Journal of Reproductive Immunology
Volume 84, Issue 2 , Pages 176-185 , March 2010

Pro-inflammatory and anti-inflammatory cytokines in human preterm and term cervical ripening

  • Aurelija Dubicke

      Affiliations

    • Department of Woman and Child Health, Karolinska Institute, FRH-lab C4:U1, KBH, 171 76 Stockholm, Sweden
    • Corresponding Author InformationCorresponding author. Tel.: +46 851773818; fax: +46 8323048.
  • ,
  • Emma Fransson

      Affiliations

    • Department of Woman and Child Health, Karolinska Institute, FRH-lab C4:U1, KBH, 171 76 Stockholm, Sweden
  • ,
  • Gabriele Centini

      Affiliations

    • Department of Pediatrics, Obstetrics and Reproductive Medicine, University of Siena, 53100 Siena, Italy
  • ,
  • Eva Andersson

      Affiliations

    • Department of Woman and Child Health, Karolinska Institute, FRH-lab C4:U1, KBH, 171 76 Stockholm, Sweden
  • ,
  • Birgitta Byström

      Affiliations

    • Department of Woman and Child Health, Karolinska Institute, FRH-lab C4:U1, KBH, 171 76 Stockholm, Sweden
  • ,
  • Anders Malmström

      Affiliations

    • Department of Experimental Medical Science, University of Lund, 221 84 Lund, Sweden
  • ,
  • Felice Petraglia

      Affiliations

    • Department of Pediatrics, Obstetrics and Reproductive Medicine, University of Siena, 53100 Siena, Italy
  • ,
  • Eva Sverremark-Ekström

      Affiliations

    • Department of Immunology, The Wenner-Gren Institute, Stockholm University, 106 91 Stockholm, Sweden
  • ,
  • Gunvor Ekman-Ordeberg

      Affiliations

    • Department of Woman and Child Health, Karolinska Institute, FRH-lab C4:U1, KBH, 171 76 Stockholm, Sweden

Received 23 June 2009 ,Revised 12 December 2009 ,Accepted 15 December 2009.

