Targeting the B cell receptor pathway in non-Hodgkin lymphoma

References

• Taccioli G, Rathbun G, Oltz E, et al. Impairment of V(D)J recombination in double-strand break repair mutants. Science. 1993;260:207–210.
   PubMed Web of Science ®Google Scholar
• Srinivasan L, Sasaki Y, Calado DP, et al. PI3 kinase signals BCR-dependent mature B cell survival. Cell. 2009;139:573–586.
   PubMed Web of Science ®Google Scholar
• Bannish G, Fuentes-Panana EM, Cambier JC, et al. Ligand-independent signaling functions for the B lymphocyte antigen receptor and their role in positive selection during B lymphopoiesis. J Exp Med. 2001;194:1583–1596.
   PubMed Web of Science ®Google Scholar
• Li Z, Woo CJ, Iglesias-Ussel MD, et al. The generation of antibody diversity through somatic hypermutation and class switch recombination. Genes Dev. 2004;18:1–11.
   PubMed Web of Science ®Google Scholar
• Reth M. Antigen receptor tail clue. Nature. 1989;338:383–384.
   PubMed Web of Science ®Google Scholar
• Saijo K, Schmedt C, Su IH, et al. Essential role of Src-family protein tyrosine kinases in NF-kappaB activation during B cell development. Nat Immunol. 2003;4:274–279.
   PubMed Web of Science ®Google Scholar
• Niemann CU, Wiestner A. B-cell receptor signaling as a driver of lymphoma development and evolution. Semin Cancer Biol. 2013;23:410–421.
   PubMed Web of Science ®Google Scholar
• Lam KP, Kuhn R, Rajewsky K. In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell. 1997;90:1073–1083.
   PubMed Web of Science ®Google Scholar
• Mocsai A, Ruland J, Tybulewicz VL. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat Rev Immunol. 2010;10:387–402.
   PubMed Web of Science ®Google Scholar
• Buggy JJ, Elias L. Bruton tyrosine kinase (BTK) and its role in B-cell malignancy. Int Rev Immunol. 2012;31:119–132.
   PubMed Web of Science ®Google Scholar
• De Gorter DJ, Beuling EA, Kersseboom R, et al. Bruton’s tyrosine kinase and phospholipase Cgamma2 mediate chemokine-controlled B cell migration and homing. Immunity. 2007;26:93–104.
   PubMed Web of Science ®Google Scholar
• Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell. 2012;149:274–293.
   PubMed Web of Science ®Google Scholar
• Warsame AA, Aasheim HC, Nustad K, et al. Splenic marginal zone lymphoma with VH1-02 gene rearrangement expresses poly- and self-reactive antibodies with similar reactivity. Blood. 2011;118:3331–3339.
   PubMed Web of Science ®Google Scholar
• Bende RJ, Aarts WM, Riedl RG, et al. Among B cell non-Hodgkin’s lymphomas, MALT lymphomas express a unique antibody repertoire with frequent rheumatoid factor reactivity. J Exp Med. 2005;201:1229–1241.
   PubMed Web of Science ®Google Scholar
• Craig VJ, Arnold I, Gerke C, et al. Gastric MALT lymphoma B cells express polyreactive, somatically mutated immunoglobulins. Blood. 2010;115:581–591.
   PubMed Web of Science ®Google Scholar
• Zhu D, Bhatt S, Lu X, et al. Chlamydophila psittaci-negative ocular adnexal marginal zone lymphomas express self polyreactive B-cell receptors. Leukemia. 2015;29:1587–1599.
   PubMed Web of Science ®Google Scholar
• Sachen KL, Strohman MJ, Singletary J, et al. Self-antigen recognition by follicular lymphoma B-cell receptors. Blood. 2012;120:4182–4190.
   PubMed Web of Science ®Google Scholar
• Cha S-C, Qin H, Kannan S, et al. Nonstereotyped Lymphoma B Cell Receptors Recognize Vimentin as a Shared Autoantigen. J Immunol. 2013;190:4887–4898.
   PubMed Web of Science ®Google Scholar
• Minden MD-V, Ubelhart R, Schneider D, et al. Chronic lymphocytic leukaemia is driven by antigen-independent cell-autonomous signalling. Nature. 2012;489:309–312.
   PubMed Web of Science ®Google Scholar
• Catera R, Silverman GJ, Hatzi K, et al. Chronic lymphocytic leukemia cells recognize conserved epitopes associated with apoptosis and oxidation. Mol Med (Cambridge, Mass). 2008;14:665–674.
