Insights into the function of YciM, a heat shock membrane protein required to maintain envelope integrity in escherichia coli

Journal of Bacteriology

Volumn 196, Issue 2, 2014, Pages 300-309

  Nicolaes, Valérie ^a,b,c   Hajjaji, Hayat El ^a,c   Davis, Rebecca M ^d   Van der Henst, Charles ^a,b,e   Depuydt, Matthieu ^a,c   Leverrier, Pauline ^a,c   Aertsen, Abram ^f   Haufroid, Vincent ^g   de Choudens, Sandrine Ollagnier ^h   De Bolle, Xavier ^e   Ruiz, Natividad ^d   Collet, Jean Francois ^a,b,c  

^a DE DUVE INSTITUTE   (Belgium)

^b WELBIO   (Belgium)

^c Brussels Center for Redox Biology   (Belgium)

^d OHIO STATE UNIVERSITY   (United States)

^e UNIVERSITY OF NAMUR   (Belgium)

^f UNIVERSITY OF LEUVEN   (Belgium)

^g UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^h Laboratoire Biopuces   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDASE; BACTERIAL ENZYME; BACTERIAL PROTEIN; HEAT SHOCK PROTEIN; IRON; MEMBRANE PROTEIN; PEPTIDOGLYCAN; RUBREDOXIN; UNCLASSIFIED DRUG; YCIM PROTEIN;

AMINO TERMINAL SEQUENCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; CELL STRUCTURE; CONTROLLED STUDY; CYTOPLASM; DELETION MUTANT; ENZYME ACTIVITY; ENZYME REGULATION; ESCHERICHIA COLI; HEAT SENSITIVITY; HUMAN; OSMOLARITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION;

EID: 84890909511     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00921-13     Document Type: Article

References (50)

