Molecular systems biology of sic1 in yeast cell cycle regulation through multiscale modeling

Advances in Experimental Medicine and Biology

Volumn 736, Issue , 2012, Pages 135-167

  Barberis, Matteo ^a,b  

^a HUMBOLDT UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR; CYCLIN DEPENDENT KINASE INHIBITOR 1B; PROTEIN SIC1; UNCLASSIFIED DRUG;

ARTICLE; CARCINOGENESIS; CDKN1B GENE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; COMPUTER MODEL; CONTROLLED STUDY; ENZYME REGULATION; MATHEMATICAL COMPUTING; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; MULTISCALE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS; SYSTEMS BIOLOGY; TUMOR SUPPRESSOR GENE; YEAST CELL;

AMINO ACID SEQUENCE; BINDING SITES; CELL CYCLE; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLIN-DEPENDENT KINASE INHIBITOR PROTEINS; CYCLIN-DEPENDENT KINASES; CYCLINS; GENE REGULATORY NETWORKS; HUMANS; MODELS, GENETIC; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NEOPLASMS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SYSTEMS BIOLOGY; TIME FACTORS;

SACCHAROMYCES CEREVISIAE;

EID: 84855975693     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4419-7210-1_7     Document Type: Article

References (195)

1. Obaya AJ, Sedivy JM (2002) Regulation of cyclin-Cdk activity in mammalian cells. Cell Mol Life Sci 59(1):126-142 (Pubitemid 34117361)
2. Morgan DO (1995) Principles of CDK regulation. Nature 374(6518):131-134
3. De Clercq A, Inze D (2006) Cyclin-dependent kinase inhibitors in yeast, animals, and plants: a functional comparison. Crit Rev Biochem Mol Biol 41(5):293-313 (Pubitemid 44258247)
4. Sherr CJ, Roberts JM (1995) Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 9(10):1149-1163
5. Sherr CJ, Roberts JM (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13(12):1501-1512 (Pubitemid 29297917)
6. Tsihlias J, Kapusta L, Slingerland J (1999) The prognostic significance of altered cyclindependent kinase inhibitors in human cancers. Annu Rev Med 50:401-423 (Pubitemid 29117075)
7. Besson A, Dowdy SF, Roberts JM (2008) CDK inhibitors: cell cycle regulators and beyond. Dev Cell 14(2):159-169 (Pubitemid 351189186)
8. Chu IM, Hengst L, Slingerland JM(2008) The Cdk inhibitor p27 in human cancer: prognostic potential and relevance to anticancer therapy. Nat Rev Cancer 8(4):253-267 (Pubitemid 351430863)
9. Abukhdeir AM, Park BH (2008) P21 and p27: roles in carcinogenesis and drug resistance. Expert Rev Mol Med 10:e19
10. Hershko DD (2008) Oncogenic properties and prognostic implications of the ubiquitin ligase Skp2 in cancer. Cancer 112(7):1415-1424 (Pubitemid 351441154)
11. Mishra A, Godavarthi SK, Jana NR (2009) UBE3A/E6-AP regulates cell proliferation by promoting proteasomal degradation of p27. Neurobiol Dis 36(1):26-34
12. Slingerland J, Pagano M (2000) Regulation of the cdk inhibitor p27 and its deregulation in cancer. J Cell Physiol 183(1):10-17 (Pubitemid 30130220)
13. Lloyd RV, Erickson LA, Jin L, Kulig E, Qian X, Cheville JC, Scheithauer BW(1999) p27kip1: a multifunctional cyclin-dependent kinase inhibitor with prognostic significance in human cancers. Am J Pathol 154(2):313-323 (Pubitemid 29094081)
14. Belletti B, Nicoloso MS, Schiappacassi M, Chimienti E, Berton S, Lovat F, Colombatti A, Baldassarre G (2005) p27(kip1) functional regulation in human cancer: a potential target for therapeutic designs. Curr Med Chem 12(14):1589-1605 (Pubitemid 40895003)
15. Polyak K, Lee MH, Erdjument-Bromage H, Koff A, Roberts JM, Tempst P, MassaguéJ (1994) Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78(1):59-66
16. Toyoshima H, Hunter T (1994) p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity, is related to p21. Cell 78(1):67-74 (Pubitemid 24228301)
17. Coats S, Flanagan WM, Nourse J, Roberts JM (1996) Requirement of p27Kip1 for restriction point control of the fibroblast cell cycle. Science 272(5263):877-880
18. Ray A, James MK, Larochelle S, Fisher RP, Blain SW (2009) p27Kip1 inhibits cyclin D-cyclin-dependent kinase 4 by two independent modes. Mol Cell Biol 29(4):986-999
19. LaBaer J, Garrett MD, Stevenson LF, Slingerland JM, Sandhu C, Chou HS, Fattaey A, Harlow E (1997) New functional activities for the p21 family of CDK inhibitors. Genes Dev 11(7):847-862 (Pubitemid 27175292)
20. Cheng M, Olivier P, Diehl JA, Fero M, Roussel MF, Roberts JM, Sherr CJ (1999) The p21(Cip1) and p27(Kip1) CDK 'inhibitors' are essential activators of cyclin D-dependent kinases in murine fibroblasts. EMBO J 18(6):1571-83 (Pubitemid 29127070)
21. Fero ML, Randel E, Gurley KE, Roberts JM, Kemp CJ (1998) The murine gene p27Kip1 is haplo-insufficient for tumour suppression. Nature 396(6707):177-180 (Pubitemid 28523620)
22. Loda M, Cukor B, Tam SW, Lavin P, Fiorentino M, Draetta GF, Jessup JM, Pagano M (1997) Increased proteasome-dependent degradation of the cyclin-dependent kinase inhibitor p27 in aggressive colorectal carcinomas. Nat Med 3(2):231-234 (Pubitemid 27064711)
