ATM mutation rather than BIRC3 deletion and/or mutation predicts reduced survival in 11q-deleted chronic lymphocytic leukemia: Data from the UK LRF CLL4 trial

Haematologica

Volumn 99, Issue 4, 2014, Pages 736-742

  Rose Zerilli, Matthew J J ^a   Forster, Jade ^a   Parker, Helen ^a   Parker, Anton ^b   Rodri, Ana Éguez ^c   Chaplin, Tracy ^d   Gardiner, Anne ^b   Steele, Andrew J ^a   Collins, Andrew ^a   Young, Bryan D ^d   Skowronska, Anna ^e   Catovsky, Daniel ^f   Stankovic, Tatjana ^e   Oscier, David G ^a,b   Strefford, Jonathan C ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b ROYAL BOURNEMOUTH HOSPITAL   (United Kingdom)

^c CSIC   (Spain)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^e UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^f INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; PROTEIN P53; ANTINEOPLASTIC AGENT; BIRC3 PROTEIN, HUMAN; INHIBITOR OF APOPTOSIS PROTEIN;

ADULT; AGED; ARTICLE; BIRC3 GENE; CHRONIC LYMPHATIC LEUKEMIA; COHORT ANALYSIS; DNA DAMAGE; DNA EXTRACTION; FEMALE; GENE; GENE DELETION; GENE MUTATION; GENOMIC IN SITU HYBRIDIZATION; HUMAN; JACOBSEN SYNDROME; MAJOR CLINICAL STUDY; MALE; MICROARRAY ANALYSIS; OVERALL SURVIVAL; PROGRESSION FREE SURVIVAL; QUANTITATIVE ASSAY; SINGLE NUCLEOTIDE POLYMORPHISM; TREATMENT OUTCOME; VERY ELDERLY; CANCER STAGING; CHROMOSOME 11; CHROMOSOME ABERRATION; GENETICS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MIDDLE AGED; MORTALITY; MUTATION; OUTCOME ASSESSMENT; PROGNOSIS;

ADULT; AGED; AGED, 80 AND OVER; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CHROMOSOME ABERRATIONS; CHROMOSOMES, HUMAN, PAIR 11; FEMALE; GENE DELETION; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; MIDDLE AGED; MUTATION; NEOPLASM STAGING; PATIENT OUTCOME ASSESSMENT; POLYMORPHISM, SINGLE NUCLEOTIDE; PROGNOSIS; SEQUENCE DELETION;

EID: 84897434576     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2013.098574     Document Type: Article

References (40)