1. Gould IM. 2008. The epidemiology of antibiotic resistance. Int. J. Antimicrob. Agents 32(Suppl 1):S2-S9. http://dx.doi.org/10.1016/j.ijantimicag.2008.06.016.
2. Ruiz N, Kahne D, Silhavy TJ. 2006. Advances in understanding bacterial outer-membrane biogenesis. Nat. Rev. Microbiol. 4:57-66. http://dx.doi.org/10.1038/nrmicro1322.
3. Leverrier P, Vertommen D, Collet JF. 2010. Contribution of proteomics toward solving the fascinating mysteries of the biogenesis of the envelope of Escherichia coli. Proteomics 10:771-784. http://dx.doi.org/10.1002/pmic.200900461.
4. Van Wielink JE, Duine JA. 1990. How big is the periplasmic space? Trends Biochem. Sci. 15:136-137. http://dx.doi.org/10.1016/0968-0004(90)90208-S.
5. 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. http://dx.doi.org/10.1038/nrmicro2069.
6. Ricci DP, Silhavy TJ. 2012. The Bam machine: a molecular cooper. Biochim. Biophys. Acta 1818:1067-1084. http://dx.doi.org/10.1016/j.bbamem.2011.08.020.
7. 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. http://dx.doi.org/10.1038/nrmicro2184.
8. Rigel NW, Silhavy TJ. 2012. Making a beta-barrel: assembly of outer membrane proteins in Gram-negative bacteria. Curr. Opin. Microbiol. 15:189-193. http://dx.doi.org/10.1016/j.mib.2011.12.007.
9. Ruiz N, Falcone B, Kahne D, Silhavy TJ. 2005. Chemical conditionality: a genetic strategy to probe organelle assembly. Cell 121:307-317. http://dx.doi.org/10.1016/j.cell.2005.02.014.
10. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008. http://dx.doi.org/10.1038/msb4100050.
11. 32, reveals a multifaceted cellular response to heat stress. Genes Dev. 20:1776-1789. http://dx.doi.org/10.1101/gad.1428206.
12. Uehara T, Parzych KR, Dinh T, Bernhardt TG. 2010. Daughter cell separation is controlled by cytokinetic ring-activated cell wall hydrolysis. EMBO J. 29:1412-1422. http://dx.doi.org/10.1038/emboj.2010.36.
13. Bremer E, Silhavy TJ, Weisemann JM, Weinstock GM. 1984. Lambda placMu: a transposable derivative of bacteriophage lambda for creating lacZ protein fusions in a single step. J. Bacteriol. 158:1084-1093.
14. Cherepanov PP, Wackernagel W. 1995. Gene disruption in Escherichia coli: TcR andKmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9-14. http://dx.doi.org/10.1016/0378-1119(95)00193-A.
15. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685. http://dx.doi.org/10.1038/227680a0.
16. Collet JF, D'Souza JC, Jakob U, Bardwell JC. 2003. Thioredoxin 2, an oxidative stress-induced protein, contains a high affinity zinc binding site. J. Biol. Chem. 278:45325-45332. http://dx.doi.org/10.1074/jbc.M307818200.
17. Jakob U, Eser M, Bardwell JC. 2000. Redox switch of hsp33 has a novel zinc-binding motif. J. Biol. Chem. 275:38302-38310. http://dx.doi.org/10.1074/jbc.M005957200.
18. Beinert H. 1983. Semi-micro methods for analysis of labile sulfide and of labile sulfide plus sulfane sulfur in unusually stable iron-sulfur proteins. Anal. Biochem. 131:373-378. http://dx.doi.org/10.1016/0003-2697(83)90186-0.
19. Sliusarenko O, Heinritz J, Emonet T, Jacobs-Wagner C. 2011. Highthroughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics. Mol. Microbiol. 80:612-627. http://dx.doi.org/10.1111/j.1365-2958.2011.07579.x.
20. Raetz CR, Whitfield C. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635-700. http://dx.doi.org/10.1146/annurev.biochem.71.110601.135414.
21. Hagan CL, Silhavy TJ, Kahne D. 2011. beta-Barrel membrane protein assembly by the Bam complex. Annu. Rev. Biochem. 80:189-210. http://dx.doi.org/10.1146/annurev-biochem-061408-144611.
22. Narita S, Masui C, Suzuki T, Dohmae N, Akiyama Y. 2013. Protease homolog BepA (YfgC) promotes assembly and degradation of beta-barrel membrane proteins in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 110: E3612-3621. http://dx.doi.org/10.1073/pnas.1312012110.
23. Casadaban MJ, Cohen SN. 1980. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J. Mol. Biol. 138:179-207. http://dx.doi.org/10.1016/0022-2836(80)90283-1.
24. Casadaban MJ. 1976. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J. Mol. Biol. 104:541-555. http://dx.doi.org/10.1016/0022-2836(76)90119-4.
25. Cho BK, Zengler K, Qiu Y, Park YS, Knight EM, Barrett CL, Gao Y, Palsson BO. 2009. The transcription unit architecture of the Escherichia coli genome. Nat. Biotechnol. 27:1043-1049. http://dx.doi.org/10.1038/nbt.1582.
26. Daley DO, Rapp M, Granseth E, Melen K, Drew D, von Heijne G. 2005. Global topology analysis of the Escherichia coli inner membrane proteome. Science 308:1321-1323. http://dx.doi.org/10.1126/science.1109730.
27. Nielsen H, Engelbrecht J, Brunak S, von Heijne G. 1997. A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Int. J. Neural Syst. 8:581-599. http://dx.doi.org/10.1142/S0129065797000537.
28. von Heijne G, Gavel Y. 1988. Topogenic signals in integral membrane proteins. Eur. J. Biochem. 174:671-678. http://dx.doi.org/10.1111/j.1432-1033.1988.tb14150.x.
