Targeting TNF-related apoptosis-inducing ligand (TRAIL) receptor by natural products as a potential therapeutic approach for cancer therapy

Experimental Biology and Medicine

Volumn 240, Issue 6, 2015, Pages 760-773

  Dai, Xiaoyun ^a   Zhang, Jingwen ^a   Arfuso, Frank ^b   Chinnathambi, Arunachalam ^c   Zayed, M E ^c   Alharbi, Sulaiman Ali ^c   Kumar, Alan Prem ^a,b,d,e   Ahn, Kwang Seok ^f   Sethi, Gautam ^a,b,c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b CURTIN UNIVERSITY   (Australia)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e UNIVERSITY OF NORTH TEXAS   (United States)

^f Kyung Hee University   (South Korea)

Author keywords

apoptosis; cancer; natural products; NF B; TRAIL

Indexed keywords

CASPASE; DEATH RECEPTOR 4; DEATH RECEPTOR 5; DULANERMIN; EPIDERMAL GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAPATUMUMAB; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 14; NATURAL PRODUCT; PROTEIN KINASE B; SMALL INTERFERING RNA; STAT3 PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; TUMOR SUPPRESSOR PROTEIN; ANTINEOPLASTIC AGENT; CANCER ANTIBODY; MONOCLONAL ANTIBODY; STAT3 PROTEIN, HUMAN; TNFRSF10A PROTEIN, HUMAN; TNFRSF10B PROTEIN, HUMAN; TNFSF10 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER THERAPY; CELL PROLIFERATION; CELL SURVIVAL; INTRACELLULAR SIGNALING; NON SMALL CELL LUNG CANCER; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SENSITIZATION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; HUMAN; METABOLISM; NEOPLASM;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEOPLASM; ANTINEOPLASTIC AGENTS; APOPTOSIS; DRUG RESISTANCE, NEOPLASM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; NEOPLASMS; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; STAT3 TRANSCRIPTION FACTOR; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84930795938     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1177/1535370215579167     Document Type: Article

References (141)

1. Hanahan D,Weinberg RA.Hallmarks of cancer: the next generation.Cell. 2011;144:646-74
2. Green DR,Kroemer G.The pathophysiology of mitochondrial cell death.Science. 2004;305:626-9
3. Galluzzi L,Kepp O,Kroemer G.Mitochondria: master regulators of danger signalling.Nat Rev Mol Cell Biol. 2012;13:780-8
4. Olivier M,Hollstein M,Hainaut P.TP53 mutations in human cancers: origins, consequences, and clinical use.Cold Spring Harbor Perspect Biol. 2010;2:a001008-a001008
5. Carswell EA,Old LJ,Kassel RL,Green S,Fiore N,Williamson B.An endotoxin-induced serum factor that causes necrosis of tumors.Proceedings of the National Academy of Sciences of the United States of America. 1975;72:3666-70
6. Trauth BC,Klas C,Peters AM,Matzku S,Moller P,Falk W,Debatin KM,Krammer PH.Monoclonal antibody-mediated tumor regression by induction of apoptosis.Science. 1989;245:301-5
7. Itoh N,Yonehara S,Ishii A,Yonehara M,Mizushima S,Sameshima M,Hase A,Seto Y,Nagata S.The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis.Cell. 1991;66:233-43
8. Ogasawara J,Watanabe-Fukunaga R,Adachi M,Matsuzawa A,Kasugai T,Kitamura Y,Itoh N,Suda T,Nagata S.Lethal effect of the anti-Fas antibody in mice.Nature. 1993;364:806-9
9. 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;271:12687-90
10. Wiley SR,Schooley K,Smolak PJ,Din WS,Huang CP,Nicholl JK,Sutherland GR,Smith TD,Rauch C,Smith CA,Goodwin RG.Identification and characterization of a new member of the TNF family that induces apoptosis.Immunity. 1995;3:673-82
11. 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.Safety and antitumor activity of recombinant soluble Apo2 ligand.J Clin Invest. 1999;104:155-62
12. 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.Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo.Nat Med. 1999;5:157-63
13. Gasparian ME,Chernyak BV,Dolgikh DA,Yagolovich AV,Popova EN,Sycheva AM,Moshkovskii SA,Kirpichnikov MP.Generation of new TRAIL mutants DR5-A and DR5-B with improved selectivity to death receptor 5.Apoptosis: Int J Program Cell Death. 2009;14:778-87
