Dual role of hematopoietic progenitor kinase 1 (HPK1) as a positive regulator of 1α,25-dihydroxyvitamin D-induced differentiation and cell cycle arrest of AML cells and as a mediator of vitamin D resistance

Cell Cycle

Volumn 11, Issue 7, 2012, Pages 1364-1373

  Chen Deutsch, Xiangwen ^a   Studzinski, George P ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

AML differentiation; Caspase inhibition; Cell cycle arrest; Differentiation resistance; HPK1; Signaling pathways; Vitamin D

Indexed keywords

1,25 DIHYDROXYERGOCALCIFEROL; 4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CARNOSIC ACID; CASPASE INHIBITOR; HEMATOPOIETIC CELL KINASE; HEMATOPOIETIC PROGENITOR KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 4; UNCLASSIFIED DRUG; VITAMIN D;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRAIN HL 60; CELL STRAIN U937; ENZYME ACTIVITY; ENZYME INDUCTION; HUMAN; LEUKEMIA CELL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION;

EID: 84860322664     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.19765     Document Type: Article

References (58)

1. Nowak D, Stewart D, Koeffler HP. Differentiation therapy of leukemia: 3 decades of development. Blood 2009; 113:3655-65; PMID:19221035; http://dx.doi. org/10.1182/blood-2009-01-198911.
2. Miyaura C, Abe E, Kuribayashi T, Tanaka H, Konno K, Nishii Y, et al. 1Alpha,25-Dihydroxyvitamin D3 induces differentiation of human myeloid leukemia cells. Biochem Biophys Res Commun 1981; 102:937-43; PMID:6946774; http://dx.doi.org/10.1016/0006-291X(81)91628-4.
3. Koeffler HP. Induction of differentiation of human acute myelogenous leukemia cells: therapeutic implications. Blood 1983; 62:709-21; PMID:6192859.
4. Huang ME, Ye YC, Chen SR, Chai JR, Lu JX, Zhoa L, et al. Use of all-trans retinoic acid in the treatment of acute promyelocytic leukemia. Blood 1988; 72:567-72; PMID:3165295.
5. Castaigne S, Chomienne C, Daniel MT, Ballerini P, Berger R, Fenaux P, et al. All-trans retinoic acid as a differentiation therapy for acute promyelocytic leukemia. I. Clinical results. Blood 1990; 76:1704-9; PMID:2224119.
6. Raffoux E, Cras A, Recher C, Boëlle PY, de Labarthe A, Turlure P, et al. Phase 2 clinical trial of 5-azacitidine, valproic acid, and all-trans retinoic acid in patients with high-risk acute myeloid leukemia or myelodysplastic syndrome. Oncotarget 2010; 1:34-42; PMID:21293051.
7. Deeb KK, Trump DL, Johnson CS. Vitamin D signalling pathways in cancer: potential for anticancer therapeutics. Nat Rev Cancer 2007; 7:684-700; PMID:17721433; http://dx.doi.org/10.1038/nrc2196.
8. Trump DL, Deeb KK, Johnson CS. Vitamin D: considerations in the continued development as an agent for cancer prevention and therapy. Cancer J 2010; 16:1-9; PMID:20164683; http://dx.doi.org/10.1097/PPO.0b013e3181c51ee6.
9. Wajchmann HJ, Rathod B, Song S, Xu H, Wang X, Uskokovic MR, et al. Loss of deoxcytidine kinase expression and tetraploidization of HL60 cells following long-term culture in 1,25-dihydroxyvitamin D3. Exp Cell Res 1996; 224:312-22; PMID:8612708; http://dx.doi.org/10.1006/excr.1996.0141.
10. 1 phase. Oncogene 1998; 16:2729-37; PMID:9652739; http:// dx.doi.org/10.1038/sj.onc.1201803.
11. 1 block but not differentiation of HL60 cells. Leukemia 1998; 12:1256-65; PMID:9697881; http://dx.doi.org/10.1038/sj.leu.2401088.
