Direct binding of arsenic trioxide to AMPK and generation of inhibitory effects on acute myeloid leukemia precursors

Molecular Cancer Therapeutics

Volumn 14, Issue 1, 2015, Pages 202-212

  Beauchamp, Elspeth M ^a,b   Kosciuczuk, Ewa M ^a,b   Serrano, Ruth ^a,b   Nanavati, Dhaval ^a   Swindell, Elden P ^a,c,d   Viollet, Benoit ^e   O'Halloran, Thomas V ^a,c   Altman, Jessica K ^a,b   Platanias, Leonidas C ^a,b  

^a JESSE BROWN VA MEDICAL CENTER   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d Northwestern University   (United States)

^e INSTITUT COCHIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC TRIOXIDE; CYSTEINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; ANTINEOPLASTIC AGENT; ORGANOARSENIC DERIVATIVE; OXIDE; S6 KINASE; TARGET OF RAPAMYCIN KINASE;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DRUG PROTEIN BINDING; ENZYME INHIBITION; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TUMOR XENOGRAFT; ANIMAL; CELL PROLIFERATION; DRUG EFFECTS; DRUG SCREENING; HUMAN; LEUKEMIA, MYELOID, ACUTE; METABOLISM; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTINEOPLASTIC AGENTS; ARSENICALS; CELL LINE, TUMOR; CELL PROLIFERATION; HUMANS; LEUKEMIA, MYELOID, ACUTE; MICE; OXIDES; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84921311060     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-14-0665-T     Document Type: Article

References (54)

