Characteristics and outcome of patients with acute myeloid leukaemia and t(8;16)(p11;p13): results from an International Collaborative Study.

Abnormal Karyotype Adolescent Adult Aged Antineoplastic Combined Chemotherapy Protocols / therapeutic use Chromosomes, Human, Pair 16 / ultrastructure Chromosomes, Human, Pair 8 / ultrastructure Combined Modality Therapy Consolidation Chemotherapy Disease Progression Disease-Free Survival Female Follow-Up Studies Hematopoietic Stem Cell Transplantation Humans International Cooperation Leukemia, Myeloid, Acute / epidemiology Male Middle Aged Mutation Myelodysplastic Syndromes / epidemiology Neoplasms, Second Primary / chemically induced Oncogene Proteins, Fusion / genetics Remission Induction Survival Analysis Translocation, Genetic Whole Genome Sequencing

acute myeloid leukaemia allogeneic haematopoietic cell transplantation outcome t(8;16)(p11;p13)/MYST3-CREBBP whole-genome sequencing

Journal

British journal of haematology

ISSN: 1365-2141

Titre abrégé: Br J Haematol

Pays: England

ID NLM: 0372544

Informations de publication

Date de publication:
03 2021

Historique:

received: 10 10 2020

accepted: 03 12 2020

pubmed: 3 2 2021

medline: 10 8 2021

entrez: 2 2 2021

Statut: ppublish

Résumé

In acute myeloid leukaemia (AML) t(8;16)(p11;p13)/MYST3-CREBBP is a very rare abnormality. Previous small series suggested poor outcome. We report on 59 patients with t(8;16) within an international, collaborative study. Median age was 52 (range: 16-75) years. AML was de novo in 58%, therapy-related (t-AML) in 37% and secondary after myelodysplastic syndrome (s-AML) in 5%. Cytogenetics revealed a complex karyotype in 43%. Besides MYST3-CREBBP, whole-genome sequencing on a subset of 10 patients revealed recurrent mutations in ASXL1, BRD3, FLT3, MLH1, POLG, TP53, SAMD4B (n = 3, each), EYS, KRTAP9-1 SPTBN5 (n = 4, each), RUNX1 and TET2 (n = 2, each). Complete remission after intensive chemotherapy was achieved in 84%. Median follow-up was 5·48 years; five-year survival rate was 17%. Patients with s-/t-AML (P = 0·01) and those with complex karyotype (P = 0·04) had an inferior prognosis. Allogeneic haematopoietic cell transplantation (allo-HCT) was performed in 21 (36%) patients, including 15 in first complete remission (CR1). Allo-HCT in CR1 significantly improved survival (P = 0·04); multivariable analysis revealed that allo-HCT in CR1 was effective in de novo AML but not in patients with s-AML/t-AML and less in patients exhibiting a complex karyotype. In summary, outcomes of patients with t(8;16) are dismal with chemotherapy, and may be substantially improved with allo-HCT performed in CR1.

Identifiants

DOI: 10.1111/bjh.17336 PMID: 33529373

pubmed: 33529373

doi: 10.1111/bjh.17336

doi:

Substances chimiques

Oncogene Proteins, Fusion 0

Types de publication

Journal Article Multicenter Study Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

Pagination

832-842

Subventions

Organisme : Olympia-Morata fellowship program from the Medical Faculty of the Heidelberg University

Organisme : Ministry of the Czech Republic

ID : 15-25809A

Organisme : NCI NIH HHS

ID : P50 CA100632

Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Références

Haferlach T, Kohlmann A, Klein HU, Ruckert C, Dugas M, Williams PM, et al. AML with translocation t(8;16)(p11;p13) demonstrates unique cytomorphological, cytogenetic, molecular and prognostic features. Leukemia. 2009;23:934-43.

Borrow J, Stanton VP, Andresen JM, Becher R, Behm FG, Chaganti RS, et al. The translocation t(8;16)(p11;p13) of acute myeloid leukemia fuses a putative acetyltransferase to the CREB-binding protein. Nat Genet. 1996;14:33-41.

Champagne N, Pelletier N, Yang X-J. The monocytic leukemia zinc finger protein MOZ is a histone acetyltransferase. Oncogene. 2001;20:404-9.

