Effector mechanisms of sunitinib-induced G1 cell cycle arrest, differentiation, and apoptosis in human acute myeloid leukaemia HL60 and KG-1 cells

Annals of Hematology

Volumn 92, Issue 3, 2013, Pages 301-313

  Teng, Chieh Lin Jerry ^a,b,c   Yu, Chang Tze Ricky ^d   Hwang, Wen Li ^a   Tsai, Jia Rong ^a   Liu, Hsiang Chun ^a   Hwang, Guang Yuh ^b   Hsu, Shih Lan ^a  

^a TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^b TUNGHAI UNIVERSITY   (Taiwan)

^c CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL CHI NAN UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Bcl 2; Differentiation; PKC; Sunitinib

Indexed keywords

CASPASE 2; CASPASE 3; CASPASE 8; CASPASE 9; CYCLIN D1; CYCLIN D3; CYCLIN DEPENDENT KINASE 2; DEATH RECEPTOR 4; DEATH RECEPTOR 5; FAS ANTIGEN; FAS LIGAND; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN MCL 1; PROTEIN P130; PROTEIN P27; PROTEIN PRB1; PUMA PROTEIN; SUNITINIB; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL SURFACE; CELL VIABILITY; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKEMIA CELL; LEUKEMIA CELL HL60; LEUKEMIA CELL KG1; MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL DIFFERENTIATION; G1 PHASE CELL CYCLE CHECKPOINTS; HL-60 CELLS; HUMANS; INDOLES; LEUKEMIA, MYELOID, ACUTE; PYRROLES; TREATMENT OUTCOME; TUMOR CELLS, CULTURED;

EID: 84873996482     PISSN: 09395555     EISSN: 14320584     Source Type: Journal    
DOI: 10.1007/s00277-012-1627-7     Document Type: Article

References (48)

