Browse > Article

Tumor Necrosis Factor-Related Apoptosis-Inducing Ligand Activates Pro-Survival Signaling Pathways, Nuclear Factor-${\kappa}B$ and Extracellular Signal-Regulated Kinase 1/2 in Trophoblast Cell Line, JEG-3  

Ka Hakhyun (Department of Biological Resources and Technology, Yonsei University)
Publication Information
Abstract
Tumor necrosis factor-related apoptosis inducing ligand (TRAIL) is a well-known inducer of apoptotic cell death in many tumor cells. 1RAIL is expressed in human placenta, and cytotrophoblast cells express 1RAIL receptors. However, the role of TRAIL in human placentas and cytotrophoblast cells is not. well understood. In this study a trophoblast cell line, JEG-3, was used as a model system to examine the effect of TRAIL. on key intracellular signaling pathways involved in the control of trophoblastic cell apoptosis and survival JEG-3 cells expressed receptors for 1RAIL, death receptor (DR) 4, DR5, decoy receptor (OcR) 1 and DeR2. Recombinant human TRAIL (rhTRAIL) did not have a cytotoxic effect determined by MIT assay and did not induce apoptotic cell death determined by poly-(ADP-ribose) polymerase cleavage assay. rhTRAIL induced a rapid and transient nuclear translocation of nuclear $factor-{\kappa}B(NF-{\kappa}B)$ determined by immunoblotting using nuclear protein extracts. rhTRAIL rapidly activated extracellular signal-regulated protein kinase (ERK) 1/2 as determined by immnoblotting for phospho-ERK1/2. However, c-Jun N-terminal kinase (JNK), p38 mitogen-activated protein kinase (p38MAPK) and Akt (protein kinase B) were not activated by rhTRAIL. The ability of 1RAIL to induce $NF-{\kappa}B$ and ERK1/2 suggests that interaction between TRAIL and its receptors may play an important role in trophoblast cell function during pregnancy.
Keywords
Tumor necrosis factor-related apoptosis-inducing ligand; Nuclear factor-KB; Extracellular signal­regulated protein kinase 1/2; Trophoblast cell;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Degli-Esposti MA, Dougall WC, Smolak PJ, Waugh JY, Smith CA, Goodwin RG (1997): The novel receptor TRAIL-R4 induces NF-$\kappa$B and protects against TRAIL-mediated apoptosis, yet retains an incomplete death domain. Immunity 7:813-820   DOI   ScienceOn
2 Franke TF, Hornik CP, Segev L, Shostak GA, Sugimoto C (2003): PI3K/ Akt and apoptosis: size matters. Oncogene 22:8983-8998   DOI   ScienceOn
3 Ghosh S, Karin M (2002): Missing pieces in the NF-$\kappa$B puzzle. Cell 109:S81-S96   DOI   ScienceOn
4 Leverkus M, Sprick MR., Wachter T, Mengling T, Baumann B, Serfling E, Brocker EB, Goebeler M, Neumann M Walczak H (2003): Proteasome inhibition results in TRAIL sensitization of primary keratinocytes by removing the resistance-mediating block of effector caspase maturation. Mol Cell Biol 23:777-790   DOI   ScienceOn
5 Milani D, Zauli G, Rimondi E, Celeghini C, Marmiroli S, Narducci P, Capitani S, Secchiero P (2003): Tumour necrosis factor-related apoptosis-inducing ligand sequentially activates pro-survival and pro-apoptotic pathways in SK-N-MC neuronal cells. J Neurochem 86: 126-135   DOI   ScienceOn
6 Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, Cobb MH (2001): Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 22:153-183   DOI   ScienceOn
