Penicillin-binding protein 5 can form a homo-oligomeric complex in the inner membrane of Escherichia coli

Protein Science

Volumn 20, Issue 9, 2011, Pages 1520-1529

  Skoog, Karl ^a   Bruzell, Filippa Stenberg ^a   Ducroux, Aurélie ^a   Hellberg, Mårten ^a   Johansson, Henrik ^b,c   Lehtiö, Janne ^b,c   Högbom, Martin ^a   Daley, Daniel O ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c SCIENCE FOR LIFE LABORATORY   (Sweden)

Author keywords

Homo oligomer; Membrane protein; Penicillin binding protein; Peptidoglycan biogenesis

Indexed keywords

DETERGENT; HOMODIMER; OLIGOMER; PENICILLIN BINDING PROTEIN 5; PENTAPEPTIDE; PEPTIDOGLYCAN;

ARTICLE; CATALYSIS; CELL MEMBRANE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION;

CELL MEMBRANE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; PENICILLIN-BINDING PROTEINS; PEPTIDOGLYCAN; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

ESCHERICHIA COLI;

EID: 84860390560     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.677     Document Type: Article

References (56)

1. Holtje J.V. (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62:181-203.
2. Scheffers D.J., Pinho M.G. (2005) Bacterial cell wall synthesis: New insights from localization studies. Microbiol Mol Biol Rev 69:585-607.
3. Vollmer W., Bertsche U. (2007) Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochim Biophys Acta 1778:1714-1734.
4. Den Blaauwen T., De Pedro M.A., Nguyen-Disteche M., Ayala J.A. (2008) Morphogenesis of rod-shaped sacculi. FEMS Microbiol Rev 32:321-344. (Pubitemid 351257813)
5. Waxman D.J., Strominger J.L. (1983) Penicillin-binding proteins and the mechanism of action of beta-lactam antibiotics. Annu Rev Biochem 52:825-869. (Pubitemid 13030694)
6. Cabeen M.T., Jacobs-Wagner C. (2005) Bacterial cell shape. Nat Rev Microbiol 3:601-610. (Pubitemid 41052147)
7. Macheboeuf P., Contreras-Martel C., Job V., Dideberg O., Dessen A. (2006) Penicillin binding proteins: Key players in bacterial cell cycle and drug resistance processes. FEMS Microbiol Rev 30:673-691. (Pubitemid 44199345)
8. Holtje J.V. (1996) A hypothetical holoenzyme involved in the replication of the murein sacculus of Escherichia coli. Microbiology 142(pt 8):1911-1918.
9. Harris F., Phoenix D.A. (1998) The Escherichia coli low molecular mass penicillin-binding proteins and a putative membrane bound protein complex. Membr Cell Biol 11:591-596. (Pubitemid 28291188)
10. Alaedini A., Day R.A. (1999) Identification of two penicillin-binding multienzyme complexes in Haemophilus influenzae. Biochem Biophys Res Commun 264: 191-195. (Pubitemid 29500486)
11. Romeis T., Holtje J.V. (1994) Specific interaction of penicillin-binding proteins 3 and 7/8 with soluble lytic transglycosylase in Escherichia coli. J Biol Chem 269: 21603-21607. (Pubitemid 24274795)
12. Vollmer W., Von Rechenberg M., Holtje J.V. (1999) Demonstration of molecular interactions between the murein polymerase PBP1B, the lytic transglycosylase MltA, and the scaffolding protein MipA of Escherichia coli. J Biol Chem 274:6726-6734. (Pubitemid 29111094)
13. Bertsche U., Kast T., Wolf B., Fraipont C., Aarsman M.E., Kannenberg K., Von Rechenberg M., Nguyen-Disteche M., Den Blaauwen T., Holtje J.V., Vollmer W. (2006) Interaction between two murein (peptidoglycan) synthases, PBP3 and PBP1B, in Escherichia coli. Mol Microbiol 61:675-690. (Pubitemid 44324092)
14. Van den Ent F., Leaver M., Bendezu F., Errington J., De Boer P., Lowe J. (2006) Dimeric structure of the cell shape protein MreC and its functional implications. Mol Microbiol 62:1631-1642. (Pubitemid 44813809)
15. Muller P., Ewers C., Bertsche U., Anstett M., Kallis T., Breukink E., Fraipont C., Terrak M., Nguyen-Disteche M., Vollmer W. (2007) The essential cell division protein FtsN interacts with the murein (peptidoglycan) synthase PBP1B in Escherichia coli. J Biol Chem 282: 36394-36402.
16. Derouaux A., Wolf B., Fraipont C., Breukink E., Nguyen- Disteche M, Terrak M (2007) The monofunctional glycosyltransferase of Escherichia coli localizes to the cell division site and interacts with the penicillin-binding protein 3 (PBP3), FtsW and FtsN. J Bacteriol 190: 1831-1834.