14. Wagner KW,Punnoose EA,Januario T,Lawrence DA,Pitti RM,Lancaster K,Lee D,von Goetz M,Yee SF,Totpal K,Huw L,Katta V,Cavet G,Hymowitz SG,Amler L,Ashkenazi A.Death-receptor O-glycosylation controls tumor-cell sensitivity to the proapoptotic ligand Apo2L/TRAIL.Nat Med. 2007;13:1070-7
15. Scaffidi C,Schmitz I,Krammer PH,Peter ME.The role of c-FLIP in modulation of CD95-induced apoptosis.J Biol Chem. 1999;274:1541-8
16. Gonzalvez F,Ashkenazi A.New insights into apoptosis signaling by Apo2L/TRAIL.Oncogene. 2010;29:4752-65
17. Luo X,Budihardjo I,Zou H,Slaughter C,Wang X.Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors.Cell. 1998;94:481-90
18. 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
19. Hinz S,Trauzold A,Boenicke L,Sandberg C,Beckmann S,Bayer E,Walczak H,Kalthoff H,Ungefroren H.Bcl-XL protects pancreatic adenocarcinoma cells against CD95- and TRAIL-receptor-mediated apoptosis.Oncogene. 2000;19:5477-86
20. Sun SY,Yue P,Zhou JY,Wang Y,Choi Kim HR,Lotan R,Wu GS.Overexpression of BCL2 blocks TNF-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in human lung cancer cells.Biochem Biophys Res Commun. 2001;280:788-97
21. 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;22:3842-52
22. 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;11:681-90
23. Braeuer SJ,Buneker C,Mohr A,Zwacka RM.Constitutively activated nuclear factor-kappaB, 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: MCR. 2006;4:715-28
24. 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;178:1923-30
25. 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 Therapeut. 2007;6:2103-12
26. 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 TRAIL- and CD95-mediated apoptosis of glioblastoma cells.Oncogene. 2012;31:1468-74
27. Ou D,Wang X,Metzger DL,Robbins M,Huang J,Jobin C,Chantler JK,James RF,Pozzilli P,Tingle AJ.Regulation of TNF-related apoptosis-inducing ligand-mediated death-signal pathway in human beta cells by Fas-associated death domain and nuclear factor kappaB.Human Immunol. 2005;66:799-809
28. Ravi R,Bedi GC,Engstrom LW,Zeng Q,Mookerjee B,Gelinas C,Fuchs EJ,Bedi A.Regulation of death receptor expression and TRAIL/Apo2L-induced apoptosis by NF-kappaB.Nat Cell Biol. 2001;3:409-16
29. Chen X,Kandasamy K,Srivastava RK.Differential roles of RelA (p65) and c-Rel subunits of nuclear factor kappa B in tumor necrosis factor-related apoptosis-inducing ligand signaling.Cancer Res. 2003;63:1059-66
30. Trauzold A,Siegmund D,Schniewind B,Sipos B,Egberts J,Zorenkov D,Emme D,Roder C,Kalthoff H,Wajant H.TRAIL promotes metastasis of human pancreatic ductal adenocarcinoma.Oncogene. 2006;25:7434-9
31. Varfolomeev E,Maecker H,Sharp D,Lawrence D,Renz M,Vucic D,Ashkenazi A.Molecular determinants of kinase pathway activation by Apo2 ligand/tumor necrosis factor-related apoptosis-inducing ligand.J Biol Chem. 2005;280:40599-608
32. 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;274:30603-10
33. Lin Y,Devin A,Cook A,Keane MM,Kelliher M,Lipkowitz S,Liu ZG.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;20:6638-45
34. Corazza N,Jakob S,Schaer C,Frese S,Keogh A,Stroka D,Kassahn D,Torgler R,Mueller C,Schneider P,Brunner T.TRAIL receptor-mediated JNK activation and Bim phosphorylation critically regulate Fas-mediated liver damage and lethality.J Clin Investig. 2006;116:2493-9
35. 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;282:28960-70
36. Park KJ,Lee SH,Lee CH,Jang JY,Chung J,Kwon MH,Kim YS.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;382:726-9
37. Mucha SR,Rizzani A,Gerbes AL,Camaj P,Thasler WE,Bruns CJ,Eichhorst ST,Gallmeier E,Kolligs FT,Goke B,De Toni EN.JNK inhibition sensitises hepatocellular carcinoma cells but not normal hepatocytes to the TNF-related apoptosis-inducing ligand.Gut. 2009;58:688-98
38. 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;21:701-10
39. 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;100:1415-24
40. Son JK,Varadarajan S,Bratton SB.TRAIL-activated stress kinases suppress apoptosis through transcriptional upregulation of MCL-1.Cell Death Different. 2010;17:1288-301
41. Lee MW,Park SC,Yang YG,Yim SO,Chae HS,Bach JH,Lee HJ,Kim KY,Lee WB,Kim SS.The involvement of reactive oxygen species (ROS) and p38 mitogen-activated protein (MAP) kinase in TRAIL/Apo2L-induced apoptosis.FEBS Lett. 2002;512:313-8
