Copanlisib for the treatment of adults with relapsed follicular lymphoma

References

• National Cancer Institute. Surveillance, epidemiology, and end results program. Cancer stat facts: Non-Hodgkin lymphoma. 2017 [cited 2020 Jan 27[th]]. Available from: https://seer.cancer.gov/statfacts/html/nhl.html
   Google Scholar
• Swerdlow SH, Campo E, Harris NL, et al. WHO classification of tumours of haematopoietic and lymphoid tissues. In: Bosman FT, Jaffe ES, Lakhani SR, et al., editors. WHO classification of tumours. Lyon, France: IARC; 2008.
   Google Scholar
• Rimsza LM, Li H, Braziel RM, et al. Impact of histological grading on survival in the SWOG S0016 follicular lymphoma cohort. Haematologica. 2018;103:151–153.
   Web of Science ®Google Scholar
• Ott G, Katzenberger T, Lohr A, et al. Cytomorphologic, immunohistochemical, and cytogenetic profiles of follicular lymphoma: 2 types of follicular lymphoma grade 3. Blood. 2002;99:3806–3812.
   PubMed Web of Science ®Google Scholar
• Lackraj T, Goswami R, Kridel R. Pathogenesis of follicular lymphoma. Best Pract Res Clin Haematol. 2018;31(1):2–14.
   PubMed Web of Science ®Google Scholar
• Kahl BS, Yang DT. Follicular lymphoma: evolving therapeutic strategies. Blood. 2016;127:2055–2063.
   PubMed Web of Science ®Google Scholar
• Freedman A. Follicular lymphoma: 2018 update on diagnosis and management. Am J Hematol. 2018;93(2):296–305.
   PubMed Web of Science ®Google Scholar
• Conconi A, Lobetti‐Bodoni C, Montoto S, et al. Life expectancy of young adults with follicular lymphoma. Ann Oncol. 2015;26:2317–2322.
   PubMed Web of Science ®Google Scholar
• Sorigue M, Tuset V, Sancho JM. Treatment of localized-stage follicular lymphoma. Eur J Haematol. 2018 May 12;101:245–256. [Epub ahead of print].
   Web of Science ®Google Scholar
• Ardeshna KM, Qian W, Smith P, et al. Rituximab versus a watch‐and‐wait approach in patients with advanced‐stage, asymptomatic, non‐bulky follicular lymphoma: an open‐label randomised phase 3 trial. Lancet Oncol. 2014;15:424–435.
   PubMed Web of Science ®Google Scholar
• Brice P, Bastion Y, Lepage E, et al. Comparison in low-tumor-burden follicular lymphomas between an initial no-treatment policy, prednimustine, or interferon alfa: a randomized study from the Groupe d’Etude des Lymphomes Folliculaires. Groupe d’Etude des Lymphomes de l’Adulte. J Clin Oncol. 1997;15(3):1110–1117.
   PubMed Web of Science ®Google Scholar
• Hiddemann W, Kneba M, Dreyling M, et al. Frontline therapy with rituximab added to the combination of cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) significantly improves the outcome for patients with advanced‐stage follicular lymphoma compared with therapy with chop alone: results of a prospective randomized study of the German low‐grade lymphoma study group. Blood. 2005;106:3725–3732.
   PubMed Web of Science ®Google Scholar
• Luminari S, Ferrari A, Manni M, et al. Long‐term results of the FOLL05 trial comparing R‐CVP versus R‐CHOP versus R‐FM for the initial treatment of patients with advanced‐stage symptomatic follicular lymphoma. J Clin Oncol. 2018;36:689–696.
   PubMed Web of Science ®Google Scholar
• Luminari S, Bellei M, Biasoli I, et al. Follicular lymphoma – treatment and prognostic factors. Rev Bras Hematol Hemoter. 2012;34(1):54–59.
   PubMedGoogle Scholar
• Sehn LH, Chua N, Mayer J, et al. Obinutuzumab plus bendamustine versus bendamustine monotherapy in patients with rituximab‐refractory indolent non‐hodgkin lymphoma (GADOLIN): A randomised, controlled, open‐label, multicentre, phase 3 trial. Lancet Oncol. 2016;17:1081–1093.
