Non-canonical kinase signaling by the death ligand TRAIL in cancer cells: Discord in the death receptor family

Cell Death and Differentiation

Volumn 20, Issue 7, 2013, Pages 858-868

  Azijli, K ^a,b   Weyhenmeyer, B ^a   Peters, G J ^b   De Jong, S ^a   Kruyt, F A E ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Kinases; Metastasis; Non apoptotic; RIP1

Indexed keywords

DEATH RECEPTOR; FAS ANTIGEN; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOTRANSFERASE; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN KINASE P60; RECEPTOR; RECEPTOR INTERACTING PROTEIN 1; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ANGIOGENESIS; CANCER CELL; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; ENZYME ACTIVATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; DISEASE MODELS, ANIMAL; HUMANS; I-KAPPA B KINASE; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEOPLASMS; NF-KAPPA B; PHOSPHOTRANSFERASES; RECEPTORS, DEATH DOMAIN; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84880271502     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2013.28     Document Type: Review

References (120)

1. Ashkenazi A. Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat Rev Drug Discov 2008; 7: 1001-1012.
2. Pitti RM, Marsters SA, Ruppert S, Donahue CJ, Moore A, Ashkenazi A. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J Biol Chem 1996; 271: 12687-12690.
3. Wiley SR, Schooley K, Smolak PJ, Din WS, Huang CP, Nicholl JK et al. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 1995; 3: 673-682.
4. Fulda S, Debatin KM. Exploiting death receptor signaling pathways for tumor therapy. Biochim Biophys Acta 2004; 1705: 27-41.
5. LeBlanc HN, Ashkenazi A. Apo2L/TRAIL and its death and decoy receptors. Cell Death Differ 2003; 10: 66-75.
6. Merino D, Lalaoui N, Morizot A, Schneider P, Solary E, Micheau O. Differential inhibition of TRAIL-mediated DR5-DISC formation by decoy receptors 1 and 2. Mol Cell Biol 2006; 26: 7046-7055.
7. Adams C, Totpal K, Lawrence D, Marsters S, Pitti R, Yee S et al. Structural and functional analysis of the interaction between the agonistic monoclonal antibody Apomab and the proapoptotic receptor DR5. Cell Death Differ 2008; 15: 751-761.
8. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA et al. Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 1999; 104: 155-162.
9. van der Sloot AM, Tur V, Szegezdi E, Mullally MM, Cool RH, Samali A et al. Designed tumor necrosis factor-related apoptosis-inducing ligand variants initiating apoptosis exclusively via the DR5 receptor. Proc Natl Acad Sci USA 2006; 103: 8634-8639.
10. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M et al. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 1999; 5: 157-163.
11. Lemke J, Noack A, Adam D, Tchikov V, Bertsch U, Roder C et al. TRAIL signaling is mediated by DR4 in pancreatic tumor cells despite the expression of functional DR5. J Mol Med (Berl) 2010; 88: 729-740.
12. MacFarlane M, Inoue S, Kohlhaas SL, Majid A, Harper N, Kennedy DB et al. Chronic lymphocytic leukemic cells exhibit apoptotic signaling via TRAIL-R1. Cell Death Differ 2005; 12: 773-782.
13. Bellail AC, Tse MC, Song JH, Phuphanich S, Olson JJ, Sun SY et al. DR5-mediated DISC controls caspase-8 cleavage and initiation of apoptosis in human glioblastomas. J Cell Mol Med 2010; 14: 1303-1317.
14. Kelley RF, Totpal K, Lindstrom SH, Mathieu M, Billeci K, Deforge L et al. Receptorselective mutants of apoptosis-inducing ligand 2/tumor necrosis factor-related apoptosisinducing ligand reveal a greater contribution of death receptor (DR) 5 than DR4 to apoptosis signaling. J Biol Chem 2005; 280: 2205-2212.
