Personalizing treatment for chronic lymphocytic leukemia

References

• Rozman C, Montserrat E. Chronic lymphocytic leukemia. N. Engl. J. Med.333(16), 1052–1057 (1995).
   PubMed Web of Science ®Google Scholar
• Abrisqueta P, Pereira A, Rozman C et al. Improving survival in patients with chronic lymphocytic leukemia (1980–2008): the Hospital Clinic of Barcelona experience. Blood114(10), 2044–2050 (2009).
   PubMed Web of Science ®Google Scholar
• Dohner H, Stilgenbauer S, Benner A et al. Genomic aberrations and survival in chronic lymphocytic leukemia. N. Engl. J. Med.343(26), 1910–1916 (2000).
   PubMed Web of Science ®Google Scholar
• Dohner H, Fischer K, Bentz M et al. p53 gene deletion predicts for poor survival and non-response to therapy with purine analogs in chronic B-cell leukemias. Blood85(6), 1580–1589 (1995).
   PubMed Web of Science ®Google Scholar
• Grever MR, Lucas DM, Dewald GW et al. Comprehensive assessment of genetic and molecular features predicting outcome in patients with chronic lymphocytic leukemia: results from the US Intergroup Phase III Trial E2997. J. Clin. Oncol.25(7), 799–804 (2007).
   PubMed Web of Science ®Google Scholar
• Collins RJ, Verschuer LA, Harmon BV, Prentice RL, Pope JH, Kerr JF. Spontaneous programmed death (apoptosis) of B-chronic lymphocytic leukaemia cells following their culture in vitro. Br. J. Haematol.71(3), 343–350 (1989).
   PubMed Web of Science ®Google Scholar
• Granziero L, Ghia P, Circosta P et al. Survivin is expressed on CD40 stimulation and interfaces proliferation and apoptosis in B-cell chronic lymphocytic leukemia. Blood97(9), 2777–2783 (2001).
   PubMed Web of Science ®Google Scholar
• Gine E, Martinez A, Villamor N et al. Expanded and highly active proliferation tumors identify a histological subtype of chronic lymphocytic leukemia (‘accelerated’ chronic lymphocytic leukemia) with aggressive clinical behavior. Haematologica95(9), 1526–1533 (2010).
   PubMed Web of Science ®Google Scholar
• Pedersen IM, Kitada S, Leoni LM et al. Protection of CLL B cells by a follicular dendritic cell line is dependent on induction of Mcl-1. Blood100(5), 1795–1801 (2002).
   PubMed Web of Science ®Google Scholar
• Fais F, Ghiotto F, Hashimoto S et al. Chronic lymphocytic leukemia B cells express restricted sets of mutated and unmutated antigen receptors. J. Clin. Invest.102(8), 1515–1525 (1998).
   PubMed Web of Science ®Google Scholar
• Longo PG, Laurenti L, Gobessi S, Sica S, Leone G, Efremov DG. The Akt/Mcl-1 pathway plays a prominent role in mediating antiapoptotic signals downstream of the B-cell receptor in chronic lymphocytic leukemia B cells. Blood111(2), 846–855 (2008).
   PubMed Web of Science ®Google Scholar
• Cuni S, Perez-Aciego P, Perez-Chacon G et al. A sustained activation of PI3K/NF-κB pathway is critical for the survival of chronic lymphocytic leukemia B cells. Leukemia18(8), 1391–1400 (2004).
   PubMed Web of Science ®Google Scholar
• Endo T, Nishio M, Enzler T et al. BAFF and APRIL support chronic lymphocytic leukemia B-cell survival through activation of the canonical NF-κB pathway. Blood109(2), 703–710 (2007).
   PubMed Web of Science ®Google Scholar
• Hewamana S, Alghazal S, Lin TT et al. The NF-κB subunit Rel A is associated with in vitro survival and clinical disease progression in chronic lymphocytic leukemia and represents a promising therapeutic target. Blood111(9), 4681–4689 (2008).