42. Weldon CB,Parker AP,Patten D,Elliott S,Tang Y,Frigo DE,Dugan CM,Coakley EL,Butler NN,Clayton JL,Alam J,Curiel TJ,Beckman BS,Jaffe BM,Burow ME.Sensitization of apoptotically-resistant breast carcinoma cells to TNF and TRAIL by inhibition of p38 mitogen-activated protein kinase signaling.Int J Oncol. 2004;24:1473-80
43. Zhang L,Zhu H,Davis JJ,Jacob D,Wu S,Teraishi F,Gutierrez A,Wang Y,Fang B.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
44. Milani D,Zauli G,Rimondi E,Celeghini C,Marmiroli S,Narducci P,Capitani S,Secchiero P.Tumour necrosis factor-related apoptosis-inducing ligand sequentially activates pro-survival and pro-apoptotic pathways in SK-N-MC neuronal cells.J Neurochem. 2003;86:126-35
45. 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;22:2869-81
46. Song JJ,Lee YJ.Differential cleavage of Mst1 by caspase-7/-3 is responsible for TRAIL-induced activation of the MAPK superfamily.Cell Signal. 2008;20:892-906
47. 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;580:6565-9
48. Belyanskaya LL,Ziogas A,Hopkins-Donaldson S,Kurtz S,Simon HU,Stahel R,Zangemeister-Wittke U.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;60:355-65
49. Vilimanovich U,Bumbasirevic V.TRAIL induces proliferation of human glioma cells by c-FLIPL-mediated activation of ERK1/2.Cell Mol Life Sci: CMLS. 2008;65:814-26
50. Fresno Vara JA,Casado E,de Castro J,Cejas P,Belda-Iniesta C,Gonzalez-Baron M.PI3K/Akt signalling pathway and cancer.Cancer Treat Rev. 2004;30:193-204
51. Song JJ,Kim JH,Sun BK,Alcala MA,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;22:377-85
52. Azijli K,Yuvaraj S,Peppelenbosch MP,Wurdinger T,Dekker H,Joore J,van Dijk E,Quax WJ,Peters GJ,de Jong S,Kruyt FA.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;125:4651-61
53. 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-e10226
54. Cursi S,Rufini A,Stagni V,Condo I,Matafora V,Bachi A,Bonifazi AP,Coppola L,Superti-Furga G,Testi R,Barila D.Src kinase phosphorylates Caspase-8 on Tyr380: a novel mechanism of apoptosis suppression.EMBO J. 2006;25:1895-905
55. Van Schaeybroeck S,Kelly DM,Kyula J,Stokesberry S,Fennell DA,Johnston PG,Longley DB.Src and ADAM-17-mediated shedding of transforming growth factor-alpha is a mechanism of acute resistance to TRAIL.Cancer Res. 2008;68:8312-21
56. Takeda K,Hayakawa Y,Smyth MJ,Kayagaki N,Yamaguchi N,Kakuta S,Iwakura Y,Yagita H,Okumura K.Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells.Nat Med. 2001;7:94-100
57. Kayagaki N,Yamaguchi N,Nakayama M,Takeda K,Akiba H,Tsutsui H,Okamura H,Nakanishi K,Okumura K,Yagita H.Expression and function of TNF-related apoptosis-inducing ligand on murine activated NK cells.J Immunol. 1999;163:1906-13
58. Gong B,Almasan A.Genomic organization and transcriptional regulation of human Apo2/TRAIL gene.Biochem Biophys Res Commun. 2000;278:747-52
59. Toomey NL,Deyev VV,Wood C,Boise LH,Scott D,Liu LH,Cabral L,Podack ER,Barber GN,Harrington WJ.Induction of a TRAIL-mediated suicide program by interferon alpha in primary effusion lymphoma.Oncogene. 2001;20:7029-40
60. Takeda K,Smyth MJ,Cretney E,Hayakawa Y,Kayagaki N,Yagita H,Okumura K.Critical role for tumor necrosis factor-related apoptosis-inducing ligand in immune surveillance against tumor development.J Exp Med. 2002;195:161-9
61. Mace TA,Yamane N,Cheng J,Hylander BL,Repasky EA.The potential of the tumor microenvironment to influence Apo2L/TRAIL induced apoptosis.Immunol Investig. 2006;35:279-96
62. Cretney E,Takeda K,Yagita H,Glaccum M,Peschon JJ,Smyth MJ.Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice.J Immunol. 2002;168:1356-61
63. Seki N,Hayakawa Y,Brooks AD,Wine J,Wiltrout RH,Yagita H,Tanner JE,Smyth MJ,Sayer TJ.Tumor necrosis factor-related apoptosis-inducing ligand-mediated apoptosis is an important endogenous mechanism for resistance to liver metastases in murine renal cancer.Cancer Res. 2003;63:207-13
64. Grosse-Wilde A,Voloshanenko O,Bailey SL,Longton GM,Schaefer U,Csernok AI,Schutz G,Greiner EF,Kemp CJ,Walczak H.TRAIL-R deficiency in mice enhances lymph node metastasis without affecting primary tumor development.J Clin Investig. 2008;118:100-10
