The TLR2 ligand FSL-1 and the TLR5 ligand flagellin mediate pro-inflammatory and pro-labour response via MyD88/TRAF6/NF-κB-Dependent signalling

American Journal of Reproductive Immunology

Volumn 71, Issue 5, 2014, Pages 401-417

  Lim, Ratana ^a,b   Barker, Gillian ^a,b   Lappas, Martha ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MERCY HOSPITAL FOR WOMEN   (Australia)

Author keywords

Foetal membranes; MyD88; Myometrium; NFkappa B; TLR2; TLR5

Indexed keywords

3-(4-METHYLPHENYLSULFONYL)-2-PROPENENITRILE; CYCLOOXYGENASE 2; DIACYLGLYCEROL; FLAGELLIN; FSL-1 LIPOPROTEIN, SYNTHETIC; GELATINASE B; IL6 PROTEIN, HUMAN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; MMP9 PROTEIN, HUMAN; MYD88 PROTEIN, HUMAN; MYELOID DIFFERENTIATION FACTOR 88; NITRILE; OLIGOPEPTIDE; PTGS2 PROTEIN, HUMAN; SMALL INTERFERING RNA; SULFONE; TLR2 PROTEIN, HUMAN; TLR5 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 5; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; EMBRYO MEMBRANE; FEMALE; FETUS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MYOMETRIUM; PREGNANCY; SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUE;

CYCLOOXYGENASE 2; DIGLYCERIDES; EXTRAEMBRYONIC MEMBRANES; FEMALE; FETUS; FLAGELLIN; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-6; INTERLEUKIN-8; MATRIX METALLOPROTEINASE 9; MYELOID DIFFERENTIATION FACTOR 88; MYOMETRIUM; NF-KAPPA B; NITRILES; OLIGOPEPTIDES; PREGNANCY; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SULFONES; TISSUE CULTURE TECHNIQUES; TNF RECEPTOR-ASSOCIATED FACTOR 6; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 5;

EID: 84898812077     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12229     Document Type: Article

References (62)

