Phenotypic characterization of leukemia-initiating stem cells in chronic myelomonocytic leukemia.


Journal

Leukemia
ISSN: 1476-5551
Titre abrégé: Leukemia
Pays: England
ID NLM: 8704895

Informations de publication

Date de publication:
11 2021
Historique:
received: 13 11 2020
accepted: 11 03 2021
revised: 04 02 2021
pubmed: 1 4 2021
medline: 31 12 2021
entrez: 31 3 2021
Statut: ppublish

Résumé

Chronic myelomonocytic leukemia (CMML) is a stem cell-derived neoplasm characterized by dysplasia, uncontrolled expansion of monocytes, and substantial risk to transform to secondary acute myeloid leukemia (sAML). So far, little is known about CMML-initiating cells. We found that leukemic stem cells (LSC) in CMML reside in a CD34

Identifiants

pubmed: 33785864
doi: 10.1038/s41375-021-01227-z
pii: 10.1038/s41375-021-01227-z
pmc: PMC7611912
mid: EMS119146
doi:

Substances chimiques

Antigens, CD34 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3176-3187

Subventions

Organisme : Austrian Science Fund FWF
ID : F 4704
Pays : Austria
Organisme : Austrian Science Fund FWF
ID : P 30625
Pays : Austria

Informations de copyright

© 2021. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Storniolo AM, Moloney WC, Rosenthal DS, Cox C, Bennett JM. Chronic myelomonocytic leukemia. Leukemia. 1990;4:766–70.
pubmed: 2232890
Bennett JM, Catovsky D, Daniel MT, Flandrin G, Galton DA, Gralnick HR, et al. Proposals for the classification of the myelodysplastic syndromes. Br J Haematol. 1982;51:189–99.
pubmed: 6952920 doi: 10.1111/j.1365-2141.1982.tb08475.x
Bennett JM, Catovsky D, Daniel MT, Flandrin G, Galton DA, Gralnick H, et al. The chronic myeloid leukaemias: guidelines for distinguishing chronic granulocytic, atypical chronic myeloid, and chronic myelomonocytic leukaemia. Proposals by the French–American–British cooperative leukaemia group. Br J Haematol. 1994;87:746–54.
pubmed: 7986717 doi: 10.1111/j.1365-2141.1994.tb06734.x
Patnaik MM, Parikh SA, Hanson CA, Tefferi A. Chronic myelomonocytic leukaemia: a concise clinical and pathophysiological review. Br J Haematol. 2014;165:273–86.
pubmed: 24467717 doi: 10.1111/bjh.12756
McCullough KB, Patnaik MM. Chronic myelomonocytic leukemia: a genetic and clinical Update. Curr Hematol Malig Rep. 2015;10:292–302.
pubmed: 26122388 doi: 10.1007/s11899-015-0271-4
Arber DA, Orazi A, Hasserjian R, Thiele J, Borowitz MJ, Beau MML, et al. The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood. 2016;127:2391–405.
pubmed: 27069254 doi: 10.1182/blood-2016-03-643544
Orazi A, Bennett JM, Germing U, Brunning RD, Bain BJ, Cazzola M et al. Chronic myelomonocytic leukaemia. In: WHO classification of tumours of haematopoietic and lymphoid tissues. IARC Press, 2017, pp 82–86.
Kohlmann A, Grossmann V, Klein H-U, Schindela S, Weiss T, Kazak B, et al. Next-generation sequencing technology reveals a characteristic pattern of molecular mutations in 72.8% of chronic myelomonocytic leukemia by detecting frequent alterations in TET2, CBL, RAS, and RUNX1. J Clin Oncol. 2010;28:3858–65.
pubmed: 20644105 doi: 10.1200/JCO.2009.27.1361
Itzykson R, Duchmann M, Lucas N, Solary E. CMML: clinical and molecular aspects. Int J Hematol. 2017;105:711–9.
pubmed: 28455647 doi: 10.1007/s12185-017-2243-z
Patnaik MM, Tefferi A. Chronic myelomonocytic leukemia: 2020 update on diagnosis, risk stratification and management. Am J Hematol. 2020;95:97–115.
pubmed: 31736132 doi: 10.1002/ajh.25684
