Blockade of ataxia telangiectasia mutated sensitizes hepatoma cell lines to sorafenib by interfering with Akt signaling

Cancer Letters

Volumn 319, Issue 1, 2012, Pages 98-108

  Fujimaki, Shun ^a   Matsuda, Yasunobu ^a   Wakai, Toshifumi ^b   Sanpei, Ayumi ^b   Kubota, Masayuki ^b   Takamura, Masaaki ^b   Yamagiwa, Satoshi ^b   Yano, Masahiko ^b   Ohkoshi, Shogo ^b   Aoyagi, Yutaka ^b  

^a NIIGATA UNIVERSITY   (Japan)

^b NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

Author keywords

Akt; Ataxia telangiectasia mutated (ATM); Caffeine; Hepatoma; Sorafenib

Indexed keywords

2 MORPHOLINO 6 (1 THIANTHRENYL) 4 PYRANONE; ATM PROTEIN; CAFFEINE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; RNA; SORAFENIB;

ANTINEOPLASTIC ACTIVITY; ARTICLE; ATM GENE; CANCER CELL CULTURE; CELL MIGRATION; CELL MOTILITY; CELL STRAIN HEPG2; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG POTENTIATION; DRUG RESISTANCE; GENE; GENE SILENCING; HEPATOMA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; BENZENESULFONATES; CAFFEINE; CARCINOMA, HEPATOCELLULAR; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DNA-BINDING PROTEINS; DRUG SCREENING ASSAYS, ANTITUMOR; DRUG SYNERGISM; HUMANS; LIVER NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PYRIDINES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

ATAXIA TELANGIECTASIA;

EID: 84858082260     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.12.043     Document Type: Article

References (42)

