Reliable cell cycle commitment in budding yeast is ensured by signal integration

eLife

Volumn 2015, Issue 4, 2015, Pages

  Liu, Xili ^a,c   Wang, Xin ^a   Yang, Xiaojing ^a   Liu, Sen ^b   Jiang, Lingli ^a   Qu, Yimiao ^a   Hu, Lufeng ^a   Ouyang, Qi ^a   Tang, Chao ^a  

^a PEKING UNIVERSITY   (China)

^b CHINA THREE GORGES UNIVERSITY   (China)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 3; G1 PHASE SPECIFIC TRANSCRIPTIONAL REPRESSOR; MESSENGER RNA; PEPTIDES AND PROTEINS; PLASMID VECTOR; UNCLASSIFIED DRUG; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CELL CYCLE; CELL GROWTH; CELL SIZE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DATA ANALYSIS; DECISION MAKING; ENZYME ACTIVITY; FEEDBACK SYSTEM; FLOW RATE; GROWTH RATE; INTRACELLULAR SIGNALING; MICROFLUIDIC ANALYSIS; NONHUMAN; NUTRIENT; OPEN READING FRAME; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; STOCHASTIC MODEL; TIME-LAPSE VIDEO MICROSCOPY; YEAST; BUDDING YEAST; CELL CYCLE G1 PHASE; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SIGNAL TRANSDUCTION; TIME FACTOR;

ANIMALIA; SACCHAROMYCETALES;

CELL CYCLE; G1 PHASE; SACCHAROMYCES CEREVISIAE PROTEINS; SACCHAROMYCETALES; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 85006299242     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.03977     Document Type: Article

References (64)