Pich A, Riera L, Sismondi F, Godio L, Davico Bonino L, Marmont F, et al. JAK2V617F activating mutation is associated with the myeloproliferative type of chronic myelomonocytic leukaemia. J Clin Pathol. 2009;62:798–801.
pubmed: 19734476 doi: 10.1136/jcp.2009.065904
Gur HD, Loghavi S, Garcia-Manero G, Routbort M, Kanagal-Shamanna R, Quesada A, et al. Chronic myelomonocytic leukemia with fibrosis is a distinct disease subset with myeloproliferative features and frequent JAK2 p.V617F mutations. Am J Surg Pathol. 2018;42:799–806.
pubmed: 29596070 doi: 10.1097/PAS.0000000000001058
Sperr WR, Horny H-P, Valent P. Spectrum of associated clonal hematologic non-mast cell lineage disorders occurring in patients with systemic mastocytosis. Int Arch Allergy Immunol. 2002;127:140–2.
pubmed: 11919425 doi: 10.1159/000048186
Sotlar K, Fridrich C, Mall A, Jaussi R, Bültmann B, Valent P, et al. Detection of c-kit point mutation Asp-816 –> Val in microdissected pooled single mast cells and leukemic cells in a patient with systemic mastocytosis and concomitant chronic myelomonocytic leukemia. Leuk Res. 2002;26:979–84.
pubmed: 12363464 doi: 10.1016/S0145-2126(02)00041-3
Valent P, Orazi A, Savona MR, Patnaik MM, Onida F, van de Loosdrecht AA, et al. Proposed diagnostic criteria for classical chronic myelomonocytic leukemia (CMML), CMML variants and pre-CMML conditions. Haematologica. 2019;104:1935–49.
pubmed: 31048353 pmcid: 6886439 doi: 10.3324/haematol.2019.222059
Patnaik MM, Vallapureddy R, Lasho TL, Hoversten KP, Finke CM, Ketterling RP, et al. A comparison of clinical and molecular characteristics of patients with systemic mastocytosis with chronic myelomonocytic leukemia to CMML alone. Leukemia. 2018;32:1850–6.
pubmed: 29712989 doi: 10.1038/s41375-018-0121-1
Itzykson R, Kosmider O, Renneville A, Gelsi-Boyer V, Meggendorfer M, Morabito M, et al. Prognostic score including gene mutations in chronic myelomonocytic leukemia. J Clin Oncol. 2013;31:2428–36.
doi: 10.1200/JCO.2012.47.3314 pubmed: 23690417
Elena C, Gallì A, Such E, Meggendorfer M, Germing U, Rizzo E, et al. Integrating clinical features and genetic lesions in the risk assessment of patients with chronic myelomonocytic leukemia. Blood. 2016;128:1408–17.
pubmed: 27385790 pmcid: 5036538 doi: 10.1182/blood-2016-05-714030
Palomo L, Garcia O, Arnan M, Xicoy B, Fuster F, Cabezón M, et al. Targeted deep sequencing improves outcome stratification in chronic myelomonocytic leukemia with low risk cytogenetic features. Oncotarget. 2016;7:57021–35.
pubmed: 27486981 pmcid: 5302970 doi: 10.18632/oncotarget.10937
Itzykson R, Fenaux P, Bowen D, Cross NCP, Cortes J, De Witte T, et al. Diagnosis and treatment of chronic myelomonocytic leukemias in adults: recommendations from the European hematology association and the European leukemiaNet. Hemasphere. 2018;2:e150.
pubmed: 31723789 pmcid: 6745959 doi: 10.1097/HS9.0000000000000150
Kröger N, Zabelina T, Guardiola P, Runde V, Sierra J, Van Biezen A, et al. Allogeneic stem cell transplantation of adult chronic myelomonocytic leukaemia. A report on behalf of the chronic leukaemia working party of the european group for blood and marrow transplantation (EBMT). Br J Haematol. 2002;118:67–73.
pubmed: 12100129 doi: 10.1046/j.1365-2141.2002.03552.x
de Witte T, Bowen D, Robin M, Malcovati L, Niederwieser D, Yakoub-Agha I, et al. Allogeneic hematopoietic stem cell transplantation for MDS and CMML: recommendations from an international expert panel. Blood. 2017;129:1753–62.
pubmed: 28096091 pmcid: 5524528 doi: 10.1182/blood-2016-06-724500
