Pim2 is required for maintaining multiple myeloma cell growth through modulating TSC2 phosphorylation

Blood

Volumn 122, Issue 9, 2013, Pages 1610-1620

  Lu, Jing ^a   Zavorotinskaya, Tatiana ^a   Dai, Yumin ^a   Niu, Xiao Hong ^a   Castillo, Joseph ^a   Sim, Janet ^a   Yu, Jianjun ^a   Wang, Yingyun ^a   Langowski, John L ^a   Holash, Jocelyn ^a   Shannon, Kevin ^b   Garcia, Pablo D ^a  

^a NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINO PIPERIDINE PYRIDYL CARBOXAMIDE; ANTINEOPLASTIC AGENT; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; P70S6K PROTEIN; PHOSPHOTRANSFERASE INHIBITOR; PIM2 PROTEIN; PIM3 PROTEIN; PROTEIN; PROTEIN KINASE B; PROTEIN KINASE PIM 1; S6RP PROTEIN; SHORT HAIRPIN RNA; TUBERIN; UNCLASSIFIED DRUG; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; ONCOPROTEIN; PIM2 PROTEIN, HUMAN; PIPERIDINE DERIVATIVE; PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE; PYRIDINE DERIVATIVE; TARGET OF RAPAMYCIN KINASE; TUMOR SUPPRESSOR PROTEIN;

ACUTE MONOCYTIC LEUKEMIA; ACUTE MONOCYTIC LEUKEMIA CELL LINE; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER GROWTH; CELL PROLIFERATION; CHRONIC MYELOID LEUKEMIA; CHRONIC MYELOID LEUKEMIA CELL LINE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; GENE EXPRESSION; GENE SILENCING; GENETIC BACKGROUND; MOUSE; MULTIPLE MYELOMA; MULTIPLE MYELOMA CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; DRUG EFFECTS; DRUG SCREENING; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; TUMOR CELL LINE; TUMOR VOLUME; DRUG ANTAGONISM; DRUG EFFECT;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; HUMANS; MICE; MODELS, BIOLOGICAL; MULTIPLE MYELOMA; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PIPERIDINES; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PYRIDINES; TOR SERINE-THREONINE KINASES; TUMOR BURDEN; TUMOR SUPPRESSOR PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84888039072     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-01-481457     Document Type: Article

References (49)

