Interactions between late-acting proteins required for peptidoglycan synthesis during sporulation

Journal of Molecular Biology

Volumn 399, Issue 4, 2010, Pages 547-561

  Fay, Allison ^a   Meyer, Pablo ^a   Dworkin, Jonathan ^a  

^a Department of Neurology and the Taub Institute for Research on Alzheimer's Disease and the Aging Brain   (United States)

Author keywords

Bacterial cell division; Bacterial growth; Peptidoglycan; Sporulation

Indexed keywords

BINDING PROTEIN; HYBRID PROTEIN; PEPTIDOGLYCAN; PHENETICILLIN;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL GROWTH; BINDING AFFINITY; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; IMMUNOPRECIPITATION; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PURIFICATION; SPOROGENESIS; WILD TYPE;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 77954763191     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.04.036     Document Type: Article

References (57)

1. van Heijenoort J. Recent advances in the formation of the bacterial peptidoglycan monomer unit. Nat. Prod. Rep. 2001, 18:503-519.
2. Gerard P., Vernet T., Zapun A. Membrane topology of the Streptococcus pneumoniae FtsW division protein. J. Bacteriol. 2002, 184:1925-1931.
3. Lara B., Ayala J.A. Topological characterization of the essential Escherichia coli cell division protein FtsW. FEMS Microbiol. Lett. 2002, 216:23-32.
4. Real G., Fay A., Eldar A., Pinto S.M., Henriques A.O., Dworkin J. Determinants for the subcellular localization and function of a nonessential SEDS protein. J. Bacteriol. 2008, 190:363-376.
5. Ikeda M., Sato T., Wachi M., Jung H.K., Ishino F., Kobayashi Y., Matsuhashi M. Structural similarity among Escherichia coli FtsW and RodA proteins and Bacillus subtilis SpoVE protein, which function in cell division, cell elongation, and spore formation, respectively. J. Bacteriol. 1989, 171:6375-6378.
6. Henriques A.O., Glaser P., Piggot P.J., Moran C.P. Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol. Microbiol. 1998, 28:235-247.
7. Ishino F., Park W., Tomioka S., Tamaki S., Takase I., Kunugita K., et al. Peptidoglycan synthetic activities in membranes of Escherichia coli caused by overproduction of penicillin-binding protein 2 and rodA protein. J. Biol. Chem. 1986, 261:7024-7031.
8. Holtje J.V. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 1998, 62:181-203.
9. Khattar M.M., Addinall S.G., Stedul K.H., Boyle D.S., Lutkenhaus J., Donachie W.D. Two polypeptide products of the Escherichia coli cell division gene ftsW and a possible role for FtsW in FtsZ function. J. Bacteriol. 1997, 179:784-793.
10. Khattar M.M., Begg K.J., Donachie W.D. Identification of FtsW and characterization of a new ftsW division mutant of Escherichia coli. J. Bacteriol. 1994, 176:7140-7147.
11. Boyle D.S., Khattar M.M., Addinall S.G., Lutkenhaus J., Donachie W.D. ftsW is an essential cell-division gene in Escherichia coli. Mol. Microbiol. 1997, 24:1263-1273.
12. Vasudevan P., Weaver A., Reichert E.D., Linnstaedt S.D., Popham D.L. Spore cortex formation in Bacillus subtilis is regulated by accumulation of peptidoglycan precursors under the control of sigma K. Mol. Microbiol. 2007, 65:1582-1594.
13. Nakagawa J., Tamaki S., Tomioka S., Matsuhashi M. Functional biosynthesis of cell wall peptidoglycan by polymorphic bifunctional polypeptides. Penicillin-binding protein 1Bs of Escherichia coli with activities of transglycosylase and transpeptidase. J. Biol. Chem. 1984, 259:13937-13946.
14. Ishino F., Mitsui K., Tamaki S., Matsuhashi M. Dual enzyme activities of cell wall peptidoglycan synthesis, peptidoglycan transglycosylase and penicillin-sensitive transpeptidase, in purified preparations of Escherichia coli penicillin-binding protein 1A. Biochem. Biophys. Res. Commun. 1980, 97:287-293.
15. Suzuki H., van Heijenoort Y., Tamura T., Mizoguchi J., Hirota Y., van Heijenoort J. In vitro peptidoglycan polymerization catalysed by penicillin binding protein 1b of Escherichia coli K-12. FEBS Lett. 1980, 110:245-249.