   PubMed Web of Science ®Google Scholar
• Rai KR, Peterson BL, Appelbaum FR et al. Fludarabine compared with chlorambucil as primary therapy for chronic lymphocytic leukemia. N. Engl. J. Med.343(24), 1750–1757 (2000).
   PubMed Web of Science ®Google Scholar
• Catovsky D, Richards S, Matutes E et al. Assessment of fludarabine plus cyclophosphamide for patients with chronic lymphocytic leukaemia (the LRF CLL4 trial): a randomised controlled trial. Lancet370(9583), 230–239 (2007).
   PubMed Web of Science ®Google Scholar
• Eichhorst BF, Busch R, Hopfinger G et al. Fludarabine plus cyclophosphamide versus fludarabine alone in first-line therapy of younger patients with chronic lymphocytic leukemia. Blood107(3), 885–891 (2006).
   PubMed Web of Science ®Google Scholar
• Flinn IW, Neuberg DS, Grever MR et al. Phase III trial of fludarabine plus cyclophosphamide compared with fludarabine for patients with previously untreated chronic lymphocytic leukemia: US Intergroup Trial E2997. J. Clin. Oncol.25(7), 793–798 (2007).
   PubMed Web of Science ®Google Scholar
• Bosch F, Ferrer A, Villamor N et al. Fludarabine, cyclophosphamide, and mitoxantrone as initial therapy of chronic lymphocytic leukemia: high response rate and disease eradication. Clin. Cancer Res.14(1), 155–161 (2008).
   PubMed Web of Science ®Google Scholar
• Keating MJ, O’Brien S, Albitar M et al. Early results of a chemoimmunotherapy regimen of fludarabine, cyclophosphamide, and rituximab as initial therapy for chronic lymphocytic leukemia. J. Clin. Oncol.23(18), 4079–4088 (2005).
   PubMed Web of Science ®Google Scholar
• Tam CS, O’Brien S, Wierda W et al. Long-term results of the fludarabine, cyclophosphamide, and rituximab regimen as initial therapy of chronic lymphocytic leukemia. Blood112(4), 975–980 (2008).
   PubMed Web of Science ®Google Scholar
• Bosch F, Abrisqueta P, Villamor N et al. Rituximab, fludarabine, cyclophosphamide, and mitoxantrone: a new, highly active chemoimmunotherapy regimen for chronic lymphocytic leukemia. J. Clin. Oncol.27(27), 4578–4584 (2009).
   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. Lancet376(9747), 1164–1174 (2010).
   PubMed Web of Science ®Google Scholar
• Rawstron AC, Kennedy B, Evans PA et al. Quantitation of minimal disease levels in chronic lymphocytic leukemia using a sensitive flow cytometric assay improves the prediction of outcome and can be used to optimize therapy. Blood98(1), 29–35 (2001).
   PubMed Web of Science ®Google Scholar
• van Dongen JJ, Langerak AW, Bruggemann M et al. Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: report of the BIOMED-2 Concerted Action BMH4-CT98-3936. Leukemia17(12), 2257–2317 (2003).
   PubMed Web of Science ®Google Scholar
• Moreton P, Kennedy B, Lucas G et al. Eradication of minimal residual disease in B-cell chronic lymphocytic leukemia after alemtuzumab therapy is associated with prolonged survival. J. Clin. Oncol.23(13), 2971–2979 (2005).
   PubMed Web of Science ®Google Scholar
• Keating MJ, O’Brien S, Kontoyiannis D et al. Results of first salvage therapy for patients refractory to a fludarabine regimen in chronic lymphocytic leukemia. Leuk. Lymphoma43(9), 1755–1762 (2002).
   PubMed Web of Science ®Google Scholar
• Grever MR, Lucas DM, Dewald GW et al. Comprehensive assessment of genetic and molecular features predicting outcome in patients with chronic lymphocytic leukemia: results from the US Intergroup Phase III Trial E2997. J. Clin. Oncol.25(7), 799–804 (2007).
   PubMed Web of Science ®Google Scholar
• Shanafelt TD, Witzig TE, Fink SR et al. Prospective evaluation of clonal evolution during long-term follow-up of patients with untreated early-stage chronic lymphocytic leukemia. J. Clin. Oncol.24(28), 4634–4641 (2006).
