Boolean model of yeast apoptosis as a tool to study yeast and human apoptotic regulations

Frontiers in Physiology

Volumn 3 DEC, Issue , 2012, Pages

  Kazemzadeh, Laleh ^a,b   Cvijovic, Marija ^a   Petranovic, Dina ^a  

^a CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Apoptosis; Bcl 2 family; Bir1; Boolean modeling; Hog1; Stm1; VCP

Indexed keywords

APOPTOSIS REGULATORY PROTEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BIR1P; PROTEIN HOG1P; PROTEIN KINASE B; PROTEIN STM1P; UNCLASSIFIED DRUG; VALOSIN CONTAINING PROTEIN;

APOPTOSIS; ARTICLE; BOOLEAN MODEL; CELL SURVIVAL; COMPUTER MODEL; CONTROLLED STUDY; HEAT STRESS; MATHEMATICAL MODEL; MOLECULAR MODEL; PROTEIN FUNCTION; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; YEAST;

EID: 84884138464     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00446     Document Type: Article

References (93)

1. Aerts, A. M., Zabrocki, P., François, I. E., Carmona-Gutierrez, D., Govaert, G., Mao, C., et al. (2008). Ydc1p ceramidase triggers organelle fragmentation, apoptosis and accelerated ageing in yeast. Cell. Mol. Life Sci. 65, 1933-1942.
2. Ahn, S. H., Diaz, R. L., Grunstein, M., and Allis, C. D. (2006). Histone H2B deacetylation at lysine 11 is required for yeast apoptosis induced by phosphorylation of H2B at serine 10. Mol. Cell 24, 211-220.
3. Albertyn, J., and Hohmann, S. (1994). Characterization of the osmotic-stress response in Saccharomyces cerevisiae: osmotic stress and glucose repression regulate glycerol-3-phosphate dehydrogenase independently. Curr. Genet. 25, 12-18.
4. Almeida, B., Silva, A., Mesquita, A., Sampaio-Marques, B., Rodrigues, F., and Ludovico, P. (2008). Drug-induced apoptosis in yeast. Biochim. Biophys. Acta 7, 1436-1448.
5. Blanchard, F., Rusiniak, M. E., Sharma, K., Sun, X., Todorov, I., Castellano, M. M., et al. (2002). Targeted destruction of DNA replication protein Cdc6 by cell death pathways in mammals and yeast. Mol. Biol. Cell 13, 1536-1549.
6. Braun, R. J., and Zischka, H. (2008). Mechanisms of Cdc48/VCP-mediated cell death-from yeast apoptosis to human disease. Biochim. Biophys. Acta 1783, 1418-1435.
7. Brewster, J. L., de Valoir, T., Dwyer, N. D., Winter, E., and Gustin, M. C. (1993). An osmosensing signal transduction pathway in yeast. Science 259, 1760-1763.
8. Buttner, S., Eisenberg, T., Carmona-Gutierrez, D., Ruli, D., Knauer, H., Ruckenstuhl, C., et al. (2007). Endonuclease G regulates budding yeast life and death. Mol. Cell 25, 233-246.
9. Carmona-Gutierrez, D., Eisenberg, T., Büttner, S., Meisinger, C., Kroemer, G., and Madeo, F. (2010a). Apoptosis in yeast: triggers, pathways, subroutines. Cell. Death Differ. 17, 763-773.
10. Carmona-Gutierrez, D., Ruckenstuhl, C., Bauer, M. A., Eisenberg, T., Buttner, S., and Madeo, F. (2010b). Cell death in yeast: growing applications of a dying buddy. Cell Death Differ. 17, 733-734.
11. Cherry, J. M., Hong, E. L., Amundsen, C., Balakrishnan, R., Binkley, G., Chan, E. T., et al. (2011). Saccharomyces genome database: the genomics resource of budding yeast. Nucleic Acids Res. 40, D700-D705. [Database issue]
12. Datta, S. R., Dudek, H., Tao, X., Masters, S., Fu, H., Gotoh, Y., et al. (1997). Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91, 231-241.
