Ehrlichia chaffeensis TRP120 binds a G+C-rich motif in host cell DNA and exhibits eukaryotic transcriptional activator function

Infection and Immunity

Volumn 79, Issue 11, 2011, Pages 4370-4381

  Zhu, Bing ^a   Kuriakose, Jeeba A ^a   Luo, Tian ^a   Ballesteros, Efren ^c   Gupta, Sharu ^c   Fofanov, Yuriy ^c   McBride, Jere W ^a,b  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

^c UNIVERSITY OF HOUSTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL11 CHEMOKINE; DNA BINDING PROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; TANDEM REPEAT PROTEIN 120; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BACTERIUM CULTURE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; DNA BINDING; DNA SEQUENCE; EHRLICHIA CHAFFEENSIS; GENE CONTROL; GENE TARGETING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HOST CELL; INTRACELLULAR BACTERIUM; MONONUCLEAR PHAGOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; TANDEM REPEAT; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION; WESTERN BLOTTING;

ANTIBODIES, BACTERIAL; BACTERIAL PROTEINS; BASE COMPOSITION; BASE SEQUENCE; BINDING SITES; CELL LINE; DNA; EHRLICHIA CHAFFEENSIS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; PROTEIN BINDING; REPRODUCIBILITY OF RESULTS; TRANS-ACTIVATORS;

EID: 80052480067     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05422-11     Document Type: Article

References (69)

