A Human-Like Senescence-Associated Secretory Phenotype Is Conserved in Mouse Cells Dependent on Physiological Oxygen

Coppé, Jean-Philippe; Patil, Christopher K.; Rodier, Francis; Krtolica, Ana; Beauséjour, Christian M.; Parrinello, Simona; Hodgson, J. Graeme; Chin, Koei; Desprez, Pierre-Yves; Campisi, Judith; Blagosklonny, Mikhail V.

doi:10.1371/journal.pone.0009188

A Human-Like Senescence-Associated Secretory Phenotype Is Conserved in Mouse Cells Dependent on Physiological Oxygen

Journal Article · Thu Feb 11 23:00:00 EST 2010 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0009188· OSTI ID:1627397

Coppé, Jean-Philippe ^[1]; Patil, Christopher K. ^[2]; Rodier, Francis ^[2]; Krtolica, Ana ^[3]; Beauséjour, Christian M. ^[4]; Parrinello, Simona ^[3]; Hodgson, J. Graeme ^[5]; Chin, Koei ^[5]; Desprez, Pierre-Yves ^[6]; Campisi, Judith ^[2]; Blagosklonny, Mikhail V.

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division; Buck Inst. for Age Research, Navato, CA (United States); DOE/OSTI
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division; Buck Inst. for Age Research, Navato, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division
Univ. of Montreal, QC (Canada). Centre de Recherche du CHU Ste-Justine et De´partement de Pharmacologie
Univ. of California, San Francisco, CA (United States). Comprehensive Cancer Center. Dept. of Lab. Medicine
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division; Buck Inst. for Age Research, Navato, CA (United States); California Pacific Medical Center Research Inst., San Francisco, CA (United States)

Cellular senescence irreversibly arrests cell proliferation in response to oncogenic stimuli. Human cells develop a senescence-associated secretory phenotype (SASP), which increases the secretion of cytokines and other factors that alter the behavior of neighboring cells. We show here that ‘‘senescent’’ mouse fibroblasts, which arrested growth after repeated passage under standard culture conditions (20% oxygen), do not express a human-like SASP, and differ from similarly cultured human cells in other respects. However, when cultured in physiological (3%) oxygen and induced to senesce by radiation, mouse cells more closely resemble human cells, including expression of a robust SASP. We describe two new aspects of the human and mouse SASPs. First, cells from both species upregulated the expression and secretion of several matrix metalloproteinases, which comprise a conserved genomic cluster. Second, for both species, the ability to promote the growth of premalignant epithelial cells was due primarily to the conserved SASP factor CXCL-1/KC/GRO-a. Further, mouse fibroblasts made senescent in 3%, but not 20%, oxygen promoted epithelial tumorigenesis in mouse xenographs. Our findings underscore critical mouse-human differences in oxygen sensitivity, identify conditions to use mouse cells to model human cellular senescence, and reveal novel conserved features of the SASP.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC03-76SF00098

OSTI ID:: 1627397

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 2 Vol. 5; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Targetable mechanisms driving immunoevasion of persistent senescent cells link chemotherapy-resistant cancer to aging Muñoz, Denise P.; Yannone, Steven M.; Daemen, Anneleen JCI Insight, Vol. 4, Issue 14 https://doi.org/10.1172/jci.insight.124716	journal	July 2019
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Cellular senescence in brain aging and neurodegenerative diseases: evidence and perspectives Baker, Darren J.; Petersen, Ronald C. Journal of Clinical Investigation, Vol. 128, Issue 4 https://doi.org/10.1172/jci95145	journal	February 2018
DNA double-strand break repair is impaired in presenescent Syrian hamster fibroblasts Solovjeva, Ljudmila; Firsanov, Denis; Vasilishina, Anastasia BMC Molecular Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12867-015-0046-4	journal	October 2015
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Cellular senescence in development, regeneration and disease Rhinn, Muriel; Ritschka, Birgit; Keyes, William M. Development, Vol. 146, Issue 20 https://doi.org/10.1242/dev.151837	journal	October 2019
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Senescent human melanocytes drive skin ageing via paracrine telomere dysfunction Victorelli, Stella; Lagnado, Anthony; Halim, Jessica The EMBO Journal, Vol. 38, Issue 23 https://doi.org/10.15252/embj.2019101982	journal	October 2019
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Cells exhibiting strong p16 INK4a promoter activation in vivo display features of senescence J. S., Parker,; B. O., Diekman,; N. E., Sharpless, National Academy of Sciences https://doi.org/10.17615/3gsg-s066	text	January 2019
Vascular Smooth Muscle Cell Senescence Promotes Atherosclerosis and Features of Plaque Vulnerability. Wang, Julie; Uryga, Anna; Reinhold, Johannes Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.22794	text	January 2015
A Proteomic Atlas of Senescence-Associated Secretomes for Aging Biomarker Development Basisty, Nathan; Kale, Abhijit; Jeon, Okhee SSRN Electronic Journal https://doi.org/10.2139/ssrn.3380253	journal	January 2019
Characterization of DNA damage-induced cellular senescence by ionizing radiation in endothelial cells Kim, Kwang Seok; Kim, Jung Eun; Choi, Kyu Jin International Journal of Radiation Biology, Vol. 90, Issue 1 https://doi.org/10.3109/09553002.2014.859763	journal	September 2013
IGF Binding Protein-5 Induces Cell Senescence Sanada, Fumihiro; Taniyama, Yoshiaki; Muratsu, Jun Frontiers in Endocrinology, Vol. 9 https://doi.org/10.3389/fendo.2018.00053	journal	February 2018
Age- and Tissue-Specific Expression of Senescence Biomarkers in Mice Hudgins, Adam D.; Tazearslan, Cagdas; Tare, Archana Frontiers in Genetics, Vol. 9 https://doi.org/10.3389/fgene.2018.00059	journal	February 2018
Targeting senescent cells enhances adipogenesis and metabolic function in old age Xu, Ming; Palmer, Allyson K.; Ding, Husheng eLife, Vol. 4 https://doi.org/10.7554/elife.12997	journal	December 2015

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