Prognostic significance of combined MN1, ERG, BAALC, and EVI1 (MEBE) expression in patients with myelodysplastic syndromes

Annals of Hematology

Volumn 91, Issue 8, 2012, Pages 1221-1233

  Thol, Felicitas ^a   Yun, Haiyang ^a   Sonntag, Ann Kathrin ^a   Damm, Frederik ^a   Weissinger, Eva M ^a   Krauter, Jürgen ^a   Wagner, Katharina ^a   Morgan, Michael ^a   Wichmann, Martin ^a   Göhring, Gudrun ^a   Bug, Gesine ^b   Ottmann, Oliver ^b   Hofmann, Wolf Karsten ^c   Schambach, Axel ^a   Schlegelberger, Brigitte ^a   Haferlach, Torsten ^d   Bowen, David ^e   Mills, Ken ^f   Ganser, Arnold ^a   Heuser, Michael ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d MLL MUNICH LEUKEMIA LABORATORY   (Germany)

^e LEEDS TEACHING HOSPITALS NHS TRUST   (United Kingdom)

^f QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Gene expression; MDS; Prognosis; Score; Splicing

Indexed keywords

ISOCITRATE DEHYDROGENASE 2; MYC PROTEIN; TRANSCRIPTION FACTOR ERG; TRANSCRIPTION FACTOR FLI 1;

ACUTE GRANULOCYTIC LEUKEMIA; ADULT; AGED; ANIMAL CELL; ARTICLE; ASXL1 GENE; BAALC GENE; CLINICAL FEATURE; CONTROLLED STUDY; DISEASE COURSE; ERG GENE; EVI1 GENE; FEMALE; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; IDH1 GENE; KARYOTYPE; MAJOR CLINICAL STUDY; MALE; MN1 GENE; MOUSE; MYELODYSPLASTIC SYNDROME; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGNOSIS; PROTEIN DNA BINDING; RISK ASSESSMENT; SCORING SYSTEM; SURVIVAL TIME; VALIDATION PROCESS;

EID: 85027941662     PISSN: 09395555     EISSN: 14320584     Source Type: Journal    
DOI: 10.1007/s00277-012-1457-7     Document Type: Article

References (55)