1. Callaghan WM, MacDorman MF, Rasmussen SA, Qin C, Lackritz EM: The contribution of preterm birth to infant mortality rates in the United States. Pediatrics 2006; 118:1566-1573.
2. Saigal S, Doyle LW: an overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet 2008; 371:261-269.
3. Marlow N, Wolke D, Bracewell MA, Samara M, Grp ES: Neurologic and developmental disability at six years of age after extremely preterm birth. N Engl J Med 2005; 352:9-19.
4. Korvenranta E, Lehtonen L, Rautava L, Häkkinen U, Andersson S, Gissler M, Hallman M, Leipälä J, Peltola M, Tammela O, Linna M: Group ftPPIS: impact of very preterm birth on health care costs at five years of age. Pediatrics 2010; 125:e1109-e1114.
5. Hodek JM, von der Schulenburg JM, Mittendorf T: Measuring economic consequences of preterm birth - Methodological recommendations for the evaluation of personal burden on children and their caregivers. Health Econ Rev 2011; 1:6.
6. Romero R, Espinoza J, Kusanovic JP, Gotsch F, Hassan S, Erez O, Chaiworapongsa T, Mazor M: The preterm parturition syndrome. BJOG 2006; 113(Suppl 3):17-42.
7. Christiaens I, Zaragoza DB, Guilbert L, Robertson SA, Mitchell BF, Olson DM: Inflammatory processes in preterm and term parturition. J Reprod Immunol 2008; 79:50-57.
8. Menon R, Fortunato SJ: Infection and the role of inflammation in preterm premature rupture of the membranes. Best Pract Res Clin Obst Gynaecol 2007; 21:467-478.
9. Rice GE: Cytokines and the initiation of parturition. Front Horm Res 2001; 27:113-146.
10. 2 isozymes in pregnancy and parturition. Prostaglandins Leukot Essent Fatty Acids 2004; 70:87-100.
11. Bowen JM, Chamley L, Keelan JA, Mitchell MD: Cytokines of the placenta and extra-placental membranes: Roles and regulation during human pregnancy and parturition. Placenta 2002; 23:257-273.
12. Olson DM: The role of prostaglandins in the initiation of parturition. Best Pract Res Clin Obstet Gynaecol 2003; 17:717-730.
13. Fata JE, Ho AT, Leco KJ, Moorehead RA, Khokha R: Cellular turnover and extracellular matrix remodeling in female reproductive tissues: functions of metalloproteinases and their inhibitors. Cell Mol Life Sci 2000; 57:77-95.
14. Lappas M, Rice GE: The role and regulation of the nuclear factor kappa B signalling pathway in human labour. Placenta 2007; 28:543-556.
15. Lappas M, Rice GE: Transcriptional regulation of the processes of human labour and delivery. Placenta 2009; 30(Suppl A):S90-S95.
16. Lindstrom TM, Bennett PR: The role of nuclear factor kappa B in human labour. Reproduction 2005; 130:569-581.
17. Vasselon T, Detmers PA: Toll receptors: a central element in innate immune responses. Infect Immun 2002; 70:1033-1041.
18. Barton GM, Medzhitov R: Toll-like receptor signaling pathways. Science 2003; 300:1524-1525.
19. Muzio M, Natoli G, Saccani S, Levrero M, Mantovani A: The human toll signaling pathway: divergence of nuclear factor kappaB and JNK/SAPK activation upstream of tumor necrosis factor receptor-associated factor 6 (TRAF6). J Exp Med 1998; 187:2097-2101.
20. Medzhitov R, Preston-Hurlburt P, Kopp E, Stadlen A, Chen CQ, Ghosh S, Janeway CA: MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol Cell 1998; 2:253-258.
21. Nishimura M, Naito S: Tissue-specific mRNA expression profiles of human toll-like receptors and related genes. Biol Pharm Bull 2005; 28:886-892.
22. Patni S, Wynen LP, Seager AL, Morgan G, White JO, Thornton CA: Expression and activity of toll-like receptors 1-9 in the human term placenta and changes associated with labor at term. Biol Reprod 2009; 80:243-248.
23. Gillaux C, Mehats C, Vaiman D, Cabrol D, Breuiller-Fouche M: Functional screening of TLRs in human amniotic epithelial cells. J Immunol 2011; 187:2766-2774.
24. Thota C, Farmer T, Garfield RE, Menon R, Al-Hendy A: Vitamin D elicits anti-inflammatory response, inhibits contractile-associated proteins, and modulates Toll-like receptors in human myometrial cells. Reprod Sci 2013; 20:463-475.
