Escherichiacoli low-molecular-weight penicillin-binding proteins help orient septal FtsZ, and their absence leads to asymmetric cell division and branching

Molecular Microbiology

Volumn 84, Issue 2, 2012, Pages 203-224

  Potluri, Lakshmi Prasad ^a,c   de Pedro, Miguel A ^b   Young, Kevin D ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FTSZ PROTEIN; PENICILLIN BINDING PROTEIN; PENICILLIN BINDING PROTEIN 5; PENICILLIN BINDING PROTEIN 6; PEPTIDOGLYCAN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CYTOSKELETON PROTEIN; FTSZ PROTEIN, BACTERIA;

ARTICLE; BACTERIAL CELL WALL; BACTERIAL STRAIN; BRANCHING MORPHOGENESIS; CELL COUNT; CELL DIVISION; CELL ELONGATION; CELL SHAPE; CELL STRUCTURE; CYTOPLASM; ESCHERICHIA COLI; MICROBIAL MORPHOLOGY; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; Z RING; ASYMMETRIC CELL DIVISION; BIOLOGICAL MODEL; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY;

ESCHERICHIA COLI;

ASYMMETRIC CELL DIVISION; BACTERIAL PROTEINS; CYTOSKELETAL PROTEINS; ESCHERICHIA COLI; MODELS, BIOLOGICAL; PENICILLIN-BINDING PROTEINS;

EID: 84859443989     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08023.x     Document Type: Article

References (73)