1. Arava, Yoav, Yulei Wang, John D Storey, Chih Long Liu, Patrick O Brown, and Daniel Herschlag. 2003. “Genome-Wide Analysis of mRNA Translation Profiles in Saccharomyces cerevisiae.” Proceedings of the National Academy of Sciences of the United States of America 100 (7) (April 1): 3889–94. doi:10.1073/pnas.0635171100.
2. Avraham, Nurit, Ilya Soifer, Miri Carmi, and Naama Barkai. 2013. “Increasing Population Growth by Asymmetric Segregation of a Limiting Resource during Cell Division.” Molecular Systems Biology 9 (656) (January): 656. doi:10.1038/msb.2013.13.
3. Balázsi, Gábor, Alexander van Oudenaarden, and James J Collins. 2011. “Cellular Decision Making and Biological Noise: From Microbes to Mammals.” Cell 144 (6) (March 18): 910–25. doi:10.1016/j.cell.2011.01.030.
4. Bishop, AC, JA Ubersax, DT Petsch, DP Matheos, NS Gray, J Blethrow, E Shimizu, et al. 2000. “A Chemical Switch for Inhibitor-Sensitive Alleles of Any Protein Kinase.” Nature 407: 395–401. doi:10.1038/35030148.
5. Bogacz, Rafal, Eric Brown, Jeff Moehlis, Philip Holmes, and Jonathan D Cohen. 2006. “The Physics of Optimal Decision Making: A Formal Analysis of Models of Performance in Two-Alternative Forced-Choice Tasks.” Psychological Review 113 (4) (October): 700–65. doi:10.1037/0033-295X.113.4.700.
6. Bowman, Nicholas E, Konrad P Kording, and Jay A Gottfried. 2012. “Temporal Integration of Olfactory Perceptual Evidence in Human Orbitofrontal Cortex.” Neuron 75 (5) (September 6): 916–27. doi:10.1016/j.neuron.2012.06.035.
7. Charvin, Gilles, Frederick R Cross, and Eric D Siggia. 2008. “A Microfluidic Device for Temporally Controlled Gene Expression and Long-Term Fluorescent Imaging in Unperturbed Dividing Yeast Cells.” PloS One 3 (1) (January): e1468. doi:10.1371/journal.pone.0001468.
8. Charvin, Gilles, Catherine Oikonomou, and ED Siggia. 2010. “Origin of Irreversibility of Cell Cycle Start in Budding Yeast.” PLoS Biology 8 (1) (January): e1000284. doi:10.1371/journal.pbio.1000284.
9. Chen, KC, Laurence Calzone, A Csikasz-Nagy, Frederick R Cross, Bela Novak, and John J Tyson. 2004. “Integrative Analysis of Cell Cycle Control in Budding Yeast.” Molecular Biology of the Cell 15 (August): 3841–3862. doi:10.1091/mbc.E03.
10. Chivian, Dylan. 2006. “Homology Modeling Using Parametric Alignment Ensemble Generation with Consensus and Energy-Based Model Selection.” Nucleic Acids Research 34 (17) (January): e112. doi:10.1093/nar/gkl480.
11. Colomina, Neus, Eloi Garı, and Emili Verge. 2007. “Cyclin Cln3 Is Retained at the ER and Released by the J Chaperone Ydj1 in Late G1 to Trigger Cell Cycle Entry.” Molecular Cell 26: 649–662. doi:10.1016/j.molcel.2007.04.023.
12. Costanzo, Michael, Joy L Nishikawa, Xiaojing Tang, Jonathan S Millman, Oliver Schub, Kevin Breitkreuz, Danielle Dewar, Ivan Rupes, Brenda Andrews, and Mike Tyers. 2004. “CDK Activity Antagonizes Whi5, an Inhibitor of G1/S Transcription in Yeast.” Cell 117 (7) (June 25): 899–913. doi:10.1016/j.cell.2004.05.024.
13. Cross, Frederick R, and Christa M Blake. 1993. “The Yeast Cln3 Protein Is an Unstable Activator of Cdc28.” Molecular and Cellular Biology 13 (6): 3266–3271. doi:10.1128/MCB.13.6.3266.Updated.
14. Di Talia, Stefano, Jan M Skotheim, James M Bean, Eric D Siggia, Frederick R Cross, and Stefano Di Talia. 2007. “The Effects of Molecular Noise and Size Control on Variability in the Budding Yeast Cell Cycle.” Nature 448 (7156) (August 23): 947–51. doi:10.1038/nature06072.
15. Doncic, Andreas, and Jan M Skotheim. 2013. “Feedforward Regulation Ensures Stability and Rapid Reversibility of a Cellular State.” Molecular Cell 50 (6) (June 27): 856–68. doi:10.1016/j.molcel.2013.04.014.
