1887

Abstract

To evaluate the potential contribution of extracellular enzymes to the pathogenicity of mycobacteria, the presence of selected enzyme activities was investigated in the culture filtrates of the obligate human pathogen BCG, the opportunistic pathogens and , and the non-pathogenic species and . For and , 22 enzyme activities were detected in the culture filtrates and/or cell surfaces, of which eight were absent from the culture fluids of non-pathogens: alanine dehydrogenase, glutamine synthetase, nicotinamidase, isonicotinamidase, superoxide dismutase, catalase, peroxidase and alcohol dehydrogenase. These activities, which correspond to secreted enzymes, formed a significant part (up to 92%) of the total enzyme activities of the bacteria and were absent from the culture fluids and the cell surfaces of the non-pathogenic species and . The extracellular location of superoxide dismutase and glutamine synthetase seemed to be restricted to the obligate pathogens examined. The difference in the enzyme profiles was not attributable to the growth rates of the two groups of bacteria. The presence of the eight enzyme activities in the outermost compartments of obligate pathogens and their absence in those of non-pathogens provides further evidence that these enzymes may be involved in the pathogenicity of mycobacteria. In addition, the eight enzyme activities were demonstrated in the cell extract of . Stepwise erosion of the cell surface of to expose internal capsular constituents showed that the various enzyme activities, with the possible exception of superoxide dismutase, were located more deeply in the cell envelope of this bacterium. This suggests that the molecular architecture of the mycobacterial envelopes may play an important role in the pathogenicity of these organisms.

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1998-02-01
2024-04-18
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References

  1. Abou-Zeid C., Smith I., Grange J., Steele J., Rook G. 1986; Subdivision of daughter strains of Bacille Calmette-Guérin (BCG) according to secreted protein patterns.. J Gen Microbiol 132:3047–3053
    [Google Scholar]
  2. Akao T., Kusaka T., Kobashi K. 1981; Two esterases released from Mycobacterium smegmatis for the hydrolysis of long chain acyl-CoAs and Tween.. J Biochem 90:1661–1669
    [Google Scholar]
  3. Andersen A. B., Brennan P. 1994 Proteins and antigens of Mycobacterium tuberculosis . In Tuberculosis: Pathogenesis, Protection and Control pp 307–332 Edited by Bloom B. R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  4. Andersen A. B., Andersen P., Ljungqvist L. 1992; Structure and function of a 40,000-molecular-weight protein antigen of Mycobacterium tuberculosis . Infect Immun 60:2317–2323
    [Google Scholar]
  5. Andersen P., Askgaard D., Ljungqvist L., Bennedsen J., Heron I. 1991; Proteins released from Mycobacterium tuberculosis during growth.. Infect Immun 59:1905–1910
    [Google Scholar]
  6. Barclay R., Wheeler P. R. 1989; Metabolism of mycobacteria in tissues. In The Biology of the Mycobacteria 3Clinical Aspects of Mycobacterial Disease pp 37–106 Edited by Ratledge C., Stanford J., Grange J. M. San Diego, CA: Academic Press;
    [Google Scholar]
  7. Bloom B. R., Murray C. J. L. 1992; Tuberculosis: commentary on a reemergent killer.. Science 257:1055–1064
    [Google Scholar]
  8. Bönicke R. 1962; L’identification des mycobactéries à l’aide de méthodes biochimiques.. Bull Un Int Tuberc 32:13–76
    [Google Scholar]
  9. de Bruyn J., Johannes A., Weckx M., Beumer-Jochmans M. -P. 1981; Partial purification and characterization of an alcohol dehydrogenase of Mycobacterium tuberculosis var. bovis (BCG).. J Gen Microbiol 124:359–363
    [Google Scholar]
  10. Buttiaux R., Beerens H., Tacquet A. 1966 Mycobactéries. Recherche des mycobactéries dans les produits pathologiques. Techniques d’isolement et d’identification.. In Manuel de Techniques Bactériologiques 2nd edn, pp 540–541 Paris: Editions Médicales Flammarion;
    [Google Scholar]
  11. Casal M., Linares M. J. 1984; Enzyme profile of Mycobacterium tuberculosis . Eur J Clin Microbiol 3:155–156
    [Google Scholar]
  12. Chang Y. -Y., Cronan J. E. Jr 1982; Mapping non-selectable genes of Escherichia coli by using transposon Tn10: location of a gene affecting pyruvate oxidase.. J Bacteriol 151:1279–1289
    [Google Scholar]
