Fn14•Trail Effectively Inhibits Hepatocellular Carcinoma Growth

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Aronin, Alexandra ^a   Amsili, Shira ^b   Prigozhina, Tatyana B ^a   Tzdaka, Kobi ^a   Rachmilewitz, Jacob ^a   Shani, Noam ^b   Tykocinski, Mark L ^c   Dranitzki Elhalel, Michal ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b KAHR Medical Ltd   (Israel)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FN14 PROTEIN; FN14 TRAIL PROTEIN; HYBRID PROTEIN; REGULATOR PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; TWEAK PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG POTENCY; DRUG TOLERABILITY; HUMAN; HUMAN CELL; LIVER CELL; LIVER CELL CARCINOMA; MALE; MOUSE; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; TUMOR XENOGRAFT;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIVER NEOPLASMS; MALE; MICE; MOLECULAR SEQUENCE DATA; RECEPTORS, TUMOR NECROSIS FACTOR; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SOLUBILITY; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR NECROSIS FACTORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84885399010     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077050     Document Type: Article

References (45)

1. Nordenstedt H, White DL, El-Serag HB, (2010) The changing pattern of epidemiology in hepatocellular carcinoma. Dig Liver Dis 42 (Suppl 3):: S206-S214. doi:10.1016/S1590-8658(10)60507-5. PubMed: 20547305.
2. Thomas MB, Jaffe D, Choti MM, Belghiti J, Curley S, et al. (2010) Hepatocellular carcinoma: consensus recommendations of the National Cancer Institute Clinical Trials Planning Meeting. J Clin Oncol 28: 3994-4005. doi:10.1200/JCO.2010.28.7805. PubMed: 20679622.
3. Gaur U, Aggarwal BB, (2003) Regulation of proliferation, survival and apoptosis by members of the TNF superfamily. Biochem Pharmacol 66: 1403-1408. doi:10.1016/S0006-2952(03)00490-8. PubMed: 14555214.
4. Chicheportiche Y, Bourdon PR, Xu H, Hsu YM, Scott H, et al. (1997) TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J Biol Chem 272: 32401-32410. doi:10.1074/jbc.272.51.32401. PubMed: 9405449.
5. Wiley SR, Winkles JA, (2003) TWEAK, a member of the TNF superfamily, is a multifunctional cytokine that binds the TweakR/Fn14 receptor. Cytokine Growth Factor Rev 14: 241-249. doi:10.1016/S1359-6101(03)00019-4. PubMed: 12787562.
6. Feng SL, Guo Y, Factor VM, Thorgeirsson SS, Bell DW, et al. (2000) The Fn14 immediate-early response gene is induced during liver regeneration and highly expressed in both human and murine hepatocellular carcinomas. Am J Pathol 156: 1253-1261. doi:10.1016/S0002-9440(10)64996-6. PubMed: 10751351.
7. Kawakita T, Shiraki K, Yamanaka Y, Yamaguchi Y, Saitou Y, et al. (2004) Functional expression of TWEAK in human hepatocellular carcinoma: possible implication in cell proliferation and tumor angiogenesis. Biochem Biophys Res Commun 318: 726-733. doi:10.1016/j.bbrc.2004.04.084. PubMed: 15144899.
8. Tran NL, McDonough WS, Donohue PJ, Winkles JA, Berens TJ, et al. (2003) The human Fn14 receptor gene is up-regulated in migrating glioma cells in vitro and overexpressed in advanced glial tumors. Am J Pathol 162: 1313-1321. doi:10.1016/S0002-9440(10)63927-2. PubMed: 12651623.
9. Tran NL, McDonough WS, Savitch BA, Fortin SP, Winkles JA, et al. (2006) Increased fibroblast growth factor-inducible 14 expression levels promote glioma cell invasion via Rac1 and nuclear factor-kappaB and correlate with poor patient outcome. Cancer Res 66: 9535-9542. doi:10.1158/0008-5472.CAN-06-0418. PubMed: 17018610.
10. Holoch PA, Griffith TS, (2009) TNF-related apoptosis-inducing ligand (TRAIL): a new path to anti-cancer therapies. Eur J Pharmacol 625: 63-72. doi:10.1016/j.ejphar.2009.06.066. PubMed: 19836385.
11. Johnstone RW, Frew AJ, Smyth MJ, (2008) The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer 8: 782-798. doi:10.1038/nrc2465. PubMed: 18813321.
12. Fabregat I, (2009) Dysregulation of apoptosis in hepatocellular carcinoma cells. World J Gastroenterol 15: 513-520. doi:10.3748/wjg.15.513. PubMed: 19195051.
