Single-cell mass cytometry reveals intracellular survival/proliferative signaling in FLT3-ITD-mutated AML stem/progenitor cells

Cytometry Part A

Volumn 87, Issue 4, 2015, Pages 346-356

  Han, Lina ^a   Qiu, Peng ^b   Zeng, Zhihong ^a   Jorgensen, Jeffrey L ^a   Mak, Duncan H ^a   Burks, Jared K ^a   Schober, Wendy ^a   Mcqueen, Teresa J ^a   Cortes, Jorge ^a   Tanner, Scott D ^c,d   Roboz, Gail J ^e   Kantarjian, Hagop M ^a   Kornblau, Steven M ^a   Guzman, Monica L ^e   Andreeff, Michael ^a   Konopleva, Marina ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b Emory University   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d DVS Sciences   (Canada)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

acute myeloid leukemia; Flow cytometry; Leukemia stem cells; Mass cytometry; Western blotting

Indexed keywords

CD135 ANTIGEN; CYTOKINE; DACTOLISIB; EIF4EBP1 PROTEIN, HUMAN; FLT3 PROTEIN, HUMAN; IMIDAZOLE DERIVATIVE; LEUKOCYTE ANTIGEN; MTOR PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOPROTEIN; PROTEIN KINASE B; QUINOLINE DERIVATIVE; S6 KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; STEM CELL FACTOR; TARGET OF RAPAMYCIN KINASE;

ACUTE MYELOID LEUKEMIA; ANTAGONISTS AND INHIBITORS; CANCER STEM CELL; CELL PROLIFERATION; CELL SURVIVAL; CYTOLOGY; FLOW CYTOMETRY; GENETICS; HUMAN; IMMUNOLOGY; MASS SPECTROMETRY; METABOLISM; PROCEDURES; SIGNAL TRANSDUCTION; STAINING; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTIGENS, CD; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CYTOKINES; FLOW CYTOMETRY; FMS-LIKE TYROSINE KINASE 3; HUMANS; IMIDAZOLES; LEUKEMIA, MYELOID, ACUTE; MASS SPECTROMETRY; NEOPLASTIC STEM CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOPROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; QUINOLINES; RIBOSOMAL PROTEIN S6 KINASES; SIGNAL TRANSDUCTION; STAINING AND LABELING; STEM CELL FACTOR; TOR SERINE-THREONINE KINASES;

EID: 84925361935     PISSN: 15524922     EISSN: 15524930     Source Type: Journal    
DOI: 10.1002/cyto.a.22628     Document Type: Article

References (38)

