PIM kinase (and Akt) biology and signaling in tumors

Pharmacology and Therapeutics

Volumn 151, Issue , 2015, Pages 41-49

  Warfel, Noel A ^a,b   Kraft, Andrew S ^a,b  

^a Department of Cellular and Molecular Medicine ^*  (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Akt; Cancer; Oncogenes; PIM kinases; Therapeutic resistance

Indexed keywords

ACICLOVIR; MESSENGER RNA; MOLONEY MURINE LEUKEMIA VIRUS KINASE; PIM KINASE; PROTEIN KINASE; PROTEIN KINASE B; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; PROTEIN KINASE PIM 1; PROTO-ONCOGENE PROTEINS PIM;

APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL CYCLE REGULATION; CELL GROWTH; DRUG EFFICACY; ENZYME REGULATION; GENE CONTROL; HUMAN; MALIGNANT NEOPLASTIC DISEASE; MOLONEY MURINE LEUKEMIA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; VIRUS DNA CELL DNA INTERACTION; VIRUS INHIBITION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CYCLE; CELL SURVIVAL; DRUG RESISTANCE; ENZYMOLOGY; METABOLISM; NEOPLASMS; PATHOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; HUMANS; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-PIM-1; SIGNAL TRANSDUCTION;

EID: 84930087907     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2015.03.001     Document Type: Review

References (117)

1. M. Adam, V. Pogacic, M. Bendit, R. Chappuis, M.C. Nawijn, J. Duyster, C.J. Fox, C.B. Thompson, J. Cools, and J. Schwaller Targeting PIM kinases impairs survival of hematopoietic cells transformed by kinase inhibitor-sensitive and kinase inhibitor-resistant forms of Fms-like tyrosine kinase 3 and BCR/ABL Cancer Res 66 2006 3828 3835
2. J.M. Adams, A.W. Harris, C.A. Pinkert, L.M. Corcoran, W.S. Alexander, S. Cory, R.D. Palmiter, and R.L. Brinster The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice Nature 318 1985 533 538
3. T.L. Aho, J. Sandholm, K.J. Peltola, H.P. Mankonen, M. Lilly, and P.J. Koskinen Pim-1 kinase promotes inactivation of the pro-apoptotic Bad protein by phosphorylating it on the Ser112 gatekeeper site FEBS Lett 571 2004 43 49
4. J.D. Allen, E. Verhoeven, J. Domen, M. van der Valk, and A. Berns Pim-2 transgene induces lymphoid tumors, exhibiting potent synergy with c-myc Oncogene 15 1997 1133 1141
5. M. Bachmann, H. Hennemann, P.X. Xing, I. Hoffmann, and T. Moroy The oncogenic serine/threonine kinase Pim-1 phosphorylates and inhibits the activity of Cdc25C-associated kinase 1 (C-TAK1): a novel role for Pim-1 at the G2/M cell cycle checkpoint J Biol Chem 279 2004 48319 48328
6. M. Bachmann, C. Kosan, P.X. Xing, M. Montenarh, I. Hoffmann, and T. Moroy The oncogenic serine/threonine kinase Pim-1 directly phosphorylates and activates the G2/M specific phosphatase Cdc25C Int J Biochem Cell Biol 38 2006 430 443
7. A. Barthel, S.T. Okino, J. Liao, K. Nakatani, J. Li, J.P. Whitlock Jr., and R.A. Roth Regulation of GLUT1 gene transcription by the serine/threonine kinase Akt1 J Biol Chem 274 1999 20281 20286
8. D. Baytel, S. Shalom, I. Madgar, R. Weissenberg, and J. Don The human Pim-2 proto-oncogene and its testicular expression Biochim Biophys Acta 1442 1998 274 285
