The core autophagy protein ATG4B is a potential biomarker and therapeutic target in CML stem/progenitor cells

Blood

Volumn 123, Issue 23, 2014, Pages 3622-3634

  Rothe, Katharina ^a,b   Lin, Hanyang ^a,b   Lin, Kevin B L ^a   Leung, Amy ^a   Wang, Hui Mi ^a   Malekesmaeili, Mehrnoush ^a   Brinkman, Ryan R ^a   Forrest, Donna L ^a,b   Gorski, Sharon M ^a,c   Jiang, Xiaoyan ^a,b  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY PROTEIN 4B; AUTOPHAGY PROTEIN 5; BECLIN 1; BIOLOGICAL MARKER; CD34 ANTIGEN; IMATINIB; MICRORNA 34A; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; CHRONIC MYELOID LEUKEMIA; CLINICAL ARTICLE; DRUG TARGETING; FEMALE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; STEM CELL; TREATMENT RESPONSE; UPREGULATION;

ADULT; ANTIGENS, CD34; AUTOPHAGY; BIOMARKERS, PHARMACOLOGICAL; CELLS, CULTURED; CYSTEINE ENDOPEPTIDASES; HUMANS; K562 CELLS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MOLECULAR TARGETED THERAPY; NEOPLASTIC STEM CELLS; PROGNOSIS; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL;

EID: 84902184873     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-07-516807     Document Type: Article

References (56)