15. Pennarun B, Meijer A, de Vries EG, Kleibeuker JH, Kruyt F, de Jong S. Playing the DISC: turning on TRAIL death receptor-mediated apoptosis in cancer. Biochim Biophys Acta 2010; 1805: 123-140.
16. Ozoren N, El-Deiry WS. Defining characteristics of types I and II apoptotic cells in response to TRAIL. Neoplasia 2002; 4: 551-557.
17. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000; 102: 33-42.
18. Vanlangenakker N, Vanden Berghe T, Vandenabeele P. Many stimuli pull the necrotic trigger, an overview. Cell Death Differ 2012; 19: 75-86.
19. Jouan-Lanhouet S, Arshad MI, Piquet-Pellorce C, Martin-Chouly C, Le Moigne-Muller G, Van HF et al. TRAIL induces necroptosis involving RIPK1/RIPK3-dependent PARP-1 activation. Cell Death Differ 2012; 19: 2003-2014.
20. Falschlehner C, Emmerich CH, Gerlach B, Walczak H. TRAIL signaling: decisions between life and death. Int. J Biochem Cell Biol 2007; 39: 1462-1475.
21. Stegehuis JH, de Wilt LH, de Vries EG, Groen HJ, de Jong S, Kruyt FA. TRAIL receptor targeting therapies for non-small cell lung cancer: current status and perspectives. Drug Resist Updat 2010; 13: 2-15.
22. Hellwig CT, Rehm M. TRAIL signaling and synergy mechanisms used in TRAIL-based combination therapies. Mol Cancer Ther 2012; 11: 3-13.
23. Hotte SJ, Hirte HW, Chen EX, Siu LL, Le LH, Corey A et al. A phase 1 study of mapatumumab (fully human monoclonal antibody to TRAIL-R1) in patients with advanced solid malignancies. Clin Cancer Res 2008; 14: 3450-3455.
24. Merchant MS, Geller JI, Baird K, Chou AJ, Galli S, Charles A et al. Phase I trial and pharmacokinetic study of lexatumumab in pediatric patients with solid tumors. J Clin Oncol 2012; 30: 4141-4147.
25. Soria JC, Smit E, Khayat D, Besse B, Yang X, Hsu CP et al. Phase 1b study of dulanermin (recombinant human Apo2L/TRAIL) in combination with paclitaxel, carboplatin, and bevacizumab in patients with advanced non-squamous non-small-cell lung cancer. J Clin Oncol 2010; 28: 1527-1533.
26. Tolcher AW, Mita M, Meropol NJ, von MM, Patnaik A, Padavic K et al. Phase I pharmacokinetic and biologic correlative study of mapatumumab, a fully human monoclonal antibody with agonist activity to tumor necrosis factor-related apoptosisinducing ligand receptor-1. J Clin Oncol 2007; 25: 1390-1395.
27. Varfolomeev E, Maecker H, Sharp D, Lawrence D, Renz M, Vucic D et al. Molecular determinants of kinase pathway activation by Apo2 ligand/tumor necrosis factor-related apoptosis-inducing ligand. J Biol Chem 2005; 280: 40599-40608.
28. Song JH, Tse MC, Bellail A, Phuphanich S, Khuri F, Kneteman NM et al. Lipid rafts and nonrafts mediate tumor necrosis factor related apoptosis-inducing ligand induced apoptotic and nonapoptotic signals in non small cell lung carcinoma cells. Cancer Res 2007; 67: 6946-6955.
29. Ouyang W, Yang C, Liu Y, Xiong J, Zhang J, Zhong Y et al. Redistribution of DR4 and DR5 in lipid rafts accounts for the sensitivity to TRAIL in NSCLC cells. Int. J Oncol 2011; 39: 1577-1586.
30. Vucic D, Dixit VM, Wertz IE. Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death. Nat Rev Mol Cell Biol 2011; 12: 439-452.