16. Popham D.L., Setlow P. Cloning, nucleotide sequence, and regulation of the Bacillus subtilis pbpF gene, which codes for a putative class A high-molecular-weight penicillin-binding protein. J. Bacteriol. 1993, 175:4870-4876.
17. Suzuki H., Nishimura Y., Hirota Y. On the process of cellular division in Escherichia coli: a series of mutants of E. coli altered in the penicillin-binding proteins. Proc. Natl Acad. Sci. USA 1978, 75:664-668.
18. Sauvage E., Kerff F., Terrak M., Ayala J.A., Charlier P. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol. Rev. 2008, 32:234-258.
19. Adam M., Fraipont C., Rhazi N., Nguyen-Disteche M., Lakaye B., Frere J.M., et al. The bimodular G57-V577 polypeptide chain of the class B penicillin-binding protein 3 of Escherichia coli catalyzes peptide bond formation from thiolesters and does not catalyze glycan chain polymerization from the lipid II intermediate. J. Bacteriol. 1997, 179:6005-6009.
20. Zhao G., Yeh W.K., Carnahan R.H., Flokowitsch J., Meier T.I., Alborn W.E., et al. Biochemical characterization of penicillin-resistant and -sensitive penicillin-binding protein 2x transpeptidase activities of Streptococcus pneumoniae and mechanistic implications in bacterial resistance to beta-lactam antibiotics. J. Bacteriol. 1997, 179:4901-4908.
21. Pisabarro A.G., Prats R., Vaquez D., Rodriguez-Tebar A. Activity of penicillin-binding protein 3 from Escherichia coli. J. Bacteriol. 1986, 168:199-206.
22. Alaedini A., Day R.A. Identification of two penicillin-binding multienzyme complexes in Haemophilus influenzae. Biochem. Biophys. Res. Commun. 1999, 264:191-195.
23. Begg K.J., Spratt B.G., Donachie W.D. Interaction between membrane proteins PBP3 and rodA is required for normal cell shape and division in Escherichia coli. J. Bacteriol. 1986, 167:1004-1008.
24. Karimova G., Dautin N., Ladant D. Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J. Bacteriol. 2005, 187:2233-2243.
25. Datta P., Dasgupta A., Singh A.K., Mukherjee P., Kundu M., Basu J. Interaction between FtsW and penicillin-binding protein 3 (PBP3) directs PBP3 to mid-cell, controls cell septation and mediates the formation of a trimeric complex involving FtsZ, FtsW and PBP3 in mycobacteria. Mol. Microbiol. 2006, 62:1655-1673.
26. Pastoret S., Fraipont C., den Blaauwen T., Wolf B., Aarsman M.E., Piette A., et al. Functional analysis of the cell division protein FtsW of Escherichia coli. J. Bacteriol. 2004, 186:8370-8379.
27. Henriques A.O., de Lencastre H., Piggot P.J. A Bacillus subtilis morphogene cluster that includes spoVE is homologous to the mra region of Escherichia coli. Biochimie 1992, 74:735-748.
28. Daniel R.A., Drake S., Buchanan C.E., Scholle R., Errington J. The Bacillus subtilis spoVD gene encodes a mother-cell-specific penicillin-binding protein required for spore morphogenesis. J. Mol. Biol. 1994, 235:209-220.
29. Piggot P.J., Coote J.G. Genetic aspects of bacterial endospore formation. Bacteriol. Rev. 1976, 40:908-962.
30. Eichenberger P., Jensen S.T., Conlon E.M., van Ooij C., Silvaggi J., Gonzalez-Pastor J.E., et al. The sigmaE regulon and the identification of additional sporulation genes in Bacillus subtilis. J. Mol. Biol. 2003, 327:945-972.
31. Mercer K.L., Weiss D.S. The Escherichia coli cell division protein FtsW is required to recruit its cognate transpeptidase, FtsI (PBP3), to the division site. J. Bacteriol. 2002, 184:904-912.
32. Akiyama Y., Kihara A., Tokuda H., Ito K. FtsH (HflB) is an ATP-dependent protease selectively acting on SecY and some other membrane proteins. J. Biol. Chem. 1996, 271:31196-31201.
33. Sloma A., Rufo G.A., Theriault K.A., Dwyer M., Wilson S.W., Pero J. Cloning and characterization of the gene for an additional extracellular serine protease of Bacillus subtilis. J. Bacteriol. 1991, 173:6889-6895.
34. Scheffers D.J., Jones L.J., Errington J. Several distinct localization patterns for penicillin-binding proteins in Bacillus subtilis. Mol. Microbiol. 2004, 51:749-764.
35. Rubio A., Pogliano K. Septal localization of forespore membrane proteins during engulfment in Bacillus subtilis. EMBO J. 2004, 23:1636-1646.
36. Miyawaki A., Tsien R.Y. Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Methods Enzymol. 2000, 327:472-500.
