013).
pubmed: 23794709 doi: 10.1189/jlb.0213066
Momose, T. et al. Interferon-gamma increases CD62L expression on human eosinophils. Int. Arch. Allergy Immunol. 120(Suppl 1), 30–33 (1999).
pubmed: 10529600 doi: 10.1159/000053590
Daniels, R. H., Finnen, M. J., Hill, M. E. & Lackie, J. M. Recombinant human monocyte IL-8 primes NADPH-oxidase and phospholipase A2 activation in human neutrophils. Immunology 75, 157 (1992).
pubmed: 1537592 pmcid: 1384818
Mol, S. et al. Efficient neutrophil activation requires two simultaneous activating stimuli. Int. J. Mol. Sci. 22, 10106 (2021).
pubmed: 34576270 pmcid: 8467451 doi: 10.3390/ijms221810106

Auteurs

Louis Reot (L)

Center for Immunology of Viral, Auto-Immune, Hematological and Bacterial Diseases [IMVA-HB/Infectious Disease Models and Innovative Therapies (IDMIT)], Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Inserm, Université Paris-Saclay, Fontenay-aux-Roses, France.

Cindy Adapen (C)

Center for Immunology of Viral, Auto-Immune, Hematological and Bacterial Diseases [IMVA-HB/Infectious Disease Models and Innovative Therapies (IDMIT)], Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Inserm, Université Paris-Saclay, Fontenay-aux-Roses, France.

Claude Cannou (C)

Center for Immunology of Viral, Auto-Immune, Hematological and Bacterial Diseases [IMVA-HB/Infectious Disease Models and Innovative Therapies (IDMIT)], Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Inserm, Université Paris-Saclay, Fontenay-aux-Roses, France.
Mucosal Immunity and Sexually Transmitted Infection Control (MISTIC) Group, Department of Virology, Institut Pasteur, Université Paris Cité, Paris, France.

Natalia Nunez (N)

Life&Soft, Fontenay-aux-Roses, France.

Sabrine Lakoum (S)

Life&Soft, Fontenay-aux-Roses, France.

Camille Pimienta (C)

Center for Immunology of Viral, Auto-Immune, Hematological and Bacterial Diseases [IMVA-HB/Infectious Disease Models and Innovative Therapies (IDMIT)], Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Inserm, Université Paris-Saclay, Fontenay-aux-Roses, France.

Laetitia Lacroix (L)

Center for Immunology of Viral, Auto-Immune, Hematological and Bacterial Diseases [IMVA-HB/Infectious Disease Models and Innovative Therapies (IDMIT)], Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Inserm, Université Paris-Saclay, Fontenay-aux-Roses, France.

Olivier Binois (O)

Service de Biologie de la Reproduction CECOS, Assistance Publique Hôpitaux de Paris, Hôpital Antoine Béclère, Université Paris-Saclay, Clamart, France.

Nelly Frydman (N)

Service de Biologie de la Reproduction CECOS, Assistance Publique Hôpitaux de Paris, Hôpital Antoine Béclère, Université Paris-Saclay, Clamart, France.

Marie-Thérèse Nugeyre (MT)

Center for Immunology of Viral, Auto-Immune, Hematological and Bacterial Diseases [IMVA-HB/Infectious Disease Models and Innovative Therapies (IDMIT)], Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Inserm, Université Paris-Saclay, Fontenay-aux-Roses, France.
Mucosal Immunity and Sexually Transmitted Infection Control (MISTIC) Group, Department of Virology, Institut Pasteur, Université Paris Cité, Paris, France.

Roger Le Grand (R)

Center for Immunology of Viral, Auto-Immune, Hematological and Bacterial Diseases [IMVA-HB/Infectious Disease Models and Innovative Therapies (IDMIT)], Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Inserm, Université Paris-Saclay, Fontenay-aux-Roses, France.

Elisabeth Menu (E)

Center for Immunology of Viral, Auto-Immune, Hematological and Bacterial Diseases [IMVA-HB/Infectious Disease Models and Innovative Therapies (IDMIT)], Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Inserm, Université Paris-Saclay, Fontenay-aux-Roses, France. elisabeth.menu@cea.fr.
Mucosal Immunity and Sexually Transmitted Infection Control (MISTIC) Group, Department of Virology, Institut Pasteur, Université Paris Cité, Paris, France. elisabeth.menu@cea.fr.

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