Placenta
Volume 30, Issue 2 , Pages 111-123 , February 2009

Human Tumour Necrosis Factor: Physiological and Pathological Roles in Placenta and Endometrium

,Accepted 16 October 2008.

References 

  1. Carswell EA, Old LJ, Kassel RL, Green S, Fiore N, Williamson B. An endotoxin-induced serum factor that causes necrosis of tumors. Proc Natl Acad Sci U S A. 1975;72:3666–3670
  2. Pennica D, Nedwin GE, Hayflick JS, Seeburg PH, Derynck R, Palladino MA, et al. Human tumour necrosis factor: precursor structure, expression and homology to lymphotoxin. Nature. 1984;312:724–729
  3. Nedwin GE, Naylor SL, Sakaguchi AY, Smith D, Jarrett-Nedwin J, Pennica D, et al. Human lymphotoxin and tumor necrosis factor genes: structure, homology and chromosomal localization. Nucleic Acids Res. 1985;13:6361–6373
  4. Old LJ. Tumor necrosis factor (TNF). Science. 1985;230:630–632
  5. Aggarwal BB, Aiyer RA, Pennica D, Gray PW, Goeddel DV. Human tumour necrosis factors: structure and receptor interactions. Ciba Found Symp. 1987;131:39–51
  6. Narachi MA, Davis JM, Hsu YR, Arakawa T. Role of single disulfide in recombinant human tumor necrosis factor-alpha. J Biol Chem. 1987;262:13107–13110
  7. Zhang G. Tumor necrosis factor family ligand-receptor binding. Curr Opin Struct Biol. 2004;14:154–160
  8. Kriegler M, Perez C, DeFay K, Albert I, Lu SD. A novel form of TNF/cachectin is a cell surface cytotoxic transmembrane protein: ramifications for the complex physiology of TNF. Cell. 1988;53:45–53
  9. Tang P, Hung MC, Klostergaard J. Human pro-tumor necrosis factor is a homotrimer. Biochemistry. 1996;35:8216–8225
  10. Eck MJ, Sprang SR. The structure of tumor necrosis factor-alpha at 2.6A resolution. Implications for receptor binding. J Biol Chem. 1989;264:17595–17605
  11. Black RA, Rauch CT, Kozlosky CJ, Peschon JJ, Slack JL, Wolfson MF, et al. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature. 1997;385:729–733
  12. Locksley RM, Killeen N, Lenardo MJ. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell. 2001;104:487–501
  13. Smith CA, Farrah T, Goodwin RG. The TNF receptor superfamily of cellular and viral proteins: activation, costimulation, and death. Cell. 1994;76:959–962
  14. Naismith JH, Sprang SR. Modularity in the TNF-receptor family. Trends Biochem Sci. 1998;23:74–79
  15. Chan FK, Chun HJ, Zheng L, Siegel RM, Bui KL, Lenardo MJ. A domain in TNF receptors that mediates ligand-independent receptor assembly and signaling. Science. 2000;288:2351–2354
  16. Wajant H, Pfizenmaier K, Scheurich P. Tumor necrosis factor signaling. Cell Death Differ. 2003;10:45–65
  17. Grell M, Douni E, Wajant H, Lohden M, Clauss M, Maxeiner B, et al. The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80kDa tumor necrosis factor receptor. Cell. 1995;83:793–802
  18. Wallach D, Engelmann H, Nophar Y, Aderka D, Kemper O, Hornik V, et al. Soluble and cell surface receptors for tumor necrosis factor. Agents Actions Suppl. 1991;35:51–57
  19. Solomon KA, Pesti N, Wu G, Newton RC. Cutting edge: a dominant negative form of TNF-alpha converting enzyme inhibits proTNF and TNFRII secretion. J Immunol. 1999;163:4105–4108
  20. McDermott MF, Aksentijevich I, Galon J, McDermott EM, Ogunkolade BW, Centola M, et al. Germline mutations in the extracellular domains of the 55kDa TNF receptor, TNFR1, define a family of dominantly inherited autoinflammatory syndromes. Cell. 1999;97:133–144
  21. Sriram K, O'Callaghan JP. Divergent roles for tumor necrosis factor-alpha in the brain. J Neuroimmune Pharmacol. 2007;2:140–153
  22. Taylor PC, Peters AM, Paleolog E, Chapman PT, Elliott MJ, McCloskey R, et al. Reduction of chemokine levels and leukocyte traffic to joints by tumor necrosis factor alpha blockade in patients with rheumatoid arthritis. Arthritis Rheum. 2000;43:38–47
  23. Blam ME, Stein RB, Lichtenstein GR. Integrating anti-tumor necrosis factor therapy in inflammatory bowel disease: current and future perspectives. Am J Gastroenterol. 2001;96:1977–1997
  24. Feldmann M, Maini RN. Lasker clinical medical research award. TNF defined as a therapeutic target for rheumatoid arthritis and other autoimmune diseases. Nat Med. 2003;9:1245–1250
  25. Mannel DN, Echtenacher B. TNF in the inflammatory response. Chem Immunol. 2000;74:141–161
  26. Beutler B, Greenwald D, Hulmes JD, Chang M, Pan YC, Mathison J, et al. Identity of tumour necrosis factor and the macrophage-secreted factor cachectin. Nature. 1985;316:552–554
  27. Ledgerwood EC, Pober JS, Bradley JR. Recent advances in the molecular basis of TNF signal transduction. Lab Invest. 1999;79:1041–1050
  28. Bradley JR. TNF-mediated inflammatory disease. J Pathol. 2008;214:149–160
  29. Jiang Y, Woronicz JD, Liu W, Goeddel DV. Prevention of constitutive TNF receptor 1 signaling by silencer of death domains. Science. 1999;283:543–546
  30. Hsu H, Huang J, Shu HB, Baichwal V, Goeddel DV. TNF-dependent recruitment of the protein kinase RIP to the TNF receptor-1 signaling complex. Immunity. 1996;4:387–396
  31. Yang J, Lin Y, Guo Z, Cheng J, Huang J, Deng L, et al. The essential role of MEKK3 in TNF-induced NF-kappaB activation. Nat Immunol. 2001;2:620–624
