Yeast as a tool to study bacterial effectors

Current Opinion in Microbiology

Volumn 12, Issue 1, 2009, Pages 18-23

  Curak, Jasna ^a   Rohde, John ^b   Stagljar, Igor ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BACTERIAL PROTEINS; DRUG DISCOVERY; SACCHAROMYCES CEREVISIAE; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); EUKARYOTA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 59849115493     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2008.11.004     Document Type: Review

References (35)

1. Bhavsar A.P., Guttman J.A., and Finlay B.B. Manipulation of host-cell pathways by bacterial pathogens. Nature 449 (2007) 827-834
2. Alegado R.A., Campbell M.C., Chen W.C., Slutz S.S., and Tan M.W. Characterization of mediators of microbial virulence and innate immunity using the Caenorhabditis elegans host-pathogen model. Cell Microbiol 5 (2003) 435-444
3. Botham C.M., Wandler A.M., and Guillemin K. A transgenic Drosophila model demonstrates that the Helicobacter pylori CagA protein functions as a eukaryotic Gab adaptor. PLoS Pathog 4 (2008) e1000064
4. Siggers K.A., and Lesser C.F. The yeast Saccharomyces cerevisiae: a versatile model system for the identification and characterization of bacterial virulence proteins. Cell Host Microbe 4 (2008) 8-15
5. Valdivia R.H. Modeling the function of bacterial virulence factors in Saccharomyces cerevisiae. Eukaryot Cell 3 (2004) 827-834
6. Engqvist-Goldstein A.E., and Drubin D.G. Actin assembly and endocytosis: from yeast to mammals. Annu Rev Cell Dev Biol 19 (2003) 287-332
7. Gruenberg J., and Stenmark H. The biogenesis of multivesicular endosomes. Nat Rev Mol Cell Biol 5 (2004) 317-323
8. Suter B., Auerbach D., and Stagljar I. Yeast-based functional genomics and proteomics technologies: the first 15 years and beyond. Biotechniques 40 (2006) 625-644
9. Alto N.M., Shao F., Lazar C.S., Brost R.L., Chua G., Mattoo S., McMahon S.A., Ghosh P., Hughes T.R., Boone C., and Dixon J.E. Identification of a bacterial type III effector family with G protein mimicry functions. Cell 124 (2006) 133-145. Used PGA to identify a conserved process affected by a novel activator of GTPases. One of the first examples of utilizing genome-wide tools of yeast to decipher effector function.
10. Tong A.H., Evangelista M., Parsons A.B., Xu H., Bader G.D., Page N., Robinson M., Raghibizadeh S., Hogue C.W., Bussey H., et al. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294 (2001) 2364-2368
11. Kramer R.W., Slagowski N.L., Eze N.A., Giddings K.S., Morrison M.F., Siggers K.A., Starnbach M.N., and Lesser C.F. Yeast functional genomic screens lead to identification of a role for a bacterial effector in innate immunity regulation. PLoS Pathog 3 (2007) e21
12. Li H., Xu H., Zhou Y., Zhang J., Long C., Li S., Chen S., Zhou J.M., and Shao F. The phosphothreonine lyase activity of a bacterial type III effector family. Science 315 (2007) 1000-1003
13. Campodonico E.M., Chesnel L., and Roy C.R. A yeast genetic system for the identification and characterization of substrate proteins transferred into host cells by the Legionella pneumophila Dot/Icm system. Mol Microbiol 56 (2005) 918-933
14. de Felipe K.S., Glover R.T., Charpentier X., Anderson O.R., Reyes M., Pericone C.D., and Shuman H.A. Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog 4 (2008) e1000117
15. Darsow T., Odorizzi G., and Emr S.D. Invertase fusion proteins for analysis of protein trafficking in yeast. Methods Enzymol 327 (2000) 95-106
16. Shohdy N., Efe J.A., Emr S.D., and Shuman H.A. Pathogen effector protein screening in yeast identifies Legionella factors that interfere with membrane trafficking. Proc Natl Acad Sci U S A 102 (2005) 4866-4871. Developed 'PEPSY' analysis which combines an unbiased genetic approach to screen for bacterial effectors that disrupt highly conserved eukaryotic processes that have robust assays in yeast.
17. Vida T.A., and Emr S.D. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 128 (1995) 779-792