   PubMed Web of Science ®Google Scholar
• Chu CC, Catera R, Zhang L, et al. Many chronic lymphocytic leukemia antibodies recognize apoptotic cells with exposed nonmuscle myosin heavy chain IIA: implications for patient outcome and cell of origin. Blood. 2010;115:3907–3915.
   PubMed Web of Science ®Google Scholar
• Seiler T, Woelfle M, Yancopoulos S, et al. Characterization of structurally defined epitopes recognized by monoclonal antibodies produced by chronic lymphocytic leukemia B cells. Blood. 2009;114:3615–3624.
   PubMed Web of Science ®Google Scholar
• Hoogeboom R, Van Kessel KP, Hochstenbach F, et al. A mutated B cell chronic lymphocytic leukemia subset that recognizes and responds to fungi. J Exp Med. 2013;210:59–70.
   PubMed Web of Science ®Google Scholar
• Yamamoto K. Pathogenesis of Sjogren’s syndrome. Autoimmun Rev. 2003;2:13–18.
   PubMed Web of Science ®Google Scholar
• Ekstrom Smedby K, Vajdic CM, Falster M, et al. Autoimmune disorders and risk of non-Hodgkin lymphoma subtypes: a pooled analysis within the InterLymph Consortium. Blood. 2008;111:4029–4038.
   PubMed Web of Science ®Google Scholar
• Malfertheiner P, Megraud F, O’Morain CA, et al. Management of Helicobacter pylori infection–the Maastricht IV/Florence Consensus Report. Gut. 2012;61:646–664.
   PubMed Web of Science ®Google Scholar
• Zucca E, Copie-Bergman C, Ricardi U, et al. Gastric marginal zone lymphoma of MALT type: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2013;24(Suppl 6):vi144–8.
   PubMed Web of Science ®Google Scholar
• Ruskone-Fourmestraux A, Fischbach W, Aleman BM, et al. EGILS consensus report. Gastric extranodal marginal zone B-cell lymphoma of MALT. Gut. 2011;60:747–758.
   PubMed Web of Science ®Google Scholar
• Quinn ER, Chan CH, Hadlock KG, et al. The B-cell receptor of a hepatitis C virus (HCV)-associated non-Hodgkin lymphoma binds the viral E2 envelope protein, implicating HCV in lymphomagenesis. Blood. 2001;98:3745–3749.
   PubMed Web of Science ®Google Scholar
• Marcucci F, Mele A. Hepatitis viruses and non-Hodgkin lymphoma: epidemiology, mechanisms of tumorigenesis, and therapeutic opportunities. Blood. 2011;117:1792–1798.
   PubMed Web of Science ®Google Scholar
• Gisbert JP, Garcia-Buey L, Pajares JM, et al. Systematic review: regression of lymphoproliferative disorders after treatment for hepatitis C infection. Aliment Pharmacol Ther. 2005;21:653–662.
   PubMed Web of Science ®Google Scholar
• Lanemo Myhrinder A, Hellqvist E, Sidorova E, et al. A new perspective: molecular motifs on oxidized LDL, apoptotic cells, and bacteria are targets for chronic lymphocytic leukemia antibodies. Blood. 2008;111:3838–3848.
   PubMed Web of Science ®Google Scholar
• Steininger C, Widhopf GF, Ghia EM, et al. Recombinant antibodies encoded by IGHV1-69 react with pUL32, a phosphoprotein of cytomegalovirus and B-cell superantigen. Blood. 2012;119:2293–2301.
   PubMed Web of Science ®Google Scholar
• Binder M, Müller F, Frick M, et al. CLL B-cell receptors can recognize themselves: alternative epitopes and structural clues for autostimulatory mechanisms in CLL. Blood. 2013;121:239–241.
   PubMed Web of Science ®Google Scholar
• Davis RE, Ngo VN, Lenz G, et al. Chronic active B-cell-receptor signalling in diffuse large B-cell lymphoma. Nature. 2010;463:88–92.
   PubMed Web of Science ®Google Scholar
• Lenz G, Davis RE, Ngo VN, et al. Oncogenic CARD11 Mutations in Human Diffuse Large B Cell Lymphoma. Science. 2008;319:1676–1679.
