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Research Articles

p38MAPK Plays a Crucial Role in Stromal-Mediated Tumorigenesis

Elise Alspach, Kevin C. Flanagan, Xianmin Luo, Megan K. Ruhland, Hui Huang, Ermira Pazolli, Maureen J. Donlin, Timothy Marsh, David Piwnica-Worms, Joseph Monahan, Deborah V. Novack, Sandra S. McAllister and Sheila A. Stewart
Elise Alspach
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
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Kevin C. Flanagan
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
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Xianmin Luo
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
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Megan K. Ruhland
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
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Hui Huang
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
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Ermira Pazolli
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
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Maureen J. Donlin
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
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Timothy Marsh
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
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David Piwnica-Worms
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
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Joseph Monahan
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
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Deborah V. Novack
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
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Sandra S. McAllister
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
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Sheila A. Stewart
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
Departments of 1Cell Biology and Physiology, 2Medicine, and 3Pathology and Immunology; 4BRIGHT Institute, Washington University School of Medicine; Departments of 5Biochemistry & Molecular Biology and 6Molecular Microbiology & Immunology, Saint Louis University School of Medicine; 7Confluence Life Sciences, Inc., St. Louis, Missouri; 8Hematology Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston; 9Harvard Stem Cell Institute and Broad Institute of Harvard and MIT, Cambridge, Massachusetts; and 10Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, Texas
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DOI: 10.1158/2159-8290.CD-13-0743 Published June 2014
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Abstract

Neoplastic cells rely on the tumor microenvironment (TME) for survival and progression factors. Indeed, senescent and cancer-associated fibroblasts (CAF) express factors that promote tumorigenesis that are collectively referred to as the senescence-associated secretory phenotype (SASP). Despite their importance in tumorigenesis, the mechanisms that control TME-derived factor expression remain poorly understood. Here, we address a key unanswered question: how the SASP is sustained in senescent fibroblasts and CAFs. We find that the mitogen-activated protein kinase p38 (p38MAPK) controls AUF1 occupancy on SASP mRNAs and thus controls their stability. The importance of this regulatory mechanism is underscored by our findings that stromal-specific p38MAPK inhibition abrogates the tumor-promoting activities of CAFs and senescent fibroblasts. Our data suggest that targeting SASP mRNA stability through inhibition of p38MAPK will significantly aid the development of clinical strategies to target the TME.

Significance: The TME plays a key role in tumorigenesis. We demonstrate that p38MAPK governs a posttranscriptional mechanism that sustains the protumorigenic SASP. Inhibition of p38MAPK abrogates the tumor-promoting activities of CAFs and senescent fibroblasts. Thus, p38MAPK is a TME-specific Achilles' heel that may be exploited as a new therapeutic target. Cancer Discov; 4(6); 716–29. ©2014 AACR.

See related commentary by Isacke and Barcellos-Hoff, p. 637

This article is highlighted in the In This Issue feature, p. 621

Footnotes

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

  • Received October 10, 2013.
  • Revision received March 19, 2014.
  • Accepted March 20, 2014.
  • ©2014 American Association for Cancer Research.
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June 2014
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p38MAPK Plays a Crucial Role in Stromal-Mediated Tumorigenesis
Elise Alspach, Kevin C. Flanagan, Xianmin Luo, Megan K. Ruhland, Hui Huang, Ermira Pazolli, Maureen J. Donlin, Timothy Marsh, David Piwnica-Worms, Joseph Monahan, Deborah V. Novack, Sandra S. McAllister and Sheila A. Stewart
Cancer Discov June 1 2014 (4) (6) 716-729; DOI: 10.1158/2159-8290.CD-13-0743

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p38MAPK Plays a Crucial Role in Stromal-Mediated Tumorigenesis
Elise Alspach, Kevin C. Flanagan, Xianmin Luo, Megan K. Ruhland, Hui Huang, Ermira Pazolli, Maureen J. Donlin, Timothy Marsh, David Piwnica-Worms, Joseph Monahan, Deborah V. Novack, Sandra S. McAllister and Sheila A. Stewart
Cancer Discov June 1 2014 (4) (6) 716-729; DOI: 10.1158/2159-8290.CD-13-0743
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