Defining a role for Interferon Epsilon in normal and complicated pregnancies

. 2022 Jul ; 8 (7) : e09952. [epub] 20220716

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35898609
Odkazy

PubMed 35898609
PubMed Central PMC9309660
DOI 10.1016/j.heliyon.2022.e09952
PII: S2405-8440(22)01240-3
Knihovny.cz E-zdroje

Interferon epsilon (IFNe) is a recently described cytokine that is constitutively expressed in the female reproductive tract. However, the role of this hormonally regulated cytokine during human pregnancy is poorly understood. Moreover, whether IFNe participates in host immune response against bacteria-driven intra-amniotic infection or cervical human papillomavirus infection during pregnancy is unknown. Herein, using a unique set of human samples derived from multiple study cohorts, we aimed to uncover the role of IFNe in normal and complicated pregnancies. We showed that IFNe is expressed in the myometrium, cervix, and chorioamniotic membranes, and may therefore represent a constitutive element of host defense mechanisms in these tissues during pregnancy. The expression of IFNe in the myometrium and cervix appeared greater in late gestation than in mid-pregnancy, but did not seem to be impacted by labor. Notably, concentrations of IFNe in amniotic fluid, but not cervical fluid, were increased in a subset of women undergoing spontaneous preterm labor with intra-amniotic infection, indicating that IFNe could participate in anti-microbial responses in the amniotic cavity. However, stimulation with Ureaplasma parvum and/or lipopolysaccharide did not enhance IFNE expression by amnion epithelial or cervical cells in vitro, implicating alternative sources of this cytokine during intra-amniotic or cervical infection, respectively. Collectively, our results represent the first characterization of IFNe expression by human reproductive and gestational tissues during normal pregnancy and suggest a role for this cytokine in intra-amniotic infection leading to preterm birth.

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Hardy M.P., et al. Characterization of the type I interferon locus and identification of novel genes. Genomics. 2004;84(2):331–345. PubMed

Fung K.Y., et al. Interferon-epsilon protects the female reproductive tract from viral and bacterial infection. Science. 2013;339(6123):1088–1092. PubMed PMC

Hermant P., et al. IFN-epsilon is constitutively expressed by cells of the reproductive tract and is inefficiently secreted by fibroblasts and cell lines. PLoS One. 2013;8(8) PubMed PMC

Demers A., et al. The mucosal expression pattern of interferon-epsilon in rhesus macaques. J. Leukoc. Biol. 2014;96(6):1101–1107. PubMed PMC

Bourke N.M., et al. Human IFNε: spaciotemporal expression, hormone regulation and innate immunity in the female reproductive tract. bioRxiv. 2018 PubMed

Fischer C.D., et al. Interferon epsilon is constitutively expressed in equine endometrium and up-regulated during the luteal phase. Anim. Reprod. Sci. 2018;195:38–43. PubMed

Delhaye S., et al. Neurons produce type I interferon during viral encephalitis. Proc. Natl. Acad. Sci. U.S.A. 2006;103(20):7835–7840. PubMed PMC

Nickodem C., et al. Interferon epsilon in the reproductive tract of healthy and genital herpes simplex virus-infected pregnant women: results of a pilot study. Am. J. Reprod. Immunol. 2018;80(3) PubMed

Liu L., et al. Global, regional, and national causes of under-5 mortality in 2000-15: an updated systematic analysis with implications for the Sustainable Development Goals. Lancet. 2016;388(10063):3027–3035. PubMed PMC

Taylor B.D., et al. Interferon epsilon and preterm birth subtypes; a new piece of the type I interferon puzzle during pregnancy? Am. J. Reprod. Immunol. 2022;87(4) PubMed PMC

Romero R., et al. Infection and labor. V. Prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am. J. Obstet. Gynecol. 1989;161(3):817–824. PubMed

Wehmeyer A., et al. Sjögren syndrome: comparative studies in local ocular and serum immunoglobulin concentrations with special reference to secretory IgA. Int. Ophthalmol. 1991;15(3):147–151. PubMed

Yoon B.H., Chang J.W., Romero R. Isolation of Ureaplasma urealyticum from the amniotic cavity and adverse outcome in preterm labor. Obstet. Gynecol. 1998;92(1):77–82. PubMed

Kim M., et al. Biovar diversity of Ureaplasma urealyticum in amniotic fluid: distribution, intrauterine inflammatory response and pregnancy outcomes. J. Perinat. Med. 2003;31(2):146–152. PubMed

