Cytokine IL-6 secretion by trophoblasts regulated via sphingosine-1-phosphate receptor 2 involving Rho/Rho-kinase and Rac1 signaling pathways

Molecular Human Reproduction

Volumn 19, Issue 8, 2013, Pages 528-538

  Goyal, Pankaj ^a   Brünnert, Daniela ^a   Ehrhardt, Jens ^a   Bredow, Marike ^a   Piccenini, Svea ^a   Zygmunt, Marek ^a  

^a UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

IL 6; PI3 kinase; Placenta; Sphingosine 1 phosphate; Trophoblast

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; 4 (2,6 DICHLORO 4 PYRIDINYL) 1 (1,3 DIMETHYL 4 ISOPROPYL 1H PYRAZOLO[3,4 B]PYRIDIN 6 YL)SEMICARBAZIDE; 4 AMINO 6 [2 [[4 (DIETHYLAMINO) 1 METHYLBUTYL]AMINO] 6 METHYL 4 PYRIMIDINYL] 2 METHYLQUINOLINE; INTERLEUKIN 6; PHOSPHATIDYLINOSITOL 3 KINASE; RAC1 PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR 2; UNCLASSIFIED DRUG;

ARTICLE; CELL LINE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE SILENCING; HUMAN; HUMAN CELL; MOLECULAR BIOLOGY; PLACENTA; PRIORITY JOURNAL; SECRETORY PATHWAY; SIGNAL TRANSDUCTION; TROPHOBLAST;

IL-6; PI3-KINASE; PLACENTA; SPHINGOSINE 1-PHOSPHATE; TROPHOBLAST;

AMIDES; AMINOQUINOLINES; CELL LINE; CHROMONES; CYCLOHEXIMIDE; DACTINOMYCIN; FEMALE; HUMANS; INTERLEUKIN-6; LYSOPHOSPHOLIPIDS; MORPHOLINES; PHOSPHATIDYLINOSITOL 3-KINASES; PREGNANCY; PYRAZOLES; PYRIDINES; PYRIMIDINES; RAC1 GTP-BINDING PROTEIN; RECEPTORS, LYSOSPHINGOLIPID; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SPHINGOSINE; TROPHOBLASTS;

EID: 84880709429     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gat023     Document Type: Article

References (50)