23. Slingerland J, Pagano M (2000) Regulation of the cdk inhibitor p27 and its deregulation in cancer. J Cell Physiol 183(1):10-17 (Pubitemid 30130220)
24. Coqueret O (2003) New roles for p21 and p27 cell-cycle inhibitors: a function for each cell compartment? Trends Cell Biol 13(2):65-70 (Pubitemid 36135887)
25. Futcher B (1996) Cyclins and the wiring of the yeast cell cycle. Yeast 12(16):1635-1646 (Pubitemid 27055831)
26. Nasmyth K (1996) At the heart of the budding yeast cell cycle. Trends Genet 12(10): 405-412 (Pubitemid 26336483)
27. Cross FR, Yuste-Rojas M, Gray S, Jacobson MD (1999). Specialization and targeting of B-type cyclins. Mol Cell 4(1):11-9 (Pubitemid 29386127)
28. Murray AW (2004) Recycling the cell cycle: cyclins revisited. Cell 116(2):221-234 (Pubitemid 38167314)
29. Bloom J, Cross FR (2007) Multiple levels of cyclin specificity in cell-cycle control. Nat Rev Mol Cell Biol 8(2):149-160 (Pubitemid 46432532)
30. Chang F, Herskowitz I (1990) Identification of a gene necessary for cell cycle arrest by a negative growth factor of yeast: FAR1 is an inhibitor of a G1 cyclin, CLN2. Cell 63(5):999-1011 (Pubitemid 120034941)
31. Peter M, Herskowitz I (1994) Direct inhibition of the yeast cyclin-dependent kinase Cdc28-Cln by Far1. Science 265(5176):1228-1231 (Pubitemid 24291980)
32. Mendenhall MD (1993) An inhibitor of p34CDC28 protein kinase activity from Saccharomyces cerevisiae. Science 259(5092):216-219 (Pubitemid 23041796)
33. Schwob E, Bohm T, Mendenhall MD, Nasmyth K (1994) The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae. Cell 79(2):233-244
34. Alberghina L, Martegani E, Mariani L, Bortolan G (1983-1984) A bimolecular mechanism for the cell size control of the cell cycle. Biosystems 16(3-4):297-305 (Pubitemid 14125486)
35. Alberghina L, Porro D, Cazzador L (2001) Towards a blueprint of the cell cycle. Oncogene 20(9):1128-1134 (Pubitemid 32238862)
36. Deshaies RJ (1997) Phosphorylation and proteolysis: partners in the regulation of cell division in budding yeast. Curr Opin Genet Dev 7(1):7-16 (Pubitemid 27092758)
37. Zachariae W, Nasmyth K (1999) Whose end is destruction: cell division and the anaphasepromoting complex. Genes Dev 13(16):2039-2058 (Pubitemid 29407346)
38. Knapp D, Bhoite L, Stillman DJ, Nasmyth K (1996) The transcription factor Swi5 regulates expression of the cyclin kinase inhibitor p40SIC1. Mol Cell Biol 16(10):5701-5707 (Pubitemid 26315090)
39. Toyn JH, Johnson AL, Donovan JD, Toone WM, Johnston LH (1997) The Swi5 transcription factor of Saccharomyces cerevisiae has a role in exit from mitosis through induction of the cdk-inhibitor Sic1 in telophase. Genetics 145(1):85-96
40. Aerne BL, Johnson AL, Toyn JH, Johnston LH (1998) Swi5 controls a novel wave of cyclin synthesis in late mitosis. Mol Biol Cell 9(4):945-956 (Pubitemid 28173645)
41. Schneider BL, Yang QH, Futcher AB (1996) Linkage of replication to start by the Cdk inhibitor Sic1. Science 272(5261):560-562 (Pubitemid 26138202)
42. Verma R, Annan RS, Huddleston MJ, Carr SA, Reynard G, Deshaies RJ (1997) Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase. Science 278(5337):455-460 (Pubitemid 27454428)
43. Thornton BR, Toczyski DP (2003) Securin and B-cyclin/CDK are the only essential targets of the APC. Nat Cell Biol 5(12):1090-1094 (Pubitemid 37509116)
44. Nash P, Tang X, Orlicky S, Chen Q, Gertler FB, Mendenhall MD, Sicheri F, Pawson T, Tyers M (2001) Multisite phosphorylation of a CDK inhibitor sets a threshold for the onset of DNA replication. Nature 414(6863):514-521 (Pubitemid 33131529)
45. Skowyra D, Craig KL, Tyers M, Elledge SJ, Harper JW (1997) F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91(2): 209-219 (Pubitemid 27456388)
46. Feldman RM, Correll CC, Kaplan KB, Deshaies RJ (1997) A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 91(2):221-230 (Pubitemid 27456389)
47. 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(8):1427-1437 (Pubitemid 27385567)
48. Verma R, McDonald H, Yates JR 3rd, Deshaies RJ (2001) Selective degradation of ubiquitinated Sic1 by purified 26S proteasome yields active S phase cyclin-Cdk. Mol Cell 8(2):439-448 (Pubitemid 32831560)
49. Rossi RL, Zinzalla V, Mastriani A, Vanoni M, Alberghina L (2005) Subcellular localization of the cyclin dependent kinase inhibitor Sic1 is modulated by the carbon source in budding yeast. Cell Cycle 4(12):1798-1807 (Pubitemid 41827327)
50. Lengronne A, Schwob E (2002) The yeast CDK inhibitor Sic1 prevents genomic instability by promoting replication origin licensing in late G(1). Mol Cell 9(5):1067-1078 (Pubitemid 34626675)
51. Caburet S, Conti C, Bensimon A (2002) Combing the genome for genomic instability. Trends Biotechnol 20(8):344-350 (Pubitemid 34804423)
52. Nugroho TT Mendenhall MD (1994) An inhibitor of yeast cyclindependent protein kinase plays an important role in ensuring the genomic integrity of daughter cells. Mol Cell Biol 14(5):3320-3328 (Pubitemid 24132744)
