The MinD Protein is a Membrane ATPase Required for the Correct Placement of the Escherichia Coli Division Site

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1991 Dec 1

PMID 1836760

Citations 127

Authors

P A de Boer

R E Crossley

A R Hand

L I Rothfield

Affiliations

Soon will be listed here.

Abstract

The proper placement of the cell division site in Escherichia coli requires the site-specific inactivation of potential division sites at the cell poles in a process that is mediated by the MinC, MinD and MinE proteins. During the normal division cycle MinD plays two roles. It activates the MinC-dependent mechanism that is responsible for the inactivation of potential division sites and it also renders the division inhibition system sensitive to the topological specificity factor MinE. MinE suppresses the division block at the normal division site at mid-cell but not all cell poles, thereby ensuring the normal division pattern. In this study the MinD protein was purified to homogeneity and shown to bind ATP and to have ATPase activity. When the putative ATP binding domain of MinD was altered by site-directed mutagenesis, the mutant protein was no longer able to activate the MinC-dependent division inhibition system. Immunoelectron microscopy showed that MinD was located in the inner membrane region of the cell envelope. These results show that MinD is a membrane ATPase and suggest that the ATPase activity plays an essential role in the functions of the MinD protein during the normal division process.

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References

Abeles A, FRIEDMAN S, Austin S . Partition of unit-copy miniplasmids to daughter cells. III. The DNA sequence and functional organization of the P1 partition region. J Mol Biol. 1985; 185(2):261-72. DOI: 10.1016/0022-2836(85)90402-4. View

Bejar S, Bouche J . A new dispensable genetic locus of the terminus region involved in control of cell division in Escherichia coli. Mol Gen Genet. 1985; 201(2):146-50. DOI: 10.1007/BF00425651. View

Seeley T, Grossman L . The role of Escherichia coli UvrB in nucleotide excision repair. J Biol Chem. 1990; 265(13):7158-65. View

de Boer P, Crossley R, Rothfield L . Central role for the Escherichia coli minC gene product in two different cell division-inhibition systems. Proc Natl Acad Sci U S A. 1990; 87(3):1129-33. PMC: 53424. DOI: 10.1073/pnas.87.3.1129. View

DONACHIE W, Begg K . Genes and the replication cycle of Escherichia coli. Res Microbiol. 1990; 141(1):64-75. DOI: 10.1016/0923-2508(90)90099-c. View

Jaffe A, Boye E, Dari R . Rule governing the division pattern in Escherichia coli minB and wild-type filaments. J Bacteriol. 1990; 172(6):3500-2. PMC: 209166. DOI: 10.1128/jb.172.6.3500-3502.1990. View

Mulder E, ElBouhali M, Pas E, Woldringh C . The Escherichia coli minB mutation resembles gyrB in defective nucleoid segregation and decreased negative supercoiling of plasmids. Mol Gen Genet. 1990; 221(1):87-93. DOI: 10.1007/BF00280372. View

Walker J, Saraste M, Runswick M, Gay N . Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982; 1(8):945-51. PMC: 553140. DOI: 10.1002/j.1460-2075.1982.tb01276.x. View

Devereux J, Haeberli P, SMITHIES O . A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984; 12(1 Pt 1):387-95. PMC: 321012. DOI: 10.1093/nar/12.1part1.387. View

10.

Casadaban M, Cohen S . Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol. 1980; 138(2):179-207. DOI: 10.1016/0022-2836(80)90283-1. View

11.

Tanaka M, Haniu M, Yasunobu K . The amino acid sequence of Clostridium pasteurianum iron protein, a component of nitrogenase. III. The NH2-terminal and COOH-terminal sequences, tryptic peptides of large cyanogen bromide peptides, and the complete sequence. J Biol Chem. 1977; 252(20):7093-100. View

12.

Bradford M . A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72:248-54. DOI: 10.1016/0003-2697(76)90527-3. View

13.

de Boer P, Cook W, Rothfield L . Bacterial cell division. Annu Rev Genet. 1990; 24:249-74. DOI: 10.1146/annurev.ge.24.120190.001341. View

14.

Labie C, BOUCHE F, Bouche J . Minicell-forming mutants of Escherichia coli: suppression of both DicB- and MinD-dependent division inhibition by inactivation of the minC gene product. J Bacteriol. 1990; 172(10):5852-5. PMC: 526903. DOI: 10.1128/jb.172.10.5852-5855.1990. View

15.

Reinstein J, Brune M, Wittinghofer A . Mutations in the nucleotide binding loop of adenylate kinase of Escherichia coli. Biochemistry. 1988; 27(13):4712-20. DOI: 10.1021/bi00413a020. View

16.

Pai E, Kabsch W, Krengel U, Holmes K, John J, Wittinghofer A . Structure of the guanine-nucleotide-binding domain of the Ha-ras oncogene product p21 in the triphosphate conformation. Nature. 1989; 341(6239):209-14. DOI: 10.1038/341209a0. View

17.

de Boer P, Crossley R, Rothfield L . Isolation and properties of minB, a complex genetic locus involved in correct placement of the division site in Escherichia coli. J Bacteriol. 1988; 170(5):2106-12. PMC: 211093. DOI: 10.1128/jb.170.5.2106-2112.1988. View

18.

Cahill K, Carmichael G . Deletion analysis of the polyomavirus late promoter: evidence for both positive and negative elements in the absence of early proteins. J Virol. 1989; 63(9):3634-42. PMC: 250953. DOI: 10.1128/JVI.63.9.3634-3642.1989. View

19.

Parsonage D, Senior A . Directed mutations of the strongly conserved lysine 155 in the catalytic nucleotide-binding domain of beta-subunit of F1-ATPase from Escherichia coli. J Biol Chem. 1988; 263(10):4740-4. View

20.

Bejar S, BOUCHE F, Bouche J . Cell division inhibition gene dicB is regulated by a locus similar to lambdoid bacteriophage immunity loci. Mol Gen Genet. 1988; 212(1):11-9. DOI: 10.1007/BF00322439. View