   PubMed Web of Science ®Google Scholar
• Compagno M, Lim WK, Grunn A, et al. Mutations of multiple genes cause deregulation of NF-[kgr]B in diffuse large B-cell lymphoma. Nature. 2009;459:717–721.
   PubMed Web of Science ®Google Scholar
• Zhang J, Grubor V, Love CL, et al. Genetic heterogeneity of diffuse large B-cell lymphoma. Proceedings of the National Academy of Sciences of the United States of America 2013;110:1398–1403.
   Google Scholar
• Gyrd-Hansen M, Meier P. IAPs: from caspase inhibitors to modulators of NF-kappaB, inflammation and cancer. Nat Rev Cancer. 2010;10:561–574.
   PubMed Web of Science ®Google Scholar
• Mansouri L, Sutton LA, Ljungstrom V, et al. Functional loss of IkappaBepsilon leads to NF-kappaB deregulation in aggressive chronic lymphocytic leukemia. J Exp Med. 2015;212:833–843.
   PubMed Web of Science ®Google Scholar
• Yan Q, Huang Y, Watkins AJ, et al. BCR and TLR signaling pathways are recurrently targeted by genetic changes in splenic marginal zone lymphomas. Haematologica. 2012;97:595–598.
   PubMed Web of Science ®Google Scholar
• Dierlamm J, Baens M, Wlodarska I, et al. The apoptosis inhibitor gene API2 and a novel 18q gene, MLT, are recurrently rearranged in the t(11;18)(q21;q21) associated with mucosa-associated lymphoid tissue lymphomas. Blood. 1999;93:3601–3609.
   PubMed Web of Science ®Google Scholar
• Maes B, Demunter A, Peeters B, et al. BCL10 mutation does not represent an important pathogenic mechanism in gastric MALT-type lymphoma, and the presence of the API2-MLT fusion is associated with aberrant nuclear BCL10 expression. Blood. 2002;99:1398–1404.
   PubMed Web of Science ®Google Scholar
• Willis TG, Jadayel DM, Du MQ, et al. Bcl10 is involved in t(1;14)(p22;q32) of MALT B cell lymphoma and mutated in multiple tumor types. Cell. 1999;96:35–45.
   PubMed Web of Science ®Google Scholar
• Royo C, Salaverria I, Hartmann EM, et al. The complex landscape of genetic alterations in mantle cell lymphoma. Semin Cancer Biol. 2011;21:322–334.
   PubMed Web of Science ®Google Scholar
• Sander S, Calado Dinis P, Srinivasan L, et al. Synergy between PI3K Signaling and MYC in Burkitt Lymphomagenesis. Cancer Cell. 2012;22:167–179.
   PubMed Web of Science ®Google Scholar
• Schmitz R, Young RM, Ceribelli M, et al. Burkitt lymphoma pathogenesis and therapeutic targets from structural and functional genomics. Nature. 2012;490:116–120.
   PubMed Web of Science ®Google Scholar
• Abubaker J, Bavi PP, Al-Harbi S, et al. PIK3CA mutations are mutually exclusive with PTEN loss in diffuse large B-cell lymphoma. Leukemia. 2007;21:2368–2370.
   PubMed Web of Science ®Google Scholar
• Lenz G, Wright GW, Emre NC, et al. Molecular subtypes of diffuse large B-cell lymphoma arise by distinct genetic pathways. Proceedings of the National Academy of Sciences of the United States of America 2008;105:13520–13525.
   Google Scholar
• Havranek O, Xu J, Kohrer S, et al. Tonic B-cell receptor signaling in diffuse large B-cell lymphoma. Blood. 2017;130:995–1006.
   PubMed Web of Science ®Google Scholar
• Rudelius M, Pittaluga S, Nishizuka S, et al. Constitutive activation of Akt contributes to the pathogenesis and survival of mantle cell lymphoma. Blood. 2006;108:1668–1676.
   PubMed Web of Science ®Google Scholar
• Dal Col J, Zancai P, Terrin L, et al. Distinct functional significance of Akt and mTOR constitutive activation in mantle cell lymphoma. Blood. 2008;111:5142–5151.
   PubMed Web of Science ®Google Scholar
• Perez-Galan P, Dreyling M, Wiestner A. Mantle cell lymphoma: biology, pathogenesis, and the molecular basis of treatment in the genomic era. Blood. 2011;117:26–38.
   PubMed Web of Science ®Google Scholar
• Imbruvica [package insert]. Sunnyvale, CA: Pharmacyclics, LLC; 2017.