  13. Clemens D., L, Lee B. -Y., Horwitz M. A. 1995; Purification, characterization and genetic analysis of Mycobacterium tuberculosis urease, a potentially critical determinant of host–pathogen interaction.. J Bacteriol 177:5644–5652
    [Google Scholar]
  14. Cossart P., Boquet P., Normark S., Rappuoli R. 1996; Cellular microbiology emerging.. Science 271:315–316
    [Google Scholar]
  15. Daffé M. 1996; Structure de l’enveloppe de Mycobacterium tuberculosis . Méd Mal Infect 26:891–897
    [Google Scholar]
  16. Daffé, M. & Draper P. 1998; The envelope layers of mycobacteria with reference to their pathogenicity.. Adv Microb Physiol 39:131–203
    [Google Scholar]
  17. Dave J. A., Schwager S. L. U., Scholle R. R., Ehlers M. R. W. 1996; Detection of proteases produced by Mycobacterium tuberculosis under defined culture conditions. In Abstracts of the Third International Conference on the Pathogenesis of Mycobacterial InfectionsStockholm p 59
    [Google Scholar]
  18. Draper P., Rees R. J. W. 1970; Electron transparent zone of mycobacteria may be a defence mechanism.. Nature 228:860–861
    [Google Scholar]
  19. Escuyer V., Haddad N., Frehel C., Berche P. 1996; Molecular characterization of a surface-exposed superoxide dismutase of Mycobacterium avium . Microb Pathog 20:41–55
    [Google Scholar]
  20. Harth G., Clemens D. L., Horwitz M. A. 1994; Glutamine synthetase of Mycobacterium tuberculosis: extracellular release and characterization of its enzyme activity.. Proc Natl Acad Sci USA 91:9342–9346
    [Google Scholar]
  21. Imboden P., Rene S., Small P., Schoolnik G. K. 1996; Regulation of Mycobacterium tuberculosis gene expression by oxygen tension.. In Abstracts of the Third International Conference on the Pathogenesis of Mycobacterial InfectionsStockholm p 3
    [Google Scholar]
  22. Jayaram H. N., Ramakrishnan T., Vaidyanathan C. S. 1968; l-Asparaginases from Mycobacterium tuberculosis strains H37Rv and H37Ra.. Arch Biochem Biophys 126:165–174
    [Google Scholar]
  23. Johansen K. A., Gill R. E., Vasil M. L. 1996; Biochemical and molecular analysis of phospholipase C and phospholipase D activity in mycobacteria.. Infect Immun 64:3259–3266
    [Google Scholar]
  24. Kannan K. B., Katoch V. M., Sharma V. D., Bharadwaj V. P. 1987; Extracellular enzymes of mycobacteria.. FEMS Microbiol Lett 48:31–33
    [Google Scholar]
  25. Kilburn J. O., Best G. K. 1977; Characterization of autolysins from Mycobacterium smegmatis . J Bacteriol 29:750–755
    [Google Scholar]
  26. Kurioka S., Matsuda M. 1976; Phospholipase C assay using p-nitrophenylphosphoryl-choline together with sorbitol and its application to studying the metal and detergent requirement of the enzyme.. Anal Biochem 75:281–289
    [Google Scholar]
  27. Lemassu A., Daffé M. 1994; Structural features of the exocellular polysaccharides of Mycobacterium tuberculosis . Biochem J 297:351–357
    [Google Scholar]
  28. Lemassu A., Ortalo-Magné A., Bardou F., Silve G., Lanéelle M. -A., Daffé M. 1996; Extracellular and surface-exposed poly-saccharides of non-tuberculous mycobacteria.. Microbiology 142:1513–1520
    [Google Scholar]
  29. Luthman M., Holmgren A. 1982; Rat liver thioredoxin and thioredoxin reductase: purification and characterization.. Biochemistry 21:6628–6633
    [Google Scholar]
  30. Meers J. L., Tempest D. W., Brown C. M. 1970; Glutamine(amide): 2-oxoglutarate amino transferase oxido-reductase (NADP), an enzyme involved in the synthesis of glutamate by some bacteria.. J Gen Microbiol 64:187–194
    [Google Scholar]
  31. Middlebrook G. 1954; Isoniazid-resistance and catalase activity of tubercle bacilli.. Am Rev Tuberc 69:471–472
    [Google Scholar]
  32. Middlebrook G., Cohn M. L. 1953; Some observations on the pathogenicity of isoniazid-resistant variants of tubercle bacilli.. Science 118:297–299
    [Google Scholar]
  33. Migliore D., Acharya N. P. V., Jollès P. 1966; Caractérisation de quantités importantes d’acide glutamique dans les parois de mycobactéries de souches humaines virulentes.. C R Acad Sci Ser D 263:846–848
    [Google Scholar]
  34. Moran N. 1996; WHO issues another gloomy tuberculosis report.. Nature Medicine 2:377
    [Google Scholar]
  35. Muftic M. 1967; Application of chromogenic substrates to the determination of peptidases in mycobacteria.. Folia Microbiol 12:500–507
    [Google Scholar]
  36. Nagai S., Wiker H. G., Harboe M., Kinomoto M. 1991; Isolation and partial characterization of major protein antigens in the culture fluid of Mycobacterium tuberculosis . Infect Immun 59:372–382