Dick JE, Lapidot T, Pflumio F. Transplantation of normal and leukemic human bone marrow into immune-deficient mice: development of animal models for human hematopoiesis. Immunol Rev. 1991;124:25–43.
pubmed: 1804779 doi: 10.1111/j.1600-065X.1991.tb00614.x
Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367:645–8.
pubmed: 7509044 doi: 10.1038/367645a0
Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3:730–7.
pubmed: 9212098 doi: 10.1038/nm0797-730
Eisterer W, Jiang X, Christ O, Glimm H, Lee KH, Pang E, et al. Different subsets of primary chronic myeloid leukemia stem cells engraft immunodeficient mice and produce a model of the human disease. Leukemia. 2005;19:435–41.
pubmed: 15674418 doi: 10.1038/sj.leu.2403649
Kavalerchik E, Goff D, Jamieson CHM. Chronic myeloid leukemia stem cells. J Clin Oncol. 2008;26:2911–5.
pubmed: 18539972 doi: 10.1200/JCO.2008.17.5745
Krause DS, Van Etten RA. Right on target: eradicating leukemic stem cells. Trends Mol Med. 2007;13:470–81.
pubmed: 17981087 pmcid: 4344828 doi: 10.1016/j.molmed.2007.09.003
Misaghian N, Ligresti G, Steelman LS, Bertrand FE, Bäsecke J, Libra M, et al. Targeting the leukemic stem cell: the Holy Grail of leukemia therapy. Leukemia. 2009;23:25–42.
pubmed: 18800146 doi: 10.1038/leu.2008.246
Copland M. Chronic myelogenous leukemia stem cells: what’s new? Curr Hematol Malig Rep. 2009;4:66–73.
pubmed: 20425417 doi: 10.1007/s11899-009-0010-9
Valent P. Targeting of leukemia-initiating cells to develop curative drug therapies: straightforward but nontrivial concept. Curr Cancer Drug Targets. 2011;11:56–71.
pubmed: 21062243 doi: 10.2174/156800911793743655
Taussig DC, Miraki-Moud F, Anjos-Afonso F, Pearce DJ, Allen K, Ridler C, et al. Anti-CD38 antibody-mediated clearance of human repopulating cells masks the heterogeneity of leukemia-initiating cells. Blood. 2008;112:568–75.
pubmed: 18523148 doi: 10.1182/blood-2007-10-118331
Jamieson CHM, Ailles LE, Dylla SJ, Muijtjens M, Jones C, Zehnder JL, et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med. 2004;351:657–67.
pubmed: 15306667 doi: 10.1056/NEJMoa040258
Järås M, Johnels P, Hansen N, Agerstam H, Tsapogas P, Rissler M, et al. Isolation and killing of candidate chronic myeloid leukemia stem cells by antibody targeting of IL-1 receptor accessory protein. Proc Natl Acad Sci USA. 2010;107:16280–5.
pubmed: 20805474 pmcid: 2941341 doi: 10.1073/pnas.1004408107
Herrmann H, Sadovnik I, Cerny-Reiterer S, Rülicke T, Stefanzl G, Willmann M, et al. Dipeptidylpeptidase IV (CD26) defines leukemic stem cells (LSC) in chronic myeloid leukemia. Blood. 2014;123:3951–62.
pubmed: 24778155 doi: 10.1182/blood-2013-10-536078
Saito Y, Kitamura H, Hijikata A, Tomizawa-Murasawa M, Tanaka S, Takagi S, et al. Identification of therapeutic targets for quiescent, chemotherapy-resistant human leukemia stem cells. Sci Transl Med. 2010;2:17ra9–17ra9.
pubmed: 20371479 pmcid: 3005290 doi: 10.1126/scitranslmed.3000349
Hosen N, Park CY, Tatsumi N, Oji Y, Sugiyama H, Gramatzki M, et al. CD96 is a leukemic stem cell-specific marker in human acute myeloid leukemia. Proc Natl Acad Sci USA. 2007;104:11008–13.
pubmed: 17576927 pmcid: 1904175 doi: 10.1073/pnas.0704271104
van Rhenen A, van Dongen GAMS, Kelder A, Rombouts EJ, Feller N, Moshaver B, et al. The novel AML stem cell associated antigen CLL-1 aids in discrimination between normal and leukemic stem cells. Blood. 2007;110:2659–66.
pubmed: 17609428 doi: 10.1182/blood-2007-03-083048
