Yeast as a model eukaryote in toxinology: A functional genomics approach to studying the molecular basis of action of pharmacologically active molecules

Toxicon

Volumn 60, Issue 4, 2012, Pages 558-571

  Mattiazzi, Mojca ^a,d   Petrovič, Uroš ^a   Križaj, Igor ^a,b,c  

^a JO EF STEFAN INSTITUTE   (Slovenia)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

^c Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins   (Slovenia)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Functional genomics; High throughput screening; Neurobiology; Phospholipase A 2; Saccharomyces cerevisiae

Indexed keywords

AMMODYTOXIN A; FUNGAL PROTEIN; NEUROTOXIN; PHOSPHOLIPASE A2;

AMINO ACID SEQUENCE; DEGENERATIVE DISEASE; EUKARYOTE; EXPERIMENTAL MODEL; FUNCTIONAL GENOMICS; FUNGAL STRAIN; GENE INTERACTION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENOTYPE PHENOTYPE CORRELATION; HAPLOINSUFFICIENCY; HIGH THROUGHPUT SCREENING; MEDICAL RESEARCH; MOLECULAR MECHANICS; NEUROBIOLOGY; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PLASMID; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; REVIEW; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; TOXICOLOGY; YEAST;

EUKARYOTIC CELLS; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENES, FUNGAL; GENOME, FUNGAL; GENOMICS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MODELS, THEORETICAL; PROTEOME; SACCHAROMYCES CEREVISIAE; TOXICOLOGY;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84863774663     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2012.03.014     Document Type: Review

References (154)

1. Babcock M., de Silva D., Oaks R., Davis-Kaplan S., Jiralerspong S., Montermini L., Pandolfo M., Kaplan J. Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science 1997, 276:1709-1712.
2. Bach S., Talarek N., Andrieu T., Vierfond J.M., Mettey Y., Galons H., Dormont D., Meijer L., Cullin C., Blondel M. Isolation of drugs active against mammalian prions using a yeast-based screening assay. Nat. Biotechnol. 2003, 21:1075-1081.
3. Baetz K., McHardy L., Gable K., Tarling T., Reberioux D., Bryan J., Andersen R.J., Dunn T., Hieter P., Roberge M. Yeast genome-wide drug-induced haploinsufficiency screen to determine drug mode of action. Proc. Natl. Acad. Sci. Unites States Am 2004, 101:4525-4530.
4. Baker K., Sengupta D., Salazar-Jimenez G., Cornish V.W. An optimized dexamethasone-methotrexate yeast 3-hybrid system for high-throughput screening of small molecule-protein interactions. Anal. Biochem. 2003, 315:134-137.
5. Bassett D.E., Boguski M.S., Spencer F., Reeves R., Kim S., Weaver T., Hieter P. Genome cross-referencing and XREFdb: implications for the identification and analysis of genes mutated in human disease. Nat. Genet. 1997, 15:339-344.
6. Bastow E.L., Gourlay C.W., Tuite M.F. Using yeast models to probe the molecular basis of amyotrophic lateral sclerosis. Biochem. Soc. Trans. 2011, 39:1482-1487.
7. Blackburn E.H. Telomeres and telomerase: the means to the end (Nobel lecture). Angew. Chem. Int. Ed. Engl. 2010, 49:7405-7421.
8. Bodovitz S., Joos T., Bachmann J. Protein biochips: the calm before the storm. Drug Discov. Today 2005, 10:283-287.
9. Botstein D., Chervitz S.A., Cherry J.M. Yeast as a model organism. Science 1997, 277:1259-1260.
10. Boutros M., Kiger A.A., Armknecht S., Kerr K., Hild M., Koch B., Haas S.A., Paro R., Perrimon N. Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 2004, 303:832-835.
11. Bruce C., Fitches E.C., Chougule N., Bell H.A., Gatehouse J.A. Recombinant conotoxin, TxVIA, produced in yeast has insecticidal activity. Toxicon 2011, 58:93-100.
12. Butcher R.A., Schreiber S.L. A small molecule suppressor of FK506 that targets the mitochondria and modulates ionic balance in Saccharomyces cerevisiae. Chem. Biol. 2003, 10:521-531.
13. Butcher R.A., Bhullar B.S., Perlstein E.O., Marsischky G., LaBaer J., Schreiber S.L. Microarray-based method for monitoring yeast overexpression strains reveals small-molecule targets in TOR pathway. Nat. Chem. Biol. 2006, 2:103-109.
14. Carpenter A.E., Jones T.R., Lamprecht M.R., Clarke C., Kang I.H., Friman O., Guertin D.A., Chang J.H., Lindquist R.A., Moffat J., Golland P., Sabatini D.M. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol. 2006, 7:R100.
15. Castrejon F., Gomez A., Sanz M., Duran A., Roncero C. The RIM101 pathway contributes to yeast cell wall assembly and its function becomes essential in the absence of mitogen-activated protein kinase Slt2p. Eukaryot. Cell 2006, 5:507-517.
16. Castrillo J.I., Oliver S.G. Yeast as a touchstone in post-genomic research: strategies for integrative analysis in functional genomics. J. Biochem. Mol. Biol. 2004, 37:93-106.
17. Chen S.C., Zhao T., Gordon G.J., Murphy R.F. Automated image analysis of protein localization in budding yeast. Bioinformatics 2007, 23:i66-71.
18. Chien P., Weissman J.S., DePace A.H. Emerging principles of conformation-based prion inheritance. Annu. Rev. Biochem. 2004, 73:617-656.
19. Chopra V., Fox J.H., Lieberman G., Dorsey K., Matson W., Waldmeier P., Housman D.E., Kazantsev A., Young A.B., Hersch S. A small-molecule therapeutic lead for Huntington's disease: preclinical pharmacology and efficacy of C2-8 in the R6/2 transgenic mouse. Proc. Natl. Acad. Sci. Unites States Am 2007, 104:16685-16689.