   Google Scholar
• Calquence [package insert]. Wilmington, DE: AstraZeneca Pharmaceuticals LP; 2017.
   Google Scholar
• Furman RR, Cheng S, Lu P, et al. Ibrutinib resistance in chronic lymphocytic leukemia. N Engl J Med. 2014;370:2352–2354.
   PubMed Web of Science ®Google Scholar
• Woyach JA, Furman RR, Liu TM, et al. Resistance mechanisms for the Bruton’s tyrosine kinase inhibitor ibrutinib. N Engl J Med. 2014;370:2286–2294.
   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
• Advani RH, Buggy JJ, Sharman JP, et al. Bruton tyrosine kinase inhibitor ibrutinib (PCI-32765) has significant activity in patients with relapsed/refractory B-cell malignancies. J Clin Oncol. 2013;31:88–94.
   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
• Burger JA, Tedeschi A, Barr PM, et al. Ibrutinib as Initial Therapy for Patients with Chronic Lymphocytic Leukemia. N Engl J Med. 2015;373:2425–2437.
   PubMed Web of Science ®Google Scholar
• Leong DP, Caron F, Hillis C, et al. The risk of atrial fibrillation with ibrutinib use: a systematic review and meta-analysis. Blood. 2016;128:138–140.
   PubMed Web of Science ®Google Scholar
• Wang ML, Rule S, Martin P, et al. Targeting BTK with ibrutinib in relapsed or refractory mantle-cell lymphoma. N Engl J Med. 2013;369:507–516.
   PubMed Web of Science ®Google Scholar
• Wang ML, Lee H, Chuang H, et al. Ibrutinib in combination with rituximab in relapsed or refractory mantle cell lymphoma: a single-centre, open-label, phase 2 trial. Lancet Oncol. 2016;17:48–56.
   PubMed Web of Science ®Google Scholar
• Noy A, De Vos S, Thieblemont C, et al. Targeting Bruton tyrosine kinase with ibrutinib in relapsed/refractory marginal zone lymphoma. Blood. 2017;129:2224–2232.
   PubMed Web of Science ®Google Scholar
• Byrd JC, Harrington B, O’Brien S, et al. Acalabrutinib (ACP-196) in Relapsed Chronic Lymphocytic Leukemia. N Engl J Med. 2016;374:323–332.
   PubMed Web of Science ®Google Scholar
• Tan EH, Chan A. Evidence-based treatment options for the management of skin toxicities associated with epidermal growth factor receptor inhibitors. Ann Pharmacother. 2009;43:1658–1666.
   PubMed Web of Science ®Google Scholar
• Wang M, Rule S, Zinzani PL, et al. Acalabrutinib in relapsed or refractory mantle cell lymphoma (ACE-LY-004): a single-arm, multicentre, phase 2 trial. Lancet. 2017;391(10121):659–667.
   Google Scholar
• Liu D, Mamorska-Dyga A. Syk inhibitors in clinical development for hematological malignancies. J Hematol Oncol. 2017;10:145.
   PubMed Web of Science ®Google Scholar
• Barr PM, Wei C, Roger J, et al. Syk inhibition with fostamatinib leads to transitional B lymphocyte depletion. Clin Immunol. 2012;142:237–242.
   PubMed Web of Science ®Google Scholar
• Sharman J, Hawkins M, Kolibaba K, et al. An open-label phase 2 trial of entospletinib (GS-9973), a selective spleen tyrosine kinase inhibitor, in chronic lymphocytic leukemia. Blood. 2015;125:2336–2343.
   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. Blood. 2010;115:2578–2585.
   PubMed Web of Science ®Google Scholar
• Skinner M, Philp K, Lengel D, et al. The contribution of VEGF signalling to fostamatinib-induced blood pressure elevation. Br J Pharmacol. 2014;171:2308–2320.
   PubMed Web of Science ®Google Scholar
• Ramanathan S, Di Paolo JA, Jin F, et al. Pharmacokinetics, Pharmacodynamics, and Safety of Entospletinib, a Novel pSYK Inhibitor, Following Single and Multiple Oral Dosing in Healthy Volunteers. Clin Drug Investig. 2017;37:195–205.
   PubMed Web of Science ®Google Scholar
• Barr PM, Saylors GB, Spurgeon SE, et al. Phase 2 study of idelalisib and entospletinib: pneumonitis limits combination therapy in relapsed refractory CLL and NHL. Blood. 2016;127:2411–2415.