1. Cuypers HT, Selten G, Quint W, et al. Murine leukemia virus-induced T-cell lymphomagenesis: integration of proviruses in a distinct chromosomal region. Cell. 1984;37(1):141-150.
2. van Lohuizen, M, Verbeek S, Krimpenfort P, et al. Predisposition to lymphomagenesis in pim-1 transgenic mice: cooperation with c-myc and N-myc in murine leukemia virus-induced tumors. Cell. 1989;56(4):673-682.
3. Berns A, Breuer M, Verbeek S, van Lohuizen, M. Transgenic mice as a means to study synergism between oncogenes. Int J Cancer Suppl. 1989; 4:22-25.
4. Valdman A, Fang X, Pang ST, Ekman P, Egevad L. Pim-1 expression in prostatic intraepithelial neoplasia and human prostate cancer. Prostate. 2004;60(4):367-371.
5. Gong J, Wang J, Ren K, Liu C, Li B, Shi Y. Serine/threonine kinase Pim-2 promotes liver tumorigenesis induction through mediating survival and preventing apoptosis of liver cell. J Surg Res. 2009;153(1):17-22.
6. Nawijn MC, Alendar A, Berns A. For better or for worse: The role of Pim oncogenes in tumorigenesis. Nat Rev Cancer. 2011;11(1): 23-34.
7. Alvarado Y, Giles FJ, Swords RT. The PIM kinases in hematological cancers. Expert Rev Hematol. 2012;(5):81-96.
8. Matikainen S, Sareneva T, Ronni T, Lehtonen A, Koskinen PJ, Julkunen I. Interferon-Alpha activates multiple STAT proteins and upregulates proliferation-Associated IL-2Ralpha, c-myc, and pim-1 genes in human T cells. Blood. 1999;93(6): 1980-1991.
9. Zhu N, Ramirez LM, Lee RL, Magnuson NS, Bishop GA, Gold MR. CD40 signaling in B cells regulates the expression of the Pim-1 kinase via the NF-kappa B pathway. J Immunol. 2002; 168(2):744-754.
10. Yan B, Zemskova M, Holder S, et al. The PIM-2 kinase phosphorylates BAD on serine 112 and reverses BAD-induced cell death. J Biol Chem. 2003;278(46):45358-45367.
11. Zhang Y, Wang Z, Magnuson NS. Pim-1 kinasedependent phosphorylation of p21Cip1/WAF1 regulates its stability and cellular localization in H1299 cells. Mol Cancer Res. 2007;5(9):909-922.
12. Morishita D, Katayama R, Sekimizu K, Tsuruo T, Fujita N. Pim kinases promote cell cycle progression by phosphorylating and downregulating p27Kip1 at the transcriptional and posttranscriptional levels. Cancer Res. 2008; 68(13):5076-5085.
13. Brault L, Gasser C, Bracher F, Huber K, Knapp S, Schwaller J. PIM serine/threonine kinases in the pathogenesis and therapy of hematologic malignancies and solid cancers. Haematologica. 2010;95(6):1004-1015.
14. Barretina J, Caponigro G, Stransky N, et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature. 2012;483(7391):603-607.
15. Peterson TR, Laplante M, Thoreen CC, et al. Deptor is an mTOR inhibitor frequently overexpressed in multiple myeloma cells and required for their survival. Cell. 2009;137(5): 873-886.
16. Lin YW, Beharry ZM, Hill EG, et al. A small molecule inhibitor of Pim protein kinases blocks the growth of precursor T-cell lymphoblastic leukemia/lymphoma. Blood. 2010;115(4): 824-833.
17. Wang L, Rhodes CJ, Lawrence JC Jr. Activation of mammalian target of rapamycin (mTOR) by insulin is associated with stimulation of 4EBP1 binding to dimeric mTOR complex 1. J Biol Chem. 2006;281(34):24293-24303.
18. Harris TE, Chi A, Shabanowitz J, Hunt DF, Rhoads RE, Lawrence JC Jr. mTOR-dependent stimulation of the association of eIF4G and eIF3 by insulin. EMBO J. 2006;25(8):1659-1668.
19. Kim DH, Sarbassov DD, Ali SM, et al. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell. 2002;110(2):163-175.
20. Zhang F, Beharry ZM, Harris TE, et al. PIM1 protein kinase regulates PRAS40 phosphorylation and mTOR activity in FDCP1 cells. Cancer Biol Ther. 2009;8(9):846-853.
21. Beharry Z, Mahajan S, Zemskova M, et al. The Pim protein kinases regulate energy metabolism and cell growth. Proc Natl Acad Sci USA. 2011; 108(2):528-533.
22. Inoki K, Li Y, Xu T, Guan KL. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev. 2003;17(15): 1829-1834.
23. Li Y, Corradetti MN, Inoki K, Guan KL. TSC2: filling the GAP in the mTOR signaling pathway. Trends Biochem Sci. 2004;29(1):32-38.
24. Bullock AN, Debreczeni J, Amos AL, Knapp S, Turk BE. Structure and substrate specificity of the Pim-1 kinase. J Biol Chem. 2005;280(50): 41675-41682.
