AMPK Protects Leukemia-Initiating Cells in Myeloid Leukemias from Metabolic Stress in the Bone Marrow

Cell Stem Cell

Volumn 17, Issue 5, 2015, Pages 585-596

  Saito, Yusuke ^a   Chapple, Richard H ^a   Lin, Angelique ^a   Kitano, Ayumi ^a   Nakada, Daisuke ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

AML; AMPK; dietary restriction; DNA damage; glycolysis; leukemia initiating cells; metabolic stress; ROS

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE;

ACUTE MYELOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; CONTROLLED STUDY; DIET RESTRICTION; DNA DAMAGE; ENZYME INHIBITION; LEUKEMIA CELL; LEUKEMOGENESIS; METABOLIC STRESS; MOUSE; MYELOID LEUKEMIA; NONHUMAN; OXIDATIVE STRESS; PHYSIOLOGICAL STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; ACUTE MYELOID LEUKEMIA; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CANCER STEM CELL; DEFICIENCY; ENZYMOLOGY; KNOCKOUT MOUSE; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; SPLEEN;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BONE MARROW; DNA DAMAGE; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; NEOPLASTIC STEM CELLS; OXIDATIVE STRESS; SPLEEN;

EID: 84947749584     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2015.08.019     Document Type: Article

References (68)

