Dissecting the role of TP53 alterations in del(11q) chronic lymphocytic leukemia

  1. Quijada‐Álamo, Miguel 12
  2. Pérez‐Carretero, Claudia 12
  3. Hernández‐Sánchez, María 1245
  4. Rodríguez‐Vicente, Ana‐Eugenia 12
  5. Herrero, Ana‐Belén 12
  6. Hernández‐Sánchez, Jesús‐María 12
  7. Martín‐Izquierdo, Marta 12
  8. Santos‐Mínguez, Sandra 12
  9. del Rey, Mónica 12
  10. González, Teresa 2
  11. Rubio‐Martínez, Araceli 8
  12. García de Coca, Alfonso 9
  13. Dávila‐Valls, Julio 7
  14. Hernández‐Rivas, José‐Ángel 10
  15. Parker, Helen 3
  16. Strefford, Jonathan C. 3
  17. Benito, Rocío 12
  18. Ordóñez, José‐Luis 12
  19. Hernández‐Rivas, Jesús‐María 126
  1. 1 Cancer Research Center University of Salamanca, IBSAL, IBMCC, CSIC Salamanca Spain
  2. 2 Department of Hematology University Hospital of Salamanca Salamanca Spain
  3. 3 School of Cancer Sciences Faculty of Medicine University of Southampton Southampton UK
  4. 4 Department of Medical Oncology Dana‐Farber Cancer Institute Boston Massachusetts USA
  5. 5 Broad Institute of Harvard and MIT Cambridge Massachusetts USA
  6. 6 Department of Medicine University of Salamanca Salamanca Spain
  7. 7 Department of Hematology Hospital Nuestra Señora de Sonsoles Ávila Spain
  8. 8 Department of Hematology Hospital Miguel Servet Zaragoza Spain
  9. 9 Department of Hematology Hospital Clínico de Valladolid Valladolid Spain
  10. 10 Department of Hematology Hospital Universitario Infanta Leonor, Universidad Complutense Madrid Spain
Zugehörigkeit anzeigen +
Zeitschrift:
Clinical and Translational Medicine

ISSN: 2001-1326,  2001-1326

Datum der Publikation: 2021

Ausgabe: 11

Nummer: 2

Art: Artikel

DOI: 10.1002/CTM2.304 WoS: WOS:000624468800012 GOOGLE SCHOLAR lock_openOpen Access editor