  32. Devin A, Lin Y, Yamaoka S, Li Z, Karin M, Liu Z. The alpha and beta subunits of IkappaB kinase (IKK) mediate TRAF2-dependent IKK recruitment to tumor necrosis factor (TNF) receptor 1 in response to TNF. Mol Cell Biol. 2001;21:3986–3994
  33. Schutze S, Machleidt T, Adam D, Schwandner R, Wiegmann K, Kruse ML, et al. Inhibition of receptor internalization by monodansylcadaverine selectively blocks p55 tumor necrosis factor receptor death domain signaling. J Biol Chem. 1999;274:10203–10212
  34. Wang L, Du F, Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell. 2008;133:693–703
  35. Ichijo H, Nishida E, Irie K, ten Dijke P, Saitoh M, Moriguchi T, et al. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science. 1997;275:90–94
  36. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, Takeda K, et al. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep. 2001;2:222–228
  37. Rivas MA, Carnevale RP, Proietti CJ, Rosemblit C, Beguelin W, Salatino M, et al. TNF alpha acting on TNFR1 promotes breast cancer growth via p42/P44 MAPK, JNK, Akt and NF-kappa B-dependent pathways. Exp Cell Res. 2008;314:509–529
  38. MacEwan DJ. TNF receptor subtype signalling: differences and cellular consequences. Cell Signal. 2002;14:477–492
  39. Zhang R, Xu Y, Ekman N, Wu Z, Wu J, Alitalo K, et al. Etk/Bmx transactivates vascular endothelial growth factor 2 and recruits phosphatidylinositol 3-kinase to mediate the tumor necrosis factor-induced angiogenic pathway. J Biol Chem. 2003;278:51267–51276
  40. Jaattela M, Kuusela P, Saksela E. Demonstration of tumor necrosis factor in human amniotic fluids and supernatants of placental and decidual tissues. Lab Invest. 1988;58:48–52
  41. Chen HL, Yang YP, Hu XL, Yelavarthi KK, Fishback JL, Hunt JS. Tumor necrosis factor alpha mRNA and protein are present in human placental and uterine cells at early and late stages of gestation. Am J Pathol. 1991;139:327–335
  42. Hunt JS, Chen HL, Hu XL, Tabibzadeh S. Tumor necrosis factor-alpha messenger ribonucleic acid and protein in human endometrium. Biol Reprod. 1992;47:141–147
  43. Yang Y, Yelavarthi KK, Chen HL, Pace JL, Terranova PF, Hunt JS. Molecular, biochemical, and functional characteristics of tumor necrosis factor-alpha produced by human placental cytotrophoblastic cells. J Immunol. 1993;150:5614–5624
  44. Vince G, Shorter S, Starkey P, Humphreys J, Clover L, Wilkins T, et al. Localization of tumour necrosis factor production in cells at the materno/fetal interface in human pregnancy. Clin Exp Immunol. 1992;88:174–180
  45. Philippeaux MM, Piguet PF. Expression of tumor necrosis factor-alpha and its mRNA in the endometrial mucosa during the menstrual cycle. Am J Pathol. 1993;143:480–486
  46. von Wolff M, Classen-Linke I, Heid D, Krusche CA, Beier-Hellwig K, Karl C, et al. Tumour necrosis factor-alpha (TNF-alpha) in human endometrium and uterine secretion: an evaluation by immunohistochemistry, ELISA and semiquantitative RT-PCR. Mol Hum Reprod. 1999;5:146–152
  47. Jokhi PP, King A, Sharkey AM, Smith SK, Loke YW. Screening for cytokine messenger ribonucleic acids in purified human decidual lymphocyte populations by the reverse-transcriptase polymerase chain reaction. J Immunol. 1994;153:4427–4435
  48. Tabibzadeh S. Ubiquitous expression of TNF-alpha/cachectin immunoreactivity in human endometrium. Am J Reprod Immunol. 1991;26:1–4
  49. Jokhi PP, King A, Loke YW. Cytokine production and cytokine receptor expression by cells of the human first trimester placental-uterine interface. Cytokine. 1997;9:126–137
  50. Gustafsson C, Hummerdal P, Matthiesen L, Berg G, Ekerfelt C, Ernerudh J. Cytokine secretion in decidual mononuclear cells from term human pregnancy with or without labour: ELISPOT detection of IFN-gamma, IL-4, IL-10, TGF-beta and TNF-alpha. J Reprod Immunol. 2006;71:41–56
  51. Bergqvist A, Nejaty H, Froysa B, Bruse C, Carlberg M, Sjoblom P, et al. Production of interleukins 1beta, 6 and 8 and tumor necrosis factor alpha in separated and cultured endometrial and endometriotic stromal and epithelial cells. Gynecol Obstet Invest. 2000;50:1–6
  52. Witkin SS, Liu HC, Davis OK, Rosenwaks Z. Tumor necrosis factor is present in maternal sera and embryo culture fluids during in vitro fertilization. J Reprod Immunol. 1991;19:85–93
  53. King A, Jokhi PP, Smith SK, Sharkey AM, Loke YW. Screening for cytokine mRNA in human villous and extravillous trophoblasts using the reverse-transcriptase polymerase chain reaction (RT-PCR). Cytokine. 1995;7:364–371
  54. Hung TH, Charnock-Jones DS, Skepper JN, Burton GJ. Secretion of tumor necrosis factor-alpha from human placental tissues induced by hypoxia-reoxygenation causes endothelial cell activation in vitro: a potential mediator of the inflammatory response in preeclampsia. Am J Pathol. 2004;164:1049–1061
  55. Pijnenborg R, McLaughlin PJ, Vercruysse L, Hanssens M, Johnson PM, Keith JC, et al. Immunolocalization of tumour necrosis factor-alpha (TNF-alpha) in the placental bed of normotensive and hypertensive human pregnancies. Placenta. 1998;19:231–239
  56. Tabibzadeh S, Zupi E, Babaknia A, Liu R, Marconi D, Romanini C. Site and menstrual cycle-dependent expression of proteins of the tumour necrosis factor (TNF) receptor family, and BCL-2 oncoprotein and phase-specific production of TNF alpha in human endometrium. Hum Reprod. 1995;10:277–286