29. Beam CE, Saveson CJ, Lovett ST. 2002. Role for radA/sms in recombination intermediate processing in Escherichia coli. J. Bacteriol. 184:6836-6844. http://dx.doi.org/10.1128/JB.184.24.6836-6844.2002.
30. Lovenberg W, Sobel BE. 1965. Rubredoxin: a new electron transfer protein from Clostridium pasteurianum. Proc. Natl. Acad. Sci. U. S. A. 54:193-199. http://dx.doi.org/10.1073/pnas.54.1.193.
31. Lee HJ, Lian LY, Scrutton NS. 1997. Recombinant two-iron rubredoxin of Pseudomonas oleovorans: overexpression, purification and characterization by optical,CDand 113CdNMRspectroscopies. Biochem. J. 328:131-136.
32. Zheng P, Takayama SJ, Mauk AG, Li H. 2012. Hydrogen bond strength modulates the mechanical strength of ferric-thiolate bonds in rubredoxin. J. Am. Chem. Soc. 134:4124-4131. http://dx.doi.org/10.1021/ja2078812.
33. Blatch GL, Lassle M. 1999. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21:932-939. http://dx.doi.org/10.1002/(SICI)1521-1878(199911)21:11932::AID-BIES53.0.CO;2-N.
34. Liu J, Oganesyan N, Shin DH, Jancarik J, Yokota H, Kim R, Kim SH. 2005. Structural characterization of an iron-sulfur cluster assembly protein IscU in a zinc-bound form. Proteins 59:875-881. http://dx.doi.org/10.1002/prot.20421.
35. Zhang J, Kasciukovic T, White MF. 2012. The CRISPR associated protein Cas4 is a 5' to 3' DNA exonuclease with an iron-sulfur cluster. PLoS One 7:e47232. http://dx.doi.org/10.1371/journal.pone.0047232.
36. Ramelot TA, Cort JR, Goldsmith-Fischman S, Kornhaber GJ, Xiao R, Shastry R, Acton TB, Honig B, Montelione GT, Kennedy MA. 2004. Solution NMR structure of the iron-sulfur cluster assembly protein U (IscU) with zinc bound at the active site. J. Mol. Biol. 344:567-583. http://dx.doi.org/10.1016/j.jmb.2004.08.038.
37. 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. http://dx.doi.org/10.1073/pnas.0805309105.
38. Burdett ID, Murray RG. 1974. Septum formation in Escherichia coli: characterization of septal structure and the effects of antibiotics on cell division. J. Bacteriol. 119:303-324.
39. Meisel U, Holtje JV, Vollmer W. 2003. Overproduction of inactive variants of the murein synthase PBP1B causes lysis in Escherichia coli. J. Bacteriol. 185:5342-5348. http://dx.doi.org/10.1128/JB.185.18.5342-5348.2003.
40. Yao Z, Kahne D, Kishony R. 2012. Distinct single-cell morphological dynamics under beta-lactam antibiotics. Mol. Cell 48:705-712. http://dx.doi.org/10.1016/j.molcel.2012.09.016.
41. Hara H, Yamamoto Y, Higashitani A, Suzuki H, Nishimura Y. 1991. Cloning, mapping, and characterization of the Escherichia coli prc gene, which is involved in C-terminal processing of penicillin-binding protein 3. J. Bacteriol. 173:4799-4813.
42. Ohara M, Wu HC, Sankaran K, Rick PD. 1999. Identification and characterization of a new lipoprotein, NlpI, in Escherichia coli K-12. J. Bacteriol. 181:4318-4325.
43. Schmidt KL, Peterson ND, Kustusch RJ, Wissel MC, Graham B, Phillips GJ, Weiss DS. 2004. A predicted ABC transporter, FtsEX, is needed for cell division in Escherichia coli. J. Bacteriol. 186:785-793. http://dx.doi.org/10.1128/JB.186.3.785-793.2004.
44. Bernhardt TG, de Boer PA. 2004. Screening for synthetic lethal mutants in Escherichia coli and identification of EnvC (YibP) as a periplasmic septal ring factor with murein hydrolase activity. Mol. Microbiol. 52:1255-1269. http://dx.doi.org/10.1111/j.1365-2958.2004.04063.x.
45. Peters NT, Morlot C, Yang DC, Uehara T, Vernet T, Bernhardt TG. 2013. Structure-function analysis of the LytM domain of EnvC, an activator of cell wall remodelling at the Escherichia coli division site. Mol. Microbiol. 89:690-701. http://dx.doi.org/10.1111/mmi.12304.
46. Tamae C, Liu A, Kim K, Sitz D, Hong J, Becket E, Bui A, Solaimani P, Tran KP, Yang H, Miller JH. 2008. Determination of antibiotic hypersensitivity among 4,000 single-gene-knockout mutants of Escherichia coli. J. Bacteriol. 190:5981-5988. http://dx.doi.org/10.1128/JB.01982-07.
47. Braun V, Sieglin U. 1970. The covalent murein-lipoprotein structure of the Escherichia coli cell wall. The attachment site of the lipoprotein on the murein. Eur. J. Biochem. 13:336-346.
48. Braun V, Wolff H. 1970. The murein-lipoprotein linkage in the cell wall of Escherichia coli. Eur. J. Biochem. 14:387-391. http://dx.doi.org/10.1111/j.1432-1033.1970.tb00301.x.
49. Paradis-Bleau C, Markovski M, Uehara T, Lupoli TJ, Walker S, Kahne DE, Bernhardt TG. 2010. Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases. Cell 143:1110-1120. http://dx.doi.org/10.1016/j.cell.2010.11.037.
50. Typas A, Banzhaf M, van den Berg van Saparoea B, Verheul J, Biboy J, Nichols RJ, Zietek M, Beilharz K, Kannenberg K, von Rechenberg M, Breukink E, den Blaauwen T, Gross CA, Vollmer W. 2010. Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 143:1097-1109. http://dx.doi.org/10.1016/j.cell.2010.11.038.