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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.041400-0
2010-09-01
2020-09-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/9/2855.html?itemId=/content/journal/micro/10.1099/mic.0.041400-0&mimeType=html&fmt=ahah

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 A105:5117–5122
    [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 Microbiol25:167–171
    [Google Scholar]
  3. Baake M., Doenecke D., Albig W.. 2001; Characterisation of nuclear localisation signals of the four human core histones. J Cell Biochem81:333–346
    [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 J20:285–294
    [Google Scholar]
  5. Bolton S. J., Perry V. H.. 1997; Histone H1; a neuronal protein that binds bacterial lipopolysaccharide. J Neurocytol26:823–831
    [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 A58:1977–1983
    [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. Cell89:1111–1119
    [Google Scholar]
  8. Das R., Burke T., Plow E. F.. 2007; Histone H2B as a functionally important plasminogen receptor on macrophages. Blood110:3763–3772
    [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. Genomics90:712–722
    [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 (Mosc64:494–503
    [Google Scholar]
  11. Featherstone C., Jackson S. P.. 1999; Ku, a DNA repair protein with multiple cellular functions?. Mutat Res434:3–15
    [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 pp571–607 Edited by Walker J. M.. Totowa, NJ: Humana Press;
    [Google Scholar]
  13. Hackstadt T.. 1996; The biology of rickettsiae. Infect Agents Dis5:127–143
    [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 Immun61:1926–1935
    [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 Immun67:4201–4207
    [Google Scholar]
  16. Herren T., Burke T. A., Das R., Plow E. F.. 2006; Identification of histone H2B as a regulated plasminogen receptor. Biochemistry45:9463–9474
    [Google Scholar]
  17. Holers V. M., Kotzin B. L.. 1985; Human peripheral blood monocytes display surface antigens recognized by monoclonal antinuclear antibodies. J Clin Invest76:991–998
    [Google Scholar]
  18. Kedes L. H.. 1979; Histone genes and histone messengers. Annu Rev Biochem48:837–870
    [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 A95:10425–10430
    [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 Biol38:963–968
    [Google Scholar]
  21. Li H., Walker D. H.. 1998; rOmpA is a critical protein for the adhesion of Rickettsia rickettsii to host cells. Microb Pathog24:289–298
    [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 Microbiol7:777–783
    [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 Immun71:6165–6170
    [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 Sci1078:384–388
    [Google Scholar]
  25. Martinez J. J., Cossart P.. 2004; Early signaling events involved in the entry of Rickettsia conorii into mammalian cells. J Cell Sci117:5097–5106
    [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. Cell123:1013–1023
    [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 Biol14:692–699
    [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. Biochemistry30:1682–1691
    [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 Biol12:185–193
    [Google Scholar]
  30. Munderloh U. G., Kurtti T. J.. 1989; Formulation of medium for tick cell culture. Exp Appl Acarol7:219–229
    [Google Scholar]
  31. Munderloh U. G., Kurtti T. J.. 1995; Cellular and molecular interrelationships between ticks and prokaryotic tick-borne pathogens. Annu Rev Entomol40:221–243
    [Google Scholar]
  32. Poinsot D., Charlat S., Mercot H.. 2003; On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confronting the models with the facts. Bioessays25:259–265
    [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 Microbiol72:5589–5595
    [Google Scholar]
  34. Pornwiroon W., Bourchookarn A., Paddock C. D., Macaluso K. R.. 2009; Proteomic analysis of Rickettsia parkeri strain portsmouth. Infect Immun77:5262–5271
    [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 Invest86:1301–1305
    [Google Scholar]
  36. Qiu H., Wang Y.. 2008; Quantitative analysis of surface plasma membrane proteins of primary and metastatic melanoma cells. J Proteome Res7:1904–1915
    [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 Tech16:297–305
    [Google Scholar]
  38. Reif K. E., Macaluso K. R.. 2009; Ecology of Rickettsia felis: a review. J Med Entomol46:723–736
    [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 Immunol178:7292–7301
    [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 Immun26:714–727
    [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 Biol13:25–35
    [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 Microbiol74:3151–3158
    [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 Hematol30:212–220
    [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 Infect8:801–809
    [Google Scholar]
  45. Watson K., Gooderham N. J., Davies D. S., Edwards R. J.. 1999; Nucleosomes bind to cell surface proteoglycans. J Biol Chem274:21707–21713
    [Google Scholar]
  46. Weiss E.. 1982; The biology of rickettsiae. Annu Rev Microbiol36:345–370
    [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 Immun73:6668–6673
    [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 Entomol45:267–275
    [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 Hyg73:662–666
    [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 Chem280:23057–23065
    [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 Sci96:461–468
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.041400-0
Loading
/content/journal/micro/10.1099/mic.0.041400-0
Loading

Data & Media loading...

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