1887

Microbiology Society logo

Volume 145, Issue 11

Actin-related proteins in and their interactions with actin-binding proteins Free

Abstract

A group of prokaryotic actin-related proteins (PARP) with an of 43000 was detected in . These proteins were enriched by a depolymerization/polymerization cycle, under similar conditions to those used to polymerize muscle actin, and purified by affinity chromatography on a DNase I-Sepharose column. Three isoforms of PARP (-PARP) with pI values of 58, 615 and 62 were detected. -PARP were recognized by four different anti-actin antibodies (one anti-muscle and three anti-cytoplasmic isoforms). -PARP were also recognized by antibodies against PARP (-PARP) and against actin-binding proteins such as α-actinin and spectrin, and also by a monoclonal antibody against heat-shock cognate protein 70 (Hsc70). Specific binding of phalloidin to -PARP was detected both in permeabilized cells and . Purified -PARP can polymerize under similar conditions to those required for skeletal muscle actin polymerization and the filaments formed appear to be decorated with myosin subfragment-1 (S1) as observed by transmission electron microscopy. The amino acid composition of -PARP revealed more similarities to muscle γ-actin and the cytoplasmic β-actin isoform than to eukaryotic actin-related proteins.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): ABP, actin-binding proteins , actin-binding proteins , actin-related proteins , Actinobacillus pleuropneumoniae , Ap, Actinobacillus pleuropneumoniae , ARP, actin-related proteins , Av, Anabaena variabilis , CD, cytochalasin D , cytoskeleton-like structure , Hsc, heat-shock cognate protein , Hsp, heat-shock protein , PARP, prokaryotic actin-related proteins , prokaryotic actin-related proteins , S1, myosin subfragment-1 and TRITC, tetramethylrhodamine isothiocyanate
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-145-11-3235
1999-11-01
2023-11-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/145/11/1453235a.html?itemId=/content/journal/micro/10.1099/00221287-145-11-3235&mimeType=html&fmt=ahah

