Targeting of GSK3β promotes imatinib-mediated apoptosis in quiescent CD34+ chronic myeloid leukemia progenitors, preserving normal stem cells

Blood

Volumn 119, Issue 10, 2012, Pages 2335-2345

  Reddiconto, Giovanni ^a   Toto, Claudia ^b   Palamà, Ilaria ^b   De Leo, Simone ^b   De Luca, Emanuela ^b   De Matteis, Serena ^b   Dini, Luciana ^b   Passerini, Carlo Gambacorti ^c   Di Renzo, Nicola ^a   Maffia, Michele ^b   Coluccia, Addolorata Maria Luce ^a,b  

^a VITO FAZZI HOSPITAL   (Italy)

^b UNIVERSITY OF SALENTO   (Italy)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; BCR ABL PROTEIN; BETA CATENIN; CCAAT ENHANCER BINDING PROTEIN ALPHA; CD34 ANTIGEN; CYCLIN D1; DASATINIB; GLYCOGEN SYNTHASE KINASE 3BETA; IMATINIB; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE P60; PROTEIN P27;

APOPTOSIS; ARTICLE; CANCER STEM CELL; CELLULAR DISTRIBUTION; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DRUG MECHANISM; DRUG SELECTIVITY; DRUG TARGETING; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; LEUKEMIA CELL; LEUKEMOGENESIS; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION;

EID: 84858032395     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-06-361261     Document Type: Article

References (48)