   PubMed Web of Science ®Google Scholar
• Zenz T, Krober A, Scherer K et al. Monoallelic TP53 inactivation is associated with poor prognosis in chronic lymphocytic leukemia: results from a detailed genetic characterization with long-term follow-up. Blood112(8), 3322–3329 (2008).
   PubMed Web of Science ®Google Scholar
• Zenz T, Habe 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. Blood114(13), 2589–2597 (2009).
   PubMed Web of Science ®Google Scholar
• Rossi D, Cerri M, Deambrogi C et al. The prognostic value of TP53 mutations in chronic lymphocytic leukemia is independent of Del17p13: implications for overall survival and chemorefractoriness. Clin. Cancer Res.15(3), 995–1004 (2009).
   PubMed Web of Science ®Google Scholar
• Dicker F, Herholz H, Schnittger S et al. The detection of TP53 mutations in chronic lymphocytic leukemia independently predicts rapid disease progression and is highly correlated with a complex aberrant karyotype. Leukemia23(1), 117–124 (2009).
   PubMed Web of Science ®Google Scholar
• Saddler C, Ouillette P, Kujawski L et al. Comprehensive biomarker and genomic analysis identifies p53 status as the major determinant of response to MDM2 inhibitors in chronic lymphocytic leukemia. Blood111(3), 1584–1593 (2008).
   PubMed Web of Science ®Google Scholar
• Barekati Z, Radpour R, Kohler C et al. Methylation profile of TP53 regulatory pathway and mtDNA alterations in breast cancer patients lacking TP53 mutations. Hum. Mol. Genet.19(15), 2936–2946 (2010).
   PubMed Web of Science ®Google Scholar
• 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.25(34), 5448–5457 (2007).
   PubMed Web of Science ®Google Scholar
• Zenz T, Mohr J, Eldering E et al. miR-34a as part of the resistance network in chronic lymphocytic leukemia. Blood113(16), 3801–3808 (2009).
   PubMed Web of Science ®Google Scholar
• Deriano L, Guipaud O, Merle-Beral H et al. Human chronic lymphocytic leukemia B cells can escape DNA damage-induced apoptosis through the nonhomologous end-joining DNA repair pathway. Blood105(12), 4776–4783 (2005).
   PubMed Web of Science ®Google Scholar
• Dreger P, Corradini P, Kimby E et al. Indications for allogeneic stem cell transplantation in chronic lymphocytic leukemia: the EBMT transplant consensus. Leukemia21(1), 12–17 (2007).
   PubMed Web of Science ®Google Scholar
• Hillmen P, Skotnicki AB, Robak T et al. Alemtuzumab compared with chlorambucil as first-line therapy for chronic lymphocytic leukemia. J. Clin. Oncol.25(35), 5616–5623 (2007).
   PubMed Web of Science ®Google Scholar
• Lozanski G, Heerema NA, Flinn IW et al. Alemtuzumab is an effective therapy for chronic lymphocytic leukemia with p53 mutations and deletions. Blood103(9), 3278–3281 (2004).
   PubMed Web of Science ®Google Scholar
• Osuji NC, Del Giudice I, Matutes E, Wotherspoon AC, Dearden C, Catovsky D. The efficacy of alemtuzumab for refractory chronic lymphocytic leukemia in relation to cytogenetic abnormalities of p53. Haematologica90(10), 1435–1436 (2005).
   PubMed Web of Science ®Google Scholar
• Stilgenbauer S, Dohner H. Campath-1H-induced complete remission of chronic lymphocytic leukemia despite p53 gene mutation and resistance to chemotherapy. N. Engl. J. Med.347(6), 452–453 (2002).
   PubMed Web of Science ®Google Scholar
• Stilgenbauer S, Zenz T, Winkler D et al. Subcutaneous alemtuzumab in fludarabine-refractory chronic lymphocytic leukemia: clinical results and prognostic marker analyses from the CLL2H study of the German Chronic Lymphocytic Leukemia Study Group. J. Clin. Oncol.27(24), 3994–4001 (2009).
