95
Views
5
CrossRef citations to date
0
Altmetric
Review

Strategies For Targeting Chronic Myeloid Leukaemia Stem Cells

, , & ORCID Icon
Pages 45-52 | Published online: 06 Nov 2019

References

  • Freireich EJ, Wiernik PH, Steensma DP. The leukemias: a half-century of discovery. J Clin Oncol. 2014;32:3463–3469. doi:10.1200/JCO.2014.57.103425185093
  • Goldman JM. Chronic myeloid leukemia: a historical perspective. Semin Hematol. 2010;47:302–311. doi:10.1053/j.seminhematol.2010.07.00120875546
  • Melo JV, Barnes DJ. Chronic myeloid leukaemia as a model of disease evolution in human cancer. Nat Rev Cancer. 2007;7:441–453. doi:10.1038/nrc214717522713
  • Chereda B, Melo JV. Natural course and biology of CML. Ann Hematol. 2015;94 Suppl 2:S107–S121. doi:10.1007/s00277-015-2325-z25814077
  • Apperley JF. Chronic myeloid leukaemia. Lancet. 2015;385:1447–1459. doi:10.1016/S0140-6736(13)62120-025484026
  • Lambert GK, Duhme-Klair A-K, Morgan T, Ramjee MK. The background, discovery and clinical development of BCR-ABL inhibitors. Drug Discov Today. 2013;18:992–1000. doi:10.1016/j.drudis.2013.06.00123769978
  • Sontakke P, Jaques J, Vellenga E, Schuringa JJ. Modeling of chronic myeloid leukemia: an overview of in vivo murine and human xenograft models. Stem Cells Int. 2016;2016:1625015. doi:10.1155/2016/162501527642303
  • Saglio G, Morotti A, Mattioli G, et al. Rational approaches to the design of therapeutics targeting molecular markers: the case of chronic myelogenous leukemia. Ann N Y Acad Sci. 2004;1028:423–431. doi:10.1196/annals.1322.05015650267
  • Hochhaus A, Larson RA, Guilhot F, et al. Long-term outcomes of imatinib treatment for chronic myeloid leukemia. N Engl J Med. 2017;376:917–927. doi:10.1056/NEJMoa160932428273028
  • Morotti A, Panuzzo C, Fava C, Saglio G. Kinase-inhibitor-insensitive cancer stem cells in chronic myeloid leukemia. Expert Opin Biol Ther. 2014;14:287–299. doi:10.1517/14712598.2014.86732324387320
  • Zhou H, Xu R. Leukemia stem cells: the root of chronic myeloid leukemia. Protein Cell. 2015;6:403–412. doi:10.1007/s13238-015-0143-725749979
  • Holyoake TL, Vetrie D. The chronic myeloid leukemia stem cell: stemming the tide of persistence. Blood. 2017;129:1595–1606. doi:10.1182/blood-2016-09-69601328159740
  • Inoue A, Kobayashi CI, Shinohara H, et al. Chronic myeloid leukemia stem cells and molecular target therapies for overcoming resistance and disease persistence. Int J Hematol. 2018;108:365–370. doi:10.1007/s12185-018-2519-y30155588
  • 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;121:396–409. doi:10.1172/JCI3572121157039
  • Soverini S, Mancini M, Bavaro L, Cavo M, Martinelli G. Chronic myeloid leukemia: the paradigm of targeting oncogenic tyrosine kinase signaling and counteracting resistance for successful cancer therapy. Mol Cancer. 2018;17:49. doi:10.1186/s12943-018-0780-629455643
  • Ross DM, Hughes TP, Melo JV. Do we have to kill the last CML cell? Leukemia. 2011;25:193–200. doi:10.1038/leu.2010.19720844563
  • Carrà G, Torti D, Crivellaro S, et al. BCR-ABL/NF-κB signal transduction network: a long lasting relationship in philadelphia positive leukemias. Oncotarget. 2016;7:66287–66298. doi:10.18632/oncotarget.1150727563822
  • Fusella F, Seclì L, Busso E, et al. The IKK/NF-κB signaling pathway requires Morgana to drive breast cancer metastasis. Nat Commun. 2017;8:1636. doi:10.1038/s41467-017-01829-129158506
  • Hsieh M-Y, Van Etten RA. IKK-dependent activation of NF-κB contributes to myeloid and lymphoid leukemogenesis by BCR-ABL1. Blood. 2014;123:2401–2411. doi:10.1182/blood-2014-01-54794324464015