1. Byrd JC, Mrozek K, Dodge RK, Carroll AJ, Edwards CG, Arthur DC, Pettenati MJ, Patil SR, Rao KW, Watson MS, Koduru PR, Moore JO, Stone RM, Mayer RJ, Feldman EJ, Davey FR, Schiffer CA, Larson RA, Bloomfield CD (2002) Pretreatment cytogenetic abnormalities are predictive of induction success, cumulative incidence of relapse, and overall survival in adult patients with de novo acute myeloid leukemia: results from Cancer and Leukemia Group B (CALGB 8461). Blood 100(13):4325-4336. doi: 10.1182/blood-2002-03-0772
2. Petrie K, Zelent A, Waxman S (2009) Differentiation therapy of acute myeloid leukemia: past, present and future. Curr Opin Hematol 16(2):84-91. doi: 10.1097/MOH.0b013e3283257aee
3. Sanz MA, Grimwade D, Tallman MS, Lowenberg B, Fenaux P, Estey EH, Naoe T, Lengfelder E, Buchner T, Dohner H, Burnett AK, Lo-Coco F (2009) Management of acute promyelocytic leukemia: recommendations from an expert panel on behalf of the European LeukemiaNet. Blood 113(9):1875-1891. doi: 10.1182/blood-2008-04- 150250
4. Estey E, Garcia-Manero G, Ferrajoli A, Faderl S, Verstovsek S, Jones D, Kantarjian H (2006) Use of all-trans retinoic acid plus arsenic trioxide as an alternative to chemotherapy in untreated acute promyelocytic leukemia. Blood 107(9):3469-3473. doi: 10.1182/blood-2005-10-4006
5. Mathews V, George B, Lakshmi KM, Viswabandya A, Bajel A, Balasubramanian P, Shaji RV, Srivastava VM, Srivastava A, Chandy M (2006) Single-agent arsenic trioxide in the treatment of newly diagnosed acute promyelocytic leukemia: durable remissions with minimal toxicity. Blood 107(7):2627-2632. doi: 10.1182/blood-2005-08-3532
6. Koeffler HP (2010) Is there a role for differentiating therapy in non-APL AML? Best Pract Res Clin Haematol 23(4):503-508. doi: 10.1016/j.beha.2010.09. 014
7. Chow LQ, Eckhardt SG (2007) Sunitinib: from rational design to clinical efficacy. J Clin Oncol 25(7):884-896. doi: 10.1200/JCO.2006.06.3602
8. Mena AC, Pulido EG, Guillen-Ponce C (2010) Understanding the molecular-based mechanism of action of the tyrosine kinase inhibitor: sunitinib. Anti-Cancer Drugs 21(Suppl 1):S3-S11. doi: 10.1097/01.cad.0000361534.44052.c5
9. O'Farrell AM, Abrams TJ, Yuen HA, Ngai TJ, Louie SG, Yee KW, Wong LM, Hong W, Lee LB, Town A, Smolich BD, Manning WC, Murray LJ, Heinrich MC, Cherrington JM (2003) SU11248 is a novel FLT3 tyrosine kinase inhibitor with potent activity in vitro and in vivo. Blood 101(9):3597-3605. doi: 10.1182/blood-2002-07-2307
10. Fiedler W, Serve H, Dohner H, Schwittay M, Ottmann OG, O'Farrell AM, Bello CL, Allred R, Manning WC, Cherrington JM, Louie SG, Hong W, Brega NM, Massimini G, Scigalla P, Berdel WE, Hossfeld DK (2005) A phase 1 study of SU11248 in the treatment of patients with refractory or resistant acute myeloid leukemia (AML) or not amenable to conventional therapy for the disease. Blood 105(3):986-993. doi: 10.1182/blood-2004-05-1846
11. Nishioka C, Ikezoe T, Yang J, Yokoyama A (2009) Sunitinib, an orally available receptor tyrosine kinase inhibitor, induces monocytic differentiation of acute myelogenous leukemia cells that is enhanced by 1,25-dihydroxyvitamin D(3). Leukemia 23(11):2171-2173. doi: 10.1038/leu.2009.152
12. Fenton MS, Marion KM, Salem AK, Hogen R, Naeim F, Hershman JM (2010) Sunitinib inhibits MEK/ERK and SAPK/JNK pathways and increases sodium/iodide symporter expression in papillary thyroid cancer. Thyroid 20(9):965-974. doi: 10.1089/thy.2010.0008
13. Ulukaya E, Acilan C, Yilmaz Y (2011) Apoptosis: why and how does it occur in biology? Cell Biochem Funct 29(6):468-480. doi: 10.1002/cbf.1774
14. Kelly PN, Strasser A (2011) The role of Bcl-2 and its pro-survival relatives in tumourigenesis and cancer therapy. Cell Death Differ 18(9):1414-1424. doi: 10.1038/cdd.2011.17
15. Miranda MB, Johnson DE (2007) Signal transduction pathways that contribute to myeloid differentiation. Leukemia 21(7):1363-1377. doi: 10.1038/sj.leu.2404690
16. Kelly LM, Gilliland DG (2002) Genetics of myeloid leukemias. Annu Rev Genom Hum Genet 3:179-198. doi: 10.1146/annurev.genom.3.032802.115046
