Activation of SHIP via a small molecule agonist kills multiple myeloma cells

Experimental Hematology

Volumn 37, Issue 11, 2009, Pages 1274-1283

  Kennah, Michael ^a,b   Yau, Tien Yin ^c   Nodwell, Matt ^a   Krystal, Gerald ^a,d   Andersen, Raymond J ^a   Ong, Christopher J ^a,b,c   Mui, Alice L F ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b VANCOUVER COASTAL HEALTH RESEARCH INSTITUTE   (Canada)

^c VANCOUVER GENERAL HOSPITAL   (Canada)

^d BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AQX MN 100; AQX MN100; BORTEZOMIB; DEXAMETHASONE; DNA; ENZYME ACTIVATOR; PROTEIN KINASE B; PROTEIN TYROSINE PHOSPHATASE SHP; SRC HOMOLOGY 2 DOMAIN CONTAINING INOSITOL 5' PHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL KILLING; CELL STRAIN LNCAP; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DNA SYNTHESIS INHIBITION; DRUG MECHANISM; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; MULTIPLE MYELOMA; MYELOMA CELL; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; B-LYMPHOCYTES; BORONIC ACIDS; CELL LINE, TUMOR; DEXAMETHASONE; DNA REPLICATION; DRUG SCREENING ASSAYS, ANTITUMOR; DRUG SYNERGISM; ENZYME ACTIVATION; HUMANS; INOSITOL PHOSPHATES; MICE; MULTIPLE MYELOMA; NEOPLASM PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; POLYCYCLIC COMPOUNDS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-AKT; PYRAZINES; SIGNAL TRANSDUCTION;

EID: 70349826160     PISSN: 0301472X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exphem.2009.08.001     Document Type: Article

References (71)