31. Wilson NS, Dixit V, Ashkenazi A. Death receptor signal transducers: nodes of coordination in immune signaling networks. Nat Immunol 2009; 10: 348-355.
32. Chaudhary PM, Eby M, Jasmin A, Bookwalter A, Murray J, Hood L. Death receptor 5, a new member of the TNFR family, and DR4 induce FADD-dependent apoptosis and activate the NF-kappaB pathway. Immunity 1997; 7: 821-830.
33. Schneider P, Thome M, Burns K, Bodmer JL, Hofmann K, Kataoka T et al. TRAIL receptors 1 (DR4) and 2 (DR5) signal FADD-dependent apoptosis and activate NF-kappaB. Immunity 1997; 7: 831-836.
34. Sheridan JP, Marsters SA, Pitti RM, Gurney A, Skubatch M, Baldwin D et al. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 1997; 277: 818-821.
35. Henson ES, Gibson EM, Villanueva J, Bristow NA, Haney N, Gibson SB. Increased expression of Mcl-1 is responsible for the blockage of TRAIL-induced apoptosis mediated by EGF/ErbB1 signaling pathway. J Cell Biochem 2003; 89: 1177-1192.
36. Kreuz S, Siegmund D, Scheurich P, Wajant H. NF-kappaB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol Cell Biol 2001; 21: 3964-3973.
37. Mitsiades N, Mitsiades CS, Poulaki V, Chauhan D, Richardson PG, Hideshima T et al. Biologic sequelae of nuclear factor-kappaB blockade in multiple myeloma: therapeutic applications. Blood 2002; 99: 4079-4086.
38. Ravi R, Bedi GC, Engstrom LW, Zeng Q, Mookerjee B, Gelinas C et al. Regulation of death receptor expression and TRAIL/Apo2L-induced apoptosis by NF-kappaB. Nat. Cell Biol 2001; 3: 409-416.
39. Ehrhardt H, Fulda S, Schmid I, Hiscott J, Debatin KM, Jeremias I. TRAIL induced survival and proliferation in cancer cells resistant towards TRAIL-induced apoptosis mediated by NF-kappaB. Oncogene 2003; 22: 3842-3852.
40. Karacay B, Sanlioglu S, Griffith TS, Sandler A, Bonthius DJ. Inhibition of the NF-kappaB pathway enhances TRAIL-mediated apoptosis in neuroblastoma cells. Cancer Gene Ther 2004; 11: 681-690.
41. Braeuer SJ, Buneker C, Mohr A, Zwacka RM. Constitutively activated nuclear factorkappaB, but not induced NF-kappaB, leads to TRAIL resistance by up-regulation of X-linked inhibitor of apoptosis protein in human cancer cells. Mol Cancer Res 2006; 4: 715-728.
42. Roue G, Perez-Galan P, Lopez-Guerra M, Villamor N, Campo E, Colomer D. Selective inhibition of IkappaB kinase sensitizes mantle cell lymphoma B cells to TRAIL by decreasing cellular FLIP level. J Immunol 2007; 178: 1923-1930.
43. Voortman J, Resende TP, Abou El Hassan MA, Giaccone G, Kruyt FA. TRAIL therapy in non-small cell lung cancer cells: sensitization to death receptor-mediated apoptosis by proteasome inhibitor bortezomib. Mol Cancer Ther 2007; 6: 2103-2112.
44. Jennewein C, Karl S, Baumann B, Micheau O, Debatin KM, Fulda S. Identification of a novel pro-apoptotic role of NF-kappaB in the regulation of T. Oncogene 2012; 31: 1468-1474.
45. Chang L, Karin M. Mammalian MAP kinase signaling cascades. Nature 2001; 410: 37-40.
46. Muhlenbeck F, Haas E, Schwenzer R, Schubert G, Grell M, Smith C et al. TRAIL/Apo2L activates c-Jun NH2-terminal kinase (JNK) via caspase-dependent and caspaseindependent pathways. J Biol Chem 1998; 273: 33091-33098.
