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Therapy-induced secretion of spliceosomal components mediates pro-survival crosstalk between ovarian cancer cells. / Shender, Victoria O; Anufrieva, Ksenia S; Shnaider, Polina V и др.

в: Nature Communications, Том 15, № 1, 5237, 19.06.2024.

Результаты исследований: Научные публикации в периодических изданиях › статья › Рецензирование

Harvard

Shender, VO, Anufrieva, KS, Shnaider, PV, Arapidi, GP, Pavlyukov, MS, Ivanova, OM, Malyants, IK, Stepanov, GA, Zhuravlev, E, Ziganshin, RH, Butenko, IO, Bukato, ON, Klimina, KM, Veselovsky, VA, Grigorieva, TV, Malanin, SY, Aleshikova, OI, Slonov, AV, Babaeva, NA, Ashrafyan, LA, Khomyakova, E, Evtushenko, EG, Lukina, MM, Wang, Z, Silantiev, AS, Nushtaeva, AA, Kharlampieva, DD, Lazarev, VN, Lashkin, AI, Arzumanyan, LK, Petrushanko, IY, Makarov, AA, Lebedeva, OS, Bogomazova, AN, Lagarkova, MA & Govorun, VM 2024, 'Therapy-induced secretion of spliceosomal components mediates pro-survival crosstalk between ovarian cancer cells', Nature Communications, Том. 15, № 1, 5237. https://doi.org/10.1038/s41467-024-49512-6

APA

Shender, V. O., Anufrieva, K. S., Shnaider, P. V., Arapidi, G. P., Pavlyukov, M. S., Ivanova, O. M., Malyants, I. K., Stepanov, G. A., Zhuravlev, E., Ziganshin, R. H., Butenko, I. O., Bukato, O. N., Klimina, K. M., Veselovsky, V. A., Grigorieva, T. V., Malanin, S. Y., Aleshikova, O. I., Slonov, A. V., Babaeva, N. A., ... Govorun, V. M. (2024). Therapy-induced secretion of spliceosomal components mediates pro-survival crosstalk between ovarian cancer cells. Nature Communications, 15(1), [5237]. https://doi.org/10.1038/s41467-024-49512-6

Vancouver

Shender VO, Anufrieva KS, Shnaider PV, Arapidi GP, Pavlyukov MS, Ivanova OM и др. Therapy-induced secretion of spliceosomal components mediates pro-survival crosstalk between ovarian cancer cells. Nature Communications. 2024 июнь 19;15(1):5237. doi: 10.1038/s41467-024-49512-6

Author

Shender, Victoria O ; Anufrieva, Ksenia S ; Shnaider, Polina V и др. / Therapy-induced secretion of spliceosomal components mediates pro-survival crosstalk between ovarian cancer cells. в: Nature Communications. 2024 ; Том 15, № 1.

BibTeX

@article{8c9bbc72bf5d426fab17da01513f5c5f,
title = "Therapy-induced secretion of spliceosomal components mediates pro-survival crosstalk between ovarian cancer cells",
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.",
keywords = "Female, Humans, Ovarian Neoplasms/metabolism, Spliceosomes/metabolism, Cisplatin/pharmacology, Cell Line, Tumor, Drug Resistance, Neoplasm, Animals, Mice, Extracellular Vesicles/metabolism, Cell Survival/drug effects, Antineoplastic Agents/pharmacology, RNA, Small Nuclear/metabolism, DNA Repair",
author = "Shender, {Victoria O} and Anufrieva, {Ksenia S} and Shnaider, {Polina V} and Arapidi, {Georgij P} and Pavlyukov, {Marat S} and Ivanova, {Olga M} and Malyants, {Irina K} and Stepanov, {Grigory A} and Evgenii Zhuravlev and Ziganshin, {Rustam H} and Butenko, {Ivan O} and Bukato, {Olga N} and Klimina, {Ksenia M} and Veselovsky, {Vladimir A} and Grigorieva, {Tatiana V} and Malanin, {Sergey Y} and Aleshikova, {Olga I} and Slonov, {Andrey V} and Babaeva, {Nataliya A} and Ashrafyan, {Lev A} and Elena Khomyakova and Evtushenko, {Evgeniy G} and Lukina, {Maria M} and Zixiang Wang and Silantiev, {Artemiy S} and Nushtaeva, {Anna A} and Kharlampieva, {Daria D} and Lazarev, {Vassili N} and Lashkin, {Arseniy I} and Arzumanyan, {Lorine K} and Petrushanko, {Irina Yu} and Makarov, {Alexander A} and Lebedeva, {Olga S} and Bogomazova, {Alexandra N} and Lagarkova, {Maria A} and Govorun, {Vadim M}",
note = "This work was supported by grant 075-15-2019-1669 from the Ministry of Science and Higher Education of the Russian Federation (V.O.S., P.V.S., G.P.A., O.M.I., M.A.L., V.N.L., K.S.A., K.M.K. for RNAseq analyses); by the Russian Science Foundation project nos. 22-15-00462 (V.O.S., G.P.A, P.V.S., M.M.L., O.M.I. for proteomic analysis and experiments with cell cultures), 22-14-00234 (M.S.P. for splicing analysis), and 22-75-10153 (G.A.S. for RNA synthesis); by the State funding project 12403120004-7 (G.P.A. for bioinformatics analysis). We thank Dr. Roman Trikin, Dr. Eugen N. Imyanitov, and Dr. Sergey V. Razin for the critical reading and editing of the manuscript. {\textcopyright} 2024. The Author(s).",
year = "2024",
month = jun,
day = "19",
doi = "10.1038/s41467-024-49512-6",
language = "English",
volume = "15",
journal = "Nature Communications",
issn = "2041-1723",
publisher = "Nature Publishing Group",
number = "1",

