Interleukin-11 increases invasiveness of JEG-3 choriocarcinoma cells by modulating STAT3 expression

Journal of Reproductive Immunology

Volumn 82, Issue 1, 2009, Pages 1-11

  Suman, Pankaj ^a   Poehlmann, Tobias G ^b   Prakash, Golla Jaya ^a   Markert, Udo R ^b   Gupta, Satish K ^a  

^a NATIONAL INSTITUTE OF IMMUNOLOGY   (India)

^b Med Fac   (Germany)

Author keywords

ERK1 2; IL 11; JEG 3; Proliferation; STAT1; STAT3; Trophoblast invasion

Indexed keywords

CYTOKINE; GLYCOPROTEIN GP 130; INTERLEUKIN 11; INTERLEUKIN 11 RECEPTOR ALPHA; INTERLEUKIN 6 RECEPTOR; MESSENGER RNA; SMALL INTERFERING RNA; STAT1 PROTEIN; STAT3 PROTEIN; TYROSINE;

ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CELL MIGRATION; CELL PROLIFERATION; CHORIOCARCINOMA; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOMODULATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; TROPHOBLAST; UPREGULATION;

CELL LINE, TUMOR; CELL PROLIFERATION; CHORIOCARCINOMA; CYTOKINE RECEPTOR GP130; FEMALE; HUMANS; IMMUNOMODULATION; INTERLEUKIN-11; NEOPLASM INVASIVENESS; PREGNANCY; RECEPTORS, INTERLEUKIN-6; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; UTERINE NEOPLASMS;

EID: 70149089432     PISSN: 01650378     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jri.2009.07.002     Document Type: Article

References (37)

