Nuclear magnetic resonance solution structure of the peptidoglycan-binding SPOR domain from Escherichia coli DamX: Insights into septal localization

Biochemistry

Volumn 52, Issue 4, 2013, Pages 627-639

  Williams, Kyle B ^a   Yahashiri, Atsushi ^a   Arends, S J Ryan ^a,c   Popham, David L ^b   Fowler, C Andrew ^a   Weiss, David S ^a  

^a UNIVERSITY OF IOWA   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c VERTEX PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BILE SALTS; BINDING ASSAYS; CELL DIVISIONS; DELETION MUTANTS; DEOXYCHOLATE; E. COLI; PEPTIDOGLYCANS; POINT MUTATIONS; SITE DIRECTED MUTAGENESIS; SOLUTION STRUCTURES;

CELL PROLIFERATION; ESCHERICHIA COLI; PROTEINS;

NUCLEAR MAGNETIC RESONANCE;

DAMX PROTEIN; DEOXYCHOLIC ACID; ESCHERICHIA COLI PROTEIN; PEPTIDOGLYCAN; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BACTERIAL CELL; BETA SHEET; CELL DIVISION; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; HETERONUCLEAR SINGLE QUANTUM COHERENCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CELL DIVISION; CONSERVED SEQUENCE; DEOXYCHOLIC ACID; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDOGLYCAN; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SURFACE PROPERTIES;

EID: 84873876952     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301609e     Document Type: Article

References (54)