1. Cazzola M, Malcovati L (2010) Prognostic classification and risk assessment in myelodysplastic syndromes. Hematol Oncol Clin North Am 24:459-468
2. Greenberg P, Cox C, LeBeau MM et al (1997) International scoring system for evaluating prognosis in myelodysplastic syndromes. Blood 89:2079-2088 (Pubitemid 27132124)
3. Garcia-Manero G, Shan J, Faderl S et al (2008) A prognostic score for patients with lower risk myelodysplastic syndrome. Leukemia 22:538-543 (Pubitemid 351386723)
4. Thol F, Friesen I, Damm F et al (2011) Prognostic Significance of ASXL1 Mutations in patients with myelodysplastic syndromes. J Clin Oncol 29:2499-2506
5. Bejar R, Stevenson K, Abdel-Wahab O et al (2011) Clinical effect of point mutations in myelodysplastic syndromes. N Engl J Med 364:2496-2506
6. Heuser M, Beutel G, Krauter J et al (2006) High meningioma 1 (MN1) expression as a predictor for poor outcome in acute myeloid leukemia with normal cytogenetics. Blood 108:3898-3905 (Pubitemid 44864574)
7. Heuser M, Argiropoulos B, Kuchenbauer F et al (2007) MN1 overexpression induces acute myeloid leukemia in mice and predicts ATRA resistance in patients with AML. Blood 110:1639-1647 (Pubitemid 47443982)
8. Langer C, Marcucci G, Holland KB et al (2009) Prognostic importance of MN1 transcript levels, and biologic insights from MN1-associated gene and microRNA expression signatures in cytogenetically normal acute myeloid leukemia: a cancer and leukemia group B study. J Clin Oncol 27:3198-3204
9. Baldus CD, Tanner SM, Ruppert AS et al (2003) BAALC expression predicts clinical outcome of de novo acute myeloid leukemia patients with normal cytogenetics: a Cancer and Leukemia Group B Study. Blood 102:1613-1618 (Pubitemid 37022550)
10. Baldus CD, Thiede C, Soucek S et al (2006) BAALC expression and FLT3 internal tandem duplication mutations in acute myeloid leukemia patients with normal cytogenetics: prognostic implications. J Clin Oncol 24:790-797 (Pubitemid 46622046)
11. Marcucci G, Maharry K, Whitman SP et al (2007) High expression levels of the ETS-related gene, ERG, predict adverse outcome and improve molecular risk-based classification of cytogenetically normal acute myeloid leukemia: a Cancer and Leukemia Group B Study. J Clin Oncol 25:3337-3343 (Pubitemid 47325620)
12. Groschel S, Lugthart S, Schlenk RF et al (2010) High EVI1 expression predicts outcome in younger adult patients with acute myeloid leukemia and is associated with distinct cytogenetic abnormalities. J Clin Oncol 28:2101-2107
13. Damm F, Oberacker T, Thol F et al (2011) Prognostic importance of histone methyltransferase MLL5 expression in acute myeloid leukemia. J Clin Oncol 29:682-689
14. Santamaria CM, Chillon MC, Garcia-Sanz R et al (2009) Molecular stratification model for prognosis in cytogenetically normal acute myeloid leukemia. Blood 114:148-152
15. Heuser M, Yun H, Berg T et al (2011) Cell of origin in AML: susceptibility to MN1-induced transformation is regulated by the MEIS1/AbdB-like HOX protein complex. Cancer Cell 20:39-52
16. Heuser M, Berg T, Kuchenbauer F et al (2012) Functional role of BAALC in leukemogenesis. Leukemia 26(3):532-536
17. Baldus CD, Tanner SM, Kusewitt DF et al (2003) BAALC, a novel marker of human hematopoietic progenitor cells. Exp Hematol 31:1051-1056 (Pubitemid 37329749)
18. Tsuzuki S, Taguchi O, Seto M (2011) Promotion and maintenance of leukemia by ERG. Blood 117:3858-3868
19. Buonamici S, Li D, Chi Y et al (2004) EVI1 induces myelodysplastic syndrome in mice. J Clin Invest 114:713-719 (Pubitemid 39582822)
20. Goyama S, Yamamoto G, Shimabe M et al (2008) Evi-1 is a critical regulator for hematopoietic stem cells and transformed leukemic cells. Cell Stem Cell 3:207-220
21. Metzeler KH, Dufour A, Benthaus T et al (2009) ERG expression is an independent prognostic factor and allows refined risk stratification in cytogenetically normal acute myeloid leukemia: a comprehensive analysis of ERG, MN1, and BAALC transcript levels using oligonucleotide microarrays. J Clin Oncol 27:5031-5038
22. Valk PJ, Verhaak RG, Beijen MA et al (2004) Prognostically useful gene-expression profiles in acute myeloid leukemia. N Engl J Med 350:1617-1628 (Pubitemid 38528701)
23. Hofmann WK, Ganser A, Seipelt G et al (1999) Treatment of patients with low-risk myelodysplastic syndromes using a combination of all-trans retinoic acid, interferon alpha, and granulocyte colony-stimulating factor. Ann Hematol 78:125-130 (Pubitemid 29145894)
24. Stadler M, Germing U, Kliche KO et al (2004) A prospective, randomised, phase II study of horse antithymocyte globulin vs rabbit antithymocyte globulin as immune-modulating therapy in patients with low-risk myelodysplastic syndromes. Leukemia 18:460-465 (Pubitemid 38425859)
25. Passweg JR, Giagounidis AA, Simcock M et al (2011) Immunosuppressive therapy for patients with myelodysplastic syndrome: a prospective randomized multicenter phase III trial comparing antithymocyte globulin plus cyclosporine with best supportive care- SAKK 33/99. J Clin Oncol 29:303-309