DiGiulio D.B., et al. Prevalence and diversity of microbes in the amniotic fluid, the fetal inflammatory response, and pregnancy outcome in women with preterm pre-labor rupture of membranes. Am. J. Reprod. Immunol. 2010;64(1):38–57. PubMed PMC

Romero R., et al. A novel molecular microbiologic technique for the rapid diagnosis of microbial invasion of the amniotic cavity and intra-amniotic infection in preterm labor with intact membranes. Am. J. Reprod. Immunol. 2014;71(4):330–358. PubMed PMC

Romero R., et al. Clinical chorioamnionitis at term I: microbiology of the amniotic cavity using cultivation and molecular techniques. J. Perinat. Med. 2015;43(1):19–36. PubMed PMC

Cox C., et al. The common vaginal commensal bacterium Ureaplasma parvum is associated with chorioamnionitis in extreme preterm labor. J. Matern. Fetal Neonatal Med. 2016;29(22):3646–3651. PubMed

Motomura K., et al. Intra-amniotic infection with Ureaplasma parvum causes preterm birth and neonatal mortality that are prevented by treatment with clarithromycin. mBio. 2020;11(3) PubMed PMC

Tricomi V., et al. Arborization test for the detection of ruptured fetal membranes. Clinical Evaluation. Obstet. Gynecol. 1966;27(2):275–279. PubMed

Friedman M.L., McElin T.W. Diagnosis of ruptured fetal membranes. Clinical study and review of the literature. Am. J. Obstet. Gynecol. 1969;104(4):544–550. PubMed

Bennett S.L., et al. The ferning and nitrazine tests of amniotic fluid between 12 and 41 weeks gestation. Am. J. Perinatol. 1993;10(2):101–104. PubMed

Tchirikov M., et al. Mid-trimester preterm premature rupture of membranes (PPROM): etiology, diagnosis, classification, international recommendations of treatment options and outcome. J. Perinat. Med. 2018;46(5):465–488. PubMed

Yoon B.H., et al. Clinical significance of intra-amniotic inflammation in patients with preterm labor and intact membranes. Am. J. Obstet. Gynecol. 2001;185(5):1130–1136. PubMed

Kacerovsky M., et al. Bedside assessment of amniotic fluid interleukin-6 in preterm prelabor rupture of membranes. Am. J. Obstet. Gynecol. 2014;211(4):385 e1–9. PubMed

Chaemsaithong P., et al. A rapid interleukin-6 bedside test for the identification of intra-amniotic inflammation in preterm labor with intact membranes. J. Matern. Fetal Neonatal Med. 2016;29(3):349–359. PubMed PMC

Romero R., et al. Prevalence and clinical significance of sterile intra-amniotic inflammation in patients with preterm labor and intact membranes. Am. J. Reprod. Immunol. 2014;72(5):458–474. PubMed PMC

Romero R., et al. Sterile intra-amniotic inflammation in asymptomatic patients with a sonographic short cervix: prevalence and clinical significance. J. Matern. Fetal Neonatal Med. 2015;28(11):1343–1359. PubMed PMC

Romero R., et al. Sterile and microbial-associated intra-amniotic inflammation in preterm prelabor rupture of membranes. J. Matern. Fetal Neonatal Med. 2015;28(12):1394–1409. PubMed PMC

Ecker D.J., et al. New technology for rapid molecular diagnosis of bloodstream infections. Expert Rev. Mol. Diagn. 2010;10(4):399–415. PubMed

Romero R., Mazor M. Infection and preterm labor. Clin. Obstet. Gynecol. 1988;31(3):553–584. PubMed

Goldenberg R.L., Hauth J.C., Andrews W.W. Intrauterine infection and preterm delivery. N. Engl. J. Med. 2000;342(20):1500–1507. PubMed

Romero R., et al. The role of infection in preterm labour and delivery. Paediatr. Perinat. Epidemiol. 2001;15(Suppl 2):41–56. PubMed

Goldenberg R.L., et al. Epidemiology and causes of preterm birth. Lancet. 2008;371(9606):75–84. PubMed PMC

Romero R., Dey S.K., Fisher S.J. Preterm labor: one syndrome, many causes. Science. 2014;345(6198):760–765. PubMed PMC

Romero R., et al. Evidence that intra-amniotic infections are often the result of an ascending invasion - a molecular microbiological study. J. Perinat. Med. 2019;47(9):915–931. PubMed PMC

Bourne G. The foetal membranes. A review of the anatomy of normal amnion and chorion and some aspects of their function. Postgrad. Med. 1962;38:193–201. PubMed PMC