   PubMed Web of Science ®Google Scholar
• Byrd JC, Shinn C, Waselenko JK et al. Flavopiridol induces apoptosis in chronic lymphocytic leukemia cells via activation of caspase-3 without evidence of bcl-2 modulation or dependence on functional p53. Blood92(10), 3804–3816 (1998).
   PubMed Web of Science ®Google Scholar
• Pepper C, Thomas A, Hoy T et al. Leukemic and non-leukemic lymphocytes from patients with Li Fraumeni syndrome demonstrate loss of p53 function, Bcl-2 family dysregulation and intrinsic resistance to conventional chemotherapeutic drugs but not flavopiridol. Cell Cycle2(1), 53–58 (2003).
   PubMed Web of Science ®Google Scholar
• Phelps MA, Lin TS, Johnson AJ et al. Clinical response and pharmacokinetics from a Phase 1 study of an active dosing schedule of flavopiridol in relapsed chronic lymphocytic leukemia. Blood113(12), 2637–2645 (2009).
   PubMed Web of Science ®Google Scholar
• Lin TS, Ruppert AS, Johnson AJ et al. Phase II study of flavopiridol in relapsed chronic lymphocytic leukemia demonstrating high response rates in genetically high-risk disease. J. Clin. Oncol.27(35), 6012–6018 (2009).
   PubMed Web of Science ®Google Scholar
• Alvi AJ, Austen B, Weston VJ et al. A novel CDK inhibitor, CYC202 (R-roscovitine), overcomes the defect in p53-dependent apoptosis in B-CLL by down-regulation of genes involved in transcription regulation and survival. Blood105(11), 4484–4491 (2005).
   PubMed Web of Science ®Google Scholar
• Thornton PD, Matutes E, Bosanquet AG et al. High dose methylprednisolone can induce remissions in CLL patients with p53 abnormalities. Ann. Hematol.82(12), 759–765 (2003).
   PubMed Web of Science ®Google Scholar
• Pettitt AR, Matutes E, Oscier D. Alemtuzumab in combination with high-dose methylprednisolone is a logical, feasible and highly active therapeutic regimen in chronic lymphocytic leukaemia patients with p53 defects. Leukemia20(8), 1441–1445 (2006).
   PubMed Web of Science ®Google Scholar
• Castro JE, Sandoval-Sus JD, Bole J, Rassenti L, Kipps TJ. Rituximab in combination with high-dose methylprednisolone for the treatment of fludarabine refractory high-risk chronic lymphocytic leukemia. Leukemia22(11), 2048–2053 (2008).
   PubMed Web of Science ®Google Scholar
• Panayiotidis P, Jones D, Ganeshaguru K, Foroni L, Hoffbrand AV. Human bone marrow stromal cells prevent apoptosis and support the survival of chronic lymphocytic leukaemia cells in vitro. Br. J. Haematol.92(1), 97–103 (1996).
   PubMed Web of Science ®Google Scholar
• Ghia P, Strola G, Granziero L et al. Chronic lymphocytic leukemia B cells are endowed with the capacity to attract CD4+, CD40L+ T cells by producing CCL22. Eur. J. Immunol.32(5), 1403–1413 (2002).
   PubMed Web of Science ®Google Scholar
• Burger JA, Tsukada N, Burger M, Zvaifler NJ, Dell’Aquila M, Kipps TJ. Blood-derived nurse-like cells protect chronic lymphocytic leukemia B cells from spontaneous apoptosis through stromal cell-derived factor-1. Blood96(8), 2655–2663 (2000).
   PubMed Web of Science ®Google Scholar
• Chen H, Treweeke AT, West DC et al.In vitro and in vivo production of vascular endothelial growth factor by chronic lymphocytic leukemia cells. Blood96(9), 3181–3187 (2000).
   PubMed Web of Science ®Google Scholar
• Eichhorst BF, Busch R, Stilgenbauer S et al. First-line therapy with fludarabine compared with chlorambucil does not result in a major benefit for elderly patients with advanced chronic lymphocytic leukemia. Blood114(16), 3382–3391 (2009).