47. Herr I, Wilhelm D, Meyer E, Jeremias I, Angel P, Debatin KM. JNK/SAPK activity contributes to TRAIL-induced apoptosis. Cell Death Differ 1999; 6: 130-135.
48. Hu WH, Johnson H, Shu HB. Tumor necrosis factor-related apoptosis-inducing ligand receptors signal NF-kappaB and JNK activation and apoptosis through distinct pathways. J Biol Chem 1999; 274: 30603-30610.
49. Lin Y, Devin A, Cook A, Keane MM, Kelliher M, Lipkowitz S et al. The death domain kinase RIP is essential for TRAIL (Apo2L)-induced activation of IkappaB kinase and c-Jun N-terminal kinase. Mol Cell Biol 2000; 20: 6638-6645.
50. Corazza N, Jakob S, Schaer C, Frese S, Keogh A, Stroka D et al. TRAIL receptormediated JNK activation and Bim phosphorylation critically regulate Fas-mediated liver damage and lethality. J Clin Invest 2006; 116: 2493-2499.
51. Werneburg NW, Guicciardi ME, Bronk SF, Kaufmann SH, Gores GJ. Tumor necrosis factor-related apoptosis-inducing ligand activates a lysosomal pathway of apoptosis that is regulated by Bcl-2 proteins. J Biol Chem 2007; 282: 28960-28970.
52. Park KJ, Lee SH, Lee CH, Jang JY, Chung J, Kwon MH et al. Upregulation of Beclin-1 expression and phosphorylation of Bcl-2 and p53 are involved in the JNK-mediated autophagic cell death. Biochem Biophys Res Commun 2009; 382: 726-729.
53. Ohtsuka T, Buchsbaum D, Oliver P, Makhija S, Kimberly R, Zhou T. Synergistic induction of tumor cell apoptosis by death receptor antibody and chemotherapy agent through JNK/p38 and mitochondrial death pathway. Oncogene 2003; 22: 2034-2044.
54. Mucha SR, Rizzani A, Gerbes AL, Camaj P, Thasler WE, Bruns CJ et al. JNK inhibition sensitises hepatocellular carcinoma cells but not normal hepatocytes to the TNF-related apoptosis-inducing ligand. Gut 2009; 58: 688-698.
55. Ventura JJ, Hubner A, Zhang C, Flavell RA, Shokat KM, Davis RJ. Chemical genetic analysis of the time course of signal transduction by JNK. Mol Cell 2006; 21: 701-710.
56. Mahalingam D, Keane M, Pirianov G, Mehmet H, Samali A, Szegezdi E. Differential activation of JNK1 isoforms by TRAIL receptors modulate apoptosis of colon cancer cell lines. Br J Cancer 2009; 100: 1415-1424.
57. Lee MW, Park SC, Yang YG, Yim SO, Chae HS, Bach JH et al. The involvement of reactive oxygen species (ROS) and p38 mitogen-activated protein (MAP) kinase in TRAIL/Apo2L-induced apoptosis. FEBS Lett 2002; 512: 313-318.
58. Zhang L, Zhu H, Davis JJ, Jacob D, Wu S, Teraishi F et al. Lack of p38 MAP kinase activation in TRAIL-resistant cells is not related to the resistance to TRAIL-mediated cell death. Cancer Biol Ther 2004; 3: 296-301.
59. Son JK, Varadarajan S, Bratton SB. TRAIL-activated stress kinases suppress apoptosis through transcriptional upregulation of MCL-1. Cell Death Differ 2010; 17: 1288-1301.
60. Weldon CB, Parker AP, Patten D, Elliott S, Tang Y, Frigo DE et al. Sensitization of apoptotically-resistant breast carcinoma cells to TNF and TRAIL by inhibition of p38 mitogen-activated protein kinase signaling. Int J Oncol 2004; 24: 1473-1480.