   PubMed Web of Science ®Google Scholar
• Zydelig [package insert]. Foster City, CA: Gilead Sciences, Inc; 2017.
   Google Scholar
• Aliquopa [package insert]. Whippany, NJ: Bayer HealthCare Pharmaceuticals Inc; 2017.
   Google Scholar
• Dreyling M, Santoro A, Mollica L, et al. Phosphatidylinositol 3-Kinase Inhibition by Copanlisib in Relapsed or Refractory Indolent Lymphoma. J Clin Oncol. 2017;35:3898–3905.
   PubMed Web of Science ®Google Scholar
• Paul J, Soujon M, Wengner AM, et al. Simultaneous Inhibition of PI3Kdelta and PI3Kalpha Induces ABC-DLBCL Regression by Blocking BCR-Dependent and -Independent Activation of NF-kappaB and AKT. Cancer Cell. 2017;31:64–78.
   PubMed Web of Science ®Google Scholar
• Will M, Qin ACR, Toy W, et al. Rapid induction of apoptosis by PI3K inhibitors is dependent upon their transient inhibition of RAS-ERK signaling. Cancer Discov. 2014;4:334–347.
   PubMed Web of Science ®Google Scholar
• Burris HA 3rd, Flinn IW, Patel MR, et al. Umbralisib, a novel PI3Kdelta and casein kinase-1epsilon inhibitor, in relapsed or refractory chronic lymphocytic leukaemia and lymphoma: an open-label, phase 1, dose-escalation, first-in-human study. Lancet Oncol. 2018;19:486–496.
   PubMed Web of Science ®Google Scholar
• Flinn IW, Hillmen P, Montillo M, et al. Results from the phase 3 DUOTM trial: a randomized comparison of duvelisib vs ofatumumab in patients with relapsed/refractory chronic lymphocytic leukemia or small lymphocytic lymphoma. Blood. 2017;130:493.
   Google Scholar
• Greenwell IB, Flowers CR, Blum KA, et al. Clinical use of PI3K inhibitors in B-cell lymphoid malignancies: today and tomorrow. Expert Rev Anticancer Ther. 2017;17:271–279.
   PubMed Web of Science ®Google Scholar
• Chen Q, Jain N, Ayer T, et al. Economic Burden of Chronic Lymphocytic Leukemia in the Era of Oral Targeted Therapies in the United States. J Clin Oncol. 2017;35:166–174.
   PubMed Web of Science ®Google Scholar
• Chen CT, Kesselheim AS. Journey of Generic Imatinib: a case study in oncology drug pricing. J of Oncol Practice. 2017;13:352–355.
   PubMed Web of Science ®Google Scholar
• Wang SS, Vajdic CM, Linet MS, et al. Associations of non-Hodgkin Lymphoma (NHL) risk with autoimmune conditions according to putative NHL loci. Am J Epidemiol. 2015;181(6):406-421.
   Web of Science ®Google Scholar
• Cheah CY, Chihara D, Romaguera JE, et al. Patients with mantle cell lymphoma failing ibrutinib are unlikely to respond to salvage chemotherapy and have poor outcomes. Ann Oncol. 2015;26:1175–1179.
   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;1:80–87.
   PubMed Web of Science ®Google Scholar
• Kurtz DM, Green MR, Bratman SV, et al. Noninvasive monitoring of diffuse large B-cell lymphoma by immunoglobulin high-throughput sequencing. Blood. 2015;125:3679–3687.
   PubMed Web of Science ®Google Scholar
• Scherer F, Kurtz DM, Newman AM, et al. Distinct biological subtypes and patterns of genome evolution in lymphoma revealed by circulating tumor DNA. Sci Transl Med. 2016;8:364ra155–364ra155.
   PubMed Web of Science ®Google Scholar
• Gopal AK, Kahl BS, De Vos S, et al. PI3Kdelta inhibition by idelalisib in patients with relapsed indolent lymphoma. N Engl J Med. 2014;370:1008–1018.
   PubMed Web of Science ®Google Scholar
• Dreyling M, Morschhauser F, Bouabdallah K, et al. Phase II study of copanlisib, a PI3K inhibitor, in relapsed or refractory, indolent or aggressive lymphoma. Ann Oncol. 2017;28:2169–2178.
   PubMed Web of Science ®Google Scholar