1. El Serag H.B., Rudolph K.L. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007, 132:2557-2576.
2. Llovet J.M., Burroughs A., Bruix J. Hepatocellular carcinoma. Lancet 2003, 362:1907-1917.
3. Yang J.D., Roberts L.R. Hepatocellular carcinoma: a global view. Nature Reviews Gastroenterology Hepatology 2010, 7:448-458.
4. Arii S., Yamaoka Y., Futagawa S., Inoue K., Kobayashi K., Kojiro M., Makuuchi M., Nakamura Y., Okita K., Yamada R R. Results of surgical and nonsurgical treatment for small-sized hepatocellular carcinomas: a retrospective and nationwide survey in Japan. The Liver Cancer Study Group of Japan. Hepatology 2000, 32:1224-1229.
5. Kuwahara Y., Li L., Baba T., Nakagawa H., Shimura T., Yamamoto Y., Ohkubo Y., Fukumoto M. Clinically relevant radioresistant cells efficiently repair DNA double-strand breaks induced by X-rays. Cancer Science 2009, 100:747-752.
6. Wilhelm S.M., Carter C., Tang L., Wilkie D., McNabola A., Rong H., Chen C., Zhang X., Vincent P., McHugh M., Cao Y., Shujath J., Gawlak S., Eveleigh D., Rowley B., Liu L., Adnane L., Lynch M., Auclair D., Taylor I., Gedrich R., Voznesensky A., Riedl B., Post L.E., Bollag G., Trail P.A. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Research 2004, 64:7099-7109.
7. Wilhelm S.M., Adnane L., Newell P., Villanueva A., Llovet J.M., Lynch M. Preclinical overview of sorafenib, a multikinase inhibitor that targets both Raf and VEGF and PDGF receptor tyrosine kinase signaling. Molecular Cancer Therapeutics 2008, 7:3129-3140.
8. Llovet J.M., Ricci S., Mazzaferro V., Hilgard P., Gane E., Blanc J.F., de Oliveira A.C., Santoro A., Raoul J.L., Forner A., Schwartz M., Porta C., Zeuzem S., Bolondi L., Greten T.F., Galle P.R., Seitz J.F., Borbath I., Häussinger D., Giannaris T., Shan M., Moscovici M., Voliotis D., Bruix J. SHARP Investigators Study Group, Sorafenib in advanced hepatocellular carcinoma. New England Journal of Medicine 2008, 359:378-390.
9. Cheng A.L., Kang Y.K., Chen Z., Tsao C.J., Qin S., Kim J.S., Luo R., Feng J., Ye S., Yang T.S., Xu J., Sun Y., Liang H., Liu J., Wang J., Tak W.Y., Pan H., Burock K., Zou J., Voliotis D., Guan Z. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncology 2009, 10:25-34.
10. Whittaker S., Marais R., Zhu A.X. The role of signaling pathways in the development and treatment of hepatocellular carcinoma. Oncogene 2010, 29:4989-5005.
11. Kaseb A.O., Hanbali A., Cotant M., Hassan M.M., Wollner I., Philip P.A. Vascular endothelial growth factor in the management of hepatocellular carcinoma: a review of literature. Cancer 2009, 115:4895-4906.
12. Autier J., Escudier B., Wechsler J., Spatz A., Robert C. Prospective study of the cutaneous adverse effects of sorafenib, a novel multikinase inhibitor. Archives of Dermatology 2008, 144:886-892.
13. Azad N.S., Aragon-Ching J.B., Dahut W.L., Gutierrez M., Figg W.D., Jain L., Steinberg S.M., Turner M.L., Kohn E.C., Kong H.H. Hand-foot skin reaction increases with cumulative sorafenib dose and with combination anti-vascular endothelial growth factor therapy. Clinical Cancer Research 2009, 15:1411-1416.
14. Wang Z., Wang M., Carr B.I. Involvement of receptor tyrosine phosphatase DEP-1 mediated PI3K-cofilin signaling pathway in sorafenib-induced cytoskeletal rearrangement in hepatoma cells. Journal of Cell Physiology 2010, 224:559-565.
15. Rose A., Grandoch M., vom Dorp F., Rübben H., Rosenkranz A., Fischer J.W., A Weber A. Stimulatory effects of the multi-kinase inhibitor sorafenib on human bladder cancer cells. British Journal of Pharmacology 2010, 160:160: 1690-1698.
16. Abou-Alfa G.K., Johnson P., Knox J.J., Capanu M., Davidenko I., Lacava J., Leung T., Gansukh B., Saltz L.B. Doxorubicin plus sorafenib vs doxorubicin alone in patients with advanced hepatocellular carcinoma: a randomized trial. JAMA 2010, 304:2154-2160.
17. Kelley R.K., Nimeiri H.S., Vergo M.T., Bergsland E.K., Ko A.H., Munster P.N., Reinert A., Mulcahy M.F., Benson A.B., Venook A.P. A phase I trial of the combination of temsirolimus (TEM) and sorafenib (SOR) in advanced hepatocellular carcinoma (HCC). Journal of Clinical Oncology 2010, 28:TPS213.
18. Viniegra J.G., Martínez N., Modirassari P., Losa J.H., Parada Cobo C., Lobo V.J., Luquero C.I., Alvarez-Vallina L., Ramón y Cajal S., Rojas J.M., Sánchez-Prieto R. Full activation of PKB/Akt in response to insulin or ionizing radiation is mediated through ATM. Journal of Biological Chemistry 2005, 280:4029-4036.
19. Hickson I., Zhao Y., Richardson C.J., Green S.J., Martin N.M., Orr A.I., Reaper P.M., Jackson S.P., Curtin N.J., Smith G.C. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Research 2004, 64:9152-9159.
20. Sabisz M., Skladanowski A. Modulation of cellular response to anticancer treatment by caffeine: inhibition of cell cycle checkpoints, DNA repair and more. Current Pharmaceutical Biotechnology 2008, 9:325-336.
