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Volume 148, Issue 8

Permeability of to ribonucleosides Free

Abstract

Knowledge about transport in , an obligate phagolysosomal parasite, is incomplete. The authors investigated the capability of isolated, intact, host-free to transport ribonucleosides while incubated at a pH value typical of lysosomes. Because of the low activities and limitations of obtaining experimental quantities of isolated, purified , incorporation of substrate into nucleic acid was used as a trap for determination of uptake abilities. Virulent wild-type (phase I) organisms possessed uptake capability for all ribonucleosides. Both phase I and phase II (avirulent) organisms incorporated the purine nucleosides guanosine, adenosine and inosine, and showed a more limited uptake of thymidine and uridine. Both phases were poorly active in cytidine uptake. Neither phase of the organism was capable of transport and incorporation of NTPs, CMP, cytosine or uracil. Water space experiments confirmed that the uptake process concentrated the purine nucleosides within the cytoplasm of both wild-type and phase II via a low-pH-dependent mechanism. Comparison of uptake rates in versus verified that the incorporation of ribonucleosides by is a slow process. It is concluded that possesses some transport pathways consistent with utilization of pools of nucleosides found within its host cell lysosomal pathway.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): CCCP, carbonyl cyanide m-chlorophenylhydrazine , cell volume , growth in chick embryos , nucleosides and nucleotides and phase I and phase II activity
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2002-08-01
2024-04-19
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References

  1. Amano K., Williams J. C., McCaul T. F., Peacock M. G. 1984; Biochemical and immunological properties of Coxiella burnetii cell wall and peptidoglycan-protein complex fractions. J Bacteriol 160:982–988
     [Google Scholar]
  2. Amano K., Williams J. C., Missler S. R., Reinhold V. N. 1987; Structure and biological relationships of Coxiella burnetii lipopolysaccharides. J Biol Chem 262:4740–4747
     [Google Scholar]
  3. Atkinson W. H., Winkler H. H. 1985; Transport of AMP by Rickettsia prowazekii . J Bacteriol 161:32–38
     [Google Scholar]
  4. Austin F. A., Winkler H. H. 1988; Relationship of rickettsial physiology and composition to the Rickettsia-host cell interaction. In Biology of Rickettsial Diseases pp 29–49 Edited by Walker D. H. Boca Raton, FL: CRC Press;
     [Google Scholar]
  5. Banerjee-Bhatnagar N., Bolt C. R., Williams J. C. 1996; Pore-forming activity of Coxiella burnetii outer membrane protein oligomer comprised of 29·5- and 31-kDa polypeptides. Ann N Y Acad Sci 791:378–401 [CrossRef]
     [Google Scholar]
  6. Barrett A. J. 1984; Proteolytic and other metabolic pathways in lysosomes. Biochem Soc Trans 12:899–902
     [Google Scholar]
  7. Chen S.-Y., Vodkin M., Thompson H. A., Williams J. C. 1990; Isolated Coxiella burnetii synthesizes DNA during acid activation in the absence of host cells. J Gen Microbiol 136:89–96 [CrossRef]
     [Google Scholar]
  8. Christian R. G., Paretsky D. 1977; Synthesis of ribonucleotides and their participation in ribonucleic acid synthesis by Coxiella burnetii . J Bacteriol 132:841–846
     [Google Scholar]
  9. Crenshaw R. W., Fahr M. J., Wichlan D. G., Hatch T. P. 1990; Developmental cycle-specific host-free RNA synthesis in Chlamydia spp. Infect Immun 58:3194–3201
     [Google Scholar]
  10. Gimenez D. F. 1964; Staining rickettsiae in yolk-sac cultures. Stain Technol 39:135–140
     [Google Scholar]
  11. Hackstadt T., Williams J. C. 1981a; Biochemical stratagem for obligate parasitism of eukaryotic cells by Coxiella burnetii . Proc Natl Acad Sci USA 78:3240–3244 [CrossRef]
     [Google Scholar]
  12. Hackstadt T., Williams J. C. 1981b; Stability of the adenosine 5′-triphosphate pool in Coxiella burnetii: influence of pH and substrate. J Bacteriol 148:419–425
     [Google Scholar]
  13. Hackstadt T., Williams J. C. 1981c; Incorporation of macromolecular precursors by Coxiella burnetii in an axenic medium. In Rickettsiae and Rickettsial Diseases pp 431–440 Edited by Burgdorfer W., Anacker R. L. New York: Academic Press;