16. Elowitz, Michael B, Arnold J Levine, Eric D Siggia, and Peter S Swain. 2002. “Stochastic Gene Expression in a Single Cell.” Science (New York, N.Y.) 297 (5584) (August 16): 1183–6. doi:10.1126/science.1070919.
17. Ferrezuelo, Francisco, Neus Colomina, Alida Palmisano, Eloi Garí, Carme Gallego, Attila Csikász-Nagy, and Martí Aldea. 2012. “The Critical Size Is Set at a Single-Cell Level by Growth Rate to Attain Homeostasis and Adaptation.” Nature Communications 3 (August 21): 1012. doi:10.1038/ncomms2015.
18. Gallego, Carme, E Garí, Neus Colomina, Enrique Herrero, M Aldea, and Eloi Garı. 1997. “The Cln3 Cyclin Is down-Regulated by Translational Repression and Degradation during the G1 Arrest Caused by Nitrogen Deprivation in Budding Yeast.” The EMBO Journal 16 (23) (December 1): 7196–206. doi:10.1093/emboj/16.23.7196.
19. Gillespie, Daniel T. 1976. “A General Method for Numerically Simulating the Stochastic Time Evolution of Coupled Chemical Reactions.” Journal of Computational Physics 22 (4) (December): 403–434. doi:10.1016/0021-9991(76)90041-3.
20. Ginalski, K., a. Elofsson, D. Fischer, and L. Rychlewski. 2003. “3D-Jury: A Simple Approach to Improve Protein Structure Predictions.” Bioinformatics 19 (8) (May 22): 1015–1018. doi:10.1093/bioinformatics/btg124.
21. Goldstein, A L, and J H McCusker. 1999. “Three New Dominant Drug Resistance Cassettes for 653 Gene Disruption in Saccharomyces cerevisiae.” Yeast (Chichester, England) 15 (14) (October): 1541–53. doi:10.1002/(SICI)1097-0061(199910)15:14<1541::AID655YEA476>3.0.CO;2-K.
22. Gregor, Thomas, David W Tank, Eric F Wieschaus, and William Bialek. 2007. “Probing the Limits to Positional Information.” Cell 130 (1) (July 13): 153–64. doi:10.1016/j.cell.2007.05.025.
23. Hall, Duane D, David D Markwardt, Fereshteh Parviz, and Warren Heideman. 1998. “Regulation of the Cln3 – Cdc28 Kinase by cAMP in Saccharomyces cerevisiae.” The EMBO Journal 17 (15): 4370–4378. doi: 10.1093/emboj/17.15.4370
24. Hartwell, L H, J Culotti, J R Pringle, and B J Reid. 1974. “Genetic Control of the Cell Division Cycle in Yeast.” Science (New York, N.Y.) 183 (4120) (January 11): 46–51. doi: 10.1126/science.183.4120.46
25. Huh, WK, JV Falvo, LC Gerke, AS Carroll, RW Howson, J S Weissman, and Erin K O’Shea. 2003. “Global Analysis of Protein Localization in Budding Yeast.” Nature 425 (6959) (October 16): 686–91. doi:10.1038/nature02026.
26. Jansen, Gregor, Cunle Wu, Babette Schade, David Y Thomas, and Malcolm Whiteway. 2005. “Drag&Drop Cloning in Yeast.” Gene 344 (January 3): 43–51. doi:10.1016/j.gene.2004.10.016.
27. Johnston, G C, J R Pringle, and L H Hartwell. 1977. “Coordination of Growth with Cell Division in the Yeast Saccharomyces cerevisiae.” Experimental Cell Research 105 (1): 79–98. doi: 10.1016/0014-4827(77)90154-9
28. Jorgensen, Paul, and NP Edgington. 2007. “The Size of the Nucleus Increases as Yeast Cells Grow.” Molecular Biology of the Cell 18 (September): 3523–3532. doi:10.1091/mbc.E06.
29. Jorgensen, Paul, and Mike Tyers. 2004. “How Cells Coordinate Growth and Division.” Current Biology: CB 14 (23) (December 14): R1014–27. doi:10.1016/j.cub.2004.11.027.
30. Kortemme, Tanja, and David Baker. 2002. “A Simple Physical Model for Binding Energy Hot Spots in Protein-Protein Complexes.” Proceedings of the National Academy of Sciences of the United States of America 99 (22) (October 29): 14116–21. doi:10.1073/pnas.202485799.
31. Kubota, Mie, Katsuhiko Mikoshiba, and Atsushi Miyawaki. 2002. “A Variant of Yellow Fluorescent Protein with Fast and Efficient Maturation for Cell-Biological Applications.” Nature 20 (1) (January): 87–90. doi:10.1038/nbt0102-87.
32. Laabs, Tracy L, David D Markwardt, Matthew G Slattery, Laura L Newcomb, David J Stillman, and Warren Heideman. 2003. “ACE2 Is Required for Daughter Cell-Specific G1 Delay in Saccharomyces cerevisiae.” Proceedings of the National Academy of Sciences of the United States of America 100 (18) (September 2): 10275–80. doi:10.1073/pnas.1833999100.