1. A. Almeida, S. Moncada, and J.P. Bolaños Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2-kinase pathway Nat. Cell Biol. 6 2004 45 51
2. K. Barnes, J.C. Ingram, O.H. Porras, L.F. Barros, E.R. Hudson, L.G. Fryer, F. Foufelle, D. Carling, D.G. Hardie, and S.A. Baldwin Activation of GLUT1 by metabolic and osmotic stress: potential involvement of AMP-activated protein kinase (AMPK) J. Cell Sci. 115 2002 2433 2442
3. K. Birsoy, R. Possemato, F.K. Lorbeer, E.C. Bayraktar, P. Thiru, B. Yucel, T. Wang, W.W. Chen, C.B. Clish, and D.M. Sabatini Metabolic determinants of cancer cell sensitivity to glucose limitation and biguanides Nature 508 2014 108 112
4. B.R. Bochner, M. Siri, R.H. Huang, S. Noble, X.H. Lei, P.A. Clemons, and B.K. Wagner Assay of the multiple energy-producing pathways of mammalian cells PLoS ONE 6 2011 e18147
5. D. Bonnet, and J.E. Dick Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell Nat. Med. 3 1997 730 737
6. C. Bouchard, S. Lee, V. Paulus-Hock, C. Loddenkemper, M. Eilers, and C.A. Schmitt FoxO transcription factors suppress Myc-driven lymphomagenesis via direct activation of Arf Genes Dev. 21 2007 2775 2787
7. R.A. Cairns, I.S. Harris, and T.W. Mak Regulation of cancer cell metabolism Nat. Rev. Cancer 11 2011 85 95
8. R.J. Colman, R.M. Anderson, S.C. Johnson, E.K. Kastman, K.J. Kosmatka, T.M. Beasley, D.B. Allison, C. Cruzen, H.A. Simmons, J.W. Kemnitz, and et al. Caloric restriction delays disease onset and mortality in rhesus monkeys Science 325 2009 201 204
9. N.L. Curry, M. Mino-Kenudson, T.G. Oliver, O.H. Yilmaz, V.O. Yilmaz, J.Y. Moon, T. Jacks, D.M. Sabatini, and N.Y. Kalaany Pten-null tumors cohabiting the same lung display differential AKT activation and sensitivity to dietary restriction Cancer Discov. 3 2013 908 921
10. K. Deguchi, P.M. Ayton, M. Carapeti, J.L. Kutok, C.S. Snyder, I.R. Williams, N.C. Cross, C.K. Glass, M.L. Cleary, and D.G. Gilliland MOZ-TIF2-induced acute myeloid leukemia requires the MOZ nucleosome binding motif and TIF2-mediated recruitment of CBP Cancer Cell 3 2003 259 271
11. R.P. Ertl, J. Chen, C.M. Astle, T.M. Duffy, and D.E. Harrison Effects of dietary restriction on hematopoietic stem-cell aging are genetically regulated Blood 111 2008 1709 1716
12. B. Faubert, G. Boily, S. Izreig, T. Griss, B. Samborska, Z. Dong, F. Dupuy, C. Chambers, B.J. Fuerth, B. Viollet, and et al. AMPK is a negative regulator of the Warburg effect and suppresses tumor growth in vivo Cell Metab. 17 2013 113 124
13. B. Faubert, E.E. Vincent, M.C. Poffenberger, and R.G. Jones The AMP-activated protein kinase (AMPK) and cancer: many faces of a metabolic regulator Cancer Lett. 356 2 Pt A 2015 165 170
14. F. Ferrara, and C.A. Schiffer Acute myeloid leukaemia in adults Lancet 381 2013 484 495
15. C.J. Fox, P.S. Hammerman, and C.B. Thompson Fuel feeds function: energy metabolism and the T-cell response Nat. Rev. Immunol. 5 2005 844 852
16. S. Gurumurthy, S.Z. Xie, B. Alagesan, J. Kim, R.Z. Yusuf, B. Saez, A. Tzatsos, F. Ozsolak, P. Milos, F. Ferrari, and et al. The Lkb1 metabolic sensor maintains haematopoietic stem cell survival Nature 468 2010 659 663
17. J. Hao, J.N. Ho, J.A. Lewis, K.A. Karim, R.N. Daniels, P.R. Gentry, C.R. Hopkins, C.W. Lindsley, and C.C. Hong In vivo structure-activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors ACS Chem. Biol. 5 2010 245 253
18. D.G. Hardie, F.A. Ross, and S.A. Hawley AMPK: a nutrient and energy sensor that maintains energy homeostasis Nat. Rev. Mol. Cell Biol. 13 2012 251 262
19. Y. Hu, S. Swerdlow, T.M. Duffy, R. Weinmann, F.Y. Lee, and S. Li Targeting multiple kinase pathways in leukemic progenitors and stem cells is essential for improved treatment of Ph+ leukemia in mice Proc. Natl. Acad. Sci. USA 103 2006 16870 16875
20. B.J. Huntly, and D.G. Gilliland Leukaemia stem cells and the evolution of cancer-stem-cell research Nat. Rev. Cancer 5 2005 311 321
21. F. Ishikawa, S. Yoshida, Y. Saito, A. Hijikata, H. Kitamura, S. Tanaka, R. Nakamura, T. Tanaka, H. Tomiyama, N. Saito, and et al. Chemotherapy-resistant human AML stem cells home to and engraft within the bone-marrow endosteal region Nat. Biotechnol. 25 2007 1315 1321