1. Glauche I, Moore K, Thielecke L, Horn K, Loeffler M, Roeder I. Stem cell proliferation and quiescence-two sides of the same coin. PLoS Comput Biol. 2009;5(7):e1000447.
2. Grimes CA, Jope RS. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog Neurobiol. 2001;65(4):391-426. (Pubitemid 32781670)
3. Huang J, Zhang Y, Bersenev A, et al. Pivotal role for glycogen synthase kinase-3 in hematopoietic stem cell homeostasis in mice. J Clin Invest. 2009;119(12):3519-3529.
4. Jia J, Amanai K,Wang G, Tang J,Wang B, Jiang J. Shaggy/GSK3 antagonizes Hedgehog signalling by regulating Cubitus interruptus. Nature. 2002; 416(6880):548-552. (Pubitemid 34288858)
5. Foltz DR, Santiago MC, Berechid BE, Nye JS. Glycogen synthase kinase-3beta modulates Notch signalling and stability. Curr Biol. 2002; 12(12):1006-1011. (Pubitemid 34703331)
6. Reya T, Duncan AW, Ailles L, et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature. 2003;423(6938):409-414. (Pubitemid 36626987)
7. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3 specific inhibitor. Nat Med. 2004;10(1):55-63. (Pubitemid 38524699)
8. Trowbridge JJ, Xenocostas A, Moon RT, Bhatia M. Glycogen synthase kinase-3 is an in vivo regulator of hematopoietic stem cell repopulation. Nat Med. 2006;12(1):89-98. (Pubitemid 43050082)
9. Birch NW, Zeleznik-Le NJ. Glycogen synthase kinase-3 and leukemia: restoring the balance. Cancer Cell. 2010;17(6):529-531.
10. Wang Z, Smith KS, Murphy M, Piloto O, Somervaille T, Cleary ML. Glycogen synthase kinase 3 in MLL leukaemia maintenance and targeted therapy. Nature. 2008;455(7217):1205- 1210.
11. Wang Z, Iwasaki M, Ficara F, et al. GSK-3 promotes conditional association of CREB and its co-activators with MEIS1 to facilitate HOX-mediated transcription and oncogenesis. Cancer Cell. 2010;17(6):597-608.
12. Rocques N, Abou Zeid N, Sii-Felice K, et al. GSK- 3-mediated phosphorylation enhances Maf-transforming activity. Mol Cell. 2007;28(4):584- 597.
13. Sloma I, Jiang X, Eaves AC, Eaves CJ. Insights into the stem cells of chronic myeloid leukemia. Leukemia. 2010;24(11):1823-1833.
14. Eaves AC, Barnett MJ, Ponchio L, Cashman JD, Petzer AL, Eaves CJ. Differences between normal and CML stem cells: potential targets for clinical exploitation. Stem Cells. 1998;16(suppl 1):77- 83.
15. Holyoake T, Jiang X, Eaves C, Eaves A. Isolation of a highly quiescent subpopulation of primitive leukemic cells in chronic myeloid leukemia. Blood. 1999;94(6):2056-2064. (Pubitemid 29430422)
16. Bhatia R, Munthe HA, Williams AD, Zhang F, Forman SJ, Slovak ML. Chronic myelogenous leukemia primitive hematopoietic progenitors demonstrate increased sensitivity to growth factor- induced proliferation and maturation. Exp Hematol. 2000;28(12):1401-1412. (Pubitemid 32013914)
17. Udomsakdi C, Eaves CJ, Swolin B, Reid DS, Barnett MJ, Eaves AC. Rapid decline of chronic myeloid leukemic cells in long-term culture due to a defect at the leukemic stem cell level. Proc Natl Acad Sci U S A. 1992;89:6192-6196.
18. Jamieson CH et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med. 2004;351:657- 667.
19. Abrahamsson AE, et al. Glycogen synthase kinase 3beta missplicing contributes to leukemia stem cell generation. Proc Natl Acad Sci U S A. 2009;106(10):3925-3929.
20. Coluccia AM, et al. Bcr-Abl stabilizes beta-catenin in chronic myeloid leukemia through its tyrosine phosphorylation. EMBO J. 2007;26(5):1456- 1466.
21. Barnes DJ, Melo JV. Primitive, quiescent and difficult to kill: the role of non-proliferating stem cells in chronic myeloid leukemia. Cell Cycle. 2006;5: 2862-2866. (Pubitemid 44953936)
22. Holtz MS, Slovak ML, Zhang F, Sawyers CL, Forman SJ, Bhatia R. Imatinib mesylate (STI571) inhibits growth of primitive malignant progenitors in chronic myelogenous leukemia through reversal of abnormally increased proliferation. Blood. 2002;99(10):3792-3800. (Pubitemid 34534553)
23. Bhatia R, et al. Persistence of malignant hematopoietic progenitors in chronic myelogenous leukemia patients in complete cytogenetic remission following imatinib mesylate treatment. Blood. 2003;101(12):4701-4707. (Pubitemid 36857723)
24. Corbin AS, Agarwal A, Loriaux M, Cortes J, Deininger MW, Druker BJ. Human chronic myeloid leukemia stem cells are insensitive to imatinib despite inhibition of BCR-ABL activity. J Clin Invest. 2011;121(1):396-409.
25. Biederbick A, Kern HF, Elsässer HP. Monodansyl-cadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur J Cell Biol. 1995;66(1): 3-14.
26. Petzer AL, Hogge DE, Landsdorp PM, Reid DS, Eaves CJ. Self-renewal of primitive human hematopoietic cells (long-term-culture-initiating cells) in vitro and their expansion in defined medium. Proc Natl Acad Sci U S A. 1996;93(4):1470-1474.