33. Lau, Kai-yeung. 2009. “Elucidating the Systems Design Principles of the Yeast Cell Cycle Network (doctoral Dissertation).” University of California, San Francisco.
34. Li, Zhiyuan, Ming Ni, Jikun Li, Yuping Zhang, Qi Ouyang, and Chao Tang. 2010. “Decision Making of the p53 Network: Death by Integration.” Journal of Theoretical Biology 271 (1) (December 3): 205–211. doi:10.1016/j.jtbi.2010.11.041.
35. Liku, ME, VQ Nguyen, AW Rosales, K Irie, and J J Li. 2005. “CDK Phosphorylation of a Novel NLS-NES Module Distributed between Two Subunits of the Mcm2-7 Complex Prevents Chromosomal Rereplication.” Molecular Biology of the 16 (October): 5026–5039. doi:10.1091/mbc.E05.
36. Longtine, M S, A McKenzie, D J Demarini, N G Shah, A Wach, A Brachat, P Philippsen, and J R Pringle. 1998. “Additional Modules for Versatile and Economical PCR-Based Gene Deletion and Modification in Saccharomyces cerevisiae.” Yeast (Chichester, England) 14 (10) (July): 953–61. doi:10.1002/(SICI)1097-0061(199807)14:10<953::AID701YEA293>3.0.CO;2-U.
37. McInerny, C J, J F Partridge, G E Mikesell, D P Creemer, and L L Breeden. 1997. “A Novel Mcm1-Dependent Element in the SWI4, CLN3, CDC6, and CDC47 Promoters Activates M/G1-Specific Transcription.” Genes & Development 11 (10) (May 15): 1277–1288. doi:10.1101/gad.11.10.1277.
38. Menoyo, S, N Ricco, S Bru, S Hernández-Ortega, X Escoté, M Aldea, and J Clotet. 2013. “Phosphate-Activated Cyclin-Dependent Kinase Stabilizes G1 Cyclin to Trigger Cell Cycle Entry.” Molecular and Cellular Biology 33 (7) (April): 1273–84. doi:10.1128/MCB.01556-12.
39. Miller, Mary E, Frederick R Cross, Alison L Groeger, and Katherine L Jameson. 2005. “Identification of Novel and Conserved Functional and Structural Elements of the G1 Cyclin Cln3 Important for Interactions with the CDK Cdc28 in Saccharomyces cerevisiae.” Yeast (Chichester, England) 22 (13) (October 15): 1021–36. doi:10.1002/yea.1292.
40. Mumberg, D, R Müller, and M Funk. 1995. “Yeast Vectors for the Controlled Expression of Heterologous Proteins in Different Genetic Backgrounds.” Gene 156 (1) (April 14): 119–22. doi: 10.1016/0378-1119(95)00037-7
41. Parviz, F, D D Hall, D D Markwardt, and W Heideman. 1998. “Transcriptional Regulation of CLN3 Expression by Glucose in Saccharomyces cerevisiae.” Journal of Bacteriology 180 (17) (September): 4508–15.
42. Polymenis, M., and E. V. Schmidt. 1997. “Coupling of Cell Division to Cell Growth by Translational Control of the G1 Cyclin CLN3 in Yeast.” Genes & Development 11 (19) (October 1): 2522–2531. doi:10.1101/gad.11.19.2522.
43. Raser, Jonathan M, and Erin K O’Shea. 2004. “Control of Stochasticity in Eukaryotic Gene Expression.” Science (New York, N.Y.) 304 (5678) (June 18): 1811–4. doi:10.1126/science.1098641.
44. Schneider, Brandt L, Jian Zhang, J Markwardt, George Tokiwa, Tom Volpe, Sangeet Honey, and Bruce Futcher. 2004. “Growth Rate and Cell Size Modulate the Synthesis of, and Requirement for, G1 -Phase Cyclins at Start.” Molecular and Cellular Biology 24 (24): 10802–10813. doi:10.1128/MCB.24.24.10802.
45. Schulman, BA, DL Lindstrom, and E Harlow. 1998. “Substrate Recruitment to Cyclin-Dependent Kinase 2 by a Multipurpose Docking Site on Cyclin A.” Proceedings of the National Academy of Sciences of the United States of America 95 (September): 10453–10458.
46. Shou, W, JH Seol, and A Shevchenko. 1999. “Exit from Mitosis Is Triggered by Tem1-Dependent Release of the Protein Phosphatase Cdc14 from Nucleolar RENT Complex.” Cell 97 (2) (April): 233–44.
