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PMID: 25156255 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Tumour-infiltrating Gr-1+ myeloid cells antagonize senescence in cancer.

Nature ·Vol. 515 ·No. 7525 ·2014-11-06 ·Pages 134-7

Di Mitri D, Toso A, Chen JJ, Sarti M, Pinton S, Jost TR, D'Antuono R, Montani E, Garcia-Escudero R, Guccini I, Da Silva-Alvarez S, Collado M, Eisenberger M, Zhang Z, Catapano C, Grassi F, Alimonti A

Abstract

Aberrant activation of oncogenes or loss of tumour suppressor genes opposes malignant transformation by triggering a stable arrest in cell growth, which is termed cellular senescence. This process is finely tuned by both cell-autonomous and non-cell-autonomous mechanisms that regulate the entry of tumour cells to senescence. Whether tumour-infiltrating immune cells can oppose senescence is unknown. Here we show that at the onset of senescence, PTEN null prostate tumours in mice are massively infiltrated by a population of CD11b(+)Gr-1(+) myeloid cells that protect a fraction of proliferating tumour cells from senescence, thus sustaining tumour growth. Mechanistically, we found that Gr-1(+) cells antagonize senescence in a paracrine manner by interfering with the senescence-associated secretory phenotype of the tumour through the secretion of interleukin-1 receptor antagonist (IL-1RA). Strikingly, Pten-loss-induced cellular senescence was enhanced in vivo when Il1ra knockout myeloid cells were adoptively transferred to PTEN null mice. Therapeutically, docetaxel-induced senescence and efficacy were higher in PTEN null tumours when the percentage of tumour-infiltrating CD11b(+)Gr-1(+) myeloid cells was reduced using an antagonist of CXC chemokine receptor 2 (CXCR2). Taken together, our findings identify a novel non-cell-autonomous network, established by innate immunity, that controls senescence evasion and chemoresistance. Targeting this network provides novel opportunities for cancer therapy.

MeSH Terms
Animals Cell Movement Cellular Senescence/drug effects Disease Progression Docetaxel Drug Resistance, Neoplasm Humans Immunity, Innate Interleukin 1 Receptor Antagonist Protein/deficiency,metabolism Interleukin-1alpha/immunology,metabolism Male Mice Myeloid Cells/cytology,metabolism,transplantation PTEN Phosphohydrolase/deficiency,genetics,metabolism Prostatic Neoplasms/drug therapy,immunology,metabolism,pathology Receptors, Chemokine/metabolism Receptors, Interleukin-8B/antagonists & inhibitors Taxoids/pharmacology Tumor Escape Tumor Microenvironment
Chemicals
Gr-1 protein, mouse Il1rn protein, mouse Interleukin 1 Receptor Antagonist Protein Interleukin-1alpha Receptors, Chemokine Receptors, Interleukin-8B Taxoids Docetaxel PTEN Phosphohydrolase Pten protein, mouse
Authors & Affiliations
17 authors, click to expand affiliations / ORCID
Di Mitri Diletta
1] Institute of Oncology Research (IOR), Oncology Institute of Southern Switzerland, Bellinzona CH6500, Switzerland [2].
Toso Alberto
1] Institute of Oncology Research (IOR), Oncology Institute of Southern Switzerland, Bellinzona CH6500, Switzerland [2].
Chen Jing Jing
1] Institute of Oncology Research (IOR), Oncology Institute of Southern Switzerland, Bellinzona CH6500, Switzerland [2] Faculty of Biology and Medicine, University of Lausanne UNIL, Lausanne CH1011, Switzerland.
Sarti Manuela
Institute of Oncology Research (IOR), Oncology Institute of Southern Switzerland, Bellinzona CH6500, Switzerland.
Pinton Sandra
Institute of Oncology Research (IOR), Oncology Institute of Southern Switzerland, Bellinzona CH6500, Switzerland.
Jost Tanja Rezzonico
Institute for Research in Biomedicine (IRB), Bellinzona CH6500, Switzerland.
D'Antuono Rocco
Institute for Research in Biomedicine (IRB), Bellinzona CH6500, Switzerland.
Montani Erica
Institute for Research in Biomedicine (IRB), Bellinzona CH6500, Switzerland.
Garcia-Escudero Ramon
1] Institute of Oncology Research (IOR), Oncology Institute of Southern Switzerland, Bellinzona CH6500, Switzerland [2] Molecular Oncology Unit, CIEMAT, 28040 Madrid, Spain.
Guccini Ilaria
Institute of Oncology Research (IOR), Oncology Institute of Southern Switzerland, Bellinzona CH6500, Switzerland.
Da Silva-Alvarez Sabela
Laboratory of Stem Cells in Cancer and Aging, (stemCHUS) Health Research Institute of Santiago de Compostela (IDIS), Clinical University Hospital (CHUS), E15706 Santiago de Compostela, Spain.
Collado Manuel
Laboratory of Stem Cells in Cancer and Aging, (stemCHUS) Health Research Institute of Santiago de Compostela (IDIS), Clinical University Hospital (CHUS), E15706 Santiago de Compostela, Spain.
Eisenberger Mario
Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, Maryland 21231-1000, USA.
Zhang Zhe
Divisions of BioStatistics, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, Maryland 21231-1000, USA.
Catapano Carlo
Institute of Oncology Research (IOR), Oncology Institute of Southern Switzerland, Bellinzona CH6500, Switzerland.
Grassi Fabio
1] Institute for Research in Biomedicine (IRB), Bellinzona CH6500, Switzerland [2] Department of Medical Biotechnology and Translational Medicine, University of Milan, Milan I-20100, Italy.
Alimonti Andrea
1] Institute of Oncology Research (IOR), Oncology Institute of Southern Switzerland, Bellinzona CH6500, Switzerland [2] Faculty of Biology and Medicine, University of Lausanne UNIL, Lausanne CH1011, Switzerland.
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Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2014-11-06
Epub
2014-00-24
Pages
134-7
Language
English
Region
England
NLM ID
0410462
Subset
IM
Databases
GEO
Corrections
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