Effector bottleneck: Microbial reprogramming of parasitized host cell transcription by epigenetic remodeling of chromatin structure

Frontiers in Genetics

Volumn 5, Issue AUG, 2014, Pages

  Sinclair, Sara H ^a,b   Rennoll Bankert, Kristen E ^a,b   Dumler, J S ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Anaplasma phagocytophilum; Chromatin; DNA methylation; Epigenetics; Histone deacetylase; Nucleomodulin

Indexed keywords

ANKYRIN; EOSINOPHIL PEROXIDASE; FLOTILLIN 1; GUANOSINE TRIPHOSPHATASE; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; INTERLEUKIN 8; JANUS KINASE; MATRIX ATTACHMENT REGION BINDING PROTEIN; METHYLTRANSFERASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BCL 2; RAC2 PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; STAT PROTEIN; TUMOR NECROSIS FACTOR;

ANAPLASMA PHAGOCYTOPHILUM; ANAPLASMATACEAE; APOPTOSIS; CELL FUNCTION; CELLULAR STRESS SIGNAL; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CHROMOSOME 17; CHROMOSOME 6; CPG ISLAND; DNA METHYLATION; EHRLICHIA CHAFFEENSIS; EPIGENETIC REPRESSION; EPIGENETICS; GENE EXPRESSION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN GENOME; HUMAN GRANULOCYTIC ANAPLASMOSIS; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PARASITE TRANSMISSION; REVIEW; TANDEM REPEAT;

EID: 84906259458     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00274     Document Type: Review

References (68)