  • Cilloni D, Messa F, Arruga F, et al. The NF-kappaB pathway blockade by the IKK inhibitor PS1145 can overcome imatinib resistance. Leukemia. 2006;20:61–67. doi:10.1038/sj.leu.240399816270044
  • Zhu X, Wang L, Zhang B, Li J, Dou X, Zhao RC. TGF-beta1-induced PI3K/Akt/NF-kappaB/MMP9 signalling pathway is activated in philadelphia chromosome-positive chronic myeloid leukaemia hemangioblasts. J Biochem. 2011;149:405–414. doi:10.1093/jb/mvr01621288887
  • Miyazono K. Tumour promoting functions of TGF-β in CML-initiating cells. J Biochem. 2012;152:383–385. doi:10.1093/jb/mvs10622989931
  • Gallipoli P, Pellicano F, Morrison H, et al. F-a production supports CML stem and progenitor cell survival and enhances their proliferation. Blood. 2013;122:6.23984446
  • Fattahi S, Pilehchian Langroudi M, Akhavan-Niaki H. Hedgehog signaling pathway: epigenetic regulation and role in disease and cancer development. J Cell Physiol. 2018;233:5726–5735. doi:10.1002/jcp.2650629380372
  • Su W, Meng F, Huang L, Zheng M, Liu W, Sun H. Sonic hedgehog maintains survival and growth of chronic myeloid leukemia progenitor cells through β-catenin signaling. Exp Hematol. 2012;40:418–427. doi:10.1016/j.exphem.2012.01.00322240607
  • Krishnamurthy N, Kurzrock R. Targeting the Wnt/beta-catenin pathway in cancer: update on effectors and inhibitors. Cancer Treat Rev. 2018;62:50–60. doi:10.1016/j.ctrv.2017.11.00229169144
  • Zhou H, Mak PY, Mu H, et al. Combined inhibition of β-catenin and Bcr-Abl synergistically targets tyrosine kinase inhibitor-resistant blast crisis chronic myeloid leukemia blasts and progenitors in vitro and in vivo. Leukemia. 2017;31:2065–2074. doi:10.1038/leu.2017.8728321124
  • Neviani P, Santhanam R, Trotta R, 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;8:355–368. doi:10.1016/j.ccr.2005.10.01516286244
  • Neviani P, Santhanam R, Oaks JJ, et al. FTY720, a new alternative for treating blast crisis chronic myelogenous leukemia and Philadelphia chromosome-positive acute lymphocytic leukemia. J Clin Invest. 2007;117:2408–2421. doi:10.1172/JCI3109517717597
  • Neviani P, Harb JG, Oaks JJ, et al. PP2A-activating drugs selectively eradicate TKI-resistant chronic myeloid leukemic stem cells. J Clin Invest. 2013;123:4144–4157. doi:10.1172/JCI6895123999433
  • Lai D, Chen M, Su J, et al. PP2A inhibition sensitizes cancer stem cells to ABL tyrosine kinase inhibitors in BCR-ABL+ human leukemia. Sci Transl Med. 2018;10. doi:10.1126/scitranslmed.aan8735
  • Reckel S, Hamelin R, Georgeon S, et al. Differential signaling networks of Bcr–abl p210 and p190 kinases in leukemia cells defined by functional proteomics. Leukemia. 2017;31:1502–1512. doi:10.1038/leu.2017.3628111465
  • Borgo C, Cesaro L, Salizzato V, et al. Aberrant signalling by protein kinase CK2 in imatinib-resistant chronic myeloid leukaemia cells: biochemical evidence and therapeutic perspectives. Mol Oncol. 2013;7:1103–1115. doi:10.1016/j.molonc.2013.08.00624012109
  • Morotti A, Panuzzo C, Crivellaro S, et al. ABL inactivates cytosolic PTEN through Casein Kinase II mediated tail phosphorylation. Cell Cycle. 2015;14:973–979. doi:10.1080/15384101.2015.100697025608112
  • 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;41:783–792. doi:10.1038/ng.38919503090
  • Crivellaro S, Carrà G, Panuzzo C, et al. The non-genomic loss of function of tumor suppressors: an essential role in the pathogenesis of chronic myeloid leukemia chronic phase. BMC Cancer. 2016;16:314. doi:10.1186/s12885-016-2346-627184141