References

  1. Addinall S. G., Bi E., Lutkenhaus J. 1996; FtsZ ring formation in fts mutants. J Bacteriol 178:3877–3884
     [Google Scholar]
  2. Andreev O. A., Borejdo J. 1991; The myosin head can bind two actin monomers. Biochem Biophys Res Commun 177:350–356 [CrossRef]
     [Google Scholar]
  3. Barnett L. A., Cunningham M. W. 1992; Evidence for actinlike protein in a M protein-negative strain of Streptococcus pyogenes. Infect Immun 60:3932–3936
     [Google Scholar]
  4. Bauman P., Jackson S. P. 1996; An archaebacterial homologue of the essential eubacterial cell division protein FtsZ. Proc Natl Acad Sci USA 93:6726–6730 [CrossRef]
     [Google Scholar]
  5. Beck B. D., Arschott P. G., Jacobson A. 1978; Novel properties of bacterial elongation factor Tu. Proc Natl Acad Sci USA 75:1250–1254 [CrossRef]
     [Google Scholar]
  6. Bidlingmeyer B. A., Cohen S. A., Travin T. L. 1984; Rapid analysis of amino acids using pre-column derivatization. J Chromatogr 336:93–104 [CrossRef]
     [Google Scholar]
  7. Bork P., Sander C., Valencia A. 1992; An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin and hsp70 heat shock proteins. Proc Natl Acad Sci USA 89:17290–17294
     [Google Scholar]
  8. Campos A., Bernard P., Fauconnier A., Landa A., Gómez, E., Hernández, R., Willms K., Laclette J. P. 1990; Cloning and sequencing of two actin genes from Taenia solium (Cestoda). Mol Biochem Parasitol 40:87–93 [CrossRef]
     [Google Scholar]
  9. Casaregola S., Norris S., Goldberg M., Holland I. B. 1990; Identification of 180 kD protein in Escherichia coli related to a yeast heavy chain myosin. Mol Microbiol 4:505–511 [CrossRef]
     [Google Scholar]
  10. Flaherty K. M., McKay D. B., Kabsch W., Holmes K. C. 1991; Similarity of the three dimensional structure of actin and the ATPase fragment of 70 kDa heat shock cognate protein. Proc Natl Acad Sci USA 88:5041–5045 [CrossRef]
     [Google Scholar]
  11. Fleischmann R. D., Adams M. D., White O.37 other authors 1995; Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512 [CrossRef]
     [Google Scholar]
  12. Garrels J., Gibson W. 1976; Identification and characterization of multiple forms of actin. Cell 9:793–805 [CrossRef]
     [Google Scholar]
  13. Göbel U. 1983; Supramolecular structures in mycoplasmas. Yale J Biol Med 56:695–700
     [Google Scholar]
  14. Guerrero-Barrera A. L., Villalba J., Garcı́a, C., Segura M., Gómez, C., Reyes M., Hernández, M., Garcı́a, R., De la Garza M. 1995; Actin related proteins in the prokaryote Anabaena. Mol Biol CellSuppl. 6 ASCB abstracts 19a, summary 111
    [Google Scholar]
  15. Guerrero-Barrera A. L., Garcı́a-Cuéllar C. M., Villalba J. D., Segura-Nieto M., Hernández, J. M., Gómez-Lojero, C., Reyes M. E., Garcı́a, R. M., De la Garza M. 1996; Actin-related proteins in Anabaena spp. and Escherichia coli. Microbiology 142:1133–1140 [CrossRef]
     [Google Scholar]
  16. Haesebrouck F., Chiers K., Van Overbeke I., Ducatelle R. 1997; Actinobacillus pleuropneumoniae infections in pigs: the role of virulence factors in pathogenesis and protection. Vet Microbiol 58:239–249 [CrossRef]
     [Google Scholar]
  17. Herman I. M. 1993; Actin isoforms. Curr Opin Cell Biol 5:48–55 [CrossRef]
     [Google Scholar]
  18. Hiraga S. 1993; Chromosome partition in Escherichia coli. Curr Opin Genet Dev 5:789–801
     [Google Scholar]
  19. Kabsch W., Holmes K. 1995; The actin fold. FASEB J 9:167–174
     [Google Scholar]
  20. Kabsch W., Mannherz H. G., Suck D., Pai E. F., Holmes K. C. 1990; Atomic structure of actin DNase I complex. Nature 347:33–44
     [Google Scholar]
  21. Koonin E. V., Mushegian A. R., Rudd K. E. 1996; Sequencing and analysis of bacterial genomes. Curr Biol 4:404–416
     [Google Scholar]
  22. Kreuder V., Dieckhoff J., Manherz H. G. 1984; Isolation, characterization and crystallization of deoxyribonuclease I, from bovine and rat parotid gland and its interaction with rabbit skeletal muscle actin. Eur J Biochem 139:389–400 [CrossRef]