25. Kim YM, Romero R, Chaiworapongsa T, Kim GJ, Kim MR, Kuivaniemi H, Tromp G, Espinoza J, Bujold E, Abrahams VM, Mor G: Toll-like receptor-2 and -4 in the chorioamniotic membranes in spontaneous labor at term and in preterm parturition that are associated with chorioamnionitis. Am J Obstet Gynecol 2004; 191:1346-1355.
26. Haddad R, Tromp G, Kuivaniemi H, Chaiworapongsa T, Kim YM, Mazor M, Romero R: Human spontaneous labor without histologic chorioamnionitis is characterized by an acute inflammation gene expression signature. Am J Obstet Gynecol 2006; 195(394):e391-324.
27. O'Brien M, Morrison JJ, Smith TJ: Upregulation of PSCDBP, TLR2, TWIST1, FLJ35382, EDNRB, and RGS12 gene expression in human myometrium at labor. Reprod Sci 2008; 15:382-393.
28. Ilievski V, Lu SJ, Hirsch E: Activation of toll-like receptors 2 or 3 and preterm delivery in the mouse. Reprod Sci 2007; 14:315-320.
29. Montalbano AP, Hawgood S, Mendelson CR: Mice deficient in surfactant protein A (SP-A) and SP-D or in TLR2 manifest delayed parturition and decreased expression of inflammatory and contractile genes. Endocrinology 2013; 154:483-498.
30. Herbst-Kralovetz MM, Quayle AJ, Ficarra M, Greene S, Rose WA 2nd, Chesson R, Spagnuolo RA, Pyles RB: Quantification and comparison of toll-like receptor expression and responsiveness in primary and immortalized human female lower genital tract epithelia. Am J Reprod Immunol 2008; 59:212-224.
31. Schaefer TM, Desouza K, Fahey JV, Beagley KW, Wira CR: Toll-like receptor (TLR) expression and TLR-mediated cytokine/chemokine production by human uterine epithelial cells. Immunology 2004; 112:428-436.
32. Rhee SH, Im E, Riegler M, Kokkotou E, O'Brien M, Pothoulakis C: Pathophysiological role of Toll-like receptor 5 engagement by bacterial flagellin in colonic inflammation. Proc Natl Acad Sci USA 2005; 102:13610-13615.
33. Liu S, Stolz DB, Sappington PL, Macias CA, Killeen ME, Tenhunen JJ, Delude RL, Fink MP: HMGB1 is secreted by immunostimulated enterocytes and contributes to cytomix-induced hyperpermeability of Caco-2 monolayers. Am J Physiol Cell Physiol 2006; 290:C990-C999.
34. Lim R, Barker G, Lappas M: SIRT6 is decreased with preterm labor and regulates key terminal effector pathways of human labor in fetal membranes. Biol Reprod 2013; 88:17.
35. Wall C, Lim R, Poljak M, Lappas M: Dietary flavonoids as therapeutics for preterm birth: luteolin and kaempferol suppress inflammation in human gestational tissues in vitro. Oxid Med Cell Longev 2013; 2013:10.
36. Lim R, Barker G, Riley C, Lappas M: Apelin is decreased with human preterm and term labor and regulates prolabor mediators in human primary amnion cells. Reprod Sci 2013; 20:957-967.
37. Lim R, Barker G, Lappas M: A novel role for FOXO3 in human labor: Increased expression in laboring myometrium, and regulation of pro-inflammatory and pro-labor mediators in pregnant human myometrial cells. Biol Reprod 2013; 88:156.
38. Lappas M: Forkhead box O1 (FOXO1) in pregnant human myometrial cells: A role as a pro-inflammatory mediator in human parturition. J Reprod Immunol 2013; 99:24-32.
39. Lappas M: NOD1 and NOD2 regulate proinflammatory and prolabor mediators in human fetal membranes and myometrium via nuclear factor-kappa B. Biol Reprod 2013; 89:14.
40. Lappas M, Permezel M, Rice GE: 15-Deoxy-Delta(12, 14)-prostaglandin J(2) and troglitazone regulation of the release of phospholipid metabolites, inflammatory cytokines and proteases from human gestational tissues. Placenta 2006; 27:1060-1072.
41. Goldenberg RL, Culhane JF, Iams JD, Romero R: Epidemiology and causes of preterm birth. Lancet 2008; 371:75-84.
42. Akira S, Hemmi H: Recognition of pathogen-associated molecular patterns by TLR family. Immunol Lett 2003; 85:85-95.
43. Dubicke A, Andersson P, Fransson E, Andersson E, Sioutas A, Malmstrom A, Sverremark-Ekstrom E, Ekman-Ordeberg G: High-mobility group box protein 1 and its signalling receptors in human preterm and term cervix. J Reprod Immunol 2010; 84:86-94.
