Guidelines and recommendations on yeast cell death nomenclature
Authors:Didac Carmona-Gutierrez1,‡,*, Maria Anna Bauer1,‡, Andreas Zimmermann1, Andrés Aguilera2, Nicanor Austriaco3, Kathryn Ayscough4, Rena Balzan5, Shoshana Bar-Nun6, Antonio Barrientos7,8, Peter Belenky9, Marc Blondel10, Ralf J. Braun11, Michael Breitenbach12, William C. Burhans13, Sabrina Büttner1,14, Duccio Cavalieri15, Michael Chang16, Katrina F. Cooper17, Manuela Côrte-Real18, Vítor Costa19–21, Christophe Cullin22, Ian Dawes23, Jörn Dengjel24, Martin B. Dickman25, Tobias Eisenberg1,26, Birthe Fahrenkrog27, Nicolas Fasel28, Kai-Uwe Fröhlich1, Ali Gargouri29, Sergio Giannattasio30, Paola Goffrini31, Campbell W. Gourlay32, Chris M. Grant33, Michael T. Greenwood34, Nicoletta Guaragnella30, Thomas Heger35, Jürgen Heinisch36, Eva Herker37, Johannes M. Herrmann38, Sebastian Hofer1, Antonio Jiménez-Ruiz39, Helmut Jungwirth1, Katharina Kainz1, Dimitrios P. Kontoyiannis40, Paula Ludovico41,42, Stéphen Manon43, Enzo Martegani44, Cristina Mazzoni45, Lynn A. Megeney46–48, Chris Meisinger49, Jens Nielsen50–52, Thomas Nyström53, Heinz D. Osiewacz54, Tiago F. Outeiro55–58, Hay-Oak Park59, Tobias Pendl1, Dina Petranovic50,51, Stephane Picot60,61, Peter Polčic62, Ted Powers63, Mark Ramsdale64, Mark Rinnerthaler65, Patrick Rockenfeller1,32, Christoph Ruckenstuhl1, Raffael Schaffrath66, Maria Segovia67, Fedor F. Severin68, Amir Sharon69, Stephan J. Sigrist70, Cornelia Sommer-Ruck1, Maria João Sousa18, Johan M. Thevelein71,72, Karin Thevissen73, Vladimir Titorenko74, Michel B. Toledano75, Mick Tuite32, F.-Nora Vögtle49, Benedikt Westermann11, Joris Winderickx76, Silke Wissing77, Stefan Wölfl78, Zhaojie J. Zhang79, Richard Y. Zhao80, Bing Zhou81, Lorenzo Galluzzi82–84,*, Guido Kroemer84–90,*, Frank Madeo1,26,*
1 Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria. 2 Centro Andaluz de Biología, Molecular y Medicina Regenerativa-CABIMER, Universidad de Sevilla, Sevilla, Spain. 3 Department of Biology, Providence College, Providence, USA. 4 Department of Biomedical Science, University of Sheffield, Sheffield, United Kingdom. 5 Department of Physiology and Biochemistry, University of Malta, Msida, Malta. 6 Department of Biochemistry and Molecular Biology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel. 7 Department of Biochemistry and Molecular Biology, University of Miami Miller School of Medicine, Miami, USA. 8 Department of Neurology, University of Miami Miller School of Medicine, Miami, USA. 9 Department of Molecular Microbiology and Immunology, Brown University, Providence, USA. 10 Institut National de la Santé et de la Recherche Médicale UMR1078, Université de Bretagne Occidentale, Etablissement Français du Sang Bretagne, CHRU Brest, Hôpital Morvan, Laboratoire de Génétique Moléculaire, Brest, France. 11 Institute of Cell Biology, University of Bayreuth, Bayreuth, Germany. 12 Department of Cell Biology and Physiology, Division of Genetics, University of Salzburg, Salzburg, Austria. 13 Department of Molecular and Cellular Biology, Roswell Park Cancer Institute, Buffalo, NY, USA. 14 Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, Sweden. 15 Department of Biology, University of Florence, Firenze, Italy. 16 European Research Institute for the Biology of Ageing, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands. 17 Dept. Molecular Biology, Graduate School of Biomedical Sciences, Rowan University, Stratford, USA. 18 Center of Molecular and Environmental Biology, Department of Biology, University of Minho, Braga, Portugal. 19 Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal. 20 Instituto de Biologia Molecular e Celular, Universidade do Porto, Porto, Portugal. 21 Departamento de Biologia Molecular, Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Porto, Portugal. 22 CNRS, University of Bordeaux CBMN (UMR 5248), Pessac, France. 23 School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia. 24 Department of Biology, University of Fribourg, Fribourg, Switzerland. 25 Institute for Plant Genomics and Biotechnology, Texas A&M University, Texas, USA. 26 BioTechMed Graz, Graz, Austria. 27 Laboratory Biology of the Nucleus, Institute for Molecular Biology and Medicine, Université Libre de Bruxelles, Charleroi, Belgium. 