Romero R., et al. Proteomic analysis of amniotic fluid to identify women with preterm labor and intra-amniotic inflammation/infection: the use of a novel computational method to analyze mass spectrometric profiling. J. Matern. Fetal Neonatal Med. 2008;21(6):367–388. PubMed PMC

Bujold E., et al. Proteomic profiling of amniotic fluid in preterm labor using two-dimensional liquid separation and mass spectrometry. J. Matern. Fetal Neonatal Med. 2008;21(10):697–713. PubMed PMC

Romero R., et al. Isobaric labeling and tandem mass spectrometry: a novel approach for profiling and quantifying proteins differentially expressed in amniotic fluid in preterm labor with and without intra-amniotic infection/inflammation. J. Matern. Fetal Neonatal Med. 2010;23(4):261–280. PubMed PMC

Romero R., et al. The diagnostic performance of the Mass Restricted (MR) score in the identification of microbial invasion of the amniotic cavity or intra-amniotic inflammation is not superior to amniotic fluid interleukin-6. J. Matern. Fetal Neonatal Med. 2014;27(8):757–769. PubMed PMC

Romero R., et al. Evidence of perturbations of the cytokine network in preterm labor. Am. J. Obstet. Gynecol. 2015;213(6):836.e1–836.e18. PubMed PMC

Tarca A.L., et al. The cytokine network in women with an asymptomatic short cervix and the risk of preterm delivery. Am. J. Reprod. Immunol. 2017;78(3) PubMed PMC

Bhatti G., et al. Compartmentalized profiling of amniotic fluid cytokines in women with preterm labor. PLoS One. 2020;15(1):e0227881. PubMed PMC

Marks Z.R.C., et al. Properties and functions of the novel type I interferon epsilon. Semin. Immunol. 2019;43 PubMed

Gough D.J., et al. Constitutive type I interferon modulates homeostatic balance through tonic signaling. Immunity. 2012;36(2):166–174. PubMed PMC

Bocci V. Is interferon produced in physiologic conditions? Med. Hypotheses. 1980;6(7):735–745. PubMed

Viti A., et al. Effect of exercise on plasma interferon levels. J. Appl. Physiol. 1985;59(2):426–428. PubMed

Yaar M., Palleroni A.V., Gilchrest B.A. Normal human epidermis contains an interferon-like protein. J. Cell Biol. 1986;103(4):1349–1354. PubMed PMC

Tovey M.G., et al. Interferon messenger RNA is produced constitutively in the organs of normal individuals. Proc. Natl. Acad. Sci. U. S. A. 1987;84(14):5038–5042. PubMed PMC

Stifter S.A., et al. Defining the distinct, intrinsic properties of the novel type I interferon, IFN. J. Biol. Chem. 2018;293(9):3168–3179. PubMed PMC

Sharkey D.J., et al. Seminal plasma differentially regulates inflammatory cytokine gene expression in human cervical and vaginal epithelial cells. Mol. Hum. Reprod. 2007;13(7):491–501. PubMed

Abdulhaqq S.A., et al. HIV-1-negative female sex workers sustain high cervical IFNvarepsilon, low immune activation, and low expression of HIV-1-required host genes. Mucosal Immunol. 2016;9(4):1027–1038. PubMed PMC

Garcia-Minambres A., et al. Interferon epsilon promotes HIV restriction at multiple steps of viral replication. Immunol. Cell Biol. 2017;95(5):478–483. PubMed

Tasker C., et al. IFN-epsilon protects primary macrophages against HIV infection. JCI Insight. 2016;1(20) PubMed PMC

Li S.F., et al. Type I interferons: distinct biological activities and current applications for viral infection. Cell. Physiol. Biochem. 2018;51(5):2377–2396. PubMed

Romero R., et al. Infection and labor. IV. Cachectin-tumor necrosis factor in the amniotic fluid of women with intraamniotic infection and preterm labor. Am. J. Obstet. Gynecol. 1989;161(2):336–341. PubMed

Romero R., et al. Tumor necrosis factor in preterm and term labor. Am. J. Obstet. Gynecol. 1992;166(5):1576–1587. PubMed

Romero R., et al. Evidence of perturbations of the cytokine network in preterm labor. Am. J. Obstet. Gynecol. 2015;213(6):836 e1–836 e18. PubMed PMC

Matsumiya T., Prescott S.M., Stafforini D.M. IFN-epsilon mediates TNF-alpha-induced STAT1 phosphorylation and induction of retinoic acid-inducible gene-I in human cervical cancer cells. J. Immunol. 2007;179(7):4542–4549. PubMed

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