Genetically distinct leukemic stem cells in human CD34-acute myeloid leukemia are arrested at a hemopoietic precursor-like stage

Journal of Experimental Medicine

Volumn 213, Issue 8, 2016, Pages 1513-1535

  Quek, Lynn ^a,b   Otto, Georg W ^a   Garnett, Catherine ^a   Lhermitte, Ludovic ^a   Karamitros, Dimitris ^a   Stoilova, Bilyana ^a   Lau, I Jun ^a,b   Doondeea, Jessica ^a   Doondeea, Batchimeg ^a   Kennedy, Alison ^a   Metzner, Marlen ^a   Goardon, Nicolas ^a   Ivey, Adam ^c   Allen, Christopher ^d   Gale, Rosemary ^d   Davies, Benjamin ^b   Sternberg, Alexander ^e   Killick, Sally ^f   Hunter, Hannah ^g   Cahalin, Paul ^h   Price, Andrew ^b   Carr, Andrew ^b   Griffiths, Mike ⁱ   Virgo, Paul ^j   Mackinnon, Stephen ^d,k   Grimwade, David ^c   Freeman, Sylvie ^l,m   Russell, Nigel ⁿ   Craddock, Charles ^l,m   Mead, Adam ^a,b   Peniket, Andrew ^b   Porcher, Catherine ^a   Vyas, Paresh ^a,b   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b OXFORD UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e GREAT WESTERN HOSPITAL   (United Kingdom)

^f POOLE HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

^g PLYMOUTH HOSPITALS NHS TRUST   (United Kingdom)

^h BLACKPOOL TEACHING HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

ⁱ West Midlands Regional Genetics Laboratory   (United Kingdom)

^j NORTH BRISTOL NHS TRUST   (United Kingdom)

^k UNIVERSITY COLLEGE LONDON HOSPITALS   (United Kingdom)

^l UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^m UNIVERSITY HOSPITALS BIRMINGHAM NHS FOUNDATION TRUST   (United Kingdom)

ⁿ NOTTINGHAM UNIVERSITY HOSPITALS NHS TRUST   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; NUCLEOPHOSMIN; TUMOR PROTEIN;

ACUTE MYELOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER STEM CELL; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL POPULATION; CONTROLLED STUDY; EPIGENETICS; ERYTHROID PRECURSOR CELL; GENE EXPRESSION PROFILING; GENE MUTATION; GENETIC TRANSCRIPTION; GRANULOCYTE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; LEUKEMIC STEM CELL; MACROPHAGE; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; ACUTE MYELOID LEUKEMIA; ANIMAL; CANCER TRANSPLANTATION; CLINICAL TRIAL; COLONY FORMING UNIT GM; GENETICS; MALE; METABOLISM; MULTICENTER STUDY; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; XENOGRAFT;

ANIMALS; ANTIGENS, CD34; GRANULOCYTE-MACROPHAGE PROGENITOR CELLS; HETEROGRAFTS; HUMANS; LEUKEMIA, MYELOID, ACUTE; MALE; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS;

EID: 84982999606     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20151775     Document Type: Article

References (56)