1. Kyle R.A. Diagnostic criteria of multiple myeloma. Hematol Oncol Clin North Am 6 (1992) 347-358
2. Seiden M.V., and Anderson K.C. Multiple myeloma. Curr Opin Oncol 6 (1994) 41-49
3. Anderson K.C., Hamblin T.J., and Traynor A. Management of multiple myeloma today. Semin Hematol 36 (1999) 3-8
4. Covelli A. Modulation of multidrug resistance (MDR) in hematological malignancies. Ann Oncol 10 Suppl 6 (1999) 53-59
5. Schwarzenbach H. Expression of MDR1/P-glycoprotein, the multidrug resistance protein MRP, and the lung-resistance protein LRP in multiple myeloma. Med Oncol 19 (2002) 87-104
6. Podar K., Chauhan D., and Anderson K.C. Bone marrow microenvironment and the identification of new targets for myeloma therapy. Leukemia 23 (2009) 10-24
7. Hideshima T., Nakamura N., Chauhan D., and Anderson K.C. Biologic sequelae of interleukin-6 induced PI3-K/Akt signaling in multiple myeloma. Oncogene 20 (2001) 5991-6000
8. Qiang Y.W., Kopantzev E., and Rudikoff S. Insulinlike growth factor-I signaling in multiple myeloma: downstream elements, functional correlates, and pathway cross-talk. Blood 99 (2002) 4138-4146
9. Tu Y., Gardner A., and Lichtenstein A. The phosphatidylinositol 3-kinase/AKT kinase pathway in multiple myeloma plasma cells: roles in cytokine-dependent survival and proliferative responses. Cancer Res 60 (2000) 6763-6770
10. Hsu J., Shi Y., Krajewski S., et al. The AKT kinase is activated in multiple myeloma tumor cells. Blood 98 (2001) 2853-2855
11. G-Amlak M., Uddin S., Mahmud D., et al. Regulation of myeloma cell growth through Akt/Gsk3/forkhead signaling pathway. Biochem Biophys Res Commun 297 (2002) 760-764
12. Mitsiades C.S., Mitsiades N., Poulaki V., et al. Activation of NF-kappaB and upregulation of intracellular anti-apoptotic proteins via the IGF-1/Akt signaling in human multiple myeloma cells: therapeutic implications. Oncogene 21 (2002) 5673-5683
13. Alkan S., and Izban K.F. Immunohistochemical localization of phosphorylated AKT in multiple myeloma. Blood 99 (2002) 2278-2279
14. Hideshima T., Catley L., Yasui H., et al. Perifosine, an oral bioactive novel alkylphospholipid, inhibits Akt and induces in vitro and in vivo cytotoxicity in human multiple myeloma cells. Blood 107 (2006) 4053-4062
15. Frost P., Moatamed F., Hoang B., et al. In vivo antitumor effects of the mTOR inhibitor CCI-779 against human multiple myeloma cells in a xenograft model. Blood 104 (2004) 4181-4187
16. Hideshima T., Catley L., Raje N., et al. Inhibition of Akt induces significant downregulation of survivin and cytotoxicity in human multiple myeloma cells. Br J Haematol 138 (2007) 783-791
17. Vivanco I., and Sawyers C.L. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2 (2002) 489-501
18. Steck P.A., Pershouse M.A., Jasser S.A., et al. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat Genet 15 (1997) 356-362
19. Li J., Yen C., Liaw D., et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 275 (1997) 1943-1947
20. Ge N.L., and Rudikoff S. Expression of PTEN in PTEN-deficient multiple myeloma cells abolishes tumor growth in vivo. Oncogene 19 (2000) 4091-4095
21. Shi Y., Gera J., Hu L., et al. Enhanced sensitivity of multiple myeloma cells containing PTEN mutations to CCI-779. Cancer Res 62 (2002) 5027-5034
22. Zhang J., Choi Y., Mavromatis B., Lichtenstein A., and Li W. Preferential killing of PTEN-null myelomas by PI3K inhibitors through Akt pathway. Oncogene 22 (2003) 6289-6295
23. Aman M.J., Lamkin T.D., Okada H., Kurosaki T., and Ravichandran K.S. The inositol phosphatase SHIP inhibits Akt/PKB activation in B cells. J Biol Chem 273 (1998) 33922-33928
24. Liu Q., Sasaki T., Kozieradzki I., et al. SHIP is a negative regulator of growth factor receptor-mediated PKB/Akt activation and myeloid cell survival. Genes Dev 13 (1999) 786-791
25. Helgason C.D., Kalberer C.P., Damen J.E., et al. A dual role for Src homology 2 domain-containing inositol-5-phosphatase (SHIP) in immunity: aberrant development and enhanced function of b lymphocytes in ship -/- mice. J Exp Med 191 (2000) 781-794
