Genetic interaction maps in Escherichia coli reveal functional crosstalk among cell envelope biogenesis pathways

PLoS Genetics

Volumn 7, Issue 11, 2011, Pages

  Babu, Mohan ^a   Díaz Mejía, J Javier ^a,b   Vlasblom, James ^c,d   Gagarinova, Alla ^a,d   Phanse, Sadhna ^a   Graham, Chris ^a   Yousif, Fouad ^a   Ding, Huiming ^a   Xiong, Xuejian ^c   Nazarians Armavil, Anaies ^a   Alamgir, Md ^e   Ali, Mehrab ^a   Pogoutse, Oxana ^a   Pe'er, Asaf ^f   Arnold, Roland ^a   Michaut, Magali ^a   Parkinson, John ^c,d   Golshani, Ashkan ^e   Whitfield, Chris ^g   Wodak, Shoshana J ^c,d   Moreno Hagelsieb, Gabriel ^b   Greenblatt, Jack F ^a,d   Emili, Andrew ^a,d   more..

^a UNIVERSITY OF TORONTO   (Canada)

^b WILFRID LAURIER UNIVERSITY   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e CARLETON UNIVERSITY   (Canada)

^f HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^g UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENOME; BACTERIAL MEMBRANE; BACTERIAL METABOLISM; CONTROLLED STUDY; CULTURE MEDIUM; ENVIRONMENTAL STRESS; ESCHERICHIA COLI; GENE INTERACTION; GENE MAPPING; GENE MUTATION; GENETIC SCREENING; NONHUMAN;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 81755177857     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002377     Document Type: Article

References (68)