61. Milani D, Zauli G, Rimondi E, Celeghini C, Marmiroli S, Narducci P et al. Tumour necrosis factor-related apoptosis-inducing ligand sequentially activates pro-survival and proapoptotic pathways in SK-N-MC neuronal cells. J Neurochem 2003; 86: 126-135.
62. Vaculova A, Hofmanova J, Soucek K, Kozubik A. Different modulation of TRAIL-induced apoptosis by inhibition of pro-survival pathways in TRAIL-sensitive and TRAIL-resistant colon cancer cells. FEBS Lett 2006; 580: 6565-6569.
63. Belyanskaya LL, Ziogas A, Hopkins-Donaldson S, Kurtz S, Simon HU, Stahel R et al. TRAIL-induced survival and proliferation of SCLC cells is mediated by ERK and dependent on TRAIL-R2/DR5 expression in the absence of caspase-8. Lung Cancer 2008; 60: 355-365.
64. Zhang XD, Borrow JM, Zhang XY, Nguyen T, Hersey P. Activation of ERK1/2 protects melanoma cells from TRAIL-induced apoptosis by inhibiting Smac/DIABLO release from mitochondria. Oncogene 2003; 22: 2869-2881.
65. Vilimanovich U, Bumbasirevic V. TRAIL induces proliferation of human glioma cells by c-FLIPL-mediated activation of ERK1/2. Cell Mol Life Sci 2008; 65: 814-826.
66. Song JJ, Lee YJ. Differential cleavage of Mst1 by caspase-7/-3 is responsible for TRAILinduced activation of the MAPK superfamily. Cell Signal 2008; 20: 892-906.
67. Sun BK, Kim JH, Nguyen HN, Kim SY, Oh S, Lee YJ et al. TRAIL-induced caspase/p38 activation is responsible for the increased catalytic and invasive activities of Akt. Int J Oncol 2011; 38: 249-256.
68. Choo MK, Kawasaki N, Singhirunnusorn P, Koizumi K, Sato S, Akira S et al. Blockade of transforming growth factor-beta-activated kinase 1 activity enhances TRAIL-induced apoptosis through activation of a caspase cascade. Mol. Cancer Ther 2006; 5: 2970-2976.
69. Morioka S, Omori E, Kajino T, Kajino-Sakamoto R, Matsumoto K, Ninomiya-Tsuji J. TAK1 kinase determines TRAIL sensitivity by modulating reactive oxygen species and cIAP. Oncogene 2009; 28: 2257-2265.
70. Trauzold A, Wermann H, Arlt A, Schutze S, Schafer H, Oestern S et al. CD95 and TRAIL receptor-mediated activation of protein kinase C and NF-kappaB contributes to apoptosis resistance in ductal pancreatic adenocarcinoma cells. Oncogene 2001; 20: 4258-4269.
71. Gillespie S, Zhang XD, Hersey P. Variable expression of protein kinase C epsilon in human melanoma cells regulates sensitivity to TRAIL-induced apoptosis. Mol Cancer Ther 2005; 4: 668-676.
72. Shankar E, Sivaprasad U, Basu A. Protein kinase C epsilon confers resistance of MCF-7 cells to TRAIL by Akt-dependent activation of Hdm2 and downregulation of p53. Oncogene 2008; 27: 3957-3966.
73. Harper N, Hughes MA, Farrow SN, Cohen GM, MacFarlane M. Protein kinase C modulates tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by targeting the apical events of death receptor signaling. J Biol Chem 2003; 278: 44338-44347.
74. Farrow B, Thomas RP, Wang XF, Evers BM. Activation of conventional PKC isoforms increases expression of the pro-apoptotic protein Bad and TRAIL receptors. Int J Gastrointest Cancer 2002; 32: 63-72.
