Acute B lymphoblastic leukaemia-propagating cells are present at high frequency in diverse lymphoblast populations

EMBO Molecular Medicine

Volumn 5, Issue 1, 2013, Pages 38-51

  Rehe, Klaus ^a,b,f   Wilson, Kerrie ^a   Bomken, Simon ^a,b   Williamson, Daniel ^a   Irving, Julie ^a   den Boer, Monique L ^c   Stanulla, Martin ^d   Schrappe, Martin ^d   Hall, Andrew G ^a   Heidenreich, Olaf ^a,e   Vormoor, Josef ^a,b,e  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b Infectious Diseases Allergy   (United Kingdom)

^c SOPHIA CHILDREN S HOSPITAL   (Netherlands)

^d UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^e NEWCASTLE UNIVERSITY   (United Kingdom)

^f UNIVERSITY HOSPITAL REGENSBURG   (Germany)

Author keywords

Acute lymphoblastic leukaemia; Cancer stem cells; Leukaemia maintenance; Leukaemia propagating cells; Leukaemia stem cells

Indexed keywords

CD20 ANTIGEN; CD34 ANTIGEN; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CELL DIFFERENTIATION; CELL GROWTH; CELL MATURATION; CELL POPULATION; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; GENE EXPRESSION; GENE REGULATORY NETWORK; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; LEUKEMIA PROPAGATING CELL; LYMPHOBLAST; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL EXPANSION; TRANSCRIPTOMICS;

ANIMALS; ANTIGENS, CD34; CELL DIFFERENTIATION; GENE REGULATORY NETWORKS; HUMANS; IMMUNOPHENOTYPING; MICE; MODELS, BIOLOGICAL; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; PRECURSOR B-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; TRANSCRIPTOME; TRANSPLANTATION, HETEROLOGOUS;

EID: 84871990876     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201201703     Document Type: Article

References (61)

1. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983- 3988
2. Anderson K, Lutz C, van Delft FW, Bateman CM, Guo Y, Colman SM, Kempski H, Moorman AV, Titley I, Swansbury J, et al (2011) Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature 469: 356- 361
3. Andersson A, Ritz C, Lindgren D, Eden P, Lassen C, Heldrup J, Olofsson T, Rade J, Fontes M, Porwit-Macdonald A, et al (2007) Microarray-based classification of a consecutive series of 121 childhood acute leukemias: prediction of leukemic and genetic subtype as well as of minimal residual disease status. Leukemia 21: 1198- 1203
4. Bomken S, Fiser K, Heidenreich O, Vormoor J (2010) Understanding the cancer stem cell. Br J Cancer 103: 439- 445
5. Bonnet D, Dick JE (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3: 730- 737
6. Broske AM, Vockentanz L, Kharazi S, Huska MR, Mancini E, Scheller M, Kuhl C, Enns A, Prinz M, Jaenisch R, et al (2009) DNA methylation protects hematopoietic stem cell multipotency from myeloerythroid restriction. Nat Genet 41: 1207- 1215
7. Castor A, Nilsson L, Astrand-Grundstrom I, Buitenhuis M, Ramirez C, Anderson K, Strombeck B, Garwicz S, Bekassy AN, Schmiegelow K, et al (2005) Distinct patterns of hematopoietic stem cell involvement in acute lymphoblastic leukemia. Nat Med 11: 630- 637
8. Chiu PP, Jiang H, Dick JE (2010) Leukemia-initiating cells in human T-lymphoblastic leukemia exhibit glucocorticoid resistance. Blood 116: 5268- 5279
9. Clappier E, Gerby B, Sigaux F, Delord M, Touzri F, Hernandez L, Ballerini P, Baruchel A, Pflumio F, Soulier J (2011) Clonal selection in xenografted human T cell acute lymphoblastic leukemia recapitulates gain of malignancy at relapse. J Exp Med 208: 653- 661
10. Cobaleda C, Gutierrez-Cianca N, Perez-Losada J, Flores T, Garcia-Sanz R, Gonzalez M, Sanchez-Garcia I (2000) A primitive hematopoietic cell is the target for the leukemic transformation in human philadelphia-positive acute lymphoblastic leukemia. Blood 95: 1007- 1013
11. Cox CV, Evely RS, Oakhill A, Pamphilon DH, Goulden NJ, Blair A (2004) Characterization of acute lymphoblastic leukemia progenitor cells. Blood 104: 2919- 2925
12. Cox CV, Diamanti P, Evely RS, Kearns PR, Blair A (2009) Expression of CD133 on leukemia-initiating cells in childhood ALL. Blood 113: 3287- 3296
13. Den Boer ML, van Slegtenhorst M, De Menezes RX, Cheok MH, Buijs-Gladdines JG, Peters ST, Van Zutven LJ, Beverloo HB, Van der Spek PJ, Escherich G, et al (2009) A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol 10: 125- 134
14. Diamanti P, Cox CV, Blair A (2012) Comparison of childhood leukemia initiating cell populations in NOD/SCID and NSG mice. Leukemia 26: 376- 380
15. Dick JE (2008) Stem cell concepts renew cancer research. Blood 112: 4793- 4807
16. Dieter SM, Ball CR, Hoffmann CM, Nowrouzi A, Herbst F, Zavidij O, Abel U, Arens A, Weichert W, Brand K, et al (2011) Distinct types of tumor-initiating cells form human colon cancer tumors and metastases. Cell Stem Cell 9: 357- 365
17. Eppert K, Takenaka K, Lechman ER, Waldron L, Nilsson B, van Galen P, Metzeler KH, Poeppl A, Ling V, Beyene J, et al (2011) Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med 17: 1086- 1093
18. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, Conticello C, Ruco L, Peschle C, De Maria R (2008) Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 15: 504- 514
19. Gentles AJ, Plevritis SK, Majeti R, Alizadeh AA (2010) Association of a leukemic stem cell gene expression signature with clinical outcomes in acute myeloid leukemia. JAMA 304: 2706- 2715
20. Gessner A, Thomas M, Castro PG, Buchler L, Scholz A, Brummendorf TH, Soria NM, Vormoor J, Greil J, Heidenreich O (2010) Leukemic fusion genes MLL/AF4 and AML1/MTG8 support leukemic self-renewal by controlling expression of the telomerase subunit TERT. Leukemia 24: 1751- 1759
21. Goardon N, Marchi E, Atzberger A, Quek L, Schuh A, Soneji S, Woll P, Mead A, Alford KA, Rout R, et al (2011) Coexistence of LMPP-like and GMP-like leukemia stem cells in acute myeloid leukemia. Cancer Cell 19: 138- 152
22. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum HI (2003) Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 100: 15178- 15183
23. Ho MM, Ng AV, Lam S, Hung JY (2007) Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 67: 4827- 4833
24. Hong D, Gupta R, Ancliff P, Atzberger A, Brown J, Soneji S, Green J, Colman S, Piacibello W, Buckle V, et al (2008) Initiating and cancer-propagating cells in TEL-AML1-associated childhood leukemia. Science (New York) 319: 336- 339
25. Hope KJ, Jin L, Dick JE (2004) Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nat Immunol 5: 738- 743
26. Hotfilder M, Rottgers S, Rosemann A, Schrauder A, Schrappe M, Pieters R, Jurgens H, Harbott J, Vormoor J (2005) Leukemic stem cells in childhood high-risk ALL/t(9;22) and t(4;11) are present in primitive lymphoid-restricted CD34+CD19-cells. Cancer Res 65: 1442- 1449
27. Hu Y, Smyth GK (2009) ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods 347: 70- 78
28. Irving J, Jesson J, Virgo P, Case M, Minto L, Eyre L, Noel N, Johansson U, Macey M, Knotts L, et al (2009) Establishment and validation of a standard protocol for the detection of minimal residual disease in B lineage childhood acute lymphoblastic leukemia by flow cytometry in a multi-center setting. Haematologica 94: 870- 874
29. Jamieson CH, Ailles LE, Dylla SJ, Muijtjens M, Jones C, Zehnder JL, Gotlib J, Li K, Manz MG, Keating A, et al (2004) Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med 351: 657- 667
30. Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A (2007) Tumor growth need not be driven by rare cancer stem cells. Science (New York, NY) 317: 337
31. Kim YC, Wu Q, Chen J, Xuan Z, Jung YC, Zhang MQ, Rowley JD, Wang SM (2009) The transcriptome of human CD34+ hematopoietic stem-progenitor cells. Proc Natl Acad Sci USA 106: 8278- 8283
32. Kong Y, Yoshida S, Saito Y, Doi T, Nagatoshi Y, Fukata M, Saito N, Yang SM, Iwamoto C, Okamura J, et al (2008) CD34+CD38+CD19+ as well as CD34+CD38-CD19+ cells are leukemia-initiating cells with self-renewal capacity in human B-precursor ALL. Leukemia 22: 1207- 1213
33. Krejci O, Wunderlich M, Geiger H, Chou FS, Schleimer D, Jansen M, Andreassen PR, Mulloy JC (2008) p53 signaling in response to increased DNA damage sensitizes AML1-ETO cells to stress-induced death. Blood 111: 2190- 2199
34. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA, Dick JE (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367: 645- 648
35. le Viseur C, Hotfilder M, Bomken S, Wilson K, Rottgers S, Schrauder A, Rosemann A, Irving J, Stam RW, Shultz LD, et al (2008) In childhood acute lymphoblastic leukemia, blasts at different stages of immunophenotypic maturation have stem cell properties. Cancer Cell 14: 47- 58
36. Liu K, Schoonmaker MM, Levine BL, June CH, Hodes RJ, Weng NP (1999) Constitutive and regulated expression of telomerase reverse transcriptase (hTERT) in human lymphocytes. Proc Natl Acad Sci USA 96: 5147- 5152
37. Lobetti-Bodoni C, Bernocco E, Genuardi E, Boccadoro M, Ladetto M (2010) Telomeres and telomerase in normal and malignant B-cells. Hematol Oncol 28: 157- 167
38. Magee JA, Piskounova E, Morrison SJ (2012) Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer Cell 21: 283- 296.
39. McCulloch EA. (1983) Stem cells in normal and leukemic hemopoiesis (Henry Stratton Lecture, 1982). Blood 62: 1- 13
40. McDermott SP, Eppert K, Lechman ER, Doedens M, Dick JE (2010) Comparison of human cord blood engraftment between immunocompromised mouse strains. Blood 116: 193- 200
41. Meyer LH, Eckhoff SM, Queudeville M, Kraus JM, Giordan M, Stursberg J, Zangrando A, Vendramini E, Moricke A, Zimmermann M, et al (2011) Early relapse in all is identified by time to leukemia in NOD/SCID mice and is characterized by a gene signature involving survival pathways. Cancer Cell 19: 206- 217