53. SeeWL, Miller JP, Squatrito M, Holland E, Resh MD, Koff A (2010) Defective DNA doublestrand break repair underlies enhanced tumorigenesis and chromosomal instability in p27-deficient mice with growth factor-induced oligodendrogliomas. Oncogene 29(12):1720-1731
54. Schwob E (2004) Flexibility and governance in eukaryotic DNA replication. Curr Opin Microbiol 7(6):680-690 (Pubitemid 39536297)
55. Han JD (2008) Understanding biological functions through molecular networks. Cell Res 18(2):224-237
56. Kitano H (2002) Looking beyond the details: a rise in system-oriented approaches in genetics and molecular biology. Curr Genet 41(1):1-10 (Pubitemid 36075954)
57. Westerhoff HV, Alberghina L (2005) Systems biology: did we know it all along? In: Alberghina L, Westerhoff HV (eds) Systems biology definitions and perspectives. Springer Berlin
58. Papin JA, Hunter T, Palsson BO, Subramaniam S (2005) Reconstruction of cellular signaling networks and analysis of their properties. Nat Rev Mol Cell Biol 6(2):99-111 (Pubitemid 40215806)
59. Hartwell LH, Hopfield JJ, Leibler S, Murray AW (1999) From molecular to modular cell biology. Nature 402(6761 Suppl):C47-C52
60. Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM, Remor M, Hofert C, Schelder M, Brajenovic M, Ruffner H, Merino A, Klein K, Hudak M, Dickson D, Rudi T, Gnau V, Bauch A, Bastuck S, Huhse B, Leutwein C, Heurtier MA, Copley RR, Edelmann A, Querfurth E, Rybin V, Drewes G, RaidaM, Bouwmeester T, Bork P, Seraphin B, Kuster B, Neubauer G, Superti-Furga G (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415(6868):141-147 (Pubitemid 34059510)
61. Gandhi TK, Zhong J, Mathivanan S, Karthick L, Chandrika KN, Mohan SS, Sharma S, Pinkert S, Nagaraju S, Periaswamy B, Mishra G, Nandakumar K, Shen B, Deshpande N, Nayak R, Sarker M, Boeke JD, Parmigiani G, Schultz J, Bader JS, Pandey A (2006) Analysis of the human protein interactome and comparison with yeast, worm and fly interaction datasets. Nat Genet 38(3):285-293
62. Bertin N, Simonis N, Dupuy D, Cusick ME, Han JD, Fraser HB, Roth FP, Vidal M (2007) Confirmation of organized modularity in the yeast interactome. PLoS Biol 5(6):e153
63. Han JD, Bertin N, Hao T, Goldberg DS, Berriz GF, Zhang LV, Dupuy D,Walhout AJ, Cusick ME, Roth FP, Vidal M (2004) Evidence for dynamically organized modularity in the yeast protein-protein interaction network. Nature 430(6995):88-93 (Pubitemid 38915230)
64. de Lichtenberg U, Jensen LJ, Brunak S, Bork P (2005) Dynamic complex formation during the yeast cell cycle. Science 307(5710):724-727 (Pubitemid 40194642)
65. Csikasz-Nagy A, Battogtokh D, Chen KC, Novak B, Tyson JJ (2006) Analysis of a generic model of eukaryotic cell-cycle regulation. Biophys J 90(12):4361-4379 (Pubitemid 43830884)
66. Fauré A, Naldi A, Chaouiya C, Thieffry D (2006) Dynamical analysis of a generic Boolean model for the control of the mammalian cell cycle. Bioinformatics 22(14):e124-131 (Pubitemid 44288280)
67. Singhania R, Sramkoski RM, Jacobberger JW, Tyson JJ (2011) A hybrid model ofmammalian cell cycle regulation. PLoS Comput Biol 7(2):e1001077
68. Kohn KW (1998) Functional capabilities of molecular network components controlling the mammalian G1/S cell cycle phase transition. Oncogene 16(8):1065-1075 (Pubitemid 28107944)
69. Aguda BD, Tang Y (1999) The kinetic origins of the restriction point in the mammalian cell cycle. Cell Prolif 32(5):321-335 (Pubitemid 30011387)
70. Qu Z, Weiss JN, MacLellan WR (2003) Regulation of the mammalian cell cycle: a model of the G1-to-S transition. Am J Physiol Cell Physiol 284(2):C349-C364 (Pubitemid 36120073)
71. Swat M, Kel A, Herzel H (2004) Bifurcation analysis of the regulatory modules of the mammalian G1/S transition. Bioinformatics 20(10):1506-1511 (Pubitemid 39023153)
72. Novak B, Tyson JJ (2004) A model for restriction point control of the mammalian cell cycle. J Theor Biol 230(4):563-579 (Pubitemid 39195088)
73. Haberichter T, Madge B, Christopher RA, Yoshioka N, Dhiman A, Miller R, Gendelman R, Aksenov SV, Khalil IG, Dowdy SF (2007) A systems biology dynamical model ofmammalian G1 cell cycle progression. Mol Syst Biol 3:84
74. Alfieri R, BarberisM, Chiaradonna F, Gaglio D,Milanesi L, VanoniM, Klipp E, Alberghina L (2009) Towards a systems biology approach to mammalian cell cycle: modeling the entrance into S phase of quiescent fibroblasts after serum stimulation. BMC Bioinformatics 10 (Suppl 12):S16
75. Chen KC, Csikasz-Nagy A, Gyorffy B, Val J, Novak B, Tyson JJ (2000) Kinetic analysis of a molecular model of the budding yeast cell cycle. Mol Biol Cell 11(1):369-391 (Pubitemid 30075529)
76. Chen KC, Calzone L, Csikasz-Nagy A, Cross FR, Novak B, Tyson JJ (2004) Integrative analysis of cell cycle control in budding yeast. Mol Biol Cell 15(8):3841-3862 (Pubitemid 38989719)