Jacobson S, Pillus L. Modifying chromatin and concepts of cancer. Curr Opin Genet Dev. 1999;9:175-84.

Allard S, Masson J-Y, Coté J. Chromatin remodeling and the maintenance of genome integrity. Biochim Biophys Acta. 2004;1677:158-64.

Camos M, Esteve J, Jares P, Colomer D, Rozman M, Villamor N, et al. Gene expression profiling of acute myeloid leukemia with translocation t(8;16)(p11;p13) and MYST3-CREBBP rearrangement reveals a distinctive signature with a specific pattern of HOX gene expression. Cancer Res. 2006;66:6947-54.

Gervais C, Murati A, Helias C, Struski S, Eischen A, Lippert E, et al. Acute myeloid leukaemia with 8p11 (MYST3) rearrangement: an integrated cytologic, cytogenetic and molecular study by the groupe francophone de cytogénétique hématologique. Leukemia. 2008;22:1567-75.

Yang XJ, Ullah M. MOZ and MORF, two large MYSTic HATs in normal and cancer stem cells. Oncogene. 2007;26:5408-19.

Chan EM, Chan RJ, Comer EM, Goulet RJ 3rd, Crean CD, Brown ZD, et al. MOZ and MOZ-CBP cooperate with NF-kappaB to activate transcription from NF-kappaBdependent promoters. Exp Hematol. 2007;35:1782-92.

Vo N, Goodman RH. CREB-binding protein and p300 in transcriptional regulation. J Biol Chem. 2001;276:13505-8.

Blobel GA. CREB-binding protein and p300: molecular integrators of hematopoietic transcription. Blood. 2000;95:745-55.

Wadgaonkar R, Phelps KM, Haque Z, Williams AJ, Silverman ES, Collins T. CREB-binding protein is a nuclear integrator of nuclear factor-kappaB and p53 signaling. J Biol Chem. 1999;274:1879-82.

Chen J, Odenike O, Rowley JD. Leukaemogenesis: more than mutant genes. Nat Rev Cancer. 2010;10:23-36.

Coenen EA, Zwaan CM, Reinhardt D, Harrison CJ, Haas OA, de Haas V, et al. Pediatric acute myeloid leukemia with t(8;16)(p11;p13), a distinct clinical and biological entity: a collaborative study by the International-Berlin-Frankfurt-Münster AML-study group. Blood. 2013;122:2704-13.

Bennett JM, Catovsky D, Daniel MT, Flandrin G, Galton DA, Gralnick HR, et al. Proposed revised criteria for the classification of acute myeloid leukemia. a report of the French-American-British Cooperative Group. Ann Intern Med. 1985;103:620-5.

Cheson BD, Bennett JM, Kopecky KJ, Büchner T, Willman CL, Estey EH, et al. Revised recommendations of the International Working Group for Diagnosis, Standardization of Response Criteria, Treatment Outcomes, And Reporting Standards For Therapeutic Trials In Acute Myeloid Leukemia. J Clin Oncol. 2003;21:4642-9.

Mitelman F. ISCN: An international system for human cytogenetic nomenclature. Basel, Switzerland: S. Karger, 1995.

Yokota S, Kiyoi H, Nakao M, Iwai T, Misawa S, Okuda T, et al. Internal tandem duplication of the FLT3 gene is preferentially seen in acute myeloid leukemia and myelodysplastic syndrome among various hematological malignancies. A study on a large series of patients and cell lines. Leukemia. 1997;11:1605-9.

Thiede C, Steudel C, Mohr B, Schaich M, Schäkel U, Platzbecker U, et al. Analysis of FLT3-activating mutations in 979 patients with acute myelogenous leukemia: association with FAB subtypes and identification of subgroups with poor prognosis. Blood. 2002;99:4326-35.

Jabs J, Zickgraf FM, Park J, Wagner S, Jiang X, Jechow K, et al. Screening drug effects in patient-derived cancer cells links organoid responses to genome alterations. Mol Syst Biol. 2017;13(11):955.

Abecasis GRA, Auton A, Brooks LD, DePristo MA, Durbin RM, Handsaker RE, et al. An integrated map of genetic variation from 1,092 human genomes. Nature. 2012;491(7422):56-65.

