Systems level modeling of the cell cycle using budding yeast

Cancer Informatics

Volumn 3, Issue , 2007, Pages 367-380

  Ingalls, B P ^a   Duncker, B P ^a   Kim, D R ^a   McConkey, B J ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Budding yeast; Cell cycle; Dynamic modeling; Proteomics

Indexed keywords

CELL CYCLE PROTEIN; PROTEOME; TRANSCRIPTOME;

CANCER CHEMOTHERAPY; CANCER RESEARCH; CELL CYCLE; CELL CYCLE PROGRESSION; CELL DIVISION; CYTOKINESIS; DNA REPLICATION; DRUG TARGETING; FLUORESCENCE RESONANCE ENERGY TRANSFER; GEL ELECTROPHORESIS; GENE DELETION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; GENOME; NONHUMAN; NUCLEAR DIVISION; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEOMICS; REVIEW; SACCHAROMYCES CEREVISIAE; SYSTEMS BIOLOGY; TANDEM MASS SPECTROMETRY; YEAST; BUDDING YEAST; FUNGAL CELL; GENE SEQUENCE; INFORMATION PROCESSING; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; MOLECULAR MODEL; QUANTITATIVE ANALYSIS; SEQUENCE ANALYSIS;

EID: 49649116352     PISSN: 11769351     EISSN: 11769351     Source Type: Journal    
DOI: 10.1177/117693510700300020     Document Type: Review

References (118)

