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Original Article

ATM and TP53 mutations show mutual exclusivity but distinct clinical impact in mantle cell lymphoma patients

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Pages 1420-1428 | Received 17 Apr 2018, Accepted 25 Oct 2018, Published online: 10 Jan 2019

References

  • Harris SL, Levine AJ. The p53 pathway: positive and negative feedback loops. Oncogene. 2005;24:2899–2908.
  • Vousden KH, Lane DP. p53 in health and disease. Nat Rev Mol Cell Biol. 2007;8:275–283.
  • Greiner TC, Moynihan MJ, Chan WC, et al. p53 mutations in mantle cell lymphoma are associated with variant cytology and predict a poor prognosis. Blood. 1996;87:4302–4310.
  • Hernandez L, Fest T, Cazorla M, et al. p53 gene mutations and protein overexpression are associated with aggressive variants of mantle cell lymphomas. Blood. 1996;87:3351–3359.
  • Greiner TC, Dasgupta C, Ho VV, et al. Mutation and genomic deletion status of ataxia telangiectasia mutated (ATM) and p53 confer specific gene expression profiles in mantle cell lymphoma. Pnas. 2006;103:2352–2357.
  • Stefancikova L, Moulis M, Fabian P, et al. Loss of the p53 tumor suppressor activity is associated with negative prognosis of mantle cell lymphoma. Int J Oncol. 2010;36:699–706.
  • Beà S, Valdés-Mas R, Navarro A, et al. Landscape of somatic mutations and clonal evolution in mantle cell lymphoma. Proc Natl Acad Sci USA. 2013;110:18250–18255.
  • Zlamalikova L, Moulis M, Ravcukova B, et al. Complex analysis of the TP53 tumor suppressor in mantle cell and diffuse large B-cell lymphomas. Oncol Rep. 2017;38:2535–2542.
  • Aukema SM, Hoster E, Rosenwald A, et al. Expression of TP53 is associated with the outcome of MCL independent of MIPI and Ki-67 in trials of the European MCL Network. Blood. 2018;131:417–420.
  • Yamamoto K, Lee BJ, Li C, et al. Early B-cell-specific inactivation of ATM synergizes with ectopic CyclinD1 expression to promote pre-germinal center B-cell lymphomas in mice. Leukemia. 2015;29:1414–1424.
  • Lowndes NF, Murguia JR. Sensing and responding to DNA damage. Curr Opin Genet Dev. 2000;10:17–25.
  • Shiloh Y. ATM and ATR: networking cellular responses to DNA damage. Curr Opin Genet Dev. 2001;11:71–77.
  • Banin S, Moyal L, Shieh S, et al. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science. 1998;281:1674–1677.
  • Khanna KK, Keating KE, Kozlov S, et al. ATM associates with and phosphorylates p53: mapping the region of interaction. Nat Genet. 1998;20:398–400.
  • Matsuoka S, Rotman G, Ogawa A, et al. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc Natl Acad Sci USA. 2000;97:10389–10394.
  • Rotman G, Shiloh Y. ATM: from gene to function. Hum Mol Genet. 1998;7:1555–1563.
  • Fang NY, Greiner TC, Weisenburger DD, et al. Oligonucleotide microarrays demonstrate the highest frequency of ATM mutations in the mantle cell subtype of lymphoma. Proc Natl Acad Sci USA. 2003;100:5372–5377.
  • Camacho E, Hernández L, Hernández S, et al. ATM gene inactivation in mantle cell lymphoma mainly occurs by truncating mutations and missense mutations involving the phosphatidylinositol-3 kinase domain and is associated with increasing numbers of chromosomal imbalances. Blood. 2002;99:238–244.
  • Delfau-Larue MH, Klapper W, Berger F, et al. High-dose cytarabine does not overcome the adverse prognostic value of CDKN2A and TP53 deletions in mantle cell lymphoma. Blood. 2015;126:604–611.
  • Jardin F, Picquenot JM, Parmentier F, et al. Detection of gene copy number aberrations in mantle cell lymphoma by a single quantitative multiplex PCR assay: clinicopathological relevance and prognosis value. Br J Haematol. 2009;146:607–618.
