1887

Microbiology Society logo

Volume 153, Issue 2

Chlamydial SET domain protein functions as a histone methyltransferase Free

Abstract

SET domain genes have been identified in numbers of bacterial genomes based on similarity to SET domains of eukaryotic histone methyltransferases. Herein, a SET domain gene was clarified to be coincidently expressed with and genes encoding chlamydial histone H1-like proteins, Hc1 and Hc2, respectively. The SET domain protein (cpnSET) is localized in chlamydial cells and interacts with Hc1 and Hc2 through the C-terminal SET domain. As expected from conservation of catalytic sites in cpnSET, it functions as a protein methyltransferase to murine histone H3 and Hc1. However, little is known about protein methylation in the molecular pathogenesis of chlamydial infection. cpnSET may play an important role in chlamydial cell maturation due to modification of chlamydial histone H1-like proteins.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): cpnSET, Chlamydophila pneumoniae SET domain protein , EB, elementary body , FCS, fetal calf serum , GST, glutathione S-transferase , h.p.i., hours post-infection and RB, reticulate body
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.29213-0
2007-02-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/2/585.html?itemId=/content/journal/micro/10.1099/mic.0.29213-0&mimeType=html&fmt=ahah

References

  1. Alvarez-Venegas R., Avramova Z. 2002; SET-domain proteins of the Su(var)3-9, E(z) and Trithorax families. Gene 285:25–37 [CrossRef]
     [Google Scholar]
  2. Azuma Y., Yamagishi M., Ishihama A. 1993; Subunits of the Schizosaccharomyces pombe RNA polymerase II: enzyme purification and structure of the subunit 3 gene. Nucleic Acids Res 21:3749–3754 [CrossRef]
     [Google Scholar]
  3. Azuma Y., Tabb M. M., Vu L., Nomura M. 1995; Isolation of a yeast protein kinase that is activated by the protein encoded by SRP1 (Srp1p) and phosphorylates Srp1p complexed with nuclear localization signal peptides. Proc Natl Acad Sci U S A 92:5159–5163 [CrossRef]
     [Google Scholar]
  4. Azuma Y., Hirakawa H., Yamashita A., Cai Y., Rahman M. A., Suzuki H., Mitaku S., Toh H., Goto S. other authors 2006; Genome sequence of the cat pathogen, Chlamydophila felis . DNA Res 13:15–23 [CrossRef]
     [Google Scholar]
  5. Barry C. E., Hayes S. F., Hackstadt T. 1992; Nucleoid condensation in Escherichia coli that express a chlamydial histone homolog. Science 256:377–379 [CrossRef]
     [Google Scholar]
  6. Beatty W. L., Byrne G. I., Morrison R. P. 1993; Morphologic and antigenic characterization of interferon gamma-mediated persistent Chlamydia trachomatis infection in vitro. Proc Natl Acad Sci U S A 90:3998–4002 [CrossRef]
     [Google Scholar]
  7. Belland R. J., Nelson D. E., Virok D., Crane D. D., Hogan D., Sturdevant D., Beatty W. L., Caldwell H. D. 2003; Transcriptome analysis of chlamydial growth during IFN-gamma-mediated persistence and reactivation. Proc Natl Acad Sci U S A 100:15971–15976 [CrossRef]
     [Google Scholar]
  8. Byrne G. I., Ouellette S. P., Wang Z., Rao J. P., Lu L., Beatty W. L., Hudson A. P. 2001; Chlamydia pneumoniae expresses genes required for DNA replication but not cytokinesis during persistent infection of HEp-2 cells. Infect Immun 69:5423–5429 [CrossRef]
     [Google Scholar]
  9. Carlson J. H., Porcella S. F., McClarty G., Caldwell H. D. 2005; Comparative genomic analysis of Chlamydia trachomatis oculotropic and genitotropic strains. Infect Immun 73:6407–6418 [CrossRef]
     [Google Scholar]
  10. Dillon S. C., Zhang X., Trievel R. C., Cheng X. 2005; The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol 6:227 [CrossRef]
     [Google Scholar]
