A thermosensitive defect in the ATP binding pocket of FtsA can be suppressed by allosteric changes in the dimer interface

Molecular Microbiology

Volumn 94, Issue 3, 2014, Pages 713-727

  Herricks, Jennifer R ^a   Nguyen, Diep ^a   Margolin, William ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; DIMER; FTSA PROTEIN; FTSZ PROTEIN; OLIGOMER; UNCLASSIFIED DRUG; ZIPA PROTEIN; ESCHERICHIA COLI PROTEIN; FTSA PROTEIN, E COLI; MUTANT PROTEIN; PROTEIN BINDING;

ALLOSTERISM; ARTICLE; BACILLUS SUBTILIS; BINDING SITE; CELL DIVISION; CELL MEMBRANE; CONTROLLED STUDY; ESCHERICHIA COLI; HEAT SENSITIVITY; HYDROLYSIS; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PSEUDOMONAS AERUGINOSA; WILD TYPE; CHEMISTRY; ENZYMOLOGY; GENE REPRESSION; GENETICS; METABOLISM; MISSENSE MUTATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RADIATION RESPONSE; TEMPERATURE;

ADENOSINE TRIPHOSPHATE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROLYSIS; MUTANT PROTEINS; MUTATION, MISSENSE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SUPPRESSION, GENETIC; TEMPERATURE;

EID: 84911970999     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12790     Document Type: Article

References (47)