1. Aarsman, M.E., Piette, A., Fraipont, C., Vinkenvleugel, T.M., Nguyen-Disteche, M., and den Blaauwen, T. (2005) Maturation of the Escherichia coli divisome occurs in two steps. Mol Microbiol 55: 1631-1645.
2. Åkerlund, T., Nordström, K., and Bernander, R. (1993) Branched Escherichia coli cells. Mol Microbiol 10: 849-858.
3. Begg, K., Nikolaichik, Y., Crossland, N., and Donachie, W.D. (1998) Roles of FtsA and FtsZ in activation of division sites. J Bacteriol 180: 881-884.
4. Bernhardt, T.G., and de Boer, P.A. (2005) SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E.coli. Mol Cell 18: 555-564.
5. Bi, E., and Lutkenhaus, J. (1992) Isolation and characterization of ftsZ alleles that affect septal morphology. J Bacteriol 174: 5414-5423.
6. Bonis, M., Ecobichon, C., Guadagnini, S., Prevost, M.C., and Boneca, I.G. (2010) A M23B family metallopeptidase of Helicobacter pylori required for cell shape, pole formation and virulence. Mol Microbiol 78: 809-819.
7. Cabeen, M.T., and Jacobs-Wagner, C. (2005) Bacterial cell shape. Nat Rev Microbiol 3: 601-610.
8. Cabeen, M.T., and Jacobs-Wagner, C. (2007) Skin and bones: the bacterial cytoskeleton, cell wall, and cell morphogenesis. J Cell Biol 179: 381-387.
9. Cho, H., McManus, H.R., Dove, S.L., and Bernhardt, T.G. (2011) Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc Natl Acad Sci USA 108: 3773-3778.
10. Chowdhury, C., Nayak, T.R., Young, K.D., and Ghosh, A.S. (2010) A weak DD-carboxypeptidase activity explains the inability of PBP 6 to substitute for PBP 5 in maintaining normal cell shape in Escherichia coli. FEMS Microbiol Lett 303: 76-83.
11. Dai, K., and Lutkenhaus, J. (1992) The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J Bacteriol 174: 6145-6151.
12. Dajkovic, A., Lan, G., Sun, S.X., Wirtz, D., and Lutkenhaus, J. (2008) MinC spatially controls bacterial cytokinesis by antagonizing the scaffolding function of FtsZ. Curr Biol 18: 235-244.
13. Denome, S.A., Elf, P.K., Henderson, T.A., Nelson, D.E., and Young, K.D. (1999) Escherichia coli mutants lacking all possible combinations of eight penicillin binding proteins: viability, characteristics, and implications for peptidoglycan synthesis. J Bacteriol 181: 3981-3993.
14. Dinh, T., and Bernhardt, T.G. (2011) Using superfolder green fluorescent protein for periplasmic protein localization studies. J Bacteriol 193: 4984-4987.
15. Divakaruni, A.V., Baida, C., White, C.L., and Gober, J.W. (2007) The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes. Mol Microbiol 66: 174-188.
16. Dziadek, J., Madiraju, M.V., Rutherford, S.A., Atkinson, M.A., and Rajagopalan, M. (2002) Physiological consequences associated with overproduction of Mycobacterium tuberculosis FtsZ in mycobacterial hosts. Microbiology 148: 961-971.
17. Erickson, H.P., Anderson, D.E., and Osawa, M. (2010) FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Molec Biol Rev 74: 504-528.
18. Flärdh, K. (2010) Cell polarity and the control of apical growth in Streptomyces. Curr Opin Microbiol 13: 758-765.
19. Flärdh, K., and Buttner, M.J. (2009) Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7: 36-49.
20. Fu, G., Huang, T., Buss, J., Coltharp, C., Hensel, Z., and Xiao, J. (2010) In vivo structure of the E.coli FtsZ-ring revealed by photoactivated localization microscopy (PALM). PLoS ONE 5: e12682.
21. Gallant, C.V., Daniels, C., Leung, J.M., Ghosh, A.S., Young, K.D., Kotra, L., and Burrows, L.L. (2005) Common β-lactamases inhibit bacterial biofilm formation. Mol Microbiol 58: 1012-1024.
22. Geissler, B., and Margolin, W. (2005) Evidence for functional overlap among multiple bacterial cell division proteins: compensating for the loss of FtsK. Mol Microbiol 58: 596-612.
23. Geissler, B., Elraheb, D., and Margolin, W. (2003) A gain-of-function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli. Proc Natl Acad Sci USA 100: 4197-4202.
24. Ghosh, A.S., and Young, K.D. (2003) Sequences near the active site in chimeric penicillin binding proteins 5 and 6 affect uniform morphology of Escherichia coli. J Bacteriol 185: 2178-2186.