22. S. Jäger, C. Handschin, J. St-Pierre, and B.M. Spiegelman AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha Proc. Natl. Acad. Sci. USA 104 2007 12017 12022
23. S.M. Jeon, and N. Hay The double-edged sword of AMPK signaling in cancer and its therapeutic implications Arch. Pharm. Res. 38 2015 346 357
24. S.M. Jeon, N.S. Chandel, and N. Hay AMPK regulates NADPH homeostasis to promote tumour cell survival during energy stress Nature 485 2012 661 665
25. N.Y. Kalaany, and D.M. Sabatini Tumours with PI3K activation are resistant to dietary restriction Nature 458 2009 725 731
26. H. Koike-Yusa, Y. Li, E.P. Tan, Mdel.C. Velasco-Herrera, and K. Yusa Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library Nat. Biotechnol. 32 2014 267 273
27. A. Kreso, and J.E. Dick Evolution of the cancer stem cell model Cell Stem Cell 14 2014 275 291
28. A.V. Krivtsov, and S.A. Armstrong MLL translocations, histone modifications and leukaemia stem-cell development Nat. Rev. Cancer 7 2007 823 833
29. A.V. Krivtsov, D. Twomey, Z. Feng, M.C. Stubbs, Y. Wang, J. Faber, J.E. Levine, J. Wang, W.C. Hahn, D.G. Gilliland, and et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9 Nature 442 2006 818 822
30. E.J. Kurth-Kraczek, M.F. Hirshman, L.J. Goodyear, and W.W. Winder 5′ AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle Diabetes 48 1999 1667 1671
31. E.D. Lagadinou, A. Sach, K. Callahan, R.M. Rossi, S.J. Neering, M. Minhajuddin, J.M. Ashton, S. Pei, V. Grose, K.M. O'Dwyer, and et al. BCL-2 inhibition targets oxidative phosphorylation and selectively eradicates quiescent human leukemia stem cells Cell Stem Cell 12 2013 329 341
32. T. Lapidot, C. Sirard, J. Vormoor, B. Murdoch, T. Hoang, J. Caceres-Cortes, M. Minden, B. Paterson, M.A. Caligiuri, and J.E. Dick A cell initiating human acute myeloid leukaemia after transplantation into SCID mice Nature 367 1994 645 648
33. M. Laplante, and D.M. Sabatini mTOR signaling in growth control and disease Cell 149 2012 274 293
34. J. Liang, and G.B. Mills AMPK: a contextual oncogene or tumor suppressor? Cancer Res. 73 2013 2929 2935
35. V.D. Longo, and L. Fontana Calorie restriction and cancer prevention: metabolic and molecular mechanisms Trends Pharmacol. Sci. 31 2010 89 98
36. N.J. MacIver, J. Blagih, D.C. Saucillo, L. Tonelli, T. Griss, J.C. Rathmell, and R.G. Jones The liver kinase B1 is a central regulator of T cell development, activation, and metabolism J. Immunol. 187 2011 4187 4198
37. A.S. Marsin, C. Bouzin, L. Bertrand, and L. Hue The stimulation of glycolysis by hypoxia in activated monocytes is mediated by AMP-activated protein kinase and inducible 6-phosphofructo-2-kinase J. Biol. Chem. 277 2002 30778 30783
38. E.J. Masoro Overview of caloric restriction and ageing Mech. Ageing Dev. 126 2005 913 922
39. J.A. Mattison, G.S. Roth, T.M. Beasley, E.M. Tilmont, A.M. Handy, R.L. Herbert, D.L. Longo, D.B. Allison, J.E. Young, M. Bryant, and et al. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study Nature 489 2012 318 321
40. M.M. Mihaylova, D.M. Sabatini, and O.H. Yilmaz Dietary and metabolic control of stem cell function in physiology and cancer Cell Stem Cell 14 2014 292 305
41. S.J. Morrison, and D.T. Scadden The bone marrow niche for haematopoietic stem cells Nature 505 2014 327 334
42. A.G. Muntean, and J.L. Hess The pathogenesis of mixed-lineage leukemia Annu. Rev. Pathol. 7 2012 283 301
43. K. Naka, T. Hoshii, T. Muraguchi, Y. Tadokoro, T. Ooshio, Y. Kondo, S. Nakao, N. Motoyama, and A. Hirao TGF-beta-FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia Nature 463 2010 676 680
44. D. Nakada, T.L. Saunders, and S.J. Morrison Lkb1 regulates cell cycle and energy metabolism in haematopoietic stem cells Nature 468 2010 653 658
45. S.J. Neering, T. Bushnell, S. Sozer, J. Ashton, R.M. Rossi, P.Y. Wang, D.R. Bell, D. Heinrich, A. Bottaro, and C.T. Jordan Leukemia stem cells in a genetically defined murine model of blast-crisis CML Blood 110 2007 2578 2585
