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The surfaceome of multiple myeloma cells suggests potential immunotherapeutic strategies and protein markers of drug resistance

Author

Listed:
  • Ian D. Ferguson

    (University of California
    Stanford University School of Medicine)

  • Bonell Patiño-Escobar

    (University of California)

  • Sami T. Tuomivaara

    (University of California)

  • Yu-Hsiu T. Lin

    (University of California)

  • Matthew A. Nix

    (University of California)

  • Kevin K. Leung

    (University of California)

  • Corynn Kasap

    (University of California)

  • Emilio Ramos

    (University of California)

  • Wilson Nieves Vasquez

    (University of California)

  • Alexis Talbot

    (University of California
    Université de Paris)

  • Martina Hale

    (University of California)

  • Akul Naik

    (University of California)

  • Audrey Kishishita

    (University of California
    University of California)

  • Priya Choudhry

    (University of California)

  • Antonia Lopez-Girona

    (Bristol Myers Squibb/Celgene)

  • Weili Miao

    (Stanford University School of Medicine)

  • Sandy W. Wong

    (University of California)

  • Jeffrey L. Wolf

    (University of California)

  • Thomas G. Martin

    (University of California)

  • Nina Shah

    (University of California)

  • Scott Vandenberg

    (University of California)

  • Sonam Prakash

    (University of California)

  • Lenka Besse

    (Kantonsspital St. Gallen)

  • Christoph Driessen

    (Kantonsspital St. Gallen)

  • Avery D. Posey

    (University of Pennsylvania School of Medicine
    Corporal Michael J. Crescenz VA Medical Center)

  • R. Dyche Mullins

    (University of California
    Howard Hughes Medical Institute)

  • Justin Eyquem

    (University of California
    Parker Institute for Cancer Immunotherapy
    Gladstone Institute for Genomic Immunology)

  • James A. Wells

    (University of California)

  • Arun P. Wiita

    (University of California)

Abstract

The myeloma surface proteome (surfaceome) determines tumor interaction with the microenvironment and serves as an emerging arena for therapeutic development. Here, we use glycoprotein capture proteomics to define the myeloma surfaceome at baseline, in drug resistance, and in response to acute drug treatment. We provide a scoring system for surface antigens and identify CCR10 as a promising target in this disease expressed widely on malignant plasma cells. We engineer proof-of-principle chimeric antigen receptor (CAR) T-cells targeting CCR10 using its natural ligand CCL27. In myeloma models we identify proteins that could serve as markers of resistance to bortezomib and lenalidomide, including CD53, CD10, EVI2B, and CD33. We find that acute lenalidomide treatment increases activity of MUC1-targeting CAR-T cells through antigen upregulation. Finally, we develop a miniaturized surface proteomic protocol for profiling primary plasma cell samples with low inputs. These approaches and datasets may contribute to the biological, therapeutic, and diagnostic understanding of myeloma.

Suggested Citation

  • Ian D. Ferguson & Bonell Patiño-Escobar & Sami T. Tuomivaara & Yu-Hsiu T. Lin & Matthew A. Nix & Kevin K. Leung & Corynn Kasap & Emilio Ramos & Wilson Nieves Vasquez & Alexis Talbot & Martina Hale & A, 2022. "The surfaceome of multiple myeloma cells suggests potential immunotherapeutic strategies and protein markers of drug resistance," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31810-6
    DOI: 10.1038/s41467-022-31810-6
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    References listed on IDEAS

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    1. Sabarinath V. Radhakrishnan & Tim Luetkens & Sandra D. Scherer & Patricia Davis & Erica R. Vander Mause & Michael L. Olson & Sara Yousef & Jens Panse & Yasmina Abdiche & K. David Li & Rodney R. Miles , 2020. "CD229 CAR T cells eliminate multiple myeloma and tumor propagating cells without fratricide," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    2. Mahmoud Ghandi & Franklin W. Huang & Judit Jané-Valbuena & Gregory V. Kryukov & Christopher C. Lo & E. Robert McDonald & Jordi Barretina & Ellen T. Gelfand & Craig M. Bielski & Haoxin Li & Kevin Hu & , 2019. "Next-generation characterization of the Cancer Cell Line Encyclopedia," Nature, Nature, vol. 569(7757), pages 503-508, May.
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    4. Benjamin Salzer & Christina M. Schueller & Charlotte U. Zajc & Timo Peters & Michael A. Schoeber & Boris Kovacic & Michelle C. Buri & Elisabeth Lobner & Omer Dushek & Johannes B. Huppa & Christian Obi, 2020. "Engineering AvidCARs for combinatorial antigen recognition and reversible control of CAR function," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
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    Cited by:

    1. Yandan Yang & Arnold Bolomsky & Thomas Oellerich & Ping Chen & Michele Ceribelli & Björn Häupl & George W. Wright & James D. Phelan & Da Wei Huang & James W. Lord & Callie K. Winkle & Xin Yu & Jan Wis, 2022. "Oncogenic RAS commandeers amino acid sensing machinery to aberrantly activate mTORC1 in multiple myeloma," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

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