     [Google Scholar]
  23. Labbé, J. P., Harricane M. C., Boyer M., Derancourt J., Roustan C., Benyamin Y. 1996; Biochemical evidence for the presence of an unconventional actin protein in a prokaryotic organism. Comp Biochem Physiol B Biochem Mol Biol 114:287–293 [CrossRef]
     [Google Scholar]
  24. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [CrossRef]
     [Google Scholar]
  25. Lazarides E., Lindberg U. 1974; Actin is the natural occurring inhibitor of deoxyribonuclease I. Proc Natl Acad Sci USA 71:4742–4746 [CrossRef]
     [Google Scholar]
  26. Lockhart A., Kendrick-Jones J. 1998; Nucleotide-dependent interaction of the terminal N-domain of MukB with microtubules. J Struct Biol 15:303–310
     [Google Scholar]
  27. Löwe, J., Amos L. A. 1998; Crystal structure of the bacteria cell-division protein Fts-Z. Nature 391:203–206 [CrossRef]
     [Google Scholar]
  28. Lu C., Stricker J., Ericson H. P. 1998; FtsZ from Escherichia coli, Azotobacter vinelandii, and Thermotoga maritima: quantitation, GTP hydrolysis, and assembly. Cell Motil Cytoskeleton 40:71–86 [CrossRef]
     [Google Scholar]
  29. Ma X., Ehrhardt D. W., Margolin W. 1996; Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. Proc Natl Acad Sci USA 93:12998–13003 [CrossRef]
     [Google Scholar]
  30. Manjula B. N., Fischetti V. A. 1986; Sequence homology of group A streptococcal Pep M5 protein with other coiled-coil proteins. Biochem Biophys Res Commun 140:684–690 [CrossRef]
     [Google Scholar]
  31. Manjula B. N., Trus B. L., Fischetti V. A. 1985; Presence of two distinct regions in the coiled-coil structure of the streptococcal Pep M5 protein: relationship to mammalian coiled-coil proteins and implications to its biological properties. Proc Natl Acad Sci USA 82:1064–1068 [CrossRef]
     [Google Scholar]
  32. Manjula B. N., Khandke K. M., Fairwell T., Relf W. A., Sriprakash K. S. 1991; Heptad motifs within the distal subdomain of the coiled-coil rod region of M protein from rheumatic fever and nephritis associated serotypes of group A streptococci are distinct from each other: nucleotide sequence of the M57 gene and relation of the deduced amino acid sequence to other M proteins. J Protein Chem 10:369–384 [CrossRef]
     [Google Scholar]
  33. Margolin W. 1998; A green light for the bacterial cytoskeleton. Trends Microbiol 6:233–238 [CrossRef]
     [Google Scholar]
  34. Mayer F., Vogt B., Poc C. 1998; Immunoelectronmicroscopic studies indicate the existence of a cell shape preserving cytoskeleton in prokaryotes. Naturwissenschaften 85:2278–2282
     [Google Scholar]
  35. Melby T. E., Ciampaglio C. N., Briscoe G., Ericson H. 1998; The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J Cell Biol 142:1595–1604 [CrossRef]
     [Google Scholar]
  36. Minkoff L., Damadian R. 1976; Actin like protein from Escherichia coli. Concept of cytotonus has the missing link between cell metabolism and biological ion exchange resins. J Bacteriol 125:353–365
     [Google Scholar]
  37. Mische S. M., Manjula B. N., Fischetti V. A. 1987; Relation of streptococcal M protein with human and rabbit tropomyosin: the complete amino acid sequence of human cardiac alpha tropomyosin, a highly conserved contractile protein. Biochem Biophys Res Commun 142:813–818 [CrossRef]
     [Google Scholar]
  38. Miyamoto Y., Kuroda M., Munekata E., Masaki T. 1986; Stoichiometry of actin and phalloidin binding: one molecule of the toxin dominates two actin subunits. J Biochem (Tokyo) 100:1677–1680
     [Google Scholar]
  39. Mullins R. D., Kelleher J. F., Pollard T. D. 1996; Actin-like actin?. Trends Cell Biol 6:2208–2215
     [Google Scholar]
  40. Nakamura K., Watanabe S. 1978; Myosin and actin from Escherichia coli. J Biochem 83:1459–1470
     [Google Scholar]
  41. Negrete-Abascal E., Tenorio V. R., Serrano J. J., Garcı́a, C. C., de la Garza M. 1994; Secreted proteases from Actinobacillus pleuropneumoniae Serotype 1 degrade porcine gelatin, hemoglobin and immunoglobulin A. Can J Vet Res 58:83–86