7 Schneider P, Thome M, Burns K, Bodmer JL, HofmannK, Kataoka T, Holler N, Tschopp J (1997): TRAIL receptors 1 (DR4) and 2 (DRS) signal FADD-dependent apoptosis and activate NF-$\kappa$B. Immunity 7:831-836   DOI   ScienceOn
8 Sheridan JP, Marsters SA, Pitti RM, Gurney A, Skubatch M, Baldwin D, Ramakrishnan L, Gray CL, Baker K, Wood WI, Goddard AD, Godowski P, Ashkenazi A (1997) Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 277:818-821   DOI   PUBMED   ScienceOn
9 Soldani C, Scovassi AI (2002): Poly(ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis 7:321-328   DOI   ScienceOn
10 Thome M, Schneider P, Hofmann K, Fickenscher H, Meinl E, Neipel F, Mattmann C, Burns K, Bodmer JL, Schroter M, Scaffidi C, Krammer PH, Peter ME, Tschopp J (1997): Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386:517-521   DOI   ScienceOn
11 Wiley SR, Schooley K, Smolak PJ, Din WS, Huang CP, Nicholl JK, Sutherland GR, Smith TD, Rauch C, Smith CA, Goodwin RG (1995): Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 3:673-682   DOI   ScienceOn
12 Franco AV, Zhang XD, Van Berkel E, Sanders JE, Zhang XY, Thomas WD, Nguyen T, Hersey P (2001): The role of NF-$\kappa$B in TNF-related apoptosis-inducing ligand (TRA-IL)-induced apoptosis of melanoma cells. J Immunol 166:5337-5345   DOI
13 Trauzold A, Wermann H, Arlt A, Schutze S, Schafer H, Oestern S, Roder C, Ungefroren H, Lampe E, Heinrich M, Walczak H, Kalthoff H (2001): CD95 and TRAIL receptor-mediated activation of protein kinase C and NF-$\kappa$B contributes to apoptosis resistance in ductal pancreatic adenocarcinoma cells. Oncogene 20:4258-4269   DOI   ScienceOn
14 Fiorucci S, Distrutti E, Ajuebor MN, Mencarelli A, Mannucci R, Palazzetti B, Del Soldato P, Morelli A, Wallace JL (2001): NO-mesalamine protects colonic epithelial cells against apoptotic damage induced by proinflammatory cytokines. Am J Physiol Gastrointest Liver Physiol 281:G654-G665   DOI
15 Secchiero P, Melloni E, Heikinheimo M, Mannisto S, Di Pietro R, Iacone A, Zauli G (2004): TRAIL regulates normal erythroid maturation through an ERK-dependent pathway. Blood 103:517-522   DOI   ScienceOn
16 Bamberger AM, Schulte HM, Thuneke I, Erdmann I, Bamberger CM, Asa SL (1997): Expression of the apoptosis-inducing Fas ligand (FasL) in human first and third trimester placenta and choriocarcinoma cells. J Clin Endocrinol Metab 82:3173-3175   DOI   ScienceOn
17 Phillips TA, Ni J, Hunt JS (2001): Death-inducing tumour necrosis factor (TNF) superfamily ligands and receptors are transcribed in human placentae, cytotrophoblasts, placental macrophages and placental cell lines. Placenta 22:663-672   DOI   ScienceOn
18 Ravi R, Bedi GC, Engstrom LW, Zeng Q, Mookerjee B, Gelinas C, Fuchs EJ, Bedi A (2001): Regulation of death receptor expression and TRAIL/Apo2L-induced apoptosis by NF-$\kappa$B. Nat Cell Biol 3:409-416   DOI   ScienceOn
19 Secchiero P, Gonelli A, Carnevale E, Milani D, Pandolfi A, ZelIa D, Zauli G (2003): TRAIL promotes the survival and proliferation of primary human vascular endothelial cells by activating the Akt and ERK pathways. Circulation 107:2250-2256   DOI   ScienceOn
20 Chou AH, Tsai HF, Lin LL, Hsieh SL, Hsu PI, Hsu PN (2001): Enhanced proliferation and increased IFN-gamma production in T cells by signal transduced through TNF-related apoptosis-inducing ligand. J Immunol 167:1347-1352   DOI