13. Davidich, M., and Bornholdt, S. (2008). Boolean network model predicts cell cycle sequence of fission yeast. PLoS ONE 3:e1672. doi: 10.1371/journal.pone.0001672
14. de Nadal, E., Zapater, M., Alepuz, P. M., Sumoy, L., Mas, G., and Posas, P. (2004). The MAPK Hog1 recruits Rpd3 histone deacetylase to activate osmoresponsive genes. Nature 427, 370-374.
15. Di Cara, A., Garg, A., De Micheli, G., Xenarios, I., and Mendoza, L. (2007). Dynamic simulation of regulatory networks using SQUAD. BMC Bioinformatics 8:462. doi:10.1186/1471-2105-8-462
16. Drexler, H. C. A. (1997). Activation of the cell death program by inhibition of proteasome function. Proc. Natl. Acad. Sci. U.S.A. 94, 855-860.
17. Eisenberg, T., Buttner, S., Kroemer, G., and Madeo, F. (2007). The mitochondrial pathway in yeast apoptosis. Apoptosis 12, 1011-1023.
18. Fahrenkrog, B., Sauder, U., and Aebi, U. (2004). The S. cerevisiae HtrA-like protein Nma111p is a nuclear serine protease that mediates yeast apoptosis. J. Cell Sci. 117, 115-126.
19. Falasca, M. (2010). PI3K/Akt signalling pathway specific inhibitors: a novel strategy to sensitize cancer cells to anti-cancer drugs. Curr. Pharm. Des. 16, 1410-1416.
20. Fauré, A., Naldi, A., Chaouiya, C., and Thieffry, D. (2006). Dynamic analysis of a generic Boolean model for the control of the mammalian cell cycle. Bioinformatics 22, 124-131.
21. Ferrigno, P., Posas, F., Koepp, D., Saito, H., and Silver, P. A. (1998). Regulated nucleo/cytoplasmic exchange of HOG1 MAPK requires the importin beta homologs NMD5 and XPO1. EMBO J. 17, 5606-5614.
22. Frohlich, K. U., Fussi, H., and Ruckenstuhl, C. (2007). Yeast apoptosis-from genes to pathways. Semin. Cancer Biol. 17, 112-121.
23. Funahashi, A., Tanimura, N., Matsuoka, Y., Yosinaga, N., and Kitano, H. (2003). CellDesigner: a process diagram editor for gene-regulatory and biochemical networks. BIOSILICO 1, 159-162.
24. Garbarino, J., Padamsee, M., Wilcox, L., Oelkers, P. M., D'Ambrosio, D., Ruggles, K., et al. (2009). Sterol and diacylglycerol acyltransferase deficiency triggers fatty acid-mediated cell death. J. Biol. Chem. 284, 30994-31005.
25. Greenhalf, W., Stephan, C., and Chaudhuri, B. (1996). Role of mitochondria and C-terminal membrane anchor of Bcl-2 in Bax induced growth arrest and mortality in Saccharomyces cerevisiae. FEBS Lett. 380, 169-175.
26. Gupta, S., Bisht, S. S., Kukreti, R., Jain, S., and Brahmachari, S. K. (2007). Boolean network analysis of neurotransmitter signaling pathway. J. Theor. Biol. 244, 463-469.
27. Hahn, J. S., and Thiele, D. J. (2002). Regulation of the Saccharomyces cerevisiae Slt2 kinase pathway by the stress-inducible Sdp1 dual specificity phosphatase. J. Biol. Chem. 277, 21278-21284.
28. Handorf, T., and Klipp, E. (2012). Modeling mechanistic biological networks: an advanced Boolean approach. Bioinformatics 28, 557-563.
29. Hauptmann, P., Riel, C., Kunz-Schughart, L. A., Fröhlich, K. U., Madeo, F., and Lehle, L. (2006). Defects in N-glycosylation induce apoptosis in yeast. Mol. Microbiol. 59, 765-778.