Andere Publikationen in: Clinical and Translational Medicine

Bibliographische Referenzen

  • Chiorazzi N, Rai KR, Ferrarini M. Chronic lymphocytic leukemia. N Engl J Med. 2005; 352(8): 804– 815.
  • Hallek M, Cheson BD, Catovsky D, et al. iwCLL guidelines for diagnosis, indications for treatment, response assessment, and supportive management of CLL. Blood. 2018; 131(25): 2745– 2760.
  • Döhner H, Stilgenbauer S, Benner A, et al. Genomic aberrations and survival in chronic lymphocytic leukemia. N Engl J Med. 2000; 343(26): 1910– 1916.
  • Landau DA, Tausch E, Taylor-Weiner AN, et al. Mutations driving CLL and their evolution in progression and relapse. Nature. 2015; 526(7574): 525– 530.
  • Puente XS, Beà S, Valdés-Mas R, et al. Non-coding recurrent mutations in chronic lymphocytic leukaemia. Nature. 2015; 526(7574): 519– 524.
  • Döhner H, Stilgenbauer S, James MR, 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– 2522.
  • Neilson JR, Auer R, White D, et al. Deletions at 11q identify a subset of patients with typical CLL who show consistent disease progression and reduced survival. Leukemia. 1997; 11(11): 1929– 1932.
  • Stilgenbauer S, Liebisch P, James MR, et al. Molecular cytogenetic delineation of a novel critical genomic region in chromosome bands 11q22.3-923.1 in lymphoproliferative disorders. Proc Natl Acad Sci U S A. 1996; 93(21): 11837– 11841.
  • Gunnarsson R, Mansouri L, Isaksson A, et al. Array-based genomic screening at diagnosis and during follow-up in chronic lymphocytic leukemia. Haematologica. 2011; 96(8): 1161– 1169.
  • Rose-Zerilli MJJ, Forster J, Parker H, et al. 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. 2014; 99(4): 736– 742.
  • Lavin MF. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat Rev Mol Cell Biol. 2008; 9(10): 759– 769.
  • Van Dyke DL, Werner L, Rassenti LZ, et al. The Dohner fluorescence in situ hybridization prognostic classification of chronic lymphocytic leukaemia (CLL): the CLL research consortium experience. Br J Haematol. 2016; 173(1): 105– 113.
  • Hernández JÁ, Hernández-Sánchez M, Rodríguez-Vicente AE, et al. A low frequency of losses in 11q chromosome is associated with better outcome and lower rate of genomic mutations in patients with chronic lymphocytic leukemia. PLoS One. 2015; 10(11):e0143073.
  • Stankovic T, Skowronska A. The role of ATM mutations and 11q deletions in disease progression in chronic lymphocytic leukemia. Leuk Lymphoma. 2014; 55(6): 1227– 1239.
  • Yin S, Gambe RG, Sun J, et al. A murine model of chronic lymphocytic leukemia based on B cell-restricted expression of Sf3b1 mutation and ATM deletion. Cancer Cell. 2019; 35(2): 283– 296.
  • Austen B, Skowronska A, Baker C, 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– 5457.
  • Skowronska A, Parker A, Ahmed G, 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– 4532.
  • Baliakas P, Hadzidimitriou A, Sutton LA, et al. Recurrent mutations refine prognosis in chronic lymphocytic leukemia. Leukemia. 2015; 29(2): 329– 336.
  • Lozano-Santos C, García-Vela JA, Pérez-Sanz N, et al. Biallelic ATM alterations detected at diagnosis identify a subset of treatment-naïve chronic lymphocytic leukemia patients with reduced overall survival similar to patients with p53 deletion. Leuk Lymphoma. 2017; 58(4): 859– 865.
  • Malcikova J, Smardova J, Rocnova L, et al. Monoallelic and biallelic inactivation of TP53 gene in chronic lymphocytic leukemia: selection, impact on survival, and response to DNA damage. Blood. 2009; 114(26): 5307– 5314.
  • Zenz T, Eichhorst B, Busch R, et al. TP53 mutation and survival in chronic lymphocytic leukemia. J Clin Oncol. 2010; 28(29): 4473– 4479.
  • Zenz T, Häbe S, Denzel T, et al. Detailed analysis of p53 pathway defects in fludarabine-refractory chronic lymphocytic leukemia (CLL): dissecting the contribution of 17p deletion, TP53 mutation, p53-p21 dysfunction, and miR34a in a prospective clinical trial. Blood. 2009; 114(13): 2589– 2597.
  • Stilgenbauer S, Schnaiter A, Paschka P, et al. Gene mutations and treatment outcome in chronic lymphocytic leukemia: results from the CLL8 trial. Blood. 2014; 123(21): 3247– 3254.
  • Hafner A, Bulyk ML, Jambhekar A, Lahav G. The multiple mechanisms that regulate p53 activity and cell fate. Nat Rev Mol Cell Biol. 2019; 20(4): 199– 210.
  • Campo E, Cymbalista F, Ghia P, et al. TP53 aberrations in chronic lymphocytic leukemia: an overview of the clinical implications of improved diagnostics. Haematologica. 2018; 103(12): 1956– 1968.
  • Yu L, Kim HT, Kasar SN, et al. Survival of Del17p CLL depends on genomic complexity and somatic mutation. Clin Cancer Res. 2017; 23(3): 735– 745.
