Cellular Senescence: Defining a Path Forward

Vassilis Gorgoulis¹, Peter D Adams², Andrea Alimonti³, Dorothy C Bennett⁴, Oliver Bischof⁵, Cleo Bishop⁶, Judith Campisi⁷, Manuel Collado⁸, Konstantinos Evangelou⁹, Gerardo Ferbeyre¹⁰, Jesús Gil¹¹, Eiji Hara¹², Valery Krizhanovsky¹³, Diana Jurk¹⁴, Andrea B Maier¹⁵, Masashi Narita¹⁶, Laura Niedernhofer¹⁷, João F Passos¹⁴, Paul D Robbins¹⁷, Clemens A Schmitt¹⁸, John Sedivy¹⁹, Konstantinos Vougas²⁰, Thomas von Zglinicki²¹, Daohong Zhou²², Manuel Serrano²³, Marco Demaria²⁴

Affiliations

¹ Molecular Carcinogenesis Group, Department of Histology and Embryology, Medical School, National and Kapodistrian University of Athens, Athens, Greece; Biomedical Research Foundation, Academy of Athens, Athens, Greece; Faculty Institute for Cancer Sciences, Manchester Academic Health Sciences Centre, University of Manchester, Manchester, UK; Center for New Biotechnologies and Precision Medicine, Medical School, National and Kapodistrian University of Athens, Athens, Greece. Electronic address: vgorg@med.uoa.gr.
² Institute of Cancer Sciences, University of Glasgow, Glasgow G61 1BD, UK; CRUK Beatson Institute, Glasgow G61 1BD, UK; Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA 92037, USA.
³ Institute of Oncology Research (IOR), Oncology Institute of Southern Switzerland, Bellinzona, Switzerland; Università della Svizzera Italiana, Faculty of Biomedical Sciences, Lugano, Switzerland; Department of Medicine, University of Padova, Padova, Italy; Veneto Institute of Molecular Medicine, Padova, Italy.
⁴ Molecular and Clinical Sciences Research Institute, St. George's, University of London, London SW17 0RE, UK.
⁵ Laboratory of Nuclear Organization and Oncogenesis, Department of Cell Biology and Infection, Inserm U993, Institute Pasteur, Paris, France.
⁶ Centre for Cell Biology and Cutaneous Research, Blizard Institute, Barts & The London School of Medicine and Dentistry, Queen Mary University of London, 4 Newark St, London E1 2AT, UK.
⁷ Buck Institute for Research on Aging, Novato, CA, USA.
⁸ Health Research Institute of Santiago de Compostela (IDIS), Clinical University Hospital (CHUS), Santiago de Compostela, Spain.
⁹ Molecular Carcinogenesis Group, Department of Histology and Embryology, Medical School, National and Kapodistrian University of Athens, Athens, Greece.
¹⁰ Faculty of Medicine, Department of Biochemistry, Université de Montréal and CRCHUM, Montreal, QC, Canada.
¹¹ MRC London Institute of Medical Sciences (LMS), Du Cane Road, London, UK; Institute of Clinical Sciences (ICS), Faculty of Medicine, Imperial College London, Du Cane Road, London, UK.
¹² Department of Molecular Microbiology, Research Institute for Microbial Diseases, Osaka University, Osaka, Japan.
¹³ Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel.
¹⁴ Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.
¹⁵ Department of Human Movement Sciences, Faculty of Behavioural and Movement Sciences, Amsterdam Movement Sciences, Vrije Universiteit, Amsterdam, the Netherlands; Department of Medicine and Aged Care, The Royal Melbourne Hospital, The University of Melbourne, Melbourne, VIC, Australia.
¹⁶ Cancer Research UK Cambridge Institute, Li Ka Shing Centre, University of Cambridge, Cambridge CB2 0RE, United Kingdom.
¹⁷ Institute on the Biology of Aging and Metabolism, University of Minnesota, MN, USA.
¹⁸ Charité - University Medical Center, Department of Hematology, Oncology and Tumor Immunology, Virchow Campus, and Molekulares Krebsforschungszentrum, Berlin, Germany; Max-Delbrück-Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany; Kepler University Hospital, Department of Hematology and Oncology, Johannes Kepler University, Linz, Austria.
¹⁹ Department of Molecular Biology, Cell Biology and Biochemistry, and Center for the Biology of Aging, Brown University, Providence, RI, USA.
²⁰ Biomedical Research Foundation, Academy of Athens, Athens, Greece.
²¹ Newcastle University Institute for Ageing, Institute for Cell and Molecular Biology, Campus for Ageing and Vitality, Newcastle University, Newcastle upon Tyne NE4 5PL, UK.
²² Department of Pharmacodynamics, College of Pharmacy, University of Florida, Gainesville, FL, USA.
²³ Catalan Institution for Research and Advanced Studies (ICREA), Barcelona, Spain; Institute for Research in Biomedicine (IRB Barcelona), Barcelona Institute of Science and Technology (BIST), Barcelona, Spain. Electronic address: manuel.serrano@irbbarcelona.org.
²⁴ University of Groningen (RUG), European Research Institute for the Biology of Aging (ERIBA), University Medical Center Groningen (UMCG), Groningen, the Netherlands. Electronic address: m.demaria@umcg.nl.

PMID: 31675495
DOI: 10.1016/j.cell.2019.10.005

Free article

Review

Cellular Senescence: Defining a Path Forward

Vassilis Gorgoulis et al. Cell. 2019.

