1887

Abstract

The ability of each of the 11 division proteins to interact with itself and with each of the remaining proteins was studied in 66 combinations of protein pairs, using a bacterial two-hybrid system. Interactions (homo- or hetero-dimerizations) were detected between 37 protein pairs, whereas 29 protein pairs did not interact. In some cases, positive interactions of the proteins were confirmed by co-immunoprecipitation experiments in . Comparison between the division protein interaction web and that of , the only micro-organisms for which the whole division interactome has been described systematically, was also performed. At least nine division proteins, ZapA, FtsZ, FtsA, FtsK, FtsQ/DivIB, FtsB/DivIC, FtsL, FtsI and FtsW, are believed to have a conserved function between these bacteria and thus we may say that a significant part of the interactions are conserved. Out of 45 protein pairs tested in both bacteria, 30 showed the same behaviour: 23 interacted while seven did not. In agreement with these results, cross-interactions between proteins and the corresponding orthologues were observed. Taken together, these results suggest a phylogenetically conserved minimal common interactome of the division proteins.

Keyword(s): THA, two-hybrid assay
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2008-10-01
2019-11-12
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References

  1. Ayala, J. A., Garrido, T., Pedro, M. A. & Vicente, M. ( 1994; ). Molecular biology of bacterial septation. In Bacterial Cell Wall, pp. 73–101. Edited by J. M. Ghuysen & R. Hackenbeck. Amsterdam: Elsevier Science BV.
  2. Buddelmeijer, N. M. & Beckwith, J. ( 2004; ). A complex of the Escherichia coli cell division proteins FtsL, FtsB and FtsQ forms independently of its localization to the septal region. Mol Microbiol 52, 1315–1327.[CrossRef]
    [Google Scholar]
  3. Datta, P., Dasgupta, A., Bhakta, S. & Basu, J. ( 2002; ). Interaction between FtsZ and FtsW of Mycobacterium tuberculosis. J Biol Chem 277, 24983–24987.[CrossRef]
    [Google Scholar]
  4. Datta, P., Dasgupta, A., Singh, A. K., Mukheriee, P., Kundu, M. & Basu, J. ( 2006; ). Interaction between FtsW and penicillin-binding protein 3 (PBP3) directs PBP3 to mid-cell, controls cell septation and mediates the formation of a trimeric complex involving FtsZ, FtsW and PBP3 in mycobacteria. Mol Microbiol 62, 1655–1673.[CrossRef]
    [Google Scholar]
  5. Di Lallo, G., Castagnoli, L., Ghelardini, P. & Paolozzi, L. ( 2001; ). A two-hybrid system based on chimeric operator recognition for studying protein homo/heterodimerization in Escherichia coli. Microbiology 147, 1651–1656.
    [Google Scholar]
  6. Di Lallo, G.,, Fagioli, M., Barionovi, D., Ghelardini, P. & Paolozzi, L. ( 2003; ). Use of a two-hybrid assay to study the assembly of a complex multicomponent protein machinery: bacterial septosome differentiation. Microbiology 149, 3353–3359.[CrossRef]
    [Google Scholar]
  7. D'Ulisse, V., Fagioli, M., Ghelardini, P. & Paolozzi, L. ( 2007; ). Three functional subdomains of the Escherichia coli FtsQ protein are involved in its interaction with the other division proteins. Microbiology 153, 124–138.[CrossRef]
    [Google Scholar]
  8. Duong, F. & Wickner, W. ( 1997; ). Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme. EMBO J 16, 2756–2768.[CrossRef]
    [Google Scholar]
  9. Dziadek, J., Rutherford, S. A., Madiraju, M. V., Atkinson, M. A. & Rajagopalan, M. ( 2003; ). Conditional expression of Mycobacterium smegmatis ftsZ, an essential cell division gene. Microbiology 149, 1593–1603.[CrossRef]
    [Google Scholar]
  10. Erickson, H. P. ( 2007; ). Evolution of the cytoskeleton. Bioessays 29, 668–677.[CrossRef]
    [Google Scholar]
  11. Errington, J., Daniel, R. A. & Scheffers, D. J. ( 2003; ). Cytokinesis in bacteria. Microbiol Mol Biol Rev 67, 52–65.[CrossRef]
    [Google Scholar]
  12. Fadda, D., Santona, A., D'Ulisse, V., Ghelardini, P., Ennas, M. G., Whalen, M. B. & Massidda, O. ( 2007; ). Streptococcus pneumoniae DivIVA: localization and interactions in a MinCD-free context. J Bacteriol 189, 1288–1298.[CrossRef]
