Skip to main content
SpringerLink
Log in

Filamentous growth of Escherichia coli K12 elicited by dimeric, mixed-valence complexes of ruthenium

  • Original Papers
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Dimeric, mixed-valence [(Ru(II), Ru(III)] compounds of ruthenium caused filament formation in growing cultures of Escherichia coli K12. Three compounds with the general formula Ru2(NH3)6X5 · H2O (where X is a halide) were tested; in order of decreasing effectiveness (and with the concentration giving maximum effect), these were the bromo (10-5 M), chloro (10-4 to 10-5 M), and iodo (10-3 to 10-4 M) analogues. Filamentation elicited by the bromo and chloro compounds was spontaneously reversible after 3–4 h, and tentatively attributed to oxidation of the active mixed-valence form to inactive Ru(III) complexes. Several compounds known to accelerate division of filaments formed under other conditions were ineffective in reversing the filamentation, but the presence of 0,43 M-dimethylsulphoxide totally inhibited filamentation caused by the bromo or chloro compounds and by cis-Pt(NH3)2Cl2 (cisplatin), an established filamenting and antitumour agent. The ruthenium complexes bound to mammalian DNA, but were without effect on the UV spectrum or cellular content of DNA in E. coli, despite showing marked mutagenic activity in reverse mutation tests with Salmonella typhimurium. Cells remained sensitive to inhibition of division by the ruthenium complexes until immediately prior to the division event. Possibilities for the (probably complex) mode of action and the potential of related compounds for therapeutic use are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

DMSO:

dimethylsulphoxide

References

  • Adler HI, Fisher WD, Hardigree AA, Stapleton GE (1966) Repair of radiation-induced damage to the cell division mechanism of Escherichia coli. J Bacteriol 91:737–742

    Google Scholar 

  • Ames BN, McCann J, Yamasaki E (1975) Methods for detecting carcinogens and mutagens with the Salmonella mammalianmicrosome mutagenicity test. Mut Res 31:347–364

    Google Scholar 

  • Anghileri LJ (1975) The in vivo inhibition of tumour growth by ruthenium red: its relationship with the metabolism of calcium in the tumor. Z Krebsforsch 83:213–217

    Google Scholar 

  • Blumenthal LK, Zahler SA (1962) Index for measurment of synchronisation of cell populations. Science 135:724

    Google Scholar 

  • Bottomley F, Tong SB (1971) On the blue complexes formed in acidic solutions of hexaammineruthenium(II). Can J Chem 49:3739–3743

    Google Scholar 

  • Burton K (1968) Determination of DNA concentration with diphenylamine. In: Grossman L, Moldare K (eds) Methods in enzymology, vol 12 B. Academic Press, New York London, pp 163–166

    Google Scholar 

  • Churchward G, Bremer H (1977) Determination of deoxyribonucleic acid replication time in exponentially growing Escherichia coli B/r. J Bacteriol 130:1206–1213

    Google Scholar 

  • Clarke MJ (1980) Oncological implications of the chemistry of ruthenium. In: Siegel H (ed) Metal ions in biological systems, vol 11. Marcel Dekker Inc, New York Basel, pp 231–283

    Google Scholar 

  • Cleare MJ (1974) Transition metal complexes in cancer chemotherapy. Coord Chem Rev 12:349–405

    Google Scholar 

  • Darby V, Holland IB (1979) Kinetic analysis of cell division and induction and stability of recA-protein in UV irradiated lon + and lon - strains of Escherichia coli K12. Mol Gen Genet 176:121–128

    Google Scholar 

  • Durig JR, Danneman J, Behnke WD, Mercer EE (1976) The induction of filamentous growth in Escherichia coli by ruthenium and palladium complexes. Chem Biol Interact 13:287–294

    Google Scholar 

  • Edwards C (1980) Sensitivity of synchronous cultures of Bacillus subtilis to lysozyme. J Gen Microbiol 119:277–279