1. Ancellin N, Hla T. Differential pharmacological properties and signal transduction of the sphingosine 1-phosphate receptors EDG-1, EDG-3, and EDG-5. J Biol Chem 1999; 274: 18997-19002.
2. Bowen JM, Chamley L, Mitchell MD, Keelan JA. Cytokines of the placenta and extra-placental membranes: biosynthesis, secretion and roles in establishment of pregnancy in women. Placenta 2002; 23: 239-256.
3. Champion H, Innes BA, Robson SC, Lash GE, Bulmer JN. Effects of interleukin-6 on extravillous trophoblast invasion in early human pregnancy. Mol Hum Reprod 2012; 18: 391-400.
4. Cummings RJ, Parinandi NL, Zaiman A, Wang L, Usatyuk PV, Garcia JG, Natarajan V. Phospholipase D activation by sphingosine 1-phosphate regulates interleukin-8 secretion in human bronchial epithelial cells. J Biol Chem 2002; 277: 30227-30235.
5. Das C, Kumar VS, Gupta S, Kumar S. Network of cytokines, integrins and hormones in human trophoblast cells. J Reprod Immunol 2002; 53: 257-268.
6. Davis MD, Clemens JJ, Macdonald TL, Lynch KR. Sphingosine 1-phosphate analogs as receptor antagonists. J Biol Chem 2005; 280: 9833-9841.
7. Denison FC, Kelly RW, Calder AA, Riley SC. Cytokine secretion by human fetal membranes, decidua and placenta at term. Hum Reprod 1998; 13: 3560-3565.
8. Gonda K, Okamoto H, Takuwa N, Yatomi Y, Okazaki H, Sakurai T, Kimura S, Sillard R, Harii K, Takuwa Y. The novel sphingosine 1-phosphate receptor AGR16 is coupled via pertussis toxin-sensitive and -insensitive G-proteins to multiple signalling pathways. Biochem J 1999; 337: 67-75.
9. Gonzalez E, Kou R, Michel T. Rac1 modulates sphingosine 1-phosphate-mediated activation of phosphoinositide 3-kinase/Akt signaling pathways in vascular endothelial cells. J Biol Chem 2006; 281: 3210-3216.
10. Goyal P, Behring A, Kumar A, Siess W. STK35L1 associates with nuclear actin and regulates cell cycle and migration of endothelial cells. PLoS One 2011; 6: e16249.
11. Graham CH, Hawley TS, Hawley RG, MacDougall JR, Kerbel RS, Khoo N, Lala PK. Establishment and characterization of first trimester human trophoblast cells with extended lifespan. Exp Cell Res 1993; 206: 204-211.
12. Hong-Geller E, Cerione RA. Cdc42 and Rac stimulate exocytosis of secretory granules by activating the IP(3)/calcium pathway in RBL-2H3 mast cells. J Cell Biol 2000; 148: 481-494.
13. Ishihara K, Hirano T. IL-6 in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev 2002; 13: 357-368.
14. Johnstone ED, Chan G, Sibley CP, Davidge ST, Lowen B, Guilbert LJ. Sphingosine-1-phosphate inhibition of placental trophoblast differentiation through a Gi-coupled receptor response. J Lipid Res 2005; 46: 1833-1839.
15. Kandere-Grzybowska K, Letourneau R, Kempuraj D, Donelan J, Poplawski S, Boucher W, Athanassiou A, Theoharides TC. IL-1 induces vesicular secretion of IL-6 without degranulation from human mast cells. J Immunol 2003; 171: 4830-4836.
16. Kim MS, Radinger M, Gilfillan AM. The multiple roles of phosphoinositide 3-kinase in mast cell biology. Trends Immunol 2008; 29: 493-501.
17. Kishimoto T, Akira S, Narazaki M, Taga T. Interleukin-6 family of cytokines and gp130. Blood 1995; 86: 1243-1254.
18. Kojima K, Kanzaki H, Iwai M, Hatayama H, Fujimoto M, Narukawa S, Higuchi T, Kaneko Y, Mori T, Fujita J. Expression of leukaemia inhibitory factor (LIF) receptor in human placenta: a possible role for LIF in the growth and differentiation of trophoblasts. Hum Reprod 1995; 10: 1907-1911.
19. Kozawa O, Tokuda H, Matsuno H, Uematsu T. Activation of mitogen-activated protein kinase is involved in sphingosine 1-phosphate-stimulated interleukin-6 synthesis in osteoblasts. FEBS Lett 1997; 418: 149-151.
20. Lacy P, Stow JL. Cytokine release from innate immune cells: association with diverse membrane trafficking pathways. Blood 2011; 118: 9-18.
21. Lee H, Deng J, Kujawski M, Yang C, Liu Y, Herrmann A, Kortylewski M, Horne D, Somlo G, Forman S et al. STAT3-induced S1PR1 expression is crucial for persistent STAT3 activation in tumors. Nat Med 2010; 16: 1421-1428.
22. Lepley D, Paik JH, Hla T, Ferrer F. The G protein-coupled receptor S1P2 regulates Rho/Rho kinase pathway to inhibit tumor cell migration. Cancer Res 2005; 65: 3788-3795.
23. Maceyka M, Harikumar KB, Milstien S, Spiegel S. Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol 2012; 22: 50-60.
24. Manderson AP, Kay JG, Hammond LA, Brown DL, Stow JL. Subcompartments of the macrophage recycling endosome direct the differential secretion of IL-6 and TNFalpha. J Cell Biol 2007; 178: 57-69.
25. Naka T, Nishimoto N, Kishimoto T. The paradigm of IL-6: from basic science to medicine. Arthritis Res 2002; 4(Suppl 3):S233-S242.
26. Nishino E, Matsuzaki N, Masuhiro K, Kameda T, Taniguchi T, Takagi T, Saji F, Tanizawa O. Trophoblast-derived interleukin-6 (IL-6) regulates human chorionic gonadotropin release through IL-6 receptor on human trophoblasts. J Clin Endocrinol Metab 1990; 71: 436-441.