65. Wang S,El-Deiry WS.Inducible silencing of KILLER/DR5 in vivo promotes bioluminescent colon tumor xenograft growth and confers resistance to chemotherapeutic agent 5-fluorouracil.Cancer Res. 2004;64:6666-72
66. Lemke J,von Karstedt S,Zinngrebe J,Walczak H.Getting TRAIL back on track for cancer therapy.Cell Death Different. 2014;21:1350-64
67. Herbst RS,Eckhardt SG,Kurzrock R,Ebbinghaus S,O'Dwyer PJ,Gordon MS,Novotny W,Goldwasser MA,Tohnya TM,Lum BL,Ashkenazi A,Jubb AM,Mendelson DS.Phase I dose-escalation study of recombinant human Apo2L/TRAIL, a dual proapoptotic receptor agonist, in patients with advanced cancer.J Clin Oncol. 2010;28:2839-46
68. Wainberg ZA,Messersmith WA,Peddi PF,Kapp AV,Ashkenazi A,Royer-Joo S,Portera CC,Kozloff MF.A phase 1B study of dulanermin in combination with modified FOLFOX6 plus bevacizumab in patients with metastatic colorectal cancer.Clin Colorect Cancer. 2013;12:248-54
69. Kasubhai SM,Bendell JC,Kozloff M,Kapp AV,Ashkenazi A,Royer-Joo S,Portera CC.Phase Ib study of dulanermin combined with FOLFIRI (with or without bevacizumab [BV]) in previously treated patients (Pts) with metastatic colorectal cancer (mCRC).J Clin Oncol. 2012;30 (15): 3543
70. Yee L,Burris HA,Kozloff M,Wainberg Z,Pao M,Skettino S,Novotny W,Durbin B,Weston J,Hurwitz H.Phase Ib study of recombinant human Apo2L/TRAIL plus irinotecan and cetuximab or FOLFIRI in metastatic colorectal cancer (mCRC) patients (pts): preliminary results.J Clin Oncol. 2009;27 (15): 4129
71. Soria JC,Mark Z,Zatloukal P,Szima B,Albert I,Juhasz E,Pujol JL,Kozielski J,Baker N,Smethurst D,Hei YJ,Ashkenazi A,Stern H,Amler L,Pan Y,Blackhall F.Randomized phase II study of dulanermin in combination with paclitaxel, carboplatin, and bevacizumab in advanced non-small-cell lung cancer.J Clin Oncol. 2011;29:4442-51
72. Yee L, Fanale M, Dimick K, Calvert S, Robin C, Ing J. A phase IB safety and pharmacokinetic (PK) study of recombinant human Apo2L/TRAIL in combination with rituximab in patients with low-grade non-Hodgkin lymphoma. J Clin Oncol 2007;25(abstract 8078).
73. Belada D,Mayer J,Czuczman MS,Flinn IW,Durbin-Johnson B,Bray GL.Phase II study of dulanermin plus rituximab in patients with relapsed follicular non-Hodgkin’s lymphoma (NHL).J Clin Oncol. 2010;28 (15): 8104
74. Tolcher AW,Mita M,Meropol NJ,von Mehren M,Patnaik A,Padavic K,Hill M,Mays T,McCoy T,Fox NL,Halpern W,Corey A,Cohen RB.Phase I pharmacokinetic and biologic correlative study of mapatumumab, a fully human monoclonal antibody with agonist activity to tumor necrosis factor-related apoptosis-inducing ligand receptor-1.J Clin Oncol. 2007;25:1390-5
75. Hotte SJ,Hirte HW,Chen EX,Siu LL,Le LH,Corey A,Iacobucci A,Maclean M,Lo L,Fox NL,Oza AM.A phase 1 study of mapatumumab (fully human monoclonal antibody to TRAIL-R1) in patients with advanced solid malignancies.Clin Cancer Res: Off J Am Assoc Cancer Res. 2008;14:3450-5
76. Mom CH,Verweij J,Oldenhuis CNAM.Mapatumumab, a fully human agonistic monoclonal antibody that targets TRAIL-R1, in combination with gemcitabine and cisplatin: a phase I study (vol 15, pg 5584, 2009).Clin Cancer Res. 2009;15:6744-6744
77. Leong S,Cohen RB,Gustafson DL,Langer CJ,Camidge DR,Padavic K,Gore L,Smith M,Chow LQ,von Mehren M,O'Bryant C,Hariharan S,Diab S,Fox NL,Miceli R,Eckhardt SG.Mapatumumab, an antibody targeting TRAIL-R1, in combination with paclitaxel and carboplatin in patients with advanced solid malignancies: results of a phase I and pharmacokinetic study.J Clin Oncol. 2009;27:4413-21
78. Younes A,Vose JM,Zelenetz AD,Smith MR,Burris HA,Ansell SM,Klein J,Halpern W,Miceli R,Kumm E,Fox NL,Czuczman MS.A Phase 1b/2 trial of mapatumumab in patients with relapsed/refractory non-Hodgkin’s lymphoma.Br J Cancer. 2010;103:1783-7
79. Trarbach T,Moehler M,Heinemann V,Kohne CH,Przyborek M,Schulz C,Sneller V,Gallant G,Kanzler S.Phase II trial of mapatumumab, a fully human agonistic monoclonal antibody that targets and activates the tumour necrosis factor apoptosis-inducing ligand receptor-1 (TRAIL-R1), in patients with refractory colorectal cancer.Br J Cancer. 2010;102:506-12
