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
2020-07-13
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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 pp73–101 Edited by Ghuysen J. M., Hackenbeck R. Amsterdam: Elsevier Science BV;
    [Google Scholar]
  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 Microbiol52:1315–1327
    [Google Scholar]
  3. Datta P., Dasgupta A., Bhakta S., Basu J.. 2002; Interaction between FtsZ and FtsW of Mycobacterium tuberculosis. J Biol Chem277:24983–24987
    [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 Microbiol62:1655–1673
    [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. Microbiology147:1651–1656
    [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. Microbiology149:3353–3359
    [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. Microbiology153:124–138
    [Google Scholar]
  8. Duong F., Wickner W.. 1997; Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme. EMBO J16:2756–2768
    [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. Microbiology149:1593–1603
    [Google Scholar]
  10. Erickson H. P.. 2007; Evolution of the cytoskeleton. Bioessays29:668–677
    [Google Scholar]
  11. Errington J., Daniel R. A., Scheffers D. J.. 2003; Cytokinesis in bacteria. Microbiol Mol Biol Rev67:52–65
    [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 Bacteriol189:1288–1298
    [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 Genet263:213–221
    [Google Scholar]
  14. Goehring N. W., Beckwith J.. 2005; Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol15:R514–R526
    [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 Microbiol61:33–45
    [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 Microbiol52:801–814
    [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 Chem276:11980–11987
    [Google Scholar]
  18. Harry E., Monahan L., Thompson L.. 2006; Bacterial cell division: the mechanism and its precision. Int Rev Cytol253:27–94
    [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 Bacteriol187:2233–2243
    [Google Scholar]
  20. Laemmli U. K.. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685
    [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 Microbiol55:699–711
    [Google Scholar]
  22. Ma X., Margolin W.. 1999; Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J Bacteriol181:7531–7544
    [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 Bacteriol179:6788–6797
    [Google Scholar]
  24. Margolin W.. 2000; Themes and variations in prokaryotic cell division. FEMS Microbiol Rev24:531–548
    [Google Scholar]
  25. Margolin W.. 2003; Bacterial division: the fellowship of the ring. Curr Biol13:R16–R18
    [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. Microbiology144:3069–3078
    [Google Scholar]
  27. Miller J. H.. 1972; Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  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 Commun293:155–162
    [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 Microbiol50:845–855
    [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 Microbiol51:1641–1648
    [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 Microbiol55:413–424
    [Google Scholar]
  32. Osawa M., Erickson H. P.. 2006; FtsZ from divergent foreign bacteria can function for cell division in Escherichia coli. J Bacteriol188:7132–7140
    [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 Microbiol55:799–807
    [Google Scholar]
  34. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  35. Tamames J., González-Moreno M., Mingorance J., Valencia A., Vicente M.. 2001; Bringing gene order into bacterial shape. Trends Genet17:124–126
    [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 Bacteriol166:985–992
    [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 A76:4350–4354
    [Google Scholar]
  38. Vicente M., Errington J.. 1996; Structure, function and controls in microbial division. Mol Microbiol20:1–7
    [Google Scholar]
  39. Vicente M., Rico A. I.. 2006; The order of the ring: assembly of Escherichia coli cell division components. Mol Microbiol61:5–8
    [Google Scholar]
  40. Vicente M., Rico A. I., Martínez-Arteaga R., Mingorance J.. 2006; Septum enlightenment: assembly of bacterial division proteins. J Bacteriol188:19–27
    [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. Science287:116–122
    [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 Bacteriol179:5551–5559
    [Google Scholar]
  43. Weiss D. S.. 2004; Bacterial cell division and the septal ring. Mol Microbiol54:588–597
    [Google Scholar]
  44. Wojcik J., Schachter V.. 2001; Protein–protein interaction map inference using interacting domain profile pairs. Bioinformatics17 :Suppl. 1S296–S305
    [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 Res20:3305–3308
    [Google Scholar]
  46. Zapun A., Vernet T., Pinho M. G.. 2008; The different shapes of cocci. FEMS Microbiol Rev32:345–360
    [Google Scholar]
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