9. Z. Beharry, S. Mahajan, M. Zemskova, Y.W. Lin, B.G. Tholanikunnel, Z. Xia, C.D. Smith, and A.S. Kraft The Pim protein kinases regulate energy metabolism and cell growth Proc Natl Acad Sci U S A 108 2011 528 533
10. A.N. Bullock, J. Debreczeni, A.L. Amos, S. Knapp, and B.E. Turk Structure and substrate specificity of the Pim-1 kinase J Biol Chem 280 2005 41675 41682
11. L.C. Cantley The phosphoinositide 3-kinase pathway Science 296 2002 1655 1657
12. M.H. Cardone, N. Roy, H.R. Stennicke, G.S. Salvesen, T.F. Franke, E. Stanbridge, S. Frisch, and J.C. Reed Regulation of cell death protease caspase-9 by phosphorylation Science 282 1998 1318 1321
13. B. Cen, S. Mahajan, W. Wang, and A.S. Kraft Elevation of receptor tyrosine kinases by small molecule AKT inhibitors in prostate cancer is mediated by Pim-1 Cancer Res 73 2013 3402 3411
14. B. Cen, S. Mahajan, M. Zemskova, Z. Beharry, Y.W. Lin, S.D. Cramer, M.B. Lilly, and A.S. Kraft Regulation of Skp2 levels by the Pim-1 protein kinase J Biol Chem 285 2010 29128 29137
15. B. Cen, Y. Xiong, J.H. Song, S. Mahajan, R. DuPont, K. McEachern, D.J. DeAngelo, J.E. Cortes, M.D. Minden, A. Ebens, A. Mims, A.C. LaRue, and A.S. Kraft The Pim-1 protein kinase is an important regulator of MET receptor tyrosine kinase levels and signaling Mol Cell Biol 34 2014 2517 2532
16. J. Chen, M. Kobayashi, S. Darmanin, Y. Qiao, C. Gully, R. Zhao, S. Kondo, H. Wang, S.C. Yeung, and M.H. Lee Hypoxia-mediated up-regulation of Pim-1 contributes to solid tumor formation Am J Pathol 175 2009 400 411
17. J. Chen, M. Kobayashi, S. Darmanin, Y. Qiao, C. Gully, R. Zhao, S.C. Yeung, and M.H. Lee Pim-1 plays a pivotal role in hypoxia-induced chemoresistance Oncogene 28 2009 2581 2592
18. W.W. Chen, D.C. Chan, C. Donald, M.B. Lilly, and A.S. Kraft Pim family kinases enhance tumor growth of prostate cancer cells Mol Cancer Res 3 2005 443 451
19. F. Cheng, M. Weidner-Glunde, M. Varjosalo, E.M. Rainio, A. Lehtonen, T.F. Schulz, P.J. Koskinen, J. Taipale, and P.M. Ojala KSHV reactivation from latency requires Pim-1 and Pim-3 kinases to inactivate the latency-associated nuclear antigen LANA PLoS Pathog 5 2009 e1000324
20. T.L. Cibull, T.D. Jones, L. Li, J.N. Eble, L. Ann Baldridge, S.R. Malott, Y. Luo, and L. Cheng Overexpression of Pim-1 during progression of prostatic adenocarcinoma J Clin Pathol 59 2006 285 288
21. A.C. Cichon, A. Pickard, S.S. McDade, D.J. Sharpe, M. Moran, J.A. James, and D.J. McCance AKT in stromal fibroblasts controls invasion of epithelial cells Oncotarget 4 2013 1103 1116
22. A.M. Cohen, B. Grinblat, H. Bessler, D. Kristt, A. Kremer, A. Schwartz, M. Halperin, S. Shalom, D. Merkel, and J. Don Increased expression of the hPim-2 gene in human chronic lymphocytic leukemia and non-Hodgkin lymphoma Leuk Lymphoma 45 2004 951 955
23. H.T. Cuypers, G. Selten, A. Berns, and A.H. Geurts van Kessel Assignment of the human homologue of Pim-1, a mouse gene implicated in leukemogenesis, to the pter-q12 region of chromosome 6 Hum Genet 72 1986 262 265
24. L. del Peso, M. Gonzalez-Garcia, C. Page, R. Herrera, and G. Nunez Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt Science 278 1997 687 689
25. B. Deneen, S.M. Welford, T. Ho, F. Hernandez, I. Kurland, and C.T. Denny PIM3 proto-oncogene kinase is a common transcriptional target of divergent EWS/ETS oncoproteins Mol Cell Biol 23 2003 3897 3908