     [Google Scholar]
  14. Hatch T. P. 1975; Utilization of L-cell nucleoside triphosphates by Chlamydia psittaci for ribonucleic acid synthesis. J Bacteriol 122:393–400
     [Google Scholar]
  15. Hatch T. P., Al-Hossainy E., Silverman J. A. 1982; Adenine nucleotide and lysine transport in Chlamydia psittaci . J Bacteriol 150:662–670
     [Google Scholar]
  16. Heinzen R., Scidmore M., Rockey D. D., Hackstadt T. 1996; Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis . Infect Immun 64:796–809
     [Google Scholar]
  17. Hoover T. A., Williams J. C. 1990; Characterization of Coxiella burnetii pyrB . Ann N Y Acad Sci 590:485–490 [CrossRef]
     [Google Scholar]
  18. Kazar J., Skultetyova E., Brezina R. 1975; Phagocytosis of Coxiella burnetii by macrophages. Acta Virol 19:426–431
     [Google Scholar]
  19. Krauss H., Schiefer H.-G., Schmatz H.-D. 1977; Ultrastructural investigations on surface structures involved in Coxiella burnetii phase variation. Infect Immun 15:890–896
     [Google Scholar]
  20. Mallavia L., Paretsky D. 1963; Studies on the physiology of Rickettsiae. Part V. Metabolism of carbamoyl phosphate by Coxiella burnetii . J Bacteriol 86:232–238
     [Google Scholar]
  21. Mans R. J., Novelli G. D. 1960; A convenient, rapid and sensitive method of measuring the incorporation of radioactive amino acids into protein. Biochem Biophys Res Commun 3:540–543 [CrossRef]
     [Google Scholar]
  22. McCaul T. F. 1991; The developmental cycle of Coxiella burnetii . In Q Fever: the Biology of Coxiella burnetii pp 223–258 Edited by Williams J. C., Thompson H. A. Boca Raton, FL: CRC Press;
     [Google Scholar]
  23. McClarty G., Qin B. 1993; Pyrimidine metabolism by intracellular Chlamydia psittaci . J Bacteriol 175:4652–4661
     [Google Scholar]
  24. McClarty G., Tipples G. 1991; In situ studies on incorporation of nucleic acid precursors into Chlamydia trachomatis DNA. J Bacteriol 173:4922–4931
     [Google Scholar]
  25. Paretsky D., Downs C. M., Consigli R. A., Joyce B. K. 1958; Studies on the physiology of rickettsiae I. Some enzyme systems of Coxiella burnetii . J Infect Dis 103:6–11 [CrossRef]
     [Google Scholar]
  26. Parker C. T., Kloser A. W., Schnaitman C. A., Stein M. A., Gottesman S., Gibson B. W. 1992; Role of rfaG and rfaP genes in determining the lipopolysaccharide core structure and outer membrane surface properties of Escherichia coli K-12. J Bacteriol 174:2525–2538
     [Google Scholar]
  27. Pine L., Franzus M. J., Malcolm G. B. 1986; Guanine is a growth factor for Legionella species. J Clin Microbiol 23:163–169
     [Google Scholar]
  28. Pisoni R. L., Thoene J. G. 1989; Detection and characterization of a nucleoside transport system in human fibroblast lysosomes. J Biol Chem 264:4850–4856
     [Google Scholar]
  29. Pisoni R. L., Thoene J. G. 1991; The transport system of mammalian lysosomes. Biochim Biophys Acta 1071:351–373 [CrossRef]
     [Google Scholar]
  30. Redd T. 1986 Secreted protein of Coxiella burnetii PhD dissertation West Virginia University;
     [Google Scholar]
  31. Redd T., Thompson H. A. 1995; Secretion of proteins by Coxiella burnetii. Microbiology 141:363–369
     [Google Scholar]
  32. Samuel J. E., Frazier M. E., Mallavia L. P. 1988; Stability of plasmid sequences in an acute Q-fever strain of Coxiella burnetii . J Gen Microbiol 134:1795–1805
     [Google Scholar]
  33. Schramek S., Mayer H. 1982; Different sugar compositions of lipopolysaccharides isolated from phase I and pure phase II cells of Coxiella burnetii . Infect Immun 38:53–57
     [Google Scholar]
  34. Schramek S., Radziejewska-Lebrecht J., Mayer H. 1985; 3-C-branched aldoses in lipopolysaccharide of phase I Coxiella burnetii and their role as immunodominant factors. Eur J Biochem 148:455–461 [CrossRef]
     [Google Scholar]
  35. Silverman D. J., Fiset P., Wisseman C. L. Jr 1979; Simple, differential staining technique for enumerating Rickettsiae in yolk sac, tissue culture extracts, or purified suspensions. J Clin Microbiol 9:437–440
     [Google Scholar]
  36. Thompson H. A. 1988; Relationship of the physiology and composition of Coxiella burnetii to the Coxiella -host cell interaction. In Biology of Rickettsial Diseases vol. II pp 51–78 Edited by Walker D. H.