18. Rohde J.R., Breitkreutz A., Chenal A., Sansonetti P.J., and Parsot C. Type III secretion effectors of the IpaH family are E3 ubiquitin ligases. Cell Host Microbe 1 (2007) 77-83
19. Sisko J.L., Spaeth K., Kumar Y., and Valdivia R.H. Multifunctional analysis of Chlamydia-specific genes in a yeast expression system. Mol Microbiol 60 (2006) 51-66. The first ordered array of bacterial effectors for use in a yeast system. Exhaustive phenotypic analysis and cell biology approaches identified a number of Chlamydia-specific genes that have functions within host cells. An excellent guide for the construction of effector libraries for study in yeast.
20. Kumar Y., Cocchiaro J., and Valdivia R.H. The obligate intracellular pathogen Chlamydia trachomatis targets host lipid droplets. Curr Biol 16 (2006) 1646-1651
21. Deresiewicz R.L., Calderwood S.B., Robertus J.D., and Collier R.J. Mutations affecting the activity of the Shiga-like toxin I A-chain. Biochemistry 31 (1992) 3272-3280
22. Singer A.U., Rohde J.R., Lam R., Skarina T., Kagan O., Dileo R., Chirgadze N.Y., Cuff M.E., Joachimiak A., Tyers M., et al. Structure of the Shigella T3SS effector IpaH defines a new class of E3 ubiquitin ligases. Nat Struct Mol Biol 15 12 (2008) 1293-1301
23. Yoon S., Liu Z., Eyobo Y., and Orth K. Yersinia effector YopJ inhibits yeast MAPK signaling pathways by an evolutionarily conserved mechanism. J Biol Chem 278 (2003) 2131-2135
24. Mukherjee S., Keitany G., Li Y., Wang Y., Ball H.L., Goldsmith E.J., and Orth K. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312 (2006) 1211-1214
25. Hao Y.H., Wang Y., Burdette D., Mukherjee S., Keitany G., Goldsmith E., and Orth K. Structural requirements for Yersinia YopJ inhibition of MAP kinase pathways. PLoS ONE 3 (2008) e1375. This article illustrates the power of yeast to help understand effector-target interactions at the structural level.
26. World Health Organization (WHO). Deaths by Cause, Sex, and Mortality Stratum in WHO Regions, Estimates for 2001 (2002)
27. Palumbi S.R. Humans as the world's greatest evolutionary force. Science 293 (2001) 1786-1790
28. Spellberg B., Powers J.H., Brass E.P., Miller L.G., and Edwards Jr. J.E. Trends in antimicrobial drug development: implications for the future. Clin Infect Dis 38 (2004) 1279-1286
29. Arnoldo A., Curak J., Kittanakom S., Chevelev I., Lee V.T., Sahebol-Amri M., Koscik B., Ljuma L., Roy P.J., Bedalov A., et al. Identification of small molecule inhibitors of Pseudomonas aeruginosa exoenzyme S using a yeast phenotypic screen. PLoS Genet 4 (2008) e1000005. Used a yeast-based functional-genomics and chemical-genomics strategy to identify small molecule inhibitors of Pseudomonas aeruginosa effector protein ExoS.
30. Barbieri J.T. Pseudomonas aeruginosa exoenzyme S, a bifunctional type-III secreted cytotoxin. Int J Med Microbiol 290 (2000) 381-387
31. Hillenmeyer M.E., Fung E., Wildenhain J., Pierce S.E., Hoon S., Lee W., Proctor M., St Onge R.P., Tyers M., Koller D., et al. The chemical genomic portrait of yeast: uncovering a phenotype for all genes. Science 320 (2008) 362-365. A powerful demonstration of how small molecules can be used to probe gene function.
32. Falkow S. Molecular Koch's postulates applied to bacterial pathogenicity - a personal recollection 15 years later. Nat Rev Microbiol 2 (2004) 67-72
33. Huang J., Lesser C.F., and Lory S. The essential role of the CopN protein in Chlamydia pneumoniae intracellular growth. Nature 456 7218 (2008) 112-115. A yeast-based chemical genetic screen identifies molecules that target an effector from C. pneumonia, opening the door for the study of virulence factors from Chlamydiae.
34. Giaever G., Shoemaker D.D., Jones T.W., Liang H., Winzeler E.A., Astromoff A., and Davis R.W. Genomic profiling of drug sensitivities via induced haploinsufficiency. Nat Genet 21 (1999) 278-283
35. Mazurkiewicz P., Tang C.M., Boone C., and Holden D.W. Signature-tagged mutagenesis: barcoding mutants for genome-wide screens. Nat Rev Genet 7 (2006) 929-939