17. Konopleva M, Tsao T, Ruvolo P, Stiouf I, Estrov Z, Leysath CE, Zhao S, Harris D, Chang S, Jackson CE, Munsell M, Suh N, Gribble G, Honda T, May WS, Sporn MB, Andreeff M (2002) Novel triterpenoid CDDO-Me is a potent inducer of apoptosis and differentiation in acute myelogenous leukemia. Blood 99(1):326-335
18. Lange C, Calegari F (2010) Cdks and cyclins link G1 length and differentiation of embryonic, neural and hematopoietic stem cells. Cell Cycle 9(10):1893-1900
19. Blomen VA, Boonstra J (2007) Cell fate determination during G1 phase progression. Cell Mol Life Sci CMLS 64(23):3084-3104. doi: 10.1007/s00018-007- 7271-z
20. Dyson N (1998) The regulation of E2F by pRB-family proteins. Genes Dev 12(15):2245-2262
21. Yang F, Jove V, Xin H, Hedvat M, Van Meter TE, Yu H (2010) Sunitinib induces apoptosis and growth arrest of medulloblastoma tumor cells by inhibiting STAT3 and AKT signaling pathways. Mol Cancer Res MCR 8(1):35-45. doi: 10.1158/1541-7786.MCR-09-0220
22. Tong W, Kiyokawa H, Soos TJ, Park MS, Soares VC, Manova K, Pollard JW, Koff A (1998) The absence of p27Kip1, an inhibitor of G1 cyclin-dependent kinases, uncouples differentiation and growth arrest during the granulosa->luteal transition. Cell Growth Differ 9(9):787-794
23. Dzikaite V, Kanopka A, Brock JH, Kazlauskas A, Melefors O (2000) A novel endoproteolytic processing activity in mitochondria of erythroid cells and the role in heme synthesis. Blood 96(2):740-746
24. Tamir A, Petrocelli T, Stetler K, Chu W, Howard J, Croix BS, Slingerland J, Ben-David Y (2000) Stem cell factor inhibits erythroid differentiation by modulating the activity of G1-cyclin-dependent kinase complexes: a role for p27 in erythroid differentiation coupled G1 arrest. Cell Growth Differ 11(5):269-277
25. Delehouzee S, Yoshikawa T, Sawa C, Sawada J, Ito T, Omori M, Wada T, Yamaguchi Y, Kabe Y, Handa H (2005) GABP, HCF-1 and YY1 are involved in Rb gene expression during myogenesis. Genes Cells 10(7):717-731. doi: 10.1111/j.1365-2443.2005.00873.x
26. Hansen JB, Jorgensen C, Petersen RK, Hallenborg P, De Matteis R, Boye HA, Petrovic N, Enerback S, Nedergaard J, Cinti S, te Riele H, Kristiansen K (2004) Retinoblastoma protein functions as a molecular switch determining white versus brown adipocyte differentiation. Proc Natl Acad Sci U S A 101(12):4112-4117. doi: 10.1073/pnas.0301964101
27. Garriga J, Limon A, Mayol X, Rane SG, Albrecht JH, Reddy EP, Andres V, Grana X (1998) Differential regulation of the retinoblastoma family of proteins during cell proliferation and differentiation. Biochem J 333(Pt 3):645-654
28. Thomas DM, Carty SA, Piscopo DM, Lee JS, Wang WF, Forrester WC, Hinds PW (2001) The retinoblastoma protein acts as a transcriptional coactivator required for osteogenic differentiation. Mol Cell 8(2):303-316
29. Paramio JM, Lain S, Segrelles C, Lane EB, Jorcano JL (1998) Differential expression and functionally co-operative roles for the retinoblastoma family of proteins in epidermal differentiation. Oncogene 17(8):949-957. doi: 10.1038/sj.onc.1202031
30. Galderisi U, Melone MA, Jori FP, Piegari E, Di Bernardo G, Cipollaro M, Cascino A, Peluso G, Claudio PP, Giordano A (2001) pRb2/p130 gene overexpression induces astrocyte differentiation. Mol Cell Neurosci 17(3):415-425. doi: 10.1006/mcne.2000.0949
31. Raschella G, Tanno B, Bonetto F, Negroni A, Claudio PP, Baldi A, Amendola R, Calabretta B, Giordano A, Paggi MG (1998) The RB-related gene Rb2/p130 in neuroblastoma differentiation and in B-myb promoter down-regulation. Cell Death Differ 5(5):401-407. doi: 10.1038/sj.cdd.4400359
32. Chen C, Wells AD (2007) Comparative analysis of E2F family member oncogenic activity. PLoS One 2(9):e912. doi: 10.1371/journal.pone.0000912
33. Meinhardt G, Roth J, Hass R (2000) Activation of protein kinase C relays distinct signaling pathways in the same cell type: differentiation and caspase-mediated apoptosis. Cell Death Differ 7(9):795-803. doi: 10.1038/sj.cdd.4400709
