A systematic analysis of cell cycle regulators in yeast reveals that most factors act independently of cell size to control initiation of division

PLoS Genetics

Volumn 8, Issue 3, 2012, Pages

  Hoose, Scott A ^a   Rawlings, Jeremy A ^a   Kelly, Michelle M ^a   Leitch, Camille ^a   Ababneh, Qotaiba O ^a   Robles, Juan P ^a   Taylor, David ^a   Hoover, Evelyn M ^a   Hailu, Bethel ^a   McEnery, Kayla A ^a   Downing, Sabina ^a   Kaushal, Deepika ^a   Chen, Yi ^a   Rife, Alex ^a   Brahmbhatt, Kirtan A ^a   Smith, Roger ^b   Polymenis, Michael ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CBS PROTEIN; CYSTATHIONINE; FUNGAL PROTEIN; HOMOCYSTEINE; RIBOSOME PROTEIN; SERINE; UNCLASSIFIED DRUG; DNA;

ARTICLE; BIOGENESIS; CELL CYCLE REGULATION; CELL DIVISION; CELL PROLIFERATION; CELL SIZE; FLOW CYTOMETRY; GENE DELETION; GENE IDENTIFICATION; NONHUMAN; RIBOSOME; SYSTEMATIC REVIEW; YEAST; G1 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMOZYGOTE; METABOLISM; SACCHAROMYCES CEREVISIAE;

ANIMALIA;

CELL DIVISION; CELL PROLIFERATION; CELL SIZE; DNA; FUNGAL PROTEINS; G1 PHASE CELL CYCLE CHECKPOINTS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; HOMOZYGOTE; RIBOSOMES; SACCHAROMYCES CEREVISIAE;

EID: 84859253080     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002590     Document Type: Article

References (83)