1. Bromberg J., and Darnell Jr. J.E. The role of STATs in transcriptional control and their impact on cellular function. Oncogene 19 (2000) 2468-2473
2. Carson D.D., Bagchi I., Dey S.K., Enders A.C., Fazleabas A.T., Lessey B.A., and Yoshinaga K. Embryo implantation. Dev. Biol. 223 (2000) 217-237
3. Chadderton T., Wilson C., Bewick M., and Gluck S. Evaluation of three rapid RNA extraction reagents: relevance for use in RT-PCR's and measurement of low level gene expression in clinical samples. Cell Mol. Biol. (Noisy-le-grand) 43 (1997) 1227-1234
4. Chakravarty S., Suraj K., and Gupta S.K. Baculovirus-expressed recombinant human zona pellucida glycoprotein-B induces acrosomal exocytosis in capacitated spermatozoa in addition to zona pellucida glycoprotein-C. Mol. Hum. Reprod. 11 (2005) 365-372
5. Cork B.A., Li T.C., Warren M.A., and Laird S.M. Interleukin-11 (IL-11) in human endometrium: expression throughout the menstrual cycle and the effects of cytokines on endometrial IL-11 production in vitro. J. Reprod. Immunol. 50 (2001) 3-17
6. Cork B.A., Tuckerman E.M., Li T.C., and Laird S.M. Expression of interleukin (IL)-11 receptor by the human endometrium in vivo and effects of IL-11, IL-6 and LIF on the production of MMP and cytokines by human endometrial cells in vitro. Mol. Hum. Reprod. 8 (2002) 841-848
7. Dahmen H., Horsten U., Kuster A., Jacques Y., Minvielle S., Kerr I.M., Ciliberto G., Paonessa G., Heinrich P.C., and Muller-Newen G. Activation of the signal transducer gp130 by interleukin-11 and interleukin-6 is mediated by similar molecular interactions. Biochem. J. 331 (1998) 695-702
8. Dimitriadis E., Robb L., Liu Y.X., Enders A.C., Martin H., Stoikos C., Wallace E., and Salamonsen L.A. IL-11 and IL-11R alpha immunolocalisation at primate implantation sites supports a role for IL-11 in placentation and fetal development. Reprod. Biol. Endocrinol. 1 (2003) 34
9. Dimitriadis E., Stoikos C., Tan Y.L., and Salamonsen L.A. Interleukin 11 signaling components signal transducer and activator of transcription 3 (STAT3) and suppressor of cytokine signaling 3 (SOCS3) regulate human endometrial stromal cell differentiation. Endocrinology 147 (2006) 3809-3817
10. Dimitriadis E., White C.A., Jones R.L., and Salamonsen L.A. Cytokines, chemokines and growth factors in endometrium related to implantation. Hum. Reprod. Update 11 (2005) 613-630
11. Du X.X., and Williams D.A. Interleukin-11: a multifunctional growth factor derived from the hematopoietic microenvironment. Blood 83 (1994) 2023-2030
12. Ernst M., Najdovska M., Grail D., Lundgren-May T., Buchert M., Tye H., Matthews V.B., Armes J., Bhathal P.S., Hughes N.R., Marcusson E.G., Karras J.G., Na S., Sedgwick J.D., Hertzog P.J., and Jenkins B.J. STAT3 and STAT1 mediate IL-11-dependent and inflammation-associated gastric tumorigenesis in gp130 receptor mutant mice. J. Clin. Invest. 118 (2008) 1727-1738
13. Fitzgerald J.S., Poehlmann T.G., Schleussner E., and Markert U.R. Trophoblast invasion: the role of intracellular cytokine signalling via signal transducer and activator of transcription 3 (STAT3). Hum. Reprod. Update 14 (2008) 335-344
14. Fitzgerald J.S., Tsareva S.A., Poehlmann T.G., Berod L., Meissner A., Corvinus F.M., Wiederanders B., Pfitzner E., Markert U.R., and Friedrich K. Leukemia inhibitory factor triggers activation of signal transducer and activator of transcription 3, proliferation, invasiveness, and altered protease expression in choriocarcinoma cells. Int. J. Biochem. Cell Biol. 37 (2005) 2284-2296
15. Fuhrer D.K., and Yang Y.C. Complex formation of JAK2 with PP2A, P13K, and Yes in response to the hematopoietic cytokine interleukin-11. Biochem. Biophys. Res. Commun. 224 (1996) 289-296
16. Girasole G., Passeri G., Jilka R.L., and Manolagas S.C. Interleukin-11: a new cytokine critical for osteoclast development. J. Clin. Invest. 93 (1994) 1516-1524
17. Hohn H.P., Linke M., Ugele B., and Denker H.W. Differentiation markers and invasiveness: discordant regulation in normal trophoblast and choriocarcinoma cells. Exp. Cell Res. 244 (1998) 249-258
18. Karmakar S., Dhar R., and Das C. Inhibition of cytotrophoblastic (JEG-3) cell invasion by interleukin 12 involves an interferon gamma-mediated pathway. J. Biol. Chem. 279 (2004) 55297-55307
19. Kliman H.J., and Feinberg R.F. Human trophoblast-extracellular matrix (ECM) interactions in vitro: ECM thickness modulates morphology and proteolytic activity. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 3057-3061
20. Makrigiannakis A., Minas V., Kalantaridou S.N., Nikas G., and Chrousos G.P. Hormonal and cytokine regulation of early implantation. Trends Endocrinol. Metab. 17 (2006) 178-185
21. Matadeen R., Hon W.C., Heath J.K., Jones E.Y., and Fuller S. The dynamics of signal triggering in a gp130-receptor complex. Structure 15 (2007) 441-448
22. Mehler M.F., Rozental R., Dougherty M., Spray D.C., and Kessler J.A. Cytokine regulation of neuronal differentiation of hippocampal progenitor cells. Nature 362 (1993) 62-65
23. Montes M., Jaensson E.A., Orozco A.F., Lewis D.E., and Corry D.B. A general method for bead-enhanced quantitation by flow cytometry. J. Immunol. Methods 317 (2006) 45-55
24. Nakayama T., Yoshizaki A., Izumida S., Suehiro T., Miura S., Uemura T., Yakata Y., Shichijo K., Yamashita S., and Sekin I. Expression of interleukin-11 (IL-11) and IL-11 receptor alpha in human gastric carcinoma and IL-11 upregulates the invasive activity of human gastric carcinoma cells. Int. J. Oncol. 30 (2007) 825-833
25. Paiva P., Salamonsen L.A., Manuelpillai U., and Dimitriadis E. Interleukin 11 inhibits human trophoblast invasion indicating a likely role in the decidual restraint of trophoblast invasion during placentation. Biol. Reprod. 80 (2009) 302-310
26. Paiva P., Salamonsen L.A., Manuelpillai U., Walker C., Tapia A., Wallace E.M., and Dimitriadis E. Interleukin-11 promotes migration, but not proliferation, of human trophoblast cells, implying a role in placentation. Endocrinology 148 (2007) 5566-5572
27. Poehlmann T.G., Fitzgerald J.S., Meissner A., Wengenmayer T., Schleussner E., Friedrich K., and Markert U.R. Trophoblast invasion: tuning through LIF, signalling via Stat3. Placenta 26 Suppl. A (2005) S37-S41
28. Regis G., Pensa S., Boselli D., Novelli F., and Poli V. Ups and downs: The STAT1:STAT3 seesaw of Interferon and gp130 receptor signalling. Semin. Cell Dev. Biol. 4 (2008) 351-359
29. Robb L., Li R., Hartley L., Nandurkar H.H., Koentgen F., and Begley C.G. Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nat. Med. 4 (1998) 303-308
30. San Martin S., Poehlmann T., Codina-Canet C., and Markert U.R. Immunohistochemical analysis of trophoblastic cells invading through Matrigel. Placenta 29 (2008) 982-984
31. Schuringa J.J., van der S.S., Vellenga E., Eggen B.J., and Kruijer W. LIF-induced STAT3 signaling in murine versus human embryonal carcinoma (EC) cells. Exp. Cell Res. 274 (2002) 119-129
32. Takeda K., Noguchi K., Shi W., Tanaka T., Matsumoto M., Yoshida N., Kishimoto T., and Akira S. Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 3801-3804
33. Tenney R., Stansfield K., and Pekala P.H. Interleukin 11 signaling in 3T3-L1 adipocytes. J. Cell Physiol. 202 (2005) 160-166
34. Williams J.G. STAT signalling in cell proliferation and in development. Curr. Opin. Genet. Dev. 10 (2000) 503-507
35. Yang J., and Stark G.R. Roles of unphosphorylated STATs in signaling. Cell Res. 18 (2008) 443-451
36. Yoshizaki A., Nakayama T., Yamazumi K., Yakata Y., Taba M., and Sekine I. Expression of interleukin (IL)-11 and IL-11 receptor in human colorectal adenocarcinoma: IL-11 up-regulation of the invasive and proliferative activity of human colorectal carcinoma cells. Int. J. Oncol. 29 (2006) 869-876
37. Zygmunt M., Hahn D., Kiesenbauer N., Munstedt K., and Lang U. Invasion of cytotrophoblastic (JEG-3) cells is up-regulated by interleukin-15 in vitro. Am. J. Reprod. Immunol. 40 (1998) 326-331