25. Gullbrand, B., Akerlund, T., and Nordstrom, K. (1999) On the origin of branches in Escherichia coli. J Bacteriol 181: 6607-6614.
26. BAD promoter. J Bacteriol 177: 4121-4130.
27. Hempel, A.M., Wang, S.B., Letek, M., Gil, J.A., and Flardh, K. (2008) Assemblies of DivIVA mark sites for hyphal branching and can establish new zones of cell wall growth in Streptomyces coelicolor. J Bacteriol 190: 7579-7583.
28. Henderson, T.A., Young, K.D., Denome, S.A., and Elf, P.K. (1997) AmpC and AmpH, proteins related to the class C β-lactamases, bind penicillin and contribute to the normal morphology of Escherichia coli. J Bacteriol 179: 6112-6121.
29. Höltje, J.-V. (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62: 181-203.
30. Lam, H., Schofield, W.B., and Jacobs-Wagner, C. (2006) A landmark protein essential for establishing and perpetuating the polarity of a bacterial cell. Cell 124: 1011-1023.
31. Li, S.Y., Höltje, J.-V., and Young, K.D. (2004) Comparison of high-performance liquid chromatography and fluorophore-assisted carbohydrate electrophoresis methods for analyzing peptidoglycan composition of Escherichia coli. Anal Biochem 326: 1-12.
32. Li, Z., Trimble, M.J., Brun, Y.V., and Jensen, G.J. (2007) The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J 26: 4694-4708.
33. Lutkenhaus, J. (2007) Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem 76: 539-562.
34. Meberg, B.M., Sailer, F.C., Nelson, D.E., and Young, K.D. (2001) Reconstruction of Escherichia coli mrcA (PBP 1a) mutants lacking multiple combinations of penicillin binding proteins. J Bacteriol 183: 6148-6149.
35. Meberg, B.M., Paulson, A.L., Priyadarshini, R., and Young, K.D. (2004) Endopeptidase penicillin-binding proteins 4 and 7 play auxiliary roles in determining uniform morphology of Escherichia coli. J Bacteriol 186: 8326-8336.
36. Nelson, D.E., and Young, K.D. (2000) Penicillin binding protein 5 affects cell diameter, contour, and morphology of Escherichia coli. J Bacteriol 182: 1714-1721.
37. Nelson, D.E., and 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.
38. Nelson, D.E., Ghosh, A.S., Paulson, A.L., and 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.
39. Nilsen, T., Ghosh, A.S., Goldberg, M.B., and Young, K.D. (2004) Branching sites and morphological abnormalities behave as ectopic poles in shape-defective Escherichia coli. Mol Microbiol 52: 1045-1054.
40. Paradis-Bleau, C., Markovski, M., Uehara, T., Lupoli, T.J., Walker, S., Kahne, D.E., and Bernhardt, T.G. (2010) Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases. Cell 143: 1110-1120.
41. de Pedro, M.A., Quintela, J.C., Höltje, J.V., and Schwarz, H. (1997) Murein segregation in Escherichia coli. J Bacteriol 179: 2823-2834.
42. de Pedro, M.A., Young, K.D., Höltje, J.V., and Schwarz, H. (2003) Branching of Escherichia coli cells arises from multiple sites of inert peptidoglycan. J Bacteriol 185: 1147-1152.
43. de Pedro, M.A., Grunfelder, C.G., and Schwarz, H. (2004) Restricted mobility of cell surface proteins in the polar regions of Escherichia coli. J Bacteriol 186: 2594-2602.
44. Peters, N.T., Dinh, T., and Bernhardt, T.G. (2011) A fail-safe mechanism in the septal ring assembly pathway generated by the sequential recruitment of cell separation amidases and their activators. J Bacteriol 193: 4973-4983.
45. Peters, P.C., Migocki, M.D., Thoni, C., and Harry, E.J. (2007) A new assembly pathway for the cytokinetic Z ring from a dynamic helical structure in vegetatively growing cells of Bacillus subtilis. Mol Microbiol 64: 487-499.
46. Pichoff, S., and Lutkenhaus, J. (2007) Overview of cell shape: cytoskeletons shape bacterial cells. Curr Opin Microbiol 10: 601-605.
47. Pilgrim, S., Kolb-Maurer, A., Gentschev, I., Goebel, W., and Kuhn, M. (2003) Deletion of the gene encoding p60 in Listeria monocytogenes leads to abnormal cell division and loss of actin-based motility. Infect Immun 71: 3473-3484.
48. Potluri, L., Karczmarek, A., Verheul, J., Piette, A., Wilkin, J.M., Werth, N., etal. (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.
49. Priyadarshini, R., Popham, D.L., and Young, K.D. (2006) Daughter cell separation by penicillin-binding proteins and peptidoglycan amidases in Escherichia coli. J Bacteriol 188: 5345-5355.