1. Díaz-Mejía JJ, Babu M, Emili A, (2009) Computational and experimental approaches to chart the Escherichia coli cell-envelope-associated proteome and interactome. FEMS Microbiol Rev 33: 66-97.
2. Nichols RJ, Sen S, Choo YJ, Beltrao P, Zietek M, et al. (2011) Phenotypic landscape of a bacterial cell. Cell 144: 143-156.
3. Silhavy TJ, Kahne D, Walker S, (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2: a000414.
4. Haselbeck R, Wall D, Jiang B, Ketela T, Zyskind J, et al. (2002) Comprehensive essential gene identification as a platform for novel anti-infective drug discovery. Curr Pharm Des 8: 1155-1172.
5. Falconer SB, Brown ED, (2009) New screens and targets in antibacterial drug discovery. Curr Opin Microbiol 12: 497-504.
6. Babu M, Greenblatt JF, Emili A, Strynadka NC, Reithmeier RA, et al. (2010) Structure of a SLC26 Anion Transporter STAS Domain in Complex with Acyl Carrier Protein: Implications for E. coli YchM in Fatty Acid Metabolism. Structure 18: 1450-1462.
7. Park JT, Uehara T, (2008) How bacteria consume their own exoskeletons (turnover and recycling of cell wall peptidoglycan). Microbiol Mol Biol Rev 72: 211-227.
8. Ruiz N, Kahne D, Silhavy TJ, (2009) Transport of lipopolysaccharide across the cell envelope: the long road of discovery. Nat Rev Microbiol 7: 677-683.
9. Knowles TJ, Scott-Tucker A, Overduin M, Henderson IR, (2009) Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Nat Rev Microbiol 7: 206-214.
10. Ruiz N, Gronenberg LS, Kahne D, Silhavy TJ, (2008) Identification of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc Natl Acad Sci U S A 105: 5537-5542.
11. Sperandeo P, Villa R, Martorana A, Samalikova M, Grandori R, et al. (2010) New insights into the Lpt machinery for LPS transport to the cell surface: LptA-LptC interaction and LptA stability as a sensors of a properly assembled transenvelope complex. J Bacteriol In Press.
12. Typas A, Banzhaf M, van den Berg van Saparoea B, Verheul J, Biboy J, et al. (2010) Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 143: 1097-1109.
13. Wu T, Malinverni J, Ruiz N, Kim S, Silhavy TJ, et al. (2005) Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121: 235-245.
14. Hu P, Janga SC, Babu M, Diaz-Mejia JJ, Butland G, (2009) Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins. PLoS Biol 7: e1000096 doi:10.1371/journal.pbio.1000096.
15. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.0008.
16. Hartwell LH, Hopfield JJ, Leibler S, Murray AW, (1999) From molecular to modular cell biology. Nature 402: C47-52.
17. Girgis HS, Hottes AK, Tavazoie S, (2009) Genetic architecture of intrinsic antibiotic susceptibility. PLoS ONE 4: e5629 doi:10.1371/journal.pone.0005629.
18. Dixon SJ, Costanzo M, Baryshnikova A, Andrews B, Boone C, (2009) Systematic mapping of genetic interaction networks. Annu Rev Genet 43: 601-625.
19. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, et al. (2010) The genetic landscape of a cell. Science 327: 425-431.
20. Schuldiner M, Collins SR, Thompson NJ, Denic V, Bhamidipati A, et al. (2005) Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123: 507-519.
21. Bandyopadhyay S, Mehta M, Kuo D, Sung MK, Chuang R, et al. (2010) Rewiring of genetic networks in response to DNA damage. Science 330: 1385-1389.
22. Babu M, Musso G, Diaz-Mejia JJ, Butland G, Greenblatt JF, et al. (2009) Systems-level approaches for identifying and analyzing genetic interaction networks in Escherichia coli and extensions to other prokaryotes. Mol Biosyst 12: 1439-1455.
23. Butland G, Babu M, Díaz-Mejía JJ, Bohdana F, Phanse S, et al. (2008) eSGA: E. coli synthetic genetic array analysis. Nat Methods 5: 789-795.
24. Beltrao P, Cagney G, Krogan NJ, (2010) Quantitative genetic interactions reveal biological modularity. Cell 141: 739-745.
25. Bandyopadhyay S, Kelley R, Krogan NJ, Ideker T, (2008) Functional maps of protein complexes from quantitative genetic interaction data. PLoS Comput Biol 4: e1000065 doi:10.1371/journal.pcbi.1000065.
26. Ruiz N, Falcone B, Kahne D, Silhavy TJ, (2005) Chemical conditionality: a genetic strategy to probe organelle assembly. Cell 121: 307-317.
27. Sklar JG, Wu T, Kahne D, Silhavy TJ, (2007) Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev 21: 2473-2484.
28. Ebersbach G, Galli E, Moller-Jensen J, Lowe J, Gerdes K, (2008) Novel coiled-coil cell division factor ZapB stimulates Z ring assembly and cell division. Mol Microbiol 68: 720-735.
29. Price MN, Arkin AP, Alm EJ, (2006) The life-cycle of operons. PLoS Genet 2: e96 doi:10.1371/journal.pgen.0020096.
30. Faith JJ, Hayete B, Thaden JT, Mogno I, Wierzbowski J, et al. (2007) Large-scale mapping and validation of Escherichia coli transcriptional regulation from a compendium of expression profiles. PLoS Biol 5: e8 doi:10.1371/journal.pbio.0050008.
31. Lamarche MG, Kim SH, Crepin S, Mourez M, Bertrand N, et al. (2008) Modulation of hexa-acyl pyrophosphate lipid A population under Escherichia coli phosphate (Pho) regulon activation. J Bacteriol 190: 5256-5264.
32. Rowland SL, Fu X, Sayed MA, Zhang Y, Cook WR, et al. (2000) Membrane redistribution of the Escherichia coli MinD protein induced by MinE. J Bacteriol 182: 613-619.
33. Higashi K, Ishigure H, Demizu R, Uemura T, Nishino K, et al. (2008) Identification of a spermidine excretion protein complex (MdtJI) in Escherichia coli. J Bacteriol 190: 872-878.
34. Corbin BD, Wang Y, Beuria TK, Margolin W, (2007) Interaction between cell division proteins FtsE and FtsZ. J Bacteriol 189: 3026-3035.