12. Garay E, Donnelly R, Wang X, Studzinski GP. Resistance to 1,25D-induced differentiation in human acute myeloid leukemia HL60-40AF cells is associated with reduced transcriptional activity and nuclear localization of the vitamin D receptor. J Cell Physiol 2007; 213:816-25; PMID:17520689; http://dx.doi.org/10. 1002/jcp.21150.
13. Chen-Deutsch X, Garay E, Zhang J, Harrison JS, Studzinski GP. c-Jun N-terminal kinase 2 (JNK2) antagonizes the signaling of differentiation by JNK1 in human myeloid leukemia cells resistant to vitamin D. Leuk Res 2009; 33:1372-8; PMID:19339050; http://dx.doi.org/10.1016/j.leukres.2009.03.003.
14. Marcinkowska E, Wiedlocha A, Radzikowski C. Evidence that phosphatidylinositol-3-kinase and p70S6K protein are involved in differentiation of HL-60 cells induced by calcitriol. Anticancer Res 1998; 18:3507-14; PMID:9858932.
15. 3 and participates in its anti-apoptotic effect and cell cycle control in differentiating HL60 cells. Cell Cycle 2006; 5:447-51; PMID:16479173; http://dx.doi.org/10.4161/cc.5.4.2467.
16. 3 and bryostatin-1 synergize to induce monocytic differentiation of NB4 acute promyelocytic leukemia cells by modulating cell cycle progression. Exp Cell Res 2004; 294:301-11; PMID:14980523; http://dx.doi.org/10.1016/j.yexcr. 2003.11.013.
17. 3-1alpha-hydroxylase in human monocytes. J Bone Miner Res 2006; 21:37-47; PMID:16355272; http://dx.doi.org/10.1359/JBMR.050908.
18. Hughes PJ, Brown G. 1Alpha,25- dihydroxyvitamin D3-mediated stimulation of steroid sulphatase activity in myeloid leukaemic cell lines requires VDRnuc-mediated activation of the RAS/ RAF/ERK-MAP kinase signalling pathway. J Cell Biochem 2006; 98:590-617; PMID:16440327; http:// dx.doi.org/10.1002/jcb. 20787.
19. Altman JK, Sassano A, Platanias LC. Targeting mTOR for the treatment of AML. New agents and new directions. Oncotarget 2011; 2:510-7; PMID:21680954.
20. Yu WD, Ma Y, Flynn G, Muindi JR, Kong RX, Trump DL, et al. Calcitriol enhances gemcitabine anti-tumor activity in vitro and in vivo by promoting apoptosis in a human pancreatic carcinoma model system. Cell Cycle 2010; 9:3022-9; PMID:20699664; http://dx.doi.org/10.4161/cc.9.15.12381.
21. Narayanan R, Sepulveda VA, Falzon M, Weigel NL. The functional consequences of cross-talk between the vitamin D receptor and ERK signaling pathways are cell-specific. J Biol Chem 2004; 279:47298-310; PMID:15331595; http://dx.doi.org/10.1074/jbc.M404101200.
22. Shah S, Islam MN, Dakshanamurthy S, Rizvi I, Rao M, Herrell R, et al. The molecular basis of vitamin D receptor and betacatenin crossregulation. Mol Cell 2006; 21:799-809; PMID:16543149; http://dx.doi.org/10.1016/j.molcel.2006.01. 037.
23. Studzinski GP, Wang X, Ji Y, Wang Q, Zhang Y, Kutner A, et al. The rationale for deltanoids in therapy for myeloid leukemia: role of KSR-MAPK-C/EBP pathway. J Steroid Biochem Mol Biol 2005; 97:47-55; PMID:16046262; http://dx.doi.org/10.1016/j.jsbmb.2005.06.010.
24. Wang Q, Harrison JS, Uskokovic M, Kutner A, Studzinski GP. Translational study of vitamin D differentiation therapy of myeloid leukemia: effects of the combination with a p38 MAPK inhibitor and an antioxidant. Leukemia 2005; 19:1812-7; PMID:16107889; http://dx.doi.org/10.1038/sj.leu.2403916.
25. 3. Exp Cell Res 2011; 317:117-30; PMID:20804750; http://dx.doi.org/10.1016/j.yexcr.2010.08.010.
26. 3 contributes to increased expression of p35 activator of cyclindependent kinase 5 and consequent onset of the terminal phase of HL60 cell differentiation. Cancer Res 2004; 64:5425-33; PMID:15289351; http://dx.doi. org/10.1158/0008-5472.CAN-04-0806.
