Lamin B1 loss promotes lung cancer development and metastasis by epigenetic derepression of RET

被引:48
作者
Jia, Yanhan [1 ,2 ,3 ,4 ]
Vong, Joaquim Si-Long [1 ,2 ]
Asafova, Alina [1 ,2 ]
Garvalov, Boyan K. [5 ,6 ]
Caputo, Luca [1 ,2 ]
Cordero, Julio [1 ,2 ,3 ,4 ]
Singh, Anshu [1 ,2 ,3 ,4 ]
Boettger, Thomas [1 ,2 ]
Guenther, Stefan [1 ,2 ]
Fink, Ludger [7 ]
Acker, Till [6 ]
Barreto, Guillermo [1 ,2 ]
Seeger, Werner [1 ,2 ,8 ,9 ]
Braun, Thomas [1 ,2 ]
Savai, Rajkumar [1 ,2 ,8 ,9 ]
Dobreva, Gergana [1 ,2 ,3 ,4 ,10 ]
机构
[1] Max Planck Inst Heart & Lung Res, Bad Nauheim, Germany
[2] German Ctr Lung Res, Bad Nauheim, Germany
[3] Heidelberg Univ, Anat & Dev Biol, Ctr Biomed & Med Technol Mannhe CBTM, Med Fac Mannheim, Mannheim, Germany
[4] Heidelberg Univ, European Ctr Angiosci ECAS, Med Fac Mannheim, Mannheim, Germany
[5] Heidelberg Univ, European Ctr Angiosci ECAS, Med Fac Mannheim, Microvasc Biol & Pathobiol, Mannheim, Germany
[6] Justus Liebig Univ, Inst Neuropathol, Giessen, Germany
[7] UGP, Inst Pathol & Cytol, Wetzlar, Germany
[8] Justus Liebig Univ, Dept Internal Med, Giessen, Germany
[9] German Ctr Lung Res DZL, Giessen, Germany
[10] JW Goethe Univ Frankfurt, Med Fac, Frankfurt, Germany
关键词
EPITHELIAL-MESENCHYMAL TRANSITION; NUCLEAR-ENVELOPE; CELL IDENTITY; CHROMATIN; EXPRESSION; EZH2; GENE; INACTIVATION; ORGANIZATION; METHYLATION;
D O I
10.1084/jem.20181394
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
100102 ;
摘要
Although abnormal nuclear structure is an important criterion for cancer diagnostics, remarkably little is known about its relationship to tumor development. Here we report that loss of lamin B1, a determinant of nuclear architecture, plays a key role in lung cancer. We found that lamin B1 levels were reduced in lung cancer patients. Lamin B1 silencing in lung epithelial cells promoted epithelial-mesenchymal transition, cell migration, tumor growth, and metastasis. Mechanistically, we show that lamin B1 recruits the polycomb repressive complex 2 (PRC2) to alter the H3K27me3 landscape and repress genes involved in cell migration and signaling. In particular, epigenetic derepression of the RET proto-oncogene by loss of PRC2 recruitment, and activation of the RET/p38 signaling axis, play a crucial role in mediating the malignant phenotype upon lamin B1 disruption. Importantly, loss of a single lamin B1 allele induced spontaneous lung tumor formation and RET activation. Thus, lamin B1 acts as a tumor suppressor in lung cancer, linking aberrant nuclear structure and epigenetic patterning with malignancy.
引用
收藏
页码:1377 / 1395
页数:19
相关论文
共 80 条
  • [1] Inactivation of the Lamin A/C gene by CpG island promoter hypermethylation in hematologic malignancies, and its association with poor survival in nodal diffuse large B-cell lymphoma
    Agrelo, R
    Setien, F
    Espada, J
    Artiga, MJ
    Rodriguez, M
    Pérez-Rosado, AP
    Sanchez-Aguilera, A
    Fraga, MF
    Piris, MA
    Esteller, M
    [J]. JOURNAL OF CLINICAL ONCOLOGY, 2005, 23 (17) : 3940 - 3947
  • [2] Targeted mutation of serine 697 in the Ret tyrosine kinase causes migration defect of enteric neural crest cells
    Asai, Naoya
    Fukuda, Toshifumi
    Wu, Zaiqi
    Enomoto, Atsushi
    Pachnis, Vassilis
    Takahashi, Masahide
    Costantini, Frank
    [J]. DEVELOPMENT, 2006, 133 (22): : 4507 - 4516
  • [3] ASCL1 is a lineage oncogene providing therapeutic targets for high-grade neuroendocrine lung cancers
    Augustyn, Alexander
    Borromeo, Mark
    Wang, Tao
    Fujimoto, Junya
    Shao, Chunli
    Dospoy, Patrick D.
    Lee, Victoria
    Tan, Christopher
    Sullivan, James P.
    Larsen, Jill E.
    Girard, Luc
    Behrens, Carmen
    Wistuba, Ignacio I.
    Xie, Yang
    Cobb, Melanie H.
    Gazdar, Adi F.
    Johnson, Jane E.
    Minna, John D.
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2014, 111 (41) : 14788 - 14793
  • [4] Immune and Inflammatory Cell Composition of Human Lung Cancer Stroma
    Banat, G-Andre
    Tretyn, Aleksandra
    Pullamsetti, Soni Savai
    Wilhelm, Jochen
    Weigert, Andreas
    Olesch, Catherine
    Ebel, Katharina
    Stiewe, Thorsten
    Grimminger, Friedrich
    Seeger, Werner
    Fink, Ludger
    Savai, Rajkumar
    [J]. PLOS ONE, 2015, 10 (09):
  • [5] CONTROLLING THE FALSE DISCOVERY RATE - A PRACTICAL AND POWERFUL APPROACH TO MULTIPLE TESTING
    BENJAMINI, Y
    HOCHBERG, Y
    [J]. JOURNAL OF THE ROYAL STATISTICAL SOCIETY SERIES B-STATISTICAL METHODOLOGY, 1995, 57 (01) : 289 - 300
  • [6] ASCL1 and NEUROD1 Reveal Heterogeneity in Pulmonary Neuroendocrine Tumors and Regulate Distinct Genetic Programs
    Borromeo, Mark D.
    Savage, Trisha K.
    Kollipara, Rahul K.
    He, Min
    Augustyn, Alexander
    Osborne, Jihan K.
    Girard, Luc
    Minna, John D.
    Gazdar, Adi F.
    Cobb, Melanie H.
    Johnson, Jane E.
    [J]. CELL REPORTS, 2016, 16 (05): : 1259 - 1272
  • [7] Nuclear pore complexes in the maintenance of genome integrity
    Bukata, Lucas
    Parker, Stephanie L.
    D'Angelo, Maximiliano A.
    [J]. CURRENT OPINION IN CELL BIOLOGY, 2013, 25 (03) : 378 - 386
  • [8] The nuclear lamins: flexibility in function
    Burke, Brian
    Stewart, Colin L.
    [J]. NATURE REVIEWS MOLECULAR CELL BIOLOGY, 2013, 14 (01) : 13 - 24
  • [9] Regulation of Nucleotide Excision Repair by Nuclear Lamin B1
    Butin-Israeli, Veronika
    Adam, Stephen A.
    Goldman, Robert D.
    [J]. PLOS ONE, 2013, 8 (07):
  • [10] Nuclear lamin functions and disease
    Butin-Israeli, Veronika
    Adam, Stephen A.
    Goldman, Anne E.
    Goldman, Robert D.
    [J]. TRENDS IN GENETICS, 2012, 28 (09) : 464 - 471