46. C. Nombela-Arrieta, G. Pivarnik, B. Winkel, K.J. Canty, B. Harley, J.E. Mahoney, S.Y. Park, J. Lu, A. Protopopov, and L.E. Silberstein Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment Nat. Cell Biol. 15 2013 533 543
47. L.A. O'Neill, and D.G. Hardie Metabolism of inflammation limited by AMPK and pseudo-starvation Nature 493 2013 346 355
48. K.C. Patra, and N. Hay The pentose phosphate pathway and cancer Trends Biochem. Sci. 39 2014 347 354
49. W.S. Pear, J.P. Miller, L. Xu, J.C. Pui, B. Soffer, R.C. Quackenbush, A.M. Pendergast, R. Bronson, J.C. Aster, M.L. Scott, and D. Baltimore Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow Blood 92 1998 3780 3792
50. J.C. Rathmell, C.J. Fox, D.R. Plas, P.S. Hammerman, R.M. Cinalli, and C.B. Thompson Akt-directed glucose metabolism can prevent Bax conformation change and promote growth factor-independent survival Mol. Cell. Biol. 23 2003 7315 7328
51. Y. Saito, and D. Nakada The role of the Lkb1/AMPK pathway in hematopoietic stem cells and Leukemia Crit. Rev. Oncog. 19 2014 383 397
52. A. Schulze, and A.L. Harris How cancer metabolism is tuned for proliferation and vulnerable to disruption Nature 491 2012 364 373
53. D.B. Shackelford, and R.J. Shaw The LKB1-AMPK pathway: metabolism and growth control in tumour suppression Nat. Rev. Cancer 9 2009 563 575
54. D.B. Shackelford, E. Abt, L. Gerken, D.S. Vasquez, A. Seki, M. Leblanc, L. Wei, M.C. Fishbein, J. Czernin, P.S. Mischel, and R.J. Shaw LKB1 inactivation dictates therapeutic response of non-small cell lung cancer to the metabolism drug phenformin Cancer Cell 23 2013 143 158
55. T.C. Somervaille, and M.L. Cleary Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia Cancer Cell 10 2006 257 268
56. J.A. Spencer, F. Ferraro, E. Roussakis, A. Klein, J. Wu, J.M. Runnels, W. Zaher, L.J. Mortensen, C. Alt, R. Turcotte, and et al. Direct measurement of local oxygen concentration in the bone marrow of live animals Nature 508 2014 269 273
57. T. Suda, K. Takubo, and G.L. Semenza Metabolic regulation of hematopoietic stem cells in the hypoxic niche Cell Stem Cell 9 2011 298 310
58. S.M. Sykes, S.W. Lane, L. Bullinger, D. Kalaitzidis, R. Yusuf, B. Saez, F. Ferraro, F. Mercier, H. Singh, K.M. Brumme, and et al. AKT/FOXO signaling enforces reversible differentiation blockade in myeloid leukemias Cell 146 2011 697 708
59. Z. Tothova, R. Kollipara, B.J. Huntly, B.H. Lee, D.H. Castrillon, D.E. Cullen, E.P. McDowell, S. Lazo-Kallanian, I.R. Williams, C. Sears, and et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress Cell 128 2007 325 339
60. S. Wang, G.L. Dale, P. Song, B. Viollet, and M.H. Zou AMPKalpha1 deletion shortens erythrocyte life span in mice: role of oxidative stress J. Biol. Chem. 285 2010 19976 19985
61. T. Wang, J.J. Wei, D.M. Sabatini, and E.S. Lander Genetic screens in human cells using the CRISPR-Cas9 system Science 343 2014 80 84
62. Y.H. Wang, W.J. Israelsen, D. Lee, V.W. Yu, N.T. Jeanson, C.B. Clish, L.C. Cantley, M.G. Vander Heiden, and D.T. Scadden Cell-state-specific metabolic dependency in hematopoiesis and leukemogenesis Cell 158 2014 1309 1323
63. O. Warburg On the origin of cancer cells Science 123 1956 309 314
64. M.R. Warr, M. Binnewies, J. Flach, D. Reynaud, T. Garg, R. Malhotra, J. Debnath, and E. Passegué FOXO3A directs a protective autophagy program in haematopoietic stem cells Nature 494 2013 323 327
65. W.R. Wilson, and M.P. Hay Targeting hypoxia in cancer therapy Nat. Rev. Cancer 11 2011 393 410
66. N. Wu, B. Zheng, A. Shaywitz, Y. Dagon, C. Tower, G. Bellinger, C.H. Shen, J. Wen, J. Asara, T.E. McGraw, and et al. AMPK-dependent degradation of TXNIP upon energy stress leads to enhanced glucose uptake via GLUT1 Mol. Cell 49 2013 1167 1175
67. P.B. Yu, C.C. Hong, C. Sachidanandan, J.L. Babitt, D.Y. Deng, S.A. Hoyng, H.Y. Lin, K.D. Bloch, and R.T. Peterson Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism Nat. Chem. Biol. 4 2008 33 41
68. H. Zong, J.M. Ren, L.H. Young, M. Pypaert, J. Mu, M.J. Birnbaum, and G.I. Shulman AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation Proc. Natl. Acad. Sci. USA 99 2002 15983 15987