  11. Eswar N., John B., Mirkovic N., Fiser A., Ilyin V. A., Pieper U., Stuart A. C., Marti-Renom M. A., Madhusudhan M. S. other authors 2003; Tools for comparative protein structure modeling and analysis. Nucleic Acids Res 31:3375–3380 [CrossRef]
     [Google Scholar]
  12. Fahr M. J., Douglas A. L., Xia W., Hatch T. P. 1995; Characterization of late gene promoters of Chlamydia trachomatis . J Bacteriol 177:4252–4260
     [Google Scholar]
  13. Grieshaber N. A., Grieshaber S. S., Fischer E. R., Hackstadt T. 2006; A small RNA inhibits translation of the histone-like protein Hc1 in Chlamydia trachomatis . Mol Microbiol 59:541–550 [CrossRef]
     [Google Scholar]
  14. Hackstadt T., Baehr W., Ying Y. 1991; Chlamydia trachomatis developmentally regulated protein is homologous to eukaryotic histone H1. Proc Natl Acad Sci U S A 88:3937–3941 [CrossRef]
     [Google Scholar]
  15. Hahn D. L., Dodge R. W., Golubjatnikov R. 1991; Association of Chlamydia pneumoniae (strain TWAR) infection with wheezing, asthmatic bronchitis, and adult-onset asthma. JAMA 266:225–230 [CrossRef]
     [Google Scholar]
  16. Itzhaki R. F., Wozniak M. A., Appelt D. M., Balin B. J. 2004; Infiltration of the brain by pathogens causes Alzheimer's disease. Neurobiol Aging 25:619–627 [CrossRef]
     [Google Scholar]
  17. Jones S. R., Gelbart W. M. 1993; The drosophila polycomb-group gene enhancer of zeste contains a region with sequence similarity to trithorax. Mol Cell Biol 13:6357–6366
     [Google Scholar]
  18. Kalman S., Mitchell W., Marathe R., Lammel C., Fan J., Hyman R. W., Olinger L., Grimwood J., Davis R. W., Stephens R. S. 1999; Comparative genomes of Chlamydia pneumoniae and C. trachomatis . Nat Genet 21:385–389 [CrossRef]
     [Google Scholar]
  19. Kouzarides T. 2002; Histone methylation in transcriptional control. Curr Opin Genet Dev 12:198–209 [CrossRef]
     [Google Scholar]
  20. Kuzmichev A., Margueron R., Vaquero A., Preissner T. S., Scher M., Kirmizis A., Ouyang X., Brockdorff N., Abate-Shen C. other authors 2005; Composition and histone substrate of polycomb repressive group complexes change during cellular differentiation. Proc Natl Acad Sci U S A 102:1859–1864 [CrossRef]
     [Google Scholar]
  21. Liu H. Y., Badarinarayana V., Audino D. C., Rappsilber J., Mann M., Denis C. L. 1998; The NOT proteins are part of the CCR4 transcriptional complex and affect gene expression both positively and negatively. EMBO J 17:1096–1106 [CrossRef]
     [Google Scholar]
  22. Malinverni R., Kuo C. C., Campbell L. A., Grayston J. T. 1995; Reactivation of Chlamydia pneumoniae lung infection in mice by cortisone. J Infect Dis 172:593–594 [CrossRef]
     [Google Scholar]
  23. Manzur K. L., Zhou M. M. 2005; An archaeal SET domain protein exhibits distinct lysine methyltransferase activity towards DNA-associated protein MC1-alpha. FEBS Let 579:3859–3865 [CrossRef]
     [Google Scholar]
  24. Manzur K. L., Farooq A., Zeng L., Plotnikova O., Koch A. W., Sachchidanand, Zhou M. M. 2003; A dimeric viral SET domain methyltransferase specific to Lys27 of histone H3. Nat Struct Biol 10:187–196 [CrossRef]
     [Google Scholar]
  25. Marmorstein R. 2003; Structure of SET domain proteins: a new twist on histone methylation. Trends Biochem Sci 28:59–62 [CrossRef]
     [Google Scholar]
  26. Mehta S. J., Miller R. D., Ramirez J. A., Summersgill J. T. 1998; Inhibition of Chlamydia pneumoniae replication in HEp-2 cells by interferon-gamma: role of tryptophan catabolism. J Infect Dis 177:1326–1331 [CrossRef]
     [Google Scholar]
  27. Miura K., Inouye S., Sakai K., Takaoka H., Kishi F., Tabuchi M., Tanaka T., Matsumoto H., Shirai M. other authors 2001; Cloning and characterization of adenylate kinase from Chlamydia pneumoniae . J Biol Chem 276:13490–13498 [CrossRef]
