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Octyl itaconate enhances VSVΔ51 oncolytic virotherapy by multitarget inhibition of antiviral and inflammatory pathways

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Octyl itaconate enhances VSVΔ51 oncolytic virotherapy by multitarget inhibition of antiviral and inflammatory pathways. / Kurmasheva, Naziia; Said, Aida; Wong, Boaz; Kinderman, Priscilla; Han, Xiaoying; Rahimic, Anna H F; Kress, Alena; Carter-Timofte, Madalina E; Holm, Emilia; van der Horst, Demi; Kollmann, Christoph F; Liu, Zhenlong; Wang, Chen; Hoang, Huy-Dung; Kovalenko, Elina; Chrysopoulou, Maria; Twayana, Krishna Sundar; Ottosen, Rasmus N; Svenningsen, Esben B; Begnini, Fabio; Kiib, Anders E; Kromm, Florian E H; Weiss, Hauke J; Di Carlo, Daniele; Muscolini, Michela; Higgins, Maureen; van der Heijden, Mirte; Bardoul, Angelina; Tong, Tong; Ozsvar, Attila; Hou, Wen-Hsien; Schack, Vivien R; Holm, Christian K; Zheng, Yunan; Ruzek, Melanie; Kalucka, Joanna; de la Vega, Laureano; Elgaher, Walid A M; Korshoej, Anders R; Lin, Rongtuan; Hiscott, John; Poulsen, Thomas B; O'Neill, Luke A; Roy, Dominic G; Rinschen, Markus M; van Montfoort, Nadine; Diallo, Jean-Simon; Farin, Henner F; Alain, Tommy; Olagnier, David.

In: NAT COMMUN, Vol. 15, No. 1, 15.05.2024, p. 4096.

Research output: SCORING: Contribution to journal › SCORING: Journal article › Research › peer-review

Harvard

Kurmasheva, N, Said, A, Wong, B, Kinderman, P, Han, X, Rahimic, AHF, Kress, A, Carter-Timofte, ME, Holm, E, van der Horst, D, Kollmann, CF, Liu, Z, Wang, C, Hoang, H-D, Kovalenko, E, Chrysopoulou, M, Twayana, KS, Ottosen, RN, Svenningsen, EB, Begnini, F, Kiib, AE, Kromm, FEH, Weiss, HJ, Di Carlo, D, Muscolini, M, Higgins, M, van der Heijden, M, Bardoul, A, Tong, T, Ozsvar, A, Hou, W-H, Schack, VR, Holm, CK, Zheng, Y, Ruzek, M, Kalucka, J, de la Vega, L, Elgaher, WAM, Korshoej, AR, Lin, R, Hiscott, J, Poulsen, TB, O'Neill, LA, Roy, DG, Rinschen, MM, van Montfoort, N, Diallo, J-S, Farin, HF, Alain, T & Olagnier, D 2024, 'Octyl itaconate enhances VSVΔ51 oncolytic virotherapy by multitarget inhibition of antiviral and inflammatory pathways', NAT COMMUN, vol. 15, no. 1, pp. 4096. https://doi.org/10.1038/s41467-024-48422-x

APA

Kurmasheva, N., Said, A., Wong, B., Kinderman, P., Han, X., Rahimic, A. H. F., Kress, A., Carter-Timofte, M. E., Holm, E., van der Horst, D., Kollmann, C. F., Liu, Z., Wang, C., Hoang, H-D., Kovalenko, E., Chrysopoulou, M., Twayana, K. S., Ottosen, R. N., Svenningsen, E. B., ... Olagnier, D. (2024). Octyl itaconate enhances VSVΔ51 oncolytic virotherapy by multitarget inhibition of antiviral and inflammatory pathways. NAT COMMUN, 15(1), 4096. https://doi.org/10.1038/s41467-024-48422-x

Vancouver

Kurmasheva N, Said A, Wong B, Kinderman P, Han X, Rahimic AHF et al. Octyl itaconate enhances VSVΔ51 oncolytic virotherapy by multitarget inhibition of antiviral and inflammatory pathways. NAT COMMUN. 2024 May 15;15(1):4096. https://doi.org/10.1038/s41467-024-48422-x