   PubMed Web of Science ®Google Scholar
• Leonard JP, Trneny M, Izutsu K, et al. AUGMENT: A phase III randomized study of lenalidomide plus rituximab (R2) vs rituximab/placebo in patients with relapsed/refractory indolent non‐Hodgkin lymphoma. Presented at: American Society of Hematology Annual Meeting; 2018; San Diego, CA, USA.
   Google Scholar
• Rizzieri D. Zevalin(®) (ibritumomab tiuxetan): after more than a decade of treatment experience, what have we learned? Crit Rev Oncol Hematol. 2016;105:5–17.
   PubMed Web of Science ®Google Scholar
• Jurinovic V, Metzner B, Pfreundschuh M, et al. Autologous stem cell transplantation for patients with early progression of follicular lymphoma – retrospective analysis of 2 randomized trials of the German low grade lymphoma study group. Blood. 2016;128:3464.
   Google Scholar
• Matasar MJ, Luminari S, Barr PM, et al., Follicular lymphoma: recent and emerging therapies, treatment strategies, and remaining unmet needs. Oncologist. 2019;24(11):1236–1250.
   PubMed Web of Science ®Google Scholar
• Dreyling M, Ghielmini M, Marcus R, et al. Newly diagnosed and relapsed follicular lymphoma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2011;22(suppl 6):59–63.
   PubMedGoogle Scholar
• Okkenhaug K, Graupera M, Vanhaesebroeck B. Targeting PI3K in cancer: impact on tumor cells, their protective stroma, angiogenesis and immunotherapy. Cancer Discov. 2016;6:1090–1105.
   PubMed Web of Science ®Google Scholar
• Shariati M, Meric-Bernstam F. Targeting AKT for cancer therapy. Expert Opin Investig Drugs. 2019;28(11):977–988.
   PubMed Web of Science ®Google Scholar
• Gopal AK, Kahl BS, de Vos S, et al. PI3Kd inhibition by idelalisib in patients with relapsed indolent lymphoma. N Engl J Med. 2014;370:1008–1018.
   PubMed Web of Science ®Google Scholar
• Cheah CY, Fowler NH. Idelalisib in the management of lymphoma. Blood. 2016;128:331–336.
   PubMed Web of Science ®Google Scholar
• Burris HA 3rd, IW F, MR P, et al., Umbralisib, a novel PI3Kδ and casein kinase-1ε 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(4):486–496.
   PubMed Web of Science ®Google Scholar
• Flinn IW, Miller CB, Ardeshna KM, et al. Dynamo: A phase 2 study demonstrating the clinical activity of duvelisib in patients with relapsed refractory indolent non‐Hodgkin lymphoma. Blood. 2016;128:1218.
   Web of Science ®Google Scholar
• Patel K, Danilov AV, Pagel JM. Duvelisib for CLL/SLL and follicular non-Hodgkin lymphoma. Blood. 2019;134(19):1573–1577.
   PubMed Web of Science ®Google Scholar
• Flinn IW, Miller CB, Ardeshna KM, et al. DYNAMO: a phase II study of duvelisib (IPI-145) in patients with refractory indolent non-Hodgkin lymphoma. Clin Oncol. 2019;37(11):912–922.
   Web of Science ®Google Scholar
• Markham A. Copanlisib: first global approval. Drugs. 2017;77(18):2057–2062.
   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(3):573–586.
   PubMed Web of Science ®Google Scholar
• Fruman DA, Chiu H, Hopkins BD, et al. The PI3K pathway in human disease. Cell. 2017;170:605–635.
   PubMed Web of Science ®Google Scholar
• Busaidy NL, Farooki A, Dowlati A, et al. Management of metabolic effects associated with anticancer agents targeting the PI3K-Akt-mTOR pathway. J Clin Oncol. 2012;30:2919–2929.
   PubMed Web of Science ®Google Scholar
• Mensah FA, Blaize JP, Bryan LJ. Spotlight on copanlisib and its potential in the treatment of relapsed/refractory follicular lymphoma: evidence to date. Onco Targets Ther. 2018;11:4817‐4827.