13. Schattenberg JM, Schuchmann M, Galle PR, (2011) Cell death and hepatocarcinogenesis: Dysregulation of apoptosis signaling pathways. J Gastroenterol Hepatol 26 (Suppl 1):: 213-219. doi:10.1111/j.1440-1746.2010.06582.x. PubMed: 21199533.
14. Kriegl L, Jung A, Engel J, Jackstadt R, Gerbes AL, et al. (2010) Expression, cellular distribution, and prognostic relevance of TRAIL receptors in hepatocellular carcinoma. Clin Cancer Res 16: 5529-5538. doi:10.1158/1078-0432.CCR-09-3403. PubMed: 20889918.
15. Fabregat I, Roncero C, Fernández M, (2007) Survival and apoptosis: a dysregulated balance in liver cancer. Liver Int 27: 155-162. doi:10.1111/j.1478-3231.2006.01409.x. PubMed: 17311609.
16. Razmara M, Hilliard B, Ziarani AK, Murali R, Yellayi S, et al. (2009) Fn14-TRAIL, a chimeric intercellular signal exchanger, attenuates experimental autoimmune encephalomyelitis. Am J Pathol 174: 460-474.
17. Malhi H, Irani AN, Gagandeep S, Gupta S, (2002) Isolation of human progenitor liver epithelial cells with extensive replication capacity and differentiation into mature hepatocytes. J Cell Sci 115: 2679-2688. PubMed: 12077359.
18. Kobayashi N, Noguchi H, Fujiwara T, Westerman KA, Leboulch P, et al. (2000) Establishment of a highly differentiated immortalized adult human hepatocyte cell line by retroviral gene transfer. Transplant Proc 32: 2368-2369. doi:10.1016/S0041-1345(00)01702-4. PubMed: 11120203.
19. Kobayashi N, Fujiwara T, Westerman KA, Inoue Y, Sakaguchi M, et al. (2000) Prevention of acute liver failure in rats with reversibly immortalized human hepatocytes. Science 287: 1258-1262. doi:10.1126/science.287.5456.1258. PubMed: 10678831.
20. Orbach A, Rachmilewitz J, Shani N, Isenberg Y, Parnas M, et al. (2010) CD40.FasL and CTLA-4.FasL fusion proteins induce apoptosis in malignant cell lines by dual signaling. Am J Pathol 177: 3159-3168. doi:10.2353/ajpath.2010.100301. PubMed: 21088216.
21. Schneider P, Thome M, Burns K, Bodmer JL, Hofmann K, et al. (1997) TRAIL receptors 1 (DR4) and 2 (DR5) signal FADD-dependent apoptosis and activate NF-kappaB. Immunity 7: 831-836. doi:10.1016/S1074-7613(00)80401-X. PubMed: 9430228.
22. Grunert M, Gottschalk K, Kapahnke J, Gundisch S, Kieser A, et al. (2012) The adaptor protein FADD and the initiator caspase-8 mediate activation of NF-kappaB by TRAIL. Cell Death. Drosophila Inf Serv 3: e414.
23. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, et al. (1999) Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 104: 155-162. doi:10.1172/JCI6926. PubMed: 10411544.
24. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, et al. (1999) Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 5: 157-163. doi:10.1038/5517. PubMed: 9930862.
25. Ashkenazi A, Herbst RS, (2008) To kill a tumor cell: the potential of proapoptotic receptor agonists. J Clin Invest 118: 1979-1990. doi:10.1172/JCI34359. PubMed: 18523647.
26. Rosevear HM, Lightfoot AJ, Griffith TS, (2010) Conatumumab, a fully human mAb against death receptor 5 for the treatment of cancer. Curr Opin Investig Drugs 11: 688-698. PubMed: 20496264.
27. Sung ES, Park KJ, Lee SH, Jang YS, Park SK, et al. (2009) A novel agonistic antibody to human death receptor 4 induces apoptotic cell death in various tumor cells without cytotoxicity in hepatocytes. Mol Cancer Ther 8: 2276-2285. doi:10.1158/1535-7163.MCT-09-0235. PubMed: 19638452.
28. Wahl K, Siegemund M, Lehner F, Vondran F, Nüssler A, et al. (2012) Increased apoptosis induction in hepatocellular carcinoma by a novel tumor-targeted TRAIL fusion protein combined with bortezomib. Hepatology, 57: 625-36. PubMed: 22991197.
29. Siegemund M, Pollak N, Seifert O, Wahl K, Hanak K, et al. (2012) Superior antitumoral activity of dimerized targeted single-chain TRAIL fusion proteins under retention of tumor selectivity. Cell Death. Drosophila Inf Serv 3: e295.
30. Chen XP, He SQ, Wang HP, Zhao YZ, Zhang WG, (2003) Expression of TNF-related apoptosis-inducing Ligand receptors and antitumor tumor effects of TNF-related apoptosis-inducing Ligand in human hepatocellular carcinoma. World J Gastroenterol 9: 2433-2440. PubMed: 14606071.