    [Google Scholar]
  37. Tjaden J., Winkler H. H., Schwoppe C., Van Der Laan M., Mohlmann T., Neuhaus H. E. 1999; Two nucleotide transport proteins in Chlamydia trachomatis, one for net nucleoside triphosphate uptake and the other for transport of energy. J Bacteriol 181:1196–1202
     [Google Scholar]
  38. Vishwanath S., Hackstadt T. 1988; Lipopolysaccharide phase variation determines the complement-mediated serum susceptibility of Coxiella burnetii. Infect Immun. 5640–44
  39. Waag D. M., Williams J. C., Peacock M. G., Raoult D. 1991; Methods of isolation, amplification, and purification of Coxiella burnetii . In Q Fever: the Biology of Coxiella burnetii pp 73–115 Edited by Williams J. C., Thompson H. A. Boca Raton, FL: CRC Press;
     [Google Scholar]
  40. Walsh A. G., Matewish M. J., Burrows L. L., Monteiro M. A., Perry M. B., Lam J. S. 2000; Lipopolysaccharide core phosphates are required for viability and intrinsic drug resistance in Pseudomonas aeruginosa . Mol Microbiol 35:718–727 [CrossRef]
     [Google Scholar]
  41. Willems H., Jaeger C., Baljer G. 1998; Physical and genetic map of the obligate intracellular bacterium Coxiella burnetii . J Bacteriol 180:3816–3822
     [Google Scholar]
  42. Williams J. C., Peacock M. G., McCaul T. F. 1981; Immunological and biological characterization of Coxiella burnetii , phases I and II, separated from host components. Infect Immun 32:840–851
     [Google Scholar]
  43. Winkler H. H. 1976; Rickettsial permeability: an ADP-ATP transport system. J Biol Chem 251:389–396
     [Google Scholar]
  44. Winkler H. H. 1986; Membrane transport in rickettsiae. Methods Enzymol 125:253–259
     [Google Scholar]
  45. Winkler H. H., Daugherty R., Hu F. 1999; Rickettsia prowazekii transports UMP and GMP, but not CMP, as building blocks for RNA synthesis. J Bacteriol 181:3238–3241
     [Google Scholar]
  46. Wisseman C. L. Jr, Fiset P., Ormsbee R. A. 1967; Interaction of rickettsiae and phagocytic host cells. V. Phagocytic and opsonic interactions of phase I and phase II Coxiella burnetii with normal and immune human leukocytes and antibodies. J Immunol 99:669–674
     [Google Scholar]
  47. Zuerner R. L., Thompson H. A. 1983; Protein synthesis by intact Coxiella burnetii cells. J Bacteriol 156:186–191
     [Google Scholar]
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Permeability of Coxiella burnetii to ribonucleosides
Microbiology 148, 2393 (2002); https://doi.org/10.1099/00221287-148-8-2393
/content/journal/micro/10.1099/00221287-148-8-2393
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