28 Department of Biochemistry, University of Lausanne, Lausanne, Switzerland. 29 Laboratoire de Biotechnologie Moléculaire des Eucaryotes, Center de Biotechnologie de Sfax, Sfax, Tunisia. 30 Institute of Biomembranes, Bioenergetics and Molecular Biotechnologies, National Research Council, Bari, Italy. 31 Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy. 32 Kent Fungal Group, School of Biosciences, University of Kent, Canterbury, United Kingdom. 33 Faculty of Biology, Medicine and Health, The University of Manchester, Manchester, United Kingdom. 34 Department of Chemistry and Chemical Engineering, Royal Military College, Kingston, Ontario, Canada. 35 Zürich, Switzerland. 36 Department of Biology and Chemistry, University of Osnabrück, Osnabrück, Germany. 37 Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg, Germany. 38 Cell Biology, University of Kaiserslautern, Kaiserslautern, Germany. 39 Department of Systems Biology, University of Alcalá, Alcalá de Henares, Spain. 40 Division of Internal Medicine, The University of Texas MD Anderson Cancer Center, Houston, Texas, USA. 41 Life and Health Sciences Research Institute (ICVS), School of Health Sciences, University of Minho, Minho, Portugal. 42 ICVS/3B’s – PT Government Associate Laboratory, Braga/Guimarães, Portugal. 43 Institut de Biochimie et de Génétique Cellulaires, UMR5095, CNRS & Université de Bordeaux, Bordeaux, France. 44 Department of Biotechnolgy and Biosciences, University of Milano-Bicocca, Milano, Italy. 45 Instituto Pasteur-Fondazione Cenci Bolognetti – Department of Biology and Biotechnology “C. Darwin”, La Sapienza University of Rome, Rome, Italy. 46 Sprott Center for Stem Cell Research, Ottawa Hospital Research Institute, The Ottawa Hospital, Ottawa, Canada. 47 Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Canada. 48 Department of Medicine, Division of Cardiology, University of Ottawa, Ottawa, Canada. 49 Institute of Biochemistry and Molecular Biology, ZBMZ, Faculty of Medicine, University of Freiburg, Freiburg, Germany. 50 Department of Biology and Biological Engineering, Chalmers University of Technology, Gothenburg, Sweden. 51 Novo Nordisk Foundation Center for Biosustainability, Chalmers University of Technology, Gothenburg, Sweden. 52 Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, DK2800 Lyngby, Denmark. 53 Institute for Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden. 54 Institute for Molecular Biosciences, Goethe University, Frankfurt am Main, Germany. 55 Department of Experimental Neurodegeneration, Center for Nanoscale Microscopy and Molecular Physiology of the Brain, Center for Biostructural Imaging of Neurodegeneration, University Medical Center Göttingen, Göttingen, Germany. 56 Max Planck Institute for Experimental Medicine, Göttingen, Germany. 57 Institute of Neuroscience, The Medical School, Newcastle University, Framlington Place, Newcastle Upon Tyne, NE2 4HH, United Kingdom. 58 CEDOC, Chronic Diseases Research Centre, NOVA Medical School, Faculdade de Ciências Médicas, Universidade NOVA de Lisboa, Lisboa, Portugal. 59 Department of Molecular Genetics, The Ohio State University, Columbus, OH, USA. 60 Malaria Research Unit, SMITh, ICBMS, UMR 5246 CNRS-INSA-CPE-University Lyon, Lyon, France. 61 Institut of Parasitology and Medical Mycology, Hospices Civils de Lyon, Lyon, France. 62 Department of Biochemistry, Faculty of Natural Sciences, Comenius University in Bratislava, Bratislava, Slovak Republic. 63 Department of Molecular and Cellular Biology, College of Biological Sciences, UC Davis, Davis, California, USA. 64 Biosciences, University of Exeter, Exeter, United Kingdom. 65 Department of Cell Biology and Physiology, Division of Genetics, University of Salzburg, Salzburg, Austria. 66 Institute of Biology, Division of Microbiology, University of Kassel, Kassel, Germany. 67 Department of Ecology, Faculty of Sciences, University of Malaga, Malaga, Spain. 68 A.N. Belozersky Institute of physico-chemical biology, Moscow State University, Moscow, Russia. 69 School of Plant Sciences and Food Security, Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel. 70 Institute for Biology/Genetics, Freie Universität Berlin, Berlin, Germany. 