}

RIS

TY - JOUR

T1 - Therapy-induced secretion of spliceosomal components mediates pro-survival crosstalk between ovarian cancer cells

AU - Shender, Victoria O

AU - Anufrieva, Ksenia S

AU - Shnaider, Polina V

AU - Arapidi, Georgij P

AU - Pavlyukov, Marat S

AU - Ivanova, Olga M

AU - Malyants, Irina K

AU - Stepanov, Grigory A

AU - Zhuravlev, Evgenii

AU - Ziganshin, Rustam H

AU - Butenko, Ivan O

AU - Bukato, Olga N

AU - Klimina, Ksenia M

AU - Veselovsky, Vladimir A

AU - Grigorieva, Tatiana V

AU - Malanin, Sergey Y

AU - Aleshikova, Olga I

AU - Slonov, Andrey V

AU - Babaeva, Nataliya A

AU - Ashrafyan, Lev A

AU - Khomyakova, Elena

AU - Evtushenko, Evgeniy G

AU - Lukina, Maria M

AU - Wang, Zixiang

AU - Silantiev, Artemiy S

AU - Nushtaeva, Anna A

AU - Kharlampieva, Daria D

AU - Lazarev, Vassili N

AU - Lashkin, Arseniy I

AU - Arzumanyan, Lorine K

AU - Petrushanko, Irina Yu

AU - Makarov, Alexander A

AU - Lebedeva, Olga S

AU - Bogomazova, Alexandra N

AU - Lagarkova, Maria A

AU - Govorun, Vadim M

N1 - This work was supported by grant 075-15-2019-1669 from the Ministry of Science and Higher Education of the Russian Federation (V.O.S., P.V.S., G.P.A., O.M.I., M.A.L., V.N.L., K.S.A., K.M.K. for RNAseq analyses); by the Russian Science Foundation project nos. 22-15-00462 (V.O.S., G.P.A, P.V.S., M.M.L., O.M.I. for proteomic analysis and experiments with cell cultures), 22-14-00234 (M.S.P. for splicing analysis), and 22-75-10153 (G.A.S. for RNA synthesis); by the State funding project 12403120004-7 (G.P.A. for bioinformatics analysis). We thank Dr. Roman Trikin, Dr. Eugen N. Imyanitov, and Dr. Sergey V. Razin for the critical reading and editing of the manuscript. © 2024. The Author(s).

PY - 2024/6/19

Y1 - 2024/6/19

N2 - 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.

AB - 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.

KW - Female

KW - Humans

KW - Ovarian Neoplasms/metabolism

KW - Spliceosomes/metabolism

KW - Cisplatin/pharmacology

KW - Cell Line, Tumor

KW - Drug Resistance, Neoplasm

KW - Animals

KW - Mice

KW - Extracellular Vesicles/metabolism

KW - Cell Survival/drug effects

KW - Antineoplastic Agents/pharmacology

KW - RNA, Small Nuclear/metabolism

KW - DNA Repair

UR - https://www.scopus.com/record/display.uri?eid=2-s2.0-85196403437&origin=inward&txGid=2bc097ef43481f75f7742f38473daa05

U2 - 10.1038/s41467-024-49512-6

DO - 10.1038/s41467-024-49512-6

M3 - Article

C2 - 38898005

VL - 15

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 5237

ER -

ID: 60381874