75. Chen W, Wang X, Zhuang J, Zhang L, Lin Y. Induction of death receptor 5 and suppression of survivin contribute to sensitization of TRAIL-induced cytotoxicity by quercetin in non-small cell lung cancer cells. Carcinogenesis 2007; 28: 2114-2121.
76. Fresno Vara JA, Casado E, de Castro J, Cejas P, Belda-Iniesta C, Gonzalez-Baron M. PI3K/Akt signaling pathway and cancer. Cancer Treat Rev 2004; 30: 193-204.
77. Zauli G, Sancilio S, Cataldi A, Sabatini N, Bosco D, Di PR. PI-3K/Akt and NF-kappaB/Ikappa Balpha pathways are activated in Jurkat T cells in response to TRAIL treatment. J Cell Physiol 2005; 202: 900-911.
78. Ozes ON, Mayo LD, Gustin JA, Pfeffer SR, Pfeffer LM, Donner DB. NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 1999; 401: 82-85.
79. Wang D, Baldwin AS Jr. Activation of nuclear factor-kappaB-dependent transcription by tumor necrosis factor-alpha is mediated through phosphorylation of RelA/p65 on serine 529. J Biol Chem 1998; 273: 29411-29416.
80. Tanaka H, Fujita N, Tsuruo T. 3-Phosphoinositide-dependent protein kinase-1-mediated IkappaB kinase beta (IkkB) phosphorylation activates NF-kappaB signaling. J Biol Chem 2005; 280: 40965-40973.
81. Xu J, Zhou JY, Wei WZ, Wu GS. Activation of the Akt survival pathway contributes to TRAIL resistance in cancer cells. PLoS One 2010; 5: e10226.
82. Azijli K, Yuvaraj S, Peppelenbosch MP, Wurdinger T, Dekker H, Joore J et al. Kinome profiling of non-canonical TRAIL signaling reveals RIP1-Src-STAT3 dependent invasion in resistant non-small cell lung cancer cells. J Cell Sci 2012; 125: 4651-4661.
83. Song JJ, Kim JH, Sun BK, Alcala MA Jr., Bartlett DL, Lee YJ. c-Cbl acts as a mediator of Src-induced activation of the PI3K-Akt signal transduction pathway during TRAIL treatment. Cell Signal 2010; 22: 377-385.
84. Song JJ, An JY, Kwon YT, Lee YJ. Evidence for two modes of development of acquired tumor necrosis factor-related apoptosis-inducing ligand resistance. Involvement of Bcl-xL. J Biol Chem 2007; 282: 319-328.
85. Lalaoui N, Morle A, Merino D, Jacquemin G, Iessi E, Morizot A et al. TRAIL-R4 promotes tumor growth and resistance to apoptosis in cervical carcinoma HeLa cells through AKT. PLoS One 2011; 6: e19679.
86. De Toni EN, Kuntzen C, Gerbes AL, Thasler WE, Sonuc N, Mucha SR et al. P60-c-src suppresses apoptosis through inhibition of caspase 8 activation in hepatoma cells, but not in primary hepatocytes. J Hepatol 2007; 46: 682-691.
87. Zhang XH, Wang Q, Gerald W, Hudis CA, Norton L, Smid M et al. Latent bone metastasis in breast cancer tied to Src-dependent survival signals. Cancer Cell 2009; 16: 67-78.
88. Cursi S, Rufini A, Stagni V, Condo I, Matafora V, Bachi A et al. Src kinase phosphorylates Caspase-8 on Tyr380: a novel mechanism of apoptosis suppression. EMBO J 2006; 25: 1895-1905.
89. Van Schaeybroeck S, Kelly DM, Kyula J, Stokesberry S, Fennell DA, Johnston PG et al. Src and ADAM-17-mediated shedding of transforming growth factor-alpha is a mechanism of acute resistance to TRAIL. Cancer Res 2008; 68: 8312-8321.
90. Cretney E, Takeda K, Yagita H, Glaccum M, Peschon JJ, Smyth MJ. Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing liganddeficient mice. J Immunol 2002; 168: 1356-1361.