1. Druker BJ, Tamura S, Buchdunger E, et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med. 1996;2(5):561-566.
2. Shah NP, Tran C, Lee FY, Chen P, Norris D, Sawyers CL. Overriding imatinib resistance with a novel ABL kinase inhibitor. Science. 2004; 305(5682):399-401. (Pubitemid 38938156)
3. Weisberg E, Manley PW, Breitenstein W, et al. Characterization of AMN107, a selective inhibitor of native and mutant Bcr-Abl. Cancer Cell. 2005; 7(2):129-141. (Pubitemid 40248339)
4. Kantarjian H, Shah NP, Hochhaus A, et al. Dasatinib versus imatinib in newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med. 2010;362(24):2260-2270.
5. Saglio G, Kim DW, Issaragrisil S, et al; ENESTnd Investigators. Nilotinib versus imatinib for newly diagnosed chronic myeloid leukemia. N Engl J Med. 2010;362(24):2251-2259.
6. Chan WW, Wise SC, Kaufman MD, et al. Conformational control inhibition of the BCR-ABL1 tyrosine kinase, including the gatekeeper T315I mutant, by the switch-control inhibitor DCC-2036. Cancer Cell. 2011;19(4):556-568.
7. Cortes JE, Kantarjian H, Shah NP, et al. Ponatinib in refractory Philadelphia chromosome-positive leukemias. N Engl J Med. 2012;367(22): 2075-2088.
8. Mahon FX, Réa D, Guilhot J, et al; Intergroupe Français des Leucémies Myéloïdes Chroniques. Discontinuation of imatinib in patients with chronic myeloid leukaemia who have maintained complete molecular remission for at least 2 years: the prospective, multicentre Stop Imatinib (STIM) trial. Lancet Oncol. 2010;11(11):1029-1035.
9. Ross DM, Branford S, Seymour JF, et al. Patients with chronic myeloid leukemia who maintain a complete molecular response after stopping imatinib treatment have evidence of persistent leukemia by DNA PCR. Leukemia. 2010;24(10): 1719-1724.
10. Gorre ME, Mohammed M, Ellwood K, et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science. 2001;293(5531):876-880. (Pubitemid 32743979)
11. O'Hare T, Zabriskie MS, Eiring AM, Deininger MW. Pushing the limits of targeted therapy in chronic myeloid leukaemia. Nat Rev Cancer. 2012;12(8):513-526.
12. Jiang X, Zhao Y, Smith C, et al. Chronic myeloid leukemia stem cells possess multiple unique features of resistance to BCR-ABL targeted therapies. Leukemia. 2007;21(5):926-935. (Pubitemid 46672068)
13. Jiang X, Saw KM, Eaves A, Eaves C. Instability of BCR-ABL gene in primary and cultured chronic myeloid leukemia stem cells. J Natl Cancer Inst. 2007;99(9):680-693. (Pubitemid 47073530)
14. Graham SM, Jørgensen HG, Allan E, 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.
15. Copland M, Hamilton A, Elrick LJ, et al. Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML but does not eliminate the quiescent fraction. Blood. 2006; 107(11):4532-4539. (Pubitemid 43801382)
16. Chu S, McDonald T, Lin A, et al. Persistence of leukemia stem cells in chronic myelogenous leukemia patients in prolonged remission with imatinib treatment. Blood. 2011;118(20): 5565-5572.
17. Chen Y, Peng C, Sullivan C, Li D, Li S. Critical molecular pathways in cancer stem cells of chronic myeloid leukemia. Leukemia. 2010;24(9): 1545-1554.
18. Chomel JC, Bonnet ML, Sorel N, et al. Leukemic stem cell persistence in chronic myeloid leukemia patients with sustained undetectable molecular residual disease. Blood. 2011;118(13): 3657-3660.
19. Corbin AS, Agarwal A, Loriaux M, Cortes J, Deininger MW, Druker BJ. Human chronic myeloid leukemia stem cells are insensitive to imatinib despite inhibition of BCR-ABL activity. J Clin Invest. 2011;121(1):396-409.
20. Hamilton A, Helgason GV, Schemionek M, et al. Chronic myeloid leukemia stem cells are not dependent on Bcr-Abl kinase activity for their survival. Blood. 2012;119(6):1501-1510.
21. White E. Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer. 2012;12(6):401-410.
22. Helgason GV, Karvela M, Holyoake TL. Kill one bird with two stones: potential efficacy of BCR-ABL and autophagy inhibition in CML. Blood. 2011;118(8):2035-2043.
23. Mizushima N. Autophagy: process and function. Genes Dev. 2007;21(22):2861-2873. (Pubitemid 350133435)
24. Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol. 2007;9(10):1102-1109. (Pubitemid 47500484)
25. Kroemer G, Jäättel ä M. Lysosomes and autophagy in cell death control. Nat Rev Cancer. 2005;5(11):886-897. (Pubitemid 41746033)
26. Kirisako T, Ichimura Y, Okada H, et al. The reversible modification regulates the membranebinding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol. 2000;151(2):263-276.
27. Mizushima N, Noda T, Yoshimori T, et al. A protein conjugation system essential for autophagy. Nature. 1998;395(6700):395-398. (Pubitemid 28450691)
28. Liang XH, Jackson S, Seaman M, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 1999;402(6762):672-676. (Pubitemid 129516338)
29. Tanida I, Sou YS, Ezaki J, Minematsu-Ikeguchi N, Ueno T, Kominami E. HsAtg4B/HsApg4B/ autophagin-1 cleaves the carboxyl termini of three human Atg8 homologues and delipidates microtubule-associated protein light chain 3-and GABAA receptor-associated protein-phospholipid conjugates. J Biol Chem. 2004;279(35): 36268-36276. (Pubitemid 39128963)