80. Greco FA,Bonomi P,Crawford J,Kelly K,Oh Y,Halpern W,Lo L,Gallant G,Klein J.Phase 2 study of mapatumumab, a fully human agonistic monoclonal antibody which targets and activates the TRAIL receptor-1, in patients with advanced non-small cell lung cancer.Lung Cancer. 2008;61:82-90
81. Belch A,Sharma A,Spencer A,Tarantolo S,Bahlis NJ,Doval D.A multicenter randomized phase ii trial of mapatumumab, a TRAIL-R1 agonist monoclonal antibody, in combination with bortezomib in patients with relapsed/refractory multiple myeloma (MM).Blood. 2010;116:abstracts 5031-abstracts 5031
82. von Pawel J,Harvey JH,Spigel DR,Dediu M,Reck M,Cebotaru CL,Humphreys RC,Gribbin MJ,Fox NL,Camidge DR.Phase II trial of mapatumumab, a fully human agonist monoclonal antibody to tumor necrosis factor-related apoptosis-inducing ligand receptor 1 (TRAIL-R1), in combination with paclitaxel and carboplatin in patients with advanced non-small-cell lung cancer.Clin Lung Cancer. 2014;15:188-96 e2
83. Doi T,Murakami H,Ohtsu A,Fuse N,Yoshino T,Yamamoto N,Boku N,Onozawa Y,Hsu CP,Gorski KS,Fiberg G,Kawaguchi T,Sasaki T.Phase 1 study of conatumumab, a pro-apoptotic death receptor 5 agonist antibody, in Japanese patients with advanced solid tumors.Cancer Chemother Pharmacol. 2011;68:733-41
84. Chawla SP,Tabernero J,Kindler HL,Chiorean EG,LoRusso P,Hsu M,Haddad V,Bach BA,Baselga J.Phase I evaluation of the safety of conatumumab (AMG 655) in combination with ARM 479 in patients (pts) with advanced, refractory solid tumors.J Clin Oncol. 2010;28 (15): 3102
85. Demetri GD,Le Cesne A,Chawla SP,Brodowicz T,Maki RG,Bach BA,Smethurst DP,Bray S,Hei YJ,Blay JY.First-line treatment of metastatic or locally advanced unresectable soft tissue sarcomas with conatumumab in combination with doxorubicin or doxorubicin alone: a phase I/II open-label and double-blind study.Eur J Cancer. 2012;48:547-63
86. Paz-Ares L,Balint B,de Boer RH,van Meerbeeck JP,Wierzbicki R,De Souza P,Galimi F,Haddad V,Sabin T,Hei YJ,Pan Y,Cottrell S,Hsu CP,RamLau R.A randomized phase 2 study of paclitaxel and carboplatin with or without conatumumab for first-line treatment of advanced non-small-cell lung cancer.J Thorac Oncol. 2013;8:329-37
87. Saltz L,Infante J,Schwartzberg L,Stephenson J,Rocha-Lima C,Galimi F,Dillingham K,Hsu M,Wiezorek J,Fuchs C.Safety and efficacy of AMG 655 plus modified FOLFOX6 (mFOLFOX6) and bevacizumab (B) for the first-line treatment of patients (pts) with metastatic colorectal cancer (mCRC).J Clin Oncol. 2009;27 (15): 4079
88. Kindler HL,Garbo L,Stephenson J,Wiezorek J,Sabin T,Hsu M,Civoli F,Richards D.A phase Ib study to evaluate the safety and efficacy of AMG 655 in combination with gemcitabine (G) in patients (pts) with metastatic pancreatic cancer (PC).J Clin Oncol. 2009;27 (15): 4501-4501
89. Kindler HL,Richards DA,Garbo LE,Garon EB,Stephenson JJ,Rocha-Lima CM,Safran H,Chan D,Kocs DM,Galimi F,McGreivy J,Bray SL,Feigal EG,Loh E,Fuchs CS.A randomized, placebo-controlled phase 2 study of ganitumab (AMG 479) or conatumumab (AMG 655) in combination with gemcitabine in patients with metastatic pancreatic cancer.Ann Oncol: Off J Eur Soc Med Oncol/ESMO. 2012;23:2834-42
90. Cohn AL,Tabernero J,Maurel J,Nowara E,Sastre J,Chuah BY,Koop MV,Sakaeva DD,Mitchell EP,Dubeyy S,Suzuki S,Hei YJ,Galimi F,McCaffery I,Pan Y,Loberg R,Cottrel S,Choo SP.A randomized, placebo-controlled phase 2 study of ganitumab or conatumumab in combination with FOLFIRI for second-line treatment of mutant KRAS metastatic colorectal cancer.Ann Oncol: Off J Eur Soc Med Oncol/ESMO. 2013;24:1777-85
91. Fuchs CS,Fakih M,Schwartzberg L,Cohn AL,Yee L,Dreisbach L,Kozloff MF,Hei YJ,Galimi F,Pan Y,Haddad V,Hsu CP,Sabin A,Saltz L.TRAIL receptor agonist conatumumab with modified FOLFOX6 plus bevacizumab for first-line treatment of metastatic colorectal cancer: a randomized phase 1b/2 trial.Cancer. 2013;119:4290-8
92. Plummer R,Attard G,Pacey S,Li L,Razak A,Perrett R,Barrett M,Judson I,Kaye S,Fox NL,Halpern W,Corey A,Calvert H,Bone J.Phase 1 and pharmacokinetic study of lexatumumab in patients with advanced cancers.Clin Cancer Res: Off J Am Assoc Cancer Res. 2007;13:6187-94