77. Allen NA, Chen KC, Shaffer CA, Tyson JJ, Watson LT (2006) Computer evaluation of network dynamics models with application to cell cycle control in budding yeast. Syst Biol (Stevenage) 153(1):13-21 (Pubitemid 43153697)
78. Barik D, Baumann WT, Paul MR, Novak B, Tyson JJ (2010) A model of yeast cell-cycle regulation based on multisite phosphorylation. Mol Syst Biol 6:405
79. Li F, Long T, Lu Y, Ouyang Q, Tang C (2004) The yeast cell-cycle network is robustly designed. Proc Natl Acad Sci USA 101(14): 4781-4786 (Pubitemid 38469154)
80. Irons DJ (2009) Logical analysis of the budding yeast cell cycle. J Theor Biol 257(4):543-559
81. Fauré A, Naldi A, Lopez F, Chaouiya C, Ciliberto A, Thieffry D (2009) Modular logical modelling of the budding yeast cell cycle. Mol BioSyst 5(12):1787-1796
82. Braunewell S, Bornholdt S (2007) Superstability of the yeast cell-cycle dynamics: ensuring causality in the presence of biochemical stochasticity. J Theor Biol 245(4):638-643 (Pubitemid 46452662)
83. Palmisano A, Mura I, Priami C (2009) From ODES to language-based, executable models of biological systems. Pac Symp Biocomput 14:239-250
84. Barberis M, Beck C, Amoussouvi A, Schreiber G, Diener C, Herrmann A, Klipp E (2011) Low number of SIC1 mRNA molecules ensures low noise level in cell cycle progression of budding yeast. Mol BioSyst 7(10):2804-2812
85. Lovrics A, Csikasz-Nagy A, Zsely IG, Zador J, Turanyi T, Novak B (2006) Time scale and dimension analysis of a budding yeast cell cycle model. BMC Bioinform 7:494
86. Ciliberto A, Lukács A, Tóth A, Tyson JJ, Novák B (2005) Rewiring the exit from mitosis. Cell Cycle 4(8):1107-1112 (Pubitemid 41365371)
87. Queralt E, Lehane C, Novak B, Uhlmann F (2006) Downregulation of PP2A(Cdc55) phosphatase by separase initiates mitotic exit in budding yeast. Cell 125(4):719-732
88. Tóth A, Queralt E, Uhlmann F, Novák B (2007) Mitotic exit in two dimensions. J Theor Biol 248(3):560-573 (Pubitemid 47368376)
89. Vinod PK, Freire P, Rattani A, Ciliberto A, Uhlmann F, Novak B (2011) Computational modelling of mitotic exit in budding yeast: the role of separase and Cdc14 endocycles. J R Soc Interface 8(61):1128-1141
90. Ball DA, Ahn TH, Wang P, Chen KC, Cao Y, Tyson JJ, Peccoud J, Baumann WT (2011) Stochastic exit from mitosis in budding yeast: model predictions and experimental observations. Cell Cycle 10(6):999-1009
91. Alarcón T, Tindall MJ (2007)Modelling cell growth and its modulation of the G1/S transition. Bull Math Biol 69(1):197-214 (Pubitemid 46155351)
92. Barberis M, Klipp E, Vanoni M, Alberghina L (2007) Cell size at S phase initiation: an emergent property of the G1/S network. PLoS Comput Biol 3(4):e64
93. Bruggeman FJ, Westerhoff HV (2007) The nature of systems biology. Trends Microbiol 15(1):45-50 (Pubitemid 46043550)
94. Barberis M, De Gioia L, Ruzzene M, Sarno S, Coccetti P, Fantucci P, Vanoni M, Alberghina L (2005) The yeast cyclindependent kinase inhibitor Sic1 and mammalian p27Kip1 are functional homologues with a structurally conserved inhibitory domain. Biochem J 387(Pt 3):639-647 (Pubitemid 40685697)
95. Barberis M, Pagano MA, Gioia LD,Marin O, VanoniM, Pinna LA, Alberghina L (2005) CK2 regulates in vitro the activity of the yeast cyclin-dependent kinase inhibitor Sic1. Biochem Biophys Res Commun 336(4):1040-1048 (Pubitemid 41383427)
96. Barberis M, Klipp E (2007) Insights into the network controlling the G1/S transition in budding yeast. Genome Inform 18:85-99
97. Barberis M, Linke C, Adrover MA, Lehrach H, Posas F, Krobitsch S, Klipp E (2011) Sic1 plays a role in timing and oscillatory behaviour of B-type cyclins. Biotechnol Adv, doi:10.1016/j.biotechadv.2011.09.004
98. Archambault V, Li CX, Tackett AJ, Wasch R, Chait BT, Rout MP, Cross FR (2003) Genetic and biochemical evaluation of the importance of Cdc6 in regulating mitotic exit. Mol Biol Cell 14(11):4592-4604 (Pubitemid 37444658)
99. Coccetti P, Rossi RL, Sternieri F, Porro D, Russo GL, di Fonzo A, Magni F, Vanoni M, Alberghina L (2004) Mutations of the CK2 phosphorylation site of Sic1 affect cell size and S-Cdk kinase activity in Saccharomyces cerevisiae. Mol Microbiol 51(2):447-460 (Pubitemid 38145588)
100. Cross FR, Schroeder L, Bean JM (2007) Phosphorylation of the Sic1 inhibitor of B-type cyclins in Saccharomyces cerevisiae is not essential but contributes to cell cycle robustness. Genetics 176(3):1541-1555 (Pubitemid 47105216)
101. Aloy P, Russell RB (2006) Structural systems biology: modelling protein interactions. Nat Rev Mol Cell Biol 7(3):188-197
102. Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N, Klitgord N, Simon C, Boxem M, Milstein S, Rosenberg J, Goldberg DS, Zhang LV, Wong SL, Franklin G, Li S, Albala JS, Lim J, Fraughton C, Llamosas E, Cevik S, Bex C, Lamesch P, Sikorski RS, Vandenhaute J, Zoghbi HY, Smolyar A, Bosak S, Sequerra R, Doucette-Stamm L, Cusick ME, Hill DE, Roth FP, Vidal M (2005) Towards a proteome-scale map of the human protein-protein interaction network. Nature 437(7062):1173-1178 (Pubitemid 41509356)
