Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Logo for

Science 302 (5647): 1038-1041

Copyright © 2003 by the American Association for the Advancement of Science

Suspended Animation in C. elegans Requires the Spindle Checkpoint

Todd G. Nystul,1,2* Jesse P. Goldmark,1,2* Pamela A. Padilla,3* Mark B. Roth1{dagger}

Abstract: In response to environmental signals such as anoxia, many organisms enter a state of suspended animation, an extreme form of quiescence in which microscopically visible movement ceases. We have identified a gene, san-1, that is required for suspended animation in Caenorhabditis elegans embryos. We show that san-1 functions as a spindle checkpoint component in C. elegans. During anoxia-induced suspended animation, embryos lacking functional SAN-1 or a second spindle checkpoint component, MDF-2, failed to arrest the cell cycle, exhibited chromosome missegregation, and showed reduced viability. These data provide a model for how a dynamic biological process is arrested in suspended animation.

1 Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA 98109, USA.
2 Molecular and Cellular Biology Program, University of Washington, Seattle, WA 98109, USA.
3 Department of Biological Sciences, University of North Texas, Denton, TX 76203, USA.

Back to Top

* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: mroth{at}

Proper Cyclin B3 Dosage Is Important for Precision of Metaphase-to-Anaphase Onset Timing in Caenorhabditis elegans.
M. Tarailo-Graovac and N. Chen (2012)
g3 2, 865-871
   Abstract »    Full Text »    PDF »
Dissection of the NUP107 nuclear pore subcomplex reveals a novel interaction with spindle assembly checkpoint protein MAD1 in Caenorhabditis elegans.
E. Rodenas, C. Gonzalez-Aguilera, C. Ayuso, and P. Askjaer (2012)
Mol. Biol. Cell 23, 930-944
   Abstract »    Full Text »    PDF »
Cdc48/p97-Ufd1-Npl4 antagonizes Aurora B during chromosome segregation in HeLa cells.
G. Dobrynin, O. Popp, T. Romer, S. Bremer, M. H. A. Schmitz, D. W. Gerlich, and H. Meyer (2011)
J. Cell Sci. 124, 1571-1580
   Abstract »    Full Text »    PDF »
Regulation of Anoxic Death in Caenorhabditis elegans by Mammalian Apoptosis Signal-Regulating Kinase (ASK) Family Proteins.
T. Hayakawa, K. Kato, R. Hayakawa, N. Hisamoto, K. Matsumoto, K. Takeda, and H. Ichijo (2011)
Genetics 187, 785-792
   Abstract »    Full Text »    PDF »
Functional Redundancy of Paralogs of an Anaphase Promoting Complex/Cyclosome Subunit in Caenorhabditis elegans Meiosis.
K. K. Stein, J. E. Nesmith, B. D. Ross, and A. Golden (2010)
Genetics 186, 1285-1293
   Abstract »    Full Text »    PDF »
Suspended Animation Extends Survival Limits of Caenorhabditis elegans and Saccharomyces cerevisiae at Low Temperature.
K. Chan, J. P. Goldmark, and M. B. Roth (2010)
Mol. Biol. Cell 21, 2161-2171
   Abstract »    Full Text »    PDF »
NPP-16/Nup50 Function and CDK-1 Inactivation Are Associated with Anoxia-induced Prophase Arrest in Caenorhabditis elegans.
V. A. Hajeri, B. A. Little, M. L. Ladage, and P. A. Padilla (2010)
Mol. Biol. Cell 21, 712-724
   Abstract »    Full Text »    PDF »
Protection of C. elegans from Anoxia by HYL-2 Ceramide Synthase.
V. Menuz, K. S. Howell, S. Gentina, S. Epstein, I. Riezman, M. Fornallaz-Mulhauser, M. O. Hengartner, M. Gomez, H. Riezman, and J.-C. Martinou (2009)
Science 324, 381-384
   Abstract »    Full Text »    PDF »
Systematic Identification of Gene Activities Promoting Hypoxic Death.