93. Wakelee HA,Patnaik A,Sikic BI,Mita M,Fox NL,Miceli R,Ullrich SJ,Fisher GA,Tolcher AW.Phase I and pharmacokinetic study of lexatumumab (HGS-ETR2) given every 2 weeks in patients with advanced solid tumors.Ann Oncol: Off J Eur Soc Med Oncol/ESMO. 2010;21:376-81
94. Sikic BI,Wakelee HA,Von Mehren M,Lewis N,Calvert AH,Plummer ER.A Phase 1b study to assess the safety of lexatumumab, a human monoclonal antibody that activates TRAIL-R2, in combination with gemcitabine, pemetrexed, doxorubicin or FOLFIRI.J Clin Oncol. 2007;25:18S 14006-18S 14006
95. Merchant MS,Geller JI,Baird K,Chou AJ,Galli S,Charles A,Amaoko M,Rhee EH,Price A,Wexler LH,Meyers PA,Widemann BC,Tsokos M,Mackall CL.Phase I trial and pharmacokinetic study of lexatumumab in pediatric patients with solid tumors.J Clin Oncol. 2012;30:4141-7
96. Forero-Torres A,Shah J,Wood T,Posey J,Carlisle R,Copigneaux C,Luo F,Wojetowicz-Praga S,Percent I,Saleh M.Phase I trial of weekly tigatuzumab, an agonistic humanized monoclonal antibody targeting death receptor 5 (DR5).Cancer Biother Radiopharmaceut. 2010;25:13-9
97. Forero-Torres A,Infante JR,Waterhouse D,Wong L,Vickers S,Arrowsmith E,He AR,Hart L,Trent D,Wade J,Jin X,Wang Q,Austin T,Rosen M,Beckman R,Roemeling RV,Greenberg Jonathan,Saleh Mansoor.Phase 2, multicenter, open-label study of tigatuzumab (CS-1008), a humanized monoclonal antibody targeting death receptor 5, in combination with gemcitabine in chemotherapy-naive patients with unresectable or metastatic pancreatic cancer.Cancer Med. 2013;2:925-32
98. Reck M,Krzakowski M,Chmielowska E,Sebastian M,Hadler D,Fox T,Wang Q,Greenberg J,Beckman RA,Pawel JV.A randomized, double-blind, placebo-controlled phase 2 study of tigatuzumab (CS-1008) in combination with carboplatin/paclitaxel in patients with chemotherapy-naive metastatic/unresectable non-small cell lung cancer.Lung Cancer. 2013;82:441-8
99. Rocha Lima CM,Bayraktar S,Flores AM,MacIntyre J,Montero A,Baranda JC,Wallmark J,Portera C,Raja R,Stern H,Royer-Joo S,Amler LC.Phase Ib study of drozitumab combined with first-line mFOLFOX6 plus bevacizumab in patients with metastatic colorectal cancer.Cancer Investig. 2012;30:727-31
100. Camidge DR,Herbst RS,Gordon MS,Eckhardt SG,Kurzrock R,Durbin B,Ing J,Tohnya TM,Jason S,Ashkenazi A,Bray G,Mendelson D.A phase I safety and pharmacokinetic study of the death receptor 5 agonistic antibody PRO95780 in patients with advanced malignancies.Clin Cancer Res: Off J Am Assoc Cancer Res. 2010;16:1256-63
101. Sharma S,de Vries EG,Infante JR,Oldenhuis CN,Gietema JA,Yang L,Sanela B,Katie P,Michael G,Jeffrey WS,Howard AB.Safety, pharmacokinetics, and pharmacodynamics of the DR5 antibody LBY135 alone and in combination with capecitabine in patients with advanced solid tumors.Investig New Drugs. 2014;32:135-44
102. Fas SC,Baumann S,Zhu JY,Giaisi M,Treiber MK,Mahlknecht U,Krammer PH,Weber ML.Wogonin sensitizes resistant malignant cells to TNFalpha- and TRAIL-induced apoptosis.Blood. 2006;108:3700-6
103. Labsch S,Liu L,Bauer N,Zhang Y,Aleksandrowicz E,Gladkich J,Shonsiegel F,Herr I.Sulforaphane and TRAIL induce a synergistic elimination of advanced prostate cancer stem-like cells.Int J Oncol. 2014;44:1470-80
104. Wang C,Chen T,Zhang N,Yang M,Li B,Lu X,Cao X,Ling C.Melittin, a major component of bee venom, sensitizes human hepatocellular carcinoma cells to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis by activating CaMKII-TAK1-JNK/p38 and inhibiting IkappaBalpha kinase-NFkappaB.J Biol Chem. 2009;284:3804-13
105. Szliszka E,Zydowicz G,Janoszka B,Dobosz C,Kowalczyk-Ziomek G,Krol W.Ethanolic extract of Brazilian green propolis sensitizes prostate cancer cells to TRAIL-induced apoptosis.Int J Oncol. 2011;38:941-53
106. Hussain AR,Ahmed M,Al-Jomah NA,Khan AS,Manogaran P,Sultana M,Abubaker J,Platanisa LC,Ai-Kuraya KS,Uddin S.Curcumin suppresses constitutive activation of nuclear factor-kappa B and requires functional Bax to induce apoptosis in Burkitt’s lymphoma cell lines.Mol Cancer Therapeut. 2008;7:3318-29
