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Aging Research in Yeast
SUBCELLULAR BIOCHEMISTRY
SERIES EDITOR
J. ROBIN HARRIS, University of Mainz, Mainz, Germany
ASSISTANT EDITORS
B.B. BISWAS, University of Calcutta, Calcutta, India
P. QUINN, King’s College London, London, UK
Recent Volumes in this Series
Volume 41 Chromatic and Disease
Edited by Tapas K. Kundu and Dipak Dasgupta
Volume 42 Inflammation in the Pathogenesis of Chronic Disease
Edited by Randall E. Harris
Volume 43 Subcellular Proteomics
Edited by Eric Bertrand and Michel Faupel
Volume 44 Peroxiredoxin Systems
Edited by Leopold Folhé and J. Robin Harris
Volume 45 Calcium Signalling and Disease
Edited by Ernesto Carafoli and Marisa Brini
Volume 46 Creatine and Creatine Kinase in Health and Disease
Edited by Gajja S. Salomons and Markus Wyss
Volume 47 Molecular Mechanisms of Parasite Invasion
Edited by Barbara A. Burleigh and Dominique Soldati-Favre
Volume 48 The Cronin Family of Proteins
Edited by Christoph S. Clemen and Ludwig Eichinger
Volume 49 Lipids in Health and Disease
Edited by Peter J. Quinn and Xiaoyuan Wang
Volume 50 Genome Stability and Human Diseases
Edited by Heinz-Peter Nasheuer
Volume 51 Cholesterol Binding and Cholesterol Transport Proteins
Edited by Robin J. Harris
Volume 52 A Handbook of Transcription Factors
Edited by Tim Hughes
Volume 53 Endotoxins: Stricture, Function and Recognition
Edited by Xiaoyuan Wang and Peter J. Quinn
Volume 54 Conjugation and Deconjugation of Ubiquitin Family Modifiers
Edited by Marcus Groettrup
Volume 55 Purinergic Regulation of Respiratory Diseases
Edited by Maryse Picher and Richard C. Boucher
Volume 56 Water Soluble Vitamins
Edited by Olaf Stanger
Michael Breitenbach · S. Michal Jazwinski ·
Peter Laun
Editors
Aging Research in Yeast
123
Editors
Prof. Dr. Michael Breitenbach
Department of Cell Biology
University of Salzburg
Hellbrunnerstrasse 34
5020 Salzburg
Austria
Prof. S. Michal Jazwinski
Department of Medicine
Tulane University Health Sciences Center
Tulane Center for Aging
Tulane University
1430 Tulane Avenue SL-12
New Orleans, Louisiana 70112
USA
Dr. Peter Laun
Department of Cell Biology
University of Salzburg
Hellbrunnerstrasse 34
5020 Salzburg
Austria
ISSN 0306-0225
ISBN 978-94-007-2560-7 e-ISBN 978-94-007-2561-4
DOI 10.1007/978-94-007-2561-4
Springer Dordrecht Heidelberg London New York
Library of Congress Control Number: 2011940010
© Springer Science+Business Media B.V. 2012
No part of this work may be reproduced, stored in a retrieval system, or transmitted in any form or by
any means, electronic, mechanical, photocopying, microfilming, recording or otherwise, without written
permission from the Publisher, with the exception of any material supplied specifically for the purpose
of being entered and executed on a computer system, for exclusive use by the purchaser of the work.
Printed on acid-free paper
Springer is part of Springer Science+Business Media (www.springer.com)
INTERNATIONAL ADVISORY EDITORIAL BOARD
R. Bittman, Queens College, City University of New York, New York, USA
D. Dasgupt, Saha Institute of Nuclear Physics, Calcutta, India
A. Holzenburg, Texas A&M University, Texas, USA
S. Rottem, The Hebrew University, Jerusalem, Israel
M. Wyss, DSM Nutritional Products Ltd., Basel, Switzerland
Contents
1 Introduction ............................... 1
Michael Breitenbach, Peter Laun, and S. Michal Jazwinski
2 Oxidative Stresses and Ageing . . . . . . . . . . . . . . . . . . . . . 13
May T. Aung-Htut, Anita Ayer, Michael Breitenbach,
and Ian W. Dawes
3 The Role of Mitochondria in the Aging Processes of Yeast . . . . . 55
Michael Breitenbach, Peter Laun, J. Richard Dickinson,
Andrea Klocker, Mark Rinnerthaler, Ian W. Dawes,
May T. Aung-Htut, Lore Breitenbach-Koller,
Antonio Caballero, Thomas Nyström, Sabrina Büttner,
Tobias Eisenberg, Frank Madeo, and Markus Ralser
4 The Retrograde Response and Other Pathways
of Interorganelle Communication in Yeast Replicative Aging . . . . 79
S. Michal Jazwinski
5 Chronological Aging in Saccharomyces cerevisiae . . . . . . . . . . 101
Valter D. Longo and Paola Fabrizio
6 Aging and the Survival of Quiescent and Non-quiescent
Cells in Yeast Stationary-Phase Cultures . . . . . . . . . . . . . . . 123
M. Werner-Washburne, Sushmita Roy, and George S. Davidson
7 Maximising the Yeast Chronological Lifespan . . . . . . . . . . . . 145
Peter W. Piper
8 Amino Acid Homeostasis and Chronological Longevity
in Saccharomyces cerevisiae . . . . . . . . . . . . . . . . . . . . . . 161
John P. Aris, Laura K. Fishwick, Michelle L. Marraffini,
Arnold Y. Seo, Christiaan Leeuwenburgh, and William A. Dunn Jr.