27. 3. Cancer Res 2006; 66:4402-9; PMID:16618766; http://dx.doi.org/10.1158/0008-5472.CAN-05-3109.
28. 3. Exp Cell Res 2006; 312:2054-65; PMID:16624284; http://dx.doi.org/10.1016/j.yexcr.2006.03.003.
29. Jones JE, Wang L, Kropf PL, Duan R, Johnson DE. Src family kinase gene targets during myeloid differentiation: identification of the EGR-1 gene as a direct target. Leukemia 2009; 23:1933-5; PMID:19494839; http://dx.doi.org/10. 1038/leu.2009.118.
30. Geest CR, Coffer PJ. MAPK signaling pathways in the regulation of hematopoiesis. J Leukoc Biol 2009; 86:237-50; PMID:19498045; http://dx.doi.org/10.1189/jlb.0209097.
31. Hu MC, Qiu WR, Wang X, Meyer CF, Tan TH. Human HPK1, a novel human hematopoietic progenitor kinase that activates the JNK/SAPK kinase cascade. Genes Dev 1996; 10:2251-64; PMID:8824585; http://dx.doi.org/10.1101/gad.10.18. 2251.
32. Kiefer F, Tibbles LA, Anafi M, Janssen A, Zanke BW, Lassam N, et al. HPK1, a hematopoietic protein kinase activating the SAPK/JNK pathway. EMBO J 1996; 15:7013-25; PMID:9003777.
33. Arnold R, Frey CR, Müller W, Brenner D, Krammer PH, Kiefer F. Sustained JNK signaling by proteolytically processed HPK1 mediates IL-3 independent survival during monocytic differentiation. Cell Death Differ 2007; 14:568-75; PMID:17024227; http://dx.doi.org/10.1038/sj.cdd.4402042.
34. Chen YR, Meyer CF, Ahmed B, Yao Z, Tan TH. Caspase-mediated cleavage and functional changes of hematopoietic progenitor kinase 1 (HPK1). Oncogene 1999; 18:7370-7; PMID:10602493; http://dx.doi. org/10.1038/sj.onc.1203116.
35. Brenner D, Golks A, Becker M, Müller W, Frey CR, Novak R, et al. Caspase-cleaved HPK1 induces CD95L-independent activation-induced cell death in T and B lymphocytes. Blood 2007; 110:3968-77; PMID:17712048; http://dx.doi.org/10.1182/blood-2007-01-071167.
36. Caserta TM, Smith AN, Gultice AD, Reedy MA, Brown TL. Q-VD-OPh, a broad spectrum caspase inhibitor with potent antiapoptotic properties. Apoptosis 2003; 8:345-52; PMID:12815277; http://dx.doi.org/10.1023/A:1024116916932.
37. Fuchs Y, Steller H. Programmed cell death in animal development and disease. Cell 2011; 147:742-58; PMID:22078876; http://dx.doi.org/10.1016/j.cell. 2011.10.033.
38. Alvarez-Díaz S, Larriba MJ, López-Otín C, Muñoz A. Vitamin D: Proteases, protease inhibitors and cancer. Cell Cycle 2010; 9:32-7; PMID:20016282; http://dx.doi.org/10.4161/cc.9.1.10266.
39. Koeffler HP, Billing R, Lusis AJ, Sparkes R, Golde DW. An undifferentiated variant derived from the human acute myelogenous leukemia cell line (KG-1). Blood 1980; 56:265-73; PMID:6967340.
40. Wang H, Song X, Logsdon C, Zhou G, Evans DB, Abbruzzese JL, et al. Proteasome-mediated degradation and functions of hematopoietic progenitor kinase 1 in pancreatic cancer. Cancer Res 2009; 69:1063-70; PMID:19141650; http://dx.doi.org/10.1158/0008-5472.CAN-08-1751.
41. Han A, Saijo K, Mecklenbräuker I, Tarakhovsky A, Nussenzweig MC. Bam32 links the B cell receptor to ERK and JNK and mediates B cell proliferation but not survival. Immunity 2003; 19:621-32; PMID:14563325; http://dx.doi.org/ 10.1016/S1074-7613(03)00275-9.
42. Liu SK, Smith CA, Arnold R, Kiefer F, McGlade CJ. The adaptor protein Gads (Grb2-related adaptor downstream of Shc) is implicated in coupling hemopoietic progenitor kinase-1 to the activated TCR. J Immunol 2000; 165:1417-26; PMID:10903746.