107. Seo OW,Kim JH,Lee KS,Lee KS,Kim JH,Won MH,Ha KS,Kwon YG,Kim YM.Kurarinone promotes TRAIL-induced apoptosis by inhibiting NF-kappaB-dependent cFLIP expression in HeLa cells.Exp Mol Med. 2012;44:653-64
108. Ivanov VN,Partridge MA,Johnson GE,Huang SX,Zhou H,Hei TK.Resveratrol sensitizes melanomas to TRAIL through modulation of antiapoptotic gene expression.Exp Cell Res. 2008;314:1163-76
109. Thanaketpaisarn O,Waiwut P,Sakurai H,Saiki I.Artesunate enhances TRAIL-induced apoptosis in human cervical carcinoma cells through inhibition of the NF-kappaB and PI3K/Akt signaling pathways.Int J Oncol. 2011;39:279-85
110. Zhang C,Wu R,Zhu H,Hu YZ,Jiang H,Lin NM,He QJ,Yang B.Enhanced anti-tumor activity by the combination of TRAIL/Apo-2L and combretastatin A-4 against human colon cancer cells via induction of apoptosis in vitro and in vivo.Cancer Lett. 2011;302:11-9
111. Lirdprapamongkol K,Sakurai H,Abdelhamed S,Yokoyama S,Athikomkulchai S,Viriyaroj A,Awale S,Ruchirawat S,Svasti J,Saiki L.Chrysin overcomes TRAIL resistance of cancer cells through Mcl-1 downregulation by inhibiting STAT3 phosphorylation.Int J Oncol. 2013;43:329-37
112. Braig S,Bischoff F,Abhari BA,Meijer L,Fulda S,Skaltsounis L,Vollmar AM.The pleiotropic profile of the indirubin derivative 6BIO overcomes TRAIL resistance in cancer.Biochem Pharmacol. 2014;91:157-67
113. Dong Y,Yin S,Li J,Jiang C,Ye M,Hu H.Bufadienolide compounds sensitize human breast cancer cells to TRAIL-induced apoptosis via inhibition of STAT3/Mcl-1 pathway.Apoptosis: Int J Program Cell Death. 2011;16:394-403
114. Carlisi D,D’Anneo A,Angileri L,Lauricella M,Emanuele S,Santulli A,Vento R,Tesoriere G.Parthenolide sensitizes hepatocellular carcinoma cells to TRAIL by inducing the expression of death receptors through inhibition of STAT3 activation.J Cell Physiol. 2011;226:1632-41
115. Ou YC,Li JR,Kuan YH,Raung SL,Wang CC,Hung YY,Pan PH,Lu HC,Chen CJ.Luteolin sensitizes human 786-O renal cell carcinoma cells to TRAIL-induced apoptosis.Life Sci. 2014;100:110-7
116. Lee J,Hwangbo C,Lee JJ,Seo J,Lee JH.The sesquiterpene lactone eupatolide sensitizes breast cancer cells to TRAIL through down-regulation of c-FLIP expression.Oncol Reports. 2010;23:229-37
117. Choi WY,Jin CY,Han MH,Kim GY,Kim ND,Lee WH,Kim SK,Choi YH.Sanguinarine sensitizes human gastric adenocarcinoma AGS cells to TRAIL-mediated apoptosis via down-regulation of AKT and activation of caspase-3.Anticancer Res. 2009;29:4457-65
118. Moon DO,Kim MO,Choi YH,Kim GY.Butein sensitizes human hepatoma cells to TRAIL-induced apoptosis via extracellular signal-regulated kinase/Sp1-dependent DR5 upregulation and NF-kappaB inactivation.Mol Cancer Therapeut. 2010;9:1583-95
119. Sung B,Ravindran J,Prasad S,Pandey MK,Aggarwal BB.Gossypol induces death receptor-5 through activation of the ROS-ERK-CHOP pathway and sensitizes colon cancer cells to TRAIL.J Biol Chem. 2010;285:35418-27
120. Kim EY,Yu JS,Yang M,Kim AK.Sub-toxic dose of apigenin sensitizes HepG2 cells to TRAIL through ERK-dependent up-regulation of TRAIL receptor DR5.Mol Cells. 2013;35:32-40
121. Gupta SC,Reuter S,Phromnoi K,Park B,Hema PS,Nair M,Aggarwal BB.Nimbolide sensitizes human colon cancer cells to TRAIL through reactive oxygen species- and ERK-dependent up-regulation of death receptors, p53, and Bax.J Biol Chem. 2011;286:1134-46
122. Gupta SC,Francis SK,Nair MS,Mo YY,Aggarwal BB.Azadirone, a limonoid tetranortriterpene, induces death receptors and sensitizes human cancer cells to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) through a p53 protein-independent mechanism: evidence for the role of the ROS-ERK-CHOP-death receptor pathway.J Biol Chem. 2013;288:32343-56
123. Kannappan R,Ravindran J,Prasad S,Sung B,Yadav VR,Reuter S,Madan MC,Aggarwal BB.Gamma-tocotrienol promotes TRAIL-induced apoptosis through reactive oxygen species/extracellular signal-regulated kinase/p53-mediated upregulation of death receptors.Mol Cancer Therapeut. 2010;9:2196-207
124. Yodkeeree S,Sung B,Limtrakul P,Aggarwal BB.Zerumbone enhances TRAIL-induced apoptosis through the induction of death receptors in human colon cancer cells: evidence for an essential role of reactive oxygen species.Cancer Res. 2009;69:6581-9