   PubMed Web of Science ®Google Scholar
• Thurmes P, Call T, Slager S et al. Comorbid conditions and survival in unselected, newly diagnosed patients with chronic lymphocytic leukemia. Leuk. Lymphoma49(1), 49–56 (2008).
   PubMed Web of Science ®Google Scholar
• Extermann M. Measuring comorbidity in older cancer patients. Eur. J. Cancer36(4), 453–471 (2000).
   PubMed Web of Science ®Google Scholar
• Foon KA, Boyiadzis M, Land SR et al. Chemoimmunotherapy with low-dose fludarabine and cyclophosphamide and high dose rituximab in previously untreated patients with chronic lymphocytic leukemia. J. Clin. Oncol.27(4), 498–503 (2009).
   PubMed Web of Science ®Google Scholar
• Friedberg JW, Sharman J, Sweetenham J et al. Inhibition of Syk with fostamatinib disodium has significant clinical activity in non-Hodgkin lymphoma and chronic lymphocytic leukemia. Blood115(13), 2578–2585 (2010).
   PubMed Web of Science ®Google Scholar
• Burger M, Hartmann T, Krome M et al. Small peptide inhibitors of the CXCR4 chemokine receptor (CD184) antagonize the activation, migration, and antiapoptotic responses of CXCL12 in chronic lymphocytic leukemia B cells. Blood106(5), 1824–1830 (2005).
   PubMed Web of Science ®Google Scholar
• Niedermeier M, Hennessy BT, Knight ZA et al. Isoform-selective phosphoinositide 3´-kinase inhibitors inhibit CXCR4 signaling and overcome stromal cell-mediated drug resistance in chronic lymphocytic leukemia: a novel therapeutic approach. Blood113(22), 5549–5557 (2009).
   PubMed Web of Science ®Google Scholar
• Lapalombella R, Andritsos L, Liu Q et al. Lenalidomide treatment promotes CD154 expression on CLL cells and enhances production of antibodies by normal B cells through a PI3-kinase-dependent pathway. Blood115(13), 2619–2629 (2010).
   PubMed Web of Science ®Google Scholar
• Chanan-Khan A, Miller KC, Musial L et al. Clinical efficacy of lenalidomide in patients with relapsed or refractory chronic lymphocytic leukemia: results of a Phase II study. J. Clin. Oncol.24(34), 5343–5349 (2006).
   PubMed Web of Science ®Google Scholar
• Ferrajoli A, Lee BN, Schlette EJ et al. Lenalidomide induces complete and partial remissions in patients with relapsed and refractory chronic lymphocytic leukemia. Blood111(11), 5291–5297 (2008).
   PubMed Web of Science ®Google Scholar
• Andritsos LA, Johnson AJ, Lozanski G et al. Higher doses of lenalidomide are associated with unacceptable toxicity including life-threatening tumor flare in patients with chronic lymphocytic leukemia. J. Clin. Oncol.26(15), 2519–2525 (2008).
   PubMed Web of Science ®Google Scholar
• Hallaert DY, Jaspers A, van Noesel CJ, van Oers MH, Kater AP, Eldering E. c-Abl kinase inhibitors overcome CD40-mediated drug resistance in CLL: implications for therapeutic targeting of chemoresistant niches. Blood112(13), 5141–5149 (2008).
   PubMed Web of Science ®Google Scholar
• O’Brien S, Moore JO, Boyd TE et al. Randomized Phase III trial of fludarabine plus cyclophosphamide with or without oblimersen sodium (Bcl-2 antisense) in patients with relapsed or refractory chronic lymphocytic leukemia. J. Clin. Oncol.25(9), 1114–1120 (2007).
   PubMed Web of Science ®Google Scholar
• Balakrishnan K, Wierda WG, Keating MJ, Gandhi V. Gossypol, a BH3 mimetic, induces apoptosis in chronic lymphocytic leukemia cells. Blood112(5), 1971–1980 (2008).