26. Luo J.M., Liu Z.L., Hao H.L., Wang F.X., Dong Z.R., and Ohno R. Mutation analysis of SHIP gene in acute leukemia. Zhongguo Shi Yan Xue Ye Xue Za Zhi 12 (2004) 420-426
27. Fukuda R., Hayashi A., Utsunomiya A., et al. Alteration of phosphatidylinositol 3-kinase cascade in the multilobulated nuclear formation of adult T cell leukemia/lymphoma (ATLL). Proc Natl Acad Sci U S A 102 (2005) 15213-15218
28. Vanderwinden J.M., Wang D., Paternotte N., Mignon S., Isozaki K., and Erneux C. Differences in signaling pathways and expression level of the phosphoinositide phosphatase SHIP1 between two oncogenic mutants of the receptor tyrosine kinase KIT. Cell Signal 18 (2006) 661-669
29. Liang X., Hajivandi M., Veach D., et al. Quantification of change in phosphorylation of BCR-ABL kinase and its substrates in response to Imatinib treatment in human chronic myelogenous leukemia cells. Proteomics 6 (2006) 4554-4564
30. Ghigo A., and Hirsch E. Isoform selective phosphoinositide 3-kinase gamma and delta inhibitors and their therapeutic potential. Recent Pat Inflamm Allergy Drug Discov 2 (2008) 1-10
31. Harvey R.D., and Lonial S. PI3 kinase/AKT pathway as a therapeutic target in multiple myeloma. Future Oncol 3 (2007) 639-647
32. Ihle N.T., and Powis G. Take your PIK: phosphatidylinositol 3-kinase inhibitors race through the clinic and toward cancer therapy. Mol Cancer Ther 8 (2009) 1-9
33. Ong C.J., Ming-Lum A., Nodwell M., et al. Small molecule agonists of SHIP1 inhibit the phosphoinositide 3-kinase pathway in hematopoietic cells. Blood 110 (2007) 1942-1949
34. Helgason C.D., Damen J.E., Rosten P., et al. Targeted disruption of SHIP leads to hematopoietic perturbations, lung pathology, and a shortened life span. Genes Dev 12 (1998) 1610-1620
35. Yang L., Williams D.E., Mui A., et al. Synthesis of pelorol and analogues: activators of the inositol 5-phosphatase SHIP. Org Lett 7 (2005) 1073-1076
36. Peacock J.W., Palmer J., Fink D., et al. PTEN loss promotes mitochondrially dependent type II Fas-induced apoptosis via PEA-15. Mol Cell Biol 29 (2009) 1222-1234
37. Qasimi P., Ming-Lum A., Ghanipour A., et al. Divergent mechanisms utilized by SOCS3 to mediate interleukin-10 inhibition of tumor necrosis factor alpha and nitric oxide production by macrophages. J Biol Chem 281 (2006) 6316-6324
38. Alessi D.R., Andjelkovic M., Caudwell B., et al. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 15 (1996) 6541-6551
39. Wu X., Senechal K., Neshat M.S., Whang Y.E., and Sawyers C.L. The PTEN/MMAC1 tumor suppressor phosphatase functions as a negative regulator of the phosphoinositide 3-kinase/Akt pathway. Proc Natl Acad Sci U S A 95 (1998) 15587-15591
40. Liu Q., Oliveira-Dos-Santos A.J., Mariathasan S., et al. The inositol polyphosphate 5-phosphatase ship is a crucial negative regulator of B cell antigen receptor signaling. J Exp Med 188 (1998) 1333-1342
41. Hideshima T., Chauhan D., Podar K., Schlossman R.L., Richardson P., and Anderson K.C. Novel therapies targeting the myeloma cell and its bone marrow microenvironment. Semin Oncol 28 (2001) 607-612
42. Hideshima T., Mitsiades C., Akiyama M., et al. Molecular mechanisms mediating antimyeloma activity of proteasome inhibitor PS-341. Blood 101 (2003) 1530-1534
43. Mitsiades N., Mitsiades C.S., Poulaki V., et al. Molecular sequelae of proteasome inhibition in human multiple myeloma cells. Proc Natl Acad Sci U S A 99 (2002) 14374-14379
44. Hayashi T., Hideshima T., Akiyama M., et al. Ex vivo induction of multiple myeloma-specific cytotoxic T lymphocytes. Blood 102 (2003) 1435-1442
45. Klein B., Tarte K., Jourdan M., et al. Survival and proliferation factors of normal and malignant plasma cells. Int J Hematol 78 (2003) 106-113
46. Lentzsch S., Chatterjee M., Gries M., et al. 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 (2004) 1883-1890
47. Harris S.J., Parry R.V., Westwick J., and Ward S.G. Phosphoinositide lipid phosphatases: natural regulators of phosphoinositide 3-kinase signaling in T lymphocytes. J Biol Chem 283 (2008) 2465-2469
48. Ward S.G., and Finan P. Isoform-specific phosphoinositide 3-kinase inhibitors as therapeutic agents. Curr Opin Pharmacol 3 (2003) 426-434