17. Legaree B.A., Clarke A.J. (2008) Interaction of penicillinbinding protein 2 with soluble lytic transglycosylase B1 in Pseudomonas aeruginosa. J Bacteriol 190:6922-6926.
18. Sung M.T., Lai Y.T., Huang C.Y., Chou L.Y., Shih H.W., Cheng W.C., Wong C.H., Ma C. (2009) Crystal structure of the membrane-bound bifunctional transglycosylase PBP1b from Escherichia coli. Proc Natl Acad Sci USA 106:8824-8829.
19. Fraipont C., Alexeeva S., Wolf B., Van der Ploeg R., Schloesser M., Den Blaauwen T., Nguyen-Disteche M. (2011) The integral membrane FtsW protein and peptidoglycan synthase PBP3 form a sub-complex in Escherichia coli. Microbiology 157(Pt 1):251-259.
20. Zijderveld C.A., Aarsman M.E., Den Blaauwen T., Nanninga N. (1991) Penicillin-binding protein 1B of Escherichia coli exists in dimeric forms. J Bacteriol 173: 5740-5746.
21. Charpentier X., Chalut C., Remy M.H., Masson J.M. (2002) Penicillin-binding proteins 1a and 1b form independent dimers in Escherichia coli. J Bacteriol 184: 3749-3752. (Pubitemid 34625687)
22. Bertsche U., Breukink E., Kast T., Vollmer W. (2005) In vitro murein peptidoglycan synthesis by dimers of the bifunctional transglycosylase- transpeptidase PBP1B from Escherichia coli. J Biol Chem 280:38096-38101. (Pubitemid 41642424)
23. Kishida H., Unzai S., Roper D.I., Lloyd A., Park S.Y., Tame J.R. (2006) Crystal structure of penicillin binding protein 4 (dacB) from Escherichia coli, both in the native form and covalently linked to various antibiotics. Biochemistry 45:783-792. (Pubitemid 43122243)
24. Potluri L., Karczmarek A., Verheul J., Piette A., Wilkin J.M., Werth N., Banzhaf M., Vollmer W., Young K.D., Nguyen-Disteche M., Den Blaauwen T. (2010) Septal and lateral wall localization of PBP5, the major D,D-carboxypeptidase of Escherichia coli, requires substrate recognition and membrane attachment. Mol Microbiol 77:300-323
25. Popham D.L., Young K.D. (2003) Role of penicillin-binding proteins in bacterial cell morphogenesis. Curr Opin Microbiol 6:594-599. (Pubitemid 38020056)
26. Nelson D.E., Young K.D. (2000) Penicillin binding protein 5 affects cell diameter, contour, and morphology of Escherichia coli. J Bacteriol 182:1714-1721. (Pubitemid 30121137)
27. Nelson D.E., Young K.D. (2001) Contributions of PBP 5 and DD-carboxypeptidase penicillin binding proteins to maintenance of cell shape in Escherichia coli. J Bacteriol 183:3055-3064. (Pubitemid 32433522)
28. Nelson D.E., Ghosh A.S., Paulson A.L., Young K.D. (2002) Contribution of membrane-binding and enzymatic domains of penicillin binding protein 5 to maintenance of uniform cellular morphology of Escherichia coli. J Bacteriol 184:3630-3639. (Pubitemid 34625672)
29. Ghosh A.S., Chowdhury C., Nelson D.E. (2008) Physiological functions of D-alanine carboxypeptidases in Escherichia coli. Trends Microbiol 16:309-317.
30. Sarkar S.K., Chowdhury C., Ghosh A.S. (2010) Deletion of penicillin-binding protein 5 (PBP5) sensitises Escherichia coli cells to beta-lactam agents. Int J Antimicrob Agents 35:244-249.
31. Davies C., White S.W., Nicholas R.A. (2001) Crystal structure of a deacylation-defective mutant of penicillinbinding protein 5 at 2.3-Å resolution. J Biol Chem 276: 616-623. (Pubitemid 32050861)
32. Nicholas R.A., Krings S., Tomberg J., Nicola G., Davies C. (2003) Crystal structure of wild-type penicillin-binding protein 5 from Escherichia coli: Implications for deacylation of the acyl-enzyme complex. J Biol Chem 278: 52826-52833. (Pubitemid 38035881)
33. Nicola G., Peddi S., Stefanova M., Nicholas R.A., Gutheil W.G., Davies C. (2005) Crystal structure of Escherichia coli penicillin-binding protein 5 bound to a tripeptide boronic acid inhibitor: A role for Ser-110 in deacylation. Biochemistry 44:8207-8217. (Pubitemid 40799901)
34. Sauvage E., Powell A.J., Heilemann J., Josephine H.R., Charlier P., Davies C., Pratt R.F. (2008) Crystal structures of complexes of bacterial DD-peptidases with peptidoglycan-mimetic ligands: The substrate specificity puzzle. J Mol Biol 381:383-393.