30. Hers, I., Vincent, E. E., and Tavaré, J. M. (2011). Akt signalling in health and disease. Cell. Signal. 23, 1515-1527.
31. Hirabayashi, M., Inoue, K., Tanaka, K., Nakadate, K., Ohsawa, Y., Kamei, Y., et al. (2001). VCP/p97 in abnormal protein aggregates, cytoplasmic vacuoles, and cell death, phenotypes relevant to neurodegeneration. Cell Death Differ. 8, 977-984.
32. Hohmann, S. (2002). Osmotic stress signaling and osmoadaptation in yeast. Microbiol. Mol. Biol. Rev. 66, 300-372.
33. Hohmann, S. (2009). Control of high osmolarity signalling in the yeast Saccharomyces cerevisiae. FEBS Lett. 583, 4025-4029.
34. Hucka, M., Finney, A., Sauro, H. M., Bolouri, H., Doyle, J. C., and Kitano, H. (2003). The systems biology markup language (SBML): a medium for representation and exchange of biochemical network models. Bioinformatics 19, 524-531.
35. Imamuraab, S., Ojimaa, N., and Yamashitaa, M. (2003). Cold-inducible expression of the cell division cycle gene CDC48 and its promotion of cell proliferation during cold acclimation in zebrafish cells. FEBS Lett. 549, 14-20.
36. Ishigaki, S., Hishikawa, N., Niwa, J., Iemura, S., Natsume, T., Hori, S., et al. (2004). Physical and functional interaction between dorfin and valosin-containing protein that are colocalized in ubiquitylated inclusions in neurodegenerative disorders. J. Biol. Chem. 279, 51376-51385.
37. Janes, K. A., Albeck, J. G., Sorger, S. G. P. K., Lauffenburger, D. A., and Yaffe, M. B. (2005). A systems model of signaling identifies a molecular basis set for cytokine-induced apoptosis. Science 310, 1646-1653.
38. Kanehisa, M., and Goto, S. (2000). KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30.
39. Kataoka, T., Powers, S., McGill, C., Fasano, O., Strathern, J., Broach, J., et al. (1984). Genetic analysis of yeast RAS1 and RAS2 genes. Cell 37, 437-445.
40. Kauffman, S. A. (1969). Metabolic stability and epigenesis in randomly constructed genetic nets. J. Theor. Biol. 22, 437-467.
41. Kharbanda, S., Pandey, P., Schofield, L., Israels, S., Roncinske, R., Yoshida, K., et al. (1997). Role for Bcl-xL as an inhibitor of cytosolic cytochrome C accumulation in DNA damage-induced apoptosis. Proc. Natl. Acad. Sci. U.S.A. 13, 6939-6942.
42. Khoury, C. M., Yang, Z., Li, X. Y., Vignali, M., Fields, S., and Greenwood, M. T. (2008). A TSC22-like motif defines a novel antiapoptotic protein family. FEMS Yeast Res. 8, 540-563.
43. Klamt, S., Saez-Rodriguez, J., Lindquist, J. A., Simeoni, L., and Gilles, E. D. (2006). A methodology for the structural and functional analysis of signaling and regulatory networks. BMC Bioinformatics 7:56. doi:10.1186/1471-2105-7-56
44. Krasley, E., Cooper, K. F., Mallory, M. J., Dunbrack, R., and Strich, R. (2006). Regulation of the oxidative stress response through Slt2p-dependent destruction of cyclin C in Saccharomyces cerevisiae. Genetics 172, 1477-1486.
45. Krumsiek, J., Pölsterl, S., Wittmann, D. M., and Theis, F. J. (2010). Odefy - from discrete to continuous models. BMC Bioinformatics 11:233. doi:10.1186/1471-2105-11-233
46. Li, C., Donizelli, M., Rodriguez, N., Dharuri, H., Endler, L., Chelliah, V., et al. (2010). BioModels Database: an enhanced, curated and annotated resource for published quantitative kinetic models. BMC Syst. Biol. 4:92. doi:10.1186/1752-0509-4-92
47. Li, W., Sun, L., Liang, Q., Wang, J., Mo, W., and Zhou, B. (2006). Yeast AMID homologue Ndi1p displays respiration-restricted apoptotic activity and is involved in chronological aging. Mol. Biol. Cell 17, 1802-1811.
