Preeclampsia-related inflammatory cytokines regulate interleukin-6 expression in human decidual cells

American Journal of Pathology

Volumn 172, Issue 6, 2008, Pages 1571-1579

  Lockwood, Charles J ^a   Yen, Chih Feng ^b   Basar, Murat ^c   Kayisli, Umit A ^a   Martel, Maritza ^a   Buhimschi, Irina ^a   Buhimschi, Catalin ^a   Huang, S Joseph ^a   Krikun, Graciela ^a   Schatz, Frederick ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^c ISTANBUL UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DECIDUA; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FIRST TRIMESTER PREGNANCY; GENE EXPRESSION REGULATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOGENESIS; INFLAMMATION; PREECLAMPSIA; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

EID: 44849116010     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2008.070629     Document Type: Article

References (56)

1. Redman CW, Sargent IL: Pre-eclampsia, the placenta and the maternal systemic inflammatory response - a review. Placenta 2003, 24 (Suppl A):S21-S27
2. Sibai BM, Dekker G, Kupferminic M: Pre-eclampsia. Lancet 2005, 365:785-799
3. Pijnenborg R, Bland JM, Robertson WB, Brosens I: Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 1983, 4:397-413
4. Zhou Y, Damsky CH, Fisher SJ: Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. One cause of defective endovascular invasion in this syndrome? J Clin Invest 1997, 99:2152-2164
5. Lunell NO, Lewander R, Mamoun I, Nylund L, Sarby S, Thornstrom S: Uteroplacental blood flow in pregnancy induced hypertension. Scand J Clin Lab Invest Suppl 1984, 169:S28-S35
6. Soleymanlou N, Jurisica I, Nevo O, Ietta F, Zhang X, Zamudio S, Post M, Caniggia I: Molecular evidence of placental hypoxia in preeclampsia. J Clin Endocrinol Metab 2005, 90:4299-4308
7. Taylor RN, Grimwood J, Taylor RS, McMaster MT, Fisher SJ, North RA: Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. Am J Obstet Gynecol 2003, 188:177-182
8. Nadar SK, Karalis I, Al Yemeni E, Blann AD, Lip GY: Plasma markers of angiogenesis in pregnancy induced hypertension. Thromb Haemost 2005, 94:1071-1076
9. Thadhani R, Mutter WP, Wolf M, Levine RJ, Taylor RN, Sukhatme VP, Ecker J, Karumanchi SA: First trimester placental growth factor and soluble fms-like tyrosine kinase 1 and risk for preeclampsia. J Clin Endocrinol Metab 2004, 89:770-775
10. Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Kim MR, Espinoza J, Bujold E, Goncalves L, Gomez R, Edwin S, Mazor M: Plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated prior to the clinical diagnosis of pre-eclampsia. J Matern Fetal Neonatal Med 2005, 17:3-18
11. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thadhani R, Karumanchi SA, CPEP Study Group: Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006, 355:992-1005
12. Sargent IL, Germain SJ, Sacks GP, Kumar S, Redman CW: Trophoblast deportation and the maternal inflammatory response in preeclampsia. J Reprod Immunol 2003, 59:153-160
13. Levine RJ, Qian C, Leshane ES, Yu KF, England LJ, Schisterman EF, Wataganara T, Romero R, Bianchi DW: Two-stage elevation of cell-free fetal DNA in maternal sera before onset of preeclampsia. Am J Obstet Gynecol 2004, 190:707-713
14. Barden A, Ritchie J, Walters B, Michael C, Rivera J, Mori T, Croft K, Beilin L: Study of plasma factors associated with neutrophil activation and lipid peroxidation in preeclampsia. Hypertension 2001, 38:803-808