26. S.M. Dhanasekaran, T.R. Barrette, D. Ghosh, R. Shah, S. Varambally, K. Kurachi, K.J. Pienta, M.A. Rubin, and A.M. Chinnaiyan Delineation of prognostic biomarkers in prostate cancer Nature 412 2001 822 826
27. J. Domen, M. Von Lindern, A. Hermans, M. Breuer, G. Grosveld, and A. Berns Comparison of the human and mouse PIM-1 cDNAs: nucleotide sequence and immunological identification of the in vitro synthesized PIM-1 protein Oncog Res 1 1987 103 112
28. S. Faivre, G. Kroemer, and E. Raymond Current development of mTOR inhibitors as anticancer agents Nat Rev Drug Discov 5 2006 671 688
29. J.D. Feldman, L. Vician, M. Crispino, G. Tocco, M. Baudry, and H.R. Herschman Seizure activity induces PIM-1 expression in brain J Neurosci Res 53 1998 502 509
30. K.M. Fischer, C.T. Cottage, M.H. Konstandin, M. Volkers, M. Khan, and M.A. Sussman Pim-1 kinase inhibits pathological injury by promoting cardioprotective signaling J Mol Cell Cardiol 51 2011 554 558
31. M. Friedmann, M.S. Nissen, D.S. Hoover, R. Reeves, and N.S. Magnuson Characterization of the proto-oncogene Pim-1: kinase activity and substrate recognition sequence Arch Biochem Biophys 298 1992 594 601
32. C. Fujii, Y. Nakamoto, P. Lu, K. Tsuneyama, B.K. Popivanova, S. Kaneko, and N. Mukaida Aberrant expression of serine/threonine kinase Pim-3 in hepatocellular carcinoma development and its role in the proliferation of human hepatoma cell lines Int J Cancer 114 2005 209 218
33. N. Fujita, S. Sato, K. Katayama, and T. Tsuruo Akt-dependent phosphorylation of p27Kip1 promotes binding to 14-3-3 and cytoplasmic localization J Biol Chem 277 2002 28706 28713
34. P.D. Garcia, J.L. Langowski, Y. Wang, M. Chen, J. Castillo, C. Fanton, M. Ison, T. Zavorotinskaya, Y. Dai, J. Lu, X.H. Niu, S. Basham, J. Chan, J. Yu, M. Doyle, P. Feucht, R. Warne, J. Narberes, T. Tsang, C. Fritsch, A. Kauffmann, E. Pfister, P. Drueckes, J. Trappe, C. Wilson, W. Han, J. Lan, G. Nishiguchi, M. Lindvall, C. Bellamacina, J.A. Aycinena, R. Zang, J. Holash, and M.T. Burger Pan-PIM kinase inhibition provides a novel therapy for treating hematologic cancers Clin Cancer Res 20 2014 1834 1845
35. K. Gottlob, N. Majewski, S. Kennedy, E. Kandel, R.B. Robey, and N. Hay Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase Genes Dev 15 2001 1406 1418
36. R. Grundler, L. Brault, C. Gasser, A.N. Bullock, T. Dechow, S. Woetzel, V. Pogacic, A. Villa, S. Ehret, G. Berridge, A. Spoo, C. Dierks, A. Biondi, S. Knapp, J. Duyster, and J. Schwaller Dissection of PIM serine/threonine kinases in FLT3-ITD-induced leukemogenesis reveals PIM1 as regulator of CXCL12-CXCR4-mediated homing and migration J Exp Med 206 2009 1957 1970
37. J.J. Gu, Z. Wang, R. Reeves, and N.S. Magnuson PIM1 phosphorylates and negatively regulates ASK1-mediated apoptosis Oncogene 28 2009 4261 4271
38. A. Hahn-Windgassen, V. Nogueira, C.C. Chen, J.E. Skeen, N. Sonenberg, and N. Hay Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity J Biol Chem 280 2005 32081 32089
39. P.S. Hammerman, C.J. Fox, M.J. Birnbaum, and C.B. Thompson Pim and Akt oncogenes are independent regulators of hematopoietic cell growth and survival Blood 105 2005 4477 4483