Majeti R, Chao MP, Alizadeh AA, Pang WW, Jaiswal S, Gibbs KD, et al. CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell. 2009;138:286–99.
pubmed: 19632179 pmcid: 2726837 doi: 10.1016/j.cell.2009.05.045
Zhang Y, He L, Selimoglu-Buet D, Jego C, Morabito M, Willekens C, et al. Engraftment of chronic myelomonocytic leukemia cells in immunocompromised mice supports disease dependency on cytokines. Blood Adv. 2017;1:972–9.
pubmed: 29296739 pmcid: 5737594 doi: 10.1182/bloodadvances.2017004903
Yoshimi A, Balasis ME, Vedder A, Feldman K, Ma Y, Zhang H, et al. Robust patient-derived xenografts of MDS/MPN overlap syndromes capture the unique characteristics of CMML and JMML. Blood. 2017;130:397–407.
pubmed: 28576879 pmcid: 5533204 doi: 10.1182/blood-2017-01-763219
Ramshaw HS, Bardy PG, Lee MA, Lopez AF. Chronic myelomonocytic leukemia requires granulocyte-macrophage colony-stimulating factor for growth in vitro and in vivo. Exp Hematol. 2002;30:1124–31.
pubmed: 12384142 doi: 10.1016/S0301-472X(02)00903-7
Rongvaux A, Willinger T, Martinek J, Strowig T, Gearty SV, Teichmann LL, et al. Development and function of human innate immune cells in a humanized mouse model. Nat Biotechnol. 2014;32:364–72.
pubmed: 24633240 pmcid: 4017589 doi: 10.1038/nbt.2858
Valent P, Schmidt G, Besemer J, Mayer P, Zenke G, Liehl E, et al. Interleukin-3 is a differentiation factor for human basophils. Blood. 1989;73:1763–9.
pubmed: 2469498 doi: 10.1182/blood.V73.7.1763.1763
Saito H, Hatake K, Dvorak AM, Leiferman KM, Donnenberg AD, Arai N, et al. Selective differentiation and proliferation of hematopoietic cells induced by recombinant human interleukins. PNAS. 1988;85:2288–92.
pubmed: 3258425 pmcid: 279976 doi: 10.1073/pnas.85.7.2288
Sadovnik I, Hoelbl-Kovacic A, Herrmann H, Eisenwort G, Cerny-Reiterer S, Warsch W, et al. Identification of CD25 as STAT5-dependent growth regulator of leukemic stem cells in Ph+ CML. Clin Cancer Res. 2016;22:2051–61.
pubmed: 26607600 doi: 10.1158/1078-0432.CCR-15-0767
Hadzijusufovic E, Keller A, Berger D, Greiner G, Wingelhofer B, Witzeneder N, et al. STAT5 is expressed in CD34
pmcid: 7225958 doi: 10.3390/cancers12041021
Wingelhofer B, Neubauer HA, Valent P, Han X, Constantinescu SN, Gunning PT, et al. Implications of STAT3 and STAT5 signaling on gene regulation and chromatin remodeling in hematopoietic cancer. Leukemia. 2018;32:1713–26.
pubmed: 29728695 pmcid: 6087715 doi: 10.1038/s41375-018-0117-x
Wingelhofer B, Maurer B, Heyes EC, Cumaraswamy AA, Berger-Becvar A, de Araujo ED, et al. Pharmacologic inhibition of STAT5 in acute myeloid leukemia. Leukemia. 2018;32:1135–46.
pubmed: 29472718 pmcid: 5940656 doi: 10.1038/s41375-017-0005-9
Müller‐Thomas C, Heider M, Piontek G, Schlensog M, Bassermann F, Kirchner T, et al. Prognostic value of indoleamine 2,3 dioxygenase in patients with higher‐risk myelodysplastic syndromes treated with azacytidine. Br J Haematol. 2020;190:361–70.
pubmed: 32350858 doi: 10.1111/bjh.16652
Mangaonkar AA, Reichard KK, Binder M, Coltro G, Lasho TL, Carr RM, et al. Bone marrow dendritic cell aggregates associate with systemic immune dysregulation in chronic myelomonocytic leukemia. Blood Adv. 2020;4:5425–30.
pubmed: 33152058 pmcid: 7656937 doi: 10.1182/bloodadvances.2020002415
Lou Y, Shao L, Mao L, Lu Y, Ma Y, Fan C, et al. Efficacy and predictive factors of venetoclax combined with azacitidine as salvage therapy in advanced acute myeloid leukemia patients: a multicenter retrospective study. Leuk Res. 2020;91:106317.
pubmed: 32092584 doi: 10.1016/j.leukres.2020.106317

