Hyperthermia-enhanced TRAIL- and mapatumumab-induced apoptotic death is mediated through mitochondria in human colon cancer cells

Journal of Cellular Biochemistry

Volumn 113, Issue 5, 2012, Pages 1547-1558

  Song, Xinxin ^a,b   Kim, Han Cheon ^a,b   Kim, Seog Young ^a,b   Basse, Per ^a,b   Park, Bae Hang ^a,b   Lee, Byeong Chel ^a,b   Lee, Yong J ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

APOPTOSIS; Bax; CYTOCHROME c; HYPERTHERMIA; JNK; MAPATUMUMAB; PARP; ROS; TRAIL

Indexed keywords

CASPASE; CYTOCHROME C; DEATH RECEPTOR 4; DEATH RECEPTOR 5; MAPATUMUMAB; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; ARTICLE; COLON CANCER; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HYPERTHERMIA; LIVER METASTASIS; MITOCHONDRIAL MEMBRANE POTENTIAL; OLIGOMERIZATION; PRIORITY JOURNAL;

ANTIBODIES, MONOCLONAL; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; COMBINED MODALITY THERAPY; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYPERTHERMIA, INDUCED; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIVER NEOPLASMS; MITOCHONDRIA; PROTO-ONCOGENE PROTEINS; REACTIVE OXYGEN SPECIES; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84858079420     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24023     Document Type: Article

References (48)

