Inhibition of Akt induces significant downregulation of survivin and cytotoxicity in human multiple myeloma cells

British Journal of Haematology

Volumn 138, Issue 6, 2007, Pages 783-791

  Hideshima, Teru ^a   Catley, Laurence ^a   Raje, Noopur ^a   Chauhan, Dharminder ^a   Podar, Klaus ^a   Mitsiades, Constantine ^a   Tai, Yu Tzu ^a   Vallet, Sonia ^a   Kiziltepe, Tanyel ^a   Ocio, Enrique ^a   Ikeda, Hiroshi ^a   Okawa, Yutaka ^a   Hideshima, Hiromasa ^a   Munshi, Nikhil C ^a   Yasui, Hiroshi ^a   Richardson, Paul G ^a   Anderson, Kenneth C ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

catenin; Akt; Multiple myeloma; Perifosine; Survivin

Indexed keywords

BETA CATENIN; BORTEZOMIB; CASPASE 3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PERIFOSINE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; SURVIVIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CANCER CELL CULTURE; CELL ADHESION; CELL GROWTH; CELL SURVIVAL; COCULTURE; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOTOXICITY; DOWN REGULATION; DRUG MECHANISM; DRUG POTENTIATION; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HUMAN; HUMAN CELL; MOUSE; MULTIPLE MYELOMA; MYELOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCID MOUSE; STROMA CELL; TUMOR XENOGRAFT; UPREGULATION;

ANIMALS; APOPTOSIS; BORONIC ACIDS; CELL LINE, TUMOR; CELL PROLIFERATION; DOWN-REGULATION; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, ANIMAL; MULTIPLE MYELOMA; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; PHOSPHORYLCHOLINE; PROTEASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PYRAZINES; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSPLANTATION, HETEROLOGOUS;

EID: 34548181762     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2007.06714.x     Document Type: Article

References (52)