  57. Hunt JS, Chen HL, Miller L. Tumor necrosis factors: pivotal components of pregnancy?. Biol Reprod. 1996;54:554–562
  58. Yelavarthi KK, Hunt JS. Analysis of p60 and p80 tumor necrosis factor-alpha receptor messenger RNA and protein in human placentas. Am J Pathol. 1993;143:1131–1141
  59. Knofler M, Mosl B, Bauer S, Griesinger G, Husslein P. TNF-alpha/TNFRI in primary and immortalized first trimester cytotrophoblasts. Placenta. 2000;21:525–535
  60. Austgulen R, Espevik T, Mecsei R, Scott H. Expression of receptors for tumor necrosis factor in human placenta at term. Acta Obstet Gynecol Scand. 1992;71:417–424
  61. Yui J, Hemmings D, Garcia-Lloret M, Guilbert LJ. Expression of the human p55 and p75 tumor necrosis factor receptors in primary villous trophoblasts and their role in cytotoxic signal transduction. Biol Reprod. 1996;55:400–409
  62. Knofler M, Stenzel M, Husslein P. Shedding of tumour necrosis factor receptors from purified villous term trophoblasts and cytotrophoblastic BeWo cells. Hum Reprod. 1998;13:2308–2316
  63. Austgulen R, Liabakk NB, Brockhaus M, Espevik T. Soluble TNF receptors in amniotic fluid and in urine from pregnant women. J Reprod Immunol. 1992;22:105–116
  64. Bornstein SR, Rutkowski H, Vrezas I. Cytokines and steroidogenesis. Mol Cell Endocrinol. 2004;215:135–141
  65. Wuttke W, Jarry H, Pitzel L, Knoke I, Spiess S. Luteotrophic and luteolytic actions of ovarian peptides. Hum Reprod. 1993;8(Suppl 2):141–146
  66. Terranova PF, Rice VM. Review: cytokine involvement in ovarian processes. Am J Reprod Immunol. 1997;37:50–63
  67. Yui J, Garcia-Lloret M, Wegmann TG, Guilbert LJ. Cytotoxicity of tumour necrosis factor-alpha and gamma-interferon against primary human placental trophoblasts. Placenta. 1994;15:819–835
  68. Straszewski-Chavez SL, Visintin IP, Karassina N, Los G, Liston P, Halaban R, et al. XAF1 mediates tumor necrosis factor-alpha-induced apoptosis and X-linked inhibitor of apoptosis cleavage by acting through the mitochondrial pathway. J Biol Chem. 2007;282:13059–13072
  69. Garcia-Lloret MI, Yui J, Winkler-Lowen B, Guilbert LJ. Epidermal growth factor inhibits cytokine-induced apoptosis of primary human trophoblasts. J Cell Physiol. 1996;167:324–332
  70. Pijnenborg R, Luyten C, Vercruysse L, Keith JC, Van Assche FA. Cytotoxic effects of tumour necrosis factor (TNF)-alpha and interferon-gamma on cultured human trophoblast are modulated by fibronectin. Mol Hum Reprod. 2000;6:635–641
  71. Smith S, Francis R, Guilbert L, Baker PN. Growth factor rescue of cytokine mediated trophoblast apoptosis. Placenta. 2002;23:322–330
  72. Smith SC, Guilbert LJ, Yui J, Baker PN, Davidge ST. The role of reactive nitrogen/oxygen intermediates in cytokine-induced trophoblast apoptosis. Placenta. 1999;20:309–315
  73. Garcia-Lloret MI, Winkler-Lowen B, Guilbert LJ. Monocytes adhering by LFA-1 to placental syncytiotrophoblasts induce local apoptosis via release of TNF-alpha. A model for hematogenous initiation of placental inflammations. J Leukoc Biol. 2000;68:903–908
  74. Bauer S, Pollheimer J, Hartmann J, Husslein P, Aplin JD, Knofler M. Tumor necrosis factor-alpha inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first-trimester villous explant cultures. J Clin Endocrinol Metab. 2004;89:812–822
  75. Fukushima K, Miyamoto S, Komatsu H, Tsukimori K, Kobayashi H, Seki H, et al. TNFalpha-induced apoptosis and integrin switching in human extravillous trophoblast cell line. Biol Reprod. 2003;68:1771–1778
  76. Boyle JJ, Weissberg PL, Bennett MR. Tumor necrosis factor-alpha promotes macrophage-induced vascular smooth muscle cell apoptosis by direct and autocrine mechanisms. Arterioscler Thromb Vasc Biol. 2003;23:1553–1558
  77. Harris LK, Keogh RJ, Wareing M, Baker PN, Cartwright JE, Aplin JD, et al. Invasive trophoblasts stimulate vascular smooth muscle cell apoptosis by a fas ligand-dependent mechanism. Am J Pathol. 2006;169:1863–1874
  78. Keogh RJ, Harris LK, Freeman A, Baker PN, Aplin JD, Whitley GS, et al. Fetal-derived trophoblast use the apoptotic cytokine tumor necrosis factor-alpha-related apoptosis-inducing ligand to induce smooth muscle cell death. Circ Res. 2007;100:834–841
  79. Knofler M, Saleh L, Bauer S, Galos B, Rotheneder H, Husslein P, et al. Transcriptional regulation of the human chorionic gonadotropin beta gene during villous trophoblast differentiation. Endocrinology. 2004;145:1685–1694
  80. Knofler M, Saleh L, Bauer S, Vasicek R, Griesinger G, Strohmer H, et al. Promoter elements and transcription factors involved in differentiation-dependent human chorionic gonadotrophin-alpha messenger ribonucleic acid expression of term villous trophoblasts. Endocrinology. 2000;141:3737–3748
  81. Ringler GE, Kao LC, Miller WL, Strauss JF. Effects of 8-bromo-cAMP on expression of endocrine functions by cultured human trophoblast cells. Regulation of specific mRNAs. Mol Cell Endocrinol. 1989;61:13–21
  82. Marth C, Brattia M, Muller-Holzner E, Mayer I, Zech J, Tabarelli M, et al. Modulation of secretion of human chorionic gonadotropin by biologic response modifiers on term placenta and choriocarcinoma cells. Mol Biother. 1989;1:140–144