35. Whitfield C, (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75: 39-68.
36. Hug I, Feldman MF, (2010) Analogies and homologies in lipopolysaccharide and glycoprotein biosynthesis in bacteria. Glycobiology 21: 138-151.
37. Majdalani N, Gottesman S, (2005) The Rcs phosphorelay: a complex signal transduction system. Annu Rev Microbiol 59: 379-405.
38. Gottesman S, Stout V, (1991) Regulation of capsular polysaccharide synthesis in Escherichia coli K12. Mol Microbiol 5: 1599-1606.
39. Berg JM, Tymoczko JL, Stryer L, (2002) Protein Turnover and Amino Acid Catabolism New York W. H. Freeman.
40. Collins SR, Miller KM, Maas NL, Roguev A, Fillingham J, et al. (2007) Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446: 806-810.
41. Taura T, Ito K, (1991) Does protein secretion activity vary during the cell cycle of Escherichia coli? J Biochem 109: 811-815.
42. Oliver DB, Beckwith J, (1981) E. coli mutant pleiotropically defective in the export of secreted proteins. Cell 25: 765-772.
43. Chung HS, Yao Z, Goehring NW, Kishony R, Beckwith J, et al. (2009) Rapid beta-lactam-induced lysis requires successful assembly of the cell division machinery. Proc Natl Acad Sci U S A 106: 21872-21877.
44. Heidrich C, Ursinus A, Berger J, Schwarz H, Holtje JV, (2002) Effects of multiple deletions of murein hydrolases on viability, septum cleavage, and sensitivity to large toxic molecules in Escherichia coli. J Bacteriol 184: 6093-6099.
45. Uehara T, Dinh T, Bernhardt TG, (2009) LytM-domain factors are required for daughter cell separation and rapid ampicillin-induced lysis in Escherichia coli. J Bacteriol 191: 5094-5107.
46. Chng SS, Ruiz N, Chimalakonda G, Silhavy TJ, Kahne D, (2010) Characterization of the two-protein complex in Escherichia coli responsible for lipopolysaccharide assembly at the outer membrane. Proc Natl Acad Sci U S A 107: 5363-5368.
47. Vaara M, Nurminen M, (1999) Outer membrane permeability barrier in Escherichia coli mutants that are defective in the late acyltransferases of lipid A biosynthesis. Antimicrob Agents Chemother 43: 1459-1462.
48. Mamat U, Meredith TC, Aggarwal P, Kühl A, Kirchhoff P, et al. (2008) Single amino acid substitutions in either YhjD or MsbA confer viability to 3-deoxy-d-manno-oct-2-ulosonic acid-depleted Escherichia coli. Mol Microbiol 67: 633-648.
49. Narita S, Tokuda H, (2009) Biochemical characterization of an ABC transporter LptBFGC complex required for the outer membrane sorting of lipopolysaccharides. FEBS Lett 583: 2160-2164.
50. Sperandeo P, Lau FK, Carpentieri A, De Castro C, Molinaro A, et al. (2008) Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J Bacteriol 190: 4460-4469.
51. Vogel J, Papenfort K, (2006) Small non-coding RNAs and the bacterial outer membrane. Curr Opin Microbiol 9: 605-611.
52. Eddy SR, (2001) Non-coding RNA genes and the modern RNA world. Nat Rev Genet 2: 919-929.
53. Geissmann T, Chevalier C, Cros MJ, Boisset S, Fechter P, et al. (2009) A search for small noncoding RNAs in Staphylococcus aureus reveals a conserved sequence motif for regulation. Nucleic Acids Res 37: 7239-7257.
54. Tjaden B, Goodwin SS, Opdyke JA, Guillier M, Fu DX, et al. (2006) Target prediction for small, noncoding RNAs in bacteria. Nucleic Acids Res 34: 2791-2802.
55. Sarsero JP, Wookey PJ, Pittard AJ, (1991) Regulation of expression of the Escherichia coli K-12 mtr gene by TyrR protein and Trp repressor. J Bacteriol 173: 4133-4143.
56. Pulvermacher SC, Stauffer LT, Stauffer GV, (2009) Role of the sRNA GcvB in regulation of cycA in Escherichia coli. Microbiology 155: 106-114.
57. Noinaj N, Guillier M, Barnard TJ, Buchanan SK, (2010) TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 64: 43-60.
58. Tischler J, Lehner B, Fraser AG, (2008) Evolutionary plasticity of genetic interaction networks. Nat Genet 40: 390-391.
59. Srinivas N, Jetter P, Ueberbacher BJ, Werneburg M, Zerbe K, et al. (2010) Peptidomimetic antibiotics target outer-membrane biogenesis in Pseudomonas aeruginosa. Science 327: 1010-1013.
60. Typas A, Nichols RJ, Siegele DA, Shales M, Collins SR, et al. (2008) High-throughput, quantitative analyses of genetic interactions in E. coli. Nat Methods 5: 781-787.
61. Collins SR, Schuldiner M, Krogan NJ, Weissman JS, (2006) A strategy for extracting and analyzing large-scale quantitative epistatic interaction data. Genome Biol 7: R63.
62. Le Meur N, Gentleman R, (2008) Modeling synthetic lethality. Genome Biol 9: R135.
63. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statist Soc Ser B 57: 589-300.
64. Muckstein U, Tafer H, Hackermuller J, Bernhart SH, Stadler PF, et al. (2006) Thermodynamics of RNA-RNA binding. Bioinformatics 22: 1177-1182.
65. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, et al. (2005) Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res 12: 291-299.
66. Babu M, Butland G, Pogoutse O, Li J, Greenblatt JF, et al. (2009) Sequential peptide affinity purification system for the systematic isolation and identification of protein complexes from Escherichia coli. Methods Mol Biol 564: 373-400.
67. Tran AX, Trent MS, Whitfield C, (2008) The LptA protein of Escherichia coli is a periplasmic lipid A-binding protein involved in the lipopolysaccharide export pathway. J Biol Chem 283: 20342-20349.
68. Huang KC, Mukhopadhyay R, Wen B, Gitai Z, Wingreen NS, (2008) Cell shape and cell-wall organization in Gram-negative bacteria. Proc Natl Acad Sci U S A 105: 19282-19287.