9 DNA Damage and DNA Replication Stress in Yeast Models
of Aging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187
William C. Burhans and Martin Weinberger
vii
viii Contents
10 Yeast Aging and Apoptosis . . . . . . . . . . . . . . . . . . . . . . . 207
Peter Laun, Sabrina Büttner, Mark Rinnerthaler,
William C. Burhans, and Michael Breitenbach
11 Cellular Homeostasis in Fungi: Impact on the Aging Process . . . . 233
Christian Q. Scheckhuber, Andrea Hamann, Diana Brust,
and Heinz D. Osiewacz
12 Genome-Wide Analysis of Yeast Aging . . . . . . . . . . . . . . . . 251
George L. Sutphin, Brady A. Olsen, Brian K. Kennedy,
and Matt Kaeberlein
13 Genetic Approaches to Aging in Budding and Fission
Yeasts: New Connections and New Opportunities . . . . . . . . . . 291
Bo-Ruei Chen and Kurt W. Runge
14 Evolution of Asymmetric Damage Segregation:
A Modelling Approach . . . . . . . . . . . . . . . . . . . . . . . . . 315
Armin Rashidi, Thomas B.L. Kirkwood, and Daryl P. Shanley
15 Cellular Ageing and the Actin Cytoskeleton . . . . . . . . . . . . . 331
David Amberg, Jane E. Leadsham, Vasillios Kotiadis,
and Campbell W. Gourlay
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 353
Contributors
David Amberg Department of Biochemistry and Molecular Biology, SUNY
Upstate Medical University, Syracuse, NY, USA, [email protected]
John P. Aris Department of Anatomy and Cell Biology, University of Florida,
Gainesville, FL 32610-0235, USA, [email protected]
May T. Aung-Htut School of Biotechnology and Biomolecular Sciences,
University of New South Wales, Sydney, NSW 2052, Australia,
Anita Ayer School of Biotechnology and Biomolecular Sciences, University of
New South Wales, Sydney, NSW 2052, Australia, [email protected]
Michael Breitenbach Division of Genetics, Department of Cell Biology,
University of Salzburg, Salzburg, Austria, [email protected]
Lore Breitenbach-Koller Division of Genetics, Department of Cell Biology,
University of Salzburg, Salzburg, Austria,
Diana Brust Faculty of Biosciences, Institute of Molecular Biosciences and
Cluster of Excellence Macromolecular Complexes, Johann Wolfgang Goethe
University, 60438 Frankfurt/Main, Germany, [email protected]
William C. Burhans Department of Molecular and Cellular Biology, Roswell
Park Cancer Institute, Buffalo, NY 14222, USA, [email protected]
Sabrina Büttner Institute of Molecular Biosciences, University of Graz, Graz,
Austria, [email protected]
Antonio Caballero MRC Centre for Developmental Neurobiology, Guy’s
Campus, King’s College London, London, UK, [email protected]
Bo-Ruei Chen Department of Genetics, Case Western Reserve University School
of Medicine, Cleveland, OH 44106, USA, [email protected]
ix
x Contributors
George S. Davidson Department of Biology, University of New Mexico,
Albuquerque, NM 87131, USA, [email protected]
Ian W. Dawes School of Biotechnology and Biomolecular Sciences, University of
New South Wales, Sydney, NSW 2052, Australia, [email protected]
J. Richard Dickinson Department of Biochemistry, Cambridge Systems Biology
Centre, University of Cambridge, Cambridge, UK,
William A. Dunn Jr. Department of Anatomy and Cell Biology, University of
Florida, Gainesville, FL 32610-0235, USA, [email protected]
Tobias Eisenberg Institute of Molecular Biosciences, University of Graz, Graz,
Austria, [email protected]
Paola Fabrizio Laboratory of Molecular and Cellular Biology, UMR5239 CNRS,
Ecole Normale Supérieure de Lyon, Lyon, France, [email protected]
Laura K. Fishwick Department of Anatomy and Cell Biology, University of
Florida, Gainesville, FL 32610-0235, USA, [email protected]
Campbell W. Gourlay Kent Fungal Group, School of Biosciences, University of
Kent, Canterbury, Kent CT2 7NJ, UK, [email protected]
Andrea Hamann Faculty of Biosciences, Institute of Molecular Biosciences and
Cluster of Excellence Macromolecular Complexes, Johann Wolfgang Goethe
University, 60438 Frankfurt/Main, Germany, [email protected]
S. Michal Jazwinski Department of Medicine, Tulane University Health Sciences
