Microbial Cell (Jan 2018)
Guidelines and recommendations on yeast cell death nomenclature
- 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 Cullin,
- Ian Dawes,
- Jörn Dengjel,
- Martin B. Dickman,
- Tobias Eisenberg,
- Birthe Fahrenkrog,
- Nicolas Fasel,
- Kai-Uwe Fröhlich,
- Ali Gargouri,
- Sergio Giannattasio,
- Paola Goffrini,
- Campbell W. Gourlay,
- Chris M. Grant,
- Michael T. Greenwood,
- Nicoletta Guaragnella,
- Thomas Heger,
- Jürgen Heinisch,
- Eva Herker,
- Johannes M. Herrmann,
- Sebastian Hofer,
- Antonio Jiménez-Ruiz,
- Helmut Jungwirth,
- Katharina Kainz,
- Dimitrios P. Kontoyiannis,
- Paula Ludovico,
- Stéphen Manon,
- Enzo Martegani,
- Cristina Mazzoni,
- Lynn A. Megeney,
- Chris Meisinger,
- Jens Nielsen,
- Thomas Nyström,
- Heinz D. Osiewacz,
- Tiago F. Outeiro,
- Hay-Oak Park,
- Tobias Pendl,
- Dina Petranovic,
- Stephane Picot,
- Peter Polčic,
- Peter Polčic,
- Mark Ramsdale,
- Mark Rinnerthaler,
- Patrick Rockenfeller,
- Christoph Ruckenstuhl,
- Raffael Schaffrath,
- Maria Segovia,
- Fedor F. Severin,
- Amir Sharon,
- Stephan J. Sigrist,
- Cornelia Sommer-Ruck,
- Maria João Sousa,
- Johan M. Thevelein,
- Karin Thevissen,
- Vladimir Titorenko,
- Michel B. Toledano,
- Mick Tuite,
- F.-Nora Vögtle,
- Benedikt Westermann,
- Joris Winderickx,
- Silke Wissing,
- Stefan Wölfl,
- Zhaojie J. Zhang,
- Richard Y. Zhao,
- Bing Zhou,
- Lorenzo Galluzzi,
- Guido Kroemer,
- Frank Madeo
Affiliations
- Didac Carmona-Gutierrez
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- Maria Anna Bauer
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- Andreas Zimmermann
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- Andrés Aguilera
- Centro Andaluz de Biología, Molecular y Medicina Regenerativa-CABIMER, Universidad de Sevilla, Sevilla, Spain.
- Nicanor Austriaco
- Department of Biology, Providence College, Providence, USA.
- Kathryn Ayscough
- Department of Biomedical Science, University of Sheffield, Sheffield, United Kingdom.
- Rena Balzan
- Department of Physiology and Biochemistry, University of Malta, Msida, Malta.
- Shoshana Bar-Nun
- Department of Biochemistry and Molecular Biology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel.
- Antonio Barrientos
- Department of Biochemistry and Molecular Biology, University of Miami Miller School of Medicine, Miami, USA.
- Peter Belenky
- Department of Molecular Microbiology and Immunology, Brown University, Providence, USA.
- Marc Blondel
- 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.
- Ralf J. Braun
- Institute of Cell Biology, University of Bayreuth, Bayreuth, Germany.
- Michael Breitenbach
- Department of Cell Biology and Physiology, Division of Genetics, University of Salzburg, Salzburg, Austria.
- William C. Burhans
- Department of Molecular and Cellular Biology, Roswell Park Cancer Institute, Buffalo, NY, USA.
- Sabrina Büttner
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- Duccio Cavalieri
- Department of Biology, University of Florence, Firenze, Italy.
- Michael Chang
- European Research Institute for the Biology of Ageing, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.
- Katrina F. Cooper
- Dept. Molecular Biology, Graduate School of Biomedical Sciences, Rowan University, Stratford, USA.
- Manuela Côrte-Real
- Center of Molecular and Environmental Biology, Department of Biology, University of Minho, Braga, Portugal.
- Vítor Costa
- Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal.
- Christophe Cullin
- CNRS, University of Bordeaux CBMN (UMR 5248), Pessac, France.
- Ian Dawes
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia.
- Jörn Dengjel
- Department of Biology, University of Fribourg, Fribourg, Switzerland.
- Martin B. Dickman
- Institute for Plant Genomics and Biotechnology, Texas A&M University, Texas, USA.
- Tobias Eisenberg
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- Birthe Fahrenkrog
- Laboratory Biology of the Nucleus, Institute for Molecular Biology and Medicine, Université Libre de Bruxelles, Charleroi, Belgium.
- Nicolas Fasel
- Department of Biochemistry, University of Lausanne, Lausanne, Switzerland.
- Kai-Uwe Fröhlich
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- Ali Gargouri
- Laboratoire de Biotechnologie Moléculaire des Eucaryotes, Center de Biotechnologie de Sfax, Sfax, Tunisia.
- Sergio Giannattasio
- Institute of Biomembranes, Bioenergetics and Molecular Biotechnologies, National Research Council, Bari, Italy.
- Paola Goffrini
- Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy.
- Campbell W. Gourlay
- Kent Fungal Group, School of Biosciences, University of Kent, Canterbury, United Kingdom.
- Chris M. Grant
- Faculty of Biology, Medicine and Health, The University of Manchester, Manchester, United Kingdom.
- Michael T. Greenwood
- Department of Chemistry and Chemical Engineering, Royal Military College, Kingston, Ontario, Canada.
- Nicoletta Guaragnella
- Institute of Biomembranes, Bioenergetics and Molecular Biotechnologies, National Research Council, Bari, Italy.
- Thomas Heger
- Zürich, Switzerland.