71 Laboratory of Molecular Cell Biology, Institute of Botany and Microbiology, KU Leuven, Leuven, Belgium. 72 Center for Microbiology, VIB, Leuven-Heverlee, Belgium. 73 Centre of Microbial and Plant Genetics, KU Leuven, Leuven, Belgium. 74 Biology Department, Concordia University, Montreal, Canada. 75 Institute for Integrative Biology of the Cell (I2BC), SBIGEM, CEA-Saclay, Université Paris-Saclay, Gif-sur-Yvette, France. 76 Department of Biology, Functional Biology, KU Leuven, Leuven-Heverlee, Belgium. 77 Cevec Pharmaceuticals, Cologne, Germany. 78 Institute of Pharmacy and Molecular Biotechnology, Heidelberg University, Heidelberg, Germany. 79 Department of Zoology and Physiology, University of Wyoming, Laramie, USA. 80 Department of Pathology, University of Maryland School of Medicine, Baltimore, USA. 81 School of Life Sciences, Tsinghua University, Beijing, China. 82 Department of Radiation Oncology, Weill Cornell Medical College, New York, NY, USA. 83 Sandra and Edward Meyer Cancer Center, New York, NY, USA. 84 Université Paris Descartes/Paris V, Paris, France. 85 Equipe 11 Labellisée Ligue Contre le Cancer, Centre de Recherche des Cordeliers, Paris, France. 86 Cell Biology and Metabolomics Platforms, Gustave Roussy Comprehensive Cancer Center, Villejuif, France. 87 INSERM, U1138, Paris, France. 88 Université Pierre et Marie Curie/Paris VI, Paris, France. 89 Pôle de Biologie, Hôpital Européen Georges Pompidou, Paris, France. 90 Karolinska Institute, Department of Women’s and Children’s Health, Karolinska University Hospital, Stockholm, Sweden.
Keywords:
accidental cell death, apoptosis, autophagic cell death, autophagy, caspases, mitochondrial membrane permeabilization, mitotic catastrophe, model organism, necrosis, reactive oxygen species, regulated cell death, Saccharomyces cerevisiae
Related Article(s)?
Corresponding Author(s):
Conflict of interest statement:
The authors declare no conflict of interest.
Please cite this article as:
Didac Carmona-Gutierrez, Maria Anna Bauer, Andreas Zimmermann, Andrés Aguilera, Nicanor Austriaco, Kathryn Ayscough, Rena Balzan, Shoshana Bar-Nun, Antonio Barrientos, Peter Belenky, Marc Blondel, Ralf J. Braun, Michael Breitenbach, William C. Burhans, Sabrina Büttner, Duccio Cavalieri, Michael Chang, Katrina F. Cooper, Manuela Côrte-Real, Vítor Costa, Christophe Cul-lin, Ian Dawes, Jörn Dengjel, Martin B. Dickman, Tobias Eisenberg, Birthe Fahrenkrog, Nicolas Fasel, Kai-Uwe Fröh-lich, Ali Gargouri, Sergio Giannattasio et al (2018). Guidelines and recommendations on yeast cell death nomencla-ture. Microbial Cell 5(1): 4-31. doi: 10.15698/mic2018.01.607
© 2018 Carmona-Gutierrez et al. This is an open-access article released under the terms of the Creative Commons Attribution (CC BY) license, which allows the unrestricted use, distribution, and reproduction in any medium, provided the original author and source are acknowledged.
Abstract:
Elucidating the biology of yeast in its full complexity has major implications for science, medicine and industry. One of the most critical processes determining yeast life and physiology is cellular demise. However, the investigation of yeast cell death is a relatively young field, and a widely accepted set of concepts and terms is still missing. Here, we propose unified criteria for the definition of accidental, regulated, and programmed forms of cell death in yeast based on a series of morphological and biochemical criteria. Specifically, we provide consensus guidelines on the differential definition of terms including apoptosis, regulated necrosis, and autophagic cell death, as we refer to additional cell death routines that are relevant for the biology of (at least some species of) yeast. As this area of investigation advances rapidly, changes and extensions to this set of recommendations will be implemented in the years to come. Nonetheless, we strongly encourage the authors, reviewers and editors of scientific articles to adopt these collective standards in order to establish an accurate framework for yeast cell death research and, ultimately, to accelerate the progress of this vibrant field of research.
doi: 10.15698/mic2018.01.607
Volume 5, pp. 4 to 31, published 01/01/2018.