34. Macfarlane DE, Manzel L (1994) Activation of beta-isozyme of protein kinase C (PKC beta) is necessary and sufficient for phorbol ester-induced differentiation of HL-60 promyelocytes. Studies with PKC beta-defective PET mutant. J Biol Chem 269(6):4327-4331
35. Mischak H, Pierce JH, Goodnight J, Kazanietz MG, Blumberg PM, Mushinski JF (1993) Phorbol ester-induced myeloid differentiation is mediated by protein kinase C-alpha and -delta and not by protein kinase C-beta II, -epsilon, -zeta, and -eta. J Biol Chem 268(27):20110-20115
36. Noti JD, Reinemann BC, Johnson AK (2001) The leukocyte integrins are regulated by transcriptional and post-transcriptional mechanisms in a leukemic cell that overexpresses protein kinase C-zeta. Int J Oncol 19(6):1311-1318
37. Deshpande RV, Peterson RH, Moore MA (1997) Granulocyte colony-stimulating factor-induced activation of protein kinase-C in myeloid cells. J Cell Biochem 66(3):286-296
38. Schittenhelm MM, Yee KW, Tyner JW, McGreevey L, Haley AD, Town A, Griffith DJ, Bainbridge T, Braziel RM, O'Farrell AM, Cherrington JM, Heinrich MC (2006) FLT3 K663Q is a novel AML-associated oncogenic kinase: determination of biochemical properties and sensitivity to Sunitinib (SU11248). Leukemia 20(11):2008-2014. doi: 10.1038/sj.leu.2404374
39. Xin H, Zhang C, Herrmann A, Du Y, Figlin R, Yu H (2009) Sunitinib inhibition of Stat3 induces renal cell carcinoma tumor cell apoptosis and reduces immunosuppressive cells. Cancer Res 69(6):2506-2513. doi: 10.1158/0008-5472.CAN-08-4323
40. Nishioka C, Ikezoe T, Yang J, Takeshita A, Taniguchi A, Komatsu N, Togitani K, Koeffler HP, Yokoyama A (2008) Blockade of MEK/ERK signaling enhances sunitinib-induced growth inhibition and apoptosis of leukemia cells possessing activating mutations of the FLT3 gene. Leuk Res 32(6):865-872. doi: 10.1016/j.leukres.2007.09.017
41. Ping SY, Wu CL, Yu DS (2010) Sunitinib can enhance BCG mediated cytotoxicity to transitional cell carcinoma through apoptosis pathway. Urol Oncol. doi: 10.1016/j.urolonc.2010.07.001
42. Miller SC, Huang R, Sakamuru S, Shukla SJ, Attene-Ramos MS, Shinn P, Van Leer D, Leister W, Austin CP, Xia M (2010) Identification of known drugs that act as inhibitors of NF-kappaB signaling and their mechanism of action. Biochem Pharmacol 79(9):1272-1280. doi: 10.1016/j.bcp.2009.12.021
43. Sonpavde G, Jian W, Liu H, Wu MF, Shen SS, Lerner SP (2009) Sunitinib malate is active against human urothelial carcinoma and enhances the activity of cisplatin in a preclinical model. Urol Oncol 27(4):391-399. doi: 10.1016/j.urolonc.2008.03.017
44. Zwolak P, Jasinski P, Terai K, Gallus NJ, Ericson ME, Clohisy DR, Dudek AZ (2008) Addition of receptor tyrosine kinase inhibitor to radiation increases tumour control in an orthotopic murine model of breast cancer metastasis in bone. Eur J Cancer 44(16):2506-2517. doi: 10.1016/j.ejca.2008.07.011
45. Ikezoe T, Yang Y, Nishioka C, Bandobashi K, Nakatani H, Taguchi T, Koeffler HP, Taguchi H (2006) Effect of SU11248 on gastrointestinal stromal tumor-T1 cells: enhancement of growth inhibition via inhibition of 3-kinase/Akt/mammalian target of rapamycin signaling. Cancer Sci 97(9):945-951. doi: 10.1111/j.1349-7006.2006.00263.x
46. Guerin O, Formento P, Lo Nigro C, Hofman P, Fischel JL, Etienne-Grimaldi MC, Merlano M, Ferrero JM, Milano G (2008) Supra-additive antitumor effect of sunitinib malate (SU11248, Sutent) combined with docetaxel. A new therapeutic perspective in hormone refractory prostate cancer. J Cancer Res Clin Oncol 134(1):51-57. doi: 10.1007/s00432-007-0247-4
47. Yoon CY, Lee JS, Kim BS, Jeong SJ, Hong SK, Byun SS, Lee SE (2011) Sunitinib malate synergistically potentiates anti-tumor effect of gemcitabine in human bladder cancer cells. Korean J Urol 52(1):55-63. doi: 10.4111/kju.2011.52.1.55
48. Ding W, Cai T, Zhu H, Wu R, Tu C, Yang L, Lu W, He Q, Yang B (2010) Synergistic antitumor effect of TRAIL in combination with sunitinib in vitro and in vivo. Cancer Lett 293(2):158-166. doi: 10.1016/j.canlet.2010.01.005