1. Aberle, H., Bauer, A., Stappert, J., Kispert, A. Kemler, R. (1997) β-catenin is a target for the ubiquitin-proteasome pathway. Embo Journal, 16, 3797 3804.
2. Altieri, D.C. (2003a) Survivin in apoptosis control and cell cycle regulation in cancer. Progress in Cell Cycle Research, 5, 447 452.
3. Altieri, D.C. (2003b) Survivin, versatile modulation of cell division and apoptosis in cancer. Oncogene, 22, 8581 8589.
4. Ambrosini, G., Adida, C. Altieri, D.C. (1997) A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nature Medicine, 3, 917 921.
5. Amit, S., Hatzubai, A., Birman, Y., Andersen, J.S., Ben-Shushan, E., Mann, M., Ben-Neriah, Y. Alkalay, I. (2002) Axin-mediated CKI phosphorylation of beta-catenin at Ser 45: a molecular switch for the Wnt pathway. Genes Development, 16, 1066 1076.
6. Bailey, H.H., Mahoney, M.R., Ettinger, D.S., Maples, W.J., Fracasso, P.M., Traynor, A.M., Erlichman, C. Okuno, S.H. (2006) Phase II study of daily oral perifosine in patients with advanced soft tissue sarcoma. Cancer, 107, 2462 2467.
7. Covelli, A. (1999) Modulation of multidrug resistance (MDR) in hematological malignancies. Annals of Oncology, 10, 53 59.
8. Cross, D.A., Alessi, D.R., Cohen, P., Andjelkovich, M. Hemmings, B.A. (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature, 378, 785 789.
9. Damiano, J.S., Cress, A.E., Hazlehurst, L.A., Shtil, A.A. Dalton, W.S. (1999) Cell adhesion mediated drug resistance (CAM-DR): role of integrins and resistance to apoptosis in human myeloma cell lines. Blood, 93, 1658 1667.
10. (waf1/cip1) promoter by Sp1. Cancer Research, 64, 743 750.
11. Fukuda, S. Pelus, L.M. (2006) Survivin, a cancer target with an emerging role in normal adult tissues. Molecular Cancer Therapy, 5, 1087 1098.
12. Gajate, C. Mollinedo, F. (2007) Edelfosine and perifosine induce selective apoptosis in multiple myeloma by recruitment of death receptors and downstream signaling molecules into lipid rafts. Blood, 109, 711 719.
13. kip1 levels and contributes to cell adhesion mediated drug resistance (CAM-DR). Oncogene, 19, 4319 4327.
14. Hideshima, T. Anderson, K.C. (2002) Molecular mechanisms of novel therapeutic approaches for multiple myeloma. Nature Review Cancer, 2, 927 937.
15. Hideshima, T., Nakamura, N., Chauhan, D. Anderson, K.C. (2001) Biologic sequelae of interleukin-6 induced PI3-K/Akt signaling in multiple myeloma. Oncogene, 20, 5991 6000.
16. Hideshima, T., Chauhan, D., Hayashi, T., Podar, K., Akiyama, M., Gupta, D., Richardson, P., Munshi, N. Anderson, K.C. (2002) The biological sequelae of stromal cell-derived factor-1α in multiple myeloma. Molecular Cancer Therapy, 1, 539 544.
17. Hideshima, T., Mitsiades, C., Akiyama, M., Hayashi, T., Chauhan, D., Richardson, P., Schlossman, R., Podar, K., Munshi, N.C., Mitsiades, N. Anderson, K.C. (2003) Molecular mechanisms mediating antimyeloma activity of proteasome inhibitor PS-341. Blood, 101, 1530 1534.
18. Hideshima, T., Bergsagel, P.L., Kuehl, W.M. Anderson, K.C. (2004) Advances in biology of multiple myeloma: clinical applications. Blood, 104, 607 618.
19. Hideshima, T., Podar, K., Chauhan, D. Anderson, K.C. (2005a) Cytokines and signal transduction. Best Practice Research Clinical Haematology, 18, 509 524.
20. Hideshima, H., Bradner, J.E., Wong, J., Richardson, D.C., Schreiber, P., S.L. Anderson, K.C. (2005b) Small molecule inhibition of proteasome and aggresome function induces synergistic anti-tumor activity in multiple myeloma. Proceedings of the National Academy of Sciences of the United States of America, 102, 8567 8572.
21. Hideshima, T., Catley, L., Yasui, H., Ishitsuka, K., Raje, N., Mitsiades, C., Podar, K., Munshi, N.C., Chauhan, D., Richardson, P.G. Anderson, K.C. (2006a) Perifosine, an oral bioactive novel alkylphospholipid, inhibits Akt and induces in vitro and in vivo cytotoxicity in human multiple myeloma cells. Blood, 107, 4053 4062.
22. Hideshima, T., Neri, P., Tassone, P., Yasui, H., Ishitsuka, K., Raje, N., Chauhan, D., Podar, K., Mitsiades, C., Dang, L., Munshi, N., Richardson, P., Schenkein, D. Anderson, K.C. (2006b) MLN120B, a novel IKKβ inhibitor, blocks multiple myeloma cell growth in vitro and in vivo. Clinical Cancer Research, 12, 5887 5894.