1. Alarcón, T., Byrne, H.M. and Maini, P.K. 2004. A mathematical model of the effects of hypoxia on the cell-cycle of normal and cancer cells. Journal of Theoretical Biology, 229:395-411.
2. 1/S transition. Bulletin of Mathematical Biology, 69:197-214.
3. Amberg, D.C., Burke, D.J. and Strathern, J.N. 2005. Methods in yeast genetics, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
4. Audhya, A., Loewith, R., Parsons, A.B. et al. 2004. Genome-wide lethality screen identifies new P14, 5P2 effectors that regulate the actin cytoskeleton. EMBO Journal, 23:3747-57.
5. 1/S network. PLOS Computational Biology, 3:e64.
6. Battogtokh, D., Asch, D.K., Case, M.E., Arnold, J. and Schüttler, H.-B. 2002. An ensemble method for identifying regulatory circuits with special reference to the qa gene cluster of Neurospora crassa. Proc. Natl. Acad. Sci. USA., 99:16904-9.
7. Battogtokh, D. and Tyson, J.J. 2004. Bifurcation analysis of a model of the budding yeast cell cycle. Chaos, 14:653-61.
8. Brown, K.S. and Sethna, J.P. 2003. Statistical mechanical approaches to models with many poorly known parameters. Physical Review E, 68:021904.
9. Brown, K.S., Hill, C.C., Calero, G.A. et al. 2004. The statistical mechanics of complex signaling networks: nerve growth factor signaling. Physical Biology, 1:184-95.
10. Byrne, H.M., Alarcon, T., Owen, M.R., Webb, S.D. and Maini, P.K. 2006. Modelling aspects of cancer dynamics: a review. Philosophical Transactions of the Royal Society. A, 364:1563-78.
11. Chang, M., Bellaoui, M., Zhang, C. et al. 2005. RMI1/NCE4, a suppressor of genome instability, encodes a member of the RecQ helicase/Topo III complex. EMBO Journal, 24:2024-33.
12. Chaplain, M.A.J., McDougall, S.R. and Anderson, A.R.A. 2006. Mathematical modeling of tumor-induced angiogenesis. Annu. Rev. Biomed. Eng., 8:233-57.
13. Chassagnole, C., Jackson, R.C., Hussain, N. et al. 2006. Using a mammalian cell cycle simulation to interpret differential kinase inhibition in antitumour pharmaceutical development. BioSystems, 83:91-7.
14. Chen, H.-C., Lee, H.-C., Lin, T.-Y., Li, W.-H. and Chen, B.-S. 2004. Quantitative characterization of the transcriptional regulatory network in the yeast cell cycle. Bioinformatics, 20:1914-27.
15. Chen, K.C., Csikasz-Nagy, A., Gyorffy, B., Val, J., Novak, B. and Tyson, J.J. 2000. Kinetic analysis of a molecular model of the budding yeast cell cycle. Molecular Biology of the Cell, 11:369-91.
16. Chen, K.C., Calzone, L., Csikasz-Nagy, A., Cross, F.R., Novak, B. and Tyson, J.J. 2004. Integrative analysis of cell cycle control in budding yeast. Molecular Biology of the Cell, 15:3841-62.
17. Cho, R.J., Campbell, M.J., Winzeler, E.A. et al. 1998. A genome-wide transcriptional analysis of the mitotic cell cycle. Molecular Cell, 2:65-73.
18. Ciliberto, A., Novak, B. and Tyson, J.J. 2003. Mathematical model of the morphogenesis checkpoint in budding yeast. Journal of Cell. Biology, 163:1243-54.
19. Cretich, M., Damin, F., Pirri, G. and Chiari, M. 2006. Protein and peptide arrays: recent trends and new directions. Biomolecular engineering, 23:77-88.
20. Cross, F.R., Archambault, V., Miller, M. and Klovstad, M. 2002. Testing a mathematical model of the yeast cell cycle. Molecular Biology of the Cell, 13:52-70.
21. Cross, F.R. 2003. Two redundant oscillatory mechanisms in the yeast cell cycle. Developmental Cell, 4:741-52.
22. Csikász-Nagy, A., Battogtokh, D., Chen, K.C., Novak, B. and Tyson, J.J. 2006. Analysis of a generic model of eukaryotic cell-cycle regulation. Biophysical Journal, 90:4361-79.
23. Culotti, J. and Hartwell, L.H. 1971. Genetic control of the cell division cycle in yeast. 3. Seven genes controlling nuclear division. Experimental Cell. Research, 67:389-401.
24. Davierwala, A.P., Haynes, J., Li, Z., Brost, R.L. et al. 2005. The synthetic genetic interaction spectrum of essential genes. Nature Genetics, 37:1147-52.
25. Flory, M.R., Lee, H., Bonneau, R. et al. 2006. Quantitative proteomic analysis of the budding yeast cell cycle using acid-cleavable isotope-coded affinity tag reagents. Proteomics, 6:6146-57.
26. Gavin, A.-C., Bosche, M., Krause, R. et al. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature, 415:141-7.
27. Gavin, A.-C., Aloy, P., Grandi, P. et al. 2006. Proteome survey reveals modularity of the yeast cell machinery. Nature, 440:631-6.
28. Gembitsky, D.S., Lawlor, K., Jacovina, A., Yaneva, M. and Tempst, P. 2004. A prototype antibody microarray platform to monitor changes in protein tyrosine phosphorylation. Molecular and Cellular Proteomics, 3:1102-18.
29. Ghaemmaghami, S., Huh, W.-K., Bower, K. et al. 2003. Global analysis of protein expression in yeast. Nature, 425:737-41.