Center, Tulane Center for Aging, Tulane University, New Orleans, LA 70112,
USA, [email protected]
Matt Kaeberlein Department of Pathology, University of Washington, Seattle,
WA 98195-7470, USA, [email protected]
Brian K. Kennedy Buck Institute, Novato, CA 94945, USA,
Thomas B.L. Kirkwood Institute for Ageing and Health, Campus for Ageing and
Vitality, Newcastle University, Newcastle Upon Tyne NE4 5PL, UK,
Andrea Klocker Division of Genetics, Department of Cell Biology, University of
Salzburg, Salzburg, Austria, [email protected]
Vasillios Kotiadis Kent Fungal Group, School of Biosciences, University of Kent,
Canterbury, Kent CT2 7NJ, UK, [email protected]
Peter Laun Division of Genetics, Department of Cell Biology, University of
Salzburg, Salzburg, Austria, [email protected]
Contributors xi
Jane E. Leadsham Kent Fungal Group, School of Biosciences, University of
Kent, Canterbury, Kent, CT2 7NJ, UK, [email protected]
Christiaan Leeuwenburgh Department of Aging and Geriatric Research,
University of Florida, Gainesville, FL 32611-2610, USA, [email protected]
Valter D. Longo Department of Biological Sciences, Andrus Gerontology Center,
University of Southern California, Los Angeles, CA 90089-0191, USA,
Frank Madeo Institute of Molecular Biosciences, University of Graz, Graz,
Austria, [email protected]
Michelle L. Marraffini Department of Anatomy and Cell Biology, University of
Florida, Gainesville, FL 32610-0235, USA, [email protected]
Thomas Nyström Department of Cell and Molecular Biology (CMB), University
of Gothenburg, Göteborg, Sweden, [email protected]
Brady A. Olsen Department of Pathology, University of Washington, Seattle, WA
98195-7470, USA, [email protected]
Heinz D. Osiewacz Faculty of Biosciences, Institute of Molecular Biosciences
and Cluster of Excellence Macromolecular Complexes, Johann Wolfgang Goethe
University, 60438 Frankfurt/Main, Germany, [email protected]
Peter W. Piper Department of Molecular Biology and Biotechnology, The
University of Sheffield, Sheffield S10 2TN, UK, [email protected]
Markus Ralser Max Planck Institute for Molecular Genetics, Berlin, Germany,
Armin Rashidi Institute for Ageing and Health, Campus for Ageing and Vitality,
Newcastle University, Newcastle Upon Tyne NE4 5PL, UK, [email protected]
Mark Rinnerthaler Division of Genetics, Department of Cell Biology,
University of Salzburg, Salzburg, Austria, [email protected]
Sushmita Roy Broad Institute, 7 Cambridge Center, Cambridge, MA 02142,
USA, [email protected]
Kurt W. Runge Department of Molecular Genetics, Lerner Research Institute,
Cleveland Clinic Lerner College of Medicine, Cleveland, OH 44195, USA,
Christian Q. Scheckhuber Faculty of Biosciences, Institute of Molecular
Biosciences and Cluster of Excellence Macromolecular Complexes, Johann
Wolfgang Goethe University, 60438 Frankfurt/Main, Germany,
xii Contributors
Arnold Y. Seo Department of Anatomy and Cell Biology, University of Florida,
Gainesville, FL 32610-0235, USA, [email protected]
Daryl P. Shanley Institute for Ageing and Health, Campus for Ageing and
Vitality, Newcastle University, Newcastle Upon Tyne NE4 5PL, UK,
George L. Sutphin Department of Pathology and the Molecular and Cellular
Biology Program, University of Washington, Seattle, WA 98195-7470, USA,
Martin Weinberger Department of Molecular and Cellular Biology, Roswell
Park Cancer Institute, Buffalo, NY 14222, USA,
M. Werner-Washburne Department of Biology, University of New Mexico,
Albuquerque, NM 87131, USA, [email protected]
Chapter 1
Introduction
Michael Breitenbach, Peter Laun, and S. Michal Jazwinski
Abstract Aging in yeast is now a well researched area with hundreds of new
research and review papers appearing every year. The chapters following in this
book written by some of the leading experts in the field will give an overview of
the most relevant areas of yeast aging. The purpose of this chapter is to give the
newcomer an introduction to the field including some basic technical questions.
