Role of precision medicine in the treatment of chronic lymphocytic leukaemia

References

• Hallek M, Cheson BD, Catovsky D, et al. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia : a report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute – Working Group 1996 guidelines. Blood. 2008;111(12):5446–5456.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Hamblin BTJ, Davis Z, Gardiner A, et al. Unmutated Ig V. Blood. 1999;94:1848–1854.
   PubMed Web of Science ®Google Scholar
• Zenz T, Eichhorst B, Busch R, et al. TP53 mutation and survival in chronic lymphocytic leukemia. J. Clin. Oncol. 2010;28(29):4473–4479.
   PubMed Web of Science ®Google Scholar
• Precision Medicine Initiative | National Institutes of Health (NIH) [Internet]. [cited 2015 Dec 1]. Available from: https://www.nih.gov/precision-medicine-initiative-cohort-program
   Google Scholar
• Precision Medicine Initiative | The White House [Internet]. [cited 2015 Dec 1]. Available from: https://www.whitehouse.gov/precision-medicine
   Google Scholar
• Genomics England | 100,000 Genomes Project [Internet]. [cited 2015 Dec 1]. Available from: http://www.genomicsengland.co.uk/
   Google Scholar
• Binet JL, Auquier A, Dighiero G, et al. A new prognostic classification of chronic lymphocytic leukemia derived from a multivariate survival analysis. Cancer. 1981;48(1):198–206.
   PubMed Web of Science ®Google Scholar
• Rai K, Sawitsky A, Cronkite E, et al. Clinical staging of chronic lymphocytic leukemia. Blood. 1975;46:219–235.
   PubMed Web of Science ®Google Scholar
• Tobin G, Thunberg U, Johnson A, et al. Somatically mutated Ig V H 3-21 genes characterize a new subset of chronic lymphocytic leukemia Brief report Somatically mutated Ig V H 3-21 genes characterize a new subset of chronic lymphocytic leukemia. Blood. 2002;99(6):2262–2264.
   PubMed Web of Science ®Google Scholar
• Thorselius M, Krober A, Murray F, et al. Strikingly homologous immunoglobulin gene rearrangements and poor outcome in V H 3-21 – using chronic lymphocytic leukemia patients independent of geographic origin and mutational status. Blood. 2006;107(7):2889–2894.
   PubMed Web of Science ®Google Scholar
• Hamblin TJ, Orchard JA., Ibbotson RE, et al. CD38 expression and immunoglobulin variable region mutations are independent prognostic variables in chronic lymphocytic leukemia, but CD38 expression may vary during the course of the disease. Blood. 2002;99(3):1023–1029.
   PubMed Web of Science ®Google Scholar
• Rassenti LZ, Huynh L, Toy TL, et al. ZAP-70 compared with immunoglobulin heavy-chain gene mutation status as a predictor of disease progression in chronic lymphocytic leukemia. N Engl J Med. 2004;351:893–901.
   PubMed Web of Science ®Google Scholar
• Gentile M, Cutrona G, Neri A, et al. Predictive value of Beta2-microglobulin (Beta2-m) levels in chronic lymphocytic leukemia since Binet A stages. Haematologica. 2009;94(6):887–888.
   PubMed Web of Science ®Google Scholar
• Gattei V, Bulian P, Del Principe MI, et al. Relevance of CD49d protein expression as overall survival and progressive disease prognosticator in chronic lymphocytic leukemia. Blood. 2008;111(2):865–873.
   PubMed Web of Science ®Google Scholar
• Rossi D, Zucchetto A, Rossi FM, et al. CD49d expression is an independent risk factor of progressive disease in early stage chronic lymphocytic leukemia. Haematologica. 2008;93(10):1575–1579.
   PubMed Web of Science ®Google Scholar
• Baumann T, Delgado J, Santacruz R, et al. CD49d (ITGA4) expression is a predictor of time to first treatment in patients with chronic lymphocytic leukaemia and mutated IGHV status. Br. J. Haematol. 2015;n/a–n/a. doi:10.1111/bjh.13788.