  • Ito K, Bernardi R, Morotti A, et al. PML targeting eradicates quiescent leukaemia-initiating cells. Nature. 2008;453:1072–1078. doi:10.1038/nature0701618469801
  • Lee Y-R, Chen M, Pandolfi PP. The functions and regulation of the PTEN tumour suppressor: new modes and prospects. Nat Rev Mol Cell Biol. 2018;19:547–562. doi:10.1038/s41580-018-0015-029858604
  • Zhang J, Grindley JC, Yin T, et al. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature. 2006;441:518–522. doi:10.1038/nature0474716633340
  • Yilmaz ÖH, Valdez R, Theisen BK, et al. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature. 2006;441:475–482. doi:10.1038/nature0470316598206
  • Peng C, Chen Y, Yang Z, et al. PTEN is a tumor suppressor in CML stem cells and BCR-ABL-induced leukemias in mice. Blood. 2010;115:626–635. doi:10.1182/blood-2009-06-22813019965668
  • Morotti A, Panuzzo C, Crivellaro S, et al. BCR-ABL disrupts PTEN nuclear-cytoplasmic shuttling through phosphorylation-dependent activation of HAUSP. Leukemia. 2014;28:1326–1333. doi:10.1038/leu.2013.37024317448
  • Carrà G, Panuzzo C, Torti D, et al. Therapeutic inhibition of USP7-PTEN network in chronic lymphocytic leukemia: a strategy to overcome TP53 mutated/deleted clones. Oncotarget. 2017;8:35508–35522. doi:10.18632/oncotarget.v8i2228418900
  • Zhou J, Nie D, Li J, et al. PTEN is fundamental for elimination of leukemia stem cells mediated by Gsk126 targeting EZH2 in chronic myelogenous leukemia. Clin Cancer Res. 2018;24:145–157. doi:10.1158/1078-0432.CCR-17-153329070525
  • Liang R, Ghaffari S. Stem cells seen through the FOXO lens: an evolving paradigm. Curr Top Dev Biol. 2018;127:23–47.29433739
  • Naka K, Hoshii T, Muraguchi T, et al. TGF-β–FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia. Nature. 2010;463:676–680. doi:10.1038/nature0873420130650
  • Pellicano F, Scott MT, Helgason GV, et al. The antiproliferative activity of kinase inhibitors in chronic myeloid leukemia cells is mediated by FOXO transcription factors. Stem Cells. 2014;32:2324–2337. doi:10.1002/stem.174824806995
  • Ferretti R, Palumbo V, Di Savino A, et al. Morgana/chp-1, a ROCK inhibitor involved in centrosome duplication and tumorigenesis. Dev Cell. 2010;18:486–495. doi:10.1016/j.devcel.2009.12.02020230755
  • Di Savino A, Panuzzo C, Rocca S, et al. Morgana acts as an oncosuppressor in chronic myeloid leukemia. Blood. 2015;125:2245–2253. doi:10.1182/blood-2014-05-57500125678499
  • Zilfou JT, Lowe SW. Tumor suppressive functions of p53. Cold Spring Harb Perspect Biol. 2009;1:a001883. doi:10.1101/cshperspect.a00188320066118
  • Kastenhuber ER, Lowe SW. Putting p53 in context. Cell. 2017;170:1062–1078. doi:10.1016/j.cell.2017.08.02828886379
  • Johansson B, Fioretos T, Mitelman F. Cytogenetic and molecular genetic evolution of chronic myeloid leukemia. Acta Haematol. 2002;107:76–94. doi:10.1159/00004663611919388
  • Crivellaro S, Panuzzo C, Carrà G, et al. Non genomic loss of function of tumor suppressors in CML: BCR-ABL promotes IκBα mediated p53 nuclear exclusion. Oncotarget. 2015;6:25217–25225. doi:10.18632/oncotarget.461126295305
  • Abraham SA, Hopcroft LEM, Carrick E, et al. Dual targeting of p53 and c-MYC selectively eliminates leukaemic stem cells. Nature. 2016;534:341–346. doi:10.1038/nature1828827281222
  • Ungerstedt JS. Epigenetic modifiers in myeloid malignancies: the role of histone deacetylase inhibitors. Int J Mol Sci. 2018;19.
