Membrane Localization of MinD is Mediated by a C-terminal Motif That is Conserved Across Eubacteria, Archaea, and Chloroplasts

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2002 Nov 9

PMID 12424340

Citations 114

Authors

Tim H Szeto

Susan L Rowland

Lawrence I Rothfield

Glenn F King

Affiliations

Soon will be listed here.

Abstract

MinD is a widely conserved ATPase that has been demonstrated to play a pivotal role in selection of the division site in eubacteria and chloroplasts. It is a member of the large ParA superfamily of ATPases that are characterized by a deviant Walker-type ATP-binding motif. MinD localizes to the cytoplasmic face of the inner membrane in Escherichia coli, and its association with the inner membrane is a prerequisite for membrane recruitment of the septation inhibitor MinC. However, the mechanism by which MinD associates with the membrane has proved enigmatic; it seems to lack a transmembrane domain and the amino acid sequence is devoid of hydrophobic tracts that might predispose the protein to interaction with lipids. In this study, we show that the extreme C-terminal region of MinD contains a highly conserved 8- to 12-residue sequence motif that is essential for membrane localization of the protein. We provide evidence that this motif forms an amphipathic helix that most likely mediates a direct interaction between MinD and membrane phospholipids. A model is proposed whereby the membrane-targeting motif mediates the rapid cycles of membrane attachment-release-reattachment that are presumed to occur during pole-to-pole oscillation of MinD in E. coli.

Citing Articles

MinD proteins regulate CetZ1 localization in .

Brown H, Duggin I Front Microbiol. 2024; 15:1474697.

PMID: 39651350 PMC: 11621097. DOI: 10.3389/fmicb.2024.1474697.

Positioning of cellular components by the ParA/MinD family of ATPases.

Pulianmackal L, Vecchiarelli A Curr Opin Microbiol. 2024; 79:102485.

PMID: 38723344 PMC: 11407121. DOI: 10.1016/j.mib.2024.102485.

Septum site placement in - identification and characterisation of mycobacterial homologues of MinD.

Kishore V, Gaiwala Sharma S, Raghunand T Microbiology (Reading). 2023; 169(8).

PMID: 37526955 PMC: 10482377. DOI: 10.1099/mic.0.001359.

Anchors: A way for FtsZ filaments to stay membrane bound.

Naha A, Haeusser D, Margolin W Mol Microbiol. 2023; 120(4):525-538.

PMID: 37503768 PMC: 10593102. DOI: 10.1111/mmi.15067.

Multiple ParA/MinD ATPases coordinate the positioning of disparate cargos in a bacterial cell.

Pulianmackal L, Limcaoco J, Ravi K, Yang S, Zhang J, Tran M Nat Commun. 2023; 14(1):3255.

PMID: 37277398 PMC: 10241942. DOI: 10.1038/s41467-023-39019-x.

References

Huang H, Ball J, Billheimer J, Schroeder F . The sterol carrier protein-2 amino terminus: a membrane interaction domain. Biochemistry. 1999; 38(40):13231-43. DOI: 10.1021/bi990870x. View

Kanamaru K, Fujiwara M, Kim M, Nagashima A, Nakazato E, Tanaka K . Chloroplast targeting, distribution and transcriptional fluctuation of AtMinD1, a Eubacteria-type factor critical for chloroplast division. Plant Cell Physiol. 2001; 41(10):1119-28. DOI: 10.1093/pcp/pcd037. View

Szeto J, Ramirez-Arcos S, Raymond C, Hicks L, Kay C, Dillon J . Gonococcal MinD affects cell division in Neisseria gonorrhoeae and Escherichia coli and exhibits a novel self-interaction. J Bacteriol. 2001; 183(21):6253-64. PMC: 100108. DOI: 10.1128/JB.183.21.6253-6264.2001. View