1. Al-Shahrour, F., et al. 2007. FatiGO+: a functional profiling tool for genomic data. Integration of functional annotation, regulatory motifs and interaction data with microarray experiments. Nucleic Acids Res. 35:W91-W96.
2. Al-Shahrour, F., et al. 2006. BABELOMICS: a systems biology perspective in the functional annotation of genome-scale experiments. Nucleic Acids Res. 34:W472-W476.
3. Arbibe, L. 2008. Immune subversion by chromatin manipulation: a 'new face' of host-bacterial pathogen interaction. Cell. Microbiol. 10:1582-1590.
4. Bailey, T. L., and C. Elkan. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2:28-36.
5. Bolton, E. C., et al. 2007. Cell- and gene-specific regulation of primary target genes by the androgen receptor. Genes Dev. 21:2005-2017.
6. Carroll, J. S., et al. 2005. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122:33-43.
7. Chong, H. K., et al. 2010. Genome-wide interrogation of hepatic FXR reveals an asymmetric IR-1 motif and synergy with LRH-1. Nucleic Acids Res. 38:6007-6017.
8. Chow, B. K., V. Ting, F. Tufaro, and R. T. MacGillivray. 1991. Characterization of a novel liver-specific enhancer in the human prothrombin gene. J. Biol. Chem. 266:18927-18933.
9. Citti, C., M. F. Kim, and K. S. Wise. 1997. Elongated versions of Vlp surface lipoproteins protect Mycoplasma hyorhinis escape variants from growthinhibiting host antibodies. Infect. Immun. 65:1773-1785.
10. Clifton, D. R., et al. 2005. Tyrosine phosphorylation of the chlamydial effector protein Tarp is species specific and not required for recruitment of actin. Infect. Immun. 73:3860-3868.
11. Collins, N. E., et al. 2005. The genome of the heartwater agent Ehrlichia ruminantium contains multiple tandem repeats of actively variable copy number. Proc. Natl. Acad. Sci. U. S. A. 102:838-843.
12. Courtois, G., J. G. Morgan, L. A. Campbell, G. Fourel, and G. R. Crabtree. 1987. Interaction of a liver-specific nuclear factor with the fibrinogen and alpha 1-antitrypsin promoters. Science 238:688-692.
13. Doyle, C. K., K. A. Nethery, V. L. Popov, and J. W. McBride. 2006. Differentially expressed and secreted major immunoreactive protein orthologs of Ehrlichia canis and E. chaffeensis elicit early antibody responses to epitopes on glycosylated tandem repeats. Infect. Immun. 74:711-720.
14. Duverger, E., V. Carpentier, A. C. Roche, and M. Monsigny. 1993. Sugardependent nuclear import of glycoconjugates from the cytosol. Exp. Cell Res. 207:197-201.
15. Duverger, E., C. Pellerin-Mendes, R. Mayer, A. C. Roche, and M. Monsigny. 1995. Nuclear import of glycoconjugates is distinct from the classical NLS pathway. J. Cell Sci. 108(Pt 4):1325-1332.
16. Gardella, S., et al. 2002. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep. 3:995-1001.
17. Gravekamp, C., D. S. Horensky, J. L. Michel, and L. C. Madoff. 1996. Variation in repeat number within the alpha C protein of group B streptococci alters antigenicity and protective epitopes. Infect. Immun. 64:3576-3583.
18. Gupta, S., J. A. Stamatoyannopoulos, T. L. Bailey, and W. S. Noble. 2007. Quantifying similarity between motifs. Genome Biol. 8:R24.
19. Gurlebeck, D., B. Szurek, and U. Bonas. 2005. Dimerization of the bacterial effector protein AvrBs3 in the plant cell cytoplasm prior to nuclear import. Plant J. 42:175-187.
20. Gurlebeck, D., F. Thieme, and U. Bonas. 2006. Type III effector proteins from the plant pathogen Xanthomonas and their role in the interaction with the host plant. J. Plant Physiol. 163:233-255.
21. Hardon, E. M., M. Frain, G. Paonessa, and R. Cortese. 1988. Two distinct factors interact with the promoter regions of several liver-specific genes. EMBO J. 7:1711-1719.
22. Heuer, H., Y. N. Yin, Q. Y. Xue, K. Smalla, and J. H. Guo. 2007. Repeat domain diversity of avrBs3-like genes in Ralstonia solanacearum strains and association with host preferences in the field. Appl. Environ. Microbiol. 73:4379-4384.
23. Huang, B., et al. 2010. Anaplasma phagocytophilum APH_1387 is expressed throughout bacterial intracellular development and localizes to the pathogen-occupied vacuolar membrane. Infect. Immun. 78:1864-1873.