125. Lee HH,Jeong JW,Lee JH,Kim GY,Cheong J,Jeong YK,Yoo YH,Choi YH.Cordycepin increases sensitivity of Hep3B human hepatocellular carcinoma cells to TRAIL-mediated apoptosis by inactivating the JNK signaling pathway.Oncol Reports. 2013;30:1257-64
126. Prasad S,Yadav VR,Kannappan R,Aggarwal BB.Ursolic acid, a pentacyclin triterpene, potentiates TRAIL-induced apoptosis through p53-independent up-regulation of death receptors: evidence for the role of reactive oxygen species and JNK.J Biol Chem. 2011;286:5546-57
127. Park MH,Jo M,Won D,Song HS,Song MJ,Hong JT.Snake venom toxin from Vipera lebetina turanica sensitizes cancer cells to TRAIL through ROS- and JNK-mediated upregulation of death receptors and downregulation of survival proteins.Apoptosis: Int J Program Cell Death. 2012;17:1316-26
128. Sung B,Prasad S,Ravindran J,Yadav VR,Aggarwal BB.Capsazepine, a TRPV1 antagonist, sensitizes colorectal cancer cells to apoptosis by TRAIL through ROS-JNK-CHOP-mediated upregulation of death receptors.Free Rad Biol Med. 2012;53:1977-87
129. Hsu YL,Hou MF,Tsai EM,Kuo PL.Tricetin, a dietary flavonoid, induces apoptosis through the reactive oxygen species/c-Jun NH2-terminal kinase pathway in human liver cancer cells.J Agricul Food Chem. 2010;58:12547-56
130. Lamy V,Bousserouel S,Gosse F,Minker C,Lobstein A,Raul F.Lupulone triggers p38 MAPK-controlled activation of p53 and of the TRAIL receptor apoptotic pathway in human colon cancer-derived metastatic cells.Oncol Reports. 2011;26:109-14
131. Lepage C,Leger DY,Bertrand J,Martin F,Beneytout JL,Liagre B.Diosgenin induces death receptor-5 through activation of p38 pathway and promotes TRAIL-induced apoptosis in colon cancer cells.Cancer Lett. 2011;301:193-202
132. Kim EY,Ryu JH,Kim AK.CAPE promotes TRAIL-induced apoptosis through the upregulation of TRAIL receptors via activation of p38 and suppression of JNK in SK-Hep1 hepatocellular carcinoma cells.Int J Oncol. 2013;43:1291-300
133. Subramaniam A,Loo SY,Rajendran P,Manu KA,Perumal E,Li F,Shanmugam MK,Siveen KS,Park JI,Ahn KS,Hui KM,Kumar AP,Sethi G.An anthraquinone derivative, emodin sensitizes hepatocellular carcinoma cells to TRAIL induced apoptosis through the induction of death receptors and downregulation of cell survival proteins.Apoptosis: Int J Program Cell Death. 2013;18:1175-87
134. Xiaowen H,Yi S.Triptolide sensitizes TRAIL-induced apoptosis in prostate cancer cells via p53-mediated DR5 up-regulation.Mol Biol Reports. 2012;39:8763-70
135. Tomasetti M,Andera L,Alleva R,Borghi B,Neuzil J,Procopio A.Alpha-tocopheryl succinate induces DR4 and DR5 expression by a p53-dependent route: implication for sensitisation of resistant cancer cells to TRAIL apoptosis.FEBS Lett. 2006;580:1925-31
136. Zhou J,Lu GD,Ong CS,Ong CN,Shen HM.Andrographolide sensitizes cancer cells to TRAIL-induced apoptosis via p53-mediated death receptor 4 up-regulation.Mol Cancer Therapeut. 2008;7:2170-80
137. Chen CY,Tai CJ,Cheng JT,Zheng JJ,Chen YZ,Liu TZ,Yiin S,Chern CL.6-Dehydrogingerdione sensitizes human hepatoblastoma Hep G2 cells to TRAIL-induced apoptosis via reactive oxygen species-mediated increase of DR5.J Agric Food Chem. 2010;58:5604-11
138. Lin FL,Hsu JL,Chou CH,Wu WJ,Chang CI,Liu HJ.Activation of p38 MAPK by damnacanthal mediates apoptosis in SKHep 1 cells through the DR5/TRAIL and TNFR1/TNF-alpha and p53 pathways.Eur J Pharmacol. 2011;650:120-9
139. Soria JC,Smit E,Khayat D,Besse B,Yang X,Hsu CP,Reese D,Wiezorek J,Blackhall F.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;28:1527-33
140. Herbst RS,Kurzrock R,Hong DS,Valdivieso M,Hsu CP,Goyal L,Gloria J,Yuying CH,Susan W,John SH,Greg F,Patricia ML.A first-in-human study of conatumumab in adult patients with advanced solid tumors.Clin Cancer Res: Off J Am Assoc Cancer Res. 2010;16:5883-91
141. Paz-Ares L,Torres JMS,Diaz-Padilla I,Links M,Reguart N,Boyer M,Wiezorek J,Sabin T,Pan Y,Meerbeeck JV.Safety and efficacy of AMG 655 in combination with paclitaxel and carboplatin (PC) in patients with advanced non-small cell lung cancer (NSCLC).J Clin Oncol. 2009;27 (15): e19048