30. Gingras, A.-G., Aebersold, R. and Raught, B. 2005. Advances in protein complex analysis using mass spectrometry. Journal of Physiology, 563:11-21.
31. Goehring, A.S., Mitchell, D.A., Tong, A.H.Y. et al. 2003. Synthetic lethal analysis implicates Ste20p, a p21-activated protein kinase, in polarisome activation. Molecular Biology of the Cell, 14:1501-16.
32. Goffeau, A., Barrell, B.G., Bussey, H. et al. 1996. Life with 6000 genes. Science, 274:546-67.
33. Goldbeter, A. 1991. A minimal cascade model for the mitotic oscillator involving cyclin and cdc2 kinase. Proc. Natl. Acad. Sci. USA., 88:9107-11.
34. Goldbeter, A. 1996. Biochemical Oscillations and Cellular Rhythms, Cambridge University Press, Cambridge, UK.
35. Graumann, J., Dunipace, L.A., Seol, J.H. et al. 2004. Applicability of tandem affinity purification MudPIT to pathway proteomics in yeast. Molecular and Cellular Proteomics, 3:226-37.
36. Gruhler, A., Olsen, J.V., Mohammed, S. et al. 2005. Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Molecular and Cellular Proteomics, 4:310-27.
37. Gygi, S.P., Rist, B., Gerber, S.A. et al. 1999. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nature Biotechnology, 17:994-9.
38. Hartwell, L.H., Culotti, J. and Reid, B. 1970. Genetic control of the cell-division cycle in yeast, I. Detection of mutants. Proc. Natl. Acad. Sci. USA., 66:352-9.
39. Hartwell, L.H. 1971a. Genetic control of the cell division cycle in yeast. II. Genes controlling DNA replication and its initiation. Journal of Molecular Biology, 59:183-94.
40. Hartwell, L.H. 1971b. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Experimental Cell Research, 69:265-76.
41. Ho, Y., Gruhler, A., Heilbut, A. et al. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature, 415:180-3.
42. Huh, W.K., Falvo, J.V., Gerke, L.C. et al. 2003. Global analysis of protein localization in budding yeast. Nature, 425:686-91.
43. Hyver, C. and Le Guyader, H. 1990. MPF and cyclin: modelling of the cell cycle minimum oscillator. BioSystems, 24:85-90.
44. Ideker, T., Thorsson, V., Ranish, J.A. et al. 2001. Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science, 292:929-34.
45. Ingolia, N.T. and Murray, A.W. 2004. The ups and downs of modeling the cell cycle. Current Biology, 14:R771-R777.
46. Ito, T., Chiba, T., Ozawa, R. et al. 2001. A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA., 98:4569-74.
47. Julka, S. and Regnier, F. 2004. Quantification in proteomics through stable isotope coding: a review. Journal of Proteome Research, 3:350-63.
48. Jorgensen, P., Nelson, B., Robinson, M.D. et al. 2002. High-resolution genetic mapping with ordered arrays of Saccharomyces cerevisiae deletion mutants. Genetics, 162:1091-9.
49. Kauffman, S. and Wille, J.J. 1975. The mitotic oscillator in Physarum polycephalum. Journal of Theoretical Biology, 55:47-93.
50. Kelly, T.J. and Brown, G.W. 2000. Regulation of chromosome replication. Annual Review of Biochemistry, 69:829-80.
51. Klipp, E., Nordlander, B., Kruger, R., Gennemark, P. and Hohmann, S. 2005. Integrative model of the response of yeast to osmotic shock. Nature Biotechnology, 23:975-82.
52. Kloosterman, W.P. and Plasterk, R.H.A. 2006. The diverse functions of microRNAs in animal development and disease. Dev. Cell, 11:441-50.
53. Kofahl, B. and Klipp, E. 2004. Modelling the dynamics of the yeast pheromone pathway. Yeast, 21:831-50.
54. Kolkman, A., Olsthoorn, M.M., Heeremans, C.E., Heck, A.J. and Slijper, M. 2005. Comparative proteome analysis of Saccharomyces cerevisiae grown in chemostat cultures limited for glucose or ethanol. Molecular and Cellular Proteomics, 4:1-11.
55. Kopf, E., Shnitzer, D. and Zharhary, D. 2005. Panorama Ab microarray cell signaling kit: a unique tool for protein expression analysis. Proteomics, 5(9):2412-6.
56. Krogan, N.J., Cagney, G., Yu, H. et al. 2006. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature, 440:637-43.
57. Lauffenburger, D. A. 2000. Cell Signaling pathways as control modules: complexity for simplicity? Proc. Natl. Acad. Sci. USA., 97:5031-33.
58. Lei, M. and Tye, B.K. 2001. Initiating DNA synthesis: from recruiting to activating the MCM complex. Journal of Cell Science, 114:1447-54.
59. Li, F., Long, T., Lu, Y., Ouyang, Q. and Tang, C. 2004. The yeast cell-cycle network is robustly designed. Proc. Natl. Acad. Sci. USA., 101:4781-6.
60. Lill, J. 2003. Proteomic tools for quantitation by mass spectrometry. Mass Spectrometry Reviews, 22:182-94.
61. Link, A.J., Fleischer, T.C., Weaver, C.M., Gerbasi, V.R. and Jennings, J.L. 1999. Direct analysis of protein complexes using mass spectrometry. Nature Biotechnology, 17:676-82.
