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Acute myeloid leukemia

Immunomodulation with pomalidomide at early lymphocyte recovery after induction chemotherapy in newly diagnosed AML and high-risk MDS

Leukemia volume 34, pages 1563–1576 (2020)Cite this article

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Abstract

An immunosuppressive microenvironment promoting leukemia cell immune escape plays an important role in the pathogenesis of AML. Through its interaction with cereblon, a substrate receptor for the E3 ubiquitin ligase complex, pomalidomide leads to selective ubiquitination of transcription factors Aiolos and Ikaros thereby promoting immune modulation. In this phase I trial, 51 newly diagnosed non-favorable risk AML and high-risk MDS patients were enrolled and treated with AcDVP16 (cytarabine 667 mg/m2/day IV continuous infusion days 1–3, daunorubicin 45 mg/m2 IV days 1–3, etoposide 400 mg/m2 IV days 8–10) induction therapy followed by dose- and duration-escalation pomalidomide beginning at early lymphocyte recovery. Forty-three patients (AML: n = 39, MDS: n = 4) received pomalidomide. The maximum tolerated dose of pomalidomide was 4 mg for 21 consecutive days. The overall complete remission (CR + CRi) rate, median overall survival, and disease-free survival were 75%, 27.1 and 20.6 months, respectively. Subset analyses revealed 86% CR/CRi rate in AML patients with unfavorable-risk karyotype treated with pomalidomide. Pomalidomide significantly decreased Aiolos expression in both CD4+ and CD8+ peripheral blood and bone marrow T cells, promoted T cell differentiation, proliferation, and heightened their cytokine production. Finally, pomalidomide induced distinct gene expression changes in immune function-related ontologies in CD4+ and CD8+ T cells.

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Fig. 1: Study schema and survival outcomes.
Fig. 2: Survival outcomes.
Fig. 3: Aiolos expression in T cells as a pharmacodynamic biomarker of in vivo pomalidomide effect.
Fig. 4: Pomalidomide induces unique changes in T cell gene expression in vivo.

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Acknowledgements

This data was presented at the annual American Society of Hematology conference in 2015 in Orlando, FL (poster), 2016 in San Diego, CA (poster), and 2018 in San Diego, CA (oral presentation). This study was supported in part by research funding from UM1-CA186691 and P30 CA006973 (Johns Hopkins), 5-UM1-CA186704 (University of North Carolina), and P30CA016359/5-UM1-CA186689-5 (Yale). JFZ was supported and funded by Leukemia and Lymphoma Society Special Fellow in Clinical Research Award. HAK was supported by ASBMT New Investigator Award/Gabrielle’s Angel Foundation and by the Vienna Fund for Innovative Cancer Research. AMZ is a Leukemia and Lymphoma Society Scholar in Clinical Research and is also supported by a NCI’s Cancer Clinical Investigator Team Leadership Award (CCITLA). The authors would like to thank the research support staff at Johns Hopkins Sidney Kimmel Comprehensive Cancer Center, University of North Carolina, Lineberger Comprehensive Cancer Center, and Yale Cancer Center. We would also like to thank all of the patients and their families who trusted us for their care. Without these partnerships, this trial could not have been performed.

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Author notes

  1. These authors contributed equally: Joshua F. Zeidner, Hanna A. Knaus

Authors and Affiliations

  1. University of North Carolina Lineberger Comprehensive Cancer Center, Chapel Hill, NC, USA

    Joshua F. Zeidner, Catherine C. Coombs & Matthew C. Foster

  2. Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA

    Hanna A. Knaus, Amanda L. Blackford, Raul Montiel-Esparza, Gabrielle T. Prince, Lukasz P. Gondek, Gabriel Ghiaur, Margaret M. Showel, Amy E. DeZern, Keith W. Pratz, B. Douglas Smith, Mark J. Levis, Judith E. Karp, Leo Luznik & Ivana Gojo