1. Fegan C, Robinson H, Thompson P, Whittaker JA, White D. Karyotypic evolution in CLL: identification of a new subgroup of patients with deletions of 11q and advanced or progressive disease. Leukemia. 1995;9(12):2003-8.
2. Döhner H, Stilgenbauer S, James MR, Benner A, Weilguni T, Bentz M, et al. 11q deletions identify a new subset of B-cell chronic lymphocytic leukemia characterized by extensive nodal involvement and inferior prognosis. Blood. 1997; 89(7):2516-22.
3. Neilson JR, Auer R, White D, Bienz N, Waters JJ, Whittaker JA, et al. Deletions at 11q identify a subset of patients with typical CLL who show consistent Cytogenetic analysis. Leukemia. 1997;11(11):1929-32.
4. Trbusek M, Malcikova J, Smardova J, Kuhrova V, Mentzlova D, Francova H, et al. Inactivation of p53 and deletion of ATM in B-CLL patients in relation to IgVH mutation status and previous treatment. Leukemia. 2006;20(6):1159-61.
5. Hallek M, Fischer K, Fingerle-Rowson G, Fink AM, Busch R, Mayer J, et al. Addition of rituximab to fludarabine and cyclophosphamide in patients with chronic lymphocytic leukaemia: a randomised, open-label, phase 3 trial. Lancet. 2010;376(9747):1164-74.
6. Saiya-Cork K, Collins R, Parkin B, Ouillette P, Kuizon E, Kujawski L, et al. A pathobiological role of the insulin receptor in chronic lymphocytic leukemia. Clin Cancer Res. 2011;17(9):2679-92.
7. Britt-Compton B, Lin TT, Ahmed G, Weston V, Jones RE, Fegan C, et al. Extreme telomere erosion in ATM-mutated and 11qdeleted CLL patients is independent of disease stage. Leukemia. 2012;26(4):826-30.
8. Ouillette P, Fossum S, Parkin B, Ding L, Bockenstedt P, Al-Zoubi A, et al. Aggressive chronic lymphocytic leukemia with elevated genomic complexity is associated with multiple gene defects in the response to DNA double-strand breaks. Clin Cancer Res. 2010;16(3):835-47.
9. Catovsky D, Richards S, Matutes E, Oscier D, Dyer MJS, Bezares RF, et al. Assessment of fludarabine plus cyclophosphamide for patients with chronic lymphocytic leukaemia (the LRF CLL4 Trial): a randomised controlled trial. Lancet. 2007; 370(9583):230-9.
10. Tsimberidou A-M, Tam C, Abruzzo LV, O'Brien S, Wierda WG, Lerner S, et al. Chemoimmunotherapy may overcome the adverse prognostic significance of 11q deletion in previously untreated patients with chronic lymphocytic leukemia. Cancer. 2009;115(2):373-80.
11. Schwaenen C, Nessling M, Wessendorf S, Salvi T, Wrobel G, Radlwimmer B, et al. Automated array-based genomic profiling in chronic lymphocytic leukemia: development of a clinical tool and discovery of recurrent genomic alterations. Proc Natl Acad Sci USA. 2004;101(4):1039-44.
12. Pfeifer D, Pantic M, Skatulla I, Rawluk J, Kreutz C, Martens UM, et al. Genomewide analysis of DNA copy number changes and LOH in CLL using high-density SNP arrays. Blood. 2007;109(3):1202-10.
13. Lehmann S, Ogawa S, Raynaud SD, Sanada M, Nannya Y, Ticchioni M, et al. Molecular allelokaryotyping of early-stage, untreated chronic lymphocytic leukemia. Cancer. 2008;112(6):1296-305.
14. Edelmann J, Holzmann K, Miller F, Winkler D, Bühler A, Zenz T, et al. High-resolution genomic profiling of chronic lymphocytic leukemia reveals new recurrent genomic alterations. Blood. 2012;120(24):4783-94.
15. Austen B, Powell JE, Alvi A, Edwards I, Hooper L, Starczynski J, et al. Mutations in the ATM gene lead to impaired overall and treatment-free survival that is independent of IGVH mutation status in patients with BCLL. Blood. 2005;106(9):3175-82.
16. Wang L, Lawrence MS, Wan Y, Stojanov P, Sougnez C, Stevenson K, et al. SF3B1 and other novel cancer genes in chronic lymphocytic leukemia. N Engl J Med. 2011; 365(26):2497-506.
17. Austen B, Skowronska A, Baker C, Powell JE, Gardiner A, Oscier D, et al. Mutation status of the residual ATM allele is an important determinant of the cellular response to chemotherapy and survival in patients with chronic lymphocytic leukemia containing an 11q deletion. J Clin Oncol. 2007;25(34):5448-57.
18. Pettitt AR, Sherrington PD, Stewart G, Cawley JC, Taylor AM, Stankovic T. p53 dysfunction in B-cell chronic lymphocytic leukemia: inactivation of ATM as an alternative to TP53 mutation. Blood. 2001; 98(3):814-22.
19. Best OG, Gardiner AC, Majid A, Walewska R, Austen B, Skowronska A, et al. A novel functional assay using etoposide plus nutlin-3a detects and distinguishes between ATM and TP53 mutations in CLL. Leukemia. 2008;22(7):1456-9.
20. Skowronska A, Parker A, Ahmed G, Oldreive C, Davis Z, Richards S, et al. Biallelic ATM inactivation significantly reduces survival in patients treated on the United Kingdom Leukemia Research Fund Chronic Lymphocytic Leukemia 4 trial. J Clin Oncol. 2012;30(36):4524-32.
