Determination of the structure of the MinD-ATP complex reveals the orientation of MinD on the membrane and the relative location of the binding sites for MinE and MinC

Molecular Microbiology

Volumn 79, Issue 6, 2011, Pages 1515-1528

  Wu, Wei ^a   Park, Kyung Tae ^a   Holyoak, Todd ^b   Lutkenhaus, Joe ^a  

^a Departments of Microbiology   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ESCHERICHIA COLI PROTEIN; MINC PROTEIN; MIND PROTEIN; PROTEIN MINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIUM MUTANT; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; TWO HYBRID SYSTEM;

ADENOSINE TRIPHOSPHATASES; BINDING SITES; CELL CYCLE PROTEINS; CELL MEMBRANE; DIMERIZATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; PROTEIN BINDING;

ESCHERICHIA COLI;

EID: 79952450528     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07536.x     Document Type: Article

References (60)

1. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., etal. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
2. 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.
3. Bi, E., and Lutkenhaus, J. (1993) Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring. J Bacteriol 175: 1118-1125.
4. de Boer, P.A., Crossley, R.E., and Rothfield, L.I. (1989) A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56: 641-649.
5. de Boer, P.A., Crossley, R.E., and Rothfield, L.I. (1992) Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli. J Bacteriol 174: 63-70.
6. Bragg, W.L., and Howells, E.R. (1954) X-ray diffraction by imidazole methaemoglobin. Acta Crystal 7: 409-411.
7. Chang, A.C., and Cohen, S.N. (1978) Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134: 1141-1156.
8. Cordell, S.C., and Lowe, J. (2001) Crystal structure of the bacterial cell division regulator MinD. FEBS Lett 492: 160-165.
9. Cordell, S.C., Anderson, R.E., and Lowe, J. (2001) Crystal structure of the bacterial cell division inhibitor MinC. EMBO J 20: 2454-2461.
10. 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.
11. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D60: 2126-2132.
12. Fu, X., Shih, Y.L., Zhang, Y., and Rothfield, L.I. (2001) 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 USA 98: 980-985.
13. Ghasriani, H., Ducat, T., Hart, C.T., Hafizi, F., Chang, N., Al-Baldawi, A., etal. (2010) Appropriation of the MinD protein-interaction motif by the dimeric interface of the bacterial cell division regulator MinE. Proc Natl Acad Sci USA 107: 18416-18421.
14. Hale, C.A., Meinhardt, H., and de Boer, P.A. (2001) Dynamic localization cycle of the cell division regulator MinE in Escherichia coli. EMBO J 20: 1563-1572.
15. Hare, S., Cherepanov, P., and Wang, J. (2009) Application of general formulas for the correction of a lattice-translocation defect in crystals of a lentiviral integrase in complex with LEDGF. Acta Crystallogr D Biol Crystallogr 65: 966-973.
16. Hayashi, I., Oyama, T., and Morikawa, K. (2001) Structural and functional studies of MinD ATPase: implications for the molecular recognition of the bacterial cell division apparatus. EMBO J 20: 1819-1828.
17. Hester, C.M., and Lutkenhaus, J. (2007) Soj (ParA) DNA binding is mediated by conserved arginines and is essential for plasmid segregation. Proc Natl Acad Sci USA 104: 20326-20331.
18. Holyoak, T., Fenn, T.D., Wilson, M.A., Moulin, A.G., Ringe, D., and Petsko, G.A. (2003) Malonate: a versatile cryoprotectant and stabilizing solution for salt-grown macromolecular crystals. Acta Crystallogr D Biol Crystallogr 59: 2356-2358.