References 

  1. Bachmayer N, Rafik Hamad R, Liszka L, Bremme K, Sverremark-Ekstrom E. Aberrant uterine natural killer (NK)-cell expression and altered placental and serum levels of the NK-cell promoting cytokine interleukin-12 in pre-eclampsia. Am. J. Reprod. Immunol. 2006;56(5–6):292–301
  2. Brown NL, Alvi SA, Elder MG, Bennett PR, Sullivan MH. The regulation of prostaglandin output from term intact fetal membranes by anti-inflammatory cytokines. Immunology. 2000;99(1):124–133
  3. Challis JR, Lockwood CJ, Myatt L, Norman JE, Strauss JF, Petraglia F. Inflammation and pregnancy. Reprod. Sci. 2009;16(2):206–215
  4. Chaouat G. The Th1/Th2 paradigm: still important in pregnancy?. Semin. Immunopathol. 2007;29(2):95–113
  5. de Gruijl TD, Bontkes HJ, van den Muysenberg AJ, van Oostveen JW, Stukart MJ, Verheijen RH, et al. Differences in cytokine mRNA profiles between premalignant and malignant lesions of the uterine cervix. Eur. J. Cancer. 1999;35(3):490–497
  6. Dubicke A, Akerud A, Sennstrom M, Hamad RR, Bystrom B, Malmstrom A, et al. Different secretion patterns of matrix metalloproteinases and IL-8 and effect of corticotropin-releasing hormone in preterm and term cervical fibroblasts. Mol. Hum. Reprod. 2008;14(11):641–647
  7. Dudley DJ, Hunter C, Varner MW, Mitchell MD. Elevation of amniotic fluid interleukin-4 concentrations in women with preterm labor and chorioamnionitis. Am. J. Perinatol. 1996;13(7):443–447
  8. Ekelund CK, Vogel I, Skogstrand K, Thorsen P, Hougaard DM, Langhoff-Roos J, et al. Interleukin-18 and interleukin-12 in maternal serum and spontaneous preterm delivery. J. Reprod. Immunol. 2008;77(2):179–185
  9. El-Shazly S, Makhseed M, Azizieh F, Raghupathy R. Increased expression of pro-inflammatory cytokines in placentas of women undergoing spontaneous preterm delivery or premature rupture of membranes. Am. J. Reprod. Immunol. 2004;52(1):45–52
  10. Fortunato SJ, Menon R, Lombardi SJ. Interleukin-10 and transforming growth factor-beta inhibit amniochorion tumor necrosis factor-alpha production by contrasting mechanisms of action: therapeutic implications in prematurity. Am. J. Obstet. Gynecol. 1997;177(4):803–809
  11. Fortunato SJ, Menon R, Lombardi SJ. The effect of transforming growth factor and interleukin-10 on interleukin-8 release by human amniochorion may regulate histologic chorioamnionitis. Am. J. Obstet. Gynecol. 1998;179(3 Pt 1):794–799
  12. Fortunato SJ, Menon R, Swan KF, Lombardi SJ. Interleukin-10 inhibition of interleukin-6 in human amniochorionic membrane: transcriptional regulation. Am. J. Obstet. Gynecol. 1996;175(4 Pt 1):1057–1065
  13. Gargano JW, Holzman C, Senagore P, Thorsen P, Skogstrand K, Hougaard DM, et al. Mid-pregnancy circulating cytokine levels, histologic chorioamnionitis and spontaneous preterm birth. J. Reprod. Immunol. 2008;79(1):100–110
  14. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet. 2008;371(9606):75–84
  15. Gotsch F, Romero R, Kusanovic JP, Erez O, Espinoza J, Kim CJ, et al. The anti-inflammatory limb of the immune response in preterm labor, intra-amniotic infection/inflammation, and spontaneous parturition at term: a role for interleukin-10. J. Matern. Fetal Neonatal Med. 2008;21(8):529–547
  16. Hanna N, Bonifacio L, Weinberger B, Reddy P, Murphy S, Romero R, et al. Evidence for interleukin-10-mediated inhibition of cyclo-oxygenase-2 expression and prostaglandin production in preterm human placenta. Am. J. Reprod. Immunol. 2006;55(1):19–27
  17. Jacobsson B, Holst RM, Mattsby-Baltzer I, Nikolaitchouk N, Wennerholm UB, Hagberg H. Interleukin-18 in cervical mucus and amniotic fluid: relationship to microbial invasion of the amniotic fluid, intra-amniotic inflammation and preterm delivery. Bjog. 2003;110(6):598–603
  18. Klimaviciute A, Calciolari J, Bertucci E, Abelin Tornblom S, Stjernholm-Vladic Y, Bystrom B, et al. Corticotropin-releasing hormone, its binding protein and receptors in human cervical tissue at preterm and term labor in comparison to non-pregnant state. Reprod. Biol. Endocrinol. 2006;4(1):29
  19. Menon R, Lombardi SJ, Fortunato SJ. IL-18, a product of choriodecidual cells, increases during premature rupture of membranes but fails to turn on the Fas-FasL-mediated apoptosis pathway. J. Assist. Reprod. Genet. 2001;18(5):276–284