    [Google Scholar]
  37. Ortalo-Magné A., Dupont M. -A., Lemassu A., Andersen A. B., Gounon P., Daffé M. 1995; Molecular composition of the outermost capsular material of the tubercle bacillus.. Microbiology 141:1609–1620
    [Google Scholar]
  38. Ortalo-Magné A., Lemassu A., Lanéelle M. -A., Bardou F., Silve G., Gounon P., Marchal G., Daffé M. 1996; Identification of the surface-exposed lipids on the cell envelopes of Mycobacterium tuberculosis and other mycobacterial species.. J Bacteriol 178:456–461
    [Google Scholar]
  39. Paoletti F., Mocali A. 1990; Determination of superoxide dismutase activity by purely chemical system based on NAD(P)H oxidation.. Methods Enzymol 186:209–220
    [Google Scholar]
  40. Salyers A. A., Whitt D. D. 1994 Bacterial Pathogenesis, a Molecular Approach Washington, DC: American Society for Microbiology;
    [Google Scholar]
  41. Sauton B. 1912; Sur la nutrition minérale du bacille tuberculeux.. C R Acad Sci Ser III Sci Vie 155:860–863
    [Google Scholar]
  42. Schraufstätter I. U., Halsey W. A. Jr, Hyslop P. A., Cochrane C. G. 1988; In vitro models for the study of oxidant-induced injury of cells in inflammation.. Methods Enzymol 163:328–340
    [Google Scholar]
  43. Sears C. L., Kaper J. B. 1996; Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion.. Microbiol Rev 60:167–215
    [Google Scholar]
  44. Smibert R. M., Krieg N. R. 1981 General characterization.. In Manual of Methods for General Bacteriology pp 409–443 Edited by Gerhardt P. and others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  45. Travis J., Potempa J., Maeda H. 1995; Are bacterial proteinases pathogenic factors?. Trends Microbiol 3:405–407
    [Google Scholar]
  46. Tsukamura M. 1966; Adansonian classification of mycobacteria.. J Gen Microbiol 45:253–273
    [Google Scholar]
  47. Tsukamura M. 1981; A review of the methods of identification and differentiation of mycobacteria.. Rev Infect Dis 3:841–861
    [Google Scholar]
  48. Vincent Lévy-Frébault V., Portaels F. 1992; Proposed minimal standards for the genus Mycobacterium and for description of new slowly growing Mycobacterium species.. Int J Syst Bacteriol 42:315–323
    [Google Scholar]
  49. Wagner B., Fattorini L., Wagner M., Jin S. -H., Stracke R., Amicosante G., Franceschini N., Orefici G. 1995; Antigenic properties and immunoelectron microscopic localization of Mycobacterium fortuitum β-lactamase.. Antimicrob Agents Chemother 39:739–745
    [Google Scholar]
  50. Warren L. 1959; The thiobarbituric acid assay of sialic acids.. J Biol Chem 234:1971–1975
    [Google Scholar]
  51. Wheeler P. R., Ratledge C. 1992; Control and location of acyl-hydrolysing phospholipase activity in pathogenic mycobacteria.. J Gen Microbiol 138:825–830
    [Google Scholar]
  52. Wieles B., Nagai S., Wiker H. G., Harboe M., Ottenhoff T. H. M. 1995; Identification and functional characterization of thioredoxin of Mycobacterium tuberculosis . Infect Immun 63:4946–4948
    [Google Scholar]
  53. Wietzerbin J., Lederer F., Petit J. -F. 1975; Structural study of the poly-l-glutamic acid of the cell wall of Mycobacterium tuberculosis var hominis, strain Brevannes.. Biochem Biophys Res Commun 62:246–252
    [Google Scholar]
  54. Wiker H. G., Harboe M., Nagai S. 1991; A localization index for distinction between extracellular and intracellular antigens of Mycobacterium tuberculosis . J Gen Microbiol 137:875–884
    [Google Scholar]
  55. Wilson T. M., de Lisle G. W., Collins D. M. 1995; Effect of inhA and katG on isoniazid resistance and virulence of Mycobacterium bovis . Mol Microbiol 15:1009–1015
    [Google Scholar]
  56. Woodbury R. G., Everitt M. T., Neurath H. 1981; Mast cell proteases.. Methods Enzymol 80:588–609
    [Google Scholar]
  57. Woolfolk C. A., Shapiro B., Stadtman E. R. 1966; Regulation of glutamine synthetase. I. Purification and properties of glutamine synthetase from Escherichia coli . Arch Biochem Biophys 116:177–192
    [Google Scholar]
  58. Young D. B., Kaufman S. H. E., Hermans P. W. M., Thole J. E. R. 1992; Mycobacterial protein antigens: a compilation.. Mol Microbiol 6:133–145
    [Google Scholar]
  59. Zhang Y., Lathigra R., Garbe T., Catty D., Young D. 1991; Genetic analysis of superoxide dismutase, the 23 kilodalton antigen of Mycobacterium tuberculosis . Mol Microbiol 5:381–391
    [Google Scholar]
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