19. Hsieh, C.W., Lin, T.Y., Lai, H.M., Lin, C.C., Hsieh, T.S., and Shih, Y.L. (2010) Direct MinE-membrane interaction contributes to the proper localization of MinDE in E. coli. Mol Microbiol 75: 499-512.
20. Hu, Z., and Lutkenhaus, J. (1999) Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE. Mol Microbiol 34: 82-90.
21. Hu, Z., and Lutkenhaus, J. (2000) Analysis of MinC reveals two independent domains involved in interaction with MinD and FtsZ. J Bacteriol 182: 3965-3971.
22. Hu, Z., and Lutkenhaus, J. (2001) Topological regulation of cell division in E. coli. spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipid. Mol Cell 7: 1337-1343.
23. Hu, Z., and Lutkenhaus, J. (2003) A conserved sequence at the C-terminus of MinD is required for binding to the membrane and targeting MinC to the septum. Mol Microbiol 47: 345-355.
24. Hu, Z., Gogol, E.P., and Lutkenhaus, J. (2002) Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proc Natl Acad Sci USA 99: 6761-6766.
25. Hu, Z., Saez, C., and Lutkenhaus, J. (2003) Recruitment of MinC, an inhibitor of Z-ring formation, to the membrane in Escherichia coli: role of MinD and MinE. J Bacteriol 185: 196-203.
26. Kang, G.B., Song, H.E., Kim, M.K., Youn, H.S., Lee, J.G., An, J.Y., etal. (2010) Crystal structure of Helicobacter pylori MinE, a cell division topological specificity factor. Mol Microbiol 76: 1222-1231.
27. Karimova, G., Ullmann, A., and Ladant, D. (2000) A bacterial two-hybrid system that exploits a cAMP signaling cascade in Escherichia coli. Methods Enzymol 328: 59-73.
28. Lackner, L.L., Raskin, D.M., and de Boer, P.A. (2003) ATP-dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro. J Bacteriol 185: 735-749.
29. Leonard, T.A., Butler, P.J., and Lowe, J. (2005) Bacterial chromosome segregation: structure and DNA binding of the Soj dimer - a conserved biological switch. EMBO J 24: 270-282.
30. Lutkenhaus, J. (2007) Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem 76: 539-562.
31. Lutkenhaus, J., and Sundaramoorthy, M. (2003) MinD and role of the deviant Walker A motif, dimerization and membrane binding in oscillation. Mol Microbiol 48: 295-303.
32. Ma, L.Y., King, G., and Rothfield, L. (2003) Mapping the MinE site involved in interaction with the MinD division site selection protein of Escherichia coli. J Bacteriol 185: 4948-4955.
33. Ma, L., King, G.F., and Rothfield, L. (2004) Positioning of the MinE binding site on the MinD surface suggests a plausible mechanism for activation of the Escherichia coli MinD ATPase during division site selection. Mol Microbiol 54: 99-108.
34. Mileykovskaya, E., Fishov, I., Fu, X., Corbin, B.D., Margolin, W., and Dowhan, W. (2003) Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo. J Biol Chem 278: 22193-22198.
35. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326.
36. Pichoff, S., Vollrath, B., Touriol, C., and Bouche, J.P. (1995) Deletion analysis of gene minE which encodes the topological specificity factor of cell division in Escherichia coli. Mol Microbiol 18: 321-329.
37. Pichoff, S., Alibaud, L., Guedant, A., Castanie, M.P., and Bouche, J.P. (1998) An Escherichia coli gene (yaeO) suppresses temperature-sensitive mutations in essential genes by modulating Rho-dependent transcription termination. Mol Microbiol 29: 859-869.
38. Ramirez-Arcos, S., Greco, V., Douglas, H., Tessier, D., Fan, D., Szeto, J., etal. (2004) Conserved glycines in the C terminus of MinC proteins are implicated in their functionality as cell division inhibitors. J Bacteriol 186: 2841-2855.
39. Raskin, D.M., and de Boer, P.A. (1999a) MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J Bacteriol 181: 6419-6424.