   PubMed Web of Science ®Google Scholar
• Lampson BL, Brown JR. PI3Kδ-selective and PI3Kα/δ-combinatorial inhibitors in clinical development for B-cell non-Hodgkin lymphoma. Expert Opin Investig Drugs. 2017;26(11):1267–1279.
   PubMed Web of Science ®Google Scholar
• Lannutti BJ, Meadows SA, Herman SE, et al. CAL-101, a p110delta selective phosphatidylinositol-3-kinase inhibitor for the treatment of B-cell malignancies, inhibits PI3K signaling and cellular viability. Blood. 2011;117(2):591–594.
   PubMed Web of Science ®Google Scholar
• Seiler T, Hutter G, Dreyling M. The emerging role of PI3K inhibitors in the treatment of hematological malignancies: preclinical data and clinical progress to date. Drugs. 2016;76:639–646.
   PubMed Web of Science ®Google Scholar
• Cui W, Cai Y, Wang W, et al. Frequent copy number variations of PI3K/AKT pathway and aberrant protein expressions of PI3K subunits are associated with inferior survival in diffuse large B cell lymphoma. J Transl Med. 2014;12:10–12.
   PubMed Web of Science ®Google Scholar
• Krause G, Hassenrück F, Hallek M. Copanlisib for treatment of B-cell malignancies: the development of a PI3K inhibitor with considerable differences to idelalisib. Drug Des Devel Ther. 2018;12:2577‐2590.
   Web of Science ®Google Scholar
• Gerisch M, Schwarz T, Lang D, et al. Pharmacokinetics of intravenous pan-class I phosphatidylinositol 3-kinase (PI3K) inhibitor [14C]copanlisib (BAY 80-6946) in a mass balance study in healthy male volunteers. Cancer Chemother Pharmacol. 2017;80(3):535–544.
   PubMed Web of Science ®Google Scholar
• Morschhauser F, Awada A, Machiels JP, et al. Pharmacodynamic study of copanlisib in patients with non-Hodgkin’s lymphoma and advanced solid tumors: confirmation of on-target PI3K inhibitory activity. Blood. 2017;130:1256–1259.
   Web of Science ®Google Scholar
• Liu N, Rowley BR, Bull CO, et al. BAY 80-6946 is a highly selective intravenous PI3K inhibitor with potent p110α and p110δ activities in tumor cell lines and xenograft models. Mol Cancer Ther. 2013;12:2319–2330.
   PubMed Web of Science ®Google Scholar
• Paul J, Soujon M, Wengner AM, et al. Simultaneous inhibition of PI3Kδ and PI3Kα induces ABC-DLBCL regression by blocking BCR-dependent and -independent activation of NF-κB and AKT. Cancer Cell. 2017;31(1):64–78.
   PubMed Web of Science ®Google Scholar
• Patnaik A, Appleman LJ, Tolcher AW, et al. First-in-human phase I study of copanlisib (BAY 80-6946), an intravenous pan-class I phosphatidylinositol 3-kinase inhibitor, in patients with advanced solid tumors and non-Hodgkin’s lymphomas. Ann Oncol. 2016;27:1928–1940.
   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
• 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
• Launonen A, Hiddemann W, Duenzinger U, et al. Early disease progression predicts poorer survival in patients with follicular lymphoma (FL) in the GALLIUM study. Blood. 2017;130:1490.
   Web of Science ®Google Scholar
• Santoro A, Mollica L, Leppa S, et al. Outcomes for patients with high-risk relapsed or refractory indolent B-cell lymphoma treated with copanlisib in the CHRONOS-1 study. Blood. 2018;132(Supplement 1):395.
   Google Scholar
• Dreyling M, Santoro A, Mollica L, et al. Long-term safety and efficacy of the PI3K-inhibitor copanlisib in patients with relapsed or refractory indolent lymphoma: 2-year follow-up of the CHRONOS-1 study. Am J Hematol. 2019 Dec 23. Online ahead of print.