103. Stelzl U, Worm U, Lalowski M, Haenig C, Brembeck FH, Goehler H, Stroedicke M, Zenkner M, Schoenherr A, Koeppen S, Timm J, Mintzlaff S, Abraham C, Bock N, Kietzmann S, Goedde A, Toksöz E, Droege A, Krobitsch S, Korn B, Birchmeier W, Lehrach H, Wanker EE (2005) A human protein-protein interaction network: a resource for annotating the proteome. Cell 122(6):957-968 (Pubitemid 41345212)
104. Uetz P, Giot L, Cagney G, Mansfield TA, Judson RS, Knight JR, Lockshon D, Narayan V, Srinivasan M, Pochart P, Qureshi-Emili A, Li Y, Godwin B, Conover D, Kalbfleisch T, Vijayadamodar G, Yang M, Johnston M, Fields S, Rothberg JM (2000) A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403(6770): 623-627 (Pubitemid 30103994)
105. Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, Sakaki Y (2001) A comprehensive twohybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci USA 98(8): 4569-4574 (Pubitemid 32295017)
106. Yu H, Braun P, Yildirim MA, Lemmens I, Venkatesan K, Sahalie J, Hirozane-Kishikawa T, Gebreab F, Li N, Simonis N, Hao T, Rual JF, Dricot A, Vazquez A, Murray RR, Simon C, Tardivo L, Tam S, Svrzikapa N, Fan C, de Smet AS, Motyl A, Hudson ME, Park J, Xin X, Cusick ME, Moore T, Boone C, Snyder M, Roth FP, Barabási AL, Tavernier J, Hill DE, VidalM(2008) High-quality binary protein interaction map of the yeast interactome network. Science 322(5898):104-110
107. Aloy P, Böttcher B, Ceulemans H, Leutwein C, Mellwig C, Fischer S, Gavin AC, Bork P, Superti-Furga G, Serrano L, Russell RB (2004) Structure-based assembly of protein complexes in yeast. Science 303(5666):2026-2029 (Pubitemid 38393279)
108. Aloy P, Pichaud M, Russell RB (2005) Protein complexes: structure prediction challenges for the 21st century. Curr Opin Struct Biol 15(1):15-22 (Pubitemid 40249504)
109. Aloy P, Russell RB (2004) Ten thousand interactions for the molecular biologist. Nat Biotechnol 22(10):1317-1321 (Pubitemid 39336787)
110. Aloy P, Ceulemans H, Stark A, Russell RB (2003) The relationship between sequence and interaction divergence in proteins. J Mol Biol 332(5):989-998 (Pubitemid 37108793)
111. Aloy P, Russell RB (2002) Interrogating protein interaction networks through structural biology. Proc Natl Acad Sci USA 99(9):5896-5901 (Pubitemid 34493236)
112. Lu L, Lu H, Skolnick J (2002) MULTIPROSPECTOR: an algorithm for the prediction of protein-protein interactions by multimeric threading. Proteins 49(3):350-364 (Pubitemid 35231471)
113. Lu L, Arakaki AK, Lu H, Skolnick J (2003) Multimeric threading-based prediction of protein-protein interactions on a genomic scale: application to the Saccharomyces cerevisiae proteome. Genome Res 13(6A):1146-1154 (Pubitemid 36764194)
114. Mosca R, Pons C, Fernández-Recio J, Aloy P (2009) Pushing structural information into the yeast interactome by high-throughput protein docking experiments. PLoS Comput Biol 5(8):e1000490
115. Sánchez-Díaz A, González I, Arellano M, Moreno S (1998) The Cdk inhibitors p25rum1 and p40SIC1 are functional homologues that play similar roles in the regulation of the cell cycle in fission and budding yeast. J Cell Sci 111(Pt 6):843-851 (Pubitemid 28163892)
116. PeterM,Herskovitz I (1994) Joining the complex: cyclin-dependent kinase inhibitory proteins and the cell cycle. Cell 79(2):181-184
117. Hodge A, Mendenhall M (1999) The cyclin-dependent kinase inhibitory domain of the yeast Sic1 protein is contained within the C-terminal 70 amino acids. Mol Gen Genet 262(1):55-64 (Pubitemid 29423902)
118. Russo AA, Jeffrey PD, Patten AK, Massagué J, Pavletich NP (1996) Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature 382(6589):325-331 (Pubitemid 26260452)
119. Barberis M (2000) Phenotypic analysis of Ser201/Glu and Ser201/Ala mutants in Saccharomyces cerevisiae and their functional interpretation on the basis of a three-dimensional model of Clb5/Cdc28/p40Sic1 complex built by homology. Dissertation, University of Milano-Bicocca, Milan
120. Heiner AP, Berendsen HJ, van Gunsteren WF (1992) MD simulation of subtilisin BPN' in a crystal environment. Proteins 14(4):451-464
121. Rost B, Sander C (1993) Prediction of protein secondary structure at better than 70% accuracy . J Mol Biol 232(2):584-599 (Pubitemid 23251181)
122. Rost B, Sander C, Schneider R (1994) PHD -an automatic mail server for protein secondary structure prediction. Comput Appl Biosci 10(1):53-60 (Pubitemid 24066811)
123. Rost B (1996) PHD: predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol 266:525-539
124. Dauber-Osguthorpe P, Roberts VA, Osguthorpe DJ, Wolff J, Genest M, Hagler AT (1988) Structure and energetics of ligand binding to proteins: Escherichia coli dihydrofolate reductase-trimethoprim, a drug-receptor system. Proteins 4(1): 31-47
125. Cross FR, Jacobson MD (2000) Conservation and function of a potential substrate-binding domain in the yeast Clb5 B-type cyclin. Mol Cell Biol 20(13):4782-4790 (Pubitemid 30396125)