23. Ishitsuka, K., Hideshima, T., Hamasaki, M., Raje, N., Kumar, S., Hideshima, H., Shiraishi, N., Yasui, H., Roccaro, A.M., Richardson, P., Podar, K., Le Gouill, S., Chauhan, D., Tamura, K., Arbiser, J. Anderson, K.C. (2005) Honokiol overcomes conventional drug resistance in human multiple myeloma by induction of caspase-dependent and independent apoptosis. Blood, 106, 1794 1800.
24. Kaga, S., Zhan, L., Altaf, E. Maulik, N. (2006) Glycogen synthase kinase-3β/β-catenin promotes angiogenic and anti-apoptotic signaling through the induction of VEGF, Bcl-2 and survivin expression in rat ischemic preconditioned myocardium. Journal of Molecular Cell Cardiology, 40, 138 147.
25. Kim, P.J., Plescia, J., Clevers, H., Fearon, E.R. Altieri, D.C. (2003) Survivin and molecular pathogenesis of colorectal cancer. Lancet, 362, 205 209.
26. Kioussi, C., Briata, P., Baek, S.H., Rose, D.W., Hamblet, N.S., Herman, T., Ohgi, K.A., Lin, C., Gleiberman, A., Wang, J., Brault, V., Ruiz-Lozano, P., Nguyen, H.D., Kemler, R., Glass, C.K., Wynshaw-Boris, A. Rosenfeld, M.G. (2002) Identification of a Wnt/Dvl/β-Catenin → Pitx2 pathway mediating cell-type-specific proliferation during development. Cell, 111, 673 685.
27. Klein, B., Tarte, K., Jourdan, M., Mathouk, K., Moreaux, J., Jourdan, E., Legouffe, E., De Vos, J. Rossi, J.F. (2003) Survival and proliferation factors of normal and malignant plasma cells. International Journal of Hematology, 78, 106 113.
28. Kondapaka, S.B., Singh, S.S., Dasmahapatra, G.P., Sausville, E.A. Roy, K.K. (2003) Perifosine, a novel alkylphospholipid, inhibits protein kinase B activation. Molecular Cancer Therapy, 2, 1093 1103.
29. Lentzsch, S., Gries, M., Janz, M., Bargou, R., Dorken, B. Mapara, M.Y. (2003) Macrophage inflammatory protein 1-α (MIP-1 α) triggers migration and signaling cascades mediating survival and proliferation in multiple myeloma (MM) cells. Blood, 101, 3568 3573.
30. Lentzsch, S., Chatterjee, M., Gries, M., Bommert, K., Gollasch, H., Dorken, B. Bargou, R.C. (2004) PI3-K/AKT/FKHR and MAPK signaling cascades are redundantly stimulated by a variety of cytokines and contribute independently to proliferation and survival of multiple myeloma cells. Leukemia, 18, 1883 1890.
31. Li, X., Luwor, R., Lu, Y., Liang, K. Fan, Z. (2006) Enhancement of antitumor activity of the anti-EGF receptor monoclonal antibody cetuximab/C225 by perifosine in PTEN-deficient cancer cells. Oncogene, 25, 525 535.
32. Mitsiades, C.S., Mitsiades, N., Poulaki, V., Schlossman, R., Akiyama, M., Chauhan, D., Hideshima, T., Treon, S.P., Munshi, N.C., Richardson, P.G. Anderson, K.C. (2002) Activation of NF-κB and upregulation of intracellular anti-apoptotic proteins via the IGF-1/Akt signaling in human multiple myeloma cells: therapeutic implications. Oncogene, 21, 5673 5683.
33. Moreaux, J., Legouffe, E., Jourdan, E., Quittet, P., Reme, T., Lugagne, C., Moine, P., Rossi, J.F., Klein, B. Tarte, K. (2004) BAFF and APRIL protect myeloma cells from apoptosis induced by interleukin 6 deprivation and dexamethasone. Blood, 103, 3148 3157.
34. Nyakern, M., Cappellini, A., Mantovani, I. Martelli, A.M. (2006) Synergistic induction of apoptosis in human leukemia T cells by the Akt inhibitor perifosine and etoposide through activation of intrinsic and Fas-mediated extrinsic cell death pathways. Molecular Cancer Therapy, 5, 1559 1570.
35. Okada, H. Mak, T.W. (2004) Pathways of apoptotic and non-apoptotic death in tumour cells. Nature Review Cancer, 4, 592 603.
36. (WAF1) expression in squamous carcinoma cells through a p53-independent pathway, leading to loss in cyclin-dependent kinase activity and cell cycle arrest. Cancer Research, 62, 1401 1409.
37. Podar, K. Anderson, K.C. (2005) The pathophysiological role of VEGF in hematological malignancies: therapeutic implications. Blood, 105, 1383 1395.
38. Rahmani, M., Reese, E., Dai, Y., Bauer, C., Payne, S.G., Dent, P., Spiegel, S. Grant, S. (2005) Coadministration of histone deacetylase inhibitors and perifosine synergistically induces apoptosis in human leukemia cells through Akt and ERK1/2 inactivation and the generation of ceramide and reactive oxygen species. Cancer Research, 65, 2422 2432.
