1887

Abstract

Haematophagous arthropods are the primary vectors in the transmission of , yet the molecular mechanisms mediating the rickettsial infection of arthropods remain elusive. This study utilized a biotinylated protein pull-down assay together with LC-MS/MS to identify interaction between histone H2B and . Co-immunoprecipitation of histone with rickettsial cell lysate demonstrated the association of H2B with proteins, including outer-membrane protein B (OmpB), a major rickettsial adhesin molecule. The rickettsial infection of tick ISE6 cells was reduced by approximately 25 % via RNA-mediated H2B-depletion or enzymic treatment of histones. The interaction of H2B with the rickettsial adhesin OmpB suggests a role for H2B in mediating internalization into ISE6 cells.

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2010-09-01
2024-12-14
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References

  1. Amsel A. D., Rathaus M., Kronman N., Cohen H. Y. 2008; Regulation of the proapoptotic factor Bax by Ku70-dependent deubiquitylation. Proc Natl Acad Sci U S A 105:5117–5122
    [Google Scholar]
  2. Anacker R. L., Mann R. E., Gonzales C. 1987; Reactivity of monoclonal antibodies to Rickettsia rickettsii with spotted fever and typhus group rickettsiae. J Clin Microbiol 25:167–171
    [Google Scholar]
  3. Baake M., Doenecke D., Albig W. 2001; Characterisation of nuclear localisation signals of the four human core histones. J Cell Biochem 81:333–346
    [Google Scholar]
  4. Behrens S., Maier R., de Cock H., Schmid F. X., Gross C. A. 2001; The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J 20:285–294
    [Google Scholar]
  5. Bolton S. J., Perry V. H. 1997; Histone H1; a neuronal protein that binds bacterial lipopolysaccharide. J Neurocytol 26:823–831
    [Google Scholar]
  6. Borun T. W., Scharff M. D., Robbins E. 1967; Rapidly labeled, polyribosome-associated RNA having the properties of histone messenger. Proc Natl Acad Sci U S A 58:1977–1983
    [Google Scholar]
  7. Coleman J. L., Gebbia J. A., Piesman J., Degen J. L., Bugge T. H., Benach J. L. 1997; Plasminogen is required for efficient dissemination of B. burgdorferi in ticks and for enhancement of spirochetemia in mice. Cell 89:1111–1119
    [Google Scholar]
  8. Das R., Burke T., Plow E. F. 2007; Histone H2B as a functionally important plasminogen receptor on macrophages. Blood 110:3763–3772
    [Google Scholar]
  9. de la Fuente J., Blouin E. F., Manzano-Roman R., Naranjo V., Almazan C., Perez de la Lastra J. M., Zivkovic Z., Jongejan F., Kocan K. M. 2007; Functional genomic studies of tick cells in response to infection with the cattle pathogen, Anaplasma marginale. Genomics 90:712–722
    [Google Scholar]
  10. Emelyanov V. V., Demyanova N. G. 1999; Nucleotide sequence of the gene and features of the major outer membrane protein of a virulent Rickettsia prowazekii strain. Biochemistry (Mosc 64:494–503
    [Google Scholar]
  11. Featherstone C., Jackson S. P. 1999; Ku, a DNA repair protein with multiple cellular functions?. Mutat Res 434:3–15
    [Google Scholar]
  12. Gasteiger E., Hoogland C., Gattiker A., Duvaud S., Wilkins M. R., Appel R. D., Bairoch A. 2005 Protein identification and analysis tools on the ExPASY serverThe Proteomics Protocols Handbook pp 571–607 Edited by Walker J. M. Totowa, NJ: Humana Press;
    [Google Scholar]
  13. Hackstadt T. 1996; The biology of rickettsiae. Infect Agents Dis 5:127–143
    [Google Scholar]
  14. Heinzen R. A., Hayes S. F., Peacock M. G., Hackstadt T. 1993; Directional actin polymerization associated with spotted fever group rickettsia infection of Vero cells. Infect Immun 61:1926–1935
    [Google Scholar]
  15. Heinzen R. A., Grieshaber S. S., Van Kirk L. S., Devin C. J. 1999; Dynamics of actin-based movement by Rickettsia rickettsii in Vero cells. Infect Immun 67:4201–4207