  • Salaverria I, Zettl A, Beà S, et al. Specific secondary genetic alterations in mantle cell lymphoma provide prognostic information independent of the gene expression-based proliferation signature. Jco. 2007;25:1216–1222.
  • Swerdlow SH, Campo E, Seto M, et al. Mantle cell lymphoma. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, editors. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. Lyon: IARC Press; 2017. p. 285–290.
  • Geisler CH, Kolstad A, Laurell A, et al. Long-term progression-free survival of mantle cell lymphoma after intensive front-line immunochemotherapy with in vivo–purged stem cell rescue: a nonrandomized phase 2 multicenter study by the Nordic Lymphoma Group. Blood. 2008;112:2687–2693.
  • Tavtigian SV, Oefner PJ, Babikyan D, et al. Rare, evolutionarily unlikely missense substitutions in ATM confer increased risk of breast cancer. Am J Hum Genet. 2009;85:427–446.
  • Nadeu F, Delgado J, Royo C, et al. Clinical impact of clonal and subclonal TP53, SF3B1, BIRC3, NOTCH1, and ATM mutations in chronic lymphocytic leukemia. Blood. 2016;127:2122–2130.
  • Petitjean A, Mathe E, Kato S, et al. Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database. Hum Mutat. 2007;28:622–629.
  • Cheson BD, Pfistner B, Juweid ME, et al. Revised response criteria for malignant lymphoma. J Clin Oncol. 2007;25:579–586.
  • Nygren L, Baumgartner WS, Klimkowska M, et al. Prognostic role of SOX11 in a population-based cohort of mantle cell lymphoma. Blood. 2012;119:4215–4223.
  • Nordström L, Sernbo S, Eden P, et al. SOX11 and TP53 add prognostic information to MIPI in a homogenously treated cohort of mantle cell lymphoma - a Nordic Lymphoma Group study. Br J Haematol. 2014;166:98–108.
  • Kuo PY, Leshchenko VV, Fazzari MJ, et al. High-resolution chromatin immunoprecipitation (ChIP) sequencing reveals novel binding targets and prognostic role for SOX11 in mantle cell lymphoma. Oncogene. 2015;34:1231–1240.
  • Bartek J, Bartkova J, Lukas J, et al. DNA damage signalling guards against activated oncogenes and tumour progression. Oncogene. 2007;26:7773–7779.
  • Meissner B, Kridel R, Lim RS, et al. The E3 ubiquitin ligase UBR5 is recurrently mutated in mantle cell lymphoma. Blood. 2013;121:3161–3164.
  • Zhang J, Jima D, Moffitt AB, et al. The genomic landscape of mantle cell lymphoma is related to the epigenetically determined chromatin state of normal B cells. Blood. 2014;123:2988–2996.
  • Rossi D, Ferrero S, Bruscaggin A, et al. A molecular model for the prediction of progression free survival in young mantle cell lymphoma patients treated with cytarabine-based high dose sequential chemotherapy and autologous stem cell transplantation: results from the MCL0208 Phase III trial from fondazione italiana linfomi (FIL). Blood. 2015;126:336–336.
  • Schaffner C, Idler I, Stilgenbauer S, et al. Mantle cell lymphoma is characterized by inactivation of the ATM gene. Proc Natl Acad Sci USA. 2000;97:2773–2778.
  • 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. Jco. 2007;25:5448–5457.
  • 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. Jco. 2012;30:4524–4532.
  • Mansouri L, Sutton LA, Ljungström V, et al. Feasibility of targeted next-generation sequencing of the TP53 and ATM genes in chronic lymphocytic leukemia. Leukemia. 2014;28:694–696.
  • Navrkalova V, Sebejova L, Zemanova J, et al. ATM mutations uniformly lead to ATM dysfunction in chronic lymphocytic leukemia: application of functional test using doxorubicin. Haematologica. 2013;98:1124–1131.