1. Felipe Rico J, Hassane DC, Guzman ML. Acute myelogenous leukemia stem cells: From bench to bedside. Cancer Lett 2013;338:4-9.
2. Hope KJ, Jin L, Dick JE. Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nat Immunol 2004;5:738-743.
3. Huntly BJ, Gillil DG. Leukaemia stem cells and the evolution of cancer-stem-cell research. Nat Rev Cancer 2005;5:311-321.
4. Konopleva MY, Jordan CT. Leukemia stem cells and microenvironment: Biology and therapeutic targeting. J Clin Oncol 2011;29:591-599.
5. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA, Dick JE. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994;367:645-648.
6. Jordan CT, Upchurch D, Szilvassy SJ, Guzman ML, Howard DS, Pettigrew AL, Meyerrose T, Rossi R, Grimes B, Rizzieri DA, et al. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia 2000;14:1777-1784.
7. Jan M, Snyder TM, Corces-Zimmerman MR, Vyas P, Weissman IL, Quake SR, Majeti R. Clonal evolution of preleukemic hematopoietic stem cells precedes human acute myeloid leukemia. Sci Transl Med 2012;4:149ra118
8. van Rhenen A, van Dongen GA, Kelder A, Rombouts EJ, Feller N, Moshaver B, Stigter-van Walsum M, Zweegman S, Ossenkoppele GJ, Jan Schuurhuis G. The novel AML stem cell associated antigen CLL-1 aids in discrimination between normal and leukemic stem cells. Blood 2007;110:2659-2666.
9. Jan M, Chao MP, Cha AC, Alizadeh AA, Gentles AJ, Weissman IL, Majeti R. Prospective separation of normal and leukemic stem cells based on differential expression of TIM3, a human acute myeloid leukemia stem cell marker. Proc Natl Acad Sci USA 2011;108:5009-5014.
10. Jaiswal S, Jamieson CH, Pang WW, Park CY, Chao MP, Majeti R, Traver D, van Rooijen N, Weissman IL. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 2009;138:271-285.
11. Saito Y, Kitamura H, Hijikata A, Tomizawa-Murasawa M, Tanaka S, Takagi S, Uchida N, Suzuki N, Sone A, Najima Y, et al. Identification of therapeutic targets for quiescent, chemotherapy-resistant human leukemia stem cells. Sci Transl Med 2010;2:17ra19
12. Tavakkoli M, Devlin SM, Park CY. CD99 is a therapeutic target on disease stem cells in acute myeloid leukemia and the myelodysplastic syndromes. Blood 2013;122:2891.
13. Jamieson CH, Ailles LE, Dylla SJ, Muijtjens M, Jones C, Zehnder JL, Gotlib J, Li K, Manz MG, Keating A, et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med 2004;351:657-667.
14. Miller PG, Al-Shahrour F, Hartwell KA, Chu LP, Jaras M, Puram RV, Puissant A, Callahan KP, Ashton J, McConkey ME, et al. In vivo RNAi screening identifies a Leukemia-specific dependence on integrin beta 3 signaling. Cancer Cell 2013;24:45-58.
15. Kornblau SM, Qutub A, Yao H, York H, Qiu YH, Graber D, Ravandi F, Cortes J, Andreeff M, Zhang N, et al. Proteomic profiling identifies distinct protein patterns in acute myelogenous leukemia CD34+CD38- Stem-like cells. PLoS One 2013;8:e78453
16. Eppert K, Takenaka K, Lechman ER, Waldron L, Nilsson B, van Galen P, Metzeler KH, Poeppl A, Ling V, Beyene J, et al. Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med 2011;17:1086-1093.
17. Taussig DC, Vargaftig J, Miraki-Moud F, Griessinger E, Sharrock K, Luke T, Lillington D, Oakervee H, Cavenagh J, Agrawal SG, et al. Leukemia-initiating cells from some acute myeloid leukemia patients with mutated nucleophosmin reside in the CD34(-) fraction. Blood 2010;115:1976-1984.
18. Ding L, Ley TJ, Larson DE, Miller CA, Koboldt DC, Welch JS, Ritchey JK, Young MA, Lamprecht T, McLellan MD, et al. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 2012;481:506-510.
19. Irish JM, Hovl R, Krutzik PO, Perez OD, Bruserud O, Gjertsen BT, Nolan GP. Single cell profiling of potentiated phospho-protein networks in cancer cells. Cell 2004;118:217-228.