49. Ruckle T., Schwarz M.K., and Rommel C. PI3Kgamma inhibition: towards an 'aspirin of the 21st century'?. Nat Rev Drug Discov 5 (2006) 903-918
50. Fan Q.W., Knight Z.A., Goldenberg D.D., et al. A dual PI3 kinase/mTOR inhibitor reveals emergent efficacy in glioma. Cancer Cell 9 (2006) 341-349
51. Gills J.J., and Dennis P.A. Perifosine: update on a novel Akt inhibitor. Curr Oncol Rep 11 (2009) 102-110
52. Witzig T.E., and Kaufmann S.H. Inhibition of the phosphatidylinositol 3-kinase/mammalian target of rapamycin pathway in hematologic malignancies. Curr Treat Options Oncol 7 (2006) 285-294
53. Shi Y., Yan H., Frost P., Gera J., and Lichtenstein A. Mammalian target of rapamycin inhibitors activate the AKT kinase in multiple myeloma cells by up-regulating the insulin-like growth factor receptor/insulin receptor substrate-1/phosphatidylinositol 3-kinase cascade. Mol Cancer Ther 4 (2005) 1533-1540
54. Workman P., Clarke P.A., Guillard S., and Raynaud F.I. Drugging the PI3 kinome. Nat Biotechnol 24 (2006) 794-796
55. Luo J.M., Yoshida H., Komura S., et al. Possible dominant-negative mutation of the SHIP gene in acute myeloid leukemia. Leukemia 17 (2003) 1-8
56. Choi Y., Zhang J., Murga C., et al. PTEN, but not SHIP and SHIP2, suppresses the PI3K/Akt pathway and induces growth inhibition and apoptosis of myeloma cells. Oncogene 21 (2002) 5289-5300
57. Baran C.P., Tridandapani S., Helgason C.D., Humphries R.K., Krystal G., and Marsh C.B. The inositol 5'-phosphatase SHIP-1 and the Src kinase Lyn negatively regulate macrophage colony-stimulating factor-induced Akt activity. J Biol Chem 278 (2003) 38628-38636
58. Weinstein I.B., and Joe A. Oncogene addiction. Cancer Res 68 (2008) 3077-3080 discussion 3080
59. Healy J.I., Dolmetsch R.E., Timmerman L.A., et al. Different nuclear signals are activated by the B cell receptor during positive versus negative signaling. Immunity 6 (1997) 419-428
60. Su B., and Karin M. Mitogen-activated protein kinase cascades and regulation of gene expression. Curr Opin Immunol 8 (1996) 402-411
61. LoPiccolo J., Blumenthal G.M., Bernstein W.B., and Dennis P.A. Targeting the PI3K/Akt/mTOR pathway: effective combinations and clinical considerations. Drug Resist Updat 11 (2008) 32-50
62. Chauhan D., Hideshima T., Rosen S., Reed J.C., Kharbanda S., and Anderson K.C. Apaf-1/cytochrome c-independent and Smac-dependent induction of apoptosis in multiple myeloma (MM) cells. J Biol Chem 276 (2001) 24453-24456
63. Hideshima T., Richardson P., Chauhan D., et al. The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Res 61 (2001) 3071-3076
64. Richardson P.G., Barlogie B., Berenson J., et al. A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med 348 (2003) 2609-2617
65. Richardson P.G., Sonneveld P., Schuster M.W., et al. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N Engl J Med 352 (2005) 2487-2498
66. Chauhan D., Hideshima T., and Anderson K.C. Apoptotic signaling in multiple myeloma: Therapeutic implications. Int J Hematol 78 (2003) 114-120
67. Sonneveld P., Schoester M., and de Leeuw K. Clinical modulation of multidrug resistance in multiple myeloma: effect of cyclosporine on resistant tumor cells. J Clin Oncol 12 (1994) 1584-1591
68. Shain K.H., and Dalton W.S. Cell adhesion is a key determinant in de novo multidrug resistance (MDR): New targets for the prevention of acquired MDR. Mol Cancer Ther 1 (2001) 69-78
69. Chauhan D., Uchiyama H., Akbarali Y., et al. Multiple myeloma cell adhesion-induced interleukin-6 expression in bone marrow stromal cells involves activation of NF-kappa B. Blood 87 (1996) 1104-1112
70. Chauhan D., Li G., Podar K., et al. Targeting mitochondria to overcome conventional and bortezomib/proteasome inhibitor PS-341 resistance in multiple myeloma (MM) cells. Blood 104 (2004) 2458-2466
71. Zollinger A., Stuhmer T., Chatterjee M., et al. Combined functional and molecular analysis of tumor cell signaling defines 2 distinct myeloma subgroups: Akt-dependent and Akt-independent multiple myeloma. Blood 112 (2008) 3403-3411