30. Fujita N, Hayashi-Nishino M, Fukumoto H, et al. An Atg4B mutant hampers the lipidation of LC3 paralogues and causes defects in autophagosome closure. Mol Biol Cell. 2008; 19(11):4651-4659.
31. Nair U, Yen WL, Mari M, et al. A role for Atg8-PE deconjugation in autophagosome biogenesis. Autophagy. 2012;8(5):780-793.
32. Nakatogawa H, Ishii J, Asai E, Ohsumi Y. Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis. Autophagy. 2012; 8(2):177-186.
33. Marinõ G, Uría JA, Puente XS, Quesada V, Bordallo J, López-Otín C. Human autophagins, a family of cysteine proteinases potentially implicated in cell degradation by autophagy. J Biol Chem. 2003;278(6):3671-3678. (Pubitemid 36801091)
34. Marinõ G, Fernández AF, Cabrera S, et al. Autophagy is essential for mouse sense of balance. J Clin Invest. 2010;120(7):2331-2344.
35. Betin VM, Lane JD. Caspase cleavage of Atg4D stimulates GABARAP-L1 processing and triggers mitochondrial targeting and apoptosis. J Cell Sci. 2009;122(Pt 14):2554-2566.
36. Li M, Hou Y, Wang J, Chen X, Shao ZM, Yin XM.Kinetics comparisons of mammalian Atg4 homologues indicate selective preferences toward diverse Atg8 substrates. J Biol Chem. 2011;286(9):7327-7338.
37. Read R, Savelieva K, Baker K, Hansen G, Vogel P. Histopathological and neurological features of Atg4b knockout mice. Vet Pathol. 2011;48(2): 486-494.
38. Bellodi C, Lidonnici MR, Hamilton A, et al. Targeting autophagy potentiates tyrosine kinase inhibitor-induced cell death in Philadelphia chromosome-positive cells, including primary CML stem cells. J Clin Invest. 2009;119(5): 1109-1123.
39. Crowley LC, Elzinga BM, O'Sullivan GC, McKenna SL. Autophagy induction by Bcr-Ablexpressing cells facilitates their recovery from a targeted or nontargeted treatment. Am J Hematol. 2011;86(1):38-47.
40. Drullion C, Tr égoat C, Lagarde V, et al. Apoptosis and autophagy have opposite roles on imatinibinduced K562 leukemia cell senescence. Cell Death Dis. 2012;3:e373.
41. Yu Y, Yang L, Zhao M, et al. Targeting microRNA-30a-mediated autophagy enhances imatinib activity against human chronic myeloid leukemiacells. Leukemia. 2012;26(8):1752-1760.
42. Forrest DL, Jiang X, Eaves CJ, Smith CL. An approach to the management of chronic myeloid leukemia in British Columbia. Curr Oncol. 2008; 15(2):90-97.
43. Baccarani M, Cortes J, Pane F, et al; European LeukemiaNet. Chronic myeloid leukemia: an update of concepts and management recommendations of European LeukemiaNet. J Clin Oncol. 2009;27(35):6041-6051.
44. Rio DC, Ares M Jr. Hannon GJ, Nilsen TW. Purification of RNA using TRIzol (TRI reagent). Cold Spring Harb Protoc. 2010;2010(6):pdb. prot5439.
45. Jiang X, Forrest D, Nicolini F, et al. Properties of CD341 CML stem/progenitor cells that correlate with different clinical responses to imatinib mesylate. Blood. 2010;116(12):2112-2121.
46. Zhou LL, Zhao Y, Ringrose A, et al. AHI-1 interacts with BCR-ABL and modulates BCR-ABL transforming activity and imatinib response of CML stem/progenitor cells. J Exp Med. 2008; 205(11):2657-2671.
47. Chen M, Gallipoli P, DeGeer D, et al. Targeting primitive chronic myeloid leukemia cells by effective inhibition of a new AHI-1-BCR-ABLJAK2 complex. J Natl Cancer Inst. 2013;105(6): 405-423.
48. Esquela-Kerscher A, Slack FJ. Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer. 2006;6(4):259-269.
49. Deutsch E, Maggiorella L, Wen B, et al. Tyrosine kinase inhibitor AG1024 exerts antileukaemic effects on STI571-resistant Bcr-Abl expressing cells and decreases AKT phosphorylation. Br J Cancer. 2004;91(9):1735-1741. (Pubitemid 39546148)
50. Lebovitz CB, Bortnik SB, Gorski SM. Here, there be dragons: charting autophagy-related alterations in human tumors. Clin Cancer Res. 2012;18(5):1214-1226.
51. Sheng Z, Ma L, Sun JE, Zhu LJ, Green MR. BCR-ABL suppresses autophagy through ATF5-mediated regulation of mTOR transcription. Blood. 2011;118(10):2840-2848.
52. Altman BJ, Jacobs SR, Mason EF, et al. Autophagy is essential to suppress cell stress and to allow BCR-Abl-mediated leukemogenesis. Oncogene. 2011;30(16):1855-1867.
53. Martinez-Lopez N, Athonvarangkul D, Mishall P, Sahu S, Singh R. Autophagy proteins regulate ERK phosphorylation. Nat Commun. 2013;4: 2799.
54. Marinõ G, Salvador-Montoliu N, Fueyo A, Knecht E, Mizushima N, López-Otín C. Tissue-specific autophagy alterations and increased tumorigenesis in mice deficient in Atg4C/autophagin-3. J Biol Chem. 2007;282(25): 18573-18583. (Pubitemid 47100226)
55. Shu CW, Madiraju C, Zhai D, et al. Highthroughput fluorescence assay for small-molecule inhibitors of autophagins/Atg4. J Biomol Screen. 2011;16(2):174-182.
56. Can G, Ekiz HA, Baran Y. Imatinib induces autophagy through BECLIN-1 and ATG5 genes in chronic myeloid leukemia cells. Hematology. 2011;16(2):95-99.