     [Google Scholar]
  42. Neimark H. 1977; Extraction of an actin-like protein from the prokaryote Mycoplasma pneumoniae. Proc Natl Acad Sci USA 74:4041–4054 [CrossRef]
     [Google Scholar]
  43. Niki H., Imamura R., Kitaoka M., Yamanaka K., Ogura T., Hiraga S. 1992; E. coli MukB protein involved in chromosomal partition forms a homodimer with a rod-and-hinge structure having DNA binding and ATP/GTP binding activities. EMBO J 11:5101–5109
     [Google Scholar]
  44. Nogales E., Wolf S. G., Downing K. H. 1998; Structure of the αβ tubulin dimer by electron crystallography. Nature 391:199–202 [CrossRef]
     [Google Scholar]
  45. Norris V., Turnock G., Sigee D. 1996; The Escherichia coli enzoskeleton. Mol Microbiol 19:197–204 [CrossRef]
     [Google Scholar]
  46. O’Farrel P. H. 1975; High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021
     [Google Scholar]
  47. Pardee J. D., Spudich J. A. 1982; Purification of muscular actin. Methods Enzymol 85:164–181
     [Google Scholar]
  48. Prideaux C. T., Lenghaus C., Krywult J., Hodgson A. L. M. 1999; Vaccination and protection of pigs against pleuropneumonia with a vaccine strain of Actinobacillus pleuropneumoniae produced by site-specific mutagenesis at the ApxII operon. Infect Immun 67:1962–1966
     [Google Scholar]
  49. Rosenbusch J. P., Jacobson G. R., Jaton J. C. 1976; Does a bacterial elongation factor share a common evolutionary ancestor with actin?. J Supramol Struct 5:391–396 [CrossRef]
     [Google Scholar]
  50. Sánchez, M., Valencia A., Ferrándiz, J. M., Sander C., Vicente M. 1994; Correlation between the structure and biochemical activities of FtsA, an essential cell division protein of the actin family. EMBO J 13:4919–4925
     [Google Scholar]
  51. Schägger H., von Jagow G. 1987; Tricine sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379 [CrossRef]
     [Google Scholar]
  52. Schroer T., Fyberg E., Cooper J., Waterson R., Helfman D., Pollard T. D., Meyer D. 1994; Actin-related protein nomenclature and classification. J Cell Biol 127:1777–1778 [CrossRef]
     [Google Scholar]
  53. Sharpe M. E., Errington J. 1999; Upheaval in the bacterial nucleoid. An active chromosome segregation mechanism. Trends Genet 15:70–74 [CrossRef]
     [Google Scholar]
  54. Sheterline P., Clayton J., Sparrow J. C. 1998 Actin – Protein Profile, 4th edn. New York: Oxford University Press;
     [Google Scholar]
  55. Sioud M., Baldacci G., Forterre P., Recondo A. H. 1987; Antitumour drugs inhibit growth of halophylic archaebacteria. Eur J Biochem 169:231–236 [CrossRef]
     [Google Scholar]
  56. Spudich J. A., Watt S. 1971; The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin–troponin complex with actin and the proteolytic fragments of myosin. J Biol Chem 246:4866–4871
     [Google Scholar]
  57. Usmanova A., Astier C., Méjean, C., Hubert F., Feinberg J., Benyamin Y., Roustan C. 1998; Coevolution of actin and associated proteins: an alpha-actinin-like protein in a cyanobacterium (Spirulina platensis). Comp Biochem Physiol B Biochem Mol Biol 120:4693–4700
     [Google Scholar]
  58. Vandekerckhove J., Deboben A., Nassal M., Wieland T. 1985; The phalloidin binding site of F-actin. EMBO J 4:2815–2818
     [Google Scholar]
  59. Wahl R., Rice P., Rice C. M., Kröger M. 1994; ECED – a totally integrated database of Escherichia coli K-12. Nucleic Acids Res 22:3450–3455 [CrossRef]
     [Google Scholar]
  60. Wessel D., Flügge U. L. 1984; A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138:141–143 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-145-11-3235
Loading
Actin-related proteins in Actinobacillus pleuropneumoniae and their interactions with actin-binding proteins
Microbiology 145, 3235 (1999); https://doi.org/10.1099/00221287-145-11-3235
/content/journal/micro/10.1099/00221287-145-11-3235
/content/journal/micro/10.1099/00221287-145-11-3235
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error