20. Christie K.R., Hong E.L., Cherry J.M. Functional annotations for the Saccharomyces cerevisiae genome: the knowns and the known unknowns. Trends Microbiol. 2009, 17:286-294.
21. Clare J.J., Rayment F.B., Ballantine S.P., Sreekrishna K., Romanos M.A. High-level expression of tetanus toxin fragment C in Pichia pastoris strains containing multiple tandem integrations of the gene. Bio tech 1991, 9:455-460.
22. Costanzo M., Baryshnikova A., Bellay J., Kim Y., Spear E.D., Sevier C.S., Ding H., Koh J.L., Toufighi K., Mostafavi S., Prinz J., St Onge R.P., VanderSluis B., Makhnevych T., Vizeacoumar F.J., Alizadeh S., Bahr S., Brost R.L., Chen Y., Cokol M., Deshpande R., Li Z., Lin Z.Y., Liang W., Marback M., Paw J., San Luis B.J., Shuteriqi E., Tong A.H., van Dyk N., Wallace I.M., Whitney J.A., Weirauch M.T., Zhong G., Zhu H., Houry W.A., Brudno M., Ragibizadeh S., Papp B., Pal C., Roth F.P., Giaever G., Nislow C., Troyanskaya O.G., Bussey H., Bader G.D., Gingras A.C., Morris Q.D., Kim P.M., Kaiser C.A., Myers C.L., Andrews B.J., Boone C. The genetic landscape of a cell. Science 2010, 327:425-431.
23. Cusick K.D., Boyer G.L., Wilhelm S.W., Sayler G.S. Transcriptional profiling of Saccharomyces cerevisiae upon exposure to saxitoxin. Environ. Sci. Technol. 2009, 43:6039-6045.
24. Davierwala A.P., Haynes J., Li Z., Brost R.L., Robinson M.D., Yu L., Mnaimneh S., Ding H., Zhu H., Chen Y., Cheng X., Brown G.W., Boone C., Andrews B.J., Hughes T.R. The synthetic genetic interaction spectrum of essential genes. Nat. Genet. 2005, 37:1147-1152.
25. DeJesus-Hernandez M., Mackenzie I.R., Boeve B.F., Boxer A.L., Baker M., Rutherford N.J., Nicholson A.M., Finch N.A., Flynn H., Adamson J., Kouri N., Wojtas A., Sengdy P., Hsiung G.Y., Karydas A., Seeley W.W., Josephs K.A., Coppola G., Geschwind D.H., Wszolek Z.K., Feldman H., Knopman D.S., Petersen R.C., Miller B.L., Dickson D.W., Boylan K.B., Graff-Radford N.R., Rademakers R. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011, 72:245-256.
26. DeRisi J.L., Iyer V.R., Brown P.O. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 1997, 278:680-686.
27. Dux M.P., Barent R., Sinha J., Gouthro M., Swanson T., Barthuli A., Inan M., Ross J.T., Smith L.A., Smith T.J., Webb R., Loveless B., Henderson I., Meagher M.M. Purification and scale-up of a recombinant heavy chain fragment C of botulinum neurotoxin serotype E in Pichia pastoris GS115. Protein Expr. Purif. 2006, 45:359-367.
28. Dux M.P., Huang J., Barent R., Inan M., Swanson S.T., Sinha J., Ross J.T., Smith L.A., Smith T.J., Henderson I., Meagher M.M. Purification of a recombinant heavy chain fragment C vaccine candidate against botulinum serotype C neurotoxin [rBoNTC(H(c))] expressed in Pichia pastoris. Protein Expr. Purif. 2011, 75:177-185.
29. Ericson E., Gebbia M., Heisler L.E., Wildenhain J., Tyers M., Giaever G., Nislow C. Off-target effects of psychoactive drugs revealed by genome-wide assays in yeast. PLoS Genet. 2008, 4:e1000151.
30. Fang H., Luo W., Henkel J., Barbieri J., Green N. A yeast assay probes the interaction between botulinum neurotoxin serotype B and its SNARE substrate. Proc. Natl. Acad. Sci. Unites States Am 2006, 103:6958-6963.
31. Fetchko M., Auerbach D., Stagljar I. Yeast genetic methods for the detection of membrane protein interactions: potential use in drug discovery. BioDrugs 2003, 17:413-424.
32. Fields S., Johnston M. Cell biology. Whither model organism research?. Science 2005, 307:1885-1886.
33. Fields S., Song O. A novel genetic system to detect protein-protein interactions. Nature 1989, 340:245-246.
34. Finkel J.S., Chinchilla K., Ursic D., Culbertson M.R. Sen1p performs two genetically separable functions in transcription and processing of U5 small nuclear RNA in Saccharomyces cerevisiae. Genetics 2010, 184:107-118.
35. Fiordalisi J.J., James P.L., Zhang Y., Grant G.A. Facile production of native-like kappa-bungarotoxin in yeast: an enhanced system for the production of a neuronal nicotinic acetylcholine receptor probe. Toxicon 1996, 34:213-224.
36. Foury F., Cazzalini O. Deletion of the yeast homologue of the human gene associated with Friedreich's ataxia elicits iron accumulation in mitochondria. FEBS Lett. 1997, 411:373-377.
37. Gavin A.C., Bosche M., Krause R., Grandi P., Marzioch M., Bauer A., Schultz J., Rick J.M., Michon A.M., Cruciat C.M., 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 M.A., Copley R.R., Edelmann A., Querfurth E., Rybin V., Drewes G., Raida M., Bouwmeester T., Bork P., Seraphin B., Kuster B., Neubauer G., Superti-Furga G. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 2002, 415:141-147.