21. Auer RL, Starczynski J, McElwaine S, Bertoni F, Newland AC, Fegan CD, et al. Identification of a potential role for POU2AF1 and BTG4 in the deletion of 11q23 in chronic lymphocytic leukemia. Genes Chromosomes Cancer. 2005;43(1):1-10.
22. Visone R, Rassenti LZ, Veronese A, Taccioli C, Costinean S, Aguda BD, et al. Karyotype-specific microRNA signature in chronic lymphocytic leukemia. Blood. 2009;114(18):3872-9.
23. Marasca R, Maffei R, Martinelli S, Fiorcari S, Bulgarelli J, Debbia G, et al. Clinical heterogeneity of de novo 11q deletion chronic lymphocytic leukaemia: prognostic relevance of extent of 11q deleted nuclei inside leukemic clone. Hematol Oncol. 2013; 31(2):348-55.
24. Kalla C, Scheuermann MO, Kube I, Schlotter M, Mertens D, Döhner H, et al. Analysis of 11q22-q23 deletion target genes in B-cell chronic lymphocytic leukaemia: evidence for a pathogenic role of NPAT, CUL5, and PPP2R1B. Eur J Cancer. 2007; 43(8):1328-35.
25. Landau D a, Carter SL, Stojanov P, McKenna A, Stevenson K, Lawrence MS, et al. Evolution and impact of subclonal mutations in chronic lymphocytic leukemia. Cell. 2013;152(4):714-26.
26. Rossi D, Fangazio M, Rasi S, Vaisitti T, Monti S, Cresta S, et al. Disruption of BIRC3 associates with fludarabine chemorefractoriness in TP53 wild-type chronic lymphocytic leukemia. Blood. 2012;119(12):2854-62.
27. Rossi D, Rasi S, Spina V, Bruscaggin A, Monti S, Ciardullo C, et al. Integrated mutational and cytogenetic analysis identifies new prognostic subgroups in chronic lymphocytic leukemia. Blood. 2013; 121(8):1403-12.
28. Gonzalez D, Martinez P, Wade R, Hockley S, Oscier D, Matutes E, et al. Mutational status of the TP53 gene as a predictor of response and survival in patients with chronic lymphocytic leukemia: results from the LRF CLL4 trial. J Clin Oncol. 2011; 29(16):2223-9.
29. Oscier DG, Rose-Zerilli MJJ, Winkelmann N, Gonzalez de Castro D, Gomez B, Forster J, et al. The clinical significance of NOTCH1 and SF3B1 mutations in the UK LRF CLL4 trial. Blood. 2013;121(3):468-75.
30. Best OG, Ibbotson RE, Parker AE, Davis ZA, Orchard JA, Oscier DG. ZAP-70 by flow cytometry: a comparison of different antibodies, anticoagulants, and methods of analysis. Cytometry B Clin Cytom 2006; 70(4):235-241.
31. Hamblin TJ, Davis Z, Gardiner A, Oscier DG, Stevenson FK. Unmutated Ig V(H) genes are associated with a more aggressive form of chronic lymphocytic leukemia. Blood. 1999;94(6):1848-54.
32. Parker H, Rose-Zerilli MJJ, Parker A, Chaplin T, Wade R, Gardiner A, et al. 13Q Deletion Anatomy and Disease Progression in Patients With Chronic Lymphocytic Leukemia. Leukemia. 2011;25(3):489-97.
33. Oscier DG, Gardiner AC, Mould SJ, Glide S, Davis ZA, Ibbotson RE, et al. Multivariate analysis of prognostic factors in CLL: clinical stage, IGVH gene mutational status, and loss or mutation of the p53 gene are independent prognostic factors. Blood. 2002;100(4):1177-84.
34. Starostik P, Manshouri T, Brien SO, Leukemia BCL, Lerner S, Keating M. Deficiency of the ATM protein expression defines an aggressive subgroup of B-cell chronic lymphocytic leukemia. Cancer Res 1998;58(20):4552-7.
35. Grossmann V, Kohlmann A, Schnittger S, Weissmann S, Jeromin S, Kienast J, et al. Recurrent ATM and BIRC3 mutations in patients with chronic lymphocytic leukemia (CLL) and deletion 11q22-q23. Blood. 2012;115 n. 35 ASH Annual Meeting Abstracts. (Abstract):1771.
36. Stankovic T. Ataxia telangiectasia mutateddeficient B-cell chronic lymphocytic leukemia occurs in pregerminal center cells and results in defective damage response and unrepaired chromosome damage. Blood. 2002;99(1):300-9.
37. Ouillette P, Li J, Shaknovich R, Li Y, Melnick A, Shedden K, et al. Incidence and Clinical Implications of ATM Aberrations in Chronic Lymphocytic Leukemia. Genes Chromosomes Cancer. 2012;51(12):1125-32.
38. Lozanski G, Ruppert AS, Heerema N a, Lozanski A, Lucas DM, Gordon A, et al. Variations of the ataxia telangiectasia mutated gene in patients with chronic lymphocytic leukemia lack substantial impact on progression-free survival and overall survival: a Cancer and Leukemia Group B study. Leuk Lymphoma. 2012; 53(9):1743-8.
39. Sivasubramaniam S, Sun X, Pan Y-R, Wang S, Lee EY-HP. Cep164 is a mediator protein required for the maintenance of genomic stability through modulation of MDC1, RPA, and CHK1. Genes Dev. 2008;22(5): 587-600.
40. Ferreira PG, Jares P, Rico D, Gómez-López G, Martínez-Trillos A, Villamor N, et al. Transcriptome characterization by RNA sequencing identifies a major molecular and clinical subdivision in chronic lymphocytic leukemia. Genome Res.2014; 24(2): 212-26.