1. + AML) shows a distinct gene expression profile characterized by up-regulation of genes involved in stem-cell maintenance. Blood. 106:899-902. http://dx.doi.org/10.1182/blood-2005-02-0560
2. - cells at the apex of the human hematopoietic stem cell hierarchy have distinctive cellular and molecular signatures. Cell Stem Cell. 13:161-174. http://dx.doi.org/10.1016/j.stem.2013.05.025
3. Antonchuk, J., G. Sauvageau, and R.K. Humphries. 2002. HOXB4-induced expansion of adult hematopoietic stem cells ex vivo. Cell. 109:39-45. http://dx.doi.org/10.1016/S0092-8674(02)00697-9
4. Ariki, R., S. Morikawa, Y. Mabuchi, S. Suzuki, M. Nakatake, K. Yoshioka, S. Hidano, H. Nakauchi, Y. Matsuzaki, T. Nakamura, and R. Goitsuka. 2014. Homeodomain transcription factor Meis1 is a critical regulator of adult bone marrow hematopoiesis. PLoS One. 9:e87646. http://dx.doi.org/10.1371/journal.pone.0087646
5. Bonnet, D., and J.E. Dick. 1997. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 3:730-737. http://dx.doi.org/10.1038/nm0797-730
6. Busque, L., J.P. Patel, M.E. Figueroa, A. Vasanthakumar, S. Provost, Z. Hamilou, L. Mollica, J. Li, A. Viale, A. Heguy, et al. 2012. Recurrent somatic TET2 mutations in normal elderly individuals with clonal hematopoiesis. Nat. Genet. 44:1179-1181. http://dx.doi.org/10.1038/ng.2413
7. Cancer Genome Atlas Research Network. 2013. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N. Engl. J. Med. 368:2059-2074. http://dx.doi.org/10.1056/NEJMoa1301689
8. Chen, J.Y., M. Miyanishi, S.K. Wang, S. Yamazaki, R. Sinha, K.S. Kao, J. Seita, D. Sahoo, H. Nakauchi, and I.L. Weissman. 2016. Hoxb5 marks long-term haematopoietic stem cells and reveals a homogenous perivascular niche. Nature. 530:223-227. http://dx.doi.org/10.1038/nature16943
9. Chou, W.C., J.L. Tang, S.J. Wu, W. Tsay, M. Yao, S.Y. Huang, K.C. Huang, C.Y. Chen, C.F. Huang, and H.F. Tien. 2007. Clinical implications of minimal residual disease monitoring by quantitative polymerase chain reaction in acute myeloid leukemia patients bearing nucleophosmin (NPM1) mutations. Leukemia. 21:998-1004. http://dx.doi.org/10.1038/sj.leu.2404637
10. Corces-Zimmerman, M.R., W.J. Hong, I.L. Weissman, B.C. Medeiros, and R. Majeti. 2014. Preleukemic mutations in human acute myeloid leukemia affect epigenetic regulators and persist in remission. Proc. Natl. Acad. Sci. USA. 111:2548-2553. http://dx.doi.org/10.1073/pnas.1324297111
11. Cozzio, A., E. Passegué, P.M. Ayton, H. Karsunky, M.L. Cleary, and I.L. Weissman. 2003. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev. 17:3029-3035. http://dx.doi.org/10.1101/gad.1143403
12. Eppert, K., K. Takenaka, E.R. Lechman, L. Waldron, B. Nilsson, P. van Galen, K.H. Metzeler, A. Poeppl, V. Ling, J. Beyene, et al. 2011. Stem cell gene expression programs influence clinical outcome in human leukemia. Nat. Med. 17:1086-1093. http://dx.doi.org/10.1038/nm.2415
13. Falini, B., C. Mecucci, E. Tiacci, M. Alcalay, R. Rosati, L. Pasqualucci, R. La Starza, D. Diverio, E. Colombo, A. Santucci, et al. GIM EMA Acute Leukemia Working Party. 2005. Cytoplasmic nucleophosmin in acute myelogenous leukemia with a normal karyotype. N. Engl. J. Med. 352:254-266. http://dx.doi.org/10.1056/NEJMoa041974
14. Ficara, F., L. Crisafulli, C. Lin, M. Iwasaki, K.S. Smith, L. Zammataro, and M.L. Cleary. 2013. Pbx1 restrains myeloid maturation while preserving lymphoid potential in hematopoietic progenitors. J. Cell Sci. 126:3181-3191. http://dx.doi.org/10.1242/jcs.125435
15. Genovese, G., A.K. Kähler, R.E. Handsaker, J. Lindberg, S.A. Rose, S.F. Bakhoum, K. Chambert, E. Mick, B.M. Neale, M. Fromer, et al. 2014. Clonal hematopoiesis and blood-cancer risk inferred from blood DNA sequence. N. Engl. J. Med. 371:2477-2487. http://dx.doi.org/10.1056/NEJMoa1409405