126. Schulman BA, Lindstrom DL, Harlow E (1998) Substrate recruitment to cyclin-dependent kinase 2 by a multipurpose docking site on cyclin A. Proc Natl Acad Sci USA 95(18): 10453-10458 (Pubitemid 28413088)
127. Morgan DO (1996) Under arrest at atomic resolution. Nature 382(6589):295-296 (Pubitemid 26260437)
128. Spolar RS, Record MT Jr (1994) Coupling of local folding to site-specific binding of proteins to DNA. Science 263(5148):777-784 (Pubitemid 24093205)
129. Malmqvist M (1999) BIACORE: an affinity biosensor system for characterization of biomolecular interactions. Biochem Soc Trans 27(2):335-340 (Pubitemid 29086060)
130. Lacy ER,Wang Y, Post J, Nourse A,WebbW,MapelliM,Musacchio A, Siuzdak G, Kriwacki RW (2005) Molecular basis for the specificity of p27 toward cyclin-dependent kinases that regulate cell division. J Mol Biol 349(4):764-773 (Pubitemid 40725953)
131. Lacy ER, Filippov I, Lewis WS, Otieno S, Xiao L, Weiss S, Hengst L, Kriwacki RW (2004) p27 binds cyclin-CDK complexes through a sequential mechanism involving binding-induced protein folding. Nat Struct Mol Biol 11(4):358-364 (Pubitemid 38436801)
132. Besson A, Hwang HC, Cicero S, Donovan SL, Gurian-West M, Johnson D, Clurman BE, Dyer MA, Roberts JM (2007) Discovery of an oncogenic activity in p27Kip1 that causes stem cell expansion and a multiple tumor phenotype. Genes Dev 21(14):1731-1746 (Pubitemid 47076473)
133. Johnsson B, Löfas S, Lindquist G (1991) Immobilization of proteins to a carboxymethyldextran-modified gold surface for biospecific interaction analysis in surface plasmon resonance sensors. Anal Biochem 198(2):268-277
134. Bienkiewicz EA, Adkins JN, Lumb KJ (2002) Functional consequences of preorganized helical structure in the intrinsically disordered cell-cycle inhibitor p27(Kip1). Biochemistry 41(3):752-759 (Pubitemid 34061975)
135. Galea CA, Wang Y, Sivakolundu SG, Kriwacki RW (2008) Regulation of cell division by intrinsically unstructured proteins: intrinsic flexibility, modularity, and signaling conduits. Biochemistry 47(29):7598-7609 (Pubitemid 352019491)
136. Hengst L, Dulic V, Slingerland JM, Lees E, Reed SI (1994) A cell cycle-regulated inhibitor of cyclin-dependent kinases. Proc Natl Acad Sci USA 91(12):5291-5295 (Pubitemid 24174312)
137. Bowman P, Galea CA, Lacy E, Kriwacki RW (2006) Thermodynamic characterization of interactions between p27(Kip1) and activated and non-activated Cdk2: intrinsically unstructured proteins as thermodynamic tethers. Biochim Biophys Acta 1764(2):182-189
138. Sivakolundu SG, Bashford D, Kriwacki RW (2005) Disordered p27Kip1 exhibits intrinsic structure resembling the Cdk2/cyclin A-bound conformation. J Mol Biol 353(5):1118-1128 (Pubitemid 41503276)
139. Galea CA, Nourse A, Wang Y, Sivakolundu SG, Heller WT, Kriwacki RW (2008) Role of intrinsic flexibility in signal transduction mediated by the cell cycle regulator, p27 Kip1. J Mol Biol 376(3):827-838
140. Xie H, Vucetic S, Iakoucheva LM, Oldfield CJ, Dunker AK, Uversky VN, Obradovic Z (2007) Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions. J Proteome Res 6(5):1882-1898 (Pubitemid 46814512)
141. Vucetic S, Xie H, Iakoucheva LM, Oldfield CJ, Dunker AK, Obradovic Z, Uversky VN (2007) Functional anthology of intrinsic disorder. 2. Cellular components, domains, technical terms, developmental processes, and coding sequence diversities correlated with long disordered regions. J Proteome Res 6(5):1899-1916 (Pubitemid 46814513)
142. Iakoucheva LM, Brown CJ, Lawson JD, Obradović Z, Dunker AK Intrinsic disorder in cellsignaling and cancer-associated proteins. J Mol Biol 323(3):573-584
143. Bloom J, Pagano M (2003) Deregulated degradation of the cdk inhibitor p27 and malignant transformation. Semin Cancer Biol 13(1):41-47 (Pubitemid 36269179)
144. Chu IM, Hengst L, Slingerland JM(2008) The Cdk inhibitor p27 in human cancer: prognostic potential and relevance to anticancer therapy. Nat Rev Cancer 8(4):253-267 (Pubitemid 351430863)
145. Lee J, Kim SS (2009) The function of p27 KIP1 during tumor development. Exp Mol Med 41(11):765-771
146. Blagosklonny MV (2002) Are p27 and p21 cytoplasmic oncoproteins? Cell Cycle 1(6): 391-393
147. Sicinski P, Zacharek S, Kim C (2007) Duality of p27Kip1 function in tumorigenesis. Genes Dev 21(14):1731-1746
148. Chu I, Sun J, Arnaout A, Kahn H, Hanna W, Narod S, Sun P, Tan CK, Hengst L, Slingerland J p27 phosphorylation by Src regulates inhibition of cyclin E-Cdk2. Cell 128(2): 281-294
149. Grimmler M, Wang Y, Mund T, Cilensek Z, Keidel EM, Waddell MB, Jäkel H, Kullmann M, Kriwacki RW, Hengst L (2007) Cdk-inhibitory activity and stability of p27Kip1 are directly regulated by oncogenic tyrosine kinases. Cell 128(2):269-280 (Pubitemid 46123508)