M. E. Mabon, X. Mao, Y. Jiao, B. A. Scott, and C. M. Crowder (2009)
Genetics 181, 483-496
   Abstract »    Full Text »    PDF »
Systematic Analysis in Caenorhabditis elegans Reveals that the Spindle Checkpoint Is Composed of Two Largely Independent Branches.
A. Essex, A. Dammermann, L. Lewellyn, K. Oegema, and A. Desai (2009)
Mol. Biol. Cell 20, 1252-1267
   Abstract »    Full Text »    PDF »
SPDL-1 functions as a kinetochore receptor for MDF-1 in Caenorhabditis elegans.
T. G. Yamamoto, S. Watanabe, A. Essex, and R. Kitagawa (2008)
J. Cell Biol. 183, 187-194
   Abstract »    Full Text »    PDF »
Anoxia-Induced Suspended Animation in Budding Yeast as an Experimental Paradigm for Studying Oxygen-Regulated Gene Expression.
K. Chan and M. B. Roth (2008)
Eukaryot. Cell 7, 1795-1808
   Abstract »    Full Text »    PDF »
Synthetic Lethal Interactions Identify Phenotypic "Interologs" of the Spindle Assembly Checkpoint Components.
M. Tarailo, S. Tarailo, and A. M. Rose (2007)
Genetics 177, 2525-2530
   Abstract »    Full Text »    PDF »
The AAA-ATPase FIGL-1 controls mitotic progression, and its levels are regulated by the CUL-3MEL-26 E3 ligase in the C. elegans germ line.
S. Luke-Glaser, L. Pintard, M. Tyers, and M. Peter (2007)
J. Cell Sci. 120, 3179-3187
   Abstract »    Full Text »    PDF »
Rapid effects of acute anoxia on spindle kinetochore interactions activate the mitotic spindle checkpoint.
R. Pandey, S. Heeger, and C. F. Lehner (2007)
J. Cell Sci. 120, 2807-2818
   Abstract »    Full Text »    PDF »
Suppressors of Spindle Checkpoint Defect (such) Mutants Identify New mdf-1/MAD1 Interactors in Caenorhabditis elegans.
M. Tarailo, R. Kitagawa, and A. M. Rose (2007)
Genetics 175, 1665-1679
   Abstract »    Full Text »    PDF »
Components of the Spindle Assembly Checkpoint Regulate the Anaphase-Promoting Complex During Meiosis in Caenorhabditis elegans.
K. K. Stein, E. S. Davis, T. Hays, and A. Golden (2007)
Genetics 175, 107-123
   Abstract »    Full Text »    PDF »
Glyceraldehyde-3-Phosphate Dehydrogenase Mediates Anoxia Response and Survival in Caenorhabditis elegans.
A. R. Mendenhall, B. LaRue, and P. A. Padilla (2006)
Genetics 174, 1173-1187
   Abstract »    Full Text »    PDF »
Assessing physiological complexity.
W. W. Burggren and M. G. Monticino (2005)
J. Exp. Biol. 208, 3221-3232
   Abstract »    Full Text »    PDF »
A Spindle Checkpoint Functions during Mitosis in the Early Caenorhabditis elegans Embryo.
S. E. Encalada, J. Willis, R. Lyczak, and B. Bowerman (2005)
Mol. Biol. Cell 16, 1056-1070
   Abstract »    Full Text »    PDF »
The Caenorhabditis elegans Kinetochore Reorganizes at Prometaphase and in Response to Checkpoint Stimuli.
J. H. Stear and M. B. Roth (2004)
Mol. Biol. Cell 15, 5187-5196
   Abstract »    Full Text »    PDF »
Carbon monoxide-induced suspended animation protects against hypoxic damage in Caenorhabditis elegans.
T. G. Nystul and M. B. Roth (2004)
PNAS 101, 9133-9136
   Abstract »    Full Text »    PDF »
A Werner syndrome protein homolog affects C. elegans development, growth rate, life span and sensitivity to DNA damage by acting at a DNA damage checkpoint.
S.-J. Lee, J.-S. Yook, S. M. Han, and H.-S. Koo (2004)
Development 131, 2565-2575
   Abstract »    Full Text »    PDF »
J. H. Stillman (2004)
J. Exp. Biol. 207, vi
   Full Text »    PDF »
Worms delay in deep sleep.
W. A. Wells (2003)
J. Cell Biol. 163, 929
   Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882