   PubMed Web of Science ®Google Scholar
• Balakrishnan K, Burger JA, Wierda WG, Gandhi V. AT-101 induces apoptosis in CLL B cells and overcomes stromal cell-mediated Mcl-1 induction and drug resistance. Blood113(1), 149–153 (2009).
   PubMed Web of Science ®Google Scholar
• O’Brien SM, Claxton DF, Crump M et al. Phase I study of obatoclax mesylate (GX15-070), a small molecule pan-Bcl-2 family antagonist, in patients with advanced chronic lymphocytic leukemia. Blood113(2), 299–305 (2009).
   PubMed Web of Science ®Google Scholar
• Furman RR, Asgary Z, Mascarenhas JO, Liou HC, Schattner EJ. Modulation of NF-κB activity and apoptosis in chronic lymphocytic leukemia B cells. J. Immunol.164(4), 2200–2206 (2000).
   PubMed Web of Science ®Google Scholar
• Hewamana S, Lin TT, Jenkins C et al. The novel nuclear factor-κB inhibitor LC-1 is equipotent in poor prognostic subsets of chronic lymphocytic leukemia and shows strong synergy with fludarabine. Clin. Cancer Res.14(24), 8102–8111 (2008).
   PubMed Web of Science ®Google Scholar
• Faderl S, Rai K, Gribben J et al. Phase II study of single-agent bortezomib for the treatment of patients with fludarabine-refractory B-cell chronic lymphocytic leukemia. Cancer107(5), 916–924 (2006).
   PubMed Web of Science ®Google Scholar
• Zent CS, LaPlant BR, Johnston PB et al. The treatment of recurrent/refractory chronic lymphocytic leukemia/small lymphocytic lymphoma (CLL) with everolimus results in clinical responses and mobilization of CLL cells into the circulation. Cancer116(9), 2201–2207 (2010).
   PubMed Web of Science ®Google Scholar
• Coll-Mulet L, Iglesias-Serret D, Santidrian AF et al. MDM2 antagonists activate p53 and synergize with genotoxic drugs in B-cell chronic lymphocytic leukemia cells. Blood107(10), 4109–4114 (2006).
   PubMed Web of Science ®Google Scholar
• Kojima K, Konopleva M, McQueen T, O’Brien S, Plunkett W, Andreeff M. MDM2 inhibitor nutlin-3a induces p53-mediated apoptosis by transcription-dependent and transcription-independent mechanisms and may overcome ATM-mediated resistance to fludarabine in chronic lymphocytic leukemia. Blood108(3), 993–1000 (2006).
   PubMed Web of Science ®Google Scholar
• Pathan NI, Chu P, Hariharan K, Cheney C, Molina A, Byrd J. Mediation of apoptosis by and antitumor activity of lumiliximab in chronic lymphocytic leukemia cells and CD23+ lymphoma cell lines. Blood111(3), 1594–1602 (2008).
   PubMed Web of Science ®Google Scholar
• Byrd JC, Kipps TJ, Flinn IW et al. Phase 1/2 study of lumiliximab combined with fludarabine, cyclophosphamide, and rituximab in patients with relapsed or refractory chronic lymphocytic leukemia. Blood115(3), 489–495 (2010).
   PubMed Web of Science ®Google Scholar
• Coiffier B, Lepretre S, Pedersen LM et al. Safety and efficacy of ofatumumab, a fully human monoclonal anti-CD20 antibody, in patients with relapsed or refractory B-cell chronic lymphocytic leukemia: a Phase 1–2 study. Blood111(3), 1094–1100 (2008).
   PubMed Web of Science ®Google Scholar
• Wierda WG, Kipps TJ, Mayer J et al. Ofatumumab as single-agent CD20 immunotherapy in fludarabine-refractory chronic lymphocytic leukemia. J. Clin. Oncol.28(10), 1749–1755 (2010).
   PubMed Web of Science ®Google Scholar
• Mossner E, Brunker P, Moser S et al. Increasing the efficacy of CD20 antibody therapy through the engineering of a new type II anti-CD20 antibody with enhanced direct and immune effector cell-mediated B-cell cytotoxicity. Blood115(22), 4393–4402 (2010).
   PubMed Web of Science ®Google Scholar