27. Zandstra PW, Conneally E, Petzer AL, Piret JM, Eaves CJ. Cytokine manipulation of primitive human hematopoietic cell self-renewal. Proc Natl Acad Sci U S A. 1997;94(9):4698-4703.
28. Chu S, Li L, Singh H, Bhatia R. BCR-tyrosine 177 plays an essential role in Ras and AKT activation in human hematopoietic progenitor transformation in chronic myelogenous leukemia. Cancer Res. 2007;67(14):7045-7053. (Pubitemid 47105554)
29. Chu S, Holtz M, Gupta M, Bhatia R. BCR/ABL kinase inhibition by imatinib mesylate enhances MAP kinase activity in chronic myelogenous leukemia CD34+ cells. Blood. 2004;103(8):3167- 3174.
30. Samanta AK, Lin H, Sun T, Kantarjian H, Arlinghaus RB. Janus kinase 2: a critical target in chronic myelogenous leukemia. Cancer Res. 2006;66(13):6468-6472. (Pubitemid 44085597)
31. Talpaz M, Shah NP, Kantarjian H. Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias. N Engl J Med. 2006;354(24): 2531-2541. (Pubitemid 43882349)
32. Copland M, et al. Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML but does not eliminate the quiescent fraction. Blood. 2006;107(11):4532-4539. (Pubitemid 43801382)
33. Konig H, Copland M, Chu S, Jove R, Holyoake T, Bhatia R. Effects of Dasatinib on Src kinase activity and downstream intracellular signalling in primitive chronic myelogenous leukemia hematopoietic cells. Cancer Res. 2008;68(23):9624- 9633.
34. Sheng Z, Ma L, Sun JE, Zhu LJ, Green MR. BCR-ABL suppresses autophagy through ATF5- mediated regulation of mTOR transcription. Blood. 2011;118(10):2840-2848.
35. Bellodi C, Lidonnici MR, Hamilton A, et al. Targeting autophagy potentiates tyrosine kinase inhibitor-induced cell death in Philadelphia chromosome-positive cells, including primary CML stem cells. J Clin Invest. 2009;119(5):1109- 1123.
36. Dajani R, Fraser E, Roe SM, et al. Crystal structure of glycogen synthase kinase 3 beta: structural basis for phosphate-primed substrate specificity and autoinhibition. Cell. 2001;105(6):721- 732.
37. Cole A, Frame S, Cohen P. Further evidence that the tyrosine phosphorylation of glycogen synthase kinase-3 (GSK3) in mammalian cells is an autophosphorylation event. Biochem J. 2004; 377(pt 1):249-255. (Pubitemid 38114452)
38. Hartigan JA, Xiong WC, Johnson GV. Glycogen synthase kinase 3beta is tyrosine phosphorylated by PYK2. Biochem Biophys Res Commun. 2001; 284(2):485-489. (Pubitemid 32918003)
39. Takahashi-Yanaga F, Shiraishi F, Hirata M, Miwa Y, Morimoto S, Sasaguri T. Glycogen synthase kinase-3beta is tyrosine-phosphorylated by MEK1 in human skin fibroblasts. Biochem Biophys Res Commun. 2004;316(2):411-415. (Pubitemid 38338608)
40. Lesort M, Jope RS, Johnson GV. Insulin transiently increases tau phosphorylation: involvement of glycogen synthase kinase-3beta and Fyn tyrosine kinase. J Neurochem. 1999;72(2):576- 584.
41. Naka K, Hoshii T, Muraguchi T, et al. TGF-beta- FOXO signalling maintains leukaemiainitiating cells in chronic myeloid leukaemia. Nature. 2010;463(7281):676-680.
42. Bechard M, Dalton S. Subcellular localization of glycogen synthase kinase 3beta controls embryonic stem cell self-renewal. Mol Cell Biol. 2009; 29(8):2092-2104.
43. Meares GP, Jope RS. Resolution of the nuclear localization mechanism of glycogen synthase kinase-3: functional effects in apoptosis. J Biol Chem. 2007;282(23):16989-17001. (Pubitemid 47093248)
44. Bhat RV, Shanley J, Correll MP, et al. Regulation and localization of tyrosine216 phosphorylation of glycogen synthase kinase-3beta in cellular and animal models of neuronal degeneration. Proc Natl Acad Sci U S A. 2000;97(20):11074-11079.
45. Chu S, McDonald T, Bhatia R. Role of BCR-ABL-Y177- mediated p27kip1 phosphorylation and cytoplasmic localization in enhanced proliferation of chronic myeloid leukemia progenitors. Leukemia. 2010;24:779-787.
46. Zhao F, et al. Imatinib resistance associated with BCR-ABL upregulation is dependent on HIF- 1alpha-induced metabolic reprograming. Oncogene. 2010;29:2962-2972.
47. Breccia M, Muscaritoli M, Cannella L, Loglisci G, Santopietro M, Alimena G. Modifications of fasting glucose values as first sign of resistance in chronic myeloid leukemia chronic phase patients during imatinib treatment. Leuk Res. 2010;34(5): e122-e124.
48. Breccia M, Muscaritoli M, Cannella L, Stefanizzi C, Frustaci A, Alimena G. Fasting glucose improvement under dasatinib treatment in an accelerated phase chronic myeloid leukemia patient unresponsive to imatinib and nilotinib. Leuk Res. 2008;32(10):1626-1628.