   PubMed Web of Science ®Google Scholar
• Morschhauser F, Machiels JP, Salles G, et al. On-target pharmacodynamic activity of the PI3K inhibitor copanlisib in paired biopsies from patients with malignant lymphoma and advanced solid tumors. Mol Cancer Ther. 2019 Oct 16. pii: molcanther.0466.2019. [Epub ahead of print]. DOI:https://doi.org/10.1158/1535-7163.MCT-19-0466
   Google Scholar
• Nowakowski GS, Gorbatchevsky I, Hiemeyer F, et al. CHRONOS-2: a randomized, double-blind phase III study of phosphatidylinositol-3 kinase alpha/delta inhibitor copanlisib versus placebo in patients with rituximab-refractory indolent non-Hodgkin’s lymphoma (iNHL). Cancer Res. 2015;75(15suppl):abstractCT212.
   Google Scholar
• Geritano J, Zheng H, Mongay Soler M, et al. Phase III randomized, double-blind, controlled studies of the PI3K inhibitor copanlisib in combination with rituximab or rituximab-based chemotherapy in subjects with relapsed indolent B-cell non-Hodgkin’s lymphoma (iNHL): CHRONOS-3 and CHRONOS-4. Ann Oncol. 2017;28(5):mdx373.040.
   Google Scholar
• Gerecitano J, Santoro A, Leppä S, et al. Safety run-in of copanlisib in combination with rituximab plus bendamustine in patients with relapsed indolent non-Hodgkin’s lymphoma. Hematol Oncol. 2017;35:408–410.
   PubMedGoogle Scholar
• Grommes C, Gayrilovic I, Miller AM, et al. Phase Ib of copanlisib in combination with ibrutinib in recurrent/refractory primary CNS lymphoma (PCNSL). Blood. 2019;134(Supplement 1):1598.
   PubMedGoogle Scholar
• Jiang C, Zhang R, Lee W, et al. Targeting PI3K and PLK1 to overcome ibrutinib-venetoclax resistance in mantle cell lymphoma. Blood. 2019;134(Supplement 1):4062.
   Google Scholar
• Barta SK, Fowler NH, Zain J, et al. Pembrolizumab and copanlisib for the treatment of relapsed or refractory mature T-cell lymphomas. Blood. 2019;134(Supplement 1):4031.
   Google Scholar
• Tarantelli C, Lange M, Gaudio E, et al. Copanlisib synergizes with conventional and targeted agents including venetoclax in B- and T-cell lymphoma models. Blood Adv. 2020;4(5):819‐829.
   PubMed Web of Science ®Google Scholar
• Benanni MM, Nowakoswki G, Rimsza M, et al. Copanlisib in combination with nivolumab in subjects with relapsed/refractory diffuse large B-cell lymphoma and primary mediastinal large B-cell lymphoma: A phase 2 study. Blood. 2019;134(Supplement 1):4090.
   Google Scholar
• Zinzani PL, Patnaik A, Morschhauser M, et al. Pooled safety analysis from phase I and II studies for patients with relapsed indolent non-Hodgkin’s lymphoma treated with intravenous copanlisib. Blood. 2017;130(Supplement 1):4042.
   Google Scholar
• Zinzani PL, Santoro A, Luigina Mollica L, et al. Copanlisib, a PI3K inhibitor, demonstrates a favorable long-term safety profile in a pooled analysis of patients with hematologic malignancies. Blood. 2019;134(supplement 1):4009.
   Google Scholar
• Dreyling M, Leppä S, Comeau T, et al. Outcomes for diabetic patients from the CHRONOS-1 study with relapsed or refractory indolent B-cell lymphoma treated with copanlisib. 23rd Congress of the European Hematology Association; Stockholm, Sweden; 2018 June 14–17. p. PF448 ed.
   Google Scholar
• Cheson BD, O’Brien S, Ewer MS, et al. Optimal management of adverse events from copanlisib in the treatment of patients with non-Hodgkin lymphomas. Clin Lymphoma Myeloma Leuk. 2019;19(3):135–141.
   PubMed Web of Science ®Google Scholar
• Zelenetz AD, Jagadeesh D, Reddy NM, et al. Results of the PI3Kδ inhibitor ME-401 alone or with rituximab in relapsed/refractory (R/R) follicular lymphoma (FL). J Clin Oncol. 2019;37(15):7512.
   Web of Science ®Google Scholar