150. Hidaka T, Hama S, Shrestha P, Saito T, Kajiwara Y, Yamasaki F, Sugiyama K, Kurisu K (2009) The combination of low cytoplasmic and high nuclear expression of p27 predicts a better prognosis in high-grade astrocytoma. Anticancer Res 29(2):597-603
151. Mittag T, Orlicky S, Choy WY, Tang X, Lin H, Sicheri F, Kay LE, Tyers M, Forman-Kay JD (2008) Dynamic equilibrium engagement of a polyvalent ligand with a single-site receptor. Proc Natl Acad Sci USA 105(46):17772-17777
152. Mittag T, Marsh J, Grishaev A, Orlicky S, Lin H, Sicheri F, Tyers M, Forman-Kay JD (2010) Structure/function implications in a dynamic complex of the intrinsically disordered Sic1 with the Cdc4 subunit of an SCF ubiquitin ligase. Structure 18(4):494-506
153. Brocca S, Samalíková M, Uversky VN, LottiM, Vanoni M, Alberghina L, Grandori R (2009) Order propensity of an intrinsically disordered protein, the cyclin-dependent-kinase inhibitor Sic1. Proteins 76(3):731-746
154. Brocca S, Testa L, Samalikova M, Grandori R, Lotti M (2011) Defining structural domains of an intrinsically disordered protein: Sic1, the cyclin-dependent kinase inhibitor of Saccharomyces cerevisiae. Mol Biotechnol 47(1):34-42
155. Testa L, Brocca S, Samalikova M, Santambrogio C, Alberghina L, Grandori R (2011) Electrospray ionization-mass spectrometry conformational analysis of isolated domains of an intrinsically disordered protein. Biotechnol J 6(1):96-100
156. Brocca S, Testa L, Sobott F, ?Samalikova M, Natalello A, Papaleo E, Lotti M, De Gioia L, Doglia SM, Alberghina L, Grandori R (2011) Compact conformations of an intrinsically disordered protein: the kinase-inhibitor domain of Sic1. Biophys J 100(9):2243-2252
157. Iakoucheva LM, Radivojac P, Brown CJ, O'Connor TR, Sikes JG, Obradovic Z, Dunker AK (2004) The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res 32(3):1037-1049 (Pubitemid 38854704)
158. Escote X, Zapater M, Clotet J, Posas F (2004) Hog1 mediates cell-cycle arrest in G1 phase by the dual targeting of Sic1. Nat Cell Biol 6(10):997-1002 (Pubitemid 39359853)
159. Zapater M, Clotet J, Escoté X, Posas F (2005) Control of cell
160. Bjornsti MA, Houghton PJ (2004) The TOR pathway: a target for cancer therapy. Nat Rev Cancer 4(5):335-348 (Pubitemid 38579480)
161. Zinzalla V, Graziola M, Mastriani A, Vanoni M, Alberghin L (2007) Rapamycin-mediated G1 arrest involves regulation of the Cdk inhibitor Sic1 in Saccharomyces cerevisiae. Mol Microbiol 63(5):1482-1494
162. Nishizawa M, Kawasumi M, Fujino M, Toh-e A (1998) Phosphorylation of Sic1, a cyclindependent kinase (Cdk) inhibitor, by Cdk including Pho85 kinase is required for its prompt degradation. Mol Biol Cell 9(9):2393-2405 (Pubitemid 28425884)
163. Sedgwick C, Rawluk M, Decesare J, Raithatha S, Wohlschlegel J, Semchuk P, Ellison M, Yates J 3rd, Stuart D (2006) Saccharomyces cerevisiae Ime2 phosphorylates Sic1 at multiple PXS/T sites but is insufficient to trigger Sic1 degradation. Biochem J 399(1):151-160 (Pubitemid 44505416)
164. Meggio F, Pinna LA (2003) One-thousand-and-one substrates of protein kinase CK2? FASEB J 17(3):349-368 (Pubitemid 36292951)
165. Tapia JC, Bolanos-Garcia VM, Sayed M, Allende CC, Allende JE (2004) Cell cycle regulatory protein p27KIP1 is a substrate and interacts with the protein kinase CK2. J Cell Biochem 91(5):865-879
166. Coccetti P, Zinzalla V, Tedeschi G, Russo GL, Fantinato S, Marin O, Pinna LA, Vanoni M, Alberghina L (2006) Sic1 is phosphorylated by CK2 on Ser201 in budding yeast cells. Biochem Biophys Res Commun 346(3):786-793
167. Tripodi F, Zinzalla V, Vanoni M, Alberghina L, Coccetti P (2007) In CK2 inactivated cells the cyclin dependent kinase inhibitor Sic1 is involved in cell-cycle arrest before the onset of S phase. Biochem Biophys Res Commun 359(4):921-927 (Pubitemid 46946905)
168. Xu X, Nakano T, Wick S, Dubay M, Brizuela L (1999) Mechanism of Cdk2/Cyclin E inhibition by p27 and p27 phosphorylation. Biochemistry 38(27):8713-8722
169. Klipp E, Herwig R, Kowald A, Wierling C, Lehrach H (2005) Systems biology in practice. Concepts, implementation and application. Wiley, KGaA
170. Bracken C, Iakoucheva LM, Romero PR, Dunker AK (2004) Combining prediction, computation and experiment for the characterization of protein disorder. Curr Opin Struct Biol 14(5):570-576 (Pubitemid 39311820)
171. Du JT, Li YM, Ma QF, Qiang W, Zhao YF, Abe H, Kanazawa K, Qin XR, Aoyagi R, Ishizuka Y, Nemoto T, Nakanishi H (2005) Synthesis and conformational properties of phosphopeptides related to the human tau protein. Regul Pept 130(1-2):48-5
172. Suenaga A, Kiyatkin AB, Hatakeyama M, Futatsugi N, Okimoto N, Hirano Y, Narumi T, Kawai A, Susukita R, Koishi T, Furusawa H, Yasuoka K, Takada N, Ohno Y, Taiji M, Ebisuzaki T, Hoek JB, Konagaya A, Kholodenko BN (2005) Tyr-317 phosphorylation increases Shc structural rigidity and reduces coupling of domain motions remote from the phosphorylation site as revealed by molecular dynamics simulations. J Biol Chem 279(6):4657-4662 (Pubitemid 38199058)