37. Bowler L.D., Spratt B.G. Membrane topology of penicillin-binding protein 3 of Escherichia coli. Mol. Microbiol. 1989, 3:1277-1286.
38. McLeod M.P., Warren R.L., Hsiao W.W., Araki N., Myhre M., Fernandes C., et al. The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc. Natl Acad. Sci. USA 2006, 103:15582-15587.
39. Marrec-Fairley M., Piette A., Gallet X., Brasseur R., Hara H., Fraipont C., et al. Differential functionalities of amphiphilic peptide segments of the cell-septation penicillin-binding protein 3 of Escherichia coli. Mol. Microbiol. 2000, 37:1019-1031.
40. Piette A., Fraipont C., Den Blaauwen T., Aarsman M.E., Pastoret S., Nguyen-Disteche M. Structural determinants required to target penicillin-binding protein 3 to the septum of Escherichia coli. J. Bacteriol. 2004, 186:6110-6117.
41. Yanouri A., Daniel R.A., Errington J., Buchanan C.E. Cloning and sequencing of the cell division gene pbpB, which encodes penicillin-binding protein 2B in Bacillus subtilis. J. Bacteriol. 1993, 175:7604-7616.
42. Dessen A., Mouz N., Gordon E., Hopkins J., Dideberg O. Crystal structure of PBP2x from a highly penicillin-resistant Streptococcus pneumoniae clinical isolate: a mosaic framework containing 83 mutations. J. Biol. Chem. 2001, 276:45106-45112.
43. Noirclerc-Savoye M., Morlot C., Gerard P., Vernet T., Zapun A. Expression and purification of FtsW and RodA from Streptococcus pneumoniae, two membrane proteins involved in cell division and cell growth, respectively. Protein Expression Purif. 2003, 30:18-25.
44. Born P., Breukink E., Vollmer W. In vitro synthesis of cross-linked murein and its attachment to sacculi by PBP1A from Escherichia coli. J. Biol. Chem. 2006, 281:26985-26993.
45. Bertsche U., Kast T., Wolf B., Fraipont C., Aarsman M.E., Kannenberg K., et al. Interaction between two murein (peptidoglycan) synthases, PBP3 and PBP1B, in Escherichia coli. Mol. Microbiol. 2006, 61:675-690.
46. Popham D.L. Specialized peptidoglycan of the bacterial endospore: the inner wall of the lockbox. Cell. Mol. Life Sci. 2002, 59:426-433.
47. Daniel R.A., Errington J. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 2003, 113:767-776.
48. Tiyanont K., Doan T., Lazarus M.B., Fang X., Rudner D.Z., Walker S. Imaging peptidoglycan biosynthesis in Bacillus subtilis with fluorescent antibiotics. Proc. Natl Acad. Sci. USA 2006, 103:11033-11038.
49. Severinov K., Mooney R., Darst S.A., Landick R. Tethering of the large subunits of Escherichia coli RNA polymerase. J. Biol. Chem. 1997, 272:24137-24140.
50. Zakharova N., Hoffman P.S., Berg D.E., Severinov K. The largest subunits of RNA polymerase from gastric helicobacters are tethered. J. Biol. Chem. 1998, 273:19371-19374.
51. Schwartz B., Markwalder J.A., Wang Y. Lipid II: total synthesis of the bacterial cell wall precursor and utilization as a substrate for glycosyltransfer and transpeptidation by penicillin binding protein (PBP) 1b of Escherichia coli. J. Am. Chem. Soc. 2001, 123:11638-11643.
52. Bertsche U., Breukink E., Kast T., Vollmer W. In vitro murein peptidoglycan synthesis by dimers of the bifunctional transglycosylase-transpeptidase PBP1B from Escherichia coli. J. Biol. Chem. 2005, 280:38096-38101.
53. Youngman P., Perkins J.B., Losick R. A novel method for the rapid cloning in Escherichia coli of Bacillus subtilis chromosomal DNA adjacent to Tn917 insertions. Mol. Gen. Genet. 1984, 195:424-433.
54. Molecular Biological Methods for Bacillus (Modern Microbiological Methods) 1990, Wiley, New York, NY. C.R. Harwood, S.M. Cutting (Eds.).
55. Sterlini J.M., Mandelstam J. Commitment to sporulation in Bacillus subtilis and its relationship to development of actinomycin resistance. Biochem. J. 1969, 113:29-37.
56. Kodama T., Takamatsu H., Asai K., Kobayashi K., Ogasawara N., Watabe K. The Bacillus subtilis yaaH gene is transcribed by SigE RNA polymerase during sporulation, and its product is involved in germination of spores. J. Bacteriol. 1999, 181:4584-4591.
57. Horton R.M., Cai Z.L., Ho S.N., Pease L.R. Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. BioTechniques 1990, 8:528-535.