38. Gavin A.C., Aloy P., Grandi P., Krause R., Boesche M., Marzioch M., Rau C., Jensen L.J., Bastuck S., Dumpelfeld B., Edelmann A., Heurtier M.A., Hoffman V., Hoefert C., Klein K., Hudak M., Michon A.M., Schelder M., Schirle M., Remor M., Rudi T., Hooper S., Bauer A., Bouwmeester T., Casari G., Drewes G., Neubauer G., Rick J.M., Kuster B., Bork P., Russell R.B., Superti-Furga G. Proteome survey reveals modularity of the yeast cell machinery. Nature 2006, 440:631-636.
39. Gelperin D.M., White M.A., Wilkinson M.L., Kon Y., Kung L.A., Wise K.J., Lopez-Hoyo N., Jiang L., Piccirillo S., Yu H., Gerstein M., Dumont M.E., Phizicky E.M., Snyder M., Grayhack E.J. Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes Dev. 2005, 19:2816-2826.
40. Ghaemmaghami S., Huh W.K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., Weissman J.S. Global analysis of protein expression in yeast. Nature 2003, 425:737-741.
41. Giaever G., Shoemaker D.D., Jones T.W., Liang H., Winzeler E.A., Astromoff A., Davis R.W. Genomic profiling of drug sensitivities via induced haploinsufficiency. Nat. Genet. 1999, 21:278-283.
42. Giaever G., Chu A.M., Ni L., Connelly C., Riles L., Veronneau S., Dow S., Lucau-Danila A., Anderson K., Andre B., Arkin A.P., Astromoff A., El-Bakkoury M., Bangham R., Benito R., Brachat S., Campanaro S., Curtiss M., Davis K., Deutschbauer A., Entian K.D., Flaherty P., Foury F., Garfinkel D.J., Gerstein M., Gotte D., Guldener U., Hegemann J.H., Hempel S., Herman Z., Jaramillo D.F., Kelly D.E., Kelly S.L., Kotter P., LaBonte D., Lamb D.C., Lan N., Liang H., Liao H., Liu L., Luo C., Lussier M., Mao R., Menard P., Ooi S.L., Revuelta J.L., Roberts C.J., Rose M., Ross-Macdonald P., Scherens B., Schimmack G., Shafer B., Shoemaker D.D., Sookhai-Mahadeo S., Storms R.K., Strathern J.N., Valle G., Voet M., Volckaert G., Wang C.Y., Ward T.R., Wilhelmy J., Winzeler E.A., Yang Y., Yen G., Youngman E., Yu K., Bussey H., Boeke J.D., Snyder M., Philippsen P., Davis R.W., Johnston M. Functional profiling of the Saccharomyces cerevisiae genome. Nature 2002, 418:387-391.
43. Giaever G., Flaherty P., Kumm J., Proctor M., Nislow C., Jaramillo D.F., Chu A.M., Jordan M.I., Arkin A.P., Davis R.W. Chemogenomic profiling: identifying the functional interactions of small molecules in yeast. Proc. Natl. Acad. Sci. Unites States Am 2004, 101:793-798.
44. Giorgini F., Muchowski P.J. Connecting the dots in Huntington's disease with protein interaction networks. Genome Biol. 2005, 6:210.
45. Giorgini F., Guidetti P., Nguyen Q., Bennett S.C., Muchowski P.J. A genomic screen in yeast implicates kynurenine 3-monooxygenase as a therapeutic target for Huntington disease. Nat. Genet. 2005, 37:526-531.
46. Giot L., Bader J.S., Brouwer C., Chaudhuri A., Kuang B., Li Y., Hao Y.L., Ooi C.E., Godwin B., Vitols E., Vijayadamodar G., Pochart P., Machineni H., Welsh M., Kong Y., Zerhusen B., Malcolm R., Varrone Z., Collis A., Minto M., Burgess S., McDaniel L., Stimpson E., Spriggs F., Williams J., Neurath K., Ioime N., Agee M., Voss E., Furtak K., Renzulli R., Aanensen N., Carrolla S., Bickelhaupt E., Lazovatsky Y., DaSilva A., Zhong J., Stanyon C.A., Finley R.L., White K.P., Braverman M., Jarvie T., Gold S., Leach M., Knight J., Shimkets R.A., McKenna M.P., Chant J., Rothberg J.M. A protein interaction map of Drosophila melanogaster. Science 2003, 302:1727-1736.
47. Goffeau A., Barrell B.G., Bussey H., Davis R.W., Dujon B., Feldmann H., Galibert F., Hoheisel J.D., Jacq C., Johnston M., Louis E.J., Mewes H.W., Murakami Y., Philippsen P., Tettelin H., Oliver S.G. Life with 6000 genes. Science 1996, 274(546):563-567.
48. Gray S.A., Barr J.R., Kalb S.R., Marks J.D., Baird C.L., Cangelosi G.A., Miller K.D., Feldhaus M.J. Synergistic capture of clostridium botulinum type A neurotoxin by scFv antibodies to novel epitopes. Biotechnol. Bioeng. 2011, 108:2456-2467.
49. Greenfield J.P., Xu H., Greengard P., Gandy S., Seeger M. Generation of the amyloid-beta peptide N terminus in Saccharomyces cerevisiae expressing human Alzheimer's amyloid-beta precursor protein. J. Biol. Chem. 1999, 274:33843-33846.
50. Hartman J.L.t., Garvik B., Hartwell L. Principles for the buffering of genetic variation. Science 2001, 291:1001-1004.
51. Hartwell L.H. Nobel lecture. Yeast and cancer. Biosci. Rep. 2002, 22:373-394.
52. Henthorn D.C., Jaxa-Chamiec A.A., Meldrum E. A GAL4-based yeast three-hybrid system for the identification of small molecule-target protein interactions. Biochem. Pharmacol. 2002, 63:1619-1628.
53. Hillenmeyer M.E., Fung E., Wildenhain J., Pierce S.E., Hoon S., Lee W., Proctor M., St Onge R.P., Tyers M., Koller D., Altman R.B., Davis R.W., Nislow C., Giaever G. The chemical genomic portrait of yeast: uncovering a phenotype for all genes. Science 2008, 320:362-365.
