Actin-related proteins in Anabaena spp. and Escherichia coli Free

Abstract

Actin has been described in all eukaryotic cells as the major microfilament cytoskeletal protein. Although prokaryotic cells do not have a cytoskeleton, proteins related to the latter have been found in different prokaryotic species. We have found prokaryotic actin-related proteins in the enterobacterium and in the cyanobacteria and . They were identified by the following criteria: (1) by cross-reaction with a fluorescent conjugated anti-actin (rat-brain) mAb by Western blot analysis (in total cellular extracts); (2) specific binding of acetone powder and soluble cellular extracts to DNase 1; and (3) specific binding of cells and total cellular extracts to phalloidin. In , specific binding of phalloidin labelled with rhodamine to cells was detected by spectrofluorometry. In total cellular extracts, three bands of 60, 43 and 35 kDa were weakly recognized by the mAb by Western blot analysis; this recognition increased when phalloidin was added to the extracts. Furthermore, three polypeptides of 60 kDa were isolated by binding to DNase I, showing pl values of 6.7, 6.65 and 6.6, less acidic than all reported actin pl values. In and , specific binding of phalloidin labelled with rhodamine to cells was also detected by spectrofluorometry. In total and soluble cellular extracts, the mAb recognized two bands of 45 and 40 kDa by Western blot analysis, but only the first was purified by binding to DNase I, and it showed three isoforms of pl values 6.8, 6.5 and 6.4. These results suggest the presence, in prokaryotes, of proteins with similar biochemical characteristics to eukaryotic actin.

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1996-05-01
2024-03-28
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References

  1. Barnett L.A., Cunningham M.W. Evidence for actinlike protein in a M protein-negative strain of Streptococcus pyogenes. Infect lmmun 1992; 60:3932–3936
    [Google Scholar]
  2. Beck B.P., Arscott P., Jacobson A. Novel properties of bacterial elongation factor Tu. Proc Natl Acad Sci USA 1978; 75:1250–1254
    [Google Scholar]
  3. Betina V., Micekov£ D., Nemec P. Antimicrobial properties of cytochalasins and their alteration of fungal morphology. J Gen Microbiol 1972; 71:343–349
    [Google Scholar]
  4. Bork P., Sander C., Valencia A. An ATPase domain common to prokaryotic cell cycle proteins. Proc Natl Acad Sci USA 1992; 89:7290–7294
    [Google Scholar]
  5. Bradford M. A rapid method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248–254
    [Google Scholar]
  6. Burchard R.P. Evidence for contractile flexing of the gliding bacterium Elexibacter FS-1. Nature 1982; 298:663–665
    [Google Scholar]
  7. Castenholz R.W. Culturing methods for cyanobacteria. Methods Encymol 1988; 167:68–93
    [Google Scholar]
  8. Danker P., Low I., Hasselbach W., Wieland T. Interaction of actin with phalloidin: polymerization and stabilization of F-actin. Biochim Biophys Acta 1975; 400:407–414
    [Google Scholar]
  9. De La Garza M., Gallegos B., Meza I. Characterization of a cytochalasin D-resistant mutant of Entamoeba histolytica. J Protocol 1989; 36:556–560
    [Google Scholar]
  10. Diamond L.S., Harlow D.R., Cunick C.C. A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans R Soc Trop Med Hyg 1978; 72:431–432
    [Google Scholar]
  11. Drubin D.G. Actin and actin binding proteins in yeast. Cell Motil Cytoskeleton 1990; 15:7–11
    [Google Scholar]
  12. Eda T., Kanda Y., Mori C., Kimura S. Microtubular structures in a stable staphylococcal L-form. Bacteriol 1977; 32:1024–1026
    [Google Scholar]
  13. Etho S., Matsui H., Tokuda M., Itano T., Nakamura M. Purification and immunohistochemical study of actin in mitochondrial matrix. Biochem Int 1990; 20:599–606