47. Sikorski, RS, and Philip Hieter. 1989. “A System of Shuttle Vectors and Yeast Host Strains Designed for Efficient Manipulation of DNA in Saccharomyces cerevisiae.” Genetics 122: 19–27.
48. Skotheim, Jan M, Stefano Di Talia, Eric D Siggia, Frederick R Cross, and Stefano Di Talia. 2008. “Positive Feedback of G1 Cyclins Ensures Coherent Cell Cycle Entry.” Nature 454 (7202) (July 17): 291–6. doi:10.1038/nature07118.
49. Sreekrishna, K, and R C Dickson. 1985. “Construction of Strains of Saccharomyces cerevisiae That Grow on Lactose.” Proceedings of the National Academy of Sciences of the United States of America 82 (23) (December): 7909–13.
50. Stevenson, L F, B K Kennedy, and E Harlow. 2001. “A Large-Scale Overexpression Screen in Saccharomyces cerevisiae Identifies Previously Uncharacterized Cell Cycle Genes.” Proceedings of the National Academy of Sciences of the United States of America 98 (7) (March 27): 3946–51. doi:10.1073/pnas.051013498.
51. Taberner, Francisco J, Inmaculada Quilis, and J Carlos Igual. 2009. “Spatial Regulation of the Start Repressor Whi5.” Cell Cycle (Georgetown, Tex.) 8 (18) (September 15): 3010–8. doi: 10.4161/cc.8.18.9621
52. Talia, Stefano Di, and Eric F Wieschaus. 2012. “Short-Term Integration of Cdc25 Dynamics Controls Mitotic Entry during Drosophila Gastrulation.” Developmental Cell 22 (4): 763–774. doi:10.1016/j.devcel.2012.01.019.
53. Tian, Yuan, Chunxiong Luo, Yuheng Lu, and C Tang. 2012. “Cell Cycle Synchronization by Nutrient Modulation.” Integr. Biol. 328–334. doi:10.1039/c2ib00083k.
54. Turner, Jonathan J., Jennifer C. Ewald, and Jan M. Skotheim. 2012. “Cell Size Control in Yeast.” Current Biology 22 (9) (May): R350–R359. doi:10.1016/j.cub.2012.02.041.
55. Tyers, M, G Tokiwa, and B Futcher. 1993. “Comparison of the Saccharomyces cerevisiae G1 Cyclins: Cln3 May Be an Upstream Activator of Cln1, Cln2 and Other Cyclins.” The EMBO Journal 12 (5) (May): 1955–68.
56. Tyers, M, G Tokiwa, R Nash, and B Futcher. 1992. “The Cln3-Cdc28 Kinase Complex of S. cerevisiae Is Regulated by Proteolysis and Phosphorylation.” The EMBO Journal 11 (5) (May): 1773–84.
57. Tyers, Mike, and Bruce Futcher. 1993. “Farl and Fus3 Link the Mating Pheromone Signal Transduction Pathway to Three G1-Phase Cdc28 Kinase Complexes.” Molecular and Cellular Biology 13 (9): 5659–5669. doi:10.1128/MCB.13.9.5659.Updated.
58. Visintin, R, K Craig, E S Hwang, S Prinz, M Tyers, and A Amon. 1998. “The Phosphatase Cdc14 Triggers Mitotic Exit by Reversal of Cdk-Dependent Phosphorylation.” Molecular Cell 2 (6) (December): 709–18. doi: 10.1016/S1097-2765(00)80286-5
59. Wang, Chu, Philip Bradley, and David Baker. 2007. “Protein-Protein Docking with Backbone Flexibility.” Journal of Molecular Biology 373 (2) (October 19): 503–19. doi:10.1016/j.jmb.2007.07.050.
60. Wang, Hongyin, Eloi Garí, Emili Vergés, Carme Gallego, and Martí Aldea. 2004. “Recruitment of Cdc28 by Whi3 Restricts Nuclear Accumulation of the G1 Cyclin-Cdk Complex to Late G1.” The EMBO Journal 23 (1) (January 14): 180–90. doi:10.1038/sj.emboj.7600022.
61. Wijnen, Herman. 1999. “Genetic Analysis of the Shared Role of CLN3 and BCK2 at the G1-S Transition in Saccharomyces cerevisiae.” Genetics 153 (3): 1131–43. http://www.genetics.org/content/153/3/1131.short.
62. Xiong, Wen, and James E Ferrell. 2003. “A Positive-Feedback-Based Bistable ‘Memory Module’ That Governs a Cell Fate Decision.” Nature 426 (November): 460–465. doi:10.1038/nature02119.1.
63. Yaglom, J, M H Linskens, S Sadis, D M Rubin, B Futcher, and D Finley. 1995. “p34Cdc28-Mediated Control of Cln3 Cyclin Degradation.” Molecular and Cellular Biology 15 (2): 731–741.
64. Yang, Xiaojing, Kai-Yeung Lau, Volkan Sevim, and Chao Tang. 2013. “Design Principles of the Yeast G1/S Switch.” PLoS Biology 11 (10) (October): e1001673. doi:10.1371/journal.pbio.1001673.