- Jürgen Heinisch
- Department of Biology and Chemistry, University of Osnabrück, Osnabrück, Germany.
- Eva Herker
- Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg, Germany.
- Johannes M. Herrmann
- Cell Biology, University of Kaiserslautern, Kaiserslautern, Germany.
- Sebastian Hofer
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- Antonio Jiménez-Ruiz
- Department of Systems Biology, University of Alcalá, Alcalá de Henares, Spain.
- Helmut Jungwirth
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- Katharina Kainz
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- Dimitrios P. Kontoyiannis
- Division of Internal Medicine, The University of Texas MD Anderson Cancer Center, Houston, Texas, USA.
- Paula Ludovico
- Life and Health Sciences Research Institute (ICVS), School of Health Sciences, University of Minho, Minho, Portugal.
- Stéphen Manon
- Institut de Biochimie et de Génétique Cellulaires, UMR5095, CNRS & Université de Bordeaux, Bordeaux, France.
- Enzo Martegani
- Department of Biotechnolgy and Biosciences, University of Milano-Bicocca, Milano, Italy.
- Cristina Mazzoni
- Instituto Pasteur-Fondazione Cenci Bolognetti – Department of Biology and Biotechnology “C. Darwin”, La Sapienza University of Rome, Rome, Italy.
- Lynn A. Megeney
- Sprott Center for Stem Cell Research, Ottawa Hospital Research Institute, The Ottawa Hospital, Ottawa, Canada.
- Chris Meisinger
- Institute of Biochemistry and Molecular Biology, ZBMZ, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
- Jens Nielsen
- Department of Biology and Biological Engineering, Chalmers University of Technology, Gothenburg, Sweden.
- Thomas Nyström
- Institute for Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden.
- Heinz D. Osiewacz
- Institute for Molecular Biosciences, Goethe University, Frankfurt am Main, Germany.
- Tiago F. Outeiro
- 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.
- Hay-Oak Park
- Department of Molecular Genetics, The Ohio State University, Columbus, OH, USA.
- Tobias Pendl
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- Dina Petranovic
- Department of Biology and Biological Engineering, Chalmers University of Technology, Gothenburg, Sweden.
- Stephane Picot
- Malaria Research Unit, SMITh, ICBMS, UMR 5246 CNRS-INSA-CPE-University Lyon, Lyon, France.
- Peter Polčic
- Department of Biochemistry, Faculty of Natural Sciences, Comenius University in Bratislava, Bratislava, Slovak Republic.
- Peter Polčic
- Department of Biochemistry, Faculty of Natural Sciences, Comenius University in Bratislava, Bratislava, Slovak Republic.
- Mark Ramsdale
- Biosciences, University of Exeter, Exeter, United Kingdom.
- Mark Rinnerthaler
- Department of Cell Biology and Physiology, Division of Genetics, University of Salzburg, Salzburg, Austria.
- Patrick Rockenfeller
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- Christoph Ruckenstuhl
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- Raffael Schaffrath
- Institute of Biology, Division of Microbiology, University of Kassel, Kassel, Germany.
- Maria Segovia
- Department of Ecology, Faculty of Sciences, University of Malaga, Malaga, Spain.
- Fedor F. Severin
- A.N. Belozersky Institute of physico-chemical biology, Moscow State University, Moscow, Russia.
- Amir Sharon
- School of Plant Sciences and Food Security, Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel.
- Stephan J. Sigrist
- Institute for Biology/Genetics, Freie Universität Berlin, Berlin, Germany.
- Cornelia Sommer-Ruck
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- Maria João Sousa
- Center of Molecular and Environmental Biology, Department of Biology, University of Minho, Braga, Portugal.
- Johan M. Thevelein
- Laboratory of Molecular Cell Biology, Institute of Botany and Microbiology, KU Leuven, Leuven, Belgium.
- Karin Thevissen
- Centre of Microbial and Plant Genetics, KU Leuven, Leuven, Belgium.
- Vladimir Titorenko
- Biology Department, Concordia University, Montreal, Canada.
- Michel B. Toledano
- Institute for Integrative Biology of the Cell (I2BC), SBIGEM, CEA-Saclay, Université Paris-Saclay, Gif-sur-Yvette, France.
- Mick Tuite
- Kent Fungal Group, School of Biosciences, University of Kent, Canterbury, United Kingdom.
- F.-Nora Vögtle
- Institute of Biochemistry and Molecular Biology, ZBMZ, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
- Benedikt Westermann
- Institute of Cell Biology, University of Bayreuth, Bayreuth, Germany.
- Joris Winderickx
- Department of Biology, Functional Biology, KU Leuven, Leuven-Heverlee, Belgium.
- Silke Wissing
- Cevec Pharmaceuticals, Cologne, Germany.
- Stefan Wölfl
- Institute of Pharmacy and Molecular Biotechnology, Heidelberg University, Heidelberg, Germany.
- Zhaojie J. Zhang
- Department of Zoology and Physiology, University of Wyoming, Laramie, USA.
- Richard Y. Zhao
- Department of Pathology, University of Maryland School of Medicine, Baltimore, USA.
- Bing Zhou
- School of Life Sciences, Tsinghua University, Beijing, China.
- Lorenzo Galluzzi
- Department of Radiation Oncology, Weill Cornell Medical College, New York, NY, USA.
- Guido Kroemer
- Université Paris Descartes/Paris V, Paris, France.
- Frank Madeo
- Institute of Molecular Biosciences, NAWI Graz, University of Graz, Graz, Austria.
- DOI
- https://doi.org/10.15698/mic2018.01.607
- Journal volume & issue
-
Vol. 5,
no. 1
pp. 4 – 31
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.
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