  • Zhang B, Strauss AC, Chu S, et al. Effective targeting of quiescent chronic myelogenous leukemia stem cells by histone deacetylase inhibitors in combination with imatinib mesylate. Cancer Cell. 2010;17:427–442. doi:10.1016/j.ccr.2010.03.01120478526
  • Scott MT, Korfi K, Saffrey P, et al. Epigenetic reprogramming sensitizes CML stem cells to combined EZH2 and tyrosine kinase inhibition. Cancer Discov. 2016;6:1248–1257. doi:10.1158/2159-8290.CD-16-026327630125
  • Vander Heiden MG, DeBerardinis RJ. Understanding the intersections between metabolism and cancer biology. Cell. 2017;168:657–669. doi:10.1016/j.cell.2016.12.03928187287
  • Kuntz EM, Baquero P, Michie AM, et al. Targeting mitochondrial oxidative phosphorylation eradicates therapy-resistant chronic myeloid leukemia stem cells. Nat Med. 2017;23:1234–1240. doi:10.1038/nm.439928920959
  • Saxton RA, Sabatini DM. mTOR signaling in growth, metabolism, and disease. Cell. 2017;168:960–976. doi:10.1016/j.cell.2017.02.00428283069
  • Mitchell R, Hopcroft LEM, Baquero P, et al. Targeting BCR-ABL-independent TKI resistance in chronic myeloid leukemia by mTOR and autophagy inhibition. J Natl Cancer Inst. 2018;110:467–478. doi:10.1093/jnci/djx23629165716
  • Vakana E, Platanias LC. AMPK in BCR-ABL expressing leukemias. Regulatory effects and therapeutic implications. Oncotarget. 2011;2:1322–1328. doi:10.18632/oncotarget.41322249159
  • Martinez Marignac VL, Smith S, Toban N, Bazile M, Aloyz R. Resistance to dasatinib in primary chronic lymphocytic leukemia lymphocytes involves AMPK-mediated energetic re-programming. Oncotarget. 2013;4:2550–2566. doi:10.18632/oncotarget.150824334291
  • Riva B, De Dominici M, Gnemmi I, et al. Celecoxib inhibits proliferation and survival of chronic myelogeous leukemia (CML) cells via AMPK-dependent regulation of β-catenin and mTORC1/2. Oncotarget. 2016;7:81555–81570. doi:10.18632/oncotarget.1314627835591
  • Rosilio C, Ben-Sahra I, Bost F, Peyron J-F. Metformin: a metabolic disruptor and anti-diabetic drug to target human leukemia. Cancer Lett. 2014;346:188–196. doi:10.1016/j.canlet.2014.01.00624462823
  • Shi R, Lin J, Gong Y, et al. The antileukemia effect of metformin in the Philadelphia chromosome-positive leukemia cell line and patient primary leukemia cell. Anticancer Drugs. 2015;26:913–922. doi:10.1097/CAD.000000000000026626186064
  • Prost S, Relouzat F, Spentchian M, et al. Erosion of the chronic myeloid leukaemia stem cell pool by PPARγ agonists. Nature. 2015;525:380–383. doi:10.1038/nature1524826331539
  • Rousselot P, Prost S, Guilhot J, et al. Pioglitazone together with imatinib in chronic myeloid leukemia: a proof of concept study. Cancer. 2017;123:1791–1799. doi:10.1002/cncr.v123.1028026860
  • Litwińska Z, Machaliński B. miRNAs in chronic myeloid leukemia: small molecules, essential function. Leuk Lymphoma. 2017;58:1297–1305. doi:10.1080/10428194.2016.124367627736267
  • Zhang B, Nguyen LXT, Li L, et al. Bone marrow niche trafficking of miR-126 controls the self-renewal of leukemia stem cells in chronic myelogenous leukemia. Nat Med. 2018;24:450–462. doi:10.1038/nm.449929505034
  • Salati S, Salvestrini V, Carretta C, et al. Deregulated expression of miR-29a-3p, miR-494-3p and miR-660-5p affects sensitivity to tyrosine kinase inhibitors in CML leukemic stem cells. Oncotarget. 2017;8:49451–49469. doi:10.18632/oncotarget.v8i3028533480
