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Therapy-induced secretion of spliceosomal components mediates pro-survival crosstalk between ovarian cancer cells

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  • Victoria O. Shender

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
    Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency
    Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences)

  • Ksenia S. Anufrieva

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
    Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Polina V. Shnaider

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
    Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency
    Faculty of Biology; Lomonosov Moscow State University)

  • Georgij P. Arapidi

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
    Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency
    Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences
    Moscow Institute of Physics and Technology (State University))

  • Marat S. Pavlyukov

    (Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences)

  • Olga M. Ivanova

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
    Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Irina K. Malyants

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency
    Mendeleev University of Chemical Technology of Russia)

  • Grigory A. Stepanov

    (Siberian Branch, Russian Academy of Sciences
    Novosibirsk State University)

  • Evgenii Zhuravlev

    (Siberian Branch, Russian Academy of Sciences)

  • Rustam H. Ziganshin

    (Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences)

  • Ivan O. Butenko

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Olga N. Bukato

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Ksenia M. Klimina

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
    Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Vladimir A. Veselovsky

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Tatiana V. Grigorieva

    (Kazan Federal University)

  • Sergey Y. Malanin

    (Kazan Federal University)

  • Olga I. Aleshikova

    (Gynaecology and Perinatal Medicine named after V.I. Kulakov
    Russian Research Center of Roentgenology and Radiology)

  • Andrey V. Slonov

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Nataliya A. Babaeva

    (Gynaecology and Perinatal Medicine named after V.I. Kulakov
    Russian Research Center of Roentgenology and Radiology)

  • Lev A. Ashrafyan

    (Gynaecology and Perinatal Medicine named after V.I. Kulakov
    Russian Research Center of Roentgenology and Radiology)

  • Elena Khomyakova

    (Exosome Analytics)

  • Evgeniy G. Evtushenko

    (Faculty of Chemistry; Lomonosov Moscow State University)

  • Maria M. Lukina

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
    Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Zixiang Wang

    (Shandong University; Jinan)

  • Artemiy S. Silantiev

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Anna A. Nushtaeva

    (Siberian Branch, Russian Academy of Sciences)

  • Daria D. Kharlampieva

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Vassili N. Lazarev

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
    Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Arseniy I. Lashkin

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Lorine K. Arzumanyan

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Irina Yu. Petrushanko

    (Russian Academy of Sciences)

  • Alexander A. Makarov

    (Russian Academy of Sciences)

  • Olga S. Lebedeva

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
    Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Alexandra N. Bogomazova

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
    Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Maria A. Lagarkova

    (Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical and Biological Agency)

  • Vadim M. Govorun

    (Research Institute for Systems Biology and Medicine)

Abstract

Ovarian cancer often develops resistance to conventional therapies, hampering their effectiveness. Here, using ex vivo paired ovarian cancer ascites obtained before and after chemotherapy and in vitro therapy-induced secretomes, we show that molecules secreted by ovarian cancer cells upon therapy promote cisplatin resistance and enhance DNA damage repair in recipient cancer cells. Even a short-term incubation of chemonaive ovarian cancer cells with therapy-induced secretomes induces changes resembling those that are observed in chemoresistant patient-derived tumor cells after long-term therapy. Using integrative omics techniques, we find that both ex vivo and in vitro therapy-induced secretomes are enriched with spliceosomal components, which relocalize from the nucleus to the cytoplasm and subsequently into the extracellular vesicles upon treatment. We demonstrate that these molecules substantially contribute to the phenotypic effects of therapy-induced secretomes. Thus, SNU13 and SYNCRIP spliceosomal proteins promote therapy resistance, while the exogenous U12 and U6atac snRNAs stimulate tumor growth. These findings demonstrate the significance of spliceosomal network perturbation during therapy and further highlight that extracellular signaling might be a key factor contributing to the emergence of ovarian cancer therapy resistance.

Suggested Citation

  • Victoria O. Shender & Ksenia S. Anufrieva & Polina V. Shnaider & Georgij P. Arapidi & Marat S. Pavlyukov & Olga M. Ivanova & Irina K. Malyants & Grigory A. Stepanov & Evgenii Zhuravlev & Rustam H. Zig, 2024. "Therapy-induced secretion of spliceosomal components mediates pro-survival crosstalk between ovarian cancer cells," Nature Communications, Nature, vol. 15(1), pages 1-26, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49512-6
    DOI: 10.1038/s41467-024-49512-6
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