     [Google Scholar]
  28. Morris G. M., Goodsell D. S., Huey R., Olson A. J. 1996; Distributed automated docking of flexible ligands to proteins: parallel applications of AutoDock 2.4. J Comput Aided Mol Des 10:293–304 [CrossRef]
     [Google Scholar]
  29. Perara E., Ganem D., Engel J. N. 1992; A developmentally regulated chlamydial gene with apparent homology to eukaryotic histone H1. Proc Natl Acad Sci U S A 89:2125–2129 [CrossRef]
     [Google Scholar]
  30. Rahman M. A., Azuma Y., Fukunaga H., Murakami T., Sugi K., Fukushi H., Miura K., Suzuki H., Shirai M. 2005; Serotonin and melatonin, neurohormones for homeostasis, as novel inhibitors of infections by the intracellular parasite Chlamydia . J Antimicrob Chemother 56:861–868 [CrossRef]
     [Google Scholar]
  31. Read T. D., Brunham R. C., Shen C., Gill S. R., Heidelberg J. F., White O., Hickey E. K., Peterson J., Utterback T. other authors 2000; Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res 28:1397–1406 [CrossRef]
     [Google Scholar]
  32. Read T. D., Myers G. S. A., Brunham R. C., Nelson W. C., Paulsen I. T., Heidelberg J., Holtzapple E., Khouri H., Federova N. B. other authors 2003; Genome sequence of Chlamydophila caviae ( Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae . Nucleic Acids Res 31:2134–2147 [CrossRef]
     [Google Scholar]
  33. Rosenfeld M. E., Blessing E., Lin T. M., Moazed T. C., Campbell L. A., Kuo C. 2000; Chlamydia , inflammation, and atherogenesis. J Infect Dis 181 Suppl 3:S492–S497
     [Google Scholar]
  34. Shirai M., Hirakawa H., Kimoto M., Tabuchi M., Kishi F., Ouchi K., Shiba T., Ishii K., Hattori M. other authors 2000; Comparison of whole genome sequences of Chlamydia pneumoniae J138 from Japan and CWL029 from USA. Nucleic Acids Res 28:2311–2314 [CrossRef]
     [Google Scholar]
  35. Slepenkin A., Motin V., Peterson E. M., de la Maza L. M. 2003; Temporal expression of Type III secretion genes of Chlamydia pneumoniae . Infect Immun 71:2555–2562 [CrossRef]
     [Google Scholar]
  36. Stephens R. S., Kalma S., Lammel C., Fan J., Marathe R., Aravind L., Mitchell W., Olinger L., Tatusov R. L. other authors 1998; Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis . Science 282:754–759 [CrossRef]
     [Google Scholar]
  37. Tachibana M., Sugimoto K., Fukushima T., Shinkai Y. 2001; SET-domain containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J Biol Chem 276:25309–25317 [CrossRef]
     [Google Scholar]
  38. Tao S., Kaul R., Wenman W. M. 1991; Identification and nucleotide sequence of a developmentally regulated gene encoding a eukaryotic histone H1-like protein from Chlamydia trachomatis . J Bacteriol 173:2818–2822
     [Google Scholar]
  39. Thomson N. R., Yeats C., Bell K., Holden M. T., Bentley S. D., Livingstone M., Cerdeno-Tarrago A. M., Harris B., Doggett J. other authors 2005; The Chlamydophila abortus genome sequence reveals an array of variable proteins that contribute to interspecies variation. Genome Res 15:629–640 [CrossRef]
     [Google Scholar]
  40. Xiao B., Wilson J. R., Gamblin S. J. 2003; SET domains and histone methylation. Curr Opin Struct Biol 13:699–705 [CrossRef]
     [Google Scholar]
  41. Zhang X., Yang Z., Khan S. I., Horton J. R., Tamaru H., Selker E. U., Cheng X. 2003; Structural basis for the product specificity of histone lysine methyltransferases. Mol Cell 12:177–185 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.29213-0
Loading
Chlamydial SET domain protein functions as a histone methyltransferase
Microbiology 153, 585 (2007); https://doi.org/10.1099/mic.0.29213-0
/content/journal/micro/10.1099/mic.0.29213-0
/content/journal/micro/10.1099/mic.0.29213-0
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