Tarasov A, Vilella AJ, Cuppen E, Nijman IJ, Prins P. Sambamba: fast processing of NGS alignment formats. Bioinformatics. 2015;31(12):2032-4.

Jones DTW, Jäger N, Kool M, Zichner T, Hutter B, Sultan M, et al. Dissecting the genomic complexity underlying medulloblastoma. Nature. 2012;488(7409):100-5.

Lek M, Karczewski KJ, Minikel EV, Samocha KE, Banks E, Fennell T, et al. Analysis of protein-coding genetic variation in 60,706 humans. Nature. 2016;536(7616):285-91.

Schaich M, Parmentier S, Kramer M, Illmer T, Stölzel F, Röllig C, et al. High-dose cytarabine consolidation with or without additional amsacrine and mitoxantrone in acute myeloid leukemia: results of the prospective randomized AML2003 trial. J Clin Oncol. 2013;31:2094-102.

Grimwade D, Hills RK, Moorman AV, Walker H, Chatters S, Goldstone AH, et al. 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. 2010;116:354-65.

Wheatley K, Brookes CL, Howman AJ, Goldstone AH, Milligan DW, Prentice AG, et al. Prognostic factor analysis of the survival of elderly patients with AML in the MRC AML11 and LRF AML14 trials. Br J Haematol. 2009;145:598-605.

Burnett AK, Russell NH, Culligan D, Cavanagh J, Kell J, Wheatley K, et al. The addition of the farnesyl transferase inhibitor, tipifarnib, to low dose cytarabine does not improve outcome for older patients with AML. Br J Haematol. 2012;158:519-22.

Burnett AK, Russell NH, Hills RK, Kell J, Cavenagh J, Kjeldsen L, et al. A randomized comparison of daunorubicin 90 mg/m2 vs 60 mg/m2 in AML induction: results from the UK NCRI AML17 trial in 1206 patients. Blood. 2015;125:3878-85.

Schemper M, Smith TL. A note on quantifying follow-up in studies of failure time. Control Clin Trials. 1996;17:343-6.

Kaplan E, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc. 1958;53:457-81.

Mantel N, Byar D. Evaluation of response-time data involving transient states: an illustration using heart transplant data. J Am Stat Assoc. 1974;69:81-6.

Andersen P, Gill RD. Cox's regression model for counting processes: a large sample study. Ann Stat. 1982;10:1100-20.

Simon R, Makuch RW. A non-parametric graphical representation of the relationship between survival and the occurrence of an event: application to responder versus non-responder bias. Stat Med. 1984;3:35-44.

Gray RJ. A class of k-sample tests for comparing the cumulative incidence of a competing risk. Ann Stat. 1988;16:1141-54.

R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, 2014.

Gibson CJ, Lindsley RC, Tchekmedyian V, Mar BG, Shi J, Jaiswal S, et al. Hematopoiesis associated with adverse outcomes after autologous stem-cell transplantation for lymphoma. J Clin Oncol. 2017;35:1598-605.

Bari A, Marcheselli L, Marcheselli R, Liardo EV, Pozzi S, Sacchi S, et al. Therapy-related myeloid neoplasm in non-Hodgkin lymphoma survivors. Mediterr J Hematol Infect Dis. 2011;3:e2011065.

Kayser S, Döhner K, Krauter J, Köhne C-H, Horst HA, Held G, et al. The impact of therapy-related acute myeloid leukemia (AML) on outcome in 2853 adult patients with newly diagnosed AML. Blood. 2011;117:2137-45.

Kayser S, Krzykalla J, Elliott MA, Norsworthy K, Gonzales P, Hills RK, et al. Characteristics and outcome of patients with therapy-related acute promyelocytic leukemia front-line treated with or without arsenic trioxide. Leukemia. 2017;31:2347-54.

Takahashi K, Wang F, Kantarjian H, Doss D, Khanna K, Thompson E, et al. Preleukaemic clonal haemopoiesis and risk of therapy-related myeloid neoplasms: a case-control study. Lancet Oncol. 2017;18:100-11.