15. Hubel CA, McLaughlin MK, Evans RW, Hauth BA, Sims CJ, Roberts JM: Fasting serum triglycerides, free fatty acids, and malondialdehyde are increased in preeclampsia, are positively correlated, and decrease within 48 hours post partum. Am J Obstet Gynecol 1996, 174:975-982
16. Walker JJ: Antioxidants and inflammatory cell response in preeclampsia. Semin Reprod Endocrinol 1998, 16:47-55
17. Conrad KP, Miles TM, Benyo DF: Circulating levels of immunoreactive cytokines in women with preeclampsia. Am J Reprod Immunol 1998, 40:102-111
18. 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
19. 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
20. Ellis J, Wennerholm UB, Bengtsson A, Lilja H, Pettersson A, Sultan B, Wennergren M, Hagberg H: Levels of dimethylarginines and cytokines in mild and severe preeclampsia. Acta Obstet Gynecol Scand 2001, 80:602-608
21. Jonsson Y, Rubèr M, Matthiesen L, Berg G, Nieminen K, Sharma S, Ernerudh J, Ekerfelt C: Cytokine mapping of sera from women with preeclampsia and normal pregnancies. J Reprod Immunol 2006, 70:83-91
22. Greer IA, Lyall F, Perera T, Boswell F, Macara LM: Increased concentrations of cytokines interleukin-6 and interleukin-1 receptor antagonist in plasma of women with preeclampsia: a mechanism for endothelial dysfunction? Obstet Gynecol 1994, 84:937-940
23. Takacs P, Green KL, Nikaeo A, Kauma SW: Increased vascular endothelial cell production of interleukin-6 in severe preeclampsia. Am J Obstet Gynecol 2003, 188:740-744
24. Madazli R, Aydin S, Uludag S, Vildan O, Tolun N: Maternal plasma levels of cytokines in normal and preeclamptic pregnancies and their relationship with diastolic blood pressure and fibronectin levels. Acta Obstet Gynecol Scand 2003, 82:797-802
25. Freeman DJ, McManus F, Brown EA, Cherry L, Norrie J, Ramsay JE, Clark P, Walker ID, Sattar N, Greer IA: Short- and long-term changes in plasma inflammatory markers associated with preeclampsia. Hypertension 2004, 44:708-714
26. 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
27. Gammill HS, Roberts JM: Emerging concepts in preeclampsia investigation. Front Biosci 2007, 12:2403-2411
28. Scheller J, Ohnesorge N, Rose-John S: Interleukin-6 trans-signaling in chronic inflammation and cancer. Scand J Immunol 2006, 63:321-329
29. Jones SA: Directing transition from innate to acquired immunity: defining a role for IL-6. J Immunol 2005, 175:3463-3468
30. Desai TR, Leeper NJ, Hynes KL, Gewertz BL: Interleukin-6 causes endothelial barrier dysfunction via the protein kinase C pathway. J Surg Res 2002, 104:118-123
31. Maruo N, Morita I, Ishizaki Y, Murota S: Inhibitory effects of interleukin 6 on prostaglandin I2 production in cultured bovine vascular endothelial cells. Arch Biochem Biophys 1992, 292:600-604
32. Hayashi M, Ueda Y, Ohkura T, Inaba N: Interleukin-6 concentrations in the placenta and blood in normal pregnancies and preeclampsia. Horm Metab Res 2005, 37:419-424
33. Al-Othman S, Omu AE, Diejomaoh FM, Al-Yatama M, Al-Qattan F: Differential levels of interleukin 6 in maternal and cord sera and placenta in women with pre-eclampsia. Gynecol Obstet Invest 2001, 52:60-65
34. Opsjøn SL, Austgulen R, Waage A: Interleukin-1, interleukin-6 and tumor necrosis factor at delivery in preeclamptic disorders. Acta Obstet Gynecol Scand 1995, 74:19-26
35. Kauma SW, Wang Y, Walsh SW: Preeclampsia is associated with decreased placental interleukin-6 production. J Soc Gynecol Investig 1995, 2:614-617