40. M. Hanada, J. Feng, and B.A. Hemmings Structure, regulation and function of PKB/AKT - a major therapeutic target Biochim Biophys Acta 1697 2004 3 16
41. C. Hogan, C. Hutchison, L. Marcar, D. Milne, M. Saville, J. Goodlad, N. Kernohan, and D. Meek Elevated levels of oncogenic protein kinase Pim-1 induce the p53 pathway in cultured cells and correlate with increased Mdm2 in mantle cell lymphoma J Biol Chem 283 2008 18012 18023
42. D.S. Hoover, D.G. Wingett, J. Zhang, R. Reeves, and N.S. Magnuson Pim-1 protein expression is regulated by its 5′-untranslated region and translation initiation factor elF-4E Cell Growth Differ 8 1997 1371 1380
43. M.A. Hospital, A.S. Green, C. Lacombe, P. Mayeux, D. Bouscary, and J. Tamburini The FLT3 and Pim kinases inhibitor SGI-1776 preferentially target FLT3-ITD AML cells Blood 119 2012 1791 1792
44. A. Huttmann, L. Klein-Hitpass, J. Thomale, R. Deenen, A. Carpinteiro, H. Nuckel, P. Ebeling, A. Fuhrer, J. Edelmann, L. Sellmann, U. Duhrsen, and J. Durig Gene expression signatures separate B-cell chronic lymphocytic leukaemia prognostic subgroups defined by ZAP-70 and CD38 expression status Leukemia 20 2006 1774 1782
45. E.K. Keeton, K. McEachern, K.S. Dillman, S. Palakurthi, Y. Cao, M.R. Grondine, S. Kaur, S. Wang, Y. Chen, A. Wu, M. Shen, F.D. Gibbons, M.L. Lamb, X. Zheng, R.M. Stone, D.J. Deangelo, L.C. Platanias, L.A. Dakin, H. Chen, P.D. Lyne, and D. Huszar AZD1208, a potent and selective pan-Pim kinase inhibitor, demonstrates efficacy in preclinical models of acute myeloid leukemia Blood 123 2014 905 913
46. J. Kim, M. Roh, and S.A. Abdulkadir Pim1 promotes human prostate cancer cell tumorigenicity and c-MYC transcriptional activity BMC Cancer 10 2010 248
47. K.T. Kim, K. Baird, J.Y. Ahn, P. Meltzer, M. Lilly, M. Levis, and D. Small Pim-1 is up-regulated by constitutively activated FLT3 and plays a role in FLT3-mediated cell survival Blood 105 2005 1759 1767
48. O. Kim, T. Jiang, Y. Xie, Z. Guo, H. Chen, and Y. Qiu Synergism of cytoplasmic kinases in IL6-induced ligand-independent activation of androgen receptor in prostate cancer cells Oncogene 23 2004 1838 1844
49. A.N. Kirschner, J. Wang, R. van der Meer, P.D. Anderson, O.E. Franco-Coronel, M.H. Kushner, J.H. Everett, O. Hameed, E.K. Keeton, M. Ahdesmaki, S.E. Grosskurth, D. Huszar, and S.A. Abdulkadir PIM kinase inhibitor AZD1208 for treatment of MYC-driven prostate cancer J Natl Cancer Inst 107 2015
50. K.S. Kovacina, G.Y. Park, S.S. Bae, A.W. Guzzetta, E. Schaefer, M.J. Birnbaum, and R.A. Roth Identification of a proline-rich Akt substrate as a 14-3-3 binding partner J Biol Chem 278 2003 10189 10194
51. H.K. Lin, G. Wang, Z. Chen, J. Teruya-Feldstein, Y. Liu, C.H. Chan, W.L. Yang, H. Erdjument-Bromage, K.I. Nakayama, S. Nimer, P. Tempst, and P.P. Pandolfi Phosphorylation-dependent regulation of cytosolic localization and oncogenic function of Skp2 by Akt/PKB Nat Cell Biol 11 2009 420 432
52. H.T. Liu, N. Wang, X. Wang, and S.L. Li Overexpression of Pim-1 is associated with poor prognosis in patients with esophageal squamous cell carcinoma J Surg Oncol 102 2010 683 688