1. Pringle JR, Hartwell LH, (1981) The Saccharomyces cerevisiae cell cycle. In: Strathern JD, Jones EW, Broach JR, editors. The molecular biology of the yeast Saccharomyces Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press pp. 97-142.
2. Hartwell LH, Unger MW, (1977) Unequal division in Saccharomyces cerevisiae and its implications for the control of cell division. J Cell Biol 75: 422-435.
3. Johnston GC, Pringle JR, Hartwell LH, (1977) Coordination of growth with cell division in the yeast Saccharomyces cerevisiae. Exp Cell Res 105: 79-98.
4. Blagosklonny MV, Pardee AB, (2002) The restriction point of the cell cycle. Cell Cycle 1: 103-110.
5. Slater ML, (1977) Cell Cycle of Saccharomyces cerevisiae in Populations Growing at Different Rates. Proc Natl Acad Sci U S A 74: 3850-3854.
6. Jagadish MN, Carter BL, (1977) Genetic control of cell division in yeast cultured at different growth rates. Nature 269: 145-147.
7. Carter BL, Jagadish MN, (1978) Control of cell division in the yeast Saccharomyces cerevisiae cultured at different growth rates. Exp Cell Res 112: 373-383.
8. Pardee AB, (1974) A restriction point for control of normal animal cell proliferation. Proc Natl Acad Sci U S A 71: 1286-1290.
9. Pardee AB, (1989) G1 events and regulation of cell proliferation. Science 246: 603-608.
10. Skotheim JM, Di Talia S, Siggia ED, Cross FR, (2008) Positive feedback of G1 cyclins ensures coherent cell cycle entry. Nature 454: 291-296.
11. Eser U, Falleur-Fettig M, Johnson A, Skotheim JM, (2011) Commitment to a Cellular Transition Precedes Genome-wide Transcriptional Change. Mol Cell 43: 515-527.
12. Doncic A, Falleur-Fettig M, Skotheim JM, (2011) Distinct interactions select and maintain a specific cell fate. Mol Cell 43: 528-539.
13. Bloom J, Cross FR, (2007) Multiple levels of cyclin specificity in cell-cycle control. Nat Rev Mol Cell Biol 8: 149-160.
14. Reed SI, Hadwiger JA, Richardson HE, Wittenberg C, (1989) Analysis of the Cdc28 protein kinase complex by dosage suppression. J Cell Sci Suppl 12: 29-37.
15. Hadwiger JA, Wittenberg C, Richardson HE, de Barros Lopes M, Reed SI, (1989) A family of cyclin homologs that control the G1 phase in yeast. Proc Natl Acad Sci U S A 86: 6255-6259.
16. Hadwiger JA, Wittenberg C, Mendenhall MD, Reed SI, (1989) The Saccharomyces cerevisiae CKS1 gene, a homolog of the Schizosaccharomyces pombe suc1+ gene, encodes a subunit of the Cdc28 protein kinase complex. Mol Cell Biol 9: 2034-2041.
17. Epstein CB, Cross FR, (1994) Genes that can bypass the CLN requirement for Saccharomyces cerevisiae cell cycle START. Mol Cell Biol 14: 2041-2047.
18. Surana U, Robitsch H, Price C, Schuster T, Fitch I, et al. (1991) The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell 65: 145-161.
19. Cross FR, (1988) DAF1, a mutant gene affecting size control, pheromone arrest, and cell cycle kinetics of Saccharomyces cerevisiae. Mol Cell Biol 8: 4675-4684.
20. Edwards MC, Liegeois N, Horecka J, DePinho RA, Sprague GFJ, et al. (1997) Human CPR (Cell Cycle Progression Restoration) genes impart a Far- phenotype on yeast cells. Genetics 147: 1063-1076.
21. Donachie WD, (1968) Relationship between cell size and time of initiation of DNA replication. Nature 219: 1077-1079.
22. Killander D, Zetterberg A, (1965) A quantitative cytochemical investigation of the relationship between cell mass and initiation of DNA synthesis in mouse fibroblasts in vitro. Exp Cell Res 40: 12-20.
23. Jorgensen P, Nishikawa JL, Breitkreutz BJ, Tyers M, (2002) Systematic identification of pathways that couple cell growth and division in yeast. Science 297: 395-400.
24. Zhang J, Schneider C, Ottmers L, Rodriguez R, Day A, et al. (2002) Genomic Scale Mutant Hunt Identifies Cell Size Homeostasis Genes in S. cerevisiae. Curr Biol 12: 1992-2001.
25. Carter BL, Sudbery PE, (1980) Small-sized mutants of Saccharomyces cerevisiae. Genetics 96: 561-566.
26. Sudbery PE, Goodey AR, Carter BL, (1980) Genes which control cell proliferation in the yeast Saccharomyces cerevisiae. Nature 288: 401-404.
27. Prendergast JA, Murray LE, Rowley A, Carruthers DR, Singer RA, et al. (1990) Size selection identifies new genes that regulate Saccharomyces cerevisiae cell proliferation. Genetics 124: 81-90.
28. Niu W, Li Z, Zhan W, Iyer VR, Marcotte EM, (2008) Mechanisms of cell cycle control revealed by a systematic and quantitative overexpression screen in S. cerevisiae. PLoS Genet 4: e1000120 doi:10.1371/journal.pgen.1000120.