91. Grosse-Wilde A, Voloshanenko O, Bailey SL, Longton GM, Schaefer U, Csernok AI et al. TRAIL-R deficiency in mice enhances lymph node metastasis without affecting primary tumor development. J Clin Invest 2008; 118: 100-110.
92. Ishimura N, Isomoto H, Bronk SF, Gores GJ. Trail induces cell migration and invasion in apoptosis-resistant cholangiocarcinoma cells. Am J Physiol Gastrointest Liver Physiol 2006; 290: G129-G136.
93. Trauzold A, Siegmund D, Schniewind B, Sipos B, Egberts J, Zorenkov D et al. TRAIL promotes metastasis of human pancreatic ductal adenocarcinoma. Oncogene 2006; 25: 7434-7439.
94. Zhou DH, Trauzold A, Roder C, Pan G, Zheng C, Kalthoff H. The potential molecular mechanism of overexpression of uPA, IL-8, MMP-7 and MMP-9 induced by TRAIL in pancreatic cancer cell. Hepatobiliary Pancreat Dis Int 2008; 7: 201-209.
95. Ehrenschwender M, Siegmund D, Wicovsky A, Kracht M, ttrich-Breiholz O, Spindler V et al. Mutant PIK3CA licenses TRAIL and CD95L to induce non-apoptotic caspase-8- mediated ROCK activation. Cell Death Differ 2010; 17: 1435-1447.
96. Hoogwater FJ, Nijkamp MW, Smakman N, Steller EJ, Emmink BL, Westendorp BF et al. Oncogenic K-Ras turns death receptors into metastasis-promoting receptors in human and mouse colorectal cancer cells. Gastroenterology 2010; 138: 2357-2367.
97. Gonzalvez F, Ashkenazi A. New insights into apoptosis signaling by Apo2L/TRAIL. Oncogene 2010; 29: 4752-4765.
98. Secchiero P, Gonelli A, Carnevale E, Milani D, Pandolfi A, Zella D et al. TRAIL promotes the survival and proliferation of primary human vascular endothelial cells by activating the Akt and ERK pathways. Circulation 2003; 107: 2250-2256.
99. Li JH, Kirkiles-Smith NC, McNiff JM, Pober JS. TRAIL induces apoptosis and inflammatory gene expression in human endothelial cells. J Immunol 2003; 171: 1526-1533.
100. Secchiero P, Corallini F, di Iasio MG, Gonelli A, Barbarotto E, Zauli G. TRAIL counteracts the proadhesive activity of inflammatory cytokines in endothelial cells by down-modulating CCL8 and CXCL10 chemokine expression and release. Blood 2005; 105: 3413-3419.
101. Wilson NS, Yang A, Yang B, Couto S, Stern H, Gogineni A et al. Proapoptotic activation of death receptor 5 on tumor endothelial cells disrupts the vasculature and reduces tumor growth. Cancer Cell 2012; 22: 80-90.
102. Secchiero P, Zerbinati C, Rimondi E, Corallini F, Milani D, Grill V et al. TRAIL promotes the survival, migration and proliferation of vascular smooth muscle cells. Cell Mol Life Sci 2004; 61: 1965-1974.
103. Kavurma MM, Schoppet M, Bobryshev YV, Khachigian LM, Bennett MR. TRAIL stimulates proliferation of vascular smooth muscle cells via activation of NF-kappaB and induction of insulin-like growth factor-1 receptor. J Biol Chem 2008; 283: 7754-7762.
104. Chan J, Prado-Lourenco L, Khachigian LM, Bennett MR, Di Bartolo BA, Kavurma MM. TRAIL promotes VSMC proliferation and neointima formation in a FGF-2-, Sp1 phosphorylation-, and NFkappaB-dependent manner. Circ Res 2010; 106: 1061-1071.