1. Akkoyunlu, M., Malawista, S. E., Anguita, J., and Fikrig, E. (2001). Exploitation of interleukin-8-induced neutrophil chemotaxis by the agent of human granulocytic ehrlichiosis. Infect. Immun. 69, 5577-5588. doi: 10.1128/IAI.69.9.5577-5588.2001
2. Arbibe, L., Kim, D. W., Batsche, E., Pedron, T., Mateescu, B., Muchardt, C.,et al. (2007). An injected bacterial effector targets chromatin access for transcription factor NF-κB to alter transcription of host genes involved in immune responses. Nat. Immunol. 8, 47-56. doi: 10.1038/ni1423
3. Arope, S., Harraghy, N., Pjanic, M., and Mermod, N. (2013). Molecular characterization of a human matrix attachment region epigenetic regulator. PLoS ONE 8:e79262. doi: 10.1371/journal.pone.0079262
4. Banerjee, R., Anguita, J., Roos, D., and Fikrig, E. (2000). Cutting edge: infection by the agent of human granulocytic ehrlichiosis prevents the respiratory burst by down-regulating gp91phox. J. Immunol. 164, 3946-3949. doi: 10.4049/jimmunol.164.8.3946
5. Baylin, S. B., Esteller, M., Rountree, M. R., Bachman, K. E., Schuebel, K., and Herman, J. G. (2001). Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum. Mol. Genet. 10, 687-692. doi: 10.1093/hmg/10.7.687
6. Baylin, S. B., and Herman, J. G. (2000). DNA hypermethylation in tumorigenesis: epigenetics joins genetics. Trends Genet. 16, 168-174. doi: 10.1016/S0168-9525(99)01971-X
7. Beyer, M., Thabet, Y., Muller, R. U., Sadlon, T., Classen, S., Lahl, K.,et al. (2011). Repression of the genome organizer SATB1 in regulatory T cells is required for suppressive function and inhibition of effector differentiation. Nat. Immunol. 12, 898-907. doi: 10.1038/ni.2084
8. Bierne, H., Hamon, M., and Cossart, P. (2012). Epigenetics and bacterial infections. Cold Spring Harb. Perspect. Med. 2:a010272. doi: 10.1101/cshperspect.a010272
9. Bogdanove, A. J. (2014). Principles and applications of TAL effectors for plant physiology and metabolism. Curr. Opin. Plant Biol. 19C, 99-104. doi: 10.1016/j.pbi.2014.05.007
10. Borjesson, D. L., Kobayashi, S. D., Whitney, A. R., Voyich, J. M., Argue, C. M., and Deleo, F. R. (2005). Insights into pathogen immune evasion mechanisms: Anaplasma phagocytophilum fails to induce an apoptosis differentiation program in human neutrophils. J. Immunol. 174, 6364-6372. doi: 10.4049/jimmunol.174.10.6364
11. Bork, P. (1993). Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally? Proteins 17, 363-374. doi: 10.1002/prot.340170405
12. Borroto, C. J., Cole R., Dumler, J. S., and Garcia-Garcia, J. C. (2009). Identification of candidate nuclear effectors among intracellular bacteria. Paper Presented at the Mid-Atlantic Regional Center for Excellence for Biodefense and Emerging Infectious Diseases [MARCE-2] Investigators' Meeting, Airlie Center, Warrenton, VA.
13. Brodsky, I. E., and Medzhitov, R. (2009). Targeting of immune signalling networks by bacterial pathogens. Nat. Cell Biol. 11, 521-526. doi: 10.1038/ncb0509-521
14. Bustin, M. (1999). Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol. Cell. Biol. 19, 5237-5246.
15. Cai, S., Lee, C. C., and Kohwi-Shigematsu, T. (2006). SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes. Nat. Genet. 38, 1278-1288. doi: 10.1038/ng1913
16. Carlyon, J. A., Chan, W. T., Galan, J., Roos, D., and Fikrig, E. (2002). Repression of Rac2 mRNA expression by Anaplasma phagocytophila is essential to the inhibition of superoxide production and bacterial proliferation. J. Immunol. 169, 7009-7018. doi: 10.4049/jimmunol.169.12.7009
17. Carlyon, J. A., and Fikrig, E. (2003). Invasion and survival strategies of Anaplasma phagocytophilum. Cell Microbiol. 5, 743-754. doi: 10.1046/j.1462-5822.2003.00323.x
18. Carlyon, J. A., and Fikrig, E. (2006). Mechanisms of evasion of neutrophil killing by Anaplasma phagocytophilum. Curr. Opin. Hematol. 13, 28-33. doi: 10.1097/01.moh.0000190109.00532.56