29. Stevenson LF, Kennedy BK, Harlow E, (2001) A large-scale overexpression screen in Saccharomyces cerevisiae identifies previously uncharacterized cell cycle genes. Proc Natl Acad Sci U S A 98: 3946-3951.
30. Yu L, Pena Castillo L, Mnaimneh S, Hughes TR, Brown GW, (2006) A survey of essential gene function in the yeast cell division cycle. Mol Biol Cell 17: 4736-4747.
31. Kaiser C, Michaelis S, Mitchell A, (1994) Methods in Yeast Genetics Cold Spring Harbor Cold Spring Harbor Laboratory Press.
32. Schaechter M, Maaloe O, Kjeldgaard NO, (1958) Dependency on medium and temperature of cell size and chemical composition during balanced grown of Salmonella typhimurium. J Gen Microbiol 19: 592-606.
33. Giaever G, Chu AM, Ni L, Connelly C, Riles L, et al. (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
34. Hughes TR, Roberts CJ, Dai H, Jones AR, Meyer MR, et al. (2000) Widespread aneuploidy revealed by DNA microarray expression profiling. Nat Genet 25: 333-337.
35. De Bruin RAM, McDonald WH, Kalashnikova TI, Yates J, Wittenberg C, (2004) Cln3 activates G1-specific transcription via phosphorylation of the SBF bound repressor Whi5. Cell 117: 887-898.
36. Costanzo M, Nishikawa JL, Tang X, Millman JS, Schub O, et al. (2004) CDK activity antagonizes Whi5, an inhibitor of G1/S transcription in yeast. Cell 117: 899-913.
37. Padmanabha R, Gehrung S, Snyder M, (1991) The KNS1 gene of Saccharomyces cerevisiae encodes a nonessential protein kinase homologue that is distantly related to members of the CDC28/cdc2 gene family. Mol Gen Genet 229: 1-9.
38. Reid RJ, Gonzalez-Barrera S, Sunjevaric I, Alvaro D, Ciccone S, et al. (2011) Selective ploidy ablation, a high-throughput plasmid transfer protocol, identifies new genes affecting topoisomerase I-induced DNA damage. Genome Res 21: 477-486.
39. Blank HM, Gajjar S, Belyanin A, Polymenis M, (2009) Sulfur Metabolism Actively Promotes Initiation of Cell Division in Yeast. PLoS ONE 4: e8018 doi:10.1371/journal.pone.0008018.
40. Henry KA, Blank HM, Hoose SA, Polymenis M, (2010) The unfolded protein response is not necessary for the G1/S transition, but it is required for chromosome maintenance in Saccharomyces cerevisiae. PLoS ONE 5: e12732 doi:10.1371/journal.pone.0012732.
41. Blank HM, Li C, Mueller JE, Bogomolnaya LM, Bryk M, et al. (2008) An increase in mitochondrial DNA promotes nuclear DNA replication in yeast. PLoS Genet 4: e1000047 doi:10.1371/journal.pgen.1000047.
42. Bjorklund M, Taipale M, Varjosalo M, Saharinen J, Lahdenpera J, et al. (2006) Identification of pathways regulating cell size and cell-cycle progression by RNAi. Nature 439: 1009-1013.
43. Kittler R, Pelletier L, Heninger AK, Slabicki M, Theis M, et al. (2007) Genome-scale RNAi profiling of cell division in human tissue culture cells. Nat Cell Biol 9: 1401-1412.
44. Zettel MF, Garza LR, Cass AM, Myhre RA, Haizlip LA, et al. (2003) The budding index of Saccharomyces cerevisiae deletion strains identifies genes important for cell cycle progression. FEMS Microbiol Lett 223: 253-258.
45. Mendenhall MD, Al-Jumaily W, Nugroho TT, (1995) The Cdc28 inhibitor p40SIC1. Prog Cell Cycle Res 1: 173-185.
46. Moore SA, (1988) Kinetic evidence for a critical rate of protein synthesis in the Saccharomyces cerevisiae yeast cell cycle. J Biol Chem 263: 9674-9681.
47. Unger MW, Hartwell LH, (1976) Control of cell division in Saccharomyces cerevisiae by methionyl-tRNA. Proc Natl Acad Sci U S A 73: 1664-1668.
48. Bernstein KA, Bleichert F, Bean JM, Cross FR, Baserga SJ, (2007) Ribosome Biogenesis Is Sensed at the Start Cell Cycle Checkpoint. Mol Biol Cell 18: 953-964.
49. Polymenis M, Schmidt EV, (1997) Coupling of cell division to cell growth by translational control of the G1 cyclin CLN3 in yeast. Gene Dev 11: 2522-2531.
50. Jorgensen P, Rupes I, Sharom JR, Schneper L, Broach JR, et al. (2004) A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Gene Dev 18: 2491-2505.
51. Marion RM, Regev A, Segal E, Barash Y, Koller D, et al. (2004) Sfp1 is a stress- and nutrient-sensitive regulator of ribosomal protein gene expression. Proc Natl Acad Sci U S A 101: 14315-14322.
52. Fingerman I, Nagaraj V, Norris D, Vershon AK, (2003) Sfp1 plays a key role in yeast ribosome biogenesis. Eukaryot Cell 2: 1061-1068.
53. Tong AH, Lesage G, Bader GD, Ding H, Xu H, et al. (2004) Global mapping of the yeast genetic interaction network. Science 303: 808-813.
