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Cell Fate Decisions

Destruction of a Microtubule-Bound MYC Reservoir during Mitosis Contributes to Vincristine's Anticancer Activity

Sabrina Becker, Christina Kiecke, Eva Schäfer, Ursula Sinzig, Lena Deuper, Pablo Trigo-Mourino, Christian Griesinger, Raphael Koch, Zuzanna Rydzynska, Bjoern Chapuy, Frederike von Bonin, Dieter Kube, Vivek Venkataramani, Hanibal Bohnenberger, Andreas Leha, Johanna Flach, Sascha Dierks, Holger Bastians, Brigitte Maruschak, Kamil Bojarczuk, Mateus de Oliveira Taveira, Lorenz Trümper, Gerburg M. Wulf and Gerald G. Wulf
Sabrina Becker
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Christina Kiecke
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Eva Schäfer
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Ursula Sinzig
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Lena Deuper
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Pablo Trigo-Mourino
2Max-Planck Institute for Biophysical Chemistry, Goettingen, Germany.
3Analytical Research and Development, Merck & Co., Inc., Kenilworth, New Jersey.
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Christian Griesinger
2Max-Planck Institute for Biophysical Chemistry, Goettingen, Germany.
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Raphael Koch
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Zuzanna Rydzynska
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Bjoern Chapuy
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Frederike von Bonin
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Dieter Kube
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Vivek Venkataramani
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Hanibal Bohnenberger
4Institute of Pathology, University Medicine Goettingen, Goettingen, Germany.
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Andreas Leha
5Department of Medical Statistics, University Medicine Goettingen, Goettingen, Germany.
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Johanna Flach
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Sascha Dierks
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Holger Bastians
6Department of Experimental Oncology, University Medicine Goettingen, Goettingen, Germany.
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Brigitte Maruschak
7Institute for Neuropathology, University Medicine Goettingen, Goettingen, Germany.
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Kamil Bojarczuk
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
8Department of Experimental Hematology, Institute of Hematology and Transfusion Medicine, Warsaw, Poland.
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Mateus de Oliveira Taveira
9Department of Medicine, BIDMC/Harvard Medical School, Boston, Massachusetts.
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Lorenz Trümper
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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Gerburg M. Wulf
9Department of Medicine, BIDMC/Harvard Medical School, Boston, Massachusetts.
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Gerald G. Wulf
1Department of Hematology and Medical Oncology, University Medicine Goettingen, Goettingen, Germany.
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  • For correspondence: gerald.wulf@med.uni-goettingen.de
DOI: 10.1158/1541-7786.MCR-19-1203 Published June 2020
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Abstract

Tightly regulated activity of the transcription factor MYC is essential for orderly cell proliferation. Upon deregulation, MYC elicits and promotes cancer progression. Proteasomal degradation is an essential element of MYC regulation, initiated by phosphorylation at Serine62 (Ser62) of the MB1 region. Here, we found that Ser62 phosphorylation peaks in mitosis, but that a fraction of nonphosphorylated MYC binds to the microtubules of the mitotic spindle. Consequently, the microtubule-destabilizing drug vincristine decreases wild-type MYC stability, whereas phosphorylation-deficient MYC is more stable, contributing to vincristine resistance and induction of polyploidy. PI3K inhibition attenuates postmitotic MYC formation and augments the cytotoxic effect of vincristine.

Implications: The spindle's function as a docking site for MYC during mitosis may constitute a window of specific vulnerability to be exploited for cancer treatment.

Footnotes

  • Note: Supplementary data for this article are available at Molecular Cancer Research Online (http://mcr.aacrjournals.org/).

  • Mol Cancer Res 2020;18:859–72

  • Received December 14, 2019.
  • Revision received February 11, 2020.
  • Accepted March 9, 2020.
  • Published first March 11, 2020.
  • ©2020 American Association for Cancer Research.
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Molecular Cancer Research: 18 (6)
June 2020
Volume 18, Issue 6
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Destruction of a Microtubule-Bound MYC Reservoir during Mitosis Contributes to Vincristine's Anticancer Activity
Sabrina Becker, Christina Kiecke, Eva Schäfer, Ursula Sinzig, Lena Deuper, Pablo Trigo-Mourino, Christian Griesinger, Raphael Koch, Zuzanna Rydzynska, Bjoern Chapuy, Frederike von Bonin, Dieter Kube, Vivek Venkataramani, Hanibal Bohnenberger, Andreas Leha, Johanna Flach, Sascha Dierks, Holger Bastians, Brigitte Maruschak, Kamil Bojarczuk, Mateus de Oliveira Taveira, Lorenz Trümper, Gerburg M. Wulf and Gerald G. Wulf
Mol Cancer Res June 1 2020 (18) (6) 859-872; DOI: 10.1158/1541-7786.MCR-19-1203

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Destruction of a Microtubule-Bound MYC Reservoir during Mitosis Contributes to Vincristine's Anticancer Activity
Sabrina Becker, Christina Kiecke, Eva Schäfer, Ursula Sinzig, Lena Deuper, Pablo Trigo-Mourino, Christian Griesinger, Raphael Koch, Zuzanna Rydzynska, Bjoern Chapuy, Frederike von Bonin, Dieter Kube, Vivek Venkataramani, Hanibal Bohnenberger, Andreas Leha, Johanna Flach, Sascha Dierks, Holger Bastians, Brigitte Maruschak, Kamil Bojarczuk, Mateus de Oliveira Taveira, Lorenz Trümper, Gerburg M. Wulf and Gerald G. Wulf
Mol Cancer Res June 1 2020 (18) (6) 859-872; DOI: 10.1158/1541-7786.MCR-19-1203
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