  • Pettitt AR, Sherrington PD, Stewart G, Cawley JC, Malcolm R Taylor A, Stankovic T. p53 dysfunction in B-cell chronic lymphocytic leukemia: inactivation of ATM as an alternative to TP53 mutation. Blood. 2001; 98(3): 814– 822. Greipp PT, Smoley SA, Viswanatha DS, et al. Patients with chronic lymphocytic leukaemia and clonal deletion of both 17p13.1 and 11q22.3 have a very poor prognosis. Br J Haematol. 2013; 163(3): 326– 333.
  • Arruga F, Gizdic B, Bologna C, et al. Mutations in NOTCH1 PEST domain orchestrate CCL19-driven homing of chronic lymphocytic leukemia cells by modulating the tumor suppressor gene DUSP22. Leukemia. 2017; 31(9): 1882– 1893.
  • Bretones G, Álvarez MG, Arango JR, et al. Altered patterns of global protein synthesis and translational fidelity in RPS15-mutated chronic lymphocytic leukemia. Blood. 2018; 132(22): 2375– 2388.
  • Close V, Close W, Kugler SJ, et al. FBXW7 mutations reduce binding of NOTCH1, leading to cleaved NOTCH1 accumulation and target gene activation in CLL. Blood. 2019; 133(8): 830– 839.
  • Quijada-Álamo M, Hernández-Sánchez M, Alonso-Pérez V, et al. CRISPR/Cas9-generated models uncover therapeutic vulnerabilities of del(11q) CLL cells to dual BCR and PARP inhibition. Leukemia. 2020; 34(6): 1599– 1612.
  • Hernández-Sánchez M, Rodríguez-Vicente AE, González-Gascón Y Marín I, et al. DNA damage response-related alterations define the genetic background of patients with chronic lymphocytic leukemia and chromosomal gains. Exp Hematol. 2019; 72: 9– 13.
  • Sanjana NE, Shalem O, Zhang F. Improved vectors and genome-wide libraries for CRISPR screening. Nat Methods. 2014; 11(8): 783– 784.
  • Doench JG, Hartenian E, Graham DB, et al. Rational design of highly active sgRNAs for CRISPR-Cas9–mediated gene inactivation. Nat Biotechnol. 2014; 32(12): 1262– 1267.
  • Pliatsika V, Rigoutsos I. “Off-Spotter”: very fast and exhaustive enumeration of genomic lookalikes for designing CRISPR/Cas guide RNAs. Biol Direct. 2015; 10(1): 4.
  • Strasser-Wozak EM, Hartmann BL, Geley S, et al. Irradiation induces G2/M cell cycle arrest and apoptosis in p53-deficient lymphoblastic leukemia cells without affecting Bcl-2 and Bax expression. Cell Death Differ. 1998; 5(8): 687– 693.
  • Kwok M, Davies N, Agathanggelou A, et al. ATR inhibition induces synthetic lethality and overcomes chemoresistance in TP53- or ATM-defective chronic lymphocytic leukemia cells. Blood. 2016; 127(5): 582– 595.
  • Rossi D, Fangazio M, Rasi S, et al. Disruption of BIRC3 associates with fludarabine chemorefractoriness in TP53 wild-type chronic lymphocytic leukemia. Blood. 2012; 119(12): 2854– 2862.
  • Lazarian G, Guièze R, Wu CJ. Clinical implications of novel genomic discoveries in chronic lymphocytic leukemia. J Clin Oncol. 2017; 35(9): 984– 993.
  • Brown JR, Porter DL, O'Brien SM. Novel treatments for chronic lymphocytic leukemia and moving forward. Am Soc Clin Oncol Educ B. 2014; 34: e317– e325.
  • Woyach JA, Furman RR, Liu T-M, et al. Resistance mechanisms for the Bruton's tyrosine kinase inhibitor ibrutinib. N Engl J Med. 2014; 370(24): 2286– 2294.
  • Furman RR, Cheng S, Lu P, et al. Ibrutinib resistance in chronic lymphocytic leukemia. N Engl J Med. 2014; 370(24): 2352– 2354.
  • Ahn IE, Underbayev C, Albitar A, et al. Clonal evolution leading to ibrutinib resistance in chronic lymphocytic leukemia. Blood. 2017; 129(11): 1469– 1479.
  • Amin NA, Balasubramanian S, Saiya-Cork K, Shedden K, Hu N, Malek SN. Cell-intrinsic determinants of ibrutinib-induced apoptosis in chronic lymphocytic leukemia. Clin Cancer Res. 2017; 23(4): 1049– 1059.
  • O'Brien S, Furman RR, Coutre S, et al. Single-agent ibrutinib in treatment-naïve and relapsed/refractory chronic lymphocytic leukemia: a 5-year experience. Blood. 2018; 131(17): 1910– 1919.
  • Sharman JP, Coutre SE, Furman RR, et al. Final results of a randomized, phase III study of rituximab with or without idelalisib followed by open-label idelalisib in patients with relapsed chronic lymphocytic leukemia. J Clin Oncol. 2019; 37(16): 1391– 1402.
  • Zelenetz AD, Barrientos JC, Brown JR, et al. Idelalisib or placebo in combination with bendamustine and rituximab in patients with relapsed or refractory chronic lymphocytic leukaemia: interim results from a phase 3, randomised, double-blind, placebo-controlled trial. Lancet Oncol. 2017; 18(3): 297– 311.
  • Jones JA, Robak T, Brown JR, et al. Efficacy and safety of idelalisib in combination with ofatumumab for previously treated chronic lymphocytic leukaemia: an open-label, randomised phase 3 trial. Lancet Haematol. 2017; 4(3): e114– e126.