36. Rinehart BK, Terrone DA, Lagoo-Deenadayalan S, Barber WH, Hale EA, Martin JN, Bennett WA: Expression of the placental cytokines tumor necrosis factor alpha, interleukin 1beta, and interleukin 10 is increased in preeclampsia. Am J Obstet Gynecol 1999, 181:915-920
37. Hefler LA, Tempfer CB, Gregg AR: Polymorphisms within the interleukin-1 beta gene cluster and preeclampsia. Obstet Gynecol 2001, 97:664-648
38. Reister F, Frank HG, Kingdom JC, Heyl W, Kaufmann P, Rath W, Huppertz B: Macrophage-induced apoptosis limits endovascular trophoblast invasion in the uterine wall of preeclamptic women. Lab Invest 2001, 81:1143-1152
39. 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
40. Nathan CF: Secretory products of macrophages. J Clin Invest 1987, 79:319-326
41. Dunn CL, Kelly RW, Critchley HO: Decidualization of the human endometrial stromal cell: an enigmatic transformation. Reprod Biomed 2003, 7:151-161
42. ACOG Committee on Obstetric Practice: ACOG practice bulletin. Diagnosis and management of preeclampsia and eclampsia. Number 33, January 2002. American College of Obstetricians and Gynecologists. Obstet Gynecol 2002, 99:159-167
43. Kayisli O, Kayisli UA, Luleci G, Arici A: In vivo and in vitro regulation of Akt activation in human endometrial cells is estrogen dependent. Biol Reprod 2004, 71:714-721
44. Arici A, Marshburn PB, MacDonald PC, Dombrowski RA: Progesterone metabolism in human endometrial stromal and gland cells in culture. Steroids 1999, 64:530-534
45. Gross V, Andus T, Castell J, Vom Berg D, Heinrich PC, Gerok W: Oand N-glycosylation lead to different molecular mass forms of human monocyte interleukin-6. FEBS Lett 1989, 247:323-326
46. Dimitriadis E, White CA, Jones RL, Salamonsen LA: Cytokines, chemokines and growth factors in endometrium related to implantation. Hum Reprod Update 2005, 11:613-630
47. Robertson SA, O'Connell A, Ramsay A: The effect of interleukin-6 deficiency on implantation, fetal development and parturition in mice. Proc Aust Soc Reprod Biol 2000, 31:97
48. Vandermolen DT, Gu Y: Human endometrial interleukin-6 (IL-6): in vivo messenger ribonucleic acid expression, in vitro protein production, and stimulation thereof by IL-1 beta. Fertil Steril 1996, 66:741-747
49. Dudley DJ, Trautman MS, Araneo BA, Edwin SS, Mitchell MD: Decidual cell biosynthesis of interleukin-6: regulation by inflammatory cytokines. J Clin Endocrinol Metab 1992, 74:884-889
50. Nilsson MB, Langley RR, Fidler IJ: Interleukin-6, secreted by human ovarian carcinoma cells, is a potent proangiogenic cytokine. Cancer Res 2005, 65:10794-10800
51. Lockwood CJ, Matta P, Krikun G, Koopman LA, Masch R, Toti P, Arcuri F, Huang ST, Funai EF, Schatz F: Regulation of monocyte chemoattractant protein-1 expression by tumor necrosis factor-alpha and interleukin-1beta in first trimester human decidual cells: implications for preeclampsia. Am J Pathol 2006, 168:445-452
52. Abrahams VM, Kim YM, Straszewski SL, Romero R, Mor G: Macrophages and apoptotic cell clearance during pregnancy. Am J Reprod Immunol 2004, 51:275-282
53. Trundley A, Moffett A: Human uterine leukocytes and pregnancy. Tissue Antigens 2004, 63:1-12
54. Chomarat P, Banchereau J, Davoust J, Palucka AK: IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat Immunol 2000, 1:510-514
55. Huang SJ, Schatz F, Masch R, Rahman M, Buchwalder L, Niven-Fairchild T, Tang C, Abrahams VM, Krikun G, Lockwood CJ: Regulation of chemokine production in response to pro-inflammatory cytokines in first trimester decidual cells. J Reprod Immunol 2006, 72:60-73
56. 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