    [Google Scholar]
  14. Flaherty K.M., McKay D., B.; Kabsh W., Holmes K.C. Similarity of the three dimensional structure of actin and the ATPase fragment of a 70 KDa heat shock cognate protein. Proc Natl Acad Sei USA 1991; 88:5041–5045
    [Google Scholar]
  15. Foster S.J. Purification and characterization of an ‘ actomyosin ’ complex from Escherichia coli W3110. FEMS Microbiol Lett 1993; 110:295–298
    [Google Scholar]
  16. García-Cuéllar C., Tenorio V., Cisneros B., Montañez C., Hernández J.M., Alvarez J., De La Garza M. Actin-like sequences in Escherichia coli and Salmonella typhimurium. J Cell Biol 1990; 111:148 31a
    [Google Scholar]
  17. Göbel U., Speth V., Bredy W. Filamentous structures in adherent Mycoplasma pneumoniae cells treated with non ionic detergents. J Cell Biol 1981; 91:537–543
    [Google Scholar]
  18. Gosh A., Maniloff J., Gelling D. Inhibition of Mycoplasma cell division by cytochalasin B. Cell 1978; 13:57–64
    [Google Scholar]
  19. Guerrero-Barrera A.L., García C.M., Reyes M.E., Segura M., Hernández J.M., De La Garza M. Prokaryotic actin-related proteins in enterobacterial and cyanobacterial cells. Abstr Gen Meet Am Soc Microbiol 1-81 1994268
    [Google Scholar]
  20. Heat I.B. The roles of actin in tip growth of fungi. Int Rev Cytol 1990; 123:95–127
    [Google Scholar]
  21. Hennessey E.S., Drummond D.R., Sparrow J.C. Molecular genetics of actin function. Biochem J 1993; 282:657–671
    [Google Scholar]
  22. Herman I.M. Actin isoforms. Curr Opin Cell Biol 1993; 5:48–55
    [Google Scholar]
  23. Hightower R.C., Meagher R. The molecular evolution of actin. Genetics 1986; 114:315–332
    [Google Scholar]
  24. Hiraga S. Chromosome partition in Escherichia coli. Curr Opin Genet Dev 1993; 5:789–801
    [Google Scholar]
  25. Janmey P.A. Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly. Annu Rev Physiol 1994; 56:169–191
    [Google Scholar]
  26. Kabsch W., Mannherz H.G., Suck D., Pai E.F., Holmes K.C. Anatomic structure of the actin DNase I complex. Nature 1990; 347:33–44
    [Google Scholar]
  27. Korolev E.V., Nikonov A.V., Brudnaya M.S., Snigirevskaya E.S., Sabinin G., Komissarchik Y.Y., Ivanov P., Borchsenius S. Tubular structures of Mycoplasma gallisepticum and their possible participation in cell motility. Microbiology 1994; 140:671–681
    [Google Scholar]
  28. Laemmli U. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680–685
    [Google Scholar]
  29. Lazarides E., Lindberg U. Actin is the naturally occurring inhibitor of deoxyribonuclease I. Proc Natl Acad Sei USA 1974; 71:4742–4746
    [Google Scholar]
  30. Lengsfeld A.M., Low I., Wieland T., Dancker P., Hasselbach W. Interaction of phalloidin with actin. Proc Natl Acad Sei USA 1974; 71:2803–2807
    [Google Scholar]
  31. Less-Miller J.P., Henry G., Helfman D.M. A vertebrate actin-related protein is a component of a multi-subunit complex involved in microtubule-based vesicle motility. Nature 1992; 359:244–250
    [Google Scholar]
  32. Low I., Dancker P., Wieland T. Stabilization of F-actin by phalloidin. Reversal of the destabilizing effect of cytochalasin B. FEBS Lett 1975; 54:263–265
    [Google Scholar]
  33. Lutkenhaus J. Escherichia coli cell division. Curr Opin Genet Dev 1993; 3:783–788
    [Google Scholar]
  34. Manning-Cela R., Meraz M.A., Hernández J.M., Meza I. Regulation of actin in Entamoeba histolytica. J Eukaryot Microbiol 1994; 41:360–365
    [Google Scholar]
  35. Meagher R.B., MacLean B.G. Diversity of plant actins. Cell Motil Cytoskeleton 1990; 16:164–166
    [Google Scholar]
  36. Minkoff L., Damadian R. Actin like protein from Escherichia coli. Concept of cytotonus has the missing link between cell metabolism and biological ion exchange resins. J Bacteriol 1976; 125:353–365