  3. Department of Medicine I Division of Bone Marrow Transplantation and Cellular Therapies, Medical University of Vienna, Vienna, Austria

    Hanna A. Knaus

  4. Yale Cancer Center, New Haven, CT, USA

    Amer M. Zeidan & Steven Gore

  5. Division of Bioinformatics, Biocenter, Medical University of Innsbruck, Innsbruck, Austria

    Hubert Hackl

  6. National Cancer Institute, Rockville, MD, USA

    Howard Streicher

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Contributions

JFZ, HAK, LL, and IG designed research, performed research, collected data, analyzed and interpreted data, and wrote the manuscript. AMZ, RME, GTP, LPG, GG, MMS, AED, KWP, BDS, MJL, SG, CCC, and MCF performed research. ALB and HH analyzed and interpreted the data, and performed statistical analysis. HS designed research. JEK designed research and wrote the manuscript.

Funding

This study was supported in part by research funding from UM1-CA186691 and P30 CA006973 (Johns Hopkins), 5-UM1-CA186704 (University of North Carolina), and P30CA016359/5-UM1-CA186689-5 (Yale). JFZ was supported and funded by Leukemia and Lymphoma Society Special Fellow in Clinical Research Award. HAK was supported by ASBMT New Investigator Award/Gabrielle’s Angel Foundation and by the Vienna Fund for Innovative Cancer Research. AMZ is a Leukemia and Lymphoma Society Scholar in Clinical Research and is also supported by a NCI’s Cancer Clinical Investigator Team Leadership Award (CCITLA).

Corresponding author

Correspondence to Ivana Gojo.

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Conflict of interest

JFZ reports receiving research funding from Celgene, Merck, Takeda, and Tolero Pharmaceuticals, honoraria from AbbVie, Agios, Celgene, Daiichi Sankyo, Genentech, Pfizer, and Tolero Pharmaceuticals, and has served as a consultant for AsystBio Laboratories, Celgene, Covance, and Takeda. AMZ reports receiving research funding (institutional) from Celgene, Acceleron, Abbvie, Otsuka, Pfizer, Medimmune/AstraZeneca, Boehringer-Ingelheim, Trovagene, Incyte, Takeda, and ADC Therapeutics, consultancy with and received honoraria from AbbVie, Otsuka, Pfizer, Jazz, Celgene, Ariad, Incyte, Agios, Boehringer-Ingelheim, Novartis, Acceleron, Astellas, Daiichi Sankyo, Cardinal Health, Seattle Genetics, BeyondSpring, and Takeda. None of these relationships were related to the development of this manuscript. BDS reports being on Data Safety Monitoring Board for Celgene and has served as a consultant for Agios, Bristol-Myers Squibb, Jazz, Novartis, and Pfizer. MJL reports receiving research funding from Astellas, FujiFilm, and Novartis, and has served as a consultant for Agios, Amgen, Astellas, Daiichi Sankyo, FujiFilm, Karyopharm, Menarini, and Novartis. CCC has received honoraria from Abbvie, Loxo, Pharmacyclics, Octapharma, and H3 Biomedicine, has served as a consultant for Abbvie, Covance, and Cowen & Co., and has received institutional funding from Incyte, Gilead, AROG, Loxo, and H3 Biomedicine. LL has received research support from Genentech and Merck and has a patent licensed to WindMIL Therapeutics (WO2014085437A2). IG received research funding from Merck and Amgen, and participated in the advisory board meetings for Amgen, Jazz, Novartis and Abbvie. None of these relationships were related to the development of this manuscript. All other authors declare no conflict of interest.

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Zeidner, J.F., Knaus, H.A., Zeidan, A.M. et al. Immunomodulation with pomalidomide at early lymphocyte recovery after induction chemotherapy in newly diagnosed AML and high-risk MDS. Leukemia 34, 1563–1576 (2020). https://doi.org/10.1038/s41375-019-0693-4

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