   PubMed Web of Science ®Google Scholar
• Wierda WG, O’Brien S, Wang X, et al. Multivariable model for time to first treatment in patients with chronic lymphocytic leukemia. J. Clin. Oncol. 2011;29(31):4088–4095.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Stamatopoulos B, Timbs A, Dreau H, et al. Next-generation deep sequencing reveals multiple Ighv clones in one third of CLL patients defining new prognostic subgroups and improving previous classification. In: 57th Annual Meeting of American Society of Haematology Poster 4127; 2015. Available from: https://ash.confex.com/ash/2015/webprogram/Paper81070.html.
   Google Scholar
• Jain N, Brien SO. Initial treatment of CLL : integrating biology and functional status. Blood. 2015;126(4):463–470.
   PubMed Web of Science ®Google Scholar
• Hallek M, Fischer K, Fingerle-Rowson G, et al. Addition of rituximab to fludarabine and cyclophosphamide in patients with chronic lymphocytic leukaemia: a randomised, open-label, phase 3 trial. The Lancet. 2010;376(9747):1164–1174.
   PubMed Web of Science ®Google Scholar
• 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;114:5307–5314.
   PubMed Web of Science ®Google Scholar
• Cramer P, Langerbeins P, Eichhorst B, et al. Advances in first-line treatment of chronic lymphocytic leukemia current recommendations on management and first-line treatment by the german cll study group (gcllsg). Eur. J. Haematol. 2015;n/a–n/a. doi:10.1111/ejh.12678.
   Web of Science ®Google Scholar
• Interim statement from the BCSH CLL guidelines panel British Committee for Standards in Haematology [Internet]. [cited 2015 Dec 1]. Available from: http://www.bcshguidelines.com/documents/Interim_statement_CLL_guidelines_version6.pdf
   Google Scholar
• Rossi D, Khiabanian H, Spina V, et al. Clinical impact of small TP53 mutated subclones in chronic lymphocytic leukemia. Blood. 2014;123(14):2139–2147.
   PubMed Web of Science ®Google Scholar
• Malcikova J, Stano-Kozubik K, Tichy B, et al. Detailed analysis of therapy-driven clonal evolution of TP53 mutations in chronic lymphocytic leukemia. Leukemia. 2015;29:877–885.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Puente XS, Pinyol M, Quesada V, et al. Whole-genome sequencing identifies recurrent mutations in chronic lymphocytic leukaemia. Nature. 2011;475(7354):101–105.
   Google Scholar
• Rossi D, Bruscaggin A, Spina V, et al. Mutations of the SF3B1 splicing factor in chronic lymphocytic leukemia: association with progression and fludarabine-refractoriness. Blood. 2011;118(26):6904–6908.
   Google Scholar
• Clifford R, Louis T, Robbe P, et al. SAMHD1 is mutated recurrently in chronic lymphocytic leukemia and is involved in response to DNA damage. Blood. 2014;123(7):1021–1031.
   PubMed Web of Science ®Google Scholar
• Oscier DG, Rose-Zerilli MJJ, Winkelmann N, et al. The clinical significance of NOTCH1 and SF3B1 mutations in the UK LRF CLL4 trial. Blood. 2013;121(3):468–475.
   PubMed Web of Science ®Google Scholar
• Rossi D, Fangazio M, Rasi S, et al. Disruption of BIRC3 associates with fludarabine chemorefractoriness in TP53 wild-type chronic lymphocytic leukemia. Blood. 2012;119:2854–2862.
   PubMed Web of Science ®Google Scholar
• Rossi D, Rasi S, Fabbri G, et al. Mutations of NOTCH1 are an independent predictor of survival in chronic lymphocytic leukemia. Blood. 2012;119:521–529.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Ward AJ, Cooper TA. The pathobiology of splicing. J Pathol. 2010;220:152–163.