16. Goardon, N., E. Marchi, A. Atzberger, L. Quek, A. Schuh, S. Soneji, P. Woll, A. Mead, K.A. Alford, R. Rout, et al. 2011. Coexistence of LMPP-like and GMP-like leukemia stem cells in acute myeloid leukemia. Cancer Cell. 19:138-152. http://dx.doi.org/10.1016/j.ccr.2010.12.012
17. Gorello, P., G. Cazzaniga, F. Alberti, M.G. Dell'Oro, E. Gottardi, G. Specchia, G. Roti, R. Rosati, M.F. Martelli, D. Diverio, et al. 2006. Quantitative assessment of minimal residual disease in acute myeloid leukemia carrying nucleophosmin (NPM1) gene mutations. Leukemia. 20:1103-1108. http://dx.doi.org/10.1038/sj.leu.2404149
18. Green, C.L., K.K. Koo, R.K. Hills, A.K. Burnett, D.C. Linch, and R.E. Gale. 2010. Prognostic significance of CEB PA mutations in a large cohort of younger adult patients with acute myeloid leukemia: impact of double CEB PA mutations and the interaction with FLT3 and NPM1 mutations. J. Clin. Oncol. 28:2739-2747. http://dx.doi.org/10.1200/JCO.2009.26.2501
19. Grimwade, D., R.K. Hills, A.V. Moorman, H. Walker, S. Chatters, A.H. Goldstone, K. Wheatley, C.J. Harrison, and A.K. Burnett. National Cancer Research Institute Adult Leukaemia Working Group. 2010. Refinement of cytogenetic classification in acute myeloid leukemia: determination of prognostic significance of rare recurring chromosomal abnormalities among 5876 younger adult patients treated in the United Kingdom Medical Research Council trials. Blood. 116:354-365. http://dx.doi.org/10.1182/blood-2009-11-254441
20. Hou, Y., L. Song, P. Zhu, B. Zhang, Y. Tao, X. Xu, F. Li, K. Wu, J. Liang, D. Shao, et al. 2012. Single-cell exome sequencing and monoclonal evolution of a JAK2-negative myeloproliferative neoplasm. Cell. 148:873-885. http://dx.doi.org/10.1016/j.cell.2012.02.028
21. Ishikawa, F., S. Yoshida, Y. Saito, A. Hijikata, H. Kitamura, S. Tanaka, R. Nakamura, T. Tanaka, H. Tomiyama, N. Saito, et al. 2007. Chemotherapy-resistant human AML stem cells home to and engraft within the bone-marrow endosteal region. Nat. Biotechnol. 25:1315-1321. http://dx.doi.org/10.1038/nbt1350
22. Iwama, A., H. Oguro, M. Negishi, Y. Kato, Y. Morita, H. Tsukui, H. Ema, T. Kamijo, Y. Katoh-Fukui, H. Koseki, et al. 2004. Enhanced self-renewal of hematopoietic stem cells mediated by the polycomb gene product Bmi-1. Immunity. 21:843-851. http://dx.doi.org/10.1016/j.immuni.2004.11.004
23. Jaiswal, S., P. Fontanillas, J. Flannick, A. Manning, P.V. Grauman, B.G. Mar, R.C. Lindsley, C.H. Mermel, N. Burtt, A. Chavez, et al. 2014. Age-related clonal hematopoiesis associated with adverse outcomes. N. Engl. J. Med. 371:2488-2498. http://dx.doi.org/10.1056/NEJMoa1408617
24. Jan, M., T.M. Snyder, M.R. Corces-Zimmerman, P. Vyas, I.L. Weissman, S.R. Quake, and R. Majeti. 2012. Clonal evolution of preleukemic hematopoietic stem cells precedes human acute myeloid leukemia. Sci. Transl. Med. 4:149ra118. http://dx.doi.org/10.1126/scitranslmed.3004315
25. Jovanovic, J.V., A. Ivey, A.M. Vannucchi, E. Lippert, E. Oppliger Leibundgut, B. Cassinat, N. Pallisgaard, N. Maroc, S. Hermouet, G. Nickless, et al. 2013. Establishing optimal quantitative-polymerase chain reaction assays for routine diagnosis and tracking of minimal residual disease in JAK2-V617F-associated myeloproliferative neoplasms: a joint European LeukemiaNet/MPN&MPNr-EuroNet (COST action BM0902) study. Leukemia. 27:2032-2039. http://dx.doi.org/10.1038/leu.2013.219
26. Kawagoe, H., A. Kandilci, T.A. Kranenburg, and G.C. Grosveld. 2007. Overexpression of N-Myc rapidly causes acute myeloid leukemia in mice. Cancer Res. 67:10677-10685. http://dx.doi.org/10.1158/0008-5472.CAN-07-1118
27. Kirstetter, P., M.B. Schuster, O. Bereshchenko, S. Moore, H. Dvinge, E. Kurz, K. Theilgaard-Mönch, R. Månsson, T.A. Pedersen, T. Pabst, et al. 2008. Modeling of C/EBPα mutant acute myeloid leukemia reveals a common expression signature of committed myeloid leukemia-initiating cells. Cancer Cell. 13:299-310. http://dx.doi.org/10.1016/j.ccr.2008.02.008
