Arachidonate 15-lipoxygenase is required for chronic myeloid leukemia stem cell survival

Journal of Clinical Investigation

Volumn 124, Issue 9, 2014, Pages 3847-3862

  Chen, Yaoyu ^a,f   Peng, Cong ^a,g   Abraham, Sheela A ^b,c   Shan, Yi ^a   Guo, Zhiru ^a   Desouza, Ngoc ^a   Cheloni, Giulia ^a,d   Li, Dongguang ^e   Holyoake, Tessa L ^b   Li, Shaoguang ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF FLORENCE   (Italy)

^e EDITH COWAN UNIVERSITY   (Australia)

^f NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^g HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; ARACHIDONATE 15 LIPOXYGENASE; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; PADGEM PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; 6,11-DIHYDRO-5-THIA-11-AZA-BENZO(A)-FLUORENE; BCR ABL PROTEIN; FLUORENE DERIVATIVE; LIPOXYGENASE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER STEM CELL; CELL DIVISION; CELL POPULATION; CELL SURVIVAL; CHRONIC MYELOID LEUKEMIA; COLONY FORMING UNIT GM; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; LEUKEMIA CELL; MEGAKARYOCYTE ERYTHROID PROGENITOR; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PHENOTYPE; SPLEEN; ANIMAL; C57BL MOUSE; CELL CULTURE; GENETICS; HUMAN; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; ARACHIDONATE 15-LIPOXYGENASE; CELL LINE, TUMOR; CELLS, CULTURED; FLUORENES; FUSION PROTEINS, BCR-ABL; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; LIPOXYGENASE INHIBITORS; MICE; MICE, INBRED C57BL; NEOPLASTIC STEM CELLS; P-SELECTIN;

EID: 84907011500     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI66129     Document Type: Article

References (48)

1. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100(7):3983-3988.
2. Jordan CT, Guzman ML, Noble M. Cancer stem cells. N Engl J Med. 2006;355(12):1253-1261.
3. Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer. 2003;3(12):895-902.
4. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414(6859):105-111.
5. Rossi DJ, Jamieson CH, Weissman IL. Stems cells and the pathways to aging and cancer. Cell. 2008;132(4):681-696.
6. Singh SK, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63(18):5821-5828.
7. Wang JC, Dick JE. Cancer stem cells: lessons from leukemia. Trends Cell Biol. 2005;15(9):494-501.
8. Molofsky AV, Pardal R, Morrison SJ. Diverse mechanisms regulate stem cell self-renewal. Curr Opin Cell Biol. 2004;16(6):700-707.
9. Reya T, et al. A role for Wnt signalling in selfrenewal of haematopoietic stem cells. Nature. 2003;423(6938):409-414.
10. Taipale J, Beachy PA. The Hedgehog and Wnt signalling pathways in cancer. Nature. 2001;411(6835):349-354.
11. Zhao C, et al. Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell. 2007;12(6):528-541.
12. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature. 2003;423(6937):255-260.
13. Park IK, et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature. 2003;423(6937):302-305.
14. Molofsky AV, He S, Bydon M, Morrison SJ, Pardal R. Bmi-1 promotes neural stem cell selfrenewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. Genes Dev. 2005;19(12):1432-1437.
15. Lowe SW, Sherr CJ. Tumor suppression by Ink4a-Arf: progress and puzzles. Curr Opin Genet Dev. 2003;13(1):77-83.
16. Yilmaz OH, et al. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature. 2006;441(7092):475-482.
17. Ito K, et al. PML targeting eradicates quiescent leukaemia-initiating cells. Nature. 2008;453(7198):1072-1078.
18. Neviani P, et al. The tumor suppressor PP2A is functionally inactivated in blast crisis CML through the inhibitory activity of the BCR/ABL-regulated SET protein. Cancer Cell. 2005;8(5):355-368.
19. Chen Y, Hu Y, Zhang H, Peng C, Li S. Loss of the Alox5 gene impairs leukemia stem cells and prevents chronic myeloid leukemia. Nat Genet. 2009;41(7):783-792.
20. Naka K, et al. TGF-β-FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia. Nature. 2010;463(7281):676-680.
21. Ito T, et al. Regulation of myeloid leukaemia by the cell-fate determinant Musashi. Nature. 2010;466(7307):765-768.
22. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3(7):730-737.
23. Lapidot T, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367(6464):645-648.
24. Dierks C, et al. Expansion of Bcr-Abl-positive leukemic stem cells is dependent on Hedgehog pathway activation. Cancer Cell. 2008;14(3):238-249.
25. Zhao C, et al. Hedgehog signalling is essential for maintenance of cancer stem cells in myeloid leukaemia. Nature. 2009;458(7239):776-779.
26. Hu Y, Swerdlow S, Duffy TM, Weinmann R, Lee FY, Li S. Targeting multiple kinase pathways in leukemic prognitors and stem cells is essential for improved treatment of Ph+ leukemia in mice. Proc Natl Acad Sci U S A. 2006;103(45):16870-16875.
27. Hu Y, Chen Y, Douglas L, Li S. β-Catenin is essential for survival of leukemic stem cells insensitive to kinase inhibition in mice with BCR-ABLinduced chronic myeloid leukemia. Leukemia. 2009;23(1):109-116.
28. Graham SM, et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood. 2002;99(1):319-325.
29. Marley SB, Deininger MW, Davidson RJ, Goldman JM, Gordon MY. The tyrosine kinase inhibitor STI571, like interferon-α, preferentially reduces the capacity for amplification of granulocyte-macrophage progenitors from patients with chronic myeloid leukemia. Exp Hematol. 2000;28(5):551-557.
30. Klein RF, et al. Regulation of bone mass in mice by the lipoxygenase gene Alox15. Science. 2004;303(5655):229-232.
31. Kuhn H, O'Donnell VB. Inflammation and immune regulation by 12/15-lipoxygenases. Prog Lipid Res. 2006;45(4):334-356.
32. Middleton MK, et al. Identification of 12/15-lipoxygenase as a suppressor of myeloproliferative disease. J Exp Med. 2006;203(11):2529-2540.
33. Mahipal SV, et al. Effect of 15-lipoxygenase metabolites, 15-(S)-HPETE and 15-(S)-HETE on chronic myelogenous leukemia cell line K-562: reactive oxygen species (ROS) mediate caspase-dependent apoptosis. Biochem Pharmacol. 2007;74(2):202-214.
34. Peng C, et al. Inhibition of heat shock protein 90 prolongs survival of mice with BCR-ABL-T315I-induced leukemia and suppresses leukemic stem cells. Blood. 2007;110(2):678-685.
35. Kinder M, et al. Hematopoietic stem cell function requires 12/15-lipoxygenase-dependent fatty acid metabolism. Blood. 2010;115(24):5012-5022.
36. Pelletier SD, Hong DS, Hu Y, Liu Y, Li S. Lack of the adhesion molecules P-selectin and intercellular adhesion molecule-1 accelerate the development of BCR/ABL-induced chronic myeloid leukemia-like myeloproliferative disease in mice. Blood. 2004;104(7):2163-2171.
37. Sullivan C, et al. Functional ramifications for the loss of P-selectin expression on hematopoietic and leukemic stem cells. PLoS One. 2011;6(10):e26246.
38. Corbin AS, et al. KIT signaling governs differential sensitivity of mature and primitive CML progenitors to tyrosine kinase inhibitors. Cancer Res. 2013;73(18):5775-5786.
39. Goff DJ, et al. A Pan-BCL2 inhibitor renders bone-marrow-resident human leukemia stem cells sensitive to tyrosine kinase inhibition. Cell Stem Cell. 2013;12(3):316-328.
40. Pellicano F, Copland M, Jorgensen HG, Mountford J, Leber B, Holyoake TL. BMS-214662 induces mitochondrial apoptosis in chronic myeloid leukemia (CML) stem/progenitor cells, including CD34+38- cells, through activation of protein kinase Cβ. Blood. 2009;114(19):4186-4196.
41. Peng C, et al. LSK derived LSK- cells have a high apoptotic rate related to survival regulation of hematopoietic and leukemic stem cells. PLoS One. 2012;7(6):e38614.
42. Peng C, et al. PTEN is a tumor suppressor in CML stem cells and BCR-ABL-induced leukemias in mice. Blood. 2010;115(3):626-635.
43. Wymann MP, Schneiter R. Lipid signalling in disease. Nat Rev Mol Cell Biol. 2008;9(2):162-176.
44. Radich JP, et al. Gene expression changes associated with progression and response in chronic myeloid leukemia. Proc Natl Acad Sci U S A. 2006;103(8):2794-2799.
45. Li S, Ilaria RL, Ilaria RL Jr, Million RP, Daley GQ, Van Etten RA. The P190, P210, and p230 forms of the BCR/ABL oncogene induce a similar chronic myeloid leukemia-like syndrome in mice but have different lymphoid leukemogenic activity. J Exp Med. 1999;189(9):1399-1412.
46. Hu Y, et al. Requirement of Src kinases Lyn, Hck and Fgr for BCR-ABL1-induced B-lymphoblastic leukemia but not chronic myeloid leukemia. Nat Genet. 2004;36(5):453-461.
47. Li S, Couvillon AD, Brasher BB, and Van Etten RA. Tyrosine phosphorylation of Grb2 by Bcr/Abl epidermal growth factor receptor: a novel regulatory mechanism for tyrosine kinase signaling. EMBO J. 2001;20(23):6793-6804.
48. Zhang H, et al. The Blk pathway functions as a tumor suppressor in chronic myeloid leukemia stem cells. Nat Genet. 2012;44(8):861-871.