48. Liang, Q., and Zhou, B. (2007). Copper and manganese induce yeast apoptosis via different pathways. Mol. Biol. Cell 18, 4741-4749.
49. Ligr, M., Velten, I., Fröhlich, E., Madeo, F., Ledig, M., Fröhlich, K. U., et al. (2001). The proteasomal substrate Stm1 participates in apoptosis-like cell death in yeast. Mol. Biol. Cell 12, 2422-2432.
50. Low, C. P., Shui, G., Liew, L. P., Buttner, S., Madeo, F., Dawes, I. W., et al. (2008). Caspase-dependent and -independent lipotoxic cell-death pathways in fission yeast. J. Cell. Sci. 15, 2671-2684.
51. Ludovico, P., Rodrigues, F., Almeida, A., Silva, M. T., Barrientos, A., and Côrte-Real, M. (2002). Cytochrome c release and mitochondria involvement in programmed cell death induced by acetic acid in Saccharomyces cerevisiae. Mol. Biol. Cell 13, 2598-2606.
52. Ludovico, P., Sousa, M. J., Silva, M. T., Leao, C., and Côrte-Real, M. (2001). Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 147, 2409-2415.
53. Madeo, F., Carmona-Gutierrez, D., Ring, J., Buttner, S., Eisenberg, T., and Kroemer, G. (2009). Caspase-dependent and caspase-independent cell death pathways in yeast. Biochem. Biophys. Res. Commun. 382, 227-231.
54. Madeo, F., Fröhlich, E., and Fröhlich, K. U. (1997). A yeast mutant showing diagnostic markers of early and late apoptosis. J. Cell Biol. 139, 729-734.
55. Madeo, F., Fröhlich, E., Ligr, M., Grey, M., Sigrist, S. J., Wolf, D. H., et al. (1999). Oxygen stress: a regulator of apoptosis in yeast. J. Cell Biol. 145, 757-767.
56. Madeo, F., Herker, E., Maldener, C., Wissing, S., Lächelt, S., Herlan, M., et al. (2002). A caspase-related protease regulates apoptosis in yeast. Mol. Cell 9, 911-917.
57. Mai, Z., and Liu, H. (2009). Boolean network-based analysis of the apoptosis network: irreversible apoptosis and stable surviving. J. Theor. Biol. 259, 760-769.
58. Manon, S., Chaudhuri, B., and Guérin, M. (1997). Release of cytochrome c and decrease of cytochrome c oxidase in Bax-expressing yeast cells, and prevention of these effects by coexpression of Bcl-xL. FEBS Lett. 415, 29-32.
59. Mazzoni, C., Herker, E., Palermo, V., Jungwirth, H., Eisenberg, T., Madeo, F., et al. (2005). Yeast caspase 1 links messenger RNA stability to apoptosis in yeast. EMBO Rep. 6, 1076-1081.
60. Mendoza, L., and Xenarios, I. (2006). A method for the generation of standardized qualitative dynamical systems of regulatory networks. Theor. Biol. Med. Model. 3, 13.
61. Mizuno, Y., Hori, S., Kakizuka, A., and Okamoto, K. (2003). Vacuole-creating protein in neurodegenerative diseases in humans. Neurosci. Lett. 343, 77-80.
62. Nelson, L. D., Musso, M., and Van Dyke, M. W. (2000). The yeast STM1 gene encodes a purine motif triple helical DNA-binding protein. J. Biol. Chem. 275, 5573-5581.
63. Owsianowski, E., Walter, D., and Fahrenkrog, B. (2008). Negative regulation of apoptosis in yeast. Biochim. Biophys. Acta 1783, 1303-1310.