28. Klco, J.M., D.H. Spencer, C.A. Miller, M. Griffith, T.L. Lamprecht, M. O'Laughlin, C. Fronick, V. Magrini, R.T. Demeter, R.S. Fulton, et al. 2014. Functional heterogeneity of genetically defined subclones in acute myeloid leukemia. Cancer Cell. 25:379-392. http://dx.doi.org/10.1016/j.ccr.2014.01.031
29. Koboldt, D.C., K. Chen, T. Wylie, D.E. Larson, M.D. McLellan, E.R. Mardis, G.M. Weinstock, R.K. Wilson, and L. Ding. 2009. VarScan: variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics. 25:2283-2285. http://dx.doi.org/10.1093/bioinformatics/btp373
30. Krivtsov, A.V., D. Twomey, Z. Feng, M.C. Stubbs, Y. Wang, J. Faber, J.E. Levine, J. Wang, W.C. Hahn, D.G. Gilliland, et al. 2006. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature. 442:818-822. http://dx.doi.org/10.1038/nature04980
31. Kyba, M., R.C. Perlingeiro, and G.Q. Daley. 2002. HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell. 109:29-37. http://dx.doi.org/10.1016/S0092-8674(02)00680-3
32. Laurenti, E., S. Doulatov, S. Zandi, I. Plumb, J. Chen, C. April, J.B. Fan, and J.E. Dick. 2013. The transcriptional architecture of early human hematopoiesis identifies multilevel control of lymphoid commitment. Nat. Immunol. 14:756-763. http://dx.doi.org/10.1038/ni.2615
33. Lessard, J., and G. Sauvageau. 2003. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature. 423:255-260. http://dx.doi.org/10.1038/nature01572
34. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, and R. Durbin. 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics. 25:2078-2079. http://dx.doi.org/10.1093/bioinformatics/btp352
35. Lunter, G., and M. Goodson. 2011. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21:936-939. http://dx.doi.org/10.1101/gr.111120.110
36. + cells from AML with mutated NPM1 harbor cytoplasmic mutated nucleophosmin and generate leukemia in immunocompromised mice. Blood. 116:3907-3922. http://dx.doi.org/10.1182/blood-2009-08-238899
37. McCarthy, D.J., Y. Chen, and G.K. Smyth. 2012. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 40:4288-4297. http://dx.doi.org/10.1093/nar/gks042
38. Nomdedeu, J., E. Bussaglia, N. Villamor, C. Martinez, J. Esteve, M. Tormo, C. Estivill, M.P. Queipo, R. Guardia, M. Carricondo, et al. Spanish CET LAM. 2011. Immunophenotype of acute myeloid leukemia with NPM mutations: prognostic impact of the leukemic compartment size. Leuk. Res. 35:163-168. http://dx.doi.org/10.1016/j.leukres.2010.05.015
39. Novershtern, N., A. Subramanian, L.N. Lawton, R.H. Mak, W.N. Haining, M.E. McConkey, N. Habib, N. Yosef, C.Y. Chang, T. Shay, et al. 2011. Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell. 144:296-309. http://dx.doi.org/10.1016/j.cell.2011.01.004
40. Oshima, M., M. Endoh, T.A. Endo, T. Toyoda, Y. Nakajima-Takagi, F. Sugiyama, H. Koseki, M. Kyba, A. Iwama, and M. Osawa. 2011. Genome-wide analysis of target genes regulated by HoxB4 in hematopoietic stem and progenitor cells developing from embryonic stem cells. Blood. 117:e142-e150. http://dx.doi.org/10.1182/blood-2010-12-323212
41. Park, I.K., D. Qian, M. Kiel, M.W. Becker, M. Pihalja, I.L. Weissman, S.J. Morrison, and M.F. Clarke. 2003. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature. 423:302-305. http://dx.doi.org/10.1038/nature01587
42. Potter, N.E., L. Ermini, E. Papaemmanuil, G. Cazzaniga, G. Vijayaraghavan, I. Titley, A. Ford, P. Campbell, L. Kearney, and M. Greaves. 2013. Single-cell mutational profiling and clonal phylogeny in cancer. Genome Res. 23:2115-2125. http://dx.doi.org/10.1101/gr.159913.113
43. Raczy, C., R. Petrovski, C.T. Saunders, I. Chorny, S. Kruglyak, E.H. Margulies, H.Y. Chuang, M. Källberg, S.A. Kumar, A. Liao, et al. 2013. Isaac: ultra-fast whole-genome secondary analysis on Illumina sequencing platforms. Bioinformatics. 29:2041-2043. http://dx.doi.org/10.1093/bioinformatics/btt314