  • Pellicano F, Park L, Hopcroft LEM, et al. hsa-mir183/EGR1 –mediated regulation of E2F1 is required for CML stem/progenitor cell survival. Blood. 2018;131:1532–1544. doi:10.1182/blood-2017-05-78384529437554
  • Nassar FJ, El Eit R, Nasr R. An integrative analysis of microRNA and mRNA profiling in CML stem cells. Methods Mol Biol. 2016;1465:219–241.27581151
  • Alves R, Gonçalves AC, Jorge J, et al. MicroRNA signature refine response prediction in CML. Sci Rep. 2019;9:9666. doi:10.1038/s41598-019-46132-931273251
  • Wang K, Xu Z, Wang N, Tian Y, Sun X, Ma Y. Analysis of microRNA and gene networks in human chronic myelogenous leukemia. Mol Med Rep. 2016;13:453–460. doi:10.3892/mmr.2015.450226548770
  • Yeh C-H, Moles R, Nicot C. Clinical significance of microRNAs in chronic and acute human leukemia. Mol Cancer. 2016;15:37. doi:10.1186/s12943-016-0518-227179712
  • Di Stefano C, Mirone G, Perna S, Marfe G. The roles of microRNAs in the pathogenesis and drug resistance of chronic myelogenous leukemia (Review). Oncol Rep. 2016;35:614–624. doi:10.3892/or.2015.445626718125
  • Warfvinge R, Geironson L, Sommarin MNE, et al. Single-cell molecular analysis defines therapy response and immunophenotype of stem cell subpopulations in CML. Blood. 2017;129:2384–2394. doi:10.1182/blood-2016-07-72887328122740
  • Herrmann H, Sadovnik I, Cerny-Reiterer S, et al. Dipeptidylpeptidase IV (CD26) defines leukemic stem cells (LSC) in chronic myeloid leukemia. Blood. 2014;123:3951–3962. doi:10.1182/blood-2013-10-53607824778155
  • Valent P, Sadovnik I, Ráčil Z, et al. DPPIV (CD26) as a novel stem cell marker in Ph+ chronic myeloid leukaemia. Eur J Clin Invest. 2014;44:1239–1245. doi:10.1111/eci.2014.44.issue-1225371066
  • Culen M, Borsky M, Nemethova V, et al. Quantitative assessment of the CD26+ leukemic stem cell compartment in chronic myeloid leukemia: patient-subgroups, prognostic impact, and technical aspects. Oncotarget. 2016;7:33016–33024. doi:10.18632/oncotarget.v7i2227145281
  • Raspadori D, Pacelli P, Sicuranza A, et al. Flow cytometry assessment of CD26+ leukemic stem cells in peripheral blood: a simple and rapid new diagnostic tool for chronic myeloid leukemia. Cytometry B Clin Cytom. 2019;96:294–299. doi:10.1002/cyto.b.2176430714299
  • Bocchia M, Sicuranza A, Abruzzese E, et al. Residual peripheral blood CD26+ leukemic stem cells in chronic myeloid leukemia patients during TKI therapy and during treatment-free remission. Front Oncol. 2018;8:194. doi:10.3389/fonc.2018.0019429900128
  • Galimberti S, Grassi S, Baratè C, et al. The polycomb BMI1 protein is co-expressed with CD26+ in leukemic stem cells of chronic myeloid leukemia. Front Oncol. 2018;8:555. doi:10.3389/fonc.2018.0055530574454
  • Sadovnik I, Herrmann H, Eisenwort G, et al. Expression of CD25 on leukemic stem cells in BCR-ABL1 + CML: potential diagnostic value and functional implications. Exp Hematol. 2017;51:17–24. doi:10.1016/j.exphem.2017.04.00328457753
  • Sadovnik I, Hoelbl-Kovacic A, Herrmann H, et al. Identification of CD25 as STAT5-dependent growth regulator of leukemic stem cells in Ph+ CML. Clin Cancer Res. 2016;22:2051–2061. doi:10.1158/1078-0432.CCR-15-076726607600