   PubMed Web of Science ®Google Scholar
• Wan Y, Wu CJ. SF3B1 mutations in chronic lymphocytic leukemia. Blood. 2013;121(23):4627–4634.
   PubMed Web of Science ®Google Scholar
• Jeromin S, Weissmann S, Haferlach C, et al. SF3B1 mutations correlated to cytogenetics and mutations in NOTCH1, FBXW7, MYD88, XPO1 and TP53 in 1160 untreated CLL patients. Leukemia. 2014;28:108–117.
   PubMed Web of Science ®Google Scholar
• Yoshida K, Sanada M, Shiraishi Y, et al. Frequent pathway mutations of splicing machinery in myelodysplasia. Nature. 2011;478(7367):64–69.
   PubMed Web of Science ®Google Scholar
• Papaemmanuil E, Cazzola M, Boultwood J, et al. Somatic SF3B1 mutation in myelodysplasia with ring sideroblasts. N Engl J Med. 2011;365:1384–1395.
   PubMed Web of Science ®Google Scholar
• Darding M, Meier P. IAPs: guardians of RIPK1. Cell Death Differ. 2012;19(1):58–66.
   PubMed Web of Science ®Google Scholar
• Cortese D, Sutton L, Cahill N, et al. On the way towards a ‘CLL prognostic index’: focus on TP53, BIRC3, SF3B1, NOTCH1 and MYD88 in a population-based cohort. Leukemia. 2014;28:710–713.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Laguette N, Sobhian B, Casartelli N, et al. SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature. 2011;474(7353):654–657.
   PubMed Web of Science ®Google Scholar
• Powell RD, Holland PJ, Hollis T, et al. Aicardi-Goutieres syndrome gene and HIV-1 restriction factor SAMHD1 is a dGTP-regulated deoxynucleotide triphosphohydrolase. J. Biol. Chem. 2011;286(51):43596–43600.
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1038/nature15395.
   PubMed Web of Science ®Google Scholar
• Ljungstrom V, Cortese D, Young E, et al. Whole-exome sequencing in relapsing chronic lymphocytic leukemia: clinical impact of recurrent RPS15 mutations. Blood. 2015. doi:10.1182/blood-2015-10-674572.
   Google Scholar
• Pflug N, Bahlo J, Shanafelt TD, et al. Development of a comprehensive prognostic index for patients with chronic lymphocytic leukemia. Blood. 2014;124:49–62.
   Google Scholar
• Pflug N, Bahlo J, Shanafelt TD, et al. CME article integrated mutational and cytogenetic analysis identifies new prognostic subgroups in chronic lymphocytic leukemia. Blood. 2013;121:1403–1412.
   Google Scholar
• Rossi D, Terzi-di-Bergamo L, De Paoli L, et al. Molecular prediction of durable remission after first-line fludarabine-cyclophosphamide-rituximab in chronic lymphocytic leukemia. Blood. 2015;126(16):1921–1924.
   PubMed Web of Science ®Google Scholar
• Thompson P, Tam C, O'Brien S, et al. Fludarabine, cyclophosphamide and rituximab achieves long-term disease-free survival in IGHV-mutated chronic lymphocytic leukemia. Blood. 2016;127(3):303–309.
   PubMed Web of Science ®Google Scholar
• Fischer K, Bahlo J, Fink A, et al. Long term remissions after FCR chemoimmunotherapy in previously untreated patients with CLL: updated results of the CLL8 trial. Blood. 2016;127(2):208–215.
   PubMed Web of Science ®Google Scholar
• Johnson GG, Lin K, Cox TF, et al. CYP2B6 * 6 is an independent determinant of inferior response to fl udarabine plus cyclophosphamide in chronic lymphocytic leukemia. Blood. 2013;122:4253–4258.
   Google Scholar
• Bottcher S, Ritgen M, Fischer K, et al. Minimal residual disease quantification is an independent predictor of progression-free and overall survival in chronic lymphocytic leukemia: A multivariate analysis from the randomized GCLLSG CLL8 trial. J. Clin. Oncol. 2012;30(9):980–988.