1. Waxman S, Anderson KC. History of the development of arsenic derivatives in cancer therapy. Oncologist 2001;6 Suppl 2:3-10.
2. Cohen MH, Hirschfeld S, Flamm Honig S, Ibrahim A, Johnson JR, O'Leary JJ, et al. Drug approval summaries: arsenic trioxide, tamoxifen citrate, anastrazole, paclitaxel, bexarotene. Oncologist 2001;6:4-11.
3. Platanias LC. Biological responses to arsenic compounds. J Biol Chem 2009;284:18583-7
4. Dilda PJ, Hogg PJ. Arsenical-based cancer drugs. Cancer Treat Rev 2007;33:542-64.
5. Ramadan D, Rancy PC, Nagarkar RP, Schneider JP, Thorpe C. Arsenic(III) species inhibit oxidative protein folding in vitro. Biochemistry 2009;48:424-32.
6. Swindell EP, Hankins PL, Chen H, Miodragovic DU, O'Halloran TV. Anticancer activity of small-molecule and nanoparticulate arsenic(III) complexes. Inorg Chem 2013;52:12292-304.
7. Nasr R, Guillemin MC, Ferhi O, Soilihi H, Peres L, Berthier C, et al. Eradication of acute promyelocytic leukemia-initiating cells through PML-RARA degradation. Nat Med 2008;14:1333-42.
8. Zhang XW, Yan XJ, Zhou ZR, Yang FF, Wu ZY, Sun HB, et al. Arsenic trioxide controls the fate of the PML-RARalpha oncoprotein by directly binding PML. Science 2010;328:240-3.
9. Goussetis DJ, Gounaris E, Wu EJ, Vakana E, Sharma B, Bogyo M, et al. Autophagic degradation of the BCR-ABL oncoprotein and generation of antileukemic responses by arsenic trioxide. Blood 2012;120:3555-62.
10. Shackelford D, Kenific C, Blusztajn A, Waxman S, Ren R. Targeted degradation of the AML1/MDS1/EVI1 oncoprotein by arsenic trioxide. Cancer Res 2006;66:11360-9.
11. Kapahi P, Takahashi T, Natoli G, Adams SR, Chen Y, Tsien RY, et al. Inhibition of NF-kappa B activation by arsenite through reaction with a critical cysteine in the activation loop of Ikappa B kinase. J Biol Chem 2000;275:36062-6.
12. Giafis N, Katsoulidis E, Sassano A, Tallman MS, Higgins LS, Nebreda AR, et al. Role of the p38 mitogen-activated protein kinase pathway in the generation of arsenic trioxide-dependent cellular responses. Cancer Res 2006;66:6763-71.
13. Dolniak B, Katsoulidis E, Carayol N, Altman JK, Redig AJ, Tallman MS, et al. Regulation of arsenic trioxide-induced cellular responses by Mnk1 and Mnk2. J Biol Chem 2008;283:12034-42.
14. Kannan-Thulasiraman P, Katsoulidis E, Tallman MS, Arthur JS, Platanias LC. Activation of the mitogen- and stress-activated kinase 1 by arsenic trioxide. J Biol Chem 2006;281:22446-52.
15. Verma A, Mohindru M, Deb DK, Sassano A, Kambhampati S, Ravandi F, et al. Activation of Rac1 and the p38 mitogen-activated protein kinase pathway in response to arsenic trioxide. J Biol Chem 2002;277:44988-95.
16. Goussetis DJ, Altman JK, Glaser H, McNeer JL, Tallman MS, Platanias LC. Autophagy is a critical mechanism for the induction of the antileukemic effects of arsenic trioxide. J Biol Chem 2010;285:29989-97.
17. Hayakawa F, Privalsky ML. Phosphorylation of PML by mitogen-activated protein kinases plays a key role in arsenic trioxide-mediated apoptosis. Cancer Cell 2004;5:389-401.
18. Galvin JP, Altman JK, Szilard A, Goussetis DJ, Vakana E, Sassano A, et al. Regulation of the kinase RSK1 by arsenic trioxide and generation of antileukemic responses. Cancer Biol Ther 2013;14:411-6.
19. Davison K, Mann KK, Waxman S, Miller WH Jr. JNK activation is amediator of arsenic trioxide-induced apoptosis in acute promyelocytic leukemia cells. Blood 2004;103:3496-502.
20. Mann KK, Davison K, Colombo M, Colosimo AL, Diaz Z, Padovani AM, et al. Antimony trioxide-induced apoptosis is dependent on SEK1/JNK signaling. Toxicol Lett 2006;160:158-70.
21. Redondo-Munoz J, Escobar-Diaz E, Hernandez Del Cerro M, Pandiella A, Terol MJ, Garcia-Marco JA, et al. Induction of B-chronic lymphocytic leukemia cell apoptosis by arsenic trioxide involves suppression of the phosphoinositide 3-kinase/Akt survival pathway via c-jun-NH2 terminal kinase activation and PTEN upregulation. Clin Cancer Res 2010;16:4382-91.
22. Beauchamp EM, Ringer L, Bulut G, Sajwan KP, Hall MD, Lee YC, et al. Arsenic trioxide inhibits human cancer cell growth and tumor development in mice by blocking Hedgehog/GLI pathway. J Clin Invest 2011;121:148-60.
23. Fei DL, Li H, Kozul CD, Black KE, Singh S, Gosse JA, et al. Activation of Hedgehog signaling by the environmental toxicant arsenic may contribute to the etiology of arsenic-induced tumors. Cancer Res 2010;70:1981-8.
24. Kim J, Lee JJ, Gardner D, Beachy PA. Arsenic antagonizes the Hedgehog pathway by preventing ciliary accumulation and reducing stability of the Gli2 transcriptional effector. Proc Natl Acad Sci U S A 2010;107:13432-7.
25. Carling D, Mayer FV, Sanders MJ, Gamblin SJ. AMP-activated protein kinase: nature's energy sensor. Nat Chem Biol 2011;7:512-8.
26. Woods A, Vertommen D, Neumann D, Turk R, Bayliss J, Schlattner U, et al. Identification of phosphorylation sites in AMP-activated protein kinase (AMPK) for upstream AMPK kinases and study of their roles by sitedirected mutagenesis. J Biol Chem 2003;278:28434-42.