Bibtex

@article{22149f6d643e4cc88a0250ccb09b1eaa,
title = "Octyl itaconate enhances VSVΔ51 oncolytic virotherapy by multitarget inhibition of antiviral and inflammatory pathways",
abstract = "The presence of heterogeneity in responses to oncolytic virotherapy poses a barrier to clinical effectiveness, as resistance to this treatment can occur through the inhibition of viral spread within the tumor, potentially leading to treatment failures. Here we show that 4-octyl itaconate (4-OI), a chemical derivative of the Krebs cycle-derived metabolite itaconate, enhances oncolytic virotherapy with VSVΔ51 in various models including human and murine resistant cancer cell lines, three-dimensional (3D) patient-derived colon tumoroids and organotypic brain tumor slices. Furthermore, 4-OI in combination with VSVΔ51 improves therapeutic outcomes in a resistant murine colon tumor model. Mechanistically, we find that 4-OI suppresses antiviral immunity in cancer cells through the modification of cysteine residues in MAVS and IKKβ independently of the NRF2/KEAP1 axis. We propose that the combination of a metabolite-derived drug with an oncolytic virus agent can greatly improve anticancer therapeutic outcomes by direct interference with the type I IFN and NF-κB-mediated antiviral responses.",
keywords = "Animals, Humans, Oncolytic Virotherapy/methods, Succinates/pharmacology, Mice, Cell Line, Tumor, Oncolytic Viruses, Interferon Type I/metabolism, NF-E2-Related Factor 2/metabolism, Colonic Neoplasms/therapy, Antiviral Agents/pharmacology, NF-kappa B/metabolism, I-kappa B Kinase/metabolism, Kelch-Like ECH-Associated Protein 1/metabolism, Inflammation/drug therapy, Female, Vesicular stomatitis Indiana virus/physiology, Signal Transduction/drug effects",
author = "Naziia Kurmasheva and Aida Said and Boaz Wong and Priscilla Kinderman and Xiaoying Han and Rahimic, {Anna H F} and Alena Kress and Carter-Timofte, {Madalina E} and Emilia Holm and {van der Horst}, Demi and Kollmann, {Christoph F} and Zhenlong Liu and Chen Wang and Huy-Dung Hoang and Elina Kovalenko and Maria Chrysopoulou and Twayana, {Krishna Sundar} and Ottosen, {Rasmus N} and Svenningsen, {Esben B} and Fabio Begnini and Kiib, {Anders E} and Kromm, {Florian E H} and Weiss, {Hauke J} and {Di Carlo}, Daniele and Michela Muscolini and Maureen Higgins and {van der Heijden}, Mirte and Angelina Bardoul and Tong Tong and Attila Ozsvar and Wen-Hsien Hou and Schack, {Vivien R} and Holm, {Christian K} and Yunan Zheng and Melanie Ruzek and Joanna Kalucka and {de la Vega}, Laureano and Elgaher, {Walid A M} and Korshoej, {Anders R} and Rongtuan Lin and John Hiscott and Poulsen, {Thomas B} and O'Neill, {Luke A} and Roy, {Dominic G} and Rinschen, {Markus M} and {van Montfoort}, Nadine and Jean-Simon Diallo and Farin, {Henner F} and Tommy Alain and David Olagnier",
note = "{\textcopyright} 2024. The Author(s).",
year = "2024",
month = may,
day = "15",
doi = "10.1038/s41467-024-48422-x",
language = "English",
volume = "15",
pages = "4096",
journal = "NAT COMMUN",
issn = "2041-1723",
publisher = "NATURE PUBLISHING GROUP",
number = "1",

}

RIS

TY - JOUR

T1 - Octyl itaconate enhances VSVΔ51 oncolytic virotherapy by multitarget inhibition of antiviral and inflammatory pathways