105. Chou AH, Tsai HF, Lin LL, Hsieh SL, Hsu PI, Hsu PN. Enhanced proliferation and increased IFN-gamma production in T cells by signal transduced through TNF-related apoptosis-inducing ligand. J Immunol 2001; 167: 1347-1352.
106. Robertson NM, Zangrilli JG, Steplewski A, Hastie A, Lindemeyer RG, Planeta MA et al. Differential expression of TRAIL and TRAIL receptors in allergic asthmatics following segmental antigen challenge: evidence for a role of TRAIL in eosinophil survival. J Immunol 2002; 169: 5986-5996.
107. Morel J, Audo R, Hahne M, Combe B. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) induces rheumatoid arthritis synovial fibroblast proliferation through mitogen-activated protein kinases and phosphatidylinositol 3-kinase/Akt. J Biol Chem 2005; 280: 15709-15718.
108. Rimondi E, Secchiero P, Quaroni A, Zerbinati C, Capitani S, Zauli G. Involvement of TRAIL/TRAIL-receptors in human intestinal cell differentiation. J Cell Physiol 2006; 206: 647-654.
109. Wu NL, Lee TA, Tsai TL, Lin WW. TRAIL-induced keratinocyte differentiation requires caspase activation and p63 expression. J Invest Dermatol 2011; 131: 874-883.
110. Yen ML, Tsai HF, Wu YY, Hwa HL, Lee BH, Hsu PN. TNF-related apoptosis-inducing ligand (TRAIL) induces osteoclast differentiation from monocyte/macrophage lineage precursor cells. Mol Immunol 2008; 45: 2205-2213.
111. Kim JY, Lee JY, Kim DG, Koo GB, Yu JW, Kim YS. TRADD is critical for resistance to TRAIL-induced cell death through NF-kappaB activation. FEBS Lett 2011; 585: 2144-2150.
112. Lluis JM, Nachbur U, Cook WD, Gentle IE, Moujalled D, Moulin M et al. TAK1 is required for survival of mouse fibroblasts treated with TRAIL, and does so by NF-kappaB dependent induction of cFLIPL. PLoS One 2010; 5: e8620.
113. Cao X, Pobezinskaya YL, Morgan MJ, Liu ZG. The role of TRADD in TRAIL-induced apoptosis and signaling. FASEB J 2011; 25: 1353-1358.
114. Peter ME, Budd RC, Desbarats J, Hedrick SM, Hueber AO, Newell MK et al. The CD95 receptor: apoptosis revisited. Cell 2007; 129: 447-450.
115. Desbarats J, Newell MK. Fas engagement accelerates liver regeneration after partial hepatectomy. Nat Med 2000; 6: 920-923.
116. Tamm C, Robertson JD, Sleeper E, Enoksson M, Emgard M, Orrenius S et al. Differential regulation of the mitochondrial and death receptor pathways in neural stem cells. Eur J Neurosci 2004; 19: 2613-2621.
117. Zuliani C, Kleber S, Klussmann S, Wenger T, Kenzelmann M, Schreglmann N et al. Control of neuronal branching by the death receptor CD95 (Fas/Apo-1). Cell Death Differ 2006; 13: 31-40.
118. Lee JK, Sayers TJ, Back TC, Wigginton JM, Wiltrout RH. Lack of FasL-mediated killing leads to in vivo tumor promotion in mouse Lewis lung cancer. Apoptosis 2003; 8: 151-160.
119. Barnhart BC, Legembre P, Pietras E, Bubici C, Franzoso G, Peter ME. CD95 ligand induces motility and invasiveness of apoptosis-resistant tumor cells. EMBO J 2004; 23: 3175-3185.
120. Kleber S, Sancho-Martinez I, Wiestler B, Beisel A, Gieffers C, Hill O et al. Yes and PI3K bind CD95 to signal invasion of glioblastoma. Cancer Cell 2008; 13: 235-248.