39. Richardson, P.G., Barlogie, B., Berenson, J., Singhal, S., Jagannath, S., Irwin, D., Rajkumar, S.V., Srkalovic, G., Alsina, M., Alexanian, R., Siegel, D., Orlowski, R.Z., Kuter, D., Limentani, S.A., Lee, S., Hideshima, T., Esseltine, D.L., Kauffman, M., Adams, J., Schenkein, D.P. Anderson, K.C. (2003) A phase 2 study of bortezomib in relapsed, refractory myeloma. The New England journal of medicine, 348, 2609 2617.
40. Richardson, P.G., Sonneveld, P., Schuster, M.W., Irwin, D., Stadtmauer, E.A., Facon, T., Harousseau, J.L., Ben-Yehuda, D., Lonial, S., Goldschmidt, H., Reece, D., San-Miguel, J.F., Blade, J., Boccadoro, M., Cavenagh, J., Dalton, W.S., Boral, A.L., Esseltine, D.L., Porter, J.B., Schenkein, D. Anderson, K.C. (2005) Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. The New England journal of medicine, 352, 2487 2498.
41. Romagnoli, M., Trichet, V., David, C., Clement, M., Moreau, P., Bataille, R. Barille-Nion, S. (2007) Significant impact of survivin on myeloma cell growth. Leukemia, 21, 1070 1078.
42. Ruiter, G.A., Zerp, S.F., Bartelink, H., van Blitterswijk, W.J. Verheij, M. (2003) Anti-cancer alkyl-lysophospholipids inhibit the phosphatidylinositol 3-kinase-Akt/PKB survival pathway. Anticancer Drugs, 14, 167 173.
43. Schwarzenbach, H. (2002) Expression of MDR1/P-glycoprotein, the multidrug resistance protein MRP, and the lung-resistance protein LRP in multiple myeloma. Medicine Oncology, 19, 87 104.
44. Srivastava, A.K. Pandey, S.K. (1998) Potential mechanism(s) involved in the regulation of glycogen synthesis by insulin. Molecular Cell Biochemistry, 182, 135 141.
45. Steinhusen, U., Badock, V., Bauer, A., Behrens, J., Wittman-Liebold, B., Dorken, B. Bommert, K. (2000) Apoptosis-induced cleavage of β-catenin by caspase-3 results in proteolytic fragments with reduced transactivation potential. Journal of Biology Chemistry, 275, 16345 16353.
46. Stromberg, T., Dimberg, A., Hammarberg, A., Carlson, K., Osterborg, A., Nilsson, K. Jernberg-Wiklund, H. (2004) Rapamycin sensitizes multiple myeloma cells to apoptosis induced by dexamethasone. Blood, 103, 3138 3147.
47. Tai, Y.T., Podar, K., Catley, L., Tseng, Y.H., Akiyama, M., Shringarpure, R., Burger, R., Hideshima, T., Chauhan, D., Mitsiades, N., Richardson, P., Munshi, N.C., Kahn, C.R., Mitsiades, C. Anderson, K.C. (2003) Insulin-like growth factor-1 induces adhesion and migration in human multiple myeloma cells via activation of β1-integrin and phosphatidylinositol 3'-kinase/AKT signaling. Cancer Research, 63, 5850 5858.
48. Tai, Y.T., Li, X.F., Breitkreutz, I., Song, W., Neri, P., Catley, L., Podar, K., Hideshima, T., Chauhan, D., Raje, N., Schlossman, R., Richardson, P., Munshi, N.C. Anderson, K.C. (2006) Role of B-cell-activating factor in adhesion and growth of human multiple myeloma cells in the bone marrow microenvironment. Cancer Research, 66, 6675 6682.
49. Tu, Y., Gardner, A. Lichtenstein, A. (2000) The phosphatidylinositol 3-kinase/AKT kinase pathway in multiple myeloma plasma cells: roles in cytokine-dependent survival and proliferative responses. Cancer Research, 60, 6763 6770.
50. Vink, S.R., Lagerwerf, S., Mesman, E., Schellens, J.H., Begg, A.C., van Blitterswijk, W.J. Verheij, M. (2006) Radiosensitization of squamous cell carcinoma by the alkylphospholipid perifosine in cell culture and xenografts. Clin Cancer Research, 12, 1615 1622.
51. Yasui, H., Hideshima, T., Ikeda, H., Ocio, E.M., Kiziltepe, T., Vallet, S., Okawa, Y., Neri, P., Sukhdeo, K., Podar, K., Chauhan, D., Richardson, P.G., Raje, N., Carrasco, D.R. Anderson, K.C. (2007) Novel etodolac analog SDX-308 (CEP-18082) induces cytotoxicity in multiple myeloma cells associated with inhibition of β-catenin/TCF pathway. Leukemia, 21, 535 540.
52. You, L., He, B., Xu, Z., Uematsu, K., Mazieres, J., Mikami, I., Reguart, N., Moody, T.W., Kitajewski, J., McCormick, F. Jablons, D.M. (2004) Inhibition of Wnt-2-mediated signaling induces programmed cell death in non-small-cell lung cancer cells. Oncogene, 23, 6170 6174.