  20. Mitchell MD, Simpson KL, Keelan JA. Paradoxical proinflammatory actions of interleukin-10 in human amnion: potential roles in term and preterm labour. J. Clin. Endocrinol. Metab. 2004;89(8):4149–4152
  21. Mueller T, Terada T, Rosenberg IM, Shibolet O, Podolsky DK. Th2 cytokines down-regulate TLR expression and function in human intestinal epithelial cells. J. Immunol. 2006;176(10):5805–5814
  22. Nicol AF, Fernandes AT, Grinsztejn B, Russomano FJRES, Tristao A, et al. Distribution of immune cell subsets and cytokine-producing cells in the uterine cervix of human papillomavirus (HPV)-infected women: influence of HIV-1 coinfection. Diagn. Mol. Pathol. 2005;14(1):39–47
  23. Osman I, Young A, Ledingham MA, Thomson AJ, Jordan F, Greer IA, et al. Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labour at term. Mol. Hum. Reprod. 2003;9(1):41–45
  24. Raghupathy R. Th1-type immunity is incompatible with successful pregnancy. Immunol. Today. 1997;18(10):478–482
  25. Raghupathy R, Kalinka J. Cytokine imbalance in pregnancy complications and its modulation. Front. Biosci. 2008;13:985–994
  26. Sadowsky DW, Novy MJ, Witkin SS, Gravett MG. Dexamethasone or interleukin-10 blocks interleukin-1beta-induced uterine contractions in pregnant rhesus monkeys. Am. J. Obstet. Gynecol. 2003;188(1):252–263
  27. Sahlin L, Stjernholm-Vladic Y, Roos N, Masironi B, Ekman-Ordeberg G. Impaired leukocyte influx in cervix of postterm women not responding to prostaglandin priming. Reprod. Biol. Endocrinol. 2008;6:36
  28. Sato TA, Keelan JA, Mitchell MD. Critical paracrine interactions between TNFalpha and IL-10 regulate lipopolysaccharide-stimulated human choriodecidual cytokine and prostaglandin E2 production. J. Immunol. 2003;170(1):158–166
  29. Sennstrom MB, Brauner A, Bystrom B, Malmstrom A, Ekman G. Matrix metalloproteinase-8 correlates with the cervical ripening process in humans. Acta Obstet. Gynecol. Scand. 2003;82(10):904–911
  30. Sennstrom MB, Ekman G, Westergren-Thorsson G, Malmstrom A, Bystrom B, Endresen U, et al. Human cervical ripening, an inflammatory process mediated by cytokines. Mol. Hum. Reprod. 2000;6(4):375–381
  31. Sennstrom MB, Granstrom LM, Lockwood CJ, Omazic B, Johansson O, Malmstrom A, et al. Cervical fetal fibronectin correlates to prostaglandin E2-induced cervical ripening and can be identified in cervical tissue. Am. J. Obstet. Gynecol. 1998;178(3):540–545
  32. Simhan HN, Krohn MA. First-trimester cervical inflammatory milieu and subsequent early preterm birth. Am. J. Obstet. Gynecol. 2009;
  33. Spaziani EP, Lantz ME, Benoit RR, O’Brien WF. The induction of cyclooxygenase-2 (COX-2) in intact human amnion tissue by interleukin-4. Prostaglandins. 1996;51(3):215–223
  34. Tornblom SA, Klimaviciute A, Bystrom B, Chromek M, Brauner A, Ekman-Ordeberg G. Non-infected preterm parturition is related to increased concentrations of IL-6, IL-8 and MCP-1 in human cervix. Reprod. Biol. Endocrinol. 2005;3:39
  35. Tornblom SA, Patel FA, Bystrom B, Giannoulias D, Malmstrom A, Sennstrom M, et al. 15-hydroxyprostaglandin dehydrogenase and cyclooxygenase 2 messenger ribonucleic acid expression and immunohistochemical localization in human cervical tissue during term and preterm labor. J. Clin. Endocrinol. Metab. 2004;89(6):2909–2915
  36. Trautman MS, Collmer D, Edwin SS, White W, Mitchell MD, Dudley DJ. Expression of interleukin-10 in human gestational tissues. J. Soc. Gynecol. Investig. 1997;4(5):247–253
  37. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3(7):RESEARCH0034
  38. Wang P, Wu P, Siegel MI, Egan RW, Billah MM. Interleukin (IL)-10 inhibits nuclear factor kappa B (NF kappa B) activation in human monocytes, IL-10 and IL-4 suppress cytokine synthesis by different mechanisms. J. Biol. Chem. 1995;270(16):9558–9563
  39. Wegmann TG, Lin H, Guilbert L, Mosmann TR. Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon?. Immunol. Today. 1993;14(7):353–356

PII: S0165-0378(10)00010-0

doi: 10.1016/j.jri.2009.12.004

Journal of Reproductive Immunology
Volume 84, Issue 2 , Pages 176-185 , March 2010