53. J.A. Losman, X.P. Chen, B.Q. Vuong, S. Fay, and P.B. Rothman Protein phosphatase 2A regulates the stability of Pim protein kinases J Biol Chem 278 2003 4800 4805
54. J. Lu, T. Zavorotinskaya, Y. Dai, X.H. Niu, J. Castillo, J. Sim, J. Yu, Y. Wang, J.L. Langowski, J. Holash, K. Shannon, and P.D. Garcia Pim2 is required for maintaining multiple myeloma cell growth through modulating TSC2 phosphorylation Blood 122 2013 1610 1620
55. J. Ma, H.K. Arnold, M.B. Lilly, R.C. Sears, and A.S. Kraft Negative regulation of Pim-1 protein kinase levels by the B56beta subunit of PP2A Oncogene 26 2007 5145 5153
56. D. Mahadevan, and N. Shirahatti Strategies for targeting the multidrug resistance-1 (MDR1)/P-gp transporter in human malignancies Curr Cancer Drug Targets 5 2005 445 455
57. B.D. Manning, A.R. Tee, M.N. Logsdon, J. Blenis, and L.C. Cantley Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway Mol Cell 10 2002 151 162
58. S. Matikainen, T. Sareneva, T. Ronni, A. Lehtonen, P.J. Koskinen, and I. Julkunen Interferon-alpha activates multiple STAT proteins and upregulates proliferation-associated IL-2Ralpha, c-myc, and Pim-1 genes in human T cells Blood 93 1999 1980 1991
59. K. Meja, C. Stengel, R. Sellar, D. Huszar, B.R. Davies, R.E. Gale, D.C. Linch, and A. Khwaja PIM and AKT kinase inhibitors show synergistic cytotoxicity in acute myeloid leukaemia that is associated with convergence on mTOR and MCL1 pathways Br J Haematol 167 2014 69 79
60. H. Mikkers, M. Nawijn, J. Allen, C. Brouwers, E. Verhoeven, J. Jonkers, and A. Berns Mice deficient for all PIM kinases display reduced body size and impaired responses to hematopoietic growth factors Mol Cell Biol 24 2004 6104 6115
61. K. Mizuno, T. Shirogane, A. Shinohara, A. Iwamatsu, M. Hibi, and T. Hirano Regulation of Pim-1 by Hsp90 Biochem Biophys Res Commun 281 2001 663 669
62. T. Mochizuki, C. Kitanaka, K. Noguchi, T. Muramatsu, A. Asai, and Y. Kuchino Physical and functional interactions between Pim-1 kinase and Cdc25A phosphatase. Implications for the Pim-1-mediated activation of the c-Myc signaling pathway J Biol Chem 274 1999 18659 18666
63. D. Morishita, R. Katayama, K. Sekimizu, T. Tsuruo, and N. Fujita Pim kinases promote cell cycle progression by phosphorylating and down-regulating p27Kip1 at the transcriptional and posttranscriptional levels Cancer Res 68 2008 5076 5085
64. T. Moroy, S. Verbeek, A. Ma, P. Achacoso, A. Berns, and F. Alt E mu N- and E mu L-myc cooperate with E mu Pim-1 to generate lymphoid tumors at high frequency in double-transgenic mice Oncogene 6 1991 1941 1948
65. S.M. Mumenthaler, P.Y. Ng, A. Hodge, D. Bearss, G. Berk, S. Kanekal, S. Redkar, P. Taverna, D.B. Agus, and A. Jain Pharmacologic inhibition of Pim kinases alters prostate cancer cell growth and resensitizes chemoresistant cells to taxanes Mol Cancer Ther 8 2009 2882 2893
66. M. Nakao, S. Yokota, T. Iwai, H. Kaneko, S. Horiike, K. Kashima, Y. Sonoda, T. Fujimoto, and S. Misawa Internal tandem duplication of the flt3 gene found in acute myeloid leukemia Leukemia 10 1996 1911 1918
67. M. Narlik-Grassow, C. Blanco-Aparicio, and A. Carnero The PIM family of serine/threonine kinases in cancer Med Res Rev 34 2014 136 159
