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Tumor Biology and Immunology

Stathmin Is Required for Normal Mouse Mammary Gland Development and Δ16HER2-Driven Tumorigenesis

Ilenia Segatto, Mara De Marco Zompit, Francesca Citron, Sara D'Andrea, Gian Luca Rampioni Vinciguerra, Tiziana Perin, Stefania Berton, Giorgia Mungo, Monica Schiappacassi, Cristina Marchini, Augusto Amici, Andrea Vecchione, Gustavo Baldassarre and Barbara Belletti
Ilenia Segatto
Unit of Molecular Oncology, Centro di Riferimento Oncologico di Aviano (CRO), IRCCS, National Cancer Institute, Aviano, Italy.
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Mara De Marco Zompit
Unit of Molecular Oncology, Centro di Riferimento Oncologico di Aviano (CRO), IRCCS, National Cancer Institute, Aviano, Italy.
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Francesca Citron
Unit of Molecular Oncology, Centro di Riferimento Oncologico di Aviano (CRO), IRCCS, National Cancer Institute, Aviano, Italy.
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Sara D'Andrea
Unit of Molecular Oncology, Centro di Riferimento Oncologico di Aviano (CRO), IRCCS, National Cancer Institute, Aviano, Italy.
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Gian Luca Rampioni Vinciguerra
Unit of Molecular Oncology, Centro di Riferimento Oncologico di Aviano (CRO), IRCCS, National Cancer Institute, Aviano, Italy.Faculty of Medicine and Psychology, Department of Clinical and Molecular Medicine, University of Rome "Sapienza" Sant'Andrea Hospital, Rome, Italy.
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Tiziana Perin
Unit of Pathology, Centro di Riferimento Oncologico di Aviano (CRO), IRCCS, National Cancer Institute, Aviano, Italy.
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Stefania Berton
Unit of Molecular Oncology, Centro di Riferimento Oncologico di Aviano (CRO), IRCCS, National Cancer Institute, Aviano, Italy.
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Giorgia Mungo
Unit of Molecular Oncology, Centro di Riferimento Oncologico di Aviano (CRO), IRCCS, National Cancer Institute, Aviano, Italy.
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Monica Schiappacassi
Unit of Molecular Oncology, Centro di Riferimento Oncologico di Aviano (CRO), IRCCS, National Cancer Institute, Aviano, Italy.
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  • ORCID record for Monica Schiappacassi
Cristina Marchini
Department of Biosciences and Veterinary Medicine, University of Camerino, Camerino, Italy.
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Augusto Amici
Department of Biosciences and Veterinary Medicine, University of Camerino, Camerino, Italy.
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Andrea Vecchione
Faculty of Medicine and Psychology, Department of Clinical and Molecular Medicine, University of Rome "Sapienza" Sant'Andrea Hospital, Rome, Italy.
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Gustavo Baldassarre
Unit of Molecular Oncology, Centro di Riferimento Oncologico di Aviano (CRO), IRCCS, National Cancer Institute, Aviano, Italy.
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  • For correspondence: gbaldassarre@cro.itbbelletti@cro.it
Barbara Belletti
Unit of Molecular Oncology, Centro di Riferimento Oncologico di Aviano (CRO), IRCCS, National Cancer Institute, Aviano, Italy.
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  • For correspondence: gbaldassarre@cro.itbbelletti@cro.it
DOI: 10.1158/0008-5472.CAN-18-2488 Published January 2019
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Abstract

Postnatal development of the mammary gland relies on the maintenance of oriented cell division and apicobasal polarity, both of which are often deregulated in cancer. The microtubule (MT) network contributes to control these processes; however, very little is known about the impact of altered MT dynamics in the development of a complex organ and on the role played by MT-interacting proteins such as stathmin. In this study, we report that female stathmin knock-out (STM KO) mice are unable to nurse their litters due to frank impairment of mammary gland development. In mouse mammary epithelial cells, loss of stathmin compromised the trafficking of polarized proteins and the achievement of proper apicobasal polarity. In particular, prolactin receptor internalization and localization was altered in STM KO mammary epithelial cells, leading to decreased protein stability and downmodulation of the Prl/PrlR/STAT5 signaling pathway. Absence of stathmin induced alterations in mitotic spindle orientation, accumulation of mitotic defects, and apoptosis, overall contributing to tissue disorganization and further decreasing the expansion of the mammary epithelial compartment. Loss of stathmin in MMTV-Δ16HER2 transgenic mice decreased the incidence and increased the latency of these very aggressive mammary carcinomas. Collectively, these data identify the essential mammary protein stathmin as protumorigenic and suggest it may serve as a potential therapeutic target in breast cancer.

Significance: Stathmin expression is critical to maintain oriented cell division and apicobasal polarity in normal mammary glands and to establish a protumorigenic program that eventually sustains HER2-positive breast cancer formation in mice.

Footnotes

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

  • Received August 9, 2018.
  • Revision received October 17, 2018.
  • Accepted November 19, 2018.
  • Published first November 26, 2018.
  • ©2018 American Association for Cancer Research.
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Cancer Research: 79 (2)
January 2019
Volume 79, Issue 2
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Stathmin Is Required for Normal Mouse Mammary Gland Development and Δ16HER2-Driven Tumorigenesis
Ilenia Segatto, Mara De Marco Zompit, Francesca Citron, Sara D'Andrea, Gian Luca Rampioni Vinciguerra, Tiziana Perin, Stefania Berton, Giorgia Mungo, Monica Schiappacassi, Cristina Marchini, Augusto Amici, Andrea Vecchione, Gustavo Baldassarre and Barbara Belletti
Cancer Res January 15 2019 (79) (2) 397-409; DOI: 10.1158/0008-5472.CAN-18-2488

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Stathmin Is Required for Normal Mouse Mammary Gland Development and Δ16HER2-Driven Tumorigenesis
Ilenia Segatto, Mara De Marco Zompit, Francesca Citron, Sara D'Andrea, Gian Luca Rampioni Vinciguerra, Tiziana Perin, Stefania Berton, Giorgia Mungo, Monica Schiappacassi, Cristina Marchini, Augusto Amici, Andrea Vecchione, Gustavo Baldassarre and Barbara Belletti
Cancer Res January 15 2019 (79) (2) 397-409; DOI: 10.1158/0008-5472.CAN-18-2488
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Cancer Research Online ISSN: 1538-7445
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