54. Ho C.H., Magtanong L., Barker S.L., Gresham D., Nishimura S., Natarajan P., Koh J.L., Porter J., Gray C.A., Andersen R.J., Giaever G., Nislow C., Andrews B., Botstein D., Graham T.R., Yoshida M., Boone C. A molecular barcoded yeast ORF library enables mode-of-action analysis of bioactive compounds. Nat. Biotechnol. 2009, 27:369-377.
55. Hoon S., Smith A.M., Wallace I.M., Suresh S., Miranda M., Fung E., Proctor M., Shokat K.M., Zhang C., Davis R.W., Giaever G., St Onge R.P., Nislow C. An integrated platform of genomic assays reveals small-molecule bioactivities. Nat. Chem. Biol. 2008, 4:498-506.
56. Hu X., Kang S., Chen X., Shoemaker C.B., Jin M.M. Yeast surface two-hybrid for quantitative in vivo detection of protein-protein interactions via the secretory pathway. J. Biol. Chem. 2009, 284:16369-16376.
57. Huang J., Schreiber S.L. A yeast genetic system for selecting small molecule inhibitors of protein-protein interactions in nanodroplets. Proc. Natl. Acad. Sci. Unites States Am 1997, 94:13396-13401.
58. Huang J., Zhu H., Haggarty S.J., Spring D.R., Hwang H., Jin F., Snyder M., Schreiber S.L. Finding new components of the target of rapamycin (TOR) signaling network through chemical genetics and proteome chips. Proc. Natl. Acad. Sci. Unites States Am 2004, 101:16594-16599.
59. Hughes T.R. Yeast and drug discovery. Funct. Integr. Genom 2002, 2:199-211.
60. Hughes T.R., Marton M.J., Jones A.R., Roberts C.J., Stoughton R., Armour C.D., Bennett H.A., Coffey E., Dai H., He Y.D., Kidd M.J., King A.M., Meyer M.R., Slade D., Lum P.Y., Stepaniants S.B., Shoemaker D.D., Gachotte D., Chakraburtty K., Simon J., Bard M., Friend S.H. Functional discovery via a compendium of expression profiles. Cell 2000, 102:109-126.
61. Hughes T.R., Roberts C.J., Dai H., Jones A.R., Meyer M.R., Slade D., Burchard J., Dow S., Ward T.R., Kidd M.J., Friend S.H., Marton M.J. Widespread aneuploidy revealed by DNA microarray expression profiling. Nat. Genet. 2000, 25:333-337.
62. Huh W.K., Falvo J.V., Gerke L.C., Carroll A.S., Howson R.W., Weissman J.S., O'Shea E.K. Global analysis of protein localization in budding yeast. Nature 2003, 425:686-691.
63. Ito T., Chiba T., Ozawa R., Yoshida M., Hattori M., Sakaki Y. A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. Unites States Am 2001, 98:4569-4574.
64. Ivanov P.A., Lewitin E.I., Shevelev B.I., Fominov G.V., Wojciechowska J.A., Asadi Mobarhan A.H., Vertie Y.V., Yankovsky N.K., Shevelev A.B. Sup35p yeast prion-like protein as an adapter for production of the Gag-p55 antigen of HIV-1 and the L-chain of botulinum neurotoxin in Saccharomyces cerevisiae. Res. Microbiol. 2001, 152:27-35.
65. Johnson S.K., Zhang W., Smith L.A., Hywood-Potter K.J., Todd Swanson S., Schlegel V.L., Meagher M.M. Scale-up of the fermentation and purification of the recombinant heavy chain fragment C of botulinum neurotoxin serotype F, expressed in Pichia pastoris. Protein Expr. Purif. 2003, 32:1-9.
66. Johnson B.S., McCaffery J.M., Lindquist S., Gitler A.D. A yeast TDP-43 proteinopathy model: exploring the molecular determinants of TDP-43 aggregation and cellular toxicity. Proc. Natl. Acad. Sci. Unites States Am 2008, 105:6439-6444.
67. Kaksonen M., Toret C.P., Drubin D.G. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 2005, 123:305-320.
68. Kamath R.S., Ahringer J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 2003, 30:313-321.
69. Kanemaki M., Sanchez-Diaz A., Gambus A., Labib K. Functional proteomic identification of DNA replication proteins by induced proteolysis in vivo. Nature 2003, 423:720-724.
70. Kini R.M. Venom Phospholipase A2 Enzymes: Structure, Function and Mechanism 1997, John Wiley, Chichester.
71. Koutnikova H., Campuzano V., Foury F., Dolle P., Cazzalini O., Koenig M. Studies of human, mouse and yeast homologues indicate a mitochondrial function for frataxin. Nat. Genet. 1997, 16:345-351.
72. 2 and more. Toxicon 2011, 58:219-229.
73. Krobitsch S., Lindquist S. Aggregation of huntingtin in yeast varies with the length of the polyglutamine expansion and the expression of chaperone proteins. Proc. Natl. Acad. Sci. Unites States Am 2000, 97:1589-1594.
74. Krogan N.J., Cagney G., Yu H., Zhong G., Guo X., Ignatchenko A., Li J., Pu S., Datta N., Tikuisis A.P., Punna T., Peregrin-Alvarez J.M., Shales M., Zhang X., Davey M., Robinson M.D., Paccanaro A., Bray J.E., Sheung A., Beattie B., Richards D.P., Canadien V., Lalev A., Mena F., Wong P., Starostine A., Canete M.M., Vlasblom J., Wu S., Orsi C., Collins S.R., Chandran S., Haw R., Rilstone J.J., Gandi K., Thompson N.J., Musso G., St Onge P., Ghanny S., Lam M.H., Butland G., Altaf-Ul A.M., Kanaya S., Shilatifard A., O'Shea E., Weissman J.S., Ingles C.J., Hughes T.R., Parkinson J., Gerstein M., Wodak S.J., Emili A., Greenblatt J.F. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 2006, 440:637-643.