1. Alcala MA, Jr., Park K, Yoo J, Lee DH, Park BH, Lee BC, Bartlett DL, Lee YJ,. 2010. Effect of hyperthermia in combination with TRAIL on the JNK-Bim signal transduction pathway and growth of xenograft tumors. J Cell Biochem 110: 1073-1081.
2. Alexander HR, Jr., Libutti SK, Pingpank JF, Bartlett DL, Helsabeck C, Beresneva T,. 2005. Isolated hepatic perfusion for the treatment of patients with colorectal cancer liver metastases after irinotecan-based therapy. Ann Surg Oncol 12: 138-144. (Pubitemid 40486622)
3. Ashkenazi A, Dixit VM,. 1999. Apoptosis control by death and decoy receptors. Curr Opin Cell Biol 11: 255-260. (Pubitemid 29164042)
4. Basu A, Castle VP, Bouziane M, Bhalla K, Haldar S,. 2006. Crosstalk between extrinsic and intrinsic cell death pathways in pancreatic cancer: Synergistic action of estrogen metabolite and ligands of death receptor family. Cancer Res 66: 4309-4318.
5. Bellail AC, Qi L, Mulligan P, Chhabra V, Hao C,. 2009. TRAIL agonists on clinical trials for cancer therapy: The promises and the challenges. Rev Recent Clin Trials 4: 34-41.
6. Bellavance EC, Alexander HR, Jr., 2009. TNF-based isolated hepatic perfusion. Front Biosci 14: 1771-1784.
7. Benhar M, Dalyot I, Engelberg D, Levitzki A,. 2001. Enhanced ROS production in oncogenically transformed cells potentiates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase activation and sensitization to genotoxic stress. Mol Cell Biol 21: 6913-6926. (Pubitemid 32911252)
8. Cappello F, Zummo G,. 2005. HSP60 expression during carcinogenesis: A molecular "proteus" of carcinogenesis? Cell Stress Chaperones 10: 263-264. (Pubitemid 41813373)
9. Cazanave SC, Mott JL, Elmi NA, Bronk SF, Werneburg NW, Akazawa Y, Kahraman A, Garrison SP, Zambetti GP, Charlton MR, Gores GJ,. 2009. JNK1-dependent PUMA expression contributes to hepatocyte lipoapoptosis. J Biol Chem 284: 26591-26602.
10. Ciocca DR, Calderwood SK,. 2005. Heat shock proteins in cancer: Diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones 10: 86-103. (Pubitemid 40942470)
11. Dewson G, Snowden RT, Almond JB, Dyer MJ, Cohen GM,. 2003. Conformational change and mitochondrial translocation of Bax accompany proteasome inhibitor-induced apoptosis of chronic lymphocytic leukemic cells. Oncogene 22: 2643-2654. (Pubitemid 36605612)
12. Georgakis GV, Li Y, Humphreys R, Andreeff M, O'Brien S, Younes M, Carbone A, Albert V, Younes A,. 2005. Activity of selective fully human agonistic antibodies to the TRAIL death receptors TRAIL-R1 and TRAIL-R2 in primary and cultured lymphoma cells: Induction of apoptosis and enhancement of doxorubicin- and bortezomib-induced cell death. Br J Haematol 130: 501-510. (Pubitemid 43899752)
13. Gonzalvez F, Ashkenazi A,. 2010. New insights into apoptosis signaling by Apo2L/TRAIL. Oncogene 29: 4752-4765.
14. Griffith TS, Stokes B, Kucaba TA, Earel JK, Jr., VanOosten RL, Brincks EL, Norian LA,. 2009. TRAIL gene therapy: From preclinical development to clinical application. Curr Gene Ther 9: 9-19.
15. Hafstrom LR, Holmberg SB, Naredi PL, Lindner PG, Bengtsson A, Tidebrant G, Schersten TS,. 1994. Isolated hyperthermic liver perfusion with chemotherapy for liver malignancy. Surg Oncol 3: 103-108. (Pubitemid 24237137)
16. Hail N, Jr., Lotan R,. 2009. Cancer chemoprevention and mitochondria: Targeting apoptosis in transformed cells via the disruption of mitochondrial bioenergetics/redox state. Mol Nutr Food Res 53: 49-67.
17. Hotte SJ, Hirte HW, Chen EX, Siu LL, Le LH, Corey A, Iacobucci A, MacLean M, Lo L, Fox NL, Oza AM,. 2008. A phase 1 study of mapatumumab (fully human monoclonal antibody to TRAIL-R1) in patients with advanced solid malignancies. Clin Cancer Res 14: 3450-3455.
18. Ichikawa K, Liu W, Zhao L, Wang Z, Liu D, Ohtsuka T, Zhang H, Mountz JD, Koopman WJ, Kimberly RP, Zhou T,. 2001. Tumoricidal activity of a novel anti-human DR5 monoclonal antibody without hepatocyte cytotoxicity. Nat Med 7: 954-960. (Pubitemid 32756434)
19. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D,. 2011. Global cancer statistics. CA Cancer J Clin 61: 69-90.
20. Kahraman A, Barreyro FJ, Bronk SF, Werneburg NW, Mott JL, Akazawa Y, Masuoka HC, Howe CL, Gores GJ,. 2008. TRAIL mediates liver injury by the innate immune system in the bile duct-ligated mouse. Hepatology 47: 1317-1330. (Pubitemid 351547918)
21. Klaunig JE, Xu Y, Isenberg JS, Bachowski S, Kolaja KL, Jiang J, Stevenson DE, Walborg EF, Jr., 1998. The role of oxidative stress in chemical carcinogenesis. Environ Health Perspect 106 (Suppl. 1): 289-295. (Pubitemid 28196053)
22. Koschny R, Ganten TM, Sykora J, Haas TL, Sprick MR, Kolb A, Stremmel W, Walczak H,. 2007. TRAIL/bortezomib cotreatment is potentially hepatotoxic but induces cancer-specific apoptosis within a therapeutic window. Hepatology 45: 649-658. (Pubitemid 46450616)
23. Lee YJ, Froelich CJ, Fujita N, Tsuruo T, Kim JH,. 2004. Reconstitution of caspase-3 confers low glucose-enhanced tumor necrosis factor-related apoptosis-inducing ligand cytotoxicity and Akt cleavage. Clin Cancer Res 10: 1894-1900. (Pubitemid 38375545)