1. de Boer, P. A. (2010) Advances in understanding E. coli cell fission Curr. Opin. Microbiol. 13, 730-737
2. Lutkenhaus, J., Pichoff, S., and Du, S. (2012) Bacterial cytokinesis: From Z ring to divisome Cytoskeleton 69, 778-790
3. Typas, A., Banzhaf, M., Gross, C. A., and Vollmer, W. (2012) From the regulation of peptidoglycan synthesis to bacterial growth and morphology Nat. Rev. Microbiol. 10, 123-136
4. Arends, S. J., Williams, K., Scott, R. J., Rolong, S., Popham, D. L., and Weiss, D. S. (2010) Discovery and characterization of three new Escherichia coli septal ring proteins that contain a SPOR domain: DamX, DedD, and RlpA J. Bacteriol. 192, 242-255
5. Gerding, M. A., Liu, B., Bendezu, F. O., Hale, C. A., Bernhardt, T. G., and de Boer, P. A. (2009) Self-enhanced accumulation of FtsN at division sites and roles for other proteins with a SPOR domain (DamX, DedD, and RlpA) in Escherichia coli cell constriction J. Bacteriol. 191, 7383-7401
6. Moll, A. and Thanbichler, M. (2009) FtsN-like proteins are conserved components of the cell division machinery in proteobacteria Mol. Microbiol. 72, 1037-1053
7. Finn, R. D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J. E., Gavin, O. L., Gunasekaran, P., Ceric, G., Forslund, K., Holm, L., Sonnhammer, E. L., Eddy, S. R., and Bateman, A. (2010) The Pfam protein families database Nucleic Acids Res. 38, D211-D222
8. Smith, T. J. and Foster, S. J. (1995) Characterization of the involvement of two compensatory autolysins in mother cell lysis during sporulation of Bacillus subtilis 168 J. Bacteriol. 177, 3855-3862
9. Ursinus, A., van den Ent, F., Brechtel, S., de Pedro, M., Holtje, J. V., Lowe, J., and Vollmer, W. (2004) Murein (peptidoglycan) binding property of the essential cell division protein FtsN from Escherichia coli J. Bacteriol. 186, 6728-6737
10. Lupoli, T. J., Taniguchi, T., Wang, T. S., Perlstein, D. L., Walker, S., and Kahne, D. E. (2009) Studying a cell division amidase using defined peptidoglycan substrates J. Am. Chem. Soc. 131, 18230-18231
11. de Pedro, M. A., Quintela, J. C., Holtje, J. V., and Schwarz, H. (1997) Murein segregation in Escherichia coli J. Bacteriol. 179, 2823-2834
12. Ishidate, K., Ursinus, A., Holtje, J. V., and Rothfield, L. (1998) Analysis of the length distribution of murein glycan strands in ftsZ and ftsI mutants of E. coli FEMS Microbiol. Lett. 168, 71-75
13. Obermann, W. and Holtje, J. V. (1994) Alterations of murein structure and of penicillin-binding proteins in minicells from Escherichia coli Microbiology 140 (Part 1) 79-87
14. Romeis, T., Kohlrausch, U., Burgdorf, K., and Holtje, J. V. (1991) Murein chemistry of cell division in Escherichia coli Res. Microbiol. 142, 325-332
15. Mishima, M., Shida, T., Yabuki, K., Kato, K., Sekiguchi, J., and Kojima, C. (2005) Solution structure of the peptidoglycan binding domain of Bacillus subtilis cell wall lytic enzyme CwlC: Characterization of the sporulation-related repeats by NMR Biochemistry 44, 10153-10163
16. Yang, J. C., Van Den Ent, F., Neuhaus, D., Brevier, J., and Lowe, J. (2004) Solution structure and domain architecture of the divisome protein FtsN Mol. Microbiol. 52, 651-660
17. Allain, F. H., Howe, P. W., Neuhaus, D., and Varani, G. (1997) Structural basis of the RNA-binding specificity of human U1A protein EMBO J. 16, 5764-5772
18. Birney, E., Kumar, S., and Krainer, A. R. (1993) Analysis of the RNA-recognition motif and RS and RGG domains: Conservation in metazoan pre-mRNA splicing factors Nucleic Acids Res. 21, 5803-5816
19. Nagai, K., Oubridge, C., Jessen, T. H., Li, J., and Evans, P. R. (1990) Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A Nature 348, 515-520
20. 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
21. Fribourg, S., Gatfield, D., Izaurralde, E., and Conti, E. (2003) A novel mode of RBD-protein recognition in the Y14-Mago complex Nat. Struct. Biol. 10, 433-439
22. Kadlec, J., Izaurralde, E., and Cusack, S. (2004) The structural basis for the interaction between nonsense-mediated mRNA decay factors UPF2 and UPF3 Nat. Struct. Mol. Biol. 11, 330-337
23. Varani, G. and Nagai, K. (1998) RNA recognition by RNP proteins during RNA processing Annu. Rev. Biophys. Biomol. Struct. 27, 407-445
24. Lyngstadaas, A., Lobner-Olesen, A., and Boye, E. (1995) Characterization of three genes in the dam -containing operon of Escherichia coli Mol. Gen. Genet. 247, 546-554
25. Lopez-Garrido, J., Cheng, N., Garcia-Quintanilla, F., Garcia-del Portillo, F., and Casadesus, J. (2010) Identification of the Salmonella enterica damX gene product, an inner membrane protein involved in bile resistance J. Bacteriol. 192, 893-895