   PubMed Web of Science ®Google Scholar
• Strati P, Keating MJ, O’Brien SM, et al. Outcomes of first-line treatment for chronic lymphocytic leukemia with 17p deletion. Haematologica. 2014;99(8):1350–1355.
   PubMed Web of Science ®Google Scholar
• Thompson PA, Wierda WG. Eliminating minimal residual disease as a therapeutic endpoint: working toward cure for patients with CLL. Blood. 2015;1–30. doi:10.1182/blood-2015-08-634816.
   Web of Science ®Google Scholar
• Goede V, Fischer K, Busch R, et al. Obinutuzumab plus chlorambucil in patients with CLL and coexisting conditions. N Engl J Med. 2014;370(12):1101–1110.
   PubMed Web of Science ®Google Scholar
• Fischer K, Cramer P, Busch R, et al. Bendamustine in combination with rituximab for previously untreated patients with chronic lymphocytic leukemia: a multicenter phase II trial of the German chronic lymphocytic leukemia study group. J. Clin. Oncol. 2012;30(26):3209–3216.
   PubMed Web of Science ®Google Scholar
• Schweighofer CD, Ritgen M, Eichhorst BF, et al. Consolidation with alemtuzumab improves progression-free survival in patients with chronic lymphocytic leukaemia (CLL) in first remission - long-term follow-up of a randomized phase III trial of the German CLL Study Group (GCLLSG). Br. J. Haematol. 2009;144(1):95–98.
   PubMed Web of Science ®Google Scholar
• Shanafelt TD, Ramsay AG, Zent CS, et al. Long-term repair of T-cell synapse activity in a phase II trial of chemoimmunotherapy followed by lenalidomide consolidation in previously untreated chronic lymphocytic leukemia (CLL). Blood. 2013;121(20):4137–4141.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Young R, Staudt L. Ibrutinib treatment of CLL: the cancer fights back. Cancer Cell. 2014;26(1):11–13.
   PubMed Web of Science ®Google Scholar
• Maddocks KJ, Ruppert AS, Lozanski G, et al. Etiology of ibrutinib therapy discontinuation and outcomes in patients with chronic lymphocytic leukemia. JAMA Oncol. 2015;1(1):80–88.
   PubMed Web of Science ®Google Scholar
• Woyach JA, Johnson AJ. Targeted therapies in CLL : mechanisms of resistance and strategies for management. Blood. 2015;126(4):471–477.
   PubMed Web of Science ®Google Scholar
• Coutre SE, Barrientos JC, Brown JR, et al. Management of adverse events associated with idelalisib treatment - expert panel opinion. Leuk. Lymphoma. 2015;8194:1–20.
   Google Scholar
• Morabito F, Gentile M, Seymour JF, et al. idelalisib and obinutuzumab for the treatment of patients with chronic lymphocytic leukemia: three new arrows aiming at the target. Leuk. Lymphoma. 2015;8194:1–20.
   Google Scholar
• Lipsky AH, Farooqui MZH, Tian X, et al. Incidence and risk factors of bleeding-related adverse events in patients with chronic lymphocytic leukemia treated with ibrutinib. Haematologica. 2015;100(12):1571–1578.
   PubMed Web of Science ®Google Scholar
• Kochenderfer JN, Dudley ME, Carpenter RO, et al. Donor-derived anti-CD19 chimeric-antigen-receptor-expressing T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation. Blood. 2013;122(21):151.
   Google Scholar
• Brentjens RJ, Davila ML, Riviere I, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci. Transl. Med. 2013;5(177):177ra38–177ra38.
   PubMed Web of Science ®Google Scholar
• Porter DL, Kalos M, Zheng Z, et al. Receptor therapy for B-cell malignancies. J. Cancer. 2011;2:331–332.
   PubMed Web of Science ®Google Scholar
• Kochenderfer JN, Dudley ME, Feldman SA, et al. B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood. 2012;119:2709–2720.
