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Molecular Cancer Research
Molecular Cancer Research
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Signal Transduction and Functional Imaging

SPANX Control of Lamin A/C Modulates Nuclear Architecture and Promotes Melanoma Growth

Ikrame Lazar, Bertrand Fabre, Yongmei Feng, Ali Khateb, Patrick Turko, Julia M. Martinez Gomez, Dennie T. Frederick, Mitchell P. Levesque, Lea Feld, Gao Zhang, Tongwu Zhang, Brian James, Jeny Shklover, Emily Avitan-Hersh, Ido Livneh, Marzia Scortegagna, Kevin Brown, Ola Larsson, Ivan Topisirovic, Haguy Wolfenson, Meenhard Herlyn, Keith Flaherty, Reinhard Dummer and Ze'ev A. Ronai
Ikrame Lazar
1Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.
2Technion Integrated Cancer Center, Faculty of Medicine, Technion Institute of Technology, Haifa, Israel.
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Bertrand Fabre
1Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.
2Technion Integrated Cancer Center, Faculty of Medicine, Technion Institute of Technology, Haifa, Israel.
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Yongmei Feng
1Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.
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Ali Khateb
1Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.
2Technion Integrated Cancer Center, Faculty of Medicine, Technion Institute of Technology, Haifa, Israel.
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Patrick Turko
3Department of Dermatology, University Hospital of Zurich, Zurich, Switzerland.
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Julia M. Martinez Gomez
3Department of Dermatology, University Hospital of Zurich, Zurich, Switzerland.
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Dennie T. Frederick
4Massachusetts General Hospital Cancer Center, Boston, Massachusetts.
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Mitchell P. Levesque
3Department of Dermatology, University Hospital of Zurich, Zurich, Switzerland.
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Lea Feld
2Technion Integrated Cancer Center, Faculty of Medicine, Technion Institute of Technology, Haifa, Israel.
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Gao Zhang
5The Wistar Institute, Philadelphia, Pennsylvania.
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Tongwu Zhang
6Laboratory of Translational Genomics, Division of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.
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Brian James
1Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.
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Jeny Shklover
2Technion Integrated Cancer Center, Faculty of Medicine, Technion Institute of Technology, Haifa, Israel.
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Emily Avitan-Hersh
2Technion Integrated Cancer Center, Faculty of Medicine, Technion Institute of Technology, Haifa, Israel.
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  • ORCID record for Emily Avitan-Hersh
Ido Livneh
2Technion Integrated Cancer Center, Faculty of Medicine, Technion Institute of Technology, Haifa, Israel.
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Marzia Scortegagna
1Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.
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Kevin Brown
6Laboratory of Translational Genomics, Division of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.
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Ola Larsson
7Department of Oncology-Pathology, Science for Life Laboratory, Karolinska Institutet, Stockholm, Sweden.
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Ivan Topisirovic
8Lady Davis Institute, Sir Mortimer B. Davis Jewish General Hospital, Gerald Bronfman Department of Oncology, Departments of Experimental Medicine and Biochemistry, McGill University, Montreal, Quebec, Canada.
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Haguy Wolfenson
2Technion Integrated Cancer Center, Faculty of Medicine, Technion Institute of Technology, Haifa, Israel.
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Meenhard Herlyn
5The Wistar Institute, Philadelphia, Pennsylvania.
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Keith Flaherty
4Massachusetts General Hospital Cancer Center, Boston, Massachusetts.
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Reinhard Dummer
3Department of Dermatology, University Hospital of Zurich, Zurich, Switzerland.
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Ze'ev A. Ronai
1Sanford Burnham Prebys Medical Discovery Institute, La Jolla, California.
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  • For correspondence: ronai@sbpdiscovery.org
DOI: 10.1158/1541-7786.MCR-20-0291 Published October 2020
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Abstract

Mechanisms regulating nuclear organization control fundamental cellular processes, including the cell and chromatin organization. Their disorganization, including aberrant nuclear architecture, has been often implicated in cellular transformation. Here, we identify Lamin A, among proteins essential for nuclear architecture, as SPANX (sperm protein associated with the nucleus on the X chromosome), a cancer testis antigen previously linked to invasive tumor phenotypes, interacting protein in melanoma. SPANX interaction with Lamin A was mapped to the immunoglobulin fold-like domain, a region critical for Lamin A function, which is often mutated in laminopathies. SPANX downregulation in melanoma cell lines perturbed nuclear organization, decreased cell viability, and promoted senescence-associated phenotypes. Moreover, SPANX knockdown (KD) in melanoma cells promoted proliferation arrest, a phenotype mediated in part by IRF3/IL1A signaling. SPANX KD in melanoma cells also prompted the secretion of IL1A, which attenuated the proliferation of naïve melanoma cells. Identification of SPANX as a nuclear architecture complex component provides an unexpected insight into the regulation of Lamin A and its importance in melanoma.

Implications: SPANX, a testis protein, interacts with LMNA and controls nuclear architecture and melanoma growth.

This article is featured in Highlights of This Issue, p. 1441

Footnotes

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

  • Mol Cancer Res 2020;18:1560–73

  • Received March 30, 2020.
  • Revision received May 19, 2020.
  • Accepted June 15, 2020.
  • Published first June 22, 2020.
  • ©2020 American Association for Cancer Research.
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Molecular Cancer Research: 18 (10)
October 2020
Volume 18, Issue 10
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SPANX Control of Lamin A/C Modulates Nuclear Architecture and Promotes Melanoma Growth
Ikrame Lazar, Bertrand Fabre, Yongmei Feng, Ali Khateb, Patrick Turko, Julia M. Martinez Gomez, Dennie T. Frederick, Mitchell P. Levesque, Lea Feld, Gao Zhang, Tongwu Zhang, Brian James, Jeny Shklover, Emily Avitan-Hersh, Ido Livneh, Marzia Scortegagna, Kevin Brown, Ola Larsson, Ivan Topisirovic, Haguy Wolfenson, Meenhard Herlyn, Keith Flaherty, Reinhard Dummer and Ze'ev A. Ronai
Mol Cancer Res October 1 2020 (18) (10) 1560-1573; DOI: 10.1158/1541-7786.MCR-20-0291

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SPANX Control of Lamin A/C Modulates Nuclear Architecture and Promotes Melanoma Growth
Ikrame Lazar, Bertrand Fabre, Yongmei Feng, Ali Khateb, Patrick Turko, Julia M. Martinez Gomez, Dennie T. Frederick, Mitchell P. Levesque, Lea Feld, Gao Zhang, Tongwu Zhang, Brian James, Jeny Shklover, Emily Avitan-Hersh, Ido Livneh, Marzia Scortegagna, Kevin Brown, Ola Larsson, Ivan Topisirovic, Haguy Wolfenson, Meenhard Herlyn, Keith Flaherty, Reinhard Dummer and Ze'ev A. Ronai
Mol Cancer Res October 1 2020 (18) (10) 1560-1573; DOI: 10.1158/1541-7786.MCR-20-0291
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