  83. Pedersen AM, Fulton SK, Porter L, Francis GL. Tumor necrosis factor-alpha affects in vitro hormone production by JEG-3 choriocarcinoma cell cultures. J Reprod Immunol. 1995;29:69–80
  84. Yanushpolsky EH, Ozturk M, Polgar K, Berkowitz RS, Hill JA. The effects of cytokines on human chorionic gonadotropin (hCG) production by a trophoblast cell line. J Reprod Immunol. 1993;25:235–247
  85. Monzon-Bordonaba F, Vadillo-Ortega F, Feinberg RF. Modulation of trophoblast function by tumor necrosis factor-alpha: a role in pregnancy establishment and maintenance?. Am J Obstet Gynecol. 2002;187:1574–1580
  86. Leisser C, Saleh L, Haider S, Husslein H, Sonderegger S, Knofler M. Tumour necrosis factor-alpha impairs chorionic gonadotrophin beta-subunit expression and cell fusion of human villous cytotrophoblast. Mol Hum Reprod. 2006;12:601–609
  87. Hamada AL, Nakabayashi K, Sato A, Kiyoshi K, Takamatsu Y, Laoag-Fernandez JB, et al. Transfection of antisense chorionic gonadotropin beta gene into choriocarcinoma cells suppresses the cell proliferation and induces apoptosis. J Clin Endocrinol Metab. 2005;90:4873–4879
  88. Hunt JS, Atherton RA, Pace JL. Differential responses of rat trophoblast cells and embryonic fibroblasts to cytokines that regulate proliferation and class I MHC antigen expression. J Immunol. 1990;145:184–189
  89. Pampfer S, Vanderheyden I, Vesela J, De Hertogh R. Neutralization of tumor necrosis factor alpha (TNF alpha) action on cell proliferation in rat blastocysts by antisense oligodeoxyribonucleotides directed against TNF alpha p60 receptor. Biol Reprod. 1995;52:1316–1326
  90. Kawamura K, Kawamura N, Kumagai J, Fukuda J, Tanaka T. Tumor necrosis factor regulation of apoptosis in mouse preimplantation embryos and its antagonism by transforming growth factor alpha/phosphatidylionsitol 3-kinase signaling system. Biol Reprod. 2007;76:611–618
  91. Pampfer S, Moulaert B, Vanderheyden I, Wuu YD, De Hertogh R. Effect of tumour necrosis factor alpha on rat blastocyst growth and glucose metabolism. J Reprod Fertil. 1994;101:199–206
  92. Drake BL, Head JR. Murine trophoblast cells are not killed by tumor necrosis factor-alpha. J Reprod Immunol. 1990;17:93–99
  93. Whiteside EJ, Boucaut KJ, Teh A, Garcia-Aragon J, Harvey MB, Herington AC. Elevated concentration of TNF-alpha induces trophoblast differentiation in mouse blastocyst outgrowths. Cell Tissue Res. 2003;314:275–280
  94. Huber AV, Saleh L, Bauer S, Husslein P, Knofler M. TNFalpha-mediated induction of PAI-1 restricts invasion of HTR-8/SVneo trophoblast cells. Placenta. 2006;27:127–136
  95. Rasmussen CA, Pace JL, Banerjee S, Phillips TA, Hunt JS. Trophoblastic cell lines generated from tumour necrosis factor receptor-deficient mice reveal specific functions for the two tumour necrosis factor receptors. Placenta. 1999;20:213–222
  96. Reister F, Frank HG, Kingdom JC, Heyl W, Kaufmann P, Rath W, et al. Macrophage-induced apoptosis limits endovascular trophoblast invasion in the uterine wall of preeclamptic women. Lab Invest. 2001;81:1143–1152
  97. Todt JC, Yang Y, Lei J, Lauria MR, Sorokin Y, Cotton DB, et al. Effects of tumor necrosis factor-alpha on human trophoblast cell adhesion and motility. Am J Reprod Immunol. 1996;36:65–71
  98. Lala PK, Chakraborty C. Factors regulating trophoblast migration and invasiveness: possible derangements contributing to pre-eclampsia and fetal injury. Placenta. 2003;24:575–587
  99. Renaud SJ, Postovit LM, Macdonald-Goodfellow SK, McDonald GT, Caldwell JD, Graham CH. Activated macrophages inhibit human cytotrophoblast invasiveness in vitro. Biol Reprod. 2005;73:237–243
  100. Lockwood CJ, Oner C, Uz YH, Kayisli UA, Huang SJ, Buchwalder LF, et al. Matrix metalloproteinase 9 (MMP9) expression in preeclamptic decidua and MMP9 induction by tumor necrosis factor alpha and interleukin 1 beta in human first trimester decidual cells. Biol Reprod. 2008;78:1064–1072
  101. Meisser A, Chardonnens D, Campana A, Bischof P. Effects of tumour necrosis factor-alpha, interleukin-1 alpha, macrophage colony stimulating factor and transforming growth factor beta on trophoblastic matrix metalloproteinases. Mol Hum Reprod. 1999;5:252–260
  102. Hiden U, Glitzner E, Ivanisevic M, Djelmis J, Wadsack C, Lang U, et al. MT1-MMP expression in first-trimester placental tissue is upregulated in type 1 diabetes as a result of elevated insulin and tumor necrosis factor-alpha levels. Diabetes. 2008;57:150–157
  103. Hiden U, Wadsack C, Prutsch N, Gauster M, Weiss U, Frank HG, et al. The first trimester human trophoblast cell line ACH-3P: a novel tool to study autocrine/paracrine regulatory loops of human trophoblast subpopulations – TNF-alpha stimulates MMP15 expression. BMC Dev Biol. 2007;7:137
  104. Wright A, Zhou Y, Weier JF, Caceres E, Kapidzic M, Tabata T, et al. Trisomy 21 is associated with variable defects in cytotrophoblast differentiation along the invasive pathway. Am J Med Genet A. 2004;130A:354–364
  105. Thathiah A, Brayman M, Dharmaraj N, Julian JJ, Lagow EL, Carson DD. Tumor necrosis factor alpha stimulates MUC1 synthesis and ectodomain release in a human uterine epithelial cell line. Endocrinology. 2004;145:4192–4203