64. Pereira, C., Camougrand, N., Manon, S., Sousa, M. J., and Côrte-Real, M. (2007). ADP/ATP carrier is required for mitochondrial outer membrane permeabilization and cytochrome c release in yeast apoptosis. Mol. Microbiol. 66, 571-582.
65. Qiu, J., Yoon, J. H., and Shen, B. (2005). Search for apoptotic nucleases in yeast: role of Tat-D nuclease in apoptotic DNA degradation. J. Biol. Chem. 280, 15370-15379.
66. Ring, G., Khoury, C. M., Solar, A. J., Yang, Z., Mandato, C. A., and Greenwood, M. T. (2008). Transmembrane protein 85 from both human (TMEM85) and yeast (YGL231c) inhibit hydrogen peroxide mediated cell death in yeast. FEBS Lett. 582, 2637-2642.
67. Ruchaud, S., Carmena, M., and Earnshaw, W. C. (2007). Chromosomal passengers: conducting cell division. Nat. Rev. Mol. Cell Biol. 8, 798-812.
68. Sato, T., Hanada, M., Bodrug, S., Irie, S., Iwama, N., Boise, L. H., et al. (1994). Interactions among members of the Bcl-2 protein family analyzed with a yeast two hybrid system. Proc. Natl. Acad. Sci. U.S.A. 91, 9238-9242.
69. Schlatter, R., Schmich, K., Vizcarra, I. A., Scheurich, P., Sauter, T., Borner, C., et al. (2009). On/off and beyond - a boolean model of apoptosis. PLoS Comput. Biol. 5:e1000595. doi:10.1371/journal.pcbi.1000595
70. Schmelzle, T., Beck, T., Martin, D. E., and Hall, M. N. (2004). Activation of the RAS/cyclic AMP pathway suppresses a TOR deficiency in yeast. Mol. Cell Biol. 24, 338-351.
71. Song, C., Wang, Q., and Li, C. C. (2003). ATPase activity of p97-valosin-containing protein (VCP). D2 mediate the major enzyme activity and D1 contributes in heat-induced activity. J. Biol. Chem. 278, 3648-3655.
72. Stelling, J. (2004). Mathematical models in microbial systems biology. Curr. Opin. Microbiol. 7, 513-518.
73. Thomas, R., and D'Ari, R. (1990). Biological Feedback. Boca Raton: CRC Press.
74. Uren, A. G., Coulson, E. J., and Vaux, D. L. (1998). Conservation of baculovirus inhibitor of apoptosis repeat proteins (BIRPs) in viruses, nematodes, vertebrates and yeasts. Trends Biochem. Sci. 23, 159-162.
75. Van Wuytswinkel, O., Reiser, V., Siderius, M., Kelders, M. C., Ammerer, G., Ruis, H., et al. (2000). Response of Saccharomyces cerevisiae to severe osmotic stress: evidence for a novel activation mechanism of the HOG MAP kinase pathway. Mol. Microbiol. 37, 382-397.
76. Vander Heiden, M. G., Choy, J. S., VanderWeele, D. J., Brace, J. L., Harris, M. H., Bauer, D. E., et al. (2002). Bcl-x(L) complements Saccharomyces cerevisiae genes that facilitate the switch from glycolytic to oxidative metabolism. J. Biol. Chem. 277, 44870-44876.
77. Vandermoere, F., El Yazidi-Belkoura, I., Slomianny, C., Demont, Y., Bidaux, G., Adriaenssens, E., et al. (2006). The valosin-containing protein (VCP) is a target of Akt signaling required for cell survival. J. Biol. Chem. 20, 14307-14313.
78. Vernis, L., Facca, C., Delagoutte, E., Soler, N., Chanet, R., Guiard, B., et al. (2009). A newly identified essential complex, Dre2-Tah18, controls mitochondria integrity and cell death after oxidative stress in yeast. PLoS ONE 4:e4376. doi:10.1371/journal.pone.0004376
79. Wadskog, I., Maldener, C., Proksch, A., Madeo, F., and Adler, L. (2004). Yeast lacking the SRO7/SOP1-encoded tumor suppressor homologue show increased susceptibility to apoptosis-like cell death on exposure to NaCl stress. Mol. Biol. Cell 15, 1436-1444.