19. Caturegli, P., Asanovich, K. M., Walls, J. J., Bakken, J. S., Madigan, J. E., Popov, V. L.,et al. (2000). ankA: an Ehrlichia phagocytophila group gene encoding a cytoplasmic protein antigen with ankyrin repeats. Infect. Immun. 68, 5277-5283. doi: 10.1128/IAI.68.9.5277-5283.2000
20. Chen, S. M., Dumler, J. S., Bakken, J. S., and Walker, D. H. (1994). Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. J. Clin. Microbiol. 32, 589-595.
21. Chien, M., Morozova, I., Shi, S., Sheng, H., Chen, J., Gomez, S. M.,et al. (2004). The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305, 1966-1968. doi: 10.1126/science.1099776
22. Choi, K. S., Park, J. T., and Dumler, J. S. (2005). Anaplasma phagocytophilum delay of neutrophil apoptosis through the p38 mitogen-activated protein kinase signal pathway. Infect. Immun. 73, 8209-8218. doi: 10.1128/IAI.73.12.8209-8218.2005
23. de la Fuente, J., Ayoubi, P., Blouin, E. F., Almazan, C., Naranjo, V., and Kocan, K. M. (2005). Gene expression profiling of human promyelocytic cells in response to infection with Anaplasma phagocytophilum. Cell Microbiol. 7, 549-559. doi: 10.1111/j.1462-5822.2004.00485.x
24. Dumler, J. S., Choi, K. S., Garcia-Garcia, J. C., Barat, N. S., Scorpio, D. G., Garyu, J. W.,et al. (2005). Human granulocytic anaplasmosis and Anaplasma phagocytophilum. Emerg. Infect. Dis. 11, 1828-1834. doi: 10.3201/eid1112.050898
25. Dunphy, P. S., Luo, T., and McBride, J. W. (2013). Ehrlichia moonlighting effectors and interkingdom interactions with the mononuclear phagocyte. Microbes Infect. 15, 1005-1016. doi: 10.1016/j.micinf.2013.09.011
26. Evans, M. R., Swaminathan, B., Graves, L. M., Altermann, E., Klaenhammer, T. R., Fink, R. C.,et al. (2004). Genetic markers unique to Listeria monocytogenes serotype 4b differentiate epidemic clone II (hot dog outbreak strains) from other lineages. Appl. Environ. Microbiol. 70, 2383-2390. doi: 10.1128/AEM.70.4.2383-2390.2004
27. Garcia-Garcia, J. C., Barat, N. C., Trembley, S. J., and Dumler, J. S. (2009a). Epigenetic silencing of host cell defense genes enhances intracellular survival of the rickettsial pathogen Anaplasma phagocytophilum. PLoS Pathog. 5:e1000488. doi: 10.1371/journal.ppat.1000488
28. Garcia-Garcia, J. C., Rennoll-Bankert, K. E., Pelly, S., Milstone, A. M., and Dumler, J. S. (2009b). Silencing of host cell CYBB gene expression by the nuclear effector AnkA of the intracellular pathogen Anaplasma phagocytophilum. Infect. Immun. 77, 2385-2391. doi: 10.1128/IAI.00023-09
29. Garyu, J. W., Choi, K. S., Grab, D. J., and Dumler, J. S. (2005). Defective phagocytosis in Anaplasma phagocytophilum-infected neutrophils. Infect. Immun. 73, 1187-1190. doi: 10.1128/IAI.73.2.1187-1190.2005
30. Ge, Y., Yoshiie, K., Kuribayashi, F., Lin, M., and Rikihisa, Y. (2005). Anaplasma phagocytophilum inhibits human neutrophil apoptosis via upregulation of Bfl-1, maintenance of mitochondrial membrane potential and prevention of caspase 3 activation. Cell Microbiol. 7, 29-38. doi: 10.1111/j.1462-5822.2004.00427.x
31. Gillespie, J. J., Ammerman, N. C., Dreher-Lesnick, S. M., Rahman, M. S., Worley, M. J., Setubal, J. C.,et al. (2009). An anomalous type IV secretion system in rickettsia is evolutionarily conserved. PloS ONE 4:e4833. doi: 10.1371/journal.pone.0004833
32. Gilmore, S. H., Garcia-Garcia, J. C., and Dumler, J. S. (2012). Identification of 6 novel nuclear translocated proteins in A. phagocytophilum. Paper Presented at the 25th Meeting of the American Society of Rickettsiology, Park City, UT, Abstract 130.
33. Gong, F., Sun, L., and Sun, Y. (2010). A novel SATB1 binding site in the BCL2 promoter region possesses transcriptional regulatory function. J. Biomed. Res. 24, 452-459. doi: 10.1016/S1674-8301(10)60060-7