Free article

. 2019 Oct 31;179(4):813-827.

doi: 10.1016/j.cell.2019.10.005.

Authors

Affiliations

¹ Molecular Carcinogenesis Group, Department of Histology and Embryology, Medical School, National and Kapodistrian University of Athens, Athens, Greece; Biomedical Research Foundation, Academy of Athens, Athens, Greece; Faculty Institute for Cancer Sciences, Manchester Academic Health Sciences Centre, University of Manchester, Manchester, UK; Center for New Biotechnologies and Precision Medicine, Medical School, National and Kapodistrian University of Athens, Athens, Greece. Electronic address: vgorg@med.uoa.gr.
² Institute of Cancer Sciences, University of Glasgow, Glasgow G61 1BD, UK; CRUK Beatson Institute, Glasgow G61 1BD, UK; Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA 92037, USA.
³ Institute of Oncology Research (IOR), Oncology Institute of Southern Switzerland, Bellinzona, Switzerland; Università della Svizzera Italiana, Faculty of Biomedical Sciences, Lugano, Switzerland; Department of Medicine, University of Padova, Padova, Italy; Veneto Institute of Molecular Medicine, Padova, Italy.
⁴ Molecular and Clinical Sciences Research Institute, St. George's, University of London, London SW17 0RE, UK.
⁵ Laboratory of Nuclear Organization and Oncogenesis, Department of Cell Biology and Infection, Inserm U993, Institute Pasteur, Paris, France.
⁶ Centre for Cell Biology and Cutaneous Research, Blizard Institute, Barts & The London School of Medicine and Dentistry, Queen Mary University of London, 4 Newark St, London E1 2AT, UK.
⁷ Buck Institute for Research on Aging, Novato, CA, USA.
⁸ Health Research Institute of Santiago de Compostela (IDIS), Clinical University Hospital (CHUS), Santiago de Compostela, Spain.
⁹ Molecular Carcinogenesis Group, Department of Histology and Embryology, Medical School, National and Kapodistrian University of Athens, Athens, Greece.
¹⁰ Faculty of Medicine, Department of Biochemistry, Université de Montréal and CRCHUM, Montreal, QC, Canada.
¹¹ MRC London Institute of Medical Sciences (LMS), Du Cane Road, London, UK; Institute of Clinical Sciences (ICS), Faculty of Medicine, Imperial College London, Du Cane Road, London, UK.
¹² Department of Molecular Microbiology, Research Institute for Microbial Diseases, Osaka University, Osaka, Japan.
¹³ Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel.
¹⁴ Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.
¹⁵ Department of Human Movement Sciences, Faculty of Behavioural and Movement Sciences, Amsterdam Movement Sciences, Vrije Universiteit, Amsterdam, the Netherlands; Department of Medicine and Aged Care, The Royal Melbourne Hospital, The University of Melbourne, Melbourne, VIC, Australia.
¹⁶ Cancer Research UK Cambridge Institute, Li Ka Shing Centre, University of Cambridge, Cambridge CB2 0RE, United Kingdom.
¹⁷ Institute on the Biology of Aging and Metabolism, University of Minnesota, MN, USA.
¹⁸ Charité - University Medical Center, Department of Hematology, Oncology and Tumor Immunology, Virchow Campus, and Molekulares Krebsforschungszentrum, Berlin, Germany; Max-Delbrück-Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany; Kepler University Hospital, Department of Hematology and Oncology, Johannes Kepler University, Linz, Austria.
¹⁹ Department of Molecular Biology, Cell Biology and Biochemistry, and Center for the Biology of Aging, Brown University, Providence, RI, USA.
²⁰ Biomedical Research Foundation, Academy of Athens, Athens, Greece.
²¹ Newcastle University Institute for Ageing, Institute for Cell and Molecular Biology, Campus for Ageing and Vitality, Newcastle University, Newcastle upon Tyne NE4 5PL, UK.
²² Department of Pharmacodynamics, College of Pharmacy, University of Florida, Gainesville, FL, USA.
²³ Catalan Institution for Research and Advanced Studies (ICREA), Barcelona, Spain; Institute for Research in Biomedicine (IRB Barcelona), Barcelona Institute of Science and Technology (BIST), Barcelona, Spain. Electronic address: manuel.serrano@irbbarcelona.org.
²⁴ University of Groningen (RUG), European Research Institute for the Biology of Aging (ERIBA), University Medical Center Groningen (UMCG), Groningen, the Netherlands. Electronic address: m.demaria@umcg.nl.

PMID: 31675495
DOI: 10.1016/j.cell.2019.10.005

Abstract

Cellular senescence is a cell state implicated in various physiological processes and a wide spectrum of age-related diseases. Recently, interest in therapeutically targeting senescence to improve healthy aging and age-related disease, otherwise known as senotherapy, has been growing rapidly. Thus, the accurate detection of senescent cells, especially in vivo, is essential. Here, we present a consensus from the International Cell Senescence Association (ICSA), defining and discussing key cellular and molecular features of senescence and offering recommendations on how to use them as biomarkers. We also present a resource tool to facilitate the identification of genes linked with senescence, SeneQuest (available at http://Senequest.net). Lastly, we propose an algorithm to accurately assess and quantify senescence, both in cultured cells and in vivo.

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Cellular Senescence: Defining a Path Forward

Affiliations

Cellular Senescence: Defining a Path Forward

Authors

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Abstract

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Medical