80. Walter, D., Wissing, S., Madeo, F., and Fahrenkrog, B. (2006). The inhibitor-of-apoptosis protein Bir1p protects against apoptosis in S. cervisiae and is a substrate for the yeast homologue of Omi/HtrA2. J. Cell. Sci. 119, 1843-1851.
81. Wang, Q., Song, C., and Li, C. H. (2004). Molecular perspective on p97-VCP: progress in understanding its structure and diverse biological function. J. Struct. Biol. 164, 44-57.
82. Warmka, J., Hanneman, J., Lee, J., Amin, D., and Ota, I. (2001). Ptc1, a type 2C Ser/Thr phosphatase, inactivates the HOG pathway by dephosphorylating the mitogen-activated protein kinase Hog1. Mol. Cell. Biol. 21, 51-60.
83. Weinberger, M., Ramachandran, L., Feng, L., Sharma, K., Sun, X., Marchetti, M., et al. (2005). Apoptosis in budding yeast caused by defects in initiation of DNA replication. J. Cell Sci. 118, 3543-3553.
84. Westfall, P. J., Ballon, D. R., and Thorner, J. (2004). When the stress of your environment makes you go HOG wild. Science 306, 1511-1512.
85. Winderickx, J., Delay, C., De Vos, A., Klinger, H., Pellens, K., Vanhelmont, T., et al. (2008). Protein folding diseases and neurodegeneration: lessons learned from yeast. Biochim. Biophys. Acta 1783, 1381-1395.
86. Winkler, A., Arkind, C., Mattison, C. P., Burkholder, A., Knoche, K., and Ota, I. (2002). Heat stress activates the yeast high-osmolarity glycerol mitogen-activated protein kinase pathway, and protein tyrosine phosphatases are essential under heat stress. Eukaryot. Cell 1, 163-173.
87. Wissing, S., Ludovico, P., Herker, E., Buttner, S., Engelhardt, S. M., Decker, T., et al. (2004). An AIF orthologue regulates apoptosis in yeast. J. Cell Biol. 166, 969-974.
88. Wittmann, D. M., Krumsiek, J., Saez-Rodriguez, J., Lauffenburger, D. A., Klamt, S., and Theis, F. J. (2009). Transforming Boolean models to continuous models: methodology and application to T-cell receptor signaling. BMC Syst. Biol. 3:98. doi:10.1186/1752-0509-3-98
89. Wolkenhauer, O. (2002). Mathematical modelling in the post-genome era: under-standing genome expression and regulation - a system theoretic approach. BioSystems 65, 1-18.
90. Wood, D. R., Poullet, P., Wilson, B. A., Khalil, M., Tanaka, K., Cannon, J. F., et al. (1994). Biochemical characterization of yeast RAS2 mutants reveals a new region of ras protein involved in the interaction with GTPase-activating proteins. J. Biol. Chem. 269, 5322-5327.
91. Yang, H., Ren, Q., and Zhang, Z. (2008). Cleavage of Mcd1 by caspase-like protease Esp1 promotes apoptosis in budding yeast. Mol. Biol. Cell 19, 2127-2134.
92. Young, C., Mapes, J., Hanneman, J., Al-Zarban, S., and Ota, I. (2002). Role of Ptc2 type 2C Ser/Thr phosphatase in yeast high-osmolarity glycerol pathway inactivation. Eukaryot. Cell 1, 1032-1040.
93. Zhang, N. N., Dudgeon, D. D., Paliwal, S., Levchenko, A., Grote, E., and Cunningham, K. W. (2006). Multiple signaling pathways regulate yeast cell death during the response to mating pheromones. Mol. Biol. Cell 17, 3409-3422.