50. Ramos, A., Letek, M., Campelo, A.B., Vaquera, J., Mateos, L.M., and Gil, J.A. (2005) Altered morphology produced by ftsZ expression in Corynebacterium glutamicum ATCC 13869. Microbiology 151: 2563-2572.
51. Rothfield, L. (2003) New insights into the developmental history of the bacterial cell division site. J Bacteriol 185: 1125-1127.
52. Rothfield, L., Taghbalout, A., and Shih, Y.L. (2005) Spatial control of bacterial division-site placement. Nat Rev Microbiol 3: 959-968.
53. Schmidt, J.M., and Stanier, R.Y. (1966) The development of cellular stalks in bacteria. J Cell Biol 28: 423-436.
54. Schofield, W.B., Lim, H.C., and Jacobs-Wagner, C. (2010) Cell cycle coordination and regulation of bacterial chromosome segregation dynamics by polarly localized proteins. EMBO J 29: 3068-3081.
55. Schuster, C., Dobrinski, B., and Hakenbeck, R. (1990) Unusual septum formation in Streptococcus pneumoniae mutants with an alteration in the d, d-carboxypeptidase penicillin-binding protein 3. J Bacteriol 172: 6499-6505.
56. Singh, S.P., and Montgomery, B.L. (2011) Determining cell shape: adaptive regulation of cyanobacterial cellular differentiation and morphology. Trends Microbiol 19: 278-285.
57. Suit, J.C., Barbee, T., and Jetton, S. (1967) Morphological changes in Escherichia coli strain C produced by treatments affecting deoxyribonucleic acid synthesis. J Gen Microbiol 49: 165-173.
58. Sycuro, L.K., Pincus, Z., Gutierrez, K.D., Biboy, J., Stern, C.A., Vollmer, W., and Salama, N.R. (2010) Peptidoglycan crosslinking relaxation promotes Helicobacter pylori's helical shape and stomach colonization. Cell 141: 822-833.
59. Tonthat, N.K., Arold, S.T., Pickering, B.F., Van Dyke, M.W., Liang, S., Lu, Y., etal. (2011) Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 30: 154-164.
60. Uehara, T., Parzych, K.R., Dinh, T., and Bernhardt, T.G. (2010) Daughter cell separation is controlled by cytokinetic ring-activated cell wall hydrolysis. EMBO J 29: 1412-1422.
61. Varma, A., and Young, K.D. (2004) FtsZ collaborates with penicillin binding proteins to generate bacterial cell shape in Escherichia coli. J Bacteriol 186: 6768-6774.
62. Varma, A., and Young, K.D. (2009) In Escherichia coli, MreB and FtsZ direct the synthesis of lateral cell wall via independent pathways that require PBP 2. J Bacteriol 191: 3526-3533.
63. Varma, A., de Pedro, M.A., and Young, K.D. (2007) FtsZ directs a second mode of peptidoglycan synthesis in Escherichia coli. J Bacteriol 189: 5692-5704.
64. Varma, A., Huang, K.C., and Young, K.D. (2008) The Min system as a general cell geometry detection mechanism: branch lengths in Y-shaped Escherichia coli cells affect Min oscillation patterns and division dynamics. J Bacteriol 190: 2106-2117.
65. Vollmer, W., and Bertsche, U. (2008) Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochim Biophys Acta 1778: 1714-1734.
66. Ward, J.E., Jr, and Lutkenhaus, J. (1985) Overproduction of FtsZ induces minicell formation in E.coli. Cell 42: 941-949.
67. Weiss, D.S., Chen, J.C., Ghigo, J.M., Boyd, D., and Beckwith, J. (1999) Localization of FtsI (PBP3) to the septal ring requires its membrane anchor, the Z ring, FtsA, FtsQ, and FtsL. J Bacteriol 181: 508-520.
68. Wientjes, F.B., and Nanninga, N. (1989) Rate and topography of peptidoglycan synthesis during cell division in Escherichia coli: concept of a leading edge. J Bacteriol 171: 3412-3419.
69. Woldringh, C.L., Zaritsky, A., and Grover, N.B. (1994) Nucleoid partitioning and the division plane in Escherichia coli. J Bacteriol 176: 6030-6038.
70. Young, K.D. (2003) Bacterial shape. Mol Microbiol 49: 571-580.
71. Yu, X.C., and Margolin, W. (2000) Deletion of the min operon results in increased thermosensitivity of an ftsZ84 mutant and abnormal FtsZ ring assembly, placement, and disassembly. J Bacteriol 182: 6203-6213.
72. Zapun, A., Vernet, T., and Pinho, M.G. (2008) The different shapes of cocci. FEMS Microbiol Rev 32: 345-360.
73. Zaritsky, A., Wang, P., and Vischer, N.O. (2011) Instructive simulation of the bacterial cell division cycle. Microbiology 157: 1876-1885.