24. Lee DH, Rhee JG, Lee YJ,. 2009. Reactive oxygen species up-regulate p53 and Puma; a possible mechanism for apoptosis during combined treatment with TRAIL and wogonin. Br J Pharmacol 157: 1189-1202.
25. Lee DH, Szczepanski M, Lee YJ,. 2008. Role of Bax in quercetin-induced apoptosis in human prostate cancer cells. Biochem Pharmacol 75: 2345-2355.
26. Lee BC, Park BH, Kim SY, Lee YJ,. 2011. Role of Bim in diallyl trisulfide-induced cytotoxicity in human cancer cells. J Cell Biochem 112: 118-127.
27. Lomonosova E, Chinnadurai G,. 2008. BH3-only proteins in apoptosis and beyond: An overview. Oncogene 27 (Suppl. 1): S2-S19.
28. Moretto P, Hotte SJ,. 2009. Targeting apoptosis: Preclinical and early clinical experience with mapatumumab, an agonist monoclonal antibody targeting TRAIL-R1. Expert Opin Investig Drugs 18: 311-325.
29. Park BH, Lee SB, Stolz DB, Lee YJ, Lee BC,. 2011. Synergistic interactions between heregulin and peroxisome proliferator-activated receptor-gamma (PPARgamma) agonist in breast cancer cells. J Biol Chem 286: 20087-20099.
30. 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. (Pubitemid 26175834)
31. Pukac L, Kanakaraj P, Humphreys R, Alderson R, Bloom M, Sung C, Riccobene T, Johnson R, Fiscella M, Mahoney A, Carrell J, Boyd E, Yao XT, Zhang L, Zhong L, von Kerczek A, Shepard L, Vaughan T, Edwards B, Dobson C, Salcedo T, Albert V,. 2005. HGS-ETR1, a fully human TRAIL-receptor 1 monoclonal antibody, induces cell death in multiple tumour types in vitro and in vivo. Br J Cancer 92: 1430-1441. (Pubitemid 40705010)
32. Schafer T, Sperling J, Kollmar O, Richter S, Schilling MK, Menger MD, Lindemann W,. 2010. Early effect of hepatic artery TNF-alpha infusion on systemic hemodynamics and inflammation: A dose-response study in pigs. Int J Colorectal Dis 25: 523-532.
33. Song JJ, Lee YJ,. 2003. Role of the ASK1-SEK1-JNK1-HIPK1 signal in Daxx trafficking and ASK1 oligomerization. J Biol Chem 278: 47245-47252. (Pubitemid 37452312)
34. Song JJ, Lee YJ,. 2004. Daxx deletion mutant (amino acids 501-625)-induced apoptosis occurs through the JNK/p38-Bax-dependent mitochondrial pathway. J Cell Biochem 92: 1257-1270. (Pubitemid 44264234)
35. Song JJ, Lee YJ,. 2005. Dissociation of Akt1 from its negative regulator JIP1 is mediated through the ASK1-MEK-JNK signal transduction pathway during metabolic oxidative stress: A negative feedback loop. J Cell Biol 170: 61-72. (Pubitemid 40994096)
36. Song JJ, Rhee JG, Suntharalingam M, Walsh SA, Spitz DR, Lee YJ,. 2002. Role of glutaredoxin in metabolic oxidative stress. Glutaredoxin as a sensor of oxidative stress mediated by H2O2. J Biol Chem 277: 46566-46575. (Pubitemid 35417655)
37. Tembe V, Henderson BR,. 2007. BARD1 translocation to mitochondria correlates with Bax oligomerization, loss of mitochondrial membrane potential, and apoptosis. J Biol Chem 282: 20513-20522. (Pubitemid 47100042)
38. Trarbach T, Moehler M, Heinemann V, Kohne CH, Przyborek M, Schulz C, Sneller V, Gallant G, Kanzler S,. 2010. 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 102: 506-512.
39. Varghese S, Xu H, Bartlett D, Hughes M, Pingpank JF, Beresnev T, Alexander HR, Jr., 2010. Isolated hepatic perfusion with high-dose melphalan results in immediate alterations in tumor gene expression in patients with metastatic ocular melanoma. Ann Surg Oncol 17: 1870-1877.
40. 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. (Pubitemid 29068521)
41. Xiao D, Choi S, Johnson DE, Vogel VG, Johnson CS, Trump DL, Lee YJ, Singh SV,. 2004. Diallyl trisulfide-induced apoptosis in human prostate cancer cells involves c-Jun N-terminal kinase and extracellular-signal regulated kinase-mediated phosphorylation of Bcl-2. Oncogene 23: 5594-5606. (Pubitemid 39093037)
42. Yada A, Yazawa M, Ishida S, Yoshida H, Ichikawa K, Kurakata S, Fujiwara K,. 2008. A novel humanized anti-human death receptor 5 antibody CS-1008 induces apoptosis in tumor cells without toxicity in hepatocytes. Ann Oncol 19: 1060-1067. (Pubitemid 351796330)
43. Yethon JA, Epand RF, Leber B, Epand RM, Andrews DW,. 2003. Interaction with a membrane surface triggers a reversible conformational change in Bax normally associated with induction of apoptosis. J Biol Chem 278: 48935-48941.
44. Yoo J, Lee YJ,. 2007. Effect of hyperthermia on TRAIL-induced apoptotic death in human colon cancer cells: Development of a novel strategy for regional therapy. J Cell Biochem 101: 619-630. (Pubitemid 46698847)
45. Yoo J, Lee YJ,. 2008. Effect of hyperthermia and chemotherapeutic agents on TRAIL-induced cell death in human colon cancer cells. J Cell Biochem 103: 98-109.
46. Younes A, Vose JM, Zelenetz AD, Smith MR, Burris HA, Ansell SM, Klein J, Halpern W, Miceli R, Kumm E, Fox NL, Czuczman MS,. 2010. A Phase 1b/2 trial of mapatumumab in patients with relapsed/refractory non-Hodgkin's lymphoma. Br J Cancer 103: 1783-1787.
47. Yu J, Zhang L,. 2008. PUMA, a potent killer with or without p53. Oncogene 27 (Suppl. 1): S71-S83.
48. Zeh HJ III, Brown CK, Holtzman MP, Egorin MJ, Holleran JL, Potter DM, Bartlett DL,. 2009. A phase I study of hyperthermic isolated hepatic perfusion with oxaliplatin in the treatment of unresectable liver metastases from colorectal cancer. Ann Surg Oncol 16: 385-394.