75. Kumar A., Snyder M. Emerging technologies in yeast genomics. Nat. Rev. Genet. 2001, 2:302-312.
76. Kumar A., Agarwal S., Heyman J.A., Matson S., Heidtman M., Piccirillo S., Umansky L., Drawid A., Jansen R., Liu Y., Cheung K.H., Miller P., Gerstein M., Roeder G.S., Snyder M. Subcellular localization of the yeast proteome. Genes Dev. 2002, 16:707-719.
77. Lamb J., Crawford E.D., Peck D., Modell J.W., Blat I.C., Wrobel M.J., Lerner J., Brunet J.P., Subramanian A., Ross K.N., Reich M., Hieronymus H., Wei G., Armstrong S.A., Haggarty S.J., Clemons P.A., Wei R., Carr S.A., Lander E.S., Golub T.R. The connectivity map: using gene-expression signatures to connect small molecules, genes, and disease. Science 2006, 313:1929-1935.
78. Lamprecht M.R., Sabatini D.M., Carpenter A.E. CellProfiler: free, versatile software for automated biological image analysis. Biotechniques 2007, 42:71-75.
79. Launhardt H., Hinnen A., Munder T. Drug-induced phenotypes provide a tool for the functional analysis of yeast genes. Yeast 1998, 14:935-942.
80. Lee W., St Onge R.P., Proctor M., Flaherty P., Jordan M.I., Arkin A.P., Davis R.W., Nislow C., Giaever G. Genome-wide requirements for resistance to functionally distinct DNA-damaging agents. PLoS Genet. 2005, 1:e24.
81. Lehar J., Stockwell B.R., Giaever G., Nislow C. Combination chemical genetics. Nat. Chem. Biol. 2008, 4:674-681.
82. Levy R., Forsyth C.M., LaPorte S.L., Geren I.N., Smith L.A., Marks J.D. Fine and domain-level epitope mapping of botulinum neurotoxin type A neutralizing antibodies by yeast surface display. J. Mol. Biol. 2007, 365:196-210.
83. Li S., Armstrong C.M., Bertin N., Ge H., Milstein S., Boxem M., Vidalain P.O., Han J.D., Chesneau A., Hao T., Goldberg D.S., Li N., Martinez M., Rual J.F., Lamesch P., Xu L., Tewari M., Wong S.L., Zhang L.V., Berriz G.F., Jacotot L., Vaglio P., Reboul J., Hirozane-Kishikawa T., Li Q., Gabel H.W., Elewa A., Baumgartner B., Rose D.J., Yu H., Bosak S., Sequerra R., Fraser A., Mango S.E., Saxton W.M., Strome S., Van Den Heuvel S., Piano F., Vandenhaute J., Sardet C., Gerstein M., Doucette-Stamm L., Gunsalus K.C., Harper J.W., Cusick M.E., Roth F.P., Hill D.E., Vidal M. A map of the interactome network of the metazoan C. elegans. Science 2004, 303:540-543.
84. Li Z., Vizeacoumar F.J., Bahr S., Li J., Warringer J., Vizeacoumar F.S., Min R., Vandersluis B., Bellay J., Devit M., Fleming J.A., Stephens A., Haase J., Lin Z.Y., Baryshnikova A., Lu H., Yan Z., Jin K., Barker S., Datti A., Giaever G., Nislow C., Bulawa C., Myers C.L., Costanzo M., Gingras A.C., Zhang Z., Blomberg A., Bloom K., Andrews B., Boone C. Systematic exploration of essential yeast gene function with temperature-sensitive mutants. Nat. Biotechnol. 2011, 29:361-367.
85. Lou J., Geren I., Garcia-Rodriguez C., Forsyth C.M., Wen W., Knopp K., Brown J., Smith T., Smith L.A., Marks J.D. Affinity maturation of human botulinum neurotoxin antibodies by light chain shuffling via yeast mating. Protein Eng. Des. Sel 2010, 23:311-319.
86. Luesch H., Wu T.Y., Ren P., Gray N.S., Schultz P.G., Supek F. A genome-wide overexpression screen in yeast for small-molecule target identification. Chem. Biol. 2005, 12:55-63.
87. Lum P.Y., Armour C.D., Stepaniants S.B., Cavet G., Wolf M.K., Butler J.S., Hinshaw J.C., Garnier P., Prestwich G.D., Leonardson A., Garrett-Engele P., Rush C.M., Bard M., Schimmack G., Phillips J.W., Roberts C.J., Shoemaker D.D. Discovering modes of action for therapeutic compounds using a genome-wide screen of yeast heterozygotes. Cell 2004, 116:121-137.
88. Magtanong L., Ho C.H., Barker S.L., Jiao W., Baryshnikova A., Bahr S., Smith A.M., Heisler L.E., Choy J.S., Kuzmin E., Andrusiak K., Kobylianski A., Li Z., Costanzo M., Basrai M.A., Giaever G., Nislow C., Andrews B., Boone C. Dosage suppression genetic interaction networks enhance functional wiring diagrams of the cell. Nat. Biotechnol. 2011, 29:505-511.
89. Martin-Eauclaire M.F., Sogaard M., Ramos C., Cestele S., Bougis P.E., Svensson B. Production of active, insect-specific scorpion neurotoxin in yeast. Eur. J. Biochem. 1994, 223:637-645.
90. Martzen M.R., McCraith S.M., Spinelli S.L., Torres F.M., Fields S., Grayhack E.J., Phizicky E.M. A biochemical genomics approach for identifying genes by the activity of their products. Science 1999, 286:1153-1155.
91. Mattiazzi M., Curk T., Križaj I., Zupan B., Petrovič U. Inference of the molecular mechanism of action from genetic interaction and gene expression data. OMICS 2010, 14:357-367.