Keywords Saccharomyces cerevisiae · Replicative aging · Rejuvenation ·
Asymmetric segregation · Stem cells
General Introductory Remarks
Cells of the budding yeast, S. cerevisiae, have for several decades now been considered as the prototypic eukaryotic cells, ideally suited to study and uncover many
of the basic phenomena of eukaryotic life. This is because of the unrivaled ease
and speed of genetic and molecular genetic analysis in yeast, the small genome size
(12 Mbp), the short doubling time (80 min on complex media), a fully developed
system of sexual reproduction with stable haploid as well as diploid phases enabling
complementation as well as recombination analysis (Dickinson and Schweizer
2004; Stansfield and Stark 2007).
Methods of “reverse genetics” are efficient and easy to handle making yeast one
of only two model organisms of aging where exact gene replacement resulting in
“knock in” strains can be routinely performed. The other cell type where this can
routinely be achieved at present, although with a much higher investment of time and
money, is ES cells of the mouse. In this way, any desired mutation can be introduced
at will in haploid cells in the about 4800 non-essential yeast genes. In the remaining
about 1200 “essential” yeast genes, the same is true, but a severe loss of function
would lead to death, and these mutations have to be kept in a heterozygous state.
Knowing the yeast whole genome sequence and the functional annotation of
yeast genes which has taken place over the last 15 years, and using high throughput
M. Breitenbach (B)
Division of Genetics, Department of Cell Biology,
University of Salzburg, Salzburg, Austria
e-mail: [email protected]
M. Breitenbach et al. (eds.), Aging Research in Yeast, Subcellular Biochemistry 57, 1
DOI 10.1007/978-94-007-2561-4_1, C Springer Science+Business Media B.V. 2012
2 M. Breitenbach et al.
methods and the many publicly available mutant and gene collections, including
cDNA microarrays, whole genome screening procedures have become a powerful
tool for yeast genetic research and have also been used for aging research.
However, of course, not every aspect of eukaryotic life can be modeled in yeast
and an obvious example is development and cell differentiation, which exists in
yeast, but is much more complex in higher multicellular organisms.
The questions which we are asking here are: are the cellular aging processes of
yeast which are described in this book, relevant and similar in mechanism to the
cellular aging processes observed in cultured higher cells and in higher organisms?
What can we learn from yeast aging that is relevant to understand the aging processes of higher organisms? Can this lead to interventions in the aging process of
humans that improve the lifespan and health span of humans? In order to answer
these questions, we must understand the molecular genetic pathways relevant to
aging both in yeast and in higher organisms and we have to compare the two systems
with special emphasis on highly conserved genes playing a role in those pathways. Highly conserved genes, pathways, and external interventions would point
to “public mechanisms of aging”, while such genes and pathways that are found to
influence aging only in a restricted number of organisms, are called “private mechanisms of aging” (Martin et al. 1996). One example for a public mechanism is caloric
restriction (Jiang et al. 2000; Kaeberlein et al. 2005) while an example for a private
mechanism of aging is provided by the extrachromosomal circles of ribosomal DNA
(ERCs) (Sinclair and Guarente 1997) in yeast mother cell-specific aging. The model
systems for organismic aging of higher organisms which are most highly developed
are the mouse (important because it is so closely related to humans), Drosophila
melanogaster, and Caenorhabditis elegans.
Yeast supplies us with two independent aging models which both have similarities to cellular aging processes in humans but have little to do with each other in
terms of the genes which are involved (Laun et al. 2006). The main purpose of this
Introduction is to present these two aging processes, to compare them with each
other, and to evaluate them with regard to the aging processes in the human body
for which they are claimed to be models.
Mother Cell-Specific (Replicative) Aging of Yeast Cells
Individual yeast cells of standard laboratory strains can produce only a limited number, typically 20–30, daughter cells during a lifetime (Mortimer and Johnston 1959).
This process takes about 2–3 days on complex media at 28◦C and is therefore one
of the most rapid aging processes known. The lifespan of a cell is counted in generations (buds, daughter cells produced), but not in calendar time and is actually
independent of calendar time (Müller et al. 1980). During the process, the mother
cell becomes bigger with every generation and accumulates bud scars (Fig. 1.1).
Mother cells change gradually in cycle duration (Egilmez and Jazwinski 1989) and
many other biochemical parameters like ROS content (Laun et al. 2001) and protein
carbonyl content (Aguilaniu et al. 2003), until they reach a final state of senescence