25. Peng C, Knebel A, Morrice NA, et al. Pim kinase substrate identification and specificity. J Biochem. 2007;141(3):353-362.
26. Huang J, Manning BD. A complex interplay between Akt, TSC2 and the two mTOR complexes. Biochem Soc Trans. 2009;37(Pt 1): 217-222.
27. Cathomen T, Joung JK. Zinc-finger nucleases: The next generation emerges. Mol Ther. 2008; 16(7):1200-1207.
28. Maira SM, Pecchi S, Huang A, et al. Identification and characterization of NVP-BKM120, an orally available pan-class I PI3-kinase inhibitor. Mol Cancer Ther. 2012;11(2):317-328.
29. Woodland RT, Fox CJ, Schmidt MR, et al. Multiple signaling pathways promote B lymphocyte stimulator dependent B-cell growth and survival. Blood. 2008;111(2):750-760.
30. Cohen AM, Grinblat B, Bessler H, et al. Increased expression of the hPim-2 gene in human chronic lymphocytic leukemia and non-Hodgkin lymphoma. Leuk Lymphoma. 2004; 45(5):951-955.
31. Gomez-Abad C, Pisonero H, Blanco-Aparicio C, et al. PIM2 inhibition as a rational therapeutic approach in B-cell lymphoma. Blood. 2011; 118(20):5517-5527.
32. Wang Z, Bhattacharya N, Mixter PF, Wei W, Sedivy J, Magnuson NS. Phosphorylation of the cell cycle inhibitor p21Cip1/WAF1 by Pim-1 kinase. Biochim Biophys Acta. 2002;1593(1): 45-55.
33. Fingar DC, Richardson CJ, Tee AR, Cheatham L, Tsou C, Blenis J. mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol Cell Biol. 2004;24(1):200-216.
34. Ciuffreda L, Di Sanza, C, Incani UC, Milella M. The mTOR pathway: A new target in cancer therapy. Curr Cancer Drug Targets. 2010;10(5):484-495.
35. Vignot S, Faivre S, Aguirre D, Raymond E. mTOR-Targeted therapy of cancer with rapamycin derivatives. Ann Oncol. 2005;16(4):525-537.
36. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell. 2012;149(2): 274-293.
37. Manning BD, Tee AR, Logsdon MN, Blenis J, Cantley LC. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol Cell. 2002;10(1):151-162.
38. Potter CJ, Pedraza LG, Xu T. Akt regulates growth by directly phosphorylating Tsc2. Nat Cell Biol. 2002;4(9):658-665.
39. Vander Haar, E, Lee SI, Bandhakavi S, Griffin TJ, Kim DH. Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40. Nat Cell Biol. 2007;9(3):316-323.
40. O'Reilly KE, Rojo F, She QB, et al. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res. 2006;66(3):1500-1508.
41. Carracedo A, Ma L, Teruya-Feldstein J, et al. Inhibition of mTORC1 leads to MAPK pathway activation through a PI3K-dependent feedback loop in human cancer. J Clin Invest. 2008;118(9): 3065-3074.
42. Huang J, Wu S, Wu CL, Manning BD. Signaling events downstream of mammalian target of rapamycin complex 2 are attenuated in cells and tumors deficient for the tuberous sclerosis complex tumor suppressors. Cancer Res. 2009; 69(15):6107-6114.
43. Anizon F, Shtil AA, Danilenko VN, Moreau P. Fighting tumor cell survival: Advances in the design and evaluation of Pim inhibitors. Curr Med Chem. 2010;17(34):4114-4133.
44. Dakin LA, Block MH, Chen H, et al. Discovery of novel benzylidene-1, 3-Thiazolidine-2, 4-diones as potent and selective inhibitors of the PIM-1, PIM-2, and PIM-3 protein kinases. Bioorg Med Chem Lett. 2012;22(14):4599-4604.
45. Narlik-Grassow M, Blanco-Aparicio C, Carnero A. The PIM Family of Serine/Threonine Kinases in Cancer [published online ahead of print April 10, 2013]. Med Res Rev.
46. Chen LS, Redkar S, Taverna P, Cortes JE, Gandhi V. Mechanisms of cytotoxicity to Pim kinase inhibitor, SGI-1776, in acute myeloid leukemia. Blood. 2011;118(3):693-702.
47. Asano J, Nakano A, Oda A, et al. The serine/threonine kinase Pim-2 is a novel anti-Apoptotic mediator in myeloma cells. Leukemia. 2011;25(7): 1182-1188.
48. Johrer K, Obkircher M, Neureiter D, et al. Antimyeloma activity of the sesquiterpene lactone cnicin: impact on Pim-2 kinase as a novel therapeutic target. J Mol Med (Berl). 2012;(90): 681-693.
49. Hammerman PS, Fox CJ, Birnbaum MJ, Thompson CB. Pim and Akt oncogenes are independent regulators of hematopoietic cell growth and survival. Blood. 2005;105(11): 4477-4483.