24. Impey, S., et al. 2004. Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell 119:1041-1054.
25. Johnson, D. S., A. Mortazavi, R. M. Myers, and B. Wold. 2007. Genomewide mapping of in vivo protein-DNA interactions. Science 316:1497-1502.
26. Kay, S., S. Hahn, E. Marois, R. Wieduwild, and U. Bonas. 2009. Detailed analysis of the DNA recognition motifs of the Xanthomonas type III effectors AvrBs3 and AvrBs3Deltarep16. Plant J. 59:859-871.
27. Kouwenhoven, E. N., et al. 2010. Genome-wide profiling of p63 DNAbinding sites identifies an element that regulates gene expression during limb development in the 7q21 SHFM1 locus. PLoS Genet. 6:e1001065.
28. Kumagai, Y., J. Matsuo, Y. Hayakawa, and Y. Rikihisa. 2010. Cyclic di-GMP signaling regulates invasion by Ehrlichia chaffeensis of human monocytes. J. Bacteriol. 192:4122-4133.
29. Kuwahara, J., A. Yonezawa, M. Futamura, and Y. Sugiura. 1993. Binding of transcription factor Sp1 to GC box DNA revealed by footprinting analysis: different contact of three zinc fingers and sequence recognition mode. Biochemistry 32:5994-6001.
30. Lee, E. H., and Y. Rikihisa. 1998. Protein kinase A-mediated inhibition of gamma interferon-induced tyrosine phosphorylation of Janus kinases and latent cytoplasmic transcription factors in human monocytes by Ehrlichia chaffeensis. Infect. Immun. 66:2514-2520.
31. Lefterova, M. I., et al. 2008. PPARgamma and C/EBP factors orchestrate adipocyte biology via adjacent binding on a genome-wide scale. Genes Dev. 22:2941-2952.
32. Li, X. Y., et al. 2008. Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol. 6:e27.
33. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402-408.
34. Luo, T., J. A. Kuriakose, B. Zhu, A. Wakeel, and J. W. McBride. 2011. Ehrlichia chaffeensis TRP120 interacts with a diverse array of eukaryotic proteins involved in transcription, signaling, and cytoskeleton organization. Infect. Immun. 79:4382-4391.
35. Luo, T., X. Zhang, and J. W. McBride. 2009. Major species-specific antibody epitopes of the Ehrlichia chaffeensis p120 and E. canis p140 orthologs in surface-exposed tandem repeat regions. Clin. Vaccine Immunol. 16:982-990.
36. Luo, T., X. Zhang, A. Wakeel, V. L. Popov, and J. W. McBride. 2008. A variable-length PCR target protein of Ehrlichia chaffeensis contains major species-specific antibody epitopes in acidic serine-rich tandem repeats. Infect. Immun. 76:1572-1580.
37. Luster, A. D. 1998. Chemokines-chemotactic cytokines that mediate inflammation. N. Engl. J. Med. 338:436-445.
38. MacIsaac, K. D., et al. 2010. A quantitative model of transcriptional regulation reveals the influence of binding location on expression. PLoS Comput. Biol. 6:e1000773.
39. Matthew, J., et al. 2009. Distribution and seasonality of rhinovirus and other respiratory viruses in a cross-section of asthmatic children in Trinidad, West Indies. Ital. J. Pediatr. 35:16.
40. McBride, J. W., L. M. Ndip, V. L. Popov, and D. H. Walker. 2002. Identification and functional analysis of an immunoreactive DsbA-like thio-disulfide oxidoreductase of Ehrlichia spp. Infect. Immun. 70:2700-2703.
41. McBride, J. W., and D. H. Walker. 2011. Molecular and cellular pathobiology of Ehrlichia infection: targets for new therapeutics and immunomodulation strategies. Expert Rev. Mol. Med. 13:e3.
42. Miura, K., and Y. Rikihisa. 2009. Liver transcriptome profiles associated with strain-specific Ehrlichia chaffeensis-induced hepatitis in SCID mice. Infect. Immun. 77:245-254.
43. Mukaihara, T., N. Tamura, and M. Iwabuchi. 2010. Genome-wide identification of a large repertoire of Ralstonia solanacearum type III effector proteins by a new functional screen. Mol. Plant Microbe Interact. 23:251-262.
44. Nerenz, R. D., M. L. Martowicz, and J. W. Pike. 2008. An enhancer 20 kilobases upstream of the human receptor activator of nuclear factor-kappaB ligand gene mediates dominant activation by 1,25-dihydroxyvitamin D3. Mol. Endocrinol. 22:1044-1056.
45. Nielsen, R., et al. 2008. Genome-wide profiling of PPARgamma:RXR and RNA polymerase II occupancy reveals temporal activation of distinct metabolic pathways and changes in RXR dimer composition during adipogenesis. Genes Dev. 22:2953-2967.