173. Sidorova JM, Breeden LL (2003) Precocious G1/S transitions and genomic instability: the origin connection. Mutat Res 532(1-2):5-19 (Pubitemid 37492928)
174. Kitano H, Funahashi A, Matsuoka Y, Oda K (2005) Using process diagrams for the graphical representation of biological networks. Nat Biotechnol 23(8):961-966 (Pubitemid 41114029)
175. Fitch I, Dahmann C, Surana U, Amon A, Nasmyth K, Goetsch L, Byers B, Futcher B (1992) Characterization of four B-type cyclin genes of the budding yeast Saccharomyces cerevisiae. Mol Biol Cell 3(7):805-818 (Pubitemid 23084562)
176. Koch C, Nasmyth K (1994) Cell cycle regulated transcription in yeast. Curr Opin Cell Biol 6(3):451-459 (Pubitemid 24170018)
177. Kholodenko BN (2006) Cell-signalling dynamics in time and space. Nat Rev Mol Cell Biol 7(3):165-176
178. Bailly E, Reed SI (1999) Functional characterization of rpn3 uncovers a distinct 19S proteasomal subunit requirement for ubiquitin-dependent proteolysis of cell cycle regulatory proteins in budding yeast. Mol Cell Biol 19(10):6872-6890 (Pubitemid 29441870)
179. Honey S, Schneider BL, Schieltz DM, Yates JR, Futcher B (2001) A novel multiple affinity purification tag and its use in identification of proteins associated with a cyclin-CDK complex. Nucleic Acids Res 29(4):E24
180. Archambault V, Chang EJ, Drapkin BJ, Cross FR, Chait BT, Rout MP (2004) Targeted proteomic study of the cyclin-Cdk module. Mol Cell 14(6):699-711 (Pubitemid 38780845)
181. Gavin AC, Aloy P, Grandi P, Krause R, Boesche M, Marzioch M, Rau C, Jensen LJ, Bastuck S, Dümpelfeld B, Edelmann A, Heurtier MA, Hoffman V, Hoefert C, Klein K, Hudak M, Michon AM, Schelder M, Schirle M, Remor M, Rudi T, Hooper S, Bauer A, Bouwmeester T, Casari G, Drewes G, Neubauer G, Rick JM, Kuster B, Bork P, Russell RB, Superti-Furga G (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440(7084):631-636
182. Krogan NJ, Cagney G, Yu H, Zhong G, Guo X, Ignatchenko A, Li J, Pu S, Datta N, Tikuisis AP, Punna T, Peregrín-Alvarez JM, Shales M, Zhang X, Davey M, Robinson MD, Paccanaro A, Bray JE, Sheung A, Beattie B, Richards DP, Canadien V, Lalev A, Mena F, Wong P, Starostine A, Canete MM, Vlasblom J, Wu S, Orsi C, Collins SR, Chandran S, Haw R, Rilstone JJ, Gandi K, Thompson NJ, Musso G, St Onge P, Ghanny S, Lam MH, Butland G, Altaf-Ul AM, Kanaya S, Shilatifard A, O'Shea E, Weissman JS, Ingles CJ, Hughes TR, Parkinson J, Gerstein M, Wodak SJ, Emili A, Greenblatt JF (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440(7084):637-643
183. Collins SR, Kemmeren P, Zhao XC, Greenblatt JF, Spencer F, Holstege FC, Weissman JS, Krogan NJ (2007) Toward a comprehensive atlas of the physical interactome of Saccharomyces cerevisiae. Mol Cell Proteom 6(3):439-450 (Pubitemid 46554539)
184. Breitkreutz A, Choi H, Sharom JR, Boucher L, Neduva V, Larsen B, Lin ZY, Breitkreutz BJ, Stark C, Liu G, Ahn J, Dewar-Darch D, Reguly T, Tang X, Almeida R, Qin ZS, Pawson T, Gingras AC, Nesvizhskii AI, Tyers M (2010) A global protein kinase and phosphatase interaction network in yeast. Science 328(5981):1043-1046
185. Nair DK, Jose M, Kuner T, ZuschratterW, Hartig R (2006) FRET-FLIM at nanometer spectral resolution from living cells. Opt Express 14(25):12217-12229 (Pubitemid 44907564)
186. RizzoMA, Springer GH, Granada B, Piston DW(2004) An improved cyan fluorescent protein variant useful for FRET. Nat Biotechnol 22(4):445-449 (Pubitemid 38451376)
187. Schreiber G, Barberis M, Scolari S, Klaus C, Herrmann A, Klipp E (2012) Unraveling interactions of cell cycle-regulating proteins Sic1 and B-type cyclins in living yeast cells: a FLIMFRET approach. FASEB J 26, doi:10.1096/fj.11-192518
188. Ubersax JA, Woodbury EL, Quang PN, Paraz M, Blethrow JD, Shah K, Shokat KM, Morgan DO (2003) Targets of the cyclin-dependent kinase Cdk1. Nature 425(6960):859-864 (Pubitemid 37351471)
189. Stuart D, Wittenberg C (1998) CLB5 and CLB6 are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint. Genes Dev 12(17):2698-2710 (Pubitemid 28420650)
190. Richardson H, Lew DJ, Henze M, Sugimoto K, Reed SI (1992) Cyclin-B homologs in Saccharomyces cerevisiae function in S phase and in G2. Genes Dev 6(11):2021-2034
191. López-Avilés S, Kapuy O, Novák B, Uhlmann F (2009) Irreversibility of mitotic exit is the consequence of systems-level feedback. Nature 459(7246):592-595
192. Cross FR, Archambault V,MillerM, Klovstad M (2002) Testing a mathematical model of the yeast cell cycle. Mol Biol Cell 13(1):52-70 (Pubitemid 34106058)
193. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, Weissman JS (2003) Global analysis of protein expression in yeast. Nature 425(6959): 737-741 (Pubitemid 37314318)
194. Thornton BR, Toczyski DP (2003) Securin and B-cyclin/CDK are the only essential targets of the APC. Nat Cell Biol 5(12):1090-1094 (Pubitemid 37509116)
195. MillerME, Cross FR (2001) Cyclin specificity: how many wheels do you need on a unicycle? J Cell Sci 114 (Pt 10):1811-1820