  106. Niederkorn JY. See no evil, hear no evil, do no evil: the lessons of immune privilege. Nat Immunol. 2006;7:354–359
  107. Sargent IL, Borzychowski AM, Redman CW. NK cells and pre-eclampsia. J Reprod Immunol. 2007;76:40–44
  108. 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;14:353–356
  109. Chaouat G. The Th1/Th2 paradigm: still important in pregnancy?. Semin Immunopathol. 2007;29:95–113
  110. Moffett A, Loke C. Immunology of placentation in eutherian mammals. Nat Rev Immunol. 2006;6:584–594
  111. Eide IP, Rolfseng T, Isaksen CV, Mecsei R, Roald B, Lydersen S, et al. Serious foetal growth restriction is associated with reduced proportions of natural killer cells in decidua basalis. Virchows Arch. 2006;448:269–276
  112. Paradowska E, Blach-Olszewska Z, Gejdel E. Constitutive and induced cytokine production by human placenta and amniotic membrane at term. Placenta. 1997;18:441–446
  113. Sato TA, Keelan JA, Mitchell MD. Critical paracrine interactions between TNF-alpha and IL-10 regulate lipopolysaccharide-stimulated human choriodecidual cytokine and prostaglandin E2 production. J Immunol. 2003;170:158–166
  114. Griesinger G, Saleh L, Bauer S, Husslein P, Knofler M. Production of pro- and anti-inflammatory cytokines of human placental trophoblasts in response to pathogenic bacteria. J Soc Gynecol Investig. 2001;8:334–340
  115. Leroy MJ, Dallot E, Czerkiewicz I, Schmitz T, Breuiller-Fouche M. Inflammation of choriodecidua induces tumor necrosis factor alpha-mediated apoptosis of human myometrial cells. Biol Reprod. 2007;76:769–776
  116. Christiansen OB, Nielsen HS, Kolte AM. Inflammation and miscarriage. Semin Fetal Neonatal Med. 2006;11:302–308
  117. Wilczynski JR. Th1/Th2 cytokines balance–yin and yang of reproductive immunology. Eur J Obstet Gynecol Reprod Biol. 2005;122:136–143
  118. Shaarawy M, Nagui AR. Enhanced expression of cytokines may play a fundamental role in the mechanisms of immunologically mediated recurrent spontaneous abortion. Acta Obstet Gynecol Scand. 1997;76:205–211
  119. Chernyshov VP, Vodyanik MA, Pisareva SP. Lack of soluble TNF-receptors in women with recurrent spontaneous abortion and possibility for its correction. Am J Reprod Immunol. 2005;54:284–291
  120. Winger EE, Reed JL. Treatment with tumor necrosis factor inhibitors and intravenous immunoglobulin improves live birth rates in women with recurrent spontaneous abortion. Am J Reprod Immunol. 2008;60:8–16
  121. Toder V, Fein A, Carp H, Torchinsky A. TNF-alpha in pregnancy loss and embryo maldevelopment: a mediator of detrimental stimuli or a protector of the fetoplacental unit?. J Assist Reprod Genet. 2003;20:73–81
  122. Romero R, Gotsch F, Pineles B, Kusanovic JP. Inflammation in pregnancy: its roles in reproductive physiology, obstetrical complications, and fetal injury. Nutr Rev. 2007;65:S194–S202
  123. Christiaens I, Zaragoza DB, Guilbert L, Robertson SA, Mitchell BF, Olson DM. Inflammatory processes in preterm and term parturition. J Reprod Immunol. 2008;
  124. Kniss DA, Zimmerman PD, Garver CL, Fertel RH. Interleukin-1 receptor antagonist blocks interleukin-1-induced expression of cyclooxygenase-2 in endometrium. Am J Obstet Gynecol. 1997;177:559–567
  125. Imseis HM, Zimmerman PD, Samuels P, Kniss DA. Tumour necrosis factor-alpha induces cyclo-oxygenase-2 gene expression in first trimester trophoblasts: suppression by glucocorticoids and NSAIDs. Placenta. 1997;18:521–526
  126. Pomini F, Caruso A, Challis JR. Interleukin-10 modifies the effects of interleukin-1beta and tumor necrosis factor-alpha on the activity and expression of prostaglandin H synthase-2 and the NAD+-dependent 15-hydroxyprostaglandin dehydrogenase in cultured term human villous trophoblast and chorion trophoblast cells. J Clin Endocrinol Metab. 1999;84:4645–4651
  127. Ulug U, Goldman S, Ben-Shlomo I, Shalev E. Matrix metalloproteinase (MMP)-2 and MMP-9 and their inhibitor, TIMP-1, in human term decidua and fetal membranes: the effect of prostaglandin F(2alpha) and indomethacin. Mol Hum Reprod. 2001;7:1187–1193
  128. Dudley DJ. Immunoendocrinology of preterm labor: the link between corticotropin-releasing hormone and inflammation. Am J Obstet Gynecol. 1999;180:S251–S256
  129. Kossintseva I, Wong S, Johnstone E, Guilbert L, Olson DM, Mitchell BF. Proinflammatory cytokines inhibit human placental 11beta-hydroxysteroid dehydrogenase type 2 activity through Ca2+ and cAMP pathways. Am J Physiol Endocrinol Metab. 2006;290:E282–E288
  130. Sadowsky DW, Adams KM, Gravett MG, Witkin SS, Novy MJ. Preterm labor is induced by intraamniotic infusions of interleukin-1beta and tumor necrosis factor-alpha but not by interleukin-6 or interleukin-8 in a nonhuman primate model. Am J Obstet Gynecol. 2006;195:1578–1589
  131. Cackovic M, Buhimschi CS, Zhao G, Funai EF, Norwitz ER, Kuczynski E, et al. Fractional excretion of tumor necrosis factor-alpha in women with severe preeclampsia. Obstet Gynecol. 2008;112:93–100
  132. Conrad KP, Miles TM, Benyo DF. Circulating levels of immunoreactive cytokines in women with preeclampsia. Am J Reprod Immunol. 1998;40:102–111