92. 2 and the Rim101 pathway components in S. cerevisiae reveal a role for this pathway in response to changes in membrane composition and shape. Mol. Genet. Genom. 2010, 283:519-530.
93. Mayer V.W., Goin C.J. Induction of chromosome loss in yeast by combined treatment with neurotoxic hexacarbons and monoketones. Mutat. Res. 1994, 341:83-91.
94. Melese T., Hieter P. From genetics and genomics to drug discovery: yeast rises to the challenge. Trends Pharmacol. Sci. 2002, 23:544-547.
95. Mnaimneh S., Davierwala A.P., Haynes J., Moffat J., Peng W.T., Zhang W., Yang X., Pootoolal J., Chua G., Lopez A., Trochesset M., Morse D., Krogan N.J., Hiley S.L., Li Z., Morris Q., Grigull J., Mitsakakis N., Roberts C.J., Greenblatt J.F., Boone C., Kaiser C.A., Andrews B.J., Hughes T.R. Exploration of essential gene functions via titratable promoter alleles. Cell 2004, 118:31-44.
96. Muchowski P.J., Schaffar G., Sittler A., Wanker E.E., Hayer-Hartl M.K., Hartl F.U. Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc. Natl. Acad. Sci. Unites States Am 2000, 97:7841-7846.
97. Muchowski P.J., Ning K., D'Souza-Schorey C., Fields S. Requirement of an intact microtubule cytoskeleton for aggregation and inclusion body formation by a mutant huntingtin fragment. Proc. Natl. Acad. Sci. Unites States Am 2002, 99:727-732.
98. 2 research: from cells to animals to humans. Progr. Lipid Res. 2011, 50:152-192.
99. Natter K., Leitner P., Faschinger A., Wolinski H., McCraith S., Fields S., Kohlwein S.D. The spatial organization of lipid synthesis in the yeast Saccharomyces cerevisiae derived from large scale green fluorescent protein tagging and high resolution microscopy. Mol. Cell Proteomics 2005, 4:662-672.
100. Nishida C.R., Gralla E.B., Valentine J.S. Characterization of three yeast copper-zinc superoxide dismutase mutants analogous to those coded for in familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. Unites States Am 1994, 91:9906-9910.
101. Nurse P.M. Nobel lecture. Cyclin dependent kinases and cell cycle control. Biosci. Rep. 2002, 22:487-499.
102. Oliver S.G. Functional genomics: lessons from yeast. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2002, 357:17-23.
103. Ooi S.L., Shoemaker D.D., Boeke J.D. DNA helicase gene interaction network defined using synthetic lethality analyzed by microarray. Nat. Genet. 2003, 35:277-286.
104. Pan X., Yuan D.S., Xiang D., Wang X., Sookhai-Mahadeo S., Bader J.S., Hieter P., Spencer F., Boeke J.D. A robust toolkit for functional profiling of the yeast genome. Mol. Cell 2004, 16:487-496.
105. Parsons A.B., Brost R.L., Ding H., Li Z., Zhang C., Sheikh B., Brown G.W., Kane P.M., Hughes T.R., Boone C. Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat. Biotechnol. 2004, 22:62-69.
106. Parsons A.B., Lopez A., Givoni I.E., Williams D.E., Gray C.A., Porter J., Chua G., Sopko R., Brost R.L., Ho C.H., Wang J., Ketela T., Brenner C., Brill J.A., Fernandez G.E., Lorenz T.C., Payne G.S., Ishihara S., Ohya Y., Andrews B., Hughes T.R., Frey B.J., Graham T.R., Andersen R.J., Boone C. Exploring the mode-of-action of bioactive compounds by chemical-genetic profiling in yeast. Cell 2006, 126:611-625.
107. Penalva M.A., Tilburn J., Bignell E., Arst H.N. Ambient pH gene regulation in fungi: making connections. Trends Microbiol. 2008, 16:291-300.
108. 2 enzymes. Biochemistry 2005, 44:12535-12545.
109. 2, can act in the cytosol of the nerve cell. Biochem. Biophys. Res. Commun. 2004, 324:981-985.
110. 2, inhibits G2 cell-cycle arrest in the yeast Saccharomyces cerevisiae. Biochem. J. 2005, 391:383-388.
111. Pommier Y., Cherfils J. Interfacial inhibition of macromolecular interactions: nature's paradigm for drug discovery. Trends Pharmacol. Sci. 2005, 26:138-145.
112. Potter K.J., Bevins M.A., Vassilieva E.V., Chiruvolu V.R., Smith T., Smith L.A., Meagher M.M. Production and purification of the heavy-chain fragment C of botulinum neurotoxin, serotype B, expressed in the methylotrophic yeast Pichia pastoris. Protein Expr. Purif. 1998, 13:357-365.
113. Potter K.J., Zhang W., Smith L.A., Meagher M.M. Production and purification of the heavy chain fragment C of botulinum neurotoxin, serotype A, expressed in the methylotrophic yeast Pichia pastoris. Protein Expr. Purif. 2000, 19:393-402.
114. Puccio H., Koenig M. Recent advances in the molecular pathogenesis of Friedreich ataxia. Hum. Mol. Genet. 2000, 9:887-892.
115. Reiter L.T., Potocki L., Chien S., Gribskov M., Bier E. A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Res. 2001, 11:1114-1125.