27. Noyola-Martinez N, Diaz L, Avila E, Halhali A, Larrea F, Barrera D. Calcitriol downregulates TNF-alpha and IL-6 expression in cultured placental cells from preeclamptic women. Cytokine 2013; 61: 245-250.
28. Orendi K, Kivity V, Sammar M, Grimpel Y, Gonen R, Meiri H, Lubzens E, Huppertz B. Placental and trophoblastic in vitro models to study preventive and therapeutic agents for preeclampsia. Placenta 2011; 32(Suppl 1):S49-S54.
29. Osada M, Yatomi Y, Ohmori T, Ikeda H, Ozaki Y. Enhancement of sphingosine 1-phosphate-induced migration of vascular endothelial cells and smooth muscle cells by an EDG-5 antagonist. Biochem Biophys Res Commun 2002; 299: 483-487.
30. Oskeritzian CA, Price MM, Hait NC, Kapitonov D, Falanga YT, Morales JK, Ryan JJ, Milstien S, Spiegel S. Essential roles of sphingosine-1-phosphate receptor 2 in human mast cell activation, anaphylaxis, and pulmonary edema. J Exp Med 2010; 207: 465-474.
31. Oz-Arslan D, Ruscher W, Myrtek D, Ziemer M, Jin Y, Damaj BB, Sorichter S, Idzko M, Norgauer J, Maghazachi AA. IL-6 and IL-8 release is mediated via multiple signaling pathways after stimulating dendritic cells with lysophospholipids. J Leukoc Biol 2006a;80: 287-297.
32. Oz-Arslan D, Ruscher W, Myrtek D, Ziemer M, Jin Y, Damaj BB, Sorichter S, Idzko M, Norgauer J, Maghazachi AA. IL-6 and IL-8 release is mediated via multiple signaling pathways after stimulating dendritic cells with lysophospholipids. J Leukoc Biol 2006b;80: 287-297.
33. Pandey D, Goyal P, Dwivedi S, Siess W. Unraveling a novel Rac1-mediated signaling pathway that regulates cofilin dephosphorylation and secretion in thrombin-stimulated platelets. Blood 2009; 114: 415-424.
34. Oz-Arslan D, Ruscher W, Myrtek D, Ziemer M, Jin Y, Damaj BB, Sorichter S, Idzko M, Norgauer J, Maghazachi AA. IL-6 and IL-8 release is mediated via multiple signaling pathways after stimulating dendritic cells with lysophospholipids. J Leukoc Biol 2006b;80: 287-297.
35. Pandey D, Goyal P, Dwivedi S, Siess W. Unraveling a novel Rac1-mediated signaling pathway that regulates cofilin dephosphorylation and secretion in thrombin-stimulated platelets. Blood 2009; 114: 415-424.
36. Prins JR, Gomez-Lopez N, Robertson SA. Interleukin-6 in pregnancy and gestational disorders. J Reprod Immunol 2012; 95: 1-14.
37. Ridley AJ. Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 2006; 16: 522-529.
38. Sanna MG, Liao J, Jo E, Alfonso C, Ahn MY, Peterson MS, Webb B, Lefebvre S, Chun J, Gray N et al. Sphingosine 1-phosphate (S1P) receptor subtypes S1P1 and S1P3, respectively, regulate lymphocyte recirculation and heart rate. J Biol Chem 2004; 279: 13839-13848.
39. Sanna MG, Wang SK, Gonzalez-Cabrera PJ, Don A, Marsolais D, Matheu MP, Wei SH, Parker I, Jo E, Cheng WC et al. Enhancement of capillary leakage and restoration of lymphocyte egress by a chiral S1P1 antagonist in vivo. Nat Chem Biol 2006; 2: 434-441.
40. Sansone P, Storci G, Tavolari S, Guarnieri T, Giovannini C, Taffurelli M, Ceccarelli C, Santini D, Paterini P, Marcu KB et al. IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J Clin Invest 2007; 117: 3988-4002.
41. Singh AT, Dharmarajan A, Aye IL, Keelan JA. Sphingosine-sphingosine-1-phosphate pathway regulates trophoblast differentiation and syncytialization. Reprod Biomed Online 2012; 24: 224-234.
42. Skoura A, Hla T. Regulation of vascular physiology and pathology by the S1P2 receptor subtype. Cardiovasc Res 2009; 82: 221-228.
43. Spiegel S, Milstien S. The outs and the ins of sphingosine-1-phosphate in immunity. Nat Rev Immunol 2011; 11: 403-415.
44. Stanley AC, Lacy P. Pathways for cytokine secretion. Physiology (Bethesda) 2010; 25: 218-229.
45. Stephanou A, Myatt L, Eis AL, Sarlis N, Jikihara H, Handwerger S. Ontogeny of the expression and regulation of interleukin-6 (IL-6) and IL-1 mRNAs by human trophoblast cells during differentiation in vitro. J Endocrinol 1995; 147: 487-496.
46. Sugimoto N, Takuwa N, Okamoto H, Sakurada S, Takuwa Y. Inhibitory and stimulatory regulation of Rac and cell motility by the G12/13-Rho and Gi pathways integrated downstream of a single G protein-coupled sphingosine-1-phosphate receptor isoform. Mol Cell Biol 2003; 23: 1534-1545.
47. Theoharides TC, Boucher W, Spear K. Serum interleukin-6 reflects disease severity and osteoporosis in mastocytosis patients. Int Arch Allergy Immunol 2002; 128: 344-350.
48. Wellby ML, Kennedy JA, Pile K, True BS, Barreau P. Serum interleukin-6 and thyroid hormones in rheumatoid arthritis. Metabolism 2001; 50: 463-467.
49. Windh RT, Lee MJ, Hla T, An S, Barr AJ, Manning DR. Differential coupling of the sphingosine 1-phosphate receptors Edg-1, Edg-3, and H218/Edg-5 to the G(i), G(q), and G(12) families of heterotrimeric G proteins. J Biol Chem 1999; 274: 27351-8.
50. Ye X. Lysophospholipid signaling in the function and pathology of the reproductive system. Hum Reprod Update 2008; 14: 519-536.