68. M. Narlik-Grassow, C. Blanco-Aparicio, Y. Cecilia, S. Peregrina, B. Garcia-Serelde, S. Munoz-Galvan, M. Canamero, and A. Carnero The essential role of PIM kinases in sarcoma growth and bone invasion Carcinogenesis 33 2012 1479 1486
69. M.C. Nawijn, A. Alendar, and A. Berns For better or for worse: the role of Pim oncogenes in tumorigenesis Nat Rev Cancer 11 2011 23 34
70. M. Nieborowska-Skorska, G. Hoser, P. Kossev, M.A. Wasik, and T. Skorski Complementary functions of the antiapoptotic protein A1 and serine/threonine kinase Pim-1 in the BCR/ABL-mediated leukemogenesis Blood 99 2002 4531 4539
71. T. Obata, M.B. Yaffe, G.G. Leparc, E.T. Piro, H. Maegawa, A. Kashiwagi, R. Kikkawa, and L.C. Cantley Peptide and protein library screening defines optimal substrate motifs for AKT/PKB J Biol Chem 275 2000 36108 36115
72. L.R. Pearce, D. Komander, and D.R. Alessi The nuts and bolts of AGC protein kinases Nat Rev Mol Cell Biol 11 2010 9 22
73. K.J. Peltola, K. Paukku, T.L. Aho, M. Ruuska, O. Silvennoinen, and P.J. Koskinen Pim-1 kinase inhibits STAT5-dependent transcription via its interactions with SOCS1 and SOCS3 Blood 103 2004 3744 3750
74. K.C. Qian, J. Studts, L. Wang, K. Barringer, A. Kronkaitis, C. Peng, A. Baptiste, R. LaFrance, S. Mische, and B. Farmer Expression, purification, crystallization and preliminary crystallographic analysis of human Pim-1 kinase Acta Crystallogr Sect F: Struct Biol Cryst Commun 61 2005 96 99
75. K.M. Quesnelle, A.L. Boehm, and J.R. Grandis STAT-mediated EGFR signaling in cancer J Cell Biochem 102 2007 311 319
76. E.M. Rainio, H. Ahlfors, K.L. Carter, M. Ruuska, S. Matikainen, E. Kieff, and P.J. Koskinen Pim kinases are upregulated during Epstein-Barr virus infection and enhance EBNA2 activity Virology 333 2005 201 206
77. C. Reiser-Erkan, M. Erkan, Z. Pan, S. Bekasi, N.A. Giese, S. Streit, C.W. Michalski, H. Friess, and J. Kleeff Hypoxia-inducible proto-oncogene Pim-1 is a prognostic marker in pancreatic ductal adenocarcinoma Cancer Biol Ther 7 2008 1352 1359
78. R.B. Robey, and N. Hay Is Akt the "Warburg kinase"? - Akt-energy metabolism interactions and oncogenesis Semin Cancer Biol 19 2009 25 31
79. D.D. Sarbassov, S.M. Ali, and D.M. Sabatini Growing roles for the mTOR pathway Curr Opin Cell Biol 17 2005 596 603
80. D.D. Sarbassov, D.A. Guertin, S.M. Ali, and D.M. Sabatini Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex Science 307 2005 1098 1101
81. C.J. Saris, J. Domen, and A. Berns The Pim-1 oncogene encodes two related protein-serine/threonine kinases by alternative initiation at AUG and CUG EMBO J 10 1991 655 664
82. G. Selten, H.T. Cuypers, M. Zijlstra, C. Melief, and A. Berns Involvement of c-myc in MuLV-induced T cell lymphomas in mice: frequency and mechanisms of activation EMBO J 3 1984 3215 3222
83. G.L. Semenza Targeting HIF-1 for cancer therapy Nat Rev Cancer 3 2003 721 732
84. S. Sengupta, T.R. Peterson, and D.M. Sabatini Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress Mol Cell 40 2010 310 322
85. N. Shah, B. Pang, K.G. Yeoh, S. Thorn, C.S. Chen, M.B. Lilly, and M. Salto-Tellez Potential roles for the PIM1 kinase in human cancer - a molecular and therapeutic appraisal Eur J Cancer 44 2008 2144 2151