27. Hawley SA, Davison M, Woods A, Davies SP, Beri RK, Carling D, et al. Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J Biol Chem 1996;271:27879-87.
28. Hurley RL, Anderson KA, Franzone JM, Kemp BE, Means AR, Witters LA. The Ca2+/Calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J Biol Chem 2005;280:29060-6.
29. Shaw RJ, Kosmatka M, Bardeesy N, Hurley RL, Witters LA, DePinho RA, et al. The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci U S A 2004;101:3329-35.
30. Davies SP, Carling D, Munday MR, Hardie DG. Diurnal rhythm of phosphorylation of rat liver acetyl-CoA carboxylase by the AMP-activated protein kinase, demonstrated using freeze-clamping. Effects of high fat diets. Eur J Biochem 1992;203:615-23.
31. Inoki K, Kim J, Guan KL. AMPK and mTOR in cellular energy homeostasis and drug targets. Annu Rev Pharmacol Toxicol 2012;52:381-400.
32. Egan D, Kim J, Shaw RJ, Guan KL. The autophagy initiating kinase ULK1 is regulated via opposing phosphorylation by AMPK and mTOR. Autophagy 2011;7:643-4.
33. Beauchamp EM, Platanias LC. The evolution of the TOR pathway and its role in cancer. Oncogene 2013;32:3923-32.
34. Altman JK, Yoon P, Katsoulidis E, Kroczynska B, Sassano A, Redig AJ, et al. Regulatory effects of mammalian target of rapamycin-mediated signals in the generation of arsenic trioxide responses. J Biol Chem 2008;283:1992-2001.
35. Zmijewski JW, Banerjee S, Bae H, Friggeri A, Lazarowski ER, Abraham E. Exposure to hydrogen peroxide induces oxidation and activation of AMP-activated protein kinase. J Biol Chem 2010;285:33154-64.
36. Laderoute KR, Amin K, Calaoagan JM, Knapp M, Le T, Orduna J, et al. 5′- AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Mol Cell Biol 2006;26:5336-47.
37. Moaddel R, Sharma A, Huseni T, Jones GS Jr, Hanson RN, Loring RH. Novel biotinylated phenylarsonous acids as bifunctional reagents for spatially close thiols: studies on reduced antibodies and the agonist binding site of reduced Torpedo nicotinic receptors. Bioconjug Chem 1999;10:629-37.
38. Zhang X, Yang F, Shim JY, Kirk KL, Anderson DE, Chen X. Identification of arsenic-binding proteins in human breast cancer cells. Cancer Lett 2007;255:95-106.
39. Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006;58:621-81.
40. Hurley RL, Barre LK, Wood SD, Anderson KA, Kemp BE, Means AR, et al. Regulation of AMP-activated protein kinase by multisite phosphorylation in response to agents that elevate cellular cAMP. J Biol Chem 2006;281:36662-72.
41. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, et al. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 2001;108:1167-74.
42. Roux PP, Shahbazian D, Vu H, Holz MK, Cohen MS, Taunton J, et al. RAS/ERK signaling promotes site-speci fic ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J Biol Chem 2007;282:14056-64.
43. Cool B, Zinker B, Chiou W, Kifle L, Cao N, Perham M, et al. Identification and characterization of a small molecule AMPK activator that treats key components of type 2 diabetes and the metabolic syndrome. Cell Metab 2006;3:403-16.
44. El-Mir MY, Nogueira V, Fontaine E, Averet N, Rigoulet M, Leverve X. Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. J Biol Chem 2000;275:223-8.
45. Kalender A, Selvaraj A, Kim SY, Gulati P, Brule S, Viollet B, et al. Metformin, independent of AMPK, inhibits mTORC1 in a rag GTPase-dependent manner. Cell Metab 2010;11:390-401.
46. Liu X, Chhipa RR, Pooya S, Wortman M, Yachyshin S, Chow LM, et al. Discrete mechanisms of mTOR and cell cycle regulation by AMPK agonists independent of AMPK. Proc Natl Acad Sci U S A 2014;111:E435-44.
47. Horman S, Vertommen D, Heath R, Neumann D, Mouton V, Woods A, et al. Insulin antagonizes ischemia-induced Thr172 phosphorylation of AMP-activated protein kinase alpha-subunits in heart via hierarchical phosphorylation of Ser485/491. J Biol Chem 2006;281:5335-40.
48. Soltys CL, Kovacic S, Dyck JR. Activation of cardiac AMP-activated protein kinase by LKB1 expression or chemical hypoxia is blunted by increased Akt activity. Am J Physiol Heart Circ Physiol 2006;290:H2472-9.
49. Cline DJ, Thorpe C, Schneider JP. Effects of As(III) binding on alpha-helical structure. J Am Chem Soc 2003;125:2923-9.
50. Wang X, Meng D, Chang Q, Pan J, Zhang Z, Chen G, et al. Arsenic inhibits neurite outgrowth by inhibiting the LKB1-AMPK signaling pathway. Environ Health Perspect 2010;118:627-34.
51. Liang J, Mills GB. AMPK: a contextual oncogene or tumor suppressor? Cancer Res 2013;73:2929-35.
52. Jeon SM, Chandel NS, Hay N. AMPK regulates NADPH homeostasis to promote tumour cell survival during energy stress. Nature 2012;485:661-5.
53. Green AS, Chapuis N, Maciel TT, Willems L, Lambert M, Arnoult C, et al. The LKB1/AMPK signaling pathway has tumor suppressor activity in acute myeloid leukemia through the repression of mTOR-dependent oncogenic mRNA translation. Blood 2010;116:4262-73.
54. Shackelford DB, Abt E, Gerken L, Vasquez DS, Seki A, Leblanc M, et al. LKB1 inactivation dictates therapeutic response of non-small cell lung cancer to the metabolism drug phenformin. Cancer Cell 2013;23:143-58.