46. Nonaka, Y., et al. 2010. STPR, a 23-amino acid tandem repeat domain, found in the human function-unknown protein ZNF821. Biochemistry 49:8367-8375.
47. Popov, V. L., X. Yu, and D. H. Walker. 2000. The 120 kDa outer membrane protein of Ehrlichia chaffeensis: preferential expression on dense-core cells and gene expression in Escherichia coli associated with attachment and entry. Microb. Pathog. 28:71-80.
48. Ramagopalan, S. V., et al. 2010. A ChIP-seq defined genome-wide map of vitamin D receptor binding: associations with disease and evolution. Genome Res. 20:1352-1360.
49. Rikihisa, Y. 2006. Ehrlichia subversion of host innate responses. Curr. Opin. Microbiol. 9:95-101.
50. Robertson, G., et al. 2007. Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat. Methods 4:651-657.
51. Rollins, B. J. 1997. Chemokines. Blood 90:909-928.
52. Romer, P., et al. 2007. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318:645-648.
53. Romer, P., et al. 2009. Recognition of AvrBs3-like proteins is mediated by specific binding to promoters of matching pepper Bs3 alleles. Plant Physiol. 150:1697-1712.
54. Shak, J. R., J. J. Dick, R. J. Meinersmann, G. I. Perez-Perez, and M. J. Blaser. 2009. Repeat-associated plasticity in the Helicobacter pylori RD gene family. J. Bacteriol. 191:6900-6910.
55. Sozzani, S., A. Mantovani, and P. Allavena. 1999. Control of dendritic cell migration by chemokines. Forum (Genoa, Italy) 9:325-338.
56. Struhl, K. 1989. Helix-turn-helix, zinc-finger, and leucine-zipper motifs for eukaryotic transcriptional regulatory proteins. Trends Biochem. Sci. 14:137-140.
57. Takiya, S., et al. 2009. DNA-binding property of the novel DNA-binding domain STPR in FMBP-1 of the silkworm Bombyx mori. J. Biochem. 146: 103-111.
58. Tonjum, T., D. A. Caugant, S. A. Dunham, and M. Koomey. 1998. Structure and function of repetitive sequence elements associated with a highly polymorphic domain of the Neisseria meningitidis PilQ protein. Mol. Microbiol. 29:111-124.
59. Ushijima, R., et al. 2005. Extracellular signal-dependent nuclear import of STAT3 is mediated by various importin alphas. Biochem. Biophys. Res. Commun. 330:880-886.
60. Wakeel, A., J. A. Kuriakose, and J. W. McBride. 2009. An Ehrlichia chaffeensis tandem repeat protein interacts with multiple host targets involved in cell signaling, transcriptional regulation, and vesicle trafficking. Infect. Immun. 77:1734-1745.
61. Wakeel, A., B. Zhu, X. J. Yu, and J. W. McBride. 2010. New insights into molecular Ehrlichia chaffeensis-host interactions. Microbes Infect. 12:337-345.
62. Xiong, Q., W. Bao, Y. Ge, and Y. Rikihisa. 2008. Ehrlichia ewingii infection delays spontaneous neutrophil apoptosis through stabilization of mitochondria. J. Infect. Dis. 197:1110-1118.
63. Yeamans, C., et al. 2007. C/EBPalpha binds and activates the PU.1 distal enhancer to induce monocyte lineage commitment. Blood 110:3136-3142.
64. Yu, X. J., P. Crocquet-Valdes, L. C. Cullman, and D. H. Walker. 1996. The recombinant 120-kilodalton protein of Ehrlichia chaffeensis, a potential diagnostic tool. J. Clin. Microbiol. 34:2853-2855.
65. Yu, X. J., J. W. McBride, C. M. Diaz, and D. H. Walker. 2000. Molecular cloning and characterization of the 120-kilodalton protein gene of Ehrlichia canis and application of the recombinant 120-kilodalton protein for serodiagnosis of canine ehrlichiosis. J. Clin. Microbiol. 38:369-374.
66. Yu, X. J., J. W. McBride, and D. H. Walker. 2007. Restriction and expansion of Ehrlichia strain diversity. Vet. Parasitol. 143:337-346.
67. Zhang, J. Z., M. Sinha, B. A. Luxon, and X. J. Yu. 2004. Survival strategy of obligately intracellular Ehrlichia chaffeensis: novel modulation of immune response and host cell cycles. Infect. Immun. 72:498-507.
68. Zhang, Y., et al. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9:R137.
69. Zhu, B., et al. 2009. Nuclear translocated Ehrlichia chaffeensis ankyrin protein interacts with a specific adenine-rich motif of host promoter and intronic Alu elements. Infect. Immun. 77:4243-4255.