116. Renton A.E., Majounie E., Waite A., Simon-Sanchez J., Rollinson S., Gibbs J.R., Schymick J.C., Laaksovirta H., van Swieten J.C., Myllykangas L., Kalimo H., Paetau A., Abramzon Y., Remes A.M., Kaganovich A., Scholz S.W., Duckworth J., Ding J., Harmer D.W., Hernandez D.G., Johnson J.O., Mok K., Ryten M., Trabzuni D., Guerreiro R.J., Orrell R.W., Neal J., Murray A., Pearson J., Jansen I.E., Sondervan D., Seelaar H., Blake D., Young K., Halliwell N., Callister J.B., Toulson G., Richardson A., Gerhard A., Snowden J., Mann D., Neary D., Nalls M.A., Peuralinna T., Jansson L., Isoviita V.M., Kaivorinne A.L., Holtta-Vuori M., Ikonen E., Sulkava R., Benatar M., Wuu J., Chio A., Restagno G., Borghero G., Sabatelli M., Heckerman D., Rogaeva E., Zinman L., Rothstein J.D., Sendtner M., Drepper C., Eichler E.E., Alkan C., Abdullaev Z., Pack S.D., Dutra A., Pak E., Hardy J., Singleton A., Williams N.M., Heutink P., Pickering-Brown S., Morris H.R., Tienari P.J., Traynor B.J. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011, 72:257-268.
117. Rigaut G., Shevchenko A., Rutz B., Wilm M., Mann M., Seraphin B. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 1999, 17:1030-1032.
118. Rine J., Hansen W., Hardeman E., Davis R.W. Targeted selection of recombinant clones through gene dosage effects. Proc. Natl. Acad. Sci. Unites States Am 1983, 80:6750-6754.
119. Rual J.F., Venkatesan K., Hao T., Hirozane-Kishikawa T., Dricot A., Li N., Berriz G.F., Gibbons F.D., Dreze M., Ayivi-Guedehoussou N., Klitgord N., Simon C., Boxem M., Milstein S., Rosenberg J., Goldberg D.S., Zhang L.V., Wong S.L., Franklin G., Li S., Albala J.S., Lim J., Fraughton C., Llamosas E., Cevik S., Bex C., Lamesch P., Sikorski R.S., Vandenhaute J., Zoghbi H.Y., Smolyar A., Bosak S., Sequerra R., Doucette-Stamm L., Cusick M.E., Hill D.E., Roth F.P., Vidal M. Towards a proteome-scale map of the human protein-protein interaction network. Nature 2005, 437:1173-1178.
120. Sarkar S., Perlstein E.O., Imarisio S., Pineau S., Cordenier A., Maglathlin R.L., Webster J.A., Lewis T.A., O'Kane C.J., Schreiber S.L., Rubinsztein D.C. Small molecules enhance autophagy and reduce toxicity in Huntington's disease models. Nat. Chem. Biol. 2007, 3:331-338.
121. Schuldiner M., Collins S.R., Thompson N.J., Denic V., Bhamidipati A., Punna T., Ihmels J., Andrews B., Boone C., Greenblatt J.F., Weissman J.S., Krogan N.J. Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 2005, 123:507-519.
122. Sheridan C. Protein chip companies turn to biomarkers. Nat. Biotechnol. 2005, 23:3-4.
123. Sherman F. Getting started with yeast. Methods Enzymol. 1991, 194:3-21.
124. Shoemaker B.A., Panchenko A.R. Deciphering protein-protein interactions. Part I. Experimental techniques and databases. PLoS Comput. Biol. 2007, 3:e42.
125. Shoemaker D.D., Lashkari D.A., Morris D., Mittmann M., Davis R.W. Quantitative phenotypic analysis of yeast deletion mutants using a highly parallel molecular bar-coding strategy. Nat. Genet. 1996, 14:450-456.
126. 2. J. Biol. Chem. 2002, 277:48535-48549.
127. Sinha J., Inan M., Fanders S., Taoka S., Gouthro M., Swanson T., Barent R., Barthuli A., Loveless B.M., Smith L.A., Smith T., Henderson I., Ross J., Meagher M.M. Cell bank characterization and fermentation optimization for production of recombinant heavy chain C-terminal fragment of botulinum neurotoxin serotype E (rBoNTE(H(c)): antigen E) by Pichia pastoris. J. Biotechnol. 2007, 127:462-474.
128. Smith L.A. Development of recombinant vaccines for botulinum neurotoxin. Toxicon 1998, 36:1539-1548.
129. Smith M.G., Snyder M. Yeast as a model for human disease. Curr. Protoc. Hum. Genet. 2006, Chapter 15, Unit 15 16.
130. Smith A.M., Heisler L.E., Mellor J., Kaper F., Thompson M.J., Chee M., Roth F.P., Giaever G., Nislow C. Quantitative phenotyping via deep barcode sequencing. Genome Res. 2009, 19:1836-1842.
131. Sopko R., Huang D., Preston N., Chua G., Papp B., Kafadar K., Snyder M., Oliver S.G., Cyert M., Hughes T.R., Boone C., Andrews B. Mapping pathways and phenotypes by systematic gene overexpression. Mol. Cell 2006, 21:319-330.
132. St Onge R.P., Mani R., Oh J., Proctor M., Fung E., Davis R.W., Nislow C., Roth F.P., Giaever G. Systematic pathway analysis using high-resolution fitness profiling of combinatorial gene deletions. Nat. Genet. 2007, 39:199-206.
133. Stagljar I., Korostensky C., Johnsson N., te Heesen S. A genetic system based on split-ubiquitin for the analysis of interactions between membrane proteins in vivo. Proc. Natl. Acad. Sci. Unites States Am 1998, 95:5187-5192.
134. Stelzl U., Worm U., Lalowski M., Haenig C., Brembeck F.H., Goehler H., Stroedicke M., Zenkner M., Schoenherr A., Koeppen S., Timm J., Mintzlaff S., Abraham C., Bock N., Kietzmann S., Goedde A., Toksoz E., Droege A., Krobitsch S., Korn B., Birchmeier W., Lehrach H., Wanker E.E. A human protein-protein interaction network: a resource for annotating the proteome. Cell 2005, 122:957-968.
135. Su S.S., Mitchell A.P. Identification of functionally related genes that stimulate early meiotic gene expression in yeast. Genetics 1993, 133:67-77.