AU - Kurmasheva, Naziia

AU - Said, Aida

AU - Wong, Boaz

AU - Kinderman, Priscilla

AU - Han, Xiaoying

AU - Rahimic, Anna H F

AU - Kress, Alena

AU - Carter-Timofte, Madalina E

AU - Holm, Emilia

AU - van der Horst, Demi

AU - Kollmann, Christoph F

AU - Liu, Zhenlong

AU - Wang, Chen

AU - Hoang, Huy-Dung

AU - Kovalenko, Elina

AU - Chrysopoulou, Maria

AU - Twayana, Krishna Sundar

AU - Ottosen, Rasmus N

AU - Svenningsen, Esben B

AU - Begnini, Fabio

AU - Kiib, Anders E

AU - Kromm, Florian E H

AU - Weiss, Hauke J

AU - Di Carlo, Daniele

AU - Muscolini, Michela

AU - Higgins, Maureen

AU - van der Heijden, Mirte

AU - Bardoul, Angelina

AU - Tong, Tong

AU - Ozsvar, Attila

AU - Hou, Wen-Hsien

AU - Schack, Vivien R

AU - Holm, Christian K

AU - Zheng, Yunan

AU - Ruzek, Melanie

AU - Kalucka, Joanna

AU - de la Vega, Laureano

AU - Elgaher, Walid A M

AU - Korshoej, Anders R

AU - Lin, Rongtuan

AU - Hiscott, John

AU - Poulsen, Thomas B

AU - O'Neill, Luke A

AU - Roy, Dominic G

AU - Rinschen, Markus M

AU - van Montfoort, Nadine

AU - Diallo, Jean-Simon

AU - Farin, Henner F

AU - Alain, Tommy

AU - Olagnier, David

N1 - © 2024. The Author(s).

PY - 2024/5/15

Y1 - 2024/5/15

N2 - The presence of heterogeneity in responses to oncolytic virotherapy poses a barrier to clinical effectiveness, as resistance to this treatment can occur through the inhibition of viral spread within the tumor, potentially leading to treatment failures. Here we show that 4-octyl itaconate (4-OI), a chemical derivative of the Krebs cycle-derived metabolite itaconate, enhances oncolytic virotherapy with VSVΔ51 in various models including human and murine resistant cancer cell lines, three-dimensional (3D) patient-derived colon tumoroids and organotypic brain tumor slices. Furthermore, 4-OI in combination with VSVΔ51 improves therapeutic outcomes in a resistant murine colon tumor model. Mechanistically, we find that 4-OI suppresses antiviral immunity in cancer cells through the modification of cysteine residues in MAVS and IKKβ independently of the NRF2/KEAP1 axis. We propose that the combination of a metabolite-derived drug with an oncolytic virus agent can greatly improve anticancer therapeutic outcomes by direct interference with the type I IFN and NF-κB-mediated antiviral responses.

AB - The presence of heterogeneity in responses to oncolytic virotherapy poses a barrier to clinical effectiveness, as resistance to this treatment can occur through the inhibition of viral spread within the tumor, potentially leading to treatment failures. Here we show that 4-octyl itaconate (4-OI), a chemical derivative of the Krebs cycle-derived metabolite itaconate, enhances oncolytic virotherapy with VSVΔ51 in various models including human and murine resistant cancer cell lines, three-dimensional (3D) patient-derived colon tumoroids and organotypic brain tumor slices. Furthermore, 4-OI in combination with VSVΔ51 improves therapeutic outcomes in a resistant murine colon tumor model. Mechanistically, we find that 4-OI suppresses antiviral immunity in cancer cells through the modification of cysteine residues in MAVS and IKKβ independently of the NRF2/KEAP1 axis. We propose that the combination of a metabolite-derived drug with an oncolytic virus agent can greatly improve anticancer therapeutic outcomes by direct interference with the type I IFN and NF-κB-mediated antiviral responses.

KW - Animals

KW - Humans

KW - Oncolytic Virotherapy/methods

KW - Succinates/pharmacology

KW - Mice

KW - Cell Line, Tumor

KW - Oncolytic Viruses

KW - Interferon Type I/metabolism

KW - NF-E2-Related Factor 2/metabolism

KW - Colonic Neoplasms/therapy

KW - Antiviral Agents/pharmacology

KW - NF-kappa B/metabolism

KW - I-kappa B Kinase/metabolism

KW - Kelch-Like ECH-Associated Protein 1/metabolism

KW - Inflammation/drug therapy

KW - Female

KW - Vesicular stomatitis Indiana virus/physiology

KW - Signal Transduction/drug effects

U2 - 10.1038/s41467-024-48422-x

DO - 10.1038/s41467-024-48422-x

M3 - SCORING: Journal article

C2 - 38750019

VL - 15

SP - 4096

JO - NAT COMMUN

JF - NAT COMMUN

SN - 2041-1723

IS - 1

ER -