26. Leclerc, G. J., Tartera, C., and Metcalf, E. S. (1998) Environmental regulation of Salmonella typhi invasion-defective mutants Infect. Immun. 66, 682-691
27. Ruiz, C. and Levy, S. B. (2010) Many chromosomal genes modulate MarA-mediated multidrug resistance in Escherichia coli Antimicrob. Agents Chemother. 54, 2125-2134
28. Tarry, M., Arends, S. J., Roversi, P., Piette, E., Sargent, F., Berks, B. C., Weiss, D. S., and Lea, S. M. (2009) The Escherichia coli cell division protein and model Tat substrate SufI (FtsP) localizes to the septal ring and has a multicopper oxidase-like structure J. Mol. Biol. 386, 504-519
29. Haldimann, A. and Wanner, B. L. (2001) Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria J. Bacteriol. 183, 6384-6393
30. Ottiger, M., Delaglio, F., and Bax, A. (1998) Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra J. Magn. Reson. 131, 373-378
31. Ruckert, M. and Otting, G. (2000) Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments J. Am. Chem. Soc. 122, 7793-7797
32. 15N NMR relaxation Biochemistry 33, 5984-6003
33. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293
34. 13C heteronuclear NMR spectroscopy J. Am. Chem. Soc. 113, 4371-4380
35. Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, P., Ulrich, E. L., Markley, J. L., Ionides, J., and Laue, E. D. (2005) The CCPN data model for NMR spectroscopy: Development of a software pipeline Proteins 59, 687-696
36. Lipari, G. and Szabo, A. (1982) Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. 1. Theory and range of validity J. Am. Chem. Soc. 104, 4546-4559
37. Lipari, G. and Szabo, A. (1982) Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. 2. Analysis of experimental results J. Am. Chem. Soc. 104, 4559-4570
38. Loria, J. P. and Cole, R. (2003) FAST-Modelfree: A program for rapid automated analysis of solution NMR spin-relaxation data J. Biomol. NMR 26, 203-213
39. Mandel, A. M., Akke, M., and Palmer, A. G., III (1995) Backbone dynamics of Escherichia coli ribonuclease HI: Correlations with structure and function in an active enzyme J. Mol. Biol. 246, 144-163
40. Schwieters, C. D., Kuszewski, J. J., and Clore, G. M. (2006) Using Xplor-NIH for NMR molecular structure determination Prog. Nucl. Magn. Reson. Spectrosc. 48, 47-62
41. Schwieters, C. D., Kuszewski, J. J., Tjandra, N., and Clore, G. M. (2003) The Xplor-NIH NMR molecular structure determination package J. Magn. Reson. 160, 65-73
42. DeLano, W. L. (2008) The PyMOL Molecular Graphics System, version 1.1, DeLano Scientific, San Carlos, CA.
43. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera: A visualization system for exploratory research and analysis J. Comput. Chem. 25, 1605-1612
44. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS plus: A hybrid method for predicting protein backbone torsion angles from NMR chemical shifts J. Biomol. NMR 44, 213-223
45. Sass, H. J., Musco, G., Stahl, S. J., Wingfield, P. T., and Grzesiek, S. (2001) An easy way to include weak alignment constraints into NMR structure calculations J. Biomol. NMR 21, 275-280
46. Laskowski, R. A., Rullmann, J. A. C., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8, 477-486
47. Ashkenazy, H., Erez, E., Martz, E., Pupko, T., and Ben-Tal, N. (2010) ConSurf 2010: Calculating evolutionary conservation in sequence and structure of proteins and nucleic acids Nucleic Acids Res. 38, W529-W533
48. Schleifer, K. H. and Kandler, O. (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications Bacteriol. Rev. 36, 407-477
49. Glauner, B., Holtje, J. V., and Schwarz, U. (1988) The composition of the murein of Escherichia coli J. Biol. Chem. 263, 10088-10095
50. Atrih, A., Bacher, G., Allmaier, G., Williamson, M. P., and Foster, S. J. (1999) Analysis of peptidoglycan structure from vegetative cells of Bacillus subtilis 168 and role of PBP 5 in peptidoglycan maturation J. Bacteriol. 181, 3956-3966
51. Dai, K., Xu, Y., and Lutkenhaus, J. (1993) Cloning and characterization of ftsN, an essential cell division gene in Escherichia coli isolated as a multicopy suppressor of ftsA12 (Ts) J. Bacteriol. 175, 3790-3797
52. Oubridge, C., Ito, N., Evans, P. R., Teo, C. H., and Nagai, K. (1994) Crystal structure at 1.92 Å resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin Nature 372, 432-438
53. Varani, L., Gunderson, S. I., Mattaj, I. W., Kay, L. E., Neuhaus, D., and Varani, G. (2000) The NMR structure of the 38 kDa U1A protein-PIE RNA complex reveals the basis of cooperativity in regulation of polyadenylation by human U1A protein Nat. Struct. Biol. 7, 329-335
54. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0 Bioinformatics 23, 2947-2948