35. Chen Y., Zhang W., Shi Q., Hesek D., Lee M., Mobashery S., Shoichet B.K. (2009) Crystal structures of penicillinbinding protein 6 from Escherichia coli. J Am Chem Soc 131:14345-14354.
36. Pratt J.M., Jackson M.E., Holland I.B. (1986) The C terminus of penicillin-binding protein 5 is essential for localisation to the E. coli inner membrane. EMBO J 5: 2399-2405.
37. Jackson M.E., Pratt J.M. (1987) An 18 amino acid amphiphilic helix forms the membrane-anchoring domain of the Escherichia coli penicillin-binding protein 5. Mol Microbiol 1:23-28.
38. O'Daniel P.I., Zajicek J., Zhang W., Shi Q., Fisher J.F., Mobashery S. (2010) Elucidation of the structure of the membrane anchor of penicillin-binding protein 5 of Escherichia coli. J Am Chem Soc 132:4110-4118.
39. Wittig I., Braun H.P., Schagger H. (2006) Blue native PAGE. Nat Protoc 1:418-428.
40. Stenberg F., Chovanec P., Maslen S.L., Robinson C.V., Ilag L.L., Von Heijne G., Daley D.O. (2005) Protein complexes of the Escherichia coli cell envelope. J Biol Chem 280: 34409-34419. (Pubitemid 41504568)
41. Wittig I., Beckhaus T., Wumaier Z., Karas M., Schagger H. (2010) Mass estimation of native proteins by bluen-ative electrophoresis: Principles and practical hints. Mol Cell Proteomics 9:2149-2161.
42. Maddalo G., Stenberg Bruzell F., Gotzke H., Toddo S., Bjorkholm P., Eriksson H., Chovanec P., Genevaux P., Lehtio J., Ilag L.L., Daley D.O. (2011) A systematic analysis of native membrane protein complexes in Escherichia coli. J Proteome Res 10:1848-1859.
43. Hajjar E., Bessonov A.N., Molitor A., Kumar A., Mahendran K.R., Winterhalter M., Pages J.M., Ruggerone P., Ceccarelli M. (2010) Towards screening for antibiotics with enhanced permeation properties through bacterial porins. Biochemistry 49:6928-6935.
44. Pages J.M., James C.E., Winterhalter M. (2008) The porin and the permeating antibiotic: A selective diffusion barrier in Gram-negative bacteria. Nat Rev Microbiol 6:893-903.
45. Markiewicz Z., Broome-Smith J.K., Schwarz U., Spratt B.G. (1982) Spherical E. coli due to elevated levels of D-alanine carboxypeptidase. Nature 297:702-704. (Pubitemid 12096198)
46. Chamberlin M., McGrath J., Waskell L. (1970) New RNA polymerase from Escherichia coli infected with bacteriophage T7. Nature 228:227-231.
47. Wang C.C., Schultz D.E., Nicholas R.A. (1996) Localization of a putative second membrane association site in penicillin-binding protein 1B of Escherichia coli. Biochem J 316(pt 1):149-156. (Pubitemid 26158215)
48. White S.H. (2004) The progress of membrane protein structure determination. Protein Sci 13:1948-1949.
49. Lovering A.L., De Castro L., Strynadka N.C. (2008) Identification of dynamic structural motifs involved in peptidoglycan glycosyltransfer. J Mol Biol 383:167-177.
50. Blumberg P.M., Strominger J.L. (1972) Isolation by covalent affinity chromatography of the penicillin-binding components from membranes of Bacillus subtilis. Proc Natl Acad Sci USA 69:3751-3755.
51. Blattner F.R., Plunkett G.,3rd, Bloch C.A., Perna N.T., Burland V., Riley M., Collado-Vides J., Glasner J.D., Rode C.K., Mayhew G.F., Gregor J., Davis N.W., Kirkpatrick H.A., Goeden M.A., Rose D.J., Mau B., Shao Y. (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474.
52. Rapp M., Drew D., Daley D.O., Nilsson J., Carvalho T., Melen K., De Gier J.W., Von Heijne G. (2004) Experimentally based topology models for E. coli inner membrane proteins. Protein Sci 13:937-945. (Pubitemid 38429217)
53. Daley D.O., 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. (Pubitemid 40746130)
54. Latour D.J., Weiner J.H. (1989) Assembly of Escherichia coli fumarate reductase holoenzyme. Biochem Cell Biol 67:251-259. (Pubitemid 19202900)
55. Stenberg F., Von Heijne G., Daley D.O. (2007) Assembly of the cytochrome bo3 complex. J Mol Biol 371: 765-773.
56. Groeneveld M., Slotboom D.J. (2007) Rigidity of the subunit interfaces of the trimeric glutamate transporter GltT during translocation. J Mol Biol 372:565-570. (Pubitemid 47313480)