    [Google Scholar]
  16. Herren T., Burke T. A., Das R., Plow E. F. 2006; Identification of histone H2B as a regulated plasminogen receptor. Biochemistry 45:9463–9474
    [Google Scholar]
  17. Holers V. M., Kotzin B. L. 1985; Human peripheral blood monocytes display surface antigens recognized by monoclonal antinuclear antibodies. J Clin Invest 76:991–998
    [Google Scholar]
  18. Kedes L. H. 1979; Histone genes and histone messengers. Annu Rev Biochem 48:837–870
    [Google Scholar]
  19. Khan I. U., Wallin R., Gupta R. S., Kammer G. M. 1998; Protein kinase A-catalyzed phosphorylation of heat shock protein 60 chaperone regulates its attachment to histone 2B in the T lymphocyte plasma membrane. Proc Natl Acad Sci U S A 95:10425–10430
    [Google Scholar]
  20. Kurtti T. J., Mattila J. T., Herron M. J., Felsheim R. F., Baldridge G. D., Burkhardt N. Y., Blazar B. R., Hackett P. B., Meyer J. M., Munderloh U. G. 2008; Transgene expression and silencing in a tick cell line: a model system for functional tick genomics. Insect Biochem Mol Biol 38:963–968
    [Google Scholar]
  21. Li H., Walker D. H. 1998; rOmpA is a critical protein for the adhesion of Rickettsia rickettsii to host cells. Microb Pathog 24:289–298
    [Google Scholar]
  22. Lundemose A. G., Kay J. E., Pearce J. H. 1993; Chlamydia trachomatis Mip-like protein has peptidyl-prolyl cis/trans isomerase activity that is inhibited by FK506 and rapamycin and is implicated in initiation of chlamydial infection. Mol Microbiol 7:777–783
    [Google Scholar]
  23. Macaluso K. R., Mulenga A., Simser J. A., Azad A. F. 2003; Differential expression of genes in uninfected and Rickettsia-infected Dermacentor variabilis ticks as assessed by differential-display PCR. Infect Immun 71:6165–6170
    [Google Scholar]
  24. Macaluso K. R., Mulenga A., Simser J. A., Azad A. F. 2006; Characterization of Dermacentor variabilis molecules associated with rickettsial infection. Ann N Y Acad Sci 1078:384–388
    [Google Scholar]
  25. Martinez J. J., Cossart P. 2004; Early signaling events involved in the entry of Rickettsia conorii into mammalian cells. J Cell Sci 117:5097–5106
    [Google Scholar]
  26. Martinez J. J., Seveau S., Veiga E., Matsuyama S., Cossart P. 2005; Ku70, a component of DNA-dependent protein kinase, is a mammalian receptor for Rickettsia conorii. Cell 123:1013–1023
    [Google Scholar]
  27. Marzluff W. F., Duronio R. J. 2002; Histone mRNA expression: multiple levels of cell cycle regulation and important developmental consequences. Curr Opin Cell Biol 14:692–699
    [Google Scholar]
  28. Miles L. A., Dahlberg C. M., Plescia J., Felez J., Kato K., Plow E. F. 1991; Role of cell-surface lysines in plasminogen binding to cells: identification of alpha-enolase as a candidate plasminogen receptor. Biochemistry 30:1682–1691
    [Google Scholar]
  29. Mulenga A., Macaluso K. R., Simser J. A., Azad A. F. 2003; Dynamics of Rickettsia–tick interactions: identification and characterization of differentially expressed mRNAs in uninfected and infected Dermacentor variabilis. Insect Mol Biol 12:185–193
    [Google Scholar]
  30. Munderloh U. G., Kurtti T. J. 1989; Formulation of medium for tick cell culture. Exp Appl Acarol 7:219–229
    [Google Scholar]
  31. Munderloh U. G., Kurtti T. J. 1995; Cellular and molecular interrelationships between ticks and prokaryotic tick-borne pathogens. Annu Rev Entomol 40:221–243
    [Google Scholar]
  32. Poinsot D., Charlat S., Mercot H. 2003; On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confronting the models with the facts. Bioessays 25:259–265
    [Google Scholar]
  33. Pornwiroon W., Pourciau S. S., Foil L. D., Macaluso K. R. 2006; Rickettsia felis from cat fleas: isolation and culture in a tick-derived cell line. Appl Environ Microbiol 72:5589–5595
    [Google Scholar]