62. Measday, V., Baetz, K., Guzzo, J. et al. 2005. Systematic yeast synthetic lethal and synthetic dosage lethal screens identify genes required for chromosome segregation. Proc. Natl. Acad. Sci. USA., 102:13956-61.
63. Mnaimneh, S., Davierwala, A.P., Haynes, J. et al. 2004. Exploration of essential gene functions via titratable promoter alleles. Cell, 118:31-44.
64. Moles, C., Mendes, P. and Banga, J.R. 2003. Parameter estimation in biochemcal pathways: a comparison of global optimization methods. Genome Research, 13:2467-74.
65. Nguyen, V.Q., Co, C. and Li, J.J. 2001. Cyclin-dependent kinases prevent DNA re-replication through multiple mechanisms. Nature, 411:1068-73.
66. Norel, R. and Agur, Z. 1991. A model for the adjustment of the mitotic clock by cyclin and MPF levels. Science, 251:1076-78.
67. Novak, B. and Pataki, Z. 2001. Mathematical model of the cell division cycle of fission yeast. Chaos, 11:277-86.
68. Novak, B. and Tyson, J.J. 2004. A model for restriction point control of the mammalian cell cycle. Journal of Theoretical Biology, 230:563-79.
69. Oliva, A., Rosebrock, A., Ferrezuelo, F. et al. 2005. The cell cycle-regulated genes of Schizosaccharomyces pombe. PLoS Biology, 3:e225.
70. Ong, S.E., Blagiev, B., Kratchmarova, I. et al. 2002. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Molecular and Cellular Proteomics, 1:376-86.
71. Qu, Z., Weiss, J.N. and MacLellan, W.R. 2003. Regulation of the mammalian cell cycle: a model of the Gsub1-to-S transition. American Journal of Physiology-Cell. Physiology, 284:C349-C346.
72. Parrish, J.R., Gulyas, K.D. and Finley, R.L. Jr. 2006. Yeast two-hybrid contributions to interactome mapping. Current opinion in biotechnology, 17:387-93.
73. Parsons, A.B., Lopez, A., Givoni, I.E. et al. 2006. Exploring the mode-of-action of bioactive compounds by chemical-genetic profiling in yeast. Cell, 126:611-25.
74. Perrot, M., Sagliocco, F., Mini, T. et al. 1999. Two-dimensional gel protein database of. Saccharomyces cerevisiae, Electrophoresis, 20:2280-98.
75. Prakash, A., Mallick, P., Whiteaker, J. et al. 2006. Signal maps for mass spectrometry-based comparative proteomics. Molecular and Cellular Proteomics, 5:423-32.
76. Pramila, T., Wu, W., Miles, S., Noble, W.S. and Breeden, L.L. 2006. The forkhead transcription factor Hcm1 regulates chromosome segregation genes and fills the S-phase gap in the transcriptional circuitry of the cell cycle. Genes and Development, 20:2266-78.
77. Randell, J.C.W., Bowers, J.L., Rodriguez, H.K. and Bell, S.P. 2006. Sequential ATP hydrolysis by Cdc6 and ORC directs loading of the Mcm2-7 helicase. Molecular Cell, 21:29-39.
78. Rodriguez-Fernandez, M., Mendes, P. and Banga, J.R. 2006. A hybrid approach for efficient and robust parameter estimation in biochemical pathways. BioSystems, 83:248-65.
79. Ross, P.L., Huang, Y.N., Marchese, J.N. et al. 2004. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Molecular and Cellular Proteomics, 3:1154-69.
80. Rout, M.P., Aitchison, J.D., Suprapto, A. et al. 2000. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol., 148:635-51.
81. Sachs, R.K., Hlatky, L.R. and Hahnfeldt, P. 2001. Simple models of tumor growth and anti-angiogenic or radiation treatment. Mathematical and Computer Modeling, 33:1297-305.
82. 1/S transition. Bioinformatics, 20:1506-11.
83. Schaber, J., Kofahl, B., Kowald, A. and Klipp, E. 2006. A modeling approach to quantify dynamic crosstalk between the pheromone and the starvation pathway in baker's yeast. FEBS Journal, 273:3520-33.
84. Sechi, S. and Oda, Y. 2003. Quantitative proteomics using mass spectrometry. Current Opinion in Chemical Biology, 7:70-7.
85. Semple, J.W. and Duncker, B.P. 2004. ORC-associated replication factors as biomarkers for cancer. Biotechnology Advances, 22:621-31.
86. Sha, W., Moore, J., Chen, K. et al. 2003. Hysteresis drives cell-cycle transitions in Xenopus laevis egg extracts. Proc. Natl. Acad. Sci. USA., 100:975-80.
87. Sidorova, J.M. and Breeden, L.L. 2003. Precocious G1/S transitions and genomic instability: the origin connection. Mutation Research, 532:5-19.
88. Sopko, R., Huang, D., Preston, N. et al. 2006. Mapping pathways and phenotypes by systematic gene overexpression. Molecular Cell, 21:319-30.
89. Spellman, P.T., Sherlock, G., Zhang, M.Q. et al. 1998. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Molecular Biology of the Cell, 9:3273-97.
90. Srividhya, J. and Gopinathan, M.S. 2006. A simple time delay model for eukaryotic cell cycle. Journal of Theoretical Biology, 241:617-27.