    [Google Scholar]
  13. Gaikwad, A., Babbarwal, V., Pant, V. & Mukherjee, S. K. ( 2000; ). Pea chloroplast FtsZ can form multimers and correct the thermosensitive defect of an Escherichia coli ftsZ mutant. Mol Gen Genet 263, 213–221.[CrossRef]
    [Google Scholar]
  14. Goehring, N. W. & Beckwith, J. ( 2005; ). Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol 15, R514–R526.[CrossRef]
    [Google Scholar]
  15. Goehring, N. W., Gonzalez, M. D. & Beckwith, J. ( 2006; ). Premature targeting of cell division proteins to midcell reveals hierarchies of protein interactions involved in divisome assembly. Mol Microbiol 61, 33–45.[CrossRef]
    [Google Scholar]
  16. Haeusser, D. P., Schwartz, R. L., Smith, A. M., Oates, M. E. & Levin, P. A. ( 2004; ). EzrA prevents aberrant cell division by modulating assembly of the cytoskeletal protein FtsZ. Mol Microbiol 52, 801–814.[CrossRef]
    [Google Scholar]
  17. Haney, S. A., Glasfeld, E., Hale, C., Keeney, D., He, Z. & de Boer, P. ( 2001; ). Genetic analysis of the Escherichia coli FtsZ–ZipA interaction in the yeast two-hybrid system. Characterization of FtsZ residues essential for the interactions with ZipA and with FtsA. J Biol Chem 276, 11980–11987.[CrossRef]
    [Google Scholar]
  18. Harry, E., Monahan, L. & Thompson, L. ( 2006; ). Bacterial cell division: the mechanism and its precision. Int Rev Cytol 253, 27–94.
    [Google Scholar]
  19. Karimova, G., Dautin, N. & Ladant, D. ( 2005; ). Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J Bacteriol 187, 2233–2243.[CrossRef]
    [Google Scholar]
  20. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef]
    [Google Scholar]
  21. Lara, B., Rico, A. I., Petruzzelli, S., Santona, A., Dumas, J., Biton, J., Vicente, M., Mingorance, J. & Massidda, O. ( 2005; ). Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein. Mol Microbiol 55, 699–711.
    [Google Scholar]
  22. Ma, X. & Margolin, W. ( 1999; ). Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J Bacteriol 181, 7531–7544.
    [Google Scholar]
  23. Ma, X., Sun, Q., Wang, R., Singh, G., Jonietz, E. L. & Margolin, W. ( 1997; ). Interactions between heterologous FtsA and FtsZ proteins at the FtsZ ring. J Bacteriol 179, 6788–6797.
    [Google Scholar]
  24. Margolin, W. ( 2000; ). Themes and variations in prokaryotic cell division. FEMS Microbiol Rev 24, 531–548.[CrossRef]
    [Google Scholar]
  25. Margolin, W. ( 2003; ). Bacterial division: the fellowship of the ring. Curr Biol 13, R16–R18.[CrossRef]
    [Google Scholar]
  26. Massidda, O., Anderluzzi, D., Friedli, L. & Feger, G. ( 1998; ). Unconventional organization of the division and cell wall gene cluster of Streptococcus pneumoniae. Microbiology 144, 3069–3078.[CrossRef]
    [Google Scholar]
  27. Miller, J. H. ( 1972; ). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  28. Momynaliev, K. T., Smirnova, O. V., Lazyrev, V. N., Akopian, T. A., Chelysheva, V. V., Ayala, J. A., Simankova, A. N., Borchsenius, S. N. & Govorun, V. M. ( 2002; ). Characterization of the Mycoplasma hominis ftsZ gene and its sequence variability in mycoplasma clinical isolates. Biochem Biophys Res Commun 293, 155–162.[CrossRef]
    [Google Scholar]
  29. Morlot, C., Zapun, A., Dideberg, O. & Vernet, T. ( 2003; ). Growth and division of Streptococcus pneumoniae: localization of the high molecular weight penicillin-binding proteins during the cell cycle. Mol Microbiol 50, 845–855.[CrossRef]
    [Google Scholar]
  30. Morlot, C., Noirclerc-Savoye, M., Zapun, A., Dideberg, O. & Vernet, T. ( 2004; ). The d,d-carboxypeptidase PBP3 organizes the division process of Streptococcus pneumoniae. Mol Microbiol 51, 1641–1648.[CrossRef]
    [Google Scholar]
  31. Noirclerc-Savoye, M., Le Gouellec, A., Morlot, C., Dideberg, O., Vernet, T. & Zapun, A. ( 2005; ). In vitro reconstitution of a trimeric complex of DivIB, DivIC and FtsL, and their transient co-localization at the division site in Streptococcus pneumoniae. Mol Microbiol 55, 413–424.