  34. Pornwiroon W., Bourchookarn A., Paddock C. D., Macaluso K. R. 2009; Proteomic analysis of Rickettsia parkeri strain portsmouth. Infect Immun 77:5262–5271
    [Google Scholar]
  35. Prabhakar B. S., Allaway G. P., Srinivasappa J., Notkins A. L. 1990; Cell surface expression of the 70-kD component of Ku, a DNA-binding nuclear autoantigen. J Clin Invest 86:1301–1305
    [Google Scholar]
  36. Qiu H., Wang Y. 2008; Quantitative analysis of surface plasma membrane proteins of primary and metastatic melanoma cells. J Proteome Res 7:1904–1915
    [Google Scholar]
  37. Ramakrishnan V. G., Aljamali M. N., Sauer J. R., Essenberg R. C. 2005; Application of RNA interference in tick salivary gland research. J Biomol Tech 16:297–305
    [Google Scholar]
  38. Reif K. E., Macaluso K. R. 2009; Ecology of Rickettsia felis: a review. J Med Entomol 46:723–736
    [Google Scholar]
  39. Rossmann E., Kraiczy P., Herzberger P., Skerka C., Kirschfink M., Simon M. M., Zipfel P. F., Wallich R. 2007; Dual binding specificity of a Borrelia hermsii-associated complement regulator-acquiring surface protein for factor H and plasminogen discloses a putative virulence factor of relapsing fever spirochetes. J Immunol 178:7292–7301
    [Google Scholar]
  40. Silverman D. J., Wisseman C. L. Jr 1979; In vitro studies of rickettsia–host cell interactions: ultrastructural changes induced by Rickettsia rickettsii infection of chicken embryo fibroblasts. Infect Immun 26:714–727
    [Google Scholar]
  41. Simser J. A., Mulenga A., Macaluso K. R., Azad A. F. 2004; An immune responsive factor D-like serine proteinase homologue identified from the American dog tick, Dermacentor variabilis. Insect Mol Biol 13:25–35
    [Google Scholar]
  42. Sunyakumthorn P., Bourchookarn A., Pornwiroon W., David C., Barker S. A., Macaluso K. R. 2008; Characterization and growth of polymorphic Rickettsia felis in a tick cell line. Appl Environ Microbiol 74:3151–3158
    [Google Scholar]
  43. Tai Y. T., Podar K., Kraeft S. K., Wang F., Young G., Lin B., Gupta D., Chen L. B., Anderson K. C. 2002; Translocation of Ku86/Ku70 to the multiple myeloma cell membrane: functional implications. Exp Hematol 30:212–220
    [Google Scholar]
  44. Uchiyama T., Kawano H., Kusuhara Y. 2006; The major outer membrane protein rOmpB of spotted fever group rickettsiae functions in the rickettsial adherence to and invasion of Vero cells. Microbes Infect 8:801–809
    [Google Scholar]
  45. Watson K., Gooderham N. J., Davies D. S., Edwards R. J. 1999; Nucleosomes bind to cell surface proteoglycans. J Biol Chem 274:21707–21713
    [Google Scholar]
  46. Weiss E. 1982; The biology of rickettsiae. Annu Rev Microbiol 36:345–370
    [Google Scholar]
  47. Whitworth T., Popov V. L., Yu X. J., Walker D. H., Bouyer D. H. 2005; Expression of the Rickettsia prowazekii pld or tlyC gene in Salmonella enterica serovar Typhimurium mediates phagosomal escape. Infect Immun 73:6668–6673
    [Google Scholar]
  48. Zanettii A. S., Pornwiroon W., Kearney M. T., Macaluso K. R. 2008; Characterization of rickettsial infection in Amblyomma americanum (Acari: Ixodidae) by quantitative real-time polymerase chain reaction. J Med Entomol 45:267–275
    [Google Scholar]
  49. Zavala-Castro J. E., Small M., Keng C., Bouyer D. H., Zavala-Velazquez J., Walker D. H. 2005; Transcription of the Rickettsia felis ompA gene in naturally infected fleas. Am J Trop Med Hyg 73:662–666
    [Google Scholar]
  50. Zhu G., Chen H., Choi B. K., Del P. F., Schifferli D. M. 2005; Histone H1 proteins act as receptors for the 987P fimbriae of enterotoxigenic Escherichia coli. J Biol Chem 280:23057–23065
    [Google Scholar]
  51. Zlatanova J. S., Srebreva L. N., Banchev T. B., Tasheva B. T., Tsanev R. G. 1990; Cytoplasmic pool of histone H1 in mammalian cells. J Cell Sci 96:461–468
    [Google Scholar]
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