91. Stillman, B. 2005. Origin recognition and the chromosome cycle. FEBS Letters, 579:877-84.
92. Stoll, D., Templin, M.F., Bachmann, J. and Joos, T.O. 2005. Protein microarrays: applications and future challenges. Current Opinion in Drug Discovery and Development, 8:239-52.
93. Sturgeon, C.M., Kemmer, D., Anderson, H.J. and Roberge, M. 2006. Yeast as a tool to uncover the cellular targets of drugs. Biotechnology Journal, 1:289-98.
94. Sugimoto, M., Kikuchi, S. and Tomita, M. 2005. Reverse engineering of biocheical equations from time-course data by means of genetic programming. BioSystems, 80:155-64.
95. Suter, B., Tong, A., Chang, M. et al. 2004. The origin recognition complex links replication, sister chromatid cohesion and transcriptional silencing in. Saccharomyces cerevisiae, Genetics, 167:579-91.
96. Sveiczer, A., Tyson, J.J. and Novak, B. 2001. A stochastic, molecular model of the fission yeast cell cycle: role of the nucleocytoplasmic ratio in cycle time regulation. Biophysical Chemistry, 92:1-15.
97. Szallasi, Z., Periwal, V. and Stelling, J. 2006. On modules and modularity, in. Systems Modeling in Cellular Biology, Szallazi, Z., Stelling, J. and Periwal, V. eds., MIT Press, Cambridge, MA.
98. Tong, A.H., Evangelista, M., Parsons, A.B. et al. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science, 294:2364-8.
99. Tonge, R., Shaw, J., Middleton, B. et al. 2001. Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics, 1:377-96.
100. Tsai, K.-Y. and Wang, F.-S. 2005. Evolutionary optimization with data collocation for reverse engineering of biological networks. Bioinformatics, 21:1180-8.
101. Tyson, J.J. 1991. Modeling the cell division cycle: cdc2 and cyclin interactions. Proc. Natl. Acad. Sci. USA., 88:7328-32.
102. Uetz, P., Giot, L., Cagney, G. et al. 2000. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature, 403:623-7.
103. Vido, K., Spector, D., Lagniel, G. et al. 2001. A proteome analysis of the cadmium response in Saccharomyces cerevisiae. Journal of Biological Chemistry, 276:8469-74.
104. von Mering, C., Krause, R., Snel, B. et al. 2002. Comparative assessment of large-scale data sets of protein-protein interactions. Nature, 417:399-403.
105. Wang, J., Huang, B., Xia, X. and Sun, Z. 2006. Funneled landscape leads to robustness of cell networks: yeast cell cycle. PLoS Computational Biology, 2:e147.
106. Wang, J. and Han, B. 2007. Quantifying dissipation and robustness of the yeast cell cycle: The energy landscape perspectives. Biophysical Journal, doi:10.1529/biophysj.106.094821.
107. Washburn, M.P., Ulaszek, R., Deciu, C., Schieltz, D.M. and Yates, J.R. 3rd. 2001. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nature Biotechnology, 19:242-7.
108. Wei, J., Sun, J., Yu, W. et al. 2005. Global proteome discovery using an online three-dimensional LC-MS/MS. Journal of Proteome Research, 4:801-8.
109. Wigge, P.A., Jensen, O.N., Holmes, S. et al. 1998. Analysis of the Saccharomyces spindle pole by matrix-assisted laser desorption/ionization (MALDI) mass spectrometry. Journal of Cell. Biology, 141:967-77.
110. Wildgruber, R., Reil, G., Drews, O., Parlar, H. and Gorg, A. 2002. Web-based two-dimensional database of Saccharomyces cerevisiae proteins using immobilized pH gradients from pH6 to pH12 and matrix-assisted laser desorption/ionizationtime of flight mass spectrometry. Proteomics, 2:727-32.
111. Wingren, C. and Borrebaeck, C.A. 2004. High-throughput proteomics using antibody microarrays. Expert Rev. Proteomics, 1:355-64.
112. Winzeler, E.A., Shoemaker, D.D., Astromoff, A., Liang, H. et al. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science, 285:901-6.
113. Wolf, D.M. and Arkin, A.P. 2003. Motifs, modules and games in bacteria. Current Opinion in Microbiology, 6:125-34.
114. Wolters, D.A., Washburn, M.P. and Yates, J.R. 3rd. 2001. An automated multidimensional protein identification technology for shotgun proteomics. Analytical Chemistry, 73:5683-90.
115. Wong, S.L., Zhang, L.V., Tong, A.H.Y, Li, Z. et al. 2004. Combining biological networks to predict genetic interactions. Proc. Natl. Acad. Sci. USA., 101:15682-7.
116. Yang, L., Han, Z., MacLellan, W.R., Weiss, J.N. and Qu, Z. 2006. Linking cell division to cell growth in a spatiotemporal model of the cell cycle. Journal of Theoretical Biology, 241:120-33.
117. Yi, T.-M., Kitano, H. and Simon, M.I. 2003. A quantitative characterization of the yeast heterotrimeric G protein cycle. Proc. Natl. Acad. Sci. USA., 100:10764-9.
118. Yin, Z., Stead, D. and Selway, L. 2004. Proteomic response to amino acid starvation in Candida albicans and Saccharomyces cerevisiae. Proteomics, 4:2425-36.