40. Raskin, D.M., and de Boer, P.A. (1999b) Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc Natl Acad Sci USA 96: 4971-4976.
41. Rothfield, L., Taghbalout, A., and Shih, Y.L. (2005) Spatial control of bacterial division-site placement. Nat Rev Microbiol 3: 959-968.
42. Sakai, N., Yao, M., Itou, H., Watanabe, N., Yumoto, F., Tanokura, M., and Tanaka, I. (2001) The three-dimensional structure of septum site-determining protein MinD from Pyrococcus horikoshii OT3 in complex with Mg-ADP. Structure 9: 817-826.
43. Schindelin, H., Kisker, C., Schlessman, J.L., Howard, J.B., and Rees, D.C. (1997) Structure of ADP×AIF4(-)-stabilized nitrogenase complex and its implications for signal transduction. Nature 387: 370-376.
44. Shen, B., and Lutkenhaus, J. (2009) The conserved C-terminal tail of FtsZ is required for the septal localization and division inhibitory activity of MinC(C)/MinD. Mol Microbiol 72: 410-424.
45. N in E. coli suggests how MinC disrupts Z rings. Mol Microbiol 75: 1285-1298.
46. Szeto, T.H., Rowland, S.L., Rothfield, L.I., and King, G.F. (2002) Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts. Proc Natl Acad Sci USA 99: 15693-15698.
47. Szeto, T.H., Rowland, S.L., Habrukowich, C.L., and King, G.F. (2003) The MinD membrane targeting sequence is a transplantable lipid-binding helix. J Biol Chem 278: 40050-40056.
48. Terwilliger, T.C. (2000) Maximum-likelihood density modification. Acta Crystallogr D Biol Crystallogr 56: 965-972.
49. Terwilliger, T.C. (2003a) Automated main-chain model building by template matching and iterative fragment extension. Acta Crystallogr D Biol Crystallogr 59: 38-44.
50. Terwilliger, T.C. (2003b) solve and resolve: automated structure solution and density modification. Methods Enzymol 374: 22-37.
51. Terwilliger, T.C., and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr 55: 849-861.
52. Tsai, Y.S., Sawaya, M.R., and Yeates, T.O. (2009) Analysis of lattice-translocation disorder in the layered hexagonal structure of carboxysome shell protein CsoS1C. Acta Crystallogr D Biol Crystallogr 65: 980-988.
53. Wang, J., Kamtekar, S., Berman, A.J., and Steitz, T.A. (2005a) Correction of X-ray intensities from single crystals containing lattice-translocation defects. Acta Crystallogr D Biol Crystallogr 61: 67-74.
54. Wang, J., Rho, S.H., Park, H.H., and Eom, S.H. (2005b) Correction of X-ray intensities from an HslV-HslU co-crystal containing lattice-translocation defects. Acta Crystallogr D Biol Crystallogr 61: 932-941.
55. Wu, L.J., and Errington, J. (2004) Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117: 915-925.
56. Zhao, C.R., de Boer, P.A., and Rothfield, L.I. (1995) Proper placement of the Escherichia coli division site requires two functions that are associated with different domains of the MinE protein. Proc Natl Acad Sci USA 92: 4313-4317.
57. Zhou, H., and Lutkenhaus, J. (2003) Membrane binding by MinD involves insertion of hydrophobic residues within the C-terminal amphipathic helix into the bilayer. J Bacteriol 185: 4326-4335.
58. Zhou, H., and Lutkenhaus, J. (2005) MinC mutants deficient in MinD- and DicB-mediated cell division inhibition due to loss of interaction with MinD, DicB, or a septal component. J Bacteriol 187: 2846-2857.
59. Zhou, H., Schulze, R., Cox, S., Saez, C., Hu, Z., and Lutkenhaus, J. (2005) Analysis of MinD mutations reveals residues required for MinE stimulation of the MinD ATPase and residues required for MinC interaction. J Bacteriol 187: 629-638.
60. Zhu, X., Xu, X., and Wilson, I.A. (2008) Structure determination of the 1918 H1N1 neuraminidase from a crystal with lattice-translocation defects. Acta Crystallogr D Biol Crystallogr 843-850.