31. Herr I, Schemmer P, Büchler MW, (2007) On the TRAIL to therapeutic intervention in liver disease. Hepatology 46: 266-274. doi:10.1016/S0168-8278(07)62304-6. PubMed: 17596886.
32. Wagner KW, Punnoose EA, Januario T, Lawrence DA, Pitti RM, et al. (2007) Death-receptor O-glycosylation controls tumor-cell sensitivity to the proapoptotic ligand Apo2L/TRAIL. Nat Med 13: 1070-1077. doi:10.1038/nm1627. PubMed: 17767167.
33. Yang A, Wilson NS, Ashkenazi A, (2010) Proapoptotic DR4 and DR5 signaling in cancer cells: toward clinical translation. Curr Opin Cell Biol 22: 837-844. doi:10.1016/j.ceb.2010.08.001. PubMed: 20813513.
34. Tran NL, McDonough WS, Savitch BA, Sawyer TF, Winkles JA, et al. (2005) The tumor necrosis factor-like weak inducer of apoptosis (TWEAK)-fibroblast growth factor-inducible 14 (Fn14) signaling system regulates glioma cell survival via NFkappaB pathway activation and BCL-XL/BCL-W expression. J Biol Chem 280: 3483-3492. PubMed: 15611130.
35. Ikner A, Ashkenazi A, (2011) TWEAK induces apoptosis through a death-signaling complex comprising receptor-interacting protein 1 (RIP1), Fas-associated death domain (FADD), and caspase-8. J Biol Chem 286: 21546-21554. doi:10.1074/jbc.M110.203745. PubMed: 21525013.
36. Brown SA, Cheng E, Williams MS, Winkles JA, (2013) TWEAK-Independent Fn14 Self-Association and NF-kappaB Activation Is Mediated by the C-Terminal Region of the Fn14 Cytoplasmic Domain. PLOS ONE 8: e65248. doi:10.1371/journal.pone.0065248. PubMed: 23750247.
37. Winkles JA, Tran NL, Berens ME, (2006) TWEAK and Fn14: new molecular targets for cancer therapy? Cancer Lett 235: 11-17. doi:10.1016/j.canlet.2005.03.048. PubMed: 15885893.
38. Fortin SP, Ennis MJ, Savitch BA, Carpentieri D, McDonough WS, et al. (2009) Tumor necrosis factor-like weak inducer of apoptosis stimulation of glioma cell survival is dependent on Akt2 function. Mol Cancer Res 7: 1871-1881. doi:10.1158/1541-7786.MCR-09-0194. PubMed: 19861406.
39. Giese A, Bjerkvig R, Berens ME, Westphal M, (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 21: 1624-1636. doi:10.1200/JCO.2003.05.063. PubMed: 12697889.
40. Ho DH, Vu H, Brown SA, Donohue PJ, Hanscom HN, et al. (2004) Soluble tumor necrosis factor-like weak inducer of apoptosis overexpression in HEK293 cells promotes tumor growth and angiogenesis in athymic nude mice. Cancer Res 64: 8968-8972. doi:10.1158/0008-5472.CAN-04-1879. PubMed: 15604260.
41. Nakayama M, Ishidoh K, Kojima Y, Harada N, Kominami E, et al. (2003) Fibroblast growth factor-inducible 14 mediates multiple pathways of TWEAK-induced cell death. J Immunol 170: 341-348. PubMed: 12496418.
42. Culp PA, Choi D, Zhang Y, Yin J, Seto P, et al. (2010) Antibodies to TWEAK receptor inhibit human tumor growth through dual mechanisms. Clin Cancer Res 16: 497-508. doi:10.1158/1078-0432.CCR-09-1929. PubMed: 20068083.
43. Eliopoulos AG, Davies C, Knox PG, Gallagher NJ, Afford SC, et al. (2000) CD40 induces apoptosis in carcinoma cells through activation of cytotoxic ligands of the tumor necrosis factor superfamily. Mol Cell Biol 20: 5503-5515. doi:10.1128/MCB.20.15.5503-5515.2000. PubMed: 10891490.
44. Grell M, Zimmermann G, Gottfried E, Chen CM, Grunwald U, et al. (1999) Induction of cell death by tumour necrosis factor (TNF). Receptors 2, CD40 and CD30: a role for TNF-R1 activation by endogenous membrane-anchored TNF. EMBO J 18: 3034-3043.
45. Dranitzki-Elhalel M, Huang JH, Sasson M, Rachmilewitz J, Parnas M, et al. (2007) CD40.FasL inhibits human T cells: evidence for an auto-inhibitory loop-back mechanism. Int Immunol 19: 355-363. doi:10.1093/intimm/dxm001. PubMed: 17314083.