34. Hawkins, S. M., Kohwi-Shigematsu, T., and Skalnik, D. G. (2001). The matrix attachment region-binding protein SATB1 interacts with multiple elements within the gp91phox promoter and is down-regulated during myeloid differentiation. J. Biol. Chem. 276, 44472-44480. doi: 10.1074/jbc.M104193200
35. IJdo, J. W., Carlson, A. C., and Kennedy, E. L. (2007). Anaplasma phagocytophilum AnkA is tyrosine-phosphorylated at EPIYA motifs and recruits SHP-1 during early infection. Cell Microbiol. 9, 1284-1296. doi: 10.1111/j.1462-5822.2006.00871.x
36. Jernigan, K. K., and Bordenstein, S. R. (2014). Ankyrin domains across the tree of life. Peer J. 2:e264. doi: 10.7717/peerj.264
37. Jin, Q., Yuan, Z., Xu, J., Wang, Y., Shen, Y., Lu, W.,et al. (2002). Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucleic Acids Res. 30, 4432-4441. doi: 10.1093/nar/gkf566
38. Jones, P. L., Veenstra, G. J., Wade, P. A., Vermaak, D., Kass, S. U., Landsberger, N.,et al. (1998). Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 19, 187-191. doi: 10.1038/561
39. Klein, M. B., Hu, S., Chao, C. C., and Goodman, J. L. (2000). The agent of human granulocytic ehrlichiosis induces the production of myelosuppressing chemokines without induction of proinflammatory cytokines. J. Infect. Dis. 182, 200-205. doi: 10.1086/315641
40. Kohwi-Shigematsu, T., Kohwi, Y., Takahashi, K., Richards, H. W., Ayers, S. D., Han, H. J.,et al. (2012). SATB1-mediated functional packaging of chromatin into loops. Methods 58, 243-254. doi: 10.1016/j.ymeth.2012.06.019
41. Kumar, P. P., Bischof, O., Purbey, P. K., Notani, D., Urlaub, H., Dejean, A.,et al. (2007). Functional interaction between PML and SATB1 regulates chromatin-loop architecture and transcription of the MHC Class I locus. Nat. Cell Biol. 9, 45-56. doi: 10.1038/ncb1516
42. Lee, H. C., Kioi, M., Han, J., Puri, R. K., and Goodman, J. L. (2008). Anaplasma phagocytophilum-induced gene expression in both human neutrophils and HL-60 cells. Genomics 92, 144-151. doi: 10.1016/j.ygeno.2008.05.005
43. Letourneau, A., Santoni, F. A., Bonilla, X., Sailani, M. R., Gonzalez, D., Kind, J.,et al. (2014). Domains of genome-wide gene expression dysregulation in Down's syndrome. Nature 508, 345-350. doi: 10.1038/nature13200
44. Lin, M., Kikuchi, T., Brewer, H. M., Norbeck, A. D., and Rikihisa, Y. (2011). Global proteomic analysis of two tick-borne emerging zoonotic agents: Anaplasma phagocytophilum and Ehrlichia chaffeensis. Front. Microbiol. 2:24. doi: 10.3389/fmicb.2011.00024
45. Luo, T., Kuriakose, J. A., Zhu, B., Wakeel, A., and McBride, J. W. (2011). Ehrlichia chaffeensis TRP120 interacts with a diverse array of eukaryotic proteins involved in transcription, signaling, and cytoskeleton organization. Infect. Immun. 79, 4382-4391. doi: 10.1128/IAI.05608-11
46. Luo, T., and McBride, J. W. (2012). Ehrlichia chaffeensis TRP32 interacts with host cell targets that influence intracellular survival. Infect. Immun. 80, 2297-2306. doi: 10.1128/IAI.00154-12
47. Nan, X., Ng, H. H., Johnson, C. A., Laherty, C. D., Turner, B. M., Eisenman, R. N.,et al. (1998). Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393, 386-389. doi: 10.1038/30764
48. Ng, H. H., Zhang, Y., Hendrich, B., Johnson, C. A., Turner, B. M., Erdjument-Bromage, H.,et al. (1999). MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat. Genet. 23, 58-61. doi: 10.1038/12659
49. Ohashi, N., Zhi, N., Lin, Q., and Rikihisa, Y. (2002). Characterization and transcriptional analysis of gene clusters for a type IV secretion machinery in human granulocytic and monocytic ehrlichiosis agents. Infect. Immun. 70, 2128-2138. doi: 10.1128/IAI.70.4.2128-2138.2002
50. Okano, M., Bell, D. W., Haber, D. A., and Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257. doi: 10.1016/S0092-8674(00)81656-6
51. Ottaviani, D., Lever, E., Mitter, R., Jones, T., Forshew, T., Christova, R.,et al. (2008). Reconfiguration of genomic anchors upon transcriptional activation of the human major histocompatibility complex. Genome Res. 18, 1778-1786. doi: 10.1101/gr.082313.108