44. Youssef RE, Ledingham MA, Bollapragada SS, O'Gorman N, Jordan F, Young A, Norman JE: The role of toll-like receptors (TLR-2 and-4) and triggering receptor expressed on myeloid cells 1 (TREM-1) in human term and preterm labor. Reprod Sci 2009; 16:843-856.
45. Holmlund U, Cebers G, Dahlfors AR, Sandstedt B, Bremme K, Ekstrom ES, Scheynius A: Expression and regulation of the pattern recognition receptors Toll-like receptor-2 and Toll-like receptor-4 in the human placenta. Immunology 2002; 107:145-151.
46. Dulay AT, Buhimschi CS, Zhao GM, Oliver EA, Mbele A, Jing SC, Buhimschi IA: Soluble TLR2 Is present in human amniotic fluid and modulates the intraamniotic inflammatory response to infection. J Immunol 2009; 182:7244-7253.
47. Mitsunari M, Yoshida S, Shoji T, Tsukihara S, Iwabe T, Harada T, Terakawa N: Macrophage-activating lipopeptide-2 induces cyclooxygenase-2 and prostaglandin E(2) via toll-like receptor 2 in human placental trophoblast cells. J Reprod Immunol 2006; 72:46-59.
48. Takeuchi O, Takeda K, Hoshino K, Adachi O, Ogawa T, Akira S: Cellular responses to bacterial cell wall components are mediated through MyD88-dependent signaling cascades. Int Immunol 2000; 12:113-117.
49. Takeuchi O, Kaufmann A, Grote K, Kawai T, Hoshino K, Morr M, Muhlradt PF, Akira S: Preferentially the R-stereoisomer of the mycoplasmal lipopeptide macrophage-activating lipopeptide-2 activates immune cells through a toll-like receptor 2-and MyD88-dependent signaling pathway. J Immunol 2000; 164:554-557.
50. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A: The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 2001; 410:1099-1103.
51. Filipovich Y, Lu SJ, Akira S, Hirsch E: The adaptor protein MyD88 is essential for E coli-induced preterm delivery in mice. Am J Obstet Gynecol 2009; 200:93.e1-e8.
52. Hindi SM, Paul PK, Dahiya S, Mishra V, Bhatnagar S, Kuang S, Choi Y, Kumar A: Reciprocal Interaction between TRAF6 and Notch Signaling Regulates Adult Myofiber Regeneration upon Injury. Mol Cell Biol 2012; 32:4833-4845.
53. Lappas M, Permezel M, Georgiou HM, Rice GE: Nuclear factor kappa B regulation of proinflammatory cytokines in human gestational tissues in vitro. Biol Reprod 2002; 67:668-673.
54. Lappas M, Permezel M, Georgiou HM, Rice GE: Regulation of phospholipase isozymes by nuclear factor-kappaB in human gestational tissues in vitro. J Clin Endocrinol Metab 2004; 89:2365-2372.
55. Lappas M, Permezel M, Rice GE: N-Acetyl-cysteine inhibits phospholipid metabolism, proinflammatory cytokine release, protease activity, and nuclear factor-kappaB deoxyribonucleic acid-binding activity in human fetal membranes in vitro. J Clin Endocrinol Metab 2003; 88:1723-1729.
56. Helliwell RJ, Adams LF, Mitchell MD: Prostaglandin synthases: recent developments and a novel hypothesis. Prostaglandins Leukot Essent Fatty Acids 2004; 70:101-113.
57. Watanabe K: Prostaglandin F synthase. Prostaglandins Other Lipid Mediat 2002; 68-69:401-407.
58. Keelan JA, Blumenstein M, Helliwell RJ, Sato TA, Marvin KW, Mitchell MD: Cytokines, prostaglandins and parturition-a review. Placenta 2003; 24(Suppl A):S33-S46.
59. Sparey C, Robson SC, Bailey J, Lyall F, Europe-Finner GN: The differential expression of myometrial connexin-43, cyclooxygenase-1 and -2, and Gs alpha proteins in the upper and lower segments of the human uterus during pregnancy and labor. J Clin Endocrinol Metab 1999; 84:1705-1710.
60. Vadillo-Ortega F, Estrada-Gutierrez G: Role of matrix metalloproteinases in preterm labour. BJOG 2005; 112(Suppl 1):19-22.
61. Blencowe H, Cousens S, Oestergaard MZ, Chou D, Moller AB, Narwal R, Adler A, Garcia CV, Rohde S, Say L, Lawn JE: National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet 2012; 379:2162-2172.
62. Krediet TG, Wiertsema SP, Vossers MJ, Hoeks S, Fleer A, Ruven HJT, Rijkers GT: Toll-like receptor 2 polymorphism is associated with preterm birth. Pediatr Res 2007; 62:474-476.