42. Morisot S, Wayne AS, Bohana-Kashtan O, Kaplan IM, Gocke CD, Hildreth R, Stetler-Stevenson M, Walker RL, Davis S, Meltzer PS, et al (2010) High frequencies of leukemia stem cells in poor-outcome childhood precursor-B acute lymphoblastic leukemias. Leukemia 24: 1859- 1866
43. Notta F, Mullighan CG, Wang JC, Poeppl A, Doulatov S, Phillips LA, Ma J, Minden MD, Downing JR, Dick JE (2011) Evolution of human BCR-ABL1 lymphoblastic leukaemia-initiating cells. Nature 469: 362- 367
44. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106- 110
45. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ (2008) Efficient tumour formation by single human melanoma cells. Nature 456: 593- 598
46. Quintana E, Shackleton M, Foster HR, Fullen DR, Sabel MS, Johnson TM, Morrison SJ (2010) Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell 18: 510- 523
47. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, De Maria R (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445: 111- 115
48. Schmitz M, Breithaupt P, Scheidegger N, Cario G, Bonapace L, Meissner B, Mirkowska P, Tchinda J, Niggli FK, Stanulla M, et al (2011) Xenografts of highly resistant leukemia recapitulate the clonal composition of the leukemogenic compartment. Blood 118: 1854- 1864
49. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, Chaleff S, Kotb M, Gillies SD, King M, Mangada J, et al (2005) Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol 174: 6477- 6489
50. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821- 5828
51. Somervaille TC, Matheny CJ, Spencer GJ, Iwasaki M, Rinn JL, Witten DM, Chang HY, Shurtleff SA, Downing JR, Cleary ML (2009) Hierarchical maintenance of MLL myeloid leukemia stem cells employs a transcriptional program shared with embryonic rather than adult stem cells. Cell Stem Cell 4: 129- 140
52. Son NH, Joyce B, Hieatt A, Chrest FJ, Yanovski J, Weng NP (2003) Stable telomere length and telomerase expression from naive to memory B-lymphocyte differentiation. Mech Ageing Dev 124: 427- 432
53. Stewart SA, Hahn WC, O'Connor BF, Banner EN, Lundberg AS, Modha P, Mizuno H, Brooks MW, Fleming M, Zimonjic DB, Popescu NC, Weinberg RA (2002) Telomerase contributes to tumorigenesis by a telomere length-independent mechanism. Proc Natl Acad Sci USA 99: 12606- 12611
54. Suryani S, Fulcher DA, Santner-Nanan B, Nanan R, Wong M, Shaw PJ, Gibson J, Williams A, Tangye SG (2010) Differential expression of CD21 identifies developmentally and functionally distinct subsets of human transitional B cells. Blood 115: 519- 529
55. Taussig DC, Miraki-Moud F, Anjos-Afonso F, Pearce DJ, Allen K, Ridler C, Lillington D, Oakervee H, Cavenagh J, Agrawal SG, et al (2008) Anti-CD38 antibody-mediated clearance of human repopulating cells masks the heterogeneity of leukemia-initiating cells. Blood 112: 568- 575
56. Taussig DC, Vargaftig J, Miraki-Moud F, Griessinger E, Sharrock K, Luke T, Lillington D, Oakervee H, Cavenagh J, Agrawal SG, et al (2010) Leukemia-initiating cells from some acute myeloid leukemia patients with mutated nucleophosmin reside in the CD34(-) fraction. Blood 115: 1976- 1984
57. Till JE, McCulloch EA (1961) A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res 14: 213- 222
58. van Zelm MC, van der Burg M, de Ridder D, Barendregt BH, de Haas EF, Reinders MJ, Lankester AC, Revesz T, Staal FJ, van Dongen JJ (2005) Ig gene rearrangement steps are initiated in early human precursor B cell subsets and correlate with specific transcription factor expression. J Immunol 175: 5912- 5922
59. Vormoor HJ (2009) Malignant stem cells in childhood acute lymphoblastic leukemia: the stem cell concept revisited. Cell Cycle 8: 996- 999
60. Williams RT, den Besten W, Sherr CJ (2007) Cytokine-dependent imatinib resistance in mouse BCR-ABL+, Arf-null lymphoblastic leukemia. Genes Dev 21: 2283- 2287
61. Zuber J, Rappaport AR, Luo W, Wang E, Chen C, Vaseva AV, Shi J, Weissmueller S, Fellmann C, Taylor MJ, et al (2011) An integrated approach to dissecting oncogene addiction implicates a Myb-coordinated self-renewal program as essential for leukemia maintenance. Genes Dev 25: 1628- 1640