Rothfield L, Justice S, Garcia-Lara J . Bacterial cell division. Annu Rev Genet. 2000; 33:423-48. DOI: 10.1146/annurev.genet.33.1.423. View

de Boer P, Crossley R, Hand A, Rothfield L . The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. EMBO J. 1991; 10(13):4371-80. PMC: 453190. DOI: 10.1002/j.1460-2075.1991.tb05015.x. View

Marston A, Errington J . Dynamic movement of the ParA-like Soj protein of B. subtilis and its dual role in nucleoid organization and developmental regulation. Mol Cell. 2000; 4(5):673-82. DOI: 10.1016/s1097-2765(00)80378-0. View

Hayashi I, Oyama T, Morikawa K . Structural and functional studies of MinD ATPase: implications for the molecular recognition of the bacterial cell division apparatus. EMBO J. 2001; 20(8):1819-28. PMC: 125418. DOI: 10.1093/emboj/20.8.1819. View

Koonin E . A superfamily of ATPases with diverse functions containing either classical or deviant ATP-binding motif. J Mol Biol. 1993; 229(4):1165-74. DOI: 10.1006/jmbi.1993.1115. View

Yamaichi Y, Niki H . Active segregation by the Bacillus subtilis partitioning system in Escherichia coli. Proc Natl Acad Sci U S A. 2000; 97(26):14656-61. PMC: 18974. DOI: 10.1073/pnas.97.26.14656. View

10.

Dinkins R, Reddy M, Leng M, Collins G . Overexpression of the Arabidopsis thaliana MinD1 gene alters chloroplast size and number in transgenic tobacco plants. Planta. 2002; 214(2):180-8. DOI: 10.1007/s004250100605. View

11.

Bechinger B . Understanding peptide interactions with the lipid bilayer: a guide to membrane protein engineering. Curr Opin Chem Biol. 2000; 4(6):639-44. DOI: 10.1016/s1367-5931(00)00143-5. View

12.

Johnson J, Cornell R . Amphitropic proteins: regulation by reversible membrane interactions (review). Mol Membr Biol. 1999; 16(3):217-35. DOI: 10.1080/096876899294544. View

13.

Rowland S, Fu X, Sayed M, Zhang Y, Cook W, Rothfield L . Membrane redistribution of the Escherichia coli MinD protein induced by MinE. J Bacteriol. 2000; 182(3):613-9. PMC: 94322. DOI: 10.1128/JB.182.3.613-619.2000. View

14.

Wang G, Peterkofsky A, Clore G . A novel membrane anchor function for the N-terminal amphipathic sequence of the signal-transducing protein IIAGlucose of the Escherichia coli phosphotransferase system. J Biol Chem. 2000; 275(51):39811-4. DOI: 10.1074/jbc.C000709200. View

15.

Marston A, Thomaides H, Edwards D, Sharpe M, Errington J . Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes Dev. 1998; 12(21):3419-30. PMC: 317235. DOI: 10.1101/gad.12.21.3419. View

16.

Bernstein L, Grillo A, Loranger S, Linder M . RGS4 binds to membranes through an amphipathic alpha -helix. J Biol Chem. 2000; 275(24):18520-6. DOI: 10.1074/jbc.M000618200. View

17.

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

18.

Rothfield L, Justice S . Bacterial cell division: the cycle of the ring. Cell. 1997; 88(5):581-4. DOI: 10.1016/s0092-8674(00)81899-1. View

19.

Quisel J, Lin D, Grossman A . Control of development by altered localization of a transcription factor in B. subtilis. Mol Cell. 2000; 4(5):665-72. DOI: 10.1016/s1097-2765(00)80377-9. View

20.

Fu X, Shih Y, Zhang Y, Rothfield L . The MinE ring required for proper placement of the division site is a mobile structure that changes its cellular location during the Escherichia coli division cycle. Proc Natl Acad Sci U S A. 2001; 98(3):980-5. PMC: 14695. DOI: 10.1073/pnas.98.3.980. View