21. Pullen N., Dennis P.B., Andjelkovic M., Dufner A., Kozma S.C., Hemmings B.A., Thomas G. Phosphorylation and activation of p70s6k by PDK1. Science 1998, 279:707-710.
22. Nishida H., Tatewaki N., Nakajima Y., Magara T., Ko K.M., Hamamori Y., Konishi T. Inhibition of ATR protein kinase activity by schisandrin B in DNA damage response. Nucleic Acids Research 2009, 37:5678-5689.
23. Matsuda Y., Ichida T., Fukumoto M. Hepatocellular carcinoma and liver transplantation: clinical perspective on molecular targeted strategies. Medical Molecular Morphology 2011, 44:117-124.
24. Nicholson K.M., Anderson N.G. The protein kinase B/Akt signalling pathway in human malignancy. Cell Signal 2002, 14:381-395.
25. Chen Y.L., Law P.Y., Loh H.H. Inhibition of PI3K/Akt signaling: an emerging paradigm for targeted cancer therapy. Current Medicinal Chemistry Anticancer Agents 2005, 5:575-589.
26. Ramakrishnan V., Timm M., Haug J.L., Kimlinger T.K., Wellik L.E., Witzig T.E., Rajkumar S.V., Adjei A.A., Kumar S. Sorafenib, a dual Raf kinase/vascular endothelial growth factor receptor inhibitor has significant anti-myeloma activity and synergizes with common anti-myeloma drugs. Oncogene 2010, 29:1190-1202.
27. Gedaly R., Angulo P., Hundley J., Daily M.F., Chen C., Koch A., Evers B.M. PI- 103 and sorafenib inhibit hepatocellular carcinoma cell proliferation by blocking Ras/Raf/MAPK and PI3K/AKT/mTOR pathways. Anticancer Research 2010, 30:4951-5958.
28. Chen K.F., Chen H.L., Tai W.T., Feng W.C., Hsu C.H., Chen P.J., Cheng A.L. Activation of phosphatidylinositol 3-kinase/Akt signaling pathway mediates acquired resistance to sorafenib in hepatocellular carcinoma cells. Journal of Pharmacology and Experimental Therapeutics 2011, 337:155-161.
29. Yang S., Ngo V.C., Lew G.B., Chong L.W., Lee S.S., Ong W.J., Lam W.L., Thng C.H., Koong H.N., Ong H.S., Chung A., Chow P., Lee J., Soo K.C., Huynh H. AZD6244 (ARRY-142886) enhances the therapeutic efficacy of sorafenib in mouse models of gastric cancer. Molecular Cancer Therapeutics 2009, 8:2537-2545.
30. Schult C., Dahlhaus M., Ruck S., Sawitzky M., Amoroso F., Lange S., Etro D., Glass A., Fuellen G., Boldt S., Wolkenhauer O., Neri L.M., Freund M., Junghanss C. The multikinase inhibitor Sorafenib displays significant antiproliferative effects and induces apoptosis via caspase 3, 7 and PARP in B- and T-lymphoblastic cells. BMC Cancer 2010, 10:560.
31. Alessi D.R., Andjelkovic M., Caudwell B., Cron P., Morrice N., Cohen P., Hemmings B.A. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO Journal 1996, 15:6541-6551.
32. Jacinto E., Facchinetti V., Liu D., Soto N., Wei S., Jung S.Y., Huang Q., Qin J., Su B. SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 2006, 127:125-137.
33. Li Y., Yang D.Q. The ATM inhibitor KU-55933 suppresses cell proliferation and induces apoptosis by blocking Akt in cancer cells with overactivated Akt. Molecular Cancer Therapeutics 2010, 9:113-125.
34. Halaby M.J., Hibma J.C., He J., Yang D.Q. ATM protein kinase mediates full activation of Akt and regulates glucose transporter 4 translocation by insulin in muscle cells. Cell Signal 2008, 20:1555-1563.
35. Caporali S., Levati L., Starace G., Ragone G., Bonmassar E., Alvino E., D'Atri S. AKT is activated in an ataxia-telangiectasia and Rad3-related-dependent manner in response to temozolomide and confers protection against drug-induced cell growth inhibition. Molecular Pharmacology 2008, 74:173-183.
36. Lavin M.F. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nature Reviews Molecular Cell Biology 2008, 9:669-759.
37. Wyatt M.D., Wilson D.M. Participation of DNA repair in the response to 5-fluorouracil. Cellular and Molecular Life Sciences 2009, 66:788-799.
38. Alexander A., Cai S.L., Kim J., Nanez A., Sahin M., MacLean K.H., Inoki K., Guan K.L., Shen J., Person M.D., Kusewitt D., Mills G.B., Kastan M.B., Walker C.L. ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:4153-4158.
39. Chiou J.F., Tai C.J., Wang Y.H., Liu T.Z., Jen Y.M., Shiau C.Y. Sorafenib induces preferential apoptotic killing of a drug- and radio-resistant Hep G2 cells through a mitochondria-dependent oxidative stress mechanism. Cancer Biology and Therapy 2009, 8:1904-1913.
40. Foukas L.C., Daniele N., Ktori C., Anderson K.E., Jensen J., Shepherd P.R. Direct effects of caffeine and theophylline on p110 delta and other phosphoinositide 3-kinases. Differential effects on lipid kinase and protein kinase activities. Journal of Biological Chemistry 2002, 277:37124-37130.
41. Hashimoto T., He Z., Ma W.Y., Schmid P.C., Bode A.M., Yang C.S., Dong Z. Caffeine inhibits cell proliferation by G0/G1 phase arrest in JB6 cells. Cancer Research 2004, 64:3344-3349.
42. Takeuchi A., Tsuchiya H., Yamamoto N., Hayashi K., Yamauchi K., Kawahara M., Miyamoto K., Tomita K. Caffeine-potentiated chemotherapy for patients with high-grade soft tissue sarcoma: long-term clinical outcome. Anticancer Research 2007, 27:3489-3495.