  133. Sharma A, Satyam A, SharmaLeptin JB. IL-10 and inflammatory markers (TNF-alpha, IL-6 and IL-8) in pre-eclamptic, normotensive pregnant and healthy non-pregnant women. Am J Reprod Immunol. 2007;58:21–30
  134. Vince GS, Starkey PM, Austgulen R, Kwiatkowski D, Redman CW. Interleukin-6, tumour necrosis factor and soluble tumour necrosis factor receptors in women with pre-eclampsia. Br J Obstet Gynaecol. 1995;102:20–25
  135. Kupferminc MJ, Peaceman AM, Wigton TR, Rehnberg KA, Socol ML. Tumor necrosis factor-alpha is elevated in plasma and amniotic fluid of patients with severe preeclampsia. Am J Obstet Gynecol. 1994;170:1752–1757[discussion: 7–9]
  136. Visser W, Beckmann I, Knook MA, Wallenburg HC. Soluble tumor necrosis factor receptor II and soluble cell adhesion molecule 1 as markers of tumor necrosis factor-alpha release in preeclampsia. Acta Obstet Gynecol Scand. 2002;81:713–719
  137. Kupferminc MJ, Peaceman AM, Aderka D, Wallach D, Socol ML. Soluble tumor necrosis factor receptors and interleukin-6 levels in patients with severe preeclampsia. Obstet Gynecol. 1996;88:420–427
  138. Schipper EJ, Bolte AC, Schalkwijk CG, Van Geijn HP, Dekker GA. TNF-receptor levels in preeclampsia–results of a longitudinal study in high-risk women. J Matern Fetal Neonatal Med. 2005;18:283–287
  139. Chen G, Wilson R, Wang SH, Zheng HZ, Walker JJ, McKillop JH. Tumour necrosis factor-alpha (TNF-alpha) gene polymorphism and expression in pre-eclampsia. Clin Exp Immunol. 1996;104:154–159
  140. Wang Y, Walsh SW. TNF alpha concentrations and mRNA expression are increased in preeclamptic placentas. J Reprod Immunol. 1996;32:157–169
  141. Benyo DF, Smarason A, Redman CW, Sims C, Conrad KP. Expression of inflammatory cytokines in placentas from women with preeclampsia. J Clin Endocrinol Metab. 2001;86:2505–2512
  142. Hayashi M, Ueda Y, Yamaguchi T, Sohma R, Shibazaki M, Ohkura T, et al. Tumor necrosis factor-alpha in the placenta is not elevated in pre-eclamptic patients despite its elevation in peripheral blood. Am J Reprod Immunol. 2005;53:113–119
  143. Dong M, He J, Wang Z, Xie X, Wang H. Placental imbalance of Th1- and Th2-type cytokines in preeclampsia. Acta Obstet Gynecol Scand. 2005;84:788–793
  144. Jonsson Y, Ruber M, Matthiesen L, Berg G, Nieminen K, Sharma S, et al. Cytokine mapping of sera from women with preeclampsia and normal pregnancies. J Reprod Immunol. 2006;70:83–91
  145. Hamai Y, Fujii T, Yamashita T, Nishina H, Kozuma S, Mikami Y, et al. Evidence for an elevation in serum interleukin-2 and tumor necrosis factor-alpha levels before the clinical manifestations of preeclampsia. Am J Reprod Immunol. 1997;38:89–93
  146. Heikkinen J, Mottonen M, Pulkki K, Lassila O, Alanen A. Cytokine levels in midtrimester amniotic fluid in normal pregnancy and in the prediction of pre-eclampsia. Scand J Immunol. 2001;53:310–314
  147. Meekins JW, McLaughlin PJ, West DC, McFadyen IR, Johnson PM. Endothelial cell activation by tumour necrosis factor-alpha (TNF-alpha) and the development of pre-eclampsia. Clin Exp Immunol. 1994;98:110–114
  148. Serin IS, Ozcelik B, Basbug M, Kilic H, Okur D, Erez R. Predictive value of tumor necrosis factor alpha (TNF-alpha) in preeclampsia. Eur J Obstet Gynecol Reprod Biol. 2002;100:143–145
  149. Peracoli JC, Rudge MV, Peracoli MT. Tumor necrosis factor-alpha in gestation and puerperium of women with gestational hypertension and pre-eclampsia. Am J Reprod Immunol. 2007;57:177–185
  150. Chaiworapongsa T, Romero R, Yoshimatsu J, Espinoza J, Kim YM, Park K, et al. Soluble adhesion molecule profile in normal pregnancy and pre-eclampsia. J Matern Fetal Neonatal Med. 2002;12:19–27
  151. Coata G, Pennacchi L, Bini V, Liotta L, Di Renzo GC. Soluble adhesion molecules: marker of pre-eclampsia and intrauterine growth restriction. J Matern Fetal Neonatal Med. 2002;12:28–34
  152. Leung DN, Smith SC, To KF, Sahota DS, Baker PN. Increased placental apoptosis in pregnancies complicated by preeclampsia. Am J Obstet Gynecol. 2001;184:1249–1250
  153. Kharfi A, Bureau M, Giguere Y, Moutquin JM, Forest JC. Dissociation between increased apoptosis and expression of the tumor necrosis factor-alpha system in term placental villi with preeclampsia. Clin Biochem. 2006;39:646–651
  154. Kwaan HC, Wang J, Boggio L, Weiss I, Grobman WA. The thrombogenic effect of an inflammatory cytokine on trophoblasts from women with preeclampsia. Am J Obstet Gynecol. 2004;191:2142–2147
  155. Heiskanen J, Romppanen EL, Hiltunen M, Iivonen S, Mannermaa A, Punnonen K, et al. Polymorphism in the tumor necrosis factor-alpha gene in women with preeclampsia. J Assist Reprod Genet. 2002;19:220–223
  156. Molvarec A, Jermendy A, Nagy B, Kovacs M, Varkonyi T, Hupuczi P, et al. Association between tumor necrosis factor (TNF)-alpha G-308A gene polymorphism and preeclampsia complicated by severe fetal growth restriction. Clin Chim Acta. 2008;392:52–57
  157. Canto-Cetina T, Canizales-Quinteros S, de la Chesnaye E, Coral-Vazquez R, Mendez JP, Canto P. Analysis of C-850T and G-308A polymorphisms of the tumor necrosis factor-alpha gene in maya-mestizo women with preeclampsia. Hypertens Pregnancy. 2007;26:283–291