21 Hu WH, Johnson H, Shu HB (1999): Tumor necrosis factor-related apoptosis-inducing ligand receptors signal NF-$\kappa$B and JNK activation and apoptosis through distinct pathways. J Biol Chem 274:30603-30610   DOI
22 Ashkenazi A, Dixit VM (1998): Death receptors: signaling and modulation. Science 281:1305-1308   DOI   PUBMED   ScienceOn
23 Chaudhary PM, Eby M, Jasmin A, Bookwalter A, Murray J, Hood L (1997): Death receptor 5, a new member of the TNFR family, and DR4 induce FADD-dependent apoptosis and activate the NF-$\kappa$B pathway. Immunity 7: 821-830   DOI   ScienceOn
24 Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC(1994): Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371:346-347   DOI   ScienceOn
25 Li Q Verma IM (2002): NF-$\kappa$B regulation in the immune system. Nat Rev Immunol 2:725-734   DOI   ScienceOn
26 Ka H, Hunt JS (2003): Temporal and spatial patterns of expression of inhibitors of apoptosis in human placentas. Am J Pathol 163:413-422   DOI
27 Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M, Chin W, Jones J, Woodward A, Le T, Smith C, Smolak P, Goodwin RG, Rauch CT, Schuh JC, Lynch DH (1999): Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 5:157-163   DOI   ScienceOn
28 Chen HL, Yang YP, Hu XL, Yelavarthi KK, Fishback JL, Hunt JS (1991): 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 139:327-335
29 Locksley RM, Killeen N, Lenardo MJ (2001): The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104:487-501   DOI   ScienceOn
30 Mariani SM, Krammer PH (1998): Differential regulation of TRAIL and CD95 ligand in transformed cells of the T and B lymphocyte lineage. Eur J Immunol 28:973-982   DOI   ScienceOn
31 Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA, Blackie C, Chang L, McMurtrey AE, Hebert A, DeForge L, Koumenis IL, Lewis D, Harris L, Bussiere J, Koeppen H, Shahrokh Z, Schwall RH (1999): Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 104:155-162   DOI   ScienceOn
32 Phillips TA, Ni J, Pan G, Ruben SM, Wei YF, Pace JL, Hunt JS (1999): TRAIL (Apo-2L) and TRAIL receptors in human placentas: implications for immune privilege. J Immunol 162:6053-6059
33 Kita N, Mitsushita J, Ohira S, Takagi Y, Ashida T, Kanai M, Nikaido T, Konishi I (2003): Expression and activation of MAP kinases, ERK1/2, in the human villous trophoblasts. Placenta 24:164-172   DOI   ScienceOn
34 Oya M, Ohtsubo M Takayanagi A, Tachibana M, Shimizu N, Murai M (2001): Constitutive activation of nuclear factor-kappaB prevents TRAIL-induced apoptosis in renal cancer cells. Oncogene 20:3888-3896   DOI   ScienceOn
35 Pitti RM, Marsters SA, Ruppert S, Donahue CJ, Moore A, Ashkenazi A (1996): Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J Biol Chem 271:12687-12690   DOI   ScienceOn
36 Bernard D, Quatannens B, Vandenbunder B, Abbadie C (2001): Rel/NF-$\kappa$B transcription factors protect against tumor necrosis factor (TNF)-related apoptosis-inducing ligand (TRAIL)-induced apoptosis by up-regulating the TRAIL decoy receptor DcR1. J Biol Chem 276:27322-27328   DOI   ScienceOn
37 Pan G, Ni J, Wei YF, Yu G, Gentz R, Dixit VM (1997): An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science 277:815-818   DOI   PUBMED   ScienceOn
38 Cohen GM (1997): Caspases: the executioners of apoptosis. Biochem J 326:1-16   DOI