20. Kornblau SM, Minden MD, Rosen DB, Putta S, Cohen A, Covey T, Spellmeyer DC, Fantl WJ, Gayko U, Cesano A. Dynamic single-cell network profiles in acute myelogenous leukemia are associated with patient response to standard induction therapy. Clin Cancer Res 2010;16:3721-3733.
21. Perl AE, Kasner MT, Shank D, Luger SM, Carroll M. Single-cell pharmacodynamic monitoring of S6 ribosomal protein phosphorylation in AML blasts during a clinical trial combining the mTOR inhibitor sirolimus and intensive chemotherapy. Clin Cancer Res 2012;18:1716-1725.
22. Autissier P, Soulas C, Burdo TH, Williams KC. Evaluation of a 12-color flow cytometry panel to study lymphocyte, monocyte, and dendritic cell subsets in humans. Cytometry A 2010;77A:410-419.
23. Perfetto SP, Chattopadhyay PK, Roederer M. Seventeen-colour flow cytometry: Unravelling the immune system. Nat Rev Immunol 2004;4:648-655.
24. Hulett HR, Bonner WA, Barrett J, Herzenberg LA. Cell sorting: Automated separation of mammalian cells as a function of intracellular fluorescence. Science 1969;166:747-749.
25. Bendall SC, Simonds EF, Qiu P, Amir el AD, Krutzik PO, Finck R, Bruggner RV, Melamed R, Trejo A, Ornatsky OI, et al. Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum. Science 2011;332:687-696.
26. Bandura DR, Baranov VI, Ornatsky OI, Antonov A, Kinach R, Lou X, Pavlov S, Vorobiev S, Dick JE, Tanner SD. Mass cytometry: Technique for real time single cell multitarget immunoassay based on inductively coupled plasma time-of-flight mass spectrometry. Anal Chem 2009;81:6813-6822.
27. Ornatsky O, Bandura D, Baranov V, Nitz M, Winnik MA, Tanner S. Highly multiparametric analysis by mass cytometry. J Immunol Methods 2010;361:1-20.
28. Wang L, Abbasi F, Ornatsky O, Cole KD, Misakian M, Gaigalas AK, He HJ, Marti GE, Tanner S, Stebbings R. Human CD4+ lymphocytes for antigen quantification: Characterization using conventional flow cytometry and mass cytometry. Cytometry A 2012;81A:567-575.
29. Fienberg HG, Simonds EF, Fantl WJ, Nolan GP, Bodenmiller B. A platinum-based covalent viability reagent for single-cell mass cytometry. Cytometry A 2012;81A:467-475.
30. Finck R, Simonds EF, Jager A, Krishnaswamy S, Sachs K, Fantl W, Pe'er D, Nolan GP, Bendall SC. Normalization of mass cytometry data with bead standards. Cytometry A 2013;83A:483-494.
31. Qiu P, Simonds EF, Bendall SC, Gibbs KD Jr., Bruggner RV, Linderman MD, Sachs K, Nolan GP, Plevritis SK. Extracting a cellular hierarchy from high-dimensional cytometry data with SPADE. Nat Biotechnol 2011;29:886-891.
32. Kikushige Y, Shima T, Takayanagi S, Urata S, Miyamoto T, Iwasaki H, Takenaka K, Teshima T, Tanaka T, Inagaki Y, et al. TIM-3 is a promising target to selectively kill acute myeloid leukemia stem cells. Cell Stem Cell 2010;7:708-717.
33. Qiu P. Inferring phenotypic properties from single-cell characteristics. PLoS One 2012;7:e37038
34. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997;3:730-737.
35. Taussig DC, Miraki-Moud F, Anjos-Afonso F, Pearce DJ, Allen K, Ridler C, Lillington D, Oakervee H, Cavenagh J, Agrawal SG, et al. Anti-CD38 antibody-mediated clearance of human repopulating cells masks the heterogeneity of leukemia-initiating cells. Blood 2008;112:568-575.
36. Goardon N, Marchi E, Atzberger A, Quek L, Schuh A, Soneji S, Woll P, Mead A, Alford KA, Rout R, et al. Coexistence of LMPP-like and GMP-like leukemia stem cells in acute myeloid leukemia. Cancer Cell 2011;19:138-152.
37. Gibbs KD Jr., Jager A, Crespo O, Goltsev Y, Trejo A, Richard CE, Nolan GP. Decoupling of tumor-initiating activity from stable immunophenotype in HoxA9-Meis1-driven AML. Cell Stem Cell 2012;10:210-217.
38. Gentles AJ, Plevritis SK, Majeti R, Alizadeh AA. Association of a leukemic stem cell gene expression signature with clinical outcomes in acute myeloid leukemia. JAMA 2010;304:2706-2715.