  158. Lachmeijer AM, Crusius JB, Pals G, Dekker GA, Arngrimsson R, ten Kate LP. Polymorphisms in the tumor necrosis factor and lymphotoxin-alpha gene region and preeclampsia. Obstet Gynecol. 2001;98:612–619
  159. Dizon-Townson DS, Major H, Ward K. A promoter mutation in the tumor necrosis factor alpha gene is not associated with preeclampsia. J Reprod Immunol. 1998;38:55–61
  160. Bartha JL, Romero-Carmona R, Comino-Delgado R. Inflammatory cytokines in intrauterine growth retardation. Acta Obstet Gynecol Scand. 2003;82:1099–1102
  161. Holcberg G, Huleihel M, Sapir O, Katz M, Tsadkin M, Furman B, et al. Increased production of tumor necrosis factor-alpha TNF-alpha by IUGR human placentae. Eur J Obstet Gynecol Reprod Biol. 2001;94:69–72
  162. Johnson MR, Anim-Nyame N, Johnson P, Sooranna SR, Steer PJ. Does endothelial cell activation occur with intrauterine growth restriction?. Bjog. 2002;109:836–839
  163. Kilani RT, Mackova M, Davidge ST, Winkler-Lowen B, Demianczuk N, Guilbert LJ. Endogenous tumor necrosis factor alpha mediates enhanced apoptosis of cultured villous trophoblasts from intrauterine growth-restricted placentae. Reproduction. 2007;133:257–264
  164. Kayisli UA, Mahutte NG, Arici A. Uterine chemokines in reproductive physiology and pathology. Am J Reprod Immunol. 2002;47:213–221
  165. 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
  166. Huber AV, Saleh L, Prast J, Haslinger P, Knofler M. Human chorionic gonadotrophin attenuates NF-kappaB activation and cytokine expression of endometriotic stromal cells. Mol Hum Reprod. 2007;13:595–604
  167. Roby KF, Hunt JS. Mouse endometrial tumor necrosis factor-alpha messenger ribonucleic acid and protein: localization and regulation by estradiol and progesterone. Endocrinology. 1994;135:2780–2789
  168. Tabibzadeh S, Satyaswaroop PG, von Wolff M, Strowitzki T. Regulation of TNF-alpha mRNA expression in endometrial cells by TNF-alpha and by oestrogen withdrawal. Mol Hum Reprod. 1999;5:1141–1149
  169. Tabibzadeh S. The signals and molecular pathways involved in human menstruation, a unique process of tissue destruction and remodelling. Mol Hum Reprod. 1996;2:77–92
  170. Fluhr H, Krenzer S, Stein GM, Stork B, Deperschmidt M, Wallwiener D, et al. Interferon-gamma and tumor necrosis factor-alpha sensitize primarily resistant human endometrial stromal cells to fas-mediated apoptosis. J Cell Sci. 2007;120:4126–4133
  171. Roberts M, Luo X, Chegini N. Differential regulation of interleukins IL-13 and IL-15 by ovarian steroids, TNF-alpha and TGF-beta in human endometrial epithelial and stromal cells. Mol Hum Reprod. 2005;11:751–760
  172. Cao WG, Morin M, Sengers V, Metz C, Roger T, Maheux R, et al. Tumour necrosis factor-alpha up-regulates macrophage migration inhibitory factor expression in endometrial stromal cells via the nuclear transcription factor NF-kappaB. Hum Reprod. 2006;21:421–428
  173. Singer CF, Marbaix E, Lemoine P, Courtoy PJ, Eeckhout Y. Local cytokines induce differential expression of matrix metalloproteinases but not their tissue inhibitors in human endometrial fibroblasts. Eur J Biochem. 1999;259:40–45
  174. Malik S, Day K, Perrault I, Charnock-Jones DS, Smith SK. Reduced levels of VEGF-A and MMP-2 and MMP-9 activity and increased TNF-alpha in menstrual endometrium and effluent in women with menorrhagia. Hum Reprod. 2006;21:2158–2166
  175. Chobotova K, Muchmore ME, Carver J, Yoo HJ, Manek S, Gullick WJ, et al. The mitogenic potential of heparin-binding epidermal growth factor in the human endometrium is mediated by the epidermal growth factor receptor and is modulated by tumor necrosis factor-alpha. J Clin Endocrinol Metab. 2002;87:5769–5777
  176. Chobotova K, Karpovich N, Carver J, Manek S, Gullick WJ, Barlow DH, et al. Heparin-binding epidermal growth factor and its receptors mediate decidualization and potentiate survival of human endometrial stromal cells. J Clin Endocrinol Metab. 2005;90:913–919
  177. Inoue T, Kanzaki H, Iwai M, Imai K, Narukawa S, Higuchi T, et al. Tumour necrosis factor alpha inhibits in-vitro decidualization of human endometrial stromal cells. Hum Reprod. 1994;9:2411–2417
  178. Rieger L, Kammerer U, Hofmann J, Sutterlin M, Dietl J. Choriocarcinoma cells modulate the cytokine production of decidual large granular lymphocytes in coculture. Am J Reprod Immunol. 2001;46:137–143
  179. van der Meer A, Lukassen HG, van Cranenbroek B, Weiss EH, Braat DD, van Lierop MJ, et al. Soluble HLA-G promotes Th1-type cytokine production by cytokine-activated uterine and peripheral natural killer cells. Mol Hum Reprod. 2007;13:123–133
  180. Rieger L, Hofmeister V, Probe C, Dietl J, Weiss EH, Steck T, et al. Th1- and Th2-like cytokine production by first trimester decidual large granular lymphocytes is influenced by HLA-G and HLA-E. Mol Hum Reprod. 2002;8:255–261
  181. Red-Horse K, Rivera J, Schanz A, Zhou Y, Winn V, Kapidzic M, et al. Cytotrophoblast induction of arterial apoptosis and lymphangiogenesis in an in vivo model of human placentation. J Clin Invest. 2006;116:2643–2652
  182. Gottschalk C, Malberg K, Arndt M, Schmitt J, Roessner A, Schultze D, et al. Matrix metalloproteinases and TACE play a role in the pathogenesis of endometriosis. Adv Exp Med Biol. 2000;477:483–486