Auteurs

Gregor Eisenwort (G)

Department of Medicine I, Division of Hematology and Hemostaseology, Medical University of Vienna, Vienna, Austria.
Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria.

Irina Sadovnik (I)

Department of Medicine I, Division of Hematology and Hemostaseology, Medical University of Vienna, Vienna, Austria.
Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria.

Alexandra Keller (A)

Department of Medicine I, Division of Hematology and Hemostaseology, Medical University of Vienna, Vienna, Austria.

Daniel Ivanov (D)

Department of Medicine I, Division of Hematology and Hemostaseology, Medical University of Vienna, Vienna, Austria.

Barbara Peter (B)

Department of Medicine I, Division of Hematology and Hemostaseology, Medical University of Vienna, Vienna, Austria.
Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria.

Daniela Berger (D)

Department of Medicine I, Division of Hematology and Hemostaseology, Medical University of Vienna, Vienna, Austria.
Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria.

Gabriele Stefanzl (G)

Department of Medicine I, Division of Hematology and Hemostaseology, Medical University of Vienna, Vienna, Austria.
Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria.

Karin Bauer (K)

Department of Medicine I, Division of Hematology and Hemostaseology, Medical University of Vienna, Vienna, Austria.
Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria.

Katharina Slavnitsch (K)

Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria.
Institute of Laboratory Animal Science, University of Veterinary Medicine Vienna, Vienna, Austria.

Georg Greiner (G)

Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria.
Department of Laboratory Medicine, Medical University of Vienna, Vienna, Austria.
Ihr Labor, Medical Diagnostic Laboratories, Vienna, Austria.

Karoline V Gleixner (KV)

Department of Medicine I, Division of Hematology and Hemostaseology, Medical University of Vienna, Vienna, Austria.
Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria.

Wolfgang R Sperr (WR)

Department of Medicine I, Division of Hematology and Hemostaseology, Medical University of Vienna, Vienna, Austria.
Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria.

Michael Willmann (M)

Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria.
Department for Companion Animals and Horses, Clinic for Internal Medicine, University of Veterinary Medicine Vienna, Vienna, Austria.

Heinz Sill (H)

Department of Internal Medicine, Division of Hematology, Medical University of Graz, Graz, Austria.

Peter Bettelheim (P)

Elisabethinen Hospital Linz, Linz, Austria.

Klaus Geissler (K)

Medical School, Sigmund Freud University, Vienna, Austria.

Michael Deininger (M)

Division of Hematologic Malignancies, Department of Internal Medicine, University of Utah, Salt Lake City, UT, USA.

Thomas Rülicke (T)

Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria.
Institute of Laboratory Animal Science, University of Veterinary Medicine Vienna, Vienna, Austria.

Peter Valent (P)

Department of Medicine I, Division of Hematology and Hemostaseology, Medical University of Vienna, Vienna, Austria. peter.valent@meduniwien.ac.at.
Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria. peter.valent@meduniwien.ac.at.

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