  • 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;58:859–865.
  • Pettitt AR, Sherrington PD, Stewart G, et al. p53 dysfunction in B-cell chronic lymphocytic leukemia: inactivation of ATM as an alternative to TP53 mutation. Blood. 2001;98:814–822.
  • Stankovic T, Stewart GS, Fegan C, et al. Ataxia telangiectasia mutated-deficient B-cell chronic lymphocytic leukemia occurs in pregerminal center cells and results in defective damage response and unrepaired chromosome damage. Blood. 2002;99:300–309.
  • Austen B, Powell JE, Alvi A, 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 B-CLL. Blood. 2005;106:3175–3182.
  • Rigolin GM, Saccenti E, Bassi C, et al. Extensive next-generation sequencing analysis in chronic lymphocytic leukemia at diagnosis: clinical and biological correlations. J Hematol Oncol. 2016;9:88.
  • Ahmed M, Li L, Pinnix C, et al. ATM mutation and radiosensitivity: an opportunity in the therapy of mantle cell lymphoma. Crit Rev Oncol Hematol. 2016;107:14–19.
  • Leitch HA, Gascoyne RD, Chhanabhai M, et al. Limited-stage mantle-cell lymphoma. Ann Oncol. 2003;14:1555–1561.
  • Haque W, Voong KR, Shihadeh F, et al. Radiation therapy is an effective modality in the treatment of mantle cell lymphoma, even in heavily pretreated patients. Clin Lymphoma Myeloma Leuk. 2014;14:474–479.
  • van Os NJ, Roeleveld N, Weemaes CM, et al. Health risks for ataxia-telangiectasia mutated heterozygotes: a systematic review, meta-analysis and evidence-based guideline. Clin Genet. 2016;90:105–117.
  • Weston VJ, Oldreive CE, Skowronska A, et al. The PARP inhibitor olaparib induces significant killing of ATM-deficient lymphoid tumor cells in vitro and in vivo. Blood. 2010;116:4578–4587.
  • Williamson CT, Muzik H, Turhan AG, et al. ATM deficiency sensitizes mantle cell lymphoma cells to poly(ADP-Ribose) polymerase-1 inhibitors. Mol Cancer Ther. 2010;9:347–357.
  • Golla RM, Li M, Shen Y, et al. Inhibition of poly(ADP-ribose) polymerase (PARP) and ataxia telangiectasia mutated (ATM) on the chemosensitivity of mantle cell lymphoma to agents that induce DNA strand breaks. Hematol Oncol. 2012;30:175–179.
  • Menezes DL, Holt J, Tang Y, et al. A synthetic lethal screen reveals enhanced sensitivity to ATR inhibitor treatment in mantle cell lymphoma with ATM loss-of-function. Mol Cancer Res. 2015;13:120–129.
  • Williamson CT, Kubota E, Hamill JD, et al. Enhanced cytotoxicity of PARP inhibition in mantle cell lymphoma harboring mutations in both ATM and p53. EMBO Mol Med. 2012;4:515–527.
  • 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;127:582–595.
  • Knittel G, Rehkämper T, Korovkina D, et al. Two mouse models reveal an actionable PARP1 dependence in aggressive chronic lymphocytic leukemia. Nat Commun. 2017;8:153.
  • Eskelund CW, Dahl C, Hansen JW, et al. TP53 mutations identify younger mantle cell lymphoma patients who do not benefit from intensive chemoimmunotherapy. Blood. 2017;130:1903–1910.
  • Wang ML, Blum KA, Martin P, et al. Long-term follow-up of MCL patients treated with single-agent ibrutinib: updated safety and efficacy results. Blood. 2015;126:739–745.
  • Tam CS, Anderson MA, Pott C, et al. Ibrutinib plus venetoclax for the treatment of mantle-cell lymphoma. N Engl J Med. 2018;378:1211–1223.
  • Dreyling M, Aurer I, Cortelazzo S, et al. Treatment for patients with relapsed/refractory mantle cell lymphoma: European-based recommendations. Leuk Lymphoma. 2018;59:1814–1828.

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