   PubMed Web of Science ®Google Scholar
• Mato A, Porter DL. Chronic lymphocytic leukemia : taking a big leap forward a drive through cellular therapy for CLL in 2015 : allogeneic cell transplantation and CARs. Blood. 2015;126(4):478–485.
   PubMed Web of Science ®Google Scholar
• Dreger P, Schetelig J, Andersen N, et al. Perspectives managing high-risk CLL during transition to a new treatment era : stem cell transplantation or novel agents ? Blood. 2014;124(26):3841–3849.
   PubMed Web of Science ®Google Scholar
• Furman RR, Sharman JP, Coutre SE, et al. Idelalisib and rituximab in relapsed chronic lymphocytic leukemia. N Engl J Med. 2014;370(11):997–1007.
   PubMed Web of Science ®Google Scholar
• Byrd JC, Brown JR, O'Brien S, et al. Ibrutinib versus ofatumumab in previously treated chronic lymphoid leukemia. N Engl J Med. 2014;371:213–223.
   PubMed Web of Science ®Google Scholar
• Jain P, Keating M, Wierda W, et al. Outcomes of patients with chronic lymphocytic leukemia after discontinuing ibrutinib. Blood. 2015;125(13):2062–2067. doi:10.1182/blood-2014-09-603670.
   PubMed Web of Science ®Google Scholar
• Nowell P. The clonal evolution of tumor cell populations. Science. 1976;194(4260):23–28.
   PubMed Web of Science ®Google Scholar
• Schuh A, Becq J, Humphray S, et al. Monitoring chronic lymphocytic leukemia progression by whole genome sequencing reveals heterogeneous clonal evolution patterns. Blood. 2012;120(20):4191–4196.
   PubMed Web of Science ®Google Scholar
• Landau DA, Carter S, Stojanov P, et al. Evolution and impact of subclonal mutations in chronic lymphocytic leukemia. Cell. 2013;152(4):714–726.
   PubMed Web of Science ®Google Scholar
• Ouillette P, Collins R, Shakhan S, et al. Acquired genomic copy number aberrations and survival in chronic lymphocytic leukemia. Blood. 2011;118(11):3051–3061.
   Google Scholar
• Knight SJL, Yau C, Clifford R, et al. Quantification of subclonal distributions of recurrent genomic aberrations in paired pre-treatment and relapse samples from patients with B-cell chronic lymphocytic leukemia. Leukemia. 2012;26(7):1564–1575.
   PubMed Web of Science ®Google Scholar
• Guieze R, Robbe P, Clifford R, et al. Presence of multiple recurrent mutations confers poor trial outcome of relapsed/refractory CLL. Blood. 2015;126(18):2110–2117. doi:10.1182/blood-2015-05-647578.
   PubMed Web of Science ®Google Scholar
• Rossi D, Spina V, Deambrogi C, et al. The genetics of Richter syndrome reveals disease heterogeneity and predicts survival after transformation. Blood. 2011;117(12):3391–3401.
   PubMed Web of Science ®Google Scholar
• Parikh SA, Kay NE, Shanafelt TD. How we treat Richter syndrome. Blood. 2014;123(11):1647–1657.
   PubMed Web of Science ®Google Scholar
• Byrd JC, Furman RR, Coutre SE, et al. Targeting BTK with ibrutinib in relapsed chronic lymphocytic leukemia. N Engl J Med. 2013;369:32–42.
   PubMed Web of Science ®Google Scholar
• Byrd JC, Brown JR, O’Brien S, Barrientos JC, Kay NE, Reddy NM, et al. Ibrutinib versus ofatumumab in previously treated chronic lymphoid leukemia. N Engl J Med. 2014;371(3):213–223.
   Google Scholar
• Chigrinova E, Rinaldi A, Kwee I, et al. Two main genetic pathways lead to the transformation of chronic lymphocytic leukemia to Richter syndrome. Blood. 2013;122:2673–2682.
   Google Scholar