1. Addinall, S.G., Bi, E., and Lutkenhaus, J. (1996) FtsZ ring formation in fts mutants. J Bacteriol 178: 3877-3884.
2. Beuria, T.K., Mullapudi, S., Mileykovskaya, E., Sadasivam, M., Dowhan, W., and Margolin, W. (2009) Adenine nucleotide-dependent regulation of assembly of bacterial tubulin-like FtsZ by a hypermorph of bacterial actin-like FtsA. J Biol Chem 284: 14079-14086.
3. Bi, E.F., and Lutkenhaus, J. (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354: 161-164.
4. Bork, P., Sander, C., and Valencia, A. (1992) An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc Natl Acad Sci USA 89: 7290-7294.
5. Busiek, K.K., and Margolin, W. (2014) A role for FtsA in SPOR-independent localization of the essential Escherichia coli cell division protein FtsN. Mol Microbiol 92: 1212-1226.
6. Busiek, K.K., Eraso, J.M., Wang, Y., and Margolin, W. (2012) The early divisome protein FtsA interacts directly through its 1c subdomain with the cytoplasmic domain of the late divisome protein FtsN. J Bacteriol 194: 1989-2000.
7. Cabré, E.J., Sanchez-Gorostiaga, A., Carrara, P., Ropero, N., Casanova, M., Palacios, P., etal. (2013) Bacterial division proteins FtsZ and ZipA induce vesicle shrinkage and cell membrane invagination. J Biol Chem 288: 26625-26634.
8. Corbin, B.D., Geissler, B., Sadasivam, M., and Margolin, W. (2004) Z-ring-independent interaction between a subdomain of FtsA and late septation proteins as revealed by a polar recruitment assay. J Bacteriol 186: 7736-7744.
9. Din, N., Quardokus, E.M., Sackett, M.J., and Brun, Y.V. (1998) Dominant C-terminal deletions of FtsZ that affect its ability to localize in Caulobacter and its interaction with FtsA. Mol Microbiol 27: 1051-1063.
10. van den Ent, F., and Löwe, J. (2000) Crystal structure of the cell division protein FtsA from Thermotoga maritima. EMBO J 19: 5300-5307.
11. Feucht, A., Lucet, I., Yudkin, M.D., and Errington, J. (2001) Cytological and biochemical characterization of the FtsA cell division protein of Bacillus subtilis. Mol Microbiol 40: 115-125.
12. Gayda, R.C., Henk, M.C., and Leong, D. (1992) C-shaped cells caused by an ftsA mutation in Escherichia coli. J Bacteriol 174: 5362-5370.
13. 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.
14. 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.
15. Geissler, B., Shiomi, D., and Margolin, W. (2007) The ftsA* gain-of-function allele of Escherichia coli and its effects on the stability and dynamics of the Z ring. Microbiology 153: 814-825.
16. Hale, C.A., and de Boer, P.A. (1997) Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E.coli. Cell 88: 175-185.
17. Hale, C.A., and de Boer, P.A.J. (2002) ZipA Is required for recruitment of FtsK, FtsQ, FtsL, and FtsN to the septal ring in Escherichia coli. J Bacteriol 184: 2552-2556.
18. Hale, C.A., Rhee, A.C., and de Boer, P.A. (2000) ZipA-induced bundling of FtsZ polymers mediated by an interaction between C-terminal domains. J Bacteriol 182: 5153-5166.
19. Hernández-Rocamora, V.M., García-Montañés, C., Rivas, G., and Llorca, O. (2012) Reconstitution of the Escherichia coli cell division ZipA-FtsZ complexes in nanodiscs as revealed by electron microscopy. J Struct Biol 180: 531-538.
20. Hsin, J., Fu, R., and Huang, K.C. (2013) Dimer dynamics and filament organization of the bacterial cell division protein FtsA. J Mol Biol 425: 4415-4426.
21. Kuchibhatla, A., Bhattacharya, A., and Panda, D. (2011) ZipA binds to FtsZ with high affinity and enhances the stability of FtsZ protofilaments. PLoS ONE 6: e28262.
22. Levin, P.A. (2002) Light microscopy techniques for bacterial cell biology. In Methods in Microbiology. Sansonetti, P., and Zychlinsky, A. (eds). London: Academic Press Ltd., pp. 115-132.
23. Liu, Z., Mukherjee, A., and Lutkenhaus, J. (1999) Recruitment of ZipA to the division site by interaction with FtsZ. Mol Microbiol 31: 1853-1861.
24. Loose, M., and Mitchison, T.J. (2014) The bacterial cell division proteins FtsA and FtsZ self-organize into dynamic cytoskeletal patterns. Nat Cell Biol 16: 38-46.
25. Ma, X., and Margolin, W. (1999) Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J Bacteriol 181: 7531-7544.
26. Margolin, W. (2000) Themes and variations in prokaryotic cell division. FEMS Microbiol Rev 24: 531-548.
27. Martos, A., Monterroso, B., Zorrilla, S., Reija, B., Alfonso, C., Mingorance, J., etal. (2012) Isolation, characterization and lipid-binding properties of the recalcitrant FtsA division protein from Escherichia coli. PLoS ONE 7: e39829.
28. Miroux, B., and Walker, J.E. (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol 260: 289-298.
29. Moreira, I.S., Fernandes, P.A., and Ramos, M.J. (2006) Detailed microscopic study of the full ZipA:FtsZ interface. Proteins Struct Funct Bioinformat 63: 811-821.
30. Mosyak, L., Zhang, Y., Glasfeld, E., Haney, S., Stahl, M., Seehra, J., and Somers, W.S. (2000) The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBO J 19: 3179-3191.
31. Osawa, M., and Erickson, H.P. (2013) Liposome division by a simple bacterial division machinery. Proc Natl Acad Sci USA 110: 11000-11004.
32. Paradis-Bleau, C., Sanschagrin, F., and Levesque, R.C. (2005) Peptide inhibitors of the essential cell division protein FtsA. Protein Eng Des Sel 18: 85-91.
33. Pazos, M., Natale, P., and Vicente, M. (2013) A specific role for the ZipA protein in cell division: stabilization of the FtsZ protein. J Biol Chem 288: 3219-3226.
34. Pichoff, S., and Lutkenhaus, J. (2002) Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J 21: 685-693.
35. Pichoff, S., and Lutkenhaus, J. (2007) Identification of a region of FtsA required for interaction with FtsZ. Mol Microbiol 64: 1129-1138.
36. Pichoff, S., Shen, B., Sullivan, B., and Lutkenhaus, J. (2012) FtsA mutants impaired for self-interaction bypass ZipA suggesting a model in which FtsA's self-interaction competes with its ability to recruit downstream division proteins. Mol Microbiol 83: 151-167.
37. Potluri, L.-P., Kannan, S., and Young, K.D. (2012) ZipA Is required for FtsZ-dependent preseptal peptidoglycan synthesis prior to invagination during cell division. J Bacteriol 194: 5334-5342.
38. RayChaudhuri, D. (1999) ZipA is a MAP-Tau homolog and is essential for structural integrity of the cytokinetic FtsZ ring during bacterial cell division. EMBO J 18: 2372-2383.
39. Rico, A.I., García-Ovalle, M., Mingorance, J., and Vicente, M. (2004) Role of two essential domains of Escherichia coli FtsA in localization and progression of the division ring. Mol Microbiol 53: 1359-1371.
40. Robinson, A.C., Begg, K.J., and Donachie, W.D. (1988) Mapping and characterization of mutants of the Escherichia coli cell division gene, ftsA. Mol Microbiol 2: 581-588.
41. Robinson, A.C., Begg, K.J., and MacArthur, E. (1991) Isolation and characterization of intragenic suppressors of an Escherichia coli ftsA mutation. Res Microbiol 142: 623-631.
42. Sanchez, M., Dopazo, A., Pla, J., Robinson, A.C., and Vicente, M. (1994) Characterization of mutant alleles of the cell division protein FtsA, a regulator and structural component of the Escherichia coli septator. Biochimie 76: 1071-1074.
43. Shen, B., and Lutkenhaus, J. (2009) The conserved C-terminal tail of FtsZ is required for the septal localization and division inhibitory activity of MinCC/MinD. Mol Microbiol 72: 410-424.
44. Shiomi, D., and Margolin, W. (2007a) The C-terminal domain of MinC inhibits assembly of the Z ring in Escherichia coli. J Bacteriol 189: 236-243.
45. Shiomi, D., and Margolin, W. (2007b) Dimerization or oligomerization of the actin-like FtsA protein enhances the integrity of the cytokinetic Z ring. Mol Microbiol 66: 1396-1415.
46. Szwedziak, P., Wang, Q., Freund, S., and Löwe, J. (2012) FtsA forms actin-like protofilaments. EMBO J 31: 2249-2260.
47. 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.