43. Yu J, Riou C, Davidson D, Minhas R, Robson JD, Julius M, et al. Synergistic regulation of immunoreceptor signaling by SLP-76-related adaptor Clnk and serine/threonine protein kinase HPK-1. Mol Cell Biol 2001; 21:6102-12; PMID:11509653; http://dx.doi. org/10.1128/MCB.21.18.6102-6112.2001.
44. Tsuji S, Okamoto M, Yamada K, Okamoto N, Goitsuka R, Arnold R, et al. B cell adaptor containing src homology 2 domain (BASH) links B cell receptor signaling to the activation of hematopoietic progenitor kinase 1. J Exp Med 2001; 194:529-39; PMID:11514608; http://dx.doi.org/10.1084/jem.194.4.529.
45. Li T, Yu XJ, Zhang GY. Tyrosine phosphorylation of HPK1 by activated Src promotes ischemic brain injury in rat hippocampal CA1 region. FEBS Lett 2008; 582:1894-900; PMID:18498770; http://dx.doi. org/10.1016/j.febslet.2008.05.009.
46. 3 in human leukemia HL60 cells through a vitamin D response element in the 5′-flanking region. Oncogene 2006; 25:7078-85; PMID:16732322; http://dx.doi.org/10.1038/sj.onc.1209697
47. Wang X, Wang TT, White JH, Studzinski GP. Expression of human kinase suppressor of Ras 2 (hKSR-2) gene in HL60 leukemia cells is directly upregulated by 1,25-dihydroxyvitamin D(3) and is required for optimal cell differentiation. Exp Cell Res 2007; 313:3034-45; PMID:17599832; http://dx.doi. org/10.1016/j.yexcr.2007.05.021.
48. Schlesinger TK, Fanger GR, Yujiri T, Johnson GL. The TAO of MEKK. Front Biosci 1998; 3:1181-6; PMID:9820741.
49. Kasukabe T, Okabe-Kado J, Hozumi M, Honma Y. Inhibition by interleukin 4 of leukemia inhibitory factor-, interleukin 6- and dexamethasone-induced differentiation of mouse myeloid leukemia cells: role of c-myc and junB proto-oncogenes. Cancer Res 1994; 54:592-7; PMID:8275499.
50. Hong S, Skaist AM, Wheelan SJ, Friedman AD. AP-1 protein induction during monopoiesis favors C/EBP: AP-1 heterodimers over C/EBP homodimerization and stimulates FosB transcription. J Leukoc Biol 2011; 90:643-51; PMID:21543584; http://dx.doi. org/10.1189/jlb.0111043.
51. Paz-Priel I, Friedman A. C/EBPα dysregulation in AML and ALL. Crit Rev Oncog 2011; 16:93-102; PMID:22150310.
52. 3 activate three MAPK pathways and upregulate pRb expression in differentiating HL60 cells. Cell Cycle 2002; 1:410-5; PMID:12548017; http://dx.doi.org/10.4161/cc.1.6.269.
53. Kip1 concomitant with enhancement of differentiation and cell cycle arrest induced by silibinin and 1,25-dihydroxyvitamin D(3). Cell Cycle 2010; 9:4542-51; PMID:21084834; http://dx.doi.org/10.4161/cc.9.22.13790.
54. Kip1 in human myeloid leukemia cells induced to differentiate by 1,25-dihydroxyvitamin D3. Cell Cycle 2009; 8:736-41; PMID:19221487; http://dx.doi.org/10.4161/cc.8.5.7870.
55. Boomer JS, Tan TH. Functional interactions of HPK1 with adaptor proteins. J Cell Biochem 2005; 95:34-44; PMID:15770651; http://dx.doi.org/10.1002/jcb. 20401.
56. Arnold R, Liou J, Drexler HC, Weiss A, Kiefer F. Caspase-mediated cleavage of hematopoietic progenitor kinase 1 (HPK1) converts an activator of NFkappaB into an inhibitor of NFkappaB. J Biol Chem 2001; 276:14675-84; PMID:11278403; http://dx.doi. org/10.1074/jbc.M008343200.
57. Brenner D, Golks A, Kiefer F, Krammer PH, Arnold R. Activation or suppression of NFkappaB by HPK1 determines sensitivity to activation-induced cell death. EMBO J 2005; 24:4279-90; PMID:16341093; http://dx.doi.org/10.1038/ sj.emboj.7600894.
58. 3 correlates with reduced rate of maturation of DNA replication intermediates. Cancer Res 1991; 51:3451-5; PMID:2054784.