Gillis NK, Ball M, Zhang Q, Ma Z, Zhao YL, Yoder SJ, et al. Clonal haemopoiesis and therapy-related myeloid malignancies in elderly patients: a proof-of-concept, case-control study. Lancet Oncol. 2017;18:112-21.

Quesnel B, Kantarjian H, Bjergaard JP, Brault P, Estey E, Lai JL, et al. Therapy-related acute myeloid leukemia with t(8;21), inv(16), and t(8;16): a report on 25 cases and review of the literature. J Clin Oncol. 1993;11:2370-9.

Diab A, Zickl L, Abdel-Wahab O, Jhanwar S, Gulam MA, Panageas KS, et al. Acute myeloid leukemia with translocation t(8;16) presents with features which mimic acute promyelocytic leukemia and is associated with poor prognosis. Leuk Res. 2013;37:32-6.

Stone RM, Mandrekar SJ, Sanford BL, Laumann K, Geyer S, Bloomfield CD, et al. Midostaurin plus chemotherapy for acute myeloid leukemia with a FLT3 mutation. N Engl J Med. 2017;377:454-64.

Perl AE, Altman JK, Cortes J, Smith C, Litzow M, Baer MR, et al. Selective inhibition of FLT3 by gilteritinib in relapsed or refractory acute myeloid leukaemia: a multicentre, first-in-human, open-label, phase 1-2 study. Lancet Oncol. 2017;18:1061-75.

Yehudai D, Liyanage SU, Hurren R, Rizoska B, Albertella M, Gronda M, et al. The thymidine dideoxynucleoside analog, alovudine, inhibits the mitochondrial DNA polymerase γ, impairs oxidative phosphorylation and promotes monocytic differentiation in acute myeloid leukemia. Haematologica. 2019;104:963-72.

Kolodner RD, Marsischky GT. Eukaryotic DNA mismatch repair. Curr Opin Genet Dev. 1999;9:89-96.

Kunkel TA, Erie DA. DNA mismatch repair. Annu Rev Biochem. 2005;74:681-710.

Modrich P, Lahue R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu Rev Biochem. 1996;65:101-33.

Li GM. The role of mismatch repair in DNA damage-induced apoptosis. Oncol Res. 1999;11:393-400.

Li GM. Mechanisms and functions of DNA mismatch repair. Cell Res. 2008;18:85-98.

Tervasmäki A, Mantere T, Hartikainen JM, Kauppila S, Lee HM, Koivuluoma S, et al. Rare missense mutations in RECQL and POLG associate with inherited predisposition to breast cancer. Int J Cancer. 2018;1(142):2286-92.

Cancer Genome Atlas Research Network, Ley TJ, Miller C, Ding L, Raphael BJ, Mungall AJ, Robertson A, et al. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N Engl J Med. 2013;368:2059-74.

Yu G, Yin C, Wu F, Jiang L, Zheng Z, Xu D, et al. Gene mutation profile and risk stratification in AML1-ETO-positive acute myeloid leukemia based on next-generation sequencing. Oncol Rep. 2019;42:2333-44.

Mao G, Yuan F, Absher K, Jennings CD, Howard DS, Jordan CT, et al. Preferential loss of mismatch repair function in refractory and relapsed acute myeloid leukemia: potential contribution to AML progression. Cell Res. 2008;18:281-9.

Kitabayashi I, Aikawa Y, Nguyen LA, Yokoyama A, Ohki M. Activation of AML1-mediated transcription by MOZ and inhibition by the MOZ-CBP fusion protein. EMBO J. 2001;20:7184-96.

Kayser S, Schlenk RF, Platzbecker U. Management of patients with acute promyelocytic leukemia. Leukemia. 2018;32:1277-94.

Xie W, Hu S, Xu J, Chen Z, Medeiros LJ, Tang G. Acute myeloid leukemia with t(8;16)(p11.2;p13.3)/KAT6A-CREBBP in adults. Ann Hematol. 2019;98:1149-57.

DiNardo CD, Pratz K, Pullarkat V, Jonas BA, Arellano M, Becker PS, et al. Venetoclax combined with decitabine or azacitidine in treatment-naive, elderly patients with acute myeloid leukemia. Blood. 2019;133:7-17.