    Google Scholar 

  • Ferguson CA, Murray RGE, Lancy P (1979) Effects of some platinum IV complexes on cell division of Escherichia coli. Can J Microbiol 25:545–559

    Google Scholar 

  • George J, Castellazzi M, Buttin G (1975) Prophage induction and cell division of E. coli. III. Mutations of sfiA and sfiB restore cell division in tif and lon strains and permit the expression of mutator properties in tif. Mol Gen Genet 140:309–332

    Google Scholar 

  • Gibson JF (1981) Interactions of ruthenium compounds with micro-organisms. PhD Thesis, University of London

  • Gibson JF, Poole RK, Hughes MN, Rees JF (1982) A dimeric complex of ruthenium: a new inhibitor of respiration-driven calcium transport in Escherichia coli K12. J Gen Microbiol 128:2211–2214

    Google Scholar 

  • Giraldi T, Sava G, Bertoli G, Mestroni G, Zassinovich G (1977) Antitumour action of two rhodium and ruthenium complexes in comparison with cis-diamminedichloroplatinum(II). Cancer Res 37:2662–2666

    Google Scholar 

  • Grula EA (1960) Cell division in a species of Erwinia. I. Initial observations relating to nutritional dependency. J Bacteriol 80:369–374

    Google Scholar 

  • Grula EA, Grula MM (1962) Cell division in a species of Erwina. III. Reversal of inhibition of cell division caused by D-amino acids, penicillin and ultraviolet light. J Bacteriol 83:981–988

    Google Scholar 

  • Horáček P, Drobnik J (1971) Interaction of cis-dichlorodiammineplatinum(II) with DNA. Biochim Biophys Acta 254:341–347

    Google Scholar 

  • Ingram LO, Fissher WD (1973) Stimulation of cell division by membrane-active agents. Biochem Biophys Res Comm 50: 200–210

    Google Scholar 

  • Inouye M (1972) Reversal by sodium chloride of envelope protein changes related to DNA replication and cell division of Escherichia coli. J Mol Biol 63:597–600

    Google Scholar 

  • Kauffman GB, Cowan DO (1963) Cis- and trans-dichlorodiammineplatinum(II). In: Kleinberg J (ed) Inorganic syntheses, vol VII. McGraw-Hill, New York San Franciso Toronto London, pp 233–245

    Google Scholar 

  • Kenyon CJ (1983) The bacterial response to DNA damage. Trends Biochem Sci 8:84–87

    Google Scholar 

  • Kleinwächter V (1978) Interaction of platinum(II) coordination complexes with deoxyribonucleic acid (a minireview). Stud Biophys 73:1–17

    Google Scholar 

  • Kojima M, Suda S, Hotta S, Hamada K, Suganuma A (1970) Necessity of calcium ion for cell division in Lactobacillus bifidus. J Bacteriol 104:1010–1013

    Google Scholar 

  • Lin HJ, Chargaff E (1966) On the denaturation of deoxyribonucleic acid. Biochim Biophys Acta 123:66–75

    Google Scholar 

  • Little JW, Mount DW (1982) The SOS regulatory system of Escherichia coli. Cell 29:11–22

    Google Scholar 

  • Markham BE, Brubaker RR (1980) Influence of chromosome integrity on Escherichia coli cell division. J Bacteriol 143:455–462

    Google Scholar 

  • Mathison GE (1968) Kinetics of death induced by penicillin and chloramphenicol in synchronous cultures of Escherichia coli. Nature (London) 219:405–407

    Google Scholar 

  • Mitchison JM, Vincent WS (1965) Preparation of synchronous cell cultures by sedimentation. Nature (London) 209:987–989

    Google Scholar 

  • Monti-Bragadin C, Giraldi T, Cantini M, Zessinovich G, Mestroni G (1974) Inhibition of bacterial growth and nucleic acids synthesis by planar complexes of rhodium(I). FEBS Lett 43:13–16