    [Google Scholar]
  32. Osawa, M. & Erickson, H. P. ( 2006; ). FtsZ from divergent foreign bacteria can function for cell division in Escherichia coli. J Bacteriol 188, 7132–7140.[CrossRef]
    [Google Scholar]
  33. Pinho, M. G. & Errington, J. ( 2005; ). Recruitment of penicillin-binding protein PBP2 to the division site of Staphylococcus aureus is dependent on its transpeptidation substrates. Mol Microbiol 55, 799–807.
    [Google Scholar]
  34. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  35. Tamames, J., González-Moreno, M., Mingorance, J., Valencia, A. & Vicente, M. ( 2001; ). Bringing gene order into bacterial shape. Trends Genet 17, 124–126.[CrossRef]
    [Google Scholar]
  36. Tormo, A., Ayala, J. A., de Pedro, M. A., Aldea, M. & Vicente, M. ( 1986; ). Interaction of FtsA and PBP3 proteins in the Escherichia coli septum. J Bacteriol 166, 985–992.
    [Google Scholar]
  37. Towbin, H., Staehelin, T. & Gordon, J. ( 1979; ). Electrophoretic transfer of proteins from acrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76, 4350–4354.[CrossRef]
    [Google Scholar]
  38. Vicente, M. & Errington, J. ( 1996; ). Structure, function and controls in microbial division. Mol Microbiol 20, 1–7.[CrossRef]
    [Google Scholar]
  39. Vicente, M. & Rico, A. I. ( 2006; ). The order of the ring: assembly of Escherichia coli cell division components. Mol Microbiol 61, 5–8.[CrossRef]
    [Google Scholar]
  40. Vicente, M., Rico, A. I., Martínez-Arteaga, R. & Mingorance, J. ( 2006; ). Septum enlightenment: assembly of bacterial division proteins. J Bacteriol 188, 19–27.[CrossRef]
    [Google Scholar]
  41. Walhout, A. J., Sordella, R., Lu, X., Hartley, J. L., Temple, G. F., Brasch, M. A., Thierry-Mieg, N. & Vidal, M. ( 2000; ). Protein interaction mapping in C. elegans using proteins involved in vulval development. Science 287, 116–122.[CrossRef]
    [Google Scholar]
  42. Wang, X., Huang, J., Mukherjee, A., Cao, C. & Lutkenhaus, J. ( 1997; ). Analysis of the interaction of FtsZ with itself, GTP, and FtsA. J Bacteriol 179, 5551–5559.
    [Google Scholar]
  43. Weiss, D. S. ( 2004; ). Bacterial cell division and the septal ring. Mol Microbiol 54, 588–597.[CrossRef]
    [Google Scholar]
  44. Wojcik, J. & Schachter, V. ( 2001; ). Protein–protein interaction map inference using interacting domain profile pairs. Bioinformatics 17 (Suppl. 1), S296–S305.[CrossRef]
    [Google Scholar]
  45. Yura, T., Mori, H., Nagai, H., Nagata, T., Ishihama, A., Fujita, N., Isono, K., Mizobuchi, K. & Nakata, A. ( 1992; ). Systematic sequencing of the Escherichia coli genome: analysis of the 0–2.4 min region. Nucleic Acids Res 20, 3305–3308.[CrossRef]
    [Google Scholar]
  46. Zapun, A., Vernet, T. & Pinho, M. G. ( 2008; ). The different shapes of cocci. FEMS Microbiol Rev 32, 345–360.[CrossRef]
    [Google Scholar]
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