136. Su L.J., Auluck P.K., Outeiro T.F., Yeger-Lotem E., Kritzer J.A., Tardiff D.F., Strathearn K.E., Liu F., Cao S., Hamamichi S., Hill K.J., Caldwell K.A., Bell G.W., Fraenkel E., Cooper A.A., Caldwell G.A., McCaffery J.M., Rochet J.C., Lindquist S. Compounds from an unbiased chemical screen reverse both ER-to-Golgi trafficking defects and mitochondrial dysfunction in Parkinson's disease models. Dis. Model. Mech. 2010, 3:194-208.
137. Suter B., Auerbach D., Stagljar I. Yeast-based functional genomics and proteomics technologies: the first 15 years and beyond. Biotechniques 2006, 40:625-644.
138. Szostak J.W. DNA ends: just the beginning (Nobel lecture). Angew. Chem. Int. Ed. Engl. 2010, 49:7386-7404.
139. 2 with neurotoxic activity is a calmodulin. J. Biol. Chem. 2001, 276:12493-12496.
140. 2 associates, through a non-phosphorylated binding motif, with 14-3-3 protein gamma and epsilon isoforms. Biochem. Biophys. Res. Commun. 2003, 302:691-696.
141. Šribar J., Anderluh G., Fox J.W., Križaj I. Protein disulphide isomerase binds ammodytoxin strongly: possible implications for toxin trafficking. Biochem. Biophys. Res. Commun. 2005, 329:733-737.
142. Tong A.H., Evangelista M., Parsons A.B., Xu H., Bader G.D., Page N., Robinson M., Raghibizadeh S., Hogue C.W., Bussey H., Andrews B., Tyers M., Boone C. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 2001, 294:2364-2368.
143. Treusch S., Hamamichi S., Goodman J.L., Matlack K.E., Chung C.Y., Baru V., Shulman J.M., Parrado A., Bevis B.J., Valastyan J.S., Han H., Lindhagen-Persson M., Reiman E.M., Evans D.A., Bennett D.A., Olofsson A., DeJager P.L., Tanzi R.E., Caldwell K.A., Caldwell G.A., Lindquist S. Functional links between Abeta toxicity, endocytic trafficking, and Alzheimer's disease risk factors in yeast. Science 2011, 334:1241-1245.
144. Uetz P., Giot L., Cagney G., Mansfield T.A., Judson R.S., Knight J.R., 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 J.M. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 2000, 403:623-627.
145. Uptain S.M., Lindquist S. Prions as protein-based genetic elements. Annu. Rev. Microbiol. 2002, 56:703-741.
146. Vizeacoumar F.J., van Dyk N., Vizeacoumar Frederick S., Cheung V., Li J., Sydorskyy Y., Case N., Li Z., Datti A., Nislow C., Raught B., Zhang Z., Frey B., Bloom K., Boone C., Andrews B.J. Integrating high-throughput genetic interaction mapping and high-content screening to explore yeast spindle morphogenesis. J. Cell Biol. 2010, 188:69-81.
147. Wach A., Brachat A., Pohlmann R., Philippsen P. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 1994, 10:1793-1808.
148. Willingham S., Outeiro T.F., DeVit M.J., Lindquist S.L., Muchowski P.J. Yeast genes that enhance the toxicity of a mutant huntingtin fragment or alpha-synuclein. Science 2003, 302:1769-1772.
149. Wilson R.B., Roof D.M. Respiratory deficiency due to loss of mitochondrial DNA in yeast lacking the frataxin homologue. Nat. Genet. 1997, 16:352-357.
150. Winzeler E.A., Shoemaker D.D., Astromoff A., Liang H., Anderson K., Andre B., Bangham R., Benito R., Boeke J.D., Bussey H., Chu A.M., Connelly C., Davis K., Dietrich F., Dow S.W., El Bakkoury M., Foury F., Friend S.H., Gentalen E., Giaever G., Hegemann J.H., Jones T., Laub M., Liao H., Liebundguth N., Lockhart D.J., Lucau-Danila A., Lussier M., M'Rabet N., Menard P., Mittmann M., Pai C., Rebischung C., Revuelta J.L., Riles L., Roberts C.J., Ross-MacDonald P., Scherens B., Snyder M., Sookhai-Mahadeo S., Storms R.K., Veronneau S., Voet M., Volckaert G., Ward T.R., Wysocki R., Yen G.S., Yu K., Zimmermann K., Philippsen P., Johnston M., Davis R.W. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 1999, 285:901-906.
151. Wolinski H., Petrovič U., Mattiazzi M., Petschnigg J., Heise B., Natter K., Kohlwein S.D. Imaging-based live cell yeast screen identifies novel factors involved in peroxisome assembly. J. Proteome Res. 2009, 8:20-27.
152. Yan Z., Costanzo M., Heisler L.E., Paw J., Kaper F., Andrews B.J., Boone C., Giaever G., Nislow C. Yeast barcoders: a chemogenomic application of a universal donor-strain collection carrying bar-code identifiers. Nat. Methods 2008, 5:719-725.
153. Zhang X., Smith D.L., Meriin A.B., Engemann S., Russel D.E., Roark M., Washington S.L., Maxwell M.M., Marsh J.L., Thompson L.M., Wanker E.E., Young A.B., Housman D.E., Bates G.P., Sherman M.Y., Kazantsev A.G. A potent small molecule inhibits polyglutamine aggregation in Huntington's disease neurons and suppresses neurodegeneration in vivo. Proc. Natl. Acad. Sci. Unites States Am 2005, 102:892-897.
154. Zhu H., Bilgin M., Bangham R., Hall D., Casamayor A., Bertone P., Lan N., Jansen R., Bidlingmaier S., Houfek T., Mitchell T., Miller P., Dean R.A., Gerstein M., Snyder M. Global analysis of protein activities using proteome chips. Science 2001, 293:2101-2105.