    Google Scholar 

  • Poole RK (1977) Fluctuations in buoyant density during the cell cycle of Escherichia coli K12: significance for the preparation of synchronous cultures by age selection. J Gen Microbiol 98:177–186

    Google Scholar 

  • Poole RK (1982) Rapid estimates of sizes of micro-organisms with the Coulter Nano-sizerTM. Microbios Lett 19:109–117

    Google Scholar 

  • Poole RK (1983) Mitochondria of Tetrahymena pyriformis: enumeration and sizing of isolated organelles using a Coulter counter and pulse-height analyser. J Cell Sci 61:437–451

    Google Scholar 

  • Quillardet P, Huisman O, D'Ari R, Hofnung M (1982) SOS chromotest, a direct assay of induction of an SOS function in Escherichia coli K12 to measure genotoxicity. Proc Nat Acad Sci USA 79:5971–5975

    Google Scholar 

  • Reed KC, Bygrave FL (1974) The inhibition of mitochondrial calcium transport by lanthanides and Ruthenium Red. Biochem J 140:143–155

    Google Scholar 

  • Rosenberg B (1978) Platinum complexes for the treatment of cancer. Interdisc Sci Rev 3:134–147

    Google Scholar 

  • Rosenberg B, Vancamp L, Krigas T (1965) Inhibition of cell division in Escherichia coli by electrolysis products from a platinum electrode. Nature (London) 205:698–699

    Google Scholar 

  • Rosenberg B, Renshew E, Vancamp L, Hartwick J, Drobnik J (1967) Platinum-induced filamentous growth in Escherichia coli. J Bacteriol 93:716–721

    Google Scholar 

  • Salles B, Lesca C (1982) Induction of recA protein in Escherichia coli by three platinum(II) compounds. Biochem Biophys Res Comm 105:202–208

    Google Scholar 

  • Satta G, Pardec AB (1978) Inhibition of Escherichia coli division by protein X. J Bacteriol 133:1492–1500

    Google Scholar 

  • Slater M, Schaechter M (1974) Control of cell division in bacteria. Bacteriol Rev 38:199–221

    Google Scholar 

  • Thomson AJ (1977) The mechanism of action of anti-tumour platinum compounds. Platinum Metals Rev 21:2–15

    Google Scholar 

  • Tsuruo T, Iida H, Tsukagoshi S, Sakurai Y (1980) Growth inhibition of Lewis lung carcinoma by an inorganic dye, Ruthenium Red. Gann 71:151–154

    Google Scholar 

  • Yasbin RE, Matthews CR, Clarke MJ (1980) Mutagenic and toxic effects of ruthenium. Chem Biol Interact 31:355–365

    Google Scholar 

  • Yoshiyama Y, Shimoii H, Tamura G (1981) Characterization of substances that restore impaired cell division of UV-irradiated E. coli B. Agric Biol Chem 45:1743–1751

    Google Scholar 

Download references

Author information

Author notes

  1. Jane F. Gibson

    Present address: Health and Safety Executive, Edgware Road, NW2 6LN, London, England

Authors and Affiliations

  1. Department of Microbiology, Queen Elizabeth College (University of London), Campden Hill, W8 7AH, London, England

    Jane F. Gibson & Robert K. Poole

  2. Department of Chemistry, Queen Elizabeth College (University of London), Campden Hill, W8 7AH, London, England

    Martin N. Hughes

  3. Environmental and Medical Sciences Division, Harwell Laboratory, OX11 0RA, Oxon, England

    John F. Rees

Authors
  1. Jane F. Gibson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert K. Poole
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin N. Hughes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. John F. Rees
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gibson, J.F., Poole, R.K., Hughes, M.N. et al. Filamentous growth of Escherichia coli K12 elicited by dimeric, mixed-valence complexes of ruthenium. Arch. Microbiol. 139, 265–271 (1984). https://doi.org/10.1007/BF00402012

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00402012

Key words

Search

Navigation