52. Park, J., Kim, K. J., Choi, K. S., Grab, D. J., and Dumler, J. S. (2004). Anaplasma phagocytophilum AnkA binds to granulocyte DNA and nuclear proteins. Cell Microbiol. 6, 743-751. doi: 10.1111/j.1462-5822.2004.00400.x
53. Paschos, K., and Allday, M. J. (2010). Epigenetic reprogramming of host genes in viral and microbial pathogenesis. Trends Microbiol. 18, 439-447. doi: 10.1016/j.tim.2010.07.003
54. Pennini, M. E., Perrinet, S., Dautry-Varsat, A., and Subtil, A. (2010). Histone methylation by NUE, a novel nuclear effector of the intracellular pathogen Chlamydia trachomatis. PLoS Pathog. 6:e1000995. doi: 10.1371/journal.ppat.1000995
55. Reddington, J. P., Pennings, S., and Meehan, R. R. (2013). Non-canonical functions of the DNA methylome in gene regulation. Biochem. J. 451, 13-23. doi: 10.1042/BJ20121585
56. Rennoll-Bankert, K. E., and Dumler, J. S. (2012). Lessons from Anaplasma phagocytophilum: chromatin remodeling by bacterial effectors. Infect. Disord. Drug Targets 12, 380-387. doi: 10.2174/187152612804142242
57. Rohde, J. R. (2011). Microbiology. Listeria unwinds host DNA. Science (New York, N.Y.) 331, 1271-1272. doi: 10.1126/science.1203271
58. Rolando, M., Sanulli, S., Rusniok, C., Gomez-Valero, L., Bertholet, C., Sahr, T.,et al. (2013). Legionella pneumophila effector RomA uniquely modifies host chromatin to repress gene expression and promote intracellular bacterial replication. Cell Host Microbe 13, 395-405. doi: 10.1016/j.chom.2013.03.004
59. Scorpio, D. G., Akkoyunlu, M., Fikrig, E., and Dumler, J. S. (2004). CXCR2 blockade influences Anaplasma phagocytophilum propagation but not histopathology in the mouse model of human granulocytic anaplasmosis. Clin. Diagn. Lab. Immunol. 11, 963-968. doi: 10.1128/CDLI.11.5.963-968.2004
60. Silmon de Monerri, N. C., and Kim, K. (2014). Pathogens hijack the epigenome: a new twist on host-pathogen interactions. Am. J. Pathol. 184, 897-911. doi: 10.1016/j.ajpath.2013.12.022
61. Spector, D. L. (2003). The dynamics of chromosome organization and gene regulation. Annu. Rev. Biochem. 72, 573-608. doi: 10.1146/annurev.biochem.72.121801.161724
62. Srivastava, S., Mishra, R. K., and Dhawan, J. (2010). Regulation of cellular chromatin state: insights from quiescence and differentiation. Organogenesis 6, 37-47. doi: 10.4161/org.6.1.11337
63. Stephens, R. S., Kalman, S., Lammel, C., Fan, J., Marathe, R., Aravind, L. W.,et al. (1998). Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science (New York, N.Y.) 282, 754-759. doi: 10.1126/science.282.5389.754
64. Stirzaker, C., Song, J. Z., Davidson, B., and Clark, S. J. (2004). Transcriptional gene silencing promotes DNA hypermethylation through a sequential change in chromatin modifications in cancer cells. Cancer Res. 64, 3871-3877. doi: 10.1158/0008-5472.CAN-03-3690
65. Sugio, A., Yang, B., Zhu, T., and White, F. F. (2007). Two type III effector genes of Xanthomonas oryzae Pv. oryzae control the induction of the host genes OsTFIIAγ1 and OsTFX1 during bacterial blight of rice. Proc. Natl. Acad. Sci. U.S.A. 104, 10720-10725. doi: 10.1073/pnas.0701742104
66. Thomas, V., Samanta, S., Wu, C., Berliner, N., and Fikrig, E. (2005). Anaplasma phagocytophilum modulates gp91phox gene expression through altered Interferon Regulatory Factor 1 and PU.1 levels and binding of CCAAT displacement protein. Infect. Immun. 73, 208-218. doi: 10.1128/IAI.73.1.208-218.2005
67. Yasui, D., Miyano, M., Cai, S., Varga-Weisz, P., and Kohwi-Shigematsu, T. (2002). SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419, 641-645. doi: 10.1038/nature01084
68. Zhu, B., Kuriakose, J. A., Luo, T., Ballesteros, E., Gupta, S., Fofanov, Y. et al. (2011). Ehrlichia chaffeensis TRP120 binds a G+C-rich motif in host cell DNA and exhibits eukaryotic transcriptional activator function. Infect. Immun. 79, 4370-4381. doi: 10.1128/IAI.05422-11