86. K.P. Shay, Z. Wang, P.X. Xing, I.F. McKenzie, and N.S. Magnuson Pim-1 kinase stability is regulated by heat shock proteins and the ubiquitin-proteasome pathway Mol Cancer Res 3 2005 170 181
87. K. Shuai, and B. Liu Regulation of JAK-STAT signalling in the immune system Nat Rev Immunol 3 2003 900 911
88. J.H. Song, N. An, S. Chatterjee, E. Kistner-Griffin, S. Mahajan, S. Mehrotra, and A.S. Kraft Deletion of Pim kinases elevates the cellular levels of reactive oxygen species and sensitizes to K-Ras-induced cell killing Oncogene 2014 1 9
89. J.H. Song, and A.S. Kraft Pim kinase inhibitors sensitize prostate cancer cells to apoptosis triggered by Bcl-2 family inhibitor ABT-737 Cancer Res 72 2012 294 303
90. S.P. Staal Molecular cloning of the akt oncogene and its human homologues AKT1 and AKT2: amplification of AKT1 in a primary human gastric adenocarcinoma Proc Natl Acad Sci U S A 84 1987 5034 5037
91. A. Toker, and A.C. Newton Cellular signaling: pivoting around PDK-1 Cell 103 2000 185 188
92. M. van Lohuizen, S. Verbeek, P. Krimpenfort, J. Domen, C. Saris, T. Radaszkiewicz, and A. Berns Predisposition to lymphomagenesis in Pim-1 transgenic mice: cooperation with c-myc and N-myc in murine leukemia virus-induced tumors Cell 56 1989 673 682
93. S. Verbeek, M. van Lohuizen, M. van der Valk, J. Domen, G. Kraal, and A. Berns Mice bearing the E mu-myc and E mu-Pim-1 transgenes develop pre-B-cell leukemia prenatally Mol Cell Biol 11 1991 1176 1179
94. I. Vivanco, and C.L. Sawyers The phosphatidylinositol 3-kinase AKT pathway in human cancer Nat Rev Cancer 2 2002 489 501
95. Z. Wang, N. Bhattacharya, P.F. Mixter, W. Wei, J. Sedivy, and N.S. Magnuson Phosphorylation of the cell cycle inhibitor p21Cip1/WAF1 by Pim-1 kinase Biochim Biophys Acta 1593 2002 45 55
96. Z. Wang, M. Weaver, and N.S. Magnuson Cryptic promoter activity in the DNA sequence corresponding to the Pim-1 5′-UTR Nucleic Acids Res 33 2005 2248 2258
97. N.A. Warfel, and W.S. El-Deiry HIF-1 signaling in drug resistance to chemotherapy Curr Med Chem 21 2014 3021 3028
98. N.A. Warfel, M. Niederst, and A.C. Newton Disruption of the interface between the pleckstrin homology (PH) and kinase domains of Akt protein is sufficient for hydrophobic motif site phosphorylation in the absence of mTORC2 J Biol Chem 286 2011 39122 39129
99. G. Wernig, J.R. Gonneville, B.J. Crowley, M.S. Rodrigues, M.M. Reddy, H.E. Hudon, C. Walz, A. Reiter, K. Podar, Y. Royer, S.N. Constantinescu, M.H. Tomasson, J.D. Griffin, D.G. Gilliland, and M. Sattler The Jak2V617F oncogene associated with myeloproliferative diseases requires a functional FERM domain for transformation and for expression of the Myc and Pim proto-oncogenes Blood 111 2008 3751 3759
100. X. Xie, D. Zhang, B. Zhao, M.K. Lu, M. You, G. Condorelli, C.Y. Wang, and K.L. Guan IkappaB kinase epsilon and TANK-binding kinase 1 activate AKT by direct phosphorylation Proc Natl Acad Sci U S A 108 2011 6474 6479
101. Y. Xie, M. Burcu, D.E. Linn, Y. Qiu, and M.R. Baer Pim-1 kinase protects P-glycoprotein from degradation and enables its glycosylation and cell surface expression Mol Pharmacol 78 2010 310 318