  183. Eisermann J, Gast MJ, Pineda J, Odem RR, Collins JL. Tumor necrosis factor in peritoneal fluid of women undergoing laparoscopic surgery. Fertil Steril. 1988;50:573–579
  184. Cho SH, Oh YJ, Nam A, Kim HY, Park JH, Kim JH, et al. Evaluation of serum and urinary angiogenic factors in patients with endometriosis. Am J Reprod Immunol. 2007;58:497–504
  185. Keenan JA, Chen TT, Chadwell NL, Torry DS, Caudle MR. IL-1 beta, TNF-alpha, and IL-2 in peritoneal fluid and macrophage-conditioned media of women with endometriosis. Am J Reprod Immunol. 1995;34:381–385
  186. Richter ON, Dorn C, Rosing B, Flaskamp C, Ulrich U. Tumor necrosis factor alpha secretion by peritoneal macrophages in patients with endometriosis. Arch Gynecol Obstet. 2005;271:143–147
  187. Steff AM, Gagne D, Page M, Rioux A, Hugo P, Gosselin D. Serum concentrations of insulin-like growth factor-1, soluble tumor necrosis factor receptor-1 and angiogenin in endometriosis patients. Am J Reprod Immunol. 2004;51:166–173
  188. Harada T, Enatsu A, Mitsunari M, Nagano Y, Ito M, Tsudo T, et al. Role of cytokines in progression of endometriosis. Gynecol Obstet Invest. 1999;47(Suppl. 1):34–39[discussion: 9–40]
  189. Kyama CM, Overbergh L, Debrock S, Valckx D, Vander Perre S, Meuleman C, et al. Increased peritoneal and endometrial gene expression of biologically relevant cytokines and growth factors during the menstrual phase in women with endometriosis. Fertil Steril. 2006;85:1667–1675
  190. Yamauchi N, Harada T, Taniguchi F, Yoshida S, Iwabe T, Terakawa N. Tumor necrosis factor-alpha induced the release of interleukin-6 from endometriotic stromal cells by the nuclear factor-kappaB and mitogen-activated protein kinase pathways. Fertil Steril. 2004;82(Suppl. 3):1023–1028
  191. Sakamoto Y, Harada T, Horie S, Iba Y, Taniguchi F, Yoshida S, et al. Tumor necrosis factor-alpha-induced interleukin-8 (IL-8) expression in endometriotic stromal cells, probably through nuclear factor-kappa B activation: gonadotropin-releasing hormone agonist treatment reduced IL-8 expression. J Clin Endocrinol Metab. 2003;88:730–735
  192. Zhang RJ, Wild RA, Ojago JM. Effect of tumor necrosis factor-alpha on adhesion of human endometrial stromal cells to peritoneal mesothelial cells: an in vitro system. Fertil Steril. 1993;59:1196–1201
  193. Debrock S, De Strooper B, Vander Perre S, Hill JA, D'Hooghe TM. Tumour necrosis factor-alpha, interleukin-6 and interleukin-8 do not promote adhesion of human endometrial epithelial cells to mesothelial cells in a quantitative in vitro model. Hum Reprod. 2006;21:605–609
  194. Braun DP, Ding J, Dmowski WP. Peritoneal fluid-mediated enhancement of eutopic and ectopic endometrial cell proliferation is dependent on tumor necrosis factor-alpha in women with endometriosis. Fertil Steril. 2002;78:727–732
  195. Grund EM, Kagan D, Tran CA, Zeitvogel A, Starzinski-Powitz A, Nataraja S, et al. Tumor necrosis factor-alpha regulates inflammatory and mesenchymal responses via mitogen-activated protein kinase kinase, p38, and nuclear factor kappaB in human endometriotic epithelial cells. Mol Pharmacol. 2008;73:1394–1404
  196. Na YJ, Yang SH, Baek DW, Lee DH, Kim KH, Choi YM, et al. Effects of peritoneal fluid from endometriosis patients on the release of vascular endothelial growth factor by neutrophils and monocytes. Hum Reprod. 2006;21:1846–1855
  197. Mori H, Nakagawa M, Itoh N, Wada K, Tamaya T. Danazol suppresses the production of interleukin-1 beta and tumor necrosis factor by human monocytes. Am J Reprod Immunol. 1990;24:45–50
  198. Falconer H, Mwenda JM, Chai DC, Wagner C, Song XY, Mihalyi A, et al. Treatment with anti-TNF monoclonal antibody (c5N) reduces the extent of induced endometriosis in the baboon. Hum Reprod. 2006;21:1856–1862
  199. Koninckx PR, Craessaerts M, Timmerman D, Cornillie F, Kennedy S. Anti-TNF-alpha treatment for deep endometriosis-associated pain: a randomized placebo-controlled trial. Hum Reprod. 2008;23:2017–2023
  200. Scheinfeld N. Menorrhagia and severe menstrual pain related to the use of adalimumab in a psoriatic. J Dermatolog Treat. 2008;19:188–189
  201. Perdichizzi A, Nicoletti F, La Vignera S, Barone N, D'Agata R, Vicari E, et al. Effects of tumour necrosis factor-alpha on human sperm motility and apoptosis. J Clin Immunol. 2007;27:152–162
  202. Tronchon V, Vialard F, El Sirkasi M, Dechaud H, Rollet J, Albert M, et al. Tumor necrosis factor-alpha -308 polymorphism in infertile men with altered sperm production or motility. Hum Reprod. 2008;
  203. Iborra A, Palacio JR, Martinez P. Oxidative stress and autoimmune response in the infertile woman. Chem Immunol Allergy. 2005;88:150–162
  204. Murakami T, Okamura C, Matsuzaki S, Terada Y, Yokomizo R, Noda T, et al. Prediction of pregnancy in infertile women with endometriosis. Gynecol Obstet Invest. 2002;53(Suppl. 1):26–32
  205. Sainson RC, Johnston DA, Chu HC, Holderfield MT, Nakatsu MN, Crampton SP, et al. TNF primes endothelial cells for angiogenic sprouting by inducing a tip cell phenotype. Blood. 2008;111:4997–5007

PII: S0143-4004(08)00352-4

doi: 10.1016/j.placenta.2008.10.012

Placenta
Volume 30, Issue 2 , Pages 111-123 , February 2009

Article Tools

* Image Usage & Resolution