    [Google Scholar]
  37. Nakamura K., 8í Watanabe S. Myosin-like protein and actin-like protein. J Biochem 1978; 83:1459–1470
    [Google Scholar]
  38. Nakamura K., Takahashi K., Watanabe S. Myosin and actin from Escherichia coli. J Biochem 1978; 84:1453–1458
    [Google Scholar]
  39. Neimark H.C. Extraction of an actin-like protein from the prokaryote Mycoplasma pneumoniae. Proc Natl Acad Sci USA 1977; 74:4041–4045
    [Google Scholar]
  40. Norris V., Chen M., Goldberg M., Voskvil J., McGurk G.E., Holland I.B. Calcium in bacteria: a solution for which problem. Mol Microbiol 1991; 5:775–778
    [Google Scholar]
  41. O'Farrell P.H. High resolution two dimensional electrophoresis of proteins. J Biol Chem 1975; 250:4007–4021
    [Google Scholar]
  42. Pardee J.D., Spudich J.A. Purification of muscular actin. Methods Enyymol 1982; 85:164–181
    [Google Scholar]
  43. Pérez H., Sánchez N., Vidali L., Hernández J.M., Lara M., Sánchez F. Actin isoforms in non-infected roots and symbiotic root nodules of Phaseolus vulgaris. Planta 1994; 193:51–56
    [Google Scholar]
  44. Rasheda S., Sodja A. Homology between actin coding and its adjacent sequences in widely divergent species. Biochem Biophys Res Commun 1983; 111:67–73
    [Google Scholar]
  45. Sánchez M., Valencia A., Ferrandiz M.-J., Sander C., Vicente M. Correlation between the structure and biochemical activities of FtsA, an essential cell division protein of the actin family. EMBO J 1994; 13:4919–4925
    [Google Scholar]
  46. Schwob E., Martin R.P. New yeast actin-like gene required late in the cell cycle. Nature 1992; 355:179–182
    [Google Scholar]
  47. Sioud M., Baldacci G., Forterre P., Recondo A.H. Antitumor drugs inhibit growth of halophilic archaebacteria. Eur J Biochem 1987; 169:231–236
    [Google Scholar]
  48. Spudich J.A., Watt S. The regulation of rabbit skeletal muscle contraction. J Biol Chem 1971; 246:4866–4871
    [Google Scholar]
  49. Stozharov A.N. Kinetics of biosynthesis and distribution of labeled actin-like protein in the submitochondrial fraction of rat liver. Biochi mica 1985; 50:337–345
    [Google Scholar]
  50. Tannenbaum J. Cytochalasin D alters the rate of synthesis of some Hep-2 cytoskeletal proteins. Examination by two dimensional gel electrophoresis. Eur j Biochem 1986; 155:533–542
    [Google Scholar]
  51. Vandekerckhove J., Weber K. At least six different actins are expressed in a higher mammal: an analysis based on the aminoacid sequence of the amino-terminal tryptic peptide. J Mol Biol 1978; 126:783–802
    [Google Scholar]
  52. Vandekerckhove J., Weber K. Actin typing on total cellular extracts. A highly sensitive protein-chemical procedure able to distinguish different actins. Eur J Biochem 1981; 113:595–603
    [Google Scholar]
  53. Vandekerckhove J., Weber K. Chordate muscle actins differ distinctly from invertebrate muscle actins. J Mol Biol 1984; 179:391–413
    [Google Scholar]
  54. Vandekerckhove J., Deboben A., Nassal M., Wieland T. The phalloidin binding site of F-actin. EMBO J 1985; 4:2815–2818
    [Google Scholar]
  55. Van Liere L., Mu L.R., Gibson C.E., Herdman M. Growth and physiology of Oscillatoria agardhii Gomont cultivate in continuous culture with a light-dark cycle. Arch Microbiol 1979; 123:315–318
    [Google Scholar]
  56. Wieland T. Modification of actins by phallotoxins. Naturwissenschaften 1977; 64a:303–309
    [Google Scholar]
  57. Wulf E., Deboben A., Bautz F.A., Wieland T. Fluorescent phallotoxin, a tool for the visualization of cellular actin. Proc Natl Acad Sci USA 1979; 76:4498–4502
    [Google Scholar]
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