102. Y. Xie, K. Xu, B. Dai, Z. Guo, T. Jiang, H. Chen, and Y. Qiu The 44 kDa Pim-1 kinase directly interacts with tyrosine kinase Etk/BMX and protects human prostate cancer cells from apoptosis induced by chemotherapeutic drugs Oncogene 25 2006 70 78
103. Y. Xie, K. Xu, D.E. Linn, X. Yang, Z. Guo, H. Shimelis, T. Nakanishi, D.D. Ross, H. Chen, L. Fazli, M.E. Gleave, and Y. Qiu The 44-kDa Pim-1 kinase phosphorylates BCRP/ABCG2 and thereby promotes its multimerization and drug-resistant activity in human prostate cancer cells J Biol Chem 283 2008 3349 3356
104. B. Yan, M. Zemskova, S. Holder, V. Chin, A. Kraft, P.J. Koskinen, and M. Lilly The PIM-2 kinase phosphorylates BAD on serine 112 and reverses BAD-induced cell death J Biol Chem 278 2003 45358 45367
105. M.T. Yip-Schneider, M. Horie, and H.E. Broxmeyer Transcriptional induction of Pim-1 protein kinase gene expression by interferon gamma and posttranscriptional effects on costimulation with steel factor Blood 85 1995 3494 3502
106. Z. Yu, X. Zhao, Y. Ge, T. Zhang, L. Huang, X. Zhou, L. Xie, J. Liu, and G. Huang A regulatory feedback loop between HIF-1alpha and PIM2 in HepG2 cells PLoS One 9 2014 e88301
107. M.Y. Zemskova, J.H. Song, B. Cen, J. Cerda-Infante, V.P. Montecinos, and A.S. Kraft Regulation of prostate stromal fibroblasts by the PIM1 protein kinase Cell Signal 27 2014 135 146
108. F. Zhang, Z.M. Beharry, T.E. Harris, M.B. Lilly, C.D. Smith, S. Mahajan, and A.S. Kraft PIM1 protein kinase regulates PRAS40 phosphorylation and mTOR activity in FDCP1 cells Cancer Biol Ther 8 2009 846 853
109. R. Zhang, D. Luo, R. Miao, L. Bai, Q. Ge, W.C. Sessa, and W. Min Hsp90-Akt phosphorylates ASK1 and inhibits ASK1-mediated apoptosis Oncogene 24 2005 3954 3963
110. Y. Zhang, Z. Wang, X. Li, and N.S. Magnuson Pim kinase-dependent inhibition of c-Myc degradation Oncogene 27 2008 4809 4819
111. Y. Zhang, Z. Wang, and N.S. Magnuson Pim-1 kinase-dependent phosphorylation of p21Cip1/WAF1 regulates its stability and cellular localization in H1299 cells Mol Cancer Res 5 2007 909 922
112. Y. Zhao, M.S. Hamza, H.S. Leong, C.B. Lim, Y.F. Pan, E. Cheung, K.C. Soo, and N.G. Iyer Kruppel-like factor 5 modulates p53-independent apoptosis through Pim1 survival kinase in cancer cells Oncogene 27 2008 1 8
113. B.P. Zhou, Y. Liao, W. Xia, B. Spohn, M.H. Lee, and M.C. Hung Cytoplasmic localization of p21Cip1/WAF1 by Akt-induced phosphorylation in HER-2/neu-overexpressing cells Nat Cell Biol 3 2001 245 252
114. B.P. Zhou, Y. Liao, W. Xia, Y. Zou, B. Spohn, and M.C. Hung HER-2/neu induces p53 ubiquitination via Akt-mediated MDM2 phosphorylation Nat Cell Biol 3 2001 973 982
115. N. Zhu, L.M. Ramirez, R.L. Lee, N.S. Magnuson, G.A. Bishop, and M.R. Gold CD40 signaling in B cells regulates the expression of the Pim-1 kinase via the NF-kappa B pathway J Immunol 168 2002 744 754
116. N. Zhukova Iu, M.G. Alekseeva, N.V. Zakharevich, A.A. Shtil, and V.N. Danilenko The Pim family of protein kinases: structure, functions and roles in hematopoietic malignancies Mol Biol 45 2011 755 764
117. A. Zippo, A. De Robertis, R. Serafini, and S. Oliviero PIM1-dependent phosphorylation of histone H3 at serine 10 is required for MYC-dependent transcriptional activation and oncogenic transformation Nat Cell Biol 9 2007 932 944