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Memory of stochastic single-cell apoptotic signaling promotes chemoresistance in neuroblastoma

Jordan F. Hastings, Sharissa L. Latham, Alvin Kamili, Madeleine S. Wheatley, Jeremy Z. R. Han, Marie Wong-Erasmus, Monica Phimmachanh, Max Nobis, Chiara Pantarelli, Antonia L. Cadell, et al.
(2023) SCIENCE ADVANCES. 9(9).
Author
Organization
Abstract
Gene expression noise is known to promote stochastic drug resistance through the elevated expression of individual genes in rare cancer cells. However, we now demonstrate that chemoresistant neuroblastoma cells emerge at a much higher frequency when the influence of noise is integrated across multiple components of an apoptotic signaling network. Using a JNK activity biosensor with longitudinal high-content and in vivo intravital imaging, we identify a population of stochastic, JNK-impaired, chemoresistant cells that exist because of noise within this signaling network. Furthermore, we reveal that the memory of this initially random state is retained following chemotherapy treatment across a series of in vitro, in vivo, and patient models. Using matched PDX models established at diagnosis and relapse from individual patients, we show that HDAC inhibitor priming cannot erase the memory of this resistant state within relapsed neuroblastomas but improves response in the first-line setting by restoring drug-induced JNK activity within the chemoresistant population of treatment-naive tumors.
Keywords
Multidisciplinary

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MLA
Hastings, Jordan F., et al. “Memory of Stochastic Single-Cell Apoptotic Signaling Promotes Chemoresistance in Neuroblastoma.” SCIENCE ADVANCES, vol. 9, no. 9, American Association for the Advancement of Science (AAAS), 2023, doi:10.1126/sciadv.abp8314.
APA
Hastings, J. F., Latham, S. L., Kamili, A., Wheatley, M. S., Han, J. Z. R., Wong-Erasmus, M., … Croucher, D. R. (2023). Memory of stochastic single-cell apoptotic signaling promotes chemoresistance in neuroblastoma. SCIENCE ADVANCES, 9(9). https://doi.org/10.1126/sciadv.abp8314
Chicago author-date
Hastings, Jordan F., Sharissa L. Latham, Alvin Kamili, Madeleine S. Wheatley, Jeremy Z. R. Han, Marie Wong-Erasmus, Monica Phimmachanh, et al. 2023. “Memory of Stochastic Single-Cell Apoptotic Signaling Promotes Chemoresistance in Neuroblastoma.” SCIENCE ADVANCES 9 (9). https://doi.org/10.1126/sciadv.abp8314.
Chicago author-date (all authors)
Hastings, Jordan F., Sharissa L. Latham, Alvin Kamili, Madeleine S. Wheatley, Jeremy Z. R. Han, Marie Wong-Erasmus, Monica Phimmachanh, Max Nobis, Chiara Pantarelli, Antonia L. Cadell, Yolande E. I. O’Donnell, King Ho Leong, Sophie Lynn, Fan-Suo Geng, Lujing Cui, Sabrina Yan, Joanna Achinger-Kawecka, Clare Stirzaker, Murray D. Norris, Michelle Haber, Toby N. Trahair, Franki Speleman, Katleen De Preter, Mark J. Cowley, Ozren Bogdanovic, Paul Timpson, Thomas R. Cox, Walter Kolch, Jamie I. Fletcher, Dirk Fey, and David R. Croucher. 2023. “Memory of Stochastic Single-Cell Apoptotic Signaling Promotes Chemoresistance in Neuroblastoma.” SCIENCE ADVANCES 9 (9). doi:10.1126/sciadv.abp8314.
Vancouver
1.
Hastings JF, Latham SL, Kamili A, Wheatley MS, Han JZR, Wong-Erasmus M, et al. Memory of stochastic single-cell apoptotic signaling promotes chemoresistance in neuroblastoma. SCIENCE ADVANCES. 2023;9(9).
IEEE
[1]
J. F. Hastings et al., “Memory of stochastic single-cell apoptotic signaling promotes chemoresistance in neuroblastoma,” SCIENCE ADVANCES, vol. 9, no. 9, 2023.
@article{01GXAT42JHKVWE9KZSK33G74PK,
  abstract     = {{Gene expression noise is known to promote stochastic drug resistance through the elevated expression of individual genes in rare cancer cells. However, we now demonstrate that chemoresistant neuroblastoma cells emerge at a much higher frequency when the influence of noise is integrated across multiple components of an apoptotic signaling network. Using a JNK activity biosensor with longitudinal high-content and in vivo intravital imaging, we identify a population of stochastic, JNK-impaired, chemoresistant cells that exist because of noise within this signaling network. Furthermore, we reveal that the memory of this initially random state is retained following chemotherapy treatment across a series of in vitro, in vivo, and patient models. Using matched PDX models established at diagnosis and relapse from individual patients, we show that HDAC inhibitor priming cannot erase the memory of this resistant state within relapsed neuroblastomas but improves response in the first-line setting by restoring drug-induced JNK activity within the chemoresistant population of treatment-naive tumors.}},
  articleno    = {{eabp8314}},
  author       = {{Hastings, Jordan F. and Latham, Sharissa L. and Kamili, Alvin and Wheatley, Madeleine S. and Han, Jeremy Z. R. and Wong-Erasmus, Marie and Phimmachanh, Monica and Nobis, Max and Pantarelli, Chiara and Cadell, Antonia L. and O’Donnell, Yolande E. I. and Leong, King Ho and Lynn, Sophie and Geng, Fan-Suo and Cui, Lujing and Yan, Sabrina and Achinger-Kawecka, Joanna and Stirzaker, Clare and Norris, Murray D. and Haber, Michelle and Trahair, Toby N. and Speleman, Franki and De Preter, Katleen and Cowley, Mark J. and Bogdanovic, Ozren and Timpson, Paul and Cox, Thomas R. and Kolch, Walter and Fletcher, Jamie I. and Fey, Dirk and Croucher, David R.}},
  issn         = {{2375-2548}},
  journal      = {{SCIENCE ADVANCES}},
  keywords     = {{Multidisciplinary}},
  language     = {{eng}},
  number       = {{9}},
  pages        = {{23}},
  publisher    = {{American Association for the Advancement of Science (AAAS)}},
  title        = {{Memory of stochastic single-cell apoptotic signaling promotes chemoresistance in neuroblastoma}},
  url          = {{http://doi.org/10.1126/sciadv.abp8314}},
  volume       = {{9}},
  year         = {{2023}},
}
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