54. Stark C, Breitkreutz BJ, Chatr-Aryamontri A, Boucher L, Oughtred R, et al. (2011) The BioGRID Interaction Database: 2011 update. Nucleic Acids Res 39: D698-D704.
55. Gavin AC, Aloy P, Grandi P, Krause R, Boesche M, et al. (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440: 631-636.
56. Quazi F, Aitken SM, (2009) Characterization of the S289A,D mutants of yeast cystathionine beta-synthase. Biochim Biophys Acta 1794: 892-897.
57. Cherest H, Thomas D, Surdin-Kerjan Y, (1993) Cysteine biosynthesis in Saccharomyces cerevisiae occurs through the transsulfuration pathway which has been built up by enzyme recruitment. J Bacteriol 175: 5366-5374.
58. Fowler B, (2005) Homocysteine: overview of biochemistry, molecular biology, and role in disease processes. Semin Vasc Med 5: 77-86.
59. Shan X, Kruger WD, (1998) Correction of disease-causing CBS mutations in yeast. Nat Genet 19: 91-93.
60. Watanabe M, Osada J, Aratani Y, Kluckman K, Reddick R, et al. (1995) Mice deficient in cystathionine beta-synthase: animal models for mild and severe homocyst(e)inemia. Proc Natl Acad Sci U S A 92: 1585-1589.
61. Enokido Y, Suzuki E, Iwasawa K, Namekata K, Okazawa H, et al. (2005) Cystathionine beta-synthase, a key enzyme for homocysteine metabolism, is preferentially expressed in the radial glia/astrocyte lineage of developing mouse CNS. FASEB J 19: 1854-1856.
62. Wang L, Chen X, Tang B, Hua X, Klein-Szanto A, et al. (2005) Expression of mutant human cystathionine beta-synthase rescues neonatal lethality but not homocystinuria in a mouse model. Hum Mol Genet 14: 2201-2208.
63. Shilo B, Simchen G, Pardee AB, (1978) Regulation of cell-cycle initiation in yeast by nutrients and protein synthesis. J Cell Physiol 97: 177-187.
64. Shilo B, Riddle VG, Pardee AB, (1979) Protein turnover and cell-cycle initiation in yeast. Exp Cell Res 123: 221-227.
65. Popolo L, Vanoni M, Alberghina L, (1982) Control of the yeast cell cycle by protein synthesis. Exp Cell Res 142: 69-78.
66. Wells W, (2002) Does size matter? J Cell Biol 158: 1156-1159.
67. Leslie M, (2011) How Does a Cell Know Its Size. Science 334: 1047-1048.
68. Conlon I, Raff M, (2003) Differences in the way a mammalian cell and yeast cells coordinate cell growth and cell-cycle progression. J Biol 2: 7.
69. Tzur A, Kafri R, Lebleu VS, Lahav G, Kirschner MW, (2009) Cell growth and size homeostasis in proliferating animal cells. Science 325: 167-171.
70. Van Riggelen J, Yetil A, Felsher DW, (2010) MYC as a regulator of ribosome biogenesis and protein synthesis. Nat Rev Cancer 10: 301-309.
71. Chan JC, Hannan KM, Riddell K, Ng PY, Peck A, et al. (2011) AKT Promotes rRNA Synthesis and Cooperates with c-MYC to Stimulate Ribosome Biogenesis in Cancer. Science signaling 4: ra56.
72. Oskarsson T, Trumpp A, (2005) The Myc trilogy: lord of RNA polymerases. Nat Cell Biol 7: 215-217.
73. Grewal SS, Li L, Orian A, Eisenman RN, Edgar BA, (2005) Myc-dependent regulation of ribosomal RNA synthesis during Drosophila development. Nat Cell Biol 7: 295-302.
74. Verma R, Feldman RM, Deshaies RJ, (1997) SIC1 is ubiquitinated in vitro by a pathway that requires CDC4, CDC34, and cyclin/CDK activities. Mol Biol Cell 8: 1427-1437.
75. Brauer MJ, Huttenhower C, Airoldi EM, Rosenstein R, Matese JC, et al. (2008) Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast. Mol Biol Cell 19: 352-367.
76. Guo J, Bryan BA, Polymenis M, (2004) Nutrient-specific effects in the coordination of cell growth with cell division in continuous cultures of Saccharomyces cerevisiae. Arch Microbiol 182: 326-330.
77. Tyson CB, Lord PG, Wheals AE, (1979) Dependency of Size of Saccharomyces cerevisiae Cells on Growth rate. J 138: 92-98.
78. Johnston GC, Ehrhardt CW, Lorincz A, Carter BL, (1979) Regulation of cell size in the yeast Saccharomyces cerevisiae. J Bacteriol 137: 1-5.
79. Jorgensen P, Tyers M, (2004) How cells coordinate growth and division. Curr Biol 14: R1014-R1027.
80. Kruger WD, Cox DR, (1994) A yeast system for expression of human cystathionine beta-synthase: structural and functional conservation of the human and yeast genes. Proc Natl Acad Sci U S A 91: 6614-6618.
81. Kotecha N, Krutzik PO, Irish JM, (2010) Web-based analysis and publication of flow cytometry experiments. Current protocols in cytometry Chapter 10: Unit10.17.
82. Kushnirov VV, (2000) Rapid and reliable protein extraction from yeast. Yeast 16: 857-860.
83. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T, (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27: 431-432.