26. Porter J (1989) Oral iron chelators: prospects for future development. Eur J Haematol 43:271-285 (Pubitemid 20022000)
27. Chou WC, Huang HH, Hou HA et al (2010) Distinct clinical and biological features of de novo acute myeloid leukemia with additional sex comb-like 1 (ASXL1) mutations. Blood 115:2749-2754
28. Thol F, Weissinger EM, Krauter J et al (2010) IDH1 mutations in patients with myelodysplastic syndromes are associated with an unfavorable prognosis. Haematologica 95:1668-1674
29. Thol F, Damm F, Wagner K et al (2010) Prognostic impact of IDH2 mutations in cytogenetically normal acute myeloid leukemia. Blood 116:614-616
30. Thol F, Damm F, Lüdeking A et al (2011) Incidence and prognostic influence of DNMT3A mutations in acute myeloid leukemia. J Clin Oncol 29:2889-2896
31. Damm F, Thol F, Kosmider O et al. SF3B1 mutations in myelodysplastic syndromes: clinical associations and prognostic implications. Leukemia 2011; Advance Online Publication
32. Barjesteh van Waalwijk van Doorn-Khosrovani S, Erpelinck C, van Putten WL et al (2003) High EVI1 expression predicts poor survival in acute myeloid leukemia: a study of 319 de novo AML patients. Blood 101:837-845 (Pubitemid 36139348)
33. Mills KI, Kohlmann A, Williams PM et al (2009) Microarraybased classifiers and prognosis models identify subgroups with distinct clinical outcomes and high risk of AML transformation of myelodysplastic syndrome. Blood 114:1063-1072
34. Barrett T, Suzek TO, Troup DB et al (2005) NCBI GEO: mining millions of expression profiles-database and tools. Nucleic Acids Res 33:D562-D566 (Pubitemid 40207937)
35. Subramanian A, Tamayo P, Mootha VK et al (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102:15545-15550 (Pubitemid 41528093)
36. Cui JW, Li YJ, Sarkar A et al (2007) Retroviral insertional activation of the Fli-3 locus in erythroleukemias encoding a cluster of microRNAs that convert Epo-induced differentiation to proliferation. Blood 110:2631-2640 (Pubitemid 47523187)
37. Tiemann U, Sgodda M, Warlich E et al (2011) Optimal reprogramming factor stoichiometry increases colony numbers and affects molecular characteristics of murine induced pluripotent stem cells. Cytometry A 79:426-435
38. Korn EL (1986) Censoring distributions as a measure of follow-up in survival analysis. Stat Med 5:255-260
39. Cox D (1972) Regression models and life tables. J R Stat Soc B 34:187-202
40. Thol F, Winschel C, Ludeking A et al (2011) Rare occurrence of DNMT3A mutations in myelodysplastic syndromes. Haematologica 96:1870-1873
41. Wilson NK, Foster SD, Wang X et al (2010) Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 7:532-544
42. Kandilci A, Grosveld GC (2009) Reintroduction of CEBPA inMN1- overexpressing hematopoietic cells prevents their hyperproliferation and restores myeloid differentiation. Blood 114:1596-1606
43. Salek-Ardakani S, Smooha G, de Boer J et al (2009) ERG is a megakaryocytic oncogene. Cancer Res 69:4665-4673
44. Thoms JA, Birger Y, Foster S et al (2011) ERG promotes T-acute lymphoblastic leukemia and is transcriptionally regulated in leukemic cells by a stem cell enhancer. Blood 117:7079-7089
45. Modlich U, Schambach A, Brugman MH et al (2008) Leukemia induction after a single retroviral vector insertion in Evi1 or Prdm 16. Leukemia 22:1519-1528
46. Stein S, Ott MG, Schultze-Strasser S et al (2010) Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat Med 16:198-204
47. Kataoka K, Sato T, Yoshimi A et al (2011) Evi1 is essential for hematopoietic stem cell self-renewal, and its expression marks hematopoietic cells with long-term multilineage repopulating activity. J Exp Med 208:2403-2416
48. Pradee T (2011) Over Expression of MN1 accelerates leukemia onset and confers resistance to chemotherapy by suppression of p53 and Bim. ASH Abstract 118:2501
49. Pellagatti A, Cazzola M, Giagounidis A et al (2010) Deregulated gene expression pathways in myelodysplastic syndrome hematopoietic stem cells. Leukemia 24:756-764
50. Nikpour M, Pellagatti A, Liu A et al (2010) Gene expression profiling of erythroblasts from refractory anaemia with ring sideroblasts (RARS) and effects of G-CSF. Br J Haematol 149:844-854
51. Papaemmanuil E, Cazzola M, Boultwood J et al (2011) Somatic SF3B1 mutation in myelodysplasia with ring sideroblasts. N Engl J Med 365:1384-1395
52. Yoshida K, Sanada M, Shiraishi Y et al (2011) Frequent pathway mutations of splicing machinery in myelodysplasia. Nature 478:64-69
53. Thol F, Kade S, Schlarmann C et al (2012) Frequency and prognostic impact of mutations in SRSF2, U2AF1, and ZRSR2 in patients with myelodysplastic syndromes. Blood. doi:10.1182/ blood-2011-12-399337
54. Damm F, Kosmider O, Gelsi-Boyer V et al (2012) Mutations affecting mRNA splicing define distinct clinical phenotypes and correlate with patient outcome in myelodysplastic syndromes. Blood. doi:10.1182/blood-2011-12-400994
55. Makishima H, Visconte V, Sakaguchi H et al (2012) Mutations in the spliceosome machinery, a novel and ubiquitous pathway in leukemogenesis. Blood. doi:10.1182/blood-2011-12-399774