44. Sarry, J.E., K. Murphy, R. Perry, P.V. Sanchez, A. Secreto, C. Keefer, C.R. Swider, A.C. Strzelecki, C. Cavelier, C. Récher, et al. 2011. Human acute myelogenous leukemia stem cells are rare and heterogeneous when assayed in NOD/SCID/IL2Rγc-deficient mice. J. Clin. Invest. 121:384-395. http://dx.doi.org/10.1172/JCI41495
45. Sauvageau, G., U. Thorsteinsdottir, C.J. Eaves, H.J. Lawrence, C. Largman, P.M. Lansdorp, and R.K. Humphries. 1995. Overexpression of HOXB4 in hematopoietic cells causes the selective expansion of more primitive populations in vitro and in vivo. Genes Dev. 9:1753-1765. http://dx.doi.org/10.1101/gad.9.14.1753
46. Shlush, L.I., S. Zandi, A. Mitchell, W.C. Chen, J.M. Brandwein, V. Gupta, J.A. Kennedy, A.D. Schimmer, A.C. Schuh, K.W. Yee, et al. HALT Pan-Leukemia Gene Panel Consortium. 2014. Identification of pre-leukaemic haematopoietic stem cells in acute leukaemia. Nature. 506:328-333. http://dx.doi.org/10.1038/nature13038
47. So, C.W., H. Karsunky, E. Passegué, A. Cozzio, I.L. Weissman, and M.L. Cleary. 2003. MLL-GAS7 transforms multipotent hematopoietic progenitors and induces mixed lineage leukemias in mice. Cancer Cell. 3:161-171. http://dx.doi.org/10.1016/S1535-6108(03)00019-9
48. Spencer, D.H., H.J. Abel, C.M. Lockwood, J.E. Payton, P. Szankasi, T.W. Kelley, S. Kulkarni, J.D. Pfeifer, and E.J. Duncavage. 2013. Detection of FLT3 internal tandem duplication in targeted, short-read-length, next-generation sequencing data. J. Mol. Diagn. 15:81-93. http://dx.doi.org/10.1016/j.jmoldx.2012.08.001
49. Spencer, D.H., M.A. Young, T.L. Lamprecht, N.M. Helton, R. Fulton, M. O'Laughlin, C. Fronick, V. Magrini, R.T. Demeter, C.A. Miller, et al. 2015. Epigenomic analysis of the HOX gene loci reveals mechanisms that may control canonical expression patterns in AML and normal hematopoietic cells. Leukemia. 29:1279-1289. http://dx.doi.org/10.1038/leu.2015.6
50. Subramanian, A., P. Tamayo, V.K. Mootha, S. Mukherjee, B.L. Ebert, M.A. Gillette, A. Paulovich, S.L. Pomeroy, T.R. Golub, E.S. Lander, and J.P. Mesirov. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA. 102:15545-15550. http://dx.doi.org/10.1073/pnas.0506580102
51. - fraction. Blood. 115:1976-1984. http://dx.doi.org/10.1182/blood-2009-02-206565
52. Treff, N.R., J. Su, X. Tao, L.E. Northrop, and R.T. Scott Jr. 2011. Single-cell whole-genome amplification technique impacts the accuracy of SNP microarray-based genotyping and copy number analyses. Mol. Hum. Reprod. 17:335-343. http://dx.doi.org/10.1093/molehr/gaq103
53. van Lochem, E.G., V.H. van der Velden, H.K. Wind, J.G. te Marvelde, N.A.C. Westerdaal, and J.J. van Dongen. 2004. Immunophenotypic differentiation patterns of normal hematopoiesis in human bone marrow: Reference patterns for age-related changes and disease-induced shifts. Cytometry B Clin. Cytom. 60B:1-13. http://dx.doi.org/10.1002/cyto.b.20008
54. Vassiliou, G.S., J.L. Cooper, R. Rad, J. Li, S. Rice, A. Uren, L. Rad, P. Ellis, R. Andrews, R. Banerjee, et al. 2011. Mutant nucleophosmin and cooperating pathways drive leukemia initiation and progression in mice. Nat. Genet. 43:470-475. http://dx.doi.org/10.1038/ng.796
55. Woll, P.S., U. Kjällquist, O. Chowdhury, H. Doolittle, D.C. Wedge, S. Thongjuea, R. Erlandsson, M. Ngara, K. Anderson, Q. Deng, et al. 2014. Myelodysplastic syndromes are propagated by rare and distinct human cancer stem cells in vivo. Cancer Cell. 25:794-808. http://dx.doi.org/10.1016/j.ccr.2014.03.036
56. Wong, P., M. Iwasaki, T.C.P. Somervaille, C.W.E. So, and M.L. Cleary. 2007. Meis1 is an essential and rate-limiting regulator of MLL leukemia stem cell potential. Genes Dev. 21:2762-2774. http://dx.doi.org/10.1101/gad.1602107