  • Kobayashi CI, Takubo K, Kobayashi H, et al. The IL-2/CD25 axis maintains distinct subsets of chronic myeloid leukemia-initiating cells. Blood. 2014;123:2540–2549. doi:10.1182/blood-2013-07-51784724574458
  • Mukaida N, Tanabe Y, Baba T. Chemokines as a conductor of bone marrow microenvironment in chronic myeloid leukemia. Int J Mol Sci. 2017;18:1824. doi:10.3390/ijms18081824
  • Agarwal P, Isringhausen S, Li H, et al. Mesenchymal niche-specific expression of Cxcl12 controls quiescence of treatment-resistant leukemia stem cells. Cell Stem Cell. 2019;24:769–784.e6. doi:10.1016/j.stem.2019.02.01830905620
  • Karsli-Uzunbas G, Guo JY, Price S, et al. Autophagy is required for glucose homeostasis and lung tumor maintenance. Cancer Discov. 2014;4:914–927. doi:10.1158/2159-8290.CD-14-036324875857
  • Ravanan P, Srikumar IF, Talwar, T. Autophagy: The spotlight for cellular stress responses. Life Sci. 2017;188:53–67. doi:10.1016/j.lfs.2017.08.02928866100
  • Najafi M, Farhood B, Mortezaee K. Cancer stem cells (CSCs) in cancer progression and therapy. J Cell Physiol. 2019;234:8381–8395. doi:10.1002/jcp.v234.630417375
  • Baquero P, Dawson A, Mukhopadhyay A, et al. Targeting quiescent leukemic stem cells using second generation autophagy inhibitors. Leukemia. 2018;33:981–994.30185934
  • Liu Y, Song H, Song H, Feng X, Zhou C, Huo Z. Targeting autophagy potentiates the anti-tumor effect of PARP inhibitor in pediatric chronic myeloid leukemia. AMB Express. 2019;9:108. doi:10.1186/s13568-019-0836-z31309361
  • Hughes A, Clarson J, Tang C, et al. CML patients with deep molecular responses to TKI have restored immune effectors and decreased PD-1 and immune suppressors. Blood. 2017;129:1166–1176. doi:10.1182/blood-2016-10-74599228049640
  • Brück O, Blom S, Dufva O, et al. Immune cell contexture in the bone marrow tumor microenvironment impacts therapy response in CML. Leukemia. 2018;32:1643–1656. doi:10.1038/s41375-018-0175-029925907
  • Tarafdar A, Hopcroft LEM, Gallipoli P, et al. CML cells actively evade host immune surveillance through cytokine-mediated downregulation of MHC-II expression. Blood. 2017;129:199–208. doi:10.1182/blood-2016-09-74204927793879
  • Zitvogel L, Rusakiewicz S, Routy B, Ayyoub M, Kroemer G. Immunological off-target effects of imatinib. Nat Rev Clin Oncol. 2016;13:431–446. doi:10.1038/nrclinonc.2016.4127030078
  • Sinclair A, Park L, Shah M, et al. CXCR2 and CXCL4 regulate survival and self-renewal of hematopoietic stem/progenitor cells. Blood. 2016;128:371–383. doi:10.1182/blood-2015-08-66178527222476
  • Warda W, Larosa F, Neto Da Rocha M, et al. CML hematopoietic stem cells expressing IL1RAP can be targeted by chimeric antigen receptor-engineered T cells. Cancer Res. 2019;79:663–675. doi:10.1158/0008-5472.CAN-18-107830514753
  • Ghelli Luserna di Rora A, Iacobucci I, Martinelli G. The cell cycle checkpoint inhibitors in the treatment of leukemias. J Hematol Oncol. 2017;10:77. doi:10.1186/s13045-017-0443-x28356161
  • Baba T, Naka K, Morishita S, Komatsu N, Hirao A, Mukaida N. MIP-1α